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Advances in

MARINE BIOLOGY VOLUME 6

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 6 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

and

SIR MAURICE YONGE Edinburgh, Scotland

Academic Press London and New York

1968

ACADEMIC

PRESS INC. (LONDON) LTD.

BERKELEY

.----.?. L

/ti

/ "

-

'

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 1968 by Academic Press Inc. (London) Ltd.

All rights reserved

NO PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM B Y PHOTOSTAT, MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION FROM THE PUBLISHERS

Library of Congress Catalog Card Number: 6 3 - 1 4 0 4 0

PRINTED I N GREAT BRITAIN B Y THE WHITEFRIARS LONDON AND TONBRIDOE

PRESS LTD.

CONTRIBUTORS TO VOLUME 6 J. E. CARROZ, Legislation Research Branch, Department of Relations and Legal Affairs, F.A.O., Rome, Italy. .

Public

E. GHIRARDELLI, Istituto d i Zoologia oe Anatomia Gomparata della Universita d i Trieste, Ituly.

J. A. GULLAND, Department of Fisheries, F.A.O., Rome, Italy. W. MACNAE, Department of Zoology, University of the Witwatersrand, Johannesburg,South Africa.

This Page Intentionally Left Blank

CONTENTS

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11. The Need for Management . . .. .. A. The Depletion of Marine Resources. . B. Theoretical Studies . . .. ..

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16

111. Methods of Regulation .. .. .. A. Types of Regulation . . .. .. B. Limitation of the Amount of Fishing

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The Mechanics of Management and InternationalLaw . . A. Territorial Sea and Fishing Zones . . .. .. B. Specialized Fishery Bodies . . .. .. ..

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45

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CONTRIBUTORSTO VOLUME6

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of Fishery Resources

Management

J. A. GULLAND and J. E. CARROZ

I. Introduction . .

IV.

V.

VI.

VII.

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Problems and Prospects for FutureProgress A. Achievements of Present Bodies .. B. The Need for FurtherResearch .. C. InternationalManagement . . ..

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45 50 53

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Appendix : Table of InternationalBodies Concerned with .. .. .. .. .. Fishery Management

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Acknowledgements . . References

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vii

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CONTENTS

Vlll

A General Account of t h e Fauna and Flora of Mangrove Swamps and Forests i n t h e Indo-West-Pacific Region WILLIAMMACNAE

I. Introduction . . .. .. .. A. The Word “Mangrove” .. B. Early Historical References . . C. Indo-west-Pacific Shores .. D. Sea-shore Plant Associations. .

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75 77

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115

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.. .. .. 111. Adaptations Shown by the Flora . . A. Adaptations to Growing in Ill-consolidated Muds. B. Specializations of Stems and Leaves .. ..

136

11. Zonation of Mangroves .. .. A. The Landward Fringe .. .. B. Zone of Ceriops Thickets C. Zone of Bruguiera Forests . . D. Zones of Rhizophora Forests E. Seaward Avicennia Fringes . . F . SonneratiaZone .. .. G. Variations .. .. .. H. Mangrove Soils .. .. I. Control of Zonation . . ..

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76

91 103 105

118 121 124

136 140

C. Relationship between the Mangrove Root and Shoot .. .. . . 144 Systems .. .. .. .. .. . . 145 D. Viviparity .. .. .. .. .. . . 148 E. Succession .. .. .. IV. Distribution of Terrestrial Animals within the Mangal. . A. Birds Associated with Mangals .. .. .. B. Amphibians and Reptiles . . .. .. ..

C. Mammals D. Insects . .

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150 153 156 157 157

ix

CONTENTS

V.

VI.

Distribution of Marine Animals within the Mangal . . 165 A. Vertical Zonation Affecting Tree Dwelling Animals 165 B. “Horizontal” Zonation through the Mangal . . 167 Specializations Shown by the Fauna .. .. A. Birds, Mammals, Reptiles and Amphibians B. Insects . . .. .. .. .. .. C. Marine Animals .. .. .. ..

., .

181 181

I

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182

.,

184

VII. Geographical Distribution . . .. .. .. ., 219 A. Extratropical Extensions of Mangroves and their Associated Fauna . . . . .. .. . . 219 B. Biogeographical Comment . . .. .. . . 222

VIII. Uses Made by Man of the Mangal and its Products A. Uses of the Timber . . .. .. .. B. Pond Culture of Fish and Prawns . . .. C. Reclamation . . .. .. .. .. D. Salt Production .. .. .. ..

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. . 238 . . 240

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241

X. Bibliography and References

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241

IX. Acknowledgements . .

Some Aspects of the Biology of the Chaetognaths ELVEZIOGHIRARDELLI

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271

11. General Morphology. . .. .. A. The Eyes, Hooks and Teeth . . B. Integument, Fins and Tail . . C. Corona ciliata . . .. ..

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I. Introduction . .

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273 274 281 .1

X

COXTEXTS

111. Reproduction. . .. .. .. .. .. A. The Male Genital Apparatus. . .. .. B. The Female Reproductive Apparatus. General .. C. Spermatogenesisand Oogenesis .. .. D. Fertilization . . .. .. .. .. E. Laying of Eggs .. .. .. F. Habitat and Cycles of Sexual Maturity . . IV. V.

Regeneration . .

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289

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289 292 309 322 335 343

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. . 351

Affinities and Systematic Position . .

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VI. Laboratory Experiments VII, Acknowledgements . .

*

355

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. . 365

364

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AUTHORINDEX . .

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. . 377

TAXONOMIC INDEX ..

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. . 395

VIII. References

SUBJECTINDEX

Adv. mar. B i d , Vol. 6, 1968, pp. 1-71

MANAGEMENT OF FISHERY RESOURCES* J. A. CULLAND? Department of Fisheries, F.A.O., Rome, Italy and

J. E. CARROZ Legislation Research Bran,ch, Department of Public Relations and Legal Affairs, F.A.O., Eome, Italy I. Introduction .. .. .. .. .. .. .. 11. The Need for Management .. .. .. .. .. A. The Depletion of Marine Kesources .. .. R. Theoretical Studies . . .. .. .. .. 111. Methods of Regulation . . .. .. .. .. .. 4 .. Types of Regulation . . . . .. .. .. B. Limitation of the Amount of Fishing .. .. IV. The Mechanics of Management and InternationalLaw .. A. Territorial Sea and Fishing Zones . . . . .. R. Specialized Fishery Bodies . . .. .. .. V. Problems and Prospects for Future Progress .. .. A. Achievements of Present Bodies . . .. .. B. The Need for FurtherResearch .. .. .. C. InternationalManagement . . . . .. .. VI. Acknowledgements .. .. .. .. .. .. VII. Roferences .. .. .. .. .. .. .. Appendix: Table of International Bodies Concerned with Management . . . . .. .. .. .. ..

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1 7 7 16 25 25 29 34 35 39 45 45 50 53 56 56

Fishery

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..

62

I. INTRODUCTION The estimated world production of fish has more than doubled in the last two decades, from less than 20 million metric tons in 1948 to over 50 million tons in 1965 (see Table I ;F.A.O., 1966a). This increase, which is considerably faster than the increase of either the human population or the production of food as a whole, means that fish are making an increasingly important contribution to the world's food supply, particularly of animal protein. In the world as a whole, fish * This paper was first published, undcr the same title, as Chapter I V in "The State of Food and Agriculture 1967 "(F.A.O., Rome, 1967). Some changes have been made from the original version, principally in order to make the presentation more suitable for a scientific audience. I n so far as there are differences from tho earlier publication, these represent the views of the authors and are not necessarily those of the F.A.O. Formerly of the Fisheries Laboratory, Lowestuft, England. 1

2

J. A . GULLAND A N D J. E. CARROZ

contribute about 10% of the total animal protein intake, but con siderably more in some areas such as the Far East (see Table 11). While a n increasing proportion of the total catch is not used directly for human consumption but is converted to fish meal, this fish is used for producing human food in commercially more attractive forms by feeding it to chicken, trout, etc. ; recent developments in marine fish culture suggest that in the future further supplies of fish meal will be needed to produce valuable marine fish such as plaice (Pleuronectes platessa L.), sole (Solea solea (L.)) or yellowtail (Xeriola quinqueradiata (Temminck & Schlegel)) (Shelbourne, 1964), or shellfish such as prawns or lobster. The increased catches, due both to increased local fishing and especially the rapidly increasing number of mobile factory and other vessels operating far from their home bases, have intensified the TABLEIA. WORLDFISH PRODUCTION, 1948-65 Million metric tons live weight. (FromF.A.O., 1966a.)

Total world production:.

.

Africa . North America South America Asia . . Europe . Oceania . U.S.S.R. .

.

1948

1958

1960

1962

1963

1964

1965

19.6

32.8

39.5

46.4

47.6

52.0

52.4

2.6 4.5 8.3 18.6 8.7 0.1 3.6

2.7 4.4 8.4 19.0 9.0 0.1 4.0

3.0 4.3 11.0 19.3 9.7 0.2 4.5

3.1 4.4 9.0 19.9 10.8 0.2 5.0

6.4 29.0 3.5 0.6

6.5 35.3 3.8 0.8

6.7 36.1 4.1 0.7

6.8 40.7 3.8 0.7

7.2 40.4 4.1 0.7

17.5 5.7 8.1 4.8 15.3 1.0

Continent (region)

.

.

. .

. .

. .

1.0 3.6 0.5 6.8 6-1 0.1 1.5

2.1 4.0 1.6 14.6 7.8 0.1 2.6

2.3 4.1 4.4 17.4 8.1 0.1 3.1

Group of species Vrcshwatcr fishes. . 2.5 Marine fishes . . 14.7 Crustaceans, molluscs . . 2.0 Other aquatic animalsand plants 0.4

5.4 23.9 2.9 0.6

Utilization Human consumption Fresh . Breezing . Curing . Canning . Other purposes Reduction . Miscellaneous .

.

14.5 2-7 7.3 3.0

16.3 3.4 7.5 3.7

16.9 4.3 8.1 4.1

17.3 4.7

.

9.7 1.0 5.0 1.4

4.1

17.6 5.1 8.4 4.4

.

1.5

.

1.0

4.3 1.0

7.6 1.0

12.0 1.0

12.0 1.0

15.5 1.0

. ,

8.5

3

MANAGEMENT O F BTSHERY RESOllRCES

TABLEIB. MARINEFISHES PRODUCTION, 1948-65 Million metric tons livc weight. (FromF.A.O., 1966a.) 1948

1958

1960

1962

1963

1964

1965

14.7

23.9

29.0

35.3

36.1

40.7

40.4

Species 0.5 0.8 3.6 4.5 1.2 2.2 0.5 1.8 4.7 7.4 0.4 1.0 0.6 1.0 0.3 0.3 2.9 4.9

1.2 5.0 2.4 1.7 10.2 1.0 1.1 0.4 6.0

1.2 5.5 2.6 2.1 14.8 1.2 1.1 0.4 6.4

1.0 5.9 2.7 1.9 15.1 1.2 1.2 0.4 6.7

1.0 6.0 2.9 2.0 18.7 1.2 1.4 0.4 7.1

1.0 6.5 3-0 2.1 17.4 1.2 1-7 0.4 7.1

Principal marine fishing areas 8.0 9.1 9.8 10.3 North Atlantic . . 5.1 2.2 3.4 4.3 Central and South Atlantic . 0.8 0.7 0.8 0.8 MeditcrraneanandBlackSeas 1.7 1.5 1.8 Indian Occan . . 1.0 4.1 4.6 3.7 2.5 North Pacific . . 3.1 8.2 8.8 9.9 Contra1Pacific . 7.7 0.2 1.3 4.0 South Pacific . .

10.9 5.2 0.9 1.7 4-5 10.2 7.8

11.5 5.6 1.0 1.9 4.9 10.0 10.5

12.7 6.2 0.9 1.9

Total marine fishes:

.

.

Flounders,halibuts, soles . Cods, hakcs, haddocks . . Redfish, basses, congers . Jacks, mullcts . . Herrings, sardines, anchovies. Tunas, bonitos, skipjacks . Mackerels . . . Sharks, rays . . Unsorted and other . .

.

5-4 10.3 8.4

problems of overfishing, and the possible need of regulations and management t o make the best use of the resources. At the time of the 1949 U.N. Scientific Conference on the Conservation and Utilization of Resources a t Lake Success, the only overfished stocks were a limited number of stocks of high-priced species, mainly in the North Atlantic and North Pacific (e.g. the plaice in the North Sea, the halibut and salmon in the north-east Pacific), and the Conference drew up a map showing some thirty stocks then believed t o be underfished (see Fig. 1). Of these stocks about half are now probably in need of proper management, including the cod (Gadus morhua L.), redfish (Sebastes spp.) and herring (Clupea harengus L.) in the North Atlantic, and a t least some species of tunas in most of the oceans. The classical response of the fishing industry t o overfishing in one stock has been to move to other, usually more distant stocks, but it is clear that this process cannot continue much longer. Some blank spaces in the Lake Success map have been filled by more recently discovered resources, e.g. oil sardine (Xardinella spp.) and Rastrelliger spp. in the Arabian Sea, or hake (Merlucciusspp.) off the west coasts of the Americas, but it is significant

15'

5 0'

45" 3 On 15O O0 15O

3 On

4 !I0 6 On I

I

150"

I

I

12O0

,

I

gon

1

I

6 0"

I

I

3 '0

I

I

Do

I

I

3 0"

I

I

6 0"

I

I

90n

I

1

120'

I

I

150"

I

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I

180n

FIG. 1. Map showing latent marine fishery resources (fish stocks believed to be underfished in 1949). Circled stocks are those now certainly or probably in need of management (the "pilchard " off the west coast of South America presumably refers to the anchoveta stock). Of the tunas, the yellowfin is probably heavily exploited in all areas, but further expansion may be possible for other species such as skipjack or bonito. (From United Nations, 1931.)

5

MANAGEMENT O F FISHERY RESOURCES

TABLE11. PER CAPUT PROTEIN SUPPLIES, BY REGION(RECENT PERIOD) Prom "State of Food and Agriculture 1964 ",F.A.O. Rome.

Fish

Anirnal protein -~

Total protein

Region

~

-~

U.S.S.R.

.

North Amorica. . Oceania . Latin Amorica . . Far East (incl. mainland China) . . Near East . Africa . High-calorie countries* Low-calorie countricst

.

_.________

As "/b of A s yo of total Total total protein protein ( g per caput per day)

A s yo of animal protein

~____

_ _

~~~~

Wcsterri Europe . Eastern Europe and

World

Total

-

.

83

39

47

2.4

2.9

6.2

.

94 93 94 67

33 66 62 24

35 71 66 36

1.9 2.5 2.2 1.5

2.0 2.7 2.3 2.2

5.8 3.8 3.5 6.3

56 76

8 14

14 18

2.2 1.1

3.9 1.4

27.5 7.9

.

61 90 58

11 44 9

18

.

49 16

1.3 2.4 1.9

2.1 2.7 3.3

11.8 5.5 21.1

.

68

20

29

2.3

3.4

11.5

. f

.

. . .

* Europe, North America,

Oceania, Hiver Plate countries.

?- Latin America, P a r East and Near East, Africa.

that these additions have been in the areas (IndianOcean, south-east Pacific) away from the old centres of fishery development, and no major new resources have been discovered in the North Atlantic, or north-west Pacific. At the present rate of development few substantial unexploited stocks of fish accessible to the present types of gear will remain in another twenty years. Thus the problem of international management is becoming increasingly urgent. This problem is not confined t o the high seas, but occurs also in inland waters, especially in the larger rivers and lakes where the biological problems are essentially the same as in the sea, even though the problems of international fishing may be much less. For certain stocks which are particularly vulnerable, e.g. salmon going upstream to spawn, the problems of overfishing may become more intensive than in any purely marine fishery. Inlandwaters also present other problems, such as pollution, and the alternative use of water resources-power, irrigation etc.-which may conflict with fisheries. These are less pressing in the sea, though there are similar problems, for instance the use of the other resources of the sea-bed such as minerals or oil, which

6

J. A. GULLAND AND J. E. CARROZ

may also conflict with fisheries. However, these problems will not be considered further here; nor will this article be concerned with the problems of fish culture in ponds, brackish water or enclosed parts of the sea, except that such culture may have an indirect effect on the open water fisheries by increasing the demand for cheap supplies of food for the choicer varieties of fish being farmed. The problems of overfishing arise because, in default of definite arrangements, the fishery resources are not the responsibility of any single person or body. Next year’s catches depend on how much is taken this year, but in the open sea the individual fisherman can do little to ensure better fishing for himself next year-if lie does not catch fish while he can, someone else will catch them. Thus effective management depends on the participation of all, or at least of the great majority, of those exploiting a given stock of fish. The problems are more complex when many countries are concerned or when more than one species of fish is caught (especially when there may be biological interactions between the stocks, e.g. one species being the main food of another),but the main problems are essentially the same even when a single stock is exploited by a single country. The first problem is biological: t o understand the population dynamics of the stock or stocks concerned, and thus make quantitative assessments of the probable effect on the stocks and on future catches of any regulatory measure. Until this biological understanding is available, it is unrealistic to consider the other problems of regulation, though at first the biological study need not be very intense. A simple study may show that a stock is in urgent need of regulation, and any effective measure would be bound to improve matters; only as the first measures take effect will more detailed biological data be needed to determine the precise needs for further measures. Too often conservation measures have been delayed, and great damage done to the stock and the fishery on it by the demand for complete and conclusive biological evidence; the final conclusive proof that a stock is being depleted is when it becomes extinct. Biological considerations are, of course, only the first step; the aim of fishery management is not primarily to maintain the stocks of fish, but to make the best use of the resources in terms of larger or cheaper supplies of fish to the consumer, better income to the fishermen, etc. The desired result of regulation, especially when the objective is t o take about the same catch more cheaply, can therefore only be ensured by taking into account the probable economic and other non-biological effects of proposed regulation. Economic and similar considerations will also become increasingly important in resolving disputes between

MANAGEMENT O F FISHERY RESOURCES

7

groups of fishermen with conflicting interests, e.g. one group fishing herring and another group taking cod which feed on herring. However, problems of management, and indeed some of the outstanding examples of the failure to achieve proper management, have occurred when there has been no conflict of long-term interests, but merely a conflict between the long-term interest for the fishery as a whole and the immediate desire of the individual fisherman to catch as much as he can today. It is natural not to be greatly concerned with a problem until it becomes urgent; thus so long as most fish stocks were not too heavily fished, and there remained alternative unexploited stocks t o which the fleets exploiting the overfished stocks could turn, the problems of fishery management have received too little attention. This is particularly unfortunate because of the need, from several considerations, to take action as early as possible. Biologically, the assessment of any fishery depends on measuring the effect on the stock of changes in fishing. This assessment is made much easier and more precise if data are available from periods of very light fishing. Detailed and expensive biological studies of the stocks after the fishery has become very intense cannot substitute for reliable data on such simple things as the average size of fish, or the average catch per boat, from the periods of light fishing. Similarly, the practical problems of regulations are much less if regulatory measures are considered well before the stocks are clearly overfished ;the social problems in limiting further entry t o a fishery are much less than those in reducing the existing number of boats or number of fishermen. For all these reasons, therefore, the various problems relating to proper management of fishery resources deserve urgent attention.

11. THENEEDFOR MANAGEMENT A. The depletion of marine resources A hundred years ago most people, including leading scientists, believed that the living resources of the sea were essentially inexhaustible-" there are more good fish in the sea than ever came out of i t ". K,epeated experience since then, a t first for the most valuable or vulnerable species, has shown how false this assumption was. The first stocks to show depletion were those close to the ports of the industrial nations. Shortly after the development of the steam trawler-one of the earliest applications of modern industrial techniques to fishing-the stocks of plaice in the North Sea showed signs of depletion. The average annual landings of plaice by individual trawling smacks was clearly decreasing as early as 1880, even though the total landings were still

8

J. A . (:ULLAND A N D J.

E. CARROZ

increasing (Wimpenny, 1053). Convincing proof that this decline, and the decline in stocks of other valuable species, was due to fishing was provided by the severe restrictions on fishing during the two world wars. Immediately after each war the catches of the individual trawlers were several times the pre-war avesages (see Fig. 2) (Wimpenny, 1953 ; Margetts and Holt, 1948). Similar recoveries were noted in other stocks where the amount of fishing was greatly reduced, e.g. the haddock (Melanogrammus aegle,finus (L.)) in the North Sea and a t Faroes (Parrish and Jones, 1953), the hake (Merluccius mqrluccizcs L.) to the south-west of the British Isles (Hickling, 1946) and yellow sea bream (Taius tumifrons (Tanaka & Schlegel))in the East China Sea (Shindo, I -+

I

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I

I

I

c L

-

920 -

200 - m

c c

I

c

r: g 1 5 2; -

'sc ma)

3s -a

9 P-4,

- 1 0 - tr

G -m c x 342 b

a

Q\

c

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A ma L J

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1

1960). These and other similar changes show clearly not only how fish stocks can be depleted by fishing but also that the process is reversible. Thus with proper management stocaks can build up again, even such vulnerable stocks as whales ; for instance, the southern right whale (Eubalaena australis (Desm.)) is returning to Ncw Zealand waters (Gaskin, 1964), and the numbers of California gray whales, after having been very severely reduced by unrestricted catches, were given complete protection and have incrcased at around 10% per year-close to the rate for the Antarctic stocks of blue and fin whales calculated from their reproductive and mortality rates (Rice, 1961). Because of the difficulties, discwssed later, in achieving proper management of major mariiie resources, especially in international waters, there are far more examples of stocks declining in the absence of proper managements. One example of an important stock being

MANAGEMENT

O F FISHERY RESOVRCES

9

built up by regulation is the Pacific halibut. This large, long-lived and ecouomically valuable fish is particularly vulnerable to overfishing and by the 1920s the stocks had been severely depleted. As a result of conventions between the two countries concerned (U.S.A. and Canada) the amount of fishing in 1960 was about half w h a t it was in 1930; the stock has been increascd one- to threefold, and the catches have increased from a minimum of 43 million lb in 1931 to more than 65 million lb in 1960 (ChapmanP t al., 1962). The management of this stock has thus been highly successful in maintaining the stock and the catch, but the full benefits of management have not been achieved. Although the amount of fishing, in terms of the impact on the stock, has been halved, the costs have been nowhere near halved, since the number of ships operating has increased while the length of season has been very severely reduced. Both the catching and marketing side of the industry are therefore operating at a very low level of efficiency (Crutchfieldand Zellner, 1963). I n the absence of regulation and management of the over-exploited stocks, the response of the industries concerned has been to turn to other, more distant or less immediately attractive stocks. After the North Sea had shown itself to be capable of producing only limited quantities of the preferred species-cod, plaice, etc.-the fishing industries of the industrial nations, such as England and Germany, turned to the "distant water " grounds, especially Iceland and the Barents Sea. I n the North Sea, fishing was continued with the existing vessels which were not suitable for fishing the more distant grounds, and as these vessels were lost or scrapped without being replaced the level of exploitation in the North Sea by countries with interests on distant water fishing fell. Thus, even in 1050, virtually all the English North Sea trawlers then operating were built before 1925." As a result the level of fishing on the North Sea plaice stocks has recently been lower than a t any time (other than during the war periods) for the past eighty years ; this, combined with favourable natural conditions has provided record catches in 1964 (incidentally confirming the predictions, by Russell (1942), Bevcrton and Holt (1957) and others, based on the analysis of the heavily fished stocks of the 1930s, that a moderate decrease in the amount of fishing would give an increase in total catch) (Gulland,1967, 1968a). The catches of other iiiiportant demersal species (cod and haddock) have also been very high in recent years. These fish are caught by rather different groups of vessels from plaice, haddock

* VcsscIs of other countries, especially Uenmark, rrmained fishing in the North Sea but changed in part t o other stocks, such as hcrring or sand-eels.

10

J. A . GULLAND AND J. E. CARROZ

especially being a major interest to Scottish fishermen, and Scottish fishing has not expanded to distant waters to anything like the same extent as English fishing. Thus it is not clear whether the fishing on these species has declined to the same extent as the fishing on plaice though the cod stocks in the central North Sea seem to have also benefited from reduced fishing (M.A.F.F., U.K., 1962). Certainly the recent good catches have been due in part to outstanding year-classes, especially the 1962 haddock year-class (M.A.F.F., U.K., 1966). There may well have been a decrease in effort; also haddock catches in particular are likely t o have benefited from the larger mesh sizes introduced under the 1946 Overfishing Convention (I.C.E.S., 1957). The diversion of the main attention of some of the countries bordering the North Sea has therefore allowed some a t least of the North Sea demersal stocks to recover temporarily t o a level not far from the optimum. However, a t this level of fishing any increase in fishing would, in the long term, reduce the total catch. The recent success of North Sea fishing is attractingsome of the resources of ships and capital back to the North Sea, and without some restriction only a fraction of the resources a t present devoted to distant water fishing could quickly reduce the North Sea stocks again to the low level of the 1930s. Temporarily, though, some North Sea demersal stocks have benefited from diversion of fishing to other stocks, but these latter stocks have in their turn become depleted. The first of the distant water stocks to become depleted were the small but economically attractive stocks, such as the plaice off Iceland and in the Barents Sea; the abundanceof these stocks, as measured by the catch per hour, had been reduced as early as 1925 to a small fraction of their initial level. Russell (1942) and more recently Gulland (1961) describe clearly the decline in catch per hour of plaice and other species by English trawlers fishing a t Iceland, and the relation of this decline to the changes in the total amount of fishing. The larger cod stocks were able to support a greater total amount of fishing, but by the mid-1950s they too werc being heavily exploited. For instance, despite an increasein the amoufit of fishing since 1946 of several times (possibly as much as tenfold), the catches of cod from the Arcto-Norwegian stock (living in the waters between northNorway, Russia and Spitsbergen)has fluctuated between 600 000 and I 300 000 tons with no evidence of any increasing trend (see Fig. 3) (I.C.E.S., 1966). I n the last decade the further expansion of European fishing, including diversion of some of the effort formerly engaged in fishing the depleted stocks of the north-east Atlantic, and also increasing numbers of new freezer and factory trawlers (Fig. 4), especially from eastern

11

MANAGEMENT O F FISHERY RESOURCES

I400

m v1

0

t 0 c

7

x

c 0

v)

L

0 2

Cn

II:

D t

c + 0

500 0 L

+

d

Total effort d’

I

I

I

I

I

I

I

1930

35

40

115

50

55

60

0

FIG. 3. Arctic cod. 0-0, Total landings (in thousandsof tons); 0 - - - 0, total effort in English units (ton-hours x 10-8). (From I.C.E.S., 1966, Liaison Committee Report .)

FIG.4. The Ross Vanyuard, a modern British freozer trawler, capable of catching and freezing several hundred tons of fish during a 6-week voyage. (Photo: Pishinq News.)

Europe, has been directed to the north-west Atlantic, and more recently t o the centraI and southernAtlantic. Some of the stocks of the western Atlantic were already heavily fished by local fisheries, as well as by the long-established southern European fisheries for salt cod, but in the last few years some of the stocks, such as those off west Greenland,

12

J . A. GULLAX’IU A N D J . E. CARROZ

which until recently had been only lightly exploited, have become depleted (see the annual reports of the I.C.N.A.F. Assessment subCommittee in the I.C.N.A.F. Red Books ; Beverton and Hodder, 1962) (Figs. 5 an d 6). The exploitation of the pelagic species (particularlyherring)has not (up t o 1965) gone so far as tha t of the bottom-living cod, haddock, etc., but some of the local stocks of herring, such as those in the southern North Sea have been seriously depleted b y fishing, and lately there has been increasing concern about other herring stocks (see recent I.C.E.S. Liaison Committee reports). These events in the North Atlantic may be summarized in the form of a map showing the approximate date at which the fishing on each stock reached a level a t which further increase in the amount of fishing would give no appreciable increase in the sustained yield (see Fig. 7 ) . Most recently a major part of the expansion of Europeanfishing has been outside the North Atlantic, particularly off the west coast of Africa. Even as far away as off the roasts of South Africa and South West Africa by 1965 the country taking the biggest catch of hake (Merluccius cupensis Castlenau), the main bottom-living species, was

FIG. 5. The internationalfishing fleet on the Labrador Uanlrs. Trawlors from East Germany and Russia photographed from a British freezer trawler. (Photo: Fishing News.)

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O F FISHERY RESOURCES

13

FIG.6 . Why thc trawlers go t o Labrador;the cod-end of the trawl, with several tons of fish, comes on board a freezer trawler. (Photo: Fishing News.)

Spain (118 000 tons compared with 87 000 tons in 1965 by South Africa, and a total by all countries in 1948 of 39 000 tons). This expansion by industrialized countries has been both directly through increasing numbers of larger and long-rangefreezing and factory ships, especially from Eastern European countries, and also indirectly through investment in locally based fleets in the coast'alcountries. I n addition these countries are developing their own off-shore fisheries. Similar developments have taken place in the other oceans, particularly in the northern Pacific, from where Japanese and more recently Soviet fisheries have been expanding farther and farther afield. European and Japanese vessels are now exploiting the same stocks of fish, such as the hake off the south-west coast of Africa. Even relatively poor countries are rapidly developing long-distance fisheries ; Korea, for instance, has a substantial fleet fishing for tuna in the central Pacific and in the Atlantic.

II

I

I

I

I

I

I

I

I

I

I

I

I

I

I

FIG.7. The spread of overfishing ” in the North Atlantic. The years are the approximate dates by which fishing on the stocks indkated scnchd u lcvol heyond. which increases in fidiirig givc n o s u s h i i i d incruust: in total ca.tch. G , c:otl; H , ha,ddock; F , plaice; I?, redfish; I I K , h d r c ; Hg, herr,ing. ‘I

MANAGEMENT O F FISIIERY RESOURCES

15

There remain large stocks of fish which are still substantially unexploited, not only in under-developed areas, such as the oil-sardines (Xardinella spp.) and Indianmackerel (Rastrelliger spp.) in the Arabian Sea, but even in centres of intense fishing, such as the blue whiting (Hicromesistius poutassou (Risso)) off the west coast of the British Isles. However, despite the continuing improvement in fishing methods, the fishing gears in use now are fundamentally the same as those in use fifty years ago-the seines, trawls and hooks and lines. Similarly the types of fish being caught are the same, being those in which the diffused production of the sea has been concentrated either in large shoals, such as anchovies or sardines; on the bottom, such as the cods and flounders; or in large animals, such as tuna and whales, for which a single vessel can catch the animals from a very wide area (for instance one vessel long-lining for tuna can shoot 50 miles of line each day). Thus, despite the vast expanse of the open oceans in relation to the areas a t present exploited, the number of unexploited but practicably exploitable stocks of fish is not large, and unless there is a technical breakthrough which would make the harvesting of new types of resources economically feasible, e.g. the direct harvesting of krill (Euphausia superba Dana) in the Antarctic instead of indirectly via whales (Burukovskii and Iarogov, 1965 ; Stasenko, 1965 ; Osochenko, 1965), or of small oceanic fish, the present rate of expansion of the world fish production cannot be maintained indefinitely, possibly for no more than ten or fifteen years. Thus the proportion of the total world catch which comes from heavily exploited stocks needing proper management will rapidly increase, and it will become increasingly difficult to avoid the problems of proper management of an overfished stock by turning to other, less heavily exploited stocks. The need for proper management policies is therefore becoming rapidly more urgent. I n fact, the frequent failure to achieve proper management in the heavily exploited stocks is having immediate effects in several ways on the catches of lightly fished stocks. Most obviously, much more fishing effort in terms of ships, men and other resources is involved in the overexploited fisheries than would be needed under proper management, and these resources could well be directed to other stocks. Thus, for example, it has been estimated that the total effort spent on some of the major stocks of cod and haddock in the north-east Atlantic has increased so far that substantially the same (or possibly slightly greater) catch could be taken with half to two-thirds of the present level of fishing. If the resources, whether of ships, men or capital, represented by the excess half to one-third of the present effort, could be diverted to other less heavily fished stocks, e.g. in the central and south Atlantic,

16

J . A . CIJLLAND AND

J. E. CARROZ

and assuming that the catch rates of the individual vessels might be rather lower, a t least in terms of value, than when fishing for cod in the north-east Atlantic, their total catch would still be probably around half a million tons. Since the north-east Atlantic catch would remain the same, this half million tons would be a net addition to the total world catch taken a t no extra cost. The wrong type of management can also inhibit the development of fishing on unexploited stocks by discouraging or prohibiting the use of the most effective type of gear. Thus on the west coast of North America restrictions on the use of trawls, introduced to protect the catches of the highly priced halibut and the interests of sports fishermen, have hindered the exploitation of the very large stocks of hake and other species. Also the general failure to achieve good management is very likely to discourage governments or commercial interests from investing large sums in developing fisheries whose long-term future is uncertain. For these and other reasons proper management implies far more than merely ensuring, through appropriate regulations on the amount of fishing or the size offish caught, that the maximum sustained yield is taken from those stocks which would otherwise be overfished, important though this is.

B. Theoretical studies The effect of fishing on a stock of fish has been described by means of a range of models of varying mathematical complexity (see, for instance, Ricker, 1958; Beverton and Holt, 1957; Schaefer, 1954, 1967a; Schaefer and Beverton, 1963; Gulland, 1965, 1967); but the implications for rational inanagement are much the same. I n the absence of fishing a stock of fish will be large, including a relatively high proportion of big. old individuals, and the increase in the total biomass due to growth of the individuals arid recruitment of young fish will be balanced over a period by the losses due to naturaldeaths. When fishing begins the large stock gives large catches to each vessel, even though the total catch is small. Any fishing will tend to reduce the stock abundance,but at the reduced stock levels the losses due to natural deaths will be less than the gains due to growth and recruitment. If the catch taken is equal to this surplus, the stock will not change : any catch greater than this sustainable yield will decrease the stock, while a smaller catch will allow the stock to increase. This sustainable yield is small for very large stocks, because natural deaths are only just less than the growth and recruitment; equally it is small for very small stocks, where the absolute value of the increase due to growth and recruitment will be small. Thus the greatest sustainable yield will be taken a t some inter-

MANAGEMENT O F FISHERY RESOURCES

17

mediate stock level. This level may be achieved by some moderate amount of fishing on all sizes of fish, or pssibbly quite heavy fishing selectively applied to the larger fish. An example of this technique applied to a major oceanic fishery, the fishery for yellowfin tuna in the eastern tropical Pacific, is given in Fig. 8. The effect of fishing is best shown by relating the stock level (in this case measured by the catch per day fishing by a standard vessel) to the amount of fishing (here measured by the estimated number of days fishing). Each point in the diagram corresponds to the data for one year in the period 1934-65; the Figure shows clearly the decline in T o t a l catch,millions o f p o u n d s

1

v ) 3 0

L

a -

a L

Z

c '-

V c

m L'

F i s h i n g e f f o r t i n thousands o f s t a n d a r d d a y s FIG.8. Relationships among fishing effort, apparcnt abundance, and catch for yellowfin tuna i n the eastcrn Pacific Ocean, 1034-66. The points connected by thc solid line are based on apparent abundance mcasurcd by baitboat data only, while the isolated points for 1959-66 are h s e t l on apparent abundancc measiired by data from baitboats and seincrs combinctl. (From I.-A.T.T.C., i966.)

stock with increasing fishing, and the straight line which best describes this decline. Also shown in the diagram are curves connectingthe points with the samc total catch. For the observed line the highest catch is a t the point corresponding to an equilibrium catch of some 90 000 short tons, taken with an amount of fishing, in standard units, of 32 000 days. A more analytical approach is to follow the history of a brood of fish from the time they reach a fishable size, as in the models of Ricker (1958) and Beverton and Holt (1957). At low rates of fishing the fish may survive for a long time, so the average age and size are high;

18

J. A. CULLAND AND J. E. CARROZ

however, the total numbers caught, and the total weight, are small. Equally a t very high rates of fishing, applied as soon as the fish are big enough t o be caught, although the numbers caught will be very large, they will not survive long enough to grow much, so that the total catch will be only moderate, consisting of very small fish. The greatest catch from a given brood is taken by allowing the fish to grow to a reasonable size, either by only fishing moderately hard or by using some selective gear (e.g. trawls with large meshes) which will only catch the larger fish, allowing the small ones t o escape and grow. I n addition, it is not improbable that the average number of young produced by the low stocks when fishing is heavy will be less than those produced from larger stocks, although this is not as obvious as it may seem. Most marine fish produce very large numbers of eggs (sometimes millions), so that even a very small adult stock could produce a large brood, and evidence from some stocks shows that the adult stock can be reduced substantially without any significant reduction in the number of young produced which recruit to the fishery in later years (Beverton, 1962). The number of young produced each year often fluctuates very widely quite independently of changesin the adult stock, and these fluctuations make it very difficult within any particular stock of fish t o determine whether a reduction in the number of adults results, on the average, in any significant reduction in the number of young. This uncertainty has often, in practice, led to the assumption that the number of recruits is independent of the adult stock, i.e. that there is no need for regulatory measures to maintain the adult stock. However, this assumption can lead to disaster for the fishery if in fact it is false. The obvious example of the disasters following a failure t o maintain an adequate breeding stock is that of the Antarctic whales. Since they are mammals, producing only one young every other year, there is no doubt that a reduction in the adult stock would result in fewer young animals recruiting t o the future stock. Under proper management these Antarctic stocks could maintain annual catches of around 6 000 blue whales and 20 000 fin whales : a t present the blue whales have had to be given complete protection, but even if hunted intensively only a few hundred could be caught (Chapmanet al., 1964, 1965). I n the 1965-66 season only 2 300 fin whales were caught, and even this small total will only allow the depleted fin whale stock to rebuild rather slowly. Thus failure of proper management has meant a loss in annual catch of 6 000 blue whales, and 18 000 fin whales, which would have yielded about a quarterof a million tons of oil, and equivalent quantities of whale meat and other by-products. Similar disasters to fish stocks are less well established, but a possible example is the California sardine (Xardinops

MANAGEMENT O F FISHERY RESOURCES

19

caerulea (Girard))fishery, which declined from over half a million tons annually around 1940 to only 3 000 tons in 1963, due to failure of recruitment. It is possible that this failure of recruitment was caused a t least in part by the reduction in the adult stock by the heavy fishing of the 1930s and 1940s (MacGregor, 1964 ; Murphy, 1966). I n other major fisheries uncertainty concerning the relation between adult stock and subsequent recruitment is of immediate practical relevance in considering the present need for management. Thus for the Arcto-Norwegian stock of cod a reduction in the amount of fishing to half the high level occurring in 1965 would, if recruitment were independent of adult stock, result in a slight increase in sustained catch (I.C.E.S., 1966). However, there are definite signs that the recruitment is reduced a t the low stock correspondingto the 1965 level of fishing (Garrod, 1966) ;if so, continued fishing a t the 1965 level could very greatly reduce the stock, and result in sustained catches very substantially below those that could be obtained a t lower levels of fishing. Again, in the Peruvian anchoveta fishery, it is fairly clear that increased fishing will not appreciably increase the yield per recruit and any small increase in yield would be accompanied by a substantial fall in catch per unit effort (Boerema et al., 1965), and therefore it is desirable to discourage any further increase in effort. It is, however, possible that increased fishing, by reducing the spawning stock, will reduce the future recruitment; this reduction in recruitment could well cause a loss in total catch of several million tons per year. I n this case it would be not only desirable, but virtually essential, to prevent any appreciable increase in fishing. It is also conceivable, and consistent with the data a t present available, that reduced adult stocks would, because of reduced competition for food between adults and young, result in increased recruits ; increased fishing might therefore substantially increase the total catch. Having stated the uncertainty, it is not easy to resolve it. Certain theoretical models relating stock and recruitment have been developed and curves relating recruitment to adult stock proposed which ranged from the asymptotic to the parabolic (Ricker, 1954; Beverton and Holt, 1957 ; Radovich, 1962). However, the observed data, in the form of pairs of values of adult stocks and subsequent recruitment, are usually few (accumulatinga t the rate of only one pair per year), and are often very variable, so that the form of the stock/recruitment curve often remains very uncertain (Gulland, 1967). Probably the problems can only be resolved by a better basic understanding of the processes determining the survival from egg to adult, particularly the early larval stages. This will probably require both work at sea-detailed surveys

20

J . A. GULLAND AND J. E. CARROZ

of younger stages-to estimate the basic population parameters both of the young fish themselves and also of other relevant populations, especially the food of the larvae (Ahlstrom, 1954, 1965 ; Baranenkova, 1965), and work in the laboratory-estimation of food requirements of the larvae, the effects of reduced food on growth and survival, etc. This adds up to a substantial volume of research, but it is probably the field in which marine biological research has most to offer in improving the scientific advice on fishery management. Using the techniques outlined previously of estimating the population abundance, its rate of change, and the growth, mortality and recruitment rates, the biologist can draw up, with a greater or less degree of precision, sets of curves relating the total catch from a stock of fish to the amount of fishing and to the sizes of fish caught. These curves form the essential basis of proper management. I n drawing up these curves the biologist has to ignore, in the first instance, many of the complexities of the real situation. Thus the simplest, and most frequently used form of the Beverton and Holt yield equation ignores possibIe changes in the growth pattern, or in the naturalmortality rate. However as the authorsshow, any likely changes in these will not alter the general shape of the yield curves, and hence will not affect the nature of the biologists’ advice concerning a fishery which is to any extent “overfished ”. When, perhaps as a result of this advice, the fishery approaches to what may be its optimum condition, then these complexities, and others such as the interaction between different species, etc., may well have to be taken into account in order to define the optimum more accurately. There are other effects, in particular the precise nature of the relation between adult stock and the subsequent number of recruits, which, as discussed above, may alter the whole shape of the yield curves. However, the direction of the change will be generally known-at larger stocks (i.e. with reduced fishing mortality or increased size of fish caught)the recruitment (andhence future stocks and future catches) will almost certainly be greater than predicted on the basis of constant recruitment. Thus the yield curves, and assessments based on them, assuming constant recruitment, will be conservative, in the sense that they will provide a lower limit to the benefits from conservation actions. These relations between yield and effort and between yield and size of fish caught are interdependent, so that the form of the curve relating the yield to the size of fish caught depends on the amount of fishing. It will, except a t very low rates of fishing, have a maximum, and the position of this maximum will depend on the amount of fishing. The greater the amount of fishing, the greater will be the size of fish a t

MANAGEMENT

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21

which the maximum occurs, and also the greater the catch a t the maximum, i.e. a t high fishing rates most fish will be caught, so that it is worth waiting until the fish are well grown, while a t low fishing rates it is better to start catching them when quite small as otherwise they may not be caught at all. Equally, the relation between the amount of fishing and the catch depends on the sizes of fish caught. At low rates of fishing, the catch will increase nearly in proportion to the increase in fishing, whatever sizes are caught (see Fig. 9). If small fish are caught, the increase in catch will soon become proportionally less than the increase in fishing, and the curve of catch against effort will tend to

FIG.9. The relation between fishing mortality and the averagc long-term catch.

flatten out, reach a maximum a t some moderate level of fishing, and decrease, possibly sharply if recruitment is affected, a t higher levels of fishing. If small fish are protected, e.g. by using large mesh nets, the catch will tend t o continue increasing with increasing fishing to higher levels of efforts, so that the maximum yield will be greater and occur a t higher rates of fishing. If only quite large fish are caught, the catch may continue to increase (but very slowly) with increasing fishing, however intense, and the greatest possible yield from a brood of fish would be taken by waiting until the fish reach optimum size and then harvesting them all. I n open waters such immediate harvesting would require an impossibly large fishing effort, but is, of course, common practice in pond culture or animal husbandry in general. The two families of curves may be combined to give contour diagrams showing the yield for any combination of fishing effort and

22

J. A . GULLAND AND J. E. CARROZ

size a t first capture (Beverton and Holt, 1957 ; Dickie and McCracken, 1955 ; Mako, 1961 ; Misu, 1964). Such curves describe the biological situation, but this is not all that is required for management. I n particular, the value of the catch and the cost of catching it must also be considered. The value of the catch will depend on biological factors such as the size of fish (small fish being nearly always less valuable than medium or large fish), and on their condition-fish which have just spawned, for example, often being not very valuable-as well as on economic factors such as the variation of price with supply. The factors can be introduced into the equation t o give expressions for the catch in value, but to a first approximation it is normally sufficient to take the value as being proportional to the weight caught, though most conservation measures tend t o increase the average size of the fish caught, and hence their average price. Other things being equal (and the results of regulation may well be to make them not equal) the cost of fishing will be closely proportional to the amount of fishing, but little affected by the sizes of fish caught. Therefore, if the size of fish caught can be regulated (and it may not be practicable for some gears, e.g. purse seines),the size should be regulated to give the maximum yield for the current amount of fishing, being adjusted as necessary if the amount of fishing changes. It is not so certain that, for rational management, the amount of fishing on a particular stock should be adjusted to give the maximum catch from that stock, even if such a maximum exists a t a practicable level of fishing. The fact that the well-being of a fishery cannot be measured solely by the total weight of the catch, and that there is a need for an objective of management less narrow than the maximum catch has been pointed out by many authors, both biologists and economists (e.g. Graham, 1943; Beverton and Holt, 1957; Schaefer, 1957b; Bell, 1959; Gordon, 1954; Christy and Scott, 1965; Gulland, 1968b). I n the absence of regulation, the fishery will tend to stabilize a t a level where the value of the catch is about equal to the total costs of catching. If the fish are valuable, and easy to capture, and also if small fish cannot be protected, then it is likely that this equilibrium will be reached a t a level of fishing greater than that giving the maximum sustainable yield. A reduction of effort to the level of the maximum yield should result in an increasein the value of the catch, and reduction of costs, and must therefore be beneficial, but a further reduction is also likely to be desirable. Close to the maximum the curve of catch against effort is very flat, so that a small to moderate reduction in effort will result in a negligible reduction of catch. That is, perhaps 98% of the

23

MANAGEMENT O F FISHERY RESOURCES

maximum catch may be taken with only SOYo of the effort required to take the maximum, and the cost per ton of taking the last 2% would be around ten times that of taking the first 98%. Blmost certainly the resources in ships, men and money in taking the last 2% would be much better employed elsewhere-even when the demand is for fish a t almost any cost there are likely to be alternative and relatively unexploited stocks t o which the surplus effort could be diverted. So long as alternative underfished stocks exist the apparent contradiction between the biological objective of greatest physical yield, and the economic objective of greatest economic yield (cf. Christy and Scott, 1965, p. 219) is valid only if considerationis restricted to the individual heavily fished stock. The greatest physical yield from the oceans as a whole will be possible only if the presently overfished stocks are harvested as efficiently as possible. The objective, therefore, of rational management should be to maintain the fishing effort a t the level giving the greatest net returns (value of catch less cost of capture),i.e. at the level where the marginal cost of adding one unit of effort (one extra vessel) is just equal t o the marginal value of the increase in hhe sustained catch resulting from the extra effort, rather than the marginal value being zero (if the effort is at the level giving the maximum sustained yield), or even negative (if the effort is past the maximum). This is shown diagrammatically in Fig. 10, in which the curve in Fig. 9 relating catch (in terms of weight) to the amount of fishing (basically in terms of the proportion of the stock removed per year) is replaced by a curve relating value of the catch to the cost of catching it. To a first approximation the value of the catch is proportional t o the weight caught, and the cost is proportional t o the amount of fishing. Then the equilibrium position is the point A where the line of equal costs and value cuts the curve. I n this example it is beyond the level of fishing which gives the maximum catch, A,, and a reduction of fishingto produce the maximum sustained yield will also produce a surplus of value over costs equal t o A,&. However, a further reduction of fishing to bring the catch to the point A , will produce an even bigger surplus A$,. This simple statement of the immediate economic aspects of management becomes more complex when considering several stocks of fish, or fishing carried out by several countries. Since each country will have different costs, and set different values to the fish, the optimum position for each country will be different. However, if two countries have been fishing the same stock for some time, without great changes, both will presumably have about the same equilibrium position, so that their optimum positions will also be similar. I n any case, if the total effort has increased beyond the A.M.B.-6

2

24

J. A. CULLAND AND J. E. CARROZ

costs FIG.10. The relation between costs of fishing and value of the catch. Point A , where the line of equal costs and values cuts the curve, is the equilibrium position without regulation. The greatest net return, A,-B,, is obtained by limiting fishing to about one-third of the equilibrium level.

level giving the maximum catch, it will be in the interest of all to reduce the effort, even if the magnitude of the reduction in the effort required to reach the various optimum positions may be different. Difference in national interests, and indeed differences between different groups of fishermen in the same country, are likely to be more serious when several stocks of fish of different species are concerned. No species of fish exists in isolation, but may compete with one species for food, be eaten by a second, and feed on a third, and all these stocks may be exploited by different fishermen whose catches will therefore interact. Also fishermen, while catching one species, may incidentally catch another species which is of primary interest to some other fishermen ; for example, in the North Sea, vessels trawling for herring often catch numbers of small haddock (Sahrhage,1959). In such situations it is normally impossible to take the maximum sustainable yield of all the species being exploited : for instance,the maximum yield of haddock would only be taken if no small haddock were killed by herring trawls, which could only be achieved by prohibiting trawling for herring, and this would reduce the catch of herring (I.C.E.S., 1960). Thus, a unique objective of management cannot easily be defined, though the biologist can, a t least in principle, calculate what the effects of possible regulatory action would be, and hence those regulations can be introduced

MANAGEMENT

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25

which would improve the fisheries of the area as a whole. Thus the damage done by herring trawlers in reducing the haddock catches is less than the extra value of herring taken by the trawlers; therefore restriction of herring trawling to protect the haddock fishery would not be justified when considering the North Sea as a whole. This example also illustrates an important practical difficulty in complex fisheries. I n a simple fishery the restrictions and benefits of regulation can be equitably shared-if the effort should be reduced by 20%, then each group of fishermen can reduce their effort by SOY0, and their share of the catch will be unaltered. I n the North Sea, the losses are being sustained by the haddock fishermen (mainly Scotsmen) and the herring trawlers (from other countries) are unrestricted ; if the biological conclusionshad been different, and herring trawling should be restricted in order t o increase the total North Sea catch, then the losses would all have been t o the herring fishermen, and the gains to the haddock fishermen. These considerations do not, of course, make the need for proper management any less, but do increase the need for the proper quantitative understanding of quite complex biological situations, and for the balancing of the interests of each group of fishermen. They show that while the ultimate objective of fishery management in a region might well be to ensure the greatest total net yield from all the stocks taken together, this objective must be modified to ensure that the restrictions and gains are equitably shared. It may, however, still be attained if there is some system whereby those with the biggest gains pay compensation in some form to those with small gains, or losses.

111. METHODSOF REGULATION A. Types of regulation Any regulation can affect the stocks of fish and future catches only in one or both of two ways : by changing either the total fishing effort (i.e. the fishing mortality, the proportion of the stock caught each year), or the sizes of fish caught. However, a variety of different methods of regulation can be used to achieve one or other of these results ; they include : (a) limitation on the sizes of fish that can be landed ; (b) closed areas ; (c) closed seasons ; (d) limitation on the type of gear ; (e) limitation on total catch ; and (f) limitation on total effort. The effectiveness of these methods must be judged against the objectives of management, which will generally be to achieve the greatest surplus of total value of catch over the total cost of catching it. Thus, regulations to change the sizes of fish caught should not increase the cost of fishing ; regulations aimed at reducing the fishing mortality by some restriction on the amount of fishing, which are intended to

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J. A. GULLAND AND J . E. CARROZ

result in the long run in about the same, or possibly even greater, catches with less fishing, should ensure that the cost of fishing can be reduced roughly in proportion to the reduction in fishing mortality. The need for enforcement must also be considered and a good regulation should be both easy and inexpensive to enforce. An important step towards proper fulfilment of a regulation i s the belief by the fishermen that the regulation is necessary t o produce better catches in the future, and that foreign fishermen are also obeying the regulation (to many fishermen, a foreigner is anyone outside his immediate circle). To reduce this suspicion of “foreigners ”it is important that enforcement is not only effective but also seen to be effective. Lately several international commissions have taken steps towards joint enforcement by inspectors of different nationalities on each other’s vessels. (a) S i z e limits are effective methods of controlling the size of fish removed from the stock for those fisheries where undersized fish which are caught accidentally can be returned to the water alive, or where the fisherman can judge the size of fish before capture. Thus size limits are widely used in lobster (Homarusspp.)androcklobster (Panulirus,Jasus, etc.) fisheries, where the animals are caught in traps, and in whaling, where the gunner can judge the size of the whale quite closely before deciding t o fire the harpoon. I n most fisheries the chances of undersized fish surviving after being returned to the water are small. Even if the fish are alive when brought on deck, the fisherman’sfirst interest is in looking after the fish he is going to market (e.g. gutting them and putting them on ice), and preparing the gear t o catch more fish, and only afterwards may he return the undersized fish to the sea, by which time they will be dead. Even for lobsters a significant proportion of the undersized animalsmay die, either from the direct effort of capture and removal from the sea or from increased exposure to predators (Bowen and Chittleborough, 1966). Where few undersized animals survive, size limits by themselves will only reduce the present landings without helping to improve future catches or landings. However, size limits can be of indirect value by discouraging the fishermen from fishing in areas or with gears that would catch quantities of undersized and hence commercially valueless fish. They can help the enforcement of other regulatory methods, such as mesh regulation or closure of nursery areas, by reducing the economic attractions of infringement. (b) Closed areas and (c) closed seasons can be considered together as they can often be combined, i.e. closure of a certain area for a limited period, have similar effects and, in fact, for some migratory fish may be virtually equivalent. As limitations on the amount of fishing they are

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not likely to be ideal ; the fishing mortality may be reduced, but it is most unlikely that the costs can be reduced in proportion. Initially a closure of, say, 10% of the normal fishing season will reduce the fishing mortality and the running costs (but not the capital costs) by about l o % , but the long-term effects are likely to be the same as for uiiallocated catch quotas, discussed in more detail below, i.e. an increasingly wasteful entry of new vessels, etc., as the catfell per unit effort rises, necessitating a progressive shortening of the season to maintain the effort (mortality) a t the desired level. Closed areas or closed seasons can also be used to control the sizes of fish caught if there are areas where or times when small fish are particularly common ; for instance, the smaller fish of several species tend t o remain in inshore or shallower areas, and closure of these nursery areas would give effcctive protection of these smaller fish. I n addition, there nzay be times or places where the fish are in poor condition (e.g. after spawning), and when closure would allow the fish to recover and thus give a larger and more valuable catch. Such closures (other than a closure of all areas to fishing for a season) are particularly valuable when there are alternative grounds which can be fished profitably while the nursery areas are closed. Otherwise such closures would involve temporary lay-up of vessels, or diversion to an unprofitable fishery, and hence add to the cost of the fishery. (d) Regulation of the type of gear may be divided Into those banning or restricting the use of more efficient, or "damaging ", gears, i.e. aimed a t reducing the fishing mortality, and those, such as mesh regulations, aimed a t controlling the sizes of fish caught. The former types have little justification as a permanent feature of fishery management ; they only succeed in reducing the fishing mortality to the extent that they increase the costs of catching a given proportion of the stock. They may be necessary when increased fishing effort will severely reduce the total catch, e.g. by reducing the number of recruits, but when used they are an implicit admission of failure to achieve any ketter management. Regulation of the gear to control the sizes of fish caught, especially mesh regulation of trawls, are useful and have been introduced widely in the North Atlantic, and also in other areas, such as the East China Sea. Generally, they do not affect the cost of fishing, and indeed a trawl with larger meshes may be cheaper and fish more effectively on the larger fish. The selectivity of many gears, such as purse seines, cannot be altered in practice-they catch all the fish in a shoal-while that of others, e.g. long-lines, can only be altered rather imprecisely-larger hooks tend to catch larger fish, but the relation is far from exact. Even

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for trawls, selection takes place over a range of sizes. If it is desired to take fish of a certain size and bigger, the mesh size can be chosen t o retain half of the fish of the critical size, and release half of them, but some fish considerably smaller will be retained, and others considerably larger than the critical size will escape. If the fisherman sees some of these larger fish escape while he is hauling his net, he will become less willing to use larger meshes, especially as a fish in the water looks larger than one on deck. Because of the range of sizes over which selection takes place, and also because the selection apparently varies with the condition of the fish, the exact material and treatment of the twine in the net (especially the cod-end of the trawl), the magnitude of the catch, duration of haul, etc., the measurement of selection raises many practical problems (Gulland, 1964b). A considerable volume of literature has grown up concerned with the subject (see especially the report of the Joint I.C.N.A.F./I.C .E.S./F.A. 0. Special Scientific meeting (I.C.N.A.F., 1963) which contains papers not solely concerned with selection in trawls, and the reports of the various I.C.E.S. working groups (I.C.E.S., 1964, 1965)). For selectivity experiments outside the North Atlantic, see Aoyama (1961), Cassie (1955) and Longhurst (1959, 1960). A more serious limitation to mesh size and similar regulationsis that many of the fisheries to which they are applied exploit several species, which may be caught in the same haul. Especially when different groups of fishermen prefer different species, i t is impracticable to introduce a mesh size sufficiently large to provide effective regulation for the stocks of the larger species without causing unacceptable reductions in the catches of the smaller species. For example, in the North Sea the biggest catches of bottom-living species are of cod, haddock and plaice, all of which, and the trawl catch as a whole, would be increased by the use of meshes of 100 mm and over-probably for cod and plaice up to a t least 150 mm. However, i t has proved impossible to introduce meshes larger than 80 mm because they would cause losses of the smaller species (especially sole (Xolea solea L.) and whiting (MerZangusrnerlangus (L.)),and these are of major importance to some groups of fishermen. I n any case, even the mesh size (ca 110 mm) which would give the greatest total yield of all species would give considerably less than the sum of the yields from individual species, if the optimum mesh was used for each: ca 80 mni for soles and ca 150 mm for cod, etc. (I.C.E.S., 1957). The most fundamental disadvantage of mesh regulation as the only method of management is that its very success tends to cause changes which lose much of the benefits. The improved catches attract new

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entrants to the fishery, thus reducing the stock again until the returns to the individual fishermen are back to their previous level.

B. Limitation of the amount of Jishing Proper management must therefore include some control over the amount of fishing (the fishing mortality), through direct limitation of total catch or total effort, supported where necessary and practicable by measures such as mesh regulation to control the sizes of fish caught. Some of the practical problems depend on whether the amount of fishing is measured as input (fishing effort, e.g. number of hours fishing by a standard vessel, etc.) or as output (catch),but the more important question as far as many of the economic results are concernedis whether the total amount of fishing is set as a simple overall quota, and when this is reached all fishing stops, or whether individual quotas are set for each group of fishermen. If only an overall quota is set, then everyone will scramble to obtain the maximum share for themselves. This scramble, clearly predictable on theoretical grounds, has occurred in all the major stocks regulated by a simple quota ; for example, the Antarctic whaling (until the nations concerned agreed how to share the quota), or the Pacific halibut (Hippoglossus stenolepis Schmidt) (quotas have generally been set in terms of catch, but the same results may be expected if there is a simple effort quota, e.g. fishing continues until the effort totals 1000 days fishing). As a result of the increasing resources invested, and the correspondingreduction of the length of the season, the cost of exerting a unit of fishing effort rose roughly in proportion t o the reduction in total effort, leaving the total cost of capture about the same. Regulation by means of a simple unallocated quota cannot, in the long run, achieve any substantial reduction of cost, and the benefit of regulation and the reduction of effort will be limited to any increase in catch, though this may be substantial for some stocks (e.g. whales ; Gulland, 1966a). If the total quota is allocated to groups of fishermen within which competition is reduced or eliminated, then the dissipation of the potential benefits of regulation by excessive costs should not occur. Each group of fishermen can organize its activities so as to take its share of the catch a t the least cost, or perhaps take advantage of the benefits of regulation in other ways, e.g. one country might wish for social reasons t o ensure a living for the maximum number of fishermen. As regulation becomes effective and the stocks build up, the difference between the value of the catch and the cost of catching it will increase, possibly very greatly, making the right to a share of the catch increasingly valuable.

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For instance, it is likely that the cost of harvesting the salmon of the Pacific coast of North America could be reduced by about threequarters by having a management policy which allowed the most effective gears to be used. If such a policy could be introduced then the right to catch, say, $1 000 000 worth of salmon would be worth $750 000, the actual costs of capture, including a reasonable return on capital, accounting for only $250 000. Clearly in such a situation tlie problem of allocating the shares of the quota will become acute. In national fisheries these problems are soluble, a t least in principle. There is a central body which can enforce any decision as to how the quota is allocated, and ensure that fishing is not carried out by those with no quota. An attractive method that has been proposed is that the excess allocation should be reduced by charging a very substantial licence fee, equal to nearly the difference between value of catch and cost of capture (e.g. $700 000 for a licence t o take $1 000 000 worth o f salmon). The money obtained from these licences can then be spent in suitable ways: to offset all the cost of management and associated research, to provide research into alternative stocks, for general welfare of tlie fishermen, as well as a contribution to central government funds. The significanceof this scheme is that there is an explicit realization that in a well-managed fishery there may be a very considerable surplus of the value of the catch above the cost of catching it, and a definite decision is made as to who shall get this surplus. To some extent a t least the primary problem of fishery managemen-that fish stocks are a commoii property resource-has been overcome. Though the stocks do not become the property of tlie government or similar body, the government does have a large degree of authorityover the management. It also would have a direct financial incentive in proper management because the surplus of value over costs, and hence the price the fishermen would be prepared t o pay for licences, depends critically on the management methods. Internationalfisheries present much more complex problems in the allocation of the share of the catch, and particularly to countries wishing to enter a fishery for the first time. Many countries are rapidly expanding their fisheries, and would be most, unwilling to accept allocations based directly on the catches in previous years. If the target figures for future years are known, then a t least in principle they form in the short term an equitable and reasonable basis for allocation. At the least when allocating a quota for, say, 1970, the likely national sharesin 1970 in the absence of any regulation or allocationare probably a better guide to allocation than the catches in 1966. For instance, if a country a t present taking 20% of the catch plans to double its fishing,

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and if the othcrs do not change, its share would go up t o about 33%) the share of the others going down accordingly, Quotas allocated in these proportions would then be equitable in the sense that with regulation each country would take the same share of catch as it would have done in the absence of regulation. As the stocks build up under good management the allocation will become more difficult, since fishing will become more attractive and more countries will desire t o increase their fishery. I n whatever way the limit is set, either as a single overall quota or allocated to groups of fishermen, it must be defined either in terms of catch or amount of fishing, e.g. number of days at sea. The objective, in biological terms, is t o achieve a certain fishing mortality, i.e. t o capture a certain proportion of the stock each year. Neither the catch nor the amount of fishing (at least in readily measurable physical terms) will bear an absolutely constant relation to the fishing mortality. The catch corresponding to a desired fishing mortality will depend on the stock abundance,while the amount of fishing effort required to exert a given fishing mortality will depend on the efficiency of the operation chosen as the unit of effort (e.g. a day at sea by a vessel of a certain size) and whether the distribution and behaviour of the fish make them more or less catchable. The catch is readily definable in standard terms (though the increasing numbers of vessels freezing and processing at sea will complicate the precise measurement of the catch in terms of round fresh (live) weight). The definition of fishing effort in standard terms is much more difficult, especially if a limit is set as a single quota requiring the efforts exerted by all the vessels engaged in the fishery t o be expressed in the same terms. The difficulties of effort measurement are less if there is allocation of quota, explicitly or implicitly ; e.g. if all countriesagree to reduce their amount of fishing (as measured in various national units) by a certain percentage, or if limitation is set by issuing licences. I n the latter case the problem of standard measurement of effort may only become serious when a licensed fisherman wishes to improve his efficiency by getting a bigger or newer vessel, or by changing his type of gear. The measurement of the amount of fishing in terms of catch also has its difficulties, chiefly through the need to have a measure of the abundance of the fish stock. Many fish stocks fluctuate widely in abundance due to varying strengths of year-classes, while the quota for a year or a season must be set reasonably in advance of the season. Some system of forecasting the stock is required, and this can usually be done with a varying degree of precision, though sometimes requiring special rescarch effort, e.g. the use of research vessels to survey the 2'

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abundance of fish as yet too small to be fished. Fortunately, a t least with the longer-lived species, moderate errors in setting the quotas in one year can be corrected by suitable adjustment in the subsequent year without appreciable loss, but this does require that the administrative machinery for setting and adjusting the quota is reasonably rapid. The complexities of regulation are further increased when more than one species of fish is considered. Apart from the fisheries on shoalingfish such as anchoveta, herring, etc., few of the other important fisheries of the world are based exclusively on one species. Within a large fishing region the proportion caught of different species varies from ground t o ground, and also often from season to season on the same ground. The needs for regulation of the various species also tend to vary, possibly very widely; the more valuable species may be seriously over-exploited, while others be hardly exploited a t all. Proper management must therefore ensure suitable regulation for the former species, without discouraging fishing on the others, and this is not easy. Thus the success of the regulation of the Pacific halibut might be judged by comparing the catches in recent years of ca 15 000 tons of halibut in the Atlantic (where there are no special regulations to protect the halibut, which because of its potentially long life, slow growth, and high value is especially vulnerable to too heavy fishing) with nearly 40 000 tons in the Pacific, where halibut fishing is strictly regulated. However, it might possibly equally validly be argued that the failure of the halibut regulation is measured by the comparison of the total catches of all species from the areas in which halibut occur in significant quantities. About 1; million tons of other bottom-living fish (cods, redfishes and flounders) are caught annually off the east coast of Canada (T.C.N.A.F. areas 2-4), but until recently only about 60 000 tons were taken off the west coast of Canada and Alaska from the grounds covered by the Halibut Commission. I n the last few years very large catches have been taken in the area by trawlers from Japan and the U.S.R.R. but these countries are not members of the Halibut Commission. A most serious failurein a rather different way, throughnot considering individual stocks but only the overall total, has occurred in Antarctic whaling, where the stocks of blue, fin and sei whales have been in succession the main object of the industry (Fig. 11). Attention did not switch from the preferred to the next most preferred species (blue t o fin, or fin to sei) until the former had been drastically depleted. Although now only the sei whale stocks (the smallest stock of the three) are abundant enough to support any appreciable catches, the actual catches in any one of the past seasons which have so decimated the

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FIG.11. A whale catcher with its catch. A photograph taken in 1952 during the rich years of post-war whaling. (Photo: F.A.O.)

stocks were probably less than the annual catches which could have been sustained indefinitely if all three stocks had been maintained and harvested a t the optimum level. Ideally, therefore, separate limits (catch or effort quotas) should be set for each species, but this raises the problem when two or more species are caught together in varying proportions of what happens when the limit for one species has been reached. Often it is then uneconomic or impracticable to carry on a fishery directed solely on the other species. The experience of the International Whaling Commission does, however, suggest a possible technique for managing multi-species fisheries; that is by setting an overall quota, with catches of each

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species contributingtowards this quota with different weighting factors. For whales these factors were set to give approximately equal economic value, i.e. one blue whale unit (BWU) is equal to one blue whale, two fin whales or six sei whales; but they could equally well be set (and adjusted as necessary) to take into account the need for protection for each species. Thus in, say, 1955 the blue whde stocks were seriously over-exploited, the fin whales probably a t about the optimum level, and the sei whales virtually untouched. Appropriate factors might then have been 1 BWU = 0.5 blue whales = 2 fin whales = 15 sei whales

so that, provided also that the total quota had been allocated to countries or expeditions, there would be strong discouragement t o kill blue whales, and equally a positive inducement t o go after sei whales. This section cannot include all possible methods of regulation, and more especially all the problems likely to arise where they are introduced. Certain general conclusions can be made. Regulations controlling the sizes of fish caught can only be used in limited types of fisheries (e.g. in trawl nets where the mesh size can be changed). I n these fisheries they can have definite, if limited beneficial effects, but the benefits tend to be dissipated unless there is also control of the amount of fishing. The essential step in f ~ dmanagement l is therefore to control the amount of fishing and this will, in an overfished stock, produce a considerable surplus of value of catch above costs. An important decision should be made as to how, and by whom, this surplus shall be taken, otherwise it is probable that the surplus will be dissipated in some form of excessive costs. Rational management usually involves restriction of free entry into the fishery, which may be relatively easy in a national fishery or when a nation has been allocated a national quota, i.e. where there is a central body, having strong authority and powers of enforcement, but is not so easy in international fisheries. For these, limitation of entry may involve such questions as the extent of exclusive fishery limits, and the powers of internationalcommissions, and these are discussed in the following section.

IV. THE MECHANICSOF MANAGEMENTAND INTERNATIONAL LAW Nations can approach the problem of making fisheries management a reality in two ways: first, the national approach, by taking appropriate measures in sea areas off their shores over which they exercise sovereignty (territorial sea) or over which they claim jurisdiction over fisheries (fishery zones), fishermen of other countries usually being completely excluded ; second, the international approach, by setting

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O F FISHERY RESOURCES

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up international commissions with responsibility for somc particular fishery or groups of fisheries on the high seas. These approaches are closely related to the general questions of the law of the sea and to the principles of conservation of natural resources. Since the seventeenth century, when the development of seabornc trade and the emergence of powerful maritime nations led to a shift from the notion of closed seas claimed by a few countries to the concept of open seas, the two basic principles of the law of the sea have been that a strip of offshorewaters should be under the exclusive sovereignty of the coastal state and that the high seas beyond should be free. These principles were originally intended to satisfy and reconcile reasons of national security and the freedom of trade and navigation. But they applied to all activities in both areas and accordingly defined the legal framework within which fishing activities were carried on. The exclusive fishing rights of coastal states off their own shores and the freedom of fishing on the high seas are still the basic principles on which international fisheries law rests ; efforts have, however, been made recently to define more clearly the extent to which these rights and this freedom may be exercised. A. Territorial sea and fishing zones The exact delimitation of the sea where a coastal state enjoys exclusive fishing rights is of great importance, as it has a direct bearing on the regulation of fisheries and in particular demarcates these waters from the high seas where conservation and management problems are clearly international in nature, though the movements and migrations of many species of fish make such man-made limits often unrealistic. Until recently the sea area where coastal states had exclusive jurisdiction over fisheries was, in all cases, co-extensive with the territorial sea, i.e. the belt of sea immediately offshore where coastal states exercise sovereignty to the same degree as over their own land territory. The area claimed by any state as territorial sea, however, varied greatly between individual states, claims of areas from 3 t o 12 nautical miles being most common, though in exceptional cases claims covered a much wider area. The breadth of the territorial sea was considered by the United Nations Conference on the Law of the Sea in 1958. Although the Conference adopted a convention on the territorial sea, including rules on the baseline for measuring its width, no agreement was reached on the width itself (United Nations, 1958). A second Conference was held in 1960 ; there again no agreement was reached (United Nations, 1960). One proposal, which failed to be

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adopted by only one vote of the two-thirds majority required, had a definite influence on subsequent national and international measures. The proposal envisaged : (1) Allowing states to claim as territorial sea an area extending up to 6 miles from the coast. ( 2 ) Allowing states to claim exclusive fishing rights in a fishing zone immediately beyond the territorial sea extending up to 12 miles from the coast. States whose vessels had hahitually fished in the outer 6 miles of the fishing zone (i.e. the entire fishing zone if states claimed a 6-mile territorial sea plus a 6-mile fishing zone) for a period of five years immediately preceding 1 January 1958 would have been entitled to continue such fishing for a period of ten years after 31 October 1960. (3) Allowing a coastal state, subject to certain safeguards, to claim preferential fishing rights in any area of the high seas adjacent to its exclusive fishing zone, when it was scientifically established that a special situation or condition made the exploitation of the living resources of the high seas in that area of fundamental importance to the economic development of the coastal state or for food supplies for its population. Since 1960, several states have enacted legislation providing for an exclusive fishing zone extending to 12 miles from the coast. In addition, bilateral agreements have bccn concluded on the basis of the 1960 proposal and a European Fisheries Convention was signed in 1964. While the Convention does not contain any statement on the breadth of the territorial sea, it does provide that the contracting parties have the exclusive right to fish and exclusive jurisdiction in matters of fisheries within the belt of 6 miles measured from the baseline of their territorial sea ;within the belt between the 6 and 12 mile limit, the right to fish shall be exercised only by the coastal state and by any other contracting parties, the fishing vessels of which have habitually fished in that belt between 1 January 1953 and 31 December 1962. Thc right granted t o the fishing vessels of the other contracting parties is not limited in time, but they may not direct their fishing effort towards stocks of fish or fishing grounds substantially different from those which they have habitually exploited. Furthermore,the coastal state may, under the Convention, regulate fisheries within the 6-12 mile belt, provided that there is no discrimination in form or in fact against duly authorized fishing vessels of other contracting parties. The Convention does not specify that contracting parties will claim an exclusive 1 2 mile fishing zone with respect to all states not parties to the Convention.

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As can be seen, there is today an obvious lack of uniformity in the delimitation of the offshore area where coastal states have exclusive fishing rights. Thus, national claims vary as to the breadth of the territorial sea. Furthermore, in many countries, there is a trend to dissociate fishery limits entirely from the territorial sca. When states establish a fishing zone extending further than the territorial sea, the zone concerned is not always exclusive and fishing rights may be granted, either for a transitional period or without specified time-limit, to fishing vessels of certain other states. Mention should also be made of the recent practice whereby certain coastal states in Asia, without claiming jurisdiction over fisheries, reserve the right t o regulate fishing in a zone contiguous to their territorial sea and exclusive fishing zone, should this be necessary for conservation purposes. Such additional zone usually extends up to 100 miles.

High seas At the beginning of this century it had already been recognized that the living resources of the sea were not inexhaustible and that, in view of the freedom of fishing enjoyed by all nations on the high seas, it would be necessary to ensure the rational exploitation of the resources through international collaboration. At the same time, it became clear that more research was needed into the biological and environmental aspects of fisheries in the interest of this objective. As a beginning, measures to achieve co-ordination of scientific research and to take positive steps in managing the resources were taken on a regional basis. The InternationalCouncil for the Exploration of the Sea was established in 1902 to encourage and co-ordinate investigation of the eastern North Atlantic Ocean, including the waters off Greenland and Iceland. I n 1911 a convention was concluded for the preservation and protection of fur seals and sea otters in the waters of the North Pacific Ocean. The question arose as to whether it was possible to make a global approach to the problem of conservation and management of the resources of the sea by seeking the widest possible agreement not only on the basic principles which should govern all regional conventions but also on the basic rules t o be observed in areas of potential conflict. The League of Nations considered including the exploitation and conservation of the products of the sea among the subjects to be submitted to an international codification conference. The major fishing countries, however, believed that the diversity of the biological, economic and political problems arising in different fishing areas would

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make it preferable t o draw up regulations in relation to the needs of particular fishing areas, by agreement between the nations directly concerned. The general problem of the rules applicable t o the high seas was selected by the United Nations in 1949 for consideration as a topic for codification by the InternationalLaw Commission. The draft articles prepared by the Commission in 1951 contained a provision proposing that it would be the duty of states to accept as binding upon their nationals any system of fisheries regulation in any area of the high seas where an international authority believed that such measures were essential for the protection of the resources against waste or extermination. This international authority was to be created within the framework of the United Nations and could have acted at the request of any interested state. The provision concerned was not, however, retained in the final version of the draft articles submitted to the 1958 United Nations Conference on the Law of the Sea. The 1958 Conference adopted several international instruments, including a Convention on Fishing and Conservation of the Living Resources of the High Seas. The Convention, which came into force in 1966, is the first attempt t o deal with the problem generally on a world scale. Its scope is of necessity limited and i t aims mainly at promoting the adoption of conservation measures and a t providing for machinery designed to facilitate the settlement of disputes. It also contains provisions stressing the special interests of coastal states in the maintenance of the productivity of the living resources in any area of the high seas adjacent to their territorial sea and their right to take part on an equal footing in any system of research and regulation for the conservation of the living resources in that area, even though their nationals do not carry on fishing there. The 1958 Conference fully realized that the Convention referred to above would have to be supplemented by special and regional agreements. It adopted a resolution recommending that the states concerned should co-operate in establishing the necessary conservation measures through international conservation bodies covering particular areas of the high seas or particular species of living marine resources. It also recommended that these bodies should be used, in so far as practicable, for the conduct of negotiations on conservation measures envisaged in the Convention, for the settlement of disputes and for the implementation of agreed conservation measures. I n the resolution, the Conference specifically referred t o the report of the International Technical Conference on the Conservation of the Living Resources of the Sea, which had been convened in 1955 to make appropriate scientific and

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technical recommendations in preparation for the 1958 Conference on the Law of the Sea (United Nations, 1956). The 1955 Technical Conference had come to the conclusionthat the system of international fishery regulation based on the geographical and biological distribution of marine populations seemed, in general, to be the most suitable way of handling these problems. This system was based upon conventions signed by the nations concerned.

B. Xpecialized Jishery bodies Most of the existing internationalfishery bodies were established by conventions conchded after the Second World War. Five of them were set up under the auspices of F.A.O. pursuant to the relevant provisions of its Constitution. Certain fishery bodies were established to cover a particular sea or specified lake or river systems (e.g. the Joint Commission for Black Sea Fisheries or the Great Lakes Fishery Commission). Others were set up to serve a region of the high seas which is precisely delineated by longitude and latitude (e.g. the International Commission for the Northwest Atlantic Fisheries and the North-East Atlantic Fisheries Commission). The area of competence of many fishery bodies, however, is defined only in general terms (e.g. the Eastern Pacific Ocean for the Inter-AmericanTropical Tuna Commission or the Indo-Pacific area for the Indo-Pacific Fisheries Council). The absence of well-defined geographical limits may sometimes be advantageousin that it allows of flexibility in taking account of surveys and investigations into the biology of the species concerned. It should, however, be noted that each time member countries are requested to provide data to co-ordinate or conduct research, or each time a commission needs t o formulate conservation measures, a specific area has to be defined. What seems important is that the area of competence should be large enough to encompass the entire range of the stocks constituting the resource with which the commission is concerned. It may be mentioned in this connexion that most conventions setting up international fishery bodies include in their area of competence the territorial sea of member countries. The great majority of international fishery bodies were set up to deal with sea fisheries. Actually, a glance a t a map delineating, by oceans and seas, their areas of competence, would show that practically all the marine waters of the planet are covered and even, in certain regions, several times over. This should not, however, lead to the conclusion that all the living resources of the sea are the object of scientific investigation and management measures. I n fact, the

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composition, species coverage, functions, powers and activities of internationalfishery bodies vary considerably. The effectiveness of these bodies depends to a very great extent on the participation and collaboration of all the states concerned. Such states would normally be limited to those whose nationals and vessels carry out fishing operations in the geographic area served in the region. The provisions of the basic instruments concerning eligibility for membership do not always make it possible for all these states to participate. I n several cases the fisheries bodies are, as it were, land-based, since only states whose territories are situated in the area of competenee may become members. These include the Regional Fisheries Advisory Commission for the South-West Atlantic and the Regional Fisheries Commission for Western Africa, both set up under the Constitution of F.A.O. A certain number o f conventions do not provide expressly or implicitly for the possibility of later accessions, but this should not necessarily be interpreted as excluding the acceptance of new members. Several conventions provide that membership of the fisheries body is open, under certain conditions, to states other than the coastal states in the area of competence or t o states other than original members. Thus, any states whose nationals participate in fisheries in the area of competence o f the Inter-American Tropical Tuna Commission may become members of the Commission with the unanimous consent of the contracting parties. Only a few commissions are open to any states which adhere to the basic instrument simply by addressing the required notification to the depositary government. They include the International Commission for the Northwest Atlantic Fisheries, the International Whaling Commission, and the North-East Atlantic Fisheries Commission. When the membership of international fishery bodies is open, acceptance of all rights and duties as a member of such bodies is entirely voluntary. Under existing rules of international law, neither the states whose nationals or vessels carry out fishing operations on the high seas in the area of competence of a fisheries body, nor the coastal states in cases where a stock or stocks of fish inhabit both the fishing areas under their jurisdiction and areas of the adjacent high seas, may be compelled t o become full members of the body or to comply with any conservation measure it may formulate. The 1958 United Nations Conferenceon the Law of the Sea could only adopt recommendations on the subject, urging states concerned to co-operate. Many international fishery commissions and councils were set up to deal with all fisheries resources within their area of competence.

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Notable exceptions are the International Whaling Commission, the North Pacific Fur Seal Commission, the International Pacific Halibut Commission, the Inter-American Tropical Tuna Commission, and the InternationalPacific Salmon Fisheries Commission. There are in practice marked differences in the manner in which fishery bodies deal with any particular stock of fish. This depends to a great extent on the functions of the body concerned. A first category of fishery bodies comprises those which deal mainly with the encouragement,promotion, and co-ordination of researchand which, in the course of their activities, may offer advice and make recommendations on the need for conservation measures. Examples of this type of body are the InternationalCouncil for the Exploration of the Sea, the International Commission for the Scientific Exploration of the Mediterranean Sea, and the commissions and councils set up under the Constitution of F.A.O. A second category includes fishery bodies, the main function of which is to formulate conservation measures on the basis of scientific research, but this research is not normally carried out by their own staffs (e.g. the International North Pacific Fisheries Commission, the Joint Commission for Black Sea Fisheries, the North-East Atlantic Fisheries Commission ; the last of these receives its scientific advice from another international body, the International Council for the Exploration of the Sea, included in the first category). A third category comprises the fisheries commissions which formulate conservation measures on the basis of scientific investigations carried out by their own staff. They are the Inter-American Tropical Tuna Commission, the International Pacific Salmon Fisheries Commission, and the InternationalPacific Halibut Commission. Conventions do not always specify the type of conservation and management measures that may be formulated by the international fishery bodies they establish. Detailed listing of conservation measures shows that these are normally confined mainly t o prohibitions and limitations ; these include most of the measures listed a t the beginning of the previous section: open and closed seasons or areas, minimum sizes of mesh of fishing nets, size limits of fish and regulation of the use of certain types of fishing gear, appliances and equipment. I n a few cases, the conservation measures expressly include prescribing a maximum or overall catch limit (e.g. InternationalCommissjoii for the Northwest Atlantic Fisheries, International Whaling Commission, and InternationalPacific Halibut Commission). Few commissions expressly include limitation of effort, and the North-East Atlantic Fisheries Commission places limitation of effort (and catch)in a separate,inactive,

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category of regulations which can only be actively considered after a specific recommendation to this effect has been passed by the Commissioii. Very few conventions list specific measures of a positive nature. An exception is the convention setting up the North-EastAtlantic Fisheries Commission which provides that the Commission may elaborate measures for the improvement and the increase of marine resources, which may include artificial propagation and the transplantation of organisms and of young. Before reaching agreement on the type of conservation measure that needs to be formulated, international fishery bodies normally consider not only the biological and simple economic effects outlined in the previous section, but also the problems of feasibility and enforcement. It should be pointed out that in most cases member countries are not under a legal obligation to comply with the conservation and management measures formulated by fishery bodies. The power of the majority of existing commissionsis limited to making recommendations, either because the convention concerned expressly so provides, or because the conservation measures have to be approved by member countries before they can be applied. I n a few cases a procedure has been evolved to facilitate acceptance of the measures formulated by commissions. These measures may be called potentially binding recommendations or conditional decisions. Thus the North-East Atlantic Fisheries Commission may recommend a number of conservation measures and member countries undertake to give effect t o any such recommendation adopted by not less than a two-thirds majority of the delegations present and voting. However, any member country may object to the recommendation within a specified period, in which case it is under no obligation to give effect to its terms. A somewhat similar procedure exists with respect to the measures formulated by the InternationalWhaling Commission and by the Permanent Commission for the South Pacific. When conservation measures are binding on member countries, each country is required t o ensure their application on the high seas by its own nationals and vessels. There is, however, a trend towards a certain measure of international control. I n fact, several conventions establishing fishery bodies (e.g. the International Pacific Salmon Fisheries Commission, the International North Pacific Fisheries Commission, the International Pacific Halibut Commission, the Japanese-Soviet Fisheries Commission for the North-West Pacific, and the North Pacific Fur Seal Commission) grant to each member country

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the right to control the general application of conservation measures on the high seas as among the contracting parties. They prescribe, with certain differences of detail, a procedure whereby duly authorized officials of any member country may search and seize vessels of other member countries which are acting in violation of the convention or of regulationsadopted under it. Suchvessels must be delivered as promptly as practicable to the authorized officials of the member country having jurisdiction over them. Only the authorities of that country may conduct prosecutions and impose penalties. Though these commissions with interactional control measures a t present in operation have limited membership (a maximum of four countries), efforts to ensure international control are not restricted to commissions with a small membership or a limited species coverage. The Convention for the Regulation of Whaling was amended to enable the International Whaling Commission to deal with methods of inspection, and an internationalobserver scheme has been devised but it has not yet proved possible to bring it into operation. Both the InternationalCommission for the Northwest Atlantic Fisheries and the North-East Atlantic Fisheries Commission have also concerned themselves recently with the international enforcement of regulations in their area of competence and they have the matter under active consideration. International control will become increasingly important, as i t is gradually being recognized that, when scientific evidence calls for measures t o be taken, the purposes of conservation and management can best be achieved by limiting the amount of fishing (fishing mortality) either by control of the fishing effort or by regulation of the amount of total catch. The full benefit from limitation on fishing will, as mentioned earlier, only be achieved with some system of allocation of the total quota, whether of catch or of effort (e.g. days fishing). Several conventions contain provisions on the manner in which the yield from the resources is to be portioned among member countries. The convention setting up the InternationalPacific Salmon Fisheries Commission lays down the principle that the two member countries (Canada and the U.S.A.) should share equally in the fishery and, consequently, one of the tasks of the Commission is to regulate the fishery with a view to allowing, as nearly as practicable, an equal portion of the fish that may be caught each year to be taken by the fishermen of each member country. The convention establishing the North Pacific Fur Seal Commission, which has four member countries, provides for a system of quotas to

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ensure the distribution of the resources which migrate between the territory of certain member countries and the high seas. As all member countries agree to restrict killing of fur seals to the home islands and to prohibit sealing on the high seas in the Pacific Ocean north of the 30th parallel of latitude north, a portion of the total yield is granted to those member countries which do not own any islands on which the seals breed and which otherwise would have no share in the fishery as a result of their agreement not t o engage in sealing on the high seas. Of the total number of seal skins taken commercially each season on land, both the U.S.A. and the U.S.S.R. deliver to Canada and Japan 1.5%) each of the gross take in number and value. The convention setting up the InternationalNorth Pacific Fisheries Commission also contains provisions on the subject, as it embodies rules laying down what is known as the princiFle of abstention. According t o this principle, states not fishing a specific stock in recent years are required t o abstain from fishing this resource when states participating in the fishcries have created, built up, or restored the resource through the expenditure of time, effort and money on research and management, and through restraints on their own fishermen. It should, however, be scientifically established that the continuingand increasingproductivity of the resource is the result of and dependent on such action by the participating states, and that the resource is so fully utilized that an increase in the amount of fishing would not result in any substantial increase in the sustainable yield. Most conventions do not, however, prescribe how- the yield from the resource should be allocated. Internationalfishery bodies have thus to face this problem a t the time of fixing the maximum catch to be taken. For example, every year since 1961, the Inter-American Tropical Tuna Commission has recommended the establishment of a total catch limit of yellowfin tuna in a specified area of the eastern Pacific and the closure of fishing operations a t such date as the quantity landed plus the expected landings of vessels a t sea reach an amount slightly less than the total catch permitted. Under this system, fishing countries can freely compete for a maximum share within the total limit set by the Commission. This required, of course, not only the agreement of member countries but also the co-operation of other countries fishing in the area. As certain countries would prefer to be allotted a national quota, efforts are being made to reach a solution. Antarctic whaling may be cited as an example of a shift from the principle of free competition within an overall catch limit to the adoption of national quotas. While for many years the expeditions from the Antarctic whaling countries took part in what were known as

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whaling Olympics ”, in an effort t o maximize their share of the total quota set by the Commission, the countries started negotiations in 1958 with a view t o agreeing on national quotas. An instrument was signed in 1962 for a four-year period. The overall limits are fixed by the International Whaling Commission, but the arrangements on the distribution of the total catch are made by the countries concerned. The general problem of allocation of the yield from the resources of the sea was considered to some extent by the 1955 International Technical Conference on the Conservation of the Living Resources of the Sea and to a greater degree by the 1958 United Nations Conference on the Law of the Sea. Discussions a t the 1958 Conference centred on the principle of abstention and on the concept of a preferential share for coastal states. No specific provision pertaining to the apportionment of the yield from the resources was included in the Convention on Fishing and Conservation of the Living Resources of the High Seas. The Conferenceadopted, however, a Resolution on the special situation of countries or territories whose people are overwhelmingly dependent upon coastal fisheries for their livelihood or economic development. The membership, area and scope of responsibility and main measures in use of the various Commissions have been set out in P.A.O. Reports (P.A.O., 1966b). Most of these Commissions issue extensive reports which outline not only the progress made in introducing various regulations, but also the results of the scientific research on which the regulations are based. C<

V. PROBLEMS AND PROSPECTS FOR FUTURE PROGRESS A. Achievements of present bodies Any discussion of the prospects for future progress in fishery management must start with a consideration of what progress has been achieved so far. Earlier sections have described the methods of regulation, and the powers and objectives of the Commissions that have been set up. I n these sections it appeared that regulation of the size of animals caught, though in the long run less important than control of the amount of fishing, presented fewer problems. This has been borne out by the experience of most of the international commissions. I n the fisheriesfor which many commissions are responsible little regulation of the size of fish caught is possible. For instance, the Pacific Halibut Commission limits fishing gears to long-lines, which catch the bigger fish, but further adjustmentof the sizes caught is impracticable though fishing on the “nursery” grounds is discouraged by minimum size limits of 5 lb. Where adjustment of size is possible, it has gen&ally received considerable attention from the commission concerned. Thus,

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the InternationalWhaling Commission has set size limits which should protect the small, generally immature, whales, and also, for pelagic operations, almost all the female sperm whales (for this species, which is polygamous, rational management is presumably to limit the kill mainly or entirely to the surplus males). Unfortunately, there is good evidence that these size limits have, at least in some years, been extensively violated; this underlines the need for some system of international inspection or enforcement, especially when the incentive for infringement is large. As the experience of the Antarctic baleen whaling shows (in which infringements of the size limits have probably not been serious), size limits by themselves are very far from being a sufficient method of management. Both North Atlantic Commissions have been deeply involved with control of the sizes of fish caught, especially regulation of the size of meshes in trawl nets, and such regnlations are in force, or in the process of being brought into force, in most of the areas with which they are concerned (see Annual Reports of I.C.N.A.F. and N.E.A.F.C.). I n fact in many areas the limit t o which mesh regulations can be usefully applied, a t least under the framework of the present commissions, is being approached. I n part this is because the present mesh size is the optimum a t the present rate of fishing (this may be so, for example, for the sole in the North Sea), but more often because a further increase in mesh size would be unacceptable for other reasons. Earlier it was shown that the presence of relatively small-sized species of fish (e.g. soles in the North Sea), of which the catch would be reduced if larger meshes were used, prevents the use of mesh sizes which would be much better for the larger species (e.g. cod and plaice). This is one example of the inequitable results of mesh (or in fact any other) regulation likely to occur in a heterogeneous fishery. Another example in a single species fishery is that for cod off the west coast of Greenland, which is fished by both otter trawlers and vessels using hooks and lines; the immediate losses of small fish when the larger mesh is used are confined to the trawlers, but the long-term benefits from increased stocks accrue to both groups of fishermen (I.C.N.A.F., 1966). The net long-term benefits to the liners will therefore always be greater than those of the trawlers. Moderate increases in mesh size (up t o and somewhat above those so far proposed) would benefit both gears, but still larger meshes (up to 170 mm) would increase the total catch, but only at the cost of reducing the catch of trawlers. Since the Comlr\ission’sstatutes contain no provision whereby some of the benefits which the liners would gain can be transferredfrom them to the trawlers, such mesh sizes are clearly unacceptable to the trawler fishermen. They would still be unacceptable

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in a single national fishery if the nationals concerned used, as do the Portuguese. both types of gear. There have also been various practical and administrative difficulties in putting mesh regulation into force-questions of how precisely to measure meshes, the use of extra pieces of netting t o reduce chafing which may also obstruct the meshes, and, particularly, the question of enforcement. These problems should not be underestimated, but good progress is being made towards solving them. So far as it is possible for them to go, regulations of the sizes caught have been reasonably successfully introduced and the major problem facing all commissions is the control on the total amount of fishing. Most of the commissioiis referred to in the previous section have a t least discussed the problem of restricting the amount of fishing, and several have some effective restriction, generally in terms of a limit to the total catch. The success of effort regulations may be gauged by whether they have achieved both the biological objective (to build up the stock, maintain it at the desired level and hence take the optimum catch), and the economic objective (to reduce costs in proportion to the reduction in fishing mortality, and hence achieve the potential surplus of value over costs). An outstanding example of management t h a t is successful on both counts is that of the fur seal (Callorhinzcs uysinus L.) in the North Pacific. The stocks have built up very greatly (Kenyon et al., 1956; Chapman, 1961), so much so that, since to some extent the fur seals eat fish of commercial valuc, it has been argued that they have increased to an undesirable degree when considering the best use of the marine resources of the North Pacific as a whole. Most of the harvest is taken as surplus juvenile males when they are segregated in compact groups on the breeding islands, so that the cost of operations are presumably low. The figures of resultant net economic yield are not available, but 150/, of the q o s s value of several million dollars of the catch from the Pribilofs is sent to Japan and Canada, in consideration for not carrying out seeling on the high seas, and it is doubtful whether the net profit to the U.S. Government (who carries out the operations) is any less. As mentioned in an earlier section, in biological terms the restriction on the catches of halibut off the uest coast of North America has been successful in building up the stocks of halibut after they had been severely depleted ; between 1031 (when regulations first came into force) and 1960 the stocks in different areas increased two t o three times, and the catches rose by up to 50% (Thompson, 1950; I.N.P.F.C., 1 9 6 2 ~ ;Chapman et al., 1962). However, because of the scramble

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by fishermen tro secure the greatest share of the quota, there have not been commensurate economic benefits (Crutchfield and Zellner, 1963). While, as is well known, regulation of Antarctic whaling has not been successful (see Annual Reports of the I.W.C., especially the reports by Committee of Three Scientists and the 14th and 16th Annual Reports; Chapman et al., 1964, 1965), this is more because of the biological characteristics of the stock, which make the penalties for any failure to achieve proper management very severe, than because the InternationalWhaling Commission has been so much less diligent than many of the fisheries commissions. I n fact, catches of Antarctic whales have been restricted since 1947, and this restriction has served to slow the decline in the stocks (Gulland, 1966a). I n addition, the more recent agreements on the division of the quota have served to increase the economic efficiency of the industry, and hence delay the time when the decline in the stocks would bring about the economic collapse of the industry (though it is arguable that the latter, by delaying effective management, may not in the long run be a good thing). These examples, and others where limitations of the amount of fishing have been effected (e.g. in some salmon fisheries in the North Pacific), have certain features in common. First, and probably most important in determining whether restriction can be easily introduced, is that the biological situation is comparativdy simple. Only one species, or a group of closely related species (e.g. of whales, or of salmon) is concerned, and it was clear to all, without the need of detailed scientific research and analysis, that the stocks concerned were being or could be severely affected by fishing, though there was argument, especially for the whales, as t o the extent of the depletion. For salnion there has also been very great argument on the details of the effects of fishing, especially on the quantitative effects of the fishery for them on the high seas (I.N.P.F.C., 1962a,b;Taguschi, 1961;Parker, 1963; Gulland, 1964a). The situation in most cases was also simple in that only a few countries were concerned, and they all generally used the same catchingmethods. A second important point is that the fisheries (using the word t o cover sealing and whaling) were isolated in the sense that the surplus effort resulting from restriction would not, a t least clearly and immediately, be applied to some other, possibly equally heavily exploited stock. I n the North Atlantic the realization that any restriction of effort in a limited area, say in the Barents Sea cod fishery, would result in a corresponding increase in effort in Iceland and other areas, with

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little or no long-term benefit, is one reason why progress on catch limitation has been slow. This suggests that while for biological reasons regulations should be considered separately for each unit stock, i.e. within quite small areas, the implications of such regulations must be considered over much wider areas, so that the area of interest of the regulatory body must be equally wide. For instance,the whole northern parts of the areas of responsibility of the two North Atlantic Commissions (north of the British Isles and Nova Scotia) must often be considered as a single unit. Also important, in the two cases (fur seals and whales) where allocation of the quota has been made, is that the entry of new countries was not likely (for the whaling agreement it was explicitly stated that the entry of a new country would make the agreement on the division of the total quota void). The high cost of a whaling factory ship, and the low state of the stock, discouraged any other country from entering the industry, while for the fur seals the four countries concernedJapan, U.S.S.R., Canada and U.S.A.-are the only ones with easy access to the stocks, though perhaps the problem of processing and disposing of the catch also deters possible new entrants. For the whales, the failure t o achieve the biological objectives in maintaining the stock by setting a sufficiently low quota more than balanced any economic success in taking the quota in an efficient manner, and there has been no surplus; for the fur seals there is a surplus, and it is being successfully achieved. While the fur seals are not owned by anyone, the Government of the breeding islands does have definite powers of management. The whole of the yield is, in the first instance, taken by the managing Government, only later being shared among the other Governments. I n this way some of the disadvantages of the common property nature of marine resources-that they are no one’s direct interest and responsibility to maintain-have been avoided. Another, and in some ways rather surprising, feature is the lack in some of the cases where limitation of the amount of fishing has been achieved, of any economic uniformity among the countries concerned -both the U.S.A. and U.S.S.R. belong to the Fur Seal Commission, while the Antarctic whaling industries included both the rapidly developing industries of Japan and the U.S.S.R. and the declining industries of Great Britain and the Netherlands. The economic attractions of taking the same or greater catch at substantially reduced costs are likely to be so great that any differences in the valuation of the catch, or the breakdown of costs, will make little difference to the desirability of taking action.

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B. The need f o r further research From the experience of the commissions which have already taken action to restrict the amount of fishing, and of the other commissions which are actively considering such action, some of the requirements for achieving full management can be deduced. First, the essential basis of any management is the proper biological understanding of the state of the stocks concerned. Unless the administrators know what the probable effects of regulation on the stock and future catches may be, they have no means of assessing the desirability of taking action. The fishery scientist should be able to provide estimates of the effects of any regulatory measure proposed, not only on the stock directly concerned, but on related stocks. For instance, a complete study of thc fishing on the Peruvian anclioveta (Fig. 12), and the need for regulation of the fishery on it, should include an assessment of the effect of different amounts of fishing on the food available to the guano birds, and hence the likely effects on the guano industry. Theoretically the chain of related stocks, the first preying on the second, which competes

FIG.12. A catch of anchoveta off Peru, which supports the biggest fishery in the ~ o r l d . An estimated 583 660 000 individual fish were taken from a single year-class (Boerema et ul., 1965). (Photo: F.A.O.)

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for food with a third, could be extended almost indefinitely, taking into account the widely ranging movements of many species, so that the scientist should set limits beyond which the possible interactions can, €or practical purposes, be ignored. Any assessment of the effect of proposed regulations, or of the absence of regulations, must be subject to some degree of uncertainty, so that complete scientific advice will include some indication of the degree of uncertainty involved. The nature of the uncertaintiesis such that statistical presentation of confidence limits, etc., are generally not relevant, and the statement has to bc to some degree subjective, including judgments on such things as whether a particular mathematical model is applicable to a given situation. The important question is whether the relative advantages of different regulations (or no regulation) will be changed. For example, calculations may show that in a certain trawl fishery an increase in mesh size will result in an immediate drop in catch in the first year of 5 2 % , followed by an increase %Tithinthree to four years to a level 4.7% above the original level (i.c. regarding the small fish released as an investment, they will nearly as a group double in weight). I n fact, they may rather more than double, making the gain perhaps S%, or the gain may be only 4%, but in any event the larger mesh will give a small gain, and advice in that form can be given t o the regulatory body. Another form of uncertainty is that many stocks fluctuate for reasons quite independent of fishery, e.g. due to variation in year-class strength (Hjort, 1914). I n such fisheries the predictions made are generallynot of the actual catch in the future,but are comparisonsof the catch that would be taken if the proposed regulations were introduced, with the catch taken if different regulations, or if none, were in force. Proper management, therefore, requires good scientific knowledge based on adequate data. They are essential for all stocks, not merely those in immediate need of regulation, since one aspect of proper management is to avoid unnecessary restrictions, and to be sure of this requires a certain minimum supply of data. More important, the proper understanding of a heavily exploited stock depends on the comparison of the characteristics of the stocks (abundance, as measured, say, by catch per unit effort, the proportions of different ages and sizes, etc.) under heavy and light fishing, and therefore requires adequate information from the period when fishing was still light. Though in any fishery a stage could be reached when the possible benefits from improved management based on better scientific information will be less than the additional costs of getting that information,

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this stage is nowhere being approached even in the most intensively studied fisheries. I n many areas even the information on total catches is not available, while other basic data that should be collected routinely (the breakdown of total catch by species and by small areas corresponding to biological unit stocks, the effort involved in taking the catch, the size and age composition of the catch, etc.) are lacking or scarce in nearly all areas. There is, therefore, an urgent need for better collection of these data, as well as more original scientific research in interpreting the data as they become available. The other type of action needed to attain proper management lies in the administrative field. As a preliminary there is probably still need for greater awareness of the very large economic benefits that can arise from proper management and, conversely, of the danger of losing most of these potential benefits even when the regulations introduced are successful so far as the biological effects on the stocks are concerned. This does require some degree of economic analysis, but when a stock is in need of regulation the economic implications are likely to be so obvious, once considered a t all, that the analysis need only be very simple, and even major differences in the economic factors in the countries concerned are likely to be unimportant. What the analysis will show is the magnitude of the net economic yield (possible value of catch, less cost of catching)that could be taken from the stock. The next important decision is how this yield is t o be taken and distributed, and it is this decision for which, with the exception of the special case of the fur seal, there is little administrative machinery. A distinction should be made here between two aspects of the yield from a fishery : the gross physical yield, in terms of fish, and the net economic yield, the difference between the value of the catch and cost of catching it. I n an unmanaged fishery this latter yield tends towards zero or is a t least no more than will provide a reasonable returnon the capital, etc., invested, so that discussions on allocation of yield have generally centred round the allocation of catch, although the potential net economic yield from a properly managed fishery can be very high. However, the differing requirements of various countries may mean that the catch is divided in quite different proportions from the economic yield : a country with a low supply of protein might place its emphasis on having a large share of the total catch, while another country might be more interested in the net economic yield. Thus a coastal state might decide to make use of the fishery resources within its territorial waters by allowing a certain number of foreign vessels to fish in these waters for a suitable fee, rather than forbidding foreign fishing entirely; the coastal state might then take a smaller proportion

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of the catch, but a large proportion of the net yield. Some of the failures to achieve the potential benefits of management may be ascribed to the lack of consideration of the net economic yield, as opposed to the gross catch. M'ithout a more or less explicit decision concerning how the net yield should be taken and distributed, it is almost certain that the potential net yield will be dissipated in excess costs of one kind or another.

C. International marmgement The net yield can be taken explicitly if there is a single managing authorityeither carrying out operationsitself (e.g. the U.S. Government for the Pribilof fur seals) or charging a tax or licence fee. For most commissions, however, the assumption seems to be that the benefit will accrue directly to the fishermen, who will be able to reduce their costs in proportion to the reduction in the amount of fishing. But this desirable state of affairs is unlikely to continue if there is no restriction of entry into the fishery. If fishing becomes as attractive as it should, then new countries will want to join in, and those already participating will want to increase their share. Initially, agreement on the shares of the participating countries may be reached reasonably objectively on the basis of existing catches and plans for the immediate future, but later such a basis will become less and less firm. Again the fur seal is an exception, since the allocation of 15% of the gross take to the potentially pelagic countries, and the rest to the owners of the breeding islands, represents something like the shares of the catch under freefor-all conditions where the land-based operations will have advantages. The so-called abstention principle, whereby a country will abstain from entering any fishery which is being properly managed, is one attempt to restrict new entrants, but is attractive only to the countries with established fisheries. Unless the amount a country considers it stands to lose by being kept out of one fishery is balanced by what it gains in an established fishery in another area, or there is some other incentive for abstaining, it may not become an effective principle. Both the problem of new entrants, and of the shares of established participants may be lessened if the shares can be transferred, as was done in fact, though not in form, through the sale and transfer of factory ships under the Agreement on Antarctic Whaling. This would probably work for countries wishing t o increase their share, and who would prefer to pay for an increased share rather than lose their existing share of the benefits of proper management through breakdown of agreements. This constraint would be less effective for countries entering a fishery for the first time.

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The alternative methods of taking the net economic yield proposed earlier (tax or licences, or a single operating body) would both involve a managing body with very much greater powers than the present commissions. Only in special circumstances would it be feasible for the operations to be carried out directly by the managing authority, and it would be more practicakde for control to be by tax or licence. Since the purposes of such licences would be to reduce the difficulties of allocation of the share of the quota, and of discouragingnew entries, by making fishing only moderately attractive, i.e. t o ensure that the value of the catch is not much greater than the cost of catching plus the licence fee, as regulation becomes effective the licence fee should become substantial. The question of how this large income from licence fees is used will then become very important. Since an immediate redistribution of all the net yield from licence fees among participating countries would not reduce the attractions (and hence also the problems) for new entrants-except for the losses due to administrative costs-a considerable portion of the profits should be shared more widely. The first call on the income might then be to finance all the costs of management, including the closely related research. The profits could also be used for more widely ranging research, not only into the population dynamics of the stocks immediately concerned, and of other stocks in the area, including the development of fisheries on hitherto unexploited stocks, but also more fundamental biological and oceanographic research into more efficient ways of catching and utilizing the potential natural production of fish (at present any improvement in catching techniques only adds to the difficulties of regulation, and in some regulated fisheries is positively discouraged, which is economic nonsense) and into positive methods of increasing the natural production-" farming the sea ". Another part of the profits might go to those actually engaged in fishing, assuming that the managing body did not carry out its own operations directly. If the management of a particular stock was part of a more widespread agreement on fishing (possibly world-wide) then another part of the profits could be shared among all the parties to the agreement. This would give even those not a t present fishing in an area some direct interest in the proper management of that area, and hence make the abstention principle more generally appealing. Finally, the managing body itself might be able to use a share outside the immediate field of fisheries. Thus perhaps on the continental shelf it might be the coastal state andthe money would go to the national treasury, or, especially in the open oceans, the body might be an agency of the United Nations, with the money going to the central

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U.N. budget as suggested by Christy and Scott (1965); for instance, the Ninth General Assembly of the International Union for the Conservation of Nature and Natural Resources approved a resolut.ion urging the early development of a specialized agency under the United Nations for the management and conservation of whales. The possibility that the coastal state should, with international agreement, have some degree of managerial authority over part of a high seas fishery is a quite different concept from a simple extension of exclusive fishery limits. A wide extension of such limits would a t first sight ease the problems of management by removing them from the international to the national sphere. However, it does not seem a practicable solution for many reasons-politically it would be unacceptable t o many countries, and biologically many stocks range over wide areas and cannot be effectively managed by unilateral action in one area. Also, if the fishery limits were applied in the most usual manner of excluding all foreign fishing vessels, possibly with temporary exceptions for nations with traditional rights, many coastal states might not have the economic or technical capacity t o harvest the full potential of the stocks. The potential of such stocks would therefore be wasted by under-exploitation just as much as the potential of some stocks is a t present wasted by over-exploitation. Fuller use in such situations might be achieved by something less than complete banning of foreign fishing, e.g. by charging a licence fee for fishing within the limits. The concept of having t o pay t o fish on the high seas, even to an international body, is not one that will be accepted lightly. The preceding discussion suggests very strongly that without this or some other fundamentally new approach t o management, the full potential net economic yield of the fish stocks of the world will not be attained. The present type of commission is probably capable, given good scientific advice, and a reasonable attitude among its members, of maintaining the stocks with which they are concerned and the catches from these stocks, but not capable of ensuring that the catches are taken a t as low a cost as possible. The wastage involved, and the benefits from proper management, are very large; even a t present the resources wasted in excessive costs of capture in just two groups of stocks-the salmon in the North Pacific and the cod of the north-east Atlanticcould, if rationally utilized, increase the total world catch of fish by perhaps 5%. The present catches of cod in the area could probably be taken with around half the present costs, while, whatever the merits in terms of total catch of taking salmon on the high seas or in coastal waters, none of the methods a t present used seem an efficient way of harvesting an animal which could be persuaded to swim almost inside A.DI.B.-6

3

66

J. A. GULLAND AND J. E. CARROZ

a suitably placed processing plant. This discrepancy between what the resources deployed in fishing do produce, and what they could produce will tend to widen as more and more of the world’s accessible stocks of fish become heavily fished. Without some fundamentally new approach it is doubtful if the fisheries of the world can maintain their recent record of increasing production faster than the increase in world population. VI. ACKNOWLEDGEMENTS The authors wish to acknowledge the helpful comments and criticisms of their colleagues in F.A.O., and of the members of F.A.O.’s Advisory Committee on Marine Resources Research, especially of their chairman,Dr C. E. Lucas, a t whose suggestion the original version was revised for a scientific audience.

VII.

REFERENCES

Ahlstrom, A. H. (1954). Distribution and abundance of eggs and larval populations of the Pacific sardine. Fishery Bull. Fish Wildl. Serv. U.S. 93, 83-140. Ahlstrom, A. H. (1965). A rcview of the effects of the environment of the Pacific sardine. Spec. Publs int. CommnN W . Atlant. Fish. 6, 53-74. Aoyama, T. (1961). Tho selective action of trawl nets and its application to the management of Japanese trawl fisheries in the East China and Yellow Sea. Bull. Seikai Reg. Fish. Res. Lab. 23, 63 pp. Baranenkova, A. S. (1965). Notes on the condition of formation of the ArctoNorwegian tribe of cod of the 1959-1961 year-classes during the f i s t year of life. Spec. Publs int. Commn N W . Atlant. Fish. 6, 397-410. Bell, F. H. (1959). Economic aspects of regulations of the Pacific halibut fishery. I n “Biological and Economic Aspects of Fisheries Management ”,pp. 51-55. University of Washington Press, Seattle. Beverton, R. J. H. (1962). Long-term dynamics of certain North Sea fish populations. I n ‘‘The Exploitation of Natural Animal Populations ” (E.D. LeCren and M. W. Holdgate, cds.), pp. 242-259. Blackwells, Oxford. Bcverton, R . J. H. and Hodder, V. M. (1962). Report of the working group of scientists on fishery assessment in relation t o regulation problems. A. Proc. int. Commn N W . Atlant. Fish. Suppl. 11, 81 pp. Beverton, R . J. H. and Holt, S. J. (1957). On the dynamics of exploited fish populations. Fishery Invest., Lond. (2), 10, 533 pp. Boerema, L. K., Saetersdal, G., Tsukayama, I., Valdivia, J. E. and Alegre, B. (1965). Report on the effects of fishing on the Peruvian stock of anchovy. F.A.O. Fish. tech. Pap. 55,44 pp. Bowen, B. K. and Chittleborough, R. G. (1966). Preliminary assessments of stocks of the Western Australian crayfish, Panulirus cygnus George. Aust. J . mar. Freshwat. Res. 1 7 ( 1 ) , 93-121. Burukovskii, R. N. and Iarogov, B. A. (1965). [Studies on the Antarctic krill in the scope to organize a fishery on krill.] I n “Antarkticheskii krill, biologiia i prornysel ”,pp. 5-17. AtlantiNIRO, Kaliningrad. [In Russian.] Cassie, R. M. (1955). The escapement of small fish from trawl nets. New Zealand Mar. Dept. Fish. Bull. 11.

MANAGEMENT OF FISHERY RESOURCES

57

Chapman,D. G. (1961). Population dynamics of the Alaska fur seal herd. Trans. N . A m . Wildl. Conf. 26, 356-369. Chapman, D. G., Myrhe, R . J. and Southward, G. N. (1962). Utilization of Pacific halibut stocks: estimation of maximum sustainable yield. Rep. int. Pacif. Halibut Commn, 1960, 31. Chapman, D. G., Allen, K. R. and Holt, S. J. (1964). Report of the committee of three scientists on the special scientific investigations of the Antarctic whalc stocks. Rep. int. Whal. Commn 14, 32-106. Chapman, D. G., Allen, K. R., Gulland, J. A. and Holt, S. J. (1965). Report of the committee of four scientists on the special scientific investigations of the Antarctic whale stocks. Rep. int. Whal.Commn 15,47-63. Christy, F. T., Jr., and Scott, A. (1965). “The Common Wealth in 0cea.nFisheries. Some Problems of Growth and Economic Allocation ”, p. 219. Johns Hopkins Press, Baltimore. Crutchfield, T. A. and Zellner, A. (1963). Economic aspccts of the Pacific halibut fishery. Fishery industr. Res. 1( I ) , 173 pp. Dickie, L. K. and McCracken, F. D. (1955). Isopleth diagram to predict equilibrium yields of a small flounder fishery. J. Fish. Res. B d Can. 12(2), 187-209. F.A.O. (1966a). Catches and landings 1965. Y b . Fish. Statist. 20 pp. var. F.A.O. (196613). Department of Fisheries and Department of Public Relations and Legal Affairs, International Fishery Bodies. Papers presented at the first session of the Committee on Fisheries, Rome, 13-18 June 1966. P.A.O. Fish. tech. Pap. 64, 41 pp. Garrod, D. J. (1966). Stock a,nd recruitment data for Arcto-Norwegian cod. I.C.E.S., CM 1966/g:8 (mimeo). Gaskin, D. E. (1964). Return of the southern right whale (Eubalaenaaustralis Derm.) to New Zealand waters, 1963. Tuatara 12(2), 115-118. Gordon, H. S. (1954). The economic theory of a common property resource: the fishery. J . polit. Econ. 62, 124-142. Graham, M. (1943). “The Fish Gate.” Faber & Faber, London. Graham, M. (1956). “Sea Fisheries.” Edward Arnold, London. Gulland, J. A. (1961). Fishing and the stocks of fish a t Iceland. Fishery Invest. Lond. (2), 32(4), 52 pp. Gulland, J. A. (1964a). Review of Parker (1963) 4.”. J . Cons. perm. int. Explor. Mer 29(1), 117-119. Gulland, J. A. (196413). Variations in selection factors, and mesh differentials. J. Cons. perm. int. Explor. Mer 29(2), 155-165. Gulland, J. A. (1965). Manual of methods for fish stock assessment. Part 1. Fish population analysis. F.A.O. Fish. tech. Pap. 40, Rev. 1, 68 pp. Gulland, J. A. (1966a). The effect of regulation on Antarctic whale catches. J. Cons. perm. int. Explor. Mer 30(3), 308-315. Gulland, J.A. (1966b). North Sea plaice stocks. Lub. Leaf. Fish. Lab. Lowestoft 11, 18 pp. Gulland, J.A. (1967). The effects of fishing on the production and catches of fish. I n “The Biological Basis of FreshwaterFish Production” (S. D. Gerking, ed.). Blackwell Sci. Pub., Oxford. Gulland, J. A. (1968a). Recent changes in thc North Sea plaice fishery. J . Cons. perm. int. Explor. Mer (in press). Gulland, J. A. (1968b). The concept of the maximum sustainable yield and fisherymanagement. F.A.O. Fish. tech. Pap. 70,13pp.

58

J . A. CULLAND AND J . E. CARROZ

Hickling, C. F. (1946). The recovery of a deep-sea fishery. Fishery Invest., Lond. 1 7 ~ ) . Hjort, J. (1914). Fluctuationsin the great fisheries of northern Europe viewed in the light of biological research. R app. P.-v. Re'un.Cons. perm. int. Explor. Mer 20, 228 pp. I.A.T.T.C. (1966). Rep. inter-Am.trop. T u n a Commn, 1965. I.C.E.S. (1957). InternationalFisheries Convention 1946. Report of the Ad Hoc Committee established a t the fonrth meeting of the Permanent Commission, September 1956. J . Cons. perm. int. Explor. Mer 23(1), 7-37. I.C.E.S. (1960). InternationalFisheries Convention 1946. Committee on mesh difficulties. Report of the scientific sub-committee presented a t the seventh meeting of the Permanent Commission, November 1958. Rapp. P.-v. Re'un. Cons. perm. int. Explor. Mer 151, 39 pp. I.C.E.S. (1964). Report of the mesh selection working group. Cooper Res. Rep. int. Coun. Explor. Sea 2, 156 pp. I.C.E.S. (1965). Report of the 1962 Iceland trawl mesh selection working group. Cooper Res. Rep. int. Coun. Explor. Sea 3, 42 pp. I.C.E.S. (1966). Report of the Arctic fisheries working group. Annex 1 to the 1965 Liaison Committee report. Cooper Res. Rep. int. Coun. Explor. Sea (R), 15-32. I.C.N.A.F. (1963). The selectivity of fishing gear. Proceedings of Joint I.C.N.A.F./F.A.O. Special Scientific Meeting. Lisbon, 1957, Vol. 2. Spec. Publs int. Commn N W . Atlant. Fish. 5, 225 pp. I.C.N.A.F. (1966). Standing Committee on Research and Statistics. Proceedings for the annual meeting. Appendix 1. Report of the sub-committee on assessments. Redbk int. Commn N W . Atlant. Fish. 1966, 1, 27-53. I.N.P.F.C. (1962a). The exploitation, scientific investigation and management of salmon (genus Oncorhyncus) stocks on the Pacific coast of Canada in relation to the abstention provisions of the North Pacific convention. Bull. i n t . N . I'acif. Fish. Commn 9, 112 pp. I.N.P.F.C. (196213).The exploitation, scientific investigation and management of salmon (genusOncorhyncus)stocks on the Pacific coast of the United States in relation to the abstention provisions of the North Pacific convention. Bull. int. N . Pacif. Fish Commn 10, 160 pp. I.N.P.F.C. ( 1 9 6 2 ~ ) .The exploitation, scientific investigation and management of halibut (Hippoglossus stenolepis Schmidt) on the Pacific coast of North America in relation to the abstention provisions of the North Pacific fisheries convention. Bull. int. N. Pacij. Fish. Commn 7. Kenyon, A. R., Scheffer, V. B. and Chapman, D. G. (1956). A population study of the Alaska fur seal herd. Spec. scient. Rep. U.S. Fish Wildl. Serv. Fisheries, 48, 77 pp. Longhurst, A. R. (1959). Prediction of selection factors in a tropical trawl fishery. Nature, Lond. 184, 1170. Longhurst, A. R . (1960). Mesh selection factors in the trawl fishery off tropical West Africa. J . Cons. perm. int. Explor. Mer 25(3), 318-325. MacGregor, J.S. (1964). The relation between spawning-stock size and year-class size for the Pacific sardine. Fishery Bull. Fish Wildl. Serv. U.S. 6 3 ( 2 ) , 477-491. M.A.F.F., U.K. (1962). Ministry of Agriculture and Fisheries, and Department of Agriculture and Fisheries for Scotland. F ish Stk Rec. 1961, 57 pp.

(a,

MANAGEMENT OF FISHERY RESOURCES

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M.A.F.F., U.K. (1966). Ministry of Agriculture, Fisheries and Food, and Department of Agriculture and Il’isheriesfor Scotland. Fieh Stk Rec. 1965, 39 pp. Mako, H. (1961). Studies on the demersal fish resources in the East China and the Yellow Seas, based on fishery statistics by the market categories in fish size. Bull. Seikai Reg. Fish, Res. Lab. 24, 113 pp. Margetts, A. R . and Holt, S. J. (1948). The effect of the 1939-45 war on the English North Sea trawl fisheries. Rapp. P.-v. R&n. Cons. perm. int. Explor. Mer 122, 27-46. Misu, H. (1964). Fisheries biology on the ribbon fish (Trichiuruslepturus L.) in the East China and the Yellow Seas. Bull. Seikai Reg. Fish. Res. Lab. 32, 1-58. Murphy, G. I. (1966). Population biology of the Pacific sardine (Sardinops caerulea). Proc. CaZq. Acad. Sci. (4), 34(1), 1-84. Osochenko, E. I. (1965). [Economic evaluation of utilization of krill for fishmeal production.] In. “Antarkticheskii kril’, biologiia i promysel ”, pp. 78-83. AtlantNIRO, Kaliningrad. [In Russian.] Parker, R . R . (1963). On the problem of maximum yield from North Pacific sockeye salmon stocks. J . Fish. Res. B d Can. 20, 1371-1396. Parrish, B. B. arid Jones, R. (1953). Haddock bionomics 1. The state of the haddock stocks in the North Sea 1946-50, and at Faroes 1914-50. Mar. Res. 1952 4, 1-27. Radovich, J . (1962). Effects of sardine spawning, stock size and environment on year-class production. Calif. Fish Game 48 (2), 123-140. Rice, D. W. (1961). Census of the Californian gray whale 1959j60. Norsk Hvalfangsttid. 6, 219-225. Ricker, W. E. (1954). Stock and recruitment. J . Fish. Res. Bd Can. 2 ( 5 ) , 559-623. Ricker, W. E. (1958). Handbook of computations for biological statistics of fish populations. Bull. Fish. Res. Bd Can. 119, 300 pp. Russell, E. S. (1942). ‘‘The Overfishing Problem.” Cambridge University Press, London. Sahrhage, D. (1959). Untersuchungen iiber die Vernichturig untermassiger Schellfische durch die deutsche Herringschleppnetzfischerei in der Nordsee. Ber. dt. wiss. Kommn Meeresforsch. 15 (2), 105-131. Schaefer, M. B. (1954). Some aspects of the dynamics of populations important to the management of the commercial marine fisheries. Bull. inter-Am.trop. Tuna Commn 1, 26 pp. Schaefer,M. B. (1957a). A study of the dynamics of populations important to the management of the commercial marine fisheries. Bull. inter-Am.trop. Tuna Commn 2, 245-285. Schaefer, M. B. (1957b). Some considerations of population dynamics and economics in relation t o the management of the commercial marine fisheries. J . Fish. Res. B d Can. 14(5), 669-681. Schaefer,M. B. and Beverton, R. J.H. (1963). Fishery dynamics-their analyses and interpretation. In “The Sea” (M. N. Hill, ed.), Vol. 2, pp. 464-483. Wiley, New York. Shelbourne,J.E. (1964). The artificial propagationof marine fish. I n “Advances in Marine Biology ” (F.S. Russell, ed.), Vol. 2, pp. 1-84. Academic Press, London. Shindo, S. (1960). Studies on the stock of yellow seabream i n the East China Sea. Bull. Seikai Reg. Fish. Res. Lab. 20, 198 pp.

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Stasenko, V. 0. (1965). [Characteristics of rational methods of capture of krill and industrial efficiency of selected fishing methods.] I n “Antarlrticheskii kril’, biologiia i promysel ”, pp. 67-77. AtlantNIRO, Kaliningrad. [In Riissian.] Taguschi, K. (1961). A trial to estimate the instantaneous rate of natural mortality of adult salmon (Oncorhyncus sp.) and the consideration of rationality of offshore fishery. 2 . For red salmon (Oncorhyncusnerka) 1961. Bull. J a p . SOC.scient. Fish. 27, 972-978. Thompson, W. F. (1950). “The Effect of Fishing on Stocks of Halibut in the Pacific.” University of Washington Press, Seattle. United Nations (1951). Proceedings of the United Nations scientific conference on the conservation and utilization of resources. 17 August-6 September, 1949. Lake Success, New York. Vol. 7, Wildlife and Fish Resources. United Nations (1956). Paperspresented at the internationaltechnical conference on the conservation of the living resources of the sea. UN Doc. No. A/Conf. 1017. United Nations (1958). United Nations Conference on the Law of the Sea. Official record, 7 vols. UN Doc. No. A/Conf. 13. United Nations (1960). Second United Nations Confercnce on the Law of the Sea. Official record. UN Doc. No. A/Conf. 19. Wimpenny, R . S. (1953). ‘‘The Plaice.” Edward Arnold. London.

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APPENDIX: INTERNATIONAL BODIES Name of body

Headquarters

Date established and auspices 1902 Conference (now 1964 Convention)

Area of competence

International Council for the Exploration of the Sea (I.C.E.S.)

Copenhagen, Denmark

Atlantic Ocean and adjacent seas (but with particular reference t o the North Atlantic)

International Commission for the Scientific Exploration of the Mediterranean (I.C.S.E.M.)

Monaco

1919 Conference

Mediterranean Sea and adjacent waters

International Pacific Halibut Commission (I.P.H.C.)

Seattle, Washington, U.S.A.

1923 Convention (now 1953 Convention)

Territorial sea of members and high seas off western coasts of Canada and U.S.A., including southern and western coasts of Alaska

International Pacific Salmon Fisheries Commission (I.P.S.F.C.)

New Westminster, British Columbia, Canada

1930 Convention and Protocols of 1937 and 1956

Fraser River and its tributaries ; territorial sea and high seas o f fthe estuary

International Whaling Commission (I.W.C.)

London, 1J.K.

1946 Convention and Protocol of 1956

______~_________-__-_~

_ _ _ _ _ ~ All waters in which whaling is prosecuted by factory ships, land stations and whale catchers under the jurisdiction of members

(Note. This table is based on information available a t l!vi/67) 67

CONCERNEDWITH FISHERY MANAGEMENT Membership

Resources covered

Functions

~

Eligibility

Actual

All

To promote research; to draw up programmes required for this purpose; to publish the results of research carried out under its auspices or to encourage their publication

Any state which signed the 1964 Convention; after its entry into force, any state which makes an application for accession, upon approval of threequarters of the member countries

Belgium, Denmark, Finland, France, Federal Republic of Germany, Iceland, Ireland, Italy, Netherlands, Norway, Poland, Portugal, Spain, Sweden, U.S.S.R. and U.K. Canadaand U.S.A. have indicated that they will apply for membership

Not specified

To promote oceanographic and biological studies

Coastal states in the area of competence

Algeria, France, Greece, Israel, Italy, Monaco, Morocco, Roumania, Spain, Tunisia, Turkey, U.A.R., Yugoslavia

Halibut

To carry out research and to publish results; to adopt conservation measures such as catch regulation, size control, open and close season, vessel and gear control, licensing. A system of internationalcontrol of approved regulations is provided for on the high seas as between members

Signatory states

Canada, U.S.A.

Sockeye and pink salmon

To carry out research;to adopt conservation measures such as catch regulation and gear control ; to apportion catch equally between members. &4system of internationalcontrol of approved regulations is provided for on the high seas as between members

Signatory states

Canada, U.S.A.

To encourage or, if necessary, to organize research ; to adopt conservation measures, such as open and close seasons and areas, size control, catch regulation and gear control. Members may submit objections to conservation measures

Signatory states and any state giving notice of adherence

Argentina, Australia, Canada, Denmark, France, Iceland, Japan,Mexico, Netherlands, New Zealand, Norway, Panama, South Africa, U.K., U.S.A., U.S.S.R.

~

~

Whale stocks

63

S*

APPENDIX: ~

~~~

~

Date established und auspices

Name of body

Hectdqunrters

Indo-Pacific Fisheries Council (I.P.F.C.)

F.A.O. Reg. Office, Bangkok, Thailand

1948 Agreement concluded under aegis of F.A.O. (Article XIV of F.A.O. Constitution)

Inland waters and territorial sea of members and the Indo-Pacificarea (undefined)

International Commission for the Northwest Atlantic Fisheries (I.C.N.A.F.)

Dartmouth, Nova Scotia, Canada

1949 Convention and Protocols of 1956, 1963 and 1965

North-west Atlantic as defined : eastern limit approx. 42"W. latitude ;southern limit approx. 39" N. longitude. The territorial sea of members is excluded

Inter-American Tropical Tuna Commission (I.A.T.T.C.)

La Jolla, California,, U.S.A.

1949 Convention

Eastern Pacific Ocean (not defined)

-

-

General Fisheries Council for the Mediterranean (G.F.C.M.)

Area of competence

-

F.A.O. Headquarters, Rome, Italy

1949 Agreement concluded under aegis of F.A.O. (Article XIV of F.A.O. Constitution)

04

Inland waters and territorial sea of members and Mediterranean Sea and contiguous waters

(continued) Resources covered

Membership

-

Functions

Eligibility

Actual

All

To encourage and co-ordinate research ; to recommend or undertake co-operative research and development projects; to advise F.A.O. and members on fishery matters ;to publish and disseminate information

F.A.O. member nations and, if approved by twothirds majority of the Council, other members of U.N.

Australia, Burma, Cambodia, Ceylon, France, India, Indonesia, Japan, Republic of Korea, Federation of Malaysia, Netherlands, New Zealand, Pakistan, Philippines, Thailand, U.K., U.S.A., Vietnam

All, but with particular referenceto cod group, flatfish and rosefish

To obtain and collate scientific and statistical information; if necessary, to carry out research;to adopt conservation measures such as open and close seasons and areas, size control, gear control and catch regulation. Protocols to the 1949 Convention were signed in 1965 to facilitate the entry into force of conservation measures and to enable the Commission to make proposals for national and internationalmeasures of control on the high seas as among members

Signatory states and any state giving notice of adherence

Canada, Denmark, France, Fed. Republic of Germany, Iceland, Italy, Norway, Poland, Portugal, Roumania, Spain, U.K., U.S.A., U.S.S.R.

Yellowfin and skipjack tuna, fish used as bait for tuna and other fish taken by tuna vessels

To carry out research;to appraise scientific information; to collect statistics on catches and fishing activities ; and to recommend conservation measures to members

Signatory states and other states by unanimous agreement of contractingparties

Costa Rica, Ecuador, Mexico, Panama, U.S.A.

All

To encourage and co-ordinate research ;to recommend or undertake co-operative research and development projects; to advise F.A.O. and members on fishery matters ;to publish and disseminate information

F.A.O. member nations and, if approved by twothirds majority of the Council, other members of U.N.

Cyprus, France, Greece, Israel, Italy, Lebanon, Libya, Malta, Monaco, Morocco, Spain, Tunisia, Turkey, U.A.R., U.K., Yugoslavia

65

APPENDIX: Name of body

Headquarters

Date established and auspices

Area

of

competence

International North Pacific Fisheries Commission (I.N.P.F.C.)

Vancouver, British Columbia, Canada

1952 Convention

Permanent Commission for the South Pacific

Lima, Peru

1952 Agreement

Japanese-Soviet Fisheries Commission for the North-West Pacific

Meets in member countries in rotation

1956 Treaty

All waters of the North-West Pacific Ocean, including the Sea of Japan,the Sea of Okhotsk and the Bering Sea. The territorial sea of members is excluded

Commission for Fisheries Research in the Western Pacific

Peking, Chinese People’s Republic

1956 Convention

Western Pacific Ocean, including the Sea of Japan, the Yellow Sea and the East and South China Seas. The territorial sea of members is included

North Pacific Fur Seal Commission (N.P.F.S.C.)

Washington,

1957 Interim Convention and Protocol of 1963

North Pacific Ocean

U.S.A.

All waters of the North Pacific Ocean including the adjacent seas. The territorial sea of members is excluded

_______ South Pacific (not defined)

(Note. Internationalagreements on the conservation of N. Pacific fur seals date from 1911.)

66

(continued) Resources covered

Membership Functions Eligibility

All, but with particular reference to halibut, herring and salmon

To study fish stocks and determine stocks requiring conservation measures ; to administer the abstention system ;to compile and study records submitted by members ;and to recommend conservation measures. A system of international control of measures accepted by members is provided for on the high seas

All

To encourage research ; to advise members on fishery matters; to adopt conservation measures such as open and close seasons and areas, protected species, gear control. Members may submit objections to conservation measures

All, but with particular referenceto salmon, trout, herring and crab

To prescribe fishing methods ; to regulate Lhe catch of certain species ; to determine statistics required; and generally to make recommendations concerning the preservation and increase of fishery resources in the area. A system of international control of conservation measures is provided for on the high seas as between members ___~ To prepare plans for joint research ;to organize exchange of information;to elaborate and to recommend Conservation measures

Signatory states

Actual Canada, Japan,U.S.A.

__-_____ Signatory states Chilc, Ecuador, Peru

-

All

Fur seals

To formulate and co-ordinate research programmes; to determine nnniber of seals to be marked ;to consider possibility of pelagic sealing and t o make recommendations thereon. A system of international control is provided for on the high seas as among members

Signatory states

Japan,U.S.S.R.

_____ Signatory states and, Chinese People’s Republic, Mongolia, with the agreement of North Korea, North all ContractingParties, Vietnam, U.S.S.R. any state in the Western Pacific basin Signatory states

Canada, Japan,

U.S.A., U.S.S.R.

67

APPENDIX: Name of body Joint Commission for the Conservation of Seals in the North-East Atlantic

Headquarters Meets in member countries in rotation

Date established and auspices

Area of competence

1957 Agreement

North-east Atlantic Ocean east of Cape Farewell, namely the Greenland and Norwegian Seas, the Denmark Strait, the area of Jan Mayen Island and the Barents Sea L

North-East Atlantic Fisheries Commission (N.E.A.F.C.)

London, U.K.

1959 Convention

Joint Commission for Black Sea Fisheries

Meets in member countries in rotation

1959 Convention

Regional Fisheries Commission for Western Africa (R.F.C.W.A.)

Not yet fixed

1961 F.A.O. regional body (Article VI of F.A.O. Constitution)

Inland waters and territorial sea of members and waters of south-east Atlantic (not defined)

Regional Fisheries Advisory Commission for the South-West Atlantic (C.A.R.P.A.S.)

F.A.O. Reg. Office, Rio de Janeiro, Brazil

1961 F.A.O. regional body (Article V I of F.A.O. Constitution)

Inland waters and territorial sea of members and waters of south-west Atlantic (not defined)

Joint Commission for Fisheries Cooperation

Meets in member countries in rotation

1962 Agreement

Not defined (the purpose of the Agreement is t o promote co-operation in marine fishing generally)

All waters of north-east Atlantic and Arctic Oceans and their dependent seas, as defined : western limit approx. 42" W. longitude, southernlimit 36" N. latitude, eastern limit 51' E. longitude. The Baltic and MediterraneanSeas are excluded ~

~ black Sea

_

_

_

-___

_

~

I

88

1

,

(continued) Resources covered

Membership Furactions Eligibility

Actual

Greenland seal, hooded seal and walrus

To propose research programmes to be carried out by members independently or jointly ;to recommend conservation measures and, if necessary, to make proposals concerning implementation of approved regulations

Signatory states and with the consent of Contracting Parties, any state interested in the regulation of hunting operations

Norway, U.S.S.R.

All

To keep all fisheries under review ;to recommend conservation measures such as open and close seasons and areas, size control, gear control and improvement of resources generally. Members may submit objections to conservation measures

Signatory states and any state giving notice of accession

Belgium, Denmark, France, Fed. Republic of Germany, Iceland, Ireland, Netherlands, Norway, Poland, Portugal, Spain, Sweden, U.K., U.S.S.R.

All

To co-ordinate the planning of research ;to develop co-ordinated measures for regulating fisheries and developing commercial fishing ; to recommend conservation measures and t o prescribe size limits of fish

Signatory states and other Black Sea states giving notice of accession

Bulgaria, Roumania, U.S.S.R.

All

To advise F.A.O. and members on fishery matters ; t o encourage co-operation in fishery exploitation, to promote research, liaison and discussion

F.A.O. member nations with territories in the region or responsible for international relations of non-self-governing territories in the region

Cameroon, Congo (Brazz.), Congo (Kinshasa),Gabon, Ghana, Guinea, Ivory Coast, Liberia, Mauritania,Morocco, Nigeria, Portugal, Senegal, Spain, U.K.

All

To advise F.A.O. and members on fishery matters ; t o encourage co-operation in fishery exploitation, to promote research, liaison and discussions

F.A.O. member nationsof the American continent whose territories have coasts bordering on the western Atlantic Ocean south of the Equator

Argentina, Brazil, Uruguay

All

To prepare plans for scientific and technical co-operation and mutual assistance in the development of fishing in the open sea ;to organize the exchange of experience and information;to make recommendations on fishery matters

Signatory states (however accessions have been accepted)

Bulgaria, Dem. Republic of Germany, Poland, Roumania, U.S.S.R.

-

69

APPENDIX Name of body

Headquarters

Date established and auspices

Area of competence

Japan-Republic of Korea Joint Fisheries Commission

Meets in member countries in rotation

1965 Agreement

Sea areas of mutual interest, including joint control zones as defined and joint resources survey zones

International Commission for the Conservation of Atlantic Tunas (I.C.C.A.T.)

To be determined

1966 Convention

All waters of the Atlantic Ocean, including the adjacent seas

70

(continued) Resources covered

Membership

___~

Functions

Eligibility

Actual

All

To recommend research;to recommend measures concerning fishing operations, conservation measures and approprkte penalties ; to review situation as regards joint control zones and joint resources survey zones

Signatory statcs

Japan,Republic of Korea

Tuna and tuna-like fishes and other species exploited in tuna fishing

To collect and analyse statistics ; to promote and co-ordinateresearch ; to rccornmend conservation measures

States members of U.N. or of any specialized agenry

Signatories of Convention as a t 30th March 1967 : Brazil, Japan, Republic of Korea, Spain, U.S.A.

71

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Adw. mar. Biol., Vol. 6, 1968, pp.73-270

A GENERAL ACCOUNT OF THE FAUNA AND FLORA OF MANGROVE SWAMPS AND FORESTS IN THE INDO-WEST-PACIFIC REGION WILLIAMMACNAE Department of Zoology, University of the Witwatersrand, Johannesburg,South Africa I. Introduction ,. .. .. .. .. .. .. .. .. 74 A. The Word "Mangrove " . . .. .. .. .. . . 75 B. Early Historical References . . . . .. .. .. . . 76 C. Indo-west-Pacific Shores .. .. .. .. .. ,. 77 D. Sea-shore Plant Associations .. .. .. .. ., 85 11. Zonation of Mangroves . . . . .. .. .. .. .. . . 89 A. The Landward Fringe .. .. .. .. .. 91 B. Zone of Ceriops Thickets .. .. .. .. .. .. 103 C. Zone of Bruguiera Forests . . .. .. .. .. . . 105 .. .. .. .. . . 108 D. Zones of Rhizophora Forests E. Seaward Avicennia Fringes . . . . .. .. .. .. 112 F. Sonneratia Zone .. .. .. .. .. .. . . 115 G. Variations .. .. .. .. .. .. .. . . 118 H. Mangrove Soils .. .. .. .. .. .. . . 121 I. Control of Zonation . . . . .. .. .. .. . . 124 111. Adaptations Shown by the Flora .. .. .. .. .. . . 136 A. Adaptations to Growing in Ill-consolidated Muds . . ,. 136 B. Specializations of Stems and Leaves .. .. .. . . 140 C. Relationship betwccn the Mangrove Root and Shoot Systems . . 144 .. .. .. .. .. .. .. . . 145 D. Viviparity E. Succession .. .. .. .. .. .. .. . . 148 .. .. .. 150 IV. Distribution of Terrestrial Animals within the Mangal A. Birds Associated with Mangals .. .. .. .. . . 153 B. Amphibians and Reptiles .. .. .. .. .. .. 156 C. Mammals .. .. .. .. .. .. .. .. 157 D. Insects.. .. .. .. .. .. .. .. .. 157 V. Distribution of Marine Animals within the Mangal . . . . . . .. 165 .. 165 A. Vertical Zonation Affecting Tree Dwelling Animals B. "Horizontal "Zonation through the Mangal . . .. ,. 167 VI. Specializations Shown by the Fauna . . .. .. .. .. .. 181 A. Birds, Mammals, Reptiles and Amphibians .. .. . . 181 B. Insects.. .. .. .. .. ,. .. .. . . 182 C. Marine Animals .. .. .. .. .. .. .. 184 VII. Geographical Distribution .. .. .. . . .. .. . . 219 A. Extratropical Extensions of Mangroves and their Associated Fauna .. .. .. .. .. .. .. . . 219 .. .. .. .. .. 222 B. Biogeographical Comment . . 73

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VIII. Uses Made by Man of the Mangal and Its Products A. Uses of the Timber . . .. .. .. B. Pond Culture of Fish and Prawns . . . . C. Reclamation . . .. .. .. .. D. Salt Production .. .. .. .. IX. Acknowledgements .. .. .. .. .. X. Bibliography and References . . .. .. ..

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Tissue of no seam and sk i n of no scale .she weuves this: Dream of a huntsmanpale That in his antlered Mangrove waits Knsnared ; And I cannot touch him. From Virginia R. Noreno,

Batik Maker ".A s i a Magazine, Hong Kong, 23 January1967.

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It has been said of many ecological papers that since there is no theory of ecology it does not really matter whether they were written five years ago or five years hence. Much descriptive ecology certainly comes under this censure and so may the review which follows. Yet the association of trees and of animals which constitutes a mangrove swamp is an association of which little has been written. We know what trees grow there and what forms the shrub layer ; we do not know the whole story of how these plants cope with the variables in the environment. We know something of some of the animals which are associated with mangroves but we know practically nothing about most of them. We do not know why they are there, unless i t be that they seek shade. We do not know how most of them live. We do not know why some genera have undergone a very wide degree of local speciation often almost parochial, nor why others have maintained a singleness of species which is remarkably widespread. What we do know is summarized below and pointers are given to where more research would be useful.

I. INTRODUCTION Mangroves are trees or bushes growing between the level of high water of spring tides and a level close t o but above mean sea-level. They range all round the oceans of the tropics, only on sheltered shores, a n d they penetrate into the estuaries of rivers where salt water penetrates. Mangrove forests reach their maximum development and greatest luxuriancein parts of South East Asia, Malaya, Sumatra and parts of Borneo where rainfall is high and not seasonal, b u t they occur as scrub thickets even on desert shores. Within these forests live a host of animals, often many individuals of a small range of species and genera. Some of these are derived from

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the land, but most are from the sea. Of the land animals, roosting flocks of fruit bats, fishing and insectivorous birds and many insects are conspicuous. Of the marine animals, crabs and molluscs live permanently in the forest, and prawns and fishes come in on the tide to feed on the apparently abundant nutriment provided by the mangrove soils. The mangrove swamp is clearly one route from sea to land. It is a route followed by the most primitive of the pulmonate snails (Morton. 1955), by land crabs (Harms, 1929, 1930) and perhaps is attempted by some fish. But there seems to be 110 way by which it can be used by land animals to invade the sea. It is also a route from the sea to fresh water as indicated by several neritid snails, and from fresh water towards the sea as indicated by its invasion by various aquatic insect larvae. I n South East Asia man uses mangrove areas for the establishment of ponds for the culture of fish and prawns, and for timber. In East Africa mangroves are exploited for timber alone. A. The word ''mangrove " The English word "mangrove "is commonly used in one or other of two senses. It may be applied to a community of trees or shrubs which grow in the sea, or it may be applied to any one of the individual species which constitute that association. I n the latter sense i t is usual to restrict it to the woody shrubs or trees. The word is of doubtful origin and there is no good record of when it first came into use. It is usually considered to be a compound of the Portuguese word mangue with the English grove. I n Portuguese the word mangue is used in the second of the two senses given above, i.e. it is a mangrove tree or bush; the community is termed mangal. The French manglier is akin and also applies to the individual kinds of tree; pale'tuvier and more recently mangrove are used for the community. All these may be akin to the Malay manygi-manggi, a word not used today in Malaya but persisting in eastern Indonesia where it is used in Ambon for Avicennia (Bakhuizen van der Brink, 1921). Dutch uses vloedbosschen for the community and mangrove for individual kinds of tree. German use seems to follow the English. To avoid confusion I shall use the word mangal when dealing with the forest community, and the word mangrove for individual kinds of tree. The languages of South East Asia distinguish individual trees and tend to apply the name of one or other of these to the community. The name usually chosen for the community is that applied to the genus

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Rhizophora, which implies that this genus of trees is the most important to these people. B. Early historical references A detailed account of the references to mangroves in European literature is given by Bowman (1917), much of it repeated by Davis (1940). Bretzl (1903) made a study of the references in European classical literature and compared the plants mentioned with those occurring,in his own day, along the shores of the Red Sea and between the Indus delta and the Persian Gulf. Bakhuizen van der Brink (1921) mentions that an inscription found in the Wadi Hamanat on the old caravan route between Koptos and Kosseir mentions mangroves on the Red Sea. The inscription dates from the Egyptian king Assa (3580-3536 B.c.). Theophrastus in his “Historia Plantarum ” (305 B.c.) quotes widely from the reports given by Aristobulus of the voyage by Nearchus in 325 from the Indus delta to the Persian Gulf while Alexander the Great made the journey overland. Nearchus describes trees around 14 m (45 ft) tali, in blossom with white flowers scented like violets, growing in the sea and with trunks ‘‘held up by their roots like a polyp ”. The leaves are described as being like those of a laurel. Such a description would apply to Rhizophora. Pliny in his “Historia naturalis”(A.D. 7 7 ) quotes this and adds that similar trees occurred along the Red Sea. Plutarch in his “Moralia ” ( A . D . 7 0 ) is much concerned with the problem as to how these trees nourish themselves from sea water. Arrian in the “Anabasis ” (A.D. 136) gives a few sentences about trees that grow in the sea. Theophrastus also gives a description of a mangrove swamp or mangal with its creeks through which a boat may pass, but none of the other authors took up this point. Arrian’s mention of mangroves is the last until the Middle Ages. Abou’l Abbas en-Nabaty, a Moorish botanist living in Spain, gave in 1230 an account of a journey through Arabia, Syria and Iraq. His book is no longer extant but one of his pupils quotes from it and from other Moorish and Arab botanists. References t o Rhizophora are clear, it is called by them kendela, a name cognate with the Latin candela, and this name persists in Arabic and Swahili to the present day. (This name, which bears reference to the shape of the seedling, has been given to the least common mangrove genus of the Rhizophoraceae, Kandelia.) These Moorish authors describe how the bark of Rhixophora is used in tanning-a use still current-and ascribe to it medicinal virtues. Reference is also made to Avicennia which they call quorm.

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The next mention of mangroves comes from the reports of the sixteenth-century explorers. Aviedo first described the American mangroves in 1526, but not till 1678 do we find accounts of Indian Ocean mangroves in van Rheede’s “Hortus malabaricus ”. John Ray (1693) gives a sound account drawn from various travellers’ tales, and from then on references become more common so that by the middle of the eighteenth century it was possible for Linnd to give modern names to several species. All these accounts leave many questions unanswered. Nearchus described trees of around 14 m (45 f t ) tall ; yet, if Bretzl’s account is to be accepted, and there is no reason to doubt him, no trees of this height occurred in 1900 anywhere along these shores. Only scrub mangroves occur too, nowadays, along Red Sea shores. Where have the tall trees gone? We know that, for the most part, the Ancients never planted trees, other than fruit trees ; we know that the Arabs and the Persians also never planted trees, yet they built ships and houses in which timber was important. Mangrove timber is still the basis of much Arab domestic architecture, and is collected from the mangrove forests of East Africa. The Arabs sail ships which are known in English by the name of dhow, a word of unknown origin: masts of these dhows are frequently made from the trunk of a mangrove tree, either of Sonneratia, of Rhizophora or of Bruguiera-all trees which give a long, clean, tapering trunk. One is tempted to suggest that the handy occurrence of mangrove trees on Red Sea shores and along the Persian Gulf provided the timber for the first sea-going ships. But no one tells us how, or from what wood, these early boats were made.

C. Indo-west-Pacific shores Mangroves grow only on sheltered shores. Within the tropics many, if not most, of the shores of the Indo-west-Pacific biogeographic region are protected by reefs of coral lying along the edge of the continental shelf. Such reefs, and in certain regions a multiplicity of islands, break the force of the waves so that considerable lengths of coastline, both of continents and of large islands, are not subjected to strong wave action. Other shore lines tend to run parallel to the direction of the prevailing winds and so they, too, come to be, in fact, sheltered shores even though on a map they appear to be open t o the sea. South of the tropics, but within the trade wind zones of the Southern Hemisphere, long stretches of high sand dunes run along the eastern coasts of Africa, Australia and Madagascar. These dunes are ancient formations and reach altitudes of 60 m a t Durban Bluff, of 114 m a t

FIG.1. Map of the Indo-west-Pacificbiogeographic region. Coastlines where mangroves occur have been heavily outlined. Localities mentioned in the text are indicated.

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Inhaca Island off Lourenyo Marques, and of 279 m on Moreton Island a t the same latitude in Queensland. Rivers entering the sea in these dune regions are deflected northwards and large bays develop behind the growing tips of the dune systems. The sheltered parts of Durban Bay, of the Bay of Lourenpo Marques and of Moreton Bay are, or until recently were, occupied by well-developed and well-zoned mangals. Farther north reefs of coral develop off shore. Off Africa, reefs, mostly fringing reefs, are more or less continuous from Pebane in north central Mopmbique to Somalia. Off Australia, the Great Barrier Reef is much better known. I n many areas the sea is shallow and the short but quite high waves disturb the bottom close to the beach making the sea turbid so that corals are rare. The shores do not develop high dunes ; instead, one finds systems of cheniers, low dunes rarely reaching elevations of 20 m and running approximately parallel to one another and to the present shore line. These may occur in several sequences (see Fig. l l ) , especially where the deltas of large rivers bring down, or have in the past brought down, quantities of alluvium which is sorted by wave action and the sand deposited on the cheniers and the finer material elsewhere. Such a succession of cheniers seen .from the air resembles a series of giant ripple marks. The most seaward chenier is typically colonized just above high water mark by a narrow zone, often only one to four trees in width, of Casuarina equisetifolia L. These trees also occur in a similar single series on relatively stable sandy coastlines along oceanic or other shores exposed to wave action. The most famous example of this occurs along almost the entire east coast of the Malay Peninsula (Watson, 1928). Shorter examples are common on all suitable tropical shores of the Indo-west-Pacific. These narrow zones of Casuarinq equisettfolia give the impression of having been planted by man. Why else would they be so regular? Although provision of wind breaks and dune binding has been achieved by planting these trees on coastal dunes on Mauritiusbetween 1945 and 1950 (Sauer, 1962), these long, continental, very narrow belts of Casuarina are not there by human design. Small rivers are deflected northwards in the southern hemisphere and southwards in the northern by the growing tips of cheniers or beach ridges and they may be closed off. Between the successive cheniers the lows are sometimes under freshwater influence, becoming extensive swamps of reeds, sedges or papyrus ; or open ponds ” with water lilies, floating ferns mainly species of Azolla, and nowadays the alien water hyacinth (Eichhornia crassipes (Mart.) Solms.), imported from America. Sometimes the lows are brackish,under marine influence l1

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by way of estuaries of the small rivers or as a result of seepage through the base of the chenier, then mangroves encroach and may develop into dense forests. Mangrove forests of this nature are extensive to the north and south of Beira, and in the region formed by the vagaries in the Holocene of the deltas of the Zambezi and neighbouring rivers. Along the shores of Sarawak and other parts of Borneo mangroves occur on shores facing the South China and Java Seas. But these shores, by virtue of their direction, run in such a way that they are sheltered from the strongest winds that prevail in those seas. Winds of gale force are rare in the belt within a few degrees of and on either side of the Equator in the Indo-Australianarchipelago. Elsewhere mangroves are associated with estuaries. Some of the largest mangrove forests in East Africa are associated with the deltas of the Zambezi and Rufiji rivers. The most extensive mangals in the world are associated with the deltas of rivers entering the Bay of Bengal, the Straits of Malacca-both on the Malayan and Sumatran sides (the Straits of Malacca, in fact, constitute a drowned estuary)in southern Borneo, in New Guinea, and in Thailand and adjoining territories t o the eastward. Mangroves are, therefore, almost always estuarine or else have developed in lagoons and lows behind cheniers or in the shelter of fringing or barrier reefs of coral, or of bluffs or islands. Mangal development, as may be expected, shows a relationship to the steepness of the shore and to the range of the tides. The shore exposed between tide-marks, in regions where the tide is appreciable, includes two distinct sections: (1) a portion exposed a t low tides, and this does not concern us for it is never colonized by mangroves, and ( 2 ) a portion entirely covered by water only a t high spring tides. This is the schorre in international terminology-“ salt marsh ”in England, America and Australia. In the tropics and warmer subtropics around the Indian Ocean a zoned mangal occupies almost the entire schorre: but only in the humid tropics will the mangrove zonation tend t o be complete. In drier regions or where rainfallis seasonal only the lower level will be occupied by mangroves. Here a low cliff-“ a salting cliff ”-often divides the schorre into two levels: of these the “low marsh” will tend to be occupied by a more or less well-developed mangal, and the “high marsh )’will be either bare or occupied by a variety of halophytes. Guilcher (1963) records such a pattern in Madagascar and ascribes it “to the long dry season and to the high temperature, which lead to complete desiccation of the surface and crystallization of salt during neap tides so that no plant is able to grow there ”. Such bare areas are

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described by Fosberg (1961) a t Gladstone in Queensland, and their development is discussed by Macnae (1966, 1967) with conclusions similar to those of Guileher." Mangroves penetrate only a short way upstream in the estuaries of some rivers and very far in others. I n the main channel of the Zambezi delta, the Rio Cuama, mangroves penetrate only some 15 km from the mouth. I n the Rio Maputo, runninginto the Bay of Lourenyo Marques, trees of Avicennia marina (Borsk.) Vierh. with a few Bruguiera gymnorhiza (L.) Lmk. and an occasional Rhizophora mucronata Lmk. extend upstream for less than 8 km. The tide goes far beyond this, above the village of Salamangasome 40 km upstream. At this village an association dominated by Barringtonia racemosa (L.) B1. and peopled by estuarine crabs occupies the "high marsh "which is quite narrow (Macnae, unpublished information). I n the Musi river of southern Sumatramangroves extend as far as Palembang, 50 km inland ; in the Kikori river of Papua they extend some 100 km upstream ; Bruguiera and Xonneratia were found 320 km up the Fly river in southern New Guinea (van Steenis in Ding Hou, 1958). I n the upper parts of tidal estuaries fresh water may be pushed back by the tidal wave, particularly when the discharge of the river is normally high. It has been shown by many authors (see Emery et al., 1957) that salt water penetrates an estuary in the form of a wedge which tapers upstream so that the fresh water lies on the surface and the "salt wedge "creeps along the bottom. As Alexander et al. (1932, 1935) showed, this "salt wedge " creeps farther upstream in the mud on the bottom. Hence it is not surprising that mangroves penetrate far upstream. The short penetration of the Zambezi delta has two causes : the banks are high, indicating that the trees would have to be very deep-rooted to reach the "salt wedge "; also there is a bar across the mouth which impedes the entry of sea water. The mouths of the rivers mentioned by van Steenis probably have no bars, and the banks are low. The Hooghly river, a distributary of the Ganges, is navigable by ocean vessels as far as Calcutta, and has a tidal portion of over 300 km. Mangroves extend beyond Calcutta.

Geological signi$cance of mangroves Davis (1940)has shown that in Floridamangroves have an important function in relation to the accumulation of coastal sediments. This is

* Guilcher (1965) has pointed out that such bare areas occur in the vicinity of Port Moresby in New Guinea on a coast with a seasonal rainfall due to its boing in the rain shadow of the central mountain chain.

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probably always true. Van Bemmelen (1949) records extensive shifts of the coastline of Sumatra,Java and Borneo as the result of accretion in mangrove areas. Van Steenis (in Ding Hou, 1958) commented that Junghuhnin 1853 had pointed out that “the mangrove follows the silting up of a coastal area rather than precedes and initiates the accumulation of mud or other soil and that it establishes itself merely on accrescent coasts ”. Palembang in south-eastern Sumatra was one of the ports visited by Marco Polo in 1292; it was still a coastal or river-mouth port 400 years ago, it is now 50 km inland. The rate of accretion is therefore around 125 m per annum. Near Indramajuin north-western Java it is 108 m per year ; in the Bodri delta an accretion of around 200 m per annum is threatening to close the port of Semarang (East Java). A similar rate of accretion is reported for the retreat of the sea from Hanoi in North Viet Nam (dat)afrom ~7anBemmelen, 1949). Anderson (1964) records that the Baram and Limbang flood plains in Sarawak have been extended seawards a t an estimated rate of 27.8 m (90 ft) per annum since the sea reached its present level there some 5 400 years ago. The silt which forms the mud so characteristic of mangrove areas has its origin in the load brought down by rivers. Guilcher (1963) comments that the mass of material in suspension carried to and fro by the rising and falling tide may be derived from the river or from material being resorted by wave action in the shallows just off shore. At Majunga in Madagascar Lafond (1957) showed that the mud was lateritic, derived from the deforested slopes of’the escarpment drained by the rivers; in Malaya and Indonesia the source is again from the rivers (van Bemmelen, 1949; Schuster, 1952; Carter, 1959). I n some areas with a limestone hinterland or with a coral reef nearby the intertidal deposits are formed of marl (Schuster, 1952 ; Davis, 1940). These materials all settle out a t the slack of the tide. The current velocity of the tide falls off rapidly as it goes farther into the mangal and the water can no longer support its load, which then falls out. Much of the material settles in the seaward fringe, but due to a time lag between the moment a t which the current is no longer able to carry its load and the moment when the material reaches the bottom, some of the material may be carried farther into the swamp. According to Guilcher (1963), this “settling lag effect ” may carry fine silt even to the inner reaches of the marsh. Guilcher goes on to write that “the minimum velocity required to erode a sediment after it has been deposited is higher than the maximum velocity a t which these same particles can settle : this ‘ scour lag ’ favours an excess of deposition ”.

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Such settlement a t the seaward end of a creek is prevented when the time taken for settlement is longer than the slack of the water at low tide. I n areas where the uppermost intertidal levels are bare of vegetation the deposits are often sandy. This is almost certainly the result of a very short period of inundation, duringwhich the tiny waves waft away any fine material from amongst the sand grains and no time is available for deposition. Many mangrove areas result from accretion on recently submerged coastlands. Obdeyn in several papers published between 1941 and 1944 has followed the history of the Sumatran, Javan and Malayan coastlines from a study of Chinese, Indian and other historical records. He has shown that during the early historical period Sumatra was still joined to the mainland and to Java, and that the Malay Peninsula extended southwards through the Riouw-Lingga archipelago almost as far as the tin islands of Bangka and Billiton. The suggestion follows that the silting up of estuaries in south-east Sumatra followed the opening of the Straits and the subsequent development of backwaters some distance from the tidal rips which run in t,he narrow channels between the islands. Such alterations of shore level are of twofold origin. I n Malaya and the Sunda archipelago, change of sea-level is due both to eustatic changes resulting from the Pleistocene Ice Ages and to epeirogenic movements resulting from the processes of deformation and mountain building which began in the Tertiary and still continue. India, Africa and Australia have been affected by the former ; western Malaya and the Sunda are mainly by the latter. I n many of the niangals of Sarawak there occur odd little clumps of terrestrial forest often only a few acres or less in extent. Anderson (in conversation) has commented that the soils of these islands of terrestrial forest suggest that they have not been derived by normal processes of accretion. But their origin has not been investigated! The Sunda Shelf extends far out into the South China Sea (see Fig. 7 5 , p. 227). This shelf is of interest in relation to the spread of several animals and plants and its eastern and southern margins correspond to “Wallace’s Line ”, the south-eastward limit of purely Asiatic land animals. The Sahul Shelf connected Australia and New Guinea and several islands between, and it forms the limit reached by many purely Australian land animals. The Sofala Shelf off cent,ral Mopambique is probably contemporaneous, as also is the shelf off Queensland within the Great Barrier Reef. All these processes, then, have made the shores of the Indian Ocean

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and the western Pacific Ocean very suitable for the establishment of mangroves and mangrove swamps. The geological history of the mangroves is also quite a long one. Muller (1961, 1964) has shown from a study of cores taken in peat swamp and mangrove forests in Borneo that nypa pollen and a Brownlowia-type pollen were already common a t the beginning of the Eocene ; that pollen of the Rhizophoraceae appeared late in the Eocene or early in the Oligocene; that pollen resembling that of Sonneratia caseolaris (L.) Engl. appeared early in the Miocene, and pollen resembling that of S. alba B1. late in the Miocene; and finally that pollen of an avicennia type appeared in the mid-Miocene. These cores were also of interest, in that they showed the presence of pollen similar to that of Aegialitis and Camptosternon, two mangrove genera no longer growing in Borneo, both now being restricted to more eastern areas in the Molluccas, New Guinea etc. Muller also quotes the following facts about the geological history of mangroves and other associated plants. The fruits of Nypa have been described from the London Clay flora (Eocene) of England (Chandler, 1951) and equivalent deposits in Belgium. Pollen of rhizophora-type has been reported from the Oligocene onwards from Venezuela, Nigeria and New Guinea (Kuyl et al., 1955). Chandler (1951) reports fruits resembling those of Rhizophoraceae from the London Clay. Wood and flowers resembling those of Sonneratiu have been found in India-wood from Pliocene and flowers from Deccan Intertrappean beds attributed to Eocene (Mahabale and Deshpande, 1959 ; Prakash, 1960).

D. Sea-shore plant associations Leaving aside the algal associations which occur on rocky shores, characteristic associations, principally of higher plants, grow on the different types of non-rocky substrata which occur along shores of the Indian and west Pacific Oceans. Schimper (1891) recognized four associations. (a) The Mangal-forests growing below high tide mark, and comprising several species of trees and a few of non-woody herbaceous plants. (b) The Nypa Association-occurring to landward and upstream of a mangal, dominated by the rhizomatous palm, Nypa fruticans Wurmb., and supporting a few isolated trees, chiefly Heritiera littoralis (L.) Dryand. and Excoecaria agallocha L., a few shrubs, lianes and ferns chiefly Acrostichum aureum L. (Fig. 3).

FIG.3. N y p a fruticosu at the edge of a distributary of the Sarawak river below Kuching. I n tho nypa swamp behind, trees of Excoecaria agallocha and Heritiera littoralis were conspicuous. (Mid-tide, January 1967.)

Barringtonia racemosa and associated trees, upstream of mangroves near Inhambane (lat. 23"S.), Mopambique. (Septomber 1966.) (1) B. racemosa; ( 2 ) Brachylaena discolor; ( 3 ) Mimusops caffra; (4) Euclea natalensis; (5) Ozoroa obovata; ( 6 ) Siderozylon inerme and Phragmites communis.

FIG. 4.

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FIG.5. The pes-caprae association a t the foot of sand dunes on Inhaca Island. In the background is a group of tall bushes of the silvery leaved Sophora tomentosa, and in the foreground creepers of Ipomoea pes-caprae.

(c) The BarringtoniaAssociation-dominated by either Barringtoizia

asiatica Kunz. when it occurs behind a pes-caprae association, or by B. racemosa and/or Heritiera sp. if the association occurs behind a mangal. All of these trees prefer a relatively welldrained soil (Fig. 4). Schiniper did not distinguish between these but lumped them together. (d) The Pes-caprae Association-dominated by Ipomoea pes-caprae Roth., usually accompanied by Canavallia sp., by shrubs of Sophora sp. (most commonly S. tomentosa L.), of Xcaevola sp., of a single row of trees of Casuarina equisetifolia, and often planted out with trees of Cocos nucifera L. (Fig. 5 ) . Of these associations the pes-caprae and the barringtonia asiatica associations are always supralittoral, in the sense given to this word by Lewis (1964), and normally characteristic of sandy shores; they will not concern us further. The mangal is always littoral, in the sense of Lewis, and never extends above high water mark. The nypa association and the barringtonia asiatica association are associations of overlap and straddle high water mark of ordinary spring tides, and may extend above extreme high water mark. Both are indicative of strong freshwater influence, but the nypa association tends to occur on more A.M.B.-6

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or less permanently waterlogged soils. The barringtonia racemosa association occurs on relatively well-drained soils which may show a seasonal water-logging. The first three of these associations occur only on sheltered shores ; the fourth is equally characteristically found on open wave-beaten shores. Members of the pes-caprae association are often useful dunefixing agents. To these four associations it may be convenient to add a fifth association which occurs from mean sea-level downwards, on sheltered ;hores or in rock pools on open shores. (e) The Cymodocea Association-dominated by one or other of the species of Cymodocea intermingled with species of Diplanthera, Enhalus, Halodule, Halophila, Syringodium, Thalassia and

Zostera. Again this association does not really concern us except as it may occasionally encroach on the lower zones of the mangal. Schimper (1891) was dealing only with the plant associations in the region between India and western Indonesia, drought-stricken areas did not come within his survey. When evaporation comes to exceed the availability of fresh water Schimper’s first three associations become highly modified. The nypa and barringtonia racemosa associations become less and less conspicuous and in their stead occurs : (f ) The Saltwort Association-dominated by bushes or low shrubs of species of the perennial Arthrocnenum and the annual Xalicornia. When evaporation becomes excessive, bare areas devoid of any vegetation supervene, and then all plant communities are restricted to the vicinity of creeks, occasionally with a fringe of halophytes around high water mark. I n summary, one may recognize on Indo-west-Pacific shores above the level of high water of neap tides, two basic plant associations. ( 1 ) Just above high water mark of ordinary spring tides there occurs

on exposed shores or sandy shores the lpomoea pes-caprae Association, and this with only a few of the associates varying, extends from semi-desert shores t o the ever-wet, where rain may fall abundantly at all seasons. I n the humid tropics this may be associated with a Barringtonia asiatica Association. ( 2 ) On sheltered and muddy shores, the Mangal stretches from near mean sea-level upwards to extreme high water mark. As variants a t higher levels we may find (a) a Nypa Association,

FAUNA AND FLORA O F MANGROVE

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(b) a Barringtonia racemosa Association, or ( c ) a Saltwort Association. The first two are diagnostic of areas under freshwater domination where evaporation and transpiration are more than balanced by a high rainfall and/or supply of fresh water from large rivers. The saltwort association occurs where evaporation and transpiration are in excess of the supply of fresh water.

11. ZONATION OF MANGROVES Three schemes have been proposed in descriptions of the zonation of mangroves, two of these base the zonation on physical features of the environment while the third follows more recent practice and names the zones from the genus dominant in each one. 1. Watson (1928) in a pioneering study of Malayan mangroves recognized five classes based on frequency of inundation (Fig. 6). (i) Species growing on land flooded at all high tides: no species normally exists under these conditions but Rhizophora mucronata will do so exceptionally. (ii) Species growing on land flooded by medium high tides: species of Avicennia, A . alba, A . marina (Forst.) Vierh. (= A . intermedia Griff) and Xonneratia griflithii Kurz., and, bordering rivers, R. mucronata. (iii) Species growing where they are flooded by normal high tides: the majority of mangroves thrive under these conditions but the rhizophoras tend t o become dominant. (iv) Species growing on land flooded by spring tides only: such areas are a little too dry for the rhizophoras and suit Bruguiera gymnorhiza and B. cylindrica (L.) B1. better. (v) Species on land flooded by equinoctial or other exceptional tides only : B. gymnorhiza dominant but Rhizophora apiculata B1. and Xylocarpus granatus survive. 2 . De Haan (1931) introduced salinity of soil water as the factor controlling distribution with tidal flooding as a subsidiary factor. His scheme has two main divisions each with subdivisions. A. A brackish to salt water zone with salinities a t flood tide of between lo%, and 30%,. A1. Areas flooded once or twice daily on each of 20 days per month. A2. Areas flooded ten to nineteen times per month. A3. Areas flooded nine times or less in each month. A4. Areas flooded on a few days only, in each year.

Rhizophoro mucronato Rhizophora

1opiculato Bruguiero 1 parvif/ora

1 Rhizophoro styloso

+

*

Bruguiero cylindrico Bruguiero sexongulo Bruguiero qymnorhiza Heritiera

Xylocorpus

f

Xylocorpus molluccense Intsio Forest

1

'? gronotum

Sannerotio griffithii

1 Avicennia

p ZEZ"marino

A vicennio albo Acrostichum auraum Somphires Sesuvium

FIG.6. A diagram (redrawn from Watson, 1928) ''to illustrate the typical, but, by no means inevitable, distribution of the more important mangrove species ". This diagram is based on the distribution of trees on the Malayan west coast.

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B. A fresh to brackish water zone with salinities between O x , and lo%,. B1. Areas more or less under the influence of the tides. B2. Areas seasonally flooded. It is clear that A1 and A4 are equivalent t o Watson’s classes (i) and (v) respectively; A2 overlaps Watson’s classes (ii) and (iii) and A3 overlaps (iii) and (iv). B1 includes both barringtonia racemosa and nypa associations and B 2 includes peat and other swamp forests and areas dominated by Hibiscus tiliaceus L. 3. Walter and Steiner (1936) working on the mangal at Tanga in East Africa named the zones after the dominant tree. This was followed by Macnae and Kalk (1962) (cf. Fig. 19) and developed and extended by Macnae (1966) in a way which may be applied in any mangrove area (see Fig. 7 ) . There are distinguished : (1) The landward fringe. (2) Zone of ceriops thickets. (3) Zone of bruguiera forests. (4) Zone of the rhizophora forests. (5) The seaward avicennia zone. (6) The sonneratia zone. Modifications may be expected in the first three of these zones, and the last is not present on all shores for i t is restricted t o warmer coastlines. Watson’s figure showing the distribution of mangrove species in Malaya (Fig. 6) clearly indicates that he appreciated that the zonation followed this pattern.

A. The landward fringe This zone is the most highly variable of all the zones of the mangal. The soils may be predominantly sandy or predominantly muddy ; they may be well drained or waterlogged ; they may be rich, derived from recent volcanic rocks; or poor, derived from ancient granites and quartzites ; they may be marly, derived from limestones or peaty with much organic matter. The salinity of the soil water may be high or low. Each of these produces some variation but in general the mangals vary within two facies :(1)following on a forested supralittoral,and (2) following on a non-forested supralittoral, i.e. of grassland, scrub or desert. 1. Following o n a forested supralittoral

The word forest is used here to include rain forest only. Where climax rain forest has developed, or is capable of being developed, the

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FIG. 7. Mosaic of air photographs of a large area of mangrove forest in northern Moqambique, an almost unexploited forest. (1) A bare area between E.H.W. and H.W.M.O.S.T. covered by blue-green algae and occasional clumps of halophytes ; (2) bare area below H.W.M.O.S.T. colonized by Uca universa; (3) Avicennia parkland with Uca lactea f. annulipes, Sesarma eulimene, S. ortmanni and Cerithidea decollata ; (4) Forest of Avicennia marina with Sesarma meinerti and S. guttatum ; ( 5 ) thickets of Ceriops tagal and/or forest of Bruguiera gymnorhiza with Sesarma guttatum, S . meinerti and S . smithii; (6) forest of Rhizophora mucronata; (7) mixed forest of R. mucronata, Sonneratia alba, Avicennia marina and Bruguiera gymnorhiza (in that order of abundance) with Upogebia sp., AZpheus sp. and mud-skippers; (8) seaward fringe of Sonneratia alba. (By courtesy of the Secretary for Lands, Mogambique.)

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landward fringe of the mangal also contains tall trees-in other words the rain forest continues into the littoral, but there will be an abrupt change in species at the level of extreme high water (see Fig. 8). There may, in fact, be a slight “salting cliff ”marking the change. Observations in Australia (Macnae, 1966) suggest that such a rain forest mangal will only develop in areas with a rainfall of over 2 000 mm (80 in) and then only when there is an appreciable fall during the drier season. I n Malaya the landward fringe constitutes Watson’s (1928) class (v), which is inundated by extreme high tides, and the upper part of his class (iv), inundated by normal high tides. It corresponds alsowith de Haan’s (1931) classes A3 and A4. Each of these three shows slight differences from the others. The forests studied by Watson were clearly under marine domination and the dominant trees were mangroves. Those studied by de Haan appear to have been less saline for the trees of the barringtonia racemosa association were dominant. Watson reports that Bruguiera gymnorhiza may be dominant if the soil is heavy and wet; and with it may occur old trees of Rhizophora apiculata, of Xylocarpus moluccensis Roem. and good stands of Intsia bijuga (Colebr.) 0. Kunz.; lianas and other climbers and also various epiphytes will be common. Avicennia oficinalis L. is common, occasionally abundanta t this level in South East Asia from the Indus delta to New Guinea. I n eastern Africa A. marina extends up to this level. I n the levels reached by normal spring tides Xylocarpus granatum and Lumnitzera littorea Voigt form large trees : Bruguiera parvijlora W & A and B. cylindrica may form dense stands and B. sexangula Poir. may occur with B. cylindrica ; Avicennia lanata Ridl. is also, on the eastern shores of the Malayan peninsula and on the island of Singapore, characteristic of this level. There is almost always an undergrowth of ferns, the short Acrostichum speciosum Willd. in shade, and the larger A. aureum L. in clearings where it may form a stand 3 m high. If the soil is friable R. apiculata will be dominant. Degraded forests of this sort occurring just above high water mark in the centre of “mangrove islands ” off the west coast of Malaya are known to foresters as hutan darat-dry forest. De Haan recognizes three variants, firstly a lumnitzera littorea association which develops on firm shallow soils with banks of marl, with a very uneven surface. The tree layer is thin with occasional well-grown trees of Bruguiera gymnorhiza, Lurnnitzera littorea, Xylocarpus granatum, Heritiera littoralis, Ficus microcarpa L.f., Terminalia catappa L. and Barringtonia racemosa. The undergrowth is a thick wilderness of Xcyphiphora hydrophyllacea Gaertn. and of Acrostichum sp. (de Haandoes not distinguish between A. aureumand A. speciosum).

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A variant of this develops on firm soils of uneven surface. The tree layer contains Xylocarpus granatum, Heritiera littoralis, Ficus retusa, Intsia bijuga with Nypa in muddy gullies. The undergrowth is a thick layer of Derris he~erophylla(Willd.) Back. and Acrostichum sp. A third variant occurs on moderately firm soils with a tree layer including Bruguiera sexangula, Dolichandrone spathacea (L.f.) K. Schum., Barringtonia racemosa, Terminalia catappa, Ficus microcarpa, Lngerstroemia speciosa Pers., Corypha utan Lam. and along the creeks X ylocarpus granatum and Oncosperma jilanzentosum B1. A dense undergrowth comprises Acanthus ilicifolius L., Derris heterophylla, Acrostichum sp. and Crinum sp. These three associations seem in some unrecorded way to have been determined by the natureof the soil and, in addition, show an increasing dependence on fresh water; they may be considered to be variants merging into the barringtonia racemosa association as described below or into peat swamp forest. The relationshipbetween nature of soil and its associated vegetation in the mangrove areas is hinted a t but not definitely shown by some unpublished observations made in Sarawak by Anderson (personal communication). He has demonstrated that, in a transect from the seaward mangrove fringe to fully developed peat forest, there is a transition from almost purely mineral soils in the seaward avicennia fringes, to muck soils (with up to 65% humic material) supporting an association containing Nypa fruticans, Avicennia officinalis, Acanthus ilicifolius, Sonneratia caseolaris, Acrostichum sp. and with Bruguiera sexangula as the dominant tree, and finally into peat soils with around 95% organic matter. These latter occur only just above high water mark. Comments relating one species or anotherto more friable sandy soils or to clays are common in the literature but without definition of what is meant. I n Australia a luxuriant mangal occurs only in the wettest parts of Queensland between the Hinchinbrook channel and the Daintree river, and there only on heavy volcanic soils. Its development is not so lush on quartzitic soils in this same area. I n eastern Africa such an association occurs only a t the mouth of the Rufiji delta and on Mafia Island, where the rainfall is higher than even a few miles inland. I n north Queensland and in the Rufiji delta the landward fringe contains specimens of each and every mangrove tree occurring in the area, no one species is dominant. Most trees are well grown and only a few saplings are present. This is the area where Heritiera littoralis is normally to be found both in eastern Africa south to Inhambane and

FIG.8. e

The distribution of mangrove species on the Queensland coast in tho region between Mossman and Cardwell. The diagram is based on the air photographs of the area just north of Cairns and personal observation. The rainfall is around 2 000 mm with some rain in the drier months. The transect scheme follows the figures used in Fig. 6. Certain apparently significant tidal levels are indicated, the numbers refer to days per month or per year on which tide reaches this level.

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in Queensland. Lunznitzera littorea is only found in this zone in Queensland. L. racemosa is characteristic of this zone in eastern Africa but it never becomes a well-grown tree.

The barringtonia msociations Associations dominated by species of Barringtonia occur in two distinct types of environment. (i) The barringtonia asiatica association. An association with Barringtonia asiatica (= B. speciosa L.f.) as dominant or as a very conspicuous associate occurs behind the pes-caprae association on sandy beaches. This is the facies described by Schimper (1891). Although this association does not concernus here, it does in fact, often include several trees which may occur in the ecotone of a mangal. Such are Terminalia catappa, Thespesia populnea and Pandanus tectorius. (ii) The barriiigtonia racemosa association (see Fig. 4). This association would seem t o reach maximum development along the shores of eastern Africa, between Kenya and Natal, and locally in southern Java (de Haan, 1931). I n eastern Africa (personal observation) it tends t o occur on quite well drained soils behind and upstream of a mangal. Thus it is equivalent to the nypa association of so much of South East Asia. I n eastern Africa the trees and bushes of B. racemosa are overgrown by climbers such as Derris trifoliata Lour., Entada phaseoloides (L.) Merr. Caesalpinia bonduc L. Heritiera littoralis is often co-dominant. Hibiscus tiliaceus is conspicuous in wetter localities and Thespesia popuknea in more sandy areas. I n the Zambezi delta Thespesiopsis mossambica Excel1 and Hillcoat and Pandunus livingstoniana Rendle are conspicuous. Other members of the association are indicated in Fig. 4. I n the Sunderbans and other deltaic forests facing the Bay of Bengal this association is represented by forests dominated by Heritiera littoralis and other species of this genus (Champion, 1936). On the banks of distributaries of the Zambezi Delta the barringtonia association occurs on the levees adjoining the river, and a forest of Bruguiera gymnorhiza occurs beyond a t only a slightly lower level. On the banks of the Maputo river (which enters the Bay of Lourengo Marques) above the township of Bela Vista where the river, while still tidal, is not under marked salt-water influence, Barringtonia racemosa occurs on the uppermost part of the banks just below high water mark. It occurs in a pure stand and is overgrown by lianas of Entada phaseoloides, the large bean-like seeds of which are commonly found cast up along high tide mark on tropical and subtropical Indian Ocean a.

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shores. These two plants also occur together in the lagoons of small rivers in southern Natal, just behind the coastal dunes through which the rivers break, when occasional floods raise the level in the lagoon sufficiently (personal observation). b. T h e nypa association The nypa association constitutes one of the most important, and from the air most conspicuous, features of the mangal throughout the Indo-Malaysian and South East Asiatic regions (Fig. 10). It occupies extensive, often very extensive, areas in the region flooded by the highest spring tides (Fig. 19). A notable feature of the area occupied by the association is the large number of huge (up to 3 m high) mounds of Thalassina anomala and these affect considerably the facies shown by the association. When nypa is very dense there may be little else, for other plants are shaded out. I n such an area the palms present a veritable wall along the banks of rivers or creeks. Occasional trees of Heritiera littoralis, of Xylocarpus granutus, X . moluccensis, Bruguiera sexangula, B. gymnorhixa or of Lumnitzera littorea may stand out conspicuously at higher levels and trees of Rhixophora apiculata a t only fractionally lower levels. Excoecaria agallocha, Bruguiera cylindrica and Sonneratia caseoluris are frequent associates. Hibiscus tiliaceus and species of Pandanus will also occur in places where the water is almost fresh. The mounds cast up by Thalassina often reach heights above high water mark. At levels where they may occasionally be flooded they are colonized by Acrostichum speciosum and by the lianas Clerodendron inerme (L.) Gaertn., Cynanchum carnosum Hort., Entada scheferi Ridl. ( ? = E. phaseoloides) as well as by rotans, Calamus aquatilis Ridl. and these will sprawl over the trees rather than over the nypa of which the slippery leaves seem to offer little to grasp. At higher levels terrestrial plants may colonize. I have seen a juvenile coconut tree on such a mound in the Sarawak river delta. Because of its uses to man as thatch and for various other purposes including sugar production, the nypa association is often kept artificially clear. Though not in the usual sense of the word cultivated, it is cared for and as a result of leaf cutting access between palms is easier. Usually the creeks and rivers are lined by a dense wall of the palms but various mangroves may develop between ; these include Avicennia oficinalis, Kandelia Icandel, Brownlowia tersa (L.) Kost., Aegiceras corniculatum and most characteristically, Sonneratia caseolaris. The ecotone or zone of passage between the nypa association and the freshwater swamp forest is often indicated by a narrow and continuous

Nypa swamp

Thalassina large Sesorma spp North Borneo

FIG.9. The pattern of distribution of mangroves a t Sandakanin Sabah (North Borneo) as seen in a typical transect. The nypa swamp is very extensive with occasional trees of Heritiera and Ezcoecaria conspicuous. The zoned forest is dominated by Rhizophora apiculata and has a fringe of Avicennia or of Sonneratia.

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FIG.10. Mosair of air photographs of virgin mangroves in Sabah (North Borneo). (1) Nypa swamp; (2) forest of Rhizophora mucronata; ( 3 ) forest of R. apiculata; (4) mixed mangroves with outstandingtrees of Bruguiera gyrnnorhiza and B. sexangula ; (5) area exploited by indiscriminate felling. The pock marks in zones 2 and 3 are areas where some ten t o twelve trees have been injured by lightning. Note the evenness of the canopy in these areas, seemingly a prerequisite for this type of lightning damage. (Courtesy of the Director, Lands and Survey Dept., Jesselton, Sabah.)

belt of Oncosperma tigillaria (Jack.)Ridl., the nibong palm. This belt is reported to be extensive in Sumatra from whence large numbers of poles of nibong are exported to Malaya for use as piles in jetties, houses, board walks and fish traps. 2 . Following o n a savannah, grassland or desert With a reduction in rainfall the forested landward fringe, whether a mangrove association, a barriiigtonia association or a nypa-hibiscustiliaceus association, thins out, eventually to disappear. My own observations in Australia and eastern Africa indicate that where there is an intermediate rainfall, between 1500 and 500 mm, the landward fringe of mangroves is reduced to a narrow zone, containing well-developed trees, or merely shrubs, of Avicennia marina and shrubs of Lurnnitxera racemosa, and rarely with any admixture of other species. Occasionally where the slope of land is gentle, particularly where the tidal range is considerable, this landward fringe widens and well-developed trees of Awicennia marina some 5-7 m tall are spread as in a parkland, with, beneath, a carpet of Xesuvium portulacastrum or

FIG.11. The distributionof mangroves in the district of Townsville, Queensland. The mangroves are restricted to the edge of the sea and to the vicinity of tho creeks. Osbornia and Ipornoea pes-caprae grow on cheniers. There are extensive bare areas. The rainfall is around 1 000 mm and highly seasonal. Based on air photographs. For explanationof transect, see Figs. 6 and S.

FIG. 12. Air photograph of the mangrove forest in the Sac0 da Inhaca (lat. 26"S.), southern Moqambique. Recognizable are a seaward fringe of Avicennia marina, trees up to 15 m ; creek fringes of Rhizophora mucronata, trees up to 10 m ;and the dense thickets of Ceriops tagal. Avicennia also occurs with Lumnitzera racernoas as stunted shrubs a t the edges of the clear areas. D, Sandy areas occupied by Dotilla fenestrata ; M, areas of sandy m i d with Macrophthalmus grandidieri; S, areas occupied by halophytes and oiily submerged at extreme high waters ;U, areasoccupied hy Uca inversa ( U . lactea f. annulipes is abundant wherever Avicennia trees occur). The transects are lines along which the salinity of the ground water was sampled in July 1963 and the numbers indicate the salinity in g/litre. (By courtesy of the Secretary for Lands, Mopmbique.)

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Variations in the landward fringe of Avicennia marina in Mopmbique. FIG.13. Avicennia parkland at Inhaca (lat. 26"s.)with Juncus kraussii, Arthrocnemurn decumhens and Sesuuium portulacastrum. Such areas support large populations of Uca lactea f. annulipes, Sesarma ortmanni and Cerithidea decollata, and Macrophthalmus depressus spreads up to this level. (April 1967.)

FIG.14. Dwarfed Avicennia nzarina a t Inhambane (lat. 23"S.), with Chenolea diffusa. The dwarfing is probably due to mineral deficiencies. (Photo: A. 0. D. Mogg, J u l y 1963.)

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FIG.15. Dwarfed Auicennia at Quissanga (lat. 12°K) with Sesuvium portulacastrum and Arthrornemum indicum (right). Note extensive bare areas due to high salinity of ground water-in July 1967 the salt crystals glistened on the surface a t low tide. (July 1967 just after last of spring tide series, mid-tide.)

of saltworts, species of Arthrocnemum(Fig. 19). I n the region between Chinde and Quelimane just to the north of the Zambezi Delta such parklands are extensive and the species of Arthrocnemumis A . indicum Moq. Tand. At Inhaca,in southernMoqambique, A . decumbensTolken is common. South of Townsville and in the Broad Sound area of Queensland such parklands cover many acres and A . leiostachyum (Benth.)Paulsen (if, indeed, this is different from A . indicum)and A . hnlocnemoidesNees var. pergranulntu~ J.M. Black form the field layer. At various places in south Queensland A. quinquejlorumUng.-Stenb. replaces A . leiostachyum. The level of ordinary high water mark is indicated by the presence of Chenolea diflusa L. and by one or other of the forms of Juncus maritimus Lam. (in southern Africa J . kraussi Hochst. ; in Australia J . maritimus). Clumps of Acrostichum aureum occur a t the upper edges of the parklands in Mogambique. A. speciosum does not occur under these conditions a t this level even in Queensland where it alone is present. Where such parklands and fringes have not developed, this zone will, apart from a few clumps of saltwort, be bare (Fig. 15).

B. Zone of ceriops thickets Ceriops tagal occurs from the Moqambique-Natal border along the eastern coast of Africa and Madagascarvia India and Ceylon to Taiwan (Formosa)in the north and t o Queensland and New Caledonia in the south. It is a mangrove which rarely reaches tree dimensions, but rather is a shrub ranging in height from around 1 to 6 m.

--___-

FIG.16. Patternof distributionof mangroves on Magnetic Island, off Townsville, Queensland,based on air photographs and personal observation. I n comparison with Figs. 6 and 8, a zone of Ceriops tagal is interposed between the landwardfringe and the bruguiera forest. This zone of Ceriops is interrupted by bare areas. The rainfall is around 1 500 mm, and seasonal, but seepage water from the mountainkeeps the streams perennial. This type of distribution is typical for areas of intermediate rainfall; it gives way to the pattern shown in Fig. 11 when evaporation and transpirationcome t o be excessive. Explanationof transect as in Figs. 6 and 8.

Canopy: R. mucronato

Canopy: R. apiculato

4

3 2 1

,

Small sesormas

FIGS.17-19. Diagrams of transects to show the distribution of plants and animals in mangrove forests. KEY Eam, Ellobium auk-midce Bb, Boleaphthalmw boddaerti II!, Ilyagrapsus sp. or spp. Caf, Caasidula auris-felis Cc, Cerithidea cingulata La. Leiopecten sordidul w Cm, Clistocoeloma merguiense M a , Macrophthalmus sp. Go, Cerithidea obtusa Mc, Metaplax crenatus M e , Metaplax elegana Eaj, Ellobium auris-judm

In each transect the number of tides per annum reaching certain levels is indicated. Pc, Pk, Ps, Sb,

Periophthalmus chrysospilos Periophthalmus kalolo Periophthalmodon schlosseri Syncera brevicula Sv, Scurtelaos wiridis T m , Teleacop’um spp.

Uc, Ud, Urn, Up,

Ur, ut,

Uca coarctata Uca dussumieri Ucamanii Upogebia sp. Uca rosea uca triangularis

FIG.17. The pattern in deltaic forests in western Malaya, cf. Fig. 6. The snails show a zonation in two directions, vertically in the trees and “horizontally” along the surface of the soil. The animals listed in Fig. 18 occur here as well. FIG.18. The pattern shown on the western seaboard of Malaya, as, for example, south of Kuala Selangor. FIG. 19. The pattern of distribution a t Inhaca in southern Mopambique, in a swamp with abundant seepage water from adjacent freshwater fens.

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I n the ever-wet of Malaya and Indonesia a ceriops zone is not well marked but, rather, species of Ceriops occur within a bruguiera forest or, as in Sabah and peninsular Thailand,in association with Rhizophora spp. where these form well-developed and mature virgin forests. Under these circumstancesC . tagak reaches tree dimensions of upwards of 10 m and some 20 cm in diameter a t the base of the trunk above the buttresses. Trees of this size are mentioned by Watson (1028) without his being explicit as t o where they may be found. I n regions of intermediate rainfall and on soils which are well drained, dense thickets of C. tagal follow the landward fringe a t a level immersed by all spring tides, i.e. a t the lower levels of Watson’s class (iv) and the upper levels of his class (iii) (Figs. 16 and 19). Within these thickets all stages of development from newly germinated seedlings through saplings to mature small trees may be found in almost pure stands. I n Australia the most common associate is Bruguiera exaristata. OccasionaItrees of Avicennia marina, B. gymnorhiza, Xylocarpus granatum and X . moluccensis also occur ; Xcyphiphora hydrophyllacea occurred in this zone along the Hinchinbrook channel. I n eastern Africa only A . marina and B. gymnorhiza are present as associates. The trees of Ceriops are always taller a t the lower margins : where they merge with the trees in the zone of bruguiera forests they reach similar heights to the adjacent bruguiera trees which, in turn, are not so tall as those farther downward.

C . Zone of bruguiera forests Watson recognized three types of bruguiera forest, dominated respectively by B. cylindrica, B. parvijlora and B. gymnorhiza. Forests of B. cylindrica are characteristically developed on stiff, bIue clay soils with a shallow humus layer and a well-marked surface drainage but no creeks. I n Malaya such forests occur along the long stretches of the western coastline which lie between the major rivers (Fig. 17). These forests of B. cytindrica develop behind a seaward fringe of Avicenniu marina (= A. intermedia). The purity of these stands as seen today may be the result of thinning out other species. The soil surface is almost level and few animals were seen, these were mainly small sesarmas (personal observation). B. parvijlora is essentially an opportunist species and not popular with foresters because its timber is said to be inferior to that of other species. I n Australia (Macnae, 1966) and in Burma (Rogers, quoted by Watson, 1928) this species is also opportunist and tall groves occur in areas which have formerly been cleared (Fig. 20). I n Malaya, too, it frequently takes over an area which has been cleared and may then act

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FIG. 20. Forest of Bruguiera pawi$ora at Nind’s creek, near Innisfail, Queensland: trees 20 cm in diameter and ra 30 m tall. One tree of Rhizophora stylosa can he seen. (Photo: B. Campbell, January 1964.)

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as a nurse tree to the colonization of Rhizophora spp. or other more valuable Bruguiera spp. (Watson, 1928). Watson considers the forests of B. gynznorhiza to be “ t h e final stage in the development of the littoral forests and the beginning of the transition to inland forms ”. He finds that, once established, there is little regeneration beneath these trees and that successive humus deposits and the activities of Thalassina anomala (Herbst) gradually lift the soil level so that in due course it is raised above the reach of the tides. At this stage Xylocarpus moluccensis, Intsia bijuga, Ficus microcarpa, Pandanus spp. and Daerrtonorops leptopus and many other plants come in. I n Watson’s opinion, then, a forest of B. gymnorhiza is the transition t o a well-developed landward fringe. At Tjilatjap in southern Java, de Haan (1931) also described three variants of the bruguiera forests. He recognized a Bruguiera gymnorhiza Association developing in his zones A2-A3 (p. 89) on soils which are mainly firm and flat with few crab hills (i.e. mounds of Thalassina). Here there are tall trees of B. gymnorhiza in the upper part of A2 and in zone A3 these become intermingled with tall trees of Xylocarpus granatum and Heritiera littoralis; clumps of Excoecaria agallocha occur in places where the soil level has been raised. Ceriops tagal and C. decandra (Griff.) Ding Hou are sporadic. Undergrowth is scanty in deep shade, thick in clearings, and consists of Derris heterophylla, Paramignya littoralis Miq., and in the less shady places a dense growth of Acrostichum spp. From this he separated a Bruguiera cylindrica Association and a Xylocarpus-Heritiera Association. These two have much in common, differing only in the dominant species. Both develop in zones A3-A4 and both are intermediate to the landward fringe. Both occur on more or less firm clays ; in both the surface is irregular due to the burrowing activities of crustaceans. These are open forests in which on the one hand B. cylindrica and on the other Xylocarpus granatum and Heritiera littoralis are dominant. With them occur Excoecaria a,gallocha, Xylocarpus moluccensis, Cynometra ramijlora L. and Intsia bijuga. The undergrowth is usually thick, of Derris heterophylla, Acrostichum sp. with Nypa in muddy gullies. I n Australia and Africa forests of B. gymnorhiza extend up to the landward fringe only where there is abundant rain. I n regions of lower rainfallthey are sandwiched between ceriops thickets and the rhizophora forest and occupy the middle of the mangrove area. Bruguiera forests in South East Asia and in Australia frequently

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support a ‘‘herb-layer ” of the fern Acrostichunz speciosunz which tends to be restricted to the mounds cast up by Thalassina anomala (Fig. 5 2 , p. 170) ; the lower lcvels of the soil surface arc bare or colonized by mats of algae, mostly blue-green.

D. Zones of rhixophoraforests I n the popular mind a mangrove swamp is usually visualized as being a forest of species of Rhizophora with arching prop roots making

FIG.21. Forest of Rhizophora upiculuta with trees 30-40 cm in diameter and ca 40 m tall, on a falling tide in the estuary of the Besitang river a t Pangkalan Gusu, Aru Bay, north-eastSumatra. (Photo: C. G. G. J. van Gteenis, April 1937.)

passage difficult, an “antlered ” mangrove (Fig. 21). Such a forest is also in Watson’s (1928) opinion the highest development of a mangal. Three species of Rhixophora occur in the Indo-west-Pacific mangals and they may overlap to some extent. R. mucronata is the commonest and most widespread extending from Malaya to New Guinea, to the Ryii-Kyii Islands and to Africa. R. stylosa occurs from Malaya to

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l i k . 22. Forest of R. mucronata with trees 30-40 cm in diameter and ca 35 m tall, on a falling title, south of Ranong, peninsular Thailantl (wcst coast). The man is I .80 m tall. (February 1967.)

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Queensland; R. apiculata from Malaya throughout South East Asia to India and Ceylon and to north Queensland. R. apiculata is more tolerant of fresh water than the others. In Malaya and the northern part of the Indo-Australian archipelago R. stylosa appears to be restricted to shores in the shelter of coral reefs, and those are often sandy. In Australia and southern New Guinea it occurs in the muddy soils which, elsewhere, are colonized by R. mucronata. All may produce tall graceful trees and grow a t several levels from areas flooded at all

FIG.23. Regeneration in a forest of R. apiculata, south of Ranong, trees of R. apiculata up to 40 cm in diameter and 35 m tall. Some of the slender trees me of Ceriops spp. (February1967).

high tides upwards to those which are only flooded occasionally. I n some rhizophora forests undergrowth is rare and then usually of saplings of Rhixophora. I n others, such as the majority of virgin rhizophora forests in South East Asia and the adjoining islands, there is a copious undergrowth of Ceriops tagal, C. decandra, Bruguiera. cylindrica and B. parvi$ora, the first and last being the commonest. All these trees form an understorey reaching some 15-20 m tall in these conditions. As much as two-thirds of the mangal in Sandakan Bay (Sabah, formerly North Borneo) may be occupied by extensive forests of R. apiculata. Along the west coast of peninsular Thailand, just south of the Burma border, some areas are occupied by extensive forests of

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R. npiculata and others of R. mucronata. Vu van Cuong (1964) reports that R. apiculata is the most important and most abundanttree in the mangals of Cambodia and Viet Nam. I n Queensland and eastern Africa the soil in the rhizophora forests is usually soft. It is aerated by the activities of alpheid prawns when it is semi-fluid and by thalassiiiideanprawns such as species of Upogebia when it is more solid.

FIG.24. Forest of young R. rnucronata, approximately 10 years old growing in an area felled for tannin production in the bay behind Cabo de Bartolomeu Dias (lat. 21"50'S.), Mopmbique. (September 1966.)

A glance a t Watson's sketch plan of the distribution of mangroves in the Malayan mangals will show that in Malaya two types of rhizophora forest occur. This is also true of Thailand, South East Asia and the wetter parts of the Indonesian archipelago. A forest of R. mucronata occurs in areas dominated by sea water, a forest of R. apiculata in areas dominated by fresh water. Hence a forest of R. nzucronata will lie behind a seaward fringe and pass backwards (Fig. 6) and upstream into a forest of R. apiculata. The forest of R. mucronata will run alongside a channel, river or creek where water of salinity around ZO%, or above overflows the banks but will give way t o the other when water with a salinity of less than 15%, floods the forests.

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E. Beaward nvicenniafringes Along most coasts on which mangroves occur the most seaward zone of trees is made up of a pure stand of one or other of two or three species of Avicennia. There has been a considerable confusion over the identity of several species of Avicennia* and the latest revision by Moldenke (1960), although helpful, does not completely disentangle the confusion. Moldenke presents no evidence that he has seen the trees in the field. Most of the confusion that exists concerns the species which occupy the seaward fringes. Watson (1928) has shown that in Malaya Avicennia alba and A . murina (= A . intermedia)occupy different sectors of this fringe (Fig. 25). After having seen several mangals in Malaya and South East Asia I accept and can confirm Watson’s observations-but there are difficulties! Normally these two species are readily distinguishable-A. albu with pointed leaves and whitish reverse being quite easily separable from A . marina with bluntly tipped leaves and yellowish reverse. However, where they overlap there are intermediates.

* I n the preparationof this review the taxonomy of the genus Avicenniahas presented many difficulties. I n the most recent revision of the genus Moldenke (1960) recognizes six species in the Indo-west-Pacific. These are A . alba Bl., A . balanophoraMoldenke, A. eucalyptifolia Zipp. ex Miq., A . Zanata Ridl., A . marina (Forsk.)Vierh., and A . oficinalis L. Of these A . balanophora need not concern us for it i s recorded only from a few localities in Queensland. Bakhuizen van der Brink (1921) recognized only two species, A . marina and A . offccinalis. (Ridley’s (1920) description of A . Zanata,known only from the mainland of Malaya, would seem to have appeared too late for Bakhuizen’s consideration.) These are in fact the only taxonomic studies on this genus. To both Moldenke and Bakhuizen, A . marinais a polytypic species but to each authorit differs in extent. Both accept that the typical variety is an African and western Indian Ocean form, and that the var. resinijera is south-easternin distribution from New Guinea to New Zealand. Both acccpt the var. rumphiana as representing the species in Malaysian landward fringes. But this variety is clearly difficult. Moldenke recognized one specimen (Watson and Burkill, 3795, 9.viii.l918) both as A . Zanata and as A . marina var. rumphiana. Should these, then, be synonymous? Moldenke considers that Bakhuizen’s var. intermedia Griff. is the typical form of A . marina. I would concur. Bakhuizen considered A . alba to be a, variety of A . marina; Moldenke considers it t o have specific status. The two rarely overlap ecologically, and so behave as good species. Intermediates occur, possibly these are hybrids. Moldenke (1958) has recorded that hybridization may occur in American species. Moldcnke’s A. ezicalyptifolia seems to be restricted t o the highly calcareous beaches of coral shores-either low-wooded-island reefs of the Queensland Great Barrier or coral shores in eastern Indonesia and the Philippines. It may, perhaps, be an ecological variety, an ecotype of A . marina which i t closely resembles. I n this review- I shall accept A. alba, A. lanata, A . marina and A . oficiimlis. A . lanata and A . oficinalis are species characteristic of the landward fringes or of fresh water dominated areas in the mangal. A . aZba and A . marina are characteristicof the seaward fringes but have a wide tolerance (see p. 131). Of these A . marinaispolytypic with both geographical and ccological subspecies or varieties. A . eucalyptifolia seems to me to be an ecotype of A . marina but for the present it may best be left incertaesedis.

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FIG.25. A forest of Avicelznia marina in the seaward fringe a t Quissanga (lat. l2%.), Moqambique. Mud-skippers were common here. (July 1967.)

Ridley (1930) has suggested that A . intermedia was a hybrid between A. nlha and A . oBcinaZis; this must be incorrect. Moldenke (1958) has suggested that hybridization may occur where several species of this genus grow together. With hybridization a feasibility i t is not surprising that confusion has arisen. A . marina.is a very widespread species, the only representative of the genus over most of the Indo-west-Pacific, and as will be shown below has several physiological races. I n Malaya and adjacent areas of South

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East Asia A . marina (known locally as A . intermedia) occurs on the seaward fringe of a mangal facing the sea rather than a channel, creek or river. On such beaches it is a pioneer. Since these beaches face seaward and are exposed to light wave action the substratum is relatively firm. Behind, this passes into a forest of Bruguiera cylindrica. Along the entrance to channels,etc., A . marina gives way to A . alba and since wave action is less the substratum is very soft. I n the area of overlap individual trees may be difficult to identify as one species or the other. Behind the forest of A . alba, one finds a forest of Rhizophora mucronata. I n India, around Bombay, only A . alba is present and it occupies the entire, or almost the entire, mangal. The trees are kept short by cutting and the young branches fed to water buffalo. I n the absence of A . alba, A. marina occupies the entire seaward fringe. Moldenke (1960) recognizes a third species in this ecological group, Avicennia eucalyptifolia Zipp. ex Miq., and most of the localities from which he records this species are in the vicinity of coral reefs (Fig. 26) or off-shore coral islands from the Philippines to Queensland. On stable coasts the seaward avicennia fringe is very narrow, often only one to three trees deep. On accrescent coasts it may be more than 4 km (4 mile) wide. This is the case on many shores along the Straits of Malacca and parts of Borneo and New Guinea. On such shores seedlings of A. marina or of A . alba colonize the new banks of alluvium, develop into saplings, young trees and finally a well-developed orchard of tall avicennia trees under the shelter of which seedlings of species of Rhizophora develop. The substratum is firmer than the mud banks in front. This firmness is due to the dense mat of nutritive roots lying some 10-35 cm below the surface. Anderson (unpublished data) has shown that in Sarawak the alluvium on which these avicennia trees develop is deficient in organic material which represents only 5-15% of the soil content. On the shore of Trinity Bay near Cairns in north Queensland saplings of Aegiceras corniculaturn occurred with the saplings of Avicennia marina. At this level a considerable quantity of seepage water came out on to the beach, and presumably kept the salinity of the soil water within the range preferred by Aegiceras (Macnae, 1966). The thickets of saplings and seedlings extend down almost to mean sea-level. At the lower levels many seedlings get coated with fine silt, deposited by the tide-these seedlings die. Seedlings and saplings of Avicennia cannot grow well under conditions of shade. Macnae (1963)

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FIG.26. Avicennia ? m a r i mor A . ?eucalyptifoliaa t Low Isles, Queensland. The appearance of these trees is characteristic of trees growing under the influence of strong winds on the thin soil of coral reefs. (From a colour transparency, March 1962.)

has pointed out that avicennia seedlings die under the shade of their parent and also that even old trees die when they are overtopped by the rhizophora or bruguiera trees, for the development of which they have acted as shading nurses. Sa,plingsmay also be strangled by colonization of barnacles if these are abundantlocally. Sapling development of this type would appear t o influence deposition-the substratumbetween the saplings is very soft. This zone corresponds to the base of Watson’s class (ii) and upper portion of his class (i).

F. Sonneratia zone I n South East Asia Sonneratia griflthii and/or AS.alba, in Africa and Australia S. alba alone and in India from Bombay t o Burma S. apetala

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FIG.27. Sonneratia alba a t Quissanga (lat. 12"S.),Moqarnbique,growing in a sheltered bay which is very quiet and with little or no freshwater influence. (July 1967.)

may grow t o seaward of the avicennia fringe. These trees grow a t such a level that some of them are wetted daily. They lie below the level of high water of the lowest neaps. I n many places where this zone occurs, but not in all, saplings may grow beyond and push the outer edge further seaward. to be found growing Hardly ever are Sonneratia alba and S. grifithii

FIG.28. t3onneratia alba in the Bako National Park, Sarawak; elderly trees under quite strongwave action a t high tide; there is very little regenerationhere. (January1967.)

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together. But what determines which will occur is difficult to say. In bays protected from the prevailing winds, but not necessarily from other winds, pure stands of Sonneratia develop. Often these show no regeneration at all, nor any conspicuous fauna (Figs. 27 and 28). Along river banks and in other areas where the salinity is reduced by abundant fresh water, S. caseolaris is dominant. This species also occurs alongside creeks a t the back of the mangal. De Haan recognizes a t Tjilatjap an avicennia-sonneratia alba association which develops in zone Al, on soils which are mostly level, soft and deep. These are young unconsolidated soils. The tree layer comprises Avicenniu marina and Sonneratia alba with an undergrowth of Acanthus ilicifolius and of saplings of Aegiceras corniculatum. This association is compounded of my sonneratiazone and seaward avicennia zone. Muller and Hou-Liu (1966) have described suspected hybrids between 8. alba and 8. caseolaris and between X. alba and X. ovata. These were found in the mangals of Brunei. Sonneratia would appear to prefer warmer conditions than do most of the others-it does not come south of Inhambane on the Moqambique coast nor south of Innisfail in Queensland. This zone corresponds to Watson’s class (i). 1. Bostrychietum

The pneumatophores of Avicennia, and of Sonneratia, the prop roots of Rhizophora and the knee roots of Bruguiera gymnorhiza may locally

be densely covered with a bostrychietum which is an association of algae comprising several species of the genera Rostrychia, Caloglossa, Catenella and of Murrayella. For the identity of these see Post (1963, 1964a,b, 1966), where one will find detailed descriptions and distributions of the various species. Many of these appear to be widespread in the Indo-west-Pacific, not only from Africa to Australia and Japan,but also from the cool waters of southern Africa and Victoria to the tropics. A problem associated with this association is its relatively localized distribution within the seaward fringe of a mangal. The roots of one group of trees will be thickly clothed with algae and neighbouringtrees will be bare of them. Does their presence interfere with the proper functioning of the roots, and do the roots, in due course, cast off the bark invested by the algae? The presence of this association on the roots of the mangroves allows comparisons with rocky shores, for this association occurs too on the shaded side of, and under, overhanging portions of the rocks, just a t or just above or just below the level colonized by rock oysters.

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G. Variations Variation in development of these zones is t o be expected, yet in each and every mangal visited by the author they are recognizable. The succession is only complete when there is an excess of available fresh water over loss by evaporation and transpiration. Fresh water may be supplied to a mangal from two sources : either it falls as rain or it is kirought down into the area by rivers flowing from an area with a higher rainfall. I n the deltas of both the Rufiji and Zambezi rivers the rainfall is insufficient to account for the dense and well-developed mangrove forests. Over much of these areas the rainfall is around 750 mm and seasonal, but the rivers bring down enough water to influence the water table and give enough to enable proper development of the trees and allow of a complete succession and zonation. When evaporation and transpiration exceed the available fresh water t o the extent that the soil water becomes hypersaline, the zonation becomes interrupted. This interruption appears first in the ceriops zone (Fig. 16, p. 104). Towards the centre of this zone the bushes become stunted, rarely growing above waist height. They die off and recolonization does not follow. With increasing excess of evaporation this bare area expands both t o landward and to seaward. A few ceriops bushes grow alongside the trees in the landward avicennia fringe and a few occur just above the level of the bruguiera forest, narrowed in its turn to an insignificant remnant behind the line of Rhizophora mucronata or R. stylosa along the edges of creeks. This may be seen in Figs. 8, 11 and 16 which represent mangroves in localities differing from one another only in rainfall and in excess of evaporation and transpiration. When the substratum is composed of a well-drained sand rather than a mud, and no silt is availabIe for conversion into mud the entire facies may change. Three mangals of bhis sort are known to me ; one is a t Kosi Bay on the Natal-Mopambique border, anothera t Inhambane some 400 km t o the north a t latitude 23"s. (Fig. 14), and the third within the Bako National Park a t the entrance to the delta of the Sarawak river in Borneo. The streams draining into these areas come from hinterlands which are to a large extent uncultivated with porous sandy soils of recent origin, soils which seem to require much supplementing to grow crops successfully. No silt, then, enters the bays. At Kosi Bay Lumnitxera racemosa has become dominant in the entire mangal behind a seaward fringe of Avicennia m r i n a . Rhizophoraceous mangroves play a minor role alongside creeks where Rhixophora mucronata and Bruguiera gymnorhiza grow on soils enriched

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by decaying mats of phragmites and other grasses which grow on the moist soil behind. At Inhambaneextensive sandbanks are exposed a t times of low tide and almost the entire area capable of colonization by mangroves is occupied by dwarf bushes, mostly close to or just above waist height. Among these Avicennia marina is dominant and bushes of Xonneratia ulba and Ceriops tugal are scarce (Fig. 14). Only upstream in the small rivers where beds of Phragmites and T y p h u provide a mass of decaying leafage do the mangroves reach tree height, and in these stretches they form a river bank fringe t o a narrow forest of Heritiera littoralis and this may be backed by a belt of Acrostichum aureum which in turn gives way to a sward of Xporobolus virginicus and samphires or saltworts, Xalicornia pachystachya Ung.-Sternb., Arthrocnemum indicum and A . natalense (Bunge ex Ung.-Sternb.) Moss in Adamson. As one proceeds farther upstream a barringtonia racemosa association follows.

FIG.29. Distribution of mangroves at Low Isles, Queensland. Here Rhizophora stylosa grows in an area permanently submerged and named the "Mangrove Park "by Stephenson et al. (1931). The map was prepared from that given by Stephenson et al. with emendations from that given by Fairbridge and Teichert (1947). (From Macnae, 1966.) A.X.B.-G

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At the Bako National Park the mangal in the small estuary of the Sungei Lakei besar, a stream which drains virgin forest on a Tertiary sandstone, had also developed .in sand and showed a similar pattern of those mangroves which prefer well-drained soils ; these included Xonneratia alba, Rhizophora apiculata, Ceriops tagal, Excoecaria agallocha and Osbornia octodonta F.v.M. mostly in mixed stands with little tendency to zonation. The mangrove forests associated with the low-wooded-island reefs of the Great Barrier Reef system also depart from the norm. At Low Isles (Big. 29), while the upper part of the mangrove zonation is almost normal, the seaward fringe is peculiar (T. A. Stephenson et al., 1931; W. Stephenson et al., 1958; Macnae, 1966). The landward fringe is very narrow but contains trees such as Osbornia octodonta, Pemphis acidula L., Excoecaria agallocha, Avicennia marina, Aegialitis annulata R. Br. and others. The seaward fringe extends below the level of the water table-if not below mean sea-level-and in a shallow lagoon some 20 cm deep a t low water of springs one finds well-grown trees of R. stylosa forming what Stephenson et al. (1931) termed the "Mangrove Park "(Big. 30). It is quite surprisingin such a locality to see the prop

FIG. 30. Rhizopho~astylosa a t Low Isles, Queensland, a clump of trees in the "mangrove

park ". These trces grow a t a lower level than usual and are always immersed in water; Hippopus and giant anemones grow among the prop roots. (Froma colour transparency,March 1962.)

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roots of Rhizophora associated with the animals characteristic of the midlittoral flats and pools. The trees in this "Mangrove Park )'may go for weeks on end without the surface of the soil drying out. On the seaward side the pioneer is Aegialitis annulata which elsewhere in Queenslandgrows as a sprawling shrub in the landward fringe.

H. Mangrove soils Mangroves live in a habitat characterized by a high salt content and a high water content. The soils have a low oxygen content and abundant hydrogen sulphide. They are fine grained soils, often semi-fluid and ill consolidated, and in parts with abundanthumus-mangrove peat, a fibrous soil composed largely of the remains of roots and other woody structures. Anderson (unpublished information) has sampled the soils in two transects across the mangal from the seaward fringe into the peat forest in Sarawak. The locality is on the Maludam-Triso peninsula, a belt of almost featureless forest lying between the estuaries of the Batang Lupar and the B. Saribas in central Sarawak. The soils here within the mangal are greenish-grey silty clays of apparently marine or estuarine origin. Soluble salts seem to be leached out by rain water and replaced by the tides. At higher levels in the mangal the clays are mined and mixed thoroughly by the mud lobster, Thalassina anornula,and thrown into mounds reaching 3 m high. I n the nypa zones of the mangal these clays come to be covered by peat soils. There is a marked and abrupt change in conductivity (a measure related to salinity), in pH and in loss of weight on ignition a t the interphase where the zone dominated by mangrove trees passes over to the zone dominated by Nypa. The estuarine or marine clays of the seaward avicennia fringe have an average conductivity of between 5 000 and 8 000 p mhos, a pH of more than 7 , and a loss of weight on ignition of between 5 and 15%. Similar figures prevail through the rhizophora forests. On the other hand, the muck soils of the nypa zone show a low conductivity, 0-1 000 p mhos hence a low salinity, a p H falling gradually to the acid Ievel of peat forests and a loss of weight on ignition of up t o 80 and 90%. I n the peat forest soils this loss of weight is more than 95%. The mangrove soils are young soils for the most part, and have been well sorted before deposition. The silt brought in from the sea by the rising tide will containshells of foraminiferansand debris from molluscan and other shells. This calcareous material, together with the brokendown shells of molluscs which live within the mangrove and its mud, forms a most important constituent of mangrove mud, and of other intertidal muds. Much of the calcareous material of molluscan shells is

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made available to other organisms by the action of sulphur bacteria which, in the anoxic muds, corrode the sulphur-containingconchiolin of the shells. I n this way the shells become more fragile and the water has access t o the crystals of calcium carbonate so raising the alkalinity of the soil. The quality of the soil in mangrove swamps depends ultimately on the source of its alluvium. Rivers draining quartzitic areas carry an alluvium of poor quality. Rivers draining ancient granitic areas also carry silt of poor quality. Rivers drainingareas of recent or moderately recent volcanic soils produce an alluvium of high quality. The effects of soil quality are evident, for example, in Java and in Queensland. I n Java the Braiitas river draws its water from the volcanic mountains of East Java and produces a highly productive alluvium (Schuster, 1952); in Queensland the Barron and Johnstone rivers come from areas with abundant Tertiary volcanics, and on their flood plains is produced much of Queensland’ssugar and their estuaries support high and dense mangroves. I n contrast the marl and limestone areas of the island of Madura off north-east Java yield poor alluvium (Schuster, 1952); this is true, too, of many of the rivers of Africa, a continent of old leachedout soils, and also the quartzites of much of coastal Queensland,which support the scrub forest known as Wallum (Coaldrake, 1961), and produce poor soils and low mangroves. Nutrients are scarce in such soils. But such sources cannot entirely account for the rapid deposition of soils in certain areas. I n an area such as the Straits of Malacca silt and alluvium may be derived from two sources. They may have an origin in the erosive activity of the rivers of Sumatra and of Malaya. But also some silt and alluvium may be derived from now submarine sediments which had been laid down on river flood plains during the Pleistocene and are now being eroded from narrow submarinegullies by tidal currents. The fertility of this “fossil ”alluvium will depend on its history and origins before being deposited. Alluvium deposited in an estuary or mangrove area is not of itself productive. Macnae (1957) has commented that on the banks of the Gaintoos estuary some 60 miles west of Port Elizabeth the intertidal muds are barren since they have been deposited too recently. Schuster (1952) has shown that biological processes are necessary before the alluvium can be utilized by higher plants. These processes involve a number of organisms, bacteria, blue-green algae, diatoms and green algae. Important amongst these are nitrifying bacteria and sulphate reducing bacteria. Schuster (1952) lists several species of algae, which he argues are important food for prawns and fish (Chanoschanos (Forsk.)

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and Tilapia mossambica Peters) in fish ponds developed in mangrove areas. The blue-green and green algae seem t o show substratum preferences and the former may convert a soil into a suitable habitat for the latter. The blue-greens prefer a soft, hydrophilic, biologically active mud with much organic matter, whereas green algae prefer a more or less solid soil with an adequate supply of nitrate and phosphate. These inorganic radicles may have been released by the oxidative action of blue-green algae and bacteria on humus in the soil, converting ammonia to nitrate, and releasing bound phosphate. The faeces of the animals living in the mangal are an important constituent of the surface layers of the soil and must constitute a source of nitrate, phosphate and other substances for the photosynthetic micro-organisms of the soil. Only in the upper layers is the soil well oxygenated. Sulphatereducing bacteria flourish in anoxic conditions and are completely anaerobic. They obtain the sulphate from the soil water or from organic sulphur-containingdebris. The presence of hydrogen sulphide reduces the ferric compounds in the soil t o various hydrated ferrous sulphides which give mangrove soils their characteristic black colour. Only the surface layers to a depth of a few centimetres are oxygenated and show amounts decreasing with depth. Tube dwelling thalassinidean prawns, such as species of Upogebia and Thnlassina, by their activities of fanning a current of water through their burrow systems oxygenate the soils immediately surrounding the burrow. Alplieid prawns create mazes of shallow burrows in water-logged soil and help in keeping the upper layers oxygenated and so assist the bacteria, and other organisms, in making available the ions required by higher plants. It would seem, too, that the presence of shell or other calcareous debris in the soil is essential for the proper development of mangroves, particularly in areas of higher salinity. It is noteworthy that in citrus orchards on the Sundays River Valley (near Port Elizabeth, South Africa) where, perforce, the orchards are often irrigated with brackish water derived from Cretaceous marine shales, a generous dressing of lime prevents the scorching of the leaves on the trees. The presence of calcium ions seems to reduce or prevent any damage which may be done by excess of sodium ions, because calcium reduces the level of internal sodium. When the mangal has been cleared by cutting out the timber, what happens to the mangrove soils? Why do recently cleared areas often become a desert, useful only for salt production? Such areas may be seen along the shores of the Gulf of Thailand both west and east of Bangkok. When cleared areas have been used for prawn and fish

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cultivation in ponds, can they revert to mangrove forests when the ponds are neglected? So far as I am aware no one has studied the processes of degradation of mangrove forest soils. But one wonders if oxidation of peats with consequent loss of fertility may account for the bare areas so characteristic of the mangals in regions with low or seasonal rainfall.

I. Control of zonation While a zonation is normally found in a mangal colonized by more than one species of tree, the form of zonation described above is not inevitable, though it covers most of the associations which may be found intertidally on the upper shore within the tropics around the Indian Ocean. Macnae (1966) ascribed control of the distribution of mangrove trees and hence their zonation to the interaction of: ( 1 ) frequency of tidal flooding; (2) salinity of soil water; and (3) waterlogging of the soil. All of these are modified by the presence of creeks, gullies, rivers and channels; and the second and third will depend on : (i) rainfall and/or the supply of fresh water; (ii) evaporation and transpiration, and (iii) the nature and quality of the soil. 1. Frequency of tidal Jlooding It is clear that the zones of trees are associated, in the first instance, with rising ground level and the resulting falling off in frequency of tidal flooding. This formed the basis for Watson’s (1928) inundation classes and for de Haan’s (1931) zones. A comparison in tabular form is given in Table I. De Haan took into account in his scheme the effect of fresh water, and so his scheme has a slightly wider coverage than does that suggested by Watson. These zones based on physical features alone are not universally applicable but apply only in regions where the mangal covers the whole of its potential area of development. I n Table I these have been printed in such a way that equivalent zones are on the same line. The zones will vary in width with the nature of the slope of the shore; and with the range of the tide. I n Ceylon where the tidal range has a maximum of 7 5 cm the mangrove zones are telescoped very strongly, and during the wet monsoon the tide may give the appearance of never going out a t all so that the lower, more seaward zones are continuously under water for weeks on end and even the higher zones are flooded more frequently than usual. Where the tidal range is great, and the slope of shore gentle, mangroves may be very extensive and some miles deep; as, for example, at Port Swettenham and several localities in Sumatra, where the tidal range approaches 5 m.

TABLEI. ZONATION

WITHIN

A

MANGAL

De Haan (1931)

Watson (1928)

Brackish t o salt water-salinity at high tide 10-30%, A l . Areas flooded once or twice daily on each of 20 days per month

Dominant plant and system used in this paper

A.

1. On land flooded at all high tides

2 . Areas flooded by ‘‘medium high tides

”

A2. Areas flooded 10-19 times per month 3. Areas flooded by normal high tides A3. Areas flooded 9 times per month

4. Areas flooded by spring tides only 5. Areas flooded by exceptional high tides

A4. Areas flooded on only a few days in each month B. Fresh to brackish water-salinity O-lO%, B1. Areas more or less under the influence of the tide B2. Areas seasonally flooded either by fresh or brackish water

Seaward fringe of Xonneratia alba, or apetala or grifithii Zone of Avicennia marina Zone of rhizophora forest

kU

Zone of bruguiera forests Forests of the landward fringe Xylocarpus granatum or Lumnitzera littorea or Bruguiera sexangula or Mamphire association or Barringtoniaassociation

0

r F P

r

Es

0

Nypa associat,ion

‘(Medium high tides ” seem to be those which enter the lower levels of the mangal, but they do not penetrate far.

‘‘Normal high tides ” seem to be those which enter far into the mangal of the Malayan forests but do not reach H.W.M.O.S.T.

F 3.t 01

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The shore profile may also affect the manner of deposition of silt, etc., carried in suspension by the tide, and so control the distribution of animals and plants. All shores of sand or mud show a tendency t o flatten out a t one or more intertidal levels. I n regions with a large intertidal range there is usually a succession of flats a t different levels. This phenomenon has been shown by Macnae and Kalk (1962) t o influence the apparent distribution of plants and animals across the flats a t Inhaca, off Lourenqo Marques, and Macnae (1966) (Fig. 31) has shown an extreme example a t and near St. Lawrence in the Broad Sound region of central Queensland. I n many mangrove-bearing coasts visited by the author the same peculiarity is evident. On coasts where material is accruing one normally will find a continuity of slope downwards from the landward fringe to the seaward edge of the mangal. But on others there seems to have been an alternation of periods of accretion and periods of erosion. This naturally gives rise to a differentiation in levels. I n such areas, as for example on the northernshores of Pulau Ketani off Port Swettenham, this will result in a bruguiera forest coming up against a fringe of Sonneratia colonizing a new lower level (Fig. 32). Such an easy explanation is not always offered. I n SandakanBay, north Borneo, as much as three-quartersof the mangal is occupied by a forest dominated by Rhizophora apiculata. Only a narrow zone dominated by Bruguiera parvi$ora with Ceriops tagal and Xylocarpus granatum and with a few scattered bushes of N y p a fruticans and fewer trees of Heritiera littoralis intervenes between the rhizophora forest and the local facies of rain forests growing on sloping ground. This pattern is also shown within the mangals along the western coast of peninsular Thailand between Ranong and Phangnga. Here Ceriops tagal and C . decandra are more abundant in the understorey than is Rruguiern parvi$ora. I n these areas the shore has tended to flatten out a t the level of the rhizophora forests and here only, for the landward fringe and the seaward fringes are quite narrow. I n the estuary of the Lubok river west and slightly north of Sandakan Bay and in other places in Borneo extensive nypa swamps occur in addition to, and following directly on, the rhizophora forests (Figs. 9 and 10). Here, then, the apparent flattening of the shore has extended into a zone under more marked freshwater domination. Along much of the west coast of Malaya the widest zones in the mangal are the zones of bruguieraforests which are separated from the sea by avicennia or sonneratia fringes.

-Halosere

Grassland

St Lawrence, Queensland Rainfoll 1000 rnrn

FIG.31. Diagram to show the pattern of distribution of mangroves at St. Lawrence, Queensland. The tidal range exceeds 8 m and the intertidal region shows several zones of flattening. A very extensive grass-covered plain lies approximately 75 em above extreme high water mark. This is separated by a salting cliff of some 40 cm from a halosere which is covered only by very high tides and this in turn by a n interrupted mangrove forest with trees up to 15-17 m tall. (From Rlacnae, 1966.)

1

Bruguiera etc.

Rhizoohora

FIG.32. Diagram of a transect to show erosion and subsequent regeneration. This is based on a shore north of the township on the island of Pulau Ketam off Port Swettenham in Malaya. It is drawn from air photographs and observations made on the ground. The distribution of animals is similar to that shown in Figs. 17 and 18 apart from the presence of xanthid crabs in the crevices of the ‘‘salting cliff” and the presence of the crab Mucrophthalmus erato occupying a hollowed out and decayed mangrove root (X).

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Each of these levels tends to have its own peculiarities of soil consistency, mineral content and hence of fauna and flora. Exactly why beaches level off in this way has not been fully explained : it must be a function of tidal velocity and of material in suspension. By general consent (Spooner and Moore, 1940; Emery et al., 1957 ; Guilcher, 1963) tidal currents in estuaries and off-shore channels are strongest, when, a t low tide, they are confined within the channels. Although the rate of rise and fall of the tide is highest when it is crossing the flats, the fact that it is crossing these flats causes a slowing down of the current and allows deposition here. When the water has reached the upper flats within the mangrove the flow is furtherimpeded by the obstruction caused by the trees and their pneumatophores. The region where these are most thickly developed is in the seaward fringes of Avieennia and of Xonneratia and within the rhizophora forests, and these appear to be the region of greatest deposition. Beyond the seaward fringe the bank of accretion slopes, sometimes quite steeply, down to mean sealevel. These muds are very soft and ill-consolidated. Behind the seaward fringe the soils are firm and well consolidated. The boundary between these soft and firm soils lies towards the upper margins of the rhizophora forests. The soft, ill-consolidated soils are always waterlogged, and are reached by all or almost all tides. But why does this belt of soil always slope down as soon as it emerges from the shade and protection of the seaward mangrove fringe? Are such soils in a state of flux? Do they flow outwards? They are certainly capable of it and the area over which a man has walked, or rather wallowed or half swum, will immediately show signs of downward and outward flowing movements of the soil. It would seem that on some occasions at least, the soil particles lie on the slope a t a critical angle. The firmer soils within the mangal are exposed to the air for a few days each fortnight when the tide does not reach them. This absence of surface water allows them to be compacted because withdrawal of water brings the particles closer together. The biological processes described by Schuster (1952) assist in this compacting. Figures 8, 11 and 16 indicate the relationships between intertidal level and zonation of mangroves in several areas under different rainfall and evaporation-transpirationregimes. Although rainfall figures are available, figures for evaporation-transpirationare unobtainable and can only be guessed. Mangroves occur on tropical shores from the ever-wet to desert ;i.e. from regions of high rainfall and high humidity to regions of low rainfall or no rainfall, and of excessive evaporation and transpiration.

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Only in the former do they reach their maximum development. Only the hardiest survive on desertic shores-Lewinsohn (1963 in Zitt.) tells me that Avicennia marina still occurs a t the southern tip of the Sinai Peninsula, a locality from which Ascherson described its occurrence in 1903.

Only in areas with a rainfall above 2 000 mm is a complete succession of mangroves found. On the Queensland coast the succession is complete only on that stretch between the Hinchinbrook channel and Mossman where the rainfall is over 2 000 mm and a t Tully and Innisfail reaches 4 000 mm tapering off both to north and to south. On the coast of eastern Africa there is no comparable belt with a complete succession. Similar interruption in the zonation occurs in the drier parts of India and in Timor and various localities in eastern Indonesia. These figures also indicate that frequently one zone, usually either one of the variants of the bruguiera forests (e.g. either the bruguiera gymnorhiza forest or ceriops thickets) or one of the variants of the landward fringe, is dominant. At Port Swettenham and Cairns the bruguiera gymnorhiza forests are highly developed; a t Magnetic Island, ceriops thickets; a t Townsville, St. Lawrence, Inhaca and Tanga the bare areas exposed for days on end dominate the upper intertidal areas. De Haan’s scheme is based on the number of days on which the tide reaches certain levels on the mangrove area. Reference to Figs. 8, 11 and 16 will indicate the importance of this. On the transect across the mangal on Magnetic Island only the seaward fringe and part of the rhizophora forest are immersed a t each of the sixty tides per month. A maximum of twenty-five tides per month reach the bare area, in some months none reaches this level. Between four and twenty-one tides per month reach beyond the upper margin of the ceriops thickets and only twenty-two tides per year or a maximum of seven in one month reach high water mark. For several months on end no tides reach this level. As a result of the high rainfall (ca 1 500 mm) and run-offfrom the mountain the landward fringe receives an ample water supply and supports a forest. The Townsville transect indicates that all areas which are wetted by fewer than 117 tides per year (varying from four to twenty-one per month) are bare of vegetation. Not even saltworts or halophytic grasses occur. When these areas have been wetted by the tide the water drains away; but much is drawn up by capillary action and evaporated to leave a glittering crust of crystalline salt. There is insufficient rain and insufficient seepage through the soil to wash the salt away.

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2 . Xalinity tolerance Around Darwin and a t several localities in northern Western Australia the mangroves are creek based and there are extensive bare areas (at Darwin in spite of a rainfall of over 2 000 mm though this is concentrated into a few months only in summer). It would appear that the intense evaporation during the dry months concentrates the salt in the soil of the flats to levels above that tolerated by most plants and none but the most resistant will grow. Salinities of water in soils a t Manly, south of Brisbane (Badham, in litt.) and a t Inhaca (observations by myself and others) often exceed loo%,. At Inhaca trees of Avicennia marina and Lumnitzera racemosa grow in soils with a salinity of over 90%, (Fig. 33). I n such places A . micrinu is dwarfed, forming copses rarely more than waist height. Such copses are very extensive a t Inhambane (lat. 24"s. in Moqambique). Ceriops tagal will grow, apparently healthily, but certainly not as tall bushes, where salinities exceed BOX,. At Inhaca a copse of elderly gnarled Rhizophora mucronata grows in soil of %%,, and similar copses of R. stylosa occur a t Darwin in soils of similar salinity of ground water. Avicennia marina appears to have the widest range of salinity tolerance of all mangroves. It can grow in almost fresh water or in soils of water salinity exceeding go%,. Under the latter conditions the trees are dwarfed, with very extensive root systems and with large numbers of salt-secreting glands. Under conditions of fresh water the root system is not disproportionately extensive and salt-secreting glands are absent from the leaves. No doubt this wide salinity tolerance is responsible for the wide range of this tree. Species with a lower tolerance range are restricted to a narrow zone with a mangrove. Sonneratia alba, 5'. apetala andX . griSfithii are all found in the seaward fringe and would seem to prefer waters of near normal salinity. On the other hand, 8. caseolaris only grows where the salinity is low, less than

lo%,.

Species of Bruguiera normally grow in those portions of the mangrove with salinities less than as%,. B. parvi$ora reaches its maximum development around 20%,; B. sexangula prefers soils with a low salinity, lo%, or less. B. gymnorhiza has a tolerance of from around 10-25%,.

Aegiceras corniculatum is always an indicator of the presence of fresh water. Hence it may be found on the shores of bays along the seepage line, along the banks of tidal rivers upstream of any other mangrove-species or where a fresh water swamp merges with a mangrove.

S. ortmonni

Inhoca, MaSambique

Rainfoll 750 mrn

- U.

urvillei

U. urvillei

O t

FIG.33. Diagram to show the distribution of mangroves and the associated fauna in the Sac0 da Inhaca, a bay on Inhaca Island, southern MoGambique. Bare areas are conspicuous and the mangrove swamp is dominated by thickets of C e r i o p tagal with bushes averaging 1:-2 m tall. Rhizophora mucronata reaches 10 m tall and the trees are slender. Bruguiera gyrnnorhiza is rare, occupying a narrow belt behind the rhizophora trees. The seaward zone of Awicennia marina is of a single row of old trees around 10 m tall and sprawling. The figures indicate the salinity (in g per litre) of the soil water.

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3. Waterlogging of the soil Certain species of mangrove only grow in well-drained soils. These include Xylocarpus spp., Lumnitxera spp. and such mangrove associates as Osbornia octodonta and Pemphis acidula. Avicennia marina, particularly a t its distributional limits, becomes taller in the better drained soils at creek edges than farther back. Also the trees of the barringtonia association show preferences for well-drained soils, while those of the nypa association grow in waterlogged soils.

To sum up : a complete zonation will only be found in an area with a considerable intertidal range, with a high rainfall a t all seasons, i.e. with an excess of water availability over loss by evaporation and transpiration, and where silt in suspension is available to ensure that a deposition of mud on the surface of the soil is always raising the soil level so enabling the mangrove to extend seaward. 4. Influence of gullies, creeks, rivers and channels These are names for four sizes of waterway in a mangal. A gully will probably dry out a t low tide and be continuouswith a creek which retains water a t low tide. A river will be larger and like the larger creeks will have an origin on the land rather than within the mangal. A channel is a seaway formed by anastomosingof creeks and rivers and surrounding islands within the mangal. Some of these islands in Sumatra may be very large, large enough to be included in ordinary atlas maps of the area. Gullies and creeks are a natural result of the drainage pattern of all intertidal flats whether extensive off-shore "waddens " as in North Holland, or salt marshes or mangals. The larger creeks are the continuation of small streams coming off the land; others have their origin in gullies which result from the stresses set up in the soil when the tide ebbs. All creeks tend to cut down to a level close to that of mean sea-level. As a result they cut below the water table and hence the drainage in their vicinity is improved. Thus species of mangrove, characteristic, even diagnostic of well-drained soils, tend t o cluster the edges of creeks. At the seaward end Sonneratia alba, 8. apetala or S. griflthii and Avicennia marina border the mouth of the creek ; upstream they are replaced by rhizophoras with prop roots arching into the water. These in turn become interspersed and later replaced by Xylocarpus granatum, species of Avicennia ( A . alba and A . intermedia in South East Asia, A . marina elsewhere) and towards the limit of saline influenceAegiceras

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WILLIAM MACNAE

corniculatum, species of Pandanus and other components of the barringtoniaand nypa associations. Behind there persists the bruguiera forests which may be extensive or merely a strip separating the creek from ceriops thickets. Towards the latitudinal limits of mangroves where normally dvicennia marina is the only mangrove present, the trees bordering the creeks are taller as a result of better drainage as the banks of the creek a,re approached. This is stressed by Chapman (in Chapman and Ronaldson, 1958) in his study of mangroves near Auckland, New Zealand. Chapman suggests that waterlogging of the soil causes

FIG.34. A chenier being developed in front of a forest of Rhizophora. mucronata. Note juvenile Casuarina equ.isetifolia, Thespasia. populnen and even COCOS ?amifera with Ipomoea pes-caprae along the tide mark.

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dwarfing. The only other locality where I have seen dwarfing similar to that near Auckland is a t Inhambane in Moqambique, but here dwarfing is due to hypersalinity in an infertile well-drained sandy soil. 5 . Effects of erosion on mangrove shores

It has been shown above that a fully zoned mangal is typically developed on a shore which is recently emergent or t o which silt or other material is accruing. A mangal on a stable shore line tends to be less extensive in width, to have a high proportion of mature trees, and

FIG.35. Erosion of rhizophora forest. Note the shallow root system. This photograph was taken 300 m from Fig. 34. A field of Sonneratia griflthii and Avicennia marina extended to seaward on the lower platform. Xanthid crabs are common among the exposed roots.

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WlLLIAM MACNAE

t o be shut in from wave action by the development of cheniers or some other form of sand dune. But all this may change as a result of vagaries of currents either in the rivers or in tidal channels just off shore. A shore of accretion may become a shore which is being actively eroded. What, then, is the effect on the mangal? Carter (1959) has made a short study of these problems on the western shore line of Malaya. She indicates that species of mangrove react differently. Species of Avicennia and of Xonneratia are more vulnerable than species of Bruguiera and these more vulnerable than species of Rhizophora. This bears a direct relationship to the depth of rooting of the trees. The soils of the seaward fringes are ill-consolidated and so clearly very susceptible t o slight changes of currents, changes which tend to remove and not deposit soil. Hence these fringes will soon succumb to wave action. It will take a slightly longer period to breach the rhizophora forests, but once this is done the remainder of the mangal is quickly destroyed merely because the soil is washed from under the trees. It is this sort of process which has been responsible, according to van Bemmelen (1949), Umbgrove (1949) and Obdeyn (1941a-c, 1942a,b, 1943, 1944))for the widening of the Straits of Malacca and for the reorganization of shore lines on either side of these straits and southwards along the north shore of Sumatra. Erosion of a shore often, if not always, follows on the removal by man of a mangal. Certain of the areas studied by Carter (1959) show erosion as a result of human interference, as for example at Pontian in south Johore where cultivation comes right up to the shore. Here attempts have been made to recolonize with species of Avicennia planted behind a shelter of fishing stakes and brushwood. This has been to some extent successful (Rep. For. Adm. Malaya, 1956).

111. ADAPTATIONS SHOWNBY

THE

FLORA

A. Adaptations to growing in ill-consolidated muds Very few species of mangrove are deep rooted, or have persistent tap roots. Almost all are shallow rooted but the root systems are often extensive and may cover a wide area. Rhizophoraceous trees have seedlings with a long radicle which would seem well suited t o develop into a tap root., but as soon as the seedling becomes established in the mud the radicle develops little further. I n Rhizophora (Figs. 35 and 36) its function is taken over by a system of bunches of roots developed at the end of the prop roots about a foot underground. These roots are thick and air filled and give rise to nutritive roots which penetrate the

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137

FIG.36. Diagrams to show the rooting system of species of Rhizophom. There is no tap root, and the prop roots end in a knob-like mass from which anchoring roots radiate. The uppermost ones bear most of the nutritive roots (cf. Fig. 35).

uppermost layers of the soil. In Bruguiera and Ceriops a system of air-filled cable roots send knees up above the surface and these possess lenticels (Fig. 3 7 ) : nutritive roots are also given off in the subsurface layers. The rooting systems of Xonneratia spp., Avicennia spp. and Xylocarpus spp. have no tap roots a t any time. These trees develop very extensive systems of cable roots which lie some 20-50 em below the surface (Fig. 38). Many specimens of Xonneratia and of Avicennia

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WILLIAM MACNAE

FIG.37. Rooting system of Ceriops tayal. Note buttresses a t the base of the trunk and thr krire roots. Inhaca Island. (Photo : A. 0. D. Mogg.)

growing in the seaward fringe give the impression of floating in the mud. The root system of Sonneratia has been described by Troll (1930) and by Troll and Dragendorff (1931) in relation to its functioning. Trees of Avicennia and of Sonneratia develop several different kinds of roots. The main rooting system consists of large cable roots which give off anchoringroots downwards and aerial roots or pneuinatophores upwards. These pneumatophoresin their turn produce a large number of nutritive roots which penetrate the mineral-richsubsurface layers of the soil. Troll suggests that the main function of the pneumatophores is that, by their upward growth through the soil accruing on the Nutritive

root

root

FIG.38. Diagram to show the pattern of the rooting system of Sonneratia spp. Species of Avicennia, Lumnitzera racemosa, Xylocarpus moluccense and X . australasicum have a similar root system.

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surface, they ensure that nutritive roots can always be pushed out into these rich layers. These layers of soil also contain some oxygen as the result of the activities of burrowing animals. I have frequently found bivalves in cocoons formed by interlacing roots and byssus threads. The bivalves extend their siphons t o the surface and circulate sea water through their mantle cavities. This activity helps oxygenate the mud around them which is always paler than that only a little farther away. Troll suggested that the respiratory function of the pneumatophores is less important than the nutritive function. But this is not necessarily so. Emould (1921) suggested and Scholander et al. (1955) have shown that, in both Avicennia nitida and Rhizophora mangle from Florida,the air capillary system of the roots is in communication with the lenticels of the pneumatophoresor prop roots. I n the case of Avicennia when the tide covered the lenticels on the air roots the pressure in the root system began to drop and continued to do so until the tide began to fall. Then air was rapidly sucked in. At low tide oxygen concentration was around lO-lS%, when submerged the oxygen content fell, to return again to this level when the lenticels were exposed to air as the tide ebbed. This rhythm was not present in trees growing a t a high level where the roots were rarely submerged. When the lenticels were closed by greasing them, the oxygen in the roots fell reaching in one or two days 1 % or less, proving that the pneumatophores are chimneys serving as ventilators of the root system in the anaerobic mud. I n the case of Rhizophora the lenticels on the prop roots acted as ventilators and the oxygen concentration of the underground roots displayed a similar variation to that shown by the cable roots of Avicennia. The deeper layers of the mud are not only anoxic but are also saturated with hydrogen sulphide, so i t is essential that there should be no communication between the anchoringroots and the soil around them. But some hydrogen sulphide may be present in the upper layers of the soil in which the absorptive roots lie. When one realizes that those polychaetes which live in such muds are relatively insensitive to hydrogen sulphide (and to cyanide) one wonders why no work appears to have been done on the sensitivity of mangrove trees to such poisoning. The form of the pneumatophores varies from slender pencil-like structures in Lumnitzera racernosa and Avicennia spp. (Figs. 14 and 25) to stout knobbly structures in Xonneratia spp. and Xylocarpus moluccensis. Geriops spp. and Bruguiera spp. possess variants of knee roots which rise above the surface and go down again; these are connected to,

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WILLIAM MACNAE

FIG.39. Rooting system of Xylocarpus granatum. Note the sub-aerial flanges on the lateral cable roots. March 1962.)

Near Innisfail, Qucensland. (From 8 colour transparency,

or in fact are, the cable roots of the trees. Xylocarpus granatum, when growing in markedly anoxic soils, has an upwardly projecting flange along those of its cable roots which are lying just below the surface (Fig. 39). I n Rhizophora spp. the prop roots are first derived from the hypocotyl, but once the seedling is established they are derived from the stem. I n R. apiculata particularly, they may originate in any part of the sub-aerialparts of the tree. These roots until they reach soil level are normally unbranched; branching of a prop root is usually the result of injury.

B. Xpecializations of stems and leaves This is a subject of dispute. A review of the general physiology of halophytic plants including mangroves has been given by Uphof (1941). A summary of the relationships between the structure of mangrove plants and their physiology has also been given by Reinders-Gowentak (1953) and van Steenis (in Ding Hou, 1958). These two do not agree with Uphof’s findings, for Uphof discounts the xeromorphic structure of mangroves which they accept. Sehimper (1891) and in the first edition of his “Pflanzengeographie ” (1898) classified the mangroves among xerophytes, basing

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his arguments on the fact that they grow in water of quite high salinity and that the leaves of most mangroves show a degree of succulence in having water storage tissue in the leaves. He considered the environment to be “physiologically dry ”. Uphof and also von Faber (p. 35 of his revision of the third edition of Schimper’s “Pflanzengeographie”, 1935) regard this assumption as being unjustified. Mullan (1931a,b, 1932-33) and Walter and Steiner (1936) show that the stomata of mangroves are not protected and that they are present on both surfaces of the leaves. According t o von Faber (1935, loc. cit.) the transpiration rates of both Avicenniu marina and Rhizophoru mucronata are higher than that of Mungifera indica (the mango tree) under similar conditions of temperature and humidity. No evidence is given as to what these conditions were! On the other hand, Walter and Steiner regard the transpiration rate as being low. I n the species they studied at Tanga (Tanzania), viz. A . marina, R. mucronatu, S. alba, C. tagal and L. racenzosa, they recorded values lower than those found by Stocker (1935) for tropical glycophytes. More work on this subject appears to be necessary. The function of the water storage tissue present in the leaves is unknown. I n Sonnerutia ulba Walter and Steiner record that leaves on the lower branches have more of it than those on the upper branches. Figure 40 shows this difference. Uphof argues that, since the water storage tissue in most mangroves lies between the upper epidermis and the palisade chlorenchyma, its function may be to filter off heat rays. On the other hand, its central position in Sonneratia precludes this. No work appears to have been done on mangroves equivalent t o that on the biochemical functions of succulence in various desertic plants of the family Crassulaceae. The osmotic pressure of halophytes is normally higher than that of non-halophytes, but again values given by different workers show much variation. Taken generally, values given by more recent workers using kryoscopic methods are lower than those of earlier workers using plasmolytic methods. Kryoscopic techniques demand a quantity of fluid. This is normally obtained either by homogenizing several leaves and then finding the osmotic pressure of the filtrate or by pressing fluid from leaves. I n either case the contents of all the cells in a leaf are mixed. It may well be that the contents of the water storage cells have a lower osmotic pressure than the chlorenchyma which formed tbe substrate of the plasmolytic observations. Walter and Steiner (1936)found values around 32 atm for SonrLerutia alba and Rhizophora mucronata. The soil water showed an osmotic

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pressure of 23-25 atm (this is normal for sea water). On the other hand, Avicennia marina varied between 35 and 46 atm. Sen Gupta (1938) found similar values in the Ganges delta (at the mouth of the Haringhanga river) listing Aegiceras corniculatum with 38.2 atm, R. mucronata 32.1 atm, Avicennia marina 25.9 atm, Ceriops decandra 26.7 atm, Lunznitzera racenzosa 41.9 atm, and Xylocarpus granatum with 39.9 atm against a water analysis of 9.84 atm. Whether the osmotic pressure shows variation with varying salinity of the soil does not seem to have been investigated. According t o Cooper and Pasha (1935) the suction pressure or hydrostatic pressure follows the values of the osmotic pressure. They record suction pressures 60-82 atm in the stem of Xonneratia apetala at Bombay against osmotic pressures of 60-85 atm with a soil water osmotic pressure of around 25 atm. The discrepancy in measurements of osmotic pressures seems to point t o a need for further investigations. Salt excretion occurs in species of Avicennia, in Aegiceras corniculatun?,and in Acanthus ilicifolius through epidermal glands (Fig. 40) of very similar form in the three genera. Those of Aegiceras were first described by Areschoug (1902a,b) and by Schmidt (1904a). Mullan (1931a) gave descriptions of all of them and pointed out that these glands occur on both leaf surfaces and on the petioles as well. He also reported that they are more abundant on the leaves of trees and bushes growing in hypersaline areas and absent from plants of Acanthus ilicifolius growing in fresh water. Ruhland (1915) studied them in Aegialitis unnulata, and Walter and Steiner (1936) those of Avicennia marina. Scholander et al. (1962) have given some attention to the salt balance in mangrove trees. They have shown that the xylem sap of species bearing salt glands (Aegialitis annulata, Aegiceras corniculatum and Avicennia marina) had a concentration of 0.2-0.5% sodium chloride. The xylem sap of Rhizophora mucronata which does not have salt glands contained one-tenth of that amount and Hibiscus tiliaceus less than one-hundredth.They give no comparablefigure for Sonneratia, the wood of which is said to corrode iron nails as a result of its salt content. FIG.40. Diagrams to illustrate the leaf anatomy of Sonneratia (A, B), Rhizophora (C, D) and Awicennia (E). I n the older leaves of Sonneratia and Rhizophora (B and D) the water storage tissue is much increased in extent by increase in size of cell. (Partlyafter Walter and Steiner, 1936.) Diagrams to show salt-excreting cells of Aconthus (F),Aegiceras (G) and Avicennia (H). There is a close resemblance of the form of the glands in these genera. (Partlyafter Mullan, 1931a.)

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E A vicennio

A Sonnerotio

B

C Rhizophora

D

rr

Acanthus

Aegiceras

A vicennia

FIG.40

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The Auid excreted was collected from bubbles of fluid which came t o lie above the salt glands. This fluid had been prevented from evaporating by coating the leaf with a film of grease. The fluid excreted was found to be some ten to twelve times as concentrated as the sap and higher than sea water on many occasions. They also point out that excretion proceeds even when the leaves are coated with salt: "It would appear that the glandular cells are capable of full activity, even though in direct contact with a saturated brine ". These workers also studied the hydrostatic or suction pressure and the transpirationrate. For transpiration, average day-time rates came out as follows: Aegialitis 5 mg/dm2/min, Aegiceras 2 . 5 , and Avicennia 6 . 5 . Comparable values for non-salt-secreting forms were Rhixophora 2 . 5 , Sonneratia alba 1-5, Lurnnitxera littorea 6.5, Hibiscus 6.5, and Eugenia suborbicularis 7.5. Measurements of the hydrostatic pressure suggested that salt separation requires an energy source and active transport, since the hydrostatic pressure is insufficient to allow separation by ultrafiltration.

C. Relationship between the mangrove root and shoot systems Avicennia marina would appear to be not only the most geographically widespread mangrove species occurring in the Indo-west-Pacific but also capable of growing at any level within the mangal, unless, of course, it has been superseded by another species. To what is this wide perspective in distribution due? After accompanying me through various mangals in the vicinity of Lourenqo Marques, Dr. P. Myerscough of the Botany Department, Edinburgh University, made a suggestion which may be worth following up. To quote from his letter:

Avicennia marina seems capable of growing under the least favourable nutritional conditions, as well as under the most favourable-if not ousted from them by other species. It seems to be the most plastic species in its growth, apparently capable of producinga widely rangingroot system under poor condit,ions[Figs. 14 and 151 together with a relatively sparsely leaved and slow growing and therefore undemandingshoot system ; undemanding both on nutrients and water transpired. Bruguiera gymnorhimon the other hand may be the least plastic species, it appearsto have an intensely crowded root system which is not wide ranging and a top growth which is leafy, casting a deep shade, and also relatively rapidly growing and so high demanding. In other words it has a growth pattern geared to make best use of optimal nutritional conditions, shading out would-be competitors above ground and crowding out their roots below. But these have poor survival value in poor conditions. Nothing of this has been tested experimentally but my familiarity with the distribution of mangrove species in the mangals along the

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coast of Moqambique and elsewhere suggests that experimental measurements may be worth while and that even in-the-field estirnations may yield evidence to verify such a suggestion. Under conditions of very poor soils, as for example in the Bay of Inhambane, Avicennia marina occupies the whole mangal and other species appear t o be unable to grow well enough to supersede it.

D. Viviparity Many species of mangrove show an apparent viviparity. The zygote, once formed, develops uninterruptedly through the embryo into the seedling without the intervention of any resting stage. This viviparity is frequently cited as a n adaptation to life in the mangrove zones. But other equally successful mangroves do, in fact, possess seeds with a resting stage.

FIG.41. Flowers and young fruit of Sonneratia alba, Quissanga, northern Moqambique. I have often wondered if these flowers are bat pollinated; they open in the evening and are not scented. (July 1967.)

The apparent viviparity is found in all the mangrove species of the Rhizophoraceae, in species of Avicennia and in Aegiceras corniculaturn (Fig. 42). It is not found in the species of Sonneratia nor in those of Xylocarpus, nor in Lumnitzera nor in any of the others. If there is any advantage in the possession of such viviparous seedlings it can only be in that they may root more quickly when they become grounded.

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I n the Rhizophoraceae, endosperm is unimportant. The radicle develops rapidly and grows out from the apex of the fruit through the tip of a cotyledonary body. This radicle continues to grow, in shape like a cigar, until it reaches a considerable length, up to 40 cm in R. mucronata (Fig. 42, 2). I n species of Rhizophora and of Ceriops the cotyledonary body emerges from the fruit around the radicle, and its appearance indicates that the seedling is almost ready to drop. This body does not emerge in species of Bruguiera (Fig. 42, 1 and 3). Its function is to absorb nutrients from the fruit. The seedling alone is dropped in species of Rhizophora and of Ceriops but in Bruguiera the

PIG. 42. Seedlings of viviparous species of mangrove.

( 1 ) Bruguiera yymnorhiza; ( 2 ) Rhizophora mucronata; (3) Bruguiera parvi$ora with plumule emorging through calyx; (4) Avicennia marina (a) newly germinated, (b) plumule elongating; ( 5 ) Aegiceras corniculatum (a) bunch of fruits, (b) young fruit and (c) germinating fruit.

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b F M

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whole fruit drops. I n B. parviJora the plumule breaks through the base of the fruit and the fruit, collar-like, encircles the junction of plumule and radicle (Fig. 42, 3). Growth continues as soon as the seedling is grounded. Most do not germinate in the mud beneath the parent tree but may float for some time before settling. In Aegiceras corniculatum (Fig. 42, 5a,b,c), quoting from van Steenis (in Ding Hou, 1958), "the embryo ruptures the testa and fills the pericarp which then starts to enlarge in proportion to the growth of the embryo ; after the enlarged fruit has fallen the embryo pierces the pericarp ". I n Avicennia spp. (Fig. 42, 4) there is a similar development and when the fruit drops i t seems to absorb water and then splits and the seedling breaks out of the pericarp. No description has been given of seedling development of Lumnitxera spp. I n Xylocarpus the fruit is very large (Figs. 43 and 44) ; that of X . granatum reachesthe size of a baby's head, and that of X . moluccense of a cricket ball. These fruits drop, float around, become grounded, rot, split and liberate the seeds which are by now ready to germinate. The time interval is unknown. Again nothing has been reported on the germination methods of such opportunist species as the beach thistles, Acanthus ilicifolius. I n development the ferns Acrostichum aureum and A . speciosum are normal. Spores of the former germinate in the landward fringe on bare soil or on cast up jetsam brought in by the tide. Spores of the latter behave differently. As has been mentioned above, this species is common in the bruguieraforests. On the floor of these forests Thalassina anomala casts up its mounds, the upper parts of which rise above the levels reached by all but extreme tides. On these higher parts of the mounds the surface dries out a little, becomes bound by blue-green algae and in these algal mats the fern spores germinate, and so a field layer is produced and the general soil level gradually raised by the ferns.

E . Xuccession Of the trees and herbaceous plants constituting a mangrove the following species seem to prefer t o germinate and become established in full sunlight or at most in only slight shade : "Acanthusilicifolius Ceriops decandra "Xonneratiaalba Lurnnitzera racemosa "apetala Aegialitis annulata "grifithii "Avicenniaalba Rhizaphora stylosa "marina mucronata Aegiceras corniculatum apiculata

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Of these the starred species are probably incapable of proper development in the shade of any tree, the others are more tolerant and may germinate and develop in the shade or in the open. Normally the pioneer on sheltered sea shores is Avicennia alba or A . marina or under special circumstancesXonneratia sp. Seedlings of these may be found far out on the beach but the level at which they occur will lie between mean sea-level and high water of the lowest neaps. Most of these seedlings become coated with silt and this acts, in the same way as shade, to kill off the seedlings. Those at higher levels develop into saplings, long and slender, giving each other support. A few a t the outer edge, from the beginning, develop as well-shaped, young trees. Chapman ( 1940) states that "successful colonization by these seedlings depends either upon a very shallow sea-where there is only a small tidal rise-otherwise there must be a considerable tidal rise and fall so that they are exposed for some hours during the day ". Once established the avicennias and the species of Sonneratia cause accretion by impeding water movement, the soil level rises, and others, spp. of Rhixophora, Bruguiera and Xylocarpus, germinate from stranded seeds or seedlings and become established. All these trees tend t o grow taller than the pioneers, overtop them and these then die off. Hence one rarely finds a well-grown tree of Avicennia marina in a rhizophora or bruguiera forest. Occasionally an old stag-headed tree of Sonneratia alba persists in these forests. Such trees are quite common in the Rufiji delta. The "nurse " effect of Avicennia marina at Richards Bay, Natal, has been mentioned by Macnae (1963). Against this Professor A. W. Bayer of the University of Natal, Pietermaritzburg, has suggested to me that in marginal areas such as Natal colonization of new banks of sand or of mud in a suitable estuary seems to depend on which species happens to be producing seedlings when the banks form. If it is A . marina then this species will colonize, if it is R. mucronata or B. gymnorhiza then one of these will be the first to become established. An extension of this principle may explain some of the vagaries in distribution of Avicennia alba, A. marina, Xonneratia alba and S. gri&thii in Malaysia. The species developing on an available mud bank will depend on the seeds which become grounded. But why one or sometimes another of these species develops in a pure stand is difficult to account for. Lumnitzera racemosa normally develops under light shade of landward fringe avicennias or in the shelter of grasses and rushes. Acanthusilicifolius is an opportunist. It will develop on any type of clearing and once established forms dense thickets which may prevent

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further succession because the floating seedlings cannot reach the soil. Much of the mangrove areas in Ceylon has been taken over by extensive clumps of these beach thistles. I n Malaya and western Indonesia several authors have described R. stylosa as a pioneer on coral debris in the shelter of a reef (Ding Hou, 1958). Its occurrence at Low Isles off the coast of north Queensland is compatible with this. R. nzucronata may occur in similar situations off the eastern shores of Africa and off Madagascar. R. apiculata has not been seen nor described from such localities. According to Ding Hou (1958) it develops best in clay soils and under conditions of reduced salinity. Nonetheless it is occasionally used by man to encourage deposition of silt, and thereby t o act as a pioneer. I suspect that this can only be done in areas of minimal tide. This use of R. apiculata is common in Ceylon, as for example around Negambo in areas which a previous generation of men may well have cleared of mangroves. Seedlings of R. apiculata are collected and planted in a row about 15 cm apart. This produces a dense hedge behind which accretion can take place and in due course a new plot is added to the garden of the “owner ” (personal observation). Aegialitis annulata was seen to act as a pioneer on coral debris a t Low Isles but one doubts if it would form the beginning of a succession. Species of Bruguiera and Xylocarpus and also Ceriops tagal all develop under the shade of other trees or of themselves. Hence these species are diagnostic of well-established mangroves and they themselves form an important stage in the development from mangrove to freshwater-swamp forest or terrestrial forest.

IV. DISTRIBUTION OF TERRESTRIAL ANIMALSWITHIN

THE

MAN

Just the place for a snark! ”the Bellman cried, As he landed his crew with care; Supporting each man o n the top of the tide By a finger entwined in his hair. Lewis Carroll: ‘‘The Hunting of the Snark.” “

When an animal ecologist regards critically the environment provided by the mangal he recognizes that several different kinds of unit exist in this environment. I shall list five of these. (1) The canopy of the trees, composed of the uppermost parts of the trunks, the branches, twigs, leaves, flowers and fruits, is never reached by sea water and only rarely by any spray: it constitutes an essentially terrestrial habitat and as such may be expected t o support an essentially terrestrial fauna. I n general this is so, but few, if any, detailed or even superficial studies of the environment or its fauna have been made.

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The lists of birds and mammals given below, are the result of my own sight records supplemented by records given in various taxonomic books on the birds and mammals of the regions concerned. A few studies of the insects affecting such crops as coconuts, mangoes, cloves and cashew nuts grown in the maritime regions round the Indian Ocean give hints as t o which insects might be expected in the mangrove areas nearby. The accountsgiven by Vanderplank (1960) and by Way (1954a,b) of the ecology of the tailor ant, Oecophylla sp., probably apply to the colonies of these ants on various mangrove trees (see Fig. 57). ( 2 ) The presence of rot holes in the branches, and collections of water in the clefts between branches and trunks provide a near freshwater environment for developing insects and are of medical importance in relation to mosquito carriers of viraemias, filariases and to a lesser extent malaria. (3) The surface of the soil constitutes an environment which is now submerged and now emergent and sub-aerial. The surface layers of the soil and the small collection of sodden litter above it have interstices which are now water-filled and now air-filled. The animals living there must be tolerant of both sets of conditions or have developed behavioural patterns which enable them to survive. For example, as the tide rises certain crabs and ants close their burrows with a plug of soil and remain in a bubble of air while the tidal water covers the soil. Compared with a completely terrestrial forest there is little or no litter. Dead leaves are dropped a t all seasons and only in the landward fringe do they tend to collect, there t o provide shelter for many species of tiny gastropods-species of Melampus, of Xyncera (= Assiminea), and of various other genera. Elsewhere the leaves are devoured soon after they fall. I have often seen specimens of Sesarma scrambling after and squabbling over a fallen leaf which is finally dragged to a burrow and eaten in the doorway. (4) Animals may live in the soil and by their activities modify it. (5) Permanent and semi-permanent pools may provide an environment a t a topographically higher level for animals which would normally be found only in the water courses of the mangal or a t the seaward fringe. It is only the last three of these categories that I have studied personally, and then primarily to establish what crabs and molluscs are there, their habits, zonation and distribution. Few attempts have been made to find out how any individual species arrives in its chosen environment, and once there, how it succeeds in coping with these types of environment. A.iK.B.-6

6

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Just as there is a broad similarity between the facies shown by mangrove trees all round the Indian Ocean and into the western Pacific, so there is a broad similarity in the distribution of the marine fauna of the mangrove areas. Genera and even species are common to all mangals in the Indo-west-Pacific. Some genera and some species are more restricted in distribution, and sibling species may replace one another. Although no taxonomist has dared to suggest it, one has often suspected that some of the sibling species will be found to be genetic variants, differentiated from one another by a few genes only and may well be stages of a cline. For example, Eggert (1935) has described a series of often nearly sympatric species of Periophthalmus, species which differ in small ways and several of which may in fact be, not separate species, but rather local populations of variants of a much smaller number of widespread polytypic species. Similarly several of the smaller species of Sesarma and of certain ocypodid genera may, in spite of their differences, be units of a cline. While the plants in a mangal will always show a tendency towards, and under optimal conditions always demonstrate a very distinct and characteristic zonation, it is always more difficult to define a zonation among animals. Most animals can readily move away from places when conditions become unsatisfactory, and so their distribution is governed by other factors in addition to those appertaining to the soil, the weather and the intertidal level. A few more sedentary, burrowing forms only, cannot easily move away. Animals are more likely t o be affected by conditions of shade and exposure to the sun than by the nature of the soil, by salinity (except a t extremes of high and low salinity) or by distance above mean sea-level. Several species of crab may be found wandering a t any level in the mangal but will hold territory a t some particular level. Some burrowing crabs are more widespread than non-burrowing forms, since t o some extent they create their environment. The question is often asked as to whether there is a distinct mangrove fauna or not. The answer is that there exists on all shores of mud, or mixed mud and sand, a fauna which is not found elsewhere and of which certain elements demand the shelter of vegetation. I n the tropics and subtropics these elements will always be associated with mangroves. Beyond the region of occurrence of mangroves, representatives of such a fauna may be found in the shelter of grasses such as species of Xpartina. A mangrove area, like any other intertidal area is an area of transition from the sea to the land and from the land t o the sea and hence its fauna may be derived from either.

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Of the land animals that invade the mangal many remain, in fact, terrestrial. Birds characteristicof fresh waters are attractedto mangals, seeking their food in the creeks and channels and nesting in the trees. Only a few such as the "mangrove kingfishers " are restricted to mangals. This is even more true of the mammals, amphibians and reptiles. Insects fall into two groups, some are visitors, bees drawn t o seek honey from Aegiceras and the rhizophoras; some are parasites, the beetles which bore into the living trees, and the coccids which often cover the leaves and young twigs of members of the Rhizophoraceae ; some, such as the "tailor ants ", come after the coccids ; some beetles come to bore into dead branches and trunks. All these are still terrestrial. Other insects have larvae which live in the uppermost layers of the soil and only here ; these are dependent on the soils at this level for their existence but not on the mangal, for they persist even when the mangal has been cleared. This is true of ceratopogonid larva.,e in northern and eastern Australia, where clearing of mangroves has not reduced the nuisance created by adult forms of these midges, so often miscalled sandflies. A. Birds associated with mangals One or other of several cormorants may be seen: Phalacrocorax carbo (L.) occurs all round the Indian Ocean ; of the smaller long-tailed species, P . africanus (Gm.) is found in Africa, P. melanogaster Vieillot in New Guinea and Australia, and P. niger King from India to Borneo. These last three are similar in size and appearanceand are characteristic of rivers and estuaries. Along African and Australian mangrove channels cormorants may be frequently seen, yet it is surprising that they seem to be most uncommon on the coasts of western Malaya and peninsular Thailand. Darters Anhinga anhinga (L.) are common ;they are often abundant in the larger rivers and delta distributaries, but rarely enter the more purely marine channels of the mangal. Herons use the channel banks as fishing grounds and often nest communally with cormorants and darters in the taller trees in the more isolated parts of the mangal. Egretta alba (L.), the white egret or white heron, and E . garzetta (L.),the little egret, extend from Africa to Australia. E . gularis (Bosc.) is said to pick up mud-skipping fish on the seaward fringes in India, and E . eulophotes (Swinh.) is also found along the creeks and channels in South East Asia. Nycticorax nycticorax (L.), the night heron, extends from South Africa to South East Asia and Hawaii; N . caledonicus (Gm.) replaces it from the Philippines through Indonesia to Australia. Ardeola grayii (Sykes), the paddy

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bird, is common in the landward fringes of mangals in India. Various subspecies of the green-backed heron Butorides striatus (L.) occur throughout the Indo-west-Pacificand may be met with on the banks of the mangrove channels. Ardea sumatrana Raffles is a large heron typically found along mangrove creeks in South East Asia, the Indonesian archipelago and Australia. A. cinerea L. may be seen in similar situations in eastern and southern Africa and in western India. The hammer-head Scopus umbrettus (Gm.) is often seen in African mangals, and I have seen its huge nest in a bruguiera tree on one of the distributaries of the Zambezi. Leptoptilos javanicus Horsf., the lesser adjutant, is frequently seen along the shores of the Bay of Bengal from the Sunderbansto Malaya. Sea eagles replace one another round the Indian Ocean : Haliaetus vocifer (Daudin) is common in the estuaries and mangal creeks in eastern Africa and H . leucogaster (Lath.) replaces it to the eastwards. The osprey Pandion haliaetus (L.) is cosmopolitan, but never very common in any one locality. I n southern and eastern Asia through Indonesia t o northernand eastern Australia the brahminy kite Haliastur indus (Bodd.) is a scavenger and fisher, being especially common around the towns and villages built in the mangals of Malaya. Species of Ichthyophagusare common in Indonesia, where Schuster ( 1952) reports that I. ichthyaetus may be troublesome t o farmers of fish and prawns in Java. Abdulali (1965) confirms a statement made by Butler (1899) that specimens of Spilornis cheela Hume, the serpent eagle, which had fed on crabs from the mangal creeks and channels of the Andaman islands, were usually paler in colour than were inland birds. Kingfishers may be divided into two distinct groups according to habit. The fishing species Ceryle maxima (Pallas)and Ceryle rudis (L.) are widespread in eastern Africa, in mangals as elsewhere, the latter species occurs as far east as Burma. Species of the brilliantly coloured Alcedinae find good fishing along mangal creeks as well as streams and rivers inland. Insectivorous or cancrivorous species may be restricted t o mangals. Halcyon senegaloides Smith is so restricted in eastern Africa. On the other hand, H . chloris (Bodd.) in southern and southeast Asia, its subspecies sordidus (Gould) in Australia and Pelargopsis capensis (Shaw) in South East Asia, are not restricted to mangals but occur also in the maritime forest or scrub ; however, they never go far from the sea. It has recently been reported (Medway and Nisbet, 1965) that in Malaya several species of wader may be found perching on the branches of the mangroves in the seaward fringes during the high tide period (Fig. 45). They scatter over the mud flats as soon as the tide has fallen

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sufficiently. The species involved are whimbrel Numeniusphaeopus (L.), redshank Tringa totanus (L.) and Terek sandpiper Tringa terek Latham [= Xenus cinereus (Guldenstadt)]. No doubt other waders recorded from Malaya will do the same. Normally these birds rest on bare ground or in fields behind the mangroves, but since such are completely absent from Malaya this perching habit has been adopted. I have seen whimbrel and redshank perching in trees of Avicennia marina var. alba a t Beiiut just north of Singapore and on sonneratia trees a t the inner end of Sandakan harbour in Sabah.

FIG.45. Redshanks perching on a branch of a rhizophora a t high tide. SandakanBay, January 1967, during a rain storm.

Torres Strait pigeons Ducula (or Myristicivora) spillirrhoa (a.R. Gray) during the summer months breed on the mangrove trees associated with the low-wooded-island reefs of the Great Barrier Reef. These birds feed on the mainland and that they navigate by sight is clear from the manner in which they get lost whenever a rain storm comes up late in the afternoon. Pied imperial pigeons Ducula (or Myristicivora) bicolor (Scop.) frequent islands off the Malayan coast. It is not known where they nest but the coloured illustration in Robinson and Chasen (1936) indicates that they may be similar in habit to Torres Strait pigeons. Woodpeckers Picus viridanus Blyth and P . vittatus Vieillot seek for insect larvae in the older trees of the landward fringe in Malaya and peninsular Thailand.

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Passerine birds are not common in the mangal, although the Malayan bird reports by Medway and Wells (1963, 1964) and Medway and Nisbet (1965) indicate that they are very common in the nypa zone behind. Within the mangal of Malaya the grey tit Parus major L. and the flycatcher Muscicapa rujgastra Raffles seem to be restricted t o the mangal (Medway, personal communication) and the pied fan-tailed flycatcher Rhipidura javanica (Sparrm.), the yellow-vented bulbul Pycnonotus goiaver (Scop.), and the olive bulbul P. plumosus Blyth are certainly also common in but not restricted to mangals. I n Borneo, Smythies (1960) lists a mangrove whistler Pachycephala cinerea (Blyth) and Zosterops chloris Buonaparte as being common in mangals. He also states that Nectarinia chalcostetha Jardine shows a distinct preference for the flowers of species of Bruguiera. I n the vicinity of the fishing villages and townships built on stilts within and a t the edges of mangals, in Malaya and in southernThailand, the crow Corvus macrorhynchus Wagler is a common scavenger. In eastern and southernAfrica Corvus albus Muller, the pied crow, occupies a similar niche. B. Amphibians and reptiles The edges of mangrove creeks and the banks of rivers running through mangalsare the hauntof the largest of the crocodiles,Crocodilus porosus Schneider,which extends from Ceylon and south India t o south China, the Philippines and Australia. The African C. niloticus Laurenti comes down into estuarine mangals in eastern Africa, but is not restricted to them. The water monitors Varanus niloticus (Kuhl.) in Africa and 8. salvator (Laur.) in South East Asia from Ceylon t o Indonesia are also common in mangals. Loveridge (1945) ascribed the wide distribution of the latter to its ability as a swimmer. Its compressed tail and valvular nostrils are, no doubt, adaptations t o a semi-aquatic existence. Hydrophiid snakes are of common occurrence throughout the Indo-Australianarchipelago (Smith, 1926). They have formed a source of leather in the Philippines. Two pit vipers Trimeresurus wagleri (Boie) and T . purpureomaculatus (Gray) occur within the mangal. They are sluggish snakes and do not move away when disturbed. They occur only within the Malay Peninsula and Thailand south of the isthmus of l i r a and in Sumatra. Boiga dendrophila (Boie) a cat snake, Fordonia leucobalia (Schleg.) and Bitia hydroides Gray also occur in the Malayan area, Cerberus rhynchops (Schmid.), the dog-headed water snake, may be very common and has been seen to enter crab burrows, presumably in search of its prey. One frog Runa cancrivora Gravenhorst has been reported by Pearse

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(1911) and Annandale (1920) from brackish water ponds and from mangrove areas in South East Asia. Its tadpoles are common in pools within the mangal (personal observation) and Pearse (1911) records that the eggs are laid in crab holes. Rana limnocharis has subspecies in the Philippines and in Timor which also enter salt water with impunity (Neil, 1958).

C. Mammals Of mammals a few monkeys have adopted the habit of visiting and even of living within the mangals. Monkeys become clever a t catching fish and crabs but have not been seen to eat the fruit of mangroves. Sykes’s monkey, Cercopithecus mitis Wolf, was commonly seen eating crabs on the banks of the distributaries in the Rufiji delta. Macaques, formerly included within Macaca irus Aw., a name which covers many species, are common in South East Asia and penetrate to Java and Borneo. One of the species in this group is said by Schuster (1952) to be a nuisance around the fish ponds of Java. Leaf monkeys Presbytis cristatus (Raffles) in Malaya and proboscis monkeys Nasalis larvatus (Wurmb.) in Borneo are almost entirely restricted t o mangals. Both of these have complex stomachs to deal with the mass of leafage eaten by them. Occasionally small carnivores such as the fish cat Felis viverrima Benn. and mongooses Herpestes spp. may visit mangrove areas seeking fish and small birds, and may even live there. Otters are common but rarely seen : Amblonyx cinerea 111. and Lutra (Lutrogale) perspicillata Geoff. in South East Asia ; Lufra (Hydrictis) maculicollis Licht. in eastern Africa. None of these mammals has penetrated to Madagascar or to Australia. Wild pigs Sus scroj’a L. and mouse deer Tragulus sp. are common in the nypa swamps. Flying foxes (Pteropus spp.) roost in large camps in the mangals of Australia. They have been suspected of being reservoir hosts of viraemias of man and domestic animals. Some of these camps contain 10 000-220 000 individuals (Ratcliffe, 1930). Flying foxes do not reach the African mainland but do roost in the mangals of Pemba and of Madagascar.

D. Insects The flowers of Aegiceras cornicula,tumform an important source of commercial honey in Australia and no doubt of wild honey elsewhere in its range. Bees also visit the flowers of species of Rhizophora but the honey is said by Australian aboriginalsto be poisonous. Stewart (1954)

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records that American salt marsh mosquitoes visit flowers of Avicennia before flying off to search for it blood meal. Indo-Pacific species probably also look for such a source of fuel. The nests of species of the weaver ant or tailor ant Oecophylla spp. are conspicuous (Fig. 5 7 ) , most often on trees and bushes of Bruguiera or of Ceriops or of Sonneratia caseolaris. The ecology of Oe. smaragdina has been studied by Vanderplank (1960) who has shown that a colony may consist of several nests. Little is known of the coccids which thickly clothe leaves, etc., of certain trees, particularly those colonized by Oeeophylla, nor of the beetles which bore into these trees. Lever (1952) has reported that the caterpillars of a species of the moth Argyroploce are leaf tiers which spin a not very dense web on the twigs and leaves of young trees of Sonneratia grifithii. These caterpillars do not climb to higher levels but remain where they are when the tide flows. The larva is not specially adapted t o survive submersion, but it does so without ill effect. The presence of biting insects makes difficult any investigations in mangrove areas, for their bites are vicious and may produce strong reactions in an investigator. Mosquitoes are often incredibly numerous. At Darwin, in January 1962, over eighty mosquitoes, presumably Aedes vigilax (Skuse), settled on my bared arm within two minutes. This degree of abundance is exceptional. Many mangrove-associated mosquitoes have odd breeding habits. For example Aedes pembaensis (Theobald), common from the Bay of Lourenpo Marques northward on the coast of Africa, lays its eggs on the claws of Sesarma meinerti (see Worth et al., 1961) and the larvae emerge and develop to adults in the pools a t the foot of the burrows inhabited by the crabs. These larvae and pupae are pallid (Macnae,unpublished observations). A salt-water species of Anopheles close to but probably not identical with A . gamhiae Giles, from which it has not been distinguished, is responsible for much of the malaria in coastal eastern Africa and as far east as Mauritius. This species is characteristically found in open areas behind the mangroves (Thompson, 1951 ; Paterson, 1963). Anopheles (Myzomyia) sundaicus (Rodenwaldt) is a mosquito occurring in coastal districts throughout South East Asia from India to south China and in the larger Sunda Islands but not eastwards of these. It was responsible for most of the malaria there. A . sundaicus breeds exclusively in brackish water of chlorinity 4.8-1 3 x 0 (Hodgkin, 1956). The breeding pools are, as a rule, found a t the limits of tidal rise, where the tide reaches only once or twice per month. Rain and seepage water dilute the dammed-up sea water t o a point that is suitable for the mosquito. Larvae are also common in disused boats where sea

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water and rain water mix. Prolific breeding is often associated with sunny pools in which an alga Chaetophora sp. is growing. A . (Anopheles)baezai Cater is also common in brackish pools but rarely in identical situations. It prefers more shaded areas. This form is not an habitual biter of man. Culicine mosquitoes are also abundant, finding breeding places in pools a t ground level, in water collecting a t the bases of leaves of Nypa, in rot holes in the trees and in the burrows of the crabs. Aedes fumidus Edwards (distributed from Singapore to Celebes) tends t o occur in pools on the ground ; A . niveus Ludlow (widespread from India to south China and the larger Sunda Islands) occurs in collections of water a t about 44 m high in the trees ; A. littoreus Colless is also a tree dweller. A . butleri Theo. (againwidespread from India to South China and the larger Sunda Islands) is the commonest biter of man in nypa plantations, and its larvae occur in ground pools. A. amesii (Ludlow) which occurs from Malaya and Sumatra to the Philippines and Thailand is the commonest biter of man within the mangal and it develops in rot holes. ( A . Rep. Inst. med. Res. Malaya, 1960.) My attention was drawn by Dr Ivan Polunin of the University of Singapore to mosquitoes settling on and apparently feeding on the back of the head of the mud-skipping goby Boleophthalmus boddaerti (Pallas). Unfortunately, owing to the natureof the soil and its extreme softness it was impossible to capture the mosquito. This phenomenon was first reported by Sloof and Marks (1965) who described that, in the Solomon Islands, the mosquito Aedes (Qeoskusea)long$orceprps Edwards was captured while biting a species of Periophthalmus. This species of mosquitoes breeds in the holes of land crabs* near the coast and bites man readily. It is the commonest species of its subgenus in the Solomons. Marks (1947) has shown that five species of mosquito are associated with mangroves in Australia. Aedes vigilax, a species common from Thailand to Australia, breeds in all pools to landward of the mangroves below high water mark. The eggs seem to be laid in pools left by one high tide and develop through their life cycle before the next series of high tides. The pools chosen for egg laying and in which the larvae have been found are almost always in full sunlight (twenty-two out of twenty-seven examined, were in full sunlight; four had partial shade, with the larvae in the unshaded portions). Aedes (Mucidus)alternans Westwood (which extends from Timor to New Caledonia)breeds in both

* This use of the term "land crab "is t o be discouraged-it is completely uninformative, for one cannot from the context distinguish whether the crab in question is a true land crab or a species of Sevarmu which is well on the way to becoming a land crab. 6*

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salty tidal pools and in fresh water ; this is a large mosquito exceeding 1 cm long. Aedes scutellaris (Walker) breeds in rot holes of avicennia trees from South China to Australia. Culex sitiens Wiedemann, a species widespread in the Indo-Pacific, breeds in tidal pools both in the open and under the deep shade of the landward mangrove fringe. Anopheles farauti Laveran, distributed from New Guinea to Australia, breeds in shaded pools within mangrove forests ( ? a t what level), both among roots and in more open water, as well as in sunny pools with vegetation around them. Anopheles amictus Edwards subsp. hilli Woodhill and Lee occurs in open, sunny, brackish pools on the mud flats in Australia and New Guinea. Studies on biting midges of the family Ceratopogonidae have been made by Lee (1949), Lee and Reye (1953, 1954, 1962), Reye and Lee (1962) and O’Gower (1960). They have shown that the following species occur in the mangals. Culicoides immaculatus L. & R. subimmaculatzcs L. & R. ornatus Taylor molestus (Skuse) marmoratus (Skuse) mackayensis L. & R. magnesianus L. & It. Lasiohelea townscilleptsis (Taylor)

Host Man. Man, flying fox, etc. Man, birds, flying fox, horse, etc. Man, birds, flying fox, etc. Man, horse, etc. Birds. Birds. Man, etc.

All these may be found in tropical Queensland and several are more widespread. Some hosts are listed but several seem to be indiscriminate feeders. Breeding habits are known for some: C. subimmaculatusbreeds in the low lying estuarinezone covered by spring tides, in the area between mangroves and dry land, often delimited by the presence of Salicornia. C. marmoratus has been found breeding in the same type of area. (Lee and Reye, 1962.) They may not be limited t o such areas. Some of the others may breed in rot holes or in the accumulations of humus in clefts on the trees. Lee and Reye (1962) show that there is a definite correlation of abundance of species of Culicoides with the neap tide period a t various localities as far apart as Darwin and Careel Bay (near Sydney, N.S.W.). Other species showed no such correlation. This rhythm suggested that the larvae may be found in the belt of shore around mean neap levels, and, in fact, larvae of C. subimmaculatus have been found a t this level in sandy mud and apparently associated with Mictyris longicarpus Latr., the soldier crab. Whether the association is fortuitous or obligatory is unknown.

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Similar work is now being undertaken by D. S. Kettle and his students in East Africa. The jetsam which marks high water mark, if wet and rotting, is the breeding place of several species of dolichopodid, ephydrid and other families of small flies. 1. SynchronouslyJEashingjireJlies One other and most spectacular insect phenomenon deserves mention. This is the synchronous flashing of fireflies. Buck in 1938 reviewed what was known, up to that time, about this phenomenon, and Buck and Buck (1966, 1968) reported that it is widespread in the eastern sector of the Indo-west-Pacific, from Thailand south to New Guinea and New Britain. I was introduced to this most fascinating display by Dr Ivan Polunin, University of Singapore, who with J.-M. Bassot, Institut Ochanographique,Paris, has been studying the behaviour of the fireflies for some years and continues with the investigation a t Benut in south Johore and some 70 km north-west of Singapore (Bassot and Polunin, 1968). The coastal road runs within the landward fringe of the mangal, here utilized as nypa plantations. Tidal ditches border the road. These ditches are lined by young trees of Avicennia oficinalis, and of Sonneratia caseolaris with an undergrowth of Acanthus ilicifolius and coarse grasses. As dusk gave way t o darkness one became aware that certain of tha trees were inhabited by fireflies. Exactly a t what time flashing began was not noticed but it was clear that by the time it was fully dark many were flashing in synchrony. Buck and Buck (1966, 1968) also mention the difficulty of establishing when the synchrony becomes absolute. This synchronousflashing continued without interruption and almost without variance until dawn ended the display. At least i t was continuous from dusk till midnight and clearly seen a t intervals during a night of fitful sleep, and the insects could still be seen to flash synchronously when it was light enough to see the insect as well as the flash. The display is a t its most brilliant early in the evening and as the night progresses the proportion of fireflies in synchrony usually declines, due, a t least in part, to the elimination of copulating pairs. Not all trees were chosen: only certain trees of Sonneratia caseolaris. There was some spill-over on to adjacent trees of Avicennia oficinalis and Acanthus ilicifolius but rarely on to the nypa palms. A similar restriction to a tree of A . marina was noted at the Bako National Park in Sarawak and t o trees of S. caseolaris on the banks of the river a t Suratthanion the east coast of peninsular Thailand. Buck records that

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trees of 8. caseolaris were chosen for the display on the banks of the rivers below Bangkok and below Kuching. This tree has an open willow-like foliage of broad leaves, always quivering in the slightest breeze. Fireflies displaying on such leaves will be clearly visible to others flying past. The firefly trees could be distinguished both by night and by day from distances of 100 m or so, again evidence of a clear view. Tall trees of some 15-20 m contained some fireflies. It was noticed a t Lob0 Kara in the Sarawak river delta that synchronous displays were taking place in the canopy of trees of Rhizophoraapiculata, and again oiily of selected trees. The most spectacular displays seen were in small trees some 3-4 m high. Flashes were emitted as the A

B

FIG.46. Photometer records of successive flashes of fireflies. A. Three successive flashes of a male Pteroptya sp., the period is 0.52 sec; note that each flash is double. H. Three successive flashes of a female Pteroptyz sp. C. Fifteen successive flashes of an undet,ermined number of males in an Acan,th,usbush. (Figs. 1, 3, 6, of Buck, 1968.)

fireflies ran over either surface of a leaf and were intense enough to be visible through the leaf. According to Buck and Buck (1966, 1968) and to Polunin (personal communication) flashes are given out in two distinct synchronous rhythms. One is a rapid series of flashes a t around half-second intervals (Fig. 46); the other noticeably slower. The rapid flash comes from a firefly of 5-6 mm long, and the slower flashfrom a largerone of 8-10 mm. Later in the evening stationary dull glows become visible and these may be seen t o come from copulating pairs (Fig. 47). The synchrony was not noticed on three nights spent in the Bako National Park in Sarawak. A group of four trees, two of Avicennia marina and two of Bonneratia alba, were chosen for display but no synchrony had been established by 22.00 h. This, in fact, was one of the localities visited by Buck and he reported that synchronous flashing has been recorded here, but he saw no synchrony. At the time of my visit in Januarythere were few fireflies in the trees; this would

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suggest that a quite large number are necessary to give the initial stimulus which leads t o the establishment of synchrony. There are many unanswered questions about this synchrony. It is certain that a residual population of fireflies remains in the trees during the day. They are usually stationary, often clinging to the edges of leaves, or flattened against twigs, or petioles, and in fact quite difficult to spot. The trees which are occupied by fireflies seemed to be clear of scale insects and tailor ants-these ants also show a liking for X. caseolaris, presumably because of the scale insects which live on the

FIG.47. A pair of copulating Pteroptyx spp.

twigs. This might be a factor involved in the relative scarcity of trees occupied by fireflies. Do the fireflies eat the scale insects and so keep the trees clear, or do they choose trees not attacked by scale insects? Do they feed as adults?How long do adults live? How is synchrony established? No answer is available. A newcomer quickly acquires the rhythm of the tree (Fig. 48). All trees are not quite in time with one another. At Benut and again a t Lobo Kara I had three trees in view: nos. 1 and 2 seemed to be in synchrony, so did nos. 2 and 3. But when I obscured no. 2 from view, it was clear that nos. 1 and 3 were almost but not quite in synchrony. Does distance apart of trees affect the rhythm? It would appear so. Is there an optimum density of dispersion of fireflies in a tree before synchrony is established? I presume so-my observations a t the Bako and elsewhere would suggest that there must be such an optimum, but Poluniii points out (in Eitt.) that a small number may flash synchronously under laboratory conditions.

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Polunin (personal communication) suggests that frequency of flashing is temperature controlled. He mentions that considerable temperature variations have been shown t o occur a t night, simultaneously at different distances from the ground in Malayan lowland forests. What is the identity of the fireflies and their life cycle? I n Thailand, near Singapore and in Borneo, the synchronous flashes are produced

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by males of Pteroptyx malaccae Gorham (Coleoptera Lampyridae). While both males and females are responsible for a rapid twinkling in flight the females do not flash in synchrony on the leaves. Males of P. valida E. oliv. emit long bright flashesin the trees but do not achieve synchrony. Females glow when settled on the leaves. (Buck, 1968.) Buck and Buck (19GG) record that in general in the West Indies fireflies lay their eggs in the soil beneath the trees in which they congregate. They suggest that this might not be so in the case of the synchronous flashers as a result of tidal scour. All the trees I have seen to be occupied have been a t such a level in the mangal that scour would be minimal. The mud in such localities is populated in the surface few millimetres by harpacticoid copepods, ceratopogonid midge larvae and tiny nematodes. All these would provide food for carnivorous larvae such as those of fireflies. Emergent vegetation, whether grass or pneumatophores or any other projection, would afford sites for pupation and one might expect that the pupae could withstand occasional submersion. The elucidation of problems of synchronously flashing fireflies and their life cycles would make a worthwhile study for a student resident in any area where they occur.

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V. DISTRIBUTION OF MARINEANIMALSWITHIN

165

MANGAL The fauna of marine animals living within the mangal has two components: an infauna of burrowing forms; an epifauna of errant or wandering forms. The burrowing forms are mainly crustacean but there are also a few bivalves and one genus of fish. The errant forms include several gastropod molluscs and some crabs. Gerlach (1958) has shown that nematodes and other small worms are an important constituent of the burrowing faunain Brazil but little is known about the Indo-west-Pacific forms. Only a few highly specialized polychaetes occur in the strongly deoxygenated soils of the mangal ; these include several species of Dendronereis and of Marphysa, M . mossambica Day being the commonest and most widespread (Day, in litt.). While most species of crab live in the shade of the mangrove trees and bushes a few have become adapted to living in the bare areas which develop within and at the upper edges of the mangal. The animals of marine origin show, as Berry (1964) has pointed out, two distinct modes of zonation in the mangal. I n Malaya there is, particularly in the trees and bushes of the seaward fringes, a zonation affecting those molluscs, mainly snails, which live amongst the leaves and on the twigs. Secondly there is a zonation of the faunathat is tied to the surface of the mud, and to burrowing within it. THE

A. Vertical zonation affecting tree dwelling animals This mode of zonation is, due to paucity of fauna, not shown over most of the Indo-west-Pacific zoogeographic region. Only in Malaya and adjacent areas is it clearly defined. In eastern Africa and in Queensland only Littorina (Melarapha) scabra (L.) is found on the leaves of the mangrove trees, and it tends t o be common only in the seaward fringes. I n South East Asia several species occur among the leaves, on the twigs and on the trunks. When disturbed all will drop and suspend themselves on a cord of thick mucus. Littorina melanostoma (Gray) climbs to levels well above that reached by even the highest tides. L. scabra climbs almost but not quite so high. L. carinifera (Menke) and L. undulata (Gray) occur a t a slightly lower level, at a little below ordinary high water mark. L. undulata may be found, too, on debris lying on the surface of the mud. The bivalve Enigmonia rosea (Gray) is the only other animal normally to be found on the leaves. It occurs at low levels only on the most seaward trees. This group of climbing snails all penetrate the mangal, clinging to the leaves, etc., of the trees forming the lower storeys and reaching

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almost as far as the landward fringe. Certainly they occur as far as those parts of the mangal reached by all spring tides. But at these upper levels they tend to be scarce, and seem to be restricted to lower levels of the trees.

FIG.49. Cwithidea decollata a t rest during low tide on a trunk of Avicennia marina, in the avirennia parkland, Inhaca, April 1967.

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Species of Cerithidea, a t low tide periods, cling to the more shady side of the tsees (Fig. 49) and spread out over the soil while the tide is in. They are commonest in the avicennia and bruguiera forests of the landward fringe. Nerita birmanica Phil. clings to the lowermost levels of the trunks and to the prop roots of Rhizophora. Thais ltissoti (Petit) also occurs a t this level, being especially common where the barnacle Chthainalzcswithersii Pilsbry is found on the trunks, twigs and pneumatophores. Occasionally Murex adustus also climbs off the surface of the mud on t o the bases of the trunks and on t o the prop roots, etc. Barnacles, chiefly forms or varieties of the tropicopolitan Balanus amphitrite Darwin, of which the forma cirratus Darwin is the common form a t Singapore and in Malaya and f. denticulata the common form in eastern Africa, are abundant on the prop roots of the rhizophora trees. I n South East Asia Chthamalus withersii is also common and lives a t a slightly higher level on the roots and trunks. Oysters, one or other of the spiny forms of Crassostraea cucullata (Q. and G.), are also abundant and compete for space with the barnacles. The tiny crab Nannosesarma minuta (de Man) runs about among the barnacles and oysters, as characteristic a form here as it is a t a similar level on coral islands off shore. The hermit crab Clibanarius longitarsus also climbs into the trees, reaching heights well above that reached by normal high tides.

B. “Horizontal ” zonation through the mangal The animals discussed in this section are those which live on or in the substratumand rarely if ever climb the trees. I n describing the zonation of these animals it is convenient to refer them to the zones of trees and plants described above (see Figs. 17-19, between pp. 104-105). 1. The landward fringe of the mangal

This is the equivalent of the supralittoral fringe of the Stephensons’ scheme for rocky shores. On tropical and subtropical non-rocky shores from the level of high water of ordinary spring tides upwards occur a number of crabs and hermit crabs. These animals are mostly secretive in habit and are not easily located, nor are their habits easy to study. These crabs rarely occur in the mangal except in drier areas or on islands where the pes-caprae association may abut on the mangal. To this group belong such well-known forms as the robber hermit crab Birgus latro L. which is only rarely and exceptionally encountered in the mangal. Related forms of the genus Goenobita which carry shells

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around, sometimes those of land snails, such as species of Achatina, sometimes cast up sea shells, are aIsoterrestrial but seem t o be restricted to the zone of the maritime scrub or of the barringtonia asiatica association. Species of Qeograpsus, a genus of land crabs, are of similar habit. On sandy shores just above extreme high water mark or between it and that of ordinary spring tides the burrows may be found of Cardisoma carnifex (Herbst). Very little is known about the habits of this crab and nothing of its life history. They are large crabs, often more than 90 mm across the carapace (Fig. 50), and females are bigger than males.

FIG. 50.

Cardisoma

carnifex, note the inflated branchiostegite, a characteristic of terrestrial crabs. (ca. nat. size.)

Juveniles I have never encountered and have seen no reference to their having been found. The burrows are large, almost circular in crosssection and with an untidy heap of excavated material around the entrance or to one side of it. They are deep, running in a loose spiral down to the level of the water table, or sloping gently down to the same level. During the day the burrow may be open or closed. Silas and Sankarankutty (1960) have described ‘(castle ” building by this species in the Andaman Islands. They suggest that the “castle ” building may be a seasonal activity, the castles ” being built when there is danger that the mouth of the burrow may be flooded. I have never seen such behaviour at Inhaca where the crabs are common. The feeding habits of these crabs are unknown-various authors have described them as being scavengers. All that is certain about ((

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their habits is that they tend to be nocturnal, although they may occasionally be seen during the day if it is cloudy and just after a high spring tide. Cardisonza carnqex occurs all round the Indo-west-Pacific in suitable areas. The other Indo-Pacific species of the genus C. hirtipes Dana occurs at a higher level and tends to be associated with freshwater pools (Silas and Sankarankutty, 1960). When the soil is heavy and clayey rather than sandy, and if it is water-logged, the mud lobster Thalassina anomala (Herbst) (Fig. 51)

FIG.51. Thalassina anornula,side view and front view of a female. I n the front view, note the scoop-like attitude of the second walking legs which are used to push up a mass of semi-liquid mud to build the characteristic mounds. (eu. nat. size.)

extends upwards above extreme high water mark. Its burrows, at this level, are very deep and the heaps of discarded material are often very large. This animal occurs on all suitable shores in southern and southeastern Asia from Bombay in the west and extends into Australia t o reach Moreton Bay in south Queensland. The burrows of the mud lobster are used as refuges by several of the crabs of the genus Sesarma (Fig. 53), and one is frequently told that the heaps of mud are due to

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MACNAE

FIG.52. Heaps of mud thrown up by Thalassina anomala in a ceriops zone. (Drawn from a colour transparency taken between Mossman and Port Douglas, March 1962.) (From Macnae, 1966.)

FIG.53. Sesarma srnithii. The spines on the finger of the cheliped are diagnostic of this species. I n many species of Sesarma a row of nodules occurs along this ridge of the dactyl, and by scraping these ridges together sound is produced. The pattern of nodules and hairs on the pterygostomial region is diagnostic of the genus and is used in reoxygenating water pumped up out from the gill cavity t o which the water returns. (ca. nat. size.)

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these animals, for the Thalassina are active in their excavation only a t night and on days when it is dark and rainy and so tend to escape notice. The level to which crabs of the genus Sesarma ascend on the beach seems to depend on the local climate. I n the ever-wet of Malaya and adjacent territories S. fasciata Lanchester and S. plicata (Latr.)occur on the artificial banks of prawn and fish ponds and of roadside ditches where they reach well above high water mark. These two species often extend on to the swards of halophytic grasses alongside small streams a t high levels but yet occasionally intertidal. S. ortmanni Crosnier and X. eulimene de Man appear to occupy a similar niche in the western Indian Ocean. No exact equivalent was seen in Australia. I n Pondoland, Natal, Mopambique and northwards along the coasts of East Africa as well as in Madagascar S. ortmanni and S. eulimene occur in the belt of Juncus kraussii and J . maritimus which delimits the upper intertidal region. S. eulimene extends farther upstream into the fresh water, while S. ortmanni is more strictly marine. There is a very small overlap in occurrence. These two crabs are frequently very abundant (up t o eight have been counted for each in a square metre a t Inhaca)and until recently have not been distinguished from one another. At a level only fractionally lower the larger species of Sesarma come to dominate the fauna of the mangal. None of the taxonomic accounts gives even the slightest hint as t o the level a t which occur any of the large number of species of Sesarma which have been recorded from the Indo-west-Pacific. I n Singapore, Malaya and adjacent areas seven species of large sesarmas occur : these are S. indica A.M.-Edw., S. mederi H.M.-Edw. (= S. taeniolatu auct.), S. palawanensis Rathbun, S. singaporensis Tweedie, X. tetragona Fabr., 8. versicolor Tweedie and the recently described S. chentongensis SerAne & Soh. All of these occur in the landward fringes. The slightly smaller species 8. moeschii de Man, S. crassimana de Man and S. sediliensis Tweedie together with Sarmatium inerme (de Man) are common in nypa plantations and in ditches in the landward fringe of the mangal (Tweedie, 1940). I n eastern Africa and in Queensland Sesarma meinerti de Man and S. smithii H.M.-Edw. (Fig. 53) live in this zone-a much less complex picture than that found in Malaysia. I n areas where Lumnitxera racemosa and other bushes of the landward mangrove fringe give some shelter the burrows of these two species may be very close togetherless than 15 em apart-i.e. as close as would seem feasible. At Morrumbene (lat. 22's.)in Mspambique such burrows occur in a strip only

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a metre or so wide. This is an area of very high tides (33 m). The burrows extend seawards clustered round the bases of the trees and bushes almost to the lowermost levels of the bruguiera forests. The burrows of Sesarma meinerti and of 8. smithii may be hooded and those of the latter turreted. I n Malaysia many of the sesarmas make turreted burrows pressed up against the boles of the trees, others produce hooded burrows but which species was responsible for any of these could not be determined. Sesarmine burrows are circular in cross-section, surrounded by pellets of sand or of mud and the size and form of these pellets is probably

FIG.54. Two fiddler crabs. A, Ura clzcssumieri, with a narrow front; B, Uca lactea, with a broad front. (ca. nat. size.)

characteristicof the species. All descend to the water table either in a loose spiral or in a gentle slope (Verwey, 1930, and personal observations). At the lower level of a zone of Juncus in areas where a lawn of Xesuvium portulacastrum or of saltworts spreads beneath the trees of a n ‘‘avicennia parkland ” and among the pneumatophores of these trees, both in the shade and in open sunny areas, are large populations of Uca lactea (de Haan)(Fig. 53B). I n eastern Africa the form annulipes (H.M.-Edw.) is more common, in Australia the form lactea; in areas between, intermediates occur. Some of these show a characteristic annulipes claw and lactea male pleopod, and others the reverse, while some will appear to be pure annulipes and others pure lactea. It is for these reasons that Miss Jocelyn Crane has united these two species. Uca lactea f. annulipes is almost always associated with Avicennia, particularly when it is growing in sand, and so U . lactea may be found both in the landward and in the seaward avicennia fringes or even a t slightly lower levels if the ground is sandy enough and is not occupied by Dotilla or Mictyris.

FIG. 5 5 . Representative mangrove molluscs. A, Ellobiurn auris-midae (8 cm) ; B, Gassidula anqulifera (24 em), an Australian species; C, Ellobiurn auris-judae(54 em) ; D, Ophicardelus sulcatus (14 em), an Australian species ; E, Pythia scarabaeus (2; cm),; I?, Terebralia palustris ( 6 cm); FF, T . sulcata ( 6 cm); G , Telescopium telescopzum (10 em), T . mauritsi is more inflated towards the mouth of the shell and in the last whorl ; H, Batissa triquetra (9 cm), an Australian bivalve with a purple lining; J, Geloina eoaxans (12 em) with a whitish lining; K, Cerithidea decollata (2; cm), the common African species of this widespread genus.

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The "avicennia parklands " may have a soil surface of coarse, medium or fine sand, and bare areas occur between the clumps and clones of Xesuviumportulacastrum and species of Arthrocnemum. Where the sand is coarse t o medium, U . lactea is abundant. On Australian shores, when the sand is fine to very fine, U . bellator (White) occurs. The sandy floors of drainage channels between the trees are often colonized by Macrophthalmus depressus (Ruppell) and at low tide these crabs may be found buried in the moist sand. They seem t o migrate upward during spring tides and downwards at neaps. There is no equivalent of these in the ever-wet of South East Asia where U . lactea (in both forms) seem to be limited in distribution to slightly sandy areas in clearings, or to more open beaches of sandy mud. I n eastern Africa from the Bay of Lourengo Marques northwards wherever bare areas have developed between the mangroves and high water mark, portions or the whole of these will be colonized by Uca inversa (Hoffmann). These crabs are most abundant in areas of fine to medium sand. They come to the surface t o forage and display only on the few days of spring tides, just after the tide has ebbed. At neap tide periods the burrows are blocked from within. I n Australia such areas are colonized by Uca bellator but this species does not penetrate so far towards the centre of the bare, sun-baked, salty flats. I n the ever-wet of South East Asia and north central Queensland, where the landward fringe consists either of rain forest or scrub forest, the crabs and crustaceansfrom lower levels will come higher up. There is less necessity for specializations to withstand desiccation. Snails will be abundant in the litter. These are representatives of families which have freshwater and brackish water species. The prosobranch families Synceridae (= Assimineidae) and Neritidae and the pulmonate families Ellobiidae and Amphibolidae provide several species associated with this landward fringe and some of them penetrate downwards into the bruguiera forest. The following are characteristicin Malaya and adjoining areas : Cassidula mustellina (Derh.) Nerita birmanica Phil. cLurisfelis (Brug.) Pythia scarabaeus (L.) (Fig. 55E) Ellobiur~auris-judae (L.) (Fig. 55C) Cerithidea obtusa (Lam.) aztris-midae (L.) (Fig. 55A) alata (Phil.) 2 . The bruguiera forests and ceriops thickets Both the bruguiera forests and their variant, the thickets of Ceriops tagal, are densely shaded and normally the soil is quite firm. There is only a slight tendency for litter to accumulate, but fallen branches and

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fallen trees become converted t o rotting logs and thus provide shelter for several kinds of animals. The root systems with their ascending and descending knees, and the buttresses which support the trunks also provide shelter. This portion of the maiigal supports a greater variety of ground dwelling animals than any other portion. Crabs run everywhere. Most of them are grapsids, species of Sarmatium, of Helice, of Ilyograpsus, smaller species of Sesarma mainly of the subgenus Chiromaiztes: e.g. S. eumolpe de Man, S. dussumieri H M - E d w . , S. onychophora de Man, and 8. indiarum Tweedie in Malaya ; and S. guttatum in eastern Africa. Species of the subgenus Parasesarma such as S. melissa de Man are also present in western Malaya. Two species of Metopograpsus, namely M . frontalis Miers (= M . gracilipes de Man) and M . thukuhar, are conspicuous. These two crabs seem not to overlap in distribution : the former is south-east Asian and Australian, while the latter is found in eastern Africa, Madagascar and several islands. M . messor Forsk. has been reported from mangrove areas. This is the result of a confusionof this species with M . thukuhar. M . messor occurs on stony shores as, for example, among coral debris (Tweedie, 1049b ; Forest and Guinot, 1961 ; and personal observation). I n moister places with a superficial layer of soft mud species of Cleistostomcc, Tylodiplax, Ilyoplax and of other small ocypodid crabs become common. Most of the species of these genera are rather local, and only a very small minority of species are widespread. Of all the crabs found in the bruguiera forests only Sarmntium crassum Dana and Helice leachii Hess are widespread in the Indo-westPacific. Juveniles of all species add t o the confusion of identification. The mud lobster Thalassina anomnla is abundant in forests of Bruguiera gymnorhiza and of B. sexangula but not so conspicuous in forests of B. cylindrica or of B. parv-flora. It is abundant,too, in the thickets of Ceriops tagal in the vicinity of Darwin. By its activities this animal may modify the substratum considerably. At Darwin the soil level iii ceriops thickets was as much as 50 cm above the level of adjacent bare areas. Throughout Malaysia, Indonesia and the wetter parts of Australasia the heap of soil a t the entrance of the burrow may reach a height above the level of the water a t medium high tides and become colonized by the fern Acrostichum aureum, or more commonly from Malaya t o Australia by A . speciosum, and these ferns will shelter the animals characteristic of the landward fringe. Large sesarmas which burrow a t the bases of the trees also burrow into the mounds cast up by Thalassina,or even use as refuges the side

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passages emerging on the mounds. Some of these crabs will be the same species that occur in the nypa swamps, but they tend to be reticent, indicating their presence by the form of the burrow entrance and of the pseudofaecal pellets lying around. They are rarely seen a t low tide during daylight hours. Macrophthalmusdepressus and M . paci$cus Dana may be abundant in the sandy bottoms of the shallower creeks at this level. Water lies around on the surface in shallow pools with little low mounds of mud emerging. These pools are occupied by several small crabs of which the males often sit around on the tiny eminences displaying and feeding. The females tend to remain closer to the edge of the water in the little pools. The genus characteristic of this sort of situation is Ilyoplax. I n Malaya I . dekmani (de Man), I. lingulata Rathbun, I. obliqua Tweedie, and I . punctata Tweedie are all common but tend to be local. Tweedie (1950a) has suggested that several of these species of Ilyoplax are restricted in their distribution, a result of a possibly abbreviated life history taking place in the vicinity of the pools where they have been found. Tweedie found all sizes of crabs in such pools. My own collections and observations, limited as they are, lead me t o agree with this opinion. Paracleistostoma depressum de Man, P. microcheirum Tweedie and P. longimanum Tweedie, Tylodiplax tetratylophorus de Man and Utica borneensis de Man are other small crabs which may be found in this sort of environment. I n Sarawak I found blue-clawed Ilyoplax spinimera Tweedie and another Ilyoplax sp. with pink-red claws living almost but not quite sympatrically, the former in wetter places, the latter in drier mounds. Ilyograpsus paludicola (Rathbun) is a little carnivorous grapsid, present but never very common in the bruguiera and drier rhizophora forests throughout the Indo-west-Pacific. Clistocoeloma merguiense de Man may also occur at this level. Species of Uca are common in clearings and a t the edges of the bruguiera forests and ceriops thickets. U . bellator, U . gaimardi (H.M.-Edw.), U . chloro~hthalmus(H.M.-Edw.), U . manii (Rathbun), U . rosea (Tweedie) and others are characteristic. Each species tends to be restricted to one geographical subdivision of the area. U . gaimardi is African, U . manii and U . rosea are Malaysian, U . chlorophthalmus is Micronesian, U . bellator is Australian. Of molluscs, the brackish water ellobiids, mentioned above, persist and are joined by more marine species of other families : e.g. a species of Haminea, Terebralia palustris L. (Fig. 55F), T. sulcata Born. (Fig.

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55FF)and Syncera brevicula (Yfr.) f. miniata which may be abundant. Where soft mud occurs Telescopium telescopium L. (Fig. 56G) and T. mauritsi Butot are common. Species of Cerithidea, mostly decollate forms, are common and these climb up and shelter in clumps on the bases of the trunks of the trees : C. decollata (L.) (Fig. 55K) is abundant on the African coast, C. alata, C. djadjariensis (K. Mart), C. cingulata (Gm.), C. obtusa, C. qundrata Sow. and C. weyersi Dautzenberg all occur in South East Asia and C. anticipata Iredale in Australia. Where several species occur there is probably some degree of zonation. It was most surprising t o find a saccoglossan nudibranchElysia sp. living in pools of reduced salinity in the forest of Bruguiera cylindrica near Kuala Selangor in Malaya during December 1966 and January 1967. Swimming in the same pools were tadpoles, presumably of Rana cancrivora. A second species of Elysia was common in pools among cultivated Ceriops tagal near Chonburi a few kilometres south of Bangkok. 3. Rhixophora forests I n mature forests of R. mucronata where the soil is well compacted one finds a fauna similar t o that of the bruguiera forests. I n mature forests of R. apiculata the fauna shows stronger affinities with that of the landward fringe. I n forests of R. mucronata or R. stylosa growing behind a seaward fringe on soil in an unconsolidated state the fauna is restricted to alpheid prawns, the snapping of which reveals their presence, and to species of the crab genus Nacrophthalmus. The bright blue crab Metopograpsus latifrons (White) runs round on the prop roots of the trees and scavenges amongst the debris collected among the mass of interweaving roots. This crab is mainly Indo-Australian but has recently (Macnae, unpublished data) been found in the mangroves of northern Mopambique. Of large snails, Telescopiuna telescopium will be the only one present for it alone can gain support on the mud.

4. The seaward fringes and channel banks These two will be considered together for they have much in common. I n many areas on the western coasts of the Malayan peninsula, both in Thailand and in Malaya, and in many places in the great estuaries of Borneo they differ only in extent. The seaward slopes tend to be more gentle and the channelward slopes are steeper but this merely condenses the fauna. The fauna will depend on many factors affecting the substratum: some of these depend on the degree of consolidation of the soil ; others

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depend on the fertility of the soil. There is, for example, always a very obvious increase in the number of individuals of crabs in the vicinity of the towns or villages established within the mangal. There are differences, too, between accrescent and eroding shores. These latter provide among the tumbled masses of mangrove peat many nooks and crannies analogous to a rocky shore and hence give cover to several species of xanthid crabs, a family characteristic of rocky shores and shores with scattered coral dkbris. a. Accrescent shores As has already been mentioned,many shores occupied by mangroves are continually having material deposited on them, and this material becomes colonized by species of Avicenniaor under special circumstances by species of Sonneratia. Such shores have a characteristicfauna. Most

C

FIG.56. Metaplax crenulatus. A , A female in characteristic pose (partly after a photograph by I. Polunin). The arrows indicate the direction of water flow while pumping and reoxygcnating the water ; this process is almost constant while the crab is out of water. B, Base of cheliped and pterygostome of 8. male, showing the "niusical ridge "on the pterygostome, below the orbit and the "bow "on the merus o f the cheliped. C, Dorsal view showing direction o f water flow over the back, while the crab is out of water. (ca. nat. size.)

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of the animals found here seem to depend on a burrow, or where a burrow cannot be dug, one finds forms capable of living in the soft muds. I n Malaya and adjacent regions in places where the mud, or a t least its surface layer, is semi-fluid two animals are conspicuous. These are a mud-skipper Scarteluos viridis (H. Buchanan)and a crab Nacrophthalmus latreillei (Desm.). At slightly higher levels, and among the most seaward trees where the mud has a jelly-like or custard-like consistency, these two drop out and are replaced by another mud-skipper Boleophthalnzusboddaerti (Pallas) (Fig. 68), by a mud crab Metuplax crenulatus (Gerstaecker)

FIG.5 7 . Periophthalmodon schlosseri (20 em). (Redrawn from Harms, 1931 and from a specimen caught at Pulau Ketam, blalaya.)

(Fig. 56), and fiddler crabs Uca courctuta (AM-Edw.) and U . dussumieri (H.M.-Edw.) (Fig. 54B) which are common particularly along the more sheltered channel banks. Overlapping these, two other mud-skippers become conspicuous. These are Periophthalmus chrysospilos Blkr. which makes its home in the vicinity of the most seaward or most channelward mangrove trees. It rarely goes far to seaward of the lowermost saplings. During the breeding season its aggressive behaviour to all other animals is notable. This species rarely penetrates into the mangal, and as the tide rises the fishes climb up into the trees to cling to twigs and leaves and skitter over the surface to a taller tree when a refuge becomes swamped. The n (Pallas) (Fig. 5 7 ) , other is the much Iarger P e r i o ~ h t h ~ l m o d oschlosseri in many ways a more aquatic animal. Both mud-skippers construct

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their saucer- or bowl-shaped burrows mainly a t this level and hold territory here. Only P. schlosseri extends to the inner parts of the mangal and then only a t high water. Around the bases of the small bushes of the pioneer mangroves, or around piles or posts driven into the soil, tiny crabs, such as species of Ilyoplax, Leiopecten sordidulum Kemp, Metaplax elegans de Man and others, cluster and the species of Ilyoplax may make their small burrows. Burrows of a species of Upogebia become common and may be used as refuges by these small crabsand by species of Paracleistostoma. As the ground becomes firmer under the older trees, particularly where the area has been to some extent cleared, or elsewhere where sunny patches occur on the forest floor, another series of crabs take over. I n western Malaya and peninsular Thailand there is Uca rosea (Tweedie), in Borneo U . rhizophorae Tweedie, and with them the smaller blue-speckled, orange-clawed U . triangularis (A.M.-Edw.)-its var. variabilis de Man is present in Borneo, the typical form in western Malaya. The soil a t this level is riddled with burrows of an Upogebia and these burrows are the refLiges of a host of tiny crabs. Juvenile king crabs, Tachypleus gigas (Muller) and Carcinoscopius rotundicauda (Latr.)may also be found partially buried in the mud. Adults of both may be seen in pairs, the smaller male riding on the back of the larger female as the tide leaves, while they swim downwards with the retreating water. Water snakes, most commonly Cerberus rhynchops, seek for crabs in their burrows while the tide is in and curl up in the shade of the trees during low tide periods. Snails, chiefly Xyncera brevicula and a species of Haminea that produces a purple dye, are often common on the surface of the mud under the shade of the trees. Telescopium telescopium and T . mauritsi crawl around in the wetter runnels. Cassidula auris-felis and C . mustelkina are also common on the surface of the mud as on the bases of the trunks of the trees. C. angulifera (Fig. 54B) is common in Australia. I n some localities where the mass of nutritive rootlets of Avicenizia or of Sonneratia give a degree of stability to the shore, large populations of bivalves of the genera Glaucomya and Laternula live in coccoons made by themselves. They may, in fact, be so common as to give the surface a peculiar pock-marked appearance which results from the activities of their siphons. Running around among the pneumatophores in Malaya and in Sarawak are two small crabs : Nannosesarma minuta and Clistocoeloma merguiense.

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The pattern in other parts of the Indo-west-Pacific varies a little from this. Only Pwiophthalmodon schlosseri and members of the Periophthalmus kalolo group of species extend into Queensland where Periophthalmus kalolo descends t o lower levels than in Malaya, for i t reaches the seaward fringes. Mud-skippers of the latter group alone reach eastern Africa. I n Australia Macrophthalmus latreillei, Uca coarctata and Uca dussumieri are accompanied by two others, Uca sp. around Darwin and Uca (pink claw) in Queensland. I n eastern Africa Uca urvillei (H.M.-Edw.) and U . gainzardi are common to abundant. U . dussumieri reaches Madagascar but has not yet been recorded from the African continent. Phascolosoma lurco (Selenka and de Man) is a sipunculid often very abundantin these muds. b. Eroding shores When as a result of vagaries of tidal currents a mangal is being eroded, a “salting cliff” or ‘‘mangrove scarp ”will develop, and in the crevices so provided several species of xanthid crab may be found. I n Malaya these include Epixanthus dentatus White, Eurycarcinus integrif r o m de Man, Beteropanope eucratoides Stimps., H . glabra Stimps., Myomenippe hardwickii Gray and Ozius guttatus H.M.-Edw. It is of interest that in southern Malaya, E . integrifrons should be confined to these erosion cliffs while E. natalensis (Krauss) on the coast of eastern Africa runs around the mangal forest floor from the seaward fringes into the rhizophora and bruguiera forests (Johnson,personal communication, and my own observations).

VI. SPECIALIZATIONS SHOWNBY THE FAUNA A. Birds, mammals, reptiles and amphibians The birds and mammals associated with mangals show no specializations to this environment. The nesting groups of birds and the roosting birds and flying foxes are using the mangal purely as sanctuarieswhere there is little likelihood of disturbance. Many of the birds use the creeks of the mangal in the same way as other individuals of the same species use freshwater streams in open country inland and far from the coast. Most of the reptiles display the characteristic flattenedtails shown by many other aquatic reptiles and some have salt-secreting glands associated with the lacrymal glands. Gordon et al. (1961) and Gordon and Tucker (1965) record that crab-eating frogs Rana cancrivora, both as adults and as tadpoles, are euryhaline. Under experimental conditions this lndo-Malaysian frog

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can as an adult live in salinities up to 28%, and as a tadpole in salinities up t o 39%,. Over most of the area of distribution such salinities will rarely be reached in any mangal, disturbed or undisturbed. But towards the limits of its distribution R. cancrivora lives in areas with very marked dry seasons, and here much of the mangal has been cleared and salt production carried out on the higher levels of the intertidal flats. This frog occurs both as an adult and as a tadpole in the vicinity of these salt pans. The experimental animals which Gordon et al. used came from the vicinity of Bangkok where in December-January high salinities may be encountered. Gordon and Tucker (1965) state that the tadpoles are good osmoregulators, using mechanisms similar to those employed by euryhaline teleost fishes. They suggest that the tadpoles probably drink the hyperosmotic medium and excrete the salts by some extrarenal pathway. Adults (Gordon et al., 1961) show a strong convergence to elasmobranchfishes, retaining urea within the body fluids. The change from one mechanism to the other has not been investigated. It must take place a t metamorphosis. I n Malaya, I was told by Lord Medway that metamorphosis is induced by a heavy dilution of the water in which the tadpoles are living. The development of the tadpole can apparently proceed in brackish water but is arrested just before metamorphosis ; a t this stage the tadpole enters a state analogous to the insect diapause, waiting for the flood of fresh water which will give it the stimulus and the medium of low salinity in which metamorphosis can be achieved. I n the ever-wet of Malaya this may be a t any season but in regions with wet and dry seasons metamorphosis will follow the first flood of the wet season. B. Insects The insects associated with the canopy appear to be typical terrestrial insects. The weaver ants or tailor ants Oecophylla deserve some attention (Fig. 58). These ants all look much alike and although several species have been described many authorities would recognize only one, Oe. smaragdina Fabr. Vanderplank (1960) and Way (1954a,b)have studied these ants in relation to crops which are grown close to the sea. They have shown that ants have various sizes of workers, soldiers and several queens associated with each colony. Each colony comprises several nests and usually all the nests in one tree will belong to one colony. Their food is derived from two sources: they lap up the honeydew produced by the coccids on the trees they inhabit, and, in addition to this source of fuel, they require protein which they obtain by preying

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on the coccids and other insects which may infest the trees. Vanderplank and Way both suggest that this activity of the antsoutweighs any damage done by the bugs from which they obtain the honeydew. I n orchards and in the maritime scrub these tailor ants are liable to be overcome by more pugnacious ants of the genera Pheidole,

FIG.58. Oecophylla smaragdina nest on a bush of Ceriops tagal a t Inhaca, July 1964.

Anoplolepis and occasionally Crematogaster, but these ants do not occur in the mangal and so the tailor ants would appear t o be more secure from their enemies here. I n Malaya where these pugnacious ants appear to be less prominent Oecophylla may reach high altitudes inland in the rain forest, and is often a pest in urban and other gardens. Within the mangal they tend to be most commonly found on bushes or trees of Ceriops, Bruguiera, Sonneratia caseolaris and Xylocarpus than on other kinds of tree. O n A.M.B.-6

7

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these trees they are associated with coccids and other bugs. Way (1954b) recorded that Oecophylla transplants and cares for some of these bugs on clove trees and they may well do the same on mangroves. The large numbers, always present on the leaves which are woven together to form the nest, are suggestive of this. The insects with larvae developing in the surface layers of the mud do not seem to have been studied in relation to any specializations they may show. Closely related species occur in mangrove areas and alongside freshwater courses. The same species has been recorded from both saline and fresh water. Do these differ from one another or not? One finds two almost contradictory sets of observations. The first refers to mosquito larvae swimming in saline waters. These have the anal papillae reduced in comparison with freshwater forms (see Chapter 3 of Clements, 1963). On the other hand, it has been shown that larvae of Drosophila cultured in a saline medium tend to become modified by the enlargement of two papillae at the hind end of the body. Those which can develop these survive, and their offspring also show the tendency to possess these enlarged papillae which appear to be concerned with salt regulation (Waddington, 1959,1960). Are such structures found in soildwelling fly larvae associated with the mangal? C. Marine animals When one considers the marine element in the fauna of the mangal one finds, or expects that one will find, that the animals show some degree of specialization. All animals living between tide-marks are adapted to their mode of life, whether they live on rocky, sandy or muddy shores. Such specializations tend to lie in two directions : they are related to the ability to live in air as well as in water, i.e. to an ability to resist desiccation, and also to the ability to adjust to variations in salinity. I n the ever-wet the specializations will relate primarily to living in diluted sea water. I n regions with markedly different wet and dry seasons they will relate, a t one season to diluted sea water and at the other to hypersaline conditions of soil water and to a lower humidity of the air. Many of the solutions to problems of a varying environment are to be found in patterns of behaviour, others in modifications in structure and function of organs, and examples of both may be found in one species. Many of the behavioural specializations are centred on activity concerned with burrowing and the actions and display associated with

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the burrows. Rhythmic activity centred on the progression of the tides is aIso important and much of this is as yet ill understood. Rhythms of this sort have been much studied in the laboratory (see the work of Fingerman, Vernberg, F. A. Brown Jr. and others), but little of it has been applied in the field and no work has been done on these aspects in relation to Indo-west-Pacific forms. 1. Mud-skippers

Mud-skippers are gobioid fishes highly characteristic of the mangal and/or its immediate vicinity. They comprise Boleophthalmusboddaerti (Fig. 66), Xcartelaos viridis (Fig. 76), Periophthalmodon schlosseri (Fig. 63) and species of Periophthalmus. Harms (1929) described ecological differences between species of Periophthalmus, and Eggert (1929a, 1935) sought for and recognized morphological differences between these species. Periophthalmus chrysospilos (Figs. 59 and 60) and other species with fused pelvic fins are shown by these authors to be characteristic of the seaward fringes of the mangal. A second series of often sympatric species with partially fused pelvic fins are characteristic of higher levels. Members of both groups are difficult to distinguish from one another, and a revision which takes into account not only morphological features but also ecological preferences and behavioural patterns is necessary. The group with fused pelvics is relatively uniform and may well be a polytypic species with quite well-defined varieties. The other group is much more puzzling. Herre (1941) states in relation to it that “this polymorphic species has been divided by Eggert into many species most of which are merely ill-defined varieties, but a few are valid ”which! He makes no mention. Whitley (1953) states that P. argentilineatw C. & V., P. vulgaris Eggert and P. koelreuteri Pallas are all to be included in one species, which he identifies as P. kalolo Lesson. This is the earliest name available, since he considers that P. koelreuteri, although earlier in fact, is probably not conspecific for it was described from West African coasts. P. kalolo has been recorded by McCulloch and Ogilby (1919) from rock-strewn shores in the New Hebrides and Polynesia. This habitat Harms and Eggert considered to be typical for P . harmsi Eggert, a species which is probably identical with P. kalolo. One suspects that these were wandering, immature and sexually inactive individuals, for none of the authors who describe finding mud-skippers on open rockstrewn shores give any indication that the fishes found there were occupying permanent ‘‘homes ”. My own observations in the Bako National Park in Sarawak confirm that specimens collected on a rocky

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promontory between two mangals were all juveniles, and so were wandering, they were certainly not "a t home ". Of the mud-skippers listed above, only the P. kalolo group reaches the African coasts. These fish are very difficult to identify accurately. The most recent descriptions (Smith, 1959) recognize two species from

FIGS.59 and 60. PeriopkthaZmus chrysospilos on a twig of Avicenlzia and on glass. Note the fused pelvic fins which assist the fish to cling to the twig and t o the glass by acting as suckers. (From colour transparencies by I. Polunin.)

East Afkican shores : P. kalolo (= P. koelreuteri) and P. sobrinus Eggert first described from Red Sea shores, and recorded by Smith from the Seychelles and as far south as the Bay of Lourengo Marques. These two are difficult to separate and are completely sympatric. But two species certainly occur on African coasts. One, presumably P. kalolo, makes a nest with twin turrets (Fig. 6 1 ) ; the other, presumably P. sobrinus, makes a nest with a single turret (Fig. 62). I n their discussions on the species found a t Inhaca island, Stebbins and Kalk (1961) and van Dyk (1960) call the fish P. sobrinus, but like myself they seem to have been unable to distinguish between the two species in the field. On eastern African shores mud-skippers occur within the mangal

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from a level close to the seaward fringe upwards almost to the level reached by high water of ordinary spring tides. At Benut and other

FIG.61. Periophthalmus ?kalolo. Twin turrets of nest burrow at Quissanga,July 1'367.

places near Singapore and in Malaya, in Borneo and in Queensland, mud-skippers of the kalolo group occur mainly in the middle and upper parts of this range, As the tide rises they skitter over the surface of the water from refuge to refuge but rarely climb trees in the fashion of P. chrysospilos, although they may perch, nightjar fashion, along a branch just a t or slightly above water level, or embrace a twig or root using the pectoral fins as "arms ". P. chrysospilos does not stray far from its "home "in the seaward avicennia and sonneratiafringes. As the tide rises the fishes climb into the trees and cling to the branches with the sucker formed by the fused pelvic fins. They climb up just in front of the advancing water and often keep the tail just under the surface. It is no doubt this habit

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FIG.82. Periophthalmus ?sobrims a t edge of the nest burrow a t Quissanga, July 19G7. This burrow is larger than either of the turrets shown in Fig. GI, but thc fish is similar in size to that which skipped away from the other burrows. The burrows shown in these two photographswere approximately 10 m apart.

which has given rise to the myth that these fishes absorb oxygen from the water through the skin of the tail. Periophthalrnodon schlosseri (Fig. 63) makes its "home " on quite firin mud within the avicennia fi-iiige and on creek or channel banks, and forages into the mangal following the advance of the tide (Fig. 64). Boleophthalrnzcs boddaerti (Fig. 66) occurs in large numbers (Fig. 65) in the soft mud amongst the lowermost trees of the seaward fringes and extends downwards on such soft, but not semi-fluid mud for some distance towards mid-tide level. If the mud in this stretch of shore is semi-fluid, then Xcartelaos viridis will become common and will replace

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FIG.63. Periophthalmodon schlosseri a t the edge of its nest pool a t Benut, South Johore, Malaya. (From a d o u r transparencyby I. Polunin.)

the other ; the white-eyed males of this species are conspicuous by their habit of rising momentarily on the tail, adopting a vcrtical position and then toppling over. From my own observations a t Inhaca and from those of Dr Ivan Poluninand Khoo (1966) a t and near Singaporeit is clear that individual

FIG.64. Periophthalmodon schlosseri waiting a t the edge of the tide for an opportunity to enter tho mangrove forest. (From a photograph by I. Polunin.)

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FIG.65. Boleophthalmus boddaerti "grazing "on the mud below the seaward fringe a t Benut (South Malaya) (size of fish 15 cm). (From a photograph by I. Polunin.)

mud-skippers behave as though each is strongly territorial, especially during the breeding season when the available and suitable terrain is occupied by more or less evenly scattered males, each usually accompanied by a single female. The territory is centred on a nest burrow, and defence is strongest when pairs have been formed. At the breeding

FIG.66. Boleophthalmus boddaerti on the mud at Benut, South Johore, Malaya. Just out of focus are a second specimen of Boleophthalmus, curled and with raised dorsal fin, and two specimens of Periophthalmus chrysospilos. (I.Polunin.)

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season non-territorial individuals seem to be wanderers and it is these which are likely to bc found in abnormal situations such as, for example. rocky shores. They are usually t o be seen skittering around the edges of pools or along the water’s edge in creeks. The most complete accounts available are for P.chrysospilos. The following description is taken from a rcport prepared for an Honours degree in Zoology a t the University of Singapore by Khoo (196G),

The male is cntering his bowl-shaped burrow, female in attendance; she will probably follow her mate (size of fish 10 em). (From a photograph by I. Polunin.)

FIG.6 7 . Periophthalmus chrysospilos.

supplemented by observations and comments on a film made by Dr Ivan Polunin of the same University and discussed between us a t several showings. The establishment of a territory begins with the building of a burrow by the male. A site is chosen on the exposed mud flat just below the seaward mangrove fringe and some distance away from other burrows of the same species (Fig. 67). Soft mud scooped up by the mouth is deposited around the edge of an area some 50 mm ( 2 in) in diameter. (My own observations on compIeted and occupied nests suggest that these are more usually 50 mm ( 2 in) in radius!) This process resulted in the formation of a slightly raised rim to the actual edge of the burrow. As the fish digs downwards it would appear to reach slightly firmer mud, for this adheres to form pellets which are projected over the slightly raised rim and so come t o be strewn more widely. Water gradually seeps into the burrow which becomes filled to the brim. 7*

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Once the burrow has been made the male sets about attracting a female by means of a very characteristic sexual display. On the approach of a female the male will raise himself slightly on his pectoral fins. The first dorsal fin, with its prolonged flexible orange rays, and the second dorsal fin will be erected. Then, prefaced by vigorous and repeated sinuous movements of the tail, and a concave arching of the body with both head and tail raised off the surface of the mud, the male will jump some three times. The first of these is the highest leap and the last is a movement in which he scarcely pushes himself up on his pectoral fins. These actions will be repeated as often as is necessary to attract the female. As soon as the female begins to approach, the male will raise himself 011 his pectorals and inflate his throat which has become orange coloured during the breeding season. Finally he will turn towards the burrow with the female following close behind. The male will enter, the female will hesitate a t the entrance. After a short time the male will reappear and start blowing bubbles. The female may then enter the burrow and pairing seems to become established. When pairing is successful a region of around 25 ern (1 f t ) from the burrow becomes, according to Khoo, the scene of a very vigorous display in defence of the area. The male jumps around in an abandoned fashion and chases away any other males while the female sits in the mouth of the burrow. Usually such a defence and display is successful in driving off rivals and retainingpossession of the female, but occasionally the active display of a male just beyond the edge of a territory would induce a female to leave her first choice (Khoo saw this happen once only). Fighting and confrontation is common between individual males while they are feeding, and also any crab coming within the area of influence of a specimen of P. chrysospilos is attacked and driven off. The description given by Khoo was based on observations made from a boat stranded on the mud, or some similar perch. These leave certain questions unanswered. My own observations a t times of rising tides and of falling tides suggest that breeding individuals both of P. chrysospilos and of P. schlosseri remain a t their burrows when these are submerged. On two occasions the flood tide was seen to overflow a pair of P. chryospilos a t the entrance t o their burrow. These fish did not swim away as did unmated individuals nearby. On three occasions on a falling tide a pair of P. schlosseri were seen reclining on the inside slope of the wall of a nest burrow. They had not been disturbed and had not just arrived there from elsewhere. What, then, does happen to paired individuals when the tide flows over them:!

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A second question to which one would like an answer is : does a male keep territory for more than one intertidal period? If so, for how many? On the coasts of eastern Africa the mud-skippers construct burrows of two distinct types. I n the large mangals between Quissanga and Ibo (lat. 12’s.) both are present. One type of burrow is wide mouthed and single, the rim raised about 2.5 or 3 cm above the general level of the soil. This burrow I presume to be constructed by P. sobrinus. The other type, which I presume t o be made by P. kalolo, possesses twin turrets, each one some 5-7 cm high. When examined the burrow is Y-shaped. Petit (1922) described burrow construction by P. koelreuteri (= P . kalolo). He mentions the twin turrets and describes their construction as follows : Lorsqu’il eut amorc6 ainsi son terrier, le PBriophtalmese mit B le creuser avec sa bouche, enlevant la terre, parcelle par parcelle comme nous l’avons vu tout B l’heurelorsqu’ilrecherchaitsa nourriture,mais se retournantpour dkposer chaeunede ces parcelles & 2 ou 3 centimetres de l’orifice. Ainsi fut commencke la premiere assise du rempart, du c8tk interne de laquelle et sur laquelle se seraient dBpos6es d’autresparcelles et d’autresassises. Stebbins and Kalk (1961) describe the turrets which are made of pellets of mud and mention the sight of individuals coming to the mouth of the burrow, there to squirt out, like tooth-paste from a tube, the mass of mud being carried within the mouth. At low tide this burrow appears to be used as the centre of the defended area. The male perches within the entrance and has been seen to emerge to make a sally a t another which approaches too closely. In making such a sally he raises and lowers his dorsal fins, flash-displaying the black, white and orange stripes which are such a marked feature of them (Petit, 1922, and personal observation). I n most cases the wanderer retreats without “showing the flag”, but he may, presumably if he is in a state of sexual readiness, challenge, and he may even drive away the owner of the burrow. While the male perches a t the mouth of one turret the female crouches behind him. How pairing becomes established is not known. An interesting distraction display may be seen. On approachingan occupied pair of turrets one individual may be seen to leave and skitter away, a female will be found resting quietly within the burrow (cf. drooping wing act of birds). The eggs are deposited by the female, with the male in attendance, on the walls of the burrow (de Freitas, unpublished observations). The story of the completion of hatching and early development has not been worked out in the field. Kimura (1958) has followed the sequence in the laboratory and has shown that a typical gobioid larva emerges.

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Older nests containing larvae have been described by Harms (1929, 1935) and Eggert (1935). These older nests are saucer-like with raised rims so they must have been those of P. chrysospilos or P. schlosseri. The nests of the large Periophthalnzodonschlosseri were described by Harms (1929) as saucer-like or bowl-shaped little ponds up to 1 m across. They are also described and illustrated by Verwey (1830). I have come across such bowls (nests) (Fig. 63) a t any level of the mangal except the landward fringe, but they are commonest on sloping banks just below the mangrove line along creeks or just within the seaward avicerinia fringe. The formation of the pellets making the raised edges to the nest suggest that the method of making them is similar if not identical with that described above and uscd by Yeriophthalmus chrysospilos. Boleophthalmus and Scartelaos both show vigorous display patterns the mcaning of which is not completely clear. The displays of Boleophthnlrnxs are the more confusing because i t does not appear to be possible to sex individuals in the field. A common display incident, seen while watching Boleophthalmus, is a confrontation with two individuals in a straight line (Fig. 68), open mouth to open mouth and pushing one another strongly in a fashion analogous to stags pushing antler to antler. The inside of the mouth of Boleophthalmus is a dark indigo blue, presumably of some significance in display. This species too, like

FIG.6 8 . Boleophthalrnus hodduerti (size en. 15 cm). Confrontation, note thp open mouth and then the two fish pushing one another, open mouth to open mouth. (From photographs by I. Polunin.)

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all other mud-skippers, often does a half roll on to one side and back again. They were frequently seen apparently being bitten by mosquitoes which landed just behind the eyes and above the pectoral fins to the obvious annoyance of the fish. Both Boleophthalmusboddaerti and Scartelaos viridis push themselves into the soft mud tail first. The periophthalmines go head first. It would appear that while these burrow with the mouth the former two merely push their way into the mud. B. boddaerti, S. viridis and P.schlosseri seem to be able to remainsubyerged during a great part of or, the whole of the period of tidal flooding. When submerged all mud-skippers swim with ease but rather slowly in normal fashion. On alarm they skelter along the surface, most of the body submerged but with the head and particularly the eyes above the surface, or flying-fish-likethey come right out of the water skimming the surface. On land they proceed by a series of skips and jumps. P. chrysospilos can also climb trees. The ability to perform these movements is the result of modifications of the skeleton and musculature. Eggert (1929a) made studies of several periophthalmine fishes and compared them with normal gobies, in an attempt to trace the modifications associated with migration towards land. Lele and Kulkarni (1939) described the skeleton of P. barbarus (= P . kalolo). Petit (1921) gave the first description of the mechanism of skipping on land. Van Dijk (1960) and Harris (1960) describe and discuss more fully the methods of movement and Harris attempts to correlate the different types of movement with the musculature. He studied P. koelreuteri in west Africa. Van Dijk studied the Periophthalmus occurring near Durban, South Africa (probably P. kalolo). I n addition t o normal swimming Harris recognizes three types of locomotion. (1) Ambipedal progression or "crutching ". I n this the pectoral fins are used as crutches (Figs. 69 and 70)-they are stretched forwards and then the fish swings on them and a t the end of the stroke the weight is transferred to the pelvic fins. There are no sinuous movements of the body, no alternation of limbs in a time sequence as is done by lower tetrapods such as urodeles and lizards. Hence van Dijk is mistaken in calling this type of progression "walking ". ( 2 ) Skipping on laml. This is normally an escape reaction, but is also used in feeding. I n this action the tail is bent forwards and to one side, the caudal fin rays dig into the mud. The body is straightened and the fish is projected forwards and upwards into the air. The vertical component is provided by the thrust of the pelvic fins and the pcctorals act as stabilizers.

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A

A FIG.69. Periophthalnzus koelreuteri from west Africa : cycle of fin movcmcnts during locomotion on land by crutching. Traced from a motion film. Each frame represents a timc lapse of 0.03 sec. (From Harris, 1960.)

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FIG.70. Periophthalmus koelreuteri. Autographic records made by a specimen crutching across a piece of glass covered with soot. (a) Trace of pectoral fin; (b) trace of pelvic fin ; (c) trace of caudal fin ; (d) impression of ventral part of body ; (e) trace of anal fin. (From Harris, 1960.)

(3) Skinanzing o n the water. A mud-skipper will skim across the water in a series of bounds. Each bound is preceded by a short period of swimming and during this the propulsive forces for the bound are generated. This means that the propulsive force for the bound is produced in the same way as that of a flying fish preparing for a glide. The tail, second dorsal and anal fins produce the forward thrust, the pectoral fins are held to the side during the flight which lasts about o__ ; see. P. chrysospilos is better adapted t o climbing than are members of the kalolo group or the west African P. koelreuteri because the pelvic fins have been united by webs of skin and so are able t o assume a suetorial function. I n relation to their amphibious habits the eyes are also modified. Like those of amphibians the eyes of Boleophthalmus,Periophthalmodon

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and Periophthalwms have a thick cornea, and a slight hypermetropia (Hein, 1913; Karsten, 1923; Walls, 1942). Walls has pointed out that the retina is rich in cones, the lower half having many cones and the upper half more rods. The upper half would be more frequently used for locating prey on the surface of the m u d ; the lower half for watching a rival in display. The eyes are raised above the surface of the head and can be pulled down towards the buccal cavity. This movement is frequent and seems to serve the same function as blinking in higher tetrapods. The eyes, unlike those of frogs, are not pulled down to project into the buccal cavity. The epithelia in the sides and back of the buccal cavity have been said t o serve as respiratory epithelia (Schottle, 1932), and Harms considered that accessory respiratory surfaces are present on the fins and in diverticula of the nasal sacs (see summary accounts in Grass&, 1958). The gill surfaces, according t o Schottle, are reduced in comparison with fully aquatic gobies. Schottle (1932) described the structureof the gills of several gobioid fishes in order to find specializations to life on land among mangal living species. She pointed out that while the gills of Boleophthalmus were normal and resembled those of fully aquatic gobies, the gills of the periophthalmineswere reduced. She also described that Boleophthalmu~ has highly vascularized papillae particularly in the tail region, and that Periophthalmus and Periophthalmodon possess a reticulum of capillaries in the skin between the scales ; all these were claimed to be accessory respiratory surfaces. But no one seems to have shown that these are in fact respiratory. If this be indeed their function, one wonders how salt balance is maintained, for all these fishes are curyhaline, occurring as they do in waters of variable salinity. When a mud-skipper is submerged the opercular movements are easily seen to be similar to those of other fishes--water is drawn in through the mouth and passed out by way of the opcrcular openings. Stebbins and Kalk (1961), reporting on a study of the Periophthalmus common a t Inhaca, suggest that “undcrwater respiration does not involve air trapped in the branchial cavity as suggested by Willem and Boelaert (1937) ”and confirm that while under water they respire as do other fishes for, as they describe : When the fish comes out on land it commonly pauses at the water’s edge and gulps air. This involves a quick distension of the branchialcavity. The small valvular, opercular openings are closed and, with a quantity of water held in the gill chambers as well as t h e trapped air, oxygen rich water is available for gill respirationon land. The branchialregion remains distcndecl and opercular movements are suspended.

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This would suggest that no accessory respiratory surfaces are required. Stebbins and Kalk go on t o describe feeding : When feeding the fish makes a sudden lunge t o seize its prey and simultaneously expels the air and water, forcefully and audibly, through the opercular openings, wet patches or bubbles appearingon the surfaceof the partly dried mud. The sound can be heard at a distance of 15-20 feet (46-6 m). The fish then crawls promptly t o a nearby puddle or to the tide channel, replenishes t h e water in its branchialcavity by means of a few seconds of rapid pumping with the mouth under water and once again gulps air at the surface,distendingthe opercularregion. . . . Expulsionof air and water also occurrcd in captive animalsin t h e absence of feeding. Here, then, we see a mechanism of exchange of water, both while feeding and at other times, once again suggesting that there is no need for accessory surfaces. The accounts given by Harms, by Schottle and by Willems and Bolaert all indicate that they were not entirely convinced that they had found such accessory respiratory surfaces but that they were impelled to find them following preconceived ideas. My own observations at many localities favour the ideas of Stebbins and Kalk, and suggest that they apply equally t o P. chrysospdos, Periophthalmodon schlosseri and Boleophthalmus boddaerti. Khoo (1966) has studied the food and feeding of the four mudskippers common a t Singapore. He finds that Boleophthalmus boddaerti is a herbivore. I n feeding it emerges from the water, then makes rapid side-to-side movements of the head, skimming off a thin layer of mud and algae from the surface. This mouthful of material is then manoeuvred round the mouth, as can be seen by the vibrating movements of the lips and opercular region. Muddy water is then squirted from the mouth and from the gill openings. The fish then repairs to the water’s edge, dips its mouth into the water and may be seen to drink, so replenishing the water in the branchial cavity. The intestine oE this species is very long when compared to that of non-herbivorous mud-skippers. Scartelaos v i r i d i s is more omnivorous ; its feeding technique is different. It rasps off the top layer of the mud and collects the mud into a ball under the lower jaw and this mass of food and mud is then taken into the mouth. After some sorting process in the mouth the mud is squirted out. The stomach contents show both plant and animal material. Khoo demonstrated that lifting the surface film of mud with a prepared coverslip showed only algae, whereas scraping the surface with a slide removed algae, nematodes and harpacticoid copepods which were, presumably, living just beneath the surface film.

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Periophthalmus chrysospilos tends to be carnivorous but taking some supplement of plant material. Periophthalmodon schlosseri is completely carnivorous-in the confined space of a vivarium it has eaten a specimen of Scartelaos viridis half its own size (Khoo, 1966). 2 . Crustaceans The crustaceans living in the mangal fall into a few highly specialized families. Gecarcinids tend t o occur along the landward fringe but the only one related t o the mangal is Cardisoms carnifex. The others are more terrestrial and tend to be restricted to oceanic islands. The family Grapsidae is represented by an assortment of crabs mostly belonging to the subfamily Sesarminae-they include Clisto-

coeloma, Cyclograpsus, Ilyograpsus,Helice, Metasesarma, Metopograpsus, Sarmatium, Sesarma and Utica. Some of these are burrowers, some wander around seeking shelter where they may, among knee roots of mangrove trees, under logs, stones, etc. The ocypodid genera associated with the mangrove include Camptandrium, Cleistostoma, Dotilla, Dotillopsis, Euplax, Heloecius, Hemiplax, Ilyoplax, Leiopecten, Metaplax, Paracleistostoma, Pseudogelasimus, Tmethypocoelis, Tylodiplax, Uca and some of the numerous species of Macrophthalmus; species of Ocypode may also wander into the mangal. Some representatives of these genera are found a t similar intertidal levels in cooler waters. Of xanthids, one of the most conspicuous families of crabs on tropical shores, only a few representatives have penetrated the mangal. Taxonomic accounts are rarely helpful in locating a species likely to occur in the mangal, for only occasionally do the taxonomists append any note about habitat. Thalassinideanand alpheid prawns burrow in the mud. The mounds of Thalassina anomala are a conspicuous feature of Asiatic and Australian mangrove forests. Species of Upogebia are widespread in areas where the ground is firm enough to support a U-shaped burrow. Species of Alpheus make their labyrinths in wetter areas and are dominant within certain rhizophora forests. A single stomatopod, Squilla choprai, has been described from the mangal of Malaya (Tweedie, 1935a). All these crustaceans are distributed through the mangal with several variables of which the most important concern the reference l~ nature of the substratum-its particle size and degree of consolidation, humidity, saltness of the ground water, and t o a lesser extent temperature but then only towards the northern and southern limits. Very few of the crabs listed above, apart from Cardisoma and some species of Sesarma, reach a large size. None has any great importance

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as human food although Cardisoma and some of the larger species of Sesarma are eaten locally. Each species tends t o live in groups and these groups are often exclusive and monospecific. A slight change in the nature of the ground will often show a change in fauna. a. Effects of nature of the substratum o n crustaceans

As has been mentioned above, mangroves occur on beaches composed of several grades of particle size. Although the interior of the mangal is almost always muddy there is usually some admixture of sand. The seaward fringes are muddy on shores of accretion, but they may be sandy on stable shores. The landward fringes are often sandy. I n areas of sand with some silt but not an excess of it, particularly along sunny glades and a t the edges of the mangal, in both landward and seaward fringes the dominant crab is one or other of the forms of Uca lactea. At the lower levels of the seaward fringe on sandy beaches there may be found crabs characteristic of the lower shore, and these will tend to displace Uca lactea. Species of Dotilla, Mictyris and Scopimera may all occur but never together on sandy areas in or near a mangal. These are burrowers but only Xcopimera appears to have its life centred round a permanent burrow, and it will occur when there is little or no admixture of silt, and normally a t high levels. Dotilla and Mictyris, characteristic of mid-tide levels, are similar in habit and replace one another geographically, they migrate up and down the beach remaining only in areas where the level of the water table a t low tide lies a t or just below the surface. Dried-out banks of sand show by their crumbly appearance that they have been worked over as the tide was ebbing, and crabs will return t o them to burrow in, as the tide flows. These crabs are not normally part of the mangrove fauna but only exceptionally and incidentally occur among the lowermost zone of pneumatophores of Avicennia or of Xonneratia. Mixed deposits of sand, silt and detritus are colonized by a wide variety of crabs and representatives of all the genera listed above will be found here. Some will be characteristicof well-compacted muds and others will be found in ill-compacted muds. The fauna of muds composed of fine silt is again a specialized one. Such crabs are normally covered by a felt of fine hairs and when washed they have a downy appearance. I have already pointed out this feature of crabs found in semi-fluid mud (Macnae, 1957). The work of Altevogt (1957a), Miller (1961), Ono (1965) and Cameron (1966) makes it clear that all species of several genera of these smaller ocypodid crabs show a depcndence on the size of particles in

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the substratum. All appear to feed by using a technique by means of which diatoms or particles of edible detritus are separated from the mineral fraction of the substratum. The process has been studied in certain species of Uca, Dotilb and Mictyris. Specimens of other gencra which I have examined (Heloecius, Uca) and of some which have bccn studied by Ono (Ilyoplax, Scopimera) possess a buccal armature of similar form and hence may be presumed to feed in a similar manner. All of these smaller ocypodids feed by picking up portions of the substratum, licking the particles and/or selecting some of them, and discarding the rest in the form of the subspherical pellets which arc so notable a feature of the areas inhabited by them. Male specimens of Uca use only the minor cheliped, females of D’ca and both sexes of the other genera use both chelipeds more or less alternately. Chelipeds used for this purpose are slightly hollowed a t thc tips. Thc material is then transferred to the maxillipeds for sorting. The third maxillipeds are not greatly concerned in this. The second and first maxillipeds are modified to serve as sorting agents (Fig, 71). The setae of these two limbs are highly modified, and particularly those on the meropodite and to a lesser extent those on the distal segment2 of the limb. Several of these setae havc spoon tips, others are feathery, such are characteristic of the inner surface of the second maxi1lil;cd. The setae on the outer surface of the first maxilliped are also modifiej to form, together, a stiff brush. This is illustrated in Fig. 71. The form of the spoon-tipped hairs varies. There are more of them and each individually is larger in those species picking up sand grains, and smaller individually, and fewer in those species which feed on finc particles. Figure 71 indicates these variations in a scries of species of Uca : row I represents the set of maxillipeds of U . lactea which fecds off sand ;row I1 represents those of U . urvillei which feeds off fine mud, and row I11 those of U . dussumieri which feeds off very fine mud. The series illustrated is very similar in appearance to the buccal armature of Uca pugnax, U . pugilator (Bosc) and U . minax (Le Conte) illustrated by Miller (1961) and so may be presumed to function in the way hc described. A current of water is pumped up out of the branchial chamber by the scaphognathite. This current assists in the sorting process. It would appear that the material picked up by the chelipeds is rolled between the specialized setae on the meropodite of the second maxilliped and the stiff brush of hairs on the outer surface of the meropodite of the first maxilliped. The spoon-tipped hairs would hold sand grains against the “brush ” which would scrape off the diatoms, etc., living on these grains. The current of water would wash this organic material

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and any edible detritus towards the mouth. The sand and other mineral matter would sink t o the base of the buccal cavity and be discarded when a pellet of suitable size had collected. (These pellets hold together for some time, longer than similar pellets made artificially with water, so one must presume that thcy contain mucoid material from the saliva to give cohesion.) The water would return to the branchial cavity through what has been called the Milne-Edwards opening a t the base of the outer edge of the third niaxilliped. This opening is protected by the epipodite of the third maxillipcd and the armature of setae on the base of the epipodite is finer and more dense in U . dussumiwi and U . urvillei than in the sand-feeding ( J . lactea (Fig. 71). The provision of watcr for the flotation action is also important. Some water runs into the gill cavity as has been described and is sucked back during the upstroke of the scaphognathite. But there is an inevitable wastage of water. If pools of water are available-even very shallow pools-water can be taken up through an inhalant opening between the third and fourth legs, by the action of the scaphognathite, while the crab squats down into the watcr. But in some localities water is not always available. I n such localities the crabs are dependent on their burrows. rarely straying far from them and frequently returning t o them. Since these burrows always penetrate t o the level of the water table (Verwey, 1930; Macnae and Kalk, 1962), water is available here. This would explain the apparent dependence of such species as U . lactea, U . inversa and U . bellator on the closeness of the burrow. Miller indicates that the Amerimn U . pugnax and U . pugilutor are dependent on the burrow while U . minax which lives a t a lower level is not. From his dercription U . minax is not very dissimilar in habit from the Indo-Pacific U . vocans which only by an extension of definition may be considered with the mangrove fauna. Uca vocans (Latr.) (= U . marionis (Desm.)) makes certain, often difficult to satisfy, demands on its environment. It requires the presence of sand spits interspersed with muddy areas. Burrows are constructed in the edges of the sand spits and the crabs feed on the mud flat. Since these always have little pools of water scattered over the surface, a supply of water for flotation of food is readily available and the crabs are not tied to the vicinity of the burrows. Uca vocam thus tends t o wander quite far from the home sand spit but always returns to it or to a similar one as the tide flows. The species which live in muddy areas discard most of the mud but some may pass into the gut. Such particles are normally small enough to pass through the filter in the distal chamber of the stomach. Sand

FIG.7 1 . Maxillipeds of three species of fiddler crabs which inhabit different subst,rata. From top to bottom: row I, Uea lactea f. annulipes; row 11, Uea urvillei; row 111, Uca dussumieri. Across: row A, outer view of first maxilliped; row B, inner view of second maxilliped ; row C, outer view of third maxilliped. On the meropodite of the first maxilliped there is a ‘‘brush ” of more or less tightly packed bristles, coarsest in U . lactea and finest and densest in U . dussumieri. On the meropodite of the second maxilliped there is a characteristic arrangement of setae, some of which are spoon-tipped; a typical spoon-tipped bristle from each is illustrated. The “brush‘’of the first maxilliped and the specialized setae of the second maxilliped are used to wash food material off sand grains in U . lactea, from amongst fine mud in U . urvillei, and from amongst very fine mud in U . dussumieri. The size of the spoon-tipped setae and the density of setae on the “brush ”vary in proportion to the size of the particles from amongst which the food is obtained. On the third maxilliped note the armatureof setae on the epipodite ; this closes the so-called Milne-Edwards opening to the gill cavity. Two rows of coarse setae are sufficient t o prevent sand from entering the branchial cavity of U . lactea : three rows of fine setae and four rows of fine setae are respectively necessary to prevent fine mud and silt from entering the branchialcavity of U . urvillei and U . dussumieri.

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grains rarely, if ever, enter the gut ; they are sufficiently heavy to fall t o the base of the buccal cavity and be discarded. This description of feeding techniques will explain the distribution i a relation t o particle size of the species of Uca, of Dotilla, of species of Cleistostonza and probably of most of the ocypodid gencra which occur in or near the mangal. The series of figures of maxillipeds of ocypodid species given by Ono (1965) is suggestive of the fact that each species of these genera is highly selective in its demands on the substratum. Macnae (1957) described such differences in two species of Gleistostonaa, and subsequent examination of their maxillipeds has confirmed that

FIG.72. Distribution of some ocypoclicl crabs across an estuarine beach in rolation to (a) relative hcight of the habitat of each above low water mark, and (b) soil texture arid particle size. ( 1 ) Scopimera globulosa; (2) Uca Zactea; ( 3 ) Ilyograpsus pusilla; (4) U . arcuata,; (5) Macrophthalnius japonicus; (6) Pnrcrcleistostomrt cristatum; ( 7 ) Cleistoma dilatatum. (Redrawn from Ono (1965) with the lcvel of high water mark and moan sea-level added ; data taken from H.M. Admiralty Tide Tables, Vol. 111,I’acific Ocean.)

these appendages have an armature of setae suitable for use ox thc mudbanks they inhabit. These two species, C. edwardsi McLeay and C. algoense Brnrd. have their parallels in the mangal. C. wardi Rathbun and C. macneilli in Australia live in mud semi-fluid only to a depth of about 2 cm and not outside or in more solid or more fluid mud. Figure 72 taken from Ono (1965) illustrates the distribution of seven Japanese ocypodid crabs in relation t o particle size, durationof exposure a t spring tides and relative density of population, i.e. the preferred level. I have superimposed data lines related to npproximatc levels of spring tides (these have been taken from Admiralty tide tables). Among these shore dwelling ocypodid crabs thc species of Metaplax seem t o show the beginnings of the transition from being omnivorous scavengers to more spccialized methods of feeding by filtration tech-

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niques. Members of this genus feed on edible trifles, either plant or animal, which are stranded on the mud on which they live. Their maxillipeds are relatively unmodified except in so far as they have, along the edges of the distal segments, a number of setae which would retain the food while it was being washed by the stream of water being pumped through the buccal cavity. Only one species of Macrophthalmus, namely M . depressus, is characteristicallyfound in the mangal. This species unlike many of its congeners is not a burrower ; it occurs in the sandy bottoms of drainage channels and becomes rarer as these become deeper and develop into gullies or creeks. It lies in the sand with only the eyestalks showing and appears to filter detritus and nanoplankton from the water by way of the maxillipeds which act as a fishing net. But this is not its sole method of feeding for several may be found around a piece of carrion which is picked to pieces in the normal way of crabs. Specimens were once surprisingly found by Macnae and Kalk (1962a) when digging in the sand of the “avicennia parkland” a t Inhaca. So it would appear that when the tide is full they spread out from the channels. Crabs of the genus Sesarma seem not to be restricted to any particular grade of particle size of the substratum. The species common in eastern Africa range from fine mud t o coarse sand. Recent observations seem to suggest that these crabs may be t o some extent dependent on the substratumfor a t least a part of their food. Day (1967) has reported that S. catenata a t Knysna feeds a t night by “spooning up the surface silt, sucking out the detritus, and discarding the silt as pseudofaecal pellets ”. In April 1967 a t Inhaca and again in July a t Quissanga in northern Moqambique it was noticed that pools within certaingroves of Avicennia marina had a sandy bottom which was covered by a flocculent layer of diatoms. This felt of diatoms was broken by strips from which the cover had been removed. The only animals in these pools were S. ortmanni and S . eulimene; a t Inhaca it was suspected and a t Quisssnga confirmed that both these crabs feed by delicately scooping up the surface film using the spoon-tipped chelae. As the crabs progressed they left tracks some 20 mm wide from which the brown scum had been removed. Under these circumstances no pseudofaecal pellets were made. Pseudofaecal pellets are common in areas occupied by these sesarmas on fine muddy substrata. 8. rneinerti has been seen to devour human faeces and drag such material to the burrows. I n what appeared to be the village fishermen’s latrine at Morrumbene in central Mopambique (lat. 24”s.) I found the

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densest population of this crab that I have ever seen, six burrows were counted in each of several squares of side 25 cm. Sesarmas also chop up and devour fallen leaves, which may account, to some extent, for the scarcity of these in a mangal. They nibble a t germinating seedlings of any of the mangrove trees and so may hinder regeneration of a cut-over area (Watson, 1926). But as might be expected they will also devour one another and any carrion available. Their burrows always reach to the level of the water table and then are somewhat enlarged providing a pool of water to which the crabs may retreat in order to wet their gills. Other burrowing grapsids show a similar dependence on the water table. It is more difficult to know what determines the distribution of the non-burrowing species. Metopograpsus thuicuhar in eastern Africa and $1. frontalis (= M . gracilipes) in Australia and South East Asia may be found within the bruguiera forests or rhizophora forests on firm mud, seeking shelter in the crevices provided by knee roots, logs, etc. M . latifrons is always associated with the prop roots of Rhizophora around which it scuttles with ease, showing some reluctance to going into the water or on to the surface of the mud. A few species of the thalassinideangenera Thalassina and Upogebia construct their burrows in mangrove mud. The burrows of most thalassinideanswhich have been investigated are U-shaped. It appears that the burrow is an important adjunct to the feeding techniques of the animals. This use of the burrow has been described for Upogebia by MacGinitie (1930, 1934) and MacGinitie and MacGinitie (1949). He was describing the habits of U . pugettensis (Dana)and my observations on U . africana (Ortm.) suggest that these descriptions may apply throughout the genus. Verwey (1930) stated that the burrows of Thalassina anomala were single, with a long horizontal or near horizontal shaft and a pool a t the bottom. He described no ascending arm. Sankolli (1963) gives a similar description of burrows some 200 km south of Bombay. Both describe several side arms. Campbell (inZitt.) has told me that a burrow he excavated in Queensland was found to be U-shaped with several blindly ending side arms. One arm of the U and several side burrows emerged on the hillock of mud, the other arm in a pool not far away. These accounts appear to be contradictory, but both may be correct for the extensive digging a t the end of a long horizontal arm will cause a dropping in level on the ground above, so creating a conical pool which may link up with the system of burrows beneath. This constant activity of the mud lobsters is comparable with the activity of earth-

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worms on the land and lugworms (Arenicola spp.) on temperate zone mud flats. The digging techiiiqucs used are perhaps best described as shovelling and bulldozing. The maxillipeds and anterior walking legs are normally held in thc position shown in Fig. 51, and the container formed by these would appear to scoop up the mud somewhere down below. The mud is then brought LIP and deposited outside one of the entrances on the mound. Feeding has never been described for Thalassina, and nothing is known apart from a note by Johnson (1961) to state that its gut is always full of mud, a statement which 1 can confirm. One can only presume that it makes use of the bacteria and other micro-organisms which live in the mud. b. Effects of temperuture and humidity on crustaceans The crabs living in the mangal are above ground and foraging for much of the ebb tide. But there may be days on end when, for one reason or anothcr, only a very few crabs are encountered. They tend to be more numerously visible on the days of high spring tides, and scarcely dppear a t all on the days around the lowest neap tides. To what is this due? They tend also to be more numerously visible in warmer weather. At Inhaca, July 1964 was, taken by and large, colder than is usual and between 21 June a3d 2 July few specimens were seen a t any time during a spring tide series. Was i t temperature that kept them down? Thc air temperatures during that period were between 12" and 23"C, which are well above the lethal minimum. The crabs were not moulting for they were hard when dug up and no moulting specimens were obtained. The temperature relationships of species of Xesarma do not appear to have becn studied. The relationships of the five species of Uca common a t Inhaca werc studied by Edney (1961). He showed that the normal body temperature of each species was lower than that of the air a t the timc of measurement. Each showed an upper lethal temperature which was quite sharp. For Uca inversa which lives on open sunny sandflats the upper lethal temperature was 43.3"C. For Uca lactea f. annulipes which lives in sunny glades or along the fringes of the mangal or among the plant cover of Xesuvium, or Arthrocnemum, all places where shelter is close by, the upper lethal temperature was 42.1"C. For Uca gaimardi (= U . chlorophthalmus of Edney's paper) it was 40.8"C and for U . urvillei, 40°C : both of these live in the shelter of bushes and often occur together. Uca vocans (= U . marionis) was intermediate a t 41.4"C. This quite high level puzzled Edney but in fact

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U . vocans always inhabits open flats and only rarely occurs under the shelter of any vegetation. I n September the upper lethal temperature was lower by 2°C than it was in January. There is then, some degree of acclimatization to the higher summer temperatures. L4similar acclimatization has been shown by Vernberg and Tashian (1959) to occur in the fiddler crabs of the eastern American salt marshes. Edney mentions no acclimatization towards low temperatures. At Inhaca the lower lethal temperatures lay between 7°C and 8.5"C with U. urvilei and U. gaimardi showing the lowest. This is consistent with the fact that in South Africa these two species extend farther to the south than any of the others (Macnae, 1963). This distribution into areas where air and water temperatures in estuaries reach levels below the lower lethal limit a t Inhaca suggests that these two species a t least are capable of acclimatization to low temperatures. Ono (1965) records that U. lactea hibernates in Japan! Edney's work also gives an explanation for the distribution a t Inhaca of these five species. From this one may deduce that all species of Uca which are restricted to shady places will behave t o temperature and U . gaimardi and also that those preferring open as do U . urvilei sunny glades will show upper lethal temperatures closer to those of U . lactea f. annulipes and U . inversa. Verwey (1930) recorded that for U . bellator (= U . signatus) and U . consobrinus (de Man) the highest near-lethal temperature in gradually rising temperatures was 42°C. These two species show a distribution pattern similar to U . inversa and U . lactea f. annulipes: U . bellator resembling U . iwversa but occurring on flats of finer particles. Edney also studied, on a small number of specimens only, and in what amounted t o a pilot experiment, the relationships of these five species t o loss of weight by transpiration of water. U . urvillei and U . vocans lost weight most rapidly ; U . lactea f. annulipes and U . inversa least rapidly with U . gaimardi intermediate. This againis consistent with their known habitsof exposure and distribution in the mangal of Inhaca. Although no experimental work appears to have been done on the transpiration rates or on the lethal temperatures of the other crabs in the mangal, one may presume that most would resemble U . gaimardi or even U . urvillei for most of the mangrove crabs live in shady situations and rarely expose themselves t o the sun in the way U . inversa, U . bellator or U . lactea (either form) do. No figures are a t present available which compare the humidity of the air within a mangal with that in the neighbourhoodbut outside the mangal, it may be assumedto 'Mehigher,

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c. Effects of saltness of the water on crustaceans Within the mangal there may be a considerable variation in the mineral content of the water, both above and within the substratum. This variation is due to several factors. I n long-shore mangals (and this includes embayments where the salinity of the water is close to normal) variation is due to two factors only. The water may be diluted by rainfall, and under cyclonic storm conditions this may be so considerable as to be lethal for many organisms, or as the result of high insolation in regions of low rainfall the salinity of the soil water may be increased due to evaporation and transpiration. Under these conditions very high salinities may occur in the soil watcr of the bare areas colonized in eastern Africa, Pakistan and India by Uca inversa or in Australia by U . bellator. These may well exceed 10% in the dry season. But the balance of ions does not appear to be greatly modified until the magnesium salts are deposited a t considerably higher concentrations. In estuarine regions variations may be caused both by rainfall and by run-off from the land. Under these conditions the ionic balance may be so altered that the Knudsen formula does not apply (Flemister and Flemister, 1951). Snelling (1959) and Ono (1965) have studied the distribution of crabs along an estuary, and the distributions they describe must in the main be due to salinity changes as one proceeds upstream. Snelling lists two species of CEeistostoma: C. wardi, restricted t o the vicinity of the mouth, and C. mxcneilli which replaces it upstream. One may presume that the latter is the more euryhaline of the two. Again, of the species of Uca, U . longidigitum goes farther upstream and so presumably is the most euryhaline of the three species occurring. U . vocans (= U . marionis) and U . coarctata (H.M.-Edw.) do not go far from the mouth (the last is not recorded by Snelling, but is present a t Bulimba close to the mouth (personal observation)). Heloecius cordiformi8 H.M.Edw. is restricted by firm mud rather than by salinity. Of sesarmas, Snelliiig found that S. erythrodactyla Hess was replaced by an unnamed species some 28 miles (44 km) from the mouth. I n a similar way, S. eulimene replaces S . ortmanni as one goes upstream on the Maputo river, entering the Bay of Lourengo Marques (personalobservation). Ono (1965) found that the limits of upstream penetration by the species of crabs he studied were regulated by the following chlorinities: Scopimera globosa (de Haan), 3-5%,; Macrophthalmus japonicus de Haan and Uca lactea, 2-3%,; Uca arcuata (de Haan), Cleistostoma dilatatum (de Haan)and Paracleistostoma cristatum de Man, 0.5-0 .lo%,, and Ilyoplax pusilla de Haan, 0.03-0.5%,, Such figures suggest that these crabs are all very tolerant of variable salinities.

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Miss Jocelyn Crane has suggested to me (in conversation) that in her opinion U . Zongidigitum is a form of U . bellator. If this is so, then this species is tolerant of a very wide range of salinity for in the latter form it occurs characteristically on flats with salt glistening on the surface. d. Breathing specializations The crabs living in the mangal show various degrees of adaptation towards a terrestrial life. These are mainly associated with respiratory processes m d water economy, and these two are correlated with one another. There is a tendency towards a vascularization of the walls of the gill cavity. There is also a tendency towards an economical use of water. Land crabs of the genera Cardisoma, Geograpsus and Gecarcinides and the hermits Coenobita and B i r g u s latro (see Harms, 1920, 1931) show amongst them a considerable conquest of the land. Most of these genera are not, however, normally related t o the mangal, and apart from the species ofCardisornait is doubtful if any of them have become terrestrial via the mangal. There are two Indo-Pacific species of Cardisoma: C. carnifex is or seems to be restricted t o wooded, rather than forested, terrestrial fringes of the mangrove areas, while C. hirtipes rarely, if ever, comes down to sea-level. C. carnifex during most of the year does not stir far from its burrow. C. hirtipes is reported to be able to go for several days without visiting water ;it is apparently able to live and forage for some time between its occasional visits to a well or pool of fresh or only slightly brackish water. The breathing technique used by Cardisoma is the same as that used by several other crabs which live in the mangal and its landward fringes, and also some of those characteristicof sandy beaches. Several species of Ocypode, of Uca and presumably also several of the other smaller ocypodid genera possess, like Cardisoma, gills which are reduced in number and stiff so that they do not adhere to one another out of water. The walls of the gill chamber are vascularized and so this acts as a lung. This group of crabs pump air through the water that is retained in the gill chamber and so require to make fairly frequent visits to water t o replace the water which is continually being used up in breathing activities. It has long been known that crabs of the genus Sesarrna have a mechanism which is presumed t o be connected with oxygenation of water. A streaming of water over the carapace was first described by Miiller (1863) for Aratus pisoni (H.M.-Edw.), an American sesarmine

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crab. His description was repeated by several authors,Ortmann (1901), Bab&k(1921), Stebbing (1893) and by the compilers of the Cambridge Natural History. Verwey (1930) elaborated the account having studied S. mederi (= S. taeniolata), S. meinerti, S. bataviana and the freshwater S. nodul-fera. The following account is from Verwey and has been confirmed by undergraduatestudents working a t Inhaca on S. meinerti. When these species of Sesarma are immersed in water, it can be demonstrated by the addition of carmine that water is taken in by way of openings a t the base of the third maxillipeds (the so-called MilneEdwards opening), and also above the fourth and fifth walking legs, and exhaled a t the upper edge of the buccal cavity, When crabs are in very shallow water the carapace may be raised to show above the edge of the abdomen, a slit used for the uptake of a bubble of air into the gill chamber. This process is usually rather one-sided, either the right or the left side is raised. The musculature effecting this movement has not been traced. Water is taken up from shallow puddles by a different technique. The crab squats down so that the Milne-Edwards opening is under water and Verwey has shown that water is taken up during this period of squatting. When the crabs are in shallow water or exposed to air, water is seen t o emerge from the exhalant opening and then to flow along three grooves. Two of these lead directly to reticulated areas on the outer surface of the branchiostegite, the other leads to the orbit and thence by way of a narrow groove under the lateral margin of the back. These streams of water flow over two apparently reticulated areas-that flowing over a fronto-lateral area passes directly to the Milne-Edwards opening ;that flowing over a lateral area passes rearward to collect over the opening between the fourth and fifth legs and is from time to time sucked in when the drop is big enough. Occasionally the pumping may be strong enough to cause the water to overflow from the orbits on to the back. This water too, collects a t the opening between the fourthandfifth legs. The apparentreticulation is the result of setae, regularly arranged on small elevations with the distal ends of the setae clinging together. Pumping of water up and out through the same exhalant opening is commonly found among semi-terrestrial species of Metopograpsus ; M . Zatifronswas seen by Verwey to lift the carapace in the same manner as Sesarma. Some species of Macrophthalmus, Ilyoplax and Hetaplax, when they are out of water, also show the pumping of water described for Sesarma. The pumping of Metaplax crenulatus may be so strong that occasionally one can see two small fountains spraying water up, to fall over the back, on which the lines of the pattern lead the streams toward the inhalant openings between the legs (Fig. 5 5 ) . Species of other

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ocypodids do not pump water through the gill chamber for breathing purposes but only for feeding. e. Burrowing Crustacean burrowing subserves three distinct functions : (1) provision of a refuge, ( 2 ) as a centre of territorial behaviour and so as an accessory to mating, and (3) as an accessory to feeding. Any burrow may be used for each or all of these purposes. The use of a burrow as a refuge is presumably the primitive use of a burrow. As has been shown by Verwey (1930) and noted by Macnae (1957) and by Macnae and Kalk (1962a) burrows of all crustaceans on mud banks (and this includes mangrove swamps) extend down t o the water table. At this level the single burrows of crabs widen t o form a chamber where the crab can turn. This burrow is important to Uca as a centre of activity in territory defence. But when the crabs are not in the territorial phase the burrow is merely used as a refuge, and when used thus may be occupied by several crabs after an alarm. Special behaviour of this sort has not been described for any other genus of mangrove crabs, but preliminary work strongly suggests that Xesarma meinerti does use its burrow as a centre of territorial defence and display. The use of the burrow as an accessory for feeding has not been described for any crab but it has been shown to be important in the thalassinidean genera Upogebia and Callianassa (see MacGinitie, 1930, 1934) and the same probably applies to Thalnssinaanomala (see above). Another curious use of the burrow has been described by Tweedie (1935a,b). He recorded that from a burrow occupied by Xquilla choprai he obtained eleven larvae apparently all of the same brood, and that he obtained several specimens, many immature and some mature, of Ilyoplax delsmani from. another burrow. These records suggest that some mangrove crabs pass their whole life cycle close to the burrow of their birth and possibly even indicate some parental care such as defence of the brood in the nursery. f. Scylla serrata Xcylla serrata (Forsk%l)(Fig. 73) is the only portunid crab characteristically found in the mangal. It lives in burrows and is rarely seen 'away from them. These burrows are almost always elliptical in cross section ; they are usually long, up to 5 m, and slope gently down to the water table. They are most commonly found on the banks of creeks to the level of low water in the creeks, but they may also be found on the floor of the bruguiera,andrhizophora forests or among the roots of Avicennia and Sonneratia in the seaward fringe ; an occasional burrow

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may be encountered in the landward fringe. Such burrows are easily recognizable by the shape of the entrance and the quantity of soft mud thrown out a t the entrance. Along river banks these crabs are said to ascend upstream well above saline influence, but one wonders if they are really above the influence of the “salt wedge ”.

FIG.73. Scylla serratu, the large mangrove swimming crab; a female measuring 14 cm across the carapace.

Xcylla serrata occurs throughout the Indo-west-Pacific extending southwards to the vicinity of Mossel Bay in South Africa and to Port Jacksonin Australia. It is recorded from Japan,China and from several groups of Pacific islands. The complete life cycle is not known, nor a t what stage the crabs enter the mangrove to take up residence. The smallest specimens I have encountered in South African estuaries or among the mangroves a t Inhacameasured 20 mm across the carapace. The largest reach more A.II1.B.-G

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than 200 mm, the average for females being around 160 mm, for males slightly less. I n Ceylon the average size seen on market stalls was around 50-60 mm-this was probably the result of over-collecting. I n Australia, Stephenson and Campbell ( 1960) record females reaching 165 mm and males 195 mm. SerBne’s (1952) specimens from Viet Nam range from about 60 to 95 mm. Arriola (1940) has given an account of moulting and growth from 6 x 9 mm up to 90 x 130 mm in twelve moults a t intervals increasing from 9 days for the first two stadia observed up to 23 days for the last stadium observed. The total period for which they were kept and studied was 5 months. This suggests that under Philippine conditions growth is rapid. Mating, according to Arriola, takes place just after moulting while both individuals are still soft. (De Breitas (unpublished data), who has been observing captive Penaeus indicus in Lourenyo Marques, has noted that in this species too, mating occurs just after moulting between a hard male and a soft female.) Eggs are carried around (Jide Arriola) for 17 days and hatch as zoeae. Arriola was unable to rear the larvae and no records of the duration of the planktonic period exist. Arriola records that young crabs enter the estuaries around Manila Bay between June and August in large numbers and suggests that maturity may be reached within a year. Females may migrate t o spawn their larvae or they may shed them on an ebbing tide. The widespread distribution suggests a long pelagic larval period. Crosnier (1962) records the finding of several specimens almost undigested in the stomach of a specimen of the tiger shark (Galeocerdo cuvieri Agassiz) in the Mogambique Channel about 20 km from the edge of the continental shelf and 50 km from the Madagascar coast. He comes to the conclusion that these crabs also live a t the edge of the continental shelf since the freshness of the specimens in the shark’s stomach precluded their having been caught inshore. I n shore a t InhacaXcylla has a wide range of habitats. Local Ronga fishermen have told me that the largest specimens, almost always female, are collected from burrows exposed by equinoctial tides along the channels between the sandbanks. They suggest that the crabs migrate downwards as they grow; smaller specimens are caught far up the creeks within the mangrove and larger ones as the creeks approach the sea and the mangrove edge. Specimens taken within the mangrove are always dark in colour, usually a dark mottled green, specimens from the channelsa t Inhaca are usually brownish rather than greenish. It would seem that, like most other portunids these crabs are capable of some degree of colour change related to the environment.

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It was this occurrence of larger individuals of different colour patterns that led Estampador ( 1 949) to seek for specific differences, so that he recognized three species using cytogenetic characters as his main distinguishing features. No subsequent author except Serene ( 1 952) has recognized these differences. Furthermore Estampador's cytological work appears to be rather uncritical. I n Queensland,Stephenson and Campbell (1960) record that after spates in the rivers large numbers of Scylla appear off river mouths as though they had been washed down by the increased flow of fresh water-or perhaps the dilution of water in the burrows had made them leave and then be carried passively downstream to a more suitable salinity. A similar occurrence has been noted a t the mouths of the Keiskama and Kowie rivers in the south-eastern Cape Province of South Africa (Macnae,unpublished data). More work is certainly necessary on this most delectable of the edible crabs and one on which some important,if local, fisheries depend. g. Penaeid prawns Hall (1961) has stated that mangrove areas are important feeding grounds for penaeid prawns in Malaya and Singapore. I n western Malaya and along the Straits of Malacca this is probably always true, for almost the entire coastline is mangrove-clad. But on other shores the statement needs modification. De Freitas (personalcommunication) has shown that the penaeid prawns found and fished in the Bay of Lourengo Marques fall into two groups: ( 1 ) those such as juvenile Penaeus japonicus Bate which are caught in beach seines off sandy beaches with no mangroves, and ( 2 ) those which are caught in set traps off shores in front of mangroves. These catches invariably include various sizes of P . indicus H.M.-Edw. and of Metapenaeus monoceros H.M.-Edw. and occasionally large specimens, often very large specimens, of P. monodon Fabr. and of P. semisulcatus de Haan, but never small specimens of these. Since these prawns are caught on moonless nights after a spring tide in traps set across the drainage channelsof the shore, the inference is that these prawns are migrating back to deeper water after a spell within the mangrove or on the shore in front of the mangroves above the traps. Since the prawns enter a t full tide the fish ponds of Java and elsewhere one may presume that they enter the mangal and that they feed there. But insufficient is known of the biology of penaeid prawns to make any but tentative statements. 3. iklollusca Representatives of only a few families of molluscs have invaded the mangal. Of gastropods two families only are well represented: the

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WILLIAM MACNAE

Potamididae and the Ellobiidae. Two other families are represented by one or two species : the Onchidiidae and Littorinidae. The littorinids are forms which live among the foliage of the trees of Avicennia and Xonneratia in the landward fringe. Littorina (Melarapha) scabra is widespread in the Indo-Pacific; feeding probably on the colonies of algae which grow on the twigs and older leaves, they do not seem to chew the leaves on which they are often found. The bivalve Enigmoninro+sea is a suspensionfeeder (Yonge, 1957). Peronia peroni (Cuv.) is the common onchidiid in eastern Africa and Madagascar and other species replace it elsewhere. The family Potamididae is represented by a series of species and genera. Pyrazus ebeninus J. E. Gray is a characteristic inhabitant of mud flats below mean sea-level but may occasionally extend upwards among the lowermost pneumatophores of the seaward fringe on stable shores with neither accretion nor erosion. Terebralia palustris and T . sulcata, almost sympatric species, live on the surface of firmer muds in the seaward fringes and bruguiera forests but are absent from the soft muds of the rhizophora forests. Telescopiurn telescopium is characteristically found on soft muds in the rhizophora forests, on the surface of the mud in shallow pools, and on the muddy banks of creeks. T . rnauritsi lives on the firmer muds of the sonneratia and avicennia fringes in Java and Sumatra (Butot, 1954). I n Malaya it is almost sympatric with the other, both being commonly found together. The ellohiids are commonest a t the upper level of the bruguiera forest, in ceriops thickets and under the litter of the landward fringes. This family, which Morton (1955) considers to be the most primitive of the pulmonates, has representatives of several genera in the mangal fauna: Ophicardelus, Melampus, Cassidula, Ellobiurn and Pythia are all represented by several species. Of these Pythia is the most terrestrial, its species ranging from the upper levels of the landward fringe into the rain forest above high water mark. Ophicardelus and Melampus are cryptic forms living under the leaves, logs, etc. which litter the surface of the landward fringes. Cassidula and Ellobiurnare more characteristic of the lower levels of the landward fringe and extend downwards almost t o the seaward edges of the bruguiera and rhizophora forests. Melampus still possesses a free-swimming veliger but this is suppressed in the others. To some extent these molluscs are responsible for reducing fallen leaves to humus. Although they are recorded as living on the slimy mud around the mangrove roots and pneumatophores, species of Cassidula and Ellobiurn are usually found where fallen leaves are coinmon. Ophicardelus and MelamrLpusare normally cryptic occur-

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ring under leaves and driftwood or under the trailing plants in the zone of samphires and Sesuviunz. Shells of species of Syncera (= Assimiizea) are common ton a t all levels up to the landward fringes. I n Australia specimens of Salinator are common and also of Bembicium. No work other than taxonomic has been done on this group of what v011 Martens used to call submarine snails. Their requirements are neither known nor understood. Their life cycles are not well known and have been rarely commented on. Morton (1955), discussing the evolution of the Ellobiidae, sees in them a group close to the stem of the pulmonates and places them in a position a t the base of the pulmonate stem analogous to Actaeon a t the base of the opisthobranchs. Morton would consider the estuarine and mangal-living species and genera more primitive than those he calls the marine intertidal, or coastal terrestrial or inland terrestrial forms. It is inherent in Morton's thesis that the pulmonates came from the sea by way of the mangal in the tropics or salt marshes in temperate regions. Equally little is known of the requirements of the bivalves living in the mangal. Glaucomya and Laterntila are typical mud living forms living in Coccoons of a sort among the rootlets of the mangroves of the seaward fringe. Potyrnesoda (Geloina)and Batissa are representatives of freshv,ater families which have presumably become euryhaline.

V I I . GEOGRAPHICAL DISTRIBUTION A. E'xtrutropiculextensions of naangroves and their associated fauna Mangroves reach their greatest luxuriance, both in number of species and in area covered by them within a few degrees of the Equator in countries where rain falls abundantly in all seasons. North and south of this belt one season becomes dry, the result of the shifting of the intertropical front and of the monsoon effects of the Asiatic land mass. Surprisinglythis change does not affect the constitution of the mangrove forests, although i t may and often does affect the way in which not only individual trees develop but also the way in which they are distributed in the association. As the length of the dry season and its intensity increases changes occur as described above (pp. 91-1 14). Mangroves extend beyond the tropics both northward in Asia and southward in Africa, Australia and New Zealand. Except in eastern Asia the manner of falling out of species is similar. On the African coast Sonneratia alba and Heritiera littoralis are quite common a t Inhambane (lat. 24"s.) but do not occur south of this.

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WILLIAM MACNAE

Ceriops tagal is abundant and Xylocarpus granatum is present in the Bay of Lourengo Marques (lat. 26"s.). Rhizophora mucronata and Bruguiera gymnorhiza reach their southern limit a t the estuary of the Bashee river (lat. 32'5.) and Avicennia marina a t the Kei river mouth only a few miles farther south. This is the southern limit of mangroves but elements of the fauna of the mangal reach beyond Knysna on the south coast (Macnae, 1963). Passing north into the Red Sca, B. gymnorhiza, C. tagal, R. mucronata and A . marina occur in the Bay of Massawa (lat. 15"N.),while A . marina reaches the southern tip of Sinai (lat. 29"N.) (Ascherson, 1903). I n Australia B. gymnorhiza, C. tagal, R. stylosa, Aegiceras corniculatum and Avicennia marina are common in Moreton Bay and only just cross into New South Wales a t lat. 28"s. Ae. corniculatum and A. marina occur in Sydney's Middle Harbour. A grove of A . marinm occurs in Western Port Bay (lat. 38"s.) near Melbourne. A . marina is widespread a t the head of each of St. Vincent and Spencer Gulfs in South Australia and reaches Adelaide flat. 35" 30's.). In the west most of these species occur in Shark Bay (lat. 26"s.) and A . marina occurs a t Bunbury (lat. 34"s.) (Macnae, 1966). There are few suitable localities between these two :if any occurred in the Swan river estuary they have long since disappeared. Oyama (1950) reports that the northernlimits of mangrove swamps in eastern Asia are the Yaeyama Islands (lat. 25"N.), RyG-Kyii archipelago (lat. 26-27"N.) and South China (ca lat. 25"N.). A clump of mangroves also occurs a t Ki-ire village, Kagoshima Bay, a t the south end of Kyiishii Island (lat. 35"N.) but he reports that no swamp has developed there. Van Xteenis (1962) records that only Kandelia kandel occurs here ; Oyama did not give the identity of the species. I n the same paper van Steenis records that the southernmost occurrence of any mangrove is in the North Island of New Zealand a t less than 40"s. A . marina is abundant but dwarfed in Auckland Harbour (lat. 37"s.) (Chapman and Ronaldson, 1958). The reasons for these limits are puzzling. For example, the differences in climatic conditions between Inhambane and Lourenqo Marques are not great yet they are clearly such that Xonneratia and Heritiera do not develop around the Bay of Lourengo Marques. The demes represented a t the extremes of distribution of Avicennia mccrina in Africa differ in relation t o temperature tolerances from those occurring in southern Australia and New Zealand and also from thosc in eastern Asia. Chapman and Ronaldson (1958) considered that the New Zealand groves of A . marina were limited by the occurrence of

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killing frosts. I n South Africa they grow well a t the Bashee estuary where the average daily minimum in July is 12°C and the minimum recorded in thirty-seven years is 4.4"C, but not a t East London where the average daily minimum in July is 10°C and the minimum recordcd in sixty-eight years is 2.8"C. This suggests that an absolute minimum of around 4°C is the extreme that can be tolerated. The yearly mean at Bashce is 19"C, a t East London 17*7"C, and these too are almost certainly significant-but howl As a contrast A . marina a t Western Port Bay is growing in a region where the average daily minimum for July is 4°C and the lowest temperature recorded is 0°C (figures for Melbourne, Australia, some 45 miles away). I n the Northern Hemisphere the local populations would appear to bc less tolerant. Oyama (1950) reports that the lowest temperature recorded in the Yaeyama Islands is 15°C and the average winter temperature 17-22°C. No doubt the Ryii-Kyii Islands show a comparable range. This is very similar to the temperature regimen a t Inhaca and the Bay of Lourenpo Marques a t a similar latitude in the Southern Hemisphere. Clearly the Victorian and New Zealand demes of A . marina are much more low-temperature-tolerantthan either the eastern African or east Asiatic demes. I n South Africa, Day et al. (1952) and other workers have shown that tropical animals extend farther south in estuaries than others characteristic of open coasts. Macnae (1963) has traced the southward extension of the animals associated with the mangroves a t Inhaca and has shown that many of them occur in the well-developed and wellzoned mangals a t the estuary of the Umngazanariver some 18 km south of Port St John's. A few only go farther, and several of these reach south coast localities. Two elements have to be distinguished a t Inhaca: a tropical element with species of Sesarma and Uca, with Cerithidea decollata, Peronia peroni and Terebralia palustris ; and a southern element with Upogebia africana and Sesarma catenata. The latter, naturally, extend farther to the south. The former group have mostly dropped out before or reach their limit a t Knysna. This process clearly operates too in Japanwhere tropical genera and species are common in the Inland Sea and extend northwards in estuaries along Honshu Island. I n Australia the fauna associated with the mangroves in Sydney Harbour is a depauperate tropical one-all the species recorded (see Dakin et al., 1953) being from Queensland (Macnae, 1966). On the other hand, the fauna of the mangals in Western Port Bay, in the South

222

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Australian gulfs, in New Zealand and at Bunbury are all representative of the fauna of the local mud flats, an@ though they may contain tropical genera they contain no tropical species (Womersley and Edmunds, 1958 ; Macnae, 1966). This difference between South African and Australian shores may no doubt be explained by the vagaries of circulation of the warm water currents off shore. The strongly flowing Agulhas current impinges on the Natal coast near Cape St. Lucia and runs south along the edge of the continental shelf a t a distance of about 5 miles. When approaching East London where the coast trends more strongly westward, the current gets farther off shore until near Port Elizabeth it runs some 30 miles out to sea. I n theory eddies sent off from the current will transgress over the colder waters of the counter current and bring warm water organisms and flotsam of tropical origin in shore. This may occur far to the south. Dr JohnMuir, a country physician of Riversdale between Knysna and the Cape, collected seeds of several tropical plants on local beaches and recorded (1937) finding viable seeds of Thespesia populnea and of Heritiera littoralis. The former occurs commonly in northernNatal, the latter is not found south of Inhambane close to the Tropic of Capricorn. Hence these seeds at least can retain their viability while floating considerable distances in sea water. The comparable current off the Australian east coast runs strongly only off south Queensland and northern New South Wales-southward it tends to veer away. Clearly it is not so efficient a transporter of drift material along Australian coasts, but it may well have carried seeds of Avicennia marina t o New Zealand’s North Island. Northwards the Kuro Shio transports drift seeds along the Rye-Kyfi archipelago and is no doubt responsible for the occurrenceof mangroves and the associated fauna in these islands. B. Biogeographical comment It is abundantly clear that the littoral fauna and flora of the Indo-west-Pacific region constitute a unit (Ekman, 1935, 1953), yet within this region there are quite distinct and definite divisions. As Hall (1962) has noted, Ekman recognized that the faunistic centre of thc region is the Malayan archipelago,centred on the southern tip of the Malayan peninsula, Sumatra, western Java and southwestern Borneo. The farther one moves away from this centre in any direction the more the fauna becomes progressively impoverished, and the addition of endemic elements only to a minor extent makes good the loss of Malayan forms. Such a statement is in general true also of

223

FAUNA AND FLORA O F MANGROVE SWAMPS

the marine flora, chiefly the algae and marine angiosperms. Few, if any, endemic elements replace the Malayan elements in the mangrove flora of other localities. The divisions which appear to be relatively clearly recognizable on the basis of the endemic fauna are (Fig. 74) : ( 1 ) a western division including Eastern Africa, Madagascar, the Mascarene Islands, and the shores of the Red Sea and Arabian Sea; (2) a west central division including the shores of Ceylon, the Bay of Bengal with the Aiidaman and Nicobar Islands, the coasts of Burma, the Mergui Islands, the west

FIG. 74. Subdivisions of the Indo-west-Pacific biogeographic region as indicated by locally endemic species of animals. tTnit no. 5 is somewhat speculative-there too few easily accessible faunal lists for this region.

are

coast of Malaya and Sumatra and the south coast of Java ; (3) an east central division including the east coast of Malaya and Siam, southeastern Sumatra,northern Java, southern and north-western Borneo ; (4) a north-easterndivision including the Philippines, Taiwan, northern Viet Nam, South China, the Ryii-Kyii IsIands and subtropical Japan; ( 5 ) Eastern Borneo, Celebes and the Moluccas; (6) New Guinea and Queensland; ( 7 ) the Lesser Sunda Islands and Western Australia, and (8) the island groups of the western Pacific. It must not be forgotten, moreover, that over the whole of this vast area there occur several trees, several herbs and some animals which are common t o all its parts. It is these widespread species that are responsible for the recognition of the region as a distinct unit. Such ubiquitous species include Avicennia marina, Bruguiera gymnorhiza, 8.

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WILLIAM MACNAE

Ceriops tagal, Lumnitxeraracemosa andXonneratia alba among mangrove trees ; Barringtonia racemosa, Heritiera littoralis, Entada phaseoloides, Derris trifoliata, Hibiscus tiliaceus and Thespesia populnea among mangrove associates ; Cardisoma carnifex, Helice leachii, Scylla serrata, Sesarnm meinerti, 8. smithii, Uca lactea and U . vocans among crabs; Terebralia palustris among molluscs, and Periophthalmus kalolo among fish. One doubts if each of these species is uniform throughout such a wide distribution. I have already mentioned the physiological variation within Avicennia marina, and the structuraland physiological variation within Uca lactea. Structural variations also occur in U . vocans but these affect the major chela alone and each or all of the three recognized claw forms may be found within the population of any one area. Chhapgar (1957) dividcd Indo-west-Pacific crabs into ten geographical groups which differ slightly from the above. The spread of the mangrove species must have been by means of sea-borne seeds or seedlings. How far can these be carried and still remain viable? Guppy (1906) and Muir (1937) report that seedlings of Rhizophora mucronata may still develop after 87 days afloat. Fruits and seeds of Xylocarpus, Entada and other sea-shore plants can germinate after floating for several days. Muir (1937) studied, over many years, the seeds cast up on shores near Riversdale (almost midway between Port Elizabeth and Cape Town on the south coast of Africa) and records that two of the commonest seeds on the drift line were Entada phaseoloides and Intsia bijuga, both inhabitants of the landward fringe of mangroves. These were still viable-they never germinated on the Riversdale beaches, although they could be germinated indoors. The nearest localities where Entada grows is the Bay of Lourengo Marques while Intsia is not found south or west of Madagascar. Seeds or fruits of Xylocarpus, Heritiera and Barringtonia racemosa were also cast up but rarely in a viable condition. Muir recorded that in his searches for seeds in drift he rarely found seeds or fruits of Sonneratia, Avicennia or ofrhizophoraceousmangroves far from the estuaries in which the parent trees were living. This observation seems odd and suggests that he may have searched outside the season of dispersal. The seedlings of the rhizophoraceous mangroves float horizontally on sea water, inclined in estuarine water and vertically in nearly fresh or fresh water. They have quite commonly been seen floating on the waters of the Bay of Lourengo Marques, Mombasa harbour and strait, and several other bays and estuaries visited by the author. Some of these would be transported to, and stranded on, unsuitable shores but some would reach suitable ground.

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It may be significant that the eight or so species of mangrove which have become established on the coasts of Africa, Madagascar, the Mascarene Islands and Melanesia as well as other South Pacific islands are all species which in Malaya and Indonesia have been shown to reach their optimum development in areas of near normal salinity. Insufficient is known of the life histories of the animals listed as being ubiquitous to account for their wide distribution. 1. Division 1. The western Indian Ocean

The fauna of the first division, i.e. the western Indian Ocean and its associated seas and channels, contains only a small number of endemic species. Sesarma catenata is an outlier of its genus which extends along the southern African coasts from the Bay of Lourengo Marques where it is uncommon. Southwards it becomes more abundant and it is the dominant salt marsh crab from Pondoland to Knysna and extends westwards along the southernAfrican coast to the Brede river mouth at approximately long. 21"W. Sesarma ortrnanni and 8. eulimene are two species which have only recently been distinguished from one another (Crosnier, 1965). Both occur at or near high water mark but the latter penetrates more deeply into the barringtonia racemosa association, upstream in an estuary, while the former prefers waters of higher salinity. S . guttata and 8. longipes are species common within the mangal. All four have their centre of distribution in eastern Africa and Madagascar and only S . longipes reaches Indian waters-it has been recorded from the Andaman Islands. Uca uraillei is purely African and Malgache, and U . inversa ranges from southern Africa to the vicinity of Karachi. Eurycarcinus natalensis ranges from Natal to India and is recorded from Madagascar, the Red Sea and the Nicobar Islands. (I wonder if this last specimen is in fact E. natalensis species of this genus are not easily distinguished from one another.) Cerithidea decollata is the only representative of its genus to be found in most of eastern Africa and Madagascar. Dautzenberg (1929) records C. obtusa, a widespread but eastern species, from Madagascar. Certain species are endemic t o the Red Sea, such as Sesarmajousseaurnei. The Malabar coast and the rest of the Arabian Sea's Indian shores have been colonized by the "central fauna "; Sesarrna rnederi is present and Chhapgar (1957) also records S. quadrata, S. oceanica and S. minuta, all typical Malayan species. Eurycarcinus orientalis replaces E . natalensis and continues eastwards. Several gastropods become common. Terebralia sulcata and Tele-

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MACNAE

scopiuna telescopium, both of which have been recorded as uncommon in Madagascar become a notable feature of muddy shores Salinator burmana reaches its most western extension along this coast as do brackish water bivalves of the genus Polymesoda (Geloina). On this coast the Malayan mangroves begin t o appear. Avicennia alba and A . oficinalis are conspicuous. Xonneratia apetalu is restricted to the Malabar coast where it occupies the niche utilized by S. alba in eastern Africa. 2. Divisions 2 and 3. The Indo-Malayan region

The region from Ceylon and the Coromandel coast of eastern India along the shores of the Bay of Bengal into South East Asia and including the largest islands of Indonesia, Sumatra, Java and Borneo and their satellite islands constitutes the centre of distribution of both the plants and animals of the mangal. Yet within this large region differences can be recognized and the whole area subdivided. The subdivisions follow, roughly, the three major drainage areas of the Pleistocene subcontinental peninsula of Sundaland (Fig. 75). My second division follows the western coastline and the portions of the foundered coastal plains behind this, the third division follows the north-easterncoastline and the associated foundered portion, the fifth division listed on p. 230 comprises the eastern shores of Sundaland together with Celebes and the Molluccas. There is almost no floral justification for making these subdivisions but there is considerable faunal justification. One of the few plants which may justify this is Avicennia lanata, a species common among the mangroves of eastern Malaya from Pahang southwards. Watson (1928) is explicit that it does not occur west of Singapore. Another genus with this split in distribution is Aegialitis of which Ae. rotundifolia occurs on the northern shore of the Bay of Bengal and a species of Aegialitis although no longer occurring has been recorded as fossil in Sarawak (Muller, 1964). Ae. annulata extends from eastern Indonesia to Australia. The separation of the second and third divisions was first hinted at in Smith's (1926) monograph of the sea snakes of the family Hydrophiidae (Tweedie, 1954). I n his descriptions Smith recognized six species ubiquitous in the Indo-Australian region ; seven restricted t'o Indo-Burmese shores ; seven from Malaya to the Philippines ; three were Chinese and fourteen Australian; a further eleven were shared either between the Indian and Malayan or between the Malayan and Australian regions. No explanationwas given or suggested. Significant

FAUNA AND FLORA O F MANGROVE

SWAMPS

227

FIG.7 5 . Diagrams, redrawn from Smit Sibinga in de Beaufort (1951), to indicate the extent of Sundalanda t the end of tho Pliocene and a t the height of the last glaciation when the sea stood some 150 m lower than today. The areas which would almost certainly have been colonized by mangroves are indicated.

22%

WILLIAM MACNAE

and relevant t o the present discussion is the distribution of two species, Hydrophis torquatus and H . fasciatus, each with two or more subspecies. Of these H . t. torquatus and H . f . fasciatus are distributed from India t o the northern approaches to the Straits of Malacca. H . t. aagaardi extends from eastern Malaya t o Borneo, the Philippines and South China, while H . f . atriceps extends from eastern Malaya to Borneo, South China and Australia. Mayr (1944), de Beaufort (1951), Tweedie (1954) and Hall (1962) have all noted the importance of the subcontinent of Sundalandwhich was in existence during much of the Pliocene and throughout the Pleistocene (Fig. 75). Mayr was concerned chiefly with the terrestrial fauna and Wallace’s line. He showed that this line, marking as it does the edge of the Sunda Shelf (i.e. the old shore line of Sundaland a t its greatest extent), indicates the farthest that a purely terrestrial fauna could extend over the Indo-Australianarchipelago. Similarly the edge of the Sahul Shelf marks the limits reached by the continental Australian fauna. The islands between have been invaded from both sides and show a mixture of impoverished Asian and Australian faunas. De Beaufort is in agreement with this, and van Bentham Jutting in a series of papers on the freshwater and estuarine molluscs also indicates the importance of these continental shelves. Tweedie and Hall are concerned only with marine crustaceans. Both hold that the existence of Sundalandfor such a long time separated the IndianOcean fauna from that of the South China Sea and permitted the development of sibling varieties and subspecies and even of species. It is only within historic times that these faunas have been brought into contact by the opening of the Straits of Malacca. Both these authors show that differences exist between the faunas of the west and east coasts of Malaya and they argue that mixing is, though not prevented, certainly hindered by the set of currents and by tidal turbulence at the southern entrance to the Straits. Table I1 gives Tweedie’s list of crabs so making this distinction clear. Hall recognized similar distinctions and differences between penaeid prawns. Crane (in Zitt.) also suggests that this land mass has been important in relation to speciation and distribution of fiddler crabs (Uca spp.). Guinot and Crosnier (1964) have shown too that of two sibling species of Sesarma, S. longipes extends from Natal to the Andamans while S . kraussi replaces it in the Straits of Malacca and a subspecies X. k . borneensis continues the range eastwards. It would appear that S. kraussi is a species which probably within historic times has spread by the prevailing northwards-tending tidal

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currents and is still spreading for it has been recorded from the Nicobar Islands. Dr W. S. S. van Benthem Jutting has devoted a lifetime of research to the study of terrcstrial and freshwater molluscs of the entire IndoAustralian archipelago. It is unfortunatethat nowhere does she give a TABLE11. CRABS AND SNAKESOF THE INDO-MALAYANREGION (Tweedie, 1954) U

a

b N

E

b

$

? ___

.-

~________

6 -~ -

Dotillopsis brevitarsis (de Man) Dotilloplax kempi Tweedie Camptandriumelongatum Rathbun Ilyoplax delsmani delsmani (de Man) delsmani serrata Shen longicarpa TweedLe spinimera Tweedie Scopimera proxima Kemp intermedia Balss Uca rosea (Tweedie) angustjfrons (dc Man) rhizophorae Tweedie Metaplax crenulatus (Gcrst.) tredecim Tweedie Sesarrria onycophora de Man lepida Tweedie rectipectinata Tweedie semperi Burger johorensis Tweedie k. kraussi de Man k . borneensis Tweedie Hyclropliis torquatus toryuatus Gunth. t. aagardi fasciatusfasciatus Schn. f. atriceps Gunth.

6

~

+ + + + +

+ + +

-t

+ +

+ + +

+ + +

s E

6 6

%

-~

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

complete distribution of any of the brackish water species listed and one cannot, from her papers, deduce any peculiarities of molluscan distribution similar to those shown by the crabs. Her studies do show that those islands connected by the Sunda Shelf have many species in common with one another and with continental Malaya and South East Asia. They indicate too that some differences may occur in relation to

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the three major drainage systems. For example, the faunas of northern Sumatra (Atjeh) and western Malaya have strong affinities. Likewise those of southeastern Sumatra, Java, and south Bornco. Not enough evidence is presented t o show similar affinitics between northern Borneo, eastern Malaya and South East Asia. 3. Division 4. North-eastern extensions The fourth division comprises the northernand eastern extensions of mangroves into Taiwan, South China, and the Ryfi-Kyfi Islands and an extension of the fauna associated with mangroves into subtropical Japan. So far as the mangroves themselves are concerned it is an area of progressive subtraction and the same is to some extent true of the fauna. Balss (1924) claimed that most of the tropical crustaceans fell off sharply along the chain of the Ryfi-Kyil Islands. However, his lists of crustaceans from these islands contain no mangrove-associated species apart from Thalassina anomala. But taken by and large this is apparently true also of mangrove-associated molluscs such as species of Polyrnesoda (Geloina), Terebralia sulcata, T . paldstris and species of Melampus. None of these reach southern Japan, but Oyama (1950) records that representatives of these genera and other mangroveassociated molluscs have been found fossil in Tertiary rocks in southern Japan. He also records similar deposits containing such shells even of modern species in Pleistocene deposits in Taiwan. Ono ( 1965) reports several ocypodids reaching Kyiishii Island, Japan,including Uca lactea, Scopimera globosa and Ilyoplax pusilla, all mangrove-associated crabs. Scylla serrata reaches Hong Kong and Hankow (which is some hundreds of miles up the Yangtse river).

4. Division 5 . Celebes, eastern Borneo and the Moluccas The fifth division comprises most of the islands between the edges of the Sunda and Sahul shelves. Van Benthem Jutting (1959a) gives an analysis of the distribution of freshwater and brackish water molluscs from the Moluccas, and shows that while the ellobiids have a very wide distribution only a few have western affinities but a greater proportion have eastern aEnities, i.e. with the fauna of New Guinea. I n earlier papers she shows that the fact that these islands were never connected to the islands comprising Sundaland has restricted the freshwater faunas of Celebes and the Moluccas. It is certain that this area could have been invaded by representatives of the more purely west-Pacific elements as well as by purely Indian Ocean elements over a long period, as these islands were not affected greatly by Pleistocene changes in level.

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The shore fauna and flora of this area seem t o have been little Btudied. This division has been established here as a result of its apparent isolation from the other regions but it must be considered to be tentative. The genus of Bombacaceae, Camptostemon, gives some floristic justification for this region. According to Troll (1933a) the species C. schulzii Mast. is restricted to the Moluccas, New Guinea and adjacent islands, and northern Australia, i.e. the edge of Sahul; the C. philippinensis (Vid.) Becc. is similarly restricted to eastern Borneo, Celebes and the Philippines, i.e. the western edge of the deep channel lying between Sundaland and Sahul. 5 . Division 6. New Guinea and Queensland

The sixth division is one in which the fauna of the northern section shows a distinct affinity with the "central widespread fauna "but in which toward its southern limits several typically Australian species become common. These include Cleistostoma macneilli and C. wardi and Helice crassa. Crabs of widespread occurrence include Helice leachii, Sesarma meinerti and 8. srnithii, Uca bellator, U . coarctata, U . dussumieri and U . luctea. Several of the smaller sesarmas, S. (Chiromantes) brevicristatum, 8. (C.) messa, S. (C.) lividum and 8. (C.) semperi subsp. longicristatunz have been described as new by Campbell (1967) and may be presumed to be more or less restricted to this area. One of the most characteristic crabs of this region is Heloecius cordiforrnis which would seem to be close to the ocypodid stem from which fiddler crabs of the genus Uca are sprung. It has two symmetrical chelipeds and shows a display pattern of the same basic type as that of the fiddler crabs. Euplax tridentata is another ocypodid restricted to this division. Several species of gastropods of the genus Bembicium are conspicuous in the seaward fringes. While the African mangrove fauna and the northeasternmangrove fauna extend far beyond the limits of mangrove trees, in Australia the animals of the mangal fall out before the mangrove trees themselves. The fauna of the Solomon Islands, New Britain, the New Hebrides and New Caledonia shows a strong similarity to this region-at least so far as I have been able to trace records. 6. Division 7. Lesser Xunda Islands and Western Australia

This is a division with poor mangals-not in number of species but in development. Much of the area has less rain than any of the other

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areas apart from the northern Arabian Sea, and this rain is highly seasonal in its occurrence. The mangroves, as a result, do not occupy all the potential area available. Large areas of barren salt flats are conspicuous. The fauna becomes limited to those animals with an apparently wide euryhalinity. The north-western coastline of Australia is recognized by Australian zoogeographers as the “Dampierian Province” and its distinctness was emphasized by Clark (1946) in studies of the echinoderms of northern Australia. He ascribed the differences from the Queensland fauna t o the isolation in the Pleistocene and later Tertiary provided by the Sahul shelf coastline which extended far to the north. It would seem to me that the open sea to the north would bring elements down from Celebes, the Philippines and Japan to the shores of Sahul and these would retreat to the present shore as the sea rose during the later Pleistocene and recent times. It is for this reasonthat I have tentatively included the Lesser Sunda Islands including Timor, although I have no faunal lists from these regions. Around Darwin and on other West Australian shores as far south as Shark Bay the most conspicuous fiddler crab is a species of Uca, at present undescribed, with legs of a brilliant orange red and back of a dark reddish-purplish-brown, which occupied the niche occupied elsewhere by U . urvillei. It occurs among the pneumatophores in the seaward fringes accompanied by U . dussumieri. This crab has not been seen elsewhere, by myself or by Crane (personal communication). The commonest of the smaller sesarmas has recently been described as new by Campbell (1967). This is Sesarma (Chiromantes)darwinensis. When visiting Australia I was considerably surprised to find myself familiar with many of the animals on Queensland shores, but the fauna on shores around Darwin was much less familiar. I was not there long enough to pinpoint the differences. 7 . Division 8. Paci$c islands

The eighth division comprising the islands of the western Pacific is a margin of subtraction. The closer to Indonesia the islands are the more species characteristic of the Indo-Malayan mangals will be present ; the farther out into the Ocean the fewer will be seen. I n the Fiji group the Atlantic and east Pacific species Rhizophora mangle is present as well as the west Pacific R. stylosa, (Guppy (1906) records it as R. mucronata but his diagrams of the plants clearly apply to R. stylosa; the two species were then not always distinguished). A third form of Rhizophora also occurs; this is always sterile and reproduces vegetatively. It may be a hybrid.

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Hosokawa (1957) gives a list of thirty-one species of plant occurring in the mangals of Micronesia. Of these all but one occur on Palau, the majority of the others occur in several islands of the Carolinegroup but only four extend to the more remote Marshall Islands; these arc Bruguiera conjugata, Sonneratia caseolaris, Lumnitzern littorea and Clerodendron inerme. VIII. USES MADE BY MAN OF THE MANGALAND ITSPRODUCTS A. Uses of the timber I have already suggested that mangrove timber may have been of importance t o early boat builders. Sea-going craft have been invented by mankind in several differcnt forms and in several different parts of the world. Chinese junks, Saxon and Viking long boats, Polynesian out-riggered canoes and the ships of Telmun are, or were, all prototypes. Chinese junks explored the coasts of South East Asia, Saxon and Viking long boats explored the coasts of the North Atlantic, Polynesian out-riggered canoes explored the western Pacific and reached as far as Madagascar. All these were invented by peoples who lived in areas with abundant timber. The ships of Telmun, like their descendants the Arab dhows, were developed by people who lived on shores where timber, apart from mangroves, was not easily available. When one looks at the illustrations of early boats depicted on the walls and artifacts of Egyptian tombs one realizes that the first river boats were made of bundles of reeds-such boats are still in use in the delta of the Tigris and Euphrates, on Lake Titicaca and probably elsewhere. These were replaced by boats built of wood. But the wood available was only in short lengths, presumably from the trees of one or other of the acacias which grow on the banks of the Nile. Such boats could easily "break their backs ",and so a rope ran from stem t o stern over two short masts in order to help prevent this. Such boats, however worthy on quiet river waters, would be useless a t sea. Before a boat or ship could go to sea, a keel and a stem had t o be invented. These should be heavy, straight and long. Who invented them "we just do not know and are very unlikely t o find out "(Villiers, 1952). The shores of the Gulf of Oman, and of the Persian Gulf are potentially able to support growth of mangrove trees, and 110 doubt in these early historic or prehistoric times did so. One is tempted t o suggest that it was from the tall trees of these mangrove forests that the first keels and the first stems of sea-going ships were laid down by the coastal tribes who later undertook the trade of the ancient city of Ur. These men of Telmun, the modern Bahrein, were already sailing the

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monsoons t o the Indian coasts between 2000 and 3000 B.C. These men passed their secrets to their Arab neighbours and to the Dravidians and Gujerats of southern India (Hawkes and Woolley, 1963). But mangrove timber would have to be replaced quite quickly, for it is very susceptible to attack by ship worms. This led to a search for other and more resistant timbers, and for this Malabar teak came into use. So the first timber to be used would pass into oblivion. On the other hand, out of water the timber of several species of mangrove has been found resistant to the attacks of termites. This has led to its use in the houses built in many parts of East Africa and Arabia, in areas under Arab influence. Rawlins, in a report submitbed to a Government Department in Kenya, showed the importance of this use in Arab architecture. For centuries Arab dhows have been plying between Arabia, particularly the Oman coast, and the estuaries of East Africa. Near these they established towns, Lamu, Gedi, Zanzibar, Kilwa, Ibo, and farthest south of all, Sofala. Most of these are now deserted. The essential purpose of the trade with East Africa was the collection of timber-gold and slaves were added luxuries. The timber was in the form of mangrove poles, chiefly of Rhizophora mucronata and Bruguiera gymnorhixa, both of which give clean trunks some 5 m long and averaging 10-15 cm in diameter a t the base. I n use such poles were laid across the walls to form the ceiling of one room, the interstices were filled in with rubble and plastered with mud to form the floor of the room above. This process would be continued until several storeys had been built. The mangrove pole, then, was the basis of the skyscrapers of Arabian towns. Apart from this, mangrove trees have not been much sought after for use as building timber. Some of the trees of thc landward fringes have a t times been in demand for structural and for decorative use. Much of down-town Singapore is built on piles of mangrove trees, chiefly rhizophoras. These are durable so long as they are completely buried and cut off from access by ship worms. Large trunks of Sonneratia gri$ithii have been used as posts on quays and piers. They are resistant t o ship worms but, as a result of the high salt content of the timber, iron spikes, nails and bolts are corroded. Trunks of Lunznitzera littorea have been in use for this purpose for periods ranging from twenty years in Banka t o fifty years in Riouw and were still sound (Watson, 1928). This species has also a timber useful in cabinet work, where it is classed as a rosewood. Large, well-grown specimens of this tree are rare today. Xylocarpus moluccense also produces an attractive timber resembling mahogany. X . granatum is almost always too knotty and gnarled and, since large trees go hollow it has no value as timber.

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1. Firewood and charcoal

The main use of mangrove timber today is for firewood and charcoal (Fig. 76). For this purpose the rhizophoras are preferred. I n some areas such as the extensive estuarine forests near Suratthaniin peninsular Thailand these species have been virtually exterminated. In most of South East Asia forest management has enabled the species to survive.

FIG.76. Some of a battery of over thirty kilns for charcoal production. Logs are piled close to the entrance to the kiln, baskets of charcoal ready for distribution are in the foreground. (South of Ranong, Thailand, February 1967.)

Management practice has been outlined by several authors, for its need was recognized, a t least in Malaya, towards the end of the nineteenth century. Discussions of the different types of forest management attempted and used will be found in the memoirs published by Watson (1928) and Noakes (1951). I n Malaya management on a rotational basis has been followed since 1900. I n most other countries it is more recent.

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Silvicultural rotation is designed to produce the maximum economic yield of the tree of choice. I n Malaya two types of forest are under management. I n Selangor and states to the southward, Bruguiera cylindrica is exploited. I n Perak, where the mangals are much more extensive, the species of Rhixophora are exploited. The former is used directly as firewood, because it is easily split, or as poles for scaffolding, etc. The latter are used for charcoal production. Because of the nature of the forest B. cylindricu is more easily cxtracted. The forests are relatively narrow and lie parallel to the coastline, and a n arterial road runs immediately behind them. Extraction canals are dug at right angles to the road and at convenient distances apart, and loading stations built where these impinge on the road. The canals divide the forest into strips and these strips are cut out by rotation when the trees reach an economic size. Regeneration of a cleared strip is rapid and complete and the strip is then thinned periodically, the thinnings being sold as fishing stakes, fencing stakes and for other similar purposes. Management of the very extensive mangals of the Matang in Perak is not so simple. I n these forests trees of one or other of the two species of Rhizophoru are felled, cut up into lengths, which must be convenient both for easy carrying and for easy stacking within the kiln of the charcoal burner. The larger trees are unpopular, and the most popular size of tree has a girth a t the height of the last prop root of around 50 cm (20 in). Management is designed to produce an ample supply of trees of these dimensions. Silviculture in this and other similar areas depends on various factors of which the most important are the accessibility of the forest and consequent ease of removal of timber, and then the ease and degree. of cover by regeneration, either natural or encouraged by planting Mangrove timber is all heavy, and will not float in water, so it has to be carried and hauled out manually. It has been calculated and found in practice that a rotation based on a forty-year cycle will provide trees of a size suitable for the demands of the charcoal burners. I n an undisturbed rhizophora forest the trees are close together, giving long clean stems and a continuous canopy. Younger trees and other species form several storeys beneath. In early stages of exploitation those younger trees which have reached the preferred size are cut out. The older trees remain as standards and provide seedlings for regeneration. This elementary "selection "system has disadvantages, mainly as the result of damage to younger trees. I n Malaya a variation, known as the "shelter wood "system, is used. Under this system all younger trees are cut out leaving the older trees t o give a complete

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canopy and to provide seedlings for regeneration. But the older trees left in this way are very vulnerable t o wind, and the occasional storms may cause much and expensive damage. I n practice, nowadays, it is more expedient to clear-fell an area. This area must be quite narrow to allow easy and complete regeneration; if wide, planting must follow. Slash is a nuisance, it takes about three years to decay sufficiently to collapse on to the surface of the soil. During this time seedlings may not be able to reach the soil surface and so be hindered from growing. At the game time also a good growth of ferns, either or both of the species of Acrostichum, or of beach thistles Acanthus, may have grown up through the slash and also prevent regeneration. Disposal of slash is, then, an essential of good forest management. Silvicultural practice also tends t o demand the removal of species for which there is little or no demand. For example trees of Bruguiera gymnorhiza, B. sexangula, B. parvijlora and Xylocarpus granatum are all eliminated. X . granatztm finds a use only as fuel for convertirlg the rhizophoras to charcoal. Occasionally the mischievousness of monkeys and the nibbling of crabs of the genus Sesarma will damage seedlings sufficiently to give a poor regeneration. 2 . Other uses At various times attempts have been made to utilize commercially the tanninsextracted from the bark of the rhizophoras. It seems unable to compete with that from acacias. It would seem also that bark obtained from African trees has a higher concentration of tannins than samples from South East Asia. Is this a result of the drier climate of the African mangal region? Investigations into the possible use of mangroves for pulping have been carried out by Australianworkers in New Guinea (Rep.C.S.I.R.O., 1953164, 1955/56). It would seem that woods of Excoecaria agallocha and Camptostemon spp. are useful but the rhizophoras less so. Japanesc interests have recently shown the possibility of using pulp from various rhizophoraceous mangroves as sources of cellulose for rayon manufacture. This may utilize the large amounts of Bruguiera parviflora which so often tend to replace a rhizophora forest after this has bccn cut out. The nypa palm is one of the most useful plants of the mangal. Its leaves are cut and plaited into "atap "the principal thatching material throughout South East Asia. I n poorer areas it is used to build the houses as well. The inflorescences are tapped for sugar and for alcohol production. The nibong palm is also a useful tree. I t s "cabbage "is

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uscd as a vegetable, its stem for house posts, piles and fish traps, and boards may be obtained from the hard outer wood of the stem.

B.

Pond cuZture of fish and prawns

I n various parts of South East Asia, notably Java, southern Sumatra,the Philippines and Taiwan the culture of fish and prawns in brackish water ponds created out of cleared mangals has been practised for very many years, in Java for centuries. The only modern, and the most useful, account of this culture is the detailed study by Schuster (1952) of the tambaks of Java. In the making of the fish ponds, known in Java as tambaks, the mangal has been completely cleared except for the seaward fringes. These are necessary, firstly as protection against any destructive action of the sea, and secondly because in most of the area utilized in this way, accretion is still proceeding rapidly and the presence of the mangroves of the seaward fringe renders available successive crops of seedlings for colonization of the new mud banks. Each pond is from 4 to 2 hectares (1-5 acres) in area, it may vary in shape but is usually narrow in comparisonto its length. The sites of the ponds vary from a few hundred metres to several kilometres in width. They are most extensive in the estuaries of the larger rivers. Those farthest from the sea will tend to be less saline than those behind the mangrove fringe. Each pond communicates, by way of a sluice gate, with a system of tidal canals. This enables the ponds to be drained or flooded a t suitable stages of the tide. The banks between, known as “builds,” are often planted with mangroves or other useful trees, usually species which can tolerate some salt. This helps to stabilize the banks. The caretakers of the ponds live in houses built on the banks and dispose of the manure accumulated from themselves and from their few domestic animals into the ponds. Considerable care and ingenuity has gone into the designing of the ponds and still goes into the cultivation of the soil, and the organisms which form the basis of the whole industry. The main purpose of the tambaks is to produce a marketable crop of the milk fish Chanos chanos. This fish does not breed in the ponds but has to be introduced as fry. As a subsidiary industry, other people collect the fry on certain sandy beaches where they are common, and transport them to the villages of the pond caretakers where the fry are sold and transplanted into nursery ponds adjacent to the tambaks. The cycle of production begins with an empty pond, the soil on the bottom sun baked ;it may have been turned over by digging. The pond is flooded a t a high spring tide, with a screen over the sluice to exclude as far as possible any predators or their juveniles. The screen does not

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necessarily exclude their larvae. With the addition of water, bacteria, blue-green algae and green algae succeed one another on the surface of the soil and in the plankton. When the caretaker of the pond considers that conditions are just right a number of fry are introduced from the adjacent nursery pond, the number being known from experience of the carrying capacity of the pond. The fish feed on the algae, grow, and when they have reached a weight of upwards of 250 g ($ lb) they may be harvested. I n a normal pond this weight will be reached in about 8 months. The fish can reach weights of 2-4 kg (5-10 lb). Harvesting of the crop is based on knowledge of the schooling habits of the fish, and then decoying them into a place convenient for capture; for example, they may be decoyed towards the gate by admitting a strong flow of sea water, and there they are relatively easy to net. The annual production of protein per unit of area is high, amongst the highest for any form of cultivation. I n certain of the tambaks of eastern Java, which are situated on juvenile volcanic soils, the production of Chanos may be as high as 178-338 kg per hectare (200-380 lb per acre). The average in eastern Java is around 160 kg per hectare (180 Ib per acre), while on the marl soils of Madura the yield averages only 71 kg per hectare (80 lb per acre). I n some areas the yield is improved by green manuring. Mangrove leaves or other chopped vegetation is scattered over the pond to sink and decay, and add to the available nutritive material. Of other species of fish some kinds of mullet, Mugilidae, which feed on algae in much the same way as does Chanos, give similar yields of protein. These will breed in the tambak areas and the larvae go in with the tide a t the time of filling. Another fish of varying importance and popularity is Tilapia mossambica. This fish, a stray from the eastern coa3ts of Africa, prefers the less saline waters of the ponds farthest from the sea. Yields may reach 89 kg per hect,are (100 Ib per acre) in relatively unproductive regions. At all stages they feed most economically on the green algae while chanos, a t least in youth, seems to prefer the softer blue-greens. Hence if tilapia is present growth of the green algae is easier to control and rarely, if ever, gets out of hand. Tilapia seems t o be limited to water where the depth is more than three times the depth of the fish. Where tilapia is abundantmalaria is controlled, for there seems to be some sort of an associationbetween the anopheline larvae and certain of the green algae (cf. p. 159). Tilapia also breeds in the ponds. This may be a nuisance, for these fish become sexually mature a t a small size and tend to expend their energies on sexual display and reproduction rather than on growing to a marketable size. But hybrid strains are available which give up to 98% of males and

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such strains arcuseful for culture in freshwater or brackish water fish ponds. Spread of tilapia into adjoining rice paddies is unpopular, the males, in digging their nests, uproot too much of the young rice. Hence, in spite of many advantages, tilapia is not Fopular,and attempts have been made to exterminate it in many countries. Occasionally, a t the beginning of the north-east monsoon, the pond may be drained to be filled again a few weeks later. Fry are admitted and adult chanos harvested twice a year. When the pond is drained any other fish will be harvested and marketed. There are many by-products, the most important being successive crops of penaeid prawns. Seasonal swarms of mysids and small sergestid prawns, Acetes spp., are caught, dried and made into a paste used as a savoury. The prawn crop is a most useful adjunct and while extreme yields of 740 kg per hectare (830 Ib per acre) have been obtained yields of between 23 and 63 kg per hectare (25 and 70 Ib per acre) are more usual. I n the vicinity of large Chinese settlements elsewhere in South East Asia, the ponds are used for the cultivation of prawns alone. The techniques involved have been discussed a t length by Hall (1962). A pond is cut off from an inlet or bay in the mangal. To effect this a bund is built up from materials locally available and a sluice or several sluices are built into the bund. Prawn larvae are admitted by controlling the inflow of sea water and adults are caught by trapping them in nets a t the sluices on the outgoing tide a t night. Many penaeids bury themselves in the mud by day and swim around a t night. At periods with suitable tides it may be possible to release water from the pond twice on a single night. Fishing may take place on about twenty nights per month. The yields are comparable with those of the ponds in Java. The large mangrove crab, Scylla serrata, also occurs abundantly in the tambaks of Java and the prawn ponds. It is not popular with the caretakers of the ponds for its burrows may run through the bunds and endanger their structure. None the less they are a popular article of diet with those who can obtain them. Many snails, species of Cerithidea and Telescopium telescopium, abound on the bottom of the ponds subsisting on the semi-fluid humus layer that so often collects These too are collected and eaten.

,

C. Reclamation Many of the low lying coconut groves in Ceylon and in the vicinity of Quelimane iii central Moqambique, just north of the Zambezi delta, are reclaimed mangals. The trees were felled, the slash piled into rows,

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soil thrown up from either side to cover the slash and raise the level above high water mark. A row of coconut palms was then planted along these raised banks. D. Xalt proclacfim I n mangrove areas with a strong seasonal climate the cleared mangals and the dried out areas are made into a series of shallow evaporation ponds for salt production. Such are common near Bangkok and near Lourenqo Marques. Salt is also produced in the humid tropics by an interesting technique. Old rhizomes of nypa are allowed to lie around in sea water, and the water is poured over them. The rhizomes are then burned and salt extracted from the ash (Browne, 1955). IX. ACKNOWLEDGEMENTS The compilation of this review would not have been possible without the assistance of many scientists and without considerable financialaid. I should like to thank the University of the Witwatersrand, the South African Couiicil for Scientific and Industrial Research, and the Royal Society and Nuffield Foundation for financing my research visits to many localities in the Indo-west-Pacific. Of individuals Dr J . A. R. Anderson, Professor A. J . Berry, Dr J. Carrick, Dr D. S. Johnson, Mr R. P. Kenny, Dr W. Meijer, Dr A. G. Nicholls, Dr J . Gomes Pedro, Dr I. Polunin, Dr C. G. G. J . van Steenis, Professor W. Stephenson and many others have helped me iii various ways. Miss M. Mullins and Miss C. Cargill assisted with the illustrations and Mrs E. Pienaar typed the manuscript several times. Sir Frederick Russell has been a most patient editor. To all of them I am grateful and finally t o my wife and family who have permitted me t o go off alone on prolonged research trips.

X. BIBLIOGRAPHY AND REFERENCES I n compiling this bibliography an attempt was made to include all papers dealing with the mangroves and mangrove areas of the Indo-west-Pacificbiogeographic region. It was, for the most part, prepared by Miss Margaret Thurgood as part of the requirementsfor the postgraduate Diploma in Librarianship of the University of the Witwatersrand, Johannesburg. I appreciate her assistance in this task. The bibliography is as complete as i t is possible to be, within the limits of reference journals available in Johannesburg,for the period 1930 to mid-1967. Earlierreferences have been culled from the papers consulted during the preparation of this review. Although the more important discussions of ecological problems related to the ecology of the mangrove flora and fauna have been included, much of the earlier taxonomicliteratureis not listed. Many taxonomists

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give no indication of the habitat of their organisms. Papers which discussed the economic aspects of exploitation of mangroves or of the animals occurring in their shelter have not been listed unless they include some comment of relevance to the general ecology of mangrove arcas or of the species concerned. Cert>ain popular articles and books have been included because they contain illustrations which are of greater value than the commentary or article accompanying them. Abbott, R. T. (1958). The gastropod genus Assimiizea in the Philippines. I'roc. Acad. nut. Sci. Philad. 110, 213-278. Abdulali, H. (1965). Birds of the Andaman and Nicobar Islands. J . Bombay nat. Hist. SOC. 61, 483-471. Abc, N. (1937). Ecological survey of Iwayama Bay, Palao. Palao trop. b i d . S t n Stud. 1, 217-324. Abc, N. (1942). Ecological observations on Melaraphe (Littorinopsis) scabra (Linnaeus) inhabiting the mangrove tree. Palao trop. biol. S t n Stud. 2, 391-435. Abel, 0. (1927). Fossile Mangrovcsumpfe. Paldont. 2. 8, 130-140. Acosta Solis, M. (1959). Los manglares del Ecuador. Contrnes Imt. ecunt. Cienc. mat. No. 29, 82 pp. Adriani, M. J. (1937). Sur le transpiration de quelques halophytes cultiviBs dam les milieux diffbrents en comparaison avee celle de quelques non halophytes. Proc. I<. ned. Akad. Wet. 40, 524-529. Alexander, W. B., Southgate, H. A. and Bassingdale, R. (1932). The salinity of water retained in the muddy foreshore of an estuary. J . mar. biol. Ass. U.K. is, 297--29a. Alexander, W. R., Southgate, B. A. and Bassindale, It. (1935). Survcy of thc River Tees. Part 2. The estuary: chemical arid biological. D.S.I.R. Water Pollution Research Technical Paper, No. 5. H.M.S.O., London. Almodovar, L. R. and Biebl, R. (1962). Osmotic resistance of mangrove algae around La Parquera,Puerto Ricu. Revue algol. 6, 203-208. Altevogt,, R . (1955a). Beobachtungen und Untersuchungen an indischen Winkerkrabben. 2. Morph. Okol. Tiere 43, 501-522. Altevogt,, R. (195513). Some studies on two species of Indian fiddler crabs, Uca marionis nitidus (Dana)and U . annulipes (Latr.). J . Bombay nut. Hist. SOC. 52, 702-716. Altevogt, R. (1957a). Untersuchungenzur Biologie, okologie und Physiologie indischer Winkerkrabben. 2. Morph. o k o l . Tiere 46, 1-110. Altcvogt, R. (1957b). Beitrage zur biologie und ethologie von Dotilla blanfordi, Alcocli und Dotilla myctiroides (Milne-Edwards). Z. Morph. Okol. Tieve 46, 369-388. Altevogt, R. (1959a). Okologische und ethologische Studien an Europas einziger Winkerkrabbe Uca tangeri Eydoux. 2. Morph. Okol. Tiere 48, 123-146. Altevogt, R. (1959b). Zur Okologie und Ethologie von Uca tangeri (Eydoux), Europas einziger Winkerkrabbe. I n t . Congr. Zool. 15, 891-892. Anderson, J.A. R. (1958). Observations on the ecology of pea,t swamp forests of Sa.rawak and Brunei. Proceedings of Symposium on Humid Tropical Vegetation, Tjiawi, Indonesia. Anderson, J. A. R . (1964a). The structure and development of the peat swamps of Surawak and Brunei. Malay. J . trop. Geogr. 18, 7-16. Anderson, J. A. R. (196413). Observations on climatic change in peat swamp forest in Sarawak. Commonw. For. Rev. 43 (116), 145-158.

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SOME ASPECTS OF THE BIOLOGY OF THE CHAETOGNATHS ELVEZIO GHIRARDELLI Istituto d i Zoologia e Anatomia Comnparata della Universita d i Trieste, Italy 1. Introduction .. .. .. .. .. .. 11. General Morphology .. .. .. .. .. .. A. The Eyes, Hooks and Tccth.. .. B. Integument, Fins and Tail . . . . .. C. Corona ciliata . . .. .. .. .. 111. Reproduction . . .. .. .. .. .. A. The Male Genital Apparatus .. .. B. The Female Reproductive Apparatus. General C. Spermatogenesis and Oogenesis .. .. D. Fertilization . . . . .. .. .. E. Laying o f t h e Eggs . . . . .. .. F. Habitat and Cycles of Sexual Maturity . . IV. Regeneration .. .. .. .. .. .. v. Affinities and Systematic Position . . .. .. VI . Laboratory Experiments .. .. .. .. VII. Acknowledgements .. .. .. .. .. VIII. References .. .. .. .. .. ..

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271 273 274 281 289 289 292 309 322 335 343 351 355 364 365 366

I. INTRODUCTION The purpose of this review is to cover certain aspects of the biology of the chaetognaths, paying particular attention to the biology of reproduction and to some organs and functions that have not been previously studied. Therefore, as far as morphology is concerned, only new information is mentioned and the reader is referred to the monographs quoted in the text for matter that is generally known. Obviously there may be some repetition or overlapping with other works (for example that of Alvariso), but in any event the reader will not lack references in this text to the work of previous authors. My intention has been to present a survey, as up-to-date as possible, of present knowledge concerning this interesting group of animals. 11. GENERAL MORPHOLOGY The morphology of chaetognaths has been described in several monographs, particularly those by Burfield (1927), John (1933), Kuhl (1938), Hyman (1959) and de Beauchamp (1960). I n these works, and 271

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especially in that by Kuhl, both the macroscopic and the microscopic anatomy are thoroughly dealt with. I shall therefore limit myself in the present work to some special characterswhich have a systematic or adaptational value or on which recent contributions have thrown new light. Chaetognathsall have an elongated body, similar to an arrow, hence the name “arrow worms” (Slabber, 1769) and their generic name Xagitta (Quoy and Gaimard, 1827). The body is remarkably transparent and may be divided into three regions which are morphologically well differentiated: the head, the trunk and the tail. The head is provided with a very complex musculatureand is armed by one or two rows of teeth and by a series of sheathed curved hooks ending in very sharp points. The trunk is separated from the tail by a transverse septum. Owing to the transparency of the body it is possible to see clearly the ovaries, testes and the intestine which in some cases, as in Sagitta minima, may prove a valuable systematic character (Ghirardelli, 1950b) (Fig. 1).

FIG. 1.

Diagrammatic drawing of Saqitta. c.Z. ciliary loop; a.f. anterior fins; p.f. posterior fins; c.f. caudal fin; Q female genital apparatus in the trunk; 6 nrale genital apparatusin the tail; S.W. seminal vesicles.

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A. The eyes, hooks and teeth There are two small pigmented eyes on the head. These have a central region composed of five combined pigmented cups (cupolae), one of which is much larger than the others and occupies about one half of the surface of the eye; each of the cups encloses a bundle of visual cells in connexion with prolongations of the optical nerve, connected with elements having a complicated structure. The structure of the eyes has also lately been studied under the electron microscope by Eakin and Westfall (1964). The electron microscope reveals a star-like pigmented cell in the centre of the eyc of Xagitta scrippsae Alvarico. Between the arms of the pigmented cell there are masses of processes of photo-receiving cells. Each process consists of a tubular segment containing some longitudinally aligned microtubes each with a diameter of about 500 and a length of 20 p ; a cone-shaped body composed of a core of large granulessituated at t h r base of the tubular segment ; a connecting piece which has the appearance of cones and rods, and connects the processes of the sensory cells with a fibrillar apparatusmade up of nine peripheral double small tubes (the central one is absent; the structure is of the type 9 0). Near the connecting zone there is a small typical centriole with a striated rootlet. The receptor process of the cell runs deep down into the sensory cell which seems to possess a corona of microvilli on its inner surface. A nervous fibril arises from the outer extremity of the cell and passes into the optic nerve. On the basis of these features, Eakin and Westfall also put forward some suggestions about the phylogeny of chaetognaths which are discussed below (see p. 363). The external aspect of the eye has been used by some authors as a systematic character for the determination of the species. Tokioka (1950) has compared the size and form of the cye and of the inner pigment spot, and has established several proportions that might be useful for identification of poorly preserved specimens. Net0 (1961) also regards the eye characters as useful for species determination. Similar work has been done by Fraser (1952) on chaetognathsin Scottish waters ; although feeling some doubt as to the usefulness of the method, he said that in some instancesit can be used to differentiate certainspecies. Also Furnestin(1954)has studied the eyes of cleveii species of the easternAtlantic. She has stressed that the generally well-defined limits of the central region of the eye are constant in any one species and may constitute a good classificatory character. The same holds for the pigmented septa which separate the visual cupolae : their arrangement varies very little within one species while

+

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it differs greatly between one species and another. I n Sagitta friderici Ritter-Zahony, for instance, the central region of the eye takes the form of a square, and the pigment spot may be seen to allow the five marginal clear cups. I n Sagitta hispida Conant the central region is subrectangular,slightly curved and crescent-shaped; the clear cups are often difficult t o see, four can be distinguished of which two are well separated by the pigmented walls disposed crosswise, while the other two are more or less attachedto each other. Probably the eyes function mainly as light receptors t o time the diurnal rhythms of the animal and to govern any phototactic movement (Reeve, 1966) : actually the major factor controlling the vertical distribution of Sagitta crassa Tokioka in the day-time is the photosensitivity of the animal, which nevertheless varies according to the growth stages (Murakami, 1959). However, Singarajah (1966), in laboratory experiments, observes that pressure increases cause vertical movements upward, but this response to pressure is not affected by light and is abolished by small changes in salinity, pH, temperature and violent agitation of the water. Hooks or grasping spines (Hyman, 1959; Krumbach, 1903) and teeth represent in some cases good systematic features: one or two rows of teeth may enable the worker to differentiate among some genera which are rather closely related, such as Eukrohnia which has only the posterior teeth and Krohnitta which has only the anterior teeth though well developed. I n every generation the numbers of hooks and anterior and posterior teeth change as the body length increases and also with the season (Murakami, 1959; Kado and Hirota, 1957) ; the number of posterior teeth in S. crassa increases suddenly when the food habit changes (Murakami, 1959). The sawlike hooks within the genus Xagitta are useful to distinguish the different forms of Sagitta serratodentata Krohn from all other species of the same genus, even if in this case, especially in adult animals, other features also exist which are both surer and easier to observe. Nevertheless Tokioka (1965a) does not regard the serrated feature of the hook as of great systematic value, as, under high magnification, the hook edge in some species shows sometimes an insignificant array of faint prominences regularly or irregularly arranged. Hooks and teeth are still very important charactersin the new classification of the chaetognaths proposed by Tokioka (1965a) (see page 280.)

B. Integument,fins and tail The integument may be composed of a rather smooth pluristratose epidermis. Furnestin (1967), using the electron microscope, confirms

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the multistratified nature of the epidermis and describes inter- or intrccellular nervous fibrillae which are in connection with the ventral ganglion and form a plexus which innervates the sense organs of the epidermis. I n several species there is t o be found a formation developed in the region of the neck which sometimes reaches and passes the caudal septum and has been named "collarette ) ' or lateral expansion of the epidermis (Grassi, 1883). This structure is formed by big vacuolated cells that roughly resemble the cells of the dorsal chord: this is why Grassi called the tissue forming the collarette "chordoid tissue ". It is specially developed in two genera, i.e. Spudella and Pterosagitta. It is interesting to note that the maximum development of the collarette is to be found in two species whose habitat is completely different. Pterosagitta draco (Krohn) is a typical pelagic species and the presence of the vacuolated cells seems t o serve the purpose of making floating easier. On the other hand, Spadella cephaloptera is a benthic species that lives attached, by means of special adhesive glands, t o the leaves of phanerogams or of submerged seaweeds. The collarette, though much less developed, is also present in other pelagic species like Sagitta bipunctata Quoy and Gaimard or 8. serratodentata. S. crassa also has a well-developed collarette which changes in size according t o the variations of chlorinity and temperature. There are four classes of development of the collarette from class A, characteristic of 8. crassa typica, t o class D of S. crassa forma naikaiensis (Hirota, 1959 ; see also p. 348). It was supposed that the development of the collarette of the large form of S. crassa might be significant for planktonic life (Kado and Hirota, 1957). According t o Tokioka (1965b) the development of the collarette does not seem to imply any phylogenically significant specialization. Originally the collarette might be useful as a protective tissue, but when well developed it might contribute t o the buoyancy of animals of moderate size; generally pelagic animals of much smaller size would not need such a structure. More or less conical masses of cells are often t o be noted on the epidermis, in the middle of which one sees some small bristles that are deemed to be sensory (Hertwig, 1880 ;Grassi, 1883). Two quite peculiar tufts of bristles are to be found at the sides of the neck of Pterosagitta araco. Horridge (1966) and Horridge and Boulton (1967) in Spudella cephaloptera, using the electron microscope and phase contrast microscope, were able t o observe two types of tufts along the body not previously distinguished : the tufts of bristles which are structurally not sense organs and the tufts of cilia which are. The bristles are seen in life whereas the ciliary tufts are visible only in sections or in life with

27G

ELVEZIO GHIRAHDELLI

the phase contrast microscope. They appear as a group of sensory neurons each of which bears a non-motile cilium a t the tip of the dendrite. Experiments made by Horridge and Boulton showed an accurate feeding movement toward any source vibrating a t 9-20 c/s with an amplitude of 100-500 p a t a distance of 1-3 mm. General vibration is ineffective ; stimuli which are too close, too strong or very close to the ciliary organ, cause an escape movement. Therefore the nervous system of the chaetognaths must include some mechanism of integration which discriminates the characteristic signal of typical prey a t the appropriate distance and direction (Figs. 2 , 3).

FIG.

2. Spadella cephaloptera makes a grab a t the end of a vibrating wire. It will do this in the dark. (From Horridge and Boulton, 1967, PI. 34, Fig. 1.) FIG. 3. Spadella cephaloptera. Light micrograph of two groups of projecting bristles. (From Horridge and Boulton, 1967, P1. 37, Fig. 8.)

Since chaetognaths feed as well in the dark as in the light, and baking into consideration the morphology of the eyes which arc without m y refractive means, it is unlikely that they can determine with sufficient accuracy the direction of their prey by visual means. Reevc (1966) was able to observe that Xpadella, unlike Xagitta hispida, has perhaps developed a mechanism to prevent self-predation and can distinguish between kinds rather than just size of animals. This may be effected by distinguishing between the rapid vibration of the appendages o€ most plankton animals of a suitable size and the single isolated action involved in the flick of the tail of a chaetognath (Reeve, 1966). A t the sides of the body one observes expansions of the epidermis which form one or two pairs of lateral fins. When two pairs exist, the

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first is entirely on the trunk while the second pair may be partly on the trunk section and partly on the caudal section. There are genera of chaetognaths that have only one pair of lateral fins, as for instance Eukrohnia, Krohnitta, Spaclella and Pterosagitta, while Sagitta always has two pairs: these may sometimes be connected by a small band made of the same tissue as the fin itself, as in the case of Sagittn lyra Krohn. Besides the lateral fins, chaetognaths also have a caudal fin. RGth lateral and caudal fins are always horizontally disposed. The fins are composed of two layers, one dorsal and one ventral, formed by a thin epidermis beneath which there are at least two other layers of cells that cover a furthcr epithelial plate which is the continuation of that which is in contact with the musculature of the body, An amorphous substance, which stains strongly with eosin, is interposed between these two epithelial layers, dorsal and ventral, of the fin. The thickness of this substance is not the same a t all points of the fins: it is more abundantin the region where the fins are inserted in the body, and becomes less towards the margin of the fin. The quantity of this substance also varies with age: it is completely absent at the moment of hatching, it increases with the progress of growth, and decreases somewhat in the older specimens, in Spadella a t least (Ghirardelli, 1959a). Both the lateral and caudal fins in Spadella are provided with very thin rays 2 or 3 p thick : in the lateral fins the rays are parallel with one another, 7 or 8 p apart, and sloping slightly backwards, while in the caudal fin they spread fanwise (Ghirardelli, 1959a). John (1933) thinks that these rays are formed from the amorphous substance and have a supporting function, which had indeed already been suggested by Grassi (1883). The amorphous substance itself probably also has a supporting function, considering its elasticity, especially in Xagitta. I n Spadella a more valid support function can certainly be attributed in the region of the fins to chordoid type cells (Grassi) which can be seen to be similar to those described in connexion with the collarette. I n Spadella, furthermore,the rays of the lateral fins are not immediately under the epidermis, as in Xagitta in which the epidermis is much thinner and forms a layer of cells directly covering the amorphous substance. Conditions similar to these can be found in Spadella only in the widest part of the caudal fin, i.e. towards its free margin. I n this rcgion, the fin does not exceed 30 p in thickness and is formed by two small epithelial plates, one dorsal and one ventral, covering the rays. Under the rays, or rather interposed between the dorsal and ventral rays, lies the amorphous substaiice about 8 p thick. An accurate

2i8

ELVEZIO GHIRARDELLI

description of the disposition of the fin rays was given by Grassi ; his description refers to transverse sections of the lateral fins in which the amorphous substance looks like a triangle with the shortest side in contact with the musculature of the body. Near the rays one sees elongated cells with very elongated nucleoli : it is probable that they are cells of the inner (basal)epithelial plate that have so modified. Everything points to the presumption that the rays derive from these cells and that the amorphous substance also derives from the epithelial plate. Schmidt (1951), through observations with the polarizing microscope, has brought to notice in Xagitta setosu Muller and Xagitta hexaptera d’0rbigny the presence along the rays of the fins of a substance which shows the characteristic birefraction of lipoids. The optical peculiarities of the fin rays lead further to exclusion of the suggestion that they may be constituted of collagen. According t o my researches and to the information supplied by the literature, a fin of Spadella in transverse section, starting from the deepest layer, is formed as follows : (1) Two epithelial basal layers which are the continuation of the epithelial layers in contact with the musculature of the body ; between these two layers is the amorphous substance which is, however, absent along the border of the fins and forms a middle layer less extended than the fins themselves. (2) Some layers of epithelial cells, more or less modified. (3) Outside integument epithelium. On the fins and specially on their dorsal surface there are glandular formations and tactile prominences that have been accurately described by Grassi (1883) and, as we have seen, accurately studied by Horridge and Boulton (see p. 276). The fins of chaetognaths are generally already present at the moment of hatching but in the majority of the larvae of the genus Xagitta it is not possible to make a clear distinction between anterior and posterior fins. The form and position of the fins constitute good systematic characters, in well-preserved specimens, and so do the presence and extension of rays on the fins. Even the extension of rays on the fins may, however, show some variation between specimens of different populations and also within the same population. Thus, for instance, Xagitta minima is described as generally lacking rays on the anterior fins, while in specimens in the north Adriatic the rays, though very thin, are present on the posterior side of the anterior fin. Xagitta inJlata

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in the Red Sea and the lndian Ocean is partially without rays both on anterior and posterior fins, especially in the median zone of the line of intersection on the body. This feature, however, is not t o be seen in Xagitta injlata Grassi in the Atlantic or in the Mediterranean. In X. injata in the Red Sea and Indian Ocean, the anterior fins may be longer than the posterior ones (Ghirardelli, 1947). A further feature one may consider is the length of the caudal segment in relation to the total length of the specimen. Furnestiri (1957, 1958) has carried out accurate researches on several species. She has been able to show that X. setosa which has a wide geographical distribution and lives in habitats having rather similar characters (North Sea; Mediterranean, in waters of low salinity; Black Sea), presents remarkable variations in the length of the tail segment and of the ovaries, which, however, do not break the unity of the species. Comparing X. setosa with S. euxina Moltschanoff, she could show that the latter is only a variety on a larger scale of X. setosa, and since it lives in the waters of the Black Sea it should be named 8. setosa var. euxina, though some authors (Alvarifio, 1965 ; Elian, 1960) regard it as distinct species. The same writer, still on the basis of biometrical inquiries, has further been able to confirm that X. friderici, though showing features similar to those of S. setosa, is nevertheless a separate species. I have myself been able to ascertain (Ghirardelli, 1947) that X. injata and S . hexaptera of the Red Sea and Indian Ocean, which Thiel (1938) judged two very near forms if not belonging t o the same species (he justified the differences he saw as due to a difference in age of the specimens), must actually be considered as two totally distinct species, and this mostly on the basis of the proportion between total length and the length of the tail segment. There naturally are other features that enable one to differentiate between S. hexaptera and S. injnta" ; among these are the form of the forward teeth which in X. hexaptera are always few (three or four at the most), quite elongated and poniardlike. Also the ciliary loop, notwithstanding its great variability with which I shall deal later, might be a discriminating feature. But at Naples I have observed (Ghirardelli, 1952) that the two forms of * Name correct according to Art. 19, 32, 33 of the InternationalCode of Zoological Nomenclature. Authors generally use Sugittu enflata but Ritter-Zahony (1908) pointed out that the Latin word is not enflata, as Grassi (1883) wrote, but inflata, and Baldasseroni (1915) explained further ''per il semplice fatto che in latino non esiste un verbo enflare ma esiste inflare, quindi influtu e non enJluta "[in Latin the verb is not enflare but inflare, therefore injZuta and not enflalata]. More recently de Beauchamp (1960) says "J e ne puis me rksoudre L employer le barbarisme original enJlata " [I cannot bring myself to use the original bastard form enflatu]. A.llI.B.-6

10

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ELVEZIO GHIRARDELLI

S. inJlata present in the gulf, differing in the values of the length of the tail and of the ovaries, are specimens of the same species a t different stages of their sexual maturity (see p. 346). I n order t o complete this information on the systematics of chaetognaths, one must necessarily mention the completely new classification proposed by Tokioka (1965a). According to this author, the Phylum Chaetognatha(Leuckart, 1894) is subdivided into two classes, of which the first Archisagittoidea nov. has only a single extinct species: Amiskwia sagittiformis Walcott. Although inclined t o the opinion of Owre and Bayer (1962) who consider Arniskwia as being a nemertine (see also p. 358) Tokioka cannot definitely reject the possibility that Amiskwia might represent an ancient form of recent chaetognaths. The second class Sagittoidea (Claus and Grobben, 1905) includes the living forms and is in its turn divided in two orders : (1) Phragmophora nov. Phragmatic structure made of the ventral transverse musculature in the coelom. Usually various kinds of glandularstructuresare seen on the body surface,in the neck or cephalic region. This order is divided into two families: Spadellidae (Gen. Spadella Langerhans) and Eukrohnidae (Gen. Eukrohnia RitterZahony, Heterokrohnia Ritter-Zahony and Bathyspadella Tokioka).

( 2 ) Aphragmgphora nov. The phragmatic structure is absent and thus the whole coelom is entirely hollow. Glandular structures on the body surface are scarcely developed. This order is divided into two suborders :

(i) Ctenodontina nov. (Hooks are curved gently and teeth-rows are comb-shaped, teeth are slender.) There are two families : ( a ) Sagittidae Claus and Grobben (Gen. Sagitta s.str. Quoy and Gaimard, Zonosagitta nov., Xerratosagitta Tokioka and Pathansali, Parasagitta nov., Aidanosagitta Tokioka and Pathansali,Mesosagitta nov., Solidosagitta nov., Flaccisagitta nov.). ( b ) Pterosagittidae nov. (Gen. Pterosagitta Costa).

(ii) Flabellodontina. (Hooks are curved rather abruptly and teeth are stouter than in Ctenodontina and arrangedfan-shape.)Pam. Krohnittidae (Gen. Krohnitta). I n all, 5 families, 15 genera and 65 taxa are included in Class Sagittoidea. Of 65 taxa, three are defined as subspecies, one as a variety and three as forma, thus 58 are recognized as species.

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C. Corona ciliatu Regarding external morphology, I shall limit myself to some further remarks about the corona ciliata (ciliary loop). This is an organ that is to be found on the dorsal region of the body, placed either entirely on the head or the neck or--as it occurs in some species where it has an elongated form-extending alm to a large part of the trunk. It has been regarded by Ritter Zahony (1911) as a good systematic feature.

A

C

0

A

B

C

E

D

D

E

F

FIG.4. Variations of the coronu ciliuta in Sugittu.A: normal corona ;B-I?: different shapes of ciliary loops. Above : S. inJlata;below : S. pulchru.

It must, however, be pointed out that it is difficult to observe it in preserved specimens which must be stained for the purpose. The form of the ciliated ring is, moreover, far from constant. I have studcd its variations in 8. inJEata and Sagitta pulchra Doncaster in the Red Sea and IndianOcean (Ghirardelli,1947) (Fig. 4). The ring in the former is placed entirely on the head and may be considered as made up of two distinct parts: a forward roughly trapezoidal part, and a roundish prolongation. The form of the prolongation may vary, as may the forward part of the corona too. This may take in some instances an ovular shape quite similar to the ring in S. hexaptera. Incidentally, this might be another argument in favour of the identity between the two species, about which I wrote above, but they differ, as we said, both in the values given by the proportion of

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total length to length of the tail section, and in the form of the teeth which is quite peculiar in X. hexaptera. The ciliary loop of#. pulchra has an elongated ellipsoid form, it begins before and between the eyes and extends on to the head, the neck and part of the trunk. It may be broken up into several segments, some of which may even be missing so that the ciliary loop might be present only on the trunk (Fig. 4). Several forms of corona ciliata were also observed in S. craSsa (Kado and Hirota, 1957). Its structure and function will be dealt with later (see p, 285).

Fro. 5. Head of Spndellu ccpAuZopteru (living specimen). The ellla are clearly visible; they arc inserted in thc outer corona but directed inwards. c corona: br bristles.

The corona ciliata is a characteristic organof the chaetognathsand was described for the first time by Busch (1851) in the benthic chaetognath Spadella cephaloptera. After Busch, the most important contributions have been those of Hertwig (1880), Grassi (1883), Burfield (1927), John (1933), Reisinger (1934) and Parry (1944). The name “corona ciliata ” appeared for the first time in Grassi’s monograph. which also gave the first exact description of the organ. Grassi (1853) observed that the ciliary loop in 8. cephaloptera seems to be made of two concentrical ellipses, separated by a “dividing line constantly median and parallel with the two edges, so that it seems to be formed by two small crowns opposite and concentric to each other ” (Fig. 5). Grassi had already noted in S. cephaloptera a certain difference between the cells which in a section of the ring appear on the inside and those which are situated towards the outside. The former generally

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have a globe-like shape and are richer in cytoplasm while the latter are smaller and their nuclei are reduced. The “corona ” in Spadella has been re-examined in fuller detail by Reisinger (1934) who, like Grassi, recognized two distinct regions, the inner corona and the outer corona. I n the middle regions, between the two rings of cells, there is a thin annular canal, destined to gather the products of excretion. I n the inner ring there are only glandular cells which have a pear-like shape and whose thinner extremity looks towards the annular canal. The cells of the outer ring are smaller with generally pycnotic nuclei and are provided with vibratile cilia which, according to Reisinger, should have a motor function. The majority of authors believe that the ciliated ring has a sensory function, tactile according to Grassi, John and Parry or olfa,ctory according to Hertwig. John (1933) tested the sensitive reactions of the different parts of the body in Xpadella by directing a small jet of water on to the surface of the animal ; he found that the animal endeavours to shift its position only when the jet is directed on the “corona ciliata ”. Reisinger, previously, considers it to be an excretory organ and comes to this conclusion not only on morphological grounds, but based also on the results of experiments made with vital stains. The ciliary loop would, therefore, in his opinion be an organ similar to a solenocytic protonephridium. More recently he has been modifying some of his conclusions and has confirmed some of my results (Ghirardelli, 1959e). A new work by Reisinger “Ultrastrukturforschung und Evolution ” is to be published in “Physicomedica ” Wurzburg (Reisinger, personal communication). Before concluding, I shall briefly summarize some results of my own researches on the ciliated ring (Ghirardelli, 1958b, 1959e). I n Xpadella cephaloptera the cells of the “corona ciliata ” are certainly of ectodermal origin, like those of the ventral ganglion, from which in the first 2 weeks of life they cannot be distinguished by their morphological characters. Furthermore, in the larvae, for about 15 days, the primordium of the ring and that of the ganglion are intimately connected so that the lateral-posterior regions of the former run without interruptioninto the anterior part of the latter. These anlagen are already present a t hatching : that of the future ventral ganglion shows relative dimensions distinctly larger than in adult animals and has not yet reached its final ventral position but consists of two largc masses of cells placed a t the sides of the body and extending along the whole length of the trunk. Two days later the corona ciliata placed directly beneath the single layered epidermis forms an annularstrip of much thickened cells, except in the inside of the strip where, starting from the fourteenth day a canal appears which runs through it. At

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12 days of age the cells of the "corona ciliata " tend to concentrate on the inner edge, i.e. in the region which in the adult corresponds to the glandular ring; however, they keep their character which is similar to that of the cells of the ganglion. When the gonads begin to mature, i.e. a t about 20-30 days, the loop i s already completely separated from the ventral ganglion which is now in its definitive position. The cells of the outer ring and those of the inner ring begin to differentiate at about 3 weeks of age. The former have nuclei that stain more strongly, similar to those of the cells of the sensory prominences that arc to be found on the epidermis, and are less numerous than the cells on the inner ring (Fig. 7 ) . The nuclei of the latter cells

FIG.(i. Yoirrig Spudcllu cephuloptercr 10 days old-Anlage of corona and ventral ganglion. c corona; c.9. ventral ganglion.

are somewhat larger and vesicular, and already very similar to those of the cells of the inner ring in adult individuals. I n the cytoplasm of these glandular cells, large granules of secretion begin to appear, which can be demonstrated by adequate staining. The above statements show that the ciliary loop and the ventral ganglion have a common origin from ectodermal cells which are also in all ways similar to those of the ectoblast of the gastrula;furthermore, the cells of the glandular inner corona and the sensitive cells of the outer corona arise from the same embryonal cells (Fig. 6). I n adult specimens, the secretion of the corona has the appearance of large granules which are inside the glandular cells and smaller granules outside the corona, generally to be found beneath the cuticle of the epidermis. This secretion stains by the methods most commonly used for neurosecretion, Gomori Bargmann, paraldehyde fuchsin ; it is furthermore MacManus positive. The periodic acid-Schiff-positivity resists salivary digestion, leading to the presumption that polysac-

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charides are present but not glycogen ;the common origin of the corona and ventral ganglion makes it not so surprising that the glandular part of the ciliary loop elaborates a product that presents some characteristics of a neurosecretion. Great caution is, however, advisable in extending to chaetognaths conclusions deriving from researches carried out with methods used on animals often quite far removed on the zoological scale (Ghirardelli, 195813). Gabe (1966) also states that the cells of the inner corona are of ectodermal origin, but they do not possess any of the morphological characters of neurons. They could still be considered as glandular and not neuroglandular. The staining affinities cannot be regarded as proving the neurosecretory nature of the product of the corona ciliata ”. The finely granularsecretion of the corona spreads and distributes itself on the cuticle or is interposed with the thinnest cuticular plates on the surface of the body, generally along the median dorsal line. Tt, finally gathers quite abundantly near the female genital orifices and directly inside them. The regions that are richer in grains, i.e. the corona and the region of the genital orifices up to the seminal receptscles, when observed through the fluorescence microscope, show the same yellow-green fluorescence which is peculiar to flavins. The distribution and diffusion of the grains coincides remarkably, as we shall see later, with the course followed by the spermatozoa after copulation. The coincidence of the two paths may then lead t o the idea that in Xpadella the grains of secretion may perhaps have some function in regulating the migration of the spermatozoa (see p. 324). My observations practically confirm Reisinger’s description as regards the outer and inner rings. Some doubts, however, remain about the real existence of the annular canal as a persistent formation. Actually the features seen by Reisinger and by myself could be due t o a series of vacuoli more or less empty or full according to the physiological condition of the individual, rather than to the presence of a continuous and persisting canal. Still less proved is the excretory function of the ciliated crown : it has no relation to the coelom, since it is an organ completely situated on the epidermis in the region of the neck, partially in that peculiar differentiation of the epidermis called the collarette (lateral areas of the epidermis according to Grassi) which has no relation even with the underlying musculature. The ring is so superficial that it can easily be isolated from the body by mechanical means, especially in Spaddla. Moreover, in Sagitla it is rather difficult for it to be preserved in its entirety in specimens captured by plankton nets. The least friction is ((

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enough to carry off even large portions of the ciliary loop. It is, furthermore, certainly not a fact in support of the supposed excretory functions that in reared specimens of Xpadella the ring sooner or later begins degenerating without causing the death of the animal ; beheaded Xpadella deprived also of their corona survive for several weeks. This shows that the ciliary loop is not essential for excretion, unless its functions are duplicated by other glandular structures, which in Spadella a t least, have a quite different morphological aspect and in some cases even well identifiable functions, as is the case of the adhesive glands or of the ciliated sensory tactile bodies. The beheaded specimens can survive because in them sensitivity is supplied by the ventral ganglion and by the aforementioned sensory formations of the epidermis, and because probably the material contained in the ovaries and in the intestinal walls may constitute an effective alimentary reserve. The corona ciliata has also glandular functions, as we have seen, but these are secretory and Reisinger himself has pointed out the presence of a secretion within the glandular cells of the ring. The structureof the corona, its origin, the rich innervation and the presence of cilia, seem t o confirm the hypothesis that it may have sensory purposes (Ghirardelli, 1958b); nevertheless Horridge and Boulton (1967) state that the electron microscope does not reveal the cells of the ciliary loop as nerve cells. It is then clear that it would be very useful on all grounds that the corona in Xpadella be studied again. As t o the opinion that the corona might be a phylogenetic precursor of a solenocytic protonephridium, Hyman (1959) finds this idea rather difficult to accept. Actually "as the invertebrate Deuterostomia do not have protonephridia, this would mean that Chaetognathaare looking a long way forward t o Amphioxus ". I n few other chaetognaths has the corona been studied histologically. I n Pterosagitta draco which is a bathypelagic species, the epidermis shows features quite similar to, even if more remarkablethan, those found in Spadella cephaloptera. Here too the lateral expansions of the epidermis are well developed and are constituted by typical vacuolized cells. The "corona ciliata "in Pterosagitta is partially sunk into the epidermis, as in Xpadella, and is likewise formed by two concentric strips or bands. I n sections, the two regions of the corona, though clearly recognizable, do not show constant differentiations. The cells are always disposed in such a way as to form a sort of groove whose margins may bend on themselves towards the inside, that is one towards the other. Often only the outer edge bends, so that the cells of the outer ring assume a disposition similar to a horse-shoe with the

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concavity facing the inner ring. At least two layers of cells usually form the outer ring; a similar disposition may not be present in the inner ring, which might be formed by one layer only. The inner ring is consequently less developed, and this is quite the contrary of what one may see in Spadella. This disposition is, however, not a constant one: it may vary even in the same corona, where a t some points the margins may be bent and not a t others. There is no clear separation, in Pterosagitta draco, between the inner and the outer ring. One can only say that the nuclei of the cells of the middle line, which is interposed between the two concentric rings, lie somewhat deeper than the nuclei of the lateral portions. All the cells of the corona

FIG.7. A: section of the corona ciliata of Spadelln cephaloptern.

Two types of cells can be clearly distinguished : those with a more strongly stained nucleus are ciliated cells C.C. (outer corona). the others are glandular cells g.c. (inner corona). B: corona of Sagitta bipunctata. There is no differentiation of cells; the section of the anular canal is clearly visible a.c.

are flask-shaped and oriented towards the middle line where some cytoplasmic formations can occasionally be seen near the surface of the body, looking like vacuoli. There is no difference-that may a t least be perceived through the usual means of research-between the nuclei of the inner and the outer rings : both are elongated, oriented towards the middle line and strongly pycnotic. There is no hint of a differentiation between nervous and glandular cells, as has been observed in Spudella. The corona ciliata of Pterosagitta seems t o consist of the nervous part only. It may have therefore in this chaetognath a purely sensory purpose (Ghirardelli, 1959e). Sagitta bipunctata has a very elongated corona ciliata which extends from the head on to the neck and part of the trunk : after vital staining the two strips of which it is composed become apparent. Histologically, the picture is similar to the one described for Pterosagitta (Fig. 7 ) . The nuclei of the cells of the various regions of the ciliary loop do not show noteworthy differences, all being more or less pycnotic and 10'

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similar to those of the sensory prominences. Also in Xayitta bipunctata the cells of the ring form a sort of groove as described in Pterosagitta and here it is often the inner edge that folds in such a manner that the cells of the inner ring end by being more numerous than those of the outer ring. The disposition is, however, not constant in this species either and the aspect of the inner and outer corona may vary in the same animal. All the cells of the corona have one part richer in cytoplasm inclining towards the middlc line where a vacuole may almost always be observed. It is probable that contiguous vacuoli contribute to form that sort of annular canal which Reisinger has described in Xpadella ; in Sugitta bipunctata it does not seem to be a continuous formation. X. bipunctata also lacks a well-differentiated glandular portion of the corona, since all cells have a sensory character (Ghirardelli, 1959e). The ciliary loop of X. in$ata is placed entirely on the head and has two lateral lobes that are generally well marked. I n this species, in contrast t o what has been found in X. bipunctata and Xpadella mentioned above, I have observed that there are now and then some differences between the inner and the outer ring. I n the majority of cases the two regions of the ciliated ring are exactly similar to each other, and so is the horse-shoe disposition of the cells and the usually pycnotic nuclei, but in some specimens only the cells of the outer ring have pycnotic nuclei and are certainly provided with cilia, while the nuclei of the inner ring cells are more voluminous and roundish and have a very evident chromatic reticule. They remind one of the inner corona cells in Xpadella, but they never show in their cytoplasm those characters of glandular elements which are so apparent in Spadella. It has not been possible as yet to ascertainwhether the two different sorts of cells may be connected with the physiological condition or the age of the specimens considered (Ghirardelli, 1959e). It would seem that in the pelagic chaetognaths the ciliary loop has different features from those found in the benthic form Xpadella cephaloptera. Actually in all the pelagic species considered up t o now (Pterosagitta draco, Xagitta bipunctuta, X. i7;jZata) the glandular part of the corona is indeed missing. Summing up, one may state that in pelagic chaetognathsthe ciliated ring is made up of cells that have all more or less the characters of the sensory elements of the tactile prominences or of the portion of the corona in Spadella which is deemed t o be sensitive. These cells are also distinguishable, apart from the character of their nuclei, by the presence of cilia. As far as pelagic chaetognaths are concerned, the question whether the corona is a secretory organ or a sense organ does

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not arise because of t h e absence of apparent glandular cells. What specific sensory activities are carried out b y t h e corona ciliata and whether i t serves other purposes too, are, as we have seen, open questions a n d difficult t o solve, owing especially t o the habitat of planktonic chaetognaths a n d the difficulties t h a t have t o be met in growing them or at least in keeping them in suitable experimental conditions for a long enough time t o carry out significant experiments. 111. REPROUUCTJON There are not many works of a morphological character on tho gonads and the biology of reproduction in chaetognaths, i.e. works dealing with the deposition of eggs and their ripening, a n d with peculiar cariologic a n d cytological problems, as for instance the question of the germ cells determinant and the origin of the germ line. I n historical sequence, the following works may be quoted : Butschli (1873), Hertwig (1880), Grassi (1881, 1583), Bolles-Lee (1888), Doncaster (1902), Stevens (1903, 1905, 1910), Elpatiewsky (1909, 1910, 1913, 1914), Buchner (1910a,b), Bord&s (1912, 1914, 1920), Kramp (1917), Huntsman and Reid (1921), Vasiljev (1925), Burfield (1927), Tuzet (1931), Russell (1932a,b),J o h n ji933, 1943), Sanzo (1937), Kuhl (1938), Kuhl a n d Kuhl (1965), Ussing (1938), Jagersten (1940)~Dunbar (1941, 1962), Thomson (1947), Pierce (1951), Tchindonova (1955), David (1955, 1958a,b, 1965), Furnestin (1958), Colman (1959), Murakanii (1959), Hirota (1959, 1961), Elian (1960), Owre (1960), Ghirardelli and Brandi (1961), Alvariiio (1965), Ghirardelli and Arnaud (1966), Dallot (1966), MacLaren (1966), Stone (1966) and Ghirardelli (1951, 1953a,c,d,e, 1954a,b,c,d, 1955, 1956a,b, 1959b,c,d, 1960, 1961a,b,c, 1962, 1963a,c, 1966a,b). Some of these, like Grassi’s large monographs, have already become classics, b u t notwithstanding their great value they must be considered cs obsdeto in some respects ; other works like those b y Stevens make a useful contribution. A larger number of them, however, are confined t o some particular problem, which often, as we shall see later, appears t o be far from solution. On the other hand, the researches which are being carried out for ecological purposes in all the seas of the world on the distribution of these organisms, and also on the periods of their sexual maturity, may certainly profit from a deeper knowledge of the morphological and biological facts concerning their reproduction.

A. The malP genital apparatus The chaetogmths are hermaphrodite; the male gonads are in the tail section, while the female ones are in the posterior part of the trunk,

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just in front of the septum that divides the trunk region from the tail. The male reproductive apparatus completely occupies the coelom of the caudal segment, except in Xaqitta inflata, and is separated from the trunk by a transverse septum (Fig. 1). It is formed by the testes, vas deferens and seminal vesicles, paired structures symmetrically disposed along a longitudinal septum that divides the caudal coelom in half. This septum is composed of a homogeneousmedian plate (lamina), covered on both faces by a cubic epithelium which is probably ciliated (Burfield, 1927). The anterior ventral part of the septum divides t o form a triangular space in which the anal orifice is situated. In the upper part the longitudinal septum is connected to the transverse septum ;the two chambers into which the coelom is divided, and which look more or less like pyramids, are further divided into two by two secondary longitudinal septa. These latter are extremely thin and do not show any peculiar structure except in the ventral and dorsal lines where some nuclei can be seen. Each of these septa is attached on the anterior side t o the inner wall of the body, a little behind the caudal septum. On the back, the secondary septum ends a t the level of the seminal vesicles. I n this way the subdivision of each half of the coelom cavity is not complete and both in the anterior and in the posterior part the materials contained in the coelom can circulate freely (Fig. 1). Each of the two chambers into which the coelom is divided is partially occupied by a testis: a more or less solid body, rather flattened, situated in the anterior part of the chamber, attached to the wall in the region of the lateral area and ventral longitudinal muscle. I n side view, the testis appears as a thin band extending from the transverse septum to about one-half of the tail length. Each testis is covered by a thin endothelial layer. From the testes, groups of spermatogonia continuously depart and they continue their development while floating in the liquid which fills the coelomic cavity. Masses of elements all in the same stage of development (polyplasts of Bolles-Lee or sperm morulae) or very nearly in the same stages (Bordks, 1914; Ghirardelli and Arnaud, 1966) are so formed. According to Stevens, however, different stages of spermatogenesis can also co-exist in the same mass. The masses are constantly moving and in each of the two chambers in which the caudal coelom is divided, they move in the following manner: from the posterior end of the coelom they move up along the external wall until they reach the caudal septum ; they then pass through the opening in the secondary longitudinal septum and move towards the tail passing between the secondary and the median septa. Their movement is more or less rapid depending on the species and the degree of fullness of the coelom. In

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Spadella it is always slower than in Sagitta bipunctata and related species. According to BordAs (1912, 1914) the polyplasts are incompletely separated from each other by the walls and trabeculae of a kind of net present in the testicular space. Observations in vivo do not, however, show this testicular net, but histological sections do; it seems to be due to coagulation and precipitation of the liquids which fill the cavity of the tail coelom. Much has been said about the causes of the movements of the polyplasts. Some workers believe it to be due to the ciliated cells that cover the median septum (Burfield, 1927) while for BordAs the movement of the germinal elements is simply due to the tail action of mature spermatozoa. But this explanation is hardly satisfactory, since the movement of the spermatocytes can also be seen when adult spermatozoa are absent. An important part in causing the phenomenon could also be played by the ciliation a t the mouth of the vasa deferentia. I n order to come out into the open, mature spermatozoa pass through a thin canal which opens into the caudal coelom by a ciliated funnelwhich Goodrich (1945) considered to be a propcr coelomostoma. These ducts run without noteworthy turns or convolutions within the body wall and open into the front end of the seminal vesicles. These vesicles have quite different forms according to the spccies and their degree of fullness and arc situated on the lateral areas of the body between the ends of the posterior lateral fins and the fore part of the caudal fin. They are covered by epidermis and their opening shows some quite peculiar features, particularly evident in Sagittu injata and S. serratodentata. They are generally structures of a chitinous appearance in the form of a cup, more or less reticulated (8.inflata) or with finely toothed edges (8.bipunctata and S . serratodentata pac4fica) which in some species have a systematic value (Kulh, 1938 ; Jagersten, 1940 ; Thomson, 1947; Tokioka, 1939b, 1942 ; Ghirardelli, 1950a ; Furnestin, 1957) and probably in some pelagic species are for attachingthe spcrmatophores to the body during mating (Ghirardelli, 1959c,d). (p. 333). I n S. injluta one must furtherremember the differences in the male reproductive apparatus. I n this species, the male germinal elements in the various stages of maturity are not more or less uniformly diffused in the whole trunk coelom, but they are confined to two almost ovoidal areas nearby the tail. This species then shows in the reproductive apparatus some differences from the other species of the genus Sugitta, which for purposes of classification are perhaps more important than the differences in the number and disposition of the fins.

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B. Thefemale reproductive apparatus. General The first detailed description of the morphology of the female reproductive apparatus in chaetognaths was given by Grassi in 1883. Earlier observations by Butschli (1873, Hertwig (1880) and Crassi himself (1881) are only short notes. Hertwig, by the way, argued mistakenly that the germinal epithelium had a syncytial nature and that the so-called oospermaduct is situated outside the ovary. According to the description by Grassi (1883), which pre-eminently refers to the genera Xagitta and Xpadella, the female reproductive organs in Chaetognatha are formed by two cylindrical ovaries placed in the trunk coelom before the caudal septum, one a t the right and one a t the left of the intestine. I n young specimens they occupy a small part of the lateral posterior coelom of the trunk. The germinal epithelium of the ovary, still according to Grassi, appears in transverse sectioiis as a “lobed crown ”in which four parts can be distinguished : one outer part corresponding to the attachment line on the body wall, one inner towards the intestine, one dorsal and lastly a ventral part. These parts can be distinguished by the different forms of their cellular elements. Oocytes still far from maturity have a kind of peduncle which, according to Grassi, consists of an inflated cell. The ovary is enclosed in an involucre consisting of a layer of polygonal cells, reinforced on the inner surface by a thin layer of fibrils from which transverse sepiments arise directed towards the inside. From the anterior end of the ovary a fibrous ligament arises, ending a t the level of the ventral ganglion ; another short fibrous ligament connects the posterior end of the ovary t o the transverse septum near t o the anus. On each ovary, in proximity to the line of attachmentto the body wall, runs the “oospermaduct ”, a thin canal so called by Grassi because (‘it carries the sperm to the eggs and the eggs to the outside, but it also has functions of a spermatheca ”. As regards this structure, there are the greatest differences of opinion among several authors. Krohn (1853), Leuckart and Pagenstecher (1858) had described it as a sperm pouch (Xamentasche). Keferstein (1862) believed it to be an oviduct, Wilms (1844) an excretory duct, and Huxley (1852) considered it t o be a ciliated canal. Still according to Grassi, the lumen of the sperm-oviduct varies in relation to the quantity of spermatozoa contained in it, and its wall is composed of a single layer of cells. Stevens (1910) and Elpatiewsky (1913), on the other hand, describe two layers of cells of which the inner one is a syncytium. Stevens has described the ‘(lobed crown ” of Grassi as formed by two layers of

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epithelial cells disposed in a sort of half-moon with its concavity facing towards the intestine. I n the middle of the half-moon the two epithelial layers diverge from each other and a small canal runs through the tubular space so formed, the wall of which has a syncytial character. This canal is the sperm-oviduct of Grassi. I n the concavity of the half-moon, the oocytes are inserted by means of a sort of peduncle made of two cells peculiarly differentiated : the lower club-shaped cell penetrates with its end among the cylindrical cells of the seminal receptacle. The upper kidney-shaped cell rests with its concave part on the convex one of the lower cell and is in strict connexion with the egg : it even seems partially immersed in its cytoplasm (Buchner, 1910a,b). The purpose of these cells is to allow the passage of the spermatozoon from the seminal pouch to the oocyte. The penetration of the spermatozoon into the egg cell occurs, therefore, while the oocyte is still in the ovary. When the sperm has penetrated, emission of the first polar body occurs. Immediately there follows thc second maturity division with the emission of the second polar body. Ruchner believes that the innermost cell penetrates into the egg together with the spermatozoon and that from it the germ cell determinant originates, but we shall deal with this later. 1. The female reproductive apparatus in Sagitta

The researches I have been able t o carry out on material coming from the gulf of Naples and the Bay of Villefranche have enabled me to confirm to a great extent the results of the works of earlier authors, especially of Stevens, and to correct some mistakes found in other works concerning the anatomy of the female genital apparatus in chaetognaths and particularly in Xagitta which is the genus which was more widely studied. Stevens mostly studied Sagitta elegans Verrill and X . bipunctata. I have had the opportunity also of observing, besides the latter species, S. in$ata and Xagitta minim,a Grassi. Each ovary and seminal pouch is covered by a thin endothelium which is continuous with the lining of the general cavity of the body in the region of the lateral line. It is difficult to see this membrane in section, and in any case it can be observed better in life with the phase contrast microscope. Thus each ovary is attached to the body wall laterally by means of a thin mesentery. Anteriorly the mesentery forms a triangularlamina which ends at the level of the ventral ganglion. The ovary appears t o be formed by a mass of oocytes in various stages of development and by support cells. Those oocytes which are in a more advanced stage of vitellogenesis are placed in the middle, i.e. close to that side of the ovary facing the intestine. The less developed oocytes,

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that are also the smallest, are situated nearer the external side of the ovary along which there is the germinal epithelium. On the outside of the ovary the seminal receptacle can also be seen; when empty this takes thc form of a small thin canal running along the ovary for its whole length parallel with the lateral lines of the body and opening into a raised papilla placed on thc lateral lines

FIG.8. A: longitudinal diagrammatic section of the ovary in Sagitta. B: transverse section. The two sections are not equally enlarged. e p rrescent-shaped epithelium supporting the seminal pouch: oc oorytes; s syncytial wall of the seminal pouch; sp spermatozoa in the seminal pouch; g.0. genital opening; i intestine. (From Ghirardelli, 1959.)

themselves, a little in front of the caudal septum ; anteriorly the small canal normally ends somewhat before the cephalic end of the ovary. The lumen of this canal is more or less filled with spermatozoa that appear in continuous movement ; depending on the more or less filled condition, its lumen shows irregular thickening of variable calibre. This canal really only serves as a spermatheca since large quantities of spermatozoa mass in i t (Fig. 8). For the laying of the eggs, a t the moment of their emission to the outside, another canal is formed which, though it has very strict topographical connexions with the seminal

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receptacle, is nevertheless quite distinct from it. It is present only a t the moment of the laying and therefore it has been called a temporary oviduct (Stevens, 1910). Thc seminal receptacle is closed anteriorly contrary to what Bordis (1920) affirmed ; posteriorly it turns a t a right angle towards the outside and forms the vagina which opens into the external genital papilla. The papilla is formed by a few cells which constitute a sort of small cupola; they continue towards the inside of the body in two layers. To the inner one there follows the syncytium which lines the seminal pouch. Several elongated

FIG.9. A: transverse section of the ovary of S. inflata. The seminal pouch, with its inner syncytial wall s is clearly visible. B: transverse section of the ovary of S. bipunctata. Besides the seminal pouch with the two walls, epithelial and syncytial, the crescent-shaped supporting structure can be seen. Within tho nucleus of the larger oocyte, the lamp-brush chromosonics are discernible. me mesentery, ms musculature of the body, the other letters as in Fig. 8. The two sections are drawn t o the ssme magnification.

and fusiform elements may be noted, which form a sort of sphincter closing the orifice of the seminal receptacle ; this orifice is not used in the emission of the eggs. The relations between oogonia, oocytes and support formations can be clearly seen in transverse sections. In these the most obvious formatioii is the structure that Bordis in S. bipunctata rightly compared to the samara of the maple. It is, as we already said, a sort of crescent moon whose concavity is turned medially (Fig. 9), formed by a double layer of epithelial cylindrical cells which become taller towards the ends so that they become club-like; the cells nearer to the body wall are generally taller than the ones nearer the intestine. I n the central portion the two layers separate so that a space is formed into which

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the seminal pouch is placed whose wall is of a syncytial nature. Between the syncytium and the epithelium a structureless layer is clearly visible. I n the concavity of the central portion of the crescent arc the oocytes, and it is possible to observe all the aspects of the meiotic prophase as well as the several moments of auxocytosis. BordAs believes that the crescent cells have a trophic function for the oocytes, and affirms that these cells take the place of those of the germinal epithelium as they evolve. This idea, however, does not seem acceptable to me, since forms of transition between nuclei of epithelial cells and of thc germinal cells are never seen, and furthermore the cells which constitute the crescent have a different embryonic origin (Doncaster, 1902; Stevens, 1910). I have not carried out thorough researches on this material ; I could, however, see that in Spadella one can discern at very early stages the germinal cells and those of the supporting elements. According to Stevens (1910) and BordAs (1920) there exist in the cells of the oviduct wall some contractile differentiations the nature of which has not been ascertained. Vasiljev (1925), who studied the ovary of Xpadella, believes the supposed differentiation to be the effect of staining. BordAs (1920) said he also noted a net made of amorphous elastic lengths, which being attached to the endothelial cells should constitute the so-called ovarian net whose purpose would be to support the eggs and protect them until their development was complete. I have never been able to see in my own preparations anything similar to the ovarian net, and I think that it is probably an artifact. I n transverse sections one may observe that the mesentery connecting the ovary to the body wall along the lateral line is formed by two layers which are a continuation of the thin membrane that wraps the ovary. When they come in contact with the body walls, the layers separate and line the coelom cavity ; then they continue and form the mesenteries that support the intestine. Near the opening of the genital orifice the mesenteries are no longer visible and the ovary seems to be directly inserted into the body wall. Contrary to what BordAs (1914) saw, no communicationbetween the coelom of the caudal region, where the testes are placed, and the trunk coelom, where the ovaries are, can be observed either in longitudinal or transverse sections or in vivo. We must therefore exclude the possibility that the filling of the seminal pouch may be due to the direct passage of the spermatozoa from the coelom of the tail to the ovary. I n the same species the seminal pouch, when full of spermatozoa though showing a certain variability, tends to take similar forms. I n

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Xagitta lyra, for instance, the fore end has the form of the bull) of the thermometer (Grassi, 1883). The same occurs in 8. inJlata,while in 8. bipunctata the seminal pouch shows irregular thickenings along its whole extension. I n Xagitta decipiens Fowler it is club-shaped. Also the supporting formation shows some difference, in S . inJtata for instance, it is only approximately crescent-shaped. The epithelial cells around the lumen of the pouch do not show two layers as in other species of Xagitta but are placed like rays around the lumen of the seminal pouch. Dorsally and ventrally to the pouch, the cells display their maximum length. They are club-like cells with the more enlarged end orientated towards the median region of the body ; the nucleus is also placed towards this end (Fig. 9). I n the median region of the pouch, the cells are instead lower though still presenting the clubshaped form. I n X. bipunctata in the median region of the crescent the epithelium from being cylindrical becomes cubic and this is particularly apparent in the illustrations (Fig. 9). On the external side of the pouch, i.e. on the side toward the body wall, both in S. bipunctata and in S. inJlatathe syncytium is lined with rather flat cells. 2. The accessoryfertilization cells I n order to complete the description of the reproductive apparatus in Xagitta, mention must be made of the so-called accessory fertilization cells. These have been called by different names: “picciuolo ” (stem) by Grassi (1883) in Xagitta and Spadella, “Aufhangenapparat” (Buchner 1910a),“Strangzellen”(Buchner,1910b) in Xagitta, “accessory fertilization cells” (Stevens, 1910)inXagitta, “Zweizellenapparat”(Elpatiewsky, 1913) in Xagitta, “appareil pluricellulaire”, “appareil de suspension” (Vasiljev, 1925)inSpadella, “aparatomicropilar ”,“celulassospensoras” (BordBs, 1920) in Sagitta. Some of these terms give a clear idea of the purpose of these cells, which is to connect the eggs to the seminal pouch ensuring at the same time the passage of the spermatozoon from the scminal pouch to the egg. The suspension apparatusis one of the most peculiar structures in Chaetognatha, which are themselves peculiar organisms. As we have already seen, Grassi believed the suspension apparatus to be made of one cell only in Xagitta while being multicellular in Xpadelln. Buchner and Stevens have accurately described the suspension apparatus in Xagitta and Vasiljev has done so in Xpndella. I n Sagitta bipunctata and in Xpadelln cephalopteraI have been able to confirm that the suspension apparatus consists of two cells of which the lower one is

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shaped like a thick club with a sharpened end and penetrates among the cubic cells of the epithelium of the inner side of the seminal pouch (Fig. 10) ; this cell often goes through the epithelium and juts out, at its thinnest part, over the basement membrane (Elpatiewsky, 1913 ; Ghirardelli. 1959d). This cell is provided with a very thick nucleus, with an evident nucleolus ; it is attached to a second kidney-shaped cell with the concavity in contact with the convexity of the lower cell. Its nucleus is similar to that of the other cell; the volume of these two

FIG.10. Suspension cells of Sagitta bipunctata: S.C. 7 uppcr cell inscrted into the oocyte oc; S.C. 2 lower cell. One can see tho vacuoli in the first and also in the second cell which is in contact with the basement membrane. ep epithelial wall of the pouch; sp spermatozoa in the seminal pouch; s syncytial wall of the pouch; b.m. basement membrane between epithelial and syncytial wall.

elements is much greater than that of the other cells of the ovarian epithelium, that is of thc cells of the moon crescent. Around the lower cell, a crown of smaller cells can be seen, whose nuclei are elongated in the direction of their longer axes. These cells can be compared to so many wedges placed around the lower cell of the suspension apparatus,as if to support it and better fix it in its place. BordAs (1920) ment,ionsone case in which the fertilization apparatus was made up of four cells almost equal in dimensions ; the micropilar apparatuswas present only in two of them. This micropilar apparatus should be a small canal passing through two cells and allowing the spermatozoon to pass from the seminal pouch to the egg. Buchner (1910b) was unable to make it evident, and actually this seems to be difficult. On examining my material and the numerous photographs I

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have been able to take, I feel some doubt as to the existence of this canal as a persistent structure, and especially on its being spiral shaped as some authors would have it, particularly Stevens and BordAs according to whom the small canal always remains of the same calibre. One rather has the impression that instead of a small canal there are a series of vacuoli, or a t least of particular states of the cytoplasm of the suspension cells that may show a lesser density. This does not exclude the possibility that a t certain moments and in limited areas of the cytoplasm of the support cells some cavities might form more or less in line, producing a canal-like structure. Cytoplasmic lacunae and vacuoli

FIG.11. From the left, some aspects of development of the suspension cells in Sagitta bipunctata. The arrow indicates a fully developed suspcnsion apparatus.

inside the cells, would be quite sufficient to allow the spermatozoon to pass through the two cells and penetrate the egg. At its point of contact with the second cell, the vitelline membrane of the egg is interrupted and forms a sort of micropile closed by the cell itself. Often in Sagitta and still more often in S p d e l l u the contents of the cell attachedt o the pouch seem almost to pour into the seminal pouch. At the point where this happens, one can see the spermatozoon in the act of penetrating the oocyte. The material contained in the vacuoli of the fecundation cells could therefore have the function of attractingthe sperm inside the accessory cells through which it would be led towards the egg. Such a fertilization process is, however, quite peculiar. The eggs connect with the fertilization apparatusonly during the second period of growth ; the smallest oocytes are simply in contact with the epithelium of the crescent of the seminal pouch. Figure 11 is particularly clear in this respect : small aocytes can be seen touching

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the cells of the cubic epithelium which has not yet differentiated; on the left side of the same figure are two oocytes, the smallest of which is connected with a cell that can easily be recognized as belonging to the cubic epithelium ;in the larger oocyte the process of transformation is still evident. Proceeding from the smallest oocyte a t the right side to the largest, one can observe different stages of the process through which the apparatusof fertilization is developed ; this apparatus may reasonably be considered as deriving from the cells of the crescent. I n Sagitta minima the structure of the fertilization apparatus seems to be a little more complex as there appear t o be a number of fertilization cells greater than those in 8. bipunctata. As to the support cells after fertilization, all workers agree that they degenerate. Opinions differ as to the point in the ovary where the second accessory cell degenerates. Buchner (lSlOb), Bordks (1920) and Stevens (1903) herself, believed that this cell degenerates in the ovular cytoplasm ; later Stevens (1910) and Vasiljev (1925) ruled this out. It happens sometimes that the nucleus of this cell is seen to have a pycnotic character that might be a sign of degeneration, but it has never been possible to observe further stages of the degenerative process. Though I feel rather inclined to think that tile second accessory cell does not degenerate inside the egg as some believe, the matter has some importance also for the question of the origin of the germ cell determinant : Buchner deemed that it derives from the degenerationof the fertilization accessory cell in contact with the egg. 3. Thkfemale reproductive apparatus in Spadella

Only Grassi (1883) and more recently Vasiljev (1925) and John (1933) have done adequate research on the anatomy of the female gonad in Spadella. As in Xagitta, so in Xpadella the ovaries are placed in the coelom of the trunk, directly before the caudal septum. They are generally 1 mm long but in spring may become longer, their cephalic extremity reaching the region of the neck a t the level of the ciliary loop. They are wrapped in a thin endothelium which connects them with the walls of the body. Each ovary contains a few dozen eggs of which a variable quantity has attained the maximum size. During summer the two ovaries contain about ten mature eggs, but in springtime there may be more than twenty, while in autumn they decrease to two or even one only in each ovary. We shall return t o this point when dealing with sexual maturity (p. 349). I n the median and posterior region, one normally finds the oocytes in the first periods of growth mixed with those which have completed

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30 I

their growth. I n the fore part there are often younger oocytes and also oogonia. Frontal and sagittal sections of the ovary confirm the disposition of the eggs as outlined above :anteriorly one sees the oogonia and the smaller oocytes in different stages of the meiotic prophase; towards the median region, the larger oocytes can be seen. The latter may be in their last period of growth, i.e. at the end of vitellogenesis, and clearly show the lampbrush chromosomes. Around the nucleus there are little plates or granules which form the so-called nuclear net, which is not constituted by chromatinic substance since it does not stain by the Feulgen reaction but by pyroninophilous material : we shall revert to this when dealing with the growth of oocytes (p. 312). Frontal sections are particularly suited for studying the inetaphase : it is indeed not difficult to observe the typical spindle of maturation with parallel fibres, first oriented parallel with the ovular membrane and then perpendicular to it. On the spindle the nine bivalents can easily be seen (Fig. 32). Sometimes, owing to the large dimensions of the eggs, the intestine in the region between the two ovaries has an S-bend. The ovary, as I have said, is wrapped in a thin membrane made of flat cells whose nuclei are also quite flat and strongly stainable. The membrane is tightly pressed against the body wall; in the fore part it is attached t o the lateral line by means of a thin mesentery, posteriorly it is in contact with the seminal receptacle. The ovary is further attached t o the body wall in the angle the latter forms with the caudal septum. Ventral to the ovary one sees the seminal pouch,which runsas a small canal not so long as the ovary: its anterior end is blind and is continued posteriorly into the seminal receptacle. I n the longitudinal sections it is possible to see the eggs inserted along the seminal pouch,by means of the accessory fertilization cells (Fig.12). The typical moon crescent described in Xagitta is absent. The upper wall of the seminal pouch is only somewhat enlarged and on its epithelium the eggs are inserted. Transverse sections show it sometimes as a circular and sometimes as a triangular shaped lumen: this is certainly dependent on the extent t o which it fills the pouch, and when it is strongly pressed by the mature eggs and there are not many sperms in it, its lumen even becomes virtual. The walls of the seminal pouch are made of the usual layers of cells already described when dealing with Xagitta. The outer layer is a cylindrical epithelium which is lower in the region where the seminal pouch is connected with the ovary. The nuclei of the epithelium cells are large and vesicular, ovoid, and with a generally evident nucleolus. The inner layer is syncytial with scattered nuclei generally elongated

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FIG.12. Longitudinal section of the body of Spadella cephaloptero passing through an ovary. s.p. seminal pouch; s.r. seminal receptacle full of spermatozoa. The larger oocytes are connccted t o the scrninal pouch by the fertilization cells. Among the large oocytes thero are others still in earlier stages of development. w.g. ventral ganglion.

and strongly stainable. Between the epithelial and syncytial layers a thin structureless membrane is clearly discernible. The homology between the walls of the seminal pouch of Spadella and the walls of the seminal pouch plus the whole crescent in Xagitfa is evident (Fig. 14). The seminal receptacle in section differs greatly, depending on whether it is full or empty. If empty, its structure does not differ from that of the pouch. If receptacles are full they take a bilobate form or also sometimes irregularly lobate, instead of the usual sphcrical shape (Fig. 12). Their walls are as a result quite distended and they may seem to be made of only one layer of cells. Most probably, however, this aspect of the walls is simply due to the stretching to which they are subject, and which might cause a noteworthy flattening of the epithelial cells that become hardly visible as a consequence. Despite the statement by John (1933), no direct connexion has been observed between seminal receptacle and ovary. From the receptacle, another duct originates which is much shorter than the former one and perpendicular to it and to the body wall. This small duct is the vagina : it opens to the exterior directly in front of the anterior insertion of the lateral fins, in correspondence with the genital papilla. The walls of the vagina are also made of two layers of cells w-hich are, however, quite different from those of the receptacle and seminal pouch. Actually the inner layer is a cylindrical epithelium, rather tall with big vesiculous nuclei placed a t the base of the cell ;while the outer

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Iayer is represented by a thin flat epithelium whose nuclei look somewhat stretched in the direction of the axis of the organ. The opening is, as we have said, in correspondence with the genital papilla which is a prominence constituted pre-eminently of glandular cells filled with a secretion which is strongly eosinophilic. The abundant material a t my disposal has enabled me to make a detailed study of the development of the ovary of Xpadella. Two groups of cellular elements contribute to the formation of the ovary: all the oogonia derive from the first two gonocytes which in the larva

FIG. 13. Transverso soction of the ovary of Spudella cephaloptera 7 days old. One can see the oogonia o anti the epithelial cells ep, which will form the ovary wall, seminal receptacle and seminal pourh. i intestine ; 'm,,smusculature of the body.

are situated in front of the tail septum ; the seminal receptacle, the seminal pouch, the lining of the ovaries and most probably the vagina too, all derive from mesodermal elements (Etevens, 1910 ;Bordhs, 1920). John, on the other hand, considered that the vagina is of ectodermal origin. I n young larvae, about 1 week old, one can see beside the oogonia-which in this stage number about ten-a cluster of cells which have the character of epithelial cells (Fig. 13). This primordium elongates ventrally t o the ovary and in specimens up t o 3 or 4 weeks old it forms, in the future region of the seminal pouch, a cord lined externally by cubic epithelium. The cells of the inner layer are at first rather irregularly disposed but during development a cavity begins to appear in the thickness of the cord, starting in its posterior region, in correspondence with the seminal receptacle, which lengthens toward the head. The lumen of the pouch is a t first surrounded by the same

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cells of the cord which later form the syncytium and which will later completely line the pouch and the receptacle. While the pouch and the seminal receptacle are developing, the oogonia have multiplied and the maturation prophase has begun. The young oocytes at the anterior end of the ovary do not always appear to be in contact with the walls of the seminal pouch ; when, however, they have reached a certain development, one sees that the two cells of the outer epithelial layer of the pouch become more elongated, assuming therefore somewhat larger dimensions than the nearby cells. Their appearance is often like that of a kidney or a bean so that the two cells, one in front of the other, look a little like a stoma of the leaves.

FIG.14. Sagittal section of the ovary. Two nearly ripe oocytes of SpadPlZa cephabptera with their suspension cells, the inner suspension cell engaged in the epithclium (ep) of the seminal pouch (s.P.). A narrow channel from the suspension cell opens into the seminal pouch after going through the syncgtial wall s (arrow).

As development proceeds, these two cells become ovoid, they are much larger than the nearby ones, and a nucleolus is quite evident in their nucleus. They no longer appear side by side as before, but place themselves one behind the other. The outer one sinks into the cytoplasm of the egg a t a point where, the vitelline membrane being lacking, a sort of micropile has formed. The other cell sinks among the cells of the external epithelium of the pouch, which form a cup around it : some rise to about half the lower fertilization cell, others form a circle all around the point of insertion. There is in this way a sort of funnel in which lies the fertilization cell (Fig. 14). The lower cell,

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deeply penetrating the thickness of the wall, often ends by jutting into the lumen of the seminal pouch As development proceeds. the accessory fertilization cells vacuolize and quite probably these vacuoli, commuiiicating with each other, allow the passage of the spermatozoon. When the vacuoli open into the seminal pouch, a plug of coagulable substance forms in correspondence to the insertion of the fertilization apparatus, which is in all respects similar to that observed in Sagitta. This apparatusallows the transit of the spermatozoon from the seminal pouch to the egg. This passage must be very rapid: only on a few occasions have I been able to see the spermatozoon engaged in the vacuoli which pass through the cells. Also in Spadella the fate of the fertilization apparatus after the passage of the spermiuin remains obscure. m'hile in some cases it seems that one cell a t least remains in the egg, in other more numerous cases one can be sure that the biggest oocytes lose any contact with the fecundation cell immediately after the penetration of the spermatozoon. It is confirmed that the fertilization apparatus, contrary to what Vasiljev believed, does not originate from elements of oogonial nature but derives from the epithelium of the pouch.

4. The female reproductive apparatus in Pterosagitta The structure of the female genital apparatus in Pterosagitta (Ghirardelli, 1953e) closely resembles that observed in Sagitta and Xpadella. I n young specimens-in which the eggs have not yet reached full development or the scminal pouches are not completely full-and in the caudal portion of the ovary of mature specimens, a crescent like the one described in Sagitta can be observed. The wings of the crescent are, however, shorter and the cells are irregularly disposed. Around the eggs there is always an abundant secretion of hyaline substance. At the centre of the crescent there is the small canal formed, as usual, by two layers of cells, the outer one epithelial, the one more to the inside syncytial. The ampullae a t the anterior end of each seminal pouch are the most interesting features in the female genital apparatusof Pterosagitta : when they are full of sperms they look in transmitted light like two voluminous ovoidal masses, about 1 mm long, placed on the level of the anterior extremities of the ovary. They are homologous with the anterior end of the seminal pouch in Sagitta and Xpadella, and very similar to the anterior region of the seminal pouch of Xagitta decipiens. They are not homologous with the receptacles of Spadella which correspond to the posterior region of the pouch. The two ampullae of Pterosagitta are always far from the caudal septum, but owing to their

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volume they are almost never a t the same level. As a consequence,the ovaries develop unequally, the one whose ampullae is more cephalic being the longer. The intestine, in the portion between the two ovaries, has a sinuous course because the ampullae, owing to their width, protrude beyond the median line of the body (Fig. 15). I n frontal sections the ampullae show an oval shape and appear placed a t the anterior end of each ovary. I n transverse sections they look circular and the ovary leans on them on the inner side, towards the intestine.

FIG.15. Frontal section of the ovaries of Pterosagittn clrnco with enormous ampullae or seminal receptacles s.r. which cornpress the intestine i ; s.p. seminal pouch.

The ampullae are full of spermatozoa and in the central zone there is a substance easily coagulable. The wdls of the ampullae are extremely distended and look as if made of only one layer of cells ; the nuclei are quite dispersed. This appearance is, however, probably due to the stretching of the walls by which the epithelium is flattened and the syncytium becomes so distended that the two cellular layers cannot be discerned. From the ampullae a canal issues having all the features of the seminal pouch in Spadella and Bagitta, with two cellular layers: syncytium and epithelium. At the posterior end i t opens like a funnel and forms the vagina, whose morphological features are similar to those of Spadella. The lumen of this portion of the seminal pouch remains the same for almost its whole length and is always lined by a syncytium that in Pterosagitta is quite evident. The seminal pouch is normally lateral to the ovary, but it can be more or less dorsally displaced depending on the deformations brought about by the increase in the volume of the receptacles. The inner wall of the vagina has the same structureas that of the inner wall of the seminal pouch. The outer one is formed by a sort of muff of cylindrical cells, amongst which there

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are numerous glandular elements which are filled-at the extremities turned towards the lumen of the tubule-with grains of a secretion which is strongly eosinophilic. Glandular cells are also present on the inner wallof the seminal pouch, so that often among the eggs nearertothe pouch it is possible to observe grains of a secretion quite similar to the ones just mentioned. The vagina opens a t the end of a very apparent papilla, whose walls are formed externally by a cylindrical epithelium which is cleanly separated by a basement membrane from another layer of flat elongated cells which are in turn separated from an innermost layer made of glandular cells only, rich in secretion. The oocytes in Pterosagitta have a somewhat different distribution from the one found in other chaetognaths. I n the region of the vagina the epithelium of the seminal pouch inflects towards the median line forming a sort of cap in which some oocytes are found. These show differences according to their stage of maturity :the younger ones have a large strongly stainable nucleus, with homogeneous cytoplasm, and are regularly intercalated with oocytes in their last stage of growth, whose cytoplasm is filled with yolk. The oocytes nearer to the wall come in contact with the seminal pouch by means of a formation which is similar to the one observed in Spadella and Xagitta. The fertilization apparatuson the whole seems, however, a little more elongated. Also in Pterosagitta, near the principal cells which constitute the fertilization apparatus, others can be observed whose purpose is not always very clear: they serve probably as a support to the accessory fertilization cells. I n frontal sections the ovary shows up to two layers of oocytes in their last stage of growth ; the second layer can come in contact with the walls of the seminal pouch because these eggs have a pear-like shape and a peduncle long enough to penetrate among the oocytes of the inner layer and reach the supporting epithelium. It is, however, probable that these eggs, as soon as they are fertilized, lose their contact with the epithelium. The eggs in each ovary are quite numerous : one may count 100-150 in their last stages of growth. This very large number of eggs may explain the observation made by Sanzo (1937) in the Straits of Messina. This worker found some pelagic ootheca of Pterosagitta draco : each of these ootheca were from 5 to 8 mm in length and from 5 t o 6 mm in breadth and contained from 200 to 300 eggs. Considering that the eggs had a diameter of about 300 p, and comparing them with the measurements of the adult animal, Sanzo believed it was rather unlikely that such a number of eggs could have been laid by one individual. I n my preparations I have found that the dimensions of the eggs ready to be

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laid are somewhat less, about 100-150 p. It cannot be excluded, therefore, that before or after being laid the eggs may enlarge owing to imbibition. It is, however, also possible that the large oocytes do not all ripen a t the same time. I n that case, the high number of eggs contained in each ootheca could also perhaps justify Sanzo’s supposition, i.e. that the ootheca were produced by more than one individual. This fact, however, would be quite remarkable, since P. draco is a rather uncommon species, in the Mediterraneanat least ;it is usually caught singly, a t any rate a t Naples and Villefranche. The gelatine that wraps the eggs is obviously produced by the glands described above and it has the purpose of protecting the eggs, whose development is the same a s that known for the other chaetognaths. The increase in the weight of the gclatine causes the ootheca to sink slowly, protecting the eggs from the effect of the movements of the waves and of the sudden changesin temperature and salinity that may occur in the superficial layers. 5. T h e female reproductive apparatus in Eukrohnia

I owe to the great courtesy of Dr. P. M. David the opportunity of studying some specimens of Eukrohnia bathyantarctica David and of Eukrohnia Lfotc-leriRitter-Zahony. In mature specimens, in frontal sections, the disposition of the parts which constitute the female genital apparatusis quite similar t o that seen in Pterosagitta draco. There are indeed also in this species two very large seminal ampullae ; one in each seminal pouch. The seminal pouch originates from a vagina constituted by the usual two layers of cells; the epithelium shows cubic cells in correspondence to the vagina and tall cells i n the other regions of the pouch. The latter has no uniform calibre : along its course it has one or two widenings full of spermatozoa. At its cephalic end there is a large ampulla about 1 mm long ; the whole length of the pouch plus ampulla may nieasure 2-3 mm. JThen these ampullae are completely full of spermatozoa in their central region they may show masses of sperms more aggregated than in the peripheral portion. The lining of the seminal receptacle seems to consist a t some points of only one layer of cells: this, however, may be accounted for in Eukrohnia as in Pterosagitta through the stretching to which the walls of the pouch are subject. The mature eggs near the time of laying are few and large, and their cytoplasm is full of grains of yolk. The younger eggs show, on t h e contrary, the same features as those known in other chaetognathsand they are inserted on the ovarian epithelium by means of the usual peduncle made of two cells: the nuclei of the latter are only slightly

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stainable, while those of the epithelium, on the contrary, are strongly stainable, elongated and closely massed t o one another. There are no substantial differences between the ovaries of E. bathyantarctica and E. fowleri. The few specimens a t my disposal have not allowed me to obtain transverse sections that may show the supporting structures of the eggs. I am, therefore, unable to state whether they are crescent-shaped or not. I n the male gcnital apparatusthere is one peculiarity which should be mentioned : the particular disposition of the morulac of the germinal elements in various stages of maturation, which tend to aggregate. I n conclusion, the fcmale genital apparatus in Xagitta, Spudella, Pteromgitta and Eukrohnia, although they have the same structural type, show some remarkable differences. It is interesting to observe that some species, which live in deep or cold waters, have seminal pouches with very enlarged ampullae, i.e. Sagitta decipiems, Pterosagitta draco and Eukrohnia bathyantarctica. I n Xagitta injata as we have seen both male and female genital apparatus,but especially the male one, differ considerably from those observed in the other species of Sagitta.

C. Spermatogenesis and oogenesis 1. Xpermatogenesis Spermatogenesis in chaetognaths has been studied mainly by Hertwig (1880), Bolles-Lee (1888), Stevens (1903, 1910) and BordAs (1912, 1914). The subject has been completely neglected since, and only Tuzet (1931) has studied spermiohistogenesis and Ghirardelli (195413) the kariogram of Sagitta inJEata. Spermatogenesis was studied in the past mainly on S. bipunctata. The most detailed work is that by BordBs: nevertheless, this worker also missed some details jn the morphology of the stages of the meiosis. Besides being due to the techniques employed, this was certainly due to the smallness of the elements : actually, the chromosomes do not normally exceed a length of 3 p and in the spermatocytes I1 they are very little over 1 p long. The authors who have dealt with the subject agree in giving eighteen as the diploid number. Eighteen chromosomes were found in 8. bipunctata by Boveri (1890), in X. inJlata by Buchner (191Ob) and Ghirardelli (1954), in X . minima and S. elegans by Stevens (1910). in S. setosa by Arnaud (1963) and in Xpadella cephaloptera by Ghirardelli (1959d). Recently Ghirardelli and Arnaud (1966) have resumed the subject using the squash technique. They have been able to confirm that apart from small differences in some details, meiosis in Xagitta setosa occurs according to the classic scheme. It has been possible to show a

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maximum of two chiasmata for each bivalent and t o demonstrate that their terminalization continues until the metaphase. One pair of chromosomes which Ghirardelli and Arnaud call chromosomes "m " instead of "x "as Stevciis did (and this in order to avoid any confusion with sexual chromosomes) must have their chiasmata in a distal position. This facilitates a rapid terminalization and, as a consequence, leads to a precocious division. It is indeed often possible to observe a t the first metaphase a pair of chromosomes which move to the opposite extremity of the spindle very precociously if compared with the others. They thus seem to show behaviour very similar to that of the sexual chromosomes (Fig. 16). It

FIG.16.

Spermatogonial metaphase of S. in$ata. A chromosome has divided prccociously in all plates.

must be remarked, however, that obviously one cannot properly talk of sexual chromosomes in a hermaphrodite animal such as a chaetognath. On the other hand, this phenomenon of precocious migration of a pair of chromosomes is observed only during spermatogenesis and has not yet been described during oogenesis. It is possible that there are some differences in the kariogram among the different species. Actually Ghirardelli (195413) could distinguish a t the spermatogonialmetaphases five pairs of metacentrical chromosomes in X. in$ata, while in S. setosa the pairs of metacentrical chromosomes seem to be only four (Ghirardelli and Arnaud, 1966). The structure of the sperm has been described by Tuzet (1931). The spermatozoa of Spadella and Sagitta are quite similar to each other and have rather a peculiar appearance. They have a very elongated shape, with a long and thin acrosome a t the base of which there is the anterior

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centriole ; there is an exterior chromatic thread, normally placed laterally to the head of the sperm (which is also quite elongated and thin) connected to the anterior centriole. After acetic fixation, the chromatic thread is no longer applied against the head, and it can have the aspect of an undulating membrane. The middle segment is short by comparison with the length of the head and so is the caudal flagellum. A different description of spermatozoa in chaetognaths was given by Retzius (1909) : after maceration, he observed that around the spermatozoon there were two or even three thin threads. He further wrongly considered as anterior the side which has been later described as posterior. Retzius’ researches have now only a historical value. Jagersten ( 1940) also has remarked that spermatozoa when isolated in water are practically unable to move ;on the contrary, when they are massed together they show lively movements and the masses of sperms can give rise to prolongations in different directions, whose methods of formation have been accurately described by Jagersten. The movements of the masses of spermatozoa undoubtedly have a remarkable importance in fertilization, as we shall see later. 2. Oogenesis and growth of the oocytes

Maturationand growth of the oocytes have been described especially by Stevens (1903) and BordAs (1920) who showed that in an ovary there might be oocytes of various dimensions. A structuralpeculiarity shown by the above authorsis the so-called nuclear net. It is a series of grains and small plaques which can be seen in oocytes in their first period of growth, with a diameter of about 10-15 p, whose nuclei have reached the late pachytene. I n correspondence to the nuclear membrane, one observes some peculiar granulations strongly stainable with ferric haematoxylin and pyroninophilous : they are completely Feulgen negative. These structures seem t o be abundantly supplied with ribonucleoproteins, few polysaccharides and a protein stroma which determines the persistence of stainability with iron haematoxylin and also after hydrolysis with 10% perchloric acid for 24 h at 0°C. Contrary to former belief there is no nucleolus in the eggs of Spadella cephaloptera (Ghirardelliand Brandi, 1961 ; Ghirardelli, 1961b). It is very probable that the functions of the nucleolus are taken by the small plaques of the so-called nuclear net. At the moment that these granulations begin to appear they are certainly on the inside of the nuclear membrane, but later they seem to be within the membrane itself, sometimes giving the impression that they enter into direct contact with the cytoplasm. When they have A.M.B.-6

11

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reached their maximum growth, they flatten t o form small plaques which can be clearly seen in tangential sections of the nucleus; their number increases remarkably during the second period of growth, when the synthesis of the specific ovular proteins is most active and the oocytes have exceeded 30 p in diameter and after the chromosomes at diplotene have taken on their characteristic lampbrush appearance. (Fig. 17) ; According to BordAs the grains are on the outside of the nuclear membrane in the knots of a net-like formation and are equivalent to irregularly shaped kariosomes ; this is, however, contradicted by their negative Feulgen reaction. A relationship has been observed between the quantity of ribonucleic acid (RNA) present in the plaques of the nuclear net and the

FIG.17. Oocyte of Spadella in the 2nd period of growth. Around the nucleus, the small plaques of RNA positive substance. I n the cytoplasm the RNA positive substance is placed in concentric zones. I n the nucleus the lamp-brushchromosorncscan be seen.

RNA in the cytoplasm. In the first and second periods of growth, i.e. when the nuclei are in synaptic stages, in the cytoplasm there is an increase of the materials containing RNA. This material in some cases is distributed in concentric rings around the nucleus. In the third period, i.e. at vitellogenesis, both the cytoplasm and the small plaques show a lesser quantity of RNA. There is, therefore, a course of events in the distribution of the RNA-positive materials in every way similar to that observed in the oocytes of other animals. I n the nuclear net the same process can be observed, as far as RNA-positive material is concerned, as in the nucleoli of other eggs. The greatest concentration of ribonucleoproteins occurs gcnerally in the smaller oocytes placed near the seminal pouch ; this may support the idea of BordAs (1920) that the seminal pouch may have trophic functions, producing substances which may be used by the oocytes. It does not seem, however, that this hypothesis can be extended, as

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BordAs meant, to iiiclude the accessory fertilization cells, because in these the quantity of ribonucleoproteins is aIways very small. As regards the dimensions of oocytes and the general aspect of the ovaries and testes, several classifications of the maturity stages in Chaetognatha have been proposed. Alvariiio (1965) has given an excellent review of them. Ghirardelli (1951, 1961a,c) has established (in Xagitta injlata and 8. cephaloptera) a connexion between the morphological aspect of the male and female gonads, as observed with a moderate magnification, and the cytological condition of the gonad itself: he has distinguished four stages of maturity plus an initial stage in which the gonads are not yet perfectly formed. The maturity stages according to Ghirardelli are sumrnarizcd in Table I . The knowledge and exact evaluation of the maturity stages has an obvious importance in the determination of the life cycles of chaetognathsas the researchesof several workers have shown, particularly David (1955, 1965), Fraser (1952), Russell (1932), Dallot (1967), Alvarifio (1967a), and which we shall discuss shortly (p. 343). 3. Germ cell determinant

Before leaving the subject of the eggs of chaetognaths, i t is opportune t o mention another formation which is present in the eggs, i.e. the germ cell determinant. I n 1573 Biitschli discovered that the germinal cells of chaetognaths can be singled out already in very precocious stages of embryonal development. He actually described in the gastrula of Xagitta a pluricellular formation situated on the bottom of the archenteron cavity, and identified it as the primordium of the germinal line. Hertwig (1880) stated on the contrary that this "anlage "was formed a t first by two cells only. The segregation of the germinal line is, however, still more precocious and must be related to the presence in the egg, while still unsegmented, of a peculiar cytoplasmic inclusion which appears immediately after the laying of the fertilized eggs, when the two pronuclei have not yet conjugated. Elpatiewsky (1909) was the first to describe this structure in the eggs of 8. bipunctata and he called it "besondere Korper ". At almost the same time this peculiar body was observed, still in Sagitta, by Buchner (1910) and Stevens (1910); some years later Vasiljev (1925) stated that it is found also in the eggs of Xpadella cephaloptera. According to Elpatiewsky the peculiar body or germinal determinant (Ghirardelli, 1953a-c) is a small neatly contoured mass, placed in the periphery of the egg, near the vegetative pole ;it is strongly stained by ferric haematoxylin.

TABLEI. MATURITYSTAGESOF THE GOXADS A. Examination under the binocular dissecting microscope, x 100. 13. Examination of sections.

Ovaries

Testes

Stage 0 A. Gonads not visible ;in transparentspecies primordial gonocytes can be seen. B. Primordial gonocytos.

A. Gonads not visible. I n transparent specics primordial gonocytes can be seen. B. Primordial gonocytes.

Stage I A. Gonads little developed, resembling a small mass, slightly elongated, made of spherical cells. B. Oogonia in multiplication. First ooeytes of first order in their first period of growth. Some oocytes are a t beginningof second stage. Synaptic stages in nucleus. Cytoplasm rather scarce but easily stainable. Perinuclear granulations present. Seminal pouch and crescent not yet formed. Stage I1 A. Small but easily recognizable oocytes. B. Oocytes in their second period of growth ; some may also be a t beginning of third period. Granulationsaroundnucleusmore numerous than in former stage. Lampbrush chromosomes. Strongly stainable cytoplasm. Oocytes in their second period of growth enter into contact with seminal pouch by means of fecundation cells.

A. Testes visible though very small. There a.re no male germ cells free in caudal coelom. B. Spermatogonia in multiplication.

A. First germ elements free in caudal coelom. B. Spermatogonia in multiplication. Small masses of first and second order spermatoeytes free in caudal coelom.

Stage I11

A. Large oocytes in median line of ovary, smaller laterally.

B. Oocytes at end of their second period of growth, greatest number has already reached third period. Cytoplasm is less stainable than in former stage. Vitelline inclusions present. Big and vesicular nucleus. Typical lampbrush chromosomes. Granulations around nucleus are still apparent though somewhat smaller than those seen in previous stage. Crescent, seminal pouch and accessory fertilization cell are well developed. Spermatozoa are already present in pouch. Stage I V A. Well-developed ovaries with oocytes in median part, volume of which exceeds that of oocytes in marginal region. Nuclear membrane has disappeared or is about to do so. Sometimes oocytes show polygonal contours. B. Oocytes a t end of their third period of growth. Granulations around nucleus, if still present, are quite small. First metaphase is sometimes visible. Cytoplasm is barely stainable and then only nearby granularformations. Seminal pouch and fecundation apparatus well developed. Abundant spermatozoa inside seminal pouch.

A. Numerous globular clusters of very mobile male germ elements, free in caudal coelom. Sometimes first spermatozoa are already visible. Seminal vesicles have not yet developed. B. All phases of spermatogenetic and spermiohistogenetic evolution are represented.

A. Testis is full of germ elements and particularly of spermatozoa in active movement. Seminal vesicles are well developed, with their peculiar external structures. B. All stages of spermatogeneticevolution as in stage 111, but with predominance of spermatozoa.

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According to Buchner thc germ cell determinant is a small roundish chromatic body, little differentiated, sometimes without definite structure, or more or less vesicular or even granularin appearance. The differences found by the various authors are almost certainly due to fixation and to the moment a t which the germ cell determinant has been observed. The origin of the germ cell determinant is not yet known. Theories in this connexion differ widely and are sometimes contradictory. Vasiljev believes it to be of cytoplasmic origin, while Elpatiewsky, Stevens and Buchner think it has a nuclear origin. Elpatiewsky and Stevens suppose that it may originate from the small plaques of the nuclear net; Buchner, on the other hand, thinks it derives from the nucleus of one of the accessory cells forming the peduncle which connects the oocyte to the wall of the seminal pouch. According to Vasiljev the germ cell determinant forms de novo directly after fertilization, originating from certain small grains which appear within the cytoplasm a t the vegetative pole of the egg. These grains group, unite and form a sniall spherical body with a diameter of about 8-10 p. In order better to understandwhence and how the primordium cells of the germinal line of chaetognaths may originate, and what is the function of the germ cell determinant in the differentiation of the cells of the germinal line, it is useful to outline briefly the first phases of development. The segmentation of the eggs of Chaetognatha is total and equal and it is the same both in Sagitta (Kuhl and Kuhl, 1965), whose pelagic eggs are transparent since they have very little yolk, and in Spadella cephaloptera whose eggs on the contrary are opaque, with many vitelline grains, and are laid attached to submerged bodies, generally seaweeds or leaves of marine phanerogams. When the eggs begin to segment, the germ cell determinant passes undivided into one only of the first two blastomeres which is a stem cell formed by material which will give rise to both somatic and germinal cells (mixed blastomere) ; the other blastomere, without determinant, is a purely somatic blastomere. Up to the fourth division, things continue in this way : the somatic blastomere continues giving rise only to somatic cells, the stein cell always divides to form another stem cell and a somatic blastomere. The germ cell determinant meanwhile remains undivided in the only mixed blastomere from which new somatic blastomeres continue, as we have said, to separate (Fig. 18). After the fifth division, the two cells which form from the mixed blastomere are clearly determined : one, containing the still undivided germ cell determinant, is the "anlage )'of the germinal cells, the other will become the primitive endodermal cell (Elpatiewsky, 1909). During

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FIG.

317

18. Some stagcs in the cleavage of the eggs i n 8 . inJata. Lower right: gastrula seen from the blastopore and sideways. On the bottom of the archenteronthe germ cells can be discerned.

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the next division, when the germinal cell divides for the first time, the germ cell determinant contained in it also distributes itself into the two daughter-cells. Buchner states that each receives an equal share of the determinant ; Elpatiewsky and Stevens, on the other hand, believe that the determinant splits into unequal portions between the two cells. The differentiation of the primitive cells is related to this circumstancethe spermatogonia derive from the cell which received a lesser quantity of determinant, while the oogonia originate from the other one. Up until now there has not been sufficient evidence t o affirm that the differentiation of the germinal cells is due to the different quantity of germ cell determinant they receive, and still less has it been proved that the primordium of the male line actually is the cell which receives the lesser quantity of determinant. On the contrary, it cannot be excluded that, in the same way as in other organisms with balanced hermaphroditism like Chaetognatha, the differentiation of the germ cell may be due to the action of a gradient active in a cephalocaudal direction (Vannini, 1963 ; Ghirardelli, 1965a). A t the 64-cell stage two cells are already clearly determined as germinal cells and, althoughthe somatic cells may further divide before gastrulation, the two primitive cells divide only during or after gastrulation has occurred. This explains why Hertwig (1880) located the primordium of the germinal line in two cells only, in the very young gastrula, placed on the wall of the archenteron(opposite the blastopore) and later four in Sugitta (one only Spadellu in the early gastrula, according to John, 1933). These four cells do not divide further during the subsequent phases of embryonic development, which in Spudella, at a temperature of lS"C, takes about 24 h to complete. Eight hours are necessary for the gastrulation (Ghirardelli, 1953~). I have also observed times not greatly differing from those in Sugitta inJlata, while Kuhl and Kuhl ( 1 965) have seen that gastrulationin Sagitta setosa takes a somewhat lesser time. It is likely that the differences observed might be due t o the temperature; Murakami (1959) has actually observed that the period from spawning t o hatching changes with water temperature and chlorinity. A minimum of 15 h was recorded at a temperature above 27°C. Murakamisupposed that the eggs of Sugitta crassa spawned in the sea hatch in 1 day in summer and in 2-4 in winter. At hatching two of the primitive germ cells are situated in front of the caudal septum and they will give rise to the oogonia; the other two, situated behind the septum, will originate the male germ line. It is perhaps opportune t o recall that from the two anterior cells only the oogonia arise, while all the other cells which take part in the formation

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of the female apparatus (accessory fertilization cells, seminal pouch, involucres and stroma of the gonad) have a different origin, i.e. they derive from mesodermic cells (Ghirardelli, 1959d). The primitive germ cells in the gastrula and in the larvae are also easily recognizable in vivo in Sngitta because of their larger dimensions and the typical appearance of their nuclei which are very voluminous. O n the contrary, the germ cell determinant has never yet been seen in living cells, not even under a phase contrast microscope in the eggs of Sagitta inJlata which are the most transparent we know. I n Xpndella cephaloptera, by destroying the blastomere containing the germ cell determinant with a fine glass needle, it has also been

FIG.19. (Left) Egg of Spadella cephaloptera. A t the stage 2, the blastomere with the germ cell determinant (arrow) has been killed. This blastomere has not developed, while the other has given a gastrula without germ cells. FIG.20. (Right) Electromicrograph of the germ cell determinantof Spadella cephaloptera.

possible to demonstrate that the other blastomere may give rise to a gastrula void of germ cells (Ghirardelli, 1954~).The destruction, since it was impossible to see in which of the two blastomeres the dcterminant was placed, was done by chance; but it could happen that in the material of the blastomere which had been damaged the determinant was still visible. I n those cases there was absolute certainty that the destroyed blastomere actually was the one containingthe germ cell determinant (Ghirardelli, 1954c) (Fig. 19). Obviously the ideal experimental procedure should have been to separate the first two blastomeres and then to follow the individual development of each one of them. The isolation of the first blastomeres has not been possible because of the structure of the ovular membranes. The eggs of Spadella have 11'

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indeed a very elastic shell which can be taken off, albeit with some difficulty, but it is impossible to work on the vitelline membrane without damaging it. Observations under the electron microscope have shown that the shell of the egg is made of two clearly defined layers : the outer one is about 0.1 p thick and has a fibrillous aspect due to the prescnce of short fibrils clearly oriented, the inner layer is thicker and looks finely granular (Fig. 21). The vitelline membrane is composed of three layers and intimately connected with the cytoplasm ; it is very elastic and easy to distort (Ghirardelli, 1963c, 1966b). The structure of the membrane may perhaps explain the difficulties experienced when trying to separate the two blastomeres. It also explains why the eggs change their shape so rapidly when at the moment of laying they make their way through the two cellular layers forming the wall of the seminal pouch which, due t o the presence of the eggs, separate from one another so as to form a “temporary oviduct ” (Stevens, 1910). The experiments and observations I have just mentioned, show that the eggs of Xpadella cephnloptera are eggs with a very precocious determination : there is no reason to doubt that the eggs of all Chaetognatha may have the same peculiarity in connexion with the existence of the germ cell determinant. I n the sections of the eggs of 8. cephaloptera stained with ferric haematoxylin, the germ cell determinant appears as a small roundish compact mass with a diameter of about l o p . Through opportune differentiations it is possible to make small granulations evident within the determinant. This formation stains quite strongly with pyronin but the pyroninophilia disappears after treatment with warm HC1 N/1 or the action of the ribonuclease. The determinant is, on the contrary, completely Feulgen-negative,while the Hotchkiss reaction for polysaccharides is positive. The determinant is further osmiophil like the globuli of yolk. On the basis of these data it has been possible t o conclude that the germ cell determinant of Spadella is a formation rich in RNA which probably contains a lipid fraction, given by strongly unsaturated lipids, and a glucide component revealed by the oxidizability with the periodic acid (Ghirardelli, 1953a-c). Use of the optical microscope does not allow more to be learnt than has already been said about the morphology of the germ cell determinant, and for this reason it has been deemed useful to study it also with the electron microscope. For this first research we have used eggs of Xpadella cephaloptera collected on the Zostera on the bottom of the Bay of Grignano, near Trieste. At a small electronic magnification (Ghirardelli, 1966a, 1966b), the determinant can be normally seen near the periphery of the egg and it

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32 1

is often surrounded by large yolk globules ; although it is not provided with a membrane of its own, which would isolate it from the cytoplasm, it shows a well-defined boundary (Fig. 20). At a greater magnification, the germ cell determinant appears like a mass of irregularly shaped threads, more or less branched, and of big grains and plaques, all tangled together. These single constituents do not have a uniform tissue, but form loops or even figures of eight that have not all the same opacity; this might be due to the different nature of the formations. The single constituents of the determinant are immersed in the cytoplasm which a t a certain magnification shows between the formations of the determinant itself some sack-like cavities, often more crowded in some regions of the determinant than in others. These

FIG.21. Electromicrographof the ovular membrane m and of the shell sh of the egg of Spadella cephaloptera.

cavities or vacuoli are limited by a small membrane. The threads, the loops and the plaques which form the germ cell determinant, have a finely granulated aspect, due to the presence of two types of small grains of which one is more opaque than the other. The appearanceof a part of these grains recalls that of the grains of glycogen. Other grains, and among these those leaning on the thin membranes which limit the vacuoli, are probably ribosomes. One reaches these conclusions by observing the electronic images but also by keeping in mind the data from the histochemical research reported above. At the present stage of the work, it is not possible to state anything more ; it will be necessary to submit the sections to enzymatic or other treatments so as to demolish the different constituents of the determinant in order to determine them exactly. As we have said, the determinant divides into the primitive germ cells: in their cytoplasm, and especially around the nucleus, many grains can be seen that can be related to the germ cell determinant.

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There is no doubt, therefore, that when the first germ cells form, the determinant divides between them : the first observations with the electron microscope, however, do not allow any statement as to whether it divides into equal parts or not. The various constituents of the germ cell determinant separate from each other and distribute themselves more or less regularly in the cytoplasm. Later the grains and small plaques tend to settle aroundthe nucleus of the germ cells : it would be interesting to see, in this respect, whether they mass invariably in greater quantity around the nucleus of two of the four primitive germ cells that are in the gastrula. I n some figures, one seems to see that, the grains are indeed in greater number around some nuclei, which are quite similar in their appearanceto the nuclei of young oocytes in their first and second period of growth during which the nuclear net is quite apparent. It cannot be excluded that the origin of the germ cell determinant may be traced to these perinuclear formations. Actually a t the first metaphase when the nuclear membrane disappears the perinuclear formations could disperse in the cytoplasm : these could be the grains Vasiljev saw. Later these grains could gather a t thc vegetative pole of the egg thus forming the germ cell determinant which, after dividing between the primitive germ cells, would again give rise to the nuclear net. The contiiiuity of the germinal line would thus be assured by the persistence of the germ cell determinant in its various aspects. If evidence could be found that the determinantplaces itself invariably in greater quantity around the nucleus of two only of the four primitive germ cells, it would also be proved that the differentiation of the cells themselves is strictly connected with the dctcrminant. Owing to the character of their nuclei, these cells would indeed be the first oocytes. These are a t present mere hypotheses, though fascinating ones, which need to be confirmed by further work (Ghirardelli, 1966b).

D. Fertilization 1. Fertilization in Spadella cephaloptera The possibility of self-fertilization in Chaetognatha, which are protandric hermaphrodites, is admitted by several authors (Stevens, 1910; Bord&s, 1920; Jagersten, 1940; Murakami, 1959; Dallot, 1966), while others believe that fertilization is always the consequence of mating (Grassi, 1883; Vasiljev, 1925; van Oye, 1931; John, 1933; Vannucci and Hosoe, 1952 ; Ghirardelli, 1953d, 1954a). Cross-fertilization has, however, been seen only in a few species : in an undetermined species of Xagitta by van Oye (1931), in Xagitta crassa by Murakami

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(1959) and in Spadella cephaloptera by Vasiljev (1925), and Ghirardelli (1953d, 1954a). Some authors believe that cross-fertilization is the rule (Ghirardelli and van Oye), while others think that one of the partners acts only as male and the other only as female, so that there should not be a cross-fertilization (John,1933). My work has been carried out on specimens of Xpadella cephaloptera from the prairies of Posidonia near Capo Posillipo (Naples). The Spadella concerned were always mature male, with the seminal vesicles at the completely filled stage ; the ovaries, on the other hand, were a t different stages of maturity. Before mating, two specimens approach, and touch each other repeatedly with their heads, necks and perhaps the corona ciliata: so quick are the movements that it is often impossible t o follow their succession exactly. Then the two specimens place themselves with their heads in opposite directions and their bodies almost touching. Immediately afterwards, they make a sort of scissors-like movement which is repeated several times, following which the neck and trunk region of one crosses with the caudal region of the other. Similar observations were made in 1966 a t the Helsingcar Marine Biological Laboratory by a group of students (Thorson,personal communication) (Figs. 22 and 23). After this series of very quick movements, which may last even less than 1 sec, each individual has one of its seminal vesicles empty, i.e. the one which was turned towards the partner. The contents of the vesiculae appear on the neck of each of the two individuals in the form of a spermatophore whose dimensions are the same as those of the vesiculae seminalis. The spermatophores are always laid on the dorsal median line directly behind the ciliary loop. According t o Vasiljev (1925), on the other hand, the two individuals place themselves with their heads pointing in opposite directions but in such a manner that the seminal vesicle of each is in contact with the orifice of the vesicula seminalis of the other. I n this way the spermatozoa would pass direct'ly into the receptaculus seminalis from the vesiculae which could have been broken by some stick-shaped inclusions contained in the cells surroundingthe genital papilla. I n the specimens I have observed, the exchange of the spermatophores is, apart from some rare exceptions, mutual and simultaneous. Only in some cases does the exchange occur at successive intervals, one individual giving its spermatophore to the other without receiving another at the same time. The two individuals, however, remain in contact until the second spermatophore has also been placed on the head of the partner. Furthermore, in other rare cases, as John observed, only one of the two individuals acts as a male, while the

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other acts as female. Also according to the observations made at Helsingm the exchange is not reciprocal; in fact the artist has drawn the spermatophoreplaced on the caudal region of the individual acting as female, and not near the corona. In the specimens I have observed, on the contrary, the only position chosen for the laying of the spermatophores was the one behind the corona.

FIG. 22. Preliminary phases of the meeting and the mating in Spadella cephaloplera according to the observations made in Helsingm Laboratory. Olsen.)

(Drawn by Kaj

Some seconds after the spermatophoreshave been placed on the neck, their posterior regions appear to melt (i.e. those directed towards the tail) and they give rise to a stream of spermatozoa heading towards the caudal septum. When the stream has reached a certain distance from the caudal septum, it forks and each of the two branchesheads towards the orifice and enters the receptaculus seminalis (Figs 23 and 24). Not more than 2 or 4 min have elapsed from the beginning of the migration of the spermatozoa. The penetration of all spermatozoa through the orifice of the seminal receptacle takes a little longer. When mating occurs between individuals whose receptacles are already more or less full, it may even take 20 min before all spermatozoa can enter

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the receptacles. The same individuals can also mate together several times in a short while and the act may occur in the laboratory at various hours of the day but takes place mostly in the late afternoon when evening has begun. On the other hand, the strong light used to illuminate the microscope field does not seem to disturb individuals preparing for mating or those already mated.

2 FIG.23. Spadclla cephaloptera. Position of the spermatophores spf after mating and beginning of the migration of the spermatozoa sp ;c.i. ciliary loop.

It is also possible to follow the migration of the spermatozoa experimentally, i.e. by taking off by means of a thin needle a spermatophore from one individual and placing it on the neck of another (Fig. 24). The features of migration do not change ;they do not change even if one carries out an experimental self-fertilization by placing on the neck of a specimen one of its mature spermatophores. If, however, the spermatophores are placed in regions different from the usual one, the migration of the spermatozoa does not happen in a normal manner. When the spermatophores are placed on the tail a little in front of the seminal vesicles, the sperms disperse and form irregular masses a t the sides of the body, some migrating towards the

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FIG.24. Spadella cephaloptera. Successive phases of the migration of the spermatozoa from the region of the neck where the spermatophore spf is placed behind the corona co towards the seminal receptacles s.r. ; V.S. seminal vesicles ; el. collarette. (From Ghirardelli, 1954a.)

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caudal sephum and even perhaps reaching the orifices of the receptacles. The majority, however, migrate towards the caudal fin ; the sperms form here a more or less compact clump after which they generally fall from the body. I n some instances, a sharp contraction of the tail may throw the spermatozoa forward toward the caudal septum, but these too generally detach themselves from the body after a longer or shorter period: only very few enter the seminal receptacles. The same thing occurs with spermatozoa which leave the seminal vesicles owing to some traumatic damage. I n this case, furthermore, the spermatozoa show that they are unable to climb up the tail. It is interesting t o note that if one spermatophore is placed on the neck and at the same time another is put on the tail of a specimen, the spermatozoa migrate regularly from the spermatophore on the neck, while those on the tail show the irregular behaviour we have described above. Spermatophoresplaced on the ventral region of the body, before or behind the caudal ganglion, dissolve more or less regularly: the sperms migrate to the sides of the body heading towards the anal orifice near which they mass. After a short time they part from the body and do not seem to be able t o head towards the lateral-dorsal region of the body where the orifices of the receptacles are situated. All the foregoing refers t o animals whose epidermis is in perfect condition. I n the orifices of a specimen whose receptacula seminalis had been damaged and on whose neck a spermatophore had been placed, migration occurred speedily but no division took place at the usual point : the sperms having passed the caudal septum arrived at the tail, from whence the direction of the migration was reversed and almost all spermatozoa returned to the neck. Some of them took up position on the ciliary loop, some passed the loop and took up places at irregular intervals on the head. The migration of the sperms in the two directions took about half an hour on the whole. Some hours after the beginning of the experiment, numerous sperms could still be seen on the head. If the spermatophore is placed in the centre of the ciliary loop, the sperms tend t o migrate on t o the head or t o settle on the corona itself: no migration towards the septum can be observed. If the spermatophore in beheaded specimens, deprived also of the corona ciliata, is placed on the neck shortly after the operation, the migration occurs almost always and it is regular enough. One hour after the cutting, however, the spermatozoa either migrate no more or do so in a completely irregular manner. These observations should then allow one to conclude that in Xpadella cephaloptera fertilization occurs following a reciprocal mating, though it is possible, as we have seen, t o obtain self-fertilization

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experimentally. However, self-fertilization seems difficult under natural circumstances, since it cannot be seen how the spermatozoa produced by a Spadella can reach the orifices of the seminal receptacles of thc same individual, considering the tendency they normally have to niigrate-when they are on the caudal region of the body-towards the posterior fin rather than towards the orifices of the receptacula seminis. As far as the observations of other workers are concerned, though one cannot discard the possibility that the behaviour of the Spadella from Plymouth (John,1933) and from Helsingm may differ somewhat; it cannot be excluded that in view of the speed with which the facts we described occur, some phases of the above phenomena may have escaped the observers. The factors which influence the migration-which as we have seen seem to follow a pre-arranged course-remain to be ascertained. The integrity of the teguments is an essential condition but on the dorsal region of Spadella there are no visible structures-at least not visible through the normal means of observation-to which one may with certainty attribute a determining function in leading the sperms towards the orifice of the seminal receptacles. The ciliary loop certainly plays an important role in regulatingthe migration of the spermatozoa : actually, depending on the position in which the spermatophoreis laid in respect to the corona ciliata, the migration which follows is regular or is not. Beheading with removal of the corona does not as a rule stop the migration, provided the spermatophore is placed on the neck immediately after the cutting has been done. I n connexion with the probable influence of the corona, it has been supposed that the migration of the sperms may be regulated by a chemotactic action, by some substance produced by the corona, which continually spreads along the back of the animal. This could explain how the regular migration of the sperms may also be possible in animals which are not mating, in other words a t any time when a spermatophore is placed on the neck behind the ciliary loop. It could also explain why the migration ceases some time after the specimen has been beheaded, i.e. deprived of the corona and of the secretion it produces. It seems therefore logical a t this point to relate the peculiarities of the migration of the spermatozoa on the back of Spadella to the presence of the secretion produced by the corona which spreads on to the back, massing in noteworthy quantity near the genital orifices (see p. 284). This observation is confirmed by Di Marcotullio (1966). This could also explain the greater activity shown by spermatozoa when near the genital orifices and the change of direction of the

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migrating stream when it reaches the caudal septum. Gabe himself, who does not believe the secretion of the corona to be of a neurosecretory nature (see p. 285), thinks that it is not unlikely that the product itself-probably a mucopolysaccharideor a mucoprotein-may be concerned in the migration of the spermatozoa. 2. Fertilization in Sagitta and other genera Things appear somewhat more complicated as far as Sagitta and the other genera of Chaetognathaare concerned. First of all it is much more difficult to make laboratory observations, due to their different behaviour and to the fact that it is very difficult to keep Sagitta in culture conditions long enough. It can also be presumed that the reproductive behaviour of pelagic organismsmay be different from that of benthic species, even if belonging to the same systematic group. Also few authors have dealt with the subject in pelagic Chaetognatha. We have quoted Grassi who believed that the fertilization occurred after a reciprocal mating. Stevens (1910) and Bord&s (1920) deemed self-fertilization probable, because the sperms, coming out of the vesiculae seminales placed on the posterior end of the body, could reach the receptacula by climbing along the tail and entering them. Van Oye (1931) observed that the contents of a mature vesicle in Sagitta is expelled in the form of a spermatophore more or less sphereshaped and wrapped in a mucous substance whose origin is unknown. The expulsion occurs as the consequence of a series of strong movements of trunk and tail. The spermatophoreseems then to be pushed towards the end of the caudal fin which bends so as to form a sort of gutter: it is not clear how this bending may occur in view of the absence of muscles in the caudal fin. Kuhl (1938) thinks that the phenomenon may be due to purely mechanical causes, i.e. to the leaning on the spermatophore of the terminal part of the fin, which in adult animals may be more or less damaged and is in any case very flexible. Mating according to van Oye occurs when two individuals, each carrying a spermatophore on the caudal fin, happen to meet; they then dispose themselves with the heads iii opposite directions and, since the caudal regions of the Sagitta are of about the same length, the spermatophore carried by the fin of one of them comes to face the genital orifice of the other, which in the meantime has extended. The spermatophores are then held by the latcral fins of the individuals which have been fertilized and the sperms actively penetrate the seminal receptacle. Mating is very quick; it can be repeated several times and occurs a t night. The exchange of the spermatophores is, according to van Oye, mutual, and self-fertilization must be excluded. The lateral fins may also play

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a part in this process by helping t o keep the migrating spermatozoa moving in the right direction. On fixed specimens of Xagitta ferox Doncaster from the seas around Madagascar, Dallot (personal communication) has often observed on the ventral face of the anterior fins a voluminous spermatophore attached by means of its adhesive sucker. More than one spermatophore, up to three, can sometimes be seen on a single specimen, and the seminal vesicles of the same animal may be either full or empty. Even in Sagitta neglecta Aida and X . bedoti BBranek, Dallot has seen spermatophores, but they were placed indifferently on this or that point of the body. According to Gray (1930) the spermatozoa might exceptionally enter the seminal receptacles by going through the caudal septum. Accurate observations in the laboratory, on the fertilization of the genus Xagitta have been made by Jagersten (1940), Dallot (1966) and Murakami (1959) who has been able to rear S. crassa for 3 months. Jagersten, who studied S. setosn, gave an accurate description of the fertilization process. As we have already said, this writer thinks that in Sagitta there is usually self-fertilization only and no mutual mating. The breakage of the seminal vesicles occurs along pre-ordained lines which Jagersten described. The spermatozoa migrate along the tail towards the caudal septum. The modes of the migration itself may differ in different specimens. The process occurs mostly in the night hours. Jagersten also kept specimens isolated one from another, and observed that if their seminal receptacles had been empty in the evening, in the morning they were full while one or both seminal vesicles had emptied. The migration from one vesicle is not necessarily always directly towards the seminal receptacle on the same side ; the sperms may actually migrate to the opposite side also and this migration is not prevented by the sudden movements of the animal, though obviously a certain quantity of spermatozoa may get lost. A further proof of the necessity of self-fertilization is, according t o Jagersten, the fact that young individuals whose seminal vesicles have never been filled, never show sperms in their seminal receptacles. Furthermore, specimens with full seminal receptacles always have empty scminsl vesicles and vice versa. Some objections can, however, be raised against Jagersten’s conclusions. The chaetognaths are indeed protandric hermaphrodite organisms in which the testes mature sooner than the ovaries. It is apparent that if an individual has never had full seminal vesicles, it is not yet completely mature at the male sex, and still less at its female sex : it is then unlikely or a t least difficult for fertilization t o occur. The

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second objection is that in other species and in S. setosa from other localities (Gulf of Naples, Gulf of Trieste, Villefranche) it is not infrequent to find specimens which have a t the same time full seminal vesicles and receptacles. Jagersten finally does not exclude that in the course of phylogeny reciprocal fertilization may have been substituted by self-fertilization. The evidence of reciprocal fertilization is in a cup-shaped structure that is to be found on the seminal vesicles; it detaches itself, together with the contents of the vesicles, forming a spermatophore which seems to be provided with an organ-the cup itself-so made as to adhere to the body of anotherindividual. We shall have the opportunity of dealing again with this and other similar formations which are to be found in other species of Sagitta (p. 332). Dallot (1966) also believes that fertilization is not reciprocal. He was able to raise specimens of S. setosa in isolation and found that in spite of this about 50% of the spawning gave fertilized eggs. He also observcd that the same animal might lay successively unfertilized eggs and then fertilized ones, or also that the contrary might happen; all the eggs of one spawning are, however, in the same state. There were also specimens that always laid fertilized eggs and others only unfertilized eggs. According t o Dallot, the greater number of unfertilized eggs could be explained by a state of immaturity of the seminal vesicles, or by the fact that though mature they do not open. He says that the sterility of a spawning can be guessed in advance if a short time before the expulsion of the eggs one sees the seminal vesicles full of sperms. On the other hand, seminal vesicles which open before laying provide a good indication of fertilization. Dallot has been able to confirm what Jagersten had already seen, namely, that the filling of the seminal vesicles takes place periodically. After the wall in the mature vesicles breaks, a new spermatophoreforms which will be freed a little while later. Dallot has also seen that this cycle supersedes that of the ovary : the formation of a spermatophore is generally concurrent with the period of growth of the ovary following a deposition. Finally, he was able to observe that generally the number of the cycles in the male reproductive organ is the same as that of the female apparatus. The periodicity of ripening both of the ovary and vesiculae seminales is 2 1 h. It also seems that the synchronousactivity of the seminal vesicles and of the ovaries is an essential factor to ensure the success of selffertilization. The laying of the eggs occurs before dawn. Dallot has further seen that in the animals gathered and placed under breeding conditions before their ovaries were completely mature, the seminal receptacles regularly appear empty. He thus excludes the possibility that fertilized eggs laid by animals just placed under breeding

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conditions may have already been fertilized before, by spermatozoa originating from anotherindividual. I n cases of self-fertilizationhe has been able to fully confirm Jagersten’s findings that the spermatozoa migrate along the caudal segment towards the seminal receptacles which are quickly filled. Nevertheless Dallot does not exclude, as Jagersten did, the possibility of a mating in S. setosu: but if it does exist, it is not essential for the survival of the species. At this point an histological control of the state of filling of the seminal receptacles would be desirable, since sperms present in receptacles which are not completely full escape direct observation through the binocular; subordinately it should be quite interesting to raise in isolation some specimens from the egg up to the stage of full sexual maturity: only in this way could absolute certainty be reached that the sperms present in the seminal receptacles derive from the seminal vesicles of the same specimen. Dallot’s supposition that self-fertilization does not exclude crossed fertilization, remains valid : we would add that crossed fertilization does not exclude the possibility of self-fertilization. Even Jagersten’stheory that cross-fertilization was graduallyreplaced in the course of phylogeny by self-fertilization may be suggestive, but the presence of peculiar formations on the seminal vesicles is far too constant t o be void of any functional value in the present. The seminal vesicles in AS’. inJEatuare indeed always surmounted by a small cup with smooth edges, while in S. bipunctuta the edges are shaped like saw teeth ;the different forms of S. serratodentatu are recognizable by the different aspects of their seminal vesicles. Nearby these structures there is generally a point where the seminal vesicles are thinner, and this is, therefore, considered to be the orifice of the vesicles (Tokioka, 1939a, 1942; Kuhl, 1938; Jagersten, 1940 ; Ghirardelli, 1950a, 1954a, 1959c, 1962 ; Furnestin, 1957). I have also been able t o confirm the observations made by Jagersten on 8. setosa, trying more than once and without result t o induce mating in AS’. inJEataand S. bipunctatu. On the contrary, the mature spermatophores of these two species can be detached quite easily, together with the small cup that closes the orifice of the seminal vesicles, and made to adhere with the same cup t o the body of a specimen of the same species. If the spermatophores are placed on the back, they do not adhere well and one does not observe any migration of spermatozoa as in Spudella. Sometimes the spermatozoa form regular streams and very occasionally they head towards the openings of the seminal receptacles ; but when the spermatophore is put on the genital papilla or in its immediate neighbourhood, one can see the rapid penetration of the

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spermatozoa into the seminal receptacles. Also Jagersten saw that a spermatophore placed on the tail quickly empties itself and that the sperms migrate towards the receptacles. It can furthermore be observed in some species that the openings of the receptacles may modify their shape (van Oye, 1931 ; Jiigersten, 1940; Furnestin, 1960). Again this fact leads one to suppose that the spermatophores must be attached near the genital papilla; if indeed the spermatophores are experimentally placed on the genital papilla or in its immediate neighbourhood, a very quick penetration of the spermatozoa into the receptacles can be seen. As a consequence, the peculiar structuresobserved on the vesicles and on the spermatophores might be considered in some way to be a sort of copulatory organ, whose form fits one of the female genital orifices thus making mating between individuals of different species impossible. I n this case the differences shown by the mature seminal vesicles in even quite closely related forms would have value as highly discriminative systematic characters. Thus, for instance,the various forms of Sagitta serratodentata which are similar in having the typical serrated inside edge of the hooks, but differ in their biometrical characters and mainly in the shape of their seminal vesicles, should be considered as true species, as authoritative modern authors maintain. The differentiationwhich had been established by Tokioka (1939a, 1965a), Thomson (1947) and Furnestin (1953) would find a new and more valid confirmation. For other genera of chaetognaths the observations on fertilization are rather fragmentary, certainly far less complete than those concerning the genera Xagitta and Xpadella. David (1958, 1965) has made some very interesting observations on a specimen of Eukhronia bathyantarctica. Dr. David has been so kind as to send t o nie for examination this and other specimens. I have thus been able to observe that the spermatophores are flask-shaped, wrapped externally in an undifferentiated resistant small membrane. There is a prolongation t o this membrane, the shape of the neck of a bottle or flask, which is slipped into the female genital orifice, the edges of which protrude remarkably (Figs. 25 and 26). I n one specimen only was the spermatophore intact ; in others only the torn membrane was hanging out of the genital orifices. None of the specimens I examined had mature seminal vesicles, so that no conclusion could be made as to how the spermatophores form. David, however, believes that they originate from another individual. Similar observations have also been made by Tchindonova (1955). The case of Bathyspadella edentata Tokioka described by Tokioka (1939b) is also quite interesting. This chaetognath,though very similar

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to iYpadella, shows as well some affinities with the genus Eukhronia. Figures 5 and 6 of Tokioka (1939b) recall in a surprising way the appearance of the specimen of Eukhronia bathyantarctica which I mentioned. From all these observations, it seems that it may be safely stated that in pelagic chaetognaths mating or fertilization are different in character from those described for Xpadella cephaloptera. This can easily be understood if one takes into account the different habitat, benthic in h'padella and Bathyspadella and pelagic in all other species.

FIG.25. Eukhronia bathyantarctica with a spermatophore (spf), inserted in the genital opcning. FIG.26. Detail (at a greater enlargement) of the insertion of the spermatophore (&) into the receptacle. (From Ghirardelli, 1969d-specimen supplied by Dr. David, Kat. Inst. Oceanography, Wormley.)

kindly

It is interesting to note in this connexion some peculiarity in the structure of the corona in pelagic chaetognaths. This lacks the glandular part that is so peculiar to Xpadella, or there are, as I have said, a t the most a few glandular-like cells near the sensory ones. I n no case was it possible as yet, to demonstrate the presence in these chaetognaths of a secretion produced by the corona, This could also be a valid argument in favour of the idea,that fertilizations in pelagic and benthic chaetognaths are different in character. There could be a tendency in cross-fertilization t o lay the spermatophores very near the genital orifices so that the sperms need not effect a long migration on the body of the animal, which would be rather difficult owing to the active swimming movements of pelagic Chaetognatha. I n cases of selffertilization, it is obvious that the easiest way for the spermatozoa would be instead to climb up along the tail to the female genit,al orifices.

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E. Laying of the eggs 1. Laying in Sagitta As we have said (p. 299), fertilization of the eggs is brought about by spermatozoa which go through the accessory fertilization cells. The eggs, after having been fertilized, pass through the syncytial wall of the seminal pouch and insinuate themselves between this syncytial wall and the epithelial wall, thus forming the so-called temporary oviduct (Stevens, 1905, 1910 ; Bord&s,1920 ; Ghirardelli, 1959d). The laying of the egg differs somewhat in the various species that have bccn studied ; but in any case, as far as we know, they always emerge into the open by making their way through the tissues of the pouch or seminal receptacle. I have had more than once the opportunity of observing the laying of the eggs both in Sagitta inJlata and 8. bipune~ataat the Zoological Stations a t Naples and a t Villefranche-sur-Mer. When the eggs are on the point of being laid, the nuclear membrane disappears. The eggs are a t this moment in the first metaphase and they become more opaque than usual. About half an hour after the membrane has disappeared, the egg begins passing through the temporary oviduct. It is not always easy to follow this movement when several eggs are concerned: they move simultaneously and the appearance of the ovary is being much modified. Having entered the temporary oviduct the eggs are compressed against each other, assuming somewhat polyhedral contours (Fig. 27). Usually when the eggs start their descent along the oviduct they continue to change shape, often with the regular rhythm first observed by Stevens (1910). It is, nevertheless, possible that the eggs stay in the oviduct for a certain amount of time before laying, and that in unhealthy specimens they remain there for several hours (perhapsthree, four or moro). I n some instances even several eggs can be seen descending along the duct, in others only one egg is observed and this is noticeably elongated so as to occupy a space which might bc as long as one-half of the ovary. I n some cases, the presence of bubbles (Stevens, 1910) can be noted a t the poles of the egg. Stevens bclieved them to be air, but they are instead of a moderately viscose substance. When the forward bubble reaches the genital papilla, the first muscular movements of the body of the animal occur : the genital pore seems to open suddenly, the bubble comes out and breaks, immediately followed by the egg. According to Stevens, certain times are preferred for the laying of eggs in the various species of chaetognaths. Thus, while 8. elegans preferabIy Iays between 11.00 and 18.00 h, 8. bipunetata lays a t sunset;

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FIG.27. Eggs in the temporary oviduct in Sugitta bipunctata. The arrow points to an egg just entering the oviduct. Frontal section; i intestine.

I have ascertained that in S. inJlata the laying occurs normally between 23.00 h and the first hours of the morning. I n S. setosa it occurs at sunrise (Dallot, 1966). Studies in vivo do not allow firm conclusions as to how the eggs reach the outside : only the study of sections obtained from specimens fixed in the various phases of laying has enabled Stevens to describe for the first time the passage of the eggs to the exterior. I have been able t o confirm her observations and show the first photographic evidence of the phenomenon. On the outer wall of the seminal receptacle some openings form which BordAs believed to be due to a degenerationof the bicellular suspension apparatus; though it is not possible to state with certainty how these openings form, it is highly probable that they are

S

FIG.28. Eggs of Sugitta entering the temporary oviduct : A-E: successive stages of the piercing of the epithelial wall ep of the seminal pouch. I n E the egg is already inside the temporary oviduct. sp spermatozoa; s syncytial wall of the seminal pouch. (Adapted from Stevens.)

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caused by the pressure of the eggs. When these enter the openings (Fig. 28) they change their shape: they slip into the opening with one pointed end which immediately after becomes larger, causing the separation of the epithelial membrane from the underlying syncytium. I n the cavity thus formed the egg continues to slip and thus the area of separation becomes larger. The cavity so formed has rightly been defined by Stevens as a temporary oviduct. As the eggs penetrate between the epithelinm and the syncytium, they form a series of bags a t different levels, each containing one or more eggs. When the eggs that have crossed the ovarian wall are numerous, the separation of the two layers is complete along t'he whole length of the ovary from the apex to the genital papilla (Figs. 27 and 29);

s.p.

/

D A FIG.29. From left to right, four stages of the laying of the eggs in Sagitta. The smaller oocytes which normally lie to the outer side of the ovary in contact with the seminal pouch 8.p. have been displaced to the inner side of the ovary by the large oocytes that have entered the temporary oviduct. Right: when the ovary is emptied, the small oocytes again occupy the normal position.

I n transverse sections (Fig. 30) one sees t,he wings of the crescent bending towards one another, partially enveloping all the young oocytes which are pushed medially into contact with the intestine (Fig. 31). The central region of the ovarian epithelium, instead of being concave as usual, is now almost convex. I n a longitudinal section, the eggs appear more or less crowded together owing to the pressure they exert on each other and to that

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FIG.30. Diagrammatic drawing o f the ovary of 8. bipunctata with an egg in the teniporary oviduct. The egg lies between the epithelium ep and the syncytium s of the seminal pouch ;sp spermatozoa in the seminal pouch.

exerted by the walls of the oviduct. Between one egg and the other there is a liquid, easily coagulable and strongly eosinophilic. The second maturation division generally occurs in the lumen of the temporary oviduct. It must be remembered that, when the eggs pass through thc temporary oviduct, the spermatozoa have already entered into them (see page 299). The spindles are characteristicnon-convergent spindles. It is possible that each chromosome may be polarized independently (Fig. 32). Dallot (1966) believed that the expulsion of the eggs is brought about by inner contractions of the ovarian wall, and he thus confirmed the observations of Conant (1896) on S. hispidn. On the other hand, Stevens (1910) in 8. bipuwtata and Ghirardelli

FIG. 31. Sagitla bipuizctata: transverse section o f the ovary with two eggs in the temporary oviduct. The supportingcrescent ep has been reversed backwards. The arrow indicates the first spindle; i intestine; ms muscular wall o f the body.

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(1959d) in S. bipunctata and X. infzota have seen that the eggs enter into the temporary oviduct by active movements. As the eggs pass out to the exterior, the ovary reverts to its usual appearance, or rather to one which recalls a younger ovary (Ghirardelli, 1960) : it may actually appear shortened by two-thirds (Dallot, 1966, 1967). This contraction does not last long for it is followed by an expansion phase, during which the ovary becomes longer and the ovarian membrane detaches itself

FIG. 32. Left: First maturationspindle of Sagitta bipunctata. Right: First maturation spindle of Spadella cephaloptera. The aster is missing, the fibres are orientated parallel with the egg membranes tn. The nucleus is surrounded by a zone of denser cytoplasm. (The two photographs are equally enlarged.)

more or less from the oocytes. According to Dallot, in animals in good condition and feeding normally this phase is coincident with the beginning of the growth of the oocytes whose diameters increase rapidly. The factors which determine the moment at which the eggs shall pass into the temporary oviduct are unknown. 2. Laying in Spadella As we have seen, the structure of the ovary and especially of the seminal pouch and seminal receptacle are somewhat different in Spadella cephaloptera from those described in Sagitta. Also the laying shows some peculiarities which deserve mention. Xpadella, a t the moment preceding laying, make very quick movements so that it is almost impossible t o keep them constantly within the field of observation a t the highest magnification which would be highly desirable, as the eggs issue very quickly. Also the greater opacity of the body of Spadella in comparison with that of Xagitta makes it harder to follow exactly the path followed by the eggs.

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By using certain special devices it has, nevertheless, been possible to observe the phenomenon more than once (Ghirardelli, 1956a, 1959d). The observations have been effected by placing Spadella in good condition in micro-aquaria which were prepared by using cavity slides whose depression was filled with filtered sea water and closed with a coverslip. By taking care that an air bubble remained under the cover, one limited the space at the disposal of the Spadella, and at the same time a sufficient supply of oxygen was provided for the duration of the experiment (Ghirardelli, 1956a). It has thus been possible t o use enlargements high enough ( x 400-900) to allow us to follow easily the laying of the eggs under the phase contrast microscope. I n Spadella, contrary t o what occurs with Sagitta, it is not always possible to foresee the moment of laying ; the disappearance of the nuclear membrane is not a sign of the same significance in Spadella as in Xagitta. While in Sagitta the disappearance of the nuclear membrane normally precedes the laying of the eggs by some 10 min or 1 h at the most, several hours may pass before the laying begins in Spadella. The eggs of Xpadella when nearing the time of spawning can be recognized by their size (about 250 p diameter), their noticeable opacity due to the cytoplasm being uniformly full of vitelline granules, and also by the disappearance of the nuclear membrane. I n each ovary the number of mature eggs varies from one to a dozen, in relation t o the season and the stage of maturity of the specimen. The greatest number of eggs can be seen in spring (Ghirardelli,1959c, 1963a). Also in Spadella as in Sugitta, the eggs before being laid appear compressed by one another and may take a polyhedral shape. Consequent on movements of the intestine, due also to the ingestion of food and water, the eggs change their shape t o a remarkable extent, showing that they are extremely elastic. The temperature a t which spawning occurs is between 18"and 21°C. Higher temperatures, around 25-26"C7 tend rather to inhibit than to hasten the phenomenon.The laying of the eggs, as far as I could see, occurs in the following manner. With nothing to give a hint of the imminence of the occurrence, all the eggs contained in the ovary suddenly start moving towards its posterior end. The same phenomenon can be seen simultaneously in both ovaries. As soon as the first egg touches the outer wall of the so-called vagina, a small protuberance rises from the latter, the centre of which is afterwards depressed, thus forming a small cup into which the egg settles, its anterior end lying in the direction of its movement. I n the meantime the egg has become pear-shaped and its more pointed end slips between the epithelial cells of the mall of the vagina which are pushed aside in all directions, so that the egg seems t o penetrate

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into the lumen of the vagina (Fig. 33). Since, however, there is a considerable reorganization of all the cellular tissue and the phenomenon is very quick, it is not possible to ascertain in vivo whether the eggs actually enter into the lumen of the vagina or-as happens with Xagitta-end by penetrating between the two layers of cells which form its wall. It can in any case be safely ruled out that the eggs pass, as

FIG.33. A diagram of the laying of the eggs in Spudella cephuloptera. To the right (arrow) an egg is piercing1 through the epithelial wall of the vagina v, to enter the short temporary oviduct. To the left an egg is passing to the outside. The position of the seminal pouch s.p. is indicated seen through the eggs; oc young oocytes; i intestine ;go genital opening; s.r. seminal receptacle ;t testis; 1.f. lateral fins.

John (1933) said, into the seminal receptacle : in order t o pass t o the outside they always come in contact with the walls of the vagina and never with those of the receptacle which, during the passage of the eggs, may be pushed towards the median line of the body. It should be remembered in this connexion that the vagina is placed at a right angle t o the line of the body; in the middle of it lies the spherical shaped seminal receptacle, followed by the pouch which runs parallel with the intestine. Also, observations with the phase contrast microscope have shown that the walls of the seminal receptacle always

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remain intact. Incidentally, if the eggs entered the seminal receptacle, it is difficult to understand how they could come out without causing all the spermatozoa contained in the receptacles t o come out at the same time. Once the egg has come into contact with the vagina, the axis of its movement takes a sharp turn towards the outside in a direction perpendicular to that of the longitudinal axis of the ovary. I n this way quite frequently the eggs assume the shape of an L (Fig. 33). When passing through the genital papilla, the egg is coated with a resistant membrane, provided with an elastic peduncle by which it is fixed to the substratum. The following eggs show an analogous behaviour and follow exactly the same paths. Only the last egg moves somewhat slower than the others, perhaps because it is not pushed by the vis a tergo of other eggs, and for a small fraction of time it may stop in the terminal part of the temporary oviduct. It is, moreover, not possible to say whether the movemcnts of the wall of the ovary are due t o contractions of the ovary itself, or instead more simply due to thc active movement of the eggs. These progress with amoeboid-like movements, but are very quick, as if they were slipping through a well lubricated duct or were sucked towards the outside. Their movement recalls in its peculiarities, though obviously not for the same reasons, that of planarians. Nothing is as yet known about the causcs of the movement, but everything leads one t o think that the eggs, in this phase of their existence, are provided with a certain mobility of their own. The whole process, which is so long and complicated, does not last more than 20 or 30 sec and often even less. Histological sections have confirmed that the eggs reach the opening through a kind of canal between the two layers of cells that form the walls of the vagina itself: this is formed by an outer flat epithelium and a cylindrical epithelium lying towards the lumen of the vagina. The two cellular layers are detached and the eggs come out, but without entering the vagina. I n this case, therefore, a temporary oviduct seems to form, similar to the one described in Sagitta, with this difference, however, that the penetration of the eggs occurs here at one point only of the vaginal wall, and this is because the eggs all follow the same path as the first one. The seminal pouch is not concerned in this case, though it runs ventrally along the whole ovary. Another difference is the noticeably shorter length of the temporary oviduct in Spadella, limited to a small length only of the vagina which is 80-100 p long. I n Sagitta, on the contrary, the oviduct may be as long as the ovary, in some cases even some millimetres. The disorganization of the cellular elements at the moment of laying the eggs is, however, greater in Spadella than in Sagitta; to

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understand this, it is sufficient to recall the relative dimensions of the eggs of Spadella (diameter ca 2 5 0 p ) and the way they pass t o the exterior. The consequence of this is that even in the best preparations i t is practically always impossible, at the moment of spawning, to recognize the original topographic relations between the cellular elements forming the vagina. The eggs are deposited in clusters of from four t o eight to twelve, each of which is attached to submerged bodies: in nature t o the leaves of Zosteracea or seaweeds on which they usually live. Under experimental conditions, the eggs are attached instead t o the walls of finger-bowls t o which they adhere by means of an elastic peduncle. Vasiljev assumed that Spadella laid their eggs only at night, while I have been able to observe that, in the laboratory at least, the eggs can be laid at any time of day-though with a marked preference for night hours. As far as the other genera of chaetognaths which we have mentioned in this work are concerned, we lack any observations about the laying of their eggs. Sanzo (1937) described the eggs of Pterosagitta draco, which have a very thin shell and are gathered in gelatinous oothecae which are to be found at different depths according to the stage of development. Eukrohnia hamata Mobius, which lives in very cold waters, retains, on the other hand, its few eggs by its lateral fins, which bend to form a sort of incubation pouch (MacGinitie, 1955; David, 1955). The eggs of Krohnitta are also gathered by a gelatinous adhesive secretion in packets that the animal carries for some time attached near the septum dividing the trunk from the tail (Kuhl, 1928). According to Conant (1896) the eggs of Sagitta hispida are coated by a jelly which forms in the oviduct in 20-30 min. Each ootheca contains about sixty or seventy eggs.

F. Habitat and cycles of sexual maturity Many authors have reported on the influence of environmental factors on the distribution of the chaetognaths. I shall limit myself to quoting only Baldasseroni (1914))Teodoro (1923), Russell (1932a,b, 1933, 1935, 1939), Furnestin, J. (1938), Furnestin, M. L. (1965), Thiel (1938), Pierce (194l), Gamulin (1948), Tokioka (1952), Bogorov and Vinogradov (1955), David (1955, 1958b), MacGinitie (1955), Tchindonova (1955), Bieri (1959), Fraser (1962), VuEeti6 (1963), Ghirardelli (1953b, 1959c, 1962), Hirota (1959, 1961), Murakami (1959), Cannicci (1959) and Alvarifio (1967b). I n general, there is a close relationship between the distribution of the chaetognaths and salinity and temperature, so that chaetognaths A.M.B.-6

12

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may be very good hydrologic indicators. I n some cases, as for example in the Adriatic, environmental factors act as selective factors on the number of the species. I n the south Adriatic there are ten: Sagitta minima, S. inJlata, S. serratodentata, S. setosa, S. lyra, S. bipunctata, S. decipiens, X. hexaptera, Krohnitta subtilis and Pterosagitta draco (see Hoenigman et al., 1961 ; Vu6eti6, 1963 ; Hure, 1955) ; in the northern Adriatic this number decreases (Scaccini and Ghirardelli, 1941) and in the Gulf of Trieste, where there are considerable variations in salinity and temperature, the endemic species are only three : Sagitta setosa, S. minima, S. inJlata and perhaps only S. setosa and S. minima can reproduce in the Gulf of Trieste. S. bipunctata and S. serratodentata are accidentally collected in the Gulf (Ghirardelli and Specchi, 1965 ; Ghirardelli, 1 9 6 6 ~ ) . Some chaetognaths also have value as fishing indicators, e.g. Sagitta lyra (Le Brasseur, 1959)) S. serratodentata, S. setosa, S. elegans, S. crassa, etc. Sagitta crassa also is an important food for larval stages of Ammodytes personatus and other fishes (Murakami, 1957). I n any event, chaetognaths should be regarded as good indicators of conditions in the sea, provided that knowledge of the distribution and life history of each species is given more precisely in the future; and they will be of high value in fisheries research (Murakami, 1957). This matter is more amply dealt with by Alvarifio (1965, 196713) and Furnestinet al. (1966) to whom one should refer for further references and information. We would here summarize rather the main results of research on the cycles of sexual maturity. The number of the generationsproduced in one year obviously varies according to the different species, but is also correlated with the environment. Generally, the number of generations increases as the distance from the poles becomes greater (Owre, 1960). S. elegans (Kramp, 1939; Ussing, 1938; Alvarifio, 1965) only reproduces once per year in the Arctic and Subarctic regions. The same applies to S. gazellae (David, 1955) in the Antarctic regions. S. elegans reproduces two to five times per year as its distribution becomes more southerly. Tropical species reproduce throughout the whole year. Thus, for instance, 8. elegans a t Port Erin (Pierce, 1941) has only one maturity period, from Januaryto April according to the data of 1936, from February to May according t o data gathered in 1937. It appears therefore that seasonal conditions may have an influence on the period of seuxal maturity. I n the North Sea (Wimpenny, 1937) and off the island of Nantucked (GeorgesBank), the periods of maturity may be two, one in spring and one in autumn (Clarke et al., 1943). Differencesin length among the specimens in the third stage have been

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related to variations in temperature in the course of the year. The longest specimens are to be found in the colder periods. The whole life cycle of S. elegans off Plymouth is, according to Russell (1932a,b), 43 days, and from this he suggests that there may even be five generations each year in the waters of southern England. The reproductive cycle of S. elegans arctica in the Canadianeastern Arctic has been described by Dunbar (1941, 1962) who has observed that this species has a life-span of two years. The spawning period is long, from July into the autumn and winter. The breeding cycle is two-phase or alternating, such that during the spawning season there are three broods, the smallest of which is the offspring of the largest, with an adolescent intermediate group which will spawn the following year and is normally reproductively isolated from the other (Dunbar, 1962). If this cycle is rigidly followed without any change in rhythm, a genetic isolation between the individuals born from the different spawnings might occur, which in the long run could lead to some degree of differentiation, and make even phenomena of speciation possible. The breeding cycle is determined by the slow growth rate at low temperature, to which there has been no adaptation, and not by the maximum abundance of food for the young. Hydrographical differences though not great are reflected in the biology of S. elegans arctica. Atlantic waters seem to be of some importance in their reaching earlier or later sexual maturity. I n the specialized environment of Ogac Lake which is typically warm water, the growth rate is rapid and the breeding cycle is single phase or unalternating as in cold waters. Maturity is reached at less than half the body length required in cold water (Dunbar,1962). Environmental factors have also a great influenceon size and duration of life. McLaren (1966) gives a new explanation of the known phenomenon that zooplankton organisms of the high latitudes generally develop slowly, reach a large size and live longer than the related forms of warmer waters. McLaren states that where generation length is set by marked seasonality of food supply, as in the Arctic, high fecundity and associated large size and slow development may be selected for. It is shown from analysis of the functions-length, fecundity and natural mortality -of S. elegans that large size and the two-year cycle in the Arctic seas are not signs of poor adaptation but are optimal solutions to living-in highly seasonal conditions. Reverting to S. gazellae, David (1955) examined the vertical distribution of individuals according to their age. Mature specimens can be found only at depths over 750 m, the first stage is observed prevalently at depths between 50 and 100 m, the second between 500

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and 750 m, the third between 750 and 1000 m, while the individuals of the fourth stage can only be found a t greater depths. This species migrates vertically downwards during the winter to deep waters. The different stages of maturity of S. decipiens have also a typical vertical distribution in the southern Adriatic and in the Bay of Naples (Gamulin, personal communication). S. gaxellae is typical of Antarctic waters. During winter and spring its length increases by 5 mm per month; growth is quicker in the summer months, the life cycle is one year and the animal achieves 60 mm in length in 10 or 11 months (David, 1958b, 1965). According to David the species lives oiily in Antarctic waters: consequently, the forms described as S. lyra gaxellae of the Mediterranean (Ghirardelli, 1950a) must be considered as young specimens of S. lyra (Hamon, 1962). It is, nevertheless, possible that S. gazellae has diverged from the same stock as S. lyra at a fairly recent date as an adaptation to cold-water conditions (David, 1965). Interesting observations are those of Reeve (1966) on the biology of S. hispida of Biscayne Bay (Florida). This species has one main breeding season from November to March followed by a period of summer inactivity, after which the period of rapid growth and maturity in the latter part of the year begins again. The majority of the individuals of this species do not live beyond the first year, a small proportion continue through into the second year, and a smaller fraction still, according to Owre (1960), live t o their third year. S . hispida were kept in the laboratory and fed living plankton, particularly copepods over 1 mm such as Acartia or naupliiof Arternia of the larger size ;in the experiments, they were found to have food preferences based on both size and quality and mobi1ity”ofthe food. This species shows a maximum feeding activity a t a temperature of approximately 25°C. The fluctuations of populations of S. hispida are connected with the abundance of food. When the number of adult copepods increases in October, the population of X. hispida shows a significant gain in size, maturity and number. The average increase in size in the laboratory, in 15 days, is 3.83 mm. S. in$ata shows a marked polymorphism in relation with the stages of maturity. This species is present in the Gulf of Naples in two forms which are morphologically distinct, and in each of which two phases of sexual maturity can be seen (Ghirardelli, 1951): this is quite similar in the seas to the behaviour described by Thomson (1947) for S. in$& south-east of Australia. The two forms of Sagitta are characterized by the ovaries whose length in one form does not extend beyond the anterior end of the posterior fins ; in the other they do, and their eggs are lined up reguIarly, in contrast to the short-ovary form whose eggs

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are massed without any definite order. S. inJlata with long ovaries has the tail section proportionately shorter than the form with short ovaries. It was thought a t first (Ghirardelli, 1951, 1952) that they were two separate races or two ecotypes. Later it appeared more probable that the two forms of S. inJlata are but two aspects connected with sexual maturity. Such conclusions are confirmed by cytological researches on the stages of sexual maturity (Ghirardelli, 1961a). Through these researches it has also been possible to confirm the protandry of S. inJlata and the existence of a t least two successive cycles of activity by the female gonads. The short-ovaried form almost certainly corresponds to the first period of maturity of the ovaries, the long-ovaried form to a later period of sexual maturity. Both in the first and in the second form, there may be a t least two separate phases of sexual maturity of the ovary. Furnestin (1957) has come to the same conclusion as far as the Mediterranean specimens are concerned ; in the tropical Atlantic she has observed that there can be three or even four phases of maturity. Also S. inJlata of Spanish waters shows, according to Massuti-Oliver (1954) two phases of sexual maturity, one in February-March and one in October. By biometrical research (Ghirardelli, 1962) further confirmation has been obtained of the data provided by the cytologica1 researches and thc direct observation of living specimens. Indeed, the length of the gonads, though not always strictly related to the total lcngth, is nevertheless connected with the dimensions of the specimens and actually with their age. It is, however, apparent that, the total lengths being the same, there may be specimens whose ovaries show quite different dimensions (in connexion with the stage of maturity) since there may be individuals more or less mature in their female sex, or there may also be individuals which have just laid their eggs, and in these the ovary, as we have said, undergoes a remarkable shortening. Similar observations have been made on X. setosa by Dallot (1966, 1967). Cytologically, such secondarily shortened ovaries show the same features as those of specimens which have for the first time reached a younger maturity stage, namely stage 2, corresponding to the second growth period of the oocytes (Ghirardelli, 1961a,c). If one considers that a t a length of 11 mm in the Gulf of Naples there are already mature specimens (for Furnestin, 1957, the minimum length should be 13 mm), and that there are mature specimens also at 18 mm, the reasons for the great variability of the ovaries in comparison with the total length of the animal become still clearer. The existence of two groups of individuals is also confirmed by the diagrams showing the ratios of the total length and

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caudal section (Ghirardelli, 1962). As far as the total lengths are concerned, the diagrams show a normal distribution, while those concerning the caudal segment confirm that two groups of individuals exist, though there is a good connexion between total length and the length of the caudal section which increases with the increase of the length of the body: at equal dimensions, however, there is a certain degree of variability. I n the Indian Ocean, Rao and Kelly (1962) have observed in S. injata a variation in size during the year : the maximum length of the body is coincident with the abundance of copepods. Stone (1966), in a study of S. inJEata of the Agulhas Current in South Africa, has observed that the specimens collected in neritic waters contained more eggs than those from oceanic waters. He postulates that the differences in the number of eggs per individual, between the two areas, is advantageous to the species. This adaptation would actually ensure that the species has sufficient reproductive potential to maintain populations in the oceanic area, and particularly in the neritic area which is characterized by a wide range of physical and biological parameters. Seasonal variation regarding not only reproduction but also the corona ciliata and collarette have been observed in S. crassa. First Tokioka (1940) reported some variations in these characters, and afterwards Kado and Hirota (1957) and Hirota (1959, 1961) distinguished four classes of S. crassa according t o the form of the collarette : class A is S. crassa typica, class D is the form naikaiensis and B and C are intermediate forms. X. crassa in the Sea of Mukaishima has three alternating main spawning periods, February-March, May-July, November-December, in which the generation alternates. In the two generations that the individuals mainly spawn from May to July and from November to December, the collarette belongs t o class D or C in low degree. But in the generation which the individuals mainly spawn from February t o March, the collarette is able to develop in order into class C, B and A ; the collarette comes into class C from December t o January, into class B from January to February and into class A in and after February. The development of the collarette is related to temperature and salinity. A and B forms are stenohaline and stenothermal (Hirota, 1959, 1961). X. crassa was accurately studied also by Murakami (1959) in the field population and in the laboratory, and the results of the rearing experiments were advantageously used in interpreting the results of the examination of field samples. I n this manner it was demonstrated that the forms of the collarette depend on the temperature. Both spawning

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and the release of the sperm are repeated more than twice at intervals of several days. The period from spawning t o hatching changes with water temperature and chlorinity and a minimum of 15 h was recorded a t the temperature above 27OC. The optimum range of chlorinity for 8. crassa is 17-18%. It has been remarked in Spadella cephaloptera (Ghirardelli, 1959c, 1960, 1963a) that at the end of spring and the beginning of summer some specimens can be found whose total length is on average more than that of the individuals observed in later months. Also the ovaries of individuals gathered in May are longer than those of the specimens collected in June, August and September : this can be explained easily considering that the average number of the eggs found in May in individuals in the Bay of Villefranclie is sixteen ; this number decreases to tcn in June, seven in July ; in later months normally from four to two, or even one, eggs can be seen in the ovaries. On the basis of the diminution in number of eggs laid, one could presume that the spring specimens can survive until autumn with several successive spawnings; but the progressive reduction in their length excludes this thesis. The distribution of the stages of maturity in the spring-summer period, leads one to suppose that maturity can be reached in about 2 months: 1 month from hatching to the beginning of oogenesis and spermatogenesis, and 1 month for the maturation of the gametes. This hypothesis is confirmed by observations made on specimens which have been grown in the laboratory from egg to adult. After spawning, the ovary shows a state of maturity similar to that of the younger specimens, because one sees only oocytes in the first and second periods of growth ; these young oocytes will become mature later. I n the laboratory it has been seen that about 1 month separates two successive layings. The testis, on the contrary, once it has reached maturity does not show younger stages, but only differences in its activity in connexion with the need to re-fill the seminal vesicles emptied after mating (Ghirardelli, 1954a). It still remains to be ascertained whether the spring specimens are those of the previous autumn which have found refuge on the bottom, or are a generation born from individuals which have survived the winter, or are individuals born from eggs laid in autumn and fixed as usual to submerged objects. The first hypothesis would be valid only if the individuals which pass the winter are young ones born in autumn which have not yet reached sexual maturity: they would reach it in spring, increasing their dimensions at the same time. Observations made by Furnestin and Brunet (1965) in the port of Marseille, by Nouvel (1935) at Roscoff and by John (1933) at Plymouth, confirm

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that one may find Spadella concealed in the silt on the bottom during winter months also. More precisely, from the observations by Furnestin and Brunet it appears that Spadella collected in the winter are smaller than the spring specimens and somewhat bigger than autumn and summer ones : this actually confirms thc possibility that individuals born in autumn or late summer survive the winter. For Spadella living in the prairies of Posidonia, it can be said with certainty that a direct conncxion exists between the growth, the number of eggs and the conditions of the habitat. I n springtime, the conditions become better and as a consequence there seems to be a quicker growth of the population and a greater production of eggs which rapidly repopulates the prairies of Posidonia. These observations also show the importance of laboratory experiments in order to establish the exact duration of reproductive cycles. This is also confirmed by the experiments of Dallot (1966) which I mentioned previously (p. 331). He found that in Sagitta setosa, kept under good conditions, the first batch of eggs spawned is regularly followed by another about 24 h later. This interval may increase considerably if food is insufficient. Actually an ovarian cycle continues as long as the animal is in good physiological condition. Dallot himself saw up to six successive spawnings in one individual; one kept for 20 days laid ninety-six eggs in 6 days; another laid thirty-four eggs all at once. The growth of the ovaries is noticeably quick: one individual, 79 mm long, belonging to the summer generation,showed an increase in ovary length from 0.25 mm (stage 2) to 1 mm (stage 4) in only 3 days; during this period the diameter of the oocytcs increased from 30 to 160 p though the total length of the animal remained unchanged. There might be a connexion between the intensity of predation and the stage of sexual maturity during a 24-11 cycle. It seems that S. setosa actually feeds more actively during the night and it is a t this same time that the oocytes grow more speedily (Dallot, personal communication). These observations show that the fecundity of S. setosa is more considerable than had been concluded from observations on the animals in nature. There remain, says Dallot, many questions still to be answered: the total length of the period of reproduction, whether the stock of oocytes which undergoes maturation is limited or not, what are the influences of the quantity of food available, of temperature and of the other hydrological and biological factors on the reproductive processes. As regards the number of spawnings and the duration of the spawning period, reference should be made to the review by Alvarifio (1965), who has gathered together data from many observations.

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O F THE CHAETOGNATIIS

IV. REGENERATION Only a limited number of experiments have been done on regeneration in chaetognaths. The observations of Kulmatycki (1918) and Pierce (1951) attracted my attention, since the conclusions of these two authors were in my opinion contrary to the general rule that animals in which there is a precocious determination of the germinal line do not have high regenerative powers. I n fact, accordingto Kulmatycki and Pierce, chaetognathsare gifted with considerable regenerative powers. Kulmatycki (1918) found that Xpadella could regenerate the whole caudal section, while in Xugitta, according to Pierce (1951), there is also regeneration of the head. As we have said, chaetognaths are animals in which the determination of the germinal line occurs quite early, and in general there are rather close connexions between regenerative power and the stage a t which the segregation of the germinal line occurs. Organisms with a precocious determination of the primordial germ cells have usually a very limited regenerative ability, never sufficient to allow the formation of complete new individuals from a part of the body, and they cannot regenerate important and large portions of their bodies. They lack the power of asexual reproduction by fission, by budding, and in short by all the different methods of blastogenesis (Ghirardelli, 1964d, 195913). By contrast, this power is often quite remarkable in those groups of animals in which there is no precocious determination of the germ-cell line, and in which a reserve of totipotential cells persists throughout their whole life, able to differentiate either into all somatic cells or into germ-cells. Now, chaetognaths completely lack the power of asexual reproduction and, even if their relation with other zoological groups is still not well known, they have been considered to be related to groups nearly devoid of regenerative power, as for instance the nematodes (see p. 356). All this suggested that the regenerative ability of the chaetognaths could not be as good as stated by Kulmatycki and Pierce. Therefore I have repeat,ed in Xpadella cephaloptera, with few modifications, Kulmatycki’s experiments and I have made some observations on material analogousto that described by Pierce, i.e. beheaded Xagitta inJEataand Xagitta sp. collected in plankton samples a t Villefranche and in the north Adriatic. Operations carried out upon Spndella are shown in Fig. 34; the cuts marked with the numbers 1-6 are the same as Kulmatycki’s, the cuts 7 and S correspond to new operations. The regeneration of the caudal fin is always very rapid (from 2 to 4 days), provided that the posterior part of the body proper has not been 12’

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damaged and the cut only affects the fin. Epithelial cells migrate towards the wound, where many of them appear in mitosis ; they only are responsible for the reconstitution of the fin rays and epidermal glands (Ghirardelli, 1959a). The lateral fins also may be regenerated, though more slowly, in 7-10 days. The caudal region sectioned at different levels in front of the seminal receptacles (cuts 2, 3 and 4) never regenerates. The cut muscles fold inside, a scar made of stratified

FIG.34. Diagrammatic drawing of the cuts made on Spadella cephnloptera in order to study regeneration (1-8). cl corona ciliats ; ov ovaries ;t testes ; 2f lateral fins ; S.V. seminal vesicles ;c.f. caudal fin.

epithelium is formed ; the inner cells of the epidermis vacuolize in 2 or 3 weeks a t the most, taking on the characters of definitive epidermal cells at the so-called "collarette ',. I n some cases (cut 3) the lateral fins fold towards the wound and fuse along the midline of the body (Fig. 35). The immature male germ cells remaining in the caudal coelom may continue their normal development up to the formation of sperms, but they cannot be shed to the outside because at this level the seminal vesicles do not regenerate. The latter, however, form again normally if damaged when the cut passes immediately beyond the position that they usually occupy (cut 7).

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If the cut is made directly behind the seminal vesicles, the caudal fin regenerates only rarely, or in a rudimentary manner ; if instead the cut is made more caudally, the damaged muscle bands extend after an initial contraction, the wound heals and the remaining parts of the caudal fin may grow up to form a normal fin. The muscle fibres never regenerat'e. I n this last kind of operation, a higher percentage of caudal fin regeneration was obtained in animals which were beheaded immediately after the amputation of the posterior end of the body : 56% fin regeneration in the decapitated animals against 36% in those not decapitated. We may, therefore, suggest that the presence of the head exercises an inhibiting action on the regenerative processes in the

co C.I.

FIG.

35. Cicatrization of the caudal region and regenerationof the lateral fins in Spudella cephuloptera ; c.Z. ciliary loop ;co collarette.

caudal fin, which perhaps might act indirectly via the ventral ganglion which supplies the trunk and tail (Ghirardelli, 1958a). I n the nervous system, some regenerative power is detectable in the ventral ganglion (Ghirardelli, 1958a). By contrast to the tail, the head of Spadella never regenerates (Ghirardelli, 195613, 1959a). Sometimes a thickened stump with some resemblance to a, head is formed, but in it the hooks, teeth and eyes never regenerate. The cephalic stump consists of some (four, five or more) epidermal cell layers which in the beginning are flat and cover the muscles ; the latter shorten after the cut. As we have seen in the caudal region, the epidermal cells progressively vacuolize, taking on their irreversible and definitive characters. In beheaded specimens, ripe eggs may still be laid after the operation. The unripe oocytes regress, however, probably owing to fasting,

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because obviously the decapitated animals cannot take food (Ghirardelli, 195613). Contrary t o what Pierce (1951) stated, I have been unable to observe even in Sagitta instances in which one may state with certainty that the head has regenerated. I have been able to section some specimens found in plankton in which the cephalic stump is always formed by epidermal elements that have acquired their definitive and typical characters (Fig. 36) (Ghirardelli, 1959b). I have lately found in the Adriatic some ten specimens of different species of Sagitta (8. setosa, S. minima, S. inJlata) in which the head shows some anomaly: it is

FIG.38. L e f t : anterior region of thc body of a beheaded Sagitta showing the cicatrization stump cr. Right : anterior region of the body of a bcheaded Spudella cephuloptera. The cicatrice cr is m a d e of a multistratified epidermis having the characters of the definitive epidermis ;i intestine. (x 250).

smaller than normal in comparison with the dimensions of the body and it lacks teeth and hooks. We lack, however, positive proof that these are structures in process of regeneration rather than specimens whose head has been wounded with total or partial amputation of teeth and hooks. I n nature,Sagitta may be beheaded or cut in half by predatory animals like fishes. I n some instances it is apparent that the wound closes ; in the animals in which the amputation has occurred a t the height of the ventral ganglion or just behind, a more or less sharp stump may form, which histologically has the same features as those of a definitive scar. This leads one to think that there cannot be further processes of differentiation and regeneration. There is no way of knowing how long these phenomena may last, nor how long the animals may so live. I n some specimens the stump is more rounded, and one

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may even see the eyes. I n this case, however, there is always doubt as t o whether it is true regeneration or a more or less perfect repair of an extended lesion of the cephalic region. Specimens with such features are alas quite exceptiona,l and are usually to be found in plankton samples which are generally fixed in such a manner that no careful histological researchesare possible. On the other hand,Sagitta beheaded for experimental purposes do not live in the laboratory longer than a few hours, thus making any further observation impossible. The subject is, however, very interesting and it deserves further study. I think, however, that instances of regeneration, if any, should be considered exceptional, otherwise it ought to be easy to find specimens in all phases of “regeneration ” so as to form more complete series than those of Pierce and my own. Further, as we have said before, the deficiency of regenerative power of the Chaetognatha is part of a more general picture (Ghirardelli, 1959b, 1965b). I n fact, not only the chaetognaths but also other animals, whose eggs contain a germinal determinant rich in RNA, lack extensive regenerative power, irrespective of their systematic position. A germinal determinant, associated with poor regenerative power and an absence of asexual reproduction, must therefore be a result of an analogous evolution in animals very different from each other (e.g. Chaetognatha,Cladocera, Copepoda, Rotifera, anuran Amphibia, etc.), involving the disappearance of those totipotent or a t least pluripotent cells which constitute the so-called “embryonic reserve ”. To the lack of regenerative power therefore, no discriminating character can be ascribed, supporting the relationship of the chaetognathsto any specific zoological group (Ghirardelli, 1965b).

V. AFFINITIES AND SYSTEMATIC POSITION After Slabber’s discovery ill 1769, several authors have tried to establish the affinities and the systematic position of the Chaetognatha (Ghirardelli, 196313). Two excellent reviews of works dealing with the affinities of Chaetognathaare to be found in Kuhl’s monograph (1938) and in Hyman’s treatise on zoology (1959); the majority of the data which follow are taken from these works. Darwin ( 1844), referring to Xagittn, said the species of this genus are to be remcmbered for the “obscurity of their affinities ”; in the same year Krohn refuted the conclusions of some previous authors, among whom was Darwin himself, who supported the existence of affinities between chaetognaths and molluscs. Krohn believed the chaetognaths to be rather nearer the anellids, whereas Huxley (1851) presumed they were related to the Arthropoda. Gegenbaur (1853) also denied the

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affinity with molluscs, since he did not find any likeness between the embryonic development of chaetognaths and molluscs. Leuckart (1854) classified Xagitta among the worms, but since he was unable to give it a precise systematic position within the known forms, he instituted the group of chaetognaths, which he placed between nematodes and annelids. Gegenbaur (1859), after further researches about Xagitta, instituted the new class of the Oestelminthes placed between Nemathclminthes and Annulates, all under Vermes. The name of Oestelminthes was later dropped by Gegenbaur (1870) himself and replaced by the former name of Chaetognatha, without, however, modifying the previous systematic position. Schneider ( 1 866) allied Chaetognatha with Nematoda in the phylum Nemathelminthes, based on the identical arrangement of the muscular bands in the two groups. Metschnikov (1867) stressed the affinities of chaetognaths with somc marine nematodes (i.e. Draconematid and Epsilonematid). Kowalewski (1871), aftcr a careful study of the development of the mouth and of the coelomic sacs, was unable to decide whether the affinities with molluscs or those with worms were more relevant. Hertwig (1880) dealt with the affinities of chaetogiiaths from the aspect of the theory of the germ-layer and first believed them to he near the gordiaceaiis for some features and near the annelids for others ; he did not, however, reach a definite conclusion, since he lacked the elements to decide whether the coelom is originated by enterocoelia or schyzocoelia. The cmbryology of chaetognaths still presents in our day several blank spots, especially about the origin of the body cavity and of some organs. Grassi ( 1883) examined particularly the affinities of chaetognaths with brschiopods, echinoderms and hemichordates. The differences he found, however, especially on the origin of the coelom and of the mesoderm, were such that in his own opinion it was not possible t o believe that t-he chaetognaths were connected with these groups. Affinities have also been suggested with coelenterates (Hertwig, 1880) and even with the vertebrates, as Meissner (1857) described a dorsal chord under the brains which, howcver, does not exist at all. Butschli (1910) placed Chaetognathaamong the worms and particularly among the Oligomera, which have the coelom divided into three cavities. Butschli’s classification, though it was apparently artificial, has been incliplicably accepted, says Hyman, in a treatise as important as ‘‘Handbuch der Zoologie ” (Kukenthal and Krumbach, 1923-63).

I n order to conclude this list, we may note that according to Kuhl the Chaetognatha have been considered as related to the Mollusca eight times, mainly on account of their form and the structure of their

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nervous system. They have been considered as related t o the Vermes Oligomera six times and placed near the ncrnatodes five times, twice near the annelids and once they have been connected to cach of the following groups : gordiaceans, crustaceans, arachnids, hemichordates and chordates. Finally, Hyman notes some likeness between Chaetognatha and Aschelminthes or pseudocoelomote groups based on the features of the adults : viz. Kinorhyncha, Priapulida, Rotifera, Gastrotricha, Nematoda and Gordiacea or Nematomorpha. However, on considering the larval characters and their manner of development, Hyman herself doubts whether the affinities between Chaetognatha and Aschelminthes are real, and is rather inclined to believe that they constitute an independent branch of the Deuterostomia ; this also because there "is the possibility that the chaetognaths are remotely related to the dipleurula ancestor of the other Dcutcrostomia ". MacBridc (1914) and Burfield (1927) considered the chaetognaths as a non-modified branch of Protocoelomata from which all other coelomata would derive. Lately de Beauchamp (1960) agrees with the conclusions of Claus et al. (1932) and of Hyman, in considering chaetognaths as a completely isolated phylum ; according to him, this could be even the most isolated group in the animal kingdom. Incidentally, Grassi had also come t o similar conclusions when writing : From the comparisonsmade, it is clear and apparent that as far as is now known, between Chaetognathaand any other type no relation exists which might be firmly believed to be close. Some resemblances which taken by themselves might seem t o be the expression of such a relation, when compared-as it is logical-with the relevant differences, are reduced t o simple analogies,or secondary convergencesor perhaps even t o very far affinities. (Transl.) I n my opinion, the fact that chaetognaths may show affinities or resemblances to such widely separated groups may actually prove that there is no real affinity with any of those groups. Indeed, all living organisms arc built accordingto a limited number of models of organizations, which selection has often established as the fittest for a certain habitat or manner of life ; consequently some of them are repeated in more or less identical form even in very widely separated groups. I n the majority of cases, these are simple analogies or instances of convergence, without any true homology. At this point one may ask whether-at the present state of our knowledge and considering also the most recent researches-there are still positive reasons for considering the chaetognaths to be related to one of the existing zoological groups and whether it is still worth while following the principles of the major authors of the nineteenth and

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beginning of the twentieth centuries in looking for unity in the animal world ; or whether i t is nearer the truth to believe the chaetognaths to be a group completely isolated from any other. We should therefore reconsider, under the light of these remarks and taking into account the most recent researches, the affinities that have been proposed between Chaetognathaand other phyla. As to their origin, the very few fossils known tell very little: they all belong to the same period and the same species. We only know that Amiskwia sagittiformis Walcott of the middle Cambrian in British Columbia, had no caudal septum (Walcott, 1911), the origin for which Grassi (1883) thought could be due to the necessity of separating the female gonads placed in the trunk coelom from the male ones, placed in the tail coelom, thus avoiding self-fertilization. Amiskwia is considered to be related to Sagitta. It seems to me, however, more like Spadella both in the general shape of the body, because it has only one pair of lateral fins, and because it has tentacles on the head: all these are typical features of Spadella rather than Xagitta. The size is, however, larger in Amiskwia (ca 20 mm against 5 or 6 mm at the most in Spadella cephaloptera). Furthermore in Amiskwia, contrary to what can be seen in all chaetognaths, the intestine ends a t the caudal end of the body and not at the caudal septum : this is quite a significant difference from the present-day chaetognaths. On the other hand, this fossil tells little of the evolution of the group, because it is the only one and also because no other organ is visible except the intestine. Owre and Bayer (1962) also believe that there are resemblances between Spadella and Amiskwia, but they conclude that the latter is not a chaetognath but rather a nemertine, closely related to Nectonermes rnirabilis Verrill, mainly because of the structure of the intestine, which is longer than in Chaetognatha, and the absence in Amiskzuia of the gonads, which in the opinion of these authors should have been preserved, if present, in the same way as the intestine was fossilized. The lack of a caudal septum also supports the attribution of Amiskwia to the nemertines. Thus, all phylogenetic considerations based on the study of this fossil fail. We have seen that Tokioka (1965a) though feeling some doubts as t o the actual affinity betwccii Amiskwia sagittiformis Walcott and chaetognaths, establishes for this species the Class of extinct chaetognaths Archisagittoidea. Some further affinities with other groups have now to be examined, even though they appear in some instances t o be rather weak. As for coelenterates, there remains the possibility of a comparison

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between the coelenteric cavity and the coelom of the chaetognaths. Apart from the different origin of the two cavities, the Chaetognatha are typically triblastic animals, much more differentiated than coelenterates. The affinities with the Echinodermata are limited to the very first phases of embryonic development. Chaetognaths,however, have only two primary divisions in the coelom and no true larvae, while there are three primary divisions in the coelom of echinodermsand hemichordates, which have larvae that can be referred to the dipleurula. MacBride’s (1914) consideratioiis which refer the chaetognaths to a very early blind offshoot of the Protocoelomata, which should be represented today by the Ctenophora and during the ontogenesis of the Bilateria by the dipleurula and the trochophores, are but interesting speculations, though in this way they allow the connexion of chaetop a t h s to the other bilateral Metazoa. On the other hand, though it be true that embryology may often supply elements for the Iocation of affinities between groups which a t first sight seem far apart, it is also a fact that the ways of segmentation of the eggs are few, depending on the type of egg, and often depending on the characterof the environment in which the organism lives. The relations with brachiopods, based on the comparison made by Lameere (1931) between the hooks of the chaetognaths and the lophophore, are not supported by the data obtained from the morphology of the adults nor by those obtained by studying the development. Lately the problem has been again resumed by Hadii (1963). I n his opinion the Chaetognatha derive “ b y way of neoteny from the planktonic larvae of Brachiopoda ”. They are archicoelomataand also constitute an actual aberrant group because, among all the Oligomera where Hadii places them, they are the only ones which can lead a pelagic life ; their adaptation could just be explained by their origin. Affinities with the arthropods could be based only on the structure of their nervous system and the presence, if any, of chitin in the tegument and in the tegumentary formations, though it is opportune to recall that chitin is not to be found in Arthropoda alone. There is, on the contrary, no sign of metamerism and the development shows quite a different pattern. I do not see how affinities with arachnids can be supported, as Huxley (1851) did, or with crustaceans, even with strongly modified forms like some parasitic copepods (Lernaea) or with cirripedes. Crustaceans, aIso, always have typical larvae which have allowed workers to establish with certainty that even the aberrant forms we have mentioned are crustaceans.

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The form and transparency of the body make Chaetognatha look somewhat like heteropod molluscs. The large species of Xagitta undoubtedly recall Pirola and similar species, but it is certainly a case of convergence. The nervous system does not show signs of chiastoneuria, even if the general organization may present some resemblance to that of molluscs, mainly as regards the position of the ventral ganglion which might be homologized with the pedal one of the Molluscs. There is no sign of a foot, however, and the supposed homologies between the radula and the mouth armature of the chaetognaths are certainly rather forced. There remain then still to be seen only the affinities between chaetognaths and annelids and nematodes, the groups which they seem more t o resemble. As far as annelids are concerned, both they and the chaetognaths have four longitudinal muscles which in section show a characteristic herring-bone disposition ; but in chaetognaths there is no circular musculature or any oblique muscle. The ventral ganglion of the Chaetognatha could be considered as a derivative of the ventral chain of the annelids, due to a concentration of ganglia. There is also some likeness between the hooks of the chaetognaths and the bristles of the annelids as far as their constitution is concerned. The hooks (Schmidt, 1951, 1952; Hyman, 1958) and the bristles seem actually to be of a chitinous nature, in both groups ciliated cells are prrsent and the ciliated funnel by which the male genital orifice opens to the outside, recalls the nephrostoma of the annelids. The study of the embryonic development, on the other hand, offers really few elements in support of affinities between chaetognathsand annelids. The ways of segmentation are different, the mesoderma in the Chaetognathaforms from the diverticula of the archenteron,in the annelids from the coelomic sacs. The adult annelids have a true coelom while the Chaetognathahave the appearance of pseudocoelomate animals. The only typical coelomate structures are the ciliated funnels of the sperm ducts (Hyman, 1959). There is no metamerism in the Chaetognatha, neither during the development of the ventral ganglion-which as we saw originates (Ghirardelli, 1958b) from a common anlage together with the nervous part of the ciliary loop-nor during the development of the gonoducts. Furthermore,Chaetognathaseem to lack excretory organs. The ciliary loop which Reisinger (1934) considered a solenocytic protonephridium would seem to have mainly sensory functions, and in its glandular region a secretory but not excretory function (Ghirardelli, 1959e). Reisinger (1968 in press) proposes again some affinities between ehaetognaths and the Chordata. He notes an analogy between the endostyle

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and the neural glands of the tunicates and the retrocerebral organ of the chaetognaths. Scharrer (1965) while noting a superficial likeness between the retrocerebral organ and the glomeruli that form the neuropile of the nucleus rotundus in the tegumentum of the teleostean mesencephalon, stated after examination of the retrocerebral organ with the electron microscope, that the masses of microvilli of the retrocerebral organ are similar to those described in the cerebral ganglion of the crustacean Leptodora. The occurrence of cells with microvillous borders in the central nervous system of the representatives of two different phyla, suggests a role related to functional requirements that the types of animalshave in common (Scharrer,1965). Reisinger further finds a significant likeness between the ultrastructure of the ciliary sense organs (" neuromasten ") of the chaetognathsand the sensory cell of the lateral line in the Anamniotes. Furthermore, the fin rays of actinotrichiantype with substance similar to elastoidin, remind one of those of the fins of cyclostomes and fishes and are not to be found in other invertebrates beside chaetognaths. The likeness to the Nematoda is more obvious. Like them, the chaetognaths show a cephalic armature and a cuticular lining of the body. The lateral fins could perhaps be considered similar to the alae of nematodes. The musculature is placed in four longitudinal fields, and as we have seen the adult chaetognaths have the appearance of pseudocoelomate animals like the nematodes. Also the macroscopic and microscopic structures of the intestine are similar. Other features in common are the precocious differentiation of the germinal line and the almost total inability to regenerate the amputated parts. The differences, however, are not less important. The hooks of Chaetognatha, as we have seen, have a chitinous nature, while the supposed chitin of the body-lining of nematodes is to be considered as a secreted collagen in which keratin is perhaps present but no chitin (Rizzoli, 1956). The nervous system in the two groups differs considerably. The muscular system has only the distribution of the muscular bands in four longitudinal fields, similar to that of the nematodes. This disposition is, however, common, as we saw, t o annelids also and it serves to ensure the movement by contraction of the body, in all directions, with the minimum number of muscular bands possible. The histological structure of the musculature of Nematoda and Chaetognathais quite different. The muscles of the Chaetognathashow indeed typically striated fibres. Camatini and Lanzavecchia (1966) have lately observed this fibre under the electron microscope. They were able to see that within each fibre there are numerous myofibrillae with traiisversc striae in line with cach other. Almost all of the sarcomerei

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represented by band A while the band I is particularly short. Also a short band H is apparent, as well as a zone in t,he centre of band I that can be compared with stria Z even if it shows a peculiar morphology. I n transverse sections of band A, the primary and secondary myofilaments show a reciprocal disposition practically identical with that described in the wing muscles of insects: the secondary filaments are placed a t the centre of the segment of the line connecting the two primary filaments. In band H only the primary filaments are visible ; a t the limit between bands A and I, the diameter of the primary filaments decreases till it becomes the same as that of the secondary filaments, about 70 a, and then they disappear. The appearance of the primary filaments is also peculiarly like that of the insects (Fig. 3 7 ) .

FIG.37. L e f t ; transverse section of muscle of Sagitta, under elcctron microscope, low magnification. One can see the subdivision of thc fibres in many mioflbrilles, and the well developed sarcoplasmatic reticle. Right; transverse section a t the level of band A. One sees the double hexagon organization of primary and secondary filaments. The primary filaments are clearly hollow. (From Camatini and Lanzavecchia 1966.)

Considerable differences from Nematoda are to bc notcd in the structure of the reproductive apparatusand in thcir method of growth which in Chaetognatha does not occur by moulting. Another of the most significant differences is the presence in chaetognaths of vibratile epithelia which are to be found in the ciliary loop, in the intestine and in the funnel of the spermiduct. It is well known that the vibratile epithelium is missing in the nematodes. Regarding this question Browne and Chowbury (1959) described cilia in the intestine of Ancylosfomu

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caninum but Aiidreassen (1966) says that the intestine of this nematode is not covered by cilia but has a brush border composed of microvilli ; if the cilia are t o be found in nematodes they must' undoubtedly, as in arthropods, be searched for in the sensory organs, and he concludes "that cilia have not been found in nematodes ". Nevertheless, Ross (1967) described modified cilia in sensory organs of juvenile stages of the parasitic nematode Haemonchus contortus, and Roggen et al. (1966) by electron microscope studies reveal the presence of true cilia in nerve processes connected with sensory organs of another nematode (Thoracostomn cabifornicum). Also in this case there are not vibratile cilia but, nevertheless, Rogger et al. say that the cilia which they have described lessen the gap that exists between the nematode and the remainder of the aschelminths. I n any case cilia are very ancient structures in the cell, originating before the subdivision of t8heplants and animals; in fact they have an identical structure in animals and in plants (Lanzavecchia, 1967). For this reason they may not have an indicative value as an evolutionary character. Chaetognatha,according to Colosi (1967), could be classified among the trichophores deuterostoma, while the Nematoda, like Gordiacea, Tardigrada and Arthropoda must be considered as atricha. Other authors (e.g. Grassi, Hyman) place Chaetognathabeside Brachiopoda, Phoroiioidiei or Pogonophora. Hadii, as we have seen, shares this view. D'Ancona (1966) places them among the Deuterostoma before Pogonophora and Pterobraiichia. Salfi (1965) also places them among Deuterostoma but before Echinodermata, which in his classification precede Enteropneusti and Pterobranchia. That they belong to Deuterostoma has been questioned. Hadii, incidentally, no longer believes in the division of animals into the two groups of Deuterostoma and Proterostoma. According to Hyman, "the possibility that the chaetognaths are remotely related to the Dipleurula ancestor of the Deuterostoma, is the only justification for placing them, as done here, among the Deuterostomia ". Eakin and Westfall (1964) relate the chaetognaths to the Deuterostomia, i.e. Chordata and Echinodermata,on the basis of the structure of their photoreceptive cells. The eye of Sagitta appears to be of a ciliary type : this, according to Eakin and Westfall, should place them among Deuterostomia since the photoreceptors of Proterostoma (Arthropoda, Anellida, Mollusca and Plathelminthes) are of a rhabdomeric type. According to Lanzavecchia (1965) it should be kept in mind, on the other hand, that though the cilium has a structure of the type 9 0 (like vertebrates) the outer segment has a rather primitive structure, being constituted by microvilli placed parallel with the

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dircction of the cilium, and in some respects it recalls those of the Hydrozoa. Furthermore, observations made on some Protostoma reopen the whole problem, making a deeper analysis of photoreceptive cells necessary, in connexion with the problems of phylogenesis. In fact, in the polychaete annelid Branchiomma vesiculosum the cilia transformed into photoreceptive elements, have lost the two inner 0 typical of Deuterotubules, and have therefore the symmetry 9 stomia. Afzelius (1963) has, however, found in the flagellum of mature 4 sperms of Sagitta elegans some cases in which the filaments were 9 or 10 4. Some considerations on the phylogenesis of neritic chaetognaths are reported in Alvariflo (1963) who stresses the great similarity between neritic species, and by Tokioka (1Y65b). According to the latter, the neritic forms-which for swimming should not need a transversal musculature-should have derived from the species of the subclass Phragmophora, with transversal musculature which is useful for movements on the bottom. From the neritic forms would derive the oceanic species and from these in turn the meso- and bathypelagic species of Aphragmophora. I n Tokioka's opinion, primitive characters would be the corona present only on the head and the pronounced length of the caudal section, as can be observed in Spadella and Pterosagitta. I n conclusion, I do not think that any of the elements which have been considered can actually determine the position of Chaetognathain a natural classification. They are in any case animals of a rather elevated organization, perfectly adapted to their habitat, though these remarks are no great help in clarifying their affinities a i d their systematic position. There is in my opinion, a t the present state of our knowledge, nothing else to do but to accept the conclusionsreached by the majority of the authors quoted above and say with Grassi (1883) : ''Credo insomma che le relazioni dei Chetognati rimangano oscure e sepolte, nB vedesi indizio che siano per essere scoperte fra breve "["I think after all that the relations of Chaetognatharemain obscure and buried ; nor is any sign to be seen that they might be discovered in a short while "1. Let us hope t,hat Grassi's pessimistic views may be dispelled in a shorter time than has passed since he expressed them.

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EXPERIMENTS VI. LABORATORY I n concludingthis review on the biology of chaetognaths,it is perhaps appropriate to quote observations made in the laboratory on living specimens by Stevens (1505, 1910), Kulmatycki (1918), Vasiljev (192Fi), ,John (1933), Reisinger (1934), Sanzo (1937), Jagersten (1940), Parry (1944), Ghirardelli (1950a,b, 1952, 1953d, 1954a, 1955, 1956a,b, 1958a,b,

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1959a,b, 1965b), Murakami (1959), Dallot (1966, 1967), Horridge (1966), Reeve (1964, 1966), Singarajah (1966), Horridge and Boultoii (1967). It has not been possible so far t o obtain in the laboratory the complete cycle of development in the pelagic species, but anyway the resn1t.s of these researches have supplied important information on the breeding cycle and reproduction (Stevens, 1905, 1910 ; Vasiljev, 1925 ; John, 1933 ; Jagersten, 1940 ; GhirardelIi, 1950a, 1952, 1953d, 1954a, 1956a; Dallot, 1966, 1967; Murakami, 1959; Reeve, 1964, 1966);regeneration (Kulmatycki, 1918 ; Ghirardelli, 195610, 1958a, 1959a,b, 196513); feeding (Parry, 1944 ; Reeve, 1966 ; Murakami, 1959 ; Horridge, 1966 ; Horridge and Boulton, 1967); corona ciliata and sensibility (Reisinger, 1934 ; Ghirardelli, 1958b, 1959a ;Horridge and Boulton, 1967);influence of environmental factors on morphology (Murakami, 1959) and on behaviour (Reeve, 1966 ; Sanzo, 1937, on eggs of Pterosagitta draco), and finally on chemical factors and centrifugation on the development of the eggs (Ghirardelli, 1955). Only few authors have reared for some weeks some species of chaetognaths (Ghirardelli, after 1953, Spadella ; Murakami,Sagitta crassa; Dallot, S. setosa, and Reeve, S. hispida). The reason for the few laboratory studies involving rearing of the chaetognaths, especially the planktonic ones, lies in the fact that these animals do not tolerate well the conditions of transport and those in the laboratory. Chaetognathsfor which there has been moderate success in experiments are S. hispida and S. setosa which are planktonic members of the phylum habitually frequentinginshore waters. Spadella cephaloptera is a benthic species also living in coastal waters on the seaweeds or marine phanerogams or even in rock pools. This chaetognath is quite resistant to laboratory conditions, undoubtedly because of its natural habitat. Spadella cephaloptera up to this moment is the only one species reared in the laboratory from hatching to sexual maturity (Ghirardelli, 1959~). VII. ACKNOWLEDGEMENTS The original observations recorded in the present article have been made principally a t the Zoological Stations of Naples and Villefranchesur-Mer, at the Biological Institute of Dubrovnik and the Zoological Institute of the University of Trieste, with the support of Consiglio Nazionale delle Ricerche, Rome. I remember with gratitude the late Prof. Reinhard Dohrn, former Director of the Zoological Station of Naples. I record my sincere thanks to G. Montalenti, Director of the Centro di Biologia of the C.N.R. at the Zoological Station of Naples, P. Bongis,

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Director of the Zoological Station of Villefranche, T. Camulin of Dubrovnik, P. Pasquini and E. Vannini, Directors of the Zoological Institutes of the University of Rome and Bologna, who have given me hospitality in their laboratories and placed material, instruments and libraries a t my disposal. I wish particularly to thank Prof. G. Tregouboff wit,h whom I began this work a t Villefranche many years ago. My thanks also due to M. L. Furnestin,A. Alvarifio, G. A. Horridge, G. Thorson and P. M. David who have sent me references and material for study or with whom I discussed some details of this work. Finally, I am most grateful to Sir Frederick Russell, who asked me to write this article, for his advice and for correcting the English translation. VIII. REFERENCES

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Author Index Numbers in italics

refer to pages on wh.ich the full

A Abbott, R. T., 242 Abduldi, H., 154, 242 Abe, N., 242 Abel, O., 242 Acosta Solis, M., 242 Adriani, M . J., 242 Ahlstrom, A. H., 20, 56 Afzelius, B. A., 364, 366 Al-Kholy, A. A., 251 Alegre, B., 19, 50, 56 Alexander, W . B., 82, 242 Allen, K . R., 18, 48, 57 Almodovar, L. R., 242 Altevogt, R., 201, 242 Alvarifio, A., 279, 289, 313, 343, 344, 350, 364, 366 Anderson, J . A. R., 83, 242 Andreassen, J., 363, 366 Andrews, E . A., 243 Angel, M . F., 243 Annandale,N., 157, 243 Aoyama, T., 28, 56 Areschoug, F . W . C., 142, 243 Argo, V . N., 243 Arnaud, J., 289, 290, 309, 310,366,371 Arnold, A., 244 Arriola, F. J., 216, 243 Ascherson, P., 220, 243 Aubreville, A., 243

reference is given

Balm, H., 230, 243, 244 Banerji, J., 244 Bannerjee, S . K., 244 Baranenkova, A. S., 20, 56 Barlow, B. A., 244 Barrett, C., 244 Barry, J. P., 244 BascopB, F . , 244 Bassindale. R., 82, 242 Bassot, J . M., 161, 244 Baumeister, L., 244 Bayer, A. W., 253 Bayer, M . B., 280, 358, 373 Becking, J. H., 244 Beer, C. G., 244 Belkin, J . N., 244 Bell, E". H., 22, 56 Benecke, W., 244 Bennett, I., 120, 221, 248, 266 Bennett, M . F., 244 Berry, A. J., 165, 244 Beverton, R. J . H., 9, 12, 16, 17, 18, 19, 22, 56, 59 Bews, J . W., 244 Bharucha,F . R., 244, 245, 259 Biebl, R., 242 Bieri, R., 343, 366 Bird, E . C. F., 254 Biswas, K., 244 Blatter, E., 244 Blegvad, H., 244 Blum, G., 245 Boelaert, R., 198, 269 Boerema, L. K., 19, 50, 56 Bogorov, V . G., 343, 366 Boissevain, H., 243 Bole, P. V., 245 Bolles-Lee, A., 289, 309, 366 Bonne-Wepster, J., 245 Booberg, G., 245 BordBs, M., 289, 290, 291, 295, 296,

B Baartman, T. A., 243 Bab&k,E., 213, 243 Backer, C. A., 243 Bakhuizen van der Brink, R. C., 75, 76, 112, 243 Bakhuizen van der Brink Jr., R. C., 243 Baldasseroni, V., 279, 343, 366 Ballenden, S. S t . C., 253

297, 298, 300, 303, 309, 311, 312, 322, 329, 335, 366, 367 377

13'

378

AUTHOR INDEX

Roughey, A. S., 245 Boulenger, G. A., 245 Boulton, P. S., 275, 276, 286, 365, 371

Champion, A. G., 96, 246 Chandler, M. E. J., 85, 246 Chapman, D. G., 9, 18, 47, 48, 57, 58

Bovcri, T. H., 309, 367 Bowen, B. K., 26, 5G Bowman, H. H. M., 76, 245 Bradstreet, E. D., 264 Brandi, M. L., 289, 311, 371 Bretzl, H., 76, 245 Brown, F. A., 244, 269 Brown, F. A., Jr., 245 Brown, W. H., 245 Browne, F. G., 241, 245 Browne, H. G., 362, 367 Bruce-Chwatt, L. J., 245 Brug, S . L., 245 Brunet, M., 349, 369 Brunig, E. F. W. O., 245 Ruchner, P., 289, 293, 297, 298, 300, 309, 313, 367 Buck, E., 161, 162, 164, 246 Buck, J., 161, 162, 164, 246 Buck, J. B., 246 Bucltley, T. A., 246 Buitendyk, A. M., 246 Rumpus, D. F., 344, 367 Burfield, S. T., 271, 282, 289, 290, 291, 357, 367 Burukovskii, R. N., 15, 56 Busch, W., 282, 367 Butler, A. L., 154, 246 Bntot, L. J. M., 218, 246 Butschli, O., 289, 292, 356, 3GS

Chapman, V. J.,134, 149, 220, 246 Chasen, F. N., 155, 246, 262 Chattaway, M. M., 246 Chatterjee, D., 247 Chaudhri,I. I., 247 Chhapgar,B. F., 224, 225, 247 Chiang, L. S. K., 247 Chittleborough, R. G., 26, 56 Chopra, B., 247 Chowbury, A. B., 362, 367 Christy, F. T. Jr., 22, 23, 55, 57 Chwatt, L. J., 251 Ciferri, R., 247 Clark, H. L., 232, 247 Clark, L. B., 247 Clarke, G. L., 344, 367 Claus, G., 280, 357, 367 Clements, A. N., 184, 247 Coaldrake, J. E., 122, 247 Cogger, H. G., 247 Collins, M. S., 247 Colman, J. S., 289, 367 Colosi, G., 363, 3 G i Conant, S., 343, 3137 Cooper, R. E., 142, 247 Cott, H. B., 247 Cotton, B. C., 247 Cowles, R. B., 247 Crafts, A. S., 247 Crane, J., 247, 248 Crichton, 0. W., 245 Crosnier, A., 216, 225, 228, 248, 252

C Carnatini, M., 361, 367 Cameron, A. M., 201, 246 Campbell, B., 216, 217, 266 Campbell, B. M., 231, 232, 246 Cannicci, G.. 343, 367 Cantor, T., 246 Carter, J., 83, 136, 24G Cassie, R. M., 28, 56 Cawkell, E. M., 246 Champeau, M. F., 246

Crutchfield, T. A,, 9, 48, 57 Cuatrecasas, J., 248 Cuong, H. vu van, 111, 244, 248 Cursier, H. B., 247 Curtis, A. H., 248

D Daiber, F. C., 248 Dakin, W. J., 221, 248 Dale, I. R., 248

379

AUTHOR INDEX

Dall, W., 245, 261 Dallot, S., 289, 313, 322, 330, 331, 336, 338, 339, 347, 350, 365, 367 Daly, R. A . , 248 Dalziel, J. M., 248 D’Ancona, U., 363, 367 Danhof, C . N., 248 Darwin, C., 355, 361 Das, K. N., 247 Dautzmberg, P., 225, 218 David, P. M., 289, 313, 333, 343, 344, 345, 346, 3C7, 368 Davis, J. H., 76, 82, 83, 24X Day, J . H., 207, 221, 248 Dr 13eauchamp,P., 271, 279. 357, 366 De Beaufort, L.F., 227, 228, 244 Dc Haari, 89, 93, 96, 107, 124, 125, 252 de Sousa, J., 158, 269 Delevoy, G., 249 Den Berger, L. G., 244 Doraniyagala, P. E . P., 249 Deshpande, J. V., 85, 257 Dickie, L. K., 22, 57 Di Marcotulho, A., 328, 368 Donoaster, L., 289, 296, 368 Dotj, Y., 249 Doyne, H. C., 249 Dragendorff, D., 138, 267 Drakcnstein, H. A. R h e d e tot, 249 Dunbar, M. J.,289, 345, ,368 Dunn, L. H., 249 Dnrant, C. C. L., 249

E Eakin, R. M., 273, 363, 368 Edmonds, S. J., 222, 269 Edmondson, C. H., 249 Edney, E. H., 209, 249 Eggers, H., 249 Eggcrt, B., 152, 185, 194, 195, 249 Egler, F. E., 249 Ekman, S., 222, 249 Elinn, L., 279, 289, ,368 Elpatiewsky, W., 289, 292, 297, 298, 313, 316, 368 Ely, C. A., 249 Emery, K. O., 82, 129, 249

Emoulo, M., 139, 249 Enami, S., 249 Endean, R., 120, 266 Erichson, R., 250 $!saki, T., 266 Estampador, E . P., 217, 250 Eyerdam, W. J., 250

F Faber, F. C. 7.011, 141, 250 Fairbridge, R. W., 119, 250, 262 I.”ange,R., 264 Pantham, H. B., 250 F.A.O., 1, 2, 3, 45, 57 Fernando,C. H., 254 E’crnes, G. W., 250 Fingerman,M., 245, 250, 269 Fischer, A. I?,. 245 Fischer, K. I., 250 Fischer, P. H., 250 Fischer-Piette,E., 250 Fisher, C. E. C., 250 Fitz-John,R. A., 245 Flemister, L. J., 211, 250 Flemister, S. C., 211, 250 Forest, J.,175, 250 Fosberg, F. R., 82, 250 Fourmannoir,P., 251 Fowler, H. W., 251 E’oxworthy, F. W., 251 Frane, A., 251 Fraser,J. H., 273, 313, 343, 368 Freise, F. W., 251 Freyberg, B. V., 251 Furnestin,J., 343, 368 Firnestin, M. L., 273, 274, 279, 289, 291, 332, 333, 343, 344, 347, 349, 368, 369

G Gabo, M., 285, 369 Gaimard, P., 272, 373 Gamulin, T., 343, 369 Ganapati, P. N., 251 Ganguly, D. N., 258

380

AUTHOR INDEX

Garey, W., 142, 264 Garrod, D. J., 19, 57 Gaskin, D. E., 8, 57 Gagparovid, J., 344, 371 Gegenbaur, C., 355, 356, 369 Genkel, P. A., 251 George, P . C., 251 Gerlach, S. A., 165, 251 Ghirardelli,E., 272, 277, 279, 281, 283, 285, 286, 287, 288, 289, 290, 291, 294, 298, 305, 309, 310, 311, 313, 318, 319, 322, 223, 326, 332, 334, 335, 338, 339, 340, 343, 344, 346, 347, 348, 349, 351, 352, 353, 354, 355, 360, 364, 365, 369, 370, 371, 374 Giglioli, M. E. C., 251 Gilroy, A. B., 251 Gledhill, D., 251 Glover, P. E., 851 Gohar, N . A. P., 251 Goiny, H., 251 Golley, F . B., 252 Goodrich, E . S., 291, 371 Gordon, H. R. S., 252 Gordon, H. S., 22, 57 Gordon, I., 252 Gordon, M . S., 181, 182, 252 Graham, M., 8, 22, 57 Graham, R. M., 252 Grant, E . M., 257 Grass, B. F., 252 Grass6, P . P., 198, 252 Grassi, Q. B., 275, 277, 278, 279, 282, 289, 292, 297, 300, 322, 356, 358, 364, 371 Gray, €3. B., 330, 371 Gregory, D. P., 252 Grewe, F . , 252 Grobben, K., 280, 357, 367 Guilcher, A., 80, 82, 83, 129, 252 Guiler, E. R., 252 Guillaumin, A., 252 Guinot, D., 175, 228, 250, 252 Guinot-Dumortier,D. V . B., 252 Gulland, J. A., 9, 10, 16, 18, 19, 22, 28, 29, 48, 57 Gunther, A. C. L. G., 252 Guppy, H. B., 224, 232, 252 Gurney, R., 252

H Habe, T., 252 Hadfi, J.,359, 371 Hagor, L. C., 253 Hall, D. N . F., 217, 222, 228, 240, 253 Hamilton, A. A., 253 Hammel, H. T., 142, 264 Hamon, M., 346, 371 Harms, J. W., 75, 179, 185, 194, 212, 253 Harper, F., 253 Harris, V . A,, 195, 196, 197, 253 Harrison, A. D., 221, 248 Ha.rt, M. G. R., 253 Haug, -, 253 Hawkes, J., 234, 253 Hayson, N. M., 257 Heberer, G., 253 Hediger, H., 253 Hedley, C., 253 Hein, S. A., 198, 253 Heisch, B. B., 251 Hemmingsen, E . A., 142, 264 Henkel, J. S., 253 Herre, A. W. C. T., 185, 253 Hertwig, O., 275, 282, 289, 292, 309, 313, 318, 356, 371 Hesse, P. R., 253, 254 Hickling, C. F., 8, 58 Hill, B. J.,254 Hines, M . N., 254 Hirakawa, Y . ,254 Hirota, R., 274, 275, 282, 289, 343, 348, 371, 372 Hjort, J., 51, 58 Ho, R., 254 Hodder, V . M., 12, 56 Hodgkin, E. P., 254 Hoenigman, J., 344, 371 Holle, P. A., 254 Holt, S . J.,8, 9, 16, 17, 18, 19, 22, 48, 56, 57, 59 Hora, S. L., 254 Horridge, G. A., 275, 276, 286, 365, 371 Hosoe, K., 322, 375 Hosokawa, T., 233, 254 Hou, Ding, 150, 254 Hou-Liu, S. Y., 117, 259

381

AUTHOR INDEX

Huntsman,A. G., 289, 371 Hure, ,r., 3 t 4 , 371 Huxley, T. H., 292, 355, 359, 371 Hyman, L. H., 271, 274, 286, 355, 360, 3 72

I Iarogov, B. A., 15, 56 I.A.T.T.C., 17, 58 I.C.E.S., 10, 11, 19, 24, 28, 58 I.C.N.A.F., 28, 46, 58 Inger, R. F., 254 Ingle, R. W., 254 I.N.P.F.C., 47, 48, 58

J Jdgersten, G., 289, 291, 311, 322, 330, 332, 333, 364, 365, 372 Janssonius,H. H., 254 Jardine, F., 254 Jeffrey, J . W . O., 254 Jennings, J. N., 254 John, C. C., 271, 277, 282, 283, 289, 302, 318, 322, 323, 341, 349, 364, 365, 372 Johnson,D. S., 209, 254 Johnstone,J., 254 Jones, N. O., 363, 374 Jones, R., 8, 59 Jones, S., 255

K Kado, Y., 274, 275, 282, 348, 372 Kalk, M., 91, 126, 186, 193, 198, 203, 207, 214, 257, 265 Karsten, G., 256 Karsten, H., 198, 255 Keay, R. W., 255 Keferstein, W., 292, 372 Kelly, H. M., 181, 182, 252 Kelly, S., 348, 373 Kenyon, A. R., 47, 58 Kerr, A., 255 Khan, A. A., 255 Khan, S . A., 255

Khoo, K . G., 189, 191, 199, 200, 255 Kiener, A., 255 Kienholz, R., 255 Kiet, L. C., 244 Kimura, M., 193, 256 King, D. F., 251 Knipper, H . , 256 Kong, C. P., 254 Kostermans, A. J. G. H., 256 Koumans, F . P., 256 Kovait, J., 344, 371 Kowalewsky, A., 356, 372 Kramp, P. L., 289, 344, 372 Khron, A., 292, 372 Krumbach, T. H., 274, 356, 372 Kubo, I., 256 Kuenen, Ph. H., 243 Kuhl, G., 289, 316, 372 Kuhl, W., 271, 289, 291, 316, 318, 329, 332, 343, 355, 372 Kuhlow, F., 256 Kuhn, A., 357, 367 Kukenthal, W., 356, 372 Kulkarni, R. D., 195, 256 Kulmatycki, W. J., 351, 364, 365, 3 72 Kumar, V. K. P., 256 Kummel, B., 256 Kuyl, 0. S., 85, 256

1 Lafond, J., 83, 256 Lameere, A., 359, 372 Land Res. Ser. C.S.I.R.O., 256 Lanzavecchia, G., 361, 363, 367, 372 Larue, C. D., 256 Laseron, C. F., 256 Leafl. For. Dep. Sarawak, 256 Le Brasseur, R. J., 344, 372 Lee, D. J., 160, 256, 262 Lee, J. Y., 369, 369 Lee, P., 264 Leln, S. H., 195, 256 Leuckart, R., 280, 292, 356, 372 Lever, R. J. A. W., 158, 256 Lewis, J.,256 Lewis, J. R., 87, 256

AUTHOR INDEX

Lindeman, J. C., 257 Ling, C . M., 269 Longhurst, A. R., 28, 58 Loppenthin, B., 244 Lovoridgc, A., 156, 257 Lubet, P. E., 257 Luytjes, A., 257

M McBride, E. W., 357, 359, 372 McCracken, T”. D., 22, 57 McCulloch, A. R., 185, 257 MacGinitio, G. E., 208, 214, 343, 3 72 MacGinitie, N., 208, 257 MacGregor, J. S., 19, 58 MacLaren, J. A., 289, 345, 373 Macnae, W., 81, 82, 91, 93, 105, 119, 120, 122, 124, 126, 127, 170, 201, 203, 206, 207, 210, 220, 221, 222, 257 M.A.F.F., U.K., 10, 58, 59 Mahabale, T. S., 85, 257 Mako, H., 22, 59 Malaviya, M., 257 Margetts, A. R . , 8, 59 Marks, E. N., 159, 257, 265 Marshall, T. C., 257 Massuti-Oliver, M., 347, 373 Matthew, D. M., 251 Mattingly, P. F., 257 Mauriri, C., 369, 369 Mayr, E., 225, 257 Mazumdar, J. C., 258 Medway, Lord, 154, 156, 257 Mees, G . P., 258 Meiridersma, H. W., 2ic4 Meissner, G., 356, 373 Mertens, R., 258 Metschnikov, E., 356, 373 Meyer, K. O., 256 Millaro, N. A. H., 221, 248 Miller, D. C., 201, 202, 258 Miller, 0. B., 258 Miller, R. C., 258 Milne-Redhead, E., 267 Misu, H., 22, 59

257,

114, 149, 214,

Miyake, S., 258 Miyata, I., 258 Mizuno, N., 258 Mogg, A. 0. D., 258 Moldenke, H. N., 112, 113, 114, 258 Montgomery, S. K., 258 Mookerjee, H. K., 268 Moore, H. B., 129, 265 Morin, H., 258 Morton, J. E., 75, 215, 219, 25.9 Moss, C. E., 259 Muir, J., 224, 259 Mullan, D. P., 141, 142, 259 Muller, F., 212, 259 Muller, J.,85, 117, 226, 256, 259 Murakami, A., 274, 289, 318, 322, 323, 330, 343, 344, 348, 365, 373 Murphy, G. I., 19, 59 Muzik, T. J.,256 Mgrhe, R. J., 9, 47, 57

N Natarajan,-, 26,: Navalkar, B. S., 244, 259 Neill, W. T., 157, 259 Neto, T. S., 273, 373 Nishot, I. C. T., 154, 156, 257, 258 Noakes, D. S. P., 235, 259 Noamesi, G. K., 259 Nouvel, H., 349, 373

0 Obdeyn, V., 136, 260 Odaiii, N., 258 Odum, H. T., 252 Ogilby, J . D., 186, 2Si‘ O’Gower, A. K., 160, 260 Oliveira, L. P. H. de, 2fiO Ono, Y., 201, 206, 210, 211, 230, 258, 260 Ortmanri, A. E., 213, 260 Osocheriko, E. I . , 15, 59 Owrr, H. B., 280, 289, 344, 346, 358, 373 Ow-Yang, C. K., 260 Oyama, K., 220, 221, 230, 260

383

AUTHOR INDEX

P Padmanabliaii. D., 260 Pagc.nstecht,r,H. A . , 292, 372 Painter, R. H.. 200 Palmer, J. D., 260 Pannier, P., 260 Panshin, A. J., 260 Parlrcr, R . R., 48, 59 Parrirh,€3. B., 8, 59 Parry, D. A., 282, 364, 365, 373 Pasha,S. A., 142, 247 Yatcrson, H. E., 158, 261 Patil, R . P., 260 Pearse, A. S., 156, 157, 261 Pesta, O., 261 Perricr tie la Bathie, H., 261 Peter, H . M . , 261 Petit, G,, 193, 195, 261 Pierce, E. L . , 289, 343, 344, 351, 354, 367, 373 Pillai, N. K., 261 Phny, S . C . , 261 Polunin, I. V., 161, 189, 244 Pope, E. C., 221, 245 Porter, A., 250 Post, E., 117, 261 Poujarde, J., 261 PrakasaRao, 1'. S., 268 Prakash,U., 261 Pugh, J. E., 261

Q

Rcich, E., 262 Reid, M. E., 289, 371 Reiiiders-Gouu,entak,C. A., 140, 262 Reisinger, E., 282, 283, 360, 364, 365, 373 Rep. For. Adm. Malaya, 136, 262 Rep. For. Dep. Fiji, 262 Rep. For. Res. W. Beng., 262 Retzius, G., 311, 373 Rcvelle, R., 262 Reye, E. J., 160, 256, 262 Rice, D. W., 8, 69 Richards, P. W., 262 Ricker, W. E., 16, 17, 19, 59 Ridlcy, H. N., 113, 262 Ridley, N. H . , 112, 262 Ripley, S. D., 262 Ritter-ZahonyK. von, 279, 281, 373, 374 Rizzoli, C., 361, 374 Robinson, H. C., 155, 262 Rochford, D. J., 262 Roggen, D. R., 363, 374 Ronaldson, J. W., 134, 220, 246 Rooij, N. De, 263 Roonwal, M. L., 263 Rosevear, D. R., 263 Ross, M. M. R., 363, 374 Roux, J.,263 Ruhland, W., 142, 263 Russell, E. S., 9, 10, 59 Russell, F. S., 289, 313, 343, 345, 3 74

Quoy, J.,272, 373

5 R Rabor, D. S., 253 Racek, A. A., 261 Radovich, J., 19, 39 Raimbault, R., 366, 369 Raja 13ai Naidu, K. G., 2G1, 262 Rangarajan,K . , 262 Rao, M. V. L., 251 Rao, T. S. S., 348, 373 Raski, D. J., 363, 373 Ratcliffc, Y. N., 157, 262 Raven, Th., 243 Ray, J., 77, 262 Reeve, M. R., 274, 276, 346, 365, 373

Saetersdal, G., 19, 50, $6 Sahrhage,D., 24, 69 Sakai, T., 263 Salfi, M., 363, 374 Salvoza, F. M., 263 Santieen, M. I., 245 Sankarankutty,C., 168, 169, 263, 264 Sankolli, K. N., 208, 263 Sanzn, L., 289, 307, 343, 364, 365, 374 Sauer, J. D., 79, 263 Savory, H., 263 Scaccini, A., 344, 374 Schaefer,M. B., 16, 22, 59

384

AUTHOR INDEX

Scharff, J. W., 263 Scharrer,E., 361, 374 Scheffer, V. R., 47, 58 Schimper, A. F. W., 85, 58, 96, 140, 141, 263 Schmidt, J., 142, 263, 264 Schmidt, J. W., 278, 360, 374 Schmidt-Nielsen, K., 181, 182, 252, 264 Schneider, A., 356, 374 Schneider, J., 264 Schneider, R., 2C4 Schnepper, W. C. R., 264 Scholander, P. F., 139, 264 Scholander, S. I., 139, 142, 26'4 Scholl, W., 264 Schottle, E., 198, 264 Schuster,W. H., 83, 122, 154, 157, 238, 264 Scott, A., 22, 23, 55, 57 Sen Gupta, J., 142, 264 SerBne, R., 216, 217, 264 Setten, G. G. K., 264 Shelbourne, J. E., 2, 59 Shieh, J., 269 Shindo, S., 8, 59 Sidhu, S. S., 264 Silas, E. G., 168, 169, 2G4 Silveira, F., 264 Simpson, D. A., 264 Singarajah,K. V., 274, 365, 374 Singh, T. C. N., 265 Slabber, M., 272, 374 Slooff, R., 159, 265 Smit-Sibinga, G. L., 243 Smith, H. M., 265 Smith, J. L. B., 186, 265 Smith, M. A., 156, 226, 265 Smythies, R. E., 156, 265 Snelling, B., 211, 265 Soh, C. L., 264 Sola, C. R. de, 265 Southgate, B. A., 82, 242 Southward, G. N., 9, 47, 57 Specchi, M., 344, 371 Specht, R. L., 265 Spender, M. A., 119, 120, 266 Spooner, G. M., 129, 265 Staatmans,W., 266 Stasenko, V. O., 15, 60 Stebbing, T. R. R., 213, 265

Stebbins, R. C., 186, 193, 198, 265 Steers, J. A., 266 Steiner, M., 91, 141, 142, 268 Stephens, G. C . , 245 Stephens, W. M., 266 Stephenson, A., 119, 120, 266 Stephenson, T. A., 119, 120, 2/36 Stephenson, W., 120, 216, 217, 266 Steup, F. K. M., 266 Stevens, N. M., 289, 292, 295, 296,297, 300, 303, 309, 311, 313, 320, 322, 329, 335, 338, 364, 365, 374 Stevenson, R. E., 82, 129, 249 Stewart, I. E., 157, 266 Stocker, O., 141, 266 Stocking, C. R., 247 Stone, J. H., 289, 374 Swart, H. J., 266 Sworder, G. H., 266

T Taguschi, K., 48, GO Takahashi, S., 266 Tandy, G., 119, 120, 266 Tashian, R. E., 210, 268 Taylor, E. H., 266 Taylor, J. S., 266 Tchindonova, J. G., 289, 333, 374 Teichert, C., 119, 250 Toodoro, G., 343, 374 Thiel, M. E., 279, 343, 375 Thompson, R. C. M., 158, 2/36 Thompson, W. F., 47, GO Thomson, J. M., 289, 291, 333, 266, 375 Thornton, I., 251 Tokioka, T., 273, 274, 275, 280, 332, 333, 334, 343, 348, 358, 266, 375 Tokunaga, M., 266 Tolken, H. R., 266 Tomlinson, T. E., 267 Tralau, H., 267 Troll, W., 138, 231, 267 Truman, R., 267 Tsukayama, I., 19, 50, 56 Tucker, V. A., 181, 182, 252

343,

346,

291, 364,

385

AUTHOR INDEX

Turrill, W. B., 267 Tuzet, O., 289, 309, 310, 375 Tweedie, M. W. P., 171, 175, 176, 200, 214, 226, 228, 229, 263, 267

U Umbgrove, J. H. F., 136, 267 United Nations, 4, 35, 39, 60 Uphof, J. C. Th., 140, 267 Ussing, H. H., 289, 344, 375

v Vahrmeijer, J., 267 Valdivia, J. E., 19, 50, 56 Van Balgooy, M. M. J.,265 Van Bemmelen, R. W., 83, 136, 244 Van Benthem Jutting, W. S. S., 230, 255 Van Dam, L., 139, 264 Van Dyk, D. E., 186, 195, 249 Van Eyk, M., 249 Van Oye, P., 322, 323, 329, 333, 273 Van Someren, E. C. C., 251 Van Steenis, C . G. G. J., 82, 83, 140, 220, 243, 265 Vanderplank, F. L., 151, 158, 182, 268 Vannini, E., 318, 375 Vannucci, M., 322, 375 Vasiljev, A., 289, 296, 297, 300, 313, 322, 323, 364, 365, 375 Vatova, A., 268 Venkatcswarlu, J., 268 Vernberg, F. J., 210, 268 Versteegh, F., 268 Verwey, J., 194, 203, 208, 210, 213, 214, 268 Villiers, A., 233, 268 Vinogradov, M. E., 343, 366 VuEetib, T., 343, 344, 375

w Waddington, C. H., 184, 268 Waibel, L., 268 Walcott, C . D., 358, 375 Wall, F., 268 Walls, G. L., 198, 268

Walsh, G. E., 268 Walter, H., 91, 141, 142, 268 Wanson, M., 268 Warburg, O., 268 Waterbolk, H. J.,85, 256 Watson, J. G., 79, 89, 90, 93, 105, 107, 108, 112, 124, 125, 208, 226, 234, 235, 268 Way, M. J.,151, 182, 184, 268 Webb, H. M., 245, 269 Weida, J.,243 Weinbren, M. P., 158, 269 Welch, B. L., 269 Wells, D. R., 156, 257, 258 West, O., 269 Westfall, J. A., 273, 363, 368 Wharton, W. J. L., 269 White, C . T., 269 Whitehouse, F. W., 269 Whitley, G. P., 185, 269 Wilkens, J. L., 269 Willem, V., 198, 269 Wilms, R., 292, 376 Wilson, R. F., 252 Wimpenny, R. S., 8, 344, 60, 375 Wohlenberg, E., 269 Womersley, H. B. S., 222, 269 Wood, J. G., 269 Wood-Jones, F., 269 Woolley, Sir L., 234, 253 Worth, C. B., 158, 269 Weinbren, M. P., 269 wu, Y. C., 269 Wang, Y. H. M., 269 Wyatt-Smith, J., 269 Wyrtki, K., 269

Y Yamanaka, T., 270 Yamashiro, M., 270 Yen, T. C., 270 Yonge, C . M., 218, 270 Yules, R. B., 270

Z Zellner, A., 9, 48, 57 Zonnefeld, J. J. S., 243

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Taxonomic Index A Acanthus, 142, 143, 237 ilicifolius, 94, 117, 142, 148, 149, 161 Achatina, 168 Acrostichum, 94, 107 aureum, 85, 93, 103, 119, 148, 175, 237 speciosum, 93, 97, 108, 148, 175, 237 Aedes alternans, 159 amesii, 159 butleri, 159 fumidus, 159 litoreus, 159 longiforceps, 159 niveus, 159 pembaensis, 158 scutellaris, 160 vigilax, 158, 159 Aegialitis, 85, 144 annulata, 120, 121, 142, 148, 150, 226 rotundifolia, 226 Aegiceras, 142, 143, 144, 153 corniculatum, 97, 114, 117, 131, 134, 142, 145, 146, 148, 157, 220 Aidanosagitta, 280 Alcedinao, 154 Alpheus, 92, 200 Amblonyx cinerea, 157 Amiskwia sagittiformis, 280, 358 Ammodytes personatus, 344 Anhinga anhinga, 153 Anopheles amiticus, 160 baezai, 159 farauti, 160 gambiae, 158 sundaicus, 158 Anoplolepis, 183 Aphragmophora, 280 Archisagittoidea, 280, 358 Ardea cinerea, 154 sumatrana, 154 387

Ardeola grayii, 153 Arthrocnenum, 88, 174 decumbens, lo2>lo3 halocnemoides, 103 indicum, 103, 119 zeiostachyum$ lo3 natalense, 119 quinquefzorum, lo3 Avicennia, 75, 76, 103, 129, 136, 139, 142, 143, 144, 145, 158, 172, 178, 180, 218 alba, 89, 112, 114, 133, 148, 149, 226 intermedia, 112, 113, 133 lanata, 93, 112, 226 marina, 82, 89, 92, 93, 99, 101, 102, 105, 112, 113, 114, 115, 117, 118, 119, 120, 125, 130, 131, 133, 134, 135, 141, 142, 144, 145, 146, 148, 149, 155, 161, 162, 166, 207, 220, 221, 222, 223, 224 nitida, 139 oficinalis, 93, 94, 97, 112, 161, 226 Azolla, 79

0 Balanus amphitrite, 167 Barringtonia asiatica, 87, 96 racemosa, 82, 86, 87, 93, 94, 96, 224 Bathyspadella, 280 edentata, 333 Batissa, 219 triquetra, 173 Eembicium, 219, 231 Birgus latro, 167, 212 Bitia hydroidea, 156 Boiga dendrophila, 156 Boleophthalmus boddaerti, 159, 179, 185, 188, 190, 194, 195, 197, 198, 199 Bombacaceae, 231 Bostrychia, 117 Brachylaena discolor, 86 Branchiomma vesiculosum, 364 Brownlowia tersa, 97

388

TAXONOMIC INDEX

Bruguiera, 77, 136, 139, 149, 150, 156, 158, 183 conjugata, 233 cylindrica, 93, 97, 105, 107, 110, 114, 177, 236 ezaristata, 105 gymnorhiza, 82, 89, 92, 93, 96, 97,99, 105, 107, 117, 118, 131, 144, 146, 149, 175, 220, 223, 234, 237 partiflora, 93, 105, 106, 110, 126, 131, 146, 148, 237 sexangula, 93, 94, 97, 99, 125, 131, 175, 237 Butorides striatus, 154

C Caesalpinia bonduc, 96 Calamus aquatilis, 97 Calianassa, 214 Callorhinus ursinus, 47 Caloglossa, 117 Camptandriumelongatum, 229 Camptostemon, 85 philippinensis, 231 schulzii, 231 Canavallia , 87 Carcinoscopius rotundicauda, 180 Cardisoma carnifex, 168, 169, 200, 201, 212, 224 hirtipes, 169, 212 Cassid ula, 2 1 8 angulifera, 173, 180 auris-felis, 174, 180 mustellina, 174, 180 Casuarina equisetifolia, 79, 87, 134 Catenella, 117 Ceratopogonidae, 160 Cerebus rhynchops, 156, 180 Cercopithecus mitis, 157 Ceriops, 139, 146, 158 decandra, 107, 110, 126, 142, 148 tagal, 92, 101, 103, 104, 105, 107, 110, 119, 120, 126, 131, 138, 141, 150, 174, 175, 177, 183, 220, 224 Cerithidea, 167, 240 alata, 174, 177 anticipata, 17 7

Cerithidea, cingulata, 177 decollata, 92, 102, 166, 173, 177, 221, 225 djadjariensis, 177 obtusa, 174, 177, 225 quadrata, 177 weyersi, 177 Ceryle maxima, 154 rudis, 154 Chaetognatha,280, 356, 359, 364 Chaetophora, 159 Chanos chanos, 122, 238 Chenolea diffusa, 102, 103 Chiromantes, 175 Chthamalus withersii, 167 Cleistostoma, 175, 200 algoense, 206 dilatatum, 21 1 edwardsi, 206 macneilli, 206, 211, 231 wardi, 206, 211, 231 Clerodendron inerme, 97, 233 Clibanarius longitarsus, 167 Clistocoeloma, 200 merguiense, 176, 180 Clupea harengus, 3 COCOS nucifera, 87, 134 Coenobita, 167, 212 Corvus albus, 156 macrorhynchus, 156 Corypha utan, 94 Crassostraea cucullata, 167 Crematogaster, 183 Crinum, 94 Crocodilus niloticus, 156 porosus, 156 Ctenodontina, 280 Culex sitiens, 160 Culicoides immaculatus, 160 mackayensis, 160 magnesianus, 160 naarmoratus, 160 molestus, 160 ornatus, 160 subimmaculatus, 160 Cyanchum armosum, 97

389

TAXONOMIC INDEX

Cyclograpsus, 200 Cymodocea, 88 Cynometra rami$ora, 107

D Daemonorops leptopus, 107 Dendronereis, I65 Derris heterophylla, 94, 107 trifoliata, 96, 224 Diplanthera, 88 Dolichandrone spathacea, 94 Dotilla, 200, 201, 202 fenestrata, 101 Dotilloplax kempi, 229 Dotillopsis, 200 brevitarsis, 229 Drosophila, 184 Ducula bicolor, 155 spillirrhoa, 155

E Egretta alba, 153 eulophotes, 153 gurzetta, 153 gularis, 153 Eichhornia crassipes, 79 Ellobiidae, 218 Ellobium, 218 auris-judae, 173, 174 auris-midae, 173, 174 Elysia, 177 Enhalus, 88 Enigmonia rosea, 165, 218 Entada, 224 phaseoloides, 96, 224 schefleri, 97 Epixanthus dentatus, 181 Eubalaena australis, 8 Euclea natalensis, 86 Eugenia suborbicularis, 144 Eukrohnia,274, 277, 280, 308-309 bathyantarctica, 308, 309, 333, 334 fowleri, 308, 309 hamata, 343 Eukrohnidae, 280

Euphausia superba, 15 Euplax, 200 tridentata, 231 Eurycarcinus integrifrons, 181 natalensis, 181, 225 orientalis, 225 Excoecaria agallocha, 85, 86, 97, 107, 120

F Ficus microcarpa, 93, 94, 107 retusa, 94 Pelis viverrima, 157 Flabellodontina, 280 Pluscisagitta, 280 Pordonia leueobalia, 156

G Gudus morhua, 3 Galeocerdo cuvieri, 2 16 Gecarcinids, 200 Gecarcinides, 2 12 Geloina coaxans, 173 Geograpsus, 168, 212 Glaucomya, 180, 219 Grapsidae, 200

H Haemonchus contortus, 363 Halcyon ehloris, 154 senegaloides, 154 Haliaetus leucogaster, 154 vocifer, 154 Haliastur indus, 154 Halodule, 88 Halophila, 88 Haminea, 176, 180 Helice, 200 crmsa, 231 leachii, 175, 224, 231 Heloecius, 200, 202 cordifownis, 211, 231 Hemiplax, 200

390

TAXONOMIC INDEX

Heritiera, 87 littoralis, 85, 86, 93, 94, 96, 97, 107, 119, 126, 219, 222, 224 Herpestes, 157 Heterokrohnia, 280 Heteropanope eucratoides, 181 glabra, 181 Hibiscus, 144 tiliaceus, 91, 96, 97, 142, 224 Hippoglossus stenolepis, 29 Hippopus, 120 Homarus, 26 Hydrophiidae, 226 Hydrophis .fasciatus, 228, 229 torquatus, 228, 229

I Ichthyophagus ichthyaetus, 154 Ilyograpsus, 175, 200 paludicola, 176 Ilyoplax, 175, 180, 200, 202, 213 delsmani, 176, 214, 229 lingulata, 176 obliqua, 176 punctata, 176 pusilla, 211, 230 spininrera, 176 Intsia bijuga, 93, 94, 107, 224 Ipomoea pes-caprae, 87, 134

J Juncus, 172 kraussii, 102, 103, 171 maritimus, 103, 171

K Kandelia, 76 kccndel, 97, 22 0 Krohnitta, 274, 277, 280, 343 subtilis, 344 Krohnittidae, 280

L Lagerstroeinia speciosa, 94 Lasiohelea townsvillensis, 160 Laternula, 180, 219

Leiopecten, 200 sordidulum. 180 Leptoptilos javanicus, 154 Littorina carinifera, 165 melanostoma, 165 scabra, 165, 218 undulata, 165 Lumnitzera, 133 littorea, 93, 96, 97, 125, 144, 233 racemosa, 96, 99, 101, 118, 131, 138, 139, 141, 142, 148, 149, 171, 224 Lutra maeulicollis, 157 perspicicillata, 157

M Macaca irus, 157 Macrophthalmus, 177, 200, 213 depressus, 102, 174, 176, 207 erato, 128 grandidiera, 101 japonicus, 21 1 latreillei, 179, 181 pacificus, 176 Mangifera indica, 141 Marphysa mossambica, 165 Melampus, 151, 218, 230 Malanogrammus aeglefinus, 8 Merlangus merlangus, 28 Merluccius, 3 capensis, 12 merluccius, 8 Mesosagitta, 280 Metapenaeus monoceros, 21 7 Metaplax, 200, 206 crenulatus, 178, 179, 213, 229 elegans, 180 tredecim, 229 Metasesarma, 200 Metopograpsus, 200 frontalis, 175, 208 latifrons, 177, 208, 213 messor, 175 thukuhar,175, 208 Micromesistius poutassou, 15 Mictyris, 201, 202 longicarpus, 160 Mimusops caffra, 86

TAXONOMIC INDEX

Mugilidae, 239 Murex adustus, 167 Murrayella, 117 Muscicapa ru$gastra, 156 Myomenippe hardwickii, 181

N Nannosesarma minuta, 167, 180 Nasalis larvatus, 157 Nemotoda, 361, 363 Nectarinia chalcostetha, 156 Nerita birmanica, 167, 174 Numeniusphaeopus, 155 Nycticorax caledonicus, 153 nycticorax, 153 N y p a , 85, 107 fruticans, 85, 84, 126 fruticosa, 86

0 Ocypode, 200 Oecophylla, 151, 158, 184 smaragdina, 158, 182, 183 Onchidiidae, 218 Oncosperma jilamentosum, 94 tigillaria, 99 Ophicardelus, 2 18 sulcatus, 173 Osbornia octodonta, 120, 133 Ozcroa obovata, 26 ozius guttatus, 181

P Pachycephala cinerea, 156 Pandanus, 97, 107 livingstoniona, 96, 134 tectorius, 96 Pandion haliaetus, 154 Panulirus, 26 Paracleistostoma, 180, 200 cristatum, 21 1 depressum, 176 longimanum,176 microcheirum, 176 Paramignya littoralis, 107

391

Parasagitta, 280 Parasesarma, 175 Parus major, 156 Pelargopsis capensis, 154 Pemphis acidula, 120, 133 I'enaeus indicus, 216, 217 japonicus, 217 rnonodon, 2 17 semisulcatus, 217 Periophthalrnodon schlosseri, 179, 180, 181, 185, 188, 189, 192, 194, 195, 198, 199, 200 Periophthulrnus, 152, 159, 198 argentilineatus, 185 chrysospilus, 179, 185, 186, 187, 190, 191, 192, 194, 195, 197, 199, 200 harmsi, 185 kalolo, 181, 185, 186, 187, 193, 224 koelreuteri, 185, 196, 197 sobrinus, 186, 188, 193 vulgaris, 185 Peronia peroni, 218, 221 Phalacrocorax africans, 153 carbo, 153 melanogaster, 153 niger, 153 Phascolosoma lurco, 181 Pheidole, 183 Phragmites, 1 19 communis, 86 Phragmophora, 280 Picus viridanus, 155 vittatus, 155 Pleuronectes platessa, 2 Polymesoda, 219, 226, 230 Potamididae, 218 Presbytis cristatus, 157 Pseudogelasimus, 200 Pteroptyx, 164 Pteropus, 157 Pterosagitta, 277, 280, 305-308 draco, 275, 286, 287, 288, 306, 307, 308, 309, 343, 344, 365 Pterosagittidae, 280 P y cnonotus goiaver, 156 plumosus, 156

392

TAXONOMIC INDEX

Pyrazus ebeninus, 218 Pythia, 218 scarabaeus, 173, 174

R Rana cancrivora, 156, 177, 181, 182 limnocharis, 157 Rastrelliger, 3, 15 Rhipidura javanica, 156 Bhizophora, 76, 77, 105, 117, 121, 136, 142, 143, 144, 149, 157, 167, 208, 236 apiculata, 89, 93, 97, 99, 108, 110, 111, 120, 126, 140, 148, 150, 162, 177 mangle, 139, 232 mucronata, 82, 89, 92, 99, 101, 108, 109, 110, 111, 114, 118, 131, 134, 141, 142, 146, 148, 149, 150, 177, 220, 224, 234 stylosa, 106, 108, 110, 118, 119, 120, 131, 150, 177, 220, 232 Rhizophoraceae, 76, 85, 136, 145, 146, 153

S Sagitta, 272, 280, 293-300, 316, 329, 355, 358, 362 bipunctata, 275, 287, 288, 291, 293, 295, 297, 289, 300, 309, 313, 332, 335, 336, 338, 339, 344 crussa, 274, 275, 282, 322, 330, 344, 348, 365 decipiens, 297, 309, 344, 346 elegans, 293, 309, 335, 344, 345, 364 euxina, 279 friderici, 274, 279 ferox, 330 guzellae, 344, 345, 346 hexaptera, 278, 279, 281, 282, 344 hispida, 274, 275, 338, 343, 346, 365 inflata, 278, 279, 280, 281, 288, 290, 291, 293, 295, 297, 309, 310, 313, 317, 318, 319, 332, 335, 336, 339, 344, 346, 347, 348, 351, 354 lyra, 277, 297, 344, 346

Sagitta, minima, 278, 293, 300, 309, 344, 354 neglecta, 330 pulchra, 281, 282 scrippsae, 273 serratodentata, 274, 275, 291, 332, 333, 344 setosa, 278, 279, 309, 310, 318, 330, 331, 332, 336, 344, 347, 350, 354, 365 Sagittidae, 280 Sagittoidea, 280 Salicornia, 88, 160 Salinator, 2 19 burmana, 226 Surdinella, 3, 15 Sardinops caerulea, 19 Sarmatium, 200 crassum, 175 Scopimera globosa, 230 intermedia, 229 proxima, 229 Scopus umbrettus, 154 Scylla serrata, 230, 240 Scyphiphora hydrophyllacea, 93, 105 Sebastes, 3 Seriolu guinqueradiata, 2 Serratosagitta, 280 Sesarma, 151, 152, 200, 201, 207, 212, 221 bataviana, 2 13 brevicristatum, 23 1 catenata, 221, 225 chentongensis, 171 crassimana, 17 1 darwinensis, 232 dussumieri, 175 erythrodactyla, 21 1 eulimene, 92, 171, 207, 21 1, 225 eumolpe, 175 fascia&, 171 guttatum, 92, 175, 225 indiarum, 175 indica, 171 inerme, 171 johorensis, 229 jousseaumei, 225 kraussi, 228, 229 lepida, 229

393

TAXONOMIC INDEX

Sesarma, lividum, 231 longipes, 225, 228 mederi, 171, 213, 225 meinerti, 92, 158, 171, 172, 207, 213, 214, 224, 231 melissa, 175 minuta, 225 moeschi, 171 nodulifera, 213 oceanica, 2 25 onychophora, 175, 229 ortmanni, 92, 102, 171, 207, 211, 225 plicata, 171 palawanensis, 171 quadrata, 2 25 rectipectinata, 229 sediliensis, 171 semperi, 229, 231 singaporensis, 171 smithii, 92, 170, 171, 172, 224, 231 tetragona, 171 versicolor, 171 Sesuvium portulacastrum, 99, 102, 103, 172, 174 Sideroxylon mime, 86 Solea solea, 2, 28 Solidosagitta, 280 Sonneratia, 77, 82, 126, 129, 136, 139, 142, 143, 149, 178, 180, 218 alba, 85, 92, 115, 116, 117, 119, 120, 125, 131, 133, 141, 144, 145, 148, 149, 162, 219, 224, 226 apetala, 115, 125, 131, 133, 142, 148, 226 caseolaris, 85, 94, 97, 117, 131, 158, 161, 162, 163, 183, 233 grifithii, 89, 115, 116, 125, 131, 133, 135, 148, 149, 158, 234 Sophora tomentosa, 87 Spadella, 227, 280, 291, 296, 300-305, 312, 218, 339-343, 350 cephaloptera, 275, 276, 282, 283, 284, 286, 287, 297, 302, 303, 309, 311, 313,316, 319,320,322-329, 339, 341, 349, 351, 352, 353, 354, 358, 365 Spadollidac, 280 Spilonis cheela, 154 Sporobolus virginicus, 119

Sus scrofa, 157

Syncera, 151, 219 brevicula, 177, 180 Syringodium, 88

T Tachypleus gigas, 180 T a i u s tumifrons, 8 Telescopium mauritsi, 173, 177, 180, 218 telescopium, 173, 177, 180, 218, 226, 240 Terebralia palustris, 173, 176, 218, 221, 224, 230 sukata, 173, 176, 218, 225, 230 Terminalia catappa, 93, 94, 96 Thais tissoti, 167 Thalassia, 88 Thalassina anomala, 97, 107, 108, 121, 123, 148, 169, 171, 175, 200, 208, 214, 230 Thespesia populnea, 96, 134, 222, 224 Thespesiopsis mossambica, 96 Thoracostoma californicum, 363 Tilapia mossambica, 123, 239 Tmethypocoelis, 200 Tragus, 157 Timeresurus purpureomaculatus, 156 wagleri, 156 Tringa terek, 155 totanus, 155 Tylodiplax, 175, 200 tetratylophorus, 176 T y p h a , 119

U Uca, 200, 202, 206, 214, 221 angustifrons, 229 arcuata, 21 1 bellator, 174, 176, 203, 210, 211, 212, 231 chlorophthalmus, 176 coarcta, 179, 180, 211, 231 consobinus, 2 10 dussumieri, 172, 179, 180, 202, 203, 205, 231, 232

394

TAXONOMIC INDEX

Uca, gaimardi, 176, 181, 209, 210 in.versa, 101, 174, 203, 209, 210, 211, 225 Zactea, 92, 101, 102, 172, 174, 201, 202, 203, 205, 209, 210, 211, 224, 230, 231 longidigitum, 2 11, 2 12 manii, 176 minux, 202, 203 pugilator, 202, 203 pugnux, 202, 203 rhizophorae, 180, 229 rosea, 176, 180, 229 triangularis, 180 universa, 92 urvillei, 181, 202, 203, 205, 210, 225, 232 vocans, 203, 209, 210, 211, 224 Upogebia, 92, 123, 180, 200, 208, 214 africana, 208, 221 pugettensis, 208 Utica, 200 borneensis, 176

V Varanus niloticus, 156 salvator, 156

X Xylocarpus, 133, 149, 150, 183, 224 australasicum, 138 granatum, 89, 93, 94, 97, 105, 107, 125, 126, 133, 140, 142, 147, 148, 220, 234, 237 moluccensis, 93, 97, 105, 107, 138, 139, 148, 234

Z Zonosagitta, 280 Zostera, 88 Zosterops chloris, 156

Subject Index A

B

Abstention principle, 53 Adelaide (Australia),220 Aerial roots, see Pneumatophores Africa difference of shores from Australian, 222 mangrove fauna of, 231 mangroves in, 219, 221 Agulhas current, 222 Algae, 117, 122, 159, 218 blue-green, 123, 239 green, 123, 239 Alluvium, 122 “fossil”, 122 AZpheus labyrinths, 200 Amphibians, 156 Anchoring roots, 138, 139 Anchoveta, 19, 32, 50 Annelids, 360 Ants, 151, 183 colonies, 182 nests of, 158 tailor, 151, 153, 182, 183 weaver, 158, 182 within mangals, 183 “Arrow worms”, 272 Asia, 219, see also regional entries Associations, see Plant Associations Atlantic, see North Atlantic Australia difference of shores from African, 222 mangroves in, 219, 220 species typical of, 231 Western, 231 Avicennia difficulties of taxonomy of, 112 intermediates, 112 “nurse” effect of, 149 seaward fringe of, 112, 114 wide distribution of, 144 Avicennia parkland, 92, 102, 172, 174

Bacteria nitrifying, 122 sulphate reducing, 122, 123 sulphur, 122 Barents Sea, fishing in, 10, 48 Barnacles, 115, 167 Barringtonia association, 87, 88, 89, 96, 125, 133, 225 Bashee river, 220, 221 Beaches levelling of, 129 particle sizes of, 201 Bees, 157 Bengal, Bay of, SO, 96 Birds associated with mangals, 153-156 not specializcd, 181 Bivalves, 180, 218, 219 Blastogeriesis, 351 Borneo, 80, 83 eastern, 223, 230 Bostrychietum, 117 Bottom-living species, see Deniersal species Bruguiera cylindrica association, 107 Bruguiera forcsts, 105-108, 125, 126, 134, 218 animals of, 174 types of, 105 variants of, 107, 130 Hruguiera gymnorhiza association, 107 Bunbury (Australia),220 Burrows, l68,172,174,179,18O,l84,200 importance in feeding of thalassinideans, 208, 214 permanent, 201 uses of, 214

395

C Cable roots, 137, 138, 140 Calcareous material, 121, 123 Carnivores, 157 Caterpillars, 158 Celebes, 230

396

SUBJECT INDEX

Ceriops thicket zone, 103, 104, 118, 134, 218

animals of, 174 Chaetognaths accessory fertilization cells in, 297300, 301, 302, 304,305,

307, 335

affinities of, 355-357, 359-363 as fishing indicators, 344 as isolated phylum, 357 biology of, 271-366 bristles of, 275 caudal segment, 279, 290 characterswith systematic or adaptational value, 272 crescent cells, 296 cross-fertilization, 332 cycles of sexual maturity in, 344, 345-350

diploid number of, 309 early development phases of, 316, 317

embryology of, 356 feeding movements of, 276 female gonads of, 292-297, 300-309 fertilization of, 322-334 growth of, 346 hermaphroditenature of, 289, 330 hooks of, 274 influence of environmental factors on, 343-344, 365 integument of, 274 laboratory experiments on, 364-365 life span of, 345 longitudinal septum, 290 male gonads of, 290-291, 309 mating of, 322 morphology of, 271-289 muscles of, 361-362 new classification of, 280 oogenesis in, 311 origin of, 358 possibility of self-fertilization in, 322, 328

regeneration in, 351-355 regions of body, 272 reproduction of, 289-350, 365 spermatogenesis in, 309-31 1 spermatogonia, 290 spermatophores, 323, 324, 325, 326, 327, 329, 330, 333

Chaetognaths-continued spermatozoa, 294, 298,

306, 308, 310, 311, 324, 327, 328 migration of, 326, 328 survival of winter by, 350 suspension apparatus in, 297, 298, 299 systematics of, 280, 355, 358-359, 363-364 Channels,in mangal, 133

Charcoal production, from mangrove, 235, 236

Chelipeds, of Uca, 202 Chemotactic action, 328 Cheniers, 79, 80, 134, 136 Chlorinity, 2 1 1 optimum range for Sagitta crassa, 349

Chromosomes, 309, 310, 338 lampbrush, 301, 312 precocious migration of, 310 Ciliary loop, see Corona ciliata Clines, 152 Closed areas, for fishing, 26, 27 Closed seasons, for fishing, 26, 27 Coastal sediments, 82 accretion of, 83, 149, 150, 238 influence of mangroves on, 83 Coconut groves, 240 Cod, 3, 10, 28, 55 landings of arctic, 11 stocks of, 19 Coelom cavity, 290, 296, 300, 352 “Collarette”, 275, 348, 352 Conservation measures, 41, 43 for whales, 55 international control of, 42 43 problems of feasibility and enforcement, 42 Convention on Fishing and Conservation of the Living Resources of the High Seas, 38, 45 Convention for the Regulation of Whaling, 43 Coral reefs, 77, 79, 110 Cormorants, 153 Corona ciliata, 279, 281, 282, 283, 284, 285, 286, 300, 327, 360, 36h

annularcanal of, 283 cells of, 283, 288

397

SUBJECT INDEX

Corona ciliata-continued characteristic of chaetognaths, 282 function in regulating migration of spermatozoa, 285, 328 glandular functions of, 286 researches on, 283 seasonal variation in, 348 secretion of, 284, 285 section of, 287 sensory funct,ionof, 283, 286, 289 structure in pelagic chaetognaths, 334 variations of, 281 Crabs, 75, 128, 135, 151, 152, 165, 167, 174, 175, 176, 177, 180, 181, 192, 201, 237 as food, 201, 240 breathing specializations of, 212 burrows of, 168, 172, 174, 203, 214 “castle building” by, 168 claw forms of, 224 demands on substratum, 206 distribution along estuary, 211 distribution of ocypodid, 206 feeding of, 202-203, 206, 207, 208 fiddler, 172, 179, 205, 232 land, 168, 212 more numerous in warm weather, 209 non-burrowing,207, 208 of Indo-Malayanregion, 229 pumping of water by, 213 temperature relationships of, 209, 210 water intake by, 203 water oxygenation mechanism, 212213 Creeks, in mangal, 133, 176 Crocodiles, 156 Crows, 156 Crustaceans, 230 breathing specializations of, 212 burrowing by, 214 effects of humidity on, 210 effects of substratumon, 201 effects of temperatureon, 209 effect of water saltness on, 211 specialized, living in mangals, 200 Currents, effect on mangals, 136 Cymoclocea association, 88

D Dampierian Province, 232 Darters, 153 Demersal species, 9, 10, 28, 32 Descriptive ecology, 74 Desiccation, ability of animals to resist, 184 Dhows, 77 Diatoms, 207 Diploid number of chaetognaths, 309 “Distant water” fishing grounds, 9 Drainage channels, in Avicennia parkland, 174 Durban Bay, 79

E EcologicaI differences between species, 185 Egg-laying in Sugitta, 335, 337 in Spadella, 339-343 preferred times in various chaetognaths, 335 Eggs of chaetognaths, 319, 320, 321, 336, 338, 349 production by marine fish, 18 Embryonic reserve, 355 Epidermis, multistratified nature of, in chaetognaths, 275 Epifaunaof mangal, 165 Epithelium, 303, 306, 308 cells, 352 Erosion following removal of a mangal, 136 of mangal shores, 126, 128, 135 of rhizophora forest, 135 Estuaries, penetration of mangroves into, 82 European Fisheries Convention, 36 Euryhalinity,232 Externalgenital papilla, 295, 302, 303, 307, 333, 342 Eyes of chaetognaths, 273 characters in species determination, 273-274 cups, 273

398

SUBJECT INDEX

Eyes of chaetognat,hs-continued fimct,ions, 274 photo-receiving cells, 273 strrrct>rire of, 273

F Facics, of maugals, 91, 118 “Farmingthe sea”, 54 Female reprodnct,ive apparatus of chaet,ognaths, activit)y cycles of, 347 of Eukrohnia, 308--309 of f’terosagitta, 305- 308 of Sagitta, 293-300 of Spadella, 300-305 origiii of, 319 Ferns, 237 Fertilization, in chaetognaths, 335 in Eukrohniabathyantarctica,333,334 in p-lagic chaetognaths, 334 in Sngitta, 329-333 in Spadella cephaloptem, 322-329 Filariases, mosquito carriers of, 151 Fins, of chaetognaths, 178 amorphous substarice in, 277 anterior, 279 caudal, 277 form of, 278 lateral, 276, 277 position of, 278 posterior, 279 rays of, 278 regeneration of, 353 Fireflies, synchronousflashing of, 161164 frequency, 164 optimum density for, 163 questions concerning, 163 rhythms of, 162 temperature control of, 164 Fish depletion of resources of, 7-16 in mangrove areas, 122 percentage of t,ot,al animal protein intake, 2 pond culture of, 238-240 underfished stocks of, 23 unexploited, 15 world production of, 1

Fish meal, 2 Fish ponds cycle of production in, 238-239 green manuring of, 239 harvesting of crop, 239 making of, 238 of Java, 238 prawns in, 217, 240 protein production, 239 tidal canal system, 238 yields, 239, 240 Fisheries complex, 25 international,30 national, 30 Fishery bodies, specialized, 39, 40 for part#icularregions, 39 for research, 41 for sea fisheries, 39 list of international,62-71 to formulate conservation measures, 41 Fishery management aim of, 6 bodies concerned with, 62-71 effects of wrong, 16 international,53 lack of basic data for, 52 mechanics of, 34-45 national approach to, 34 need for, 15 need for scientific knowledge, 51 objectives, 22, 23, 25 prospects for future progress in, 45 requirements for full, 50, 52 stock and recruitment, 19 Fishery regulation assessing effect of, 51 effectiveness of various methods, 25 enforcement, 26 fixing maximum catch, 44 methods, 25-34 types of, 25 with several species, 32 .Fishing effect on stock of changes in, 7 group quotas for, 29, 31 interaction of catches, 24 limitation of amount of, 29-34, 43 measurement of catch, 31

399

SUBJECT INDEX

Fishing-continued overall quotas for, 29, 33, 34 relation between mortality and catch, 21 stock recovery on reduction of, 8 theoretical models of cffect of, 16, 19 value of catch vs. cost, 22, 24 yield curves, 20 Fishing gear, 15, 16 regulation of, 27 selective, 18 Wishing mortality, 29, 31, 43 Fishing rights of coastal states delimitation of, 35, 36 preferential, 36 Fishing zones, 36, 37 Wlavins, 285 Flying foxes, 157, 181 Frogs, 156, 181-182 salt tolerance of, 182 Fruit bats, 75 Fruits of mangrove species, 145, 147, 148 Fur seals, 37, 47, 49, 53

G Gastropods, 151, 217, 231 Gastrulation, 318 Gelatine, of chaetognathootheca, 308 Germ cell determinant, 300, 313, 316, 320, 321, 322 function of, 316 origin of, 316 Germinal line, segregation of, 313, 318, 351 Gonads of chaetognaths, 289-309, 313 maturity stages of, 314-315 Great Barrier Reef, 79, 120, 155 Gross physical yield from fishing, 52 Gullies, in mangal, 133

H Haddock, 8, 10, 28 Hake, 3, 8, 12, 16 Halibut, 3 Atlantic, 32 Pacific, management of, 9, 29, 32 restriction of catch of, 47

Halibut Commission, 32 Halophytic plants osmotic pressure of. 141 physiology of, 140 Hermit crabs, I67 Herons, 153 Herring, 3, 12, 32 High seas, 35, 37 Honey, of Aegiceras, 157 Hutan darat, 93 Hyalinc substance, round eggs of Pterosagitta, 305 Hydrogen sulphidc in soils, 121, 139 Hydrophiid snakes, 156

I Iceland, fishing off, 10 Indo-Malayanregion, 223, 226 Indo-PacificFisheries Council, 39 Indo-west Pacific region, 77,78,8Y, 108 divisions on basis of endemic fauna, 223 east central division, 223, 226-229 Eastern Borneo division, 223, 23023 1 Lesser Surida Isla~idsdivision, 223, 231-232 littoral fauna and flora of, 222 marine flora of, 223 New Guinea and Queerisland division, 223, 231 north-easterndivision, 223, 230 Pacific islands division, 223, 232-233 west central division, 223, 226-229 Western Australia division, 223 western division, 223, 225 Infaunaof mangal, 165 Inhaca Island, 79, 87, 102, 126, 131, 216, 221 mangrove distribut,ion at,, 132 southern element of faima at, 221 tropical element of fauna at, 221 Inhambane,219, 220 Inland waters, fishery niariagernentin, 5 Insects, 151, 153, 157-164, 182-184 biting, 158 Inter-American Tropical Tuna Commission, 39, 40, 41, 44

400

SUBJECT INDEX

International Commission for the Northwest Atlantic Fisheries, 40, 41, 43 International Commission for the Scientific Exploration of the Mediterranean Sea, 41 InternationalCouncil for the Exploration of the Sea, 37, 41 InternationalLaw, 34 of the sea, 35 International North Pacific Fisheries Commission, 41, 42, 44 International Pacific Halibut Commission, 41, 42, 45 InternationalPacific Salmon Fisheries Commission, 41, 42 InternationalTechnical Conference on the Conservation of the Living Resources of the Sea, 45 International Whaling Commission, 33, 40, 41, 43, 45, 46, 48 Intertidal range, 126 Inundationfrequencies, 89 Ionic balance, 211

J Japanese-Soviet Fisheries Cornniission for the North-West Pacific, 42 Java, 83 Joint Commission for Black Sea Fisheries, 41

K Kagoshima Bay, 220 Kariograms, 310 Kariosomes, 3 12 Kei River, 220 Kingfishers, 153, 154 Knee roots, 139 Krill, 15 Kuro Shio current, 222

L Labrador Banks, 12, 13 Landward fringe of mangal, 91-103, 125 animals of, 167-174

Landward fringe of mangal-continued following forested supralittoral,91 following on savannah, 99 transition to, 107 Law of the sea, 35 conferences on, 35, 36 League of Nations, 37 Lesser Sunda Islands, 231 Licence fees, 30, 31 control of fishing by, 54 Limit of fishing, defining, 31 Lipoids, 278 Lobster, 26 as food, 2 mud, 121, 169, 175, 208, 209 rock, 26 Lourenpo Marques, 79, 82, 126, 144, 220, 221 Lower lethal temperature of crabs, 210 Lunzlzitzeru littorea association, 93

M Mackerel, Indian, 15 Madagascar, 80 Malacca, Straits of, 80, 228 Malaria, mosquito carriers of, 151, 158 Mammals living within mangals, 157 not specialized, 181 Mangals, 75, 80, 83, 85, 88, 94, 97, 108, 110, 111, 114, 117, 120, 193, 207, 233 clearing of, 123 distribution of marine fauna in, 152, 165-1 8 1 effect of currents on, 136 environment provided by, 150 fauna of, 150-181, 221, 231 fresh water supplies, 118 fully zoned, 135 land animals in, 153 landward fringe of, 91-103 mammals in, 157 mineral content of water in, 211 of Sarawak, 84 rain forest, 93 reclamation of, 240-241 seaward fringe of, 112-1 17 soils of, 121 specializations of fauna of, 181-219

SUBJECT INDEX

Mangals-continued variations in zones of, 118 waterways in, 133 zonation of animals in, 165 zones of, 91 Mangrove forests, 74, 80, 92, 101, see also Mangals clear-felling of, 237 management of, 235, 236, 237 of island reefs, 120 “Mangrove Kingfishers”, 153 “Mangrove Park”, 119, 120, 121 Mangrove swamps, 74, 75, 85 northern limits in eastern Asia, 220 popular idea of, 108 soils of, 122, 123 Mangrove swimming crab, 2 14-2 17 as food, 240 burrows of, 214 distribution of, 215 habitats, 216 mating of, 216 moulting and growth of, 216 Mangrove timber, 234 as firewood, 235, 236 corrosion of iron in Sonnerazia, 234 for charcoal production, 235 for decorative use, 234 for pulping, 237 for structuraluse, 234 in cabinet work, 234 in piling, 234 in shipbuilding, 77, 233 susceptibility t o shipworm attack, 234 termite resistance of, 234 use in houses, 234 weight of, 236 Mangrove zonation control of, 124-136 interruptionin, 130 relationship with intertidal levels, 129 Mangroves, 74, 80, 85, 99, 112, 129, 152, 232 “antlered”, 108 as source of timber, 77, 233 biogeographical comment on, 222233 coastlines where found, 78

401

Mangroves-continued complete succession of, 130 distribution of species, 90, 95, 98, 100, 104,facing 104, 119, 127, 132 extratropical extensions of, 219-222 frosts, effects of, 221 geographical distributionof, 219-233 geological history of, 85 geological significance of, 82-85 greatest luxuriance,219 historical references to, 76-77 latitudinal limits of, 134 north-easternextensions of, 230 origin of word, 75 penetration in estuaries, 82 preferring shade, 150 preferring sunlight, 148 relation between root and shoot systems, 144 salinity tolerance of, 131 shallow rooted, 136 shrubs, 103 southernmost occurrence of, 220 specializations of stems and leaves, 140 spread of, by seaborne seeds, 224 succession of, 148-150 temperature limits of, 221 viviparous, 145 zonation of, 89-136 Margin of subtraction, 232 Marine animals pattern of behaviour, 184 rhythmic activity of, 185 specialization of, 184 Marine fishery resources, latent, 4 Marshall Islands, 233 Massawa, Bay of, 220 Mating of pelagic chaetognaths,334 of Sagitta, 329 of Spadella cephaloptera, 323-324, 325, 327 Maturation prophase, 304 Maturation spindles, 339 Maxillipeds, 202, 203, 204-205, 209, 213 Meiosis, 309 Mesodermal elements, 303 Metaphase, spermatogonial, 310

402

SUBJECT INDEX

Microncsia, mangaIsof, 233 Micropilar apparatus, 298 Midges, 160 Milk fish, 238 Moqambique, 84, 92, 101, 116, 131 Moluccas, 230 Molluscs, 75, 151, 173, 176, 217-219 distribution of fresh-water,230 fccding of, 218 fossil, 230 Monkeys, 157, 237 Morisoori effects, 219 Moretori Bay, 220 Mosqnit,oes, 151, 158, 159, 195 associated with Anstralian mangroves, 159 larvae, in saline waters, 184 Mouse doer, 157 Muck soils, 121 Mud adaptation of plants to, 136-140 fauna of, 201 in mangrove aroas, 83, 118 Mud lobster, 121, 169, 175 burrows of, 169, 208 digging technique, 209 feeding, 209 modification of substratum by, 175 mounds of, see Thalassina mounds Mud-skippers, 113, 179, 181, 185-200 aggressive behaviour of Periophthalmus chrysospilos, 179, 192 burrows of, 180, 187, 188, 190, 191, 193 confrontation, 192, 194 “crutching”, 195, 196, 197 defence display of, 192 distraction display of, 193 eyes of, 197-198 feeding, 199 “grazing” on mud, 190 locomotion 011 land, 195- 197 nest pools of, 189 sexual display of, 192 skimming on water, 197 skipping, 195 swimming behaviour of, 195 territorial behaviour of, 190, 191 tree-climbing by, 195, 197 water-exchangemechanism, 199

Mud-skippers~continued with fused pelvic fins, 185, 186 within mangals, 186 Mullet, 239

N Nervous fibrillae, 275 Net economic yield from fishing, 52, 53 New Britain, fauna of, 231 New Caledonia, fauna of, 231 New Guinea, 82, 223, 231 New Hebridcs, fauna of, 231 New South Wales, 220 New Zealand, mangroves in, 219, 220, 222 Nibong palm, 99 uses of, 237-238 Nitrifying bacteria, 122 North Atlantic, overfishing in, 14 North-East Atlantic Fisheries Commission, 40, 41, 42, 43 North Pacific Fur Seal Commission, 41, 42, 43-44 North Sea, fishing in, 9, 10, 24, 25, 46 Northern hemisphere, mangroves in, 221 Nuclear net, 311, 312, 316, 322 Nursery areas for fish, 27, 45 Nypa association, 85, 88, 97, 125, 133 uses t o man, 97 Nypa palm, uses of, 237

0 Offshore waters, 35 lack of uniformity in delimiting, 37 Oman, Gulf of, 233 Oocytes, of chaetognaths, 292, 293, 294, 295, 298, 300, 301, 302, 304, 305, 307, 308, 312 dimensions, of, 313 growth of, 31 1 Oogenesis in chaetognaths, 31 1 Oogonia, 295, 301, 303, 304 Oospermaduct, 292, 293 Opercularmovements, 198 Osmotic pressure, 142 of halophytes, 141 Otters, 157

403

SUBJECT INDEX

Ovaries, of chaetognaths, 292, 293, 295, 296, 300, 302 development of, in Spudella, 303 endothelium of, 293, 300 germinal epithelium of, 292 in Eukrohnia, 309 in Pterosagitta, 306 in Sagitta, 294, 338 in Spadella, 300, 304 Overfishing, 3, 9 in North Atlantic, 14 need for biological approach to, 6 problems of, 6 Oviduct, temporary, of chaetognaths, 295, 335, 336, 337, 338, 339, 342 Oysters, 117

P Pacific fisheries in eastern, 17 fisheries in northern, 1 3 North, 37 Pacific islands, 232 Passerine birds, 156 Pelagic species, 12 Permanent Commission for the South Pacific, 42 Persian Gulf, 233 Pes-caprac association, 87, 88 Photo-receptors, 273, 364 Photosensitivity, 274 control of vertical distribution of Sagitta c r a ~ s aby, 274 Phototactic movement, 274 Phragmatic structure, 280 Pigeons, 155 Plaice, 2, 3, 10, 28 North Sea stocks, 9 Plant associations of sea-shore, 85 Barringtonia, 87, 88, 89, 96, 125, 133, 225 Rruguiera cylindrica, 107 Bruguiera gymnorhiza, 107 Cymoclocea, 88 Lumnitzera littorea, 93 mangal, 85 Nypa, 85, 88, 97, 125 Pes-caprae, 87, 88 Saltwort, 88, 89 Xylocarpus-Heritiera, 107

Pncumatophores, 129, 138, 172 form of, 139 functions of, 139 Pollen analysis, 85 Polymorphism, 346 Polyplasts, 291 movements of, 291 Pools, 176 Prawns, 75, 122, 123, 177, 200 as food, 2, 240 cultivation of, 240 penaeid, 217, 240 Prop roots, 121, 136, 137, 140, 167, 177, 208, 236 Protandric hermaphroditss, 330 Protein intake contribution of fish to, 2, 5 total, 5 Purse seines. 27

Q Queensland, 94, 96, 126, 223, 231 mangrove distribution in, 95, 100, 104, 119, 127

R Rainfall, seasonal, 232 Rayon production from mangrove timber, 237 Red Sea, 220 Redfish, 3 Redshank, 155 Regeneration of mangal, 128 Regeneration studies on Sagitta, 354 on Spadella cephaloptera, 352-354 Regional Fisheries Advisory Commission for the South-West Atlantic, 40 Regional Fisheries Commission for West Africa, 40 Reptiles, 156, 181 Respiratory epithelia, in mud-skipper, 198 Rhizophora forests, 108-111, 125, 129 fauna of, 177 in fresh-water areas, 111 in salt-water areas, 111 soil in, 111

404

SUBJECT INDEX

Rivers, in mangal, 133 Rooting systems, 175 of Avicennia spp., 137, 138 of Ceriops spp., 137, 138 of Rhizophora spp., 137, 140 of Sonneratia spp., 137, 138 of Xylocarpus spp., 137, 140 Rosewood, 234 Rot holes, in branches, 151 Ryii-Kyfi archipelago, 220, 221, 222

S Sahul Shelf, 84, 232 St. Vincent Gulf, 220 Salinity ability of animals to adjust to varia tion in, 184 of soil water, 89, 101, 118, 121, 124, 131 Salmon, 3, 5, 55 fishery on high seas, 48 North American Pacific, 30, 48 Salt content of Sonneratia wood, 142, 234 Salt excretion, 142 Salt flats, 232 Salt marsh, 80 compared with mangrove shore, 81 Salt pans, 182, 241 Salt production technique in humid tropics, 241 Salt-secretingglands of plants, 131, 142, 143, 144 of reptiles, 181 “Salt wcdge”, 82 “Salting cliff”, 80, 93, 128, 181 Saltwort association, 88, 89 Sand dunes, 77 Sandakan, distribution of mangroves at, 98 Sarawak, 84, 94, 116 Sardine, 3, 15, 18 Scaphognathite, 203 Schorre, 80, 81, see also Salt marsh Sea bream, 8 Sea eagles, 154 Sea-going craft, 233 Sea otters, 37 Sea snakes, 226

Seaward fringe of mangal, 112-117,120 factors affecting fauna of, 177-178 fauna of accrescent shores, 178-181 fauna of eroding shores, 181 Sonneralia zone of, 115 Seeds viability of, 224 Seedlings of mangrove species, 146 colonization by, 149 Scminal ampullae, in chaetognaths, 305, 306, 308 Scminal pouch, in chaetognaths, 293, 295, 296, 297, 298, 301, 302, 303, 304, 305, 306, 308, 312 endothelium of, 293 glandular cells of, 307 possible trophic function of, 312 Seminal receptacle, in chaetognaths, 294, 301, 302, 303, 304, 306, 323, 324, 326, 341 Seminal vesicles, in chaetognaths,290, 291, 323, 330, 331, 332 Shade and sun conditions, effect on animals, 152 Shark Bay, 220 Shellfish, 2 “Shelter wood” system, 236 Ships, use of mangrove timber in, 77, 233 Shoaling fish, 32 Shore level, alteration of, 84 Shore lines, reorganization of, 136 Shore profile, 126 flats in, 126 Silt, 83 encouraging deposition of, 150 Silvicultural rotation, 236 Sinai peninsula, 130, 220 Size limits for fishery regulations, 26, 34 Slash, from forestry operations, 237 disposal of, 237 Snails, 165, 168, 174, 177, 180 as food, 240 neritid, 75 pulnionate, 75 purple dye produced by, 180 submarine, 2 19 Snakes, 156, 180 of Indo-Malayanregion, 229

405

SUBJECT INDEX

Sofala Shelf, 84 Soil animals living in, 151 fertility of, 178 in mangrove swamps, 122 in rhizophora forests, 111 surface of, 151, 174 waterlogging of, 124, 129, 133, 134 Soil levels, raising of, 107 Soil water, salinity of, 89, 101, 118, 121, 124, 131 Soils, 94 colour, 123 compacting of, 129 degradation of, 124 flow of, 129 hydrogen sulphide content, 121, 139 of mangals, 121 oxygen content of, 121 rapid deposition of, 122 Sole, 2, 28, 46 Solomon Islands, fauna of, 231 Spencer Gulf, 220 Spermatheca, in Sugitta, 294 Spermatogenesis, 290, 291 in chaetognaths, 309-31 1 Spores of ferns, 148 Stock and recruitment in fisheries relationships, 19 theoretical models, 19 Stomata of mangroves, 141 Suction pressure, 142, 144 Sulphate reducing bacteria, 122, 123 Sulphur bacteria, 122 Sumatra, 82, 83 Sunda Shelf, 84, 228, 229 Sundabans, 96 Sundaland, pleistocene subcontinent, 226, 227 importance of, 228 Sustainableyield, 16 Sydney, 220 mangrove fauna at, 221

T Tadpoles, 177, 181 induction of metamorphosis, 182 Tambaks, see Fish ponds Tannins, 237

Teeth, of chaetognaths, 274, 279 Telmun, 233 Temperature limits of mangroves, 221 upper lethal of crabs, 209, 210 Terek sandpiper, 155 Territorial seas, 35, 36, 37 Testes, of chaetognaths, 290 Thalassina mounds, 97, 107, 108, 121, 148, 169, 170, 175, 200 Tidal flooding, frequency of, 124, 125 Tidal range, 124 Tidal wave, 82 Tide, connection with animal rhythms, 155 Tilapia culture, 239 and malarial control, 239 unpopularity in rice-growing countries, 239 Transpiration rates, of mangroves, 141, 144 Transverse septum, in chaetognaths, 272, 290 Trawlers factory, 10, 13 freezer, 10, 11, 13 steam, 7 Trawls, mesh regulation, 27, 28, 46, 47 Tree canopy, 150 Tuna, yellowfin, 17, 44

U Undergrowth, 110 United Nations Conference on the Law of the Sea of 1958, 35, 38, 39, 40, 45 of 1960, 35, 36 Upper lethal temperatures for crabs, 209, 210

V Vagina, of chaetognaths,302, 306, 307, 308, 340, 341, 342, 343 Viraemias mosquito carriers of, 151 reservoir hosts of, 157 Vitelline membrane, of Spadella egg, 320

406

SUBJECT INDEX

Vitellogcnesis, in chactognaths, 293, 312 Viviparity in mangrovcs, 145

w Waders, 154, 155 “Wallace’s Line”, 84, 228 Wastage of resources, 55 Water storage tissue of mangroves, 141 Weighting factors for fishing quotas, 34 Western Indian Ocean, 223, 225 fauna of, 225 Wertcrn Point Bay, 220, 221 Whales, 8, 49 Antarctic, 18 blue, 8, 32 conservation of, 55 fin, 8, 32 gray, 8 right, 8 sol, 32 Whaling agreement on Antarctic, 53 Antarctic, 29, 32, 33, 44-45, 48 blue whale unit (BWU), 34 lack of success of regulation, 48

Whaling-continued size limits for, 46 violations of regulations in, 46 “Whaling olympics”, 45 Whimbrel, 155 Whiting, 28 blue, 15 Wild pigs, 157 Woodpeckers, 155 World production of fish, 1, 2 marine, 3

X Xylocarpus-Heriticrnassociation, 107

Y Yaeyama Islands, 220, 221 Year-classes, 10 Yellowtail, 2 Yield from a fishery, 52 curves of, 20

Z Zambezi river, 80, 82, 96 Zonation, see mangroves