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Advances in

MARINE BIOLOGY VOLUME 4

This Page Intentionally Left Blank

Advances in

MARINE BIOLOGY VOLUME 4 Edited by

SIR FREDERICK S. RUSSELL Plymouth, England

Academic Press

London and New York

1966

ACADEMIC PRESS INC. (LONDON) LTD. BERKELEY SQUARE HOUSE BERKELEY SQUARE LONDON W . 1

U.S. Edition published by ACADEMIC PRESS INC.

111 FIlWH

AVENUE

NEW YORK, NEW YORK

10003

Copyright 0 1966 by Academic Press Inc. (London)Ltd.

All Rights Reserved

N O PART OF THIS BOOK MAY BE REPRODUCED IN ANY FORM BY PHOTOSTAT, MICROFILM, OR ANY OTHER MEANS, WITHOUT WRITTEN PERMISSION B'ROM TEE PUBLISHERS

Library of Congress Catalog Card Number: 63-14040

PRINTED IN DBEAT BBITAIN BY TEE WEITBFRXARB PRE88 LTD. LONDON AND TONBBIDQE

CONTRIBUTORS TO VOLUME 4 MALCOLMR. CLBRKE, National Institute of Oceanography, Worrnley, Bodalming, Surrey, England

CARL J. SINDERMANN, U.S. Bureau of Commercial Fisheries, Biological Laboratory, Oxford, N a y l a n d , U.S.A.

V

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CONTENTS CONTRIBUTORS TO VOLUME 4

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Diseases of Marine Fishes CARL J. SINDERMLWN I. Introduction

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11. Microbial Diseases A. Viruses . . B. Bacteria C. Fungi . D. Protozoa

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. .. .. Effects of Disease A. Epizootics and Mass Mortalities B. “Background” Effects.. .. C. Economic Effects .. ..

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VII. Immunity

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VIII. Diseases in Marine Aquaria

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IV. Genetic and Environmentally Induced Abnormalities V.

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IX. Relationship of Fish Diseaaes t o Human Diseases

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X. Future Studies of Marine Fish Diseases

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CONTENTS

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A Review of the Systematics and Ecology of Oceanic Squids MALCOLMR . CLARKE I

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Introduction A . Distribution B . Depth .. C. Life history

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Architeuthidae A . Architeuthis

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IX . Brachioteuthidae. etc . A . Brachioteuthis . . B . Cirrobrachium . . X . Pholidoteuthidae .. A . Pholidoteuthis

XI . Bathyteuthidae .. A . Bathyteuthis .. B . Ctenopteryx .. XI1. Enoploteuthidae .. A . Abralia . . .. B . Abraliopsis .. C. Enoploteuthis .. D. Pterygioteuthis . . E . Pyroteuthis .. F. Ancistrocheirus . . G . Thelidioteuthis . H . Wataseniu . I. Enqloion ..

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XV . Histioteuthidae A . Histioteuthis B. Calliteuthis

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XVI . Chiroteuthidae . . A . Bigelowia B . Chiroteuthis C . Echinoteuthis D. Entomopsis E . Chiropsis .. F. Valdemaria .. G . Mmtigoteuthis . . H . Larval chiroteuthids XVII . Lepidoteuthidae . Lepidoteuthis

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XVIII . Grimalditeuthidae . A . Grimalditeuthis XIX . Cranchiidae . . .. A. Cranchia B . Crystalloteuthis C . Liocranchia . D. Pyrgopsis . E . Leachia .. .. F. Drechselia . G. Ascocranchia . H. Egea . . .. I. Xandalops .. J . Corynommu .. K. B a t h o t h u m . L. Taonidium .. M . Teuthowenia . N . Toxeuma .. 0. Megalocranchia P. Helicocranchia . Q . Anomalocranchia R . Hensenioteuthis S. Fusocranch~ . T . Phasmatopsis .. U . Taonius V . Verrilliteuthis . W . Galiteuthis .. X . Mesonychoteuthis XX . Spirulidae .. .. A . Spirula .. .. XXI . Distribution . .. XXII . Depth .. .. .. XXIII Egg masses . .. XXIV . Growth, size and form XXV . Structural variation .. XXVI . Parasites .. .. XXVII . Ecological importance XXVIII . Economic importance XXIX . Catching methods XXX . Acknowledgments .. XXXT. References . .. AUTHOR INDEX .. .. .. SPECIESINDEX . .. .. SUBJECT INDEX . . ..

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Adv. mar. Bid.. Vol. 4, 1866, pp. 1-89

DISEASES OF MARINE FISHES CARL J. SINDERMANN U.S. Bureau of Commercial Fisheries, Biological Laboratory, Oxford, Marylund, U.S.A. "

One of the most serious gaps in our knowledge of marine ecology is the study of diseases epidemics are common occurrences in marine environments. They may be en important cause of fluctuations, and should therefore have a prominent place in research programs." Lionel A. Walford, " Living Resources of the Sea '*, Ronald Press Company, 1958, p. 147.

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. I. Introduction .. .. 11. Microbial Diseases A. Viruses .. .. .. .. .. .. B. Bacteria .. .. .. .. .. C. Fungi . . .. .. .. .. D. Protozoa .. .. .. .. .. 111. Other Parasitic Diseases . . .. .. .. A. Helminths .. .. .. .. B. Parasitic Copepods .. .. .. .. IV. Genetic and Environmentally Induced Abnormalities .. .. .. .. .. V. Effects of Disease A. Epizootics and Mass Mortalities . . .. B. " Background " Effects . . .. .. C. Economic Effects .. .. .. .. VI. Variations in Disease Prevalence . . .. .. A. Geographic Variations .. .. .. B. Temporal Variations . . .. .. .. C. Age Effects . . .. .. .. VII. Immunity . . .. .. .. .. VIII. Diseases in Marine Aquaria . . .. .. .. Ix. Relationship of Fish Diseases to Human Diseases . x. Future Studies of Marine Fish Diseases .. .. XI. Summary .. .. .. .. .. XII. References .. .. .. .. .. XIII. Acknowledgments . .. .. .. ..

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I. INTRODUCTION Research commitment to the study of marine fish diseases has been until recently sporadic and inadequate. Although knowledge of freshwater fish diseases has proliferated, especially in hatcheries, little incentive has existed for comparable investment in Understanding the ills of marine species. The vastness of the oceans, the complexity of natural factors regulating the size of fish populations, and the lack of 1

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methods to control and manipulate such factors, have tended to discourage continuing and extensive studies of such specific aspects of the marine environment as disease. Growing awareness that the human population is increasing enormously, that over two-thirds of the earth’s surface is ocean, and that we understand little of the dynamics of production in the sea, has led to increasing scrutiny in recent years of those variables that might a t any particular time become overriding in their influence on population size. Disease is one such variable. Diseases of food fishes have logically received greatest attention in past research, and will do so in the present paper. Parasites and diseases, in addition to killing the host, can materially reduce the value of fish as food for humans ; this fact serves as a further incentive to examine diseases of commercial species. Non-utilized fish may receive attention because of some academic interest, but the preponderance of research concerns food species with large biomass. The term “ disease ’’ is used here in its broadest possible sense, to include any departure from normal structure or function of the organism-encompassing those states that result from activities of infectious agents, parasite invasion and genetic or environmentally induced abnormalities. Such a broad definition of disease in marine fishes requires the inclusion of a surprising amount of widely scattered literature-probably more than can be comfortably considered in this review, and certainly more than might be expected in view of the apparent neglect of the field. Access to the literature on marine fish diseases is a t present indirect. Several general texts on fish parasites and diseases have appeared in the German language (Hofer, 1904 ; Plehn, 1924 ; Schaperclaus, 1954 ; Amlacher, 1961). The latest edition of Schaperclaus’ excellent text contains information on disease in marine as well as fresh-water fishes. Recently, several shorter texts on diseases of lower vertebrates by Reichenbach-Klinke have been translated into English, expanded, and combined into a more comprehensive work (Reichenbach-Klinke and Elkan, 1965). Kahl, Reichenbach-Klinke, and Schaperclaus have made numerous significant contributions to the German literature. Russian texts, symposium volumes and reviews (Liaiman, 1949, 1957; Dogiel, 1954, 1955; Petrushevskii, 1957; Dogiel et al., 1958; Pavlovskii, 1959, 1962; Polyanski and Bykhovskii, 1959) contain summarizations of marine studies and have appeared in English translations. Among the important contributors to the Russian literature have been Dogiel, Petrushevskii, Polyanski and Shulman. Other nations have also made significant summarizing contributions to the general literature on fish diseases. Bergman (1923) published an early monograph in Swedish; k’ujita (1943) published a text on diseases of fish and shellfish in

DISEASES OF MARINE FISHES

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Japanese; Davis (1953) published an English language text on culture and diseases of fresh-water game fishes; and Ghittino (1963a) recently published a handbook in Italian. A symposium on fish diseases held at Turin, Italy, in 1962 has been published by the Office International des Epizooties (Altara, 1963). English-language reviews and symposia on selected aspects of fish-disease research, usually including references to marine diseases, have appeared (Kudo, 1920, 1924, 1933; Sproston, 1946; Nigrelli, 1952a; Oppenheimer and Kesteven, 1953; Snieszko, 1954; Manter, 1955; Hoffman and Sindermann, 1962, Oppenheimer 1962; Sindermann, 1963; Post, 1965; Putz et al., 1965; Snieszko et al., 1965). Texts which include considerations of marine fish diseases and parasites include: Breed et al. (1957)-bacteria; Johnson and Sparrow (1961)fungi; Kudo (1954)-protozoa; Yamaguti (1958-63)-helminths; Dawes (1946, 1947) and Skrjabin (1947-62)-trematodes; Wardle and McLeod (1952)-cestodes; and Yorke and Maplestone (1926)-nematodes. Johnstone, Kabata, Linton, Nigrelli, Snieszko and Templeman are among those who have made important contributions to the English and American literature. The general plan of this paper is to consider examples of the significant diseases of marine fishes, concentrating sensibly on those that have received somewhere near adequate scientific attention, and attempting to include those caused by a wide variety of pathogens and parasites. I n the necessary process of selection a t least two things happen : (1) many examples and much literature must be neglected or not treated in sufficient depth, and (2) a natural tendency arises to choose examples close a t hand or drawn from the author’s research. Thus, illustrative material has been taken to a large extent from studies in the North Atlantic, although comparable material could be obtained from other geographic areas. Omitted is much of the great but scattered fund of published information from parasite surveys, including a large part of the ecological parasitology of the USSR, which has been effectively summarized by Dogie1 et al. (1958). Many descriptions of occasional parasites of fishes have not been considered, even though effects of such parasites may be properly included in the broad definition of disease used in this paper. The literature cited thus includes only a small part of the often extensive published information on any particular parasite group. The references, extensive as they may seem, represent a too-small sampling of the world literature. This is particularly true of the older literature, which for groups such as the Myxosporidea and Microsporidea is voluminous and elaborate. References to some of the early literature have been compiled by McGregor (1963); access to other early work can be gained through bibliographies

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CARL J. SINDERMANN

included in more recent papers. For such parasite groups as the haemogregarines, the monogenetic trematodes, the cestodes, the nematodes, or the parasitic copepods, the consideration in this paper therefore represents only a tiny, but hopefully a representative, fraction of the whole. Diseases of estuarine and anadromous species are included, as well as those of species that are strictly marine, except that treatment of anadromous fishes is limited to situations where the pathogen or parasite is of marine origin. Diseases of fishes from saline inland seas have been considered, since many of the hosts and their parasites are of marine origin. Many of the diseases discussed are characteristic of inshore or estuarine waters, where abnormal conditions are more readily noted and examined than in the open sea. Fish carcasses washed up on beaches or floating in shoals near shore are much more likely to elicit action, scientific or otherwise, than would similar events a hundred miles from shore. Also, scientific studies of marine animals in the past have often varied inversely with distance from the shore. As a result, much of the world literature on fish diseases concerns inshore events.

11. MICROBIALDISEASES Included in the category of “ microbial diseases ”, and aggregated here largely for convenience, are those of viral, bacterial, fungal and protozoal etiology. They include the infectious diseases of fishes, caused by parasites capable of destruction of host tissue and multiplication within the fish. Resultant pathology and the course of disease may depend on such factors as infective dose, virulence and resistance of the individual host animal as well as host nutrition and other environmentally influenced variables (Snieszko, 1957a, 1964). The disease condition may range from chronic to acute, with varying degrees of host response. A. 8truses ’ Virus diseases of marine fishes, although not unknown, are not reported abundantly in the scientific literature. Much of this lack of knowledge probably stems from the absence, until recently, of adequate techniques for study. With the successful establishment of fish cells in culture (Wolf and Dunbar, 1957 ;Clem et al., 1961;Wolf and Quimby, 1962), a most important tool has become available, and understanding of the role of viruses in marine fish populations should increase greatly in the next decade. Viruses are best known in marine fishes as suspected or known etiological agents of several neoplastic, hyperplastic and

DISEASES OF MARINE FISHES

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hypertrophic diseases. Lymphocystis disease and certain papillomas have long been felt to be of viral origin, based on epizootiological and transmission studies, and on the presence of inclusions in affected cells. Lymphocystis is probably the best known virus disease of marine and fresh-water fishes. First described from the European flounder, Pleuronectes jlesus (L.),* by Lowe (1874), and soon after from other species (McIntosh, 1884, 1885; Sandeman, 1892 ; Woodcock, 1904), the disease has since been reported from the orange filefish, Alutera schepfi (Walb.), by Weissenberg (1938) and Nigrelli and Smith (1939); the killifish, Fundulus heteroclitus L., by Weissenberg (1939a) ; the red mullet, Mullus surmuletus (L.), by Alexandrowicz (1951) ; and from other marine and fresh-water species (Smith and Nigrelli, 1937; Weissenberg et al., 1937; Weissenberg, 1945). Recently several cases of presumed lymphocystis in striped bass, Roccus saxatilis (Walb.), have been observed (Anonymous, 1951; Sindermann, unpublished). The disease was originally thought to be caused by parasitic protozoa or eggs of another animal laid under the skin of fish (Sandeman, 1892; Woodcock, 1904). Weissenberg (1914, 1920) and Joseph (1918) were the first to recognize lymphocystis cells as hypertrophied fibroblasts. Transmission studies (Ragin, 1927, 1928; Weissenberg, 1939b, 196lb; Wolf, 1962) have demonstrated the infectious nature of the disease and have suggested some degree of host specificity. Definitive evidence that a virus is responsible for lymphocystis was obtained by electron microscopy (Walker, 1962; Walker and Wolf, 1962) and by transmission of the disease with ultracentrifugates and bacteria-free filtrates (Weissenberg, 1951a; Wolf, 1962). Manifestations of lymphocystisinclude whitish nodules on body and fins caused by hypertrophy of fibroblasts and osteoblasts (Fig. la). The connective tissue cells grow to enormous size (5mm in some cases)and become surrounded by a thick hyaline capsule. In severe cases most of the body surface may be involved. Weissenberg (1921a)reported that in some areas up to one-third of a population of fish could be affected. A great body of literature has accumulated on lymphocystis, and much of the early work was well summarized by Nigrelli and Smith (1939). A history of research on the disease has just been published (Weissenberg, 1965). A recent and apparently sharply defined outbreak of lymphocystis

* Throughout the paper an attempt has been made to give common and scientific names of fishes when they are first mentioned, and only the common name thereafter. In some cams this is not possible, aa for example when the =me common name ia applied to several different species in different geographical are-, or when a species m y have a different common name in different areas. Scientific names of fishes from North American watera follow the recommendations of the American Faeries Society (1960).

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Lymphocystis disease of the dorsal fin ; ( 6 ) papilloma of flounder ; (c) cauliflower disease of eel. (0)

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DISEASES OF MARINE FISHES

in American plaice, Hippoglossoides platessoides (Fabr.), of the Grand Bank was reported by Templeman (1965b). Infected fish were first seen in 1960, and in 1964 the infection level in American plaice on the eastern slope of the Grand Bank was approximately lo/. Badly infected fish, called " scabby " or " seedy " by fishermen, were thrown overboard, and estimates of such discards ran as high as 300-400 pounds per set in areas of heavy infections. Trawlers usually moved to other locations where fewer fish were diseased. Templeman suggested several possible explanations for the outbreak, including the possibility that the disease is enzootic in the population and may increase in intensity periodically. Nordenberg (1962) found infections as high as 12% in flounders, Pleuronectes Jlesus, from the Oresund, with some indication of higher prevalence in the warmer months of the year. Neoplastic or hyperplastic diseases, some thought to be of virus origin, include dermal and epidermal papillomas of many flatfish species (Fig. lb). Such diseased conditions have been reported from : halibut, Hippoglossus hippoglossus L., by Johnstone (1912a) ; plaice, Pleuronectes platessa (L.), by Johnstone (1925); sole, Solea solea (L.), by Thomas (1926) ; winter flounder, Pseudopleuronectes americanus (Walb.), by Smith (1935) ; flathead sole, Hippoylossoides elnssodon Jord. and Gilb., by Wellings and Chuinard (1964) and Wellings et al. (1964); as well as from other pleuronectids. Suspected viral particles have been described from the cytoplasm, but transmission has not been reported. Similar epidermal hyperplasia, of suspected viral etiology, is common in fresh water among European cyprinids. Characterized by irregular white raised patches on the skin, the disease is often referred to as " fish pox " (Roegner-Aust and Schleich, 1951 ; Roegner-Aust, 1953). A remarkable tumorous growth of eels is aptly labelled " Blumenkohlkrankheit " or " cauliflower disease " (Fig. lc). This common chronic fibro-epithelial tumor, often of dramatic proportions, occurs principally in the head region of European eels, Anguilln anguilla (L.). Reports of the disease in European rivers and coastal waters have increased in recent years (Schaperclaus, 1954 ; Liihmann and Mann, 1957 ; Engelbrecht, 1958). Transmission has not yet been effected, but virus etiology is strongly suspected (Christiansen and Jensen, 1950). Eels with progressive tumors become emaciated and die. Schaperclaus (1953a) also found comparable growths in cod, Godus niorhun L., and papillomas have been reported from smelts, Osmerus eperlanus (L.), taken in the Baltic Sea with characteristics very similar to cauliflower disease of eels (Breslauer, 1916). A number of highly pathogenic viruses of fresh-water fishes do not cause tumors (Wolf, 1964). The diseases produced include infectious A.Y.B.-4

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CARL S . SINDERMANN

stomatitis in fishes from South American rivers (Torres and Pacheco, 1934 ; Pacheco, 1935), viral hemorrhagic septicemia of salmonids in Europe (Jensen, 1963), and infectious pancreatic necrosis of trout, Xalvelinus fontinalis (Mitchill) and S a l m guirdneri Richardson (Wolf et al., 1960). Among the anadromous species, viral etiology has been indicated for a disease of chinook salmon, Oncorhynchus tshawytscha (Walb.), from the Sacramento River, California (Ross et al., 1960; Parisot and Pelnar, 1962), and for a more widespread disease of sockeye salmon, Oncorhynchus nerka (Walb.), in the Pacific Northwest (Watson et al., 1954; Guenther et al., 1959). Transovarian transmission was hypothesized for the chinook disease, and the feeding of fingerlings with diets including salmon carcasses was implicated in the sockeye disease. The discreteness of the viruses involved, and the pathological changes in host tissue, have been summarized by Parisot et al. (1965) and Yasutake et al. (1965). Viruses that do not cause tumors have not yet been clearly demonstrated in marine fishes. Moewus (1963) reported studies of a ciliate parasite, Miamiensis avidus Thompson and Moewus, which was isolated from tumor-like nodules on seahorses, Hippocampus erectus Perry. The organism was studied as a possible vector of virus; polio virus was used in absence of a suitable laboratory strain of marine virus. Results were inconclusive, but the author’s suggestion of parasites as possible vectors of fish viruses does not seem unreasonable ; in fact it was made previously by Thomas (1931) and Nigrelli (1948) in reference to epidermal hyperplasias of cyprinids. Transmission of viral and rickettsia1 agents by parasites is known for certain diseases of mammals (swine influenza and salmon poisoning of dogs). Moewus-Kobb (1965) also reported that virus of infectious pancreatic necrosis of fresh-water fishes multiplied when introduced into cell cultures derived from a marine fish, the grunt, Haemulon sciurus (Shaw). The same cell line of grunt was found to harbor a presumed “ orphan virus ” destructive to primary explants as well as fish cell lines (Clem et al., 1965).

B. Bacteria Reports of bacterial epizootics in marine fishes are surprisingly infrequent, and in fact relatively few bacterial pathogens have been recorded from natural populations of marine fishes. This is probably due to lack of observation or to inadequate examination rather than lack of occurrence. Two examples support this view. Oppenheimer and Kesteven (1953) reported underwater observations of fish schools in which up to 10% of individuals exhibited lesions indicative of bacterial infections later demonstrated by smears and cultures. Sindermann and

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Rosenfield (1954a) in their study of bacterial tail rot of Atlantic herring, Clupea hnreagus I,. , reported observation of typical disease signs in schools of immature fish from the Maine coast (Fig. 2 ) . Among the widespread bacterial epizootics, one caused by a species of Pccsteurelln resulted in extensive and selective mortalities of white perch, Roccus nnaericnnus (Gmelin), and to a lesser extent striped bass in Chesapeake Bay during the summer of 1963 (Snieszko et al., 1964). The pathogen was isolated coiisisteiitly in pure culture from moribund white perch, and was identified as a member of the genus Pasteurellrr on the basis of morphology aiid biochemical tests. Catch statistics aiid

FIG.2.

Bacterial tail rot in jiivenilc Atlantic herring. (From Sinder~nanri,19ti3.)

unpublished observations by the author in 1964 suggested that significant population decimation had resulted from the epizootic. This is a very recent aiid as yet only partially documented example of a severe epizootic which undoubtedly has its counterparts caused by other bacterial pathogens in various parts of the world. Most of these outbreaks, because of location, or because they may not involve food fish, probably escape scientific scrutiny, aiid are viewed by local inhabitants with the same dismay aiid bewilderment that must have characterized the great human plagues aiid epidemics of past centuries. Of all the known bacterial diseases of marine fishes, nolie has a longer or more fascinating history than the " red disease " of eels,

10

CARL J . SINDERMANN

caused by Vibrio nnguillarum Bergman. The disease occurs during the warmer months in brackish and salt water ; reports have been most numerous from the Danish, German, Italian and Swedish coasts, and the Baltic and North Seas. According to Hofer (1904), the disease was known and reported as early as 1718 from the Italian coast, and extensive epizootics occurred repeatedly during the nineteenth century (reports date from 1825, 1850, 1864, 1867, 1884, 1885, 1889 and 1892). Signs of red disease include progressive reddening of fins and skin, visceral hemorrhages, reduced activity and death-often preceded by loosening and fraying of the skin. The term " red disease " was introduced by Feddersen (1896) in reporting an outbreak of the disease in Scandinavian waters. Comparable outbreaks have occurred repeatedly to the present time (Feddersen, 1897 ; Bergman, 1909 ; Bruun and Heiberg, 1932, 1935 ; Ljungberg, 1963), often causing significant mortalities and economic losses. The disease has also been reported from The Netherlands (Schaperclaus, 1927), Poland (Kocylowski, 1963), and Germany (Schaperclaus, 1934; Mattheis, 1060). Characteristically, infections become evident among eels stored, even for short periods, in live boxes. Dead eels may be found in nets, traps and impoundments during epizooticsthe disease apparently spreads very rapidly among captive fish. An extensive survey was conducted by Bruun and Heiberg (1932) documenting the widespread occurrence of the disease in Scandinavian waters a t the time, and providing information about previous outbreaks dating back to 1880-outbreaks which sometimes brought the fishery to a standstill. V'ibrio anquillarum appears to be a truly marine pathogen, limited to salinities above 9 %,, and unable to survive in fresh water. Infection may occur through gills or digestive tract. Its effect is most pronounced and mortalities are most common in late summer, in areas where sea temperatures exceed 16°C. Bruun and Heiberg raised new questions in their report on the 1931 epizootic in Danish waters by suggesting that several pathogens may be involved in red disease from different geographic areas. They pointed out that only a few of the early studies (Canestrini, 1893; Inghilleri, 1903; Bergman, 1909) included bacterial examinations, and that a t least three bacterial disease entities may be involved in salt water. Schaperclaus (1930) also demonstrated that red disease of eels in fresh water may be caused by Pseudomonas (Aeromonas) punctata Zimmerman. Other observations suggest that reddening of the skin of eels may be a generalized response t o abnormal temperatures and reduced availability of oxygen, as well as to bacterial invasion. There

DISEASES O F MARINE FISHES

11

seems little doubt, however, that a common infectious agent is involved in many of the outbreaks reported, since Vibrio anguillarum has been isolated repeatedly (Bergman, 1909; Schaperclaus, 1927 ; Nybelin, 1935b). Two types, A and B, of the Vibrio have been identified, and a toxin has been demonstrated. V . anguillarum has also been found to be pathogenic t o cod and plaice (Dannevig and Hansen, 1952; Bagge and Bagge, 1956; Ljungberg, 1963), pike (Schaperclaus, 1928; Ojala, 1963), and trout, Salmo trutta L. (Smith, 1961). Other Vibrio diseases of marine and fresh-water fishes have been reviewed by Rucker (1959). He suggested that Vibrio infections may be much more prevalent than had been previously recognized, pointing out as examples that Vibrio infections often kill Pacific herring, Clupea pallasi Val., held as live bait, and that a study by Biickmann (1952) disclosed that almost half of a sample of 117 European plaice had natural Vibrio infections. Bacterial dermatitis, sometimes accompanied by ulcerations and fin rot and usually associated with Pseudomonas, has been reported from wild populations of marine fishes. Pseudomonas ichthyodermis infections have been observed by Wells and ZoBell (1934), ZoBell and Wells (1934), and Hodgkiss and Shewan (1950). ZoBell and Wells reported evidence of the infection in killifish, Fundulus parvipinnis Girard, in their natural habitat on the Pacific Coast, and stated that 90% of these fish died of the disease when brought into aquaria during the summer. Other species, such as gobies, Gillichfhys mirnbilis Cooper, blennies, Hypsoblennius gilberti (Jordan), and smelt, Atherinops afinis (Ayres), also exhibited lesions. Characteristics of the disease included an initial whitish spot on the body surface which expanded rapidly, disintegration of melanophores, raising and sloughing of scales, minute hemorrhages and death. Smears from lesions revealed almost pure cultures of Pseudomonas ichthyodermis, but there was no evidence of systemic invasion, nor could the organism be demonstrated in the blood. Reinfections from cultures were made repeatedly; initial lesions occurred within 18 hours and death within 14 days. Mortality of fish infected from cultured pathogens was not as high as that of fish infected directly with material from lesions. The pathogen was described as a motile, Gram-negative, non-spore-forming, halophilic bacillus, with a temperature optimum for infectivity, growth and virulence in the region of 20°C. A significant finding was that fish kept in water above 30°C did not become infected and that badly diseased fish recovered rapidly if acclimated successfully to water of 32-35OC. Hodgkiss and Shewan (1950) described an intramuscular lesion in plaice and obtained presumptive evidence that Pseudomonas ichthyo-

12

CARL J. SINDERMANN

dermis was the etiological agent. More recently, Shewan (1963)has suggested that the pathogen should be placed in the genus Vibrio. Tuberculous lesions with acid-fast bacilli have been reported from a number of commercial marine fishes, including halibut (Sutherland, 1922 ; Johnstone, 1927 ; Hodgkiss and Shewan, 1950),cod (Alexander, 1913 ; Johnstone, 1913), and plaice (Hodgkiss and Shewan, op. cit.). Spontaneous lesions of this type in marine fishes have been thought until recently to be rare, so that single cases have warranted descriptions in the literature. Aronson (1926) characterized and named Mycobacteriuin marinun? from several species of marine fishes, including Atlantic croaker, Micropogon undulatus (L.) and sea bass, Centroprisfes striatus (L.), in the Philadelphia Aquarium ; this remains as the only fully-characterized Mycobacterium of marine fish origin, although others are known to exist and have been partially characterized (Alexander, 1913; Sutherland, 1922; Griffith, 1930; Reichenbach-Klinke, 1 9 5 5 ~ ) . Aronson (1938) pointed out that mycobacteria responsible for spontaneous tuberculosis in marine fishes differed from acid-fast bacilli known as human pathogens, but the classification of pathogenic mycobacteria is at present very confused (McMillen and Kishner, 1959; McMillen, 1960; Nigrelli and Vogel, 1963). A recent review by Vogel (1958)reported acid-fast bacillus disease, principally in the form of visceral lesions, in 120 species of marine and fresh-water teleosts throughout the world. Parisot (1958)has also reviewed the literature on tuberculosis in fish. He suggested that this disease may be serious for adult Pacific salmonids, and that it may be partly responsible for recent decreases in the catch. Wood and Ordal(1958),Ross et al. (1959), and Ross (1960)found high prevalence of tuberculosis in salmon returning from the sea, but attributed much of it to early exposure t o bacilli in hatchery diets which included carcasses of tuberculous fish. Walford (1958)listed tuberculosis as a disease of young Pacific salmon, and felt that the pathogen may have been acquired in the sea. Infected fish were characterized by reduced growth, incomplete gonad development, and kidney lesions containing acid-fast bacilli. I n addition to tuberculosis, Walford considered several other interesting bacterial diseases of young Pacific salmon from salt water. (1) " Hemorrhagic septicemia " occurred repeatedly and caused extensive mortalities in young salmon held in salt water. Outbreaks were found t o be caused by a Vibrio enzootic in Pacific herring, and thought to be responsible for outbreaks and mortalities in herring and sardines, Sardinops sagax (Jenyns), of the Pacific Northwest. Other organisms, such as Pseudomonas (Aeromonas) punctata have been reported to cause hemorrhagic septicemia in fresh-water pond fishes.

DISEASES OF MARINE FISHES

13

(2) " Eye disease " of salmon, cod and other bottom fishes was also caused by a Vibrio. The disease was characterized by initial destruction of the eyes, followed by bacteremia and death. This malady may be similar or identical to " Augenkrankheit " of North Sea cod (Bergman, 1912). (3) " Boil disease " was found to be a progressive and highly fatal disease of young salmon, characterized by muscle abscesses. The pathogen was a diplobacillus resembling the causative agent of kidney disease of salmon in fresh water. (4) A myxobacterial disease similar to " columnaris disease " of fresh-water salmonids was characterized by development of gray-white lesions anterior to the tail. The lesions progressed with sloughing of skin and fins. The myxobacterium Chondrococcus columnaris (Davis) Ordal and Rucker, 1944, has been described as infecting skin, gills, and fins of Fundulus hetcroclifus (Nigrelli and Hutner, 1945) and other marine species (Davis, 1922; Garnjobst, 1945). This array of infectious diseases, either of salt water origin or enhanced by salt water phases of the life history of salmon, indicates the possibilities for disease studies in this and other anadromous fish (Rucker et al., 1954). Critical problems in the study of bacterial pathogens of fish, as may be deduced from the preceding, are the correct identification of the infectious agent and the determination of its role as primary or secondary invader. Not only is bacterial classification confused (Krasilnikov, 1949 ; Breed et al., 1957 ; PrBvot, 1961), but type cultures may be unavailable, and often biochemical and physiological characterization is incomplete. Bullock (1961, 1964) has made important contributions to the systematization of methods to identify bacterial pathogens in fresh water and Colwell and Liston (1960), Shewan (1961, 1963), Shewan et al. (1954, 1958, 1960), and Scholes and Shewan (1964) have attempted similar systematization for marine bacteria. Bacterial pathogens most commonly reported from sea fishes are species of Pseudomonas, Vibrio or Mycobacterium. Many of the bacteria normally present in sea water, or on the surface of fish, can invade and cause pathological effects if fish are iiijured or subjected to other severe environmental stresses.

C. Fungi The role of fungi in the oceans has been admirably summarized in a recent book by Johnson and Sparrow (1961). Fungus diseases of marine organisms received excellent coverage by the authors, and it is startling to note that with the single exception of Ichthyophonus hoferi (Plehn and Mu1sow)-often referred to as Ichthyosporidium

14

CARL J. SINDERMANN

hoferi-which is discussed in detail in various sections of this paper, fungus diseases of marine fishes are almost unknown. Half a century of sporadic study in Europe and North America has provided evidence that one of the most serious fungus pathogens of fishes, marine or fresh water, is Ichthyophonus hoferi. Systemic infections, found in mackerel in England (Johnstone, 1913 ; Sproston, 1944), rainbow trout in Germany (Plehn and Mulsow, 1911), herring and mackerel in Canada (Sindermann, 1958), can result in widespread mortalities in these arid other species. Epizootics of the disease are characteristic of herring, Clupea harengus, of the western North Atlantic (Cox, 1916; Fish, 1934 ; Scattergood, 1948). Six such outbreaks have been reported since 1898 (Sindermann, 1963). Drastic reduction in herring abundance due to disease has been documented, and the postulation made that this disease may be the most important single limiting factor t o population growth of herring in the western North Atlantic. Whether a single species, or a complex of related forms (Schaperclaus, 1953b ; Sprague, 1965), Ichthyophonus is known as a menace to aquarium fishes in Europe (Lederer, 1936), as an introduced pathogen in trout hatcheries of western United States (Rucker and Gustafson, 1953), as a long-recognized pathogen of wild salmonids in western Europe, and as a pathogen of many other marine and fresh-water fishes. Reichenbach-Klinke (1954, 1955a) has assembled a list of more than 80 species that have been found to be infected by the fungus. The disease is systemic, with foci of infection in the heart, viscera and lateral somatic muscles (Fig. 3). A simple sequence of life history stages, described from herring (Sindermann and Scattergood, 1954), involves multiple germination of heavy-walled spores, hyphal invasion of host tissues, formation of " hyphal bodies " and sequential germination of these entities. The disease has been reported in Atlantic herring in chronic and acute phases. Acute infections were characterized by massive tissue invasion, necrosis and death within 30 days. Chronic infections exhibited cell infiltration, progressive connective-tissue encapsulation of spores and accumulation of melanophores. The disease was rarely arrested completely, however, and deaths occurred in most fish within six months. During the most recent epizootics, infections averaged about 25% of all herring sampled, and many cases were acute. Enzootic prevalence was usually well under 1% and infections during this phase have been chronic in all cases examined. Transmission of the disease has been achieved by feeding massive spore doses, derived either from cultures or from diseased fish. Increase of experimental spore doses resulted in increasing numbers of chronic

15

DISEASES OF MARlNE FISHES

infections and, beyond a certain dosage, the appearance of acute infections (Sindermann, 1963). Experimental epizootics that have been produccd in large sea water aquaria duplicate many of the events observed in nature. Herring varied individually in responses to identical spore doses ; some acquired acute infections, some acquired chronic infections, aiid some remained uninfected. A more complex life cycle for Zchthyophonus has been described from mackerel by Sproston (1944). This is the only study in which indications of sexual reproduction, in the form of liyphal fusions, were observed. Other authors have described the occasional appearance of conidia-like bodies, and the occurrence of macro- aiid micro-hyphae.

FIG.

3. Invasion ant1 destruction of lateral body niuscles of Atlantic herring by Ic.hl/t!loplromrs h o j c ~ i . Fish dissected t o show tiorinal muscle (top) and necrotic inriaclc i n acute infection (bottom).

Reiclienbach-Iilinke ( 1 9Fi6a) aiid others have raised the question of several possible species, but definitive culture studies have yet to be carried out. Reichenbach-Klinke (1956b, 1958) found Ichthyophonm to be very comnion in Mediterranean fish. Other than Zchthyophonus, reports of fungus pathogens of marine fishes are scarce in the scientific literature. Reichenbach-Klinke ( 19 5 6 ~ ) briefly described a species of Cladosporium found associated with hypertrophy of the epithelium of a cod, Gadus morhua, taken in the North Sea, but the disease is apparently rare. Reichenbach-Klinke also mentioned briefly a Cladosporium from the body cavity of two South American species of the genus Hyphessobrycon that may be found in brackish water. Apstein (1910) described infection of lumpfish, LI'

16

CARL J. SINDERMANN

C'yclopterus lunzpus (L.), by Cycloptericola marina. Cysts containing the fungus were found in the stomach wall of over half the specimens examined. It is not uncommon for diseases and parasites of fresh-water origin, including fungi, to be carried downstream with the anadromous host to the estuary and the sea, where survival is often limited. Such appears to have been the situation in the observation of Aleem et nl. (1953) of Isoachyla parasitica in Atherina riqueti in southern France. Similar external symptoms of fungus invasion have been seen in alewives, Alosa pseudoharengus (Wilson), and smelts, Osmerus mordax (Mitchill), as they enter the sea after spawning (Sindermann, unpublished). Saprolegnia infections of Pacific salmon disappeared when the fish were placed in sea water (Earp et nl., 1953), although Vishiiiac and Nigrelli (1957) have suggested that brackish-water fishes may be parasitized by the Saprolegniaceae.

D. Protozoa Sporozoa and Cnidospora* are among the best known and most serious pathogens of marine fishes, although representatives of other protozoan groups, such as the hemoflagellates and ciliates, have been studied (Laveran and Mesnil, 1902; Neumann, 1909; Tripathi, 1948; Brown, 1951; Laird, 1951; Reichenbach-Klinke, 1956d). Coccidia, Myxosporidea and Microsporidea have varied and often severe effects on their hosts, ranging from castration to nerve and muscle degeneration. Many of the species studied have characteristic and readily recognizable spore stages, which facilitate identification and encourage study. Most are specific for particular host tissues. For some, life cycles and transmission are adequately understood, but for many much remains to be learned, particularly about their ecology. 1. Coccidia

Severe and often fatal coccidian infections of mammals and birds have some counterparts in fresh-water fishes (Bespalyi, 1959) and to a lesser extent in marine species. A widely distributed disease of clupeoid fishes is that caused by Eimeria sardinae (Thdohan). The parasite localizes, often in massive numbers, in the testes (Fig. 4),where it may reduce reproductive capacity or cause complete sterility of the host (Pinto, 1956 ; Letaconnoux, 1960 ; Pinto and Barraca, 1961 ; Pinto et al., 1961). E . sardinae has been reported from the sardine, Sardina pilchardus Walb., off Portugal (Pinto, op. cit.), the sprat, Clupea

* An attempt has been made to conform to the revised system of classification of the Protozoa (Honigberg et al , 1964).

DISEASES OF MARINE FISHES

17

sprattus (L.)from the eastern North Atlantic (Thomson and Robertson, 1926). and the Atlantic herring, (‘lupea hrtrcrrgits. from the Baltic Sea (Dogiel, 1939 ; I)ollfus, 1956), Barents Sea (l’olyaiiski, 1955), IVhite Sea (Shulmaii and Shulman-i\lbova, 1953), North Sea (Kabata, 1963), and the western North Atlantic (Sindermann, 1961a). It occurred in over 50% of sardines sampled by Pinto (op. cit.) and thus must be considered a significant limitation t o the reproductive potential of th a t species. Other coccidiaii parasites of the testes of marine clupeoids have been reported. Spores of Eirrieria brevoortitrnn occur in the testes of menhaden, Brevoortici tyrannus (Latrobe), according to Hardcastle (1944) and spores of E . nishin have been described from Pacific herring

by Fujita (1934). E. brevoortiana was found in 420,: of 700 male fish examined, and was more common in adults than in juveniles. No spores were sceii in females. Eiweria may occur in other organs. E. clupearum (Th6lohan) is fourid in the liver of clupeoids, oftcii in abundance, but is usually not considered seriously pathogenic. E . g a d i has been described as R pathogen of several gadoid species by Fiebiger (1913). It parasitizes the swimbladder, where in situ germination of spores can produce heavy infections. E. crnguillae has been described as a parasite of the intestinal epithelium of eels in Europe (Leger a n d Hollaiide, 1922). Members of another coccidiaii group, the Haemogregarinidae, have long been recognized as of widespread occurrence in blood cells of fishes. Although the parasites were first reported in 1901 by Laveran a i d Mesnil, the complete life history of marine members of the group

18

CARL J. SINDERMANN

is still unknown. Haemogregarines have been described from menhaden in Florida by Saunders (1964), from arctic char, Snlvdinus nlpinus (I,.), in northern Canada by Laird (1961), from a mullet, Mugil brusiliensis Agassiz, in Brazil by Carini (1932), from javelinfish, Coelorhynchus australis (Richardson), in New Zealand by Laird (1952), and from many other fishes from diverse habitats (Laveran, 1906; Lebailly, 1906; Kudo, 1954). One species, Haemogregurina bigemina Laveraii and Mesnil, has been reported from Europe, Canada, United States, South Africa, the Red Sea and the South Pacific (Laird, 1958; Saunders, 1960). The haeniogregarines have not been reported as resporisible for mortalities.

3. Myxospor idea Diseases caused by Myxosporidea are common in marine as well as fresh-water fishes. The myxosporideans inhabiting organs such as the gall bladder are most frequently studied and described, but those localizing in the somatic muscles must be considered the most destructive and of greatest economic significance. Extensive necrosis of the flesh characterizes invasion of halibut, Hippoglossus stenolepis Schmidt, by two Myxosporidea : Unicapsula nuuscularis Davis which causes a condition known as " wormy " halibut, and Chloromyxum sp. which causes " mushy " halibut (Thompson, 1916 ; Davis, 1924). Both act t o reduce thevalue of the fish as food. Muscle necrosisin swordfish, Xiphias gladius L., from Japan has been reported by Matsumoto (1954) to be caused by the myxosporidean Chlorontyxuwb niusculoliquefaciens, and a similar " jellied " condition of swordfish from the North Atlantic has been observed (RIcGonigle and Leim, 1937). Another cnidosporan, Hexacapsula neothunni, has been associated by Arai and Matsumoto (1953) with a jellied condition of yellowfin tuna, T h u n n u s ulbacares (Bonnaterre), from Japan, and Pbrard ( 1 928) has described the degeneration of muscles of mackerel, Scomber scombrus L., resulting from parasitization by Chloromyxum histolyticum. " Milkiness "-a softening and liquefaction of the flesh of lemon sole, Parophrys vetulus Girard, and other species-was reported from the Canadian Pacific coast by Margolis (1953), Forrester (1956) and Patashnik and Groiiinger (1964) as due to a species of Chloromyxum. The condition known as " milkiness " in several species of fishes from the African coast has been associated with the presence of Kudoa (=Chloromyxum) thyrsites (Gilchrist). The parasite has been reported in snoek or barracouta, Thyrsifes atun (Euphr.), by Gilchrist (1924) ; stockfish, Merluccius capensis, by Fletcher, Hodgkiss and Shewan (1951) ; and the John Dory, Zeusfaber L., by Davies and Beyers (1947).

DISEASES O F MARINE FISHES

19

The same condition and parasite have been reported in Thyrsites ntun from Australia by Johnston and Cleland (1910) and Willis (1949). Milky ” flesh deteriorates rapidly after the fish is caught, probably due in part to a proteolytic enzyme secreted by the parasite, as postulated by Willis. In South African waters, Davies and Beyers (op. cit.) found that three-fourths of the John Dory and stockfish were infected with Kudoa thyrsites. A quarter of all John Dory were too heavily infected to be suitable for filleting. The same parasite occurred in 5 % of Australian barracouta (Roughley, 1951). The flesh of clupeoid fishes is often parasitized by Myxosporidea which produce opaque white cysts and necrotic areas (Fig. 5). A Chloromyxum occurs in the pilchard, Sardinops ocellntn, from South Africa (Rowan, 1956). Juvenile Atlantic herring, Clupen harengus, menhaden, Brevoortia fyrannus, and blueback herring, Alosa aestivnlis (Mitchill) from the Atlantic coast of North America are often parasitized by Kudoa (=Chloromyxum) clupeidae (Hahn, 1918 ; Meglitsch, 1947 ; Sindermann, 1961b). Several authors (Tyzzer, 1900 ; Linton, 1901 ; Sindermann, 1957) have noted that the parasite occurred only in smaller and younger members of the host species. As many as 75% of 1-year-old Atlantic herring from certain parts of the U.S. (Maine) coast were parasitized, but adults were not infected. Linton speculated that there were fewer infections among older fish because the vitality of the diseased fish was so impaired that they fell victim to predators in larger proportional numbers than did healthy fish. It seems equally likely that invasion occurs early in the life of the host, that spores mature and escape from cyst areas, and that evidence of disease is absent by the time the host reaches maturity. Among the anadromous fishes, the myxosporidean Henneguya salminicola Ward invades the flesh of several species of Pacific salmon, producing opaque white cysts described as “ tapioca disease ” (Fish, 1939). Spores of the parasite have also been seen in milky necrotic pockets in salmon from the eastern Pacific (Patashnik and Groninger, 1964). Similar pathological conditions and high prevalences have been described in salmon from the western Pacific by Akhmerov (1955). It can be seen from even a brief review that muscle-inhabiting Myxosporidea are of world-wide distribution and economic significance. This is particularly true of members of the genus Kudoa which was created by Meglitsch (1947) to include species removed from the genus Chloromy x u m that are histozoic with quadrate or stellate spores, These species are associated with necrosis of the flesh of living fish, and with rapid post-mortem deterioration and liquefaction. The gall-bladder-inhabiting Myxosporidea, of which there are many

20 CARL

J. SINDERMANN

DISEASES O F MARINE FISHES

21

species (Kudo, 1920), are of widespread occurrence in marine fishes. Heavy infections may cause enlargement, discoloration and disruption of function of the organ. Fantham and Porter (1912), who examined the widespread occurrence of gall bladder parasites in elasmobranchs and teleosts from the English and French coasts, found that myxosporidean parasitization caused inflammation of the organ, excess secretion of mucus and increase in viscosity of bile, enlarged livers and emaciation of the host. Gill-invading Myxosporidea are not usually of serious consequence to marine fishes. However, Shulman (1957) described an epizootic of Myxobolus exiguus in the gills of mullet, Mugil cephalus (L.),from the Black Sea in which 500-600 kg of fish per kilometer were washed up on the western shore of the Crimean Peninsula during the spring of 1949. Mechanical disruption of gill function, caused by heavy infection with myxosporidean cysts, was considered the cause of death. No abnormalities were noted in the viscera. Several species of Myxosporidea invade the cranial cartilages of fishes. One, Myxobolus aeglejini (Auerbach),occurs in plaice, Pleuronectes plntessa (L.), hake, Merluccius merluccius (L.), and haddock, Gadus aeglefinus L., of the North Sea (Johnstone, 1906 ; Auerbach, 1906, 1912 ; Kabata, 1957b). Erosion and in some instances hypertrophy of head cartilage results. Effects of M . aeglefini do not seem as severe as those caused by Myxosoma cerebralis (Hofer) in salmonid fishes. Myxosoma, a highly infectious disease agent acquired early in life in fresh water, causes " whirling disease " of juvenile salmon and trout, as well as gross skeletal abnormalities (Bogdanova, 1960 ; Hoffman ef al., 1962). The disease has long been known in central Europe, and has recently been found in Russia and United States. Dannevig and Hansen (1952) have reported symptoms indicating M . cerebralis infections in very young herring reared in aquaria. 3. Microsporidea

Several serious diseases of marine fishes result from microsporidean invasion. Smelts, Osmerus eperlanus, from Europe (Weissenberg, 191 Ic) and Osmerus mordax from North America (Schrader, 1921 ; Fantham et al., 1941) are often parasitized by Glugea hertwigi Weissenberg, which produces varying degrees of visceral involvement, to the extreme condition in which the body cavity is packed full of microsporidean cysts up to 9 mm in diameter. Heavy infections have been reported to prevent reproduction by mechanical occlusion of the vent (Haley, 1954 ; Sindermann, 1963) and lesser infections destroy areas of digestive tract and gonad and impair other metabolic functions. Haley found

22

CARL J. SINDERMANN

that 23% of the smelt he examined were infected; because of the serious pathological manifestations of the disease he suggested that it could be an important factor in the recently observed decline of the smelt fishery on the New Hampshire coast. Bogdanova (1957) reported that massive infections with G. hertwigi caused degenerative changes in sexual organs and death of the host. Dogie1 et 01. (1958) stated that

FIG.6.

Cross-sertion of Almrozoarces cimerirnniis through Plistophorn ryst.

infection of 0. Pperlanus caused functional disturbances in several organs, growth retardation, decline in fertility and mass mortality. Incidenre of Gluypa reached 25 to 50% and decline in storks of Osmerics was attributed to the parasite (Annenkova-~lilopina.1920). Templeman (1948) found a Gluyea, probably C:. hertzuigi, in capelin, Mallofus viZZosus (Muller), spawning on the Newfoundland coast. Almost one-

DISEASES OF MARINE FISHES

23

fourth of all fish examined carried cysts beneath the peritoneum or in the mesenteries. Another species of the same genus, (r. anomala (Moniez), was reported earlier (Weissenberg, 1913, 1921b) from European sticklebacks, Gnsterosteus aculeatus L. and Pungitius pungitius (L.). Hypertrophy of connective-tissue cells, resulting in thick-walled cysts up to 4 mm in diameter, occurred externally and internally. Kudo (1924) and others described deformation of the host’s body as a result of intensive G. anomala infection. The parasite has been reported as a cause of mass mortality in sticklebacks from the White Sea (Dogie1 et al., 1958). Still another species, Glugea punctifera Thelohan, is a serious intramuscular parasite of mintai, Theragra chalcograrnrna, from the Okhotsk and Japan Seas (Akhmerov, 1951). Cod from the Okhotsk Sea were also infected with this Glugea. The microsporidean Nosema lophii (Doflein) produces large tumorlike cysts in the central nervous system of the goosefish or angler-fish, Lophius piscatorius L. Parasitization results in extensive hypertrophy of host ganglion cells as the cyst develops, producing dark grape-like enlargements on the nerves. Weissenberg (1909, 1911a, 1911b, 1911c) found abundant infections at Naples; the parasite has also been reported from England and France. Another microsporidean, Plistophora macrozoarcidis Nigrelli, is an important parasite of the ocean pout, Macrozoarces aniericanus (Bloch and Schneider). Extensive tumor-like intramuscular cysts, often several centimewrs in diameter (Fig. 6), seriously reduce the marketability and utilization of this fish in the United States. Appearance of fillets containing parasite cysts on the market during 1943-44 was responsible in part for curtailment of a developing fishery for Macrozoarces, and in a few years led to complete disappearance of the species as a food fish in the United States (Fischthal, 1944; Sandholzer et al., 1945). Recent interest in reviving the fishery seems contingent on development of a suitable method of eliminating parasitized fish from processing procedures. Plistophora cysts can often be recognized by conspicuous bulges on the body of the host. The lesions are usually exposed during filleting, and a pus-like exudate of spores and tissue debris occurs when such areas are cut, Life cycle stages have been described by Nigrelli (1946). No ulceration has been seen. so the method of spore liberation has been postulated as death and decay of the host. The massive involvement of individual fish suggests sporulation in situ. Repeated auto-infection is possible in some species of Microsporidea,

24

CARL. J SINDERMANN

according to Kudo (1954), and some suggestion of it was found in Macrozoarces, since many specimens were characterized by immense numbers of minute infections involving single muscle fibers (Olsen and Merriman, 1946). Other species of Plistophora invade the flesh of fish also. Body muscles overlying the visceral cavity of the long rough dab, Drepanopsetta hippoglossoides Gill, are invaded by P. hippoglossoideos Bosanquet, forming cysts up to 10 mm long. Kabata (1959) found the parasite to be widely distributed in the North Sea. Cod of the Barents Sea were found to be infected with P. gadi by Polyanski (1955). The parasite produced large tumors (5 to 8 mm) in the body muscles.

111. OTHER PARASITIC DISEASES The invasive diseases, as considered in this paper, include those caused by the larger parasites-those that are non-multiplicative in the fish host once invasion has occurred. Of primary concern in marine fishes are the various parasitic worms and the tissue-invading copepods. Omitted from this discussion are leeches, most ectoparasitic copepods, parasitic Cirripedia and Isopoda, and lampreys, which, although of occasional concern, probably do not often exert serious effects on marine fish populations. Since the worms and copepods are large, conspicuous and often abundant, they have been observed and studied extensively. A. Helminths The helminths-trematodes, cestodes, nematodes and acanthocephala-are common parasites of marine fishes. Usually it is as larvae that the worms are of greatest significance. Adults occur in the digestive tract, but larvae are usually found in the flesh or in the viscera. The effects of worm larvae on the host include growth retardation, tissue disruption, metabolic disturbances, and even death in heavy infestations. Added economic effects include discarding of otherwise edible fish products, delay in processing operations and loss in oil yields. 1. Trematodes

Adult digenetic trematodes are common in the digestive tracts of marine fishes. Yamaguti (1958) recognized 367 genera and 1390 species from fish, but it is as larvae-as migrating cercariae and as metacercariae-that trematodes seem to be of greatest significance to the fish host. Marine teleosts serve as intermediate hosts for many trematodes, particularly those whose definitive hosts are shore-inhabiting or fish-eating birds and mammals. Metacercariae of such worms encyst

25

DISEASES OF MARINE FISHES

beneath the skin or in the body of inshore fishes. An excellent, example is the trematode Crgpfocofyle lingua (Creplin), whose life cycle in the western North Atlantic (Fig. 7 ) involves the periwinkle, Lifforina Zitform (IA.), the Atlantic herring, and the gull, LnrtiS cirgmtntus Pontoppidan. Originally a parasite of comparable species in north-

FIG.i . Life cyrle of ('ryplorolylr lingror in the uwtrrn North Atlantic

(tit)ov(,)

and rr:sult,s of parmitizat,ion of Atlmitir herring (hehiw).

western Europe (Christensen and Roth, 1 !bt9), the parasite was introduced in North American waters near t h r niiddlr of the nineteenth century, proloablg with its snail host (Stnnknrd. 1930). Cercariae of Cryptocotyle invade and encyst in the fins and integument of lierring and a number of other iiishore western Atlantic species, causing the formation of coiispicuous pigmented cysts or " black spots ". It has

26

CARL J . SINDERMANN

been demonstrated experimentally (Sindermann and Rosenfield, 1954b) that massive cercarial invasion will blind and kill immature herring, and it has been postulated that invasions of comparable magnitude are possible in the inshore habitat of the fish. Another larval fluke, Stephanostomum baccatum (Nicoll), occurs in a number of marine fishes, particularly flatfishes, from the Canadian Atlantic coast to the Baltic Sea. The life cycle, as elucidated by Wolfgang ( 1954), involves gastropods of the family Buccinidae, the winter flounder and other pleuronectids, and the sea raven, Hemitripterus americanus (Gmelin). Metacercariae occur in unpigmented cysts, concentrated on the blind side of the flatfish and in the fins, often in great numbers in larger fish. The parasite was originally reported from a halibut from the English coast by Nicoll (1907) and u a s later found in American plaice, Hippoglossoides platessoides (Fabr.), by Nicoll(1910). Dawes (1947) recorded six species of European flatfish as hosts. Many other larval trematodes occur in marine fishes. BykhovskayaPavlovskaya and Petrushevskii (1959)) for example, have listed 46 species of metacercariae from the USSR, of which almost half occurred in marine or estuarine species. Fish-eating birds and mammals have been identified as definitive hosts of most of these parasites. Mass mortalities due to larval trematode invasion have been reported from the Aral and Caspian Seas (Dogie1 and Bykhovskii, 1934; Dubinin, 1949). Red mullets, Mullus barbatus (L.) and M . surmuletus (L.) in the Mediterranean Sea are often parasitized by larval trematodes, according to Orlandini (1957). Adult digenetic trematodes are common parasites of the digestive tract, but are usually not a cause of serious disease. Cosmopolitan fish species harbor a number of adult trematodes throughout their range. Manter (1955) has reviewed the zoogeography of many, including the 20 species from Atlantic eels. He found that most of these trematodes were of marine origin, and that those characteristic of the eel in Europe were different from those reported in America. Apparently the parasites were acquired after the larval eels had separated in the Atlantic. Many of the trematode species found in marine fishes of a given geographic region are peculiar to that region, although similarities of fauna from major ocean areas such as European Atlantic and Mediterranean exist. Among the monogenetic trematodes parasitic on gills and body surfaces of marine fishes, a number become serious parasites in aquaria, where conditions for reinfestation are optimum. Only rarely, and under unusual conditions, have members of this group been demon-

DISEASES O F MARINE FISHES

27

strated to be pathogenic to fish in iiatural habitats. Heavy infestation of sticklebacks in the White Sea was felt to be partially responsible for mass mortalities (Dogie1 et uZ., 1958). Fish had beell isolated in tide pools, and the trematodes multiplied to numbers up to 1000 per fish. Two parasite species, G'yrodactylus arcuatus Bychowsky and G . bychozoskyi Sproston, were involved ; most of the fish died. Dogie1 and Lutta (193'7) studied an epizootic in the Aral Sea sturgeon. Acipenser nudiventris LOV.,caused by the gill trematode Sitzschia sturionis (Abilgaard). As a result of mortalities during 1936 the fishery, which previously had reached a peak of 400 tons per year, ceased to be of commercial significance for the next 20 years (Osmaiiov, 1959). Recent level of infestation in all conditions of salinity was reported at 50 to 75%. 2. Cestodes Adult cestodes are commoii and occasionally harmful digestivetract parasites of fishes, but, as with the trematodes, larval stages are of greatest concern to man. Larval tapeworms occur frequently in the viscera and flesh of marine and estuarine fishes (Fig. 8). The definitive hosts of many of these parasites are elasmobranchs or fisheating birds and mammals. Tapeworms which localize in the body muscles may occur in large numbers in individual hosts. Linton (1907) described such an infestation in butterfish, Poronotus triacasithus (Peck), of the North American east coast, in which several thousand larvae could be found in individual fish. Encysted plerocercoids, less than a millimeter in diameter, were concentrated in the flesh adjacent to the vertebral column, and up t o 75% of individuals in a sample were heavily infected. The parasite was identified as Otobothriuwi crenacolle Linton, which matures in the spiral valve of certain shark species, particularly the hammerhead, Sphyrna zygaenn (L.). Ripe, highly motile proglottids of the tapeworm are shed in the feces and presumably ingested by butterfish and other teleosts, in which the embryos invade the musculature and encyst. Other members of the cestode order Trypanorhyncha occur as adults in the digestive tract of elasmobranchs, and as larvae in the flesh and viscera of many teleost species. Elongate larvae of Poecilancistrium robustum (Chandler), called " spaghetti worms ", are very abundant in the flesh of drum, Pogonius croniis (L.), in the Gulf of Mexico. According to Chandler (1954) some municipal health departments have considered banning drum from markets because of frequent worm parasitization. Oppenheimer (1962) reported that spaghett,i worms were common in the flesh of many other fishes from the Gulf of

38

CARL J. SINDERMANN

Mexico. Large spotted scatrout. C p o s c i o ~nebulosus (Cuvier),harbored up t o 1 0 0 larval ori ins, a i d as niucli as 44% of a sample wcre infcstcd (Chandler, 1935a. 1935b). Many food fishes, such as herring, hake and mackerel, have becn reported t o harbor othcr trypanorhyiicli larvae (Johnstone, 1912b ; Liiitoii, 1923 ; Ruszkowski, 1931 ; Iiahl, 1937 ; Young. 1955 ; Rae, 1958). As a n example, Grillofiu erinciceus (van Beneden) is so common iii iiiaiiy North Atlantic teleosts t h a t ail extensive literature on its occurrence existed in t h e iiiiieteeiith century. Pleroceroids of the cestode were described by Johiistoiie (1912b) a s

among the most abundant helminth parasites of Irish Sra fish ; they occurred usually in mesenteries or the stomach wall, but, in hake a n d halibut, in the flesh adjacent t o the vertebral column. The life cycle was elucidated by Ruszkowski (1934). Rae (1958), in a study of the cestode in halibut of the eastern North Atlantic, found heaviest infestations in larger fish: 10 t o 20% of catches from banks off the west coasts of Scotland and Ireland were infested. Wardle (1932, 1935) reported the worm from the Canadian Pacific coast. Liiitoii (1925) described the adult stages of this and other Trypanorhyncha from sharks and skates, and Dollfus (1912) has made a n excellent critical examination of this interesting tapeworm group. Kandler (cited b y

DISEASES O F MARINE FISHES

29

Mann, 1954) reported disruption of growth as a result of tapeworm infestation of Baltic Sea turbot, Rhonibus nicrximus (I,.). Fish in their second year of life v rrc most seriously parasitized and complete recovery of normal growth rate took several years. Adult cestodes may occur in significant numbers in the digestive tract of fishes, although their prevalence in marine teleosts is low in comparison with th at of other helminths. Linton (1941) described many representatives from the western North Atlantic, and Wardle (1932, 1935) surveyed the Pacific coast fauna. The Pseudophyllidean genus Eubothrizcm Bloch (Abothrium Luhe) is common in marine and fresh-water fishes. Several species occur in the digestive tracts of cod, haddock, herring an d other sea fishes (Nybelin, 1922 ; Sprehn, 1934). Many other representatives of the Pseudophyllidea occur in teleost fishes (Wardle and McLeod, 1952), while the order Tetraphyllidea is well represented among the elasmobranchs (Woodland, 1927; Baer, 1948; Williams, 1968). 3. Nematodes

The nematode parasites of marine fishes have received attention primarily because certain larvae t h a t infest the flesh and viscera reduce the commercial value of the host. An outstanding example is the codworm, PorrocaecunL decipiens (Krabbe). The definitive host is the harbor seal, Phocn vitulina L., according to Scott (1953), and larvae occur in the flesh of cod, smelt, plaice, ocean pout and other species of inshore marine fish (Heller, 1949; Scott, 1950, 1954, 1955). Larvae may also pass from fish t o fish if infected smaller individuals (for example smelt) are eaten by cod. Olsen a n d Merriman (1946) reported ocean pout from New Brunswick t o be heavily infested-to the extent t ha t the flesh of some fish had a porous appearance. A similar parasitization of ocean pout had been described from the same area 25 years previously (Clemens an d Clemens, 1921). Scott and Martin (1957, 1959) found high prevalence b u t geographic variations in infestation of cod from the Canadian Atlantic coast ; infestation decreased in deeper waters and increased with age of the host. A survey of Porroeaecum adults in seals (Scott and Fisher, 1958) did not disclosed a direct distribution relationship with larvae in cod. Templeman et al. (1057), in an extensive survey of groundfish in the Newfoundland fishing area, found larval Porrocaecunh in cod, smelt, plaice, witch flounder (Glyptocephalus cynoglossus (L.) ), haddock and redfish (Sebastes marinus L.). Examination of over 15 000 fish disclosed that over three-fourths of all larval nematodes were Porrocaecuni ; the remainder were other larval Anisakinae. Fishes such as halibut, pollock

30

CARL J. SINDERMANN

(Pollachius virens (L.) ) and sea raven (HPwLitriptPrus americmus (Gmelin) ) living in the neighborhood of seal colonies were infested also. Marketing problems with worm-infested fillets were felt to be more serious with Porrocuecum, whose larvae are large and brown-colored, than with other larval Anisakinae, which are small and white. Studies of larval marine nematodes of the sub-family Anisakinae by a number of authors (Kahl, 1938a; Baylis, 1914) lead to some confusion about identification of larval Porrocaecum, since small specimens may lack the diagnostic intestinal caecum which separates this genus from others. Feeding studies with seals (Scott, 1953, 1956) established that most larval worms from cod, plaice, smelt and eelpout of the western North Atlantic were actually P. decipiens. Other nematode genera represented by larvae in food fishes of the North Atlantic include Eustoma and Anasakis. Templeman et al. (1957)have summarized the problems inherent in specific identification of larval Heterocheilidae. Porrocaecum larvae have been reported from 18 species of Pacific fishes, including the Pacific cod, Gadus macrocephalus Tilesius, by Yamaguti (1935). Smelt, cod, redfish and other species from the North Sea were also found to harbor this nematode (Martin, 1921; Kahl, 1936, 1939). Grainger (1959) identified as Porrocaecum larval nematodes from cod and other fishes from Greenland waters and the Barents Sea. Infestation of cod livers by larval Contracaecum aduncum (Rud.), also of the subfamily Anisakinae, has been responsible for considerable economic losses in the Baltic Sea, according to Markowski (1937), Shulman (1948, 1959), Petrushevskii and Shulman (1955) and Getsevichyute (1955). Numbers of worms per liver reached 100, and parasitized fish suffered loss of total weight and liver mass (Fig. 9). Larger, deeply penetrating worms were more harmful, and young fish or spawning fish showed less tolerance to infestation. Liver fat content and oil yield were seriously reduced by parasitization. Contracaecum was also found in cod from the White and Murman Seas, but in lesser frequencies. An interesting example of nematode parasitization that is of serious consequence t o the host has been described by Janiszewska (1939). Flounders of the eastern Atlantic are often heavily parasitized by Cucullanellus minutus (Rud.). Larvae invade the intestinal wall, causing extensive pathological changes. After overwintering, the worms re-enter the lumen of the digestive tract and mature during early summer. A common larval nematode of the subfamily Acanthocheilinae is Eustoma (Anacanthocheilus)rotundatum (Rud.), which occurs as a larva in the mesenteries and viscera of many North Atlantic fishes, including

DISEASES O F MARINE FISHES

31

cod, haddock, redfish, flatfishes and herring (Kahl, 1938b). The larvae may occasionally invade the flesh, particularly after the host fish is killed. Several recent papers from The Netherlands (Kuipers ef nl., 1960; Roskam, 1960; van Thiel et al., 1960) described severe human

al Ltvers FIn. 9. Pathologiral livers resulting from infestation by l ~ r ~ C'o/llrctcrrc,c./r,//. are from Baltic cod of equal size, and the uppermost is normal. (Iteclrann frorn Dogiel, Petrushevskii and Polyanski, 1958.)

digestive disturbances after eating lightly salted " green " herring that contained larval E. rotundaturn. As with other larval Heterocheilidae, the taxonomy of the parasite is still confused; Punt (1941), Berland (1961)and Roskam (1963) considered it a member of the genus Anisakis. It can be seen readily from these brief examples that infestation

32

CARL J. SINDERMANN

of marine fishes by larval nematodes is a matter of serious concern in many parts of the world. Adult nematodes, inhabitants of the digestive tract, occur in many species of marine fish, but appear to do less damage to the host. Among those that might be mentioned, Camellnnus m,elanocephalus (Rud.) occurs in the stomach and pyloric caeca of tuna and mackerel, and Proleptua obtusus Duj. occurs in sharks.

4. Acanth.ocephnla The " spiny headed " worms are represented as adults and as larvae in marine fishes. A common parasite of North Atlantic species is the acanthocephalan Echin.orhynchus gndi Muller. It has been reported (Linton, 1933) from the digestive tract of 54 fish species in the Woods Hole region. The worm occurs in Macrozoarcm avraericnnus in the western North Atlantic (Nigrelli, 1946) and in Zoarces viviparus (L.) from the English coast (Nicoll, 1907) and the Baltic (Markowski, 1939). It is circumpolar in dist,ributJion; having been found in diverse tJeleosts from northwestern Canada, Bering Sea, Kamchatka Peninsula and Japan, as well as from the Baltic Sea, White Sea, Murman coast, North Sea and Gulf of Maine (Dollfus, 1953). Another common acanthocephalan from the North American coast is Telosentis tenuicornis (Linton), found in a wide range of marine fish, including spot, Leiostornus xanthurus Lacepkde (Huizinga and Haley, 1962), Atlantic croaker, Micropogon undulotus, and Atlantic threadfin, Polyda.cty1us octonemus (Oirard) (Chandler, 193Fib) and the sand seatrout, Cynoscion arenccrus Ginsburg, and pigfish, Orthopristis chrysopterus (L.) (Bullock, 1957). Pom,phorh,ynchus lnevis (Miiller) is a commoii parasite of many European marine fishes, including gadoids, flatfishes and eels. It may occur in great numbers in the gut or it may penetrate the gut wall and encyst in the viscera (Wurnibach, 1937 ; Shulman, 1959). Larval acanthocephala are common in the viscera of many marine teleosts but have not been reported in the epizoobic proportions occasionally seen in fresh water-for example, several species, including Corynosomn semervne (Forssell), Corynosoina strumosum (Rud.) and Rolbosomcc vnsculosum (Rud.) occur as adults in fish-eating birds and mammals, and as larvae in mesenteries and viscera of many species of sea fishes.

B. Parnsitic c o p ~ p o d s Marine fishes are parasitized by a variety of copepods, of which several members of the families Lernaeoceridae, Pennellidae and Sphyriidae are particularly injurious to the host. Usually the adult

DISEASES O F MARINE FISHES

33

females become highly modified and penetrate the flesh, often causing extensive ulceration. Lwnaeocwn brnnchinlis (I,.) is a parasite of t,he gill region of gadoid fishes, particularly cod, whiting. pollock and other species froin both sides of the North Atlantic an d from the Pacific (Dollfus, 1953; Shulman a nd Shulman-Albova, 1953 ; Kabata, 1961 : Sherman and Wise, 1961 ; and others). L. brnnchialis has been described as a heart parasite by Schuurmans-Stekhoven ( 1 936) an d Schuurmans-Stekhoven arid P unt (1937) since the anterior end sometimes penetrates the bulbus arteriosus of the host. It has been the object of numerous studies, was reported in th e scientific literature as earlp as 1762 b y Strsm, and is considered one of the most harmful of the copepods parasitic on marine fishes. Intermediate hosts of the parasite include the lumpfish, Cyclopterus lumpus, flounder, Plruronwtes j l ~ s u s .and several other pleuronectids. The adult female copcpods, usually numbering one t o three b u t occasionally more, attach to the gill region of gadoids. The head penetrates sometimes t o the heart, in other cases to the ventral aorta or branchial arteries. causing connective-t',issue hypertrophy and the formation of blood-filled lacunae. Invasion of the heart causes thickening of the walls so t h a t the lumen of the organ is markedly reduced (Mann, 1954). Affected fish are almost always below average weight, an d death of young cod can result from blood loss a nd pathological changes in heart and aorta. Mann (1952) reported tha t infested cod were 20 t o 30% underweight, and had a lower erythrocyte count a nd decreased hemoglobin content of the blood. Extreme emaciation of whiting, Gadus nierlangus L., was reported b y Scott (1929) as t he result of L. brnnchinlis infestation. A second species, L. obtusata, has recently been distinguished by Kabata (1957a) as a parasite of the haddock. Separation was based on minor morphological variations in the adult females, site of penetration and characteristics of the male. Severe impairment of infested haddock, in the form of anemia, loss of weight, loss of liver fat and possible retardation of sexual development, was noted (Kabata, 1958). Walford (1958) cited results of a %year sampling in one English fishing port which disclosed Lernaeocern parasitization of 10% of haddock, 8004 of whiting and 20% of cod, Parasitized fish were as much a s 23:/, below normal weight. A second well-known tissue-invading copepod is 8phyrioiL lunipi (Krsyer), widely distributed in th e North Atlantic on the redfish and several other species (Fig. 10). It has been reported from the Norwegian coast (Luling, 1951). West Greenland and the Norwegian Sea (Hansen, 1923), Newfoundland (Templeman an d Squires, 1960), and the Gulf

34

CARL J. SINDERMANN

of Maine (Herrington et al., 1939 ; Nigrelli and Firth, 1939 ; Sindermann, 1961~).In the western Nort,h Atlantic Sphyrion is primarily a parasite of redfish, but to the eastward-Iceland and northwestern Europelumpfish and wolffish are more likely to be hosts. The parasite penetrates deep in the flesh where extensive host connective-tissue encapsulation occurs around the anchor-like brown anterior extensions of the body. External ulcerations are also common. After death of the

FIG.10. The tissue-invading cnpepod S‘phyrion licinpi in a rotlfish and removed to show anterior anchor.

parasite the “ c y s t s ” persist as unsightly masses in the flesh for a number of years. These cysts must be removed from fillets before marketing. An interesting and still unsolved aspect of Sphyrion infestation of redfish is its marked geographic variation in occurrence ; major centers of abundance are in the Gulf of Maine and off the coast of Labrador, and minor centers are on the southeast part of the Grand Bank and in the southern Gulf of Saint Lawrence. The parasite is absent from other major fishing banks of the western North Atlantic. According to Mann (1954) the extent of attacks on haddock varies

DISEASES OF MARINE FISHES

35

with the fishing ground, and heaviest infestations are off the North American coast, where up to 10% of fish carry the parasite. Another interesting parasitic copepod is Lermeenicus sprattae (Sowerby) which occurs embedded in the eye or occasionally in the dorsal body muscles of sprat and sardines in Europe (Baudouin, 1904, 1905; Wilson, 1917). According to Baudouin, the parasite is called " pavillon " by sardine fishermen, because it has three distinct body parts, showing the three colors of the French tricolor, called " pavillon " by sailors. The long thin body and egg cases of the parasite trail posteriorly as the host swims. Among the largest of the tissue-invading copepods are members of the genus Pennella. P. exocoeti (Holten)from flying fish, Parexocoetus brachypterus (Richardson), and Penriella jilosa (L.) from swordfish and ocean sunfish, Mola rnola (L.), may reach a length of 20 cm. The adult female of this and other members of the genus may be found almost anywhere on the host's body, with the head and neck embedded in the host organs, where large hard cysts are formed (Gnanamuthu, 1957). Parasitic copepods other than the tissue-invading forms may occasionally damage marine fish. Surface abrasions and lesions caused by the parasites can be of serious consequence to the fish host directly or as a route of entry for secondary invaders. Salmonids in the North Pacific and the North Atlantic are often parasitized by Lepeophtheirus salnionis ( K r ~ y e r )an , ectoparasite which causes severe skin erosion, and may even kill the fish host in heavy infestations (White, 1940, 1942 ; Margolis, 1958). Several members of the lernaeopodid genus Glavella, parasitic on the fins and in the branchial and buccal cavities of gadoid fishes, may cause lesions and tumors (Poulsen, 1939; NunesRuivo, 1957; Kabata, 1960, 1 9 6 3 ~ ) . Liiling (1953) has described an instance of tissue damage in tuna, T h u n n u s thynnus (L.), caused by the caligid Elytrophora brachyptera.

IV. GENETICA N D ENVIRONMENTALLY INDUCED ABNORMALITIES I n addition to abnormalities which can be associated with particular disease-causing organisms, marine fishes offer numerous examples of physiological or structural defects, or conditions which may have genetic or other causes. A number of inherited abnormalities of fishes have been studied, including defective spinal columns, pigmented tumors, cataracts, kidney tumors and association of certain pigmentproducing genes with physiological disturbances (Gordon, 1954). On the basis of his review, Gordon felt that abundant evidence existed for genetic control of certain diseases and abnormalities of fishes,

36

CARL J. SINDERMANN

despite the fact that the hereditary factors involved were usually complex. Probably the most thorough studies have been made of the genetics of pigmented tumors (Gordon, 1948, 1950). Neoplastic growths in which pigmented cells play a dominant role are found in many animals, and such neoplasms can be among the most malignant tumors known. Among fishes, neoplasms developing from melanophores are the commonest type of pigment-cell tumor, whereas tumors arising from other chromatophores are rare. For example, Gordon (1948) founcl melanotic tumors in marine or fresh-water representatives of 11 orders of elasmobranchs and teleosts. Takahashi (1929, 1934) in a 13-year survey of many types of tumors in 100 000 fish from the Sea of Japan found three melanomas, one guanophoroma and one allophoroma. Schmey (1911) reported a xanthoma from a single European shark and Smith (1934) an erythrophoroma in an American winter flounder. Epidermoid carcinomas have been reported from several species of marine fishes. Johnstone (1924a) reported an instance in whiting, Williams (1929) a case in pollock. and Beatti (1916) several examples in drum. Odontomas have been reported in a croaker, Micopogon opercularis, from South America (Roffo, 1925), and a haddock from the Grand Bank (Thomas, 1926). Mesenchymal tumors have been found in cod by Johnstone (1920, 1924b, 1926) and Williams (or). cit.). Osteomas of the vertebrae were observed frequently in the red tai, Pagrosomus mrrjor, a Japanese food fish, by Takahashi (1929). Nervesheath tumors (neurilemmomas) are frequent in the snappers (Lutianidae). Luck6 (1942) estimated that up to 1% of the snappers found in Tortugas waters had such tumors, and were called " cancer fish " by fishermen. Thomas (1931), Schlumberger and Luck6 (1948), and Luck6 and Schluniberger (1949) thoroughly reviewed the literature on tumors in fishes and found that more than 120 species were involved. On the basis of their review, the authors concluded that all the major varieties of tumors that occur in mammals and birds occur in coldblooded vertebrates. Goiter (thyroid hyperplasia) has been reported frequently from fresh-water hatcheries (see, for example, Gaylord and Marsh, 1914), but occurs only rarely in marine fishes held in aquaria. Schlumberger (1955) observed goiter in a number of pilotfish, ErheiLeis naucrates L., held in the Philadelphia Aquarium for long periods. Other species held in the same low-iodine water did not develop goiter, suggesting species variability in metabolic need for iodine. Schlumberger observed that the few reported examples of thyroid tumors in marine fishes usually occurred in those kept in aquaria for long periods. Such

DISEASES OF MARINE FISHES

37

tumors were especially characteristic of pilotfish aiid developed within a year after introduction of normal fish. Nigrelli (1952b) reported malignant thyroid tumors in both wild and captive marine fish. Tumors and hyperplastic growths in fishes may have a number of causes other than genetic. Viral etiology for diseases such as lymphocystis has already been considered. Kudo (1924) and Nigrelli aiid Smith ( 1 938, 1940) found Microsporidea and Myxosporidea associated with tissue hyperplasia in certain fishes. Smith (1936) reported papillomas of flounders possibly associated with invasion of larval trematodes, and Reichenbach-Klinke (1955b) cited several instances of fungi associated with tumors. Increasing levels of pollution in the marine environment, in addition t o killing fish and destroying habitats, may produce abnormalities. I n an interesting comparison of marine fishes taken in polluted and unpolluted areas, Young (1964) described changes in consistency of flesh, reduced weight, external lesions, exophthalmia and papillomas as characteristic of fishes from grossly polluted waters off California. External lesions on killifish, similar to those found on trawled species, were produced experimentally by introducing sewer effluent diluted with sea water. The possible association of pollution with increased occurrence of n2oplnsnis in fishes had been made previously. Luck6 aiid Schlumberger (1941) noted the common occurrence of epitheliomas in catfish, Ictalurus nebulosus (LeSueur), from the Delaware River, and Russell and Kotiii (1957) reported on papillomas of white croakers, Genyonemus linentus (Ayres), from the same California area studied by Young. Abnormalities other than tumors have long attracted scientific attention also. An unusual condition described as " jellied " flesh, noted in several flatfish species, seems unrelated to a disease organism. Templeman and Andrews (1956) reported the condition in 40% of the catch of large American plaice, Hippoglossoides platessoides (Fabr.), fished in cold waters of the Grand Bank of Newfoundland. Higher water content and lower protein content made fillets perpared from affected fish unsuitable for market. Most of the fish above 60 cm were jellied. The authors postulated that large fish in cold waters could not adequately meet protein demands of gonad development, tissue maintenance and growth. Evidence was cited for similar conditions in other flatfish species as well as in cod and haddock that suggested a generalized condition of muscle-protein impoverishment under stresses of age, low temperature and gonad development. Abnormalities in morphology are abundantly described in the scientific literature. Gemmill (1912) published a book on teratology

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CARL J. SINDERMANN

of fishes and Dawson (1964) has compiled a bibliography of fish anomalies which contains over a thousand references. Structural abnormalities in several skate species have been described recently by Templeman (1965). Included were such conditions as : separation of pectoral fins from the head, which has been observed repeatedly in the past in other parts of the North Atlantic ; curvature of the vertebral column, a condition found in many teleosts also ; and " blunt snout ", caused by skeletal defects. Letaconnoux (19491, who reported on teratological studies of marine fishes landed in Prance, also noted malformations of the pectoral fins in skates, and described an interesting condition of pigmentation of the normally unpigmented blind side of plaice, often associated with incomplete eye migration. Letaconnoux definite also observed a common abnormality of " short tail "-a abbreviation of the caudal region seen in many species of fishes, due to twisting, compression or fusion of vertebrae. A similar shortening, torsion and diminution of the caudal region has been observed frequently in immature Atlantic herring from the Gulf of Maine, especially in samples taken by bottom trawls rather than conventional surface gear (Sindermann, unpublished). Individuals of other species, such as haddock, have also been found with spinal abnormalities in the western North Atlantic. Although this condition may be due to a bone disease, it seems more likely that these and other structural abnormalities can be attributed to defective embryonic development. " Eugheadedness " (Mopskopfe), a shortening of the snout, was noted by Letaconnoux (op. c i t . ) in several teleosts, particularly the gadoids. This condition has been reported by a number of other authors. Gudger (1930) and Raiiey (1952) described it in striped bass (Fig. 1 l ) , and Maim (1954) reported on the occurrence of " pugheads " among Baltic Sea pike, thought to be genetic, but possibly influenced by environmental factors such as lack of oxygen or salinity variations during embryonic life. No difference in weight was seen in such fish as compared with normal fish, but they are so often rejected by the European shopper that they are usually culled in advance. A pugheaded herring was described by Ford (1930), who also cited earlier evidence for the hereditary origin of the abnormality in fishes. Abnormal conditions in larval fishes, some undoubtedly genetic and some due to environmental variations, are most often seen in hatcheries, but structural defects are sometimes seen in larvae and post-larvae taken in plankton collections. Experimental variation of such single factors as temperature at time of hatching can drastically modify or inhibit formation of the jaws of larvae and can cause an increase in occurrence of other gross abnormalities. Volodin (1960),

(a) LM.B.-4

"

FIG.11. Skeletal abnormalities. Pugheaded " striped baw ; ( b ) " Short-tailed " haddock; (c) fin malformation in thorny skate. 0

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CARL J. SINDERMANN

for example, found that exposures Lo low temperatures (0 to S O C ) during early incubation produced malformed larvae of bream, Abramis ballerus L., and pike (probably Esox lucius L.). Sharp changes in temperature during early development could also produce malformations or death. Physiological abnormalities in larvae are less easily identified, except as they are reflected in lack of growth and death of individuals.

V. EFBECTSOF DISEASE The significance of marine fish diseases may be assessed from the viewpoint of the host population or from that of the human predator. Epizootics may reduce the numbers of fish available to man, and in a t least some marine species disease may be a primary mechanism for regulation of population size. Diseases that weaken or disorient fish, or make them more conspicuous, can be of great importance in determining survival of individuals. Protozoan, helminth and copepod parasites of the flesh, although not often direct causes of death, can act to weaken or slow the host and are also of great economic significance in the landed catch.

A. Epizootics and mass mortalities Mass mortalities of marine, estuarine and anadromous fishes are common, even though many such events may escape scientific attention. Newspapers and interviews with fishermen would probably provide the best criteria for evaluating the extent of mortalities, except for those events that occur beyond the continental shelves. Many factors may, of course, contribute to mass deaths of marine fishes, including physical and chemical changes in the environment (BrongersmaSanders, 1957), as well as the biological realities of starvation, predation and disease. Disease is often suspect, but has infrequently been proved without question to be a cause of mass mortalities. Too often scientific study is not made, or is made too late, or the results of the study are inconclusive. Interest in the event is usually proportional to the numbers of fish dying a t the particular moment ; long-term studies necessary to understand the role of suspected pathogens have rarely been carried on. The often dramatic increase in disease prevalence that we term an epizootic is the result of interactions of such variables as susceptibility of the host population, virulence and infectivity of the pathogen, effectiveness of transmission and physical factors in the environment. Fundamentally, an epizootic of an infectious disease requires that one or more of the following conditions exist: (1) the pathogen must be

41

DISEASES OF MARINE FISHES

newly introduced in a susceptible population ; (2) infection pressure (dosage) or virulence of the pathogen must increase ; or (3) resistance of the population must be lowered. The role of environmentally related influences and stresses such as nutrition, temperature and salinity on disease prevalence must also be considered. Determination of factors prevailing a t the time of an outbreak requires very broadly based and continuous studies in ecology, immunology and pathology. Despite the fact that such ideal studies have not often been made in the past, an appreciable amount of documentation has been assembled for a few marine fish diseases with histories of epizootic prevalences and mortalities. Outstanding in this respect is the fungus disease of herring and other species, referred to earlier, caused by Ichthyophoiius hoferi. Outbreaks of this pathogen in herring of the western North Atlantic have been known since 1898 (Cox, 1916; Fish, 1934; Scattergood, 1948 ; Sindermann, 1956, 1958). The most recent occurred in the Gulf of Saint Lawrence in 1954-55, when an estimated one-half of the herring population of that gulf was killed by the disease. The estimate was based on sampling and field observations during the outbreak, and the behavior of the fishery since then has supported the original estimate. Landings declined to about half their previous level, in the absence of other factors such as change in fishing effort or market demand. Earlier work (Cox, 1916) indicated that comparable reductions in population abundance and in the fishery followed the outbreaks of 1898 and 1914. Reports of outbreaks in the Gulf of Maine also suggested major dislocations in the fishery (Scattergood, 1948). It is interesting and perhaps pertinent that the two most recent outbreaks-the only ones for which we have adequate fishery dataoccurred a t times of herring abundance, as indicated by landing statistics and general observations. One of the most remarkable aspects of the fungus disease of herring in the western North Atlantic has been its apparent periodicity-six recorded outbreaks 14 t o 25 years apart (Fig. 12). The two principal areas involved, Gulf of Maine and Gulf of Saint Lawrence, each with discrete populations of herring, have been out of phase during the most recent outbreaks; an epizootic peak in one gulf coincided with very low disease prevalence in the other. The comparatively brief interval between outbreaks suggests a t best only traiisient increase in resistance of herring populations to the disease. This hypothesis is supported : by relatively low disease prevalence (an average 27%) a t the epizootic peak, which constitutes low selection pressure ; by the fact that the most recent outbreak was a t least as severe as the first recorded outbreak in 1898 ; and by determination of mortality rates 0 2

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OARL J. SINDERMANN

in experimental epizootics of comparable intensity (Sindermann, 1958). Another disease with an even longer history of epizootic prevalences is the " red disease " of eels caused by Vibrio anguillarum. Italian literature dating back to Bonaveri in 1718 (cited by Hofer, 1904) records repeated and severe outbreaks on the coast of Italy throughout

FIG.12. Reported epizootics of Ichthyophonus in herring of the western North Atlantic. The 1940 Gulf of Saint Lawrence outbreak is included on the basis of verbal reports from fiahermen and area residents. (From Sindermann, 1963.)

the eighteenth and nineteenth centuries, and gives some estimates of numbers of eels killed. For example, Spallanzani in 1790 described an outbreak that killed almost 100000 pounds of eels from the Comachio Lagoons on the east coast of Italy near Ravenna in one 38-day observation period. The continuing presence of the disease in Italy was reported by Ghittino (1963b). Literature from northern

DISEASES OF MARINE FISHES

43

Europe, particularly Scandinavia, provides other evidence of widespread epizootics in which great numbers of eels were killed (Bruun and Heiberg, 1932, 1935). An outbreak in eels of the Baltic coast of Germany in 1959, reported by Mattheis (1960), followed a period of several decades of low prevalence. Mattheis also observed that an epizootic in eels preceded by one year an outbreak in pike. The very recent epizootic of bacterial etiology in Chesapeake Bay white perch seriously reduced the population, as indicated by field observations of shoals of dead fish, and numbers washed up on shore, as well as by a sharp decline in production. The fishery in 1964, the first post-epizootic year, was markedly reduced in comparison with previous years. Landings of white perch in 1964 were only 622000 pounds, as compared with an average of 1 5 0 0 000 pounds for the three preceding years ; no indication existed that other major variables had changed. Statements by sportsmen and local residents indicated that white perch were extraordinarily abundant in 1962, the year immediately preceding the outbreak. Mass mortalities appear t o be, and often are, catastrophic events when viewed from close proximity. Their long-term effects may be severe, even resulting in extinctions in part of the host range, or they may be slight, causing only minor depressions in population size. If reduction is severe enough and the ecological niche ” vacated long enough, the species may be replaced by another with similar ecological requirements. The original species may then persist in low abundance for a long period. This is probably the extreme consequence of disease. The more probable course of events, in view of the high reproductive potential of most teleosts, is a gradual return to former population size and only temporary disturbances of many parts of the ecosystem in which the species is enmeshed. An extensive and still emerging documentation of the degree of this dislocation can be found in studies of the fisheries in the Gulf of Saint Lawrence during and after the recent epizootic of fungus disease (Kohler, 1961 ; Sindermann, 1963 ; Tibbo and Graham, 1963). Herring were most seriously involved, and landings during the post-epizootic years were less than half their previous level (Fig. 13). Mean ages in landings decreased, growth rates increased, fewer age group8 were represented in the fishery, and relative abundance of herring larvae decreased sharply. Alewives, which have been described as less susceptible to the pathogen (Sindermann and Scattergood, 1954), acquired infections and were killed in sufficient numbers to be observed. Mackerel were also heavily infected ; mortalities occurred ; and landings decreased during the post-epizootic years. Cod did not become infected but fed on disabled herring to

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CARL J. SINDERMANN

such an extent that their growth rate during the epizootic period exceeded anything previously recorded. Cod landings in the southern Gulf of Saint Lawrence almost doubled during the immediate postepizootic period, due almost entirely to increased weight of individual fish caught, rather than to increased numbers of fish taken. Lobsters, important bottom scavengers, showed a similar but less dramatic increase in growth rate. Here then were both negative and positive short-term effects of an epizootic in herring-the negative brought about by increased infection pressure and mortalities of other species,

I

50

YEAR FIQ.13. Annual landings of Atlantic herring in the southern Gulf of Saint Lawrence, 1920-61. (From Sindermenn, 1963.)

and the positive by a temporarily increased food supply for important predators and scavengers, resulting in accelerated growth of species which in this case had a higher unit value to man.

B. " Background " effects Epizootics provide the dramatic and obvious examples of disease as a factor of resistance to the biotic potential of marine fishes. The more pedestrian, less conspicuous, but probably more significant effects of disease are those that have been variously described as " low level " or " background " effects. Disease may cause continuous subtraction of individuals by weakening and disorienting infected fish, reducing

DISEASES OF MARINE FISHES

45

their ability to escape predators and t o survive variations in the physical environment ; by blinding fish ; by making infected fish more conspicuous; or by altering behavior in ways that render fish more vulnerable t o predation. A disoriented, erratic circular swimming movement a t or near the surface has been observed as a generalized symptom of a number of diseases. It was first described by Plehn and Mulsow (191 1) as a symptom of Ichthyophonus infection in European salmonids, and has since been seen during mass mortalities of Pacific and Atlantic herring. Exophthalmia, with subsequent destruction of the eye, is another generalized symptom of several diseases, including bacterial infection and larval trematode invasion. Cataracts, usually of both eyes, were noted by Raney (1952) in striped bass. Spinal curvatures, evidently of neuro-muscular origin, have also been described as generalized signs of bacterial and fungal infections. In studies of herring diseases it has been noted that individuals with bacterial infections exhibited characteristic and easily visible whitish patches near the tail. Field observations of immature herring schools disclosed that individuals so affected were easily seen even in turbid water and during twilight. Other studies brought out the fact that diseased herring aggregated differentially in deeper water, and that samples of immature members of this pelagic species taken in bottom trawls contained higher frequencies of abnormal fish than did samples taken with conventional surface gear (purse seines and gill nets) in the same areas. Bruun and Heiberg (1932) and others have noted that, eels with " red disease " were lethargic and often motionless on the bottom where they could be caught easily by hand. Locomotion became disoriented and swimming became a series of stiff wriggling movements. Examinations of fish with extensive intramuscular myxosporidean cysts and necrosis, with heavy larval nematode infestation of muscles, or with many copepods imbedded in their flesh, lead inevitably to the conclusion that such a parasite burden, although it may not be the primary cause of death, must seriously reduce statistical chances for survival in an environment in which early and sudden death is the rule. Disease may also reduce the reproductive capacity of marine fish populations. Castration has been reported (Pinto, 1956) in European sardines as a result of invasion of the testes by Eirneria sardinae. Later studies disclosed that over 50% of the individuals sampled were parasitized. Mechanical interference with the discharge of sex products can result from massive visceral infections of smelt by Glugea hertwigi. Cysts of the parasite occupy much of the body cavity, occlude the vent and prevent normal spawning.

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CARL J. SINDERMANN

C. Economic effects Economic effects of disease in marine fishes may be categorized as follows : reduction in numbers of food fish available t o the fishery ; weight loss of individuals ; rejection by consumers and subsequent loss of interest in fishery products as food; and indirect effects, either favorable or unfavorable, on survival of other species in a food chain. Examples of economic effects in each of the categories have been mentioned throughout this paper. Second only to mortality induced directly or indirectly by disease is the often significant weight loss of diseased fish. Williams (1963) has drawn attention to possible losses of thousands of pounds of fishery products annually because of nutrient requirements of fish parasites or disruption of the host’s metabolism by disease organisms. Lernaeocera branchialis, for example, usually causes significant weight loss, so that parasitized fish are 20 to 30% below average weight. This loss can be an important economic factor if 50 to 80% of fish landed are parasitized, as is often true. Rejection of diseased fish by dealers or consumers can also be economically important. Mann (1954) has summarized some of the economic effects of parasites and diseased conditions of fish from the eastern North Atlantic ; he dealt particularly with fish as they appear on the market. He indicated that protozoans, larval nematodes and tissue-invading copepods created the most serious problems. Cited as an example was microsporidean (Qlugea stephani) infection of the intestine, gall bladder, liver and mesenteries of plaice. The parasitized fish gradually became thinner, probably due t o destruction of digestive epithelium. Also considered was another microsporidean, Plistophora ehrenbaumi Reichenow, which caused destruction of somatic muscles of catfish, Anarrhichas lupus, and produced large unsightly tumors. Mann mentioned a large catch of catfish landed a t Hamburg in 1952, from West Iceland waters, of which 10% had t o be discarded as unsuitable for human consumption. Ulcers and cysts caused by Sphyrion invasion of redfish and other species make it necessary to remove the diseased areas during processing. Since up to 25% of the catch may be parasitized, the filleting operation is slowed and many pounds of fillets must be discarded. Because of high frequency and intensity of parasitization of redfish in the Gulf of Maine, the resulting increase in processing costs, and the decrease in processed yield, it may soon be necessary to downgrade the species in that area from a food fish t o an industrial fish, utilized only as a source of fish meal and oil. Hargis (1958) has cited very interesting data from fish processors, indicating that candling and trimming t o detect and remove flesh

DISEASES OF MARINE FISHES

47

parasites can increase costs of packaging up to 80%. Of particular significance were Sphyrion “ buttons ” in redfish, Porrocaecum larvae in cod, and Stephanostomurn metacercariae in flounders. Larval nematodes are most likely t o produce consumer complaints if found in marketed fish. Eustoma (Anacanthocheilus) larvae occur in mesenteries and gonads of European herring. Mann (1964) reported them as infrequent in small herring but common in adult herring of the Norwegian coast. Larval Anisakinae are also common in herring of the North American east and west coasts. Larval nematodes invade the liver of gadoids, disrupt normal function and often cause extensive atrophy. This condition is prevalent in haddock, where larval worms may occur in the flesh as well. Presence of conspicuous larval cod worms (Porrocaecurn)in the flesh can lead to rejection of infested fish. Certain inshore grounds off Canada have not been fished for cod because of a history of consistently high nematode parasitization.

VI. VARIATIONS IN DISEASE PREVALENCE Description of the role of disease in marine fish populations must include consideration of the dynamic relationships of host, parasite and environment. Some of the consequences of these interactions are reflected in variations in the occurrence or prevalence of particular diseases with age of the host, with geographic location within the host’s range, and with time. Thus, a disease may be characteristic only of juveniles or only of adults; it may occur in one gulf and be absent in another ; or it may be abundant today and very rare ten years from now. Examples of such variability are available, although the underlying causes are sometimes obscure. A. Geographic variations Evidence has accumulated t o provide a reasonable picture of geographic variations in the occurrence and abundance of the parasitic copepod Sphyrion in redfish of the western North Atlantic. Major centers of abundance exist in the Gulf of Maine and off the coast of Labrador; minor centers occur on the south-east slope of the Grand Bank and in the south-eastern Gulf of Saint Lawrence. The parasite is absent from other major fishing banks of the western North Atlantic. Templeman and Squires (1960) have reviewed possible reasons for such marked variations, which apparently persist from year t o year. Redfish do not undertake extensive migrations and are closely associated with the bottom; both factors may be important in maintaining enzootic centers of infestation. Studies have been made during the past decade of parasitic diseases

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of sockeye salmon primarily as an aid in identifying the continental origin of high seas stocks. Margolis (1963), who summarized these studies, reported that certain parasites were peculiar to Asian stocks and others to North American. Over 50 species of parasites were encountered in the survey, many of which varied locally or seasonally, and some of which occurred throughout the range of the host species, although in different frequencies. A larval cestode, Triaenophorus crassus Forel, was found in the flesh of salmon from Bristol Bay, but was absent from Kamchatkan samples. Conversely, an adult nematode, Cucullanus truttae (Fabr.), was found in Kamchatka and Okhotsk Sea samples, but was absent from North American samples. Highly localized variations in abundance of disease were seen in myxosporidean (Kudoa clupeidae) infection of Atlantic herring in the Gulf of Maine. A sharp discontiiiuity existed on the Maine coast, documented for ten years (Sindermann, 1965), in which l-year-old fish were commonly found to be infected on the western coast and were never found to be infected on the eastern coast. This difference has been attributed largely to summer sea water temperatures, although other factors may be involved. The discontinuity wa5 so distinct that cysts of the parasite have been used as natural tags to trace subsequent movements of immature fish. The gall-bladder-inhabiting Myxosporidea of whiting have been found to vary in abundance geographically in the North Sea (Kabata, 1963b). Ceratomyxa arcuata Thdohan occurred in 46% of whiting sampled in the northern North Sea: while Myxidium sphaericum Thdlohan infection was only 1.3%. The reverse was found in the southern North Sea, with Myxidium reaching an average of 40% while Ceratomyxa averaged only 9%. This suggested the existence of two North Sea whiting stocks-a conclusion siipported by meristic data. Broader geographic variations in parasite frequencies were disclosed in a study of the distribution of larval cestodes (Trypanorhyncha) in adult herring from the north-west Atlantic. The parasites were absent in four years' sampling from the Gulf of Saint Lawrence, but increased in frequency with decreasing latitude (Fig. 14). A strikingly similar situation prevails in the Pacific. Dogie1 (1955) observed that mintai or Alaska pollock, Theragra chalcogramma, which are heavily parasitized by larval cestodes from sharks, harbored far fewer worms in Kamchatkan waters than in Japanese waters. Variations such as these are undoubtedly related to distribution and abundance of the elasmobranch definitive hosts. Differences of a comparable geographic scale were reported for two coccidians, Eimeria sardinae and E. clupearum, in herring. Polyanski

DISEASES O F MAFUXE FISHES

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(1955) reported E. sardinae but not E. clupearum in Barents Sea herring. Kabata (1963a) found both species in North Sea herring, while Shulman (1959) found E . sardinae in the Gulf of Riga but not in the Gulf of Finland. Changes associated with salinity have been observed in the occurrence of other parasites of White and Baltic Sea herring (Shulman and Shulman-Albova, 1953 ; Dogie1 et d ,1958). Several stages in the transition from strictly marine to fresh-water parasites were noted in the surveys involved.

Fro. 14. Prevalence of larval cestodes (Trypanorhyncha) in Atlantic herring (percentage infestation in black).

Other herring parasites have been examined from widely separated locations in the North Atlantic and adjacent waters (Shulman and Shulman-Albova, op. cit. ; Dollfus, 1956 ; Sindermann, 1961a). Specific locations within the hosts on either side of the Atlantic are sometimes occupied by a nucleus of similar but not always identical parasites, whereas each geographic area also superimposes its own variety of parasites because of salinity differences, presence of intermediate or definitive hosts, temperature differences, diet, depth and other factors.

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CARL J. STNDERMANN

As examples, the myxosporidean Kudoa clupeidae has been reported from herring of the western Atlantic but not the eastern, the larval nematode Eustoma rotundaturn from the eastern but not the western Atlantic, while parasites such as the coccidia mentioned above and the trematode Brachyphallus crenatua (Rud.) occur in varying frequencies on both sides of the Atlantic.

~

FIG.15.

Prevalence of Ichthyophonus in Atlantic herring of the Gulf of Saint Lawrence and the Gulf of Maine, 1965-63.

B. Temporal variations Temporal variations in prevalence of disease are most apparent in studies of epizootics. Unfortunately, long-term studies of prevalences have rarely been carried out, so that the annual increases in incidence building to epizootic levels, or the subsequent annual declines in disease abundance following epizootics, have rarely been documented for marine fish populations. Referring again to Ichthyophonus disease of western North Atlantic herring, the general sequence of events that

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has emerged from studies of several outbreaks includes a long enzootic phase of very low prevalence (< 0-1%), several years of rapidly increasing incidences reaching an epizootic peak when about 25 yoof individuals are infected and acute infections are common, then several years of rapidly declining incidences and return to the enzootic phase. Annual sampling since the most recent outbreak in Gulf of Saint Lawrence herring has provided some data to support these general observations (Fig. 15). The consistency in this sequence of events, as deduced from fragmentary observations during the years immediately preceding and following the epizootics of 1931, 1947 and 1954 suggests that future outbreaks of Ichthyophonus disease may be predicted several years in advance, if sampling of herring populations is continuous. Other diseases of herring have not exhibited the periodicity characteristic of the fungus disease. Continuous sampling for myxosporidean (Kudoa) infections has disclosed only minor variations in prevalence in those areas where the parasite occurs. It is of course possible, and even likely, that longer-term variations in abundance might be expected for this and other parasites. Similar stability in parasite abundance has been found in a 5-year study of larval nematodes (Anisakinae) and larval cestodes (Trypenorhyncha) in herring from the North American east coast. Other examples of dramatic increases in abundance of pathogens and parasites can be found in the literature. Dogie1 and Lutta (1937) studied such an outbreak in sturgeon caused by monogenetic trematodes introduced into the Aral Sea with their normal hosts. Increases of this kind are often seen in marine aquaria, and are considered in a later section.

C . Age effects The effect of host age on the parasite fauna has been examined repeatedly. Recent summarizations of Russian work (Liaiman, 1956 ; Polyanski and Shulman, 1966 ; Polyanski, 1968) indicate that significant variations with age can result from segregation into schools of similar age that often occupy different habitahs at different ages, and from changes in diet of fish with increasing age. Increase in occurrence and intensity with age is often characteristic of worm infestations, but is not necessarily true with microbial agents, many of which may be more common in young fish than in old. Polyanski and Shulman (or). cit.) have described the changes with age in the parasite fauna of cod and Reshetnikova (1955) of mullet in the Black Sea. The authors made the point that " juvenile " parasites, characteristic of very

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C A R L J. SINDERMANN

young individuals, are replaced by parasites typical of adult hosts, due to lack of association of juveniles and adults, change in habitat from inshore to offshore, and change in feeding habits and diet. Studies of Atlantic herring (Sindermann, 1963) have further demonstrated age-associated changes in parasite fauna. The body wall overlying the visceral cavity of post-larvae is sometimes infected with a species of Plistophora which has not been found in juveniles over 6 months old. Juvenile herring between 6 months and 1 year old harbor an adult cestode not seen in older fish. Juveniles between 9 months and 3 years are infected with the myxosporidean Kudoa clupeidae, which is absent in adults. Larval trematodes, Cryptocotyle lingua, are characteristic of juvenile herring because the young fish live during the warmer months in close proximity to intertidal snail populations (Sindermann and Farrin, 1962). Adult herring, which are only lightly infested, remain farther offshore except during spawning. Other parasites-larval cestodes (Trypanorhyncha) and larval nematodes (Anisakinae)-make their first appearance in juveniles about 1 year old and, depending on geographic area, gradually increase in abundance with increasing age. Disease may begin to exert effects very early in the life history of the fish. Eggs of marine fishes are often coated with microorganisms ; Oppenheimer (1955) found that hatching percentages of cod, turbot and sardine eggs were increased in bacteria-free media. Ahlstrom (1948) found abnormalities, some of which may have been disease-induced, in as many as 45% of developing Pacific sardine eggs.

VII. IMMUNITY Resistance to fish diseases involves a complex of interacting factors, including individual variability, species characteristics, seasonal influences and nutritional effects. Immunity has both cellular and humoral aspects and extends from obvious phagocytic, lytic and agglutinating activity to include such factors as the role of skin and mucus barriers and the role of gastric secretions. Some of the mechanisms of natural and acquired resistance to disease in fish have been summarized by Bissett (1947a, 1947b), Dreyer and King (1948) and Snieszko (1958); McDermott (1956) and Hirsch (1959) have reviewed the cellular and humoral mechanisms of immunity. A number of papers have appeared recently which clearly substantiate earlier findings (Blake and Anderson, 1930; Toth, 1932 ; Nybelin, 1935a ; Schaperclaus, 1938; Snieszko et al., 1938 ; Smith, 1940) of specific immunological competence in fish. Clem and Sigel (1963), Sigel et al. (1963), and Sigel and Clem (1965) studied immune responses

DISEASES OF MARINE FISHES

53

in marine teleosts and elasmobranchs to injected viral and bacterial antigens. Lemon shark, Negaprion brevirostris (Poey), produced significant titers of hemagglutination-inhibition antibodies with a high degree of specificity in response t o injected influenza virus. Lower titers and less specificity were found in similar studies of the margate, Haemulon album Cuvier. A very low degree of immunologic reactivity was evident in the sea lamprey, Petromyzon murinus L. Goiicharov (1962) hyperimmunized several cyprinid species a t 15 to 25°C with killed Pseudomonas fluorescens and other bacteria, and produced agglutinin titers as high as 10 240. The agglutinins were specific, and the reaction was temperature-dependent, since antibodies were not formed at 6 t o 7 O C . Krantz et al. (1963, 1964), in research oriented toward control of hatchery diseases through immunization, reported significant antibody response in trout to killed bacteria injected with adjuvant. Maximum agglutinin titers were reached 3 to 4 months after injection. Fish immunized with a vaccine of formalin-killed Aeromonus salmonicida, the etiological agent of furunculosis, were protected during challenge with viable pathogens, but untreated controls were not. The authors pointed out, however, that augmented natural defense mechanisms often cannot prevent infection when the fish is confronted by severe physiological or environmental stresses. Post (1963) had used a similar immunization method to achieve moderate protection of rainbow trout, Salmo gairdneri, against Aeromonas hydrophila. Spence et al. (1965) were able to produce appreciable antibody titers in rainbow trout immunized against Aeromonas salmonicida; the antiserum so produced provided passive protection of juvenile salmon when injected intraperitoneally. Several authors, including Post (1962) have suggested oral immunization as a practical mass prophylactic method, but evidence is conflicting. Duff (1942) reported resistance of trout to furunculosis after feeding an oral vaccine of killed Aeromonas salmonicida, and Ross and Klontz (1965) found increased survival of rainbow trout after oral immunization against redmouth disease.’’ Snieszko and Friddle (1949), however, were unable to demonstrate protection of young brook trout against furunculosis by oral immunization and Spence et al. (1965) found that oral vaccine did not protect salmon exposed t o Aeromonas salmonicida. Poikilothermic vertebrates such as fish are excellent subjects for basic studies of immune responses. Allen and McDaniel (1937), Pliszka (1939), Cushing (1942) and Bisset (l946,1948a, 1948b) have summarized effects of temperature on antibody production, and have demonstrated that production was minimal below 10°C. Sindermann and Honey (1964) found that certain natural heteroagglutinins of winter skates, ((

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CARL J. SINDERMANN

Raja ocellata Mitchill, varied seasonally, with minimum titers a t times of minimum environmental temperatures. Hildemann (1957) noted acceleration of rates of homograft rejection in fish coincident with increasing environmental temperature. The immune response was measured by survival time and inflammatory reactions. Duration and intensity of inflammation were closely associated with rapidity of donor-tissue destruction. Fine and Drilhon (1961) demonstrated the formation of precipitins in eels in response to injections of human serum. Wolf (1941, 1954), Snieszko (1957b) and Ehlinger (1964) found differences among strains of brook trout, Salvelinus fontinalis, in resistance to ulcer disease and furunculosis. Papermaster et al. (1964), in studies of the evolution of immune responses, found a rising level of reactivity and complexity as the phylogenetic scale from hagfish to teleost was ascended. Goncharov (1959a) reported high antibody titers in fish immunized against Achromobacter punctatum (Pseudomonas punctata), and also pointed out the prevalence of cross agglutinations in work with such immune sera. Earlier, Mann (1939) had shown that carp affected by ascites (Bauchwassersucht) developed high agglutination titers against Pseudomonas punctata, but Roegner-Aust et al. (1950) and Goncharov (1959b) presented arguments that a virus was the primary etiological agent. Sorvachev et al. (1962) described prophylactic immunization of carp with an attenuated virus vaccine. According to their report, the 1- and 2-year-old progeny of hyperimmunized carp suffered little mortality during a severe outbreak of ascites, whereas young of unvaccinated fish died in great numbers. Such findings are unique, and are more suggestive of maintenance of immunity by natural infections. Despite some continuing disagreement about the causative organism, summarized by Schaperclaus (1965) and others in a recent symposium (Snieszko et al., 1965), a body of literature on the epizootiology of this very important disease of carp has accumulated. Included are indications of acquired immunity after infection, a possible role of bacteriophage, changes in virulence and adaptation t o new hosts-all problems that may be pertinent to certain marine fish diseases. Fungus or myxosporidean invasion of fish often produces only tissue destruction with little indication of host inflammatory response. Intramuscular parasites may cause hyalinization and lysis of muscle tissue until only granular debris and spores remain. I n some individuals, however, fungus invasion elicits extensive formation of fibrous connective tissue by the host (Fig. 16). Evidence of local immunity t o monogenetic trematode infestation

Fro. 16. A.\LIi.-4

Host response in acute (above) and chronic (below) fchthyophonus infection of the body muscles of Atlantic herring. u

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has been described by several authors. Jahn and Kuhn (1932) reported heavy infestation of eyes of Serranidae and Lutianidae by the monogenetic trematode Benedenia melleni (MacCallum). Aquarium fish carried up to 2 000 worms, attached to eyes, gills and nasal cavities, and were frequently killed. Survivors usually harbored progressively fewer parasites ; this decrease was attributed t o development of local immunity and to immune mechanisms of the host mucus (Nigrelli and Breder, 1934 ; Nigrelli, 1935a, 1935b, 1935c, 1937, 1947). Immunity to other helminth parasites of fishes has not been demonstrated. VIII. DISEASESIN MARINEAQUARIA Disease control has become of increasing significance with the establishment of many new marine aquaria, oceanaria and hatcheries, where marine fishes are caught, often a t great expense, and held in captivity or actually reared under hatchery conditions. Whatever their original purpose, such artificial conditions should prove to be fruitful sources of information about diseases and epizootics in marine fishes and should also provide the needed stimulus to develop understanding of the pathogens concerned. A new technology of treatment of marine fish diseases, including many modifications of techniques used in fresh-water hatcheries and aquaria, is slowly developing (Nigrelli, 1943; Laird, 1956; Chlupaty, 1962; DeGraff, 1962; Hprjgaard, 1962; Oppenheimer, 1962; Paccaud, 1962) and should expand greatly in the next decade. As has been true in fresh water, many of the real advances in understanding the role of fish diseases in the sea can be expected from studies of individuals in captivity. This has been and will be true especially of the infectious diseases, which may in epizootic form sweep through aquarium populations, or in enzootic form result in continued attrition of valuable specimens. Several references t o diseases in aquarium environments have already been made in this paper. Infectious diseases are easily imported with fish from natural habitats, and flourish in an artificial environment because of increased effectiveness of transmission from fish to fish in a restricted body of water, because of somewhat higher environmental temperatures, or because of inadequate diet and consequent reduction in resistance. Fish in captivity are subject to much closer scrutiny than is ever possible in the sea, so abnormalities are more likely to be observed. Also, the absence of predators in most aquarium situations permits abnormal individuals (for example fish with advanced tumors) to live far beyond what would be their survival time in nature. As pointed

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out by Oppenlieimer and Kesteven (1953), external symptoms of bacterial infections are often visible only when the fish is under water. These infections can best be seen in captive fish-in fact most of the bacterial diseases of marine fishes, such as dermatitis and tuberculosis, have been observed in captive populations (Aronson, 1926 ; ZoBell, 1946 ; Nigrelli and Vogel, 1963). Bacterial pathogens, because of high infectivity and short generation time, are observed most commonly and produce severe effects in marine aquaria. Oppenheimer and Kesteven (1953) reported that of all external lesions in salt water aquaria, bacterial tail rot or fin rot was most common. This has been the author’s conclusion also, based on ten years’ observations of herring held in captivity for varying periods up to two years. The disease syndrome included progressive erosion of fins and tail, minute hemorrhages beneath scales, disorientation and roughening and raising of the integument. Pseudomonas ichthyodermis, the pathogen involved in Oppenheimer and Kesteven’s study, reached epizootic proportions during summer, and many species of fishes were infected. Other examples of skin ulcerations and fin rot of bacterial origin in captive fishes were reported by Anderson (1911), Riddell and Alexander (191 l),Wells and ZoBell (1934), Sindermann and Rosenfield (1954a) and Conroy (1963). Oppenheimer (1958) described a progressive tail rot disease of cod, Gadus morhua L., held in live boxes, accompanied by bacteremia and death usually within 48 hours from onset of symptoms. Reinfections were obtained from cultured bacterial isolates, and the causative organism was characterized as a species of Pseudomonas. The disease developed in water temperature of 5 to 9”C, and Oppenheimer’s description of symptoms is remarkably similar to that for herring. An interesting paper by Ford (1928) discusses tail abnormalities in young herring that are highly reminiscent of the effects of bacterial disease, but which are attributed by the author to “ nibbling ” by other members of the school. Lymphocystis disease is not uncommon in marine aquaria. Nigrelli and Smith (1939) noted that the disease was most abundant in summer and disappeared in winter. Successive individuals exhibited symptoms but most infected fish recovered. “ Velvet disease ” of marine fishes caused by the dinoflagellate Amyloodinium ocellatum (Brown) has assumed epizootic proportions in aquaria (Brown, 1934 ; Brown and Hovasse, 1946). Heavy mortality occurred for three years in the aquarium of the Zoological Society of London. Both cold-water and subtropical fishes were affected and mortalities began soon after arrival of specimens from Bermuda. Primary cause of deaths was the parasitic dinoflagellate Arnyloodinium 1) 2

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ocellatum on the gills and occasionally the external surfaces of 28 species. The parasite appears to be nonspecific in host selection. Laird (1956) reported it as a cause of major mortalities in a Singapore aquarium. Primarily a gill parasite, it caused hemorrhages and adhesions of gill filaments and interfered with host respiration. I n heavy infections it spread over skin and fins, giving the appearance of powdery or velvety patches. Nigrelli (1936) also reported this parasitic dinoflagellate as common on skin and gills of many species in marine aquaria. A ciliate parasite, Cryptocaryon irritans Brown, is the marine counterpart of the ubiquitous fresh-water Ichthyophthirius multiJiliis Fouquet. The parasite, only briefly described by Brown (1951), causes “ white spot disease ” because of whitish pustules formed on gills and epidermis (Fig. 17). Epizootics caused by Cryptocaryon have been described in marine aquarium fishes in Japan, London and Singapore

FIG.17.

“White spot

”

disease of seatrout.

(After Sikama, 1938.)

(Brown, 1951; Laird, 1956). Heavy infections were rarely seen in natural populations. I n Fiji, only one species, the rock cod, Epinephelus merra Bloch, was infected of 36 species examined from the same coral reef, and all infections were very light (Laird, op. cit.), but in aquarium epizootics few species were immune to infection. I n Japan 44 of 53 aquarium species were attacked (Sikama, 1938). Parasite numbers increase rapidly when the mature trophozoite drops off the host and encysts on the aquarium bottom. Multiple divisions that follow produce large numbers of motile infective stages. The emergence, in the aquarium environment, of other pathogens virtually unknown in fish from natural habitats is well illustrated in a series of studies carried out in the aquarium of the Oceanographic Institute of Monaco. Two algae, Leucosphaera Oxneri and Thallumoebella parasitica, were described by Raabe (1937, 1940a, 1940b) as responsible for epizootics and mortalities in a number of marine fish species. Other parasites, including Microsporidea and larval nematodes, were also indicted in aquarium mortalities (Raabe, 1936; Guiart,

DISEASES O F MARINE FISHES

I

59

1938). Earlier, Russell (1983) reported lesions and emaciation due t o heavy infestations of the copepod Caligus pageti on grey mullet, Mugil capito, kept in experimental ponds in Egypt. The parasite had not been seen previously in wild populations.

IX. RELATIONSHIP OF FISH DISEASESTO HUMANDISEASES An inescapable aspect of any discussion of fish diseases is their possible relationship t o human disease. Examples from the freshwater environment, such as the tapeworm Diphyllohothrium latum (L.), the nematode Onathostoma spinigeruwi Owen, atid the trematode Clonorchis sinensis (Cobbold), clearly demonstrate the role of fish in transmitting human parasites (Cameron, 1945). Fortunately, few examples can be found for a similar role for marine fishes. Recent reports from The Netherlands (van Thiel ef ul., 1960: Kuipers, 1964) describe severe reactions t o invasion of the wall of the human digestive tract by larval nematodes of the family Heterocheilidae. ingested alive with lightly salted herring. The disease, described as eosinophilic phlegmonous enteritis, is relatively rare, even in a population t h a t consumes countless numbers of herring. Williams ( 1965) has recently summarized the available information on " herring worm disease ". His opinion is t h a t larval nematodes other than Eustonia rotundaturn may be agents of the disease, and t h a t care must be taken in attempts t o identify larval nematodes from the human intestine. Eosinophilia has long been associated with many helminth infestations, and ingestion of raw fish has recently become a suspected route of transmission in outbreaks of human eosinophilic meningitis in the Pacific area (Rosen et aZ., 1961, 1962). A possible etiologic agent is the larva of the nematode Angiostrongylus cantonensis (Chen), which matures in the lungs of the rat after first invading the brain (Alicata, 1965). Infestation of the mammalian definitive host-normal or abnormal-can result from ingestion of a molluscan intermediate host or a paratenic host harboring third-stage larvae. Cheng a n d Burton (1965) have demonstrated t h a t oysters and clams can serve as experimental intermediate hosts and t h a t first-stage larvae concentrated from the feces of infected rats could survive for 27 hours in salinitiesof 2Oy& Although some epidemiological assoc4ation of consumption of raw fish with meningitis outbreaks in areas of the South Pacific has been made, the role of Angiostrongylus is less clear. as has been pointed out by Jacobs (1963). Larval trematodes, Hderophyes heterophyes (Siebold), infective t o man, occur on the integument or in the flesh of mullets, Mugil c~phalus and Mugil juponicus, found in brackish water (Belding, 1942). It is

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likely that other heterophyid metacercariae from estuarine and inshore fish may occasionally infest man. Larval tapeworms, Diplogonoporus grandis (Blanchard), infective to man, occur in marine fishes of Japan. Larval Diphyllobothriunt lntum infest pike and turbot in brackish waters of the Baltic Sea (Engelbrecht, 1958), and are dangerous parasites of man. Among the human illnesses associated with infectious agents of marine fish origin are severe inflammations of superficial wounds among fish handlers due to the bacterium Erysipelothrix insidiosa (Trevisan) as described by Sheard and Dicks (1949), Wellman (1950, 1957) and Langford and Hansen (1954). Processing plant employees may be temporarily incapacitated by these infections, which are particularly common after injury by spines of such fish as sea robins or redfish. The causative organism has been isolated repeatedly from fish slime (Sneath et al., 1951 ; Price and Bennett, 1951). Oppenheimer and Kesteven (1953) and Wellmann (1957) found that known strains of the bacterium grew well in sea water medium. Recent studies in Japan (Aiso and Matsuno, 1961 ; Sakazaki et al., 1963) have implicated the ingestion of raw marine fishes from inshore waters in summer outbreaks of human digestive disturbances. The causative agent has been identified as Vibrio parahemolyticus (Fujino). Although not recognized as pathogenic to fish, the organism has been isolated from the body surfaces and digestive tracts of live fish immediately after capture. It does not seem unlikely that increasing conditions of estuarine and inshore pollution could lead to an increasing role of inshore fishes in transfer of human pathogens. As long as raw marine products from inshore waters are eaten by humans, the possibility of disease transmission, either mechanically or as a result of multiplication of a pathogen within the marine host, must be recognized. Glantz and Krantz (1965) have used serotyping of Escherichia coli to show a relationship between bacterial isolates from fish and pollution of water. Bacteria of human origin were retained in the digestive tract of fish for short periods, but experimental studies disclosed no illness in fish fed on E. coli serotypes pathogenic to man.

X. FUTURE STUDIES OF MARINE FISHDISEASES Because of the complexity and enormity of the marine ecosystem, disease problems in fish are difficult to approach. As with other marine problems, it is likely that greatest advances will be made when descriptive studies can be combined with experimentation in circumscribed bodies of water such as aquaria, salt ponds, and artificially restricted estuaries and other arms of the sea. The recent demonstration of

DISEASES OF MARINE FISHES

61

specific immunological competence in fish further indicates that controlling factors in epizootics are not fundamentally different from those for other vertebrate groups. Individual variability in susceptibility to pathogens has been demonstrated, and the course of certain fish diseases shown to be alterable by environmental factors such as temperature and diet. Little basis exists for pessimism as to the possibility of disease control in the sea, despite the seeming immensity of the problem. True, we now stand in marine disease studies almost where our ancestors of the Middle Ages did when confronted with the great pestilences of those days. Yet the advances made since then in understanding and control of human diseases suggest that technology and techniques impossible to foresee now can lead to manipulation of the marine environmeiit and the factors that influence population size of marine fish. Some approaches have already been suggested. Certain diseases of inshore species (such as Ichthyophonus disease of herring) might be artificially supported at a level just high enough to maintain population resistance at a point where epizootics would not occur. It might be possible to overfish a population deliberately as soon as evidence of an incipient epizootic is discovered. These methods are, of course, based on present knowledge and do not constitute a legitimate portrayal of future control based on the acquisition of new information. The severe effects of epizootics on marine fish populations have been partially documented for Ichthyophonus disease of herring, red disease of eels and Pasteurella disease of white perch. Significant reduction in population size was indicated in each outbreak by reduced catches during the post-epizootic periods. It is tempting to speculate on the basis of these observations that certain of the unexplained major past fluctuations in abundance of commercial marine species may have been caused by disease. As an example, drastic decline in mackerel abundance on the Atlantic coast of North America in the late nineteenth century may have been related t o disease. During the 1954-55 fungus-disease epizootic in herring of the Gulf of Saint Lawrence, mackerel were found to be susceptible and heavily infected. Mackerel landings in the southern Gulf declined at that time to half their previous total, and have remained low to the present time. Available catch records for mackerel of the western North Atlantic, beginning in 1804, show periodic fluctuations which have been correlated with deviations in air temperatures by Taylor, Bigelow and Graham (1957), but which may well have had more immediate causes, such as periodic epizootics. It seems logical that wherever unexplained catastrophic declines in a fishery have occurred, disease must be

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strongly suspected. It is easy, however, to over-extend any point of view, so there is no implication here that every decrease in abundance can be blamed on disease. Although supporting data are sometimes inadequate and fragmentary, the author believes that the following hypotheses about the role of disease in marine fish populations can be stated : ( 1 ) Disease may exert profound effects on population size, and may a t times be one of the most important factors of environmental limitation to the biotic potential of certain marine fish species. (2) Epizootic disease in one species may have pronounced negative or positive effects on other species-predators, scavengers or competitors. (3) Disease levels may be influenced by a number of factors, including change in susceptibility of the host population, or increase in infection pressure on the host population. (4) Certain diseases and parasites common in one geographic area may be rare or absent in other areas. Microhabitats within hosts with cosmopolitan distribution may be occupied by different representatives of a genus or family of parasites in different parts of the world. (5) Some of the great past fluctuations in sea fisheries may have been caused by disease. (6) Epizootics in marine fishes may occur a t times of high population density. ( 7 ) Disease may affect fish of any age. There are some indications that earliest life history stages-eggs, larvae and juveniles-may at times be seriously affected. (8) Close scrutiny of a marine fish species usually discloses one or more diseases which might be considered " characteristic " of that species in a given geographic area, although other diseases may occur. (9) At least some disease problems in marine fish populations seem amenable to solution. Although it is difficult to predict the future course of research and the development of knowledge about marine fish diseases, it is comparatively easy to itemize areas that require exploration. One of the greatest needs is for continuity of observations, so that changes in prevalence of recognized diseases, particularly those known to occur in epizootic proportions, can be documented over extended periods. These observations should be accompanied by detailed studies of such factors as food and temperature in the environment of host populations and of mechanisms of resistance to known pathogens. Acquisition of continuous information about the size of the host populations would also be an important facet of the studies.

DISEASES OF MARINE FISHES

63

Another critical question concerns the effects of disease on the very early life history stages of fishes. It is generally accepted that much of the mortality of a given year class occurs in the embryonic and larval stages. Variables such as oxygen. temperature, salinity and food supply are undoubtedly important, as is the very obvious and extensive predation on eggs and larvae. Effects of disease, which niay also be significant, are less clearly understood, but are amenable to descriptive and experimental studies. Another research area deserving greater attention concerns the role of viruses and bacteria in marine fish populations. Enough evidence is already available to prove that bacteria can be significant primary or secondary invaders, and causes of mortality in natural as well as captive populations. Identification of bacterial pat hogens is not simple ; the classification is at present confused ; reinfection from cultured organisms is often unsuccessful ; and disease-free experimental fish that have not been exposed in the past to the same or related organisms may be very difficult to obtain. Other basic and related problems immediately present themselves-such as the role of marine bacteriophages in populations of bacteria potentially pathogenic to fish (Spencer, 1963), and the role of antibiotics elaborated by many marine organisms in suppressing bacterial populations (Lucas. 19.55 ; Nielsen, 1955). Knowledge of viruses as pathogens of marine fishes is even more rudimentary than is that for bacteria, except for tumorinducing agents. Currently available established cell cultures of marine fish origin should do much to improve our understaiding of viruses in the oceans.

XI. SUMMARY Diseases of marine fishes are less well known than those of freshwater species because : ( a ) Mortalities and epizootics in the sea are so much less apparent and less frequently observed than are those in the more restricted fresh-water habitat, that the true role of disease in the sea has not been fully appreciated. ( b ) Fresh-water hatcheries and aquaria are much more numerous than comparable salt-water facilities. Problems associated with crowding, artificial feeding and disease control for salt-water species have not had to be confronted with the same intensity of research as for fresh-water species. Much of the impetus for research and the advances in understanding of disease in fresh-water fishes have originated in the hatchery or aquarium environment ; this impetus has been largely lacking for marine species.

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( c ) The marine environment is less amenable to manipulation than is the fresh-water environment, and problems of disease control in the sea have seemed insurmountable to some people. The widely-scattered world literature on marine fish diseases encompasses a body of knowledge that is growing rapidly with increasing scrutiny of the oceans and their inhabitants as actual and potential food sources for an expanding human population. The species of fishes studied are primarily members of commercially important groups such as gadoids and clupeoids, and attention has been paid t o those conditions which affect survival or marketability. Diseases of marine fishes are important economically because they : ( 1 ) reduce the number of fish available to man; or (2) reduce the quality of fish as food. Important to (1) are epizootics and resultant mass mortalities caused by infectious agents. Less conspicuous but also important are " background " effects of disease that result in continuous direct or indirect subtraction of individuals from a population. Important t o (2) are parasites that inhabit and sometimes degrade the muscles of marine fishes. Conspicuous in this group are the Microsporidea, Myxosporidea, larval worms and tissue-invading copepods. Infectious diseases produce dramatic effects, such as epizootica and mass mortalities. Bacteria, fungi and protozoans have all been implicated in marine diseases of serious consequence. Severe shortterm effects of outbreaks on population size and on commercial landings have been observed in Atlantic herring, white perch and other species. Repeated outbreaks of certain infectious diseases, such as red disease of eels and Ichthyophonus disease of herring, have been recorded. Among the invasive diseases, larval cestodes, trematodes and nematodes can be found, often in large numbers, in the flesh and viscera of marine fishes, where they may interfere with metabolic activities and with growth, or they may otherwise reduce the value of the parasitized fish to man. Tissue-invading copepods may act in similar ways. Enzootic centers exist for certain parasites, for example larval nematodes and some copepods ; occasionally parasites such as monogenetic trematodes increase in abundance locally to produce epizootics. Abnormalities, including tumors and skeletal deformities, are known for many marine species. Most of the morphological variations, other than tumors, can probably be attributed to defects in embryonic development-in fact a wide range of abnormalities has been seen in larval fishes, especially those reared in environments in which oxygen, salinity, light or other factors deviated from normal. Studies of captive marine fishes have provided much information

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65

about diseases. Many pathogens multiply rapidly in the aquarium environment to produce epizootics ; other organisms, which may be insignificant in the natural habitat, may assume pathogenic roles. Vibrio infections are common in marine aquaria, and may quickly destroy captive populations. The dinoflagellate Amyloodinium and the ciliate Cryptocaryon have been causes of epizootics in marine aquaria, but, as far as it is known, are not significant pathogens in natural populations. Gratifying recent increases in research on fish diseases indicate that we may soon be able to assess with some reliability the role of disease in marine species.

XII. REFERENCES Ahlstrom, E. H. (1948). A record of pilchard eggs and larvae collected during surveys made in 1939 to 1941. Spec. scient. Rep.-Fish. U.S. Fish Wildl.S e w . no. 54, 76 pp. Aiso, K., and Matsuno, M. (1961). The outbreaks of enteritis-type food poisoning due to fish in Japan and its causative bacteria. J a p . J . Microbial. 5,337-46. Akhmerov, A. K . (1951). Some data on the parasites of Alaska pollock. (In Russian) Izv. tikhookean. nauchno-issled. Inst. rgb. Khoz. Okeanogr. 30, 99-104. Akhmerov, A. K . (1955). The parasite fauna of Kamchatka River fishes. (In Russian) Izv. tikhookean. nauchno-issled. Inst. rgb. Khoz. Okeanogr. 43, 99-137. Aleem, A. A., Ruivo, M., and ThBodoridBs, J. (1953). Un cas de rnaladie 8, Saprolegniale chez une Atherina des environs de Salscs. Vie Milieu, 3, 44-51. Alexander, D. M. (1913). A review of piscine tubercle with a description of an acid-fast bacillus found in the cod. Proc. Lpool biol. SOC.27, 219-26. Alexandrowicz, J. S. (1951). Lymphocystis tumours in the red mullet (MuZZua surmuletus L.). J . mar. biol. Ass. U . K . 30, 315-32. Alicata, J. E. (1965). Biology and distribution of the rat lungworm, Angiostrongylus cantonensis, and its relationship to eosinophilic meningoencephalitis and other neurological disorders of man and animals. A d v . Parasitol. 3, 223-48. Allen, F. W., and McDaniel, E. C. (1937). A study of the relation of temperature to antibody formation in cold-blooded animals. J . Imniunol. 32, 143-52. Altara, I. (ed.) (1963). Symposium EuropBen sur les maladies des poissons et l’inspection des produit,s de la p&he fluviale et maritime. Bull. mens. Off. int. Epizoot. 59, 1-152. Amlacher, E. (1961). ‘‘ Taschenbach der Fischkrankheiten”, 286 pp. Gustav Fisher Verlag, Jena. Anderson, A. G. (1911). Bacteriological investigation as to the cause of an outbreak of disease amongst the fish at the Marine Laboratory, Bay of Nigg, Aberdeen. Rep. Fish. B d . Scot. 1911, 38-45. Annenkova-Khlopina, N. P. (1920). Contribution to the study of parasitic diseases of Oswierus eperlanus. (In Russian). I z v . Otd. Rgbov. naucho-promflal. Issled. 1, 2.

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Anonynioris (1951). Diseased stripers in Connecticut are safe t.o eat. Salt Jt'ater Sports)nun, June 22, 1951, 1. Anonymous (1960). A list of common a,nd scientific na.Ines of' fishes from t.he United St,ates and Canada. Amer. Fish.Soc. Spec. Pub. no. 2, 102 pp. Apstein, C. (1910). Cyclopterus lwripus, der Seehase. Srine Fischerei und sein Wageninhalt,. Alitt. tltsrh. SeeJischJ'er. 26, 450-65. Arai, Y., and Mat)sumoto, K . (1953). On a new Sporozoa, Hexacapsula neothunne' gen. et, sp. nov., from the muscle of yellowfin tuna, Neothunn~isnmcropterus. Bull. J n p . Soc. scierit. Fish. 18, 293-8. Aronson, J . D. (1926). Spontaneous t,uherculosis in salt, wat,rr fish. J . inj'ect. Dis. 39, 315- 20. Aronson, J . D. (1938). Tuberculosis of cold blooded animals. I n " Tuberculosis and Leprosy, the Mycobncterial Distwses", Moulton, F. R. (etl.), A A A S Sympos. Series, 1, 80-6. Auerbach, M. (1906). Ein Myzoholus ini Kopfe von Grcrlus rcegleflntts I,. 2001. Am. 30, 568-70. Auerbach, M. (1912). Studien iiber die Mysosporidien dcr Norwegischen Seefische J b . Syst., 34, 1-35. nnd ihre Vcrbreit,ring. 2001. Baer, J. Q. (1948). Contribut.ions 8, l'Pt,ilde des cestodes do selacians. Part 1. Bull. Soc. ?~euchatel.Sci. nat. 71, 1-122. Bagge, J., and Bagge, 0. (1956). T'ibrio anguillaruni som Eirsag t.il iilcus-sygdom hos torsk (Cuduscallarias L.). Nord. l.'etAJed. 8, 481-92. Baudonin, M. (1904). Le Lernaeeniciis sprattae, parasite de la sardinr en Vendbe. C . R . Acnrl. Sci., Paris, 139, 998-1000. Baudouin, M. (1905). Les parasites de la sardine. Rev. xi.,Paris, no. 24, 715-22. Baylis, H . A . (1944). '' CapsuZaria marina " and the Ascaridae of marine fish. Parasitology, 36, 119-21. Beat,ti, M. (1916). Geschwiilste bei Tieren, 2. Krebsforsch. 15, 452-91. Belding, D. L. (1942). '' Textbook of Clinical Parasitology", 888 pp. AppletonCentury-Croft.s,New York. Bergman, A. M. (1909). Die rote Beulenkrankheit des A d s . Ber. bayer. biol. I-ersSta. 2, 10-54. Bergman, A. M. ( 1912). Eine ansteckende Augenkrankheit, Keratomalacie, bei Dorschen an der Sudkust,e Schwedcns. Zbl. Bakt., I. Abt,. Originale, 62, 200-12. Bergman, A. M. (1923). Fiskarnas Sjukdomar. I n Sotvattensfiske och Fiskodling. 73 pp. Svenska Jordbrukets Bok. St.ockholm. Berland, B. (1961). Nematodos from some Norwegian marine fishes. Sarsia, 2, 1-50. Bespalyi, I. I. (1959). Coccidiosis of carp in the pond fisheries of the Ukrainian SSR. (In Russian). Trctdg sovesch. po bolezn. rgb, Ikhtiol. Kom. Akad. Nauk SSSR, 1959, 48-51. Bisset, K. A. (1946). The effect, of t.emperature on non-specific infections of fish. J . Path. B a d 58, 251-8. Bisset, K.A. (l947a). Bacterial infection and immunit,y in lower vertebrates and invertebrates. J . Hyg., Camb. 45, 128--35. Bissrt, K.A. (1947b). Natural and acquired immunity in frogs and fish. J . I'ulh. Bart. 59, 679-82. Bisset, B.A. (1948a). Nat(ura1ant>ibodiesin t.he blood serum of fresh-water fish. J . Hyg., Canib. 46, 267-8.

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Wolf, K. (1962). Experimental propagation of lymphocystis disease of fishes. Virology, 18, 249-56. Wolf, K. (1964). Characteristics of viruses found in fish. Devs i n d . Microbiol. 5, 139-48. Wolf, K.,and Dunbar, C. E. (1957). Cultivation of adult teleost tissues in vitro. exp. Biol. 95, 455-8. Proc. SOC. Wolf, K., and Quimby, M. C. (1962). Established eurythermic line of fish cells i n nitro. Science, 135, 1065-6. Wolf, K., Snieszko, S. F., Dunbar, C. E., and Pyle, E. (1960). Virus nature of infectious pancreatic necrosis in trout. Proc. SOC.exp. Biol. 104, 105-8. Wolf, L. E. (1941). Further observations on ulcer disease of trout. Trans. Amer. Fish. SOC.70, 369-81. Wolf, L. E. (1954). Development of disease-resistant strains of fish. Trans. Amer. Fish. SOC.83, 342-9. Wolfgang, R. W. (1954). Studies of the trematode Stephanostomum baccatum (Nicoll, 1997). 11. Biology, with special reference to the stages affecting the winter flounder. J . Fish. Res. B d Can. 11, 963-87. Wood, J. W., and Ordal, E. J. (1958). Tuberculosis in Pacific salmon and steelhead trout. Fkh. Commn Oregon, Contr. no. 26, 38 pp.

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Woodcock, H. M. (1904). Note on a remarkable parasite of plaice and flounders. Proc. Lpool biol. SOC.18, 143-52. Woodland, W. N. F. (1927). A revised classification of the Tetraphyllidean Cestoda, with descriptions of some Phyllobothriidae from Plymouth. Proc. 2001. SOC. Lond. 1927, 519-48. Wurmbach, H. ( 1937). Zur krankheitserregenden Wirkung der Acanthocephalen. Die Kratzererkrankung der Barben in der Mosel. 2.Fisch. 35, 217-32. Yamaguti, S. (1935). Studies on the helminth fauna of Japan. Part 9. Nematodes of fishes. 1. J a p . J . Zool. 6, 337-86. Yamaguti, S. (1958-1963). “ Systema Helminthum, ” volumes I-V. Interscience Publs, New York. Yasutake, W. T., Parisot, T. J., and Klontz, G. W. (1965). Virus diseases of the Salmonidae in western United States. 11.Aspects of pathogenesis. Ann. N . Y . Acad. Sci. 126, 520-30. Yorke, W., and Maplestone, P. A. (1926). ‘‘ The Nematode Parasites of Vertebrates”, 536 pp. J. and A. Churchill, London. Young, P. H. (1964). Some effects of sewer effluent on marine life. Calij. Fish Game, 50, 33-41. Young, R. T. (1955). Tetrarhynch (cestode)life histories. Biol. BUZZ.,Woods Hole, 109, 354. ZoBell, C. E. (1946). “ Marine Microbiology”, 240 pp. Chronica Botanica, Waltham, Mass. ZoBell, C. E., and Wells N. A. (1934). An infectious dermatitis of certain marine fishes. J . infect. Dis. 55, 299-305.

XIII. ACKNOWLEDGMENTS

I would like to acknowledge with thanks, but without implication of responsibility for statements or conclusions in this paper, the suggestions and comments of Dr. Z. Kabata, Marine Laboratory, Aberdeen, Scotland; Dr. S. F. Snieszko, Dr. G. L. Hoffman, Dr. K. Wolf and Mr. G. L. Bullock, Eastern Fish Disease Laboratory, U.S. Bureau of Sport Fisheries and Wildlife, Leetown, West Virginia; Dr. A. Rosenfield and Mr. A. S. Merrill, Biological Laboratory, U.S. Bureau of Commercial Fisheries, Oxford, Maryland; and Sir Frederick Russell, Plymouth, England. Mrs. Helen Lang, Librarian, Biological Laboratory, U.S. Bureau of Commercial Fisheries, Oxford, Maryland, assisted immeasurably in the preparation of this review by acquiring publications and translations not generally available. Mrs. Emily Merrill and Mrs. Mary Ropes were especially helpful in preparing and editing the manuscript; Mrs. Miriam Schmidtmann and Mr. James Voshell prepared a number of the illustrations.

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A REVIEW OF THE SYSTEMATICS A N D ECOLOGY OF OCEANIC SQUIDS MALCOLMR . CLARKE National Institute of Oceanography. Wormley. Godalming. Surrey. England I

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Introduction A Distribution .. B . Depth C Life history Architeuthidae .. A . Architeuthia .. Ommestrephidae A Ommaatrepha B. Symplectoteuthia .. C . Doaidiew .. D . Hyaloteuthia E Ornithoteuthia F Illex G . Todaropeie .. H . Todarodea . .. I Nototodarua J . Rhynchoteuthis larvae Onychoteuthidae A . Onychoteuthia B Moroleuthia .. C . Ancietroteuthia .. D Chaunoteuthia .. E. Onychia .. .. F . Tetronychoteuthia . . .. Gonatidae .. A . Qonatua B . Qonatopaie .. .. Thysenoteuthidae . .. A . Thysanoteuthia Parateuthidae .. .. .. A . Parateuthia B . Cycloteuthia .. C. Peychroteuthia D . Alluroteuthiu Valbyteuthidae .. A Valbyteuthia Brachioteuthidae etc., A . Brachioteuthia B Cirrobrachium Pholidoteuthidae . . A Pholidoteuthia

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X I . Bathyteuthidae . A . Bathyteuthie B Ctenopteryz .. X I 1. Enoploteuthidae . . .. A . Abralia .. .. B . Abraliopsis . .. C. Enoploteuthis . D. Pterygioteuthis . E . Pyroteuthia . . .. F. Ancistrocheirwr .. G. Thelidioteuthis .. H . Watasenia . I. Enoploion . . .. XI11. Octopoteuthidae .. A . Octopoteuthis .. B . Octopodoteuthops~s. . C. Taningia . .. .. S I V. Lycoteuthidae . . .. A . Lampadioteuthis .. B . Lycoteuthis . . .. C . Nematolampis .. D . Oregoiiiateuthi8 .. E . Selenoteuthis XV . Histioteuthidae . .. A . Histioteuthia B Calliteuthis . . XVI . Chiroteuthidae .. .. A . Bigelowia . . .. B. Chiroteuthis .. C . Echinoteuthis .. D . Entomopsis .. E . Chiropsis .. F. Valdemaria .. G. Mastigoteuthia H . Larval chiroteuthids XVII . Lepidoteuthidae . .. A Lepidoteuthis .. XVIII . Grimalditeuthidae . A . Qrimalditeuthis X I X Cranchiidae . . .. .. A . Cranchia . . .. .. B . Crystalloleuthis .. C . Liocranchia .. D . PyTgOpS&9 E . Leachia . . .. .. F. Drechaelia .. G . Ascocranchia H . Egea .. .. .. I. Sandalops . . .. J . Corynomma .. K . Bathothavma L Taonidium . . .. M . Teuthowenia N Toxeuma . . .. 0 . Megalocranchia .. P. Helicocranchia

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REVIEW OF THE SYSTEMATICS AND ECOLOGY O F OCEANIC SQUIDS

Q. Anomalocranchia .. R. Henaenioteuthia s. Pueocramhia .. T. Phusmatopaia U. Taoniua .. .. V . Verrilliteuthia .. W. Cfaliteuthia . . X. &feaonychoteuthia .. Spirulidae .. A. Spirula .. .. Distribution . . . . Depth .. .. .. Egg masses .. .. Growth, size, and form Structural variation . . .. .. Parasites .. Ecological importance .. Economic importance Catching methods . .. Acknowledgments . . .. References

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I. INTRODUCTION Cephalopoda living in oceanic water include the tetrabranchiate Nautilus and some members of the dibranchiate orders, the Octopoda and the Decapoda. The living Decapoda consists of the Sepioidea containing an oceanic species (Spirulaspirula)and the teuthoid superfamilies, the entirely neritic Myopsida and the oceanic Oegopsida. The present work deals only with Spirula spirula and the superfamily Oegopsida. Compared with most animal classes very little is known of the Cephalopoda and within the Cephalopoda we are more ignorant of the oceanic squids than of the neritic squids and the octopods. Because so little is known there is perhaps a need to justify a work of this nature at this stage. Every field of study first passes through a basic-fact gathering stage; in the field of ecology this is the stage when species are described and some information concerning their ecology is accumulated. The next stage is one in which taxonomic revisions and condensation of ecological details are tackled and then the last stage is one of analysis and incorporation of the conclusions into the general pattern derived from ecological work in general. Work on oceanic squids, by which the author means those pelagic Decapoda which live for at least a large proportion of their lives over deep water, hovers between the basic data gathering and the revision stages. While a large number of species have been described, revisionists have been struggling to clarify the taxonomic situation for over half a century. The taxonomic tangle prevents any but the most limited analysis of

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ecological data but it does not prevent a presentation of the main problems and a concentration of the known facts. By such a condensation, the author hopes to make readily accessible facts which are at present very widely scattered in the literature so that future workers may see their contributions in perspective and the gaps and inadequacies in previous work may be filled and rectified. It is quite evident that squids are by no means rare in the world oceans and it may well be asked why so little is known of their ecology. The most obvious reason for this ignorance is the great difficulty we have in catching them. Even the largest nets used in oceanic waters in the past (and these may have a fishing gape of 50 ft) only catch the smaller squid of up to a foot in length and probably only a small proportion of these. Such small catches are often made in waters where large numbers can be seen sporting near the surface and where predators have stomachs packed with so-called “ rare ” squids. Gear used in the past has not only been incapable of catching many squids, it has nearly always been non-closing so that little information can be gleaned concerning the depth at which the species live. The paucity of the material and the inability of nets to catch adults (although they catch juveniles) has led to the taxonomic difficulties, It has proved desirable to treat the subject in taxonomic order because of the sparseness of the information. Such an arrangement may also be useful because no comprehensive list of oceanic squids covering the world’s oceans has been published since 1912 (Pfeffer); much of the trepidation experienced by workers who wish to identify a few squids probably arises from the difficulty in finding out what species have been described and which are currently accepted as valid species. In each of the taxonomic sections below the statement of known facts has been presented in the same order where possible. Negative statements have been avoided where possible because they would contribute nothing and would overburden the text. Where no comment is made and a heading in the following plan covers the topic, it may be assumed that nothing is known on the subject as far as the author has been able to ascertain from an extensive search of the literature. The information in each systematic section has been arranged according to the following scheme :

A. Distribution This is affected by the author’s opinions on synonymy so that it has been necessary to give a list of the most important synonyms of each species. The impression one has of distribution is also influenced by the numbers of samples taken in different areas of the globe. So

FIG. 1. Localitios at which oegopsid squids have been collected with the exception of strandings of Architeuthia. A single point may cover more than one sampling station.

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MALCOLM R. CLARKE

that a general picture of the sampling pattern of oceanic squids may be obtained, the stations given for records of all the species except stranded Architeuthis are plotted in Fig. 1 (where stations overlap only one is plotted). The apparent absence or scarcity of all squids from some areas of this chart is very probably because suitable collecting gear has not been used in those areas. Thus, Fig. 1 is a very rough measure of the squid-fishing effort in broad geographical areas and is a useful yardstick when the distribution of individual taxa is being considered. Charts are intended to show the general areas of distribution and where stations overlap only one point has been plotted. With the distribution, any particular taxonomic difficulties are mentioned, details of strandings, migrations, sources of material and environmental tolerances are given.

B. Depth As nearly all samples have been taken with open nets, the exact depth range is known for very few species. Both the depth to which the shallowest net was fished and the depth to which the deepest net was fished are given for each species. In addition, any conclusions which can be drawn from the data are discussed. Where depths are converted from fathoms they are given to the nearest 10 m. With depth, any observations on shoaling and flying are reported.

C. Life history 1. Eggs

i. the form ii. the habitat iii. the time of year 2. Larvae or juveniles i. the form ii. the depth a t which they are caught iii. the time of year they are caught

3. Growth i. the changes in relative dimensions. The word “relatively” has been used to denote ((relative to the mantle length”. Where possible relative growth has been illustrated by figures having mantle lengths the same size, ii. the growth rate

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Maturity i. the size a t the onset of maturity-male and female ii. the ultimate size reached by males and females and the species (if the largest specimen is unsexed). These should indicate the usual size attained although it is difficult to be absolutely sure of extracting all the largest specimens from the literature. Dorsal mantle lengths are used to indicate size but, when these are not available, ventral mantle lengths are used. Mantle length is measured from the extreme tip of the body to the anterior edge of the body in either the ventral or dorsal midline. Total length is measured from the extreme tip of the body to the end of the longest tentacle. iii. the sex ratio

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Mating i. Hectocotylus. The arm concerned and any unusual details about it are noted ii. Site where the spermatophores are deposited iii. Mating behaviour

6. Egg laying i. Season ii. Fecundity iii. Process of egg laying and details of behaviour 7. Food

i. the type ii. the size iii. bites 8. Predators

9. Economic uses

While all these subjects have been considered for all taxa, a few additional pieces of information have been inserted and a slight rearrangement has been thought advisable in a few instances.

11. ARCHITEUTHIDAE The single genus in this family has so many ill-described and poorly known species that it is pointless to treat each species separately. Details of the types of named species are given in Table I.

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A. Architeuthis In the western North Atlantic (Fig. 2) members of the genus have been recorded on the west coast of Greenland (Posselt, 1898; MUUS, 1962), along the north, east and south coasts of Newfoundland (Packard, 1873; Harvey, 1874; Kent, 18748,b; Verrill, 1875a, 1876, 1879b, 1881, 1882c,d,e; Frost, 1934, 1936), Nova Scotia (Verrill, 1879b), north of the Bahamas at 31"N 76"W (Steenstrup, 1898), Massachusetts (Blake, 1909),Florida (Webb, 1897; Voss, 1956a) and on the Mississippi delta (Voss, 1956b). I n the eastern North Atlantic they have been found around Iceland (Steenstrup, 1894; Murray and Hjort, 1912; Bardarson, 1919; Bruun 1945), Spitzbergen (Dons, 1910 in Grimpe 1933),the Faroes (Posselt, 1890),the west coast of Norway (NordgBrd, 1923, 1928; Grieg, 1933b; Kjennerud, 1958), north and west Denmark (Steenstrup, 1857, 1862, 1898; Knudsen, 1957), southern Sweden (Steenstrup, 1857), the east, north and west of the British Isles (summaries in Robson, 1933; Rees, 1950; Stephen, 1962),the Bay of Biscay (Cadenat, 1935, 1936), the Azores (Joubin, 1895a, 1900; Girard, 1892b; Robert Clarke, 1955; Keil, 1963), Madeira (Rees and Maul, 1956; Clarke, 1962a) and a very large squid probably of this genus between Madeira and the Canaries (Crosse and Fischer, 1862). I n the North Pacific they have been taken around the Kuril Islands (Betasheva and Akimushkin, 1955; Akimushkin, 1963), Japan (Hilgendorf, 1880; Mitsukuri and Ikeda, 1895; Sasaki, 1929a), the Bonin Islands (Iwai, 1956a). In the southern hemisphere there are several records from New Zedand (Kirk, 1880b, 1882, 1888; Dell, 1952) one from Australia (Allan, 1948) and one from the small Indian Ocean island of Saint Paul (Vdain, 1877). The author has specimens taken from Sperm whale stomachs caught near Durban and Saldanha Bay, South Africa (unpublished). Records from Antarctic waters based on fragments (Korabelnikov, 1959) need confirmation because other very large squids are found in the region which have not yet been described and confusion between fragments is possible. Nearly all records of Architeuthis are from Newfoundland (24 were examined), northern Europe (39) and New Zealand (11). Most were found after they had become stranded and this has invited speculation on the reason for their prevalence in the three regions. That the distribution does not merely reflect the whereabouts of teuthologists or areas of high population is shown by the paucity of observations in some regions which have at some time held teuthologists and fairly large populations such as the western and lower eastern United States and the Mediterranean. It was early noticed that most strand-

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FIQ. 3. Archileuthis. A. Frequency distribution of the dorsal mantle lengths of specimens for which this has been recorded. Two specimens with a " body " exceeding 16 f t (Verrill, 1881 and Crosse and Fischer, 1862) have been omitted. B. Frequency distribution of the total lengths of specimens. C. Frequency of strandings in each month for the northern and southern (hatched) hemispheres.

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ings occur where warm and cold waters meet and at first it seemed Architeuthis inhabited cold water (Ritchie, 1922); subsequent records are more indicative of a warm water origin and Bruun (1945)suggested strandings possibly occur when animals chase food into colder water and become paralysed with cold before being washed ashore. Most North Atlantic strandings have been in autumn or winter (Fig. 3, C) when the water is cooling down at the northern limit of distribution. In August the surface water off both Newfoundland and northern Europe lies between mean temperatures of 1Oo-15"C; by November these have dropped to 5"-10"C and by February to 0"-10°C. If Architeuthis were detrimentally affected by a drop in temperature indicated by a fall in surface temperatures to about 5O-1OoC the way these isotherms spread out in the eastern Atlantic could explain the more extensive area of strandings on this side compared with the more limited area of strandings in the western Atlantic (Robson, 1933). If, indeed, annual fluctuations of temperature are the cause of Architeuthis becoming stranded it probably lives at depths less than 400 m at which annual fluctuations become negligible. Robson's hypothesis (1933) that they live between 200-400 m or deeper where the surface temperatures are high is credible, though based on little evidence for it must be remembered that the main reason we tend to think they live fairly deep is that only moribund individuals have been seen a t the surface. Also, the distribution of finds around oceanic islands and coasts may be misleading as it could arise from our complete inability to catch these active animals in the open ocean. Reasons for stranding in a few specific instances have been suggested. Storms are sometimes coincident with strandings of Architeuthis (Verrill, 1882c; Allan, 1948) and other species. In Norway the distribution of strandings indicates that the squids probably reach the west coast with the Atlantic Current (Kjennerud, 1958; Nordghrd, 1928). Specimens stranded on the Mississippi delta and at Malmo (Sweden) may have been incapacitated by the low salinities of these regions. Dell (1952) suggested that the New Zealand strandings occur on coasts near to deep water and that, when chasing food, squids may become detrimentally affected if they enter shallower water. The greatest number found at any one time was the mortality of over thirty on the Grand Banks in 1875 (Verrill, 188lb). These animals cannot be very rare in the sea because they are an important and regular part of the diet of Sperm whales around Madeira (Clarke, 1962a), the Kuril Islands (Akimushkin, 1955a) and South Africa (Clarke, in preparation). Mature males have the two ventral arms hectocotylized (Knudsen,

TABLEI. DETAILSOF Name

Author

THE

Date

TYPE S P E C ~ OF N EACH SPECIESIN THE GENUS Architeuthia ON NAMES IN THE LITERATURE Locality

How cuzlght

WITH

Type material

Comments ~

A . pranceps A . haweyi A. m w h u a A . dux A . phyaeteria A . japonka A . eancti-pauli A . stocki A . vemilli A . longimanua A . kirki A . grandia A . clarkei A . nuwaji A . hartingii A . titan A . martenaii A . mouchezi

9N.Atlantic Newfoundland Jutland 31'N 76"W 38'34" 29"37'W Awa Prov. Japan St. Paul Island New Zealand New Zealand New Zealand New Zealand

sperm stomach herring net dead a t surface dead at surface vomited in fishing net stranded stranded stranded stranded stranded

England Bay of Biscay

stranded complete animal caught by Palombe complete animal buccal mass

Verrill Verrill steenatrup Steenstrup Joubin Pfeffer Velain Kirk Kirk Kirk Robson Owen Robson Cadenat Verrill

1875 1879 1867 1898 1900 1912 1877 1880 1880 1880 1887 1881 1933 1935 1880

Hilgendorf

1880 Japan

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COMMENTS

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B ~~~

beaks complete animal in parts beaks arm, suckers and pen body complete animal only description and photo complete snimal complete animal complete snimal complete animal arm

A . proboacideua More 1875b Dingle (Ireland) stranded A . bouyeri Crosse and Fischerl862 Btw. Madeira & Teneriffe dead at surface

debris, pen, fins same specimen as A. eancti-pauli description and figure only description

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proof name for A. dux in Market

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FIG. 4. -4rchiteuthis sp. stranded at Ranheim, Norway, in October 1954. (Photography by E. Sivertsen.) A.31.11.-4

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1957; Kjennerud, 1958) and a relatively enormous penis up to 78.0 cm long and extending 55.0 cm beyond the mantle opening. Presence of numerous evaginated spermatophore tubes stuck into the arms, mantle, and penis of a male shows that accidental copulation between males sometimes takes place (Kjennerud, 1958). Spermatophores vary in length between 10-18 cm (Knudsen, 1957; Kjennerud, 1958; Voss, 1956b). A male with a mantle length of 61.2 cm contained spermatophores (Voss, 1956b) whereas another 156.0 cm long had a small penis and was probably immature (Frost, 1934 from Figure). The size reached by Architeuthis is often exaggerated in semiscientific journals. All the positively identified and measured specimens have a total length of under 60 f t and a mantle length of under 17ft (Fig. 3, A and B) while most have a mantle length less than 8 ft. Weights of 48 kg (Kjennerud, 1958), 150 kg (Rees and Maul, 1956), 184 kg (Robert Clarke, 1955) and 259 kg (Frost, 1934) have been recorded for squids with mantle lengths of less than 7 ft. Extrapolation of a logarithmic plot of these 4 values against their respective mantle lengths indicates that estimates of 700-900 lb (318-408 kg), 2 000 lb (980 kg) and even 1 ton (1 000 kg) (Verrill, 1882c) are not impossible for squids with mantle lengths of 17 ft. Stomachs are almost invariably empty, but the suggestion that squid are probably poor swimmers and ill adapted for catching active prey (Robson, 1933; Voss, 1956b) seems incompatible with the many hundred large suckers up to 3 cm diameter, the very powerful buccal muscles, the short thick jaws giving maximum leverage, and the thick mantle wall. Bruun (1945) mentioned that they chase herring but gave no specific examples.

111. OMMASTREPHIDAE It will be convenient to treat the genera of this family separately. A. Ommastrephes This genus contains a complex of 0. pteropus (Steenstrup, 1855), 0. c a d i (Furtado, 1887) and 0. bartrami (Lesueur, 1821) which are not yet separable a t all stages and some historical detail is unavoidable in discussing their distribution. One difficulty is that 0. bartrami was described on the basis of a small specimen from Newfoundland which has since been lost; it may have been a young specimen of the species subsequently described as 0. caroli or 0.pteropus from larger specimens taken elsewhere in the Atlantic and Mediterranean. However, although there are large specimens which have since been referred to 0. bartrami and are undoubtedly 0. caroli, there are also many Pacific so-called

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0 . bartrami which are certainly different from 0. caroli and 0. pteropus. This problem can only be resolved by a study of the Ommastrephes species living in the western North Atlantic t o determine whether it is identical with 0. caroli or 0 . pteropus. If it should prove the same as either, then the name 0. bartrami would take priority and another name would have to be found for the Pacific so-called 0. bartrami. With these reservations we can now consider the known distribution of the three species. 0. caroli was described from a head and two females stranded in Portugal; the mantles measured 57-0 cm and 61.0 cm in length (Furtado, 1887). Since then, a number of similarly large specimens have been recorded, usually after stranding, from the British Isles (Goodrich, 70

F

W A U L MANTLE LENGTH em

FIG. 5. Size frequency distribution of a sample of Ornmastrephea caroli (black) and 0. pteropus (white) taken at Madeira, in July and August 1959.

1892; Nichols, 1905; Robson, 1925b, 192913; Meek and Goddard, 1926; Clarke and Robson, 1929; Gyngell, 1928, 1929; Stevenson, 1928, 1935; Clarke, 1930; Stephen, 1933, 1938, 1944; Clarke and Stevenson, 1935; Stendall, 1936; Rees, 1950), Holland (Steenstrup, 1898; Kaas, 1939), Juist in the North Sea (Hertling, 1938), Faroes (Liinnberg, 1891), Madeira (Rees and Maul, 1956), off the Azores (Mackintosh, 1956; Baker, 1960), southern France (Joubin, 1893a) and S. Margherita Ligure (Issel, 1925126). Some of these have been called 0. bartrami and 0. pteropus but they are almost certainly 0. caroli. Recently a large number of specimens of Ommastrephes has been collected in the eastern North Atlantic (Baker, 1960) and the author has examined these together with much additional material taken subsequently at Madeira and elsewhere (Clarke, unpublished). The size distribution of specimens from Madeira shows three groups (Fig. 5); the largest of F 2

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all are 0. caroli females: the middle group are all recognizable a s 0. pteropus from the large light organ on the dorsal side of the mantlc (Clarke, 1965a);and the smallest could be, from their detailed structure. either 0. caroli or 0. bartrawbi. However, all the small specimens are immature and we have no evidence t h a t any mature Onamastrephes, not referable to 0. caroli or 0. pteropus, are in the area. It seems safc. therefore, to conclude t h a t these small immature squids are in fact 0. caroli and t h a t there are no 0. bartrnrni in the Madeiran area. 0. caroli and 0. pteropus have different distributions; the former extends from Iceland to a t least south of the Canary Islands a n d into the Mediterranean; 0. ptmopus extends from Madeira southwards t o West Africa (Adam. 1952) and westwards t o the Gulf of Mexico (Voss, 1956b) but its occurrence in the Mediterranean is questionable. As mentioned above, 0. bartrawbi has been reported from the Pacific; from the Bering Sea (Berry, 1912d; Lucas, 1899), J a p a n (Sasaki, 1916; 1929; Utsuna, 1932), north of the Bonin Islands (Sasaki, 1929a), Formosa (Sasaki, 1929a). China (Sasaki, 1916), Chile (Pfeffer, 1912), Magellanica (Carcelles and Williamson, 1051), Marshall Islands (Berry. 1912d), Fiji Islands (Berry, 1912d), Kermadec Islands (Berry, 1 9 1 3 ~ ) . I n the Indian ocean it has been reported from South Africa (Pfeffer, 1912; Robson, 1924a; Massy, 1925, 1928b), Ceylon (Sasaki, 1916), Madagascar (Sasaki, 1916), Chagos Islands (Robson, 1921). Some but not all of these records are possibly due t o misidentification of Symplectoteuthis which is very similar. 0. bartrami variety sinuosus Lonnberg, 1896 caught off Teneriffe is probably 0. pteropus. Annual migrations are made by 0, caroli and 0.pteropus into Madeiran waters. Small 0. caroli of both sexes appear in J u l y and August and are used in large numbers for bait, a n d human consumption (Rees and Maul, 1956). Large 0. caroli (the right hand group in Fig. 5 ) are all females. After the appearance of the small 0. caroli, shoals of female 0. pteropus appear and fewer 0 . caroli are caught. The female 0. pteropus vary between 26.0-38-0 cm in mantle length. The absence of male FIG. 6. Photographs taken with the underwater camera a t a depth of 400-500 m a t 32"31'N 1 6 35'W. The camera was so arranged that it operated when a bait at the end of a rod in the field of view was pulled. I n this series a n ommastrephid (either Todarorles saqittatcta or OmrnaRtrephes pteropus) about 45 em long has become " foul-hooker1 " in the tail region of the mantle. These photographs are selected from a series of over thirty taken as the squid struggled to escape from the hook and the attacks of one or more individuals of Todarodes aagittatua. On bringing the camera to the surface, the squid had dropped off and the bait was still rtpparently untouched. D. shows how the fins may be folded round the body and the anterior edges fanned out t o act as a break.

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0. pteropus from Madeira and indeed from the whole area studied in the eastern North Atlantic (Clarke, 1965a) contrasts markedly with the situation found in the Caribbean and the West African Coast from Cape Verde Islands to 1325's (Adam, 1952, 1960c, 1962) where there are both males and females of all sizes. At present, therefore, it appears that the 0. pteropus in the eastern North Atlantic migrate into the region from the West Atlantic or from the South (Clarke, 1965a). Ovaries and nidamental glands of 0. pteropus a t Madeira indicate that egg laying has either recently taken place or is imminent and spermatophores on the buccal membranes show that mating has taken place (Clarke, in preparation); it therefore seems likely that this migration is for spawning. 0. pteropus reaches Madeira a t about the same time as the northmoving 22°C mean surface isotherm and nearly all catches of this species from R.R.S. Discovery I1 were made south of the isotherm. The southern limit of 0. pteropus seems to be 13"25'S (Adam, 1952) which is coincident with the southern limit of the 25°C isotherm. I n assessing the distribution of 0. pteropus and 0. caroli the author has ignored all records which do not include sufficient details for him to be confident of the identification. 0. caroli and 0. pteropus are the dominant near-surface forms where they occur. They can usually be seen within an hour of stopping a ship a t night except on bright moonlight nights when they are less frequently seen, apparently because they tend to stay a t greater depths (Baker, 1957b, 1960). Something of the depth range of 0.caroliis known from photographs taken with a deep-sea camera which is triggered by any pull on a baited hook (Baker, 1957a) and twice, tentacles have been caught in water bottles when they reversed thus giving a precise depth of capture (Clarke, unpublished). These records show that 0. caroli extends down to a t least 1490 m below the surface (Table 11) and, as most of the photographs were taken during dark hours, it is evident that the whole population does not migrate to the surface a t night. 0. pteropus has been recorded from 3 160 m with a non-closing net (Voss, 1956b). There can be no doubt that 0. caroli and 0. pteropus are present in enormous numbers in their areas of distribution as shown by their regular appearance a t the surface a t night. Both species form shoals of less than about fifty individuals consisting of similarly-sized individuals; each squid being no more than two or three body lengths from its neighbours. Shoals become smaller as individuals grow in size. These animals are extremely strong and rapid swimmers and specimens identified as 0. bartrami have been known to leap out of the water,

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so earning the name of "flying squid'' (Verrill, 188%; Berry, 1912d; Aratara 1954). The author has seen this behaviour by 0. caroli which were about 30 cm in total length and some degree of control in a fresh breeze was once witnessed. It is more often observed prior to the appearance of larger squid and can be interpreted as a panic, escape reaction. TABLE11. DEPTHSAND POSITIONS AT WHICH PHOTOGRAPHS OF SQUIDS HAVE BEEN TAKENOR PARTS HAVE BEEN TRAPPED IN REVERSING WATER BOTTLES (W/B).

Position 40'13" 40"06'N 37'22" 45'12" 40'05" 40"05'N 39"55'N 28'42" 40"02'N 32"31'N 28"03'N 28"04'N 28'05" 28'03" 46"57'N 33'06"

2O"OS'W 20'17'W 25"33'W 11'46'W 20'02'W 1Y56'W 20"Ol'W 17"38'W 19"52'W 16"35'W 14'02'W 14'09'W 14"09'W 14'1 1'W 07"27'W 75"44'W

Discovery Depth Station N o . (m) 3 474 3 476 3 478 3 655 3 483 3 482 3 484 3 673 3 485 3 684 5 808 5 811 5 812 5 816

300 300 300 500 GOO 600 700 900 1000 400-500 1 000 500 200 300 1 2 0 5 W/B 1490 W/B

Probably Todarodes sagittatus ? species Todarodes sagittal 11s ? species Todarodes sagittatus Probably Ommastrephes caroli Probably Ommastrephes caroli ? Todarodes sagittatus Todarodes sagittatus series of ommastrephids Todarodes sagittatus Todarodes sagittatus Todarodes sagittatus Todarodes sagittalus arm o f squid possibly 0 . caroli. tentacle club of 0 . caroli.

Larval stages of ommastrephids have often been described under the generic terms Rhynchoteuthis or Rhynchoteuthion and very little progress in relating the larvae to the adults has been made (see page 141). It is therefore of interest that two larvae, caught in the eastern North 17'02'W (Station 4724) Atlantic by R.R.S. Discovery at 27'56" with a closing Isaacs Kidd Midwater Trawl fished a t 100-230 m in September, are definitely referable to either 0. caroli or 0 . pteropus. This was determined from the form of their funnel connectives which have features distinguishing these species from all other ommastreyhids in the region. The larvae have mantle lengths of 0.47 cm and 0.93 cm respectively and show two stages of development. The smaller larva has a trunk-like proboscis (Fig. 7, A) with two large and six small suckers a t its tip (Fig. 7 , C). At its base, this proboscis has a small hole running between its two roots, from the aboral to the oral side. The

\i 0 . 47

FIG.7. Rhynchotcuthis larvae of the Ommastrephitlae. Bfantle lengths in mn arciritlicatetl. A and B. T w o stages from the North Atlantie referable to either Ominastrephes caroli or 0. p f e i o p n s from the left ( A ) and the ventral sides (B). C'. Tip of the probosris of the smaller speritnen. D. Tip of the prohoseis of the larger specimen. E. Rhynchoteuthis stage of SU,,,plertoletcthi,P otralnniensis with intestinal light organs (see p. 115). F. Tip of t h r proboscis. G , H. I, Stages referrrtl hy Chun t o the slender type of Rh!ydzotenlhis (1910, Plate S S V I I I , Figs. 2, 4, 15). J, I<, L. Stages referred hy Chun to the plump t y p e of Rhyrtdotenthis (1910, S S V I I I , Fig. 8 , 9. 11). A from the k f t side, the rest from the ventral side.

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ventral arms are minute. I n the larger larva (Fig. 7 , D) the hole through the proboscis has become much larger and almost divides the proboscis into two halves. the tentacles. The proboscis tip bears about nine pairs of small suckers (Fig. 7 , D). During growth to the adult, the arms become relatively longer, the head becomes relatively shorter and the body becomes relatively narrower compared with the mantle length. Other examples from the eastern North Atlantic possibly referable to 0. caroli and 0. pteropus have been recorded from the surface to 2 025 ni with open nets in July to September (Chun, 1913; Massy, 1916a, 1928a: Joubin, 1920, 1924). Okutani (1965) has given a brief description of larvae referred t o 0. bartrami occurring off Japan. Once the larval stage is over, change in body form is gradual (Adam, 1952). Females of 0. caroli become mature (presence of ripe ovaries and enlarged nidamental glands) at a mantle length of 40.0 cm and males (presence of spermatophores) at 30.0 cm (Clarke, 1962e). In 0. pteropus, females become mature at a mantle length of 3 0 4 cm. As we have caught apparently-healthy females of these two species which possess spent ovaries it appears that they do not necessarily die a t spawning; we have, however, no evidence that these survivors spawn a second time. The greatest size reached by females of 0. caroli known to the author is 69.0 cm (mantle length) and by males 36.0 cm; that of 0.pteropus females is 37.0 cm. The sex ratio of 0. cnroli taken in the North Atlantic by Discovery II is 46 females to 18 males. In &heWest African region the sex ratio of 0. pferopus is 22 females to 13 males (Adam, 1952). One of the ventral arms is hectocotylized in both these s p e c k hy 103s of suckers from the tip and the development of a slight groove. Spermatophores are stuck into the buccal membrane of the female. While the ovaries and nidamental glands suggest that spawning takes place in late summer and autumn in 0. caroli, spermatophores are present in males taken throughout the year (Clarke in preparation). A large 0. caroli probably lays about 360 000 eggs (calculated from the ovary of one ripe female). There is no doubt that these species are rapacious predators rapa1)le of attacking fish and squids the same size or larger than themselvcs. If one is caught on a hook the other members of the shoal turn on i t and sometimes badly damage it before it can be pulled in (Figs. 6 and 8). Such observations belie Steenstrup’s (1885) contention that 0. pfwopws feeds on small, weak animals driven into the trap formed by the arms and their membranes which function rather like a dipnet. Few stomachs have been examined. An 0. pteropus proved to contain fish.

112 MALCOLM R. CLARKE

FIG. 8. Photographs taken with deep sea camera at a depth of 1 000 m (A) and 700 m (B). Todarodes aagiltatus (A) uses its tentacles in the same way as its arms when attacking food but Ommastrephe8 pteropus is able to press-stud the base of its tentacle clubs so that the tentacles may be used together, rather like tongs.

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crustacea and squid hooks similar to those of Octopoteuthis sicula (Adam, 1952). I n 0. caroli the author has found fish and squid remains. Although bitten a number of times by 0. caroli the author has suffered no after affects which one would associate with poison. Known predators of these species are Fregata aquila (Adam, 1937a), Thynnus albacora (Adam, 1951), Germo obesus (Rees and Maul, 1956), Germo alalunga (Bouxin and Legendre, 1936), Gadus morhua and Plagiodux ferox (Jaeckel, 1958). It is remarkable that these squid, though numerous in the area, are not present in Sperm whale stomachs taken near the Azores and Madeira (Clarke, R., 1956; Clarke, 1962a). These species are used in very large numbers at Madeira for bait in the " Espada " (Aphanopus carbo) fishery and they are also used extensively for food. Recently described from argentinian waters, Omrnastrephes argentinus Castellanos, 1960 is known from 120 specimens. The distribution is said to be 38-41"s and 55-6Oow. The types were a female with a mantle length of 25.0 cm and a male of 22.0 cm.

B. Symplectoteuthis The two species of this genus can be easily distinguished from one mother. 1. Symplectoteuthis luminosa Sasaki, 1915 Eucleoteuthis luminosa Berry, 1916a ; Okada, 1927. Recorded from Japan (Sasaki, 1915b, 1929a), the Kuril islands (Akimushkin, l955b, 1957) and the Kermadec islands (Berry, 1916a) it occurs rarely but may be locally abundant at times (Fig. 9). It is characterized by longitudinal streaks on its ventral mantle which have been seen to luminesce (Sasaki, 1929a). It has been taken in water of less than 1300 m in depth (Sasaki, 1915). A female with a mantle length of 13.0 cm proved to be mature (Akimushkin, 1955b); the largest female known is 17.5 cm and the largest male is 19-5 cm in mantle length (Sasaki, 1929a); the larger males, seen by Sasaki (1929a), have spermatophores. 2. Symplectoteuthis oualaniensis (Lesson, 1830) Loligo vanicoriensis Quoy and Gaimard, 1832 Ommastrephes oceanicus d'orbigny, 1835-1848 ? 0. Tryonii Gabb, 1862b. ? 0. Ayresii Carpenter, 1864 This species largely replaces the Atlantic Ommastrephes complex in the surface waters of the Western Pacific and Indian Oceans (Fig. 9).

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First described from Oualan Island in the Caroline group (Lesson, 1830) it has since been recorded from Formosa (Sasaki, 19229a). Okinama (Sasaki, 1929;~), Laysan, (Pfeffer, 1912), the Philippines (Voss. 1963a), East Indies (Adam, 1954), New Hebrides (Hoyle. 1886). north of Admiralty islands (Hoyle, 1886), east of Cocos Islands (Hoyle, 1904b). Laccadive Islands (Berry, l912c), north-west Australia (Brazier. 1892b), Torres Strait (Brazier 1892b), Great Barrier Reef and Nickol Bay, Australia (Brazier, 1892b), Vanicoro Islands (Quoy and Gaimard, 1832), Rongslap Atoll (Voss, 1954b), Japan (Wulker, 1910), South Africa (Massy, 1925), the Red Sea (Weindl, 1912; Adam 1959, 1960b). Berry ( 1 9 1 4 ~recorded ) the species from Sunday Island in the Kermadec group but later referred these specimens to S. luminosn (Berry, 1916a). The species has been recorded in the Gulf of Panama (Dall, 1910) but Berry (1912d) claimed that it had not been certainly identified from western North America; it has since been listed for the west coast of south and central America (Voss, 1963a). To these records can be added Zanzibar, a number of stations scattered in the Arabian Sea (Clarke, unpublished), and Christmas Island (Ashmole, in press). Little is known of seasonal migration but Sasaki (1929a) mentions that they are prolific and mainly fished in summer at Okinawa. This " species " has recently been found t o consist of two distinct forms, one with and one without a large light organ on the dorsal mantle surface (Clarke, 1965a and in preparation). Because these forms also differ in the size at which they attain maturity they must be considered distinct species. We cannot separate the previous records into the two forms, but it is known that both are present in the Indian Ocean and at Christmas Island in the Pacific. Here again is an example of two, at least partially sympatric species distinguished by a large dorsal light organ (see Ommastrephes page 106). These squids come near to the surface at night and seem to be as ubiquitous and active as their Ommastrephes counterparts in the North Atlantic (page 108). A rhynchoteuthis larva was caught by R.R.S. Discovery a t 2227.6" 63"50*7'E, very near the surface with a Neuston net in July 1963. It has light organs on the intestine and a funnel connective the same as Symplectoteuthis oualaniensis except that it is not fused to the mantle. As there is only one known species of ommastrephid with these features the larva is almost certainly the S . oualaniensis with an intestinal light organ mentioned above. It is most interesting that the fusion of the funnel with the mantle is thus shown to take place after the larval stage. The larva has a very elongated proboscis (Fig. 7, E) with eight suckers at the tip, two of which are slightly

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larger than the others (Fig. 7 , F). Okutani (1965) drew attention to the great length of the proboscis in 8. oualaniensis when describing differences between rhynchoteuthis of Todarodes pacijicus and rhynchoteuthie of other ommastrephids from Japanese waters. During growth t o the adult, the arms become relatively longer, the head relatively shorter and the body relatively narrower compared with the mantle length. I n the form with a dorsal light organ, females become mature (i.e. have enlarged nidamental glands and ovaries) a t a dorsal mantle length of about 18.0 cm and males become mature (i.e. have spermatophores and a hectocotylus) a t a dorsal mantle length of less than 13.6 cm; in the form without a dorsal light organ the females become mature at less than 10.7 cm (Clarke, in preparation). The largest female of the form with a dorsal light organ, known to the author (ignoring published records because it is uncertain which form is involved), is 30.5 cm (in mantle length) and the largest male 14-0cm. I n the other form the largest female is 25.0 cm and the male 14.0 cm. The hectocotylus is slightly swollen, devoid of suckers a t the tip and has several small holes running from the base of the suckers to the sides of the arms. The spermatophores are stuck on to the buccal membranes of the female and seminal receptacles are also present (Sasaki, 1929a). The oval eggs in the oviduct measure 0.7-1.0 mm (Sasaki, 1929a). It has been recorded from stomachs of a Booby and White-capped Noddy (Voss, 1954b) and from Sula piscator (Hoyle, 1886, 1904b). At Christmas Island both forms are clearly very important in the diet of sea birds (Ashmole, in preparation). It is commonly sold for food at Okinawa (Sasaki, 1929a).

C. Dosidicus This genus is generally considered to include only one species. 1. Dosidicus gigas (d’orbigny, 1835) Ommastrephes gigas d’orbigny, see 1835-1848 Ommastrephes giganteus d’orbigny, see 1835-1 848 Dosidicus Eschrichtii Steenstrup, 1857 Dosidicus Steenstrupii Pfeffer, 1884 There are many records of this species along the western coast of South America (d’orbigny, 1835-48, 1845; Steenstrup, 1880; Martens, 1894; Steinhaus, 1903; Dall, 1910; Berry, 1912b; Pfeffer, 1912; Robson, 1929a; Schneider, 1930; Odhner, 1931; Wilhelm, 1931; Duncan, 1941; de Sylva, 1962; Garcia-Tello, 1964; etc.). It has also been recorded from the Galapagos Islands (Boone, 1933), off California (Carpenter,

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1864; Yates, 1889; Kelsey, 1907; Berry, 1911c; Phillips, 1931, 1961; Clarke and Phillips, 1936; Croker, 1937), north Queensland (Brazier, 1892b), Lord Howe Island off eastern Australia (Brazier, 1892a) and the Solomon Islands (Brazier, 1892a) (Fig. 9). A record from Perim Island in the Red Sea would seem to need confirmation (Brazier, 1892a). This species comes to the surface a t night in great numbers and is apparently the south eastern Pacific counterpart of Ommastrephes and Symplectoteuthis. After a mass mortality in Talcahuano Bay (Schneider, 1930; Wilhelm, 1931) many thousands were washed up and congested the harbours; this gave an indication of the very large numbers present in the area. At Monterey in California large numbers have been caught in certain years and although a small proportion have been sold to the Japanese (Clarke and Phillips, 1936) they have been considered a pest to the game fisheries (Croker, 1937). The Californian specimens all had a total length of less than about 5 ft (Berry, 1912b; Phillips, 1961) and reached over 30 lb in weight (Croker, 1937), but off Chile they apparently reach much larger sizes and possibly even up to a total length of 12 ft (personal communication with inhabitants of Chile). The stomachs of three specimens contained anchovies, one contained Scomberesox and two contained squid flesh out of a total of eight examined (de Sylva, 1962). The species is important in the diet of Sperm whales caught off Peru and Chile (Clarke unpublished) and is used for bait and to some extent for food in Chile and California.

D. Hyaloteuthis This genus includes a single species. 1. Hyaloteuthis pelagica ( BOSC,1802) Sepia pelagica Bosc, 1802 Ommastrephes pelagicus d’orbigny, 1835-1848

A rather rare species which is very widely distributed, being found in the Atlantic (d’orbigny, 1835-1848; 1845; Steenstrup, 1880), in the West Indies (Adam, 1957), Saint Lucia (Gray, 1849), Ascension Island (Stonehouse, 1962) and the eastern North Atlantic (Clarke unpublished), as well as in the Pacific from Japan (Sasaki, 1929a), the Bonin Islands (Sasaki, 1929a), the Marshall Islands (Voss, 1954b), north of Hawaii (Rehder, 1940) and the South Pacific (Pfeffer, 1912). These squids are caught near the surface a t night and are charac-

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terized by prominent photopliores on the ventral mantle (19 in the adult 195413). These are obvious in quite small specimens (Clarke unpublished). A female with a mantle length of only 5.3 cm was gravid (Voss, 1954b) and the largest specimen known has a mantle length of 7.1 cm (Sasaki, 1929a). The species was collected from stomachs of Anous tm7Lirosfris (Black Noddy) a t Ascension Island (Stonehouse. 1962).

--Voss,

E. Ornithoteuthis This genus contains two very rare species. 1. Ornithoteuthis volatilis (Sasaki, 1915) Ommastrephes oolatilis Sasaki, 1915b This species has been recorded from Japan (Sasaki, 1915b, 1929a; Okada. 1927). It sometimes jumps above the sea and is known as a " flying squid " by fishermen (Sasaki, 1929a). The largest male apparently has a mantle length of 31.3 cm and the largest female 20.8 cm (Sasaki, 1929a but there is a slight confusion in the text).

'2. Ornithoteuthis antillaruni (Adam, 1957) Orn ithoteuthis volatilis antillarum Adam, 1957 A species recorded from the tropical west Atlantic (Adam, 1957; Voss, 1957), West Africa (Adam, 1962) and off Morocco (Rancurel, 1964). It has only been caught near the surface. The largest male has a mantle length of 14.1 cm and the largest female a mantle length of 10.3 cm. The right ventral arm is hectocotylized and there is some sexual dimorphism in the dentition of the arm suckers and the foveola in the funnel groove (Voss, 1957). A stomach contained several Abralia with mantle lengths of 3-0 cm, a caridean shrimp and fish scales (Voss, 1957). One of the specimens was found in the stomach of Tursiops truncatus (Rancurel, 1964).

F. Illex There is some confusion between Illex illecebrosus and Illex coindeti and they have both been considered geographical forms of the same species by some authors (e.g. Pfeffer, 1912; Adam, 1939c). I . illecebrosus is the western North Atlantic form and I . coindeti the Mediterranean form but the confusion arises when examples from the North Sea and British Isles are examined (see below).

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1. Illex illecebrosus (Lesueur, 1821) Loligo illecebrosus Lesueur, 1821 Ommastrephes illecebrosus, Verrill, 1880c

In the western North Atlantic (Fig. lo), the species has been recorded at Frederikshaab, Greenland (Posselt, 1898),Hebron harbour, Labrador (Squires, 1957, 1959), off Newfoundland (Lesueur, 1821; Verrill, 1882c; Williams, 1909; Frost and Thompson, 1932, 1933, 1934; Boone, 1933; Squires, 1957; Anon, 1958),Cape Hatteras (Verrill, 1882c), Nova Scotia (Boone, 1933), Trois Pistoles, Quebec (Prbfontaine and Brunel, 1962), eastern United States (Frost and Thompson, 1932), Caribbean and Gulf of Mexico (Voss, 1955, 1956a, 1956b). The northern distribution has been said to include Iceland (Bardarson, 1919; Bruun, 1945),the Faroes (Grimpe, 1933) and northern Europe (Pfeffer, 1908b, 1912; Voss, 1956b). Because of the confusion with I . coindeti in this region the exact extent of distribution is not known. However, there is some reason to doubt Bruun’s record for Iceland which was based on a note by Grnrndal which could have referred to I . coindeti and a short passage in Murray and Hjort (1912) “Illex illecebrosus and Omrnatostrephes todarus are northern forms, of great importance on the banks of Newfoundland, and along the coasts of Iceland and Norway”. Bruun understood this to mean that both species are important on both sides of the North Atlantic, but it seems much more likely that the authors meant that I . illecebrosus was important on the western and 0. sagittatus ( = O . todarus) on the eastern side of the northern Atlantic; particularly as the latter species is not found on the western side. Other doubtful records are Joubin’s (1920) from the Bay of Biscay and Chun’s (1913) from north west Africa and the Canary Islands, all of which could have referred to I . coindeti. In view of the doubt regarding the extension of I . illecebrosus to Iceland and the Faroes, workers have sometimes been tempted into considering the species of the two sides of the Atlantic as distinct forms, but Adam (1952), by a statistical analysis of dimensions, has shown the situation to be much more complex. He found that specimens from the Bristol Channel were intermediate between I . illecebrosus and I . coindeti, but that they were closer to the former; he also found that, of the Illex appearing in the North Sea, those caught in June resembled I . coindeti, and females caught in March and May were close to I . illecebrosus. Although I . illecebrosus is most numerous near to coasts and probably lives on the upper slope and shelf, a damaged juvenile (tentatively identified as this species) has been recorded rather far from land (Joubin, 1895b). A record from Onondaga Lake A.M.B.4

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MALCOLM R. CLARKE

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arose from a bait squid being abandoned by fishermen (Clarke, 1902). Each year vast numbers of young Illex of one age class move from the south on to the Newfoundland Grand Banks and arrive in inshore waters in June (Frost and Thompson, 1932, 1933, 1934; Squires, 1967). They move along the southern and north-eastern shores and may reach Labrador in September. Although the exact relationship between

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water masses and this migration is not very clear, it seems that the squids move into the area with deep, warm, highly-saline Atlantic water from the south; they are found early in the season on the south edge of the Banks and move inshore as the temperature rises (Frost and Thompson, 1932, 1933 and 1934; Squires, 1957). Although earlier

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work suggested that fewer squid move inshore when the Banks are submerged in Arctic water, Squires (1957) found little data to support this contention. During the inshore period, they have a temperature preference of 7"-15°C near the surface with bottom temperatures of O.5"-8.O0C and large numbers are stranded (Squires, 1957). Frost and Thompson (1932, 1933, 1934) found no evidence of

122

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growth during 6 weeks of the inshore period and thought that this indicated that successive waves of young squid were entering inshore waters throughout the season. They also found that the squids taken on the Grand Banks were smaller and were eating more than those taken inshore. Squires (1957),however, found a steady growth through the season inshore and the modes in size-frequency distributions taken concurrently were the same in various sampling regions. From Squires’ data (Fig. ll), it appears that the young squid entering the region in May were probably spawned the previous summer and that three large individuals, well outside the range of the majority, were probably 2 years old. I n October and November, k s t the larger and then the smaller squids move south into deeper water. Some of the males then possess spermatophores and large testes and the larger females axe nearing maturity. Although there are some minor differences between the sexes, and the mature females are larger, there is no marked difference in proportion as in I . coindeti (Adam, 1952). Some males with 8 mantle length of 22.0 cm and all males of more than 25.0 cm, have the right or left arm hectocotylized. At a mantle length of 23.0 cm the testis is very large and, over 24.0 cm, spermatophores are present in the penis. Squires (1957) only saw two ripe females, both caught in May and with mantle lengths of 25.0 and 28.0 cm. Mating, spawning and hatching must take place somewhere to the south in deep water, probably on the continental slope of the United States where occasional adults are caught during winter (Frost and Thompson, 1932). Squires (1957) found some evidence that the squids are moving farther north in recent years than they were in the early 1930’8, but he was unable to find any cycles of annual abundance. He found that onshore winds caused the squids to “disappear” from the squidding grounds almost immediately. During the summer and autumn the squids at f i s t feed mainly on euphausids probably Meganyctiphanes and Thysanoessa (Squires, 1957) and then, as they become larger, on capelin, herring, and mackerel (Verrill, 1882c; Squires, 1957). Besides the cod and mackerel which must be important predators of Illex on the Grand Banks (Verrill, 1882c), the Pilot whale feeds almost exclusively on it during summer and autumn (Squires, 1957). It has also been taken from stomachs of Delphinapterus leucas (Vladykov, 1946) and Orthugoniscus mola (Adam, 1939~). Much of the work on this species was initiated because of its great importance to the “ fall ” cod fishery of Newfoundland, for which it provides the principal bait. Particularly before refrigeration, the fishery was frequently very adversely affected by the small numbers of

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squid in the region during some years. At other times these squids are 80 numerous that they are used as fertilizer. 2. Illex coindeti (Verany, 1837) Loligo coindetii VBrany, 1837 Loligo brogniartii Blainville, 1823 Loligo sugittata (pars) Blainville, 1825 Ommastrephes sagittatus (pars) d'orbigny, 1845 Loligo pillae VBrany, 1851 Todaropsis veranyi Jatta, 1896 Illex illecebrosus coindeti Pfeffer, 1912 ? Illex illecebrosus Chun, 1913 ?Illex illecebrosus Joubin, 1920 This species has been recorded from Scotland and the North Sea (Norman, 1890; Grimpe, 1925; Fig. lo), the English Channel (Rees, 1957),the Irish Sea (Chadwick, 1921), the west coast of France (Joubin, 1896a, 1920), Portugal (Girard, 1890a,b; Nobre, 1932), Morocco and the Canary Islands south t o 26" 3'N, (Chun, 1913; Robson, 1926a), the west African coast from 9" 14" to 14"s (Desbrosses, 1938; Adam, 1951), the western Mediterranean (V&any, 1851; Jatta, 1896; Morales, 1958; Mangold-Wirz, 1963; etc.); the Adriatic (Kolombatovitsch, 1900; Pfeffer, 1912; Gamulin-Brida, 1963) and the Red Sea (Adam, 1942a). Adam (1952) considered that more specimens are needed in order to find if there is a difference between I . coindeti from the Mediterranean and West Africa and those from western Europe. Mangold-Wirz (1963) studied the ecology of the species in the north west Mediterranean and found that migrations of two groups took place in each year. I n January a group of sexually advanced squids lie on the bottom between about 60-150 m and immature squids are caught on the bottom between 150-400 m. The advanced group move into shallower water from March until, in about July, they are caught on the bottom in water of less than 100 m. Then in August this group migrates back to water of more than 200 m depth. The immature group follows the more advanced squid inshore where they enter the littoral zone in August and September and then, they too, migrate back into deep water. This species has been found on the slope or shelf at similar depths (40-500 m) in other regions (Jatta, 1896; Joubin, 1896a; Dieuzeide, 1950; Adam, 1952). Morales (1958), however, found that a t Blanes (which is not far from the area studied by MangoldWirz) the species was fished all the year round from 110-400 m. Crosnier (1964) noted that off the Cameroun republic this species only frequents water below the thermocline. From the state of the adult gonads it appears that the reproductive

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period probably extends from February to October and the main hatching takes place from March to November (Mangold-Wirz, 1963b). Mangold-Wirz considers that the catch at any time can be arranged in four age groups, two which have been spawned within the year considered and two which were spawned in previous years (Fig. 12). The group arising from the earlier part of the spawning period grows

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Month FIG. 12. The size range during different months of Illex coindeti in part of the western Mediterranean sea and general conclusions concerning their growth after Wire (1963). Hatched area indicates the reproductive period and broken lines indicate tentative speculations concerning parts of the growth curves.

to maturity after about a year; the group arising from the late spawning period (and possibly slow growing young from the early spawning period) grow more slowly and do not spawn until they are about one and a half years old. A large group of females, over 25 cm in mantle length, may be survivors of the first spawning which possibly spawn a second time at an age of about 23 months. The males are ready to reproduce when their mantle length reaches

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10.0-14-0 cm while females reach this stage between 16.0-22.0 cm. Grimpe (1924) described the hectocotylization of both ventral arms and surmised that during copulation the male grasps the female round the head with the dorsal arms and her body with the lateral arms while introducing the ventral arms into her mantle cavity into which the spermatophores are passed. During this process the pair lie head to head, the dorsal side of the male, lying against the ventral side of the female’s head. The largest recorded male is 19.6 cm and the largest female 25.5 cm in mantle length (Girard, 1890b). The size of specimens taken off West Africa (Adam, 1952, Fig. 40) month by month suggests that hatching does not take place throughout the whole year and that the species migrates; the larger squid suddenly disappear from the catches in about November. As one would expect, the size is temporarily out of step with that of the Mediterranean squids of the same dimensions although an approximately similar size is finally reached. Mangold-Wirz (1963b) estimated that a female could produce from 6 000-12 000 eggs. These squids have been said to eat fish but otherwise nothing is known of the diet. Predators include Thunnus alalonga (Bouxin and Legendre, 1936) and Raja mouli (Adam, 1962). G. Todaropsis This genus contains a single species. 1. Todaropsis eblanue (Ball, 1841) Loligo eblanae Ball, 1841 Loligo sagittutu VBrany, 1861 Todaropsis Verunyi Girmd, 1889 Todaropsis veranii Nobre, 1936

This species probably lives on the continental slope occasionally coming on to the shelf (Fig. 10). It is common in the Ligurian Sea (Issel, 1931), at Nice (Vbrany, 1851), Barcelona (Lozano y Rey, 1905), Naples (Jatta, 1896; Pfeffer, 1912; Naef, 1923; Grimpe, 1926),Catalonian Sea (Mangold-Wirz, 1963b), Blanes (Morales, 1958) and the Adriatic (Gamulin-Brida, 1963). It is also common on the eastern side of the North and South Atlantic having been recorded from the North Sea and British Isles (Ball, 1841; Hoyle, 1891, 1903; Nichols, 1900; Pfeffer, 1908b; Massy, 1909; 1928a; Scott, 1926; Sparck, 1928; Gyngell, 1929; Stevenson, 1935; Hertling, 1936; Stephen, 1944; Rae et al., 1957; Rees, 1957; Rae, 1961), around the Atlantic coasts of Europe (Girard, 1889; 1890a, 1892, 1893; Chun, 1913; Joubin, 1920; Bouxin and Legendre, 1936) along the west coasts of North Africa (Robson, 1926a; Desbrosses, 1938) from Senegal, Gambia and Guinea (Adam, 1951,

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1952, 1962) and from the Cape (Robson, 1924a; Thore, 1945; VOSE, 1962e). There is also a record from Dalmatia (Kolombatavitsch, 1890 after Adam, 1952). It appears to favour temperatures of 9"-18"C (Mangold-Wirz, 196313). The species probably lives on or near to the bottom in depths of about 20-700 m. Grimpe (1925) found that it inhabited depths less than 200 m in the North Sea. Robson (1926a) found it at 20 m off Morocco. In regions where it is found, it is only occasionally taken and does not usually vary greatly thoughout the year except off the Scottish coast where large numbers have been recorded in some years (Rae, 1961). There is little evidence that seasonal migrations take place. In the Catalonian Sea egg laying appears to extend, from the sexual condition of the adults, for at least 9 months of the year (Mangold-Wirz, 1963b); mature females being present from March until November. In most collections there seems t o be little disparity between the number of males and females. Mangold-Wirz (1963b) found that males reach maturity at a mantle length of about 11-14 cm while females reach maturity a t about 16-19 cm. The largest recorded male is 13.0 cm (Girard, 1889) and the largest female is 27.0 cm in mantle length (Degner, 1925). Adam (1952) described the hectocotylization of the two ventral arms in the male. Spermatophores are deposited on the females in the receptaculum seminis at the base of the third arm. About 200 spermatophores are produced by each male and females can produce 5 000-10 000 eggs (Mangold-Wirz, 1963b). A large egg capsule is produced to judge from the nidamental glands, which become so enlarged that they are as long as the mantle (Adam, 1952). Nothing is known of the food of the species, but predators include Germo alalunga (Bouxin and Legendre, 1936) and Heptanchus (Adam, 1952). A t times the species has assumed economic importance because it has been confused with Loligo by fishermen but has proved unpalatable (Rae, 1961).

H. Todarodes Two of the better known species of squid belong to this genus. 1. Todarodes sagittatus (Lamarck, 1799) Loligo sagittatus Lamarck, 1799 Loligo todarus VBrany, 1851 Ommatostrephes sagittatus Pfeffer, 1908b

An Atlantic and Mediterranean form, this has been recorded so many times that only the more important works need be quoted

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(Fig. 13). It has been found in the Kara Sea (Kondakov, 1937), Barents Sea (Grimpe, 1925), off the Murmansk Coast in the White Sea (Herzenstein, 1885; Ostroumoff, 1896; Knipowitsch, 1901; North Cape of Norway (Lannberg, 1891), Finmark (Loven, 1846; Sars, 1878) all along the west Norwegian coast (LovBn, 1846; Sars, 1878; Ldnnberg,l891; Grieg, 1914,1933b; Nordgird, 1923), in the North Sea (Herklots, 1859; Pelseneer, 1882 ; Lameere, 1893; Hoek, 1893; Hoyle, 1902 ; Tesch, 1908 ; Pfeffer, 1912 ; Grimpe, 1925 ; Tinbergen 1928 ; Gyngell, 1929 ; Hertling, 1929; Kaas, 1939; Kaas et al., 1940), in the Kattegat and Skaggerak (LovBn, 1846 ; Posselt, 1889 ; Ldnnberg, 1891), extreme southern Baltic (Jaeckel, 1937), around the British Isles (Roper, 1883; McIntosh, 1907, 1927; Pawsey, et al., 1920; Ritchie, 1920a; Storrow, 1922; Massy, 1928a; Stevenson, 1935; Clarke and Stevenson, 1935; Stephen, 1937, 1944; Elmhirst, 1938; Gillespie, 1953; Rae et al., 1957; Rae and Lamont, 1963), Iceland (Steenstrup, 1880; Posselt, 1890b; Bardarson, 1919; Grimpe, 1925, 1933; Adam, 1939b; Fridriksson, 1943; Bruun, 1945), Faroes (Landt, 1800; Miirch, 1867; Steenstrup, 1880; Posselt, 1890; Pfeffer, 1912; Nielsen, 1930; Stephen, 1944), west coast of France (Fischer, 1867; Lafont, 1869, 1871; Joubin, 1893; Dautzenberg and Fischer, 1925; Bouxin and Legendre, 1936), Portugal (Joubin, 1920; Magaz, 1934), north Spain (Quirbs, 1922), Azores (Girard, 1890a, 1892), Madeira (Girard, 1892; Rees and Maul, 1956; Clarke, 1963), the Canaries (Clarke, unpublished), in the eastern North Atlantic well away from land (Joubin, 1895b, 1924), western Mediterranean (Cantraine, 1841; Chiaje, 1841; VBrany, 1851; Risso, 1854; TargioniTozzetti, 1869b; Brazier, 1892s; Joubin, 1893a, 1894c, 1920; Jat,ta, 1896; Bianco, 1903; Lozano y Rey, 1905; Mourgue, 1913; Quir6s, 1922; Naef, 1923; Issel, 1925b; Sparta, 1933; Magaz, 1934; Morales, 1958; Mangold-Wirz, 1963b) and the Adriatic (Stossich, 1880; Ninni, 1886; Kolombntovitsch, 1900; Gamulin-Brida, 1963). Adam (1962) erected a sub-species Todarodes sagittatus angolensis for specimens from the South Atlantic off Angola, and the Cape of Good Hope (Barnard, 1934). Korabelnikov (1959) published a photograph of a squid collected near Tristan da Cunha which appears to be this sub-species. The author has found the species in Sperm whale stomachs a t Durban (Clarke, in preparation). A record from western North America is almost certainly a misidentification (Berry, 1912d). Many specimens have been obtained after stranding (Ritchie, 1920a; Hertling, 1929; Rustad, 1952), at the surface at night (Massy, 1909) or in commercial trawls (Clarke, 1963) and one has even been taken by a diver (Segerstrhle, 1944). Almost every year large numbers appear off the south and south0.

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west coasts of Iceland in June or early July and by August enormous ehoals are often found in the fjords of the north west where they remain until November (Fridriksson, 1943). During September and October at night there are great shoals near the surface but in November they withdraw into the deeper part of the fjords. The inshore movement is thought to be in pursuit of fish and principally herring, because the stomachs contain herring scales with one to seven winter rings on them (Fridriksson, 1943). During the inshore period large numbers are stranded (Bruun, 1945). I n the Faroes the species is often found in very large numbers inshore in autumn (March, 1867). On the west Norwegian coast, where they are sometimes so numerous that the sea, has been described as “aboil” with them (Rustad, 1952), there is a, periodicity in their appearance which seems to be related to the catches of herring (Grieg, 1933b). I n most years only a few are found on Scottish coasts, but sometimes very large shoals appear and they may be stranded in thousands (Stephen, 1937; 1944; Elmhirst, 1938; Gillespie, 1953). Various theories have been advanced to account for the strandings (Ritchie, 1920a; Gillespie, 1953) but no real evidence in support of any of these has been advanced. Kaas et al. (1940)found they were more numerous in spring off the Netherlands. Mangold-Wirz (196313) found no evidence for annual migrations in the Catalonian Sea. However, in the Atlantic it enters the fishing grounds round Madeira in large numbers during March, April and May (Rees and Maul, 1956). The species comes to the surface at night but apparently prefers to stay on the bottom in daylight (Fridriksson, 1943; Mangold-Wirz, 1963b) where it is caught with trawls at depths between 70-800 m (Naef, 1923; Grieg, 193313; Adam, 1939b; Dieuzeide, 1950; Moral-, 1958 ; Mangold-Wirz, 196313) and in the Catalonian Sea it has a preference for a depth of 400-700 m. (Mangold-Wirz, 196313). Evidence from underwater photographs suggests that the species extends down to at least 1 000 m (Table 11, p. 109). It sometimes leaps to a considerable height above the water surface (Sykes, 1833; Aratara, 1954). Naef (1923) has figured a rhynchoteuthis larva purported to belong to this species. Relative growth involves no sudden changes in form. Growth in time has been examined by Fridriksson (1943) who found that, off Iceland, the mean mantle length on 1 7 July was 17.5 cm, on 3 August it was 21.8 cm, on 8 September it was 28.0 cm and on 14 October it was 31.3 cm (Fig. 18 p. 138). This gave growth increments in each 30 days of 7.6, 5.2 and 2.8 cm. He assumed that all these immature specimens

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were in their f i s t year and considered a large, mature male with a well developed gonad and mantle length of 64.0 cm taken in January, to be in a second year class. He then concluded that this species ‘‘ does not reach maturity at the end of its first year ”. The author has been able to supplement this work with observations on over 600 females and 6 males taken by commercial trawlers operating from Hull and Grimsby; the mode of the size distribution for March has been added to Fridriksson’s data in Fig. 18 and a tentative “growth” curve has been drawn in. Because the curve is so steep it seems more likely that the July specimens were hatched in the same year rather than the preceeding year, although migration may influence the slope of the curve and any conclusions must be considered preliminary. It is interesting to note the marked difference in slope between T. sagittatus and its near relative T. paci$cus which is also known to migrate between deep and shelf waters. Mangold-Wirz (1963b) found that spermatophores developed in males between 20.0-26.0 cm mantle length. Six males with mantle lengths of 30-40 cm taken off northern European fishing grounds all had spermatophores (Clarke,unpublished) as did an Icelandic specimen with a mantle length of 64.0 cm. Mangold-Wirz (1963b)found only two fully mature females having mantle lengths of 36.5 and 37.0 cm. Only two out of over 600 northern European females were in spawning condition and these had mantle lengths of 464-47.0 cm (Clarke unpublished). These figures possibly suggest that the colder water individuals mature at a large size, and it is interesting to note that beaks of specimens taken off Iceland become fully darkened at a larger size than those of specimens taken off Madeira. The extension of darkening has been related to the onset of sexual maturity (i.e. appearance of spermatophores and expansion of nidamental glands) in some ommastrephid species (Clarke, 1962b). The largest male from northern Europe, has a mantle length of 64.0 cm (Fridriksson, 1943),the largest female 49.0 cm (Clarke unpublished) and the largest unsexed specimen 76.0 cm (Herzenstein, 1885). From the Mediterranean the largest recorded male is 32.0 cm and the largest female 37.0 cm (Mangold-Wirz, 1963b). I n the Icelandic, Faroese and Norwegian populations sampled with commercial trawls, females greatly outnumber males (about 100 :1) (Clarke, unpublished) and they also outnumber them in samples taken in the Catalonian Sea (Mangold-Wirz, 1963b). Adam (1960a) has outlined the present poor state of knowledge concerning the hectocotylus of the male; a male in the British Museum (Natural History) caught at 62’40% 12’20’W has the right ventral arm hectocotylized and spermatophores at a mantle length of 17.8 cm.

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The buccal membrane of the female bears spermathecae for the reception of sperms. Lafont (1869) describes the sexual organs but the species he dealt with was probably Illex because he describes the attachment of spermatophores within the mantle, a circumstance not otherwise reported for T . sagittatus. The migrations inshore do not appear to be for spawning because a very small percentage of females taken have enlarged nidamental glands and large ovaries. I n the few that are in spawning condition the nidamental gland may reach 19.4 cm in length (43% mantle length) (Clarke,unpublished). Spawning possibly takes place on the continental slope in late winter or early spring off northern Europe and in September to November in the Catalonian Sea (Mangold-Wirz, 1963b). Off western France it is said to spawn in March and April (Lafont, 1871). In both northern Europe and the Mediterranean, mature males seem to be present all the year round while gravid females have only been found in March in northern Europe (Clarke, unpublished) and September in the Catalonian Sea (Mangold-Wirz, 1963b). Mangold-Wirz (1963b) calculated that the ripe females in her collection contained 12 000-15 000 eggs. In northern waters herring (with 1-7 scale rings) appear to be the principal food at least during the sojourn on the fishing grounds (Elmhirst, 1938; Fridriksson, 1943; Segerstrhle, 1944), but cod are also taken (Clarke, 1963). T . sagittatus has been recovered from stomachs of G e r m obesuv (Clarke unpublished), Germo alalunga (Joubin, 1895b; Bouxin and Legendre, 1936), Gadus morhua (Chun, 1913; Grieg, 1933b), Alepisaurus feroz (Rees and Maul, 1956), dolphin stomachs (Joubin, 1894c; 1895b), Sperm whale stomachs off South Africa (Clarke, in preparation) and probably off Tristan da Cunha (Korabelnikov, 1959). VBrany (1851) reported that the flesh of this species is tough, sour and unwholesome and the sale of it was at that time prohibited in Nice market. Its main value is for bait and Nesis (1964, in a footnote to a translation of Clarke, 1963) states that 9 618 tons were taken in 1968 at the Lofoten islands for this purpose; it is frozen, salted or dried and used for cod and halibut fishing. Yorkshire fishermen however consider it of no value for bait (Stevenson, 1935). Besides its largescale predation of commercial fish, it has sometimes proved a nuisance because it has competed with fish for baited hooks (March, 1867). 2. Todarodes paci$cus (Steenstrup, 1880) Nomenclature of this species has often been confused and it is known as Nototodarus paci$cus, N . sloanei and N . sloanei paci$cus,

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Ommustrephes sloanei, 0. sloanei pacijcus, or 0 .paciJicus. It is closely allied to T.sagittatus and is better kept in the same genus (Voss, 1963a). This is the common Japanese squid and its great commercial importance has resulted in considerable work on its ecology. It is found (Fig. 13) on both sides of Japan from Kiushu to Hokkaido (Steenstrup, 1880; Hoyle, 1886a; Sasaki, 1929a and many other authors), from the western side of the Inland Sea of Japan (Joubin, 1897b; Kojima, 1961), from Cape Clonard, Korea (Sasaki, 1929a) and it occurs very rarely in Sperm whale stomachs caught around the Kuril Islands (Beteshava and Akimushkin, 1955). Further south, Voss (1963a) did not find it off the Philippines so it apparently has a rather small area of distribution for such an active and prolific squid. The species was first thought to migrate from the south west to the north east in the Japan sea because the fishing season starts later towards the north, but Sasaki (1921) found no evidence for this and indeed detected differences in habit and sexual development between northern and southern populations. He later (192913) detected south-westerly movement in spring by marking 1 014 specimens. Mackinaka (1969) marked over 37 000 and got a recovery rate of 1.16%. Those tagged in summer near bays tended to move into the bay; some marked elsewhere migrated towards the coast; the majority, however, were caught near their liberation points. The mean speed of movement was 1.3 miles per day while the maximum speed found was 17 miles per day. Nishizawa (1954) considered that the fall off in catch rate of marked squids showed that migration in the Esan region was ‘‘ diffusive ” and he calculated the diffusion velocity as 1.8 miles per day. Sasaki (1929b) reported a squid which moved eight miles in two hours. Mackinaka (1959) found an intimate relationship between migration and the local currents. Suzuki (1963) studied hydrographic conditions and concluded that off Hokkaido the optimum water temperature for migration was 4°-100C. Summer is the main fishing season (Sasaki, 1929b; Nagata, 1957; Katoh, 1959) but large populations are also present in winter, and in both seasons large-scale strandings sometimes occur; in some cases these are possibly due to excitement immediately prior to copulation (Hamabe and Shimizu, 1959). The very large numbers taken may be judged from catch statistics; the Japanese total catch reached 600870 tons in 1952 and the development of the industry can be seen from catch statistics going back to before 1900 (Fig. 14 from Suzuki, 1963). As the mean body length lies somewhere about 23.0 om (Katoh, 1959) which corresponds to a weight of roughly 250 g (calculated from data on Ommastrephes caroli, a near relative) it will be seen that somewhere in the region of 24 x lo8 squids were taken in

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1952. I n 1952 this species accounted for 91.5% of the total cuttle fish and squid taken, which represented 13.4% of the total yield of all fisheries in Japan excluding the whale fishery (Suzuki, 1963). From 1952 to 1960 these percentages never fell below 84.7% and 6.3% respectively. The squid catch from Hokkaido contributes about 50% of the total squid caught in Japan (Suzuki, 1963). The catch was thought, at one time, to fluctuate in 4-year periods (Sasaki, 1929b) and Sasaki believed that there was also an 11-year period of fluctuation corresponding to the sunspot cycle, the maximum catch being at the the minimum sunspot activity; however, neither his

FIQ.14. Annual total squid and cuttlefish catches for Japan from 1895-1960 from Suzuki (1903).

data nor Suzuki's (1963) gives much support to this theory. By considering the catch per unit effort Suzuki (1963) has shown there was an alternate increase and decrease by years in the Sanriku Sea, off east Hokkaido and off south Hokkaido from 1956 to 1960. Factors influencing the catch are water temperature, salinity, rainfall and wind direction and strength (Sasaki, 192913). Wind was also found to influence fishing results for Illex illecebrosua off Newfoundland (page 122); temperature and salinity are merely indications of water masses and various authors have related variations in catch to variations in currents (Nagata, 1957; Suzuki, 1963), while off southern Hokkaido and Sanriku the relative population density of squids can be forecast from the types of streaming of the Tsugaru

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warm current; such types are recognized from the situation of visible surface boundary zones. At dusk the squids rise to within 40 m of the surface; at about midnight they sink or scatter and then rise again to the surface briefly just before dawn (Sasaki, 1921). During the day they are thought to swim at 100-200 m (Sasaki, 1921; Suzuki, 1963). Although previous workers (Sasaki, 1921) have unravelled a few

D

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n oc

oe

Otsp

F

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d’ FIG. 16. Mating of Todarodea paci$cuo from Hamabe (1962, Figs. 2 and 3 combined) A-D, stages in the approach and union of the male and female. E, diagramatic longitudinal section during the passage of spermatophores. Spermatophores (a) pafrom Needham’s sac (n)through the penis (p) end the funnel (f) to the hectocotylua (h) which deposits them near the mouth of the female. Here the spermatophorea diacharge the contained sperm bulb (sb) near the buccal membrane of the female where they are stored. The outer tunics of the spermatophores (otsp) then pass into the oral cavity (oc), down the oesophagus (oe) and into the stomach (a) where they are digested. F, aeparation of male and female.

details of the reproductive biology it is only recently that the full details of copulation, spawning, embryology and larval growth have been described (Hamabe and Shimizu, 1959 ; Hamabe, 1961a,b,c,d, 1962a,b, 1963). This big advance came from Hamabe’s success in keeping both sexes alive under fairly natural conditions within net cages in the sea and the following description is mainly based on his papers. During his observations copulation took place between 3

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males of 23-1-24-3 cm and 3 females of 254-26.7 cm (mantle length). At sunrise the squids became excited and copulation, lasting a few seconds, followed. Mating was achieved by the male interlocking arms with the female and then coming to lie underneath her (Fig. 16). Spermatophores were then transmitted to the mouth of the female from the cirrus by the male, with his hectocotylized arm (Fig. 15). When the spermatophores were in the female's mouth the sperm bulbs were discharged and the outer tunics of the spermatophores were

FIQ.16. Todarodea pacijicua. Spawning according to Hamabe (1962, Fig. 11). A, The nidamental glands (n.g.) first secrete a gelatinous substance. B, Eggs then pess out of the oviducts (od), are fertilized on the buccal membrane and are transferred t o the tips of the first and fourth arms. C, the oviducal gland (ovg) then produces a secretion into which the eggs are pushed and this is then enveloped by the nidamental secretion. D and E, diagrams showing the extent of the egg mBsaee laid by females kept in barrels 60 x 33 cm.

swallowed by the female. Shimizu (1962) found that these parts of the spermatophores remained in the stomach for a number of hours and concluded that their presence provides evidence of copulation by the female, for at least 10 h after being caught (at 10°C). Hamabe observed copulation at a surface temperature of 13"-1SoC and a chlorinity of 18-73°/0,. Most pairing is thought to take place from summer to winter (Sasaki, 1921). Spawning commences after a fairly brief interval (the duration apparently has not been noted). The very voluminous egg mass of about 25 litres (calculated from Hamabe, 1962b), contains 300 to 4 000

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MALCOLM R. CLARKE

ova buried in a slightly viscous, buoyant, oviducal secretion which is enveloped in a thick capsule of a viscous, albuminous, nidamental gland secretion. The egg mass is probably normally deposited on the sea floor in cavities, to judge from the habits of the captive animals. Hamabe found that spawning took place a t 15"-20"C and at a chlorinity of 19~0P19~08°/00. The spawning process is thought to start by a discharge of a mass of nidamental gland secretion alongside the arms (Fig. 16). The eggs are passed to the buccal membrane where they are fertilized and then transferred to the tips of the first and fourth arms. An oviducal secretion is then discharged and the fertilized eggs are pushed into it. Further nidamental secretion covers the egg mass and as it is denser than sea water it settles on the substratum. The whole process probably takes about two hours. Hamabe (1963) has shown that, after copulation and spawning, degeneration of body organs takes place. This led him to conclude that females probably die after spawning and sink to the sea floor, because similar changes occur in Sepia esculenta whose buoyant condition after death makes the mortality at spawnhg evident at the sea surface. The elliptical or semi-spherical eggs measure 0.7-0.8 mm in greatest diameter and are telolecithal. A partial cleavage takes place, and 12 h after spawning the blastoderm extends beyond the equator, and by 24 h the germ layer extends almost over the entire surface of the egg; by this time the shell and mantle rudiments develop at the animal pole. Development proceeds and at 40-60 h a number of granules are discharged from the embryo into the perivitelline space and the embryo then rotates. The rotation slows down, the embryo adheres to the egg membrane, Hoyle's organ secretes a membrane-softening agent and hatching takes place about 102-113 h after spawning. The newly hatched larvae measure 0.7P1.02 mm long (Fig. 17). In the sea hatching took place during May and, in the aquarium, the larvae lived up to 54 h at 15O-18"C and a chlorinity of 19~07-19~330/00. The very young larvae were unable to swim clear of the bottom. At a length of 3.0-15.0 mm the larva has the typical " rhynchoteuthis " form with fused tentacles forming a " rostrum " (Fig. 17) and after at least 2 weeks the tentacles separate. No prerhynchoteuthis stage described by Hayashi and Iszuka (1953) was found by Hamabe (1962a) or Okiyama (196513). Okiyama (1965b) has found eggs in plankton hauls and suggests that, whilst they are normally spawned on the bottom, they can become small floating masses secondarily. Both eggs and larvae increased in abundance with depth down to 50 m in the daytime suggesting their

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abundance may be greater below that depth. Both eggs and larvae have very wide tolerances to temperature and salinity. Post-larval growth involves no sudden changes in body proportions. Growth was studied by Sasaki (1921) but his work was based on very few specimens. Katoh’s (1959) data over the rather limited fishing season suggest that there are two and possibly three year groups. The great majority are less than 30 cm in mantle length and means for the months August t o January are given for both males and females.

0.1

cm

0094

03 OG2 I02 1-55 cm FIQ. 17. T o d a ~ o d m p a c i j c w . Stages in growth to the late rhynchoteuthis after Hamabe (1962, Fig. 16, Plate 111). Side (upper row) or ventral view. Mantle lengths in cm are indicated.

These individuals are thought to have hatched in the previous autumn (Fig. 18). The growth rate suggested by the means drops in the last 3 months of the season, possibly because of mortality after spawning. Large individuals, 30-40 cm (most if not all are females), may be survivors from the first spawning which are in their second year. A very large specimen of about 50 cm mantle length may be in its third year. Curves for the two sexes are very similar but females are very slightly the larger (Katoh, 1959). Katoh (1959) also found a difference in growth curves in different years. He showed that the female becomes

138

MALCOLM R. CLARKE

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sexually mature a t 20.0-25.0 cm (mantle length). I n the male the hectocotylus appears at 17.6-19.0 cm (mantle length) (Sasaki, 1921). The largest female known to the author has a mantle length of 49.3 cm (Katoh, 1959). The sex ratio a t different sizes and seasons varies considerably (Katoh, 1959). Tauti (1941) calculated the survival rate as 0.67. The main foods are Maurolicus muelleri japonicw in coastal regions and Parathemisto (Parathemisto)japonica in offshore regions (Okiyama, 1965). Larval and young stages of Todarodes pacijcus are an important part of the diet (Okutani, 1962; Okiyama, 1965). A t Ito, Okutani (1962) found that 37% of squids (291) had empty stomachs and 80% of them with food contained less than 1% of the body weight. He found no seasonal differences. One squid contained food weighing over one-sixth of the body weight. Fifty per cent of those with food contained fish, 9% contained crustacea and 7% contained molluscs (as the principal food?). The fish were myctophids and Engraulis japonica (anchovies). Crustacea included megalopa larvae of brachyuran decapods, amphipods, copepods including Calanus darwini and Euchirella sp. and Cypris larvae. Other food items included Xagitta sp., Tomopteris pacijca and a gastropod larva (Tonna). The peak period in feeding occurs at about sunset when the deep scattering layer arrives at the surface (Okiyama, 1965). Predators of the species include Raja (Sasaki, 1920), Coryphaena hippurus (Kojima, 1961), Balaen whales (Nemoto, 1957) and the Northern fur seal (Wilke and Kenyon, 1954). The great economic importance of this species has been touched on above.

I . Nototodarus The species of this Pacific Ocean genus have been confused with one another and with Todarodes pacificus in the literature. Nototodarus is distinguished by having males with both ventral arms hectocotylized. Voss (1963a) considers that the four forms within the genus are really FIG. 18. Tentative growth curves of Todarodes aagittaluefrom Icelandic and Norwegian waters (upper graph) and T . paci$cus. T . sagittatus is derived from sample means published by Fridriksson (1943) with the exception of the point for March which represents the mode of a large sample (over 600) caught in commercial trawls and measured by the author. T . paci$cus is derived from Katoh (1969). The means are based on very large commercial catches and the apparent drop from the possible growth curve in November and December is probably cauaed by mortalities after spawning. Very tentative parts of the curves are shown with broken lines. In T.aagitbtw, the period of spawning (broken arrows) is only known from very few specimens. In T.pacijicua spawning is thought to take place mainly in the Autumn (hatched).

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geographical sub-species of Nototodarus sloani and form a cline from New Zealand to Hawaii via Australia and the Philippines. 1. Nototodarus sloani sloani (Gray, 1849)

This has been recorded from various localities all round New Zealand (Gray, 1849; Hutton, 1882; Suter, 1913; Powell, 1946; Dell, 1952). There are few measurements given in the literature but the largest recorded male is 27.5 cm and the largest female is 35.6 cm in mantle length (Dell, 1952). 2. Nototodarus sloani gouldi (McCoy, 1888) The Australian sub-species has been recorded from West Australia (Berry, 1918), the Great Australian Bight (Berry, 1918; Cotton, 1960), around Tasmania (Berry, 1918; Cotton, 1942; Allan, 1945) and off Victoria and New South Wales (McCoy, 1888; Brazier, 189213; Cotton, 1942; Anon, 1964a). The adults are plentiful in all these regions (Allan, 1945). They have been taken by dipnets (Cotton, 1942) at the surface and between 100-1 130 m with open nets (Berry, 1918). A number of rhynchoteuthis larvae have been taken over the continental slope and in shallow water off eastern Australia, and Allan (1945) considered they must belong to this species, The largest had a total length of 8.0 mm. They were taken in 7 months throughout the year so there is no evidence of a limited spawning season. The males have both ventral arms hectocotylized and these are sufficiently developed to form a clasping organ (Berry, 1918) but there is no evidence for any function other than the transmission of spermatophores. The largest specimen recorded was stranded and in poor condition but was estimated at over 4 ft in total length (Cotton, 1960). The species has been taken from the stomach of a Bluefin tuna (Allan, 1945), Thunnus maccoyii and Thunnus gerrno (Cotton, 1942). An industry has developed in Victoria where, together with two other cephalopods, a total annual catch amounts to 300 000 lb. (Anon, 1964a). 3. Nototodarus sloani philippinensis Voss, 1962a This sub-species has been recorded from East Luzon and Jolo Island in the Philippines (Voss, 1962a). The two known specimens were taken at 565 m and 294 m, were both female and had mantle lengths of 18.0 cm and 10.1 cm respectively. The water temperature was 45.3'F, (7.2"C) (?bottom temperature) and the bottom was green mud.

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4. Nototodarus sloani hawaiiensis Berry, 1912

This is the Hawaiian representative of the cline described by Voss (1963s). It has been taken at Hawaii and the Midway Islands (Berry, 1912c, 1914a) at depths between 400-570 m with open nets. The largest has a mantle length of 14.7 cm (Berry, 1914a).

J. Rhynchoteuthis larvae Although small larvae with the tentacles fused together had previously been described, Chun (1903, 1910a) was the first worker to recognize them as young ommastrephids and to apply the name Rhynchoteuthis. The thirty-five specimens taken from the Atlantic and Indian oceans by the Valdivia were of two types, one slender with average sized eyes (Fig. 7 G , H, I) and the other plump with large eyes having a clearly defined pit-like area like a fovea (J, K, L). Because of the wide area from which these larvae were collected and the several ommastrephid species present it seems rather doubtful if these two “types” are in reality only two species. Other Rhynchoteuthis larvae have been described since, but few have been identified to species and these few are dealt with above in the relevant sections. IV. ONYCHOTEUTHIDAE A. Onychoteuthis 1. Onychoteuthis banksi (Leach, 1817) A large number of onychoteuthids have been reduced to synonyms of this species by various authors and they will not be given here (see Naef, 1923; Adam, 1952). Widespread in warm waters (Fig. 19), this species has been recorded from the North Atlantic and adjacent seas (LovBn, 1846; Rose, 1853; d’orbigny, 1853; Sars, 1878; Dautzenberg, 1889; Posselt, 1890; Girard, 1890a; Norman, 1890; Lonnberg, 1891; Joubin, 1893a; 1920, 1924; Hoyle, 1904b; Murray and Hjort, 1912; Pfeffer, 1912; Massy, 1916a, 1928a;Degner, 1925; Grimpe, 1925; Boone, 1933; Bouxin and Legendre, 1936; Jaeckel, 1937; Baines, 1938; Bruun, 1945; Rees, 1949; Adam, 1960c; Voss, 1955; 1956a,b, 1960a; Rees and Maul, 1956),the Mediterranean (Pfeffer, 1912; Issel, 1920b; Naef, 1923; Degner, 1925; Rees, 1949), the South Atlantic (Pfeffer, 1912; Odhner, 1923), the Indian Ocean (Pfeffer, 1912; Rees, 1949), the East Indies (Pfeffer, 1912), Philippines (Pfeffer, 1912; Elera, 1896; Boone, 1938; Voss, 1963a), Formosa (Pfeffer, 1912; Sasaki, 1916, 1929a), east Australia (Gould, 1852; Brazier, 1892b; Cotton and Godfrey, 1940; Allan, 1945), New

142 MALCOLM R. CLARKE

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Zealand (Gray, 1849; Suter, 1913; Dell, 1952), Kermadec Islands (Berry, 1914c), New Caledonia (Brazier, 1892a), Japan (Okada, 1927; Sasaki, 1929a), Hawaii (Berry, 1914a), Kuril Islands (Beteshava and Akimushkin, 1955), Bering Sea (Middendorf, 1849; Sam, 1878), British Columbia (Gabb, 1862a; Clarke, 1962b), Oregon (Pearcy, 1966), CaNornia (Carpenter, 1864; Da11, 2872; Phffer, 1922; Rice, 2963), west Mexico (Boone, 1928b), South America (Dall, 1910; Pfeffer, 1912), the central Pacific (Hoyle, 1904b) and the Antarctic (Korabelnikov, 1959). Little geographical variation has been found although Okada (1927) considered that the Japanese form should be separated as 0. borealisjuponicus. Although adults are not usually caught in large numbers, at times they are, and they may then be of commercial importance for food (Sasaki, 1929a). The species has often been caught at the surface particularly at night (e.g. Adam, 1952 ; Voss, 1963a) when it may be seen as a dark shape with a pale blue light issuing from the photophores in the mantle cavity. At night it sometimes jumps aboard vessels and is regarded as one of the “flying squids” (Brazier, 1892a; Massy, 1916c; Boone, 1933; Rees, 1949). Although it has been caught in open nets fished to as much as 4 000 m (Adam, 1960c) the available evidence suggests that it lives much nearer the surface. Degner (1925) found that, of the small individuals (up to 1.45 cm), 71.9%, representing 5.3 per haul, were at less than 30 m (65 m wire out), 18.5%, representing 2 per haul were from 30-150 m (65-300 m of wire out) and only 8.6%, representing 1.4 per haul, were deeper than 150 m (>300 m of wire out). Degner (1925) found evidence that shoals of young individuals are composed of similarly sized squids and he found as many as 28 of the same size in a single net haul. During growth the arms become relatively shorter and then longer, the head also becomes shorter and then longer, the body becomes relatively much narrower and the fms become relatively longer (Fig. 20). The larvae have a white patch under each eye and two pearl-like light organs in the mantle cavity are clearly visible through the mantle wall. I n the North Atlantic, size frequency histograms of young animals taken in the summer and in the winter are very similar (derived from data of Degner 1925 and Bouxin and Legendre, 1936) and this suggests that hatching takes place all year round; a view also supported by the occurrence of larvae less than 1.0 cm in the North Atlantic in February and May to October; (Joubin, 1920; Bouxin and Legendre, 1936; Voss, 1958, 1960a). Comparison of Degner’s with Bouxin and Legendre’s data provides an interesting reminder of the inadequacy of our sampling

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MALCOLM R. OLARKE

0.33

B

FIG. 20. Change in form during the growth of Onychoteuthia bankai (A) after Pfeffer (1912, Plate 3, Fig. 21, 13, 16; Plate 6, Fig. 1 ) and Naef (1923, Fig. 156, 163), Onychia carribaea (B)after Pfeffer (1912, Plate 1, Fig. 24 and 6) and Anciatroteuthia lichtemteinei (C) after Naef (1923, Fig. 169, 160) and Pfeffer (1912, Plate 9). Mantle lengths in cm are indicated. Onychia carribaea from the dorsal side; the rest from the ventral side.

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methods; while size histograms derived from net hauls (Degner, 1925) have a mode of 6.0-8-0 cm in July and 4.0-5.0 cm in August, those derived from tuna stomachs in the same two months have modes of 1-0-2.0 cm and 2.0-3.0 cm respectively. These were, however, in different years although the general geographical region was the same. The largest recorded male is 8.1 cm (Voss, 1956b), the largest female is 28.3 cm (Sasaki, 1916) and the largest unsexed specimen is 29.0 cm (Sasaki, 1929a) in mantle length. A female of 10.8 cm (mantle length) is described as almost adult (Naef, 1923) and one of 14.0 cm had nidamental glands 2.3x0.7 cm so that, it too was probably nearing sexual maturity. No arm is specially modified to form a hectocotylus and the sexes cannot be distinguished by external appearance. Adam (1960~)reported that the spermatophores in his largest male were 23.5% of the mantle in length. The bite of this squid is toxic and resembles a wasp sting in its effect (Clarke unpublished); this fact and the large hooks on the tentacle suggest that active and possibly large prey are taken. The species is important in the diet of Germ0 alalunga (Bouxin and Legendre, 1936) and has been recovered from stomachs of ling (Dell, 1952),Alepisaurus ferox (Rees and Maul, 1956),Gadus m r h u a (Jaeckel, 1958), Sperm whales (Beteshava and Akimushkin, 1956; Rice, 1963), Bottlenose whales (Rice, 1963-possibly Moroteuthis) the White whale (Heptner, 1930) and the Laysan Albatross (Berry, 1914a). It is dried and sold commercially for human consumption at times in Japan (Sasaki, 1929a). B. Moroteuthis 1. Moroteuthis aequatorialis Thiele, 1921 This species is only known from the type specimen found dead near the surface at 0'16" 18'7'W (Fig. 21). It is a large squid having a dorsal mantle length of 40-0 cm. 2. Moroteuthis ingens (Smith, 1881) Onychoteuthis ingens Smith 1881 Although few specimens seem to have reached museums this species is by no means uncommon in Antarctic waters (Fig. 21) and forms a principal part of the diet of Sperm whales (Clarke, R. 1956; Clark, M. R., unpublished notes). Its distribution extends from Patagonia (Smith, 1881; Pfeffer, 1912), the S. Orkneys (Hoyle, 1912) and a doubtful record from New Zealand (Massy, 1916c) to high southern latitudes (Discovery collections). As all the specimens known have been

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MALCOLM R. CLARKE

. PB

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either stranded (LGnnberg, 1898b) or removed from the stomach of predators the depth at which they live is not known. However, its occurrence in the stomach of a Ross Seal (Hoyle, 1912) suggests that it occurs at less than 200 m (King, 1964). It grows up to 47-6 cm (Pfeffer, 1912) and even 94.0 cm (Discovery collections) in mantle length. The beaks of these squids show distinct growth " rings " which are arranged in cycles according to their width and efforts have been made to relate these cycles to annual growth (Clarke, 1965b and see page 258). The male does not have an arm modified as a hectocotylus. The well-developed musculature of this species suggests that it is a very active swimmer. 3. Moroteuthis Zonnbergii Ishikawa and Wakiya, 1914 This is known from Sagami Bay, Japan (Ishikawa and Wakiya, 1914 ; Sasaki, 1929a). Besides a specimen that was stranded it has been taken at about 730-920 m with open nets. Although frequently caught it is not of economic importance (Sasaki, 1929a). The largest individual recorded has a mantle length of 27.5 cm.

4. Moroteuthis robsoni Adam, 1962 First described from South Africa (Robson, 1924a) as Moroteuthis sp. A, this was later collected at 16'35.6'5 11'19.5'E and was then given a specific name (Adam, 1962). It is an important part of the diet of Sperm whales taken near Durban (Clarke, in preparation). The species has been caught at 250 m (Robson, 1924a) and between 485 and 550 m (Adam, 1962) with open nets. The largest specimen has a mantle length of 47.0 cm. 5 . Moroteuthis robusta (Verrill, 1876)

Onychoteuthis robusta Verrill, 1876 Lestoteuthis robustu Verrill, 1880 Ancistroteuthis robustu Steenstrup, 1882 This species is confined to the North Pacific (Fig. 21) and within this region it is not uncommon in the boreal seas of the asiatic side of the N. Pacific (Sasaki, 1929a) and at times off California (Smith, 1963). It has been reported from Unalaska (Verrill, 1876; Thompson, 1900), south of the Strait of Tsugaru, Japan (Ishikawa and Wakiya, 1914), Hokkaido (Sasaki, 1929a), Aleutian Islands (Okutani and Nemoto, 1964), the Kuril region, particularly the southern end (Beteshava and Akimushkin, 1955), off British Columbia (Robbins, et d., 1937; Pike, 1950), off Oregon (Hyning and Magill, 1964; Pearcy, 1965) and off California (Classic, 1929, 1949; Phillips, 1933, 1961; Croker, 1934;

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MALUOLM R. CLAREE

Smith, 1963). A large squid identified from a description as this species was seen off south India (Baccialon, 1919). Some specimens were obtained after becoming stranded (Verrill, 1876; Thompson, 1900; Sasaki, 1929a; Smith, 1963). Many others were collected from the stomachs of Sperm whales (Pike, 1960; Okutani and Nemoto, 19641, while some have been caught with nets (Sasaki, 1929a; smith, 1963; Pearcy, 1965) and one specimen was taken by a Scuba diver (Phillips, 1961). From the evidence of captures with open nets it appears that the species occurs near the bottom at about 350-550 m off California (Phillips, 1961; Smith, 1963) and may extend to near the surface as suggested by the diver’s capture, strandings and by its capture in a fixed net (Sasaki, 1929a). Its occurrence in Sperm whales’ stomachs near the Aleutian Islands was accompanied by stones so that the whales had apparently been feeding on the bottom at least at some time. These are large squids, the largest recorded having a mantle length of over 2 m (91.5 in, Verrill, 1876). The ovary may be up to 2 5 . 0 ~ 2 0 - 0 ~ 1 4 cm . 0 in size and the nidamental gland 40.0 x 8.0 cm. which suggests that a very large egg mass is laid (Sasaki, 1929a). Ova measure 1.0 x 0.76 mm. No hectocotylus has been described. The food of Californian specimens was found to include Velella velella, a surface form, and Brisaster townsendi, a bottom living heart urchin (Smith, 1963). They are important in the diet of Sperm whales (Pike, 1960; Beteshava and Akimushkin, 1955; Okutani and Nemoto, 1964). Attempts to prepare them for food in California failed because they proved unpalatable (Smith, 1963).

C . Ancistroteuthis 1 . Ancistroteuthis lichtensteini (d’orbigny, 1839) Onychoteuthis Lichtensteinii (d’orbigny, 1839)

A rare species of the Western Mediterranean recorded from Nice (d’orbigny, 1835-48, 1845; Vbrany, 1851; Risso, 1854; TargioniTozzetti, 1869; Joubin, 1893a; Pfeffer, 1912), off the Spanish coast (Lozano e Rey, 1905; Hidalgo, 1916; Morales, 1958, 1962), off Corsica (Joubin, 1900), off Naples (Naef, 1923; Jatta, 1896*; Targioni-Tozzetti, 1869), Capri (Jatta, 1896*), Messina (Targioni-Tozzetti, 1869; Pfeffer, 1912; Troschel, 1857), Ischia (Jatta, 1896*), Genoa (Targioni-Tozzetti, 1869) and off Algeria (Aucapitaine, 1863). Outside the Mediterranean, * Some of the text and figures refer to Onychoteuthis banksi aa pointed out by Pfeffer, 1912.

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it has been recorded from the Gulf of Mexico (Voss, 1956b) but Adam (1962) considers that this needs confirmation and from 11"s 14'E off West Africa (Adam, 1962). Adam (1962) described some geographical varieties. It has been taken at the surface (Voss, 195613) and in an open net fished to as much as 570 m (Morales, 1962). During growth the arms remain about the same size relative to the mantle length, the tentacles become relatively longer, the head relatively shorter, the body relatively narrower and the fin relatively longer (Fig. 20, C). The largest specimen known to the author has a mantle length of 20.0 cm (Joubin, 1894~). According to Risso (1854 after Adam, 1942b) it inhabits gravel regions in spring and summer at Nice and spawns in summer. It has been taken from the stomach of a dolphin (Joubin, 1894c, 1900).

D . Chaunoteuthia 1. Chaunoteuthis mollis Appellof, 1890

A very rare species known from the Mediterranean (Appellof, 1890; Grimpe, 1921a; Naef, 1923),the north east Atlantic (Lonnberg, 1896b; Joubin, 1920) and off Lagos (Pfeffer, 1912). Several have been found dead at the surface and a young one was taken at about 150 m (Naef, 1923). The specimens measure up to 17.15 cm in mantle length and those which have been sexed (including the largest) are females. Specimens described by Appellof, Lbnnberg, and Grimpe have a row of spermatophores stuck into the mantle running back from the mantle connectives on either side. A young specimen, 1.25 cm in mantle length was described by Naef (1923).

E. Onychia A large number of species have been referred to this genus but the great majority should be synonymized with Onychia curribaea Lesueur, 1821. The few specimens which are possibly separable are insufficiently known and will not be treated here. The genus may prove to be monotypic when more specimens can be examined. 1. Onychia carribaea Lesueur, 1821 Loligo laticeps Owen, 1836 Ornmastrephes laticeps d'orbigny, 1836-1848 Onychiu cardioptera Gray, 1849 Loligo plagioptera Eydoux and Souleyet, 1852

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Onychia binotutu Pfeffer, 1884 Steemtrupiola atlantim Pfeffer, 1884 Teleoteuthis (Onychia) agilis Verrill, 1885s (re-examinedby VOS5, 1956b) Teleoteuthis Jattae Joubin, 1900 Cranchia cardioptera d'orbigny, 1926 after d'Orbigny 1835-1848

Specimens which are very probably this species have been taken in the Gulf of Mexico (Lesueur, 1821; Voss, 1966b),Florida (Voss, 1966a), Chesapeake Bay (Verrill, 1885a), the North Atlantic as far north as 47" North (Girard, 189213; Joubin, 1895b, 1900; Hoyle, 1906; Pfeffer, 1912; Thiele, 1921), between St. Thomas and Bermuda (Hoyle, 1886a), and Jatta (1896) recorded it from the Mediterranean but Pfeffer (1912) considered that the specimen referred to was possibly a young Abralia and Hoyle (1906) considered that this locality needed confirmation. In the South Atlantic it has been taken as far south as 38"s(Pfeffer, 1912) and South Africa (Voss, 1962e). Possible records extend much further afield (Fig. 22) and include Zanzibar, Bengal, N. Celebes, Wytotake (Lagos Is.) and the South Sea (Pfeffer, 1912). A record from the North Pacific (Hoyle, 1886a) was only doubtfully assigned to the species. Thus, the distribution pretty definitely includes a large part of the Atlantic but records elsewhere are, to some extent, doubtful. Nearly all the specimens have been taken a t or near the surface; on the few occasions they have been taken in nets lowered to any great depth these were non-closing nets which probably caught them near the surface. They have sometimes been taken in hand nets during the day from Discovery I I in the North Atlantic and are the only species of pelagic squid the adults of which are normally caught at the surface during daylight hours. I n life they have a general blue appearance and the dorsal chromatophores are almost black, making them very inconspicuous from above. I n preservative such as formal saline the blue colouration is lost. Although several have been caught in the course of a few minutes, no shoaling behaviour has been observed by the author. During growth the arms and tentacles and head become relatively longer, the body becomes relatively narrower and the fins become relatively longer (Fig. 20, B). Adults are small, the largest recorded specimen having a mantle length of 3.6 cm. (The type specimen was erroneously given as 4.6 cm but this was corrected by Pfeffer, 1912; Verrill's (1885a) specimen was given as 4.6 cm in the description but 3.0 cm in the Plate). None of the arms have been shown to be modified as a hectocotylus.

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F. Tetronychoteuthis 1. Tetronychoteuthis dussumieri d'Orbigny, 1839

This species is very rare in collections and has only been recovered from the stomachs of predators. It has been recorded north of Mauritius (d'orbigny, 1835-1848, 1845), south of Australia at 46's 120"E (Pfeffer, 1912), the Azores (R. Clarke, 1956), Madeira (Rees and Maul, 1956) and the north-west Atlantic at 46'41" 47'16'W (Rees and Clarke, 1963). Of these specimens, two were from dolphin stomachs (d'orbigny, 1835-1848; Pfeffer, 1912), several were from Sperm whale stomachs (R. Clarke, 1956; Rees and Maul, 1956) and five were from redfish (Sebastes mentelh) stomachs (Rees and Clarke, 1963). The author has a number of specimens from stomachs of Sperm whales taken off Saldanha Bay and Durban, South Africa. Robson ( 1 9 2 6 ~ )recorded fragments of Tetronychoteuthis sp. off Cape Town. Rees and Maul (1956) considered that this species belongs to the bathypelagic slope fauna living close to the bottom in the 200-2 000 m depth range. It can reach a mantle length of 72.0 cm (R. Clarke, 1956). Another species of the genus T . massyae (Pfeffer, 1912) is probably based on the young of T . dussumieri. Pfeffer described this from a specimen taken at 48"N 15'W in the North Atlantic and Allan (1945) also placed another small specimen taken off Australia at 42'40'5 148'16'E in T. massyae.

V. GONATIDAE A. Gonatus 1. Gonutus fabricii (Lichtenstein, 1818) A widely distributed species (Fig, 23) from the colder regions of the North Atlantic and North Pacific, G . fabricii is quite distinct from all other species except G. antarcticus which is often considered a southern variety of G . fabricii. It has been recorded from various positions in the Davis Strait (Fabricius, 1780; Lichtenstein, 1818; Msller, 1842; Prosch, 1849; Mdrch, 1857, 1877; Steenstrup, 1880; Posselt, 1898; Pfeffer, 1912; Grimpe, 1927; Brock in Hjort and Ruud, 1929; Muus, 1962; Nesis, 1965). South of Nova Scotia it is less frequently found, but it has been recorded off Newfoundland (Frost and Thompson, 1932, 1933, 1934) and farther south (Chun, 1913; Joubin, 1924) as far as 100 miles south of Rhode Island (Verrill, 1881a). It extends across the high Northern Atlantic (Hoyle, 1886a; Chun, 1913; Grieg, 1922) to Iceland (Mdrch, 1868; Steenstrup, 1880; Collett, 1912; Murray and Kjort, 1912; Bardarson, 1919; Bruun, 1946), Jan Mayen (Appelldf,

1

.

.

I-

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1893, Friele and Grieg, 1901), the Faroes (Mdrch, 1867, 1868; Russell, 1922), Spitzbergen (Soot-Ryen, 1925), into the Barents Sea (Grimpe, 1933) and off the Norwegian Coast (Sars, 1878; Ldnnberg, 1891; Pfeffer, 1908b; Murray and Hjort, 1912; Grieg, 1933a,b; Nesis, 1965). On the European side of the North Atlantic it is found on the western side of the British Isles (Massy, 1907, 1909, 1913, 1928a; Degner, 1925; Grimpe, 1927) and in the Bay of Biscay (Joubin and Roule, 1918; Degner, 1925). There are records from the Mediterranean at Toulon (Joubin, 1893a) and Nice (Steenstrup, 1880; Joubin, 1893s) but Carus (1890) questioned the identity of some of these. Later it was recorded in the eastern Mediterranean (Degner, 1925) but the specimen in question was the smallest in Degner's collection, with a mantle length of only 0.5 cm and at this size a misidentification seems quite possible; its presence in the Mediterranean needs confirnation. I n the Pacific it is found in the Bering Sea (Dall, 1884, 1886, 1899; Sasaki, 1929a) near the Commander Islands (Sasaki, 19298) and the Aleutians (Sasaki, 1929a);in the western North Pacific it occurs to the east of Kamtschatka and in the Okhotsk Sea (Middendorff, 1849; Sasaki, 1920, 1929a) off the Kuril Islands (Beteshava and Akimushkin, 1955; Akimushkin, 1956a) and off North Japan (Steenstrup, 1881, 1882; Sasaki, 1916, 1929a). To the east of the Aleutians it occurs in the Gulf of Alaska (Sasaki, 1929a; Okutani and Nemoto, 1964), off British Columbia (Pike, 1950; Schubert, 1955) off Oregon (Pearcy, 1965) and south to California (Berry, 1912d; Rice, 1963). Thus, although there are no records from the Arctic basin and Nesis (1966) found no evidence for their presence farther east than the western limit of the Barents Sea; the high latitude records in the Norwegian Sea and the Davis Strait suggest that the distribution is possibly continuous between the Pacific and Atlantic. All but the Mediterranean records lie to the north of the 19°C August isotherm. Nesis (1965)found that young stages were present in water at 0.1-7.36"C and that they were most numerous in water a t 5-7°C. No larvae have beep found in Baffin Bay (Muus, 1962) and there are few in the cold waters of West Greenland compared with the central Labrador region (Nesis, 1966). I n the Norwegian Sea, Nesis (1965) recorded it from 10% of hauls compared with 66% of hauls off Greenland. Larvae are abundant in the upper layers (Muus, 1962; Pearcy, 1965) and, in considering young between 0-6-8.0 cm in mantle length, Degner (1925) found that 36%, representing 3 per haul, were caught at less than 30 m (65 m of wire out), 69% representing 6 per haul at 30160 m (65-300 m of wire out) and only 6% representing 1 per haul a t more than 160 m (more than 300 m of wire out). Grimpe (1933) believed

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that young stages occur nearer the surface in high latitudes although, in the Norwegian Sea, larvae were found at a mean depth of 300 m and rarely at 0-50 m (Nesis, 1965). There is some evidence that smaller juveniles live nearer the surface (Nesis, 1965). Off Oregon, Pearcy (1965) found that an average of 0.5 squids per hour were caught in open midwater trawls fished at 200 m and 600 m, while only 0.1 per hour were caught in an open trawl fished a t 1000 m. He aIso found evidence that young squid moved down in daytime and up into the upper 200 m at night. Adults have been taken with open nets fished to 100 m and to as much as 4 000 m and have been recovered inshore (Bruun, 1946) although their usual habitat is probably at 100 to 1000 m over deep water. Hoyle (1886a) records an adult which " flew " on board a vessel. While Muus (1962) believed that there wae a short spawning period in the Greenland region; Nesis (1965) found evidence for spawning from mid-April to December with a peak period in late May and June. By combining the data of Muus (1962) and Nesis (1965) it appears that the very young juveniles of less than 1.0 cm mantle length present in May and June grow to 14-3-0 cm by July and 2-0-4.0 cm by August and September. I n September there are also animals of 8.0-20-0 cm in mantle length which were presumably spawned the previous year. From his rather sparse data Muus concluded that there is probably a 2-year development period and a large specimen of 24.0 cm was thought to be possibly 3 years old. What figures are given, however, do not exclude a 1-year development. In the Norwegian Sea the main hatching period is from late March to June or July (Nesis, 1965). Spawning seems to take place over great depths and the adults occupy the same geographical area as the young and this led Nesis (1965) to conclude that there is no spawning migration. However, in spring and summer large numbers of adults migrate into the Norwegian Sea from the Atlantic (Grimpe, 1933; MUUS,1962) and it seems possible that this is related to spawning. Off Oregon, about eight times more larvae were caught over the continental slope in summer than in winter and Pearcy (1965)suggested that this was due to an influx of squid into the region, a view supported by the size distributions of the larvae. Pearcy further concluded that hatching of Qonatus fabricii is probably not limited to a short season; however, if migration takes place, growth as shown by distribution curves may be obscured. During growth, the arms and tentacles become relatively longer and then shorter, the head becomes relatively shorter, the body becomes narrower and the fins become relatively longer (Fig. 24). Degner (1925) has described the development of hooks on the tentacle club. The

156 MALCOLM R . CLARKE

fro. 24. Change in form during growth of Gondw,fabricii after Saaaki (1929. Plate 22; Figs. 17, 16 and 14). Naef (1923, Fig. 116) and Steenatrup (1881-1882, Plate 1, Fig. 1). All from the d o r d aide. Mantle length in o m are indicated.

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largest recorded specimen has a mantle length of 30.0 cm (Okutani and Nemoto, 1964). Nesis (1965) in a detailed study of the food of the juveniles found that 49% of stomachs were empty. Copepods were present in 56% of stomachs containing food and represented 40% of the food organisms; euphausids were present in 35% of stomachs and represented 55% of the organisms; amphipods, pteropods and chaetognaths together were present in 9% of stomachs and represented 5% of the organisms. Up to three species were present in a single stomach. The food species identified were Calanus jinmarchicus, C. hyperboreus, Pareuchaeta norvegica, Metridia sp., Thysanoessa longicaudata (up to 10 in a stomach), Hyperia galba, Pseudalibrotus sp., Limacina retroversa and Sagitta maxima. The smallest squid feed on euphausid and Calanus young while the larger squid juveniles eat adult copepods, amphipods and Sagitta. While the young feed on animals much smaller than themselves, once the hooks have developed (at a mantle length of 2-5 cm) fish form an important part of the diet and the adults can feed on animals larger than themselves. There is no doubt that G. fabricii is a very important food organism being the squid of the '' Bottle nose grounds '' in the Norwegian Sea (Murray and Hjort, 1912) and the main food of the Bottlenose whale in the Atlantic (Hjort and Ruud, 1929); it has also been recovered from this whale off California (Rice, 1963) and is a very important part of the diet of Sperm whales of the Pacific (Pike, 1950; Akimushkin, 1955; Beteshava and Akimushkin, 1955; Schubert, 1955)and off Iceland (Collett, 1912). Schools of Hyperoodon ampullatus and Monodon monoceros pursue the adult squid into the Norwegian Sea from the Atlantic (Grimpe, 1933). It has been taken from Cystophora cristata (Lonnberg, 1898a) and Dall (1899) found it second only in importance to pollack in food of the northern fur seal (see also Lucas, 1899; Fiscus et al., 1965). It has been recovered from unidentified fish (Verrill, 1881a), is abundant in stomachs of coalfish (Sars, 1878), cod (Verrill, 1880b; Grieg, 1933a), tuna (Joubin and Roule, 1918), Sebastes marinus (Grieg, 1933a; Nesis, 1965), Somniosus microcephalus (Soot-Ryen, 1925), Gadus aeglejinus, G. virens, and G. morhua (Grieg, 1933a). It has also been recovered from the stomach of a gull (Sasaki, 1929a) and Fulmarus glacialis (Grieg, 1933a). Greenland eskimos use it for bait in the cod and the shellfish (paltus) industry and for human food (Nesis, 1965). 2. Gonatus antarcticus Lonnberg, 1898 Often regarded as merely the Southern form of G.fabricii, this has been

recorded from Punta Arenas, near the Straits of Magellan (Lonnberg,

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1898; Pfeffer, 1912) and off the Cape of Good Hope (Steenstrup, 1882). Specimens have also been collected at South Georgia (Clarke in preparation). The Punta Arenas specimens were stranded, while the fragments recorded off South Africa (40"s 15'18'E) were removed from albatross stomachs. The author has identified these from stomachs of both albatrosses and Sperm whales caught a t South Georgia. The largest recorded specimen has a mantle length of 17-0 cm. (LUnnberg, 1898). 3. Gonatus anonychus Pearcy and Voss, 1963

This species has only been recorded off Oregon in oceanic water (Pearcy and Voss, 1963; Pearcy, 1965). It occurs sympatrically with G. fabricii and both are sometimes even taken at the same station. Except for one record in January all other specimens (22) were taken during the late summer a t about 50 miles offshore near the 1000 fathom contour and from the surface at night. The January specimen was 145 miles from land and it seems possible that an inshore movement takes place in the summer although the better sea conditions may account for the larger catches in that season (Pearcy and Voss, 1963). The largest specimen described has a mantle length of 7.8 cm and males of 6.95 cm have well developed spermatophores in the penis and females at 6.1 cm have well developed nidamental glands. 4. Gonutus magister Berry, 1913a Qonutus fabricii (?) Berry, 1912c (para) Gonutus septemdentatw Sasaki, 1915a Berryteuthis magister Grimpe, 1933 A North Pacific species which extends from Japan (Sasaki, 1916, 1920, 1929a) through the Kuril region (Akimushkin, 1955a, 1963; Beteshava and Akimushkin, 1955), the coastal waters of the Aleutian Islands and the Gulf of Alaska (Okutani and Nemoto, 1964) to Victoria in British Columbia, Puget Sound (Berry, 1912d, 1913a) and Oregon (Pearcy, 1965). It is caught for food in Etchu province but is not commercially important elsewhere in Japan (Sasaki, 1929a), while it is one of the predominant species in the diet of Sperm whales off the Kuril Islands (Beteshava and Akimushkin, 1955) and has been described as very common in the north-east Pacific (Okutani and Nemoto, 1964). It is caught between 100 and 557 fathoms off Japan (Sasaki, 1920, 1929a) but it may come close to the surface because it has been found in the stomachs of Albatrossia pectoralis. The largest specimen known t o the author has a mantle length

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of 25.0 cm. While Sasaki (1929a) found that 8 specimens from 8.2 to 22.0 cm were immature, most of the specimens removed from stomachs of Sperm whales taken off the Aleutians and in the Gulf of Alaska were found to be mature with mantle lengths of 20.0-25.0 cm (Okutani and Nemoto, 1964). The species has been collected from stomachs of Sperm whales (Akimushkin, 1955; Okutani and Nemoto, 1964), northern fur seals (Panina, 1964;Fiscusetal., 1965)and Albatrossiapectoralis (Sasaki, 1920).

B. Gonatopsis 1. Gonatopsis borealis Sasaki, 1923 Originally described from Japan (Sasaki, 1923, 1929a) this species has also been recorded from the central and north Bering Sea, near the Aleutian Islands and in the Gulf of Alaska (Okutani and Nemoto, 1964; Akimushkin, 1957) off California (Rice, 1963) and off Oregon (Pearcy, 1965). It occurs not infrequently off Japan and is important in the diet of Sperm whales off California and the Bering Sea region. Okutani and Nemoto (1964) considered that the specimens from the Bering Sea region should be regarded as a subspecies (G. b. makko), distinct from the Japanese form and they described the distribution as probably in the bathypelagic zone of the northern North Pacific.

2. Gonatopsis octopedatus Sasaki, 1920 Only known from near Cape Patience (Sakhalin Islands) at 48' 22.5" 145'43.5'E (Sasaki, 1920, 1929a). The type was immature with a mantle length of 6.5 cm. Some authors have regarded this as identical with, or a race of, G . borealis (e.g. Grimpe, 1933).

VI. THYSANOTEUTHIDAE A. Thysanoteuthis 1. Thysanoteuthis rhombus Troschel, 1857 Thysanoteuthis elegans Troschel, 1857 Thysanoteuthis nuchulis Pfeffer, 1912 A rare species which is probably cosmopolitan in warmer waters and is usually considered to be the only one of the genus. It has been recorded in the eastern North Atlantic (Rees and Maul, 1956; Clarke, 1962b), the western North Atlantic (Voss and Erdman, 1959), the Mediterranean (Troschel, 1857; Vigelius, 1880; Weiss, 1889; Jatta, 1896; Pfeffer, 1912; Issel, 1920a; Naef, 1923; Degner, 1925; Sanzo, 1929), the South Atlantic off the Cape of Good Hope (Barnard, 1934, 1947), from Ningpo in China (Pfeffer, 1912) and from both sides of the main H*

0-4

0 45

OG

1.0

cm

1.8 8 . 0 crn FIG. 26. Early stages during the growth of Thysunoteuthis rhombus. A. The egg mass. B. An embryo within its egg capsule. C. A newly hatched individual which has a total length of 0.24 cm. D. An enlargement of a small portion of the egg mass showing the double row of embryos. E. Change in form during growth after Sanzo (1929, Figs. 1, 2, 4, 10, and 14), Issel (1920, Figs. 1, 2, 6, 7) and Naef (1923. Fig. 249, ML=8,0 cm). All from the ventral side. Mantle lengths in cm are indicated.

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island of Japan and the Bonin Islands (Sasaki, 1929a; Pfeffer's 1900 record of Japan was erroneous, Pfeffer, 1912). It is said to migrate with the Kuroshio and Tsushima currents into the Japan Sea from the south (Nishimura, 1964). It is known from strandings (Barnard, 1934, 1947) and observation (Rees and Maul, 1956), and young ones have been taken in nets (Degner, 1925) a t or near the surface. According to Japanese fishermen it jumps on to the decks of boats (Sasaki, 1929a). Sanzo (1929) considered that a pelagic egg mass recovered from the Straits of Messina belonged to this species and traced the development as far as stages described by Issel (1920a). The egg mass was a gelatinous " sausage " measuring 60 to 70 cm long by 15 to 20 cm in diameter, containing a double row of eggs disposed in the superficial layers (Fig. 25). There is a small external yolk sac and four pairs of arm buds in the early stages. During growth the arms become relatively longer and then shorter, the head becomes relatively shorter, the body relatively narrower and the fin becomes relatively much longer until it is almost the same length as the mantle (Fig. 25). The adult is extremely powerful and has a very thick mantle muscle as well as large fins and can reach 80.0 cm in mantle length (Pfeffer, 1912); several specimens of both sexes exceeding 60.0 cm in mantle length are known (Jat,ta, 1896; Pfeffer, 1912 ( 3 ) Sasaki, ; 1929a; Barnard, 1947 ( 0 ) ;Voss and Erdman, 1959; British Museum Natural History ( 3 ) ) .The left ventral arm is hectocotylized in the mature male (Pfeffer, 1912). These squid have been seen in groups of about twenty (Rees and Maul, 1956). A specimen was taken from the stomach of a blue marlin (Voss and Erdman, 1959).

VII. PARATEUTHIDAE A. Parateuthis 1. Parateuthis tunicata Thiele, 1921 This species is known only from the type specimen taken a t 64'29's 85'27'E and one other taken a t 65'15's 80"E. They were both taken with open nets fished to 3 000 m and 3 425 m respectively. The largest had a mantle length of only 0.8 cm.

B. Cycloteuthis 1. CycZoteuthis sirvenli Joubin, 1919

A North Atlantic genus and species known only from the type specimen (Joubin, 1919, 1924) caught a t 30'45'40"N 25'47'W with a " Filet Bourhe '' between the surface and 500 m at night. The mantle length is 4.9 cm.

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C . Psychroteuthis 1. Psychroteuthie glacialis Thiele, 1921 Only known from the type specimens taken from penguin and Weddel seal stomachs in the Antarctic (Thiele, 1921). The largest has a mantle length of 44.0 cm. Both third arms are hectocotylized in the mature male.

D. Alluroteuthis 1. Alluroteuthis antarcticus Odhner, 1923

A rare species recovered from two sectors of the Antarctic; from the Atlantic sector at 63'26'5 45'39'W and 64'1'5 50'30'W (Oaner, 1923) and from the Indian Ocean sector at 64"32'S 75'65'E, 66'35'5 61'13'E and 63'51'5 54'16% (Dell, 1959a). These were caught in open nets fished between depths of 2 800 m and 750 m. They are all about 1.5 to 2.7 cm in mantle length and it is possible that they are all juveniles (Dell, 1959a). Another named species Parateuthis tunicata Thiele, 1921, recovered from the Indian Ocean sector of the Antarctic may prove to be a juvenile of the same species (Odhner, 1923).

VIII. VALBYTEUTHIDAE A. Valbyteuthis 1. Valbyteuthis danae Joubin, 1931 Known only from the type specimen this was recovered in the Gulf of Panama at 7'30'N, 79'19'W. (Joubin, 1931). It was taken with an open net fished at 2 330 m and has a total length of 13.0 cm.

IX. BRACHIOTEUTHIDAE, etc. A. Brachioteuthis The species of this genus are not at all well known; those which seem reasonably distinct have been retained below but a revision may reduce some to synonyms. 1. Brachioteuthis riisei (Steenstrup, 1882) Tracheloteuthis riwei Steenstrup, 1882 Verrillwla gracilis Pfeffer, 1884 Verrilliola nymph Pfeffer, 1884 Entomopeis Ve'elainiRochebrune, 1884 E?t&nnqsis clouei Rochebrune, 1884 Trachloteuthis 1 8p. Hoyle, 188th Entmnop8is alicei Joubin, 1900 Branchioteuthis riisei Grieg, 1924

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This has been collected from all oceans (Fig. 26) including the North Atlantic (Hoyle, 1886a; 1905; Lonnberg, 1896b; Fowler, 1897; Steenstrup, 1898; Joubin, 1900, 1924; Massy, 1909, 1913, 1928a; Russell, 1909, 1922; Pfeffer, 1912; Chun, 1913; Grieg, 1922, 1924; Thiele, 1921; Degner, 1925; Stephen, 1944; Bruun, 1945), the Mediterranean (Weiss, 1889; Jatta, 1896; Hoyle, 1905; Pfeffer, 1912; Naef, 1923; Degner, 1925; Issel, 1925b), the South Atlantic (Hoyle, 1905; Chun, 1910a; Pfeffer, 1912; Massy, 1925), the Indian Ocean (Hoyle, 1905; Pfeffer, 1912), Hawaii (Berry, 1914a), the south-western Pacific (Hoyle, 1905; Pfeffer, 1912; Allan, 1945) and the south-eastern Pacific (Pfeffer, 1912). It is sometimes stated to come from all oceans from 60"N to 60"s (Pfeffer, 1912; Stephen, 1944). Although frequently taken near the surface over deep water (Hoyle, 1886a; Fowler, 1897; Massy, 1909, 1913, 1928a; Pfeffer, 1912; Chun, 1913; Stephen, 1944; Allan, 1945), it has been caught in open nets down to 3 000 m (Thiele, 1921; Joubin, 1924). On the basis of 76 specimens Degner (1925) found that 58.9% were caught at less than about 30 m (i.e. with less than 65 m of wire out), 32.9% at about 30-150 m (i.e. with between 65 and 300 m of wire out) and only 8.2% at more than about 150 m depth (i.e. with more than 300 m of wire out). During growth the arms become relatively longer, the tentacles and head relatively longer and then shorter, the body relatively broader and then narrower and the fin relatively longer (Fig. 27). At first there is a pre-orbital " snout '' but this is soon lost and the " neck '' becomes very long; this also shortens during further development. If the stages represented in Fig. 27 are really passed through in this species they indicate a remarkable reversal in relative growth and there seems some likelihood that more than one species is involved. Changes in the tentacle club have been described (Naef, 1923; Degner, 1925),but few specimens have been sexed so that the size at the onset of sexual maturity is not known. The largest recorded specimen has a mantle length of 3.35 cm (Degner, 1925). I n the North Atlantic very young stages have been caught from May to August (Massy, 1909; Degner, 1925) and in February (Massy, 1909); in the Mediterranean from April to July, September, December and February (Degner, 1925); and off east Australia in May, June, September, October and November. Thus, hatching appears to take place throughout the year as far as the data available indicate. 2. Bruchioteuthis beani Verrill, 1881a This has been recorded from eastern North America from Massachusetts toNorthCarolina (Verrill,1881s; Johnson, 1934). It has been taken

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in open nets fished at 334-1 540 m. The largest has a mantle length of 6-2 cm (Verrill, 1881a). One of the specimens was removed from a fish stomach.

0

\h

.*

0 . 35

0.73

20

v

3 . 0 5 cm

FIG.27. Change in form during growth of BrachioteuChi.9 r&ei

after Pfeffer (1912, Plate 26, Figs. 16, 13, 7, 3). All from the ventral aide. Mantle lengths in cm are indicated.

3. Brachioteuthis bowmani Russell, 1909 This species may only be a race of B. beani (Grimpe, 1933). It is only known from the type specimen taken a t 61’27” 3’42’W, north of Scotland in a depth of 778 m (i.e. t o the bottom). The type is a female with a mantle length of 6.1 cm. 4.

Brachioteuthis picta Chun, 1910a

This species has been recorded in the North Atlantic a t 51’37” 12’1’W (Massy, 1916a, 1928a) in the South Atlantic at 5’6” 9’58’W (Chun, 1910a) and in the south Indian Ocean at 43’19‘s 93’56’E (Dell, 1959a). It was taken with open nets fished t o a maximum of

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MALCOLM R. CLARKE

1 500 m and 1266 m. The largest has a mantle length of 4.8 cm (Dell, 19598).

B. Cirrobrachium 1. Cirrobrachium danae Joubin, 1933

Known only from the type taken in the North Atlantic at 12'59" 32'49'W (Joubin, 1933) it was taken a t a depth of 25 m a t night. Its mantle length is 1.6 cm. 2. Cirrobrachium Jiliferum Hoyle, 1904b The type which has no body was caught in the eastern Pacific 0'50'N 137'54'W (Hoyle, 1904b) and a specimen from the Indian Ocean taken at 25'5 57'7'E was referred to this species by Thiele (1921). The type was taken in an open trawl a t 4 560 m while the other specimen was taken a t 20 m (Thiele, 1921). The complete specimen is very small having a mantle length of 0.7 cm but it is recognizable as a young male.

X. PHOLIDOTEUTHIDAE A. Pholidoteuthis 1. Pholidoteuthis adami Voss, 1956b

This species has been recorded in the upper Gulf of Mexico between the surface and 867 m (Voss, 1956b). Schools appear on the surface several hours after sunset and sometimes " a school would swim past the ship for several hours '' (Mr. Springer's observations reported by Vow, 1956b). Voss (1956b) suggested that the species may be an important food of the Sperm whales which are very numerous in the middle part of the Gulf. Specimens with a mantle length of 30.5 cm are known. 2. Pholidoteuthis boschmai Adam, 1950b Only known from a single female taken at 5'58's 121'32'E in the Pacific, which was caught in a vertical net between 2 000 m and the surface and has a mantle length of 27.3 cm.

XI. BATHYTEUTHIDAE A. Bathyteuthis 1. Bathyteuthis abyssicola Hoyle, 1885a Benthoteuthis megalops Verrill, 1885e A widely distributed species (Fig. 28) first recorded from the Indian Ocean between Marion Island and the Crozets (Hoyle, 1886a)

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and later from other stations in the Indian Ocean (Chun, 1910a; Massy, 1916b), South Africa (Chun, 1910a; Thiele, 1921), the South Atlantic (Pfeffer, 1912; Thiele, 1921; Odhner, 1923), north Sumatra (Massy, 1916b), the Southern Ocean (Hoyle, 1886a, 1912; Thiele, 1921; Clarke unpublished), the North Atlantic (Verrill, 1885a; Hoyle, 1904b; Massy, 1916a, 1928a; Joubin, 1920, 1924; Thiele, 1921; Voss, 195613, 1960a) the Mediterranean (Pfeffer, 1912) and the eastern Pacific (Hoyle, 1904b; Robson, 1948). Specimens in the Discovery collections not previously reported are added to Fig. 28. All published records were taken with open nets and it is not always clear whether the depth given is that of the net or that of the water. However, the maximum depth of the deepest net which caught the species was 4200 m (Hoyle, 1912) and the maximum depth of the shallowest net was 400 m (Pfeffer, 1912). Discovery specimens, however, were caught with open nets (bearing a depth of net indicator) as shallow as 100 m at night and seven times with closing nets between 700 and 2 000 m (at 1 800-1 500 m, 1 050550 m, 850-950 m, 700-1 400 m, 1 800-2 000 m, 1 500-1 600 m and 1 200-1 300 m). I n view of the very large numbers of nets fished from Discovery I I in the Antarctic regions a t all depths these seven hauls are strongly indicative that the species normally lives between 700 m and 2 000 m in those regions. Specimens caught a t shallower depths are all from the lower southern latitudes, the North Atlantic Discovery collections) and the Mediterranean (Pfeffer, 1912). The species is usually found over very deep water; in the ten Discovery I1 stations a t which the soundings were accurately measured and Bathyteuthis was taken, they varied between 3 569 and 5 460 m although Massy (1916a) recorded them over soundings of 1280-1 370 m. The Discovery material shows that the species has a tolerance of salinity at least between 34.20°/,, and 34*98°/,0 and temperature between 1.50"C and 3.35"C. It does not appear to be confined to a particular density of water and in the only three instances where there is information it was found below and within 700 m of the oxygen minimum layer. The species is very distinctive a t all stages, the smallest being miniature adults except that they have prominent light organs at the bases of the three dorsal pairs of arms. With regard to the latter structures Voss (1956b) noted their absence in his own, Verrill's (1885a) and Hoyle's (1885a) descriptions, but all these have a mantle length of over 4.0 cm and a good series in the Discovery collections shows that the organs are lost, or become invisible from the surface, between mantle lengths of 2.28 and 3.7 cm. This series also shows that sexual maturity in the female is reached between 3.75 and 6.15 cm in mantle

FIG.28. Localities from which Bathyteuthis abyaaicola has been recorded previously (1) and som0 new records from the Diacovevg collection (2).

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length when the nidamental glands become enlarged and in the male at about 3.7 cm mantle length when spermatophores are found in the cirrus. The largest specimen recorded has a mantle length of 5.7 cm. (Verrill, 1885a). There is no evidence of a limited breeding season.

B. Ctenopteryx 1. Ctenopteryz siculus (VBrany, 1851) Sepioteuthis sicula VBrany, 1851 Ctenopteryx jimbriatus Appellof, 1889 Ctenopteryx cyprinoides Joubin, 1894c Calliteuthis nevroptera Jatta, 1896

This species has been taken in the North Atlantic (Joubin, 1900; Pfeffer, 1912; Chun, 1913; Degner, 1925; Bouxin and Legendre, 1936; Voss, 1960a), the South Atlantic (Chun, 191Oa; Thiele, 1921), the Mediterranean (Vbrany, 1851; Appellof, 1889; Joubin, 1894c; Jattct, 1896; Bianco, 1903; Ashworth and Hoyle, 1906; Naef, 1923; Degner, 1925; Issel, 1925b; Sparta, 1933). It has been taken near the surface a t night (Sparta, 1933) and in nets fished to a maximum depth of 2000 m (Chun, 1910a). Degner (1925) found that of 2 1 specimens 8 were a t less than 30 m depth (less than 65m of wire out,), 12 were a t 30-150 m depth (65-300 m of wire out) and only 1 was a t more than 150 m depth (more than 300 m of wire out). Issel (1925b) recorded 10 out of 11 larval specimens a t less than 100 m and the remaining one at 300 m. Evidence based on specimens taken from fish stomachs suggests that they live in groups (Bouxin and Legendre, 1936). During growth, the arms, tentacles and head all become relatively longer while the body remains almost the same shape (Fig. 29); the fin becomes relatively longer, being terminal a t a mantle length of 0.8 cm and extending the whole length of the mantle when it reaches 3.3 cm (Chun, 1913; Naef, 1923). The largest specimen has a mantle length of 5.4 cm (Ashworth and Hoyle, 1906). The species has been recorded from stomachs of Germo alalunga (Bouxin and Legendre, 1936), a dolphin (Joubin, 1894c) and from Chauliodus (Sparta, 1933). Pfeffer (1912) regarded Chun’s (1910a) specimen as a distinct form which he named C. siculus chuni.

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0.34

05

04

1.2

1.:8

cm

FIQ.29. Change in form during growth of Ctenopteryz siculzcs after Naef (1923, Figs. 117, 118, 120, 121) and Pfeffer (1912, Plate 27, Fig. 16). All from the ventral side. Mantle lengths in cm are indicated.

XII. ENOPLOTEUTHIDAE A. Abralia These fall naturally into two groups; in the sub-genus Stendralia there are the species extending from the Red Sea eastwards to Hawaii and the South Seas A. steindachneri, A. astrosticta, A. astrolineata, A . sparcki, A. lucens and A. renschi; in the sub-genus Asteroteuthia, A . andamanica, A . japonica and A. trigonura from the Indo-Pacific and A. veranyi and A . redjeldi from the Atlantic and Mediterranean. The Japanese A. multihamata is close to Asteroteuthis but also has affinities with A . stenabralia astrosticta (Sasaki, 1929a). A. armuta was referred to the sub-genus Abralia by Voss (1963a). 1. Abralia andamanica Goodrich, 1896 A species recorded from the Andaman Sea (Goodrich, 1896) (Fig. 30), the Philippines (Voss, 1963a), the Hawaiian Islands (Voss, 1963a), the Mergui Archipelago (Massy, 1916b), 14'54% 96'13'E (Massy, 1916b) and Japan (Sasaki, 1916, 1929a); Voss (1963a) considers that the Japanese and Hawaiian specimens may be distinct subspecies. It

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occurs in water of 250-1 032 m (Voss, 1963a) and a t 100-584 m (Goodrich, 1896; Massy, 1916b). The largest male recorded has a mantle length of 3.5 cm (Sasaki, 1929a) and the largest female 5.0 cm (Voss, 1963a). 2. Abralia armata (Quoy and Gaimard, 1832) Taken off the Molluccas (Quoy and Gaimard, 1832), Celebes (Quoy and Gaimard, 1832) and the Philippines (Elera, 1896). Only eleven specimens are known (Voss, 1963a) and of these the two males with mantle lengths of 2.7 and 2.9 cm have spermatophores developed. Eight females range from 2.1-2.95 cm in mantle length. The right fourth arm is hectocotylized as opposed to the left fourth arm in other Abralia species. 3. Abralia astrolineata Berry, 1914 Known only from the type specimen stranded on Sunday Island of the Kermadec group (Berry, 1914~).It is a female with a mantle length of 3.4 cm. 4. Abralia astrosticta Berry, 1909

A Pacific species, this has been recorded from Hawaii (Berry, 1909a, 1914a) and the Marshall Islands (Voss, 1954b), and there are two doubtful records from eastern Australia (Allan, 1945). Pfeffer (1912) considered that this form was a growth stage which he called Compsoteuthis but Voss (1954b)refutes this and considers it to be a distinct species. It has been taken between 350-640 m with open nets. The largest female has a mantle length of 5.7 cm (Voss, 1954b). 5. Abralia grimpei Voss, 1958 Known only from the type specimen which was collected in the It was caught at 57 m western North Atlantic at 26'25" 79'45'W. with an open net and is a female with a mantle length of 2.7 cm. 6. Abralia japonica Ishikawa, 1929 Known only from the type specimens taken in Toyama Bay, Japan Sea. The holotype is a mature female with a mantle length of 5.6 cm. 7. Abralia lucens Voss, 1963a This species has been taken in the Philippines off Leyte, Fanning Island, Christmas Island and off the Live Islands, Oceania (all by Voss, 1963a). All specimens were taken near the surface. The largest female is gravid and has a mantle length of 6.2 cm. Eggs measured 0 . 8 by

FXo. 30. Localitiee from which Abrdia 8leindachneri ( l ) ,A . renachi (2), A . aatroaticta (3), A . 8Hrcki (4). A . lucens (6),A . astrolineata ( 6 ) , A . veranyi (7). A. g r i m p i ( 8 ) . A . redfieui (9), A . andamandco (10).A . japonica ( 1 1 ) . A . trigonura (12). A . am& (13)and A . mullihamata (14) have been recorded.

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0.6 mm. This appears to be a more oceanic species than the other known species of the sub-genus Stenabralia according to Voss (1963a). 8 . Abralia multihamata Sasaki, 1929a

This is only known from seven specimens taken a t Akocho and Taihoku market in Formosa (Sasaki, 1929a). They varied from 2.5-3.2 cm in mantle length. 9. Abralia redJieldi Voss, 1955

A North Atlantic species taken near the Bahamas and off Caibarien, Cuba (Voss, 1955). It has been taken a t the surface and a t 466 m with an open net. Females with a mantle length of 2.8 cm and 2.9 cm were gravid. 10. Abralia renschi Grimpe, 1931 Known only from the types taken in Sabang Harbour of Pula We, Sumatra; these were three females between 3.7 and 4.55 cm in mantle length. 11. Abralia sparcki Grimpe, 1931 Two specimens taken off the Amboina Coast of Sawrude and between

Samar and Masbate, Philippines (Grimpe, 1931). They were taken a t the surface a t night and were both females having a mantle length of 4.7 and 4.8 cm. 12. Abralia steindachneri Weindl, 1912 This species has only been recorded from the Red Sea (Weindl, 1912; Adam, 1942a, 1955, 1959) but was identified by the author in stomach contents of tuna taken a t Zanzibar (Williams, in press). Only females have been identified and the largest described has a mantle length of 5.6 cm.

13. Abralia trigonura Berry, 1913b One specimen only has been taken off Hawaii and this was badly macerated. It has a mantle length of 2.85 cm (Berry, 1913b). 14. Abralia veranyi (Riippell, 1844) Enoploteuthis veranyi Riippell, 1844 Abralia oweni Hoyle, 1886a Abralia armata (pars) Pfeffer, 1900 Abraliopsis rnorisi (pars) Pfeffer, 1900 Aeteroteuthis veranyi Pfeffer, 1908a

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Enoploteuthis owenii Gray, 1949 Onychoteuthis (Enoploteuthis)owenii VBrany, 1951 This is the most well known Abralia species having been caught a number of times in the western Mediterranean: at Messina (Riippell, 1844; Pfeffer, 1912; Grimpe, 1931), Nice (VBrany, 1851; Pfeffer, 1912), Toulon, (Pfeffer, 1912), Naples (Naef, 1923), Genoa (Gray, 1849) and possibly off Sardinia (Issel, 1925b). From the North Atlantic it has been taken off Madeira (Berry, 1926), off Cuba (Voss, 1955), in the Gulf of Mexico (Voss, 1956b), off Florida (Voss, 1956a) and off San Salvadore (Adam, 1941a). I n the South Atlantic it is very common on the continental slope of tropical Africa (Adam, 1952). It has been taken between the surface and 550 m (Adam, 1952, 1962; Vow, 1966, 1956b). Off tropical Africa it was found in water between 8.65" and 15.40"C and in salinities of 34.87 and 38-33%, (2 surface temperatures and salinities) (Adam, 1952). With 167 specimens taken thoughout the year a t his disposal, Adam (1952) was unable to find evidence for a limited spawning period but Berry (1926) concluded that the annual summer migration into Funchal harbour was probably for spawning or mating. The left ventral arm is hectocotylized and spermatophores are attached to the female within the mantle cavity behind the nuchal cartilage (Berry, 1926; Adam, 1952). It has been recorded from the stomachs of Etmopterus hillianus (Poey) and Chlorophthalmus agassizi Bonaparte (Adam, 1952).

B. Abraliopsis Of the six species only A . morrisi is a t all well known. 1. Abraliopsis aginis (Pfeffer, 1912) Abralia (Micrabralia)afinis Pfeffer, 1912 Abraliopsis Hoylei Hoyle, 1904b This species has been taken a t four positions between Cape San Francisco and Acapulco on the western side of Central America, (Hoyle, 1904b; Pfeffer, 1912) (Fig. 31). It was taken between 5503 470 m with open nets. There is slight sexual dimorphism in the arm, there being papillae on the oral surfaces in the male (Pfeffer, 1912).

2. Abraliopsis gilchristi (Robson, 1924) Abralia gilchristi Robson, 1924a Two males were taken off South Africa a t depths of 440 m and 570 m with open nets. Robson considered that both are mature to judge from their proportions. One has a mantle length of 4.0 cm and

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the other, which is damaged, is about the same size. (Also see A . neozealandica). 3. Abraliopsis hoylei (Pfeffer, 1884) Enoploteuthis Hoylei Pfeffer, 1884 Abraliopsis morisii Pfeffer, 1900 Abralia Hoylei Pfeffer, 1908a Abraliopsis ? Hoylei Allan, 1945 The type of this species was caught off Mascaren (Pfeffer, 1884) and several specimens have since been doubtfully referred to the species; these are, a specimen from Sunday Island in the Kermadec group (Berry, 1914c), 13 taken off Eastern Australia (Allan, 1945) and 7 from the Galapagos Islands (Robson, 1948). The doubtful specimens were taken between the surface and 1 100 m with open nets and one was stranded. The largest specimen known is that of Pfeffer which has a mantle length of either 3.1 cm (1884) or 2.95 cm (1900). 4. Abraliopsis lineata (Goodrich, 1896) Abralia lineata Goodrich, 1896 Micrabralia lineata Pfeffer, 1900 This species has been taken in the Andaman Sea and off the Ganjam coast (Goodrich, 1896). It was taken with open nets fished to 160-480 m. A male has a mantle length of 1-5 cm. 5. Abraliopsis morrisi (VBrany, 1837) Onychoteuthis Morrisii VBrany, 1837 Enoploteuthis Morisii d'orbigny, 1835-1848 Abralia Morrisii Gray, 1849 This is one of the commonest of the small species of squid in the North Atlantic (Fig. 31) where it has been found between 39"N (d'orbigny, 1845) and 0'29" (Thiele, 1921) and from the Straits of Gibraltar to 64"35.5'W0(Chun, 1910a, 1913; Degner, 1925; Rees and Maul, 1956; Voss, 195613, 1960a). It has also been recorded from the Mediterranean (VBrany, 1837; Joubin, 1924; Degner, 1925; Issel, 1925b), from the Indian Ocean (Chun, 1910a), Flores Strait (Boone, 1938), and off Japan (Akimushkin, 1955). It has been caught in open nets fished a t 3 500 m (Joubin, 1924) but Degner (1925) showed that it is probably most prevalent from the surface down to about 30 m. He found that 69.5% of the squids were caught a t a depth of less than about 30 m (i.e. with less than 65 m of wire out) as opposed to 18.6% a t about 30-150 m (i.e. with 65-300 m of wire out) and only 11.8% a t more than about 150 m (i.e. with

0.3

0.7

3.95 cm

FIG. 32. Top row. Change in form during growth of Pterygioteuthis giardi after Chun (1910, Plate 12, Figs. 8, 10,6 and 2). Bottom row. Change in form during growth of Abraliop8ia after Chun (1910, Plate 7, 6, 6). Surface photophores are omitted from the largest specimen. All from the ventral side. Mantle lengths in cm are indicated.

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more than 300 m of wire out). Issel (192513) recorded 18 young specimens (0.2-0.65 cm long) which were all caught at 10-150 m. They have been caught in fairly large numbers (up t o 176) in a single haul (unpublished notes) and are therefore probably a shoaling species. Development involves some change in form and several names have been applied t o various ill-defined stages such as Nepioteuthion, Micrabralia and Compsoteuthis. From specimens which are possibly but not certainly this species, growth involves a relative shortening of the arms, tentacles and head; the body becomes relatively broader and then narrower and the fin becomes relatively longer and then shorter (Fig. 32). Considerable changes in the arrangement of light organs and in the club armature take place (Chun, 1910a; Naef, 1923; Degner, 1925). Degner (1925) found very small specimens with mantle lengths of less than 0.4 cm in February, June, July, August, and December so that spawning is probably not limited to a particular period of the year. The left ventral arm becomes hectocotylized a t mantle lengths of between 2.0 and 2.6 cm and a male of 2.65 cm mantle length had spermatophores in the penis (Voss, 1960a). A female with a mantle length of 3.8 cm was ripe (Chun, 1910a) and this is the largest female recorded, the largest male having a mantle length of 2.65 cm (Voss, 1960a). They feed on copepods and euphausids which they follow in shoals to near the water surface (Akimushkin, 1963). This species has been taken from the stomachs of a dolphin (VBrany, 1837), Alepisaurus ferox (Rees and Maul, 1956) and Coloconger raniceps Alcock (Chun, 1910a). 6. Abraliopsis neozealundica (Dell, 1959) Enoploteuthis neozeahndicu Dell, 1959b This species is only known from the east coast of Wellington, New Zealand (Dell, 1959b). It was caught with an'open net a t 90 m, and is a male with the right ventral arm hectocotylized and a mantle length of 3.7 cm. G. L. Voss (see Roper, 1966) considers that this is a synonym of A . gilchristi (Robson, 1924). 7. Abraliopsis pfefferi Joubin, 1896 Abralia (Abralia) Pfefferi Pfeffer, 1912 A North Atlantic species, this has been taken at Villefranche-surmer (Joubin, 1896c) at 36'05" 9"OO'W (Joubin, 1920) 31'45" 20'17'W and 30'45" 25"47'W (Joubin, 1924). It was taken with open nets fished between 3 660 m, 3 000 m and 1 000 m and the surface, The largest caught had a mantle length of 4.2 cm.

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C. Enoploteuthis 1. Enoploteuthis anapsis Roper, 1964 This recently described species has been caught at various positions in the North Atlantic from the Gulf of Mexico to Madeira and south to 19'16's 01'48'W (Chun, 1910a; Roper, 1964, 1966). Specimens were taken with an open net fished to as much as 2 000 m (Roper, 1964, 1966) and to as little as 10 m. A male is mature at a mantle length of 5.4 cm and a female at 1.69 cm. The largest male specimen is 7.9 cm and largest female is 7-69 cm in mantle length. The distal third of the right ventral arm is hectocotylized. During growth the arms and tentacles remain the same length relative to the mantle length while the fin becomes relatively longer and the mantle relatively narrower (Roper, 1966). There is little change in proportion between 1.69 and 7.69 cm mantle length. A specimen was taken from the stomach of Aphanopus carbo (Roper, 1966). 2. Enoploteuthis chuni Ishikawa, 1914

This is a Japanese species taken at Uwodo, Japan Sea (Ishikawa, 1914), Toyama Bay (Sasaki, 1929a) and at 32'36" 132'23'E (Sasaki, (1920). I n one instance two were taken from the stomach of a fish which was caught at 800 m. It is often caught mixed with large schools of Watasenia scintillans on the coast of Etchu Province (Sasaki, 1929a). The largest male described had a mantle length of 6.3 cm and the largest female a mantle length of 9.0 cm. The right fourth arm is hectocotylized and in five females, spermatophores were attached under the mantle, behind the nuchal cartilage (Ishikawa, 1914). It has been recorded in the stomachs of the Alaskan pollack (Shimomura and Fukataki, 1957).

3. ? Enoploteuthis dubia Adam 1960 This species is doubtfully referred to the genus and is only represented by a single male with 8 mantle length of 3.6 cm, taken at Eylath in the Red Sea (Adam, 1960b).

Enoploteuthis galaxias Berry, 1918 Euoploteuthis gakzxias Cotton, 1942 This was taken off Victoria, Australia, with open nets fished at 200-460 m: a single male has a mantle length of 7.3 cm and three 4.

females mantle lengths of 7.2, 7.8 and 8.7 cm.

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5. Enoploteuthis leptura (Leach, 1817) Loligo Smythii Leach, 1817 Loligo leptura Leach, 1817 A rare species, this has been recorded off West Africa (Leach, 1817, 1818a; d’orbigny, 1845), Madeira (Rees and Maul, 1956) and the straits of Florida (Roper, 1966). Chun’s (1910a) record is thought to be E . anapsis by Roper (1964). It has been taken from stomachs of Yellowfin tuna caught near the surface and with open nets fished to as much as 1 620 m (Roper, 1966). The largest has a mantle length of 7-9 cm (Roper, 1966). During growth the mantle decreases in width, the fins become longer and the arms and tentacles become shorter relative to the mantle length (Roper, 1966).

D. Pterygioteuthis 1. Pterygioteuthis gemrnata Chun, 1910 This species has been taken in the South Atlantic (Chun, 1910a; Thiele, 1921) and the equatorial North Atlantic (Thiele, 1921) near the surface (10 m) (Fig. 33). Voss (1958) doubts the validity of the species. The hectocotylus lacks a chitinous hook which is found in P. giardi. The female has only a right oviduct and one pair of large nidamental glands. 2. Pterygioteuthis giardi Fischer, 1896

Pyroteuthis (Pterygioteuthis)Giardi Pfeffer, 1912 This little squid has been taken in the western North Atlantic (Voss, 1956a, 1958, 1960a) (Fig. 33), the eastern North Atlantic (Fischer and Joubin, 1906; Pfeffer, 1912; Chun, 1913; Joubin, 1920), South Africa (Massy, 1925), the Indian Ocean (Chun, 1910a), the East Indies (Adam, 1954), off Queensland and New South Wales (Allan, 1945), New Zealand (Massy, 1916c), off the Galapagos Islands and the eastern Pacific (Hoyle, 1904b; Robson, 1948) and the southern tip of South America (Carcelles and Williamson, 1951). It has been caught near the surface (Massy, 1 9 1 6 ~and ) with open nets fished to as much as 2 500 m (Chun, 1910a). The largest recorded male has a mantle length of 1 - 7 cm (Chun, 1910a) and the largest female a mantle length of 2.0 cm (Voss, 1958). Males with mantle lengths of 1.6 and 1.7 cm contained spermatophores (Chun, 1910a; Joubin, 1920) and a female of 1.9 cm had mated (Pfeffer, 1912). The left ventral arm ie hectocotylized. During growth, the arms and head become relatively longer and

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then shorter, the tentacles relatively longer, the body becomes relatively narrower and the fin relatively longer (Fig. 32). The species has been taken from the stomach of Tursiops truncatus. 3. Pterygioteuthis microlampas Berry, 1913 This species is only known from the type which was caught off Hawaii (Berry, 1913b, 1914a) in 570-610 m, and fragments from an unknown locality. Both specimens are females and the type has a mantle length of 1.8 cm.

E. Pyroteuthis 1. Pyroteuthis margaritifera (Ruppell, 1844)

Enoploteuthis margaritifera Ruppell, 1844 Pterygioteuthis margaritifera Pfeffer, 1900 Chaybditeuthis maculosa Pfeffer, 1900 Pyroteuthis juv. Issel, 1908 Benthoteuthis megalops Pfeffer, 1912 This species has been recorded from the western North Atlantic (Voss, 1955, 1956a, 1958, 1960a) (Fig. 34), the eastern North Atlantic (Joubin, 1900, 1924; Rees and Maul, 1956), the western Mediterranean (Riippell, 1844; Joubin, 1894c, 1900; Jatta, 1896; Bianco, 1903; Pfeffer, 1912; Naef, 1923; Sparta, 1933; Schiifer, 1938; Gray, 1949), the eastern Mediterranean (Degner, 1925), the East Indies (Hoyle, 1886a; Adam, 1954) and the Central Pacific (Hoyle, 1886a). Joubin (1924) created the sub-species P. margaritifera aurantiaca for the Azores specimens and Pfeffer (1912) grouped Hoyle’s (1886a) Pacific specimens under the name P. margaritifera oceanica. P. margaritifera has been caught in open nets fished at a minimum of 15 m and a maximum of 5 000 m. With closing nets it was caught at four positions at approximately 100 m and 150 m (200 and 300 m of wire out) and other records suggest that it probably extends from the surface to over 1000 m. The largest recorded male has a mantle length of 3.3 cm and the largest female a mantle length of 3.52 cm (Pfeffer, 1912) but unsexed specimens reach up to 8.5 cm in total length (Joubin, 1924). A male 3-5 cm (mantle length) has a hectocotylus (Naef, 1923) and a female of the same length is gravid (Voss, 1955). Growth from the early stages is very similar to that of Pterygioteuthis giardi (Fig. 32). Degner (1925) described the development of the mantle photophores. Specimens have been found in stomachs of Alepisaurus ferox and a dolphin (Joubin, 1894~;1900).

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I

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F. Ancistrocheirus It will possibly be necessary to unite this genus with Thelidioteuthis when more material becomes available. 1. Ancistrocheirus lesueuri (d’orbigny, 1839)

Onychoteuthis Lesueurii d’orbigny, 1835-1848 Enoploteuthis Lesueurii d’orbigny, 1845

This species has been recorded from Felidu Atoll, Indian Ocean (Hoyle, 1906a) and the Azores (Joubin, 1900) and it occurs off Durban (Clarke, unpublished). The largest has a mantle length of 39.0 cm. Several specimens have been taken from the stomachs of Sperm whales (Joubin, 1900; Clarke unpublished).

G . Thelidioteuthis 1. Thelidioteuthis ulessandrini (VBrany, 1851)

Loligo Alessandrinii Vdrany, 1851 Enoploteuthis polyonyx Troschel, 1857 Onychia caribaea Steenstrup, 1880 Abralia ntegabps Verrill, 1882b Enoploteuthis pallida Pfeffer, 1884 Cdliteuthis Alessandrinii Appellof, 1889 Abraliu polyonyx Carus, 1890 Thelidioteuthis polyonyx Pfeffer, 1900

This species has been recorded fi-om the Mediterranean (VBrany, 1861; Troschel, 1857; Appellbf, 1889; Pfeffer, 1912; Joubin, 1920; Naef, 1923; Degner, 1925; Issel, 1931a), the eastern North Atlantic (Joubin, 1920), the western North Atlantic (Verrill, 1884, 1885; Voss, 1956b), the South Atlantic (Pfeffer, 1884), the Indian Ocean (Chun, 1910a), the East Indies (Adam, 1954), the Society Islands, South Pacific (Pfeffer, 1884) and off Japan (Berry, 1912c; Sasaki, 1920,1929a). It has been caught with open nets fished to as little as 25 m (Degner, 1925) and to as much as 3 000 m (Joubin, 1920) but most have been taken at less than 1 000 m. Chun (1910) first illustrated larval stages of this species and this work was later supplemented by Issel (1931a).

During growth, the arms and tentacles become relatively longer, the head becomes relatively longer and then shorter, the body becomes relatively narrower and the fin relatively longer (Fig. 35). The largest recorded specimen has a mantle length of 2.9 cm (Verrill, 18841885).

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0.2

0.18

0*3

0.7

3.2

cm

FIG. 36. Top row. Change in form during growth of Thelidwteuthis alessandrini after Chun (1910, Plate 7, Figs. 16, 18) and Pfeffer (1912, Plate 18, Fig. 1). Bottom row. Change in form during growth of Octopoteuthie Bicula after Pfeffer (1912, Plate 19, Figs. 14, 8,4, 1). All from the ventral side. Mantle lengths in cm are indicated.

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H . Wataeenia This genus is very close to Abraliopsis. 1. Watasenia scinti2Zans (Berry, 1911)

Abraliopsie scintillans Berry, 1911b Abraliopsis joubini Watas6, 1905 Abraliopsis sp. Nishikawa, 1906 Abralia (Nepioteuthion) Nishikawa Pfeffer, 1912 Abraliu (Compsoteuthis)Nishikawae Pfeffer, 1912

This is common around Japan (Watasb, 1905; Berry, 1911b, 1913d; Sasaki, 1920, 1929a; Okada, 1927; Shimomura and Fukataki, 1967) and has been recorded off Cape Clonard, Korea (Sasaki, 1929a), in the Okhotsk Sea (Sasaki, 1914) and in the North Pacific (Nemoto, 1967). It is a shoaling species and fishermen sometimes catch up to 2 million individuals in a single haul (WatasB, 1905 after Berry, 1913d). It is taken at less than 1 000 m and to within about 150 m from the surface. The largest recorded male is 5.9 cm (Berry, 1911b) and the largest female is 7.0 cm in mantle length (Sasaki, 1929a). Males having mantle lengths of 4.8 and 5.0 cm have hectocotylized right ventral arms and females with mantle lengths more than 4.8 cm have mated (Sasaki, 1920). Matsuno (1915) and Sasaki (1913) studied different aspects of the ecology of the species. Shimomura and Fukataki (1957) found that squid eggs caught at the surface from March to August, which they thought belonged to this species, appeared at the same time that adults were in spawning condition, during the fishing season. These eggs were found throughout the Japan Sea but mainly off Eastern Korea and West Honshu. Their identification was not definitely established. They occur in water a t 10°-270C and with a chlorinity of 17.5-19.3%,. Some larvae are also referred to this species on circumstantial grounds. The species is sometimes found in the stomachs of Baleen whales (Nemoto, 1957) and constitutes 8% by volume of the diet of the Northern Pacific fur seal (Wilke and Kenyon, 1954). It is also eaten by the Alaskan pollack (Teragra chulcogranzma) (Shimomura and Fukataki, 1957). From the end of April to the end of May the species is usually taken commercially in Etchu Province, Japan (Sasaki, 1929a). The catch fluctuates but is usually about 1000 tons and is used for food or is salted for fish bait. On the southern side of Sagami bay the squid is also abundant but here the individuals are smaller, slightly different in proportion and have fewer photophores (Sasaki, 1929a).

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I. Enoploion 1. Enoploion eusticum Pfeffer, 1912

This species includes several juveniles which cannot be placed elsewhere with any certainty. They have been recorded from the eastern North Atlantic at 32'00" 77'45'W (Pfeffer, 1912) and 36'17" 1'58'W (Joubin, 1920) and from the western Mediterranean at 39'32" 5'15'E and 36'54" 2'47'E (Degner, 1925). They were taken at less than about 30 m (Degner, 1925) and with an open net fished to 1 800 m (Joubin, 1920). The largest is only 0.42 cm in mantle length.

XIII. OCTOPOTEUTHIDAE A. Octopoteuthis This genus contains several named species but some of them are based on larval forms and their relationships are not clear. 1. Octopoteuthis danae (Joubin, 1931) Octopodoteuthis danae Joubin, 1931

A species having prominent light organs on the head and mantle, that is known only from the type specimen which was recovered from the North Atlantic a t 33'15" 68'20'W with an open net fished at 45 m. The mantle length is about 3.0 cm (measured from the figure). 2. Octopoteuthis sicuh Riippell, 1844 Octopodoteuthissicula Krohn, 1845 Veranya siculu Appellof, 1889

Considerable variation between the various descriptions of this species suggests that a revision based on material from a wide geographical range may show that several species are included under this name (Fig. 36). Pfeffer (1912) recognized a Mediterranean and an Atlantic form which were named as varieties by Grimpe (1922) although Degner (1925) found no difference between specimens of the two geographic regions. 0. persica Naef, 1923, 0. indica Naef, 1923 and 0. nielseni Robson, 1948 are all based on larval forms and may well prove to be synonyms. 0. sicula has been recorded from the western Mediterranean (Riippell, 1844; Krohn, 1845; Gray, 1849; VBrany, 1851; Pfeffer, 1884, 1900, 1912; Weiss, 1889; Appellof, 1889; Jatta, 1896; Ficalbi, 1899; Naef, 1916, 1921, 1923; Issel, 1925b; Degner, 1925), the eastern Mediterranean (Degner, 1925; Digby, 1949), the North Atlantic (Massy, 1907, 1909, 1913, 1928a; Pfeffer, 1912; Chun, 1913; Joubin, 1920; Bouxin and Legendre, 1936; Adam, 1960c; Rsncurel, 1964), the South Atlantic (Adam, 1952, 1960c), the Indian Ocean (Chun, 1910a),

.

FIG.

YI

36. Locafitiea from which Octopoteuthis ekula (l),0.d a m (2), 0.bngiplera (3). 0.nklecni (4) and Octopole&?wp& megaptera (6)have been recorded.

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the Philippines (Voss, 1963a),Japan (Chun, 1910a, Sasaki, 1916) and off western North America (Pearcy, 1966). The species has been taken at the surface (Massy, 1913; Joubin, 1920) and in open nets fished to 2 000 m (Degner, 1926) but most of them were taken at less than 1000 m and Degner (1925) found that out of 14 small specimens (less than 2.2 cm mantle length) one was taken at less than about 30 m (65 m of wire out), 9 were taken at 30-150 m (65-300 m of wire out) and 4 were taken at more than about 150 m (more than 300 m of wire out). Pearcy (1965),on the other hand, caught no specimens in 72 tows of a trawl fished at 0-200 m, 0.04 per hour in nets fished at 0-500 m and 0.02 per hour in nets fished at 0-1 000 m. The largest specimen, a female, has a mantle length of 13.7 cm (Adam, 1952); its nidamental glands are 3.0-3.5 cm long and the eggs are 1.0 mm in diameter. Nearly all the young stages taken in the North Atlantic were caught between May and September (Pfeffer, 1912; Joubin, 1920; Degner, 1925; Bouxin and Legendre, 1936). During growth, the arms and head become relatively longer and then shorter, the tentacles become relatively longer and are later lost altogether, the body becomes relatively wider and then narrower and the fins become relatively longer (Fig. 35). Specimens have been removed from the stomachs of Germo alalunga (Bouxin and Legendre, 1936) and Tursiops truncatus (Rancurel, 1964). 3. Octopoteuthis Zongiptera Akimushkin, 1963 The type was taken from a Sperm whale's stomach caught at 20"s 26"W. It has a mantle length of 69.0 cm. Akimushkin (1963)states that beaks of this species are fairly common in Sperm whale stomachs taken in the Kuril region. To suggest such an extension in the range on the basis of b'eaks alone seems most unwise at our present stage of knowledge. B. Octopodoteutbpsis The status of this genus is doubtful. Adam (1952) considered that it should possibly be united with Octopoteuthis while Voss (1956b)believes

that the separation into a distinct genus is justified. 1. Octopodoteuthopsis megaptera (Verrill, 1885) Ancistrocheirus megaptera Verrill, 1885a

This species has been taken in the western North Atlantic at 39'12" 72'03'W (Verrill, 1885a), 25'63" 79'46'W (Voss, 1968) and

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29'10" 87'65'W. It has been caught with open nets fished to depths of 330-1 290 m. The largest has a mantle length of 4.1 cm (Voss, 1968).

C. Taningia A genus with only one species. 1. Taningia danae Joubin, 1931 ? Enoploteuthis Molinae Harting, 1861 Cucioteuthis unguiculatus Joubin, 1898a, 1900 Cucioteuthis unguicukztus Clarke, R. 1956 Cucioteuthis unguicukzta Rees and Maul, 1956 Cucioteuthis unguicukzta Clarke, M. R. 1962a Adults of the species have been taken off the Azores (Joubin, 1898a, 1900; R. Clarke, 1956),offMadeira (Rees and Maul, 1956; Clarke, 1962a), off Durban (Clarke,in press) and from the Indian Ocean (Harting, 1861), while juveniles have been taken in the Atlantic at 14'62" 28'04'W (Joubin, 1931) and 2'43's OO"56'W (Clarke, in press). The juveniles were taken in open nets fished at 100 m and 175 m. The largest specimen described is about 140.0 cm in mantle length (Clarke, 1962a) while the smallest is 2.85 cm (Clarke, in press). During growth the arms, head and fin become shorter and the head, mantle and fin become narrower relative to the mantle length. One of the specimens contained sand grains and bits of iron oxide in the stomach. This, coupled with the fact that most of the specimens from Durban are in a mating or spawning condition suggests the species may spawn on the bottom. A gravid female had nidamental glands measuring 70.0 and 80.0 cm in length (Clarke, 1962a) and a specimen having a pen length (-mantle length) of 71.0 cm had an estimated 200 000 eggs in the ovary and oviducts. All the adults known have been recovered from Sperm whale stomachs or just after regurgitation by the same predator. XIV. LYCOTEUTHIDAE This family has recently been revised by Voss (1962d). The species are notable for the great diversity and numbers of their photophores.

A. Lampadioteuthis 1. Lampadioteuthis megaleia Berry, 1916 Since Berry's (1916a) description of this species based on one female which was collected from a beach on Sunday Island in the Kermadec group, no further specimens were reported until Young (1964) recorded two larval specimens and an adult male from the

191

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North Atlantic at 40"46'N 18"35'W and 25"ll'N 20'27'W. From Young's data the species lives a t between 0-300 m. The female is 3.0 cm, the male 3.1 cm and the two larvae are each 0.8 cm in mantle length. The male contained no spermatophores but Young considered that the right ventral arm was hectocotylized.

B . Lycoteuthis This genus contains a single species which ha8 been caught on a number of occasions but is still rather poorly known from the ecological point of view. 1. Lycoteuthis diadema (Chun, 1900) Enoploteuthis diadem Chun. 1900 Lycoteuthis Jattae Pfeffer, 1900 Thuumatolampas diadema Chun, 1903b Asthenoteuthion plunctonicum Pfeffer, 1912 ? Lycoteuthis sp. A . Robson, 19248 ? Lycoteuthis sp. Robson, 1924c Leptodontoteuthis inermis Robson, 1924c

First recorded from the South Atlantic (Fig. 37), south of Africa (Chun, 1900)it has since been taken off the Cape of Good Hope (Robson, 1926c), Natal (Robson, 1924a,c), in the western North Atlantic (Voss, 195613, 1958, 1962d), south of Australia (Pfeffer, 1912) and on the western coast of America (Pfeffer, 1900). It has been taken in open nets fished between 3 000 m and the surface but as pointed out by Voss (1962d) the records suggest that the species probably live between about 500 m and the surface. The three larvae which have been taken (Voss, 1958) were caught at 46-57 m. No males have yet been recorded and the largest of the eight females known has a mantle length of 8.3 cm (Voss, 1956b). Voss (1958) described the juvenile stage a t a mantle length of 0.72-0.87 cm and pointed out a few differences between this and the adult . The stomachs of three specimens contained fish remains, in one case those of a myctophid, and Crustacea which possess light organs (Voss, 1962d). The species has been found in fish stomachs (Voss, 1956b) and from a dolphin stomach (Pfeffer, 1900).

C . Nematolampis Only the type specimens of the single species in this genus are known. 1'

FIG.

37. Localities from which Lywteuthis diizdema ( l ) , Lampadioteuthie rnegdeia ( 2 ) . OregonMteuthis epringeri ( 3 ) . 0 . lorigeva Nematolampb reg&&

(6)and S¬cuthis a&ntiUaw (6) have been recorded.

(4).

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193

1. Nematolampis regalis Berry, 1913 The only specimens known were stranded on the beach of Sunday Island of the Kermadec group (Berry, 1913~). The mantle lengths were 2.65-3.2 cm.

D. Oregoniateuthis. This genus contains two poorly known species. 1. Oregoniateuthis lorigera (Steenstrup, 1875) Onychoteuthis lorigera Steenstrup, 1875 This species was redescribed by Voss (1962d) from a specimen recorded as Onychoteuthis lorigera by Steenstrup (1875) which came from a Sperm whale's stomach taken in the South Seas. It has a mantle length of 18-0cm and is female. 2. Oregoniateuthis springeri Voss, 1956 This has been taken on two occasions in the Gulf of Mexico (Voss, 1956b, 1962d). One specimen was taken from the stomach of a shark caught in 367 m and another was taken in an open trawl fished at 450-950 m. They were both males and had mantle lengths of 8.0 cm and 9.7 em. The male has paired genital ducts. One stomach contained crustacean remains including photophores possibly belonging to euphausids or sergestids (Voss, 1962d).

E. Selenoteuthis A genus containing only one species. 1. Selenoteuthis scintillans Voss, 1958 Voss (1958, 1962d) has recorded this from two positions, 26'22" 76'10'W and 25'11" 89'50'W from depths of 46 m and 3 290 m caught with open nets. A male has a mantle length of 3-26 cm and the three females, mantle lengths of 1-9-3.1 cm. The male genital organs are paired and the spermatophore is short, stout and unique in structure. A stomach contained unidentifiable crustacean remains.

XV. HISTIOTEUTHIDAE

A long overdue revision of this family is at present being undertaken by Professor Gilbert L. Voss and Dr. Nancy Voss. Some of their findings have already been published (Voss and Voss, 1962) and have been utilized in the following account.

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MALCOLM R. CLARKE

A. Histioteuthis The genus is now thought to contain but one species with a number of synonyms. 1. Histioteuthis bonellii F&ussac, 1835 Cranchia Bonelliana FQrussac,1835 Histioteuthis Ruppellii Vdrany, 1851 Histioteuthis Collimi Verrill, 1879a Histiopsis atlanticu Hoyle, 1885a Histioteuthis bonelliana d’orbigny, 1835-1848 A widely distributed species (Fig. 38) which has been recorded from the western Mediterranean a t Nice (Fhrussac, 1835; VBrany, 1851; Risso, 1854; d’orbigny, 1845;Weiss, 1889; Joubin, 1893a; Pfeffer, 1912), San Remo (Joubin, 1893a), the Ligurian Sea (Arbocco, 1958), Naples (Jatta, 1896; Naef, 1923), Gulf of Nisida (Naef, 1923), Messina (Naef, 1923), Capri (Bianco, 1903) and eastern Spain (Lozano y Rey, 1905; Morales, 1962), from the eastern North Atlantic (Joubin, 1900, 1924; Fischer and Joubin, 1907; Massy, 1907,1909; Degner, 1925; Bouxin and Legendre, 1936; Rees and Maul, 1956; R. Clarke, 1956; Sacarriio, 1957; Clarke, 1962a), from the western North Atlantic (Verrill, 1879a, 1882c), from South Africa (Robson, 1924c, 1926c), the South Atlantic (Hoyle, 1886a), and the south Indian Ocean (Thiele, 1921; Dell, 1959a). The species is usually thought to live at about 1400 m but there is little evidence for this because all specimens have been taken with open nets, from stomachs of predators or dead-at the surface. It has been taken in nets put to a minimum of 130-150 m (Massy, 1907) and a maximum of 4 000 m (Joubin, 1924). One was dredged a t 680 m (Verrill, 1882c) so that it seems likely they sometimes, a t least, go near the bottom at about 700 m. The majority have been caught with nets fished a t 500-1 500 m. They are always caught in ones and twos although from Sperm whale stomach contents one would get the impression that they shoaled (Clarke, 1962a). From the few small stages known (Hoyle, 1886a; Massy, 1907, 1909; Pfeffer, 1912; Naef, 1923; Degner, 1925) it appears that growth is isometric in this species, the young closely resembling the adult in proportion (Fig. 39). The most obvious diagnostic features of the species (the umbrella and the “ end organs ” on the arms) are present a t a mantle length of only 1.1 cm (Grimpe and Hoffmann, 1921; Degner, 1922). Both sexes have been caught but few specimens have been sexed. A female, 9.0 cm in mantle length, was mature (Robson, 1926~). The largest recorded specimen, a male, has a mantle length of 33.0 cm (Morales, 1962).

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3.2

062

18-3 crn

0.9

9.0 cm

Fro. 39. Top row. Change in form during growth of Hietioteecthia bonellii after Neef (1923,Fig. 186) and Pfeffer (1912,Plate 24). Bottom row. Change in form during growth of Cdlitcuthb reuerua after Voee and Voss (1962,Fig. 1).

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The species is important in the diet of Sperm whales in the Azores (R. Clarke, 1956) and Madeira (Clarke, 1962a) and has been taken from stomachs of Alepisaurus ferox (Verrill, 1879a), Aphanopus carbo (Rees and Maul, 1966)and Qermo alalunga (Bouxin and Legendre, 1936). B. Calliteuthis It is currently considered that Stigmtoteuthis, Histiopsis and Meleagroteuthis should be reduced t o synonyms of Calliteuthis which should include all species within the family except Histioteuthis bonellii. Voss and Voss (1962) consider that all the species of the Atlantic can be reduced to synonyms of the five species C . reversa Verrill, 1880a, C . elongata Voss and Voss, 1962, C. corona Voss and Voss, 1962, C. eeletaria Voss, 1960a and C . arcturi Robson, 1948 but they have not yet published a full synonymy except for C. reversa. Of species taken outside the Atlantic C. miranda Berry, 1918, C. cookiana Dell, 1951, C. dojleini Pfeffer, 1912, C . meleagroteuthis Chun, 19108 and C. separata Sasaki, 1915b are for the present considered " good '' species but there are a number of other names in the literature which may have to be resurrected later. 1. Calliteuthis arcturi Robson, 1948 Stigmatoteuthis arcturi Robson, 1948 Although Voss and Voss (1962) consider this to be a distinct species they note that the name will have to be reduced to a synonym eventually. The type wasitaken at 26'54" 57'15'W with an open net fished to 3 000 m, was female and had a mantle length of about 3.2 cm.

2. Calliteuthis celetaria Voss, 1960 Two sub-species of this have been described by Voss (1960a, 1962a). C. celetaria celetaria was caught in the North Atlantic at 32'10" 34'45'W with an open otter trawl at 730-820 m. The single specimen has a mantle length of 3.9 cm and is female. C . celetaria paci$cu was taken off Borneo, Dammi Island and off the Philippines in open nets fished between 292-494 m. All six known specimens are female. They were taken in two instances at bottom temperatures of 7-6'C and ll.28OC. 3. Calliteuthis coolciana (Dell, 1951) Histioteuthis cookiana Dell, 1951 Calliteuthis rewersa (pars) Hoyle, 1886a This has been recorded from New Zealand waters, in Cook Strait (Dell, 1951) and east of North Island (Hoyle, 1886a as C . reversa).

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Hoyle’s specimen was caught with a net fished at over 2 000 m. One of Dell’s specimens, a female, had a mantle length of 9.1 cm. Specimens have been recorded from the stomach of the ling, Genypterus blacodes (Dell, 1951) and the beaks from a giant petrel Mucronectes giganteus. 4. Calliteuthis corona Voss and Voss, 1962

Calliteuthis reversa Voss, 1956b All the specimens so far recorded were taken in the Caribbean Sea, and the Gulf of Mexico with open nets used at from 59-823 m. All those sexed are females, one of which is gravid, has a mantle length of 15.6 cm and is the largest specimen. 5. Calliteuthis do$eini (Pfeffer, 1912) Stigmatoteuthis dojleini Pfeffer, 1912 Calliteuthis ocelhta Chun, 1910a

A North Pacific species this has been taken off Japan (Chun, 1910a; Pfeffer, 1912; Sasaki, 1916, 1920, 1929a) and off western Canada (Clarke, 196213). It has been taken with an open net fished at 1 200 m. Both sexes have been taken and the male has both the dorsal arms hectocotylized (Sasaki, 1929a). The largest male known has a mantle length of 21.0 cm and the largest female 9.7 cm. The species seems to form an important part of the diet of Sperm whales off western Canada (Clarke, 1962b) and has also been taken from a Sperm whale stomach off Japan (Sasaki, 1916). 6. Calliteuthis elongata Voss and Voss, 1962

Calliteuthis reversa Joubin, 1900 This has been taken at ten localities off New England and in the Mediterranean (Voss and Voss, 1962). All the specimens were found dead or dying on the surface and all showed signs of having been fed on by predators. All the New England specimens were taken singly over a period of 57 years in July and August. The two Mediterranean specimens were found years apart within a few degrees of one another. Voss and Voss (1962) think that the data suggest some hydrographic cause for these mortalities, possibly an upwelling which brings deep living animals to the surface where the greater temperature kills them. Only females have been taken; the smallest gravid female was 11.4 cm and the largest was 18.3 cm in mantle length.

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7. Calliteuthis meleagroteuthis Chun, 1910a Neleagroteuthis Boylei Pfeffer, 1900 Meleagroteuthis Hoylei of Pfeffer (1900, 1908a, 1912), Joubin (1924) and Adam, (1954) are synonyms of this species but not C. hoylei of Berry (1912d). It has been recorded from Fonseca Bay, western Central America (Pfeffer, 1900, 1908a, 1912), Oregon (Pearcy, I965), East Luzon in the Philippines (Voss, 1963a),East Indies (Adam, 1954) and from the North Atlantic (Joubin, 1924)and has been taken between 0-695 m (Joubin, 1924; Voss, 1963a). The largest specimen collected has a mantle length of 6.6 cm. 8. Calliteuthis miranda Berry, 1918

This species has been recorded from off Victoria (Berry, 1918), New South Wales (Allan, 1945) and Tasmania (Allan, 1945) and from the southern Indian Ocean (Dell, 1959a). The type was an adult female with a mantle length of 14.0 cm but the other five specimens were juvenile. The adult was caught with an open net fished to about 500 m. 9. Calliteuthis reversa Verrill, 1880a Calliteuthis meneghinii Pfeffer, 1912 Stigdoteuthk Verrilli Pfeffer, 1912 Stigmatoteuthis Chuni Joubin, 1920 Voss and Voss (1962) have published a list of previously described specimens which they regard as belonging to this species and the author has restricted his treatment to these records. They include under several synonyms, records from the western !North Atlantic (Verrill 1880a, 1882c; Pfeffer, 1912; Joubin, 1924; Johnson, 1934; Voss, 1958; Voss and Voss, 1962), the Azores (Joubin, 1924), the eastern North Atlantic (Russell, 1909, 1922; Joubin, 1920), off Senegal (Adam, 1960c) and the western Mediterranean (Naef, 1923; Degner, 1925; Morales, 1958; Torchio, 1962). Although they have been taken in open nets fished to 5 270 m, Degner (1925) found that 15.9% of the specimens in 17.1% of hauls were taken at less than about 30 m (65 m of wire out), 61.3% of specimens in 54.3% of hauls at about 30-150 m (65-300 m of wire out) and 22.7% of specimens in 28.5% of hauls at more than about 150 m (300 m of wire out). This would suggest a rather shallower habitat for the small sizes (sampled by Degner) than has often been supposed for this species. The indices given by Voss and Voss (1962), if plotted, show that, during growth, the mantle and fin become relatively narrower, the arms relatively longer and the head and fin relatively shorter. However,

200

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R. ULARKE

there seems to be a change in growth at a mantle length of 1.0-3.0 cm after which growth of these organs is isometric up to 9.0 cm in mantle length (Fig. 39). Changes in the arrangement of photophores round the eye opening have been described (Degner, 1922, 1925). The largest male among the " verified " specimens is 9.0 cm in mantle length, the largest female is 8.7 cm (Voss and Voss, 1962) and the largest unsexed specimen is 10.0 cm (Morales, 1958). The ova of a mature female measured 0.38 x 0.47 mm. Degner (1925) found that close to 70% of Mediterranean specimens were less than 0.5 cm in mantle length in both winter and summer and both seasons yielded specimens of 0.2-0.25 cm in mantle length and this suggests spawning through the year. Young specimens 0.20.35 cm were always caught within 650 km of land or under 310 km from the 200 m line; possibly suggesting spawning on the continental slope. The species has been taken from Alepisaurus stomachs on several occasions (Voss and Voss, 1962). 10. Calliteuthis separata Sasaki, 1915b

This is probably a valid species although it was considered a possible synonym of C. meleagroteuthis Chun, 1910, by Voss (1963a). First recorded from Japan (Sasaki, 1915b, 1916, 1929a) squids thought to belong to this species form a permanent item in the diet of Sperm whales caught both north and south of the Kuril island chain (Akimushkin, 1954a, 1957). Sasaki's (1915b) specimen came from about 800 m, was a male, and had a mantle length of 3.1 cm.

XVI. CHIROTEUTHIDAE

(J

:

A

This family contains two major groups, the Chiroteuthinae, the species of which are almost all in the genus Chiroteuthis and the Mastigoteuthinae containing the single genus Mastigoteuthis. The genera Grimalditeuthis and Lepidoteuthis are very close to some members of the family (Clarke and Maul, 1962) but should perhaps be regarded as representatives of two other families. It has long been known that some, if not all, Chiroteuthis species undergo a considerable change in proportions at a relatively large size. Before this was recognized (Ficalbi, 1899) many larval forms were named as species in the genus Doratopsis and this genus has remained a useful repository for any larval forms which could not be related to an adult Chiroteuthis. Joubin (1931),while admitting the larval character of many Doratopsis species, held that some species retain this form through life and that the

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genus is therefore valid. Doratopsiform stages will be examined after adult forms have been considered (page 210). A. Bigelowia 1. Bigelowia atlanticus Macdonald and Clench, 1934 A species only known from the type specimen taken at 37"N 67"12'W in the western North Atlantic, with an open net fished to about 500700 m (1 500 m of wire out). The mantle length is 9.1 cm. B. Chiroteuthis 1. Chiroteuthis f u m e h a (Berry, 1909) This has been recorded once from near Kauai Island of the Hawaii group (Berry, 1909a). It was caught in a n open net fished at about 590-1 350 m (Berry, 1914a) and has a mantle length of 3.9 cm. The bottom was coral sand and rock. 2. Chiroteuthis grimaldii Joubin, 1895 This species is only known from the type specimen taken off the Azores a t 39"43'N 33"ZZ'W in a trawl fished to 1 445 m (Joubin, 1895b). The mantle length is 3-9 cm (measured from the figure).

3. Chiroteuthis imperator Chun, 1910 This may later prove to be a synonym of C. picteti Joubin, 1894a (Voss, 1963a). Rare, but well described, it has been recorded from the Indian Ocean (Chun, 1910a; Massy, 1916b) (Fig. 40), Amboine in the East Indies (Adam, 1954), Luzon in the Philippines (Voss, 1963a) and Japan where it is seen frequently in Sagami Bay (Sasaki, 1916, 1920, 1929a). It does not appear to have been taken in a net fished to less than 550 m (Massy, 1916b) or deeper than about 1 280 m (Sasaki, 1920). It is known to grow to a mantle length of 30.0 cm (Sasaki, 1929a). Sasaki (1929a) found that the nidamental glands of two females with mantle lengths of 22.0 cm and 25.0 cm measured respectively 1.5 x 0.6 cm and 2 . 6 x l . l cm; such an expansion in the gland with a small increase in body size suggests that maturity is just being reached at this size. 4. Chiroteuthis lucertosa (Verrill, 1881) Chiroteuthis Bonplandi Verrill, 1881c Chiroteuthis Verunyi lucertosa Pfeffer, 1912 Although Pfeffer (1912) regarded this merely as an American variety of C. veranyi, later authors have considered it t o be a distinct species.

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All records are from the North Atlantic (Fig. 40), from off Nova Scotia (Verrill, 1881c; Joubin, 1924), the Gulf of Mexico (Voss, 1956b) and the central Atlantic (Joubin, 1933). It has been taken with open nets from 520 m (Voss, 1956b) to over 4 000 m (Johnson, 1934). The largest had a mantle length of 57.0 cm. The long narrow tentacles each bear a well developed light organ at their tip and it seems possible that these act as a lure for prey which can then be arrested by the tentacular suckers and pulled in on the “ line ” (Voss, 1956b). 5. Chiroteuthis macrosoma Goodrich, 1896

This should possibly be regarded as a synonym of C. picteti Joubin, 1894a (Voss, 1963a). Known only from the type, the species was taken at 12’50’N 81’30‘E in the Indian Ocean a t a depth of 870 m. The mantle length is 38.5 cm and it is female. 6. Chiroteuthis picteti Joubin, 1894a Joubin (1924) regarded both C. macrosoma Goodrich, 1896 and C. imperator Chun, 1910 as synonyms of this species and the question has not yet been resolved (Voss, 1963a). The types were described from Amboine (Joubin, 1894a) and further specimens were recovered from the North Atlantic (Joubin, 1924) (Fig. 40). It has been taken in open nets fished to 4 300 m. The largest has a mantle length (to the back of the fins) of 23.5 cm. 7. Chiroteuthis portieri Joubin, 1912 Only known from the type specimen which was taken at 29’03” 16’08’W near the Canary Islands in an open net fished to 3 600 m (Joubin, 1912, 1916). It has a mantle length of 6.7 cm.

8. Chiroteuthis veranyi (FBrussac, 1835) Loligopsis Veranyi Fkruaaac, 1835 Loligopsis vermicolaris Ruppell, 1844 Loligopsis vermicularis Vkrany, 1851 Onychoteuthis perlatus Riaso, 1854 Loligopsis perlatus Risso, 1854 Doratopsis vermicularis Rochebrune, 1884 Hyaloteuthis vermicularis Pfeffer, 1884 The adult form has been taken in the eastern Mediterranean (Degner, 1925; Hoenigman, 1958) (Fig. 37), the western Mediterranean (FBrussac, 1836; d’orbigny, 1845; VBrany, 1861; Risso, 1854; Aucapitaine, 1863; Targioni-Tozzetti, 1869a; Carus, 1890; Ficalbi, 1899; Joubin, 1893b,

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1894c, 1899, 1900; Lozano y Rey, 1905; Chun, 1910a; Pfeffer, 1912; Naef, 1923; Degner, 1925; Adam, 1942b; Morales, 1958), the eastern North Atlantic (Chun, 1913; Joubin, 1924; Bouxin and Legendre, 1936; Rees and Maul, 1956; Adam, 1960c), the South Atlantic (Adam, 1952, 1961, 1962) and the Pacific (Berry, 1963; Pearcy, 1965). The validity of further records from the Kuril region (Akimushkin, 1954a, 1955a,

1.0

1.6

u

3.6

5.0

b0

cm

Fm. 41. Change in form during growth of Chiroteuthia ueranyi after (from left to right) Naef (1923, Fig. 191). Pfeffer (1912, Plate 46, Fig. 4, l), Adam (1962, Fig. 49) and Pfeffer (1912, Plate 44). The three smallest are referable to the larval " species " Dwatopais vermicduris. All from the ventral side. Mantle lengths (excluding the " teil ") i n cm are indicated.

1957; Beteshava and Akimushkin, 1955) cannot be assessed because a satisfactory description was not given. It has been caught in open nets fished a t 150 m (Degner, 1925) and in nets fished to 2 130 m (Adam, 1961) but has been taken most frequently at 300-500 m. Off Oregon an average of 0-5 per hour tow was caught in open midwater trawls fished a t 200 m while only 0.1 were caught in samples taken at 500 m and 1000 m (Pearcy, 1965).

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The largest recorded specimen has a mantle length of 9.1 cm, is female and has ova which are 0.11 x0-15 mm in size (Morales, 1958) while another specimen with a mantle length of only 4.2 cm was considered adult by Joubin (1924). Ficalbi (1899) first suggested that Doratopsis vermicularis is the young form of Chiroteuthis veranyi and this has since become accepted after some controversy (Pfeffer, 1900, 1912; Jatta, 1903; Chun, 1910a; Issel, 1920a, 1930; Minelli, 1921). During growth from the very curious '' Doratopsis " stage the arms and tentacles become relatively longer, the head becomes relatively shorter, the body relatively wider and the fin relatively wider but remains about the same length. Shortening of the head is due to the progressive loss of a post-orbital " neck ". While larvae often have a very long tail extending beyond the fin, which is probably always present before capture, the adults have lost this (Fig. 41). The species has been taken from stomechs of dolphins (Joubin, 1894c, 1900b) and Germo alalunga (Bouxin and Legendre, 1936) and, if Akimushkin's ( 1954a, 1955a) identifications are correct, also from Sperm whales.

C. Echinoteuthis 1. Echinoteuthis danae Joubin, 1933

The type specimens were taken in the North Atlantic at 34'40" 33'16'W, 16'03" 62'29'W, 30'57" 21'00'W, off Bermuda and the Cape Verde Islands and the species has not since been recorded. The species was taken in open nets fished to as little as 60 m and as deep as 2 680 m. The largest measured, had a total length of 4.5 cm while another had a mantle length of 2.5 cm.

D. Entomopsis The status of the species referred to this genus is doubtful. E . velaini Rochebrune, 1884 is probably a young Brachioteuthis sp. The relationship of E . clouei Rochebrune, 1884 cannot be determined from the type description. 1. Entomopsis alicei Joubin, 1900

This species was recovered from three localities in the North Atlantic: 41'40" 15'15'W, 46'22" ll'l8'W and 44'30" 10'30'W (Joubin, 1900) and no further specimens have been described. They were all taken from stomachs of tuna caught at the surface and the largest has a mantle length of 3-0 cm.

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E. Chiropsis 1. Chiropsis mega Joubin, 1933

A species with very distinctive short, broad ventral arms which has 76'55'w. only been recorded once, from the North Atlantic at 25'50" It was taken in an open net fished to 3 000 m, is a sexually mature male with a penis protruding well out of the mantle opening and has a mantle length of 17.0 cm.

F. Vuldemaria 1. VaZdemaria dame Joubin, 1931

This species has been recorded twice. from the North Atlantic: 12"ll'N 35'49'W and 17'41" 60'58'W (Joubin, 1931, 1933). It was taken with open nets fished to about 500 m and 2 680 m respectively. The type has a mantle length of 6.0 cm, Joubin (1933) described the hectocotylus of the mature male.

G . Mastigoteuthis 1. Nastigoteuthis ugassizi Verrill, 1881

A species described from the western North Atlantic (Verrill, 1881c) (Fig. 42) it has since been recorded rather dubiously from 25'52" 19'22'W (Hoyle, 1886a) on the basis of fragments of tentacle found adhering t o a dredge rope. Verrill's specimens were taken with open nets fished at 647 m and 1 632 m. Both specimens were male and had mantle lengths of 4.6 cm and 9.9 cm. One contained small Crustacea in the stomach. 2. Nastigoteuthis cordiformis Chun, 1908

A widespread species (Fig. 42) recorded from the East Indies (Chun, 1908, 1910a; Adam, 1954), the Philippines (Voss, 1963a), Japan, (Sasaki, 1920, 1929a) and the North Atlantic (Joubin, 1924). It has been taken in an open net fished to 330 m (Sasaki, 1920) and in one lowered to 2 500 m (Joubin, 1924) but nearly all the specimens have been caught with nets fished between 330-720 m. Voss (1963a) considers that this is a " typical mesopelagic species ". The largest specimen has a mantle length of 9-6 cm (Adam, 1954). It should be noted that there are a number of differences between Sasaki's description (1920, 1929a) and those of Chun (1910a) and Voss (1963a).

-1

.

ma. 42. Localities from which Mastigoteuthis schmidti ( l ) ,M . agassizi (2), M . cordiformia (3), M . gluucopsis (a), M . grimaldii ( 5 ) , M . taliamani ( 8 ) , M . dentata ( 7 ) . M.Jammea (B), M . magna ( Q ) , M . Zatip'nna (lo), M . Zevimana ( l l ) , M . hjorti (12) and M . iaeleni (13) have been recorded.

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MALCOLM R. CLARKE

3. Mastigoteuthis dentata Hoyle, 1904b

This was thought to be a synonym of M . grimuldii Fischer and Joubin, 1907 by Joubin (1924) but this opinion is not beyond dispute. It has only been recorded from the Galapagos Islands and the Gulf of Panama (Hoyle, 1904b) where it was caught with open nets fished to 930 m and 2 400 m. A female had a mantle length of 14.0 cm and a male 7.2 cm. 4. Mastigoteuthis jlammea Chun, 1908

A rare, but widely distributed species (Fig. 42), this has been recorded from the North Atlantic (Chun, 1908, 1910a, 1913) and from New Zealand waters (Dell, 195913). It has been taken with open nets fished to a minimum of 820 m and a maximum of 2 500 m. The largest specimen had a mantle length of 4.8 cm. Chun (1913) described a form which was possibly a larva of this species. 5 . Mastigoteuthis glaucopsis Chun, 1908

This rare species has been recorded in the Indian Ocean (Chun, 1908), the North Atlantic (Joubin, 1933) and has been listed for S . Africa (Massy, 1925). Joubin (1933) used the varietal name athntica for his specimen. The specimens were taken with open nets fished to 1213 m and 2 680 m. The largest had a mantle length of 11.2 cm (Joubin, 1933). 6. Mastigoteuthis grimaldii (Joubin, 1895) Chiroteuthis grimaldii Joubin, 1895b Chiroteuthopsis Grimaldii Joubin, 1900 Nmtigoteuthis dentata Hoyle, 1904b Joubin (1924) recorded more specimens than any other worker but he considered M . dentata Hoyle, 1904 and M.$arnmea Chun, 1908 to be synonyms of this species, a view which is not indisputable a t present. All but one of the specimens were from the North Atlantic (Joubin, 1896b, 1924; Fischer and Joubin, 1907; Chun, 1910a, 1913; Adam, 1960c) (Fig. 42). The exception was a very doubtful record of a larva from 42'40'5 148'16'E, off south-west Australia (Allan, 1945). It has been taken in open nets fished t o a minimum of 600-800 m (Adam, 1960c) and a maximum of 5 100 m (Joubin, 1924). The two largest known to the author have mantle lengths of 7.4 cm (Chun, 1913) and 7.8 cm (Joubin, 1924).

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7. Mastigoteuthis hjorti Chun, 1913

Known only from the type specimens taken at Michael Sars stations near 36"N 40"W and 32"N 33"W and 36'5" 43'68'W (Chun, 1913). They were taken with 1 200 m and 3 000 m of wire out which possibly meant that the nets were a t depths of 400-1 000m. The largest specimen had a mantle length of 9.5 cm. The species is remarkable in having a rhombic fin stretching the length of the body similar in form to that of Thysanoteuthis. 8. Mastigoteuthis iseleni Macdonald and Clench, 1934

71'29'W Only known from the type which was taken at 39'04" in the North Atlantic with an open net fished to about 600-800 m (1 600 m of wire out). The mantle length is 6.2 cm. 9. Mastigoteuthis Zatipinna (Sasaki, 1916) Idioteuthis latipinnu Sasaki, 1916

A single specimen was described from outside Okinose Bank, Sagami Bay, Japan by Sasaki (1916, 1929a). It was caught at about 730 m, has a mantle length of 23.8 cm and is the largest known specimen in the genus. 10. Mastigoteuthis levimana Lbnnberg, 1896 This is known only from a single specimen taken a t 43"N 24'W in the North Atlantic (Lonnberg, 1896b) which had been mutilated by a dolphin. The mantle length including the hind end measures 6.0 cm. 11. Mastigoteuthis magna Joubin, 1913

Another species known only from the type specimen, this was caught at 31'44" 42'39'W (Joubin, 1913a) with an open net fished to 3 465 m. It has a mantle length of 16.0 cm. 12. Mastigoteuthis schmidti Degner, 1925

The type was caught in the North Atlantic at 46'30" 7"OO'W (Degner, 1925) and a specimen from Madeira has been tentatively referred to this species (Rees and Maul, 1956). The type was taken with 2 700 m of wire out which probably represents a depth of capture of about 1000 m. It is 4.6 cm and the Madeiran specimen is 10.7cm in mantle length. The latter came from the stomach of Alepisaurus ferox.

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13. Mastigoteuthis talismani (Fischer and Joubin, 1906) Chiroteuthopsis Talismani Fischer and Joubin, 1906 This species is only known from the type which was taken at 34’46“ 36’11‘W in the North Atlantic (Fischer and Joubin, 1906, 1907) with an open net fished in 3 176 m ( ? sounding). The mantle length is 6-1 cm.

H. Larval chiroteuthids Relationships between the named larval chiroteuthids, other than those referred to Chiroteuthis veranyi may be best seen if they are grouped according to their proportions and arranged to show any trends between the smallest and the largest specimens (Fig. 43). The smallest forms, represented by Planctoteuthis Pfeffer (1912) and Cheiroteuthis (Doratopsis) A. Robson (1924b), have very small arms, a short “ snout ”, a very long neck ” and a broad body. I n the next ‘( stage ” represented by Doratopsis sagitta Chun (1908) and Chiroteuthis (Tankaia) borealis Sasaki, 1929a, the ventral arms are much longer than the other arms and the body is narrower. The following ‘ I stage ” overlaps the previous one in size and is represented by Doratopsis lippula Chun, 1908 and Doratopsis exophthalmica Chun, 1908 in which the ventral arms are longer still, the snout ” is longer and the (‘neck ” is shorter. The largest “ stage ” represented by Chiroteuthis = Doratopsis of Joubin (1931) is really just a much larger edition of the previous one. Chiroteuthoides hastula Berry, 1920 is a small larval form having a short neck ” and ‘ I snout ” and consequently it does not readily fit into the above series. At present, it is not possible to relate these various forms with adults but it is possible that some of them may turn out to be young of Mastigoteuthis. Joubin’s Chiroteuthis = Doratopsis (1931) is very similar to Chiroteuthis imperator. (‘

1. Planctoteuthis stage Pfeffer, 1912

Pfeffer (1912) recorded this from the North Atlantic at 41’6“ 2 l”6’W and named it Chiroteuthis (Planctoteuthis) planctonica. The specimen had a mantle length of 0-64 cm. Robson (1924b) described, FIQ. 43. Various larval chiroteuthids arranged in groups showing similarity. A, Planctoteuthia after Pfeffer (1912, Plate 46, Fig. 6); B, Cheiroteuthis (Doratopaisstage) A after Robson (1924b, Fig. 1); C, Planctoteuthis after Issel (1920, Fig. 9); D, Doratopsis sagitta after Chun (1910, Plate 46, Fig. 2); E, Chiroteuthis (Tankaiu) borealis after Sasaki (1929, Plate 24); F, Chiroteuthia veranyi after Berry (1963, Fig. 2); 0 , Doratopsia Zippula after Chun (1910, Plate 46, Fig. 7); H, Doratopais ezophthalmica after Chun (1910, Plate 46, Fig. 2); I, “ Doratopsis-Chiroteuthia larva ” of Joubin (1931, Fig. 47). C from the dored, the others from the ventral side. Mantle lengths (excluding the “ tail ”) in cm are indicated.

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A

B

F

C

1.3 -2.0

I

1.97

db 7.58

FIG.43.

cm

I *2

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MALCOLM R. CLARKE

under the name Cheiroteuthis) Doratopsis stage) A, a specimen very similar to C. (P)planctonica from near Durban, South Africa having a mantle length of 0.6 cm. 2. Doratvpsis sagittcc Chun, 1908

Only known from Chun's two specimens (1908, 1910a) which were measured in detail by Pfeffer (1912) this " species " was recovered from the North Atlantic a t 14'39" 21'61'W and the Indian Ocean at 30°6'S 87'50'E. It was taken in open vertical nets fished to 1 800 m and 2 500 m and the mantle lengths to the posterior end of the fin, are 4.2 cm and 6-45 cm. (Pfeffer, 1912 found a discrepancy between the text and the figures: the figures indicate a mantle length of 1.4 and 2.16 cm). 3. Chiroteuthis (Tankaia) borealis Sasaki, 1929 This is clearly a doratopsiform larval type and the six or eight oblique rows of minute suckers on the tentacles suggest that it is a larval form of a Mastigoteuthis species, possibly M . cordiforrnis which has been recorded from Japanese waters (Sasaki, 1920, 1929a) i.e. from the same region where the single specimen of C. (T.)borealis was taken. The mantle length is 1.2 cm (including the broken tip of the pen).

4. Doratopsis lippula Chun, 1908 This has been taken from the Atlantic at 11'28's 10'24'E* and 31'20" 34'56'W (Chun, 1908, 1910a, 1913). It was taken with open nets fished to as much as 4000 m and one had a mantle length of 4.25 cm (calculated by Pfeffer, 1912 from Chun, 191Oa). 5.

Doratopsis exophthalrnica Chun, 1908

Very similar to the previous species this has been taken at several stations in the North Atlantic (Chun, 1908, 1910a, 1913; Massy, 1913, 1928a; Degner, 1925) and in the Indian Ocean (Chun, 1910a). A damaged and doubtfully identified specimen was recorded from the Chagos Islands (Robson, 1921). It has been taken with open nets fished to as little as 100 m (200 m of wire out) (Chun, 1913) and to as much as 2 500 m (Chun, 1910a). The mantle lengths range between 0.95 cm and 2.5 cm (Chun, 1910a). 6. Chiroteuthis = Doratopsis stage Joubin, 1931 Recovered near the Azores at 37'44" 25'56'W fished to 100 m, this has a mantle length of 4.7 cm.

* Given erroneously &B ll"28'N by Chun.

in an open net

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7. Chiroteuthoides hastula Berry, 1920

Only known from Berry's specimen, this was taken at 28'59" 69'22'W and 200-0 m and has a mantle length of 1.0 cm.

XVII. LEPIDOTEUTHIDAE The scaled squid " Lepidoteuthis grimaldii, while being closely allied to the preceding family in many respects (Clarke and Maul, 1962)) has a number of differences which distinguish it from both Chiroteuthis and Nastigoteuthis so that it is convenient to place it in a distinct family for the present.

A. Lepipidoteuthis 1. Lepidoteuthis grimaZdii Joubin, 1895

This species has been collected in the North Atlantic (Joubin, 1895a, 1900; Rees and Maul, 1956; R. Clarke, 1966; Clarke, 1960, 1964; Clarke and Maul, 1962) and the South Atlantic a t 31'11's 33'13'W (Merritt, 1964). One young specimen was taken in an open net fished to 245 m and another in a closing net fished 100-270 m; both nets were supplied with depth gauges (Clarke, 1964). Although these are

the only young stages known, they show the changes of form associated with growth and there is some suggestion of a fairly rapid change when the mantle length is round about 7.0 cm (Fig. 44). At this size the arms and head become relatively longer, the tentacles relatively shorter and are lost later, and the body relatively broader. After this rapid change, growth appears to be isometric. The adult " scales are represented by papillae with knobs on in the juveniles. The largest mantle known was 97.0 cm in length when fresh and that is of a female. Nidamental glands of three females are very large, suggesting that a large egg mass is secreted. Although the ovaries are spent, the oviducts are full of eggs and this possibly suggests that the eggs are stored there temporarily prior to laying (Clarke and Maul, 1962). The two juveniles were caught in April and June. All specimens, with the exception of the juveniles, have been taken from stomachs of predators or immediately after regurgitation. Known predators are the Sperm whale in whose diet this squid is quite important to judge from beaks in the stomach (Clarke, 1962a), Qrampua grisew (Joubin, 1895a), Aphanopus carbo (Clarke and Maul, 1962) and a tuna probably Qermo obesw (Clarke and Maul,1962).

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MALCOLM R. CLARKE

A

6.0

8.5

97.0

FIG. 44. Change in form during growth of Lepidoteuthia grimaldii after Clarke (1964, Fig. 1). All from the ventral side. Mantle lengths in cm are indicated.

XVIII. GRIMALDITEUTHIDAE A. arimalditeuthis 1. Brimalditeuthis bonplandi (VBrany, 1837) Loligopsis bonphndi VBreny, 1837 QrimalditeuthisRichurdi Joubin, 1898c This species has been caught at various localities in the North Atlantic (V&any, 1837; d'orbigny, 1845; Joubin, 1898~;Chun, 1913; Voss, 3956b), at 28"s 28"W in the South Atlantic (Pfeffer, 1912) and

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it has been listed for South Africa (Massy. 1925). Chun's (1913) specimen differs slightly from the other specimens. 'l'wo specimens were found a t the surface (\'&any, 183T; Joubin, 1 8 9 8 ~and ) one was taken in a n open net fished t o 2 600 m (Chun. 1913). The largest specimen has a mantle length of 22.G cm (Joubin, 1 8 9 8 ~ ) . X specimen was recovered from the stomach of Alepisaurus fer0.r Voss, 1956b). Enoptrotruthis spinicauda (Berry, 1920) is probably a larval form and Grimpe (1965) considered t h a t i t is probably a young specimen of G, bonplandi. It was recovered from 28'51'N TO'OS'W in the North Atlantic at less than 55 m depth. The mantle length is on1.v 1.7 cm.

XIX. CRANCHIIDAE This family may be divided into two sub-families which are easily distinguished, the Craiichiinae aiid the Taoniinae. Members of the Cranchiinae have cartilaginous tubercles on the mantle and several comparatively small light organs on the bulb of the eye while squids in the 'I'aoniinae have no tubercles aiid no more than three light organs on tlie bulb of' the eye. Ascocranchia ,joubi)ii Toss 1!j62b is a n intermediate forin but the division of this large familv into two is useful for our present purposes. In both sub-families taxonomic difficulties arise from tlie naming of larval forms as separate species and, particularly in the Taoniinae. from the almost indiscriminate use of generic names. Until a large number of specimens. in addition to the types, can be examined many questions of relationship aiid nomenclature will remaiii unanswered but here a n attempt has been made t o outline the problem. C'RANCHIINAE

A. Cranchin A4clearly defined genus, i t is usually regarded as containing onr widely distributed species (Fig. 45) although geographical differences have been noted (Hogle, 1904b; Robson. 1924r) and Pfeffer (1912) named two forms C. scabra hispidn and C . s. tenuit~irtaczilata. Cruiichia scubrcc Leach, 181i Philori exis Eylais d'0rbigny , 1835-1 848 Crauchia hispida Pfeffer, 1884 Crunchin teri uite,ituciLZata Pfeffer, 1884 One of the commonest cranchiids (Figs. 45,4G), this has been recorded from the North Atlantic (d'Orhigny, 183% 1848; Steenstrup. 1861 ; 1.

216

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FIG. 45. Cramhin acabra from the right side (from a colour slide of P. RI. David).

Chun, 1910a. 1913: Pfcffw. 1912; Jou1)iu. 1920; \'ow. 1956.1M6a and b; Rees and Maul, 1956; Adam, 1 9 6 0 ~ )the . South Atlantic (Leach, 1817; Owen, 1836: Gray, 1849; Tryon, 1879; Thiele, 1921: Robson, 1 9 2 4 ~ ; Ada,m. 1962). the Indian Ocean (Chun. 191Oa; PfeEer. 1912; Thiele,

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I921), the East Indies (Pfeffer, 1912), Philippines (Voss, 1963a), the South Seas (Pfeffer, 1912),Japan (Sasaki, 1916, 1929s) and the eastern Pacific (Hoyle, 1904b; Pearcy, 1965). It has been taken with open nets fished to 3 500 m (Chun, 1910a) but has been taken at the surface at night (Hoyle, 1904b; Chun, 1913; Adam, 1960c) and frequently at less than 500 m. The smallest known young are essentially similar to the adult although Adam (1960~) described a, specimen, possibly this species, with a mantle length of 0.6 cm which did not have tubercles all over the mantle. The largest recorded male and the largest female are both 8-2 cm. in mantle length (Chun, 1910a; Voss, 1963a), while the largest unsexed specimen is 11.0 cm (Rees and Maul, 1956). A male 3.5 cm in mantle length is hectocotylized (Pfeffer, 1912). Specimens have been taken from the stomach of Alepisaurus ferox (Rees and Maul, 1956).

B . Crystalloteuthis A genus containing two poorly known species which are very similar to one another and may prove to be the same species. Both species have the short arms and protruding eyes typical of larval cranchiids but are distinguished from all other species by the possession of single cartilaginous tubercles a t each of the funnel-mantle fusions. 1. Crystalloteuthis beringiana Sasaki, 1920

This North Pacific form has been recovered from the Aleutian Islands, the Bering Islands and Japan (Sasaki, 1920, 1929a) and is common in the Bering Sea (Kondakov, 1941). It has been taken with open nets fished to as little as 107 m and as much as 4 800 m (Sasaki, 1920). The largest specimen known has a mantle length of 2.7 cm (Sasaki, 1929a). 2. Crystalloteuthis glacialis Chun, 1906

This is the southern form of the genus which has been recorded from the Indian Ocean and Australian sectors of the Antarctic between latitudes 44"s and 65"s (Chun, 1906, 1910a; Dell, 1959a). It has been taken with a closing net between 750 and 500 m. and with horizontal open nets towed between about 750 and 1710 m (Dell, 1959a). The largest specimen known has a mantle length of 3.5 cm. A.P.B.4

I

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C . Liocranchia The species of this genus form a regular part of catches made with larger nets fished in the upper levels of the sea. They are clearly characterized by two V-shaped lines of tubercles with the apex of the V near the fusions between funnel and mantle. Lamberg (1896b) showed that young specimens are globular and become elongated later in life. Two globose forms, L. gardineri Robson (1921) and L. globulus Berry (1909a), have been named as separate species and whereas the former has peculiarly thickened tentacle stalks which distinguish it from other forms, the latter will be considered under L. reinhardti here from which i t cannot be readily distinguished. Voss (1963a) has pointed out considerable discrepancies between the descriptions of L. reinhardti by various authors and the examination of specimens from a wide area will be necessary to sort them out. 1. Liocranchia gardineri Robson, 1921 Known only from the type specimen this species was found off Desroches atoll (Robson, 1921). It was caught in an open net fished to about 370 m and measures 1.0 cm from the mantle apex to the base of the arms and is probably larval. The curious tentacular stalks could result from regeneration after damage. 2. Liocranchia intermedia Robson, 1924 This species is known only from the type which is probably a male of L. reinhardti (Steenstrup, 1856), to judge from descriptions by Robson (1924~) and Voss (1962e). It was recorded from Natal, South Africa, and was taken with an open net fished at 475 m. The mantle length is about 10.7 cm. 3. Liocranchia reinhardti (Steenstrup, 1856) Leachia Reinhardti Steenstrup, 1856 Cranehia Reinhardti Steenstrup, 1861 Loligopsis (Perotis) Reinhardti Tryon, 1879 Perotw Reinhardti Rochebrune, 1884 Liocranchia Brockii Pfeffer, 1884 Cranchia Brockii Joubin, 1894a Cranchia (Liocranchia) globula Berry, 1909a A species recorded from the North Atlantic (Steenstrup, 1856; Hoyle, 1886a; Lbnnberg, 1896b; Issel, 1908; Chun, 1910a; Pfeffer, 1912; Bouxin and Legendre, 1936; Voss, 1955, 1958) (Fig. 47), the South Atlantic (Chun, 1910a; Pfeffer, 1912; Robson, 1924; Adam, 1961),

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the Indian Ocean (Chun, 1910a), the East Indies and the China Sea (Pfeffer, 1884, 1912), the Philippines (Voss, 1963a), Japan (Sasaki, 1916, 1929a), Hawaii (Berry, 1909a), the South Seas (Pfeffer, 1912), New South Wales (Pfeffer, 1912), and Chile (Pfeffer, 1912). Its occurrence in the Mediterranean seems doubtful (Naef, 1923). It has been taken near the surface (Pfeffer, 1912; Adam, 1961) and most specimens have been caught in open nets fished a t less than 500 m depth. Young specimens are more rotund. The largest male known to the author is 15.7 cm and the largest female is 10-7cm in mantle length (Voss, 19638). A male has the left ventral arm hectocotylized a t a mantle length of 4.6 cm (Ltinnberg, 1896b), but Voss (1963a) observed no spermatophores although a number of adults were a t hand. Specimens have been recovered from clewno alalunga stomachs (Bouxin and Legendre, 1936). 4. Liocranchia valdiviae Chun, 1906

This species has been recorded from the Indian Ocean (Chun, 1906, 1910a) and from Japan (Sasaki, 1929a) (Fig. 47). It has only been taken in open nets fished in excess of 900 m (Sasaki, 1920). The young of less than 1.0 cm mantle length are similar to the adult but more globose. The largest male is 4.0 cm and the largest female, which is mature, is 6.3 cm in mantle length. D . Pyrgopsis The members of this genus are characterized by a longitudinal row of tubercles running along the mantle from the funnel-mantle fusion on each side. Such tubercle rows also characterize Leachia and Drechselia (Fig. 48). Pyrgopsis species have very short arms, an elongated " rostrum " to the head and protruding eyes, all of which are probably larval characters. It seems reasonable to assume that Leachia and Drechselia species pass through a Pyrgopsis-like stage, but the presence of a hectocotylus on a male of P . pacijca precludes the possibility that all Pyrgopsis species are larval forms (Sasaki, 1929a) and the genus will be kept separate for the present. 1. Pyrgopsis atlantica Degner 1925 Known only from the type, this was recovered from 36'13" 9'44'W in the North Atlantic (Degner, 1925). It was taken with 65m of wire out which probably represented a depth of about 30 m. The mantle length is 5.0 cm.

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3.3

9.3

18.3

cm

FIQ. 48. Pyrgopsis pacific5 (left) after Pfeffer (1912, Plate 47, Fig. 16), Leachia cyclura (centre after Pfeffer (1912, Plate 47, Fig. 3) and Drechselia danae (right) after Joubin (1931, Fig. 33). All from the ventral side. Mantle lengths in cm are indicated.

2. Pyrgopsis paeiJica (Issel, 1908) Zygaenopsis pacijcu Issel, 1908 ? Loligopsis zygaena Vdrany, 1851 ? Zygocranchia zyguena Hoyle, 1909a Euzyguena pacificu Chun, 1910a This species (Fig. 48) has been recorded off Japan (Chun, 1910a; Sasaki, 1916, 1929a) between Tahiti and Pango Pango (Issel, 1908), off New Zealand (Massy, 1916c), East Australia (Allan, 1945), South Africa (Robson, 1924c; Voss, 1962e), from the North Atlantic (Thiele, 1921) and from the Mediterranean (VBrany, 1851). It has been taken near the surface (Massy, 1916c; Thiele, 1921) and with an open net fished to 600 m. The largest sexed male recorded is 5.2 cm (Sasaki, 1929a), the largest female is 5.0 cm (Sasaki, 1916) and the largest unsexed

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specimen is 7-2 cm in mantle length (Allan, 1945). While the largest male and another of 4-7 cm mantle length was reported as being hectocotylized (Chun, 1910a; Sasaki, 1929a), the largest female has small papilliform nidamental glands (Sasaki, 1929a). 3. Pyrgopsis lemur Berry, 1920 This is very close to, and may even be an Atlantic form of, P . schneehageni (Pfeffer, 1884). It has been recorded from the western North Atlantic from east of Cape Hatteras (Berry, 1920) and the Caribbean region (Voss, 1958). It has been taken at the surface and at 46 m depth. The largest specimen has a mantle length of 3.2 cm (Berry, 1920).

Pyrgopsis rhynchopfiorus Rochebrune, 1884 Zygaenopsis zygaena Pfeffer, 1900 This is possibly the same species as P. paci$ca (Issel, 1908). It has been recorded from Agulhas bank (Rochebrune, 1884) and St. Paul’s island (Pfeffer, 1912). The mantle length of the type is 2.0 cm. 4.

5. Pyrgopsis schneehageni (Pfeffer, 1884)

Loligopsis Schneehageni Pfeffer, 1884 Taonius schneehageni Hoyle, 1886a This may be a form of P . paci$ca (Robson, 1924c) and has been recorded from Chile (Pfeffer, 1884) and from 50 miles S.W. of Cape Mala, Panama (Boone, 1933). Boone’s specimens were dredged from 550 m and included the largest known specimen with a mantle length of 10-6 cm.

E. Leachia The two species in this genus are probably distinct but not all the synonyms listed for L. cyclura can definitely be excluded from being L. eschscholtzi. 1. Leachia cyclura Lesueur, 1821 Loligopsis cyclurus FBrussac, 1832 after d’orbigny, 1835-1848 Loligo Leachii Blainville, 1823 Perothis pellucida Rathke, 1833 Loligopsis cyclura d’orbigny, 1835-1848 Leachia ellipsoptera Steenstrup, 1861 This species (Fig. 48) has been recorded from the North Atlantic (Steenstrup, 1861a; Lonnberg, 1896b; Joubin, 1905b, 1920; Pfeffer, 1912; Chun, 1913; Rees and Maul, 1956; Voss, 1960a), off South Africa

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(Lesueur, 1821 given as "Pacific ocean" 37'5 33"E),from the Indian Ocean (d'orbigny, 1835-1848, 1845; Gray, 1849; Steenstrup, 1861) and the Philippines (Elera, 1896). It has been taken dead or dying a t the surface (Richard, 1903; Joubin, 1920) and has been caught in open trawls fished as deep as 1 000-1 100 m. (Voss, 1960a). The largest specimen known to the author has a mantle length of 14.5 cm (Rees and Maul, 1956). Females 4.5 cm and 5.5 cm in mantle length have very large nidamental glands and are gravid (Voss, 1960a). Ltrnnberg (1896b) mentioned a female with four large nidamental glands. 2. Leachia eschscholtzii (Rathke, 1835) Perothis eschscholtzii Rathke, 1835 This has been obtained from 28"s 310"W* (Rathke, 1835; Chun, 1910a) and 39"s 53"W (Pfeffer, 1912). The largest specimen has a mantle length of 8.45 cm (Pfeffer, 1912). Chun (1910a) mentions that his material includes a t least one mature female.

F. Drechselia A genus containing a single species having several unusual features for a cranchiid the chief of which is its robustness (Fig. 48). 1, Drechselia danae Joubin, 1931

The two known specimens of this species were caught in the eastern Pacific a t 6'40" 80"47'W and a t a depth of 2 680 m. with an open net (Joubin, 1931). The female is 17.1 cm in mantle length (from the figure) and is adult. The male has an elaborately hectocotylized right ventral arm and is roughly the same size as the female.

G. Ascocranchia A genus with a single species which has features of both the Cranchiinae and the Taoniinae (Voss, 196213). 1. Ascocranchia joubini Voss, 1962

Based on a specimen caught by the Princess Alice this was taken a t 45'02" 13'05'W in the North Atlantic (Voss, 1962b). It was caught near the surface, is a female with four nidamental glands and has a mantle length of 6.3 cm.

H. Egea The single species in this genus is probably related to Liocranchia but it has no cartilaginous tubercles on the mantle. * Position as given in paper.

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1. Egea inermis Joubin, 1933

This is known only from the types which were collected at 33’51” 66”43’W with an open net fished to 50 m. The mantle length of the largest is 4.4 cm. TAONIINAE

Most of the generic names within this sub-family are of little value and have been used indiscriminately in the past. I n some cases a generic term has been used to delineate a structural form which almost certainly corresponds to a development stage. Thus, Bathothuuma, Sandalops and Corynomma have all the features of young larval taoniids as indicated by species in which a sufficiently good series of sizes have been collected to determine the changes in form during growth (Muus, 1956). These early larval features are, eyes on long peduncles, very short arms, an elongation of the head anterior to the eyes or “rostrum ” and a sac-like body with small terminal fins. (Fig. 49). The species of the genera Taonidium and Teuthowenia have eyes on rather shorter peduncles bet still have short arms and a distinct rostrum although the latter is short in some species. Fusocranchia has sessile eyes and no rostrum but it also has minute arms, a sac-like body and pedunculate fins. The species in Megalocranchia and Helicocranchia have sessile eyes, relatively long arms and virtually no rostrum. Throughout the series there is also a trend towards a more elongate and pointed body with larger elongated fins; in the genera Taonius, Phusmatopsis and Galiteuthis, which reach from 30 cm to 1 m in mantle length, these trends are extended. I n Fig. 49 the developmental trends are shown longitudinally and the genera have been grouped transversely according to structural features which either relate them to, or separate them from, other species of their own “level” or of other “levels” of development. It is hoped that further work on developmental series will connect up some of these “genera”. I n the light of the above remarks, it will be seen that the following ecological details must be treated with extreme caution.

I. Sandabps The members of the three species are all extremely small and have early larval characters (Fig. 49). 1. Sandalops ecthambus Berry, 1920

The type and only specimen was taken north of Little Bahama

Bank in the North Atlantic at a depth of 0-100 m. It has a mantle length of 2.2 cm. K’

Sandalops Bathothaurna Corynomrna

Taonidium teuthowenia Fusocranchia

Helicocranchia Megalocranchia

FIG.49. Genera of the Taoniinas arranged in four groups possessing broadly similar features. Progression down the figure shows a progressive loss of larval features. See text for explenation (page 226).

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2. Sandalops melancholicus Chun, 1906 Hensenioteuthis rnelancholicus Massy, 1925 This is only known from a specimen taken to the north east of Tristan da Cunha a t 32"8'S 8"28'W with a vertical net fished from 1000 m. It has a mantle length of 1.15 cm. 3. Sandalops pathopsis Berry, 1920 The type is the only specimen described and was taken in the North Atlantic a t 32"33'N 72'14'W with an open net fished to 1 100 m. Its dorsal mantle length is 0.8 cm. This is probably an earlier stage of the species named S. ecthambus.

J. Corynomrna This genus contains a single species of small specimens with early larval features (Fig. 49) but mainly differing from Sandalops species in having a photophore on the liver. 1. Corynomma speculator Chun, 1906 Cranchiidarum Chun, 1903 Liguriellu podophthalma Issel, 1908 Specimens referred to this species have been recorded from the North Atlantic (Chun, 1906, 1910a, 1913), the Mediterranean (Joubin, 1924), the South Atlantic (Issel, 1908), the Indian Ocean (Chun, 1906, 1910a) and the species has been listed for South Africa (Massy, 1925). Although a young specimen was taken a t the surface (Chun, 1913) all other specimens were taken in open nets fished deeper than 600 m, and three in open nets fished to 2 000 m and over (Chun, 1906, Joubin, 1924). The largest specimen has a mantle length of 3.2 cm (Chun, 1906). Voss (1960a) considered that this might possibly be the juvenile of

Phasmatopsis oceanica.

K. Bathothauma Although the specimens of this genus grow to quite a large size and possibly reach maturity they retain many larval features (Fig. 49). 1. Bathothuma lyromma Chun, 1906 A widely distributed species, this has been recorded from the North Atlantic (Chun, 1913; Joubin, 1920; Thiele, 1921; Beebe, 1930 photo only; Desbrosses, 1938; Voss, 1960a), the Philippines (Voss, 1963a), Tasmania (Allan, 1940, 1945) and from the Eastern Pacific (Hoyle, 1909b). A small specimen has been taken near the surface

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(Allan, 1940) but all other specimens have been taken with open nets fished to 695-3 000 m with the exception of one caught in a net fished to 200 m (Voss, 1960a). Voss (1963s) figured the largest known male with a mantle length of 11.4 cm and illustrated a penis although no spermatophores were shown or mentioned in the text. The largest female has a mantle length of 8.0 cm (Voss, 1960a); whether this female or that described by Thiele (1921) are mature is not clear. Published descriptions leave some doubt as to whether the mature animal has yet been described. There are a number of differences between Voss’s large Philippine specimen (1963a) and the other specimens described but these differences may well be due to development as they show the same trends of growth described above for other taoniids (page 225, Fig. 49). Desbrosses’ (1938) specimen had a mantle length of only 1.8 cm. This differed from the larger specimens in having relatively longer eye stalks; the “appendix” of the eye is much more elongated.

L. Taonidium This genus contains some specimens in a rather later “stage of development” than the preceeding forms; the eye stalks and the rostrum of the head are shorter while the arms are still very short (Fig. 49). 1. Taonidium chuni (Pfeffer, 1912) Taonidium sp. juv. Chun, 19108 Specimens referred to this species came from 0’25” 7’E, near St. Thome (Chun, 1910a; Pfeffer, 1912), and from 25“s 57‘42’E (Thiele, 1921). The type was caught in a vertical net fished from 2 000-0 m. The type has a mantle length of 0.9 cm. 2. Taonidium suhmi (Hoyle, 1885~) Taonius suhmii Hoyle, 18868 Procaliates auhmii Lankester, 1884 Hoyle (1885c, 1886a) described several specimens under this name which vary in shape from a very young larval type with long eyestalks through a later larval type with short eyestalks and small arms to a larger specimen with relatively long arms. There is little basis for the belief that these are all the same species as they came from widely dispersed stations. Chun (191Oa) considered these were juveniles of Qaliteuthis arnucta and referred two of his own specimens to 8.

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(Taonidium) suhmi, but these have little in common with T . suhmi Hoyle, 1885 and will be dealt with under Baliteuthis armuta. Various specimens have been called by this name but a reassessment of each is beyond the scope of this work and will be necessary before a discussion of distribution can be attempted. 3. Taonidium incertum Pfeffer, 1912 Known only from the type this was taken at 47'30" a mantle length of 0.6 cm.

16'W, and has

4. Taonidium pfefferi Russell, 1909

This has been recorded from various localities in the eastern North Atlantic (Russell, 1909; Pfeffer, 1912; Massy, 1913; Degner, 1925; Bouxin and Legendre, 1936) and the Mediterranean (Degner, 1925). It has been caught in open nets fished to a depth of 550 m but Russell (1909) thought that it is probably a surface form and Degner (1926) found that 18 out of 26 were caught with less than 300 m of wire out (i.e. at a depth of less than 150 m). The largest specimen has an estimated mantle length of 3-7 cm (Massy, 1913). Two specimens were recovered from Bermo alalunga stomachs (Bouxin and Legendre, 1936).

M. Teuthowenia The specimens referred to this genus have similar larval characters to Taonidium and also have distinct but short eye stalks (Fig. 49). 1. Teuthowenia anturctica Chun, 1910 Owenda n. sp. Chun, 1903c This was considered a synonym of Desmoteuthis megabps (Prosch, 1849) by Muus (1956) on rather inadequate evidence (Dell, 1959a). It has been recorded from 55'57'5 16'14'E (Chun, 1910a), from off New Zealand (Massy, 1916c) and from the Southern Ocean at 64'21'5 116'02'E and 65'10'5 109'32'E (Dell, 1959a). It has been taken at the surface (Massy, 1916c) and in an open vertical net fished to 2 000 m (Chun, 1910a). The largest specimen has a mantle length of 1-3 cm (Chun, 1910a).

2. Teuthowenia corona Berry, 1920 The single specimen known in this species has arms approaching those of Megalocranchia in length but has other features of Teuthowenia. It was caught at 32"27'N 68'22'W at 100-0 m and has a mantle length of 2.7 cm.

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3. Teuthowenia elongata Sasaki, 1929 Having a very elongate body but otherwise being typical of Teuthowenia this has only been recorded off Misaki, Japan (Sasaki, 1929a). The type has a mantle length of 1.6 cm. 4. Teuthowenia tagoi Sasaki, 1929

A species very close to the last this has only been recorded from Enoura, Japan, and the type has a mantle length of 3.2 cm (Sasaki, 1929a).

N. Toxeuma Although members of the genus have the larval features of the head described for Taonidiurn and Teuthowenia the body is very elongated and sharply pointed. 1. Toxeuma belone Chun, 1906 Cyanchiidarum Chun, 1903c This species has been recorded from l0"S'S 97'14'E in the Indian Ocean (Chun, 1910a) and from four stations in the North Atlantic (Chun, 1913). It has been taken in open nets fished to a maximum of 2 400 m (vertical) and to less than 600 m (1 200 m wire out) (Chun, 1910a, 1913). The largest recorded has a mantle length (i.e. gladius length) of 7.1 cm.

0.Megalocranchia The species of this genus have more adult features than the genera discussed above. They have sessile eyes which are sometimes very large, the rostrum of the haad is short, the arms are a t least equal in length to the rest of the head, the body is elongated and pointed and the fins have a long fusion with the body (Fig. 49). Very few specimens referred to this genus have been sexed or had comment made on their maturity so that many of them are probably immature. 1. Megalocranchia abyssicola (Goodrich, 1896) Taonius abyssicola Goodrich, 1896 Desmoteuthis abyssicola Pfeffer, 1900 This species has been recorded from the Laccadive Sea (Goodrich, 1896). It has been taken in open nets fished to 1 660 m and 2 500 m. The largest specimen has a mantle length of 7.6 cm.

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2. Megalocranchia fisheri (Berry, 1909) Helicocranchia Jisheri Berry, 1909

This has only been taken in Pailolo Canal, Hawaii (Berry, 1909, 1914a) where it was dredged at 510 m on an ooze bottom. The mantle length was approximately 4.65 cm. 3. Megalocranchia maxima Pfeffer, 1884 Desmoteuthis mximu Pfeffer, 1900 Taonius maximus Hoyle, 1886 This has been recorded from the Cape of Good Hope (Pfeffer, 1884) and from Japanese waters (Sasaki, 1920, 1929a). Off Japan it was taken at 660 m. A male 6.0 cm in mantle length is mature (Sasaki, 1929a) and the largest specimen has a mantle length of 6.3 cm (Sasaki, 1920). 4. Megalocranchia papillata (Voss, 1960) Easily distinguished by the papillae on the mantle and funnel this is only known from the type which was caught at 32'05'N, 64'38'W in an open net fished at about 600-700 m (with 1500 m of wire out). The mantle length of this male is 4.0 cm (Voss, 1960a). 5 . Megalocranchia pardus Berry, 1916 A Pacific species, this has been recorded from the Kermadec islands (Berry, 1916a), New Zealand (Dell, 1952) and possibly off eastern Australia (Allan, 1945). The type was stranded and the other specimens were taken near the surface. The largest specimens have a mantle length of 5.0 cm (Berry, 1916a; Dell, 1952).

P. Helicocranchia The separation from Megalocranchia of some species under the name Helicocranchia is possibly not justified although the type of the latter genus differs in having pedunculate fins. 1. Helicocranchia pfefferi Massy, 1907

Teuthowenia (Helicocranchia)pfefferi Bouxin and Legendre, 1936 Muus (1956) placed this in synonymy with Desmoteuthis megalops (see Taonius megalops below) but until more evidence can be produced it seems better to keep it a distinct species. It has only been recorded from waters south-west of Ireland (Massy, 1907) and with some hesitation in the Bay of Biscay (Bouxin and Legendre, 1936). There is some confusion over the depth at which the

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MALCOLM R. CLARKE

type was caught with an open trawl; it was given originally as 650 fathoms (1 190 m) and later as 350 fathoms (639 m) (Massy, 1909). The largest measured specimen has a mantle length of 3.9 cm (Massy, 1907). All specimens other than the type were recovered from Tuna stomachs in which as many as sixteen specimens were found in a single stomach (Bouxin and Legendre, 1936). 2. Helicocranchia beebei Robson, 1948 A species only known from the rather briefly described type specimens taken to the south and south-east of COCOSIslands, the Galapagos Islands at the surface, and with open nets fished to a maximum of 1520 m. The only specimen measured has a mantle length of 5.4 cm.

Q . Anomnlocranchia The single species placed in this genus would be better grouped with Megalocranchia species. 1. Anomalocranchia impennis Robson, 1924

This species is only known from the type which was caught off South Africa with an open net fished to 760 m (Robson, 1924~).The mantle length is about 5.7 cm. R. Hensenioteuthis A genus containing only one species which Massy (1916b) removed to Teuthowenia. 1. Hensenioteuthis joubini Pfeffer, 1912

This has been recorded from the North Atlantic (Pfeffer, 1900; Joubin, 1920) and from the Indian Ocean (Massy, 1916b). It has been taken in open nets fished t o 400 m (Pfeffer, 1900) and to 1000 m (Joubin, 1900; Massy, 1916b). The largest has a mantle length of 1.4 cm (Massy, 1916b).

S . Fusocranchia 1. Fusocranchia alphu Joubin, 1920

This has been recorded from the North Atlantic a t 32'18" 23'58'W and possibly at 36'46" 26'41'W and 37'35" 24'40'W (Joubin, 1920). The specimens were taken with open nets fished to 1 000 m (the type), 3 250 m and at the surface. The largest has a mantle length of 0.97 cm and is almost certainly immature.

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T. Phasmatopsis I n this genus we may group three adult forms having light organs on the ventral side of the liver. Since the affinities of the genus were discussed by the author (Clarke, 1962d) another species has been added (Voss, 1963b). 1. Phasmatopsis cymoctypus Rochebrune, 1884 Loligopsis pavo d'orbigny, 1835-1848 (pars)

Taonius cymoctypus Hoyle, 1885b This has been recovered on two occasions, both from the vicinity of Madeira (Rochebrune, 1884; Clarke, 1962d) and both found dead at the surface. The specimens have dorsal mantle lengths of 79.0 cm and 81.0 cm and one is an adult female (Clarke, 1962d). The nidamental glands are 12.0 cm in length; the ova varied in size and colour and this led the author to suggest that ova are possibly shed in small numbers throughout adult life (Clarke, 1962d). 2. Phasmatopsis oceanica (Voss, 1960) Carynoteuthis oceanica Voss, 1960a Megalocranchia abyssicola Joubin, 1924 This species has been recorded from the North Atlantic at 32'08" 64"33'W and 32'12" 64'36'W (Voss, 1960a) and as Megalocranchia abyssicola a t 30'45" 25'47'W (Joubin, 1924). It was caught a t 0-260 m, a t night (Joubin, 1924) and with an open net fished a t about 120& 1 800 m ( 3 500 m of wire out) (Voss, 1960a). The largest female was 7.6 cm and the largest (unsexed) specimen was 8.0 cm in mantle length. 3. Phasmatopsis lucifer Vow, 1963 This species is intermediate between Phusmatopsis and Taonius because, while it is allied to the former in having flaps on the dorsal component of the funnel organ and a light organ on the tip of an arm (albeit a different arm), it is closer to Taonius in the form of the light organs on the eye bulb and in the absence of light organs on the liver. The type specimen was caught at 29'06" 88'02'W in a n open net fished at 275 m (Voss, 1963b). It is a gravid female with a mantle length of 9.6 cm. The ova appear to be uniform in size.

U. Taonius A Iarge number of specimens referabIe to this genus have been described and nearly all of them belong to T . megalops and T . pavo.

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MALQOLM R. CLARKE

1. Taonius megalops (Prosch, 1849)

Owenia megabps PTosch, 1849 Cranchia megabps Morch, 1850 Leachia hyperborea Steenstrup, 1856 Taoniua hyperboreus Steenstrup, 1861 Desmoteuthis tenera Verrill, 1882a I;oligopsia hyperborea Rochebrune, 1884 D m t e u t h i s hyperborea Pfeffer, 1900 Teuthowenia megabps Chun, 1910a Megalocranchia hyperborea Berry, 1912a Desmoteuthis megalops Muus, 1956 Megalocranchia megabps Voss, 1960a Taonius megalops Clarke, 1962d

Degner (1925) and then Muus (1956) studied the changes in growth of this species and were able to synonymize a number of species based on growth stages. The species (Fig. 50) has been recorded from west and south Greenland (Steenstrup, 1856; Mbrch, 1857; Jeffreys, 1876; Posselt, 1898; Grimpe, 1933; MUUS, 1962; Nesis, 1965), off the eastern coast of the United States (Verrill, 1882a; Hoyle, 1886a; Voss, 1960a), off Iceland and the Faroes (Prosch, 1849; Mbrch, 1867; Russell, 1909, 1922; Degner, 1925; Nielsen, 1930; Bruun, 1945), Jan Mayen (F'riele, 1879 after Grimpe, 1933), west of the British Isles (Steenstrup, 1861; Hoyle, 1886a; Massy, 1909, 1913; Degner, 1925; Stephen, 1944), in the Bay of Biscay (Hoyle, 1906b; Chun, 1913; Degner, 1925), off the Azores (Chun, 1913; Joubin, 1920), in the eastern North Atlantic (Pfeffer, 1912; Chun, 1913; Joubin, 1920,1924; Degner, 1925) and south to 1"N (Pfeffer, 1912). It does not apparently occur in the Mediterranean. There is one record from western Canada (Clarke, 1962b). It has been caught at the surface (Hoyle, 1886a; Massy, 1913) and in an open net fished to 4 500 m (Joubin, 1924). Degner (1925) found that 25% of specimens, representing 2.3 per haul, were taken at less than 30 m (65 m of wire out), 52% of specimens, representing 2 per haul were taken at 30-150 m (65-300 m of wire out) and 23% of specimens, representing 1.8 per haul were taken at more than 150 m (more than 300 m of wire out). Joubin (1933) considered that adults were only found at great depths (2 000-3 300 m) but there is little evidence to support this. Growth changes in form and the photophores on the eye bulb have been traced by Degner (1925) and Muus (1956). The largest specimen has a mantle length of 21.0 cm (Steenstrup, 1861a); very few have been sexed and there are seldom comments on their sexual maturity. Small larvae are present in both January and July off southern

. A 1 2 3 4 5 6

60. Localitiee from which T m i w megalope ( l ) , T.pellueida (2), T . paw ( 3 ) . PhaamatqpsiS cymoctypua (4), P . ocean& P . Zueijer (6) have been recorded.

(6) and

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MALCOLM R. CLARKE

Greenland (Nesis, 1965) and from February to September in the eastern North Atlantic (Degner, 1925) so that there does not appear to be a restricted breeding season. It has been taken from the stomachs of Globicephalus melas and Steno rostratus (Nielsen, 1930). 2 . Taonius pavo (Lesueur, 1821) Loligo pavo Lesueur, 1821 Loligopsis pavo (pars) d'Orbigny, 1835-48 Desmoteuthia hyperborea Verrill, 1882c This species (Fig. 50) has been recorded from the western North Atlantic (Lesueur, 1821; Verrill, 1882c), the eastern North Atlantic (Joubin, 1899, 1900, 1920; Bouxin and Legendre, 1936; Rees and Maul, 1956), Antarctic seas (Chun, 1910a), the Philippines (Voss, 1963a), off Japan (Sasaki, 1920, 1929a), the Bering Sea (Okutani and Nemoto, 1964) and off western North America (Pearcy, 1965). It has also been recorded from the Kuril region (Akimushkin, 1954b, 1955a; Beteshava and Akimushkin, 1955) but from Akimushkin's (1954b and 1957) description a t least some of these belong to Galiteuthis. It has been found dead at the surface (Joubin, 1900) and has been caught in an open net fished to 750 m (Voss, 1963a). Off Oregon, Pearcy (1965) found that more were caught with open trawls fished at about 500 m than a t 200 m or 1 000 m. The largest female is 33.0 cm (Sasaki, 1920) and the largest unsexed specimen is 33.5 cm in mantle length (Joubin, 1900). It has been taken from the stomach of Diomedia fuliginosa which suggests that it must have come near the surface although Chun (1910a) suggested that it may have been brought up by a rolling iceberg. It has also been found in stomachs of the fish Alepisaurus ferox and of Sperm whales (Okutani and Nemoto, 1964) and, if some of Akimushkin's identifications 'are correct, in Albatross stomachs (Akimushkin, 1954b).

3. Taonius thori Degner, 1925 Known only from the type specimen, this well distinguished species was taken at 46'30" 7OO'W in the North Atlantic in an open net fished a t about 900-1 300 m (2 700 m of wire out). It has a mantle length of 31.5 cm. 4. Taonius pellucida Chun, 1910 Demoteuthis pellucida Chun, 1910a This is clearly very close to T . megalops and further work may show them to be identical. It has been recorded from the South Atlantic

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(Chun, 1910a) and from the North Atlantic (Chun, 1913; Grieg, 1922, 1924). It has been taken close to the surface (Grieg, 1924) and with open nets fished to 2 200 m (Chun, 1913); a closing net fishing at

50&180 m caught a specimen. The largest specimen, which is female, has a mantle length of 7.7 cm (Chun, 1910a). Four specimens from 4.9-6-0 cm in mantle length were described as adult (Chun, 1913). 5. Taonius richardsoni (Dell, 1959) Megalocranchia richardsoni Dell, 1959b A species very close to T . pavo, this has been described from New Zealand waters (Dell, 1959b). It was caught in nets fished at depths calculated as 460,550 and 1 100 m. The largest specimen has a mantle length of 13.0 cm. One specimen was taken from a fish stomach.

6. Taonius of Iwai 1956 A specimen taken from the stomach of a Sperm whale caught near Kamchatka differs from other Taonius species in having numerous white tubercles on the mantle surface (Iwai, 1956c)and should probably be regarded as a distinct species. The mantle length is 32.8 cm.

V. Verrilliteuthis 1. Verrilliteuthis hyperborea (Steenstrup, 1861)

This species is very poorly known and it is by no means sure that all specimens referred to it are the same species; consequently it is not possible to give the distribution with any certainty. In recent years Voss (1955) recorded it off Cuba and Adam (1962) recorded it off Angola. It has previously been recorded in the Faroe-Shetland Channel (Russell, 1922) and off Ireland (Massy, 1928);it has been said to extend from Baffin Bay and Greenland to Ireland and Madeira (Stephen, 1944) but this probably includes records of Verrill which are very doubtful. The largest specimen recorded recently has a mantle length of 6.8 cm (Adam, 1962).

W. Galiteuthis Adults of this genus are all referable to C. armata Joubin, 189813, while two immature specimens were erroneously referred to G. suhmi (Hoyle, 1885d) by Chun (1910a) and Taonius richardi Joubin, 1895b, may also belong here (Chun, 1910a; Grimpe, 1933) although Pfeffer (1912) considered that it was distinct. Adult Galiteuthis are characterized by having prominent hooks on the tentacles but in younger

238

MALCOLM

R. CLARKE

specimens the hooks are small, and very young ones have tentacles devoid of hooks and are consequently often grouped under the “larval genera ” described above. 1. Galiteuthis armata Joubin, 1898

Witeuthis (Taonidium)suhmii Chun, 1910s Qaliteuthisphyllura Berry, 1911a ?Taoniuapavo (pars)Akimushkin, 1954a This species (Fig. 51) has been recorded from the Mediterranean (Joubin, 1898b, 1920, 1924; Mortars, 1917; Degner, 1925; Issel, 1920, 1925b), from the North Atlantic (Joubin, 1895b, 1920, 1924; Chun, 1910a, 1913; Degner, 1925; Voss, 1960), off South Africa (Robson, 1924c),the Antarctic (Hoyle, 1912),south of Australia (Brazier, 1892b), the Bering Sea and off Kamchatka (Sasaki, 1920, 1929a; Okutani and Nemoto, 1964),the Kuril region (Akimushkin, 1954a, 1955a; Beteshava and Akimushkin, 1955), Hokkaido in Japan (Hikita and Hikita, 1956; Iwai, 1956b), Oregon (Pearcy, 1965) and California (Berry, 191la). Iwai (1956b) considered that the Pacific and Atlantic forms differed in some respects. It has been taken with open nets fished to as little as 100 m (200 m of wire, Chun, 1913 and Issel, 1925b) and to as much as 4 000 m, but the majority were taken in nets fished between 500 and 2 000 m. The largest specimen has a mantle length of 61-0 cm (Joubin, 1924) and a male of 11.0 cm was described as adult (Chun, 1910a). During growth, the arms remain relatively the same length, the tentacles, head and eye stalks become relatively shorter, the body becomes relatively narrower and the fin relatively longer (Fig. 52). The species has been taken from stomachs of Germo alalungu (Joubin, 1895b as Taonius richurdi), Thunnus germo (Clemens and Iselin, 1963), Tursiops truncatus (Rancurel, 1964) and Sperm whales (Akimushkin, 1964a, 1955a; Iwai, 1956b; Okutani and Nemoto, 1964).

X. Mesonychoteuthis

A genus represented by one species and characterized by hooded hooks in the middle of each arm. 1. Nesonychoteuthis hamiltoni Robson, 1925. The species was described from two brachial crowns taken from the stomach of a sperm whale caught in the South Shetland area (Robson, 192Sa). Several complete specimens since collected from Sperm whale stomachs in the Antarctic are being examined by Dr. Anna Bidder

REVIEW OB THE SYSTEUTICS AND ECOLOGY OB OUEANIO SQUIDS

b

239

0.6 8

I -3

1.5

2.0

3.7

11.2

CM

Plate 69, Figs. 4. 2). The two largest from the ventral, the others from the doraal side. Mantle lengthe in cm are indicated.

Fro. 62. Change in form during growth of GuZifeuthi~arnuta after Issel (1920, Figs. 14, 16, 17, 19) and Chun (1910,

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XX. SPIRULIDAE The single species within this family, Spirula spirula, is the only truly oceanic member of the Sepioidea. A. Spirula Bruun (1943) was unable to detect specific or geographical differences between the cuttlefish referable to this genus. 1. Spirula spirula Linnaeus, 1758 Bruun (1941, 1943, 1955) made a detailed study of this species and most of the following details are based on his work. The shells are regularly washed up on shores in very large numbers and a8 such strandings occur in regions not frequented by the animal it is pointless to list the large number of records in the literature. The living animal occurs in tropical and subtropical regions in the Atlantic, Indian and Pacific Oceans (Fig. 53). Bruun (1955) considered that the water temperature is the principal factor in determining the distribution while food availability is perhaps also important. All catches have been in regions where the temperature at 400 m is 10°C or higher. On the other hand, i t does not occur in the Mediterranean, the Sula Sea or the Red Sea which may be due to the high temperatures (of over 10°C at 1 000 m) in these regions. It seems to be most numerous off the north-west African coast. Although it lives as a true pelagic species it is usually taken near continental slopes and the neighbourhood of islands is particularly favourable for its occurrence. Over 55% of specimens were taken in water less than 2 600 m deep and over 70% in water less than 3 500 m deep. The vertical distribution corresponds to the continental slope. The youngest specimens less than 0.6 cm in length are concentrated at 1 000-1 750 m, while the larger ones are found at as little as 100 m* at night and down to 1 750 m. The upper limit corresponds to water at less than 19°C. The lower limit of 1 750 m is the limit to which the shell can go without imploding due to the pressure and this wag determined by finding the pressure resistance of dead shells (Bruun, 1943). Bruun (1955) later considered that 1 750 m is probably too deep and Spirula possibly does not live below the thermocline. He concluded that it lives in the aphotic zone of the thermosphere and therefore falls within his definition of a mesopelagic animal. Spirula probably moves about in shoals, swims upright in the water and can control its buoyancy (Denton, 1961). A light organ on the apex of the body (posterior end) (Chun, 1910b) emits a pale, yellowish-green light (Bruun, 1943).

* ThereIis a:record of Spirula 0ccurring:at the surface by J. S.:Gardiner;in the narrative of “ The Fauna and Geography of the ;Maldive ~d-Leccedive:Archipelagoea.” 1, p. 6, Cambridge University Press.

c

FIG. 63. Localities from which Spirt& spirula hss been recorded.

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Because no pelagic eggs have been found and the youngest larvae are found at more than 1 000 m, Bruun (1943) considered that eggs were probably deposited on the bottom and the distribution suggests that the continental slope is the most likely area of deposition-a view substantiated by the find of a small larva embedded in ooze taken in a trawl (Bruun, 1955). The smallest larva, (mantle length=0.28 cm) which must have only just been hatched, has two chambers in the shell (Bruun, 1943).

0.2 5

1-1 2

FIG. 64. Change in form during growth of Spirula ~ p i ~ u l after c r Bruun (1946, Plate 1. Figs. 5, 3) and Chun (1910, Plate 64, Fig. 2). Smallest from the right side, the others from the dorsal side. Mantle lengths in cm are indicated.

During growth the arms and tentacles become relatively longer, the head remains the same, the body becomes relatively narrower and then wider and the fins remain the same compared with the mantle length (Fig. 54). Both the ventral arms become fully hectocotylized in males at a mantle length of 3.5-4.4 cm (Bruun, 1941, 1943, 1955; Kerr, 1931). The ovaries of females are well developed with ova 1.0 mm in diameter at a mantle length of 3.1-3-7 cm. Ripe ova are about 1.7 mm in diameter (Naef, 1923; Bruun, 1943). Males reach a mantle length of 4.2 cm and females 3.7 cm.

244

MALCOLM R. CLARKE

The breeding season must extend over a long period because larvae of less than 0.5 cm in length are present off West Africa from March to October. Size distributions for the various months suggest that most of the spawning takes place in winter. I n October the squids are half grown and they are thought to mature and breed the following winter and then perhaps die (Bruun, 1943). However, this cannot be regarded as settled because the division of the size distribution into size groups can only be described as arbitrary. A specimen was taken from the mouth of a deep-sea fish (Dall). XXI. DISTRIBUTION As pointed out in the introduction, our knowledge of the group is probably not good enough to draw general conclusions concerning the relationships between the cephalopod fauna of different geographical areas. However, it is perhaps useful to list the species recorded from general areas (Table 111, Fig. 55). Boundaries of these have been rather arbitrarily chosen and are useful for descriptive purposes rather than for marking any real faunistic barriers; in most cases their position has been determined by geographical expediency. To some extent the total number of species and the number of “endemic” species in any area is related to the amount of work done in that area (cf. Table I11 and Fig. 1). The distribution of a few of the better known species is worth noting as they are oegopsid representatives of previously recognized types. Hyaloteuthis pelagicus, Onychoteuthis banksi, Ommustrephes bartrami, Onychia carribaea, Thysanoteuthis rhombus, Brachioteuthis riisei, Lycoteuthis diadema, Cranchia scabra and the sepioid Spirula spirula are widespread in warm and temperate waters. Bathyteuthis abyssicola, Abraliopsis morissi and Histioteuthis bonellii are found in the Atlantic and Indian Ocean. Symplectoteuthis oualaniensis (both forms) and Abralia andamanica are found in the Indian Ocean and the Pacific. Better known species which are restricted to particular oceans are in the North Atlantic Illex illecebrosus, in the North Atlantic and the Mediterranean Ommastrephes caroli, Illex coindeti and Abralia veranyi, in the North and South Atlantic and Mediterranean Ommastrephes pteropus, Todarodes sagittatus and Todaropsis eblanae, in the Indian Ocean Brachioteuthis picta and in the Pacific Symplectoteuthis luminosa, Todarodes paci$cus, Dosidicus gigas and Moroteuthis robusta. Gonatus fabricii is found in the North Atlantic and North Pacific at high latitudes and it seems likely that these populations are connected at least periodically via Arctic seas. The genus Todarodes has an Atlantic species, T . sagittatus, and a North Pacific species T. paci$cua

r

I

Fxo. 66. General oceanie areas referred to in Table 111. See text page 244.

TABLEI11 The Geographical distribution of species. Presence of a species within a region is shown by a cross.

- -- --- ~~

Archileuthis epp. Ommaatrepha bartrvmi Ommcurtrepha mroli Ommaatreph pteropw Symplectoteuthie luminoaa Sympleetokuthia OualaniswG Dosidicua A a s Eyaloteuthis p e l u g h Orndhoteuthia volatilia Ornithoteuthia antillurum Illez windeti Illez illecebroeus Todaropaia eblanatl Todurodea sagittatua Todoroclee pacijcua Nototodarua sloani Onyclwteuthia banksi Moroteuthia aquatorialis Moroteuthia ingena Moroleuthia robsoni Moroteuthia robusta Ancistroteuthia lichtenateini Chaunoteuthia mollis Onychia carribaea Tetronychoteuthis duaaumieri Qbnalw,jabricii Cfonatw antarcticua

6

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6

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1

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3

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10

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20 -

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16

17

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Geographical r e g i m (as in Fig. 65).

X

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Qonatus a?ion!ychits QOnalUS niagister Qonatus borealis Uonatus octopedatus Thysanoteuthis rhombus Cycloteuthis siroenti Psychroteuthis glackzlis Alluroteuthis antarcticus Valbyteuthis danae Brachioteuthis riisei Brachioteuthis beanii Brachioteuthis boumani Brachioteuthis pic f a Cirrobrachiuni danae Cirrobrachium jiliferuni Pholidoteitthis adami Pholidoteuthis boschmai Bathyteuthis abyssicola Abralia andamanica Abralia armata Abralia aatrolintata Abralia aatrosticta Abralia grimpei Abralia japonica Abralia lucens Abralia multihamala Abralia redficldi Abralia renschi Abralia sparcki A bralia steindachneri Abralia trigonura Abralia veranyi Abraliopsis a f l n i s Abraliopsis gilch rist i Abraliopsis hoylei

_

TABLEIII.-Contd.

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--

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A&rdiopia Zinineala Abralhpsia m m % AbTal+~psiapfefferi Abaliopsia neozealandica Enoplotetdhia amps& Enoploteuthie dubia Enoploteuthie 9aAaxk.a Emphteuthia leptura Enoploteuthie chunii Pterygioteuthis gemmakz Pterygioteuthis giardi Pterygioteuthis microlampas Pyroteuthia margaritifera Ancietrocheirua leaueuri Thelklwteuthis alessandrini Watasenia scintillana Enuploion. eusticum Octopoteuthie d a m Octopoteuthie sicula Octapoteuthia h q i p t e r a Lumpadwteuthia me&& Lycoteuthia diudema Nematolumpis regalia Ozegoniateuthie lorigera Oregoniateuthia a p r i g e r i Selenoteuthie scintillana Hiatwteuthie bonellii CoUdeuthia arcturi Cdideuthie celetaria c.

7

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Geographical regions (aain Fig. 55).

” ’ 1“

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14

16

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20

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TABLEIII.-COTZ~.

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2

Maetigoteuthis talismani Lepidoteuthis grirnaMii Grimalditeuthia bonplandi Cranchia ambra Crystalloteuthia beringiana Cryskrlloteuthk glacialis Liocranchia gardinmi Lkranchia intermedia Liocranchia reinhardti Liocranchia valdiviae Pyrgopsis allonliccr Pyrgopsia pacijim Pyrgspais lemur Pyrgopeia rhynchphorzcs Pyrgopsis schneehageni Lemhia cyclura Leach& eachacholtzii Drechselia danae Aseocranch&zjoubini Egea inermis Sandalops ecthambw Sandalops melancholicus Sandalops pathopsis Corynomma speculator Bathothauma lyromma Taunidium chuni Taonidium i W u m

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T w n i d i u m pfefferi Teuthowenia antarctica Teuthowenia corona Teuthowenk elongata Teuthowenia tagoi Toxeuma belone Megalocranchb abyssicola Megalocranchia fisheri Megalocranchia maxima Megalocranchia papillata Megalocranchia pardus Hdicocranchh pfefferi Helkocranchia beebei Anmalocranchkz impen& Henaenioteuthis joubini Fuaocranchia alpha Phuarnatopais cymoctypw, Phaamatopaia oceaniuz Phuarnatopsia lucifer

X X I X

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T w ~ W WW&OpS Twnius pavo

X X

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Taoniua thahori T w n i u s pellucida Taoniw, richardsoni Vewilliteuthis hyperborea Galkteuthis armata Mesonychoteuthis hamiltoni Sp'rula spirula

X X

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252

MALCOLM R . CLARKE

which suggests that connection between the two was severed sufficiently long ago to allow the isolated populations to evolve to the species level of differentiation. A bipolar distribution within the oegopsids is perhaps shown by Gonatus fabricii which is not clearly distinguishable from the southern G. antarcticus; they may well be forms of the same species. I n addition, the Antarctic Crystalloteuthis glacialis differs very little from C . beringiana from the North Pacific. Dosidicus gigas is rather curious in being found in the eastern Pacific off Central and South America and in the western Pacific off Australia, but it has not been recorded off New Zealand; however, the limits of distribution are poorly known. Several species of the Ommastrephidae are known to migrate annually into inshore waters but few specimens are in spawning condition when caught inshore. Illex illecebrosus and I . coindeti seem to move into shallower water after food during adolescence while Todarodes paci$cus and T . sagittatus apparently move on to the continental shelf prior to spawning on the continental slope. Ommastrephes pteropus females apparently migrate into the eastern North Atlantic and leave the males further south or west; this migration is probably for spawning. Other species known to migrate annually are Gonatus fabricii, Thysanoteuthis rhombus and Abralia veranyi. Where data is available (Illex illecebrosus, Todarodes paci$cus) migrations are intimately related to movement of water masses. The little evidence we have on tolerance of oceanic squids to environmental factors (e.g. Todarodes pacijicus, Bathyteuthis abyssicola, Watasenia scintillans) suggests that they are able to live in a wide range of temperature and salinity a t least for brief periods. A few species are rather limited to particular latitudes (e.g. Gonatus fabricii, Spirula spirula) and in these species possibly temperature throughout the year is the principal factor in limiting their distribution, XXII. DEPTH The extensive use of non-closing nets makes analysis of the depth range of oceanic squids extremely difficult. Additional inaccuracy arises because depth gauges have been used infrequently and most depths have been calculated from the length of warp out and the warp angle, a method giving only a very approximate idea of the depth. It is not always clear whether authors are quoting soundings or depths of net. Here, only the depths of the shallowest and the deepest hauls which have caught a species have been noted. While these depths, in most cases, give an over-estimate of the depth a t which a species lives, they do give us a few indisputable facts which

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are to be preferred to any analysis based on the many largely-unsubstantiated comments in the literature. By counting the species with their apparent upper limits between different depths (e.g. 0-100, 100-500, 500-1 000 m) one can derive a cumulative percentage curve, which shows the percentage of oegopsid species having their upper limit shallower than each selected depth (Fig. 56, A). A similar curve may be derived to show the percentage of species having their deepest record deeper than each selected depth (Fig. 56, B). From curve A,

100

1000

2000 Depth

in

3000

4000

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metres

Fro. 66. A, Cumulative percentage curve of oegopsid species having their upper limit shallower than each selected depth. B, Cumulative percentage curve of oegopsid species having their deepest record deeper than each selected depth.

i t is evident that over half the oegopsid species enter the upper 100 m a t some stage and 90% of the species are a t times found shallower than 1 000 m. Curve B, on the other hand, shows that in about a third of the species the deepest record lies a t 0-500 m, another third Iies a t 500-1 500 m and the remaining third lies deeper than I 500 m. Thus, a large majority of oegopsid species live shallower than I 5 0 0 m, most extend into the photic zone a t some time and, more than is generally supposed, enter water between the surface and 100 m. It is instructive to examine cumulative percentage curves of the

254

MALOOLM R. CLARKE

minimum depths of species in the separate families (Fig. 57). From these curves, which are each based on rather few species, it is clear that all the ommastrephid squids are found in the upper 100 m a t times; half the onychoteuthids are found in the superficial 100 m, most of the rest are deeper than 100-500 m; 56% of cranchiids extend into the upper 100 m and the family would seem to have a fairly large depth range; almost a third of the histioteuthid species are

.

.-

.

100 500

1000

.-

-

2000

.- - - . 3000

. 4000

5000

Depth in m e t r e s

FIQ. 67. Cumulative percentage curves of species in various oogopsid families having their upper limits shallower than each selected depth. The numbers of species included in each are Ommaatrephidae 12, Onychoteuthidae 10, Histioteuthidae 10, Cranchiidae 41 and Chiroteuthidae 3 I .

sometimes found in the upper 100 m but 40% of the species of the family live only deeper than 500 m and 20% only deeper than 1 000m; the Chiroteuthidae is the deepest-living family, only 16% extend into the upper 100 m, only 42% into the upper 1000 m and the upper limits of over 20% lie deeper than 2 000 m. Collection of squids by closing nets has only been reported two or three times and therefore provides little evidence on vertical distribution. The evidence of photography and tentacles caught in reversing water

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bottles shows conclusively that Ommastrephes caroli extends from the surface to 1 490 m (Table 11). The stomach contents of predators often give some information on depth of squids. For example if species occur in bird stomachs (e.g. Hyaloteuthis pelagicus) they must come very near the surface; seals probably dive to less than about 200 m so that their food must occur shallower than this. There are six records of Sperm whales becoming entangled in telephone cables at about 1 000 m (Heezen, 1957) which strongly substantiates the theory that they feed at great depths on such species as Lepidoteuthis grimaldii, Histioteuthis bonellii, Taningia danae, etc. Perhaps such species live near the bottom on the continental slope at depths of around 1 0 0 0 m because sand grains have been taken from the stomach of Taningia danae. Very few structural variations have been related to depth; such features as luminescence, transparency, the possession of a silver reflecting layer and large eyes all seem to be as prevalent in shallow aa in deep living species. However, the one species known to come near the sea surface in daylight, (Onychia carribaea) has a general blue colouration which is seen in no other squid. Otherwise, colour seems to vary quite independently with depth. There is some evidence that pigment in the lens may vary with depth; Denton (I96Ob) found that Onychoteuthis banksi, which probably spends some time near to the sea surface, has a lens pigment which is yellower than other species examined and squids living deeper have lenses transparent down to about 310 mp. The yellow pigment would filter out much of the daylight penetrating the upper layers, a filtration unnecessary in deeper living squids only illuminated by blue or green light.

XXIII. EW MASSES Our almost complete ignorance of the eggs and early larval stages of oegopsids is the most extraordinary omission in our knowledge of cephalopod biology. From observation of egg laying females in shallow water, it would appear that Todarodes pacificus lays its egg mass on the bottom (page 136). On the other hand, except for a few references to oegopsid eggs (Stephen, 1944; Allan, 1945) there is only the description of a Thysanoteuthis rhombus egg mass (Fig. 26, p. 161), Watasenia scintillans eggs (Shimomura and Fukataki, 1957) and a few descriptions of egg masses collected or seen at the surface. Collingwood (1873) gave an admirable description of an egg mass collected in a bucket from the surface at 37"N 28"W. The egg mass resembled " one of those cylindrical knitted comforters worn by ladies " measured 2 f t long by 4 or 5 in. in diameter; was closed at both ends and floated " expanded

256

MALCOLM R. CLARKE

upon the surface of the water ”. From a small boat it could scarcely be seen and broke in two when collected. The mass consisted of semisolid, perfectly transparent, jelly containing rows or clusters of round black spots, each the size of a pin’s head, arranged in single rows along the outer part of the cylindrical mass. Each black spot proved to be an active little squid which “ leaped about in their narrow chambers ”. “ Each egg-sac was perfectly spherical and transparent.” After two or three hours, all the embryos had hatched out and had left the egg mass. This description could also apply to the other records of a gelatinous floating egg mass. Grenacher (1874) published the description of another similar egg mass collected in the North Atlantic. It had a length of about 76 cm and Grenacher was able to describe, in detail, the embryological changes taking place after capture. Hedrich described a gelatinous egg mass which was stranded and was later considered to belong t o some species of Ommastrephes (Schafer, 1956). Akimushkin (1963) described egg masses seen near the Kuril Islands which he attributed to Todarodes paci$cus and other pelagic egg masses seen floating near the surface a t a station south of Japan. The latter were ribbon-like and measured 70 x 30 x 5 cm; each egg capsule was almost spherical, 0-2 cm in diameter and contained an embryo having a free mantle border; this shows they were neither octopuses nor members of the Cranchiidae. The author knows of only three other examples of the observation of an oegopsid egg mass. I n late 1960 Dr. Hans Hass showed a film on B.B.C. television of an egg mass seen within the Addu Atoll of the Maldive Islands. Dr. Hass subsequently sent the author prints and very kindly arranged for him to see the film. The egg mass which was filmed was one of several seen; it measured 6 or 6 f t in length and about 1 ft across, was transparent, rather solid and contained a large number of eggs in spiral lines. The embryos within the eggs were oegopsid but further identification was not possible. A rough estimate from Dr. Hass’s photographs indicates that the mass possibly contained about 20 000 eggs. Dr. Hass had only seen such masses on one other occasion, in the Piscadera Bay a t Curaqao, West Indies. In both places where they were observed the bottom drops very steeply to great depths. In March 1964 another squid egg mass measuring about 6 f t long by 1 ft across was collected by R.R.S. Discovery in the Indian Ocean a t O”58’S 67”59’E. It closely resembled a large Pyroso11u;c but there were fewer dots per unit volume. It was coloured a dusky red by the small squid embryos which were scattered in the jelly. The jelly was very heavy and broke the handle of the handnet during collection; it was rather more sloppy than Pyrosoma and much of it

257

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ran through the netting (P. M. David personal communication). Some of the mass was retained and close examination has shown it to be an oegopsid species but further identification has not proved possible. It is difficult to account for the scarcity of oegopsid egg masses when one considers the great numbers of adults present in the ocean. One possibility is that the gelatinous nature causes them to break up in a net and be lost through the meshes. If this were the case, one might expect small pieces to be retained not infrequently and to be identified in the catches on more occasions than they are. The explanation that the eggs are laid on the continental slope a t depths in excess of say 1 000 m has much to recommend it. First, no nets are fished very near to the bottom on the continental slope; secondly many of the squids in Sperm whale stomachs, which are thought to feed on the slope about 1 000 m are gravid and probably actively spawning; and thirdly the fact that Todarodes paci$cus lays its egg mass on the bottom, probably on the slope. XXIV. GROWTH,SIZEAND FORM Growth rate and duration of life has been studied for very few oceanic squid species. The ommastrephids Illex illecebrosus (Fig. 11, p. 121 based on Squires) I . coindeti (Fig. 12, p. 124 based on MangoldWirz 1963), Todarodes sagittatus (Fig. 18, p. 138 based on Fridriksson, 1943 and Clarke, unpublished) and T . pacijicus (Fig. 18 based on Katoh, 1959), have been studied in some detail while the work on other oegopsids such as Gonatus fabricii and Todaropsis eblunae can only be regarded as very preliminary (see pp. 155 and 126). All the four species studied in detail appear to reach maturity after about one year but nothing is known about the earlier stages so that, although improbable, one cannot rule out a two year growth to maturity. Regarding length of life it would seem that three years may be a maximum for these species. Study of growth has relied on finding year groups in size distributions of large samples or on detecting changes in the mode or mean of a sample from month to month. Each method has a serious disadvantage; the sampling technique seriously biases the distribution of the sample (two types of gear or two variations in the use of the same gear can produce a bimodal size distribution which may be interpreted as showing two year groups); migrations of the population may suggest accelerated or decelerated growth if smaller or larger individuals enter or leave the sampling area at different times. Both these errors would be avoided if a method of age determination could be found. I*

258

MALCOLM R. CLARKE

With this in view the author examined several hundred otoliths of ommastrephids taken off Madeira and Iceland. Very minute growth laminations are detectable in Ommastrephes caroli, 0. pteropus and Todarodes sagittatus off Madeira but no major fluctuations in these could be detected; this one might expect in a warm region having small variations in temperature, etc. I n otoliths of Todarodes sagittatus taken off Iceland, the Faroes and Norway the laminations show periodic variations in thickness but the small size (less than 1 mm in length) and crystal structure has prevented the relationship between such variations and time, from being investigated. Beaks of various cephalopod species were searched for laminations by Tinbergen and Verwey (1945),Mangold-Wirz (1963b)and the author (Clarke, 1965b). The author detected laminations in Moroteuthis ingens beaks taken from Sperm whale stomachs. Laminations or microrings” vary in width and such variations are arranged in (‘cycles ”. The large number of microrings to a cycle (8-12) can be shown to eliminate chance as the prime factor in causing the formation of cycles. Although he has been unable to relate the cycles to time it would seem that further work on cycles in the beaks of other species may be fruitful. An approximate idea of the size reached by oceanic squids in general may be obtained by grouping species according to the known maximum ” mantle lengths in the various families (Table IV). It will then be seen that only the architeuthids and one species of onychoteuthid reach a mantle length greater than one metre. When the totale in any size group are plotted as a cumulative percentage (Fig. 6 8 ) it may be seen that over 60% of oegopsids have mantle lengths of less than 10 cm and over 90% of less than half a metre. However, it must be remembered that sampling gear does not usually catch the larger specimens so that these conclusions are necessarily biased towards the .smaller squids. I n considering changes in form during growth we are somewhat handicapped by inability to identify the earlier stages and by having too few specimens to distinguish individual variation. However, by considering change in the length of the arms, tentacles, head and fins and the width of the body in relation to the mantle length it is possible to draw some conclusions from the species figured here. Table V shows how, with growth, the body becomes relatively wider or narrower and the arms, tentacles, head and fin become relatively longer or shorter. In some cases there is a reversal in the relationship to the mantle length, during growth ( L S or S-L). It is apparent from Table V that there is considerable diversity among the species. Further, ((

((

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259

TABLEIV. MAXIMUMMANTLELENGTHS RECORDED FOR THE SPECIES IN EACHFAMILY. Under each family heading is the number of species having a recorded maximum length in each size group

*

Not included in totals.

there are basically three types : in Histioteuthis bonellii and Calliteuthis reversa virtually no change in form takes place and growth can be regarded as isometric above a mantle length of 3-0cm ; in Chiroteuthis veranyi, Lepidoteuthis grimaldii, Galiteuthis armata, Onychia carribaea and possibly Ctenopteryx sicula there is no “change of direction ” in the growth of the selected structures. That is, the structure either grows longer or shorter, broader or narrower throughout life (within the size limits of the specimens) ; in Thysanoteuthis rhombus, Brachioteuthis riisei, Todarodes pacijicus, Ancistroteuthis lichtensteinei, Gonatus

260

MALCOLM R. CLARKE

fabricii, Abraliopsis, Pterygioteuthis giardi, Octopoteuthis sicula, Thelidioteuthis nlessandrini some of the dimensions considered a t first increase faster than the mantle length but then their rate of growth falls behind that of the mantle length. I n the early juvenile the young arms and tentacles must be formed by their growth being faster than that of the mantle so that if, in later life, the structure becomes smaller

- Cumulative % .

50

I 20

40 Mantle lenqth

60

80

100

(cm)

Fro. 58. Cumulative percentage curve of oegopsid species with known maximum lengths not exceeding the values selected. See also Table IV.

in relation to the mantle length, clearly a t some stage there must be a change from growing faster t o growing slower than the mantle length. That this is the explanation for the apparent ‘(reversal ” in the species considered here, is supported by the fact that in all species with a reversal (except Onychoteuthis banksi) the growth rate of the structure is first faster and later slower than that of the mantle length. I n the species having this “ reversal ” we can regard it as a change from the larval condition to the juvenile. At present, it is only possible to give very broad limits between which the ‘(larval ” stage ends but clearly the change can take place over a wide range of sizes.

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SQUIDS

Onychoteuthis banksi is exceptional because the arms, tentacles and head grow slower than the mantle a t first but then later grow faster. If our assumption that the arms and tentacles must first grow faster than the mantle is correct, there must be two changes during growth, the earlier being a t a smaller size than the examples figured. Lepidoteuthis grimaldii is intermediate between the group with

TABLEV. A SUMMARY OF RELATIVE GROWTHOF VARIOUSPARTS OF THE BODY. The parts become narrower (N) or wider (W), longer (L) or shorter (S) during growth compared with the mantle. This is best seen if the mantle is drawn the same size (see page 258). W-N or L-S shows a change in the rate of growth from faster to slower than the mantle. ~~

Body

Arm

Tentacle

W-N N N N N N W-N N W-N W-N W-N same same N W W N

G S

L-S LS? s-L

Head

~

Fin

Figure

L L L L L L L L L L

25

~

Thysanoteu.this rhombus Todarodes paci$cus Onychoteuthis banksi Onychia carribaea Ancistroteuthis lichtensteinei G h a t u s fabricii Abraliopsis Pterygioteuthis giardi Octopoteuthis sicula Thelidioteuthie alessandrini Brachioteuthis riisei Ctenopteryx siculus Histioteuthis bonellii Calliteuthis reversa Chiroteuthb veranyi Lepidoteuthis grimaldii Galiteuthis armata

L-s s-L L same

L-s S

L L-S L-S

L-s

L

S S s-L L S S S

L

L L

L-s L-s L-S

L L

L-s L

S s-L

same

same S L S S

same S S

G S G S

L L

L L

L S

L L S(?)

S same same

L

17

20 20 20 24 32 32 36 35 27 29

39 39 41 44 62

and the group without a larval stage because, while i t shows no reversal in the growth rates, between mantle lengths of 6.0 and 8.6 cm there is a very rapid change to the form of the adult and growth is then isometric (Fig. 44, p. 214). Some near relatives have similarities of growth. Histioteuthis bonellii and Calliteuthis reversa, Lepidoteuthis grimaldii and Chiroteuthis veranyi are the only species in which the fins do not Iengthen during growth, and the latter two species differ from all the rest in having a mantle which gets relatively broader throughout growth.

262

MALCOLM R. CLAFCKE

XXV. STRUCTURAL VARIATION Oceanic squids vary from rapacious, fast-swimming predators, like the ommastrephids and onychoteuthids, to passive, balloon-like drifters like the cranchiids. The rapid swimmers have pointed, muscular bodies which, by powerful contractions, send jets of water from a muscular funnel. The efficiency of such a method of locomotion must be greatly increased by the fact that the thrust-producing contraction simultaneously reduces the cross-sectional area of the animal and so reduces drag. The great mobility of the funnel enables the squid to dart forwards after prey and the fins, far from being mere stabilizers, can contribute to either forward or backward movement by powerful beats, the direction of which may be modified by a flexing of the body in front of the fins. The most active species are slightly negatively buoyant and need to swim to avoid sinking deeper. Water currents used for locomotion pass over and oxygenate the gills in the mantle cavity. At the other extreme, the cranchiids increase their buoyancy by retaining ammonium ions in their greatly expanded body cavities (Denton et al., 1958; Denton, 1960a). Coupled with the less-active life which such a buoyancy system permits, cranchiids have developed a method of drawing water over the gills, independent of the locomotary system (Clarke, 1962~). A horizontal membrane divides the mantle cavity into a chamber on each side of the coelom and a ventral chamber (Fig. 59). Water can enter the paired dorsal chambers through the inhalent openings a t the sides of the head, pass through the paired spiracles in the horizontal membrane just in front of the gills, into the single ventral chamber. The water is first drawn in by the contraction of the wall of the coelom near the anterior end. The contraction travels posteriorly and pushes before it a " bolus )' of water in each of the dorsal paired chambers. Upon reaching the spiracle in the horizontal membrane the '' bolus " passes through into the ventral chamber from whence it passes out through the funnel. Continual peristaltic contractions of the coelom wall maintain this respiratory circulation while occasional contractions of the mantle are used for escape reactions; otherwise, slow locomotion is carried out by rapid paddling of the fins. Between these two extremes of life there are forms such as Taningia danae and Chiroteuthis veranyi which use locomotory currents to oxygenate the gills but are very gelatinous and are possibly neutrally buoyant as a result as found in other animals (Denton and Shaw, 1961). Structures used for catching prey are very variable. The tentacles and/or arms may have chitinous rings with or without teeth or these

i

B

C

D FIQ. 69. Respiratory currents in the Cranchiidae. A, Diagram to show the structure of a cranchiid: inhalent openings (i) at each aide of the head allow water to pase into paired dorsal mantle cavities (r is the right one) which lie either side of the fluid filled coelom (c) and are separated from the single ventral mantle cavity (v) by a thin transverse membrane (t). A spiracle ( 8 ) in front of the gill connects the dorsal mantle cavity of each side with the ventral cavity. The funnel (f) opens from the ventral mantle cavity t o the exterior. B. Water is drawn into the dorsal mantle cavities by contraction of the anterior end of the coelom. This leads to a compensctting expansion of the posterior end of the coelom and a pressure on the water in the ventral mantle cavity resulting in water issuing from the funnel. C, the coelomic contraction then passes posteriorly, simultaneously pushing water through the spiracles into the ventral mantle cavity. At the same time the expansion of the anterior end of the coelom pushes thin membranes over the inhalent openin@ and act aa ValVm to prevent Water from paasing back out of these openings as water is forced through the spiracles by the expanding anterior coelom. D, the anterior coelom expands &B the Wave of contrection peaees beyond the end of the transverse membrane.

264

MALCOLM R. CLARKE

may be developed into large hooks. Nesis (1965) found that fish are more important in the diet of Gonatus fabricii after the tentacle hooks have developed, but otherwise the relationships between diet and such features have not been studied. The carpus of the tentacle club in many species bears smooth suckers and ‘‘ press-studs ” which interlock with those of the other tentacle; this certainly enables the tentacles to be used together as tongs ” in some species (Fig. 8). Such studs and suckers sometimes extend the whole length of the tentacle stalk in species having very long tentacles such as Architeuthis. There is some variation in beak shape (Clarke, 196213) and reference has already been made to the poisonous and non-poisonous bites delivered by different species (pages 113 and 145). All species are probably exclusively carnivorous. Photophored varying from a simple, sub-cutaneous lump of luminescent tissue to complex organs with reflector, diaphragm, pigment screen and lens are widespread within the group. They are found on the eye bulb, on the head and mantle surface, on the tips of the arms and tentacles and within the mantle cavity. The eyes and apparently the liver cannot be made transparent and it is interesting to note that in the transparent squids there are photophores on the ventral side of these organs and their lateral and dorsal surfaces are silver. Such an arrangement of photophores would break up the outline of the organs when seen against weak daylight from below (W. D. Clarke, 1963) and the silver sides would blend with any intensity of background light (Denton in press). Photophores are predominantly ventral in position with the exception of the photophores on the tips of arms and on the tentacles which possibly act as lures and the large dorsal photophores of some ommastrephids which possibly warn others of danger. Eyes of squids are large relative to the body and the reason for some modifications remain a mystery. For example, species of Calliteuthis possess a left eye which is much larger than the right eye. Sound production in oegopsids has been noted in the literature several times. Steenstrup (1881) quoted old descriptions which described the sounds of ommastrephids as squeaks and moans ’’ and those of Gonatus as wailing noises and Bartsch (1916) noted the popping sound when squids jumped clear of the water. Recording and analysis of sounds beneath the water was not made before Nishimura (1961) recorded swimming noises of 1 000-4 000 c/s with a peak a t 1 500 c/s. Hashimoto and Maniwa (1963) also recorded squid school noises a t 40-6 000 c/s with a peak a t 1 000-2 000 c/s. Iversen et al. (1963) recorded individual squids and found that they produce pulses of 500-2 500 c/s a t intervals of 31-48 msec. These pulses were produced

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in bursts of 28 to 47 pulses and bursts were thought to correspond to the exhalent current through the funnel. The pulses were thought to result from the vibration of the funnel lips. Symplectoteuthis oualaniensis, Onychoteuthis banksi and Thysanoteuthis rhombus were caught during the period recordings were made. The ability to hear has not been established for any cephalopods. XXVI. PARASITES Few parasites of oceanic squids have been described and nearly all are from ommastrephids. Dobell (1909) found two species of ciliate in Illex coindeti kidney (Chromadina elegans and C. coronata) and Jepps (1931) described a ciliate (C. elegans) from the renal sacs and coelomic spaces of Spirula. Pelseneer (1928) listed a trematode from Ommastrephes. Dollfus (1964) has reviewed the cestodes from cephalopods. Illex coindeti is a host of plerocercoids of Phyllobothrium sp. and P. tumidurn; Illex illecebrosus is a host of Dinobothrium plicatum and D. planum (both also found in sharks); Todaropsis eblanae is a host of Phyllobothrium tumidum and Dibothrium plicatum; Todarodes sagittatus is a host of a plerocercoid; T . pacificus is a host of " scolex polymorphus " and Nybelinia; Dosidicus gigas is a host of Phyllobothrium and a Tetrarhynchus larval form; Gonatus fabricii and Moroteuthis robusta are hosts of Nybelinia larvae. Squires (1957) reported Phyllobothrium sp. and Dinobothrium (sensu lato) sp. in Illex illecebrosus and found that whereas more squids are infected with the former in the early season at, the Grand Banks, the percentage infected with Dinobothrium increased through the season. Trypanorhynch cestodes, thought to be Nybelinia, have been recorded from Lepidoteuthis grimaldii (Clarke and Maul, 1962). Nematodes have been reported in Illex illecebrosus (Squires, 1957) and Lepidoteuthis grimaldii (Clarke and Maul, 1962). The latter were Anisakis sp.-a genus commonly infecting Sperm whales. XXVII. ECOLOGICAL IMPORTANCE Although oceanic squids do not form a large proportion of animals caught by the kinds of nets usually employed for the collection of biological specimens, there is good reason to believe they are present in very large numbers in all oceans of the world. If a ship stops a t night in any but high latitudes, squids are attracted t o the lights and are often seen in tens or hundreds within an hour. Except for a reduction of sightings during full moon, such observations may be made night after night for months on end during a voyage. The dominant forms

TABLEVI. PREDATORS EROM WHICH SQUIDS HAVE

Birds

Albatrossia pectoralia Diomedia immutabilis Rothschild Albatross Phoebetria f usca (Hilsenberg) Fu~muruagkzeialb (Lh.) sula sula (Linn.) sula Bp. GUU

Fregata aquila (Linn.) Anoiis tenuirostris (Temminck) Anoiis minutua Boie Macronectea gigantem (Gmelin) ~

IDENTIFIED TO SPECIES AND THE SPECIES FOUND

Gonatm magiater Onychoteuthis banksi Gonatua antarcticua; Taaniua pavo Tmniua pavo Gomtua fabricii sympkxtoteuthis owckzniensis Symplectoteuthia o u a l a n i e k Gonatue fabricii Ommaatrepha pteropua Hyaloteuthis pelagicua Symplectoteuthia oualaniensia Calliteuthia cookiam

~

Balaen whales Physeter catodon Linn. ( S p e r m whale)

Cetacea

BEEN

Hyperoodon sp. Delphinapterua leucaa (Pallas) Monodon monoceros Linn. Grampus griseus (Cuvier)

Todarodea pacificus; Watasenia ecintillana T a ~ n i u pavo; a Galiteuthia arm&; Oregonkteuthia lorigera; Hiatwteuthia bonellii; Calliteuthia dojleini; Calliteuthia eeparata; Chiroteuthie veranyi; Lepidoteuthia grimaldii; Qonatua fabricii; Gonatua antarcticue; Gonatua WW&~ET; Gonatopaia borealia; Ancistrocheim lesueuri; Octopoteuthia longiptera; Taningia dam; Architeuthia spp; Dosidicua gigaa; Todarodee 8agitt&&7;Onychoteuthia bankei; Moroteuthia ingens; Moroteuthis robuata; Tetronychoteuthia duamcmieri. Onychoteuthis b a n h i ; G o m t w fabricii Illex illecebrosua; Gonatuafabricii Gonatue fabricii Lepidoteuthia grimaldii: Gonatua fabricii: Todarodea Saa'itti~&M

Globicephala melaena (Traill) Steno rostratus (Cuvier) Dolphin Tursiops truncatus (Fabricius)

Seals

Fish

Taonius megalops; Illex illecebrosus T m n i u s megalops; Illex illecebrosua Lycoteuthis diadema; Chiroteuthia veranyi; Todarodea sagittatua; Anciatroteuthk lichtensteini; Tetronychoteuthis duasumieri; Ctenopteryx siculua; Abraliopsis morrisi; Pyroteuthis margaritijera Ornithoteuthis antillarum, Pterygioteuthis giardi, Octopoteuthis sicub, Galiteuthis ar?nata.

Cyatophora cristata (Ertleben) Callorhinus ursinus (Linn.)

Gonatus jabricii

Raja sp. Raja mouli Somnwsus microcephdua (Bloch and Schneider) Etmopterua hillianua Tuna cfermo alalunga Cetti

Todarodea pacificua Illex coindeti Gonatua jabricii

Thunnua albacarea Bonnaterre Thunnua germo Lac6pAde Thunnus maccoyii Castelnau Aphanopus carbo Lowe

Todarodes pacificus; Gonatuafabricii, Wataaenia scintillans

Abralia veranyi Gonatus jabricii; (Abralia steindachneri?);Entornopsis alicei; Ommaatrephea spp. ; Hiatioteuthis bonellii: Chiroteuthia veranyi; Liocranchia reinhardti; Taonidium pjefferi; Hdicocranchia pjefferi; Gditeuthis armata; IUex coindeti; Todaropeia eblanae; Todasodea sagittatua; Onychoteuthia ban&; Ctenopteryx siculua; Octopoteuthia aicula. Ommaatrephea spp. Enoploteuthia leptura Nototodarua sloani gouldi; Galiteuthia armatu Nototadam sloani gouldi Histioteuthis bonellii; Lepidoteuthk grimaldii; Enoploteuthia ampais.

TABLEV I . 4 o n t d . Thunnua obeaua Lowe Blue marlin Scomber scombrua Linn. Gadw mwhua Linn.

Fish (cont.)

cfadua aeglejinua Linn. Gadua virena Linn. Teregra chdcogramma Pallas Molva molva (Linn.) Sebaatea marinua (Linn.) Sebaatea mentella C c n y p h n a hippurua Linn. cfenypterua blacodea Alepiaaurus ferox Lowe

Orthugoniaeus mola (Linn.) Chlwophthalmus agaasizi Bonaparte Chauliodus sp. Cobconger raniceps Allcock Reptanehua sp.

Ommaatrepha spp.; Todarodea sagittatua ; Lepidoleuthis grimaldii; Thysanoteuthia rhombus Ommaatrephea epp. Ommaatrephea spp; Onychoteuthia bank&; Gonatus fabricii; Illex illecebrosua; Todarodea sagiltatua G&us fabricii G&ua fabricii Watarrenia scintilluns; Enoploteuthia chuni Onychoteuthb b a n h i ; Calliteuthis cookiana Gonatua fabricii Tetronychoteuthis duasumieri Todarodea paci$cua Calliteuthia cookiana Ommaatrephea spp; Pyroteuthia margaritifera; Hiatioteuthk bonellii; CaUiteuthis reversa; Maatigoteuthia schmidti; Grimalditeuthb bonphndi; Cranchia scabra; T a o n i w pavo; Todarodes sagittatus ;Onychoteuthw bank&; Abrdiop& morrisi. Illex illecebroaua Abralia veranyi Ctenopteryx eiculua Abraliopsi-9 r n h i Todaropsia eblam

REVIEW

OB THE SYSTEMATICS AND ECOLOGY OF OCEANIC SQUIDS

269

seen a t the surface at night are various members of the Ommastrephidae (pages 108, 115, 117). Most species have been recorded from the stomachs of various cetaceans, seals, fish and birds (Table VI). Many of these predators eat squids almost exclusively while a large number eat varying proportions of fish in addition. Many species of squid which are important in the diet of predators are rarely, if ever, caught by man-made collecting devices. For example, if it were not for the fact that large populations of Sperm whales mainly feed on such squids as Architeuthis, Taningia, Lepidoteuthis, Histioteuthis, etc., these would be considered extremely rare (Clarke, 1962a). Large numbers of squid beaks have been reported in bottom sediments and the largest quantities have been related to areas of productivity (Belyaev, 1959, 1962; Clarke, 1962e). It was estimated that up to 15 000 beaks may be present on a square metre of bottom in some areas (Belyaev, personal communication). The majority of such beaks are very small and may represent larval mortalities. Clearly, active carnivores like squids must have a terrific influence on the balance of life in any area. The young seem to feed largely on crustacea and small fish while the larger specimens take fish and other squid. It has been suggested they have a direct effect, by predation, on certain commercial species of fish including redfish (Nesis, 1966),cod (Clarke, 1963),mackerel (Clarke, 1963)and herring (Fridriksson, 1943 etc.). They must also have an indirect effect by competing with some commercial species for food; Nesis (1965) considered that Qonatus fabricii competed with redfish in this way.

IMPORTANCE XXVIII. ECONOMIC The economic importance of cephalopods in general may be seen from Table VII. The catches tabulated are probably rather lower than those actually taken because cephalopods are often excluded from catch statistics. From the table there is some indication of a rise in the importance of cephalopods. It is rather difficult to assess the extent t o which oegopsids contribute t o the catches. However, nearly all squid taken in Japan, the country with the greatest consumption, are oegopsids including the local " common " squid Todarodes paci$cus and Watasenia scintillans. Illex illecebrosus is the squid most frequently taken off Newfoundland (Hodder, 1964) but only a small proportion of those taken are given in statistics. Again, Madeira where large catches are made, does not appear in statistics (unless it is under Portugal) ; here the principal species caught are Ommastrephes caroli, 0. pteropus and Todarodes sagittatus. In Norway Todarodes

270

MALCOLM R. CLdaKE

sagittatus is becoming economically important (LsvBs-Svendsen, 1964) and is sometimes important in North Sea catches (Ottolind, 1954). Various countries bordering the Mediterranean include Todarodes sagittatus in their catches (e.g. Italy, France, Spain) (Ghirardelli, 1961). In Australia, Nototodarus gouldi is being taken in increasing numbers (Anon, 1964). In some regions, an occasional abundance of a particular species is followed by a temporary development of a fishery; for example Dosidicus gigas has been used commercially off California a t times (Clark and Phillips, 1936). In all, the deep sea cephalopods, the oegopsids, contribute about three quarters of the total world catch of cephalopods and of these nearly all are in the Ommastrephidae. Constituents of squid have been studied by Japanese workers (Takahashi, 1960, etc.) and the protein content (20%) compares favourably with economically important fish. Use of squid for human food has been extensively studied by the Japanese; from the nutritive value and digestibility of squid meat (Tanikawa and Suno, 1952) to the manufacture of particular products such as smoked squid meat (Tanikawa et al., 1964) and canned squid (Inoue and Tanikawa, 1962). Besides its utilization as human food, squid meat is used extensively for animal food and manure and of all uses the most important must be its use as bait. It is the principal bait in theNewfoundland cod fishery (Squires, 1957) and forms an important bait for the Northern long line fishery (Nesis, 1964 footnote to translation of Clarke, 1963) and the Madeiran Espada fishery (Clarke, 1963) and for many minor and game fisheries. Should the world’s consumption of squid increase to the point where other species must be utilized, the most productive species would be the oceanic squids, providing methods of catching them could be improved. As pointed out above, species of Ommastrephes, Symplectoteuthis, Todarodes, Nototodarus and Dosidicus are dominant oceanic forms and approach the surface a t night. Only Todarodes pacijcus has been utilized to any appreciable extent. If catching methods could be developed to take the deeper living species, which are so important in the diet of Sperm whales and other predators, large untapped protein and oil resources would become available. XXIX. CATCHING METHODS The principal tool in use in most parts of the world for catching oegopsid squid is the I ‘ jig ”. This takes various forms but basically it is a grapnel-type of hook usually about 6 inches long. A ring of points, usually unbarbed, project from the tip of the shaft which may pass through a lead weight (Newfoundland style) or a bait fish (Madeira

ACCORDING TO THE CATCHIN 1964 TABLEVII. THE WORLDCATCHOF SQUIDS. COUNTRIESARRANQED (from the F.A.O. Yearbook of Fishery Statistics 1960 and 1964)

I Catch in Thousand metric tons ~

1948 Japan

I

1956

1957

1968

1959

1960

1961

1962

1963

1964

418.5 39.5 5.6 2.9

393.1 33.5 9.2

641.9 42.1 9.4

0.8

438.4 46.8 6.5 3.1

1.2 3.4 3.4

3.3

3.3

437.1 83.0 12.9 9.0 4.1 4.7 4.1 1.7 4.7

1.8 1.0 1.7 1.1 0.2

0.1

588.8 56.9 15.2 0.8 8.6 4.3 3.6 1.4 3.8 6.0 1.6 2.2 1.3 0.7 0.2 0.4 0.1

0.1 0.2

0.2 0.3

0.1

0.2

0.1 0.1 1.1 0.1 0.1

652.1 117.1 14.2 2.4 9.8 5.2 3.8 2.7 3.3 0.5 1.9 2.2 1.2 0.4 0.4 0.5 0.2 0.1 0.1 0.1 0.1 0.3 0.1 0.1

309.1 86.6 16.4 10.8 9.3 7.4 4.3 3.0 1.8 1.5 1.3 1.0 0.7 0.6 0.5 0.5 0.2 0.2 0.2 0.2 0.1 0.2 0.1

697.4

818.8

466.0

~~

105.9 1.3 4.5 0.8

0.1 2.1

301.3 8.0 6.5

434.4 18.3 4.8 7.1

346.0 21.8 4.1 8.3

8.7

0.4 2.1 0.2

0.1 Venezuela S. Africa

1955

0.1 0.5 1.9 0.4 0.2

0.6 1.4 0.6 0.3

0.1 1.0 2.7 0.5 0.2

1

0.4

0.4

1.5 0.5 0.6

0.1

I

0.1 0.1

0.1 0.1

0.1 0.1

0.1

0.1 0.1

0.1 0.1

0.1

TOTAL

2.4 9.6 0.8 2.0

6.1

0.2 0.1 0.9 0.1

327.2

468.0

383.4

471.4

0.1 0.2 0.9 0.1 0.1

0.1

-114.9

1.2 1.5 0.7 0.4 0.2 0.6 0.2

461.6

604,3

605.1

667.6

272

MALCOLM R. CLARKE

style); alternatively, the shaft may be a sperm whale tooth (Japan). The hooks may be baited or coloured to attract the squid. I n Norway it is coloured red (Lervhs-Svendsen) while in Japan white is used. Although jigs differ, the mode of operation is the same; the jig is jerked up and down for several feet and the squids take it as it moves. This traditional method has been used for many decades and possibly centuries with little modification. Quigley (1964) has recently invented a mechanical jigger consisting of motor driven drum haulers, special lure hooks and a light attraction system. With this one man can operate ten lines. Electrical fishing has been used to catch Octopus and Sepia for aquaria because they approach the anode (Lamarque, 1962) but its practical use for collection of oceanic species is probably a very long way off. Seines are effective in catching squids where the water is not too deep and, except around Japan, few oegopsids are taken in this way. However, off Scotland, Todaropsis eblanae has been caught in certain years and has proved rather a nuisance as it is unacceptable to the Continental markets to which Loligo is exported from Scotland . (Rae and Lamont, 1963; Davidson, 1963). Development of squid fisheries in deep water would probably depend on development of midwater trawls. Trawls catch a proportion of squid when operated on the bottom; Todarodes sagittatus is caught in this way off Iceland, the Faroes and northern Norway by trawlers operating from Hull and Grimsby (Clarke, 1963) and in the North Sea by Scandinavian fishermen (Otterlind, 1954). Up t o now, however, no midwater trawl has been developed which will catch any but the smallest species.

XXX. ACKNOWLEDGMENTS Dr. A. M. Bidder and Dr. W. J . Rees very kindly read and criticized the manuscript, for which I am most grateful and wish to record my sincere thanks. I would also like to express my very warm thanks to the Library Staff of the National Institute of Oceanography for their constant assistance in borrowing papers and their great help in preparing the reference list and typing the final copy of the review, and also to various members of the biological staff for their help in checking and typing the text.

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273

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c.

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Sylva, D. P. de (1962). Red water blooms off northern Chile April-May 1966 with references to the ecology of swordfish and the striped marlin. Paif. Sci. 16, 271-9. Takahashi, T. (1960). Studies on the utilization of cuttle-fish Ommaatrephes sloani pacijcus 111. The seasonal variation in the gravimetric constitution and chemical composition of the various parts of the body. Bull. Jap. SOC. acient. Fish. 26, 95-8. Tanikawa, E., Minoru, A., and Motohiro, T. (1964). Studies on a complete utilization of squid Ommastrephes sloani pacijcus. X X . Manufacture of smoked squid meat. Bull. Fa. Fish Hokkaido Univ. 14, 243-61. Tanikawa, E., and Suno, M. (1952). Studies on the complete utilization of squid Ommastrephes sloani paci;ficus). 5 . Nutritive and digestibility of squid meat. Bull. Fac. Fish. Hokkaido Univ. 3, 75-80. Targioni-Tozzetti, A. ( 1 8 6 9 ~ )Estratto . di un catalog0 sistematico e critic0 dei molluschi cefalopodi del Mediterraneo, posseduti dal R. Museo di Firenze, con alcune specie nuove. Atti SOC.ital. Sci. nut. 12, 586-99. Targioni-Tozzetti, A. (1869b). Commentario sui cefalopodi Mediterraneo del R. Museo di Firenze. Bullettino Makxologico Ihliano, 2, 141-62. and 2 09-5 2. Tauti, M. (1941). On the stock of Ommastrephea paci;ficw Appellof. Bull. Jap. SOC.scient. Fish. 10, 111-14. Tesch, J. J. (1908). Bijdrage tot de fauna der Zuidelijke Noordzee. 111. Cephalopoda ten deele verzameld met de “ Wodan ”. Jaarb. Rijksinst. Onderz. Zee, 3-24. Thiele, J. (1916). Bermerkungen uber die Systematik der achtarmigen Cephalopoden. 2001.Anz. 48, 3-4. Thiele, J. (1921). Die Cephalopoden der Deutsch Siidpolar-Expedition 1901-1903. Dt. Sudpol. Exped. 16 (Zoology Bd 8), 433-65. Thompson, D’A. W. (1900). On a rare cuttlefish, Ancistroteuthis robustta (Dall). Steenstrup. Proc. zool. SOC.Lond. 992-8. Thore, S. (1945). On the Cephalopoda of Professor 0. Carlgren’s Expedition to South Africa in 1935. K . fysiogr. Sallsk. Lund Fiirh. 15, 49-57. Thore, S. (1959). Reports on the Lund University Chile Expedition 1948-49. 33. Cephalopoda. Acta Univ. Lund. Ser. 2, 55, 1-19. Tinbergen, L., and Verwey, J. (1945). Zur Biologie von Loligo vulgaris Lam. Archs ngerl. Zool. 7 (1, 2), 213-86. Tinbergen, N. (1928). Een merkwaardige Schipbreukeling (Ommaatrephea sagittatus d’Orb.) Levende Nut. 33, 45-8. Torchio, M. (1962). Su di un interessante cefalopodo di profonditlr pescato in mar Ligure: Calliteuthia meneghinii (VBrany) 1851 (Dibranchia Histioteuthidae). Natura, Milano, 53. ( l ) , 32-37. Troschel, E. (1857). Bemerkungen uber die Cephalopoden von Messina. Arch. Naturgesch. 23, 41-76. Tryon, G.W. (1879), ‘‘ Manual of Conchology ”,Vol. I. “ Cephalopoda ”, 316 pp. Philadelphia. Utsuno, Sh. (1932). A list of the Cephalopoda of Kagoshima Bay. Venus, Kyoto, 3, 228-33. (In Japanese.) VBlain, C. (1877). Remarques gBnBrales au sujet de la faune des fles St. Paul et Ansterdam, suivies d’une description de la faune malacologique des deux iles. A r c h . 2001.exp. gbn. 6 , 1-144. VBrany, J. B. (1837). MBmoire sur six nouvelles esphces des cBphalopodes trouvbes dans le MBditerranBe B Nice. Memorie Accccd. Sci. Torino, Ser. 2 , 1, 91-8.

298

MALCOLM R. CLARKE

VBrany, J. B. (1851). " Mollusques MBditerranBens ", I. " CBphalopodes, " 132 pp. Ghnes. Verco, J. C., and Cotton, B. C. (1928). South Australian Cephalopoda. Rec. S. Auat. Mus. 4, 125-33. Verrill, A. E. (1874a). Occurrence of gigantic cuttle-fishes on the coast of Newfoundland. Am. J. Sci. Ser. 3, 7 , 158-61. Verrill, A. E. (1874b). The giant cuttle-fishes of Newfoundland and the common squids of the New England coast. Am. Nat. 8, 167-74. Verrill, A. E. (1875a). Notice of the occurrence of another gigantic cephalopod (Architeuthia)on the coast of Newfoundland, in December, 1874. Am. J. Sci. Ser. 3, 10, 213-4, also in Ann. Mag. nat. Hiat. Ser. 4, 16, 266-8. Verrill, A. E. (1875b). The gigantic cephalopods of the North Atlantic. Am. J. Sci. Ser. 3, 9, 123-30. Verrill, A. E. (18750). The gigantic cephalopods of the North Atlantic. Am. J. Sci. Ser. 3, 9, 177-85. Verrill, A. E. (1875d). The colossal cephalopods of the North Atlantic I and 11. Am. Nat. 9, 21 and 78. Verrill, A. E. (1876). Note on gigantic cephalopods-a correction. Am. J. Sci. Ser. 3, 12, 236-7. Verrill, A. E. (1877). Occurrence of another gigantic cephalopod on the coast of Newfoundland. Am. J. Sci. Ser. 3, 14, 425-6. Verrill, A. E. (1878). Notice of recent additions to the marine fauna of the eastern coast of North America. Nos I and 11. Am. J. Sci. Ser. 3, 16, 207-216 and 371-8. Verrill, A. E. (1879a). Notice of recent additions to the marine fauna of the eastern coast of North America, No. 111. Am. J. Sci. Ser. 3, 17, 239-43. Verrill, A. E. (1880a). Notice of the remarkable marine fauna occupying the outer banks of the southern coast of New England. Am. J. Sci. Ser. 3, 20, 390-403. Verrill, A. E. (1880b). Notice of recent additions to the marine invertebrate of the north-eastern coast of America. Pts. 2-3. Proc. U.S. natn. Mua. 3, 356-409. Verrill, A. E. (18800). Synopsis of the Cephalopoda of the north-eastern coast of America. Am. J. Sci. Ser. 3, 19, 284-95. Verrill, A. E. (1880d). Notice of recent additions to the marine fauna of the eastern coast of North America. No. VIII. Am. J. Sci. Ser. 3, 19, 137-40. Verrill, A. E. (1880-1881). The cephalopods of the north-eastern coast of America, Pert 11. The smaller cephalopods, including the " squids " and the octopi, with other allied forms. Tranrr. Conn. A d . Arts. Sci. 5, 259-446. Verrill, A. E. (1881a). Notice of the remarkable marine fauna occupying the outer banks off the southern coast of New England. No. 11. Am. J. Sci. Ser. 3, 22, 292-303. Verrill, A. E. (1881b). Giant squid (Architeuthia)abundant in 1875, at the Grand B d s . Am. J. Sci. Ser. 3, 21, 251-2. Verrill, A. E. (18810). Report on the cephalopods and on some additiond species dredged by the U.S.Fish Commission Steamer"' Fish-hawk ",during the season of 1880. Bull. Mua. comp. 2001. Harv. 8, 99-116. Verrill, A. E. (1882a). Notice of recent additions to the marine invertebrata of the north-eastern coast of America. Part IV. Additions to the deep-water Mollusce, taken offMartha's Vineyard, in 1880-1881. Proc. U.S.natrc. Mw. 5, 316-43.

REMEW OF THE SYSTEMATIOS AND ECOLOGY OF OCEANIC

SQUIDS

299

Verrill, A. E. (1882b). Notice of the remarkable marine fauna occupying the outer banks off the southern coast of New England, No. VII, and some additions to the fauna of Vineyard Sound. Am. J . Sci. Ser. 3, 24, 360-71. *Verrill, A. E. (1882~). Catalogue of marine Mollusca added to the fauna of New England during the past ten years. Tram. Conn. Acad. Art8 Sci. 5 , 177-257, 395-468, 447-687. Verrill, A. E. (1882d). Occurrence of an additional specimen of Architeuthie at Newfoundland. Am. J. Sci. Ser. 3, 23, 71-2. Verrill, A. E. (1882e). Report on the cephalopods of the north-eastern coast of America. Rep. U.S. Commnr Fieh. 1879, 7, 211-460. Verrill, A. E. (1883). Supplementary report on the Blake cephalopods. Bull. Mus. comp. Zool. Ham. 11, 105-16. Verrill, A. E. (1884-1885). Second catalogue of Mollusca recently added to the fauna of the New England coast and the adjacent parts of the Atlantic. Trans. Conn. Acad. Art8 Sci. 6 , 139-294. Verrill, A. E. (188th). Third catalogue of Mollusca recently added to the fauna of the New England coast and the adjacent parts of the Atlantic, consisting mostly of deep sea species with notes on others previously recorded. Tram. Conn. Acad. Arts Sci. 6 , 395-458. Verrill, A. E. (1886b). Results of the explorations made by the steamer " Alba-. tross" off the northern coast of the United States in 1883. Rep. U.S Cornmnr Fish, 11, 503-699. Verrill, A. E. (18974. A gigantic cephalopod on the Florida coast. Am. J. Sci. Ser. 4, 3, 79, 162-3 and 365-6. Verrill, A. E. (189713). The Florida monster. Science, N . Y . 5 , 392 and 476. also paper of same title published Am. Nat. 31, 304-7. Vigelius, W. J. (1881). Untersuchungen an Thysanoteuthie rhombus Trosch. Ein Beitrag zur Anatomie der Cephalopoden. Mitt. zool. Stn Neapel, 2 , 160-61. Vladykov, V. D. (1946). l h d e sup les m a m m i f h s aquatique. 4. Nourriture du marsouin blanc ou beluga (Delphinapterua leucaa) de fleuve St. Laurent. Contr. Ddp. P&h. Qudb. No. 17, 1-158. Voss, G. L. (1954a). Cephalopods of the Gulf of Mexico. Fieh Bull. Calif. 55, 475-8. Voss, G . L. (1954b).Decapodous cephalopod mollusks from the Marshall Islends. POL$.S C ~8,. 363-6. Voss, G. L. (1956). The Cephalopoda obtained by the Harvard-Havana expedition off the coast of Cuba in 1938-39. Bull. mar. Sci. Gulf Caribb. 5 , 81-115. Voss, G . L. (1956a). A checklist of the Cephalopoda of Florida. Q. J1 Fla Acad. Sci. 19, 274-82. Voss, G. L. (1956b). A review of the cephalopods of the Gulf of Mexico. BuU. mar. Sci. Gulf Caribb. 6 , 85-178. VOSS,G. L. (1957). Observations on Ornithoteuthis antilhrum Adam 1967 and ommastrephid squid from the West Indies. Bull. mar. Sci. Gulf Caribb. 7, 370-8. Voss, G. L. (1968). The cephalopods collected by the R/V " Atlantis " during the West Indian cruise of 1964. Bull. mar. Sci. Gulf Caribb. 8, 369-89. Voss, G.L. (1960). Bermudan cephalopods. FieldiOna, Zool. 39, 419-46.

*

This contains ell his previous work on cephdopode.

300

MALCOLM R. CLARKE

Voss, G. L. (1962a). Six new species and two new subspecies of cephalopods from the Philippine Islands. Proc. biol. SOC.Wash. 75, 169-76. Voss, G. L. (1962b). Ascocranchia joubini, a new genus and species of cranchiid squid from the North Atlantic. Bull Inst. ocdanogr. Monaco, No. 1242, 1-6. Voss, G.L. (1962~).List of the types and species of cephalopods in the collection of the Acadamy of Natural Sciences of Philadelphia. Notul. Nut. No. 356,l-7. Voss, G. L. (1962d). A monograph of the Cephalopoda of the North Atlantic. I. The family Lycoteuthidae. Bull. mar. Sci. Uulf Caribb. 12, 264-305. Voss, G. L. (1962e). South African cephalopods. Trans. R . SOC. S. Afr. 36,245-72. Voss, G.L. (1963a).Cephalopods of the Philippine Islands. Bull. U.S. natn. Mus. NO.234, 1-180. Voss, G. L. (1963b). A new species of cranchiid squid Phasmalopsia lucqer, from the Gulf of Mexico. Bull. mar. Sci. Gulf Caribb. 13, 77-83. Voss, G. L.,and Erdman, D. S. (1959). Thysanoteuthis rhombus. Large cephalopod new to the western Atlantic. Nautilus, 73, 23-5. Voss, N. A., and Voss, G. L. (1962). Two new species of squids of the genus Calliteuthis from the western Atlantic with a redescription of Calliteuthia reversa Verrill. Bull. mar. Sci. Gulf Caribb. 12, 169-200. Watas6, S. (1905). Luminous organs of Abraliopais, a new phosphorescent Mag. Tokyo, 17,119-22. (InJapanese.) cephalopodfromthe Japan Sea. 2002. Webb, W. de (1897). A large decapod. Nautilus, 10, 108. Weindl, T. (1912). Vorlliufige Mitteilung iiber die von S. M. Schiff, “Pola” im Roten Meere gefundenen Cephalopoden. Anz. Akad. W k s . Wien, Mathematische-naturwissenschaftliche Klasse, 49, 270-5. Weiss, F.E. (1889). On some oegopsid cuttle fishes. Q . Jl microso. Sci. 29, 76-96. Wilhelm, 0.G. (1931). Das Massensterben von Tintenfischen in der Bucht von Talcahuano. Archo 2001. ital. 16, 334-9. Wilke, F.,and Kenyon, K. W. (1954). Migration and food of the northern fur seal. Trans. 19th. N . Am. Wildl. Conf. March 9, 10 and 11, 1954, 430-40. Williams, L. W. (1909). “ The Anatomy of the Common Squid Loligo pealei Lesueur ”, 92 pp. E.J. Brill, Leiden. \Vim, K. see Mangold-Wirz, K. Woodward, B. B. (1923). Note on the capture of Spirula alive. Proc. malac. SOC.Lond. 15, 173. Wiilker, G. (1910). “ tiber japanische Cephalopoden. Beitrage zur Kenntnis der Systematik und Anatomie der Dibranchiaten ”, 71 pp. Miinchen. Wiilker, G. (1920). nber Cephalopoden des Roten Meeres. Senckenbergiana, 2, 48-58. Yates, L. G. (1889). Stray notes on the geology of the Channel Islands. The Mollusca of the Channel Islands of California. Rep. Calif. St. Min. Bur. NO. 9, 171-8. Young, R. E. (1964). A note on three specimens of the squid Lampadioteuthia megaleia Berry, 1916 (Cephalopoda: Oegopsida) from the Atlantic Ocean, with a description of the male. Bull. mar. Sci. Gulf Caribb. 14, 443-62.

Author I ndex Numbers ,initalics refer to pages on which references appear at the end of t/Le chapter.

A

B

Abbott, J. D., GO, 84 Adam, W., 106, 108, 111, 113, 115, 117, 118, 119, 122, 123, 125, 126, 127, 129, 130, 141, 143, 145, 147, 149, 173, 174, 179, 180, 182, 184, 187, 189, 199, 202, 204, 206, 208, 216, 217, 219, 221, 273 Ahlstrom, E. H., 52, 65 Aiso, K., 60, 65 Akhmerov, A. K., 19, 23, 65 Akimushkin, I. I., 98, 101, 113, 132, 143, 145, 147, 148, 154, 157, 158, 159, 176, 178, 189, 200, 204, 205, 236, 238, 256, 273, 274, 275 Aleem, A. A., 16, 65 Alexander, D. M., 12, 57, 65, 80 Alexandrowicz, J. S . , 5 , 65 Alicata, J. E., 59, 65 Allan, J., 98, 101, 140, 141, 152, 164, 171, 176, 180, 199, 208, 222, 223, 227, 228, 231, 255, 274 Allen, F. W., 53, 65 Altara, I., 3, 65 Amlacher, E., 2, 65 Anderson, A. G., 57, 65 Anderson, E. J. M., 52, 67 Andrews, G. L., 37, 86 Annenkova-Khlopina, N. P., 22, 65 Anon, 119, 140, 270, 274 Anonymous, 5 , 66 Appellof, A., 149, 152, 169, 184, 187, 2 74 Apstein, C., 15, 66 Arai, Y., 18, 66 Aratara, G. F., 109, 129, 274 Arbocco, G., 194, 274 Aronson, J. D., 12, 57, 66 Ashworth, J. H., 169, 274 Assis, M. E., 7 8 Atkinson, G. T., 127, 292 Aucapitaine, H., 148, 203, 274 Auerbach, M., 21, 66

Baccialon, A., 148, 27-1 Baer, J. C., 29, 6G Bagge, J., 11, G6 Bagge, O., 11, G'G Baines J. M., 141, 274 Baker, A. de C., 105, 108, 274 Balamuth, W., 16, 71 Ball, R., 125, 274 Bardarson, G. G., 98, 119, 127, 152, 2 74 Barnard, K. H., 127, 159, 1G1, 274 Barnes, G. A., 157, 159, 2SO Barraca, I. F., 16, 78 Bartsch, P., 264, 274 Baudouin, M., 35, 66 Baylis, H. A., 30, 66 Bearse, H. M., 34, 71 Beatti, M., 36, G6 Beebe, W., 227, 274 Belding, D. L., 59, 66 Belyeev, M., 269, 274, 275 Bennett, W. E. J., 60, 79 Bergman, A. M., 2, 10, 11, 13, 66 Berland, B., 31, 66 Berry, S. S . , 106, 109, 113, 115, 116, 117, 127, 140, 141, 143, 145, 154, 158, 164, 171, 173, 174, 176, 182, 184, 186, 190, 193, 199, 202, 204, 210, 215, 219, 221, 223, 231, 238, 275 Bespalyi, I. I., 16, 66 Beteshava, E. I., 98, 132, 143, 145. 147, 148, 154, 157, 158, 204, 236, 238, 275 Beyers, E., 18, 68 Bianco, S. Lo, 127, 169, 182, 194, 275 Bigelow, H. B., 61, 85 Bisset, K. A., 52, 53, 66, 67 Blake, I., 5 2 , 67 Blake, J. H., 98, 275 Bogdanova, E. A., 21, 28, 67 Boone, J. G., 9, 85

301

302

AUTHOR INDEX

Boone,L., 116, 119, 141, 143, 176, 223, 276 Bories, S., 59, 80 Bosc, L. A., 117, 276 Boutan, L., 276 Bouxin, J., 113, 125, 126, 127, 131, 141, 143, 145, 169, 187, 189, 194, 197, 204, 205, 219, 221, 229, 231, 232, 236, 276 Bovee, E. C., 16, 71 Bradford, A., 21, 71 Brazier, J., 115, 117, 127, 140, 141, 143, 238, 276 Breder, C. M., 56, 77 Breed, R. S., 3, 13, G7

Breslauer, T., 7, 67 Broek, A. N. C. T., 127, 129, 286 Brongersma-Sanders, M . , 40, 67 Brown, E. M., 16, 57, 58, 67 Brunel, P., 119, 292 Brunner, G., 54, 80 Bruun, A. F., 10, 43, 45, 98, 101, 104, 119, 127, 129, 141, 152, 155, 164, 234, 241, 243, 244, 67, 276 Buckrnann, A., 11, 67 Bullock G. L., 9, 13, 67, 85 Bullock, W. L., 32, 67 Burton, R. W., 59, 68 Bykhovskaya-Pavlovskaya, I. E., 26,

67 Bykhovskii, B. E., 2, 26, 69, 79

C Cadenat, J., 98, 276 Cameron, T. W. M., 59, 67 Canestrini, G., 10, G7 Cantrabe, F., 127, 276 Carcelles, A. R., 106, 180, 276 Carini, A., 18, 67 Carpenter, P. P., 113, 116, 143, 276 Carus, J. V., 203, 276 Castellanos, Z. J. A. de, 276 Cendrero, O., 294 Chadwick, H. C., 123, 276 Chandler, A. C., 27, 28, 32, 68 Chappell, R., 59, 81 Cheng, T. C., 59, 68 Chiaje, S. D., 127, 276 Chlupaty, P., 56, 68

Christensen, N., 25, 68 Christiansen, M., 7, 68 Chuinard, R. G., 7, 88 Chun, C., 110, 111, 119, 123, 126, 131, 176, 187, 206, 216, 227, 238,

141, 177, 189, 208, 217, 228, 240,

152, 164, 165, 167, 178, 179, 180, 184, 191, 198, 202, 204, 209, 210, 212, 214, 219, 221, 222, 223, 229, 230, 234, 236, 241, 243, 276, 277 Clark, F. N., 117, 270, 277 Clarke, J. M., 120, 277 Clarke, M. R., 98, 101, 106, 111, 115, 127, 130, 131, 143, 147, 159, 190, 194, 197, 198, 200, 214, 233, 234, 258, 262, 264, 269, 270, 272, 277, 293 Clarke, ,R., 98, 104, 108, 113, 145, 190, 194, 197, 213, 277 Clarke, W. D., 127, 264, 277 Clarke, W. J., 105, 127, 277, 278 Classic, R. F., 147, 278 Cleland, J. B., 19, 7 2 Clem, L. W., 4, 8, 52, 68, 83 Clemens, H. B., 238, 278 Clemens, L. S., 29, 68 Clemens, W. A., 29, 68

169, 185, 205, 216, 224, 237,

113, 152, 213, 265, 162,

Clench, W. J., 288 Collett, R., 152, 157, 278 Collingwood, C., 255, 278 Colwell, R. R., 13, 68 Condie, R. M., 54, 78 Conroy, D. A., 57, 68 Cooper, R. A., 7, 88 Corliss, J. O., 16, 71 Cotton, B. C., 140, 141, 278, 298 Cox, P., 14, 41, 68 Croker, R. S., 117, 147, 278 Crosnier, A., 278 Crosse, H., 98, 100, 278 Cunliffe, A. C., 60, 84 Cushing, J. E., 53, 68

D Dall, W. H., 115, 116, 143, 154, 157, 278 Dannevig, A., 11, 21, 68 Dautzenberg, P., 127, 141, 278

303

AU!PEOB INDEX

Davidson, C., 278 Davies, R., 18, 68 Davis, F. M., 127, 292 Davis, H. S . , 3, 13, 18, 68 Dawes, B., 3, 26, 68 Dawson, C. E., 38, 68 De Blainville, M. H., 123, 275 Degner, E., 126, 141, 143, 145, 154,

Engelbrecht, H., 7, 60, 69 Erdman, D. S . , 159, 161. 300 Emma, A., 294

F

E

Fabricius, O., 152, 279 Fagetti, E., 279 Fantham, H. B., 21, 69 Farrin, A. E., 52, 84 Feddersen, A., 10, 69 FBrussac A. de, 194, 203, 279 Ficalbi, E., 187, 200, 203, 205, 279 Fiebiger, J., 17, 69 Fine, J., 54, 69 Finstad, J., 54, 78 Firth, F. E., 34, 71, 77 Fischer, H., 180, 194, 208, 210, 279 Fischer, P., 98, 100, 127, 278, 279 Fischer, P. H., 127, 278 Fischer, W., 279 Fischthal, J. H., 23, 69 Fiscus, C. H., 157, 159, 280 Fish, F. F.,19, 41, 7 0 Fish, F. W., 14, 70 Fisher, H. O., 29, 83 Fleming, A. M., 29, 30, 86 Fletcher, L. I., 18, 70 Floodgate, G. D., 13, 83 Ford, E., 38, 57, 70 Forrester, C. R., 18, 70 Fowler, G. H., 164, 280 Friddle, S. B., 53, 85 Fridriksson, A., 127, 129, 130, 131, 139. 257, 269, 280 Friele, H., 154, 234, 280 Friis, R. R., 8, 68 Frost, N., 98, 104, 119, 120, 121, 122, 152, 280 Fryer, J. L., 53, 85 Fujita, T., 2, 17, 70 Fukataki, H., 179, 186, 255, 295 Fukumi, H., 60, 81 Furtado, A., 104, 105, 280

Earp, B. J., 12, 13, 16, 69, S l Ehlinger, N. F., 54, 69 Elera, R. P. F. deC., 141, 171, 224, 279 Elkan, H., 2, 80 Ellis, C. H . , 16, 69 Elmhirst, R., 127, 129, 131, 279

Gabb, W. M., 113, 143, 280 Gaimard, J. P., 113, 115, 171, 293 Gamulin-Brida, H., 123, 125, 127, 280 Garcia-Tello, P., 116, 280 Garnjobst, L., 13, 70

155, 182, 203, 236,

159, 161, 164, 169, 176, 178, 184, 187, 189, 194, 199, 200, 204, 209, 212, 221, 229, 234,

238,278 De Graff, F., 56, 68 De Lamarck, J. B. P. A., 126, 287 Dell, R. K., 98, 101, 140, 143, 145, 162, 165, 166, 178, 194, 197, 198, 199, 208, 217, 229, 231, 237, 278,

2 79 Denton, E. J., 241, 255, 262, 279 Desbrosses, P., 123, 125, 227, 228, 279 De Sylva, D. P., 116, 117, 297 De Webb, W., 98, 300 Dicks, H. G., 60, 83 Dieuzeide, R., 123, 129, 279 Digby, B., 187, 279 Dionne, R. D., 264, 285 Dobdl, C. C . , 265, 279 Dogie1,V. A., 2,3, 17, 22,23,26, 27,31, 48, 49, 51, 69 Dollfus, R. P., 17, 28, 32, 33, 49, 69 Dollfus, R-Ph., 265, 279 D'Orbigny, A., 113, 116, 117, 123, 148, 152, 176, 180, 184, 194, 203, 214, 215, 224, 279, 291 Dreyer, N. B., 52, 69 Drilhon, A., 54, 69 Dubinin, V. B., 26, 69 Duff, D. C . B., 53, 69 Dunbar, C. E., 3, 4, 8, 21, 71, 79 Duncan, D. D., 116, 279

G

304

AUTHOR INDEX

Gaylord, H. R., 36, 70 Geiling, E. M. K., 147, 293 Gemmill, J. F., 37, 70 Gervais, P., 280 Getsevichyute, S . I., 30, 70 Ghirardelli, E., 270, 280 Ghittino, P., 3, 42, 70 Giard, A., 280 Gilchrist, J. D. F., 18, 70 Gillespie, A., 127, 129, 280 Gilpin-Brown, J., 262, 279 Girard, A. A., 98, 123, 125, 126, 127, 141, 150, 280, 281 Glantz, P. J., 60, 70 Gnanamuthu, C. P., 35, 7U Goddard, T. R., 105, 289 Godfrey, F. K., 141, 278 Gojdics, M., 71 Goncharov, G. D., 53, 54, 70 Good, R. A., 54, 78 Goodrich, E. S . , 105, 170, 171, 176, 230, 281 Gordon, M., 35, 36, 70 Gould, A. A., 141, 281 Gourley, R. T., 7, 88 Graham, H. W., 61, 85 Graham, T. R., 43, 86 Grainger, J. H. R., 30, 70 Gray, J. E., 117, 140, 143, 174, 216, 224, 281 Grenacher, H., 256, 281 Grieg, J. A., 98, 127, 129, 131, 152, 154, 157, 164, 237, 281 G r f i t h , A. S., 12, 71 Grimpe, G., 98, 119, 123, 125, 126, 127, 141, 149, 152, 154, 155, 157, 159, 165, 173, 174, 187, 194, 215, 234, 237, 281 Groninger, H. S., 18, 19, 78 Grosnier, 123 Gudger, E. W., 38, 71 Guenther, R. W., 8, 71, 87 Gustafson, P. V., 14, 81 Guiart, J., 58, 59, 71 Gyngell, W., 105, 125, 127, 281, 282

H Hahn, C. W., 19, 71 Haley, A. J., 21, 32, 71, 7 2 Hall R. P., 71

Hamabe, M., 132, 134, 135, 136, 137, 282 Hamilton, J. E., 282 Hansen, H. J., 33, 71 Hansen, P. A., GO, 74 Hansen, S., 11, 21, 68 Hardcastle, A. B., 17, 71 Hargis, W. J., 46, 71 Harting, P., 190, 282 Harvey, M., 98, 282 Hashimoto, T., 264, 282 Hayashi, 136, 282 Hayes, P. R., 13, 83 Hedley, C., 282 Heezen, B. C . , 255, 282 Heiberg, B., 10, 43, 45, 67 Heist, C. E., 53, 73 Heller, A. F., 29, 71 Heptner, W. G., 145, 282 Herklots, J. A., 127, 283 Herrington, W. C , 34, 71 Hertling, H., 105, 125, 127, 283 Herzenstein, S., 127, 130, 283 Hidalgo, J. G., 148, 283 Hikita, T., 338, 283 Hildomann, W. H., 54, 71 Hilgendorf, F., 98, 283 Hirsch, J. G., 52, 71 Hjort, J., 98, 119, 141, 152, 154, 157, 283, 290 Hobbs, G., 13, 83 Hodder, V. M., 269, 283 Hodgkiss, W., 11, 12, 13, 18, 70, 71, 83 Hock, P. P. C., 127, 283 Hoenigmann, J., 203, 283 Hofer, B., 2, 10, 42, 71 Hoffman, G. L., 3, 21, 71, 79 Hoffman, H., 194, 281 Hcljgaard, M., 56, 71 Hollande, A. C . , 17, 74 Hollis, E., 9, 85 Honey, K. A., 53, 84 Honigberg, B. M., 16, 71 Hovasse, R., 57, 67 Hoyle, W. E., 115, 116, 125, 127, 132, 141, 143, 145, 147, 150, 152, 155, 164, 166, 167, 169, 174, 180, 182, 184, 194, 197, 206, 208, 215, 217, 219, 227, 228, 234, 238, 274, 283, 284

305

AUTHOR INDEX

Huizinga, H. W., 32, 72 Hutner, S. H., 13, 77 Hutton, F. W., 140, 284 Hyning, van, J. M., 147, 284

227, 232, 233, 234, 236, 238, 280, 285, 286

K I Ikeda, S., 98, 289 Inghilleri, F., 10, 72 Inoue, Y., 270, 284 Isayev, F. A., 54, 85 Iselin, R. A., 238, 278 Ishikawa, C., 147, 149, 284 Ishikawa, M., 284 Issel, R., 105, 125, 127, 141, 159, 160, 161, 164, 169, 174, 176, 178, 184, 187, 205, 210, 219, 222, 223, 227, 238, 240, 284, 285 Iszuka, 136, 282 Iversen, R. T. S., 264, 285 Iwai, E., 98, 237, 238, 285 Iwanami, S., 60, 81

J Jacobs, L., 59, 72 Jaeckel, S. G. A., 113, 127, 141, 145, 285 Jahn, T. L., 56, 72 Janiszewska, J., 30, 72 Jatta G., 123, 125, 127, 148, 150, 159, 161, 164, 169, 182, 187, 194, 205, 285 Jaxtheimer, R., 54, 80 Jeffreys, J. G., 234, 285 Jensen, A , , 7 , 68 Jensen, M. H., 8, 72 Jepps, M. W., 265, 285 Johnson, C. W., 164, 199, 203, 285 Johnson, T. W., 3, 13, 72 Johnston, T. H., 19, 72 Johnstone, J., 7, 12, 14, 21, 28, 36, 72 Joseph H., 5 , 72 Joubin, L., 98, 105, 111, 119, 123, 125, 127, 131, 132, 141, 143, 148, 149, 150, 152, 154, 157, 161, 162, 164, 166, 167, 169, 176, 178, 180, 182, 184, 187, 189, 190, 194, 199, 200, 202, 203, 204, 205, 206, 208, 210, 213, 214, 215, 216, 222, 223, 224,

Kaas, P., 105, 127, 129, 286 Kabata, Z., 17, 21, 24, 33, 35, 48, 49, 72, 73 Kahl, W., 28, 30, 31, 73 Kajirmura, H., 157, 159, 280 Kass, P., 286 Katoh, G., 132, 137, 139, 257, 286 Keil, A., 98, 286 Kelsey, F. W., 117, 287 Kent, W. S., 98, 287 Kenyon, K. W., 139, 186, 300 Kerr, J. G., 243, 287 Kesteven, G. L., 3, 8, 57, 60, 77 King, J. E., 147, 287 King, J. W., 52, 69 Kirk, T. W., 98, 287 Kishner, D. S . , 12, 75 Kjennerud, J., 98, 101, 104, 287 Klontz, G. W., 8, 53, 78, 81, 89 Knipowitsch, N., 127, 287 Knudsen, J., 98, 101, 104, 287 Kocylowski, B., 10, 52, 73, 85 Kohler, A. C . , 43, 73 Kojima, A., 132, 139, 287 Kolombatovitsch G., 123, 126, 127, 287 Kondakov, N. N., 127, 217, 287 Korabelnikov, L. V., 98, 127, 131, 143, 287 Kotin, P., 37, 81 Krantz, G. E., 53, 60, 70, 73 Krasilnikov, N. A., 13, 73 Krohn, A., 187, 287 Kudo, R. R., 3, 18, 21, 23,24, 37, 71, 73 Kuhn, L. R., 56, 72 Kuipers, F. C . , 31, 59, 73, 74, 86

L Lafont, A., 127, 131, 287 Laigret, J., 59, 80 Laird, M., 16, 18, 56, 58, 74 Lamarque, P., 272, 287 Lameere, A., 127, 287 Lamont, J. M., 127, 272, 293

306

AUTHOR INDEX

Landt, J. B., 127, 287 Lane, F. W., 287 Langford, G. C . , 60, 74 Lankester, E. R., 288 Laqueur, G. L., 59, 81 Laveran, A., 16, 74 Laveran, P. A., 18, 74 Leach, W. E., 180, 216, 288 Lebailly, C., 18, 74 Lederer, G., 14, 74 Legendre R., 113, 125, 126, 127, 131, 141, 143, 145, 169, 187, 189, 194, 197, 204, 205, 219, 221, 229, 231, 232, 236, 276 LBger, L., 17, 74 Leim, A. H., 18, 75 Lesson, R-P., 113, 115, 288 Lesueur, C. A., 104, 119, 150, 224, 236,

288 Letaconnoux, R., 16, 38, 74 Levine, N. D., 71 Liaiman, E. M., 2, 51, 74 Lichtenstein, K. M. H., 152, 288 Linton, E., 19, 27, 28, 29, 32, 74, 75 Liston, J., 13, 68, 83 Ljungberg, O., 10, 11, 75 Loeblich, A. R., 7 1 Lonnberg, E., 105, 127, 141, 147, 149, 154, 157, 158, 164, 209, 219, 221, 223, 288 LsvBs-Svendsen, B., 270, 288 LovBn, S., 127, 141, 288 Lowe, J., 5 , 75 Lozano, Y Rey, 125, 127, 148, 194, 204, 288 Lucas, C . E., 63, 75 Lucas, F. H., 106, 157, 288 LuckB, B., 36, 37, 75, 82

Liihmann, M., 7, 75 Liiling, K. H., 33, 35, 75 Lutta, L. S., 27, 51, 69

M McCoy, F., 140, 288 McDaniel, E. C . , 53, 65 McDermott, W., 52, 75 Macdonald, R., 288 McGonigle, R. H., 18, 75

McGregor, E. A., 3, 75 Machinaka, S., 132, 288 McIntosh, W. C . , 5, 75, 288 Mackintosh, N. A., 105, 127, 289 McLeod, J. A., 3, 29, 87 McMillen, S., 12, 75 Magaz, J., 127, 289 Magill, A. R., 147, 284 Mangold-Wirz, K., 123, 124, 125, 126, 127, 129, 130, 131, 257, 258, 289 Maniwa, Y., 264, 282 Mann, H., 7, 29, 33, 34, 38, 46, 47, 54, 75 Manker, H. W., 3, 26, 75 Maplestone, P. A., 3, 89 Marek, K., 52, 85 Margolis, L., 18, 35, 48, 75, 76 Markowski, S., 30, 32, 76 Marsh, M. C., 36, 70 Martens, E. von, 116, 289 Martin, O., 30, 76 Martin, W. R., 29, 83 Massy, A. L., 106, 111, 115, 125, 127, 141, 170, 208, 232,

143, 171, 212, 234,

145, 154, 164, 165, 167, 180, 187, 189, 194, 202, 215, 222, 227, 229, 231, 237, 289 Matsumoto, K., 18, 66, 76 Matsuno, M., 60, 65 Matsuno, S., 186, 289 Mattheis, T., 10, 43, 76 Maul, G.E., 98, 104, 105, 106, 113,127, 129, 131, 141, 145, 152, 159, 161, 176, 178, 180, 182, 190, 194, 197, 200, 209, 213, 216, 217, 223, 236, 265, 277, 293 Meek, A., 105, 289 Meglitsch, P. A., 19, 76 Merrett, N., 213, 289 Merriman, D., 24, 29, 77

Mesnil, F., 74 Meyer, W. Th., 289 Middendorf, A. T . , 143, 154, 289 Minelli, J. de, 205, 289 Minoru, A., 270, 297 Mitsukuri, K., 98, 289 Moewus, L., 4, 8, 52, 68, 76, 83 Moewus-Kobb, L., 8 , 76 Molina, G. I., 290 Maller, H. P. C., 152, 290

307

AUTHOR INDEX

Morales, E., 123, 125, 127, 129, 148, 149, 194, 199, 200, 204, 205, 290 Morch, 0. A. L., 127, 129, 131, 162, 154, 234, 290 More, A. cf., 290 Mortara, S., 238, 290 Motohiro, T., 270, 297 Mourgue, M., 127, 290 Mulsow, K., 14, 45, 79 Murray, E. G. D., 3, 13, 67 Murray, J., 98, 141, 152, 154, 157, 290 Muus, B. J., 98, 152,154,155,225,229, 231, 234, 290

N Naef, A., 125, 127, 129, 141, 144, 145, 148, 149, 156, 159, 160, 164, 169, 170, 174, 178, 182, 184, 187, 194, 196, 199, 204, 221, 243, 290 Nagata, S., 132, 133, 290 Nemoto, T., 139, 147, 148, 154, 167, 159, 186, 236, 238, 290, 291 Nesis, K. H., 131, 290 Nesis, K. N., 162, 154, 155, 157, 234, 236, 264, 269, 290 Neumann, R. 0..16, 76 Nichols, A. R., 105, 125, 291 Nicoll, W. R., 26, 32, 76 Nielsen, E., 127, 234, 236, 291 Nielsen, E. S., 63, 76 Nigrelli R. F., 3, 5, 8, 12, 13, 16, 23, 32, 34, 37, 54, 56, 57, 68, 76, 77, 84, 85, 86, 88 Ninni, A. P., 127, 291 Nishikawa, T., 132, 291 Nishimura, S., 161, 264, 291 Nishizawa, S., 291 Nobre, A., 125, 291 Nordenberg, C., 7, 77 Nordghd, O., 98, 101, 127, 291 Norman, A. M., 123, 141, 291 Nostrand, T., 23, 81 Nunes-Ruivo, L., 35, 77 Nybelin, O., 11, 29, 62, 77

Okada, Y.K., 113, 118, 143, 186, 291 Okiyama, M., 136, 139, 291 Okutani, T., 111, 116, 132, 147, 148, 154, 167, 168, 169, 236, 238, 291 Oldham, F. K., 147, 293 Olsen, Y. H., 24, 29, 77 Oppenheimer, C. H., 3, 27, 52, 56, 57, 60, 77, 78 Ordal, E. J., 12, 13, 16, 69, 81, 88 Orlandini, C., 26, 78 Ortmann, A. E., 292 Osmanov, S. O., 27, 78 Ostroumoff, A., 127, 292 Otterlind, G., 270, 272, 292 Owen, R.,216, 292

P

Pwcaud, A., 66, 78 Pacheco, G., 8, 78, 86, Packard, A. S., 98, 292 Panina, G. K., 169, 292 Papermaster, 33. W., 64,78 Parisot, T. J., 8, 12, 78, 89 Patmhnik, M., 18, 19, 78 Pavlovskii, E. N., 2, 78 Pawsey, E. L., 127, 292 Pearcy, W. G., 143, 147, 154, 156, 158, 159,189,199,204,217,236,238,292 Pelnar, J., 8, 78, 81 PBrard, C., 18, 78 Pelseneer, P., 127, 265, 292 Perkins, P. J., 264, 285 Petrushevskii, G. K., 2, 3, 17, 22, 23, 26, 27, 30, 31, 49, 67, 69, 78 Pfeffer, G., 94, 106, 116, 116, 117, 118, 119, 123. 125, 126, 127, 141, 143, 144, 145, 147, 148, 149, 160, 162, 154, 158, 169, 161, 164. 165. 167, 169, 170, 171, 174, 176, 180, 182, 184, 185, 187, 189, 191, 194, 196, 198, 199, 202, 204, 205, 210, 212, 214, 216, 216, 217, 219, 221, 222, 223, 224, 228, 229, 231, 232, 234, 237, 292 Phillips, J. B., 117, 147, 148, 270, 277, 292 0 Pike, G. C., 147, 148, 154, 157, 292 Odhner, N. H., 116, 141, 161, 167, 291 Pilcher, K. S., 53, 85 Pinto, J. S., 16, 45, 78 Ojala, O., 11, 77

308

AUTHOR INDEX

Piotrowska, W., 52, 85 Plehn, M., 2, 14, 45, 79 Pliszka, F. V., 53, 78 Polyanski, Y. I., 2, 3, 17, 22, 23, 24, 27, 31, 48, 49, 51, 69, 79 Porter, A., 21, 69 Posselt, H. J., 98, 119, 127, 141, 152, 234, 292 Post, G., 3, 53, 79 Poulsen, E., 35, 79 Powell, A. W. B., 140, 292 Prhfontaine, G., 119, 292 PrBvot, A. R., 13, 79 Price, J. E. L., 60, 79 Prosch, V., 152, 229, 234, 292 Punt, A., 31, 33, 79, 82 Putz, R. E., 3, 79 Pyle, E., 8, 88

Q Quigley, J. J., 272, 293 Quirnby, M. C., 4, 88 Quir6s, J., 127, 293 Quoy, J. R. C., 115, 171, 293

R Raabe, H., 58, 79 Rae, B., 28, 80 Rae, B. B., 125, 126,127,187,272,293, 296 Rancurel, P. 118, 187, 189, 238, 293 Raney, E. C., 38, 45, 80 Rdfn, K., 5 , 80 Rathke, H., 224, 293 Reddecliff, J. M., 53, 73 Rees, E. I. S., 152, 293 Rees, W. J., 98, 104,105, 106, 113, 123, 125, 127, 129, 131, 141, 143, 145, 152, 159, 161, 176, 178, 180, 182, 190, 194, 197, 209, 213, 216, 217, 223, 236, 293 Rehder, H. A., 117, 293 Reichenbach-Klinke, H. H., 2, 12, 14, 15, 16, 37, 80 Reshetnikova, A. V., 51, 80 Rice, D. A., 143, 145, 154, 157, 159, 293

Richard, J., 224, 293 Richardson, L. R., 21, 69 Riddell, W., 57, 80 Risso, A., 127, 148, 149, 194, 203, 293 Ritchie, J., 101, 127, 129, 293 Robbins, L. L., 147, 293 Robertson, A., 17, 86 Robson, C. W., 293 Robson, G. C., 98, 101, 104, 105, 106, 116, 125, 126, 147, 152, 167, 174, 176, 178, 180, 190, 194, 210, 212, 215, 216, 219, 222, 223, 232, 238, 277,294 Rochebrune, A. T. de, 223, 233, 294 Rodriquez, O., 294 Roegner-Aust, S., 7, 54, 80 Roffo, A., 36, 80 Roper, C. F. E., 178, 179, 180, 294 Roper, F. C. S., 127, 294 Rose, J., 141, 294 Rosen, L., 59, 80, 81 Rosenfield, A., 9, 26, 57, 64 Roskam, R. T., 31, 59, 74, Sl, 86 Ross, A. J., 8, 53, 81 Roth, H., 25, 68 Roughley, T. C., 19, 81 Roule, L., 154, 157, 286 Rowan, M. K., 19, 81 Rucker, R. R., 8, 11, 13, 14, 71,81,87 Ruivo, M., 16, 65 Ruppell, E., 173, 174, 182, 187, 294 Russell, E. S., 154, 164, 199, 229, 234, 237, 294 Russell, F. E., 37, 81 Russell, F. S., 59, 81 Rustad, D., 127, 129, 294 Ruszkowski, J. S., 28, 81 Ruud, J. T., 152, 157, 283

S S a c a r r k , G. F., 194, 295 Sakazaki, R., 60, 81 Sandeman, G., 5 , 81 Sandholzer, L. A., 23, 81 Sanzo, L., 159, 160, 161, 295 Sars, G. O., 127, 141, 143, 154, 157,295 Sasaki, M., 98, 106, 113, 115, 116, 117, 118, 132, 133, 134, 135, 137, 139,

309

AUTHOR INDEX

141, 143, 145, 147, 148, 154, 156, 157, 158, 159, 161, 170, 171, 173, 179, 184, 186, 189, 198, 200, 202, 206, 209, 210, 212, 217, 221, 222, 223, 230, 231, 236, 238, 295 Saunders, D. C., 18, 81 Scattergood, L. W., 14, 41, 43, 82, 84 Schafer, W., 182, 256, 295 Schaperclaus, W., 2, 7, 10, 11, 14, 52, 54, 82 Schleich, F., 7, 80 Schlumberger, H. G., 36, 37, 75, 82 Schmey, M., 36, 82 Schmidt, J., 295 Schneider, C. O., 116, 117, 295 Scholes, R. B., 13, 82 Schrader, F., 21, 82 Schubert, K., 154, 158, 295 Schuurmans-Stekhoven, J. H., 33, 82 Scott, A., 33, 125, 72, 82, 295 Scott, D. M., 29, 30, 82, 83 Segerstrale, G. G., 127, 131, 295 Shaw, T. I., 262, 279 Sheard, K., 60, 83 Sherman, K., 33, 83 Shewan, J. M., 11, 12, 13, 18, 70, 71, 82, 83 Shimizu, T., 132, 134, 135, 282, 295 Shimomura, T., 179, 186, 255, 295 Shulman, S. S., 17, 21, 30, 32, 33, 49, 51, 78, 79, 83 Shulman-Albova, R. E., 17, 33, 49, 83 Sigel, M. M., 4, 8, 52, 68, 83 Sikama, Y., 58, 83 Sindermann, C. J., 3, 8, 9, 14, 15, 17, 19, 21, 26, 34, 41, 42, 43, 44, 49, 52, 53, 57, 71, 83, 84 Sivertsen, E., 295 Skrjabin, K. I., 3, 84 Smith, A. G., 147, 148, 295 Smith, E. A., 145, 295 Smith, G. M, 5, 7, 11, 36, 37, 57, 77, 84, 88 Smith, I. W., 84 Smith, N. R., 3, 13, 67 Smith, W., 52, 84 Smith, W. C., 72 Sneath, P. H. A., 60, 84 Snieszko, S. F., 3, 4, 8, 9, 52, 54, 84, 85 Soot-Ryen, T., 154, 295

Sorvachev, K. F., 54, 85 Souleyet, 296 Sparck, R., 125, 296 Sparrow, F. K., 3, 13, 72 Sparta, A., 127, 169, 182, 296 Spence, K. D., 63, 85 Spencer, R., 63, 85 Sprague, V., 14, 85 Sprehn, C., 29, 85 Sproston, N. G., 3, 14, 15, 85 Squires, H. J., 29, 30, 33, 47, 119, 120, 121, 122, 265, 270, 86, 296 Steenstrup, J., 98, 104, 105, 111, 116, 117, 127, 131, 132, 152, 154, 156, 158, 162, 164, 193, 215, 219, 223, 224, 234, 237, 264, 296 Steinhaus, O., 116, 296 Stendall, J. A. S., 105, 296 Stephen, A. C., 98, 105, 125, 127, 129, 164, 237, 255, 293, 296 Stevenson, J. A., 105, 125, 127, 131, 278, 296 Stonehouse, B., 117, 118, 296 Storrow, B., 127, 296 Stossich, M., 127, 296 Stram, H., 85 Stunkard, H. W., 25, 85 Suno, M., 270, 297 Suter, H., 140, 143, 296 Sutherland, P. L., 12, 85 S u z u k i , T., 132, 133, 134, 296 Sykes, W. H., 296

T Takahashi, K., 36, 85 Takahashi, T., 270, 297 T a d w w a , E., 270, 284, 297 Targioni-Tozzetti, A., 127, 148, 203, 297 Tauti, M., 297 Taylor, C. C., 61, 85 Templeman, W. F., 22, 29, 30, 33, 37, 47, 86 Tesch., J. J., 127, 297 ThBodoridBs, J., 16, 65 Thiel, P. H. Van, 31, 59, 74, 86 Thiele, J., 150, 162, 164, 166, 167, 169, 176, 180, 194, 216, 222, 224, 228, 297

310

AUTHOR INDEX

Thomas, L., 7, 8, 36, 86 Thompson, D'A. W., 147, 148, 297 Thompson, H., 119, 120 121, 122, 152, 280 Thompson, W. F., 18, 86 Thomson, J. G., 17, 86 Thore, S., 126, 297 Tibbo, S. N., 43, 86 Tinbergen, L., 258, 297 Tinbergen, N., 127, 258, 297 Torchio, M., 199, 297 Torres, C. M., 8, 86 Toth, L., 52, 86 Tripathi, Y . R., 16, 86 Troschel, E., 148, 159, 184, 297 Tryon, G. W., 216, 297 Tyzzer, E., 19, 86

U Utsuno, Sh., 106, 297

v VBlain, C., 98, 297 VBrany, J. B., 123, 126, 127, 131, 148, 169, 174, 176, 178, 184, 187, 194, 203, 214, 215, 222, 297, 298

Verco, J. C . . 298 Verrill, A. E., 98, 100, 101, 104, 109, 119, 122, 147, 148, 150, 152, 157, 164, 165, 167, 169, 184, 189, 194, 197, 199, 202, 203, 206, 236, 298,

299 Verwey, J., 258, 297 Vigelius, W. J., 159, 299 Vishniac, H. S., 16, 86 Vives, F., 294 Vladykov, V. D., 122, 299 Vogel, H., 12, 57, 77, 86 Volodin, V. M., 38, 86 Voss, G. L., 98, 104, 106, 108, 115, 116, 117, 141, 161, 174,

118, 143, 166, 176,

119, 145, 167, 178,

126, 149, 169, 180,

132, 150, 170, 182,

139, 158, 171, 184,

140, 169, 173, 189,

190, 202, 219, 221, 233, 300

191, 203, 221, 222, 234,

193, 206, 222, 223, 236,

197, 214, 223, 224, 237,

198, 215, 224, 227, 238,

199, 216, 227, 228,

200, 217, 219, 231,

292, 299,

Voss,N.A., 193,197,198,199,200,300

w Wakiya, Y., 147, 284 Walford, L. A., 12, 33, 86 Walker, R., 6 , 86 Wallace, G. D., 59, 81 Wardle, R . A., 3, 28, 29, 87 WatasB, S., 186, 300 Watson, S. W., 8, 71, 87 Weindl, T., 115, 173, 300 Weinstein, P. P., 59, 81 Weiser, J., 71 Weiss, F. E., 159, 164, 187, 194, 300 Weissenberg, R., 5, 21, 23, 87, 88 Wellings, S . R., 7, 88 Wellmann, G., 60, 88 Wells, N. A., 11, 57, 88, 89 Wenrich, D. H., 7 1 White, 35 Wilhelm, 0. G., 116, 117, 300 Wilke, F., 139, 186, 300 Williams, G., 36, 88 Williams, H. H., 29, 46, 69, 88 Williams, L. W., 119, 300 Williamson, S. I., 106, 180, 276 Willis, A. G., 19, 88 Wilson, C. B., 35, 88 Wilson, E., 296 Wilson, F., 125, 127, 293 Wise, J. P., 33, 83 Wolf, K., 4, 6, 7, 8, 86, 88 Wolf, K. E., 3, 54, 85 Wolf, L. E., 54, 88 Wolfgang, R. W., 26, 88 Wood, J. W., 12, 81, 88 Woodcock, H. M., 5 , 89 Woodland, W. N. F., 29, 89 Woodward, B. B., 300 Wiilker, G., 115, 300 Wurmbach, H., 32, 89

311

AUTHOR INDEX

Y Yamaguti, S., 3, 24, 30, 89 Yasutake, W . T., 8, 78, 89 Y a t e s , L. G., 117, 300 Yorlie, W., 3, 89 Young, L., 23, 81 Young, P. H . , 37, 89

Young, R. E., 190, 300 Young, R. T., 28, 89

Z Zadvorochnov, S . F . , 54, 85 Zobell, C . E . , 11, 67, 88

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Species index A Abralia, sp., 118, 150, 170 Abralia afinis, 174 Abralia andamanica, 170, 172, 244, 247 Abralia armata, 170,171, 172, 173, 247 Abralia astrolineata, 170, 171, 172, 247 Abralia astrosticta, 170, 171, 172, 247 Abralh gilchristi, 174, 178 Abralia grimpei, 171, 172, 247 Abralia Hoylei, 176 Abralia japonica, 170, 171, 172, 247 Abralialucens, 170,171, 172,247 Abralia megalops, 184 Abralia Morrisii, 176 Abralia multihamata, 170, 172, 173, 247 Abralia Nishikawa, 186 Abralia oweni, 173 AbraEia Pfefferi, 178 Abralia polyonyx, 184 Abralia redjieldi, 170, 172, 173, 247 Abralia renschi, 170, 172, 173, 247 Abralia sparcki, 170, 172, 173, 247 Abraliasteindachneri, 170,173,247,267 Abralia stenabralia astrosticta, 170 Abralia trigonura, 170, 172, 173, 247 Abraliaveranyi, 170, 172, 173, 244, 247, 252, 267, 268 Abraliopsis, sp., 174, 244, 260, 261 Abraliopsis aflkis, 174, 175, 247 Abraliopsis gilchristi, 174, 175, 247 Abraliopsis Hoylei, 174, 175, 176, 247 Abraliopsis joubini, 186 Abraliopsis lineata, 175, 176, 248 Abraliopsis morrisi, 173, 175, 176, 244, 248, 267, 268 Abraliopsis neozealundica, 178, 248 Abraliopsis pfefferi, 178, 248 Abraliopsis scintillana, 186 Abramia ballerw, 40 Achromobacter punctatum, 54 Acipenser nudiventvis, 27 See also Sturgeon Aeromonas hydrophila, 53 Aeromonas sutmonicida, 63 A.M.B.-4

Alaska pollock, see Mintai Albatross, 145, 158, 266 Albatrossia pectoralis, 266 A1ePisaum 131, 145, 178, 18% 200, 209, 215, 236, 268 169 43 Alluroteuthis antarcticus, 162, 247 Alosa aestivalis, 19 Alosa pseudohurengw, 16 See also Alewife Ahtera5choePfi, 5 Amyloodinium ocellatum, 57, 65 Amwhichas lupua, 46 Anchovy, 117, 139 Anciat?mheirus Lesueuri, 184, 248, 266 Ancistrocheirua megaptera, 189 Ancistroteuthis lichtenateinei, 144, 148, 246, 259, 261, 267 Ancistroteuthis robuata, 147 AngiostrongYlm antonenaia, 69 Angler-fish, 23 Anguilla anguilla, 7, 9 See Eel Aniaakis, sp., 265 AnOrnabcranchia imPenni% 232, 251 A r m i ~minutus, 266 Anoiis tenuirostris, 118, 266 Aphunopua carbo, 113, 179, 213, 267 Architeuthk, sp., 98, 246, 266 Asocranchk joubini, 215, 224, 250 AsteroteuthW, sP~,170 Asteroteuthk veranyi, 173 Asthenoteuthion planctonicum, 191 Atherina r%ueti, 16 Arctic char, 18 Atherinops afinis, 11 See ah0 Smelt

0 Barracouta, 18, 19 Bass, sea, 12 Bass, striped, 5, 9, 38, 39, 45 Bathothauma lyromma, 227, 250 313

Y

314

SPECIES INDEX

Bathyteuthk abyssicola, 166, 244, 247, 252 Benedenia melleni, 56 Benthoteuthia magalops, 166, 182 Berryteuthis magister, 158 Bigelowia atlanticus, 249 Blenny, 11 Bolbosoma vasculoaum, 32 Brachioteuthis beani, 163, 164, 247 Brachioteuthis bowmani, 163, 164,247 Brachwteuthis picta, 163, 164, 244, 247 Brachioteuthis riisei, 162, 244, 247, 259, 261 Brachyphallua crenatus, 50 Bream, 40 Brevoortia tyrannus, 17, 19 Brisaster towsendi, 148 Butterfish, 27

Char, Artic. 18 Charybditeuthis maculosa, 182 Chauliodus, 169, 268 Chaunoteuthis mollis, 149, 246 Cheiroteuthis A.,210 Chiropsie mega, 206, 249 Chiroteuthis atlanticus, 202 Chiroteuthis Bonplandi, 202 Chiroteuthk borealis, 210, 212 Chiroteuthia famelica, 201, 202, 249 Chiroteuthis grimaldii, 201, 202, 208, 249 Chiroteuthk imperator. 202, 210, 249 Chiroteuthk lacertosa, 201, 202,249 Chiroteuthk macrosoma, 203, 249 Chiroteuthis picteti, 201, 203, 249 Chiroteuthis planctonica, 2 10 Chiroteuthis portieri, 201, 203, 249 Chiroteuthis ueranyi, 201, 203, 204, 249, 259, 261, 262, 266, 267 Chiroteuthis Veranyi lacertosa, 202 C Chiroteuthoides hastzu'u, 210, 212 Calanus jhmarchicus, 157 Chiroteuthopsia Qrimaldii, 208 Calanus hyperboreus, 157 Ghiroteuthopsis Talismani, 2 10 Caligus pageti, 59 Chloromyxum clupeidae, 19 Calliteuthis, sp., 197, 264 Chloromyxum histolyticum, 18 Calliteuthis Alessandrinii, 184 Chloromyxum musculoliquefaciena, 18 Calliteuthis arcturi, 197, 248 Chloromyxum thyrsites, 18 Calliteuthis celetaria, 197, 248, 249 Chlorophthalmua agaasizi, 174, 268 Calliteuthis cookiana, 197, 249, 266, 268 Chondrococcus columnaris, 13 Calliteuthis corona, 197, 198, 249 Chromodina coronata, 265 Calliteuthis dojleini, 197, 198, 249, 266 Chromodina elegans, 265 Calliteuthis elongata, 197, 198, 249 Cirrobrachium danae, 166,247 Calliteuthis meleagroteuthis, 197, 199, Cirrobrachium filiferum, 166, 247 200, 249 Cladosporium, sp., 15 Calliteuthis meneghinii, 199 Clam, 59 Calliteuthis miranda, 197, 199, 249 Clonorchis sinensis, 59 Calliteuthis newoptera, 169 Clupea harengus, 9, 14, 17, 19, 25, 27, Calliteuthis ocellata, 198 29 Calliteuthis reversa, 196, 197, 198, 199, See also Herring 249, 259, 261, 268 Clupea p a l h i , 11, 12 Calliteuthis separata, 197, 200,249, 266 See also Herring Callorhinus ursinua, 267 CZupea sprattus, 17 Camellanus melanocephalus, 32 See also Sprat Capelin, 22, 122 Coalfish, 157 Carp, 54 Cod, 7, 11, 12, 13, 15, 17, 23, 24, 29, 30, Carynoteuthis oceanica, 233 31, 33, 36, 37, 43, 51, 52, 57, 122, Catfish, 37, 46 157, 369 Centropristes striatus, 12 Cod, Pacific, 30 Ceratomyxa arcuata, 48 Cod, rock, 58

315

SPECIES INDEX

Coelorhynchus australis, 18 Coloconger raniceps, 268 Compsoteuthis, 171, 178 Compsoteuthis Nishzkawa, 186 Contracaecum aditncum, 30 Corynomma specdater, 227, 257 Corynosonta semerme, 32 Corynosoma strumosum, 32 Coryphaena hippurus, 139, 268 Cotoconger raniceps, 178 Cranchia Bonnelliana, 194 Cranchia Brockii, 2 19 Cranchia cardioptera, 150 Cranchia globula, 219 Cranchia hispida, 215 Cranchia megalops, 234 Cranchia Reinhardti, 2 19 Cranchia scabra, 215,218,244,250,268 Cranchia tenuitentaculata, 2 15 Cranchiidarum, 227, 230 Croaker, 12, 32, 36, 37 Cryptocaryon irritans, 58, 65 Cryptocotyle lingua, 25, 52 Crystalloteuthis beringiana, 217,250,252 Crystalloteuthis glacialis, 217, 250, 25 2 Ctenopteryx, 169 Ctenopteryx cyprinoides, 169 Ctenopteryx Jimbriatus, 169 Ctenopteryx siculus, 169, 259, 261, 267 Ctenopteryx siculus chuni, 169, 268 Cucioteuthis unguiculatus, 190 Cucullanellus minutw, 30 Cucullanus truttae, 48 Cycloptericola marina, 16 Cyclopterus lumpua, 16, 33 Cycloteuthis sirventi, 161, 247 Cynoscion arenarus, 32 Cynoscion nebulosus, 28 See also Seatrout Cyprinids, 7, 8 Cystophora cristata, 157, 260

D Dab, 24 Delphinapterus leucas, 122, 266 Desmoteuthis abyssicola, 230 Desmoteuthis hyperborea, 234, 236 Desmoteuthis maxima, 231 Desmoteuthis megalops, 231, 234 Desmoteuthis tenera, 234

Dinobothrium planum, 265 Dinobothrium plicatum, 265 Diomedia fuliginosa, 236 Dioinedia immutubilis, 260 Diphyllobothrium latum, 59 Diplogonoporus grandis, 00 Dolphin, 131, 149, 152, 169, 178, 182, 191, 205, 267 Doratopsis A., 210 Doratopsis exophthalmica, 2 10, 212 Doratopsis lippula, 210, 212 Doratopsis sagitta, 210, 212 Doratopais vemniculari~,203 Dosidicua Eschrichtii, 116 Dosidicus gigas, 114, 116, 244, 246, 252, 265, 266, 270 Dosidicus Steenstrupii, 116 Drechselia danae, 224, 250 Drepanopsetta hippoglossaidea, 24 Drum, 27, 36 Dyphyllobothrium latum, 60

E Echeneis naucrates, 36 Echinorhynchus gadi, 32 Echinoteuthis danae, 249 Eel, 6, 7, 9, 17, 26,32, 42,43, 45, 54, 61, 64 Eel pout, 30 Echinoteuthis danae, 205 Egia inermis, 225, 250 Eimeria anguillae, 17 Eimeria breuoortiana, 17 Eimeria clupearum, 17, 48, 49 Eimeria gadi, 17 Eimeria nishin, 17 Eimeria sardinae. 16, 17, 45, 48, 49 Elytrophora brachyptera, 35 Engraulis japonica, 139 Enoploion euaticum, 187,248 Enoploteuthis, sp., 179, 248 Enoploteuthis anapsis, 179, 248, 267 Enoploteuthis chuni, 179, 248, 268 Enoploteuthis diadema, 191 Enoploteuthis dubia, 179, 248 Enoploteuthis galaxias, 179, 248 Enoploteuthis Hoylei, 176 Enoploteuthis leptura, 180, 248, 267 N2

316

SPECIES INDEX

Enoploteuthia Leaueurii, 184 Enoploteuthia margaritijera, 182 Enoploteuthis Molinae, 190 Enoploteuthia Morisii,176 Enoploteuthis neozealandica, 178 Enoploteuthia owenii, 174 Enoploteuthia pallida, 184 Enoploteuthia polyonyx, 184 Enoploteuthis veranyi, 173 Enoptroteuthis spinicauda, 215 Entomopsis alicei, 162, 205, 249, 267 Entomopsis clovei, 162, 205 Entomopsis Velaini, 162, 205, 249 Epinephelu merra, 68 Erysipelothrix insidiosa, 60 Escherichia coli, 60 Esox lucius, 40 See also Pike Etmopterus hillianus, 174, 267 Eucleoteuthis luminosa, 113 Euatoma rotundatum, 30, 31, 47, 50, 59 Euzygaena pacijca, 222

F Flathead sole, 7 Flounder, 5, 6, 7, 26, 29, 30, 33, 36, 37, 47 See also Winter Flounder Fregata aquila, 113, 266 Flying fish, 35 F u l m a m glacialis, 157, 266 Fundulua heteroclitus, 5, 13 See alao Killijsh Fundulus parvipinnis, 11 Fusocranchia alpha 232, 251

ti Gadoids, 32, 33, 35, 38, 47, 64 Qadus aeglefinus, 21, 29, 157, 268 See also Haddock Cadus macrocephalus, 30 Gadus merlangua, 33 See also Whiting Ck~lusmorhua, 7, 11, 12, 13, 15, 19, 20, 29, 57, 113, 131, 145, 157, 268 See also Cod Gadua virem, 167, 268

GaliteuthG annata, 228, 237, 238, 239, 240, 251, 259, 261, 266, 267 Qaliteuthis phyllura, 238 Qaliteuthia auhmi, 229, 238 Gasteroatew aculeatus, 23, 27 Genyonemw lineatus, 37 Genypterua blcrcodea, 268 Germo alalunga, 113,126,131, 145, 169, 189, 205, 221, 229, 238, 267 Qermo obeaus, 113, 131, 213 Gillichthys mirabilis, 11 Globicella melaena, 267 Globoicephalua melua, 236 Glugea anomala, 23 Glugea hertwigi, 21, 22 Glugea punctijera, 23 Glugea atephani, 46 Blyptocephalus cynoglossua, 29 Gnathostoma apinigerum, 69 Gobies, 11 Gonatopsis borealia, 153, 159, 266 Gonatopsis octopedatua, 159 Gonatus, 152 Gonatus anonychua, 153, 158 Qonatw antarcticw, 162, 157, 246, 247, 252, 266 Qonatus borealis, 247 Gonatusjabricii, 162. 167, 158, 244,246, 252, 267, 259, 261, 264, 266, 266, 267, 268, 369 Gonatua magister, 153, 158, 247, 266 Qonatus octopedatua, 153, 247 Gonatua septemdentatua, 158 Goosefish, 23 Grampw griaeus, 213, 266 Grillotia erinaceua, 28 Grimalditeuthis bonplandi, 214, 215, 260, 268 Grimalditeuthia Richardi, 214 Grunt, 8 Gull, 26, 266 Gyrodactylus arcuatus, 27 Gyrodactylus bychowskyi, 27

H Haddock, 21, 29, 31, 33, 34, 36, 37, 38, 39,47 Haemogregarina bigemina, 18 Haemulon album, 63

317

SPEOIES INDEX

Haemulon aciurua, 8 Hake, 21, 28 Halibut, 7, 12, 18, 26, 28, 29 Helicocranchia beebei, 232, 251 Helicocranchia fisheri, 231 Helicocranchia pfefferi, 231, 251, 267 Hemitripterm americanus, 26, 30 Henneguya salminicola, 19 Hensenioteuthia joubini, 232, 251 Hensenioteuthis melancholicus, 227 Heptanchua, 126, 268 Herring, 9, 14, 17, 19, 20, 25, 28, 29, 31, 38, 41, 42, 43, 44, 45, 47,48,49, 50, 51, 52, 55, 57, 59, 61, 64, 122, 129, 369 Herring, blueback, 19 Herring, Pacific, 11, 12 Heterophyes heterophyes, 59 Hexacapsula neothunni, 18 Hippocampus erectua, 8 Hippoglossoides elassodon, 7 Hippoglossoidea plateaeoidee, 7, 26, 37 See also Plaice, American Hippogloasua hippoglossus, 7, 12, 26, 28, See also Halibut Hippoglossus stenolepsis, 18 Histiopsis, 197 Histioteuthis atlantica, 194 Histioteuthis bonellii, 194, 195, 196, 197, 244, 248, 255, 259, 261, 266, 267, 268 Hiatioteuthia bonelliana, 194 Histioteuthis Collinsi, 194 Histioteuthis cookiana, 197 Histioteuthia Riippellii, 194 Hyaloteuthis pelagica, 117, 246 Hyaloteuthia p e l q k w , 244, 256, 266 Hyaloteuthis vermicularia, 203 Hyperia galba, 157 Hyperoodon sp., 266 Hyperoodon ampullatus, 157 Hypheaaobrycon, sp., 15 Hypaoblennius gilberti, 11

I Ichthyophonus hoferi, 13, 41, 42, 45, 50, 61, 55 Ichthyophthiriw mzrltifiliia, 58

Ichthyosporidiurn hoferi, 14, 15 Ictalurw nebulosus, 37 See alao Catfiah Idioteuthis latipinna, 209 Illex coindeti, 118, 119, 120, 122, 123, 244, 246, 252, 257, 265, 267 Illex illecebroszts, 119, 133, 244, 246, 252, 257, 265, 267, 268, 269 Iaoachyla parmitica, 16

J Javelinfish, 18 John Dory, 18, 19

K Killifish, 5, 11, 13, 37 Kudoa clupeidae, IS, 20, 48, 50, 51, 52 Kudoa thyrsitm, 18, 19

L hmpadioteuthis megaleia, 190, 248 Lamprey, sea, 53 Larm argentatus, 25 Leachia cyclura, 223, 250 Leachia ellipaoptera. 223 Leachia eschacholtzii, 224, 250 Leachia hyperborea, 234 Leachia Reinhardti, 219 Leiostomw xanthurus, 32 Lepeophtheirua aalmonis, 35 Lepidoteuthia grimaldii, 213, 214, 250, 256, 259, 261, 265, 266, 267, 268 Leptodontoteuthis inermia, 191 Lerwenicua sprattae, 35 Lernaeocera branchialis, 33, 46 Lernaeocera obtusata, 33 Leatoteuthis robusta, 147 Leucosphuera oxneri, 58 Liguriella podophthalma, 227 Limacina retroversa, 157 Ling, 145 Liocranchia Brockii, 219 Liocranchia gardineri, 219, 220, 250 Liocranchia globula, 219, 220 Liocranchia intermedia, 219, 220, 250 Liocranchia rein,hardti, 219, 220, 250, 267 Liocranchia valdiviae, 220, 221, 250 Littorina littorea, 25

318

SPECIES INDEX

Lobster, 44 Loligo Alessandrinii, 184 Loligo brogniartii, 123 Loligo coindetii, 123 Loligo eblanae, 125 Loligo illecebrosus, 119 Loligo leptura, 180 Loligo laticeps, 149 Loligo Leachii, 223 Loligo pavo, 236 Loligo pillae, 123 Loligo plagioptera, 149 Loligo sagittata, 123, 125 Loligo sagittatus, 126 Loligo Smythii, 180 Loligo todarua, 126 Loligo vanicoriensis, 113 Loligopsis bonplandi, 2 14 Loligopsis cyclura, 223 Loligopsis cyclurus, 223 Loligopsis hyperborea, 234 Loligopsis pavo, 233 Loligopsis perlatus, 203 Loligopsis Reinhardti, 2 19 Loligopsis Schneehageni, 223 Loligopsis Veranyi, 203 Loligopsis vermicolaris, 203 Loligopsis zygaena, 222 Lophius piscatorius, 23 Lumpfish, 15, 33 Lycoteuthis diadema, 191, 192, 244, 248, 267 Lycoteuthis Jattae, 191

M Mackerel, 14, 15, 18, 28, 32, 43, 61, 122, 269 Macronectes giganteus, 266 Macrozoarces americanus, 22, 23, 29, 32 Mallotus villosus, 22 Margate, 53 Marlin, 161, 268 Mastigoteuthis, sp., 206, 249 Mastigoteuthis agassizi, 206, 207, 249 Mastigoteuthis cordijormiu, 206, 207, 212, 249 Mastigoteuthis dentata, 207, 208, 249 Mastigoteuthia jlammea, 207, 208, 249 Mastigoteuthis ghucopsk, 207, 208, 249

Mastigoteuthis grimaldii, 207, 208, 249 Mastigoteuthis hjorti, 207, 209, 249 Mastigoteuthis iseleni, 207, 209, 249 Mastigoteuthis latipinna, 207, 209, 249 Mastigoteuthia levimana, 207, 209, 249 Mastigoteuthis magna, 207, 209, 249 Mastigoteuthis schmidti, 207, 209, 249, 268 Mastigoteuthis talismani, 210, 250 Maurolicus muelleri japonicus, 139 Megalochranchia abyssicola, 230, 233, 26 1 Megalochranchia jisheri, 231, 251 Megalocranchia hyperborea, 234 Megalocranchia maxima, 231, 251 Megalocranchia megalops, 234 Megalochranchia papillata, 231, 251 Megalocranchia pardua, 231, 251 Megalocranchia richardsoni, 237 Meganyctiphanes, 122 Meleagroteuthis, 197 Meleagroteuthis Hoylei, 199 Menhaden, 17, 19, 21 Merlucciw capensis, 18 Merlucciw merluccius, 21, 28 Mesonychoteuthis hamiltoni, 238, 240, 251 Metridia, sp., 157 Miamiensia avidus, 8 Micrabralia aflEnis, 174 Micrabralia lineata, 176 Micropogon opercularis, 36 Micropogon undulatw L., 12, 32 See also Croaker Mintai, 23, 48 Mola mola, 35 Molva molva, 268 Monodon monoceros, 157, 266 Moroteuthis aequatorialis, 145, 246 Moroteuthis ingens, 145, 246, 258, 266 Moroteuthis lonnbergii, 146, 147 Moroteuthis robsoni, 146, 147, 246 Moroteuthis robusta, 146, 147, 244, 246, 265, 266 Mugil brasiliensis, 18 See also ASullet iMugil capito, 59 See also Mullet Mugil cephalua, 21, 59 See alao Mullet

SPECIES INDEX

Mugil japonicua, 59 See also Mullet Mullet, 5, 18, 21, 26, 51, 59 Mullet, grey, 59 Mullus barbatus, 26 See d o Mullet Mullus surmuletua, 5, 26 See also Mullet Mycobacterium, sp., 13 Mycobacterium murinum, 12 Myxidium sphaericum, 48 Myxobolus aeglejlni, 21 Myxobolus exiguus, 21 Myxosoma cerebralis, 21

310

Ommaetrepha bartranai, lo&-113, 244, 246

Ommaatrepha carol;, 104-113, 132,246. 265, 268, 269

Ommaatrephea giganieua, 116 Ommaetrephea gigaa, 116 Ommaatrephes illecebrooaua, 119, 244 Ommaetrephes laticeps, 149 Ommaatrephes oceunicua, 113 Ommaatrephes paci$cua, 132 Ommaatrephes pelugicua, 117 Ommaatrephes pteropua, 104113, 244, 246, 252, 258, 266, 269

Omnimtrephes sagittatua, 119, 123, 126 Onmaatsephes sloanei, 132 Ommaatrephea todarua, 119 N Ommastrepha Tryonii, 113 Nautilus, 93 Ommaatrephes volatilis, 118 Negaprion brevirostrb, 53 OnychiQ agilb, 160 Nematolampis regalis, 191, 192, 193, Onychia binotata, 150 248 Onychia cardioptera, 149 Nepioteuthion, 178 Onychia carribaea, 144, 149, 184, 244, Nepioteuthion Nishikawa, 186 246, 255, 259, 261 Nitzschia sturionk, 27 Onchorynchua nerka, 8, 48 Noaema lnphii, 23 Onchorynchua tahawytacha, 8 Nototodarus gouldi, 128, 270 Onychoteuthis banksi. 141, 244, 246, Nototodarua hawaiiensea, 128, 141 255, 260, 261, 265, 266, 267, 268 Nototodarus pacijlcua, 131 Onychoteuthia boredis-japonicua, 143 Nototodarus philippinens-is, 128, 140 Onychoteuthis ingens. 145 Nototodarus sloani, 128, 131, 140, 246, Onychoteuthia Lesueurii, 184 267 Onychoteuthia Lichtensteinii, 148 Nybelinia, 265 Onychoteuthia lorigera, 193 Onychoteuthis owenii, 174 Onychoteuthis perlatw, 203 0 Onychoteuthis robusta, 147 Orange filefish, 5 Octopodoteuthis danae, 187, 188 Oregoniateuthis lorigera, 192, 193, 248, Octopodoteuthis megaptera, 188, 189 266 Octopodoteuthie sicula, 186, 260 Oregonialeuthie apringeri, 192, 193, 248 Octopoteuthis danae, 187, 248 Ornithoteuthis antillarum, 118,246, 267 Octopoteuthis indica, 187 Octopnteuthw longiptera, 188, 189, 248, Ornithoteuthie volatilis, 118, 246 Orthagoniscua mola, 122, 268 266 Orthoprietis chrysopterus, 32 Octopoteuthis nielaeni, 187 Omerua eperlanua, 7, 21, 22 Octopoteuthis persica, 187 See also Smelt Octopoteuthis sicula, 113, 185, 187, 248, Osmerua mordax, 16, 21 261, 267 Ommmtrephes, 104, 256, 265, 266, 261, Otobothrium crenacolle, 27 Owenia, 229 268 Owenia megalops, 234 Ommaatrephes argentinw, 113 Oyster, 69 Ommaatrepha A y r d i , 113

320

SPECIES INDEX

P Pagrosomus major, 36 Parateuthk tunicata, 161, 162 Parathemisto japonica, 139 Pareuchaeta norvegica, 157 Parexocoetua brachypterua, 35 Parophrys vetulus, 18 Paateurella, sp., 9, 61 Pennella exocoeti, 35 Pennella filosa, 35 Perch, white, 9, 43, 61, 64 Periwinkle, 25 Perothis eschscholtzii, 224 Perothis pellucida, 223 Perotis Reinhardti, 2 19 Petromyzon marinus, 53 Phamnatopsis cymoetypus, 233, 235, 251 Phasmatopsis lucifer, 233, 235, 251 Phiximatopsis oceanica, 227, 233, 235, 251 Philonexia Eylais, 21 5 Phoca vitulina, 29 Phoebetria fuma, 266 Pholidoteuthia adami, 166, 247 Pholidoteuthis boschmai, 166, 247 Phyllobothrium, sp., 265 Phyllobothrium tumidum, 265 Pigfish, 32 Pike, 40, 43, 60 Pike, Baltic sea, 38 Pilchard, 19 Pilotfish, 36, 37 Plugiodux ferox, 113 Plaice, 7, 11, 12, 21, 29, 30, 38, 46 Plaico, American, 26, 37 Planctoteuthis, 210 Pleuronectesjleeue, 5, 7, 33 See also Flounder Pleuronectes plutessa, 7, 11, 12, 21 See also Plaice Plistophora, sp., 52 Plktophora ehrenbaumi, 46 Pliatophora gadi, 24 Plistophora hippoglossoides, 24 Pliatophora macrozoaridis, 23 Poecilancktrium robustum, 27 Pogonius cromis, 27 See also Drum

Pollachiua virens, 30 See also Pollock Pollock, 29, 33, 36, 157, 179, 186 See also Mintai Polydactylua octonemus, 32 Pomphorhynchw laeuis, 32 Poronotus trimanthus, 27 Porrocaecum, sp., 29, 30, 47 Porrocaecum decipiens, 29, 30 Pout, ocean, 22, 23, 29, 32 Procaliates suhmii, 228 Pseudalibrotus, sp., 157 Pseudomonaa, sp., 13 Pseudomonas jluorescena, 53 Pseudomonas ichthyodermis, 11, 57 Pseudomonaa (Aeromonaa) punctata 10, 11, 12, 54 Pseudopleuronectes americanus, 7, 26 See also Winter Flounder Psychroteuthis glacialis, 162, 247 Pterygioteuthis gemmata, 180, 181, 248 Pterygioteuthis giardi, 177, 180, 181, 248, 260, 261, 267 Pterygioteuthis margaritifera, 182, 248 Pterygioteuthis microlampas, 181, 182, 248 Pungitius pungitius, 22 Pyrgopsk atlantica, 221, 250 Pyrgopsk lemur, 223, 260 Pyrgopsis pacifica, 222, 250 Pyrgopsis rhynchophorus, 223, 250 Pyrgopsis schneehageni, 223, 250 Pyrosoma, 256 Pyroteuthk Giardi, 180 Pyroteuthis margaritifera, 182, 183, 267, 268

R Raja, 139, 267 Raja mouli, 125, 267 Raja ocellata, 54 Red tai, 36 Redfish, 29, 30, 31, 33, 34, 46, 47, 60, 152, 269 Rhombus maxinius, 29 See also Turbot Rhynchoteuthis larvae, 141 Roccw, americanua, 9 See also Perch, white

32 1

SPECIES INDEX

Roccus saxatilis 5, 9 See also Bass,striped Ruddcrfish, 28

S Sagitta, sp. Sagitta maxima, 157 Salmo gairdneri, 8, 53 See also Trout, rainbow Salmo trutta, 11 Salmon, 8 , 13, 21, 48, 53 Salmon, chinook, 8 Salmon, Pacific, 12, 19 Salmon, sockeye, 8, 48 Salmonids, 8, 12, 14, 24, 35, 45 Salvelinus alpinus, 18 Salvelinus fontinilis, 8, 54 See also Trout Sandalops ecthambus, 225, 227, 250 Sandalops melancholicus, 227, 250 Sandalops pathopsis, 227, 250 Saprolegnia, sp., 16 Sardina pilchardus, 16 Sardine, 12, 16, 17, 35, 4.5, 52 Sardinops ocellata, 19 Sardinops sagax, 12 Scolex polymorphus, 265 Scomber scombrua, 18, 268 Scomberesox, 117 Sea bass, 12 Seahorses, 8 Sea raven, 26, 30 Sea robin, 60 Seal, 29,30, 139, 147, 157, 159, 186,266, 267 Seatrout, 28, 58 Seatrout, sand, 32 Sebastes marinua, 29, 157, 268 See also Redjish Sebastes mentella, 268 Selenoteuthia scinti&zns, 192, 193, 248 Sepia eaculenta, 136 Sepia pelagica, 117 Sepioteuthia sicula, 169 Seriola zonata, 28 Shark, 27, 28, 32, 36, 48, 265 Shark, hammerhead, 27 Shark, lemon, 53 Skate, 28, 38, 39

Skate, winter, 63 Smelt, 7, 11, 16, 21, 22, 29, 30, 45, Snappers, 36 Snoek, 18 Sole, 7 Sole, flathead, 7 Sole, lemon, 18 Solea solea, 7 Somniosua mkrocephalue, 157, 267 Sphyrion, sp., 46, 47 Sphyrion lumpi, 33, 34 Sphyrna zygaena, 27 Spirula spirula, 93, 241, 244, 251, 252, 265 Spot, 32 Sprat, 16, 35 Steenstrupiola atluntica, 150 Stenabralia, 170 Steno rostratus, 236, 267 Stephanostomum baccatum, 26, 47 Stickleback, European, 23, 27 Stigmatoteuthis, 197 Stigmatoteuthw arcturn', 197 Stigmatoteuthw Chuni, 199 Stigmatoteuthis dojleini, 198 Stigmatoteuthb Vewilli, 199 Stockfish, 18, 19 Sturgeon, 27, 61 Sula piscator, 116 S u b sula, 266 Sunfish, ocean, 35 Swordfish, 18, 35 Symplectoteuthia, 106, 109, 113, 244 Symplectoteuthis luminoea, 113, 244, 246 Symplectoteuthis walanienai.9, 113, 244, 246, 266, 266

T Tai, red, 36 Taningia danae, 190, 256, 262 Tankaia borealb, 210, 212 Taonidium chuni, 228, 250 Taonidium incertum, 229, 260 Taonidium pfefferi, 229, 261, 267 Taonidium suhmi. 228, 238 Taonia abye&okk, 230

322

SPECIES INDEX

Taoniua cymoctypua, 233 Taoniua hyperboreua, 234 Taoniua maximua, 231 Taoniua megalops, 231, 234, 235, 251, 267 Taoniua of Iwai, 237 Taoniua pavo, 235, 236, 238, 251, 266, 268 Taoniua pellucida, 235, 236, 251 Taoniua richardi, 238 Taonius richardsoni, 237, 251 Taoniua Schneehageni, 223 Taoniua auhmii, 228 Taoniua thori, 236, 251 Teleoteuthis agilis, 150 Teleoteuthia Jattae, 150 Teloaentia tenuicornw, 32 Teregra chalcogramma, 268 Tetrarhyncua, 265 Tetronychoteuthia duawmieri, 152, 246, 266, 267, 268 Tetronychoteuthia maasyae, 152 Teuthowenia antarctica, 229, 25 1 Teuthowenia corona, 229, 251 Teuthowenia elongata, 230, 251 Teuthowenia megalops, 234 Teuthozuenia pfefferi, 231, 251 Teuthowenia tagoi, 230, 251 Thullamoebella paraaitica, 68 Thuumatolampaa diadema, 191 Thelidioteuthia alessandrini, 184, 185, 248, 260, 261 Thelidioteuthia polyonyx, 184 Theragra chalcogramma, 23, 48 Threadfin, Atlantic, 32 Thunnua alulonga, 125 Thunnw albacares, 18, 267 Thunnua germo, 140, 238, 267 Thunnua maccoyii, 140, 267 Thunnua obesua, 268 Thunnua thynnua, 35 See also Tuna Thynnua albacora, 113 Thyrsiteaatun, 18, 19 Thyaanoeeaa, 122 Thysanoeasa longicaudaia, 157 Thysanoteuthia elegana, 159 Thyaanoteuthis nuchalia, 159 Thyaanoteuthia rhombw, 159, 160, 244, 247, 252, 265, 269, 261, 266, 268

Todarodes paci’cua, 128, 130, 131, 244, 246, 252, 255, 256, 267, 259, 261, 266, 266, 267, 268, 269, 270 Todarodea sagittutua, 109,126,244,246, 252, 257, 258, 265, 266, 267, 268, 269, 270, 272 Todaropsia eblanae, 120, 125, 244, 246, 257, 265, 267, 268, 272 Todaropsia veranyi, 123, 125 Todaropsia veranii, 125 Tomopteria paci’ca, 139 Tonna, 139 Toxeuma belone, 230, 251 Trach.eloteuthiariisei, 162 Triaenophorus craasus, 48 Trout, 8, 11, 21, 53, 54 Trout, rainbow, 14, 53 Tuna, 32, 35, 140, 157, 180, 205, 267 Tuna, yellowfh, 18 Turbot, 29, 52, 60 Turaiopa truncatus, 189, 238, 267

U Unkapaula mwcularia, 18

v Valbyteuthia danae, 162, 247 Valdemaria danae, 206, 249 Velella velella, 148 Veranya aiculu, 187 Verrilliola gracilia. 162 Verrilliola nympha, 162 Verrilliteuthia hyperborea, 237, 251 Vibrio, sp., 10-13, 65 Vibrio anquillarum, 10, 11, 42 Vibrio parahemolyticus, 60

w W-enia scintillana, 179, 186, 248, 252, 255, 266, 267, 268, 269 Whale, Balaen, 139, 186, 266 Whale, Bottlenose, 145, 157 Whale, pilot, 122 Whale, sperm, 117, 127, 131, 132, 145, 148, 152, 157, 158, 159, 166, 189, 193, 194, 198, 205, 213, 236, 237, 238, 266

323

SPECIES INDEX

Whale, white, 145 Whiting, 33, 36, 48 Winter Flounder, 7, 2F, 36 Witch flounder, 29 Wolffish, 34

X x i p h k gladiUS L., 18 See also SwordJish

Z Zeus faber, 18 Zoarcea viviparus, 32 Zygaenopsis paciJica, 222 Zygaenopsis zygaena, 223 Zygocranchia zygaena, 222

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Su bj ect Index A Abnormalities, genetic and environmental, 35 carcinomas, epidermoid, 36 goiter, 36 hatcheries, 38 hyperplastic growths, 37 jellied flesh, 37 protein shortage, 37 structural abnormalities, 38 tumours, 36 Acanthocephala, 32 Algae, 58 Aquaria, disease in, 56 algae, 58 bacterial disease, 57 copepods, 69 dermatitis, 57 fin rot, 57 lymphocystis disease, 57 microsporidea, 58 nematodes, larval, 58 tail rot, 57 tuberculosis, 57 velvet disease, 57 white spot, 58

B Bacterial disease, 8 Augenkrankheit, 13 boil disease, 13 columnaris disease, 13 dermatitis, 11 epizootics, 9, 10 eye disease, 13, 45 fin rot, 11, 57 hemorrhagic septicemia, 12 Paateurella, 9 red disease of eels, 9, 42, 45 tail rot, 9, 67 tuberculosis, 12 V&io infections, 10-13, 42 Blumenkohlkrankheit, 7

C Carcinomas, 36 Cauliflower disease, 7 Cestodes, 27, 48, 52 Copepods, 32, 46, 59

D Dermatitis, 11, 57 Dinoflagellates, 57 Disease, 1 See also Bacterial disease, Fungus diaeme, Virua diaeaae bacteria, 8 copepods, 32, 46, 59 dinoflagellates, 67 fungi, 13, 41, 43, 50 helminths, 24 microbial, 4 protozoa, 16 Disease and reproductive capacity, 45 Disease and weight loss, 46 Disease control in the sea, 61 Disease, effects of, 40 background effects, 44 economic effects, 46 epizootics and mass mortalities, 40 Disease, immunity from, 52 Disease in marine aquaria, 56 Disease of fish, reIation to human disease, 69

enteritis, 59 eosinophilia, 59 larval nematodes, 59 meningitis, 69 nematodes, 69 raw fish, 59, 60 tapeworms, 60 Disease prevalence, variations in, 47 age effects, 51 geographic variations, 47 temporal variations, 50

E Epizootics, 9, 10, 14, 40, 60, G l , 62 Exophthalmia, 45 826

326

SUBJECT INDEX

F Fin rot, 11, 57 Fish pox, 7 Fungus disease, 13 Cladoaporium, 15 epizootics, 14, 41, 43 Ichthyophonus, 14, 41, 50

G Genetic abnormalities See Abnormalities Goiter, 36

H Hatcheries, 38 Helminths, 24 Acanthocephala, 32 Cestodes, 27, 48, 52 Nematodes, 29, 47, 58 Trematodes, 24, 50, 51, 52 Human disease, relation to fish disease, 59

I Ichthyophonus, 14, 41, 50 Immunization of fish, artificial, 52 Immunity from disease, 52

L Lymphocystis, 5, 57

M Microbial diseases, 4

N Nematodes, 29, 47, 58

0 Octopus, see Squid

P Papillomas, 7 Pollution, effect of, 37 Protozoa, 16 Coccidia, 16, 48, 60 Microsporidea, 21, 46

Protozoa-continued. Myxosporidea, 18, 48, 50, 51, 52

R Red disease, 9, 42, 45

S Squids, 9 1 buoyancy, 262 catching methods, 270 depth, 96, 109, 252 distribution, 94, 244 ecological importance, 265 economic importance, 269 egg masses, 135, 255 flying, 109, 118, 129, 143, 155 growth, size and form, 257 life history, 96 locomotion, 262 mating, 134 parasites, 265 photophores, 264 size, 257 sound production, 264 stranding of, 98, 100, 132 structural variation, 262 Squids, families Architeuthidae, 97 Bathyteuthidae, 166 Brachioteuthidae, 162 Chiroteuthidae, 200 Cranchiidae, 215 Enoploteuthidae, 170 Gonatidae, 152 Grimalditeuthidae, 2 14 Histioteuthidae, 193 Lepidoteuthidae, 213 Lycoteuthidae, 190 Octopoteuthidae, 187 Ommastrephidm, 104 Onychoteuthidae, 141 Parateuthidae, 161 Pholidoteuthidae, 166 Spirulidae, 241 Thysanoteuthidae, 159 Valbyteuthidae, 162 Stomatitis, 8

T Tail rot, 9, 67

SUBJECT INDEX

v Velvet disease, 57 Virus diseases, 4 Blumenkohlkrankheit, 7 cauliflower disease, 7 fish pox, 7 hemorrhagic septicemia, 8, 12 hyperplastic diseases, 7 lymphocystis, 5, 57

327

Virus diseases-continued. neoplastic diseases, 7 pancreatic necrosis, 8 papillomas, 7 stomatitis, 8 tumours, 7

w White spot disease, 58

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