Results of Long-Term Worldwide Studies on Tropical Nektonic Oceanic Squid Genus Sthenoteuthis: an Overview of the Soviet Investigations

Home , Sthenoteuthis, Sthenoteuthis pteropus

BULLETIN OF MARINE SCIENCE, 71(2): 1019–1060, 2002

MAIN RESULTS OF LONG-TERM WORLDWIDE STUDIES ON TROPICAL NEKTONIC OCEANIC SQUID GENUS STHENOTEUTHIS: AN OVERVIEW OF THE SOVIET INVESTIGATIONS

German Zuyev, Chingis Nigmatullin, Michael Chesalin and Kir Nesis

ABSTRACT Large-scale ecological investigations of oceanic squids of the genus Sthenoteuthis were carried out in the open waters of tropical zone of all three oceans during 1961–1990. They were focused on S. pteropus in the Atlantic and S. oualaniensis in the Indian and Pacific (mainly eastern Pacific) Oceans. The quantitative distribution of squids is not uniform; the areas of dense concentrations coincide with dynamically active zones of divergences and convergences and hydrological fronts. Planktonic paralarvae live in the epipelagic zone near pycnocline. Juveniles and adult squids are interzonal animals, rising to the surface during the night-time for feeding, and descend to the depths of 200–1000 m at dawn. The spatial range structure is complicated and consists of several areas with high squid abundance, which are isolated geographically and encompass different ecological parameters of the squid populations. Genetic exchange exists between these areas, thus they represent the superpopulational level of intraspecies structure. Both species, especially S. oualaniensis, are in process of active adaptive radiation. Five intraspecific forms of S. oualaniensis and two forms of S. pteropus were found. Sthenoteuthis spp. are very fast-growing animals: they can reach ML 55–60 cm and BW 8–9 kg at the age of 300 d. They are typical r-strategists with small eggs (0.75–1.0 mm), high fecundity (up to 10–22 million oocytes), monocyclic 1-yr life cycle, fast replacement of generations, quick variations of size structure and high productivity. Paralarvae and early juveniles eat mainly crustaceans while main food items of adults are micronektonic lanternfishes (Myctophidae) and squids. Adult Sthenoteuthis do not play an important role in the feeding of large oceanic top-predators. In the epipelagic ecosystems the main food chain is: crustaceans nyctoepipelagic myctophids Sthenoteuthis. A high degree of individual and social behavioral organization is characteristic of Sthenoteuthis squids. This is one of the most important prerequisites for their ecological progress. Squid biomass and productivity were preliminarily assessed. These squids are of great interest as important functional elements of oceanic ecosystems and as potential fishery resources.

Large squids of the family Ommastrephidae, subfamily Ommastrephinae, genera Dosidicus, Ommastrephes and Sthenoteuthis, play very important role in oceanic communities. Ommastrephins are medium and large nektonic predators widely distributed in the open ocean. In the true oceanic waters of the tropical zone of the world ocean they are represented by the genus Sthenoteuthis, which include two species: Atlantic orangeback squid Sthenoteuthis pteropus (Steenstrup, 1855) and Indo-Pacific purpleback squid Sthenoteuthis oualaniensis (Lesson, 1830). These squids are very abundant and dominant in number and biomass among ecologically similar nektonic epipelagic cephalopods and fish in the tropical zone of oceans and, together with flying fishes, they constitute the bulk of tropical oceanic near-surface nekton. Due to high abundance and good nutritional value these squids are prospective subjects for fisheries in the open ocean (Clarke, 1966; Zuyev and Nesis, 1971; Vovk and Nigmatullin, 1972; Voss, 1973; Okutani, 1977; Zuyev et al., 1985; Dunning and Brandt, 1985; Nigmatullin et al., 1991).

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Soviet investigations on the squid Sthenoteuthis started in the mid-1960s and conducted regularly in vast areas of the Atlantic, Indian and Pacific Oceans during 30 yrs. Specialists from several institutes participated in this work: Institute of Biology of the Southern Seas, Sevastopol (IBSS); Atlantic Research Institute of Marine Fisheries and Oceanography, Kaliningrad (AtlantNIRO); Board of Fisheries Ministry of USSR “Zaprybpromrazvedka”, Kaliningrad; Scientific-Industrial Association of Fisheries Tech- nics, Kaliningrad (NPO Promrybolovstva); Southern Research Institute of Marine Fish- eries and Oceanography, Kerch (YugNIRO); Board of Fisheries Ministry of USSR “Yugrybpromrazvedka”, Kerch; Board of Fisheries Ministry of USSR “HYDRONAUT”, Sevastopol; All-Union Research Institute of Marine Fisheries and Oceanography, Mos- cow (VNIRO); Institute of Oceanology, Moscow (IOAN), and others. The main field and laboratory effort was made in IBSS and AtlantNIRO under leaderships of G. V. Zuyev and Ch. M. Nigmatullin. The studies resulted in the development of new methods of investigation and strong intensification in the study of oceanic squid. These investigations revealed many aspects of distribution and biology of the squids, such as spatial distribution and migrations, morphology, phylogenetic relations, abundance, size-age composition, growth, reproduction, embryogenesis, food, parasites, behavior, life cycles, stock assessments and some physiological and biochemical features. This paper presents a brief review mainly of Soviet investigations, published between 1963 and 1996 (about 200 papers, mostly in Russian), summarizing modern views on the life history and distribution of the squid genus Sthenoteuthis, to provide a baseline for future scientific studies and fisheries management strategies.

MATERIALS AND METHODS

Squids of the genus Sthenoteuthis have been studied aboard Soviet research and fishery vessels in many parts of the World Ocean between 1959 and 1990. The data include material from 225 expeditions studying S. pteropus in the Atlantic Ocean, and 56 expeditions studying S. oualaniensis in the Indian and Pacific oceans. Most squids were observed and sampled at night-lighting drift stations. In total, observation of squids were accomplished at more than 9000 stations for S. pteropus, and more than 2300 stations for S. oualaniensis (Fig. 1). Estimations of abundance and biomass of the squids at water surface were obtained by the method of visual observations developed by Zuyev and Nigmatullin (1974; Zuyev et al., 1980, 1985, 1988). For proving the assessments calculated with this method, underwater observations were undertaken from a specially designed floating anti-shark cage 1.5 m in length, 1.6 m in with and 10 m in height. A SCUBA diver sat inside the cage, observing squid from distance up to 25 m (Bazanov and Parfenjuk, 1986). Vertical distribution and behavior of the squids were also studied from the Soviet manned submersibles SEVER-2 (operation depth to 2000 m), TINRO-2 (depth to 400 m) and TETHYS (to 200 m) (Gutsal, 1989; Moiseev, 1989, 1992). Squids were caught with hand and electromechanical rods equipped with various jigs and also with scoop nets, throw rings and hand harpoons. Material was also collected on many fishery research vessels with large midwater trawls (horizontal opening from 82–100 m) and ‘twin’ trawls (68–86 m). Paralarvae and juveniles of squid were caught with 20 m midwater trawl equipped with a small mesh in the codend. Basic data collected on each specimen in fresh state onboard were dorsal mantle length (ML), total body weight (BW), sex and maturity stage by 6-degree scale (Burukovsky et al., 1977; Zuyev et al., 1985), evidence of mating at buccal membrane of females, stomach fullness and presence or absence of dorsal mantle photophore. ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1021

Figure 1. Distribution of stations in which observations on squids Sthenoteuthis pteropus and Sthenoteuthis oualaniensis were made in the Atlantic and Indian oceans, correspondingly.

In total about 60,000 specimens of S. pteropus and more than 30,000 specimens of S. oualaniensis were subjected to abridged biological analysis. Stomach contents of about 2500 S. pteropus and 800 S. oualaniensis and their parasites were studied in details using methods described by Zuyev et al. (1985). Stomach content of about 700 large oceanic predators such as swordfish, dolphin fish, lancet fish, several species of tunas and sharks were also examined to assess the role of the squids in their diet. Age and growth of squids were determined using statoliths (Arkhipkin, 1988; Arkhipkin and Mikheev, 1992) and a new method based on gladius microstructure (Bizikov, 1991, 1995, 1996). Many special investigations were also made concerning squid morphology (body, arms, tentacles, beaks), development of reproductive system, female fecundity, spermatophorogenesis, embryogenesis and biochemical features.

HISTORICAL REVIEW

The study of the squid genus Sthenoteuthis has a 170-yr history. At first the purpleback squid was described under the name Loligo oualaniensis by Lesson in 1830, then the orangeback squid was described by Steenstrup as Ommastrephes pteropus in 1855. Both descriptions are rather brief, the size and sex of the holotype specimens are not indicated, and both are now lost. Both species were included in the genus Ommastrephes d’Orbigny, 1835, but then Verrill (1880) established a new genus, Sthenoteuthis, for these ommastrephids. Soon, Pfeffer (1900) separated purpleback squid into a new genus Symplectoteuthis. However, the taxonomy of the genus Ommastrephes was in a chaotic condition, without any precise criteria for species identification. Representatives of this genus were described under different names even from the northern Atlantic (Verrill, 1882; Steenstrup, 1862; Pfeffer, 1912; Naef, 1923; Rees, 1950; Adam, 1952; Jaeckel, 1958; Clarke, 1966). In 1950-1970s the majority of specialists accepted the following system: genus Ommastrephes d’Orbigny, 1835 with three species: O. bartramii (Lesueur, 1821), O. pteropus Steenstrup, 1855, and O. caroli (Furtado, 1887), and genus Symplectoteuthis Pfeffer, 1900 with two species S. oualaniensis (Lesson, 1830) and S. luminosa (Sasaki, 1915). It was considered that O. caroli is endemic of North Atlantic, O. pteropus is the 1022 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002 tropical Atlantic species and O. bartramii is widely distributed in the North Atlantic, North Pacific and South Atlantic (Clarke, 1966; Roper et al., 1984). The main reason for such taxonomic complexity lies in the lack of rich comparative material. The casual and isolated specimens, which fell into specialist’s hands, were usually collected from storm strandings or caught near the coast. Development of the oceanic fishery of tunas and other large fishes started from mid- 1950 activated national and international scientific programs, and many vessels began work in open oceanic waters. Observations and fishing for squid were included in the routine procedures of oceanographic expeditions. First observations and collections of oceanic nektonic squids were conducted by English (Baker, 1957, 1960; Clarke, 1965, 1966), American (Voss, 1956, 1966, 1973; Wormuth, 1970, 1976; Young, 1972, 1975) and Japanese scientists (Okutani, 1972, 1977; Okutani and Tung, 1978, etc.). However, these investigations were carried out incidentally and over rather limited areas and time periods. From the 1970s significant interest in oceanic resources arose due to the intro- duction of 200-mile exclusive economic zones and the exhaustion of fish stocks in traditional fishing grounds. Soviet researchers were linked to the study of oceanic squid. They put in order the subfamily Ommastrephinae, revealed the main features of their evolution (Zuyev et al., 1975; Nigmatullin, 1979) and delineated the boundaries of species ranges (Zuyev et al., 1976). As a result of the revision of the subfamily Ommastrephinae in the genus Ommastrephes only one species O. bartramii was left with O. caroli as junior synonym, orangeback and purpleback squids were united in the genus Sthenoteuthis, and Symplectoteuthis luminosa Okada, 1927 was transferred to Eucleoteuthis (Zuyev et al., 1975). Independently Wormuth (1976), using method of numerical classification, had come to a similar conclusion about the association of O. pteropus and S. oualaniensis in one genus Symplectoteuthis. However, this was incorrect because Symplectoteuthis Pfeffer, 1900 is junior synonym of Sthenoteuthis Verrill, 1882. The Soviet researchers developed new methods to count squids on the water surface (Zuyev and Nigmatullin, 1974; Zuyev et al., 1980, 1985, 1988), studying quantitative distribution in relation to abiotic and biotic environmental factors (Zuyev, 1967, 1971, 1973; Filippova, 1971, 1975; Vovk and Nigmatullin, 1972a; Nesis, 1974, 1977; Zuyev and Nigmatullin, 1975; Korzun et al., 1979; Alexandronets et al., 1983; Nigmatullin and Parfenjuk, 1988). They also studied different aspects of squid biology: reproduction (Zuyev, 1971, 1973, 1976; Klyuchnik and Nigmatullin, 1974; Burukovsky et al., 1977, 1979; Zalygalin et al., 1977), behavior (Nigmatullin, 1972, 1987; Vovk and Nigmatullin, 1972a,b; Zuyev and Nigmatullin, 1975; Parfenjuk et al., 1983; Nigmatullin and Parfenjuk, 1986), feeding and parasitofauna (Nigmatullin et al., 1977; Gaevskaya, 1977; Gaevskaya and Nigmatullin, 1981; Naidenova and Zuyev, 1978; Nigmatullin and Toporova, 1982; Filippova, 1974), population structure (Nesis, 1977; Zuyev and Nigmatullin, 1977; Zuyev and Shevchenko, 1973; Nigmatullin et al., 1983a,c; Pinchukov, 1983), including also biochemical methods (Koval, 1977). Research into these squids by non-Soviet scientists at this time were devoted mainly to their morphology and faunistic composition (Okutani, 1970; Roper, 1977; Voss, 1966; Wormuth, 1970; Young, 1972, 1975), and, to a lesser degree, their ecology (Alverson, 1963; Clarke, 1966; Ashmole and Ashmole, 1967; Suzuki et al., 1986; Young, 1975; Yamanaka et al., 1977; Hixon et al., 1980). Several articles were devoted to local fisheries for S. oualaniensis in areas off Taiwan and Okinawa (Okutani and Tung, 1978; Tung, 1973, 1976a, b). ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1023

The application of quantitative methods allowed the Soviet researchers to collect material for study of the dynamics of squid abundance, natural mortality and production characteristics (Zuyev and Zaika, 1977; Zuyev and Yusupova, 1977). As a result, conclusions about the possibility of a fishery for Sthenoteuthis were drawn (Vovk and Nigmatullin, 1972; Zuyev and Nigmatullin, 1977; Zuyev et al., 1977; Burukovsky et al., 1979). Main results of these multidisciplinary researches of squid were systematized in the monograph “Nektonic oceanic squids (genus Sthenoteuthis)” by Zuyev et al. (1985). The Soviet research activity concerning these squid was steadily growing in 1980s. Many papers were devoted to their physiological and biochemical features (Abolmasova, 1984, 1985; Abolmasova and Belokopytin, 1987; Abolmasova and Stolbov, 1991; Abolmasova et al., 1990; Belokopytin, 1982; Epstein, 1992; Grigorjeva, 1987; Rosengart et al., 1994; Stolbov, 1986; Shulman and Nigmatullin, 1981; Shulman et al., 1984, 1992; Timonina, 1980). Wide investigations on the role of these squids in trophic and their parasite fauna were carried out in the Atlantic, Indian and Pacific Oceans (Nigmatullin and Toporova, 1981; Nigmatullin et al., 1983b, 1988; Gaevskaya et al., 1983; Naidenova et al., 1985; Zuyev et al., 1985; Chesalin 1987, 1988, 1994; Shchetinnikov, 1988, 1992) and their reproductive biology (Nigmatullin et al., 1983a; Nigmatullin and Sabirov, 1987; Laptikhovsky and Murzov, 1990; Chesalin and Giragosov, 1993; Nigmatullin and Laptikhovsky, 1994; Laptikhovsky, 1995; Sabirov, 1995). Contributions to knowledge of squid biology arose from researches on their growth and age, using statoliths and gladii (Mikheev, 1988; Arkhipkin, 1988; Arkhipkin and Bizikov, 1991; Arkhipkin and Mikheev, 1992; Bizikov, 1991, 1996; Laptikhovsky et al., 1993). Great interest in squid was excited after the discovery, with manned submersibles, of large schools of S. oualaniensis in the depths of Arabian Sea in 1986 (Chesalin, 1993; Gutsal, 1989, 1991; Korzun, 1990; Korzun et al., 1992; Ruchkin, 1988; Volkov et al., 1988; Zuyev and Gutsal, 1989, 1994). In 1980–1990s some interesting ecological publications appeared about S. oualaniensis by non-Soviet specialists, based on local data (Silas et al., 1982; Harrison et al., 1983; Dunning, 1988, 1998; Young, 1994; Young and Hirota, 1998; Yatsu et al., 1998; Snyder, 1998). Non-Russian publications on S. pteropus were almost absent. Now due to work of Soviet researchers, the squids of the genus Sthenoteuthis are studied much better than any other oceanic squids.

SYSTEMATICS

Class Cephalopoda; order Teuthida; suborder Oegopsida; family Ommastrephidae; subfamily Ommastrephinae; genus Sthenoteuthis Verrill, 1880; Sthenoteuthis oualaniensis (Lesson, 1830); Sthenoteuthis pteropus (Steenstrup, 1855).

SYNONYMY

Sthenoteuthis pteropus Verrill, 1880, 1882; Pfeffer, 1900, 1912; Zuyev et al., 1975, 1985, Nesis, 1982, 1985; Architeuthis megaptera Verrill, 1880; Ommastrephes pteropus Steenstrup, 1855, 1880, 1887; Adam, 1952; Voss, 1956; Roper, 1963; Clarke, 1966; Zuyev and Nesis, 1971; Ommastrephes bartramii var. sinuosa Lönnberg, 1896; Xiphoteuthis ensifer Owen, 1881; Steenstrup, 1885. 1024 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

Sthenoteuthis oualaniensis Zuyev et al., 1975, 1985; Nesis, 1977, 1982, 1985; Loligo oualaniensis Lesson, 1830; Loligo vanicoriensis Quoy et Gaimard, 1832; Loligo brevitentaculata Quoy et Gaimard, 1832; Ommastrephes oualaniensis Férussac et d’Orbigny, 1835–1848; Gray, 1849; Steenstrup, 1880; Ommastrephes oceanicus Férussac et d’Orbigny, 1835–1848; Symplectoteuthis oualaniensis Pfeffer, 1900, 1912; Berry, 1912, 1914; Sasaki, 1929; Adam, 1952, 1962, 1973; Voss, 1954; Zuyev, 1971; Zuyev and Nesis, 1971; Voss and Williamson, 1972; Young, 1975; Wormuth, 1976; Okutani and Tung, 1978.

LOCAL NAMES

Sthenoteuthis pteropus: English – Orangeback flying squid, yellowback squid, wing- armed squid; French – Encornet dos orange; Spanish – Lomo anaranjado, pota naranja, pota de limão, lula de limão; Japanese – Nise-Akaika; Russian – Krylorukij kal’mar (wing- armed squid). Sthenoteuthis oualaniensis: English – Purpleback flying squid, yellowback squid; French – Encornet bande violette; Spanish – Pota cardenal; Japanese – Tobi-ika; Russian – Kal’mar-ualaniensis (oualaniensis squid).

EVOLUTION AND PHYLOGENY

Soviet researchers have revealed the main features of evolution of the squid family Ommastrephidae (Zuyev et al., 1975, 1985; Nesis, 1975; Nigmatullin, 1979, 1992a; Bizikov, 1991, 1996). Ancestors of modern oceanic ommastrephid squids were shallow- water animals. Subsequent evolution gave rise to near-bottom and benthopelagic squids, then the nerito-oceanic species (living offshore but near or over the slopes), and lastly, oceanic squids (living in the meso- and epipelagic layers of the open ocean) (Nesis, 1975; Nigmatullin, 1979). The comparison of morphology of gladii of fossil and living squids indicates that the ancestors of recent ommastrephids may be the fossil Plesioteuthidae. The representatives of this family, Plesioteuthis prisca (Rppell, 1829) and Paraplesioteuthis sagittata (Münster, 1843) were frequent in the Upper Jurassic (Donovan, 1977; Bizikov, 1996). Based on an analysis of morphological characteristics, systematics and phylogeny, squids of the family Ommastrephidae evolved from the small coastal forms to active nektonic predators in the hypothetical sequence: Illicinae Todarodinae Ommastrephinae with two intermediate groups: Todaropsinae and Ornithoteuthinae (Nigmatullin, 1979, 1992a). According to biogeographical and paleoclimatic data, partly supported by the records of statoliths of two ommastrephids (Dosidicus lomita, Symplectoteuthis pedroenis) in the Late Pliocene sediments (Clark and Fitch, 1979), recent fauna of Ommastrephinae had developed approximately 1.5–2 million years ago, in Upper Pliocene to Late Pleistocene (Zuyev et al., 1975). During this period a general fall of temperature took place, which was accompanied by freezing of polar areas and lowering of the oceanic level (Einarsson et al., 1967; Bogdanov et al., 1978). The faunal exchange between Pacific and Atlantic oceans was considerably reduced. In particular, it is considered that an initial species of the genus Sthenoteuthis was S. pteropus, which migrated from the Atlantic to Indian Ocean and further in Pacific Ocean. Obviously, a breakup of initial pantropical range of ancestor species of both S. pteropus and S. oualaniensis take place in Early Pleistocene ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1025

Figure 2. Scheme of squids phylogenetic relations in subfamily Ommastrephinae and had resulted in isolation of the Atlantic and Indo-Pacific parts of its range and formation of two separate species (Zuyev et al., 1975). The progressive biological evolution of the ommastrephids took place mainly by a process of aromorphosis (= anagenesis), divergence in size and the occupation of wide transoceanic ranges in the most productive off-slope and epipelagic zones, coming into competition with predatory fishes and leading to the coevolution of squids with main their prey (plankton-eating fishes, mainly myctophids). Another direction of evolution became one of specialization: decrease in size (trend to nanization), an adaptation to areas with low food abundance, reducing competition by descent into more large oceanic depth (meso- and bathypelagic zones) or to periphery of the productive centers. These are features of two other ommastrephine genera, Eucleoteuthis and Hyaloteuthis (Zuyev et al., 1975). Thus, the subfamily Ommastrephinae presents, on one hand, large and numerous active nektonic squids: Dosidicus, Ommastrephes and Sthenoteuthis, with other, small and relatively rare Eucleoteuthis and Hyaloteuthis (Fig. 2). In turn, large and ecologically active species have divided between them practically all regions of tropical to subpolar oceans and have allopatric ranges. However, evolution is continuing among these squid. In response to biotopic heterogeneity and high intensity of biotic relations there is intensive selection and intraspecific differentiation inside this relatively young group of animals (Nigmatullin, 1979; Nigmatullin et al., 1983c, 1991a; Zuyev et al., 1985; Nesis, 1985).

MORPHOLOGY

The morphology and anatomy of Sthenoteuthis features which are important for taxonomy and phylogeny, such as the shape of body and fin, structure of funnel groove, arms and tentacles, their suckers, fixing apparatus, hectocotylus, form and disposition of photophores have been thoroughly described in cephalopod monographs and reviews 1026 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

(Steenstrup, 1880, 1887; Pfeffer, 1912; Naef, 1923; Sasaki, 1929; Rees, 1950; Jaeckel, 1958; Clarke, 1965; Zuyev, 1971; Zuyev and Nesis, 1971; Wormuth, 1976; Roper, 1977; Nesis, 1982; Roper et al., 1984; Roeleveld, 1988; Filippova et al., 1997). Hard structures were also described in detail: beaks (Clarke, 1962), gladii (Toll, 1981, 1988; Bizikov, 1991, 1996), statoliths (Arkhipkin, 1988), horny rings of suckers (Adam, 1952, 1962; Roeleveld, 1982; Murzov and Nigmatullin, 1983). There are detailed researches on functional morphology of these squids, interpreted with analyses of adaptations to swimming, seizing of preys, camouflage (Zuyev, 1966), reproductive systems of males and females (Burukovsky et al., 1977; Nigmatullin and Sabirov, 1989; Laptikhovsky, 1995; Sabirov, 1995), ontogenetic variability of arm and tentacular armature (Murzov and Nigmatullin, 1983). Some important data on aspects of morphology of genus Sthenoteuthis are pre- sented below. The mantle and funnel cartilages are free in S. pteropus, while they fused on one or, more commonly, both sides in postlarval stages of S. oualaniensis. The hectocotylus of S. pteropus carries 6–8 pairs of suckers, whereas in S. oualaniensis there are 11–13 pairs (Nesis, 1982). The external morphology of S. pteropus and S. oualaniensis is very similar. The adult squids have a robust mantle, cylindrical in anterior and conical in posterior half. The fins are large, rhombic, with a blunt back end, their length is 40–50% ML and width 70–85% ML. The head is slightly compressed in the dorso-ventral direction, with large eyes. Arms are rather short, stout and have protective membranes. Suckers on the arms are located in two rows, their horny rings equipped with sharp teeth. Tentacles are powerful, strong and may be somewhat stretched or contracted. Tentacular club suckers are located in 4 rows. Rings of large suckers bear large teeth, the four longest and sharp- est are located crosswise. The funnel cartilage is shaped with longitudinal member longer than transverse one. The form of the mantle and fins change greatly during life. Juvenile squid are graceful, relatively thin, cylindrical, pencil-like with a thin-walled mantle, short arms and small fins, while adults are robust, more spindle-like, with a thick-walled mantle, and arms and fins relatively longer and fins much wider than in juveniles. The muscles of adult squid are strong, their fibres obliquely-striated, quickly-contractible and highly aerobic (Hochachka et al., 1975a,b; Moon and Hulbert, 1975; Storey, 1977). The distribution of muscles and collagen fibres in the mantle, fin, arms, and funnel have been studied in detail (Zuyev, 1966; Koval and Zhivotovskaya, 1984; Zhivotovskaya and Koval, 1985; Zhivotovskaya et al., 1987; Zhivotovskaya, 1988, 1998). The form and structure of squid mantle, arms, funnel, and fins, their changes during ontogeny, and properties of muscle layers characterize these squids as powerful swimmers for which high horizontal speed is more important than manoeuvrability (the reverse is peculiar for squids with a heart- shaped fin and thinner mantle such as Eucleoteuthis or Onychoteuthis). Juvenile Sthenoteuthis can reach such high speeds that they can leap out of the water and fly some distance in the air. During flight, S. oualaniensis extends thin protective membranes on the 3rd arms and use them as a second fin (functionally caudal because they fly tail first) similar to those seen in anti-aircraft missiles (Nesis, 1982b, 1985). Body coloration in a normal condition: red-brown dorsal part with large oval luminous spot (photophore), sides and ventral part are light, slightly silvery. The coloration quickly changes with excitation. Occasionally, bluish luminescence flares are observed on the body. Fine luminous corpuscles (size of 0.2–2.8 mm) are dispersed throughout the body sunken into the upper muscle layer under the skin (Roper, 1963). Paralarvae have photo- ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1027 phores on the ventral part of eyes and two photophores on intestine, however they become hardly appreciable in subadult squids and are not functional in adulthood.

SIZE AND LENGTH-AT-WEIGHT RELATIONSHIP

Sthenoteuthis squids are large-sized. Adult specimens may attain 65–70 cm ML. Fe- males may be about twice as large as males. The largest measured female of S. pteropus was 63 cm ML, male 28 cm; female and male of S. oualaniensis respectively 62 and 32 cm ML. The absolute length (with arms but without tentacles) may attains 100–120 cm. The weight of largest S. oualaniensis recorded was 8.9 kg (Chesalin, 1994) and of S. pteropus was 6.5–7 kg (Zuyev et al., 1985). Limits and average sizes of adult squids depend of geographic location and population variability. According to an empirical data the relationship between mantle length (ML, cm) and body weight (BW, g) were calculated, data in both species, males and females were pooled, because the species and sexual dimorphism of these relationship had no essential differences (Zuyev et al., 1985). Therefore, for the majority of calculations the following power functions are accepted:

BW = 0.099 ML2.13 in squids <4.5 cm ML,

BW = 0.019 ML3.20 in squids >4.5 cm ML.

The length-weight relationship for adult S. oualaniensis from Hawaiian waters were calculated by Suzuki et al. (1986) as BW = 0.00018 ML3.15.

Tung et al. (1973) calculated other functions for S. oualaniensis:

log BW = 2.8481 log ML – 4.0088.

For more detailed calculations, separately for each ontogenetic phase of S. oualaniensis, the following size-weight relationships were calculated by Chesalin (1993):

BW = 1.123 ML2.020 for paralarvae 0.2–1 cm,

BW = 0.805 ML2.135 for postlarvae 1.1–3 cm,

BW = 0.063 ML2.666 for juveniles 3–15 cm,

BW = 0.082 ML2.699 for middle-sized squids 15–30 cm,

BW = 0.005 ML3.506 for large-sized squids >30 cm.

For paralarvae of S. pteropus ML 1.0–9.5 mm Laptikhovsky et al. (1993) proposed

BW = 0.00053 ML 2.42. 1028 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

For studies of the trophic relations of squids and their predators the relationship between rostrum length of the upper mandible (URL, cm) and ML (cm) for S. pteropus was described by Trofimov et al. (1983):

ML = 3.41URL + 2.3.

ONTOGENETIC PHASES

Morphological features of the squids (shape of mantle and fins, prey capture apparatus), their geographical distribution, behavior and trophic relations change fundamen- tally during ontogenesis. On the basis of the analysis of these parameters some different ontogenetic phases were distinguished for species of Sthenoteuthis (Murzov and Nigmatullin, 1983; Nigmatullin, 1987a). Besides, Bizikov (1996) had divided the ontogenesis of S. oualaniensis into several periods based on character of gladius development. Summarizing these works on morphological development of the squids, but based mainly on ecological criteria, we distinguish the following six ontogenetic phases: I. Embryonic phase (mesoplanktonic): egg diameter ranges from 0.7–1.0 mm, embryos inside from 0.76–0.95 mm. External yolk sac is very small, internal yolk sac is relatively large and reduced only in the end of embryogenesis. Duration of the phase is from 4–6 d. II. Paralarva (mesoplanktonic): free-living rhynchoteuthion, ML to 1.0 cm. Tentacles fused together and form a ‘proboscis’ longer than arms. Arms are short without keels and membranes bear 14–16 smooth suckers. Gladius is weakly differentiated. III. Postlarva (macroplanktonic): ML ranges from 1.0–2.5 cm. Tentacles free in the beginning are shorter and thinner than arms, do not function. Tooth suckers are developed on arms and tentacles. Short and wide stalk appears in back end of the gladius, formed by developing halves of rachis. IV. Juvenile (micronektonic): ML from 2.6 to 8–12 (13–15) cm. The prey capture apparatus is fast-growing, squid gradually attain the adult habitus. The basic elements of gladius (lateral plates and keel) develop. V. Middle-sized adult (nektonic): ML from 8–15 to 30–35 cm. The main attributes of capture apparatus are well pronounced, but the growth of arms and tentacles continued and number of teeth increased, especially of large functionally significant club suckers. Gladius has definitive shape with characteristic thick edges of rachis, wide lateral plates and narrow short keel. VI. Large-sized adult (macronektonic): ML from 36–40 to 60–65 cm, absolute length (with arms) to >1 m. Arms and tentacles are characterized by negative allometric growth. All basic elements of gladius (edges of rigid ribs, lateral plates, keel) strengthen with simultaneous complication of internal structure.

SEXUAL DIMORPHISM

Sexual dimorphism in Sthenoteuthis is rather well expressed. Adult males can be easily distinguished from females by their more compact, narrow and streamlined body, wider fin and pointed back end of mantle, presence of hectocotylus and sometimes spermatophores, which are became visible in the mantle cavity. Most evidently sexual dimorphism is expressed in body size: the females of both species are 1.5–2 times larger than males. ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1029

GEOGRAPHIC DISTRIBUTION

The species ranges in S. pteropus and S. oualaniensis were summarized by Nesis (1982, 1985). The functional structure of species ranges and seasonal changes of their borders were considered in more detail by Alexandronets et al. (1983), Zuyev et al. (1976, 1985), and Nigmatullin (1989, 1992b; Nigmatullin et al., 1991). Both S. pteropus and S. oualaniensis are narrowly tropical oceanic species, whose ranges do not widely embrace subtropical belts. Their life cycle completely extends to the open ocean beyond continental shelves. They occur at sea surface temperatures from 16o to 32oC, but usually above 20–22oC. They avoid brackish waters near river mouths with salinity lower than 34‰. S. pteropus inhabit the tropical Atlantic and those subtropical areas adjacent to continents. The extreme points of its distribution lie at the latitude of New York (42oN) and Madeira (36oN) in the north, to Uruguay (30oS) and South Africa (32oS) in the south. The boundaries of its distribution in the central part of the ocean approximately coincide with the Tropics of Cancer and of Capricorn. The reproductive area, which was defined by the occurrence of mature females, occupies the equatorial zone, including the Caribbean Sea and Gulf of Mexico between 20oN and 20oS near continents and between 10oN and 10oS in the central part of the ocean. The boundaries of S. pteropus range undergo significant seasonal changes. During summer in the northern hemisphere (July–October) the northern boundary is displaced to the north, whereas the southern one comes nearer to equator and is located near the coasts of Brazil and Namibia at approximately 23oS and at approximately 10oS in the central part of ocean. During winter (February–March) the northern boundary is shifted to the south of Cuba and to Morocco (20–22oN), while the southern one is displaced further south. S. oualaniensis is a geographical vicariant of S. pteropus, distributed in the tropical Indian and Pacific oceans. The northern boundary of its range in the Indian Ocean is limited by the Asian continent. The southern boundary reaches the southernmost point of Africa (about 35oS), then is narrowed a little to the central area of the southern Indian Ocean and passes on to the Pacific Ocean approximately along the Tropic of Capricorn to the continental slope of South America. However, near America, westward of the Peru Current, the abundance of S. oualaniensis is low and here the Jumbo squid Dosidicus gigas predominates (Alexandronetz et al., 1983; Nigmatullin et al., 1988). The reproductive area of S. oualaniensis is located in the Indian Ocean northward of 18–22oS, and in the Pacific Ocean between 20–25oN and 16–20oS. The range boundaries are mobile and are displaced toward high latitudes with warming during summer of the appropriate hemisphere and moved to lower latitudes with the fall of water temperature. In the open ocean, the boundaries of species distribution are determined by the position of the primary (non-mixed) water masses and main frontal zones. Over continental slopes and in adjacent areas of the open ocean the secondary (mixed) water masses where there are intermediate water traits, the seasonal movement of species range boundaries are determined by seasonal latitudinal shifts of surface isotherms 20–22°C. In general, the boundaries of the both species’ ranges coincide with location of Northern and Southern Subtropical Convergences, which serve as substantial ecological barriers (biogeographical borders) for many tropical pelagic animals. These Convergences limit the spread of tropical water masses of the Trade Currents into subtropical and temperate latitudes (Alexandronetz et al., 1983; Zuyev et al., 1985; Nigmatullin, 1992b). Biotic factors, mainly shortage of food and competition with neon squid Ommastrephes bartramii is a second- 1030 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002 ary factor limiting the distribution of S. oualaniensis to oligotrophic areas of the Central Water Masses in the North and South Pacific and South Indian oceans. This is a subordi- nate factor not of biogeographical but of ecological (= biotopical) nature.

ABUNDANCE

Special attention was paid to the study of squid spatial distribution and sites with high density which considered as areas for prospective fisheries (Zuyev and Nigmatullin, 1975, 1977; Nikolsky et al., 1986; Zuyev et al., 1985; Nigmatullin, 1989). The quantitative distribution of squids at the limits of their species ranges is not uniform. The main peculiarities of the squid distribution were studied on mesoscale and macroscale levels. Macroscale distribution was considered on the basis of long-term data of quantitative squid distribution, dynamics of sexual maturation, morphological variability in adult females, and regularities of large-scale circulation of upper water layer (0–200 m). Maps of squid distribution were drawn and sites with high abundance in number and biomass (as a rule, with concentrations of >750 squids and >250 kg km−2), the so-called large-scale productive zones, were defined. The main quasi-stationary large-scale productive zones (LSPZ) of S. pteropus with a spatial dimension of hundreds and thousands miles are most pronounced in the eastern Atlantic Ocean: Northeast LSPZ between 10 and 20oN, from African coast to 25–30oW, Equatorial LSPZ between 5oN and 10oS, from 0 to 20oW, and Angolan LSPZ between 5 and 20oS, from African coast to 5oE. There are also two smaller zones of high squid density in the Gulf of Guinea between 2oN and 3oS, and in the Caribbean Sea and western Atlantic near Lesser Antilles (Fig. 3). Four large-scale productive zones of S. oualaniensis in the Indian Ocean were defined for winter season: Arabian, Somalian, Equatorial, and Mozambican LSPZs. Patterns of squid distribution sharply changes during summer due to the monsoon and only the Equa- torial LSPZ can be clearly defined. The large-scale productive zones of squid distribution coincide with dynamically active zones of divergences and convergences and oceanic fronts. The productive zones are formed mainly near areas with active vertical and horizontal movements of water mostly off the upwelling areas. For example, the spatial distribution of main large-scale productive zones of orangeback squid, Northeast, Equatorial and Angolan LSPZs is limited, correspondingly, by the divergence zone of Northern Tropical Cyclonic Gyre, Equatorial Divergence and Namibian Upwelling along southwestern African coast. The formation of productive zones of purpleback squid is closely connected with seasonal dynamics of monsoons. The strengthening of northeast monsoon in the winter is accompanied by formation of squid productive zones in areas to the north from equator, and the strengthening of southeast monsoon in the summer is resulted in development of productive zones near equator and low latitudes of the Southern Hemisphere. The distribution of the squids was studied on a mesoscale level during several expeditions with grids of stations from 5 to 30 nm apart (Arkhipkin et al., 1988; Zuyev and Nikolsky, 1993; Trotsenko and Pinchukov, 1994). The main element of squid spatial structure on the mesoscale level is the appearance of local productive zones with dimensions from 10 to 40 km (mean value 23 km), and durations of the order of weeks or months (Zuyev et al., 1985). These local zones represent sets of squid shoals, concentrated in places with favorable trophic conditions. They present the main interest for fisheries and, ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1031

Figure 3. Distribution of zones with high abundance of Sthenoteuthis pteropus in the Atlantic Ocean and Sthenoteuthis oualaniensis in the Indian Ocean. therefore, forecasting their position based on oceanographical data is one of the main tasks for this purpose. It was found that they coincide with frontal zones.

VERTICAL DISTRIBUTION

Squids of the genus Sthenoteuthis are pelagic animals, they live in the open ocean and are usually absent over the shelves and over shallow (<200 m) seamount summits. They usually first appear over continental slopes at depths >250-300 m (Zuyev et al., 1985). These squids spawn in the epipelagic zone at night. Egg masses are pelagic and probably float above the pycnocline layer (Laptikhovsky and Murzov, 1990; Chesalin and Giragosov, 1993), but there is some indication that they may even float at the sea surface (Zuyev, 1971). Paralarvae, postlarvae and early juveniles with ML up to 9 cm also usually live in the surface homogenous layer above the gradient layer, from the surface to 50–75 m. They do not apparently perform diurnal vertical migrations or these migrations are very short in distance (Klyuchnik and Nigmatullin, 1974; Nesis, 1979; Arkhipkin and Shchetinnikov, 1989; Moiseev, 1992). During daytime the main bulk of juveniles occurs near the surface in the 0–25 m layer, while at night they descend deeper, to 25–50 (75) m, going out of the zone of predatory adult squid of the same species, which rise to the surface at night (Bazanov, 1986; Zuyev et al., 1985). Late juveniles and adult squids are interzonal animals, rising to the epipelagic layer at night for feeding and descending up to 800–1200 m depth in the morning. Adult S. pteropus were observed from manned submersibles in the open Atlantic between 0 and 150 m at night, and between 500–550 and 1200 m in daylight hours (Moiseev, 1992) (Fig. 4). On moonless nights most squids are concentrated near the surface (0–25 m), while in moon- lit nights they dispersed a little deeper (10–50 m). At dawn, in a short time (about one hour), squid descended to the depth of daily habitation with maximum concentration at the depths of 600–850 m. In the twilight (before sunrise and after sunset) squid occurred in the 150–400 m range. 1032 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

Figure 4. The vertical distribution pattern of squids genus Sthenoteuthis. The density of distribution: 1- isolated individuals, 2 – high density.

Adult S. oualaniensis also rise to the surface at night and descend deeper than 400 m in daytime (Kolodnitsky and Moiseev, 1987; Sumerin and Gutsal, 1988), but a single squid was encountered as deep as 1100 m (Moiseev, 1992). A surprising phenomenon is found in the Arabian Sea. Here giant females of S. oualaniensis were monitored from the manned submersible in the layer of 200–350 m during the day, where they actively fed on dense concentrations of mesopelagic fish (Gutsal, 1989, 1991; Sumerin and Gutsal, 1988; Zuyev and Gutsal, 1989, 1994). According to our data these squids concentrate in the main epipelagic sound-scattering layer (from 70 to 120 m), which provides favorable feeding conditions. A striking phenomenon of the Ara- bian Sea is the strong oxygen minimum layer lying from 100–200 to 1000–1700 m depth (Muromtsev, 1959; Ivanenkov et al., 1964). Oxygen concentration in this layer as low as 0.1–0.2 mg L−1 (2–4% saturation); water temperature in the layer is 5–15ºC. Thus, both in the daytime and during the period of activity at night, the giant form of S. oualaniensis is partly or wholly located in the hypoxic zone with low temperature. Biochemical tests have shown that under oxygen deficiency squids can use proteins and products of their catabolism (free amino acids) for anaerobic energetic metabolism (Shulman et al., 1992a).

INTRASPECIFIC STRUCTURE

Characteristic features of these squids are the very complicated population structure and morphological distinctions between different forms. Clarke (1965) indicated that the purpleback squid divides between a dwarf, early-maturing form without dorsal photo- ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1033 phore and a late-maturing form with dorsal photophore. Nesis (1977) has found distinctions between these two forms in the proportions of the fin and mantle, structure and dimensions of hectocotylus and spermatophores. He has shown, that the formation of dorsal mantle photophore occurs in a rather narrow range of size (ML 10–12 cm) and hypothesized that in the dwarf form this process is blocked by the onset of maturation at ML 9–10 cm. Ecological differences were also observed between these forms (Nigmatullin et al., 1983b,c; Pinchukov, 1983). Later morphological differences were found between the late-maturing form and the giant Arabian Sea form, both with dorsal photophore. Bizikov (1991, 1996) found differences in the structure of gladius in these squid forms and has distinguished several intraspecific forms. On the basis of size differences, dorsal photophore and gladius morphology, five forms of S. oualaniensis can be distinguished: (1) dwarf early-maturing equatorial form without dorsal photophore; (2) dwarf late-maturing Red Sea form with dorsal photophore; (3) and (4) middle-sized late-maturing form with dorsal photophore and with single lateral axis of the gladius (3), distributed in the Red and Arabian seas and the Gulf of Aden, and with double lateral axes of the gladius (4), most common in the tropical Indian and Pacific oceans; (5) the giant form with dorsal photophore and single lateral axes, inhabiting Red Sea, Arabian Sea and the Gulf of Aden (Bizikov, 1991, 1996; Nesis, 1993, 1995). S. pteropus is also represented by a small early-maturing equatorial form and a large late-maturing form. ML in the first group is 12–20 cm for males and 16–32 cm (mode range 21–25 cm) for females, and in the second group 18–28 and 30–65 cm (mode range 38–46 cm). Representatives of the large late-maturing squids are distributed throughout the species range, but small early-maturing squids lived only in the equatorial zone and adjacent waters (Zuyev et al., 1985; Nigmatullin et al., 1991). Obviously, both these forms are widespread, but divided, in turn, into a number of populations separated by vast areas with low productivity, oceanological barriers, etc. An ecological-geographical approach to the study of the population structure of S. pteropus was applied by Zuyev (Zuyev, 1983; Zuyev and Schevchenko, 1973; Zuyev and Nigmatullin, 1975; Nigmatullin et al., 1991; Zuyev and Nikolsky, 1993; Zuyev et al., 1976, 1985, 1992). As a result it was shown that S. pteropus is represented at the limits of its extensive transoceanic range by a number of regional large-scale productive zones, which can be considered as self-repro- ducing populations. These populations are not only separated geographically, but also differ genetically. Tentative biochemical data on S. pteropus intraspecific structure (Koval, 1984) allow three groups to be distinguished in the eastern Atlantic based on the fre- quency of phenotypes of estherases of squid mantle and skin. These are the Northern, Equatorial and Southern groups, coinciding geographically with populations of North- east, Equatorial and Angolan large-scale productive zones, described above.

REPRODUCTION

Maturation of squid belonging to the different forms begins at different sizes. Mantle length of mature males in the dwarf equatorial form of S. oualaniensis is 7.5–11 cm, of mature females 10–15 cm (Zuyev et al., 1985). The size parameters of mature males and females of the middle-sized and giant forms are not exactly defined, but on preliminary data, ML of males of middle-sized squids ranges from 11–25 cm, females 16–28 cm; males of giant Arabian form have ML 24–32 cm, females 30–63 cm (Chesalin et al., 1034 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

1995). The size of mature males of S. pteropus is from 12 to 28 cm, of females from 16 to 65 cm (Zuyev et al., 1985; Nigmatullin et al., 1991). Development and functioning of the reproductive system in males and females were investigated in detail (Burukovsky et al., 1977, 1979; Zalygalin et al., 1977; Hixon et al., 1980; Zuyev et al., 1985; Nigmatullin and Sabirov, 1989; Nigmatullin and Laptikhovsky, 1994; Laptikhovsky, 1987, 1995; Sabirov, 1995). Males of both species have a structure of spermatophoric complex typical for Ommastrephinae. In immature and maturing periods before full maturation of testis, so- called ‘tentative’ spermatophores without a sperm rope are formed. These are not accumulated in the Needham’s sac and are ejected from the sac via the penis. During the period of physiological maturation the structure of tentative spermatophores is complicated and during the latter part of tentative spermatophorogenesis quasi-spermatophores are formed that have seemingly normal morphology but their sperm reservoir is empty. The morphology of normal spermatophores in both species is very similar. The size of spermatophores increases during spermatophorogenesis in the mature stage of ontogenesis due to somatic growth and the positive allometry of spermatophoric glands increas- ing in size. Their length depends on the ML of mature males: the larger males the larger spermatophores they produce (Nigmatullin and Sabirov, 1987; Sabirov, 1995). The spermatophore length (SL) in S. pteropus varies from 15 mm (ML 10.7 cm) to 42 mm (ML 24 cm), usually 32–34 mm. Their relative size is 10.6–27.1% ML. In dwarf form of S. oualaniensis the length of spermatophores is 8.8–11.7 mm, or 9.5–14.9% ML (ML 8–9.3 cm), in middle-sized form it is 16–32 mm or 12.7–26.7% ML (ML 12–16.4 cm) (Sabirov, 1995) and in giant form they are about 40–50 mm (Zuyev, 1971). The total number of spermatophores in S. pteropus with ML <16 cm is about 100–300 and with ML >17 cm - 200–500, the males of S. oualaniensis have from 200–300 spermatophores (Zalygalin et al., 1977; Nigmatullin and Sabirov, 1987; Sabirov, 1995). The spermatozoa have one flagellum and are relatively large. Their total length is 350– 450 µm. The elongated head of the sperm in S. pteropus is like a slightly curved and pointed stick, with a length of 12.6–12.9 µm, 1.5–2 times longer than in other ommastrephids. The middle part is spur-like as in other decapod cephalopods, its length is about 2.5 µm. Flagellum length is about 350–400 µm, or 3–10 times longer than in other ommastrephins. The number of spermatozoa per spermatophore varied from 2.01 ± 1.02 to 13.52 ± 2.46 millions. Larger spermatophores of larger males contained more sperms (Laptikhovsky, 1987). The development of oocytes and the structure and development of ovaries in Sthenoteuthis have been described and a maturity scale has been proposed (Burukovsky et al., 1977, 1979; Zuyev et al., 1985; Nigmatullin and Laptikhovsky, 1994; Laptikhovsky, 1995). A characteristic feature of these squids is the continuous asynchronic development of the oocytes stock in ovary. The process of the preparation for reproduction falls into 2 parts: (1) the development of the ovary and accessory organs and maturation of the ovary (physiological maturation - maturity stages I-IV), (2) production and accumulation of ripe eggs in the oviducts (functional maturation - stages V1-V3). The ova are easily distinguished from immature oocytes by their orange color and smooth texture. In mature squids, the nidamental glands are relatively large, opaque and white, whereas the glands of young squid are colorless and small. The maximal maturity index (weight of reproductive system as % of BW) of S. oualaniensis and S. pteropus varies from 11–15 to 25–30% (Zuyev et al., 1985; Harman et al., 1989; Chesalin and Giragosov, 1993; Laptikhovsky, 1995). ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1035

Maturation proceeds rapidly. As most females live for about one year, it is possible to assume that the process of female maturation lasts about 9–10 months, and direct accumulation of mature eggs and spawning activity about 1-3 mo. Ripe eggs are pinkish or raspberry-coloured, relatively small - maximal diameter in both species is 0.7–1.0 mm and weight 0.15–0.35 mg. Egg size does not depend on female size. In S. pteropus eggs are relatively uniform (average diameter 0.73–0.87 mm and weight 0.20–0.26 mg). In S. oualaniensis there are geographical and intraspecific variations in the egg size: eggs of the Indian Ocean females of all intraspecific groups (average diameter 0.70–0.79 mm, weight 0.15–0.27 mg) are significantly smaller (t = 3.324) than of females from eastern Pacific (0.76–0.94 mm, 0.22–0.35 mg). In three intraspecific groups of S. oualaniensis from the Indian Ocean, egg size is not significantly different, but the eggs of the dwarf early-maturing form are slightly smaller (0.71–0.74 mm, 0.14–0.19 mg) than of middle- sized late-maturing (0.70–0.89 mm, 0.17–0.27 mg) and giant (0.69–0.79 mm, 0.17–0.23 mg) forms, the two latter are nor different. Potential fecundity (PF) depends on adult female size. In S. pteropus PF ranged between 0.56 to 18 million eggs. In females of the small early-maturing group the PF is 1– 5 million oocytes (mode range 1.5–2 million) and for large late-maturing animals - 4–18 million (mode range 5–6 million). In the dwarf form of S. oualaniensis the PF is 300–550 thousand oocytes, in the middle-sized form PF is 0.7–8.5 million and in the giant form, 6–22 million. Relative fecundity for both species is 3000–7000 oocytes g−1 (Nigmatullin and Laptikhovsky, 1994; Laptikhovsky, 1995). Therefore, squid of this genus have one of the highest rate of potential fecundity among cephalopods. Mating occurs in the surface water layer at night in the ‘head to head’ position (Voss, 1966; Tung, 1976a; Nigmatullin and Parfenjuk, 1887). Copulation was observed to take place on the surface at night drift stations for S. oualaniensis in the eastern Pacific and S. pteropus in the eastern tropical Atlantic and with a duration of only 0.5–3 min (Nigmatullin, Parfenjuk and Laptikhovsky, unpublished). A male and a female interlace by the arms and then the male transfers spermatophores with the hectocotylus to the buccal membrane of the female. The transferred spermatophores explode and the sperm come out from the opening in the posterior end of the spermatangia into the buccal membrane cavity and by an unknown mechanism the sperm penetrate seminal receptacles. From 3– 5 to 100–150 spermatangia were found attached to the buccal membrane and buccal cone in S. oualaniensis and from 5 to 160–180 in S. pteropus. Total duration of the sperm release from a broken spermatophore is about 80-150 h and up to 200 h at 8°C, 30–45 h at 23°C, and 10–15 h at 27–29°C. Females can store viable sperm in seminal receptacles on the buccal membranes for a long time, so mating and spawning need not coincide. There are 70–120 seminal receptacles in S. oualaniensis and 57–155 in S. pteropus (Usanov, 1994). The nidamental glands secrete the large gelatinous matrix for the egg mass. There is indirect evidence that squids of genus Sthenoteuthis are multiple spawners. After spawning once they apparently continue to feed, grow, and mature additional oocytes before spawning again (Harman et al., 1989; Nigmatullin and Laptikhovsky, 1994). Spawning lasts for 1–3 mo at a relatively stable level and without a decrease in feeding rate. This is a very important characteristic for oceanic ommastrephids with their very high level of fecundity. During the individual spawning period females continue to show significant somatic growth (Nigmatullin and Laptikhovsky, 1994). 1036 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

The egg mass of S. pteropus was described based on one finding of egg mass fragments in eastern Atlantic (Laptikhovsky and Murzov, 1990) and the egg mass of S. oualaniensis was briefly described by a fragment from the Gulf of Aden (Zuyev, 1971) and from 9 giant females caught in the northwestern Arabian Sea (Chesalin and Giragosov, 1993). In the latter case the egg masses were described as translucent mucus in which many pale-crimson eggs were dispersed at a density of about 1–2 eggs cm−3. Egg diameter ranged between 0.72 and 0.86 mm, with an average of 0.81 mm. The maximal measured volume of the egg mass was about 25 L. Total numbers of eggs are estimated at tens of thousands. The embryonic development is typical for Ommastrephidae. In our experiments underdeveloped paralarvae hatched after 2.5–3 d in water temperatures of 21–25.5oC (Chesalin and Giragosov, 1993). According to a theoretical equation (Laptikhovsky, 1991) the duration of embryogenesis for Sthenoteuthis spp. at normal temperatures can be from 4 to 6 d. Spawning is not linked to the bottom and occurs in the epipelagic zone, generally at the oceanic side of western and eastern Boundary Currents (California, Peru, Canary, Brazil- ian, Benguela, etc.). At the species level, spawning takes place all-year-round, but at different intensities; different intraspecies forms differ in their time of spawning. So, the peak spawning of S. pteropus occurs from late summer till mid-autumn in both the North- ern and Southern Hemispheres. The mass maturation of males in the northeastern part of the tropical Atlantic occurs two months earlier than the mass maturation of females (Zuyev et al., 1985; Nigmatullin et al., 1991). The spawning peak of dwarf equatorial form of S. oualaniensis is in summer (Nesis, 1975; Pinchukov, 1983; Zuyev et al., 1985), of middle-sized form in Northern Hemi- sphere during autumn and winter (Okutani and Tung, 1978; Zuyev, 1971; Zuyev et al., 1985), and that of the giant Arabian form in the spring (Chesalin, 1994). In southeastern Pacific the squids of middle-sized form spawn all-year-round with peak in warm season (December–February) (Nigmatullin et al., 1983a, 1991).

AGE AND GROWTH

First investigations of the age and growth of the genus Sthenoteuthis were conducted on the basis of analysis of seasonal dynamics of size-sex structure from jigged catches (Zuyev, 1971; Zuyev and Zaika, 1977; Zuyev et al., 1979, 1985). Using the von Bertalanffy growth equation the parameters of squid linear and weight growth were calculated. Maxi- mal life span for squids based on these estimates was 2 yrs. It was assumed that males lived 10–11 mo, small early-maturing females 1 yr, and large late-maturing ones 2 yrs (Zuyev et al., 1985). Based on data of energetic metabolism, the growth curve of S. pteropus was computed (Abolmasova et al., 1990). Later age and growth rates of S. pteropus were calculated using increment counts in statoliths of all life cycle stages from paralarvae to adults (Mikheev, 1988; Arkhipkin, 1988; Arkhipkin and Mikheev, 1992; Laptikhovsky et al., 1993). In S. pteropus the paralarval stage lasts 32–38 d. The two youngest paralarvae studied were 14 d old (ML 3.2 and 3.8 mm) and the oldest one with an almost divided proboscis had 38 d (ML 9.5 mm). At the age of 14–38 d, the daily relative growth rate decreased from 7.5 to 2.8% ML d−1, and weight gain rate from 14–16 to 5.8% BW d−1. A sharp decrease of growth rate was observed during the end of paralarval stage (ML 6–9.5 mm, age 25–38 d) when the paralarval proboscis is divided. Using statoliths data it was pos- ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1037 sible to define age structure, growth and mortality (Laptikhovsky et al., 1993). Relative growth rate of juveniles remains relatively high (7–8% BW d−1). Juvenile S. pteropus attain ML 10–11 cm by age of 100–110 d. In mature females the relative growth rate is the lowest (1.8–2.5% BW d−1). Absolute daily growth rate reaches maximal value 40–70 g d–1 in large late-maturing females ML 45–50 cm. No differences in growth rate were observed between immature males and females. Sexual dimorphism in growth rate appears at the age of 90–100 d. The majority of males become mature at 120–150 d and almost all males older 170–180 d were mature. A sharp decrease in male growth rate was observed at the age 120–180 d (2.4–3% BW d−1) in comparison with females (3.2–4.2% BW d−1). Males completely finished maturation at the age 270–280 d. Females began maturing at the age 200–220 d and mass maturation was observed at 240–300 d. All females studied were mature and mostly in spawning stage at ages over 300–320 d. Maxi- mal age of a spent male (ML 18.6 cm) was 306 d and a spawned female (ML 42.2 cm) 372 d. The life span of S. pteropus females from all size groups does not exceed 1 yr and that of males is 1–2 mo shorter (Mikheev, 1988; Arkhipkin and Mikheev, 1992). Successful use of the gladius as a recording structure enables us to study the real growth of a given individual, rather than obtain the statistical correlation of length/weight versus age, by using statolith counting. Using gladii the data on individual and group age, growth and production for the different forms of S. oualaniensis were defined more accurately (Bizikov, 1990, 1991, 1995, 1996). The growth pattern of linear increase was either slightly sigmoid or almost linear, while growth in weight followed a power-type pattern and may be attributable to the fact that it is connected with spawning. Generally, females grew faster than males. The duration of life cycle in dwarf early-maturing equatorial form of S. oualaniensis was estimated at about 6 mo, of middle-sized tropical, Red Sea and Arabian Sea forms (both sexes) about 1 yr, and giant Red Sea and Arabian Sea forms also about 1 yr. Therefore, their growth rate should be different and that better called not early- and late-maturing but slowly- and fast-growing forms. The largest daily increment in length in the middle-sized squids was 1.0 mm, while in the giant female’s 3.8 mm. The monthly production of 1-yr-old giants is at 9 least times that of the middle-sized squids of the same age (Bizikov, 1995, 1996). Analysis of individual growth rates in giant spawning females of S. oualaniensis revealed a growth rhythm of roughly one-month periodicity with phases of rapid growth (17–21 d; 1.6–3.6 mm d−1) alternating with phases of slow growth (12–14 days; 0.4–1.2 mm d−1); this may be connected with spawning (Bizikov, 1995, 1996).

BIOTIC RELATIONS

PREY.—Feeding of S. pteropus and S. oualaniensis has been studied in detail (Filippova, 1974; Tung, 1976b; Wormuth, 1976; Nigmatullin et al., 1977, 1983b; Nigmatullin and Toporova, 1982; Zuyev et al., 1985; Chesalin, 1987, 1988, 1994, 1996; Shchetinnikov, 1988, 1992). These squid are active predators with a wide food spectrum. A total of 105 species of bony fishes and pelagic invertebrates were found in the stomachs of S. pteropus: 54 fish species from 17 families, 30 species of crustaceans from 16 families and 15 species of cephalopods from 10 families. Most abundant in the squid diet are fishes of the families Myctophidae (22 species), Exocoetidae (6), Gonostomatidae (4), Gempylidae and 1038 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

Table 1. Changes of main preys of the squid S. pteropus during its ontogenesis.

Odntogenetic size group Meain foo Prey siz No of prey Consumer (cm) in stomach level (specimens) (average level) Paralarvae (0.1−0n.8 cm) M--Iicro- and mesozooplankto I Postlarvae (1.0−2s.5 cm) M5esoplanktonic crustacean 0. −13.0 −5)II-III (II Early juveniles (3−9scm) M1acroplanktonic crustacean −39−1)2 II-IV (III Late juveniles (9−1s5 cm) M2icronektonic fishe −56−8)III-V (IV Adult, middle-sized (15−3s5 cm) M3icronektonic fishe −83−6)IV-V (IV Adult, large-sized (35−6s5 cm) N6ektonic fishes and squid −125 −5)IV-V (V Paralepididae (3 in each). Among crustaceans the most frequent are copepods, amphipods, decapods, and euphausiids, among cephalopods prevailed squids, including own juveniles, Onychoteuthis banksii and various Enoploteuthidae (Chesalin, 1994). Besides, the representatives of tunicates, chaetognaths, ostracods, etc., were found. In general, 65 prey taxa were found in the diet of S. oualaniensis in the Indian Ocean (Chesalin, 1994) and southeastern Pacific (Shchetinnikov, 1988). Most common are fishes (26 species, including 14 myctophids), followed by crustaceans (16 species) and cephalopods (16 species). Food species spectrum changes during squid ontogeny. In juveniles it is dominated by meso- and macroplanktonic invertebrates, mainly copepods, amphipods and euphausiids, in adulthood it includes micronektonic and nektonic fish, such as plankton-eating myctophids, flying fishes and Vinciguerria nimbaria, and predatory fish such as gempylids, paralepidids, etc. and squids (mainly own juveniles, Onychoteuthis banksii and enoploteuthids) (Table 1). Fragments of crustaceans (copepods, amphipods) and squid lens were found in alimentary canal of S. oualaniensis paralarvae (Vecchione, 1991), hence, their main food items are likely to be mesozooplankton. The postlarvae and early juveniles occupy the niche of micronektonic epipelagic plankton-eaters; the late juveniles and middle-sized squids are small and middle-sized nektonic nycto-epipelagic predators; large-sized squids are large nektonic epi- and mesopelagic predators. The strategy of squid feeding behavior significantly changes during growth. Early juveniles can be referred to active-grazing predators, late juveniles and middle-sized squids are predator-pursuers, while large-sized adults are attacking predators. It is necessary to note that giant females of S. oualaniensis in the Arabian Sea consume mainly myctophids, which are numerous and inactive in the layer 100–200 m. So, these giants do not pass to trophic level of large nektonic predators (as attacking predators) and by their type of behavior they remain active-grazed predators. Experiments with squids in captivity have shown, that the digestion rate in the squid stomach is high and the time to full digestion of meal takes approximately 3–5 h in early juveniles; 5–8 h in late juveniles and 8–10 h in middle-sized squids (Nigmatullin, 1981; Zuyev et al., 1985; Chesalin, 1994). To determine the daily food rations many calculations were made for different size-age group of squids using field data on daily dynamics of stomach content and experimental data on the rate of food digestion (Nigmatullin, 1981; Nikolsky and Chesalin, 1983; Lipskaya, 1986; Chesalin, 1988, 1994, 1996). The daily food ration varies from 28% BW in juveniles to 3–4% BW in adult males. The estimations of daily food ration for adult S. ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1039 oualaniensis were based on decrease of their liver weight during experimental starvation: 9–12% BW (Shulman and Nigmatullin, 1981). From data on nitrogen excretion rates, the ration size of S. oualaniensis was estimated at 6.5% BW, and for S. pteropus of same size 6.7% BW (Shulman et al., 1984). The results of all research show very high food rations of these squids are needed to maintain their active mode of life. The average daily food ration for middle-sized squids (15 to 35 cm ML) was calculated 5–10% BW, while the rations for the majority of adult pelagic fishes is 1–5% BW (Chesalin, 1994). PREDATORS.—Squids of the genus Sthenoteuthis play some role in the feeding of top predators, inhabiting epipelagic layer: sharks, bony fishes, mammals and sea birds (Welch, 1950; Alverson, 1963; Miyazaki et al., 1973; Borodulina, 1974; Young, 1975; Clarke et al., 1976; Wormuth, 1976; Belopolsky and Shuntov, 1980; Harrison et al., 1983; Zuyev et al., 1985; Nigmatullin, 1986; Shchetinnikov, 1988; Zamorov et al., 1993; Abita-Gardenas et al., 1997; Robertson and Chivers, 1997). Plankton-eating fish, small squids, large chaetognaths, jellyfishes, and carnivorous fishes eat the paralarvae and early juveniles of squid. Squid juveniles from 3–10 cm are the prey for a wide variety of species such as large squids, tunas, dolphin fish, snake mackerel, lancet fish (Alepisaurus spp.) and small sharks. They are consumed by sea birds that lay eggs and feed their chicks on land and therefore play an appreciable role in the transfer of matter from marine to terrestrial communities. Tunas and lancet fish eat middle-sized squid too but only occasionally (Nigmatullin, 1986). Main predators of middle-sized squid are dolphins, swordfishes and some active species of sharks. Large-sized squids are inac- cessible for tunas and they have fewer predators: adult swordfishes, dolphins, toothed whales and large sharks. In some areas, such as the Arabian Sea, large oceanic predators rarely occur, therefore S. oualaniensis, owing to its high abundance, large size, short life span, fast growth, and high food ration almost completely monopolize the trophic niche of top predators and become the ‘master’ of the Arabian Sea (Chesalin, 1994). The main food chain in the epipelagic ecosystems is: mesoplanktonic crustaceans myctophids Sthenoteuthis. HELMINTHS.—The fauna of squid helminth parasites consists of 15 species in S. pteropus (3 trematodes, 8 cestodes, 2 acanthocephalans, and 2 nematodes) and 9 species in S. oualaniensis (2 trematodes, 3 cestodes, 2 acanthocephalans, and 2 nematodes) (Gaevskaya, 1977; Naidenova and Zuyev, 1978; Gaevskaya and Nigmatullin, 1981; Gaevskaya et al., 1983; Naidenova et al., 1985; Zuyev et al., 1985; Gaevskaya and Shukhgalter, 1992). All helminths, except for acanthocephalans and juvenile Hirudinella ventricosa, are present as larval forms. Their adult stages are mostly parasites of cartilaginous and bony fishes and marine mammals. The majority of helminths are localized in the squid alimentary canal. The intensity of infection is generally low, from several to tens individuals. Only trematode larvae are recorded in juvenile squid in high abundance (up to 20,000 individuals). Size-age variability of the helminths and the degree and incidence of helminth infestation in S. pteropus have been analyzed in relation to age changes in the host ecology. The only factor responsible for the helminth infestation of the squids and their transfer to final hosts is food. Early juveniles are infested only by trematodes, other helminths occur in squid of ML >12 cm. The extent and intensity of infection increase with squid size. Almost all helminth species found in the squids use other animals (mostly bony fishes) as intermediate hosts at the same stages of their life cycle. The use of fish by squid as prey is an important factor contributing to the secondary accumulation in the squid of common helminth species. Thus the helminth fauna of squid has the character of a sec- 1040 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002 ondary ‘initial fish helminth fauna’. Trophic and parasitic relations of squids are synchro- nized. Due to their wide distribution, high abundance, quick alternation of cohorts and diversity of trophic relations being relatively stable over time, the squid Sthenoteuthis spp. is an important, sometimes obligatory, link in the life cycle of many their helminths between the first and second intermediate and the final hosts, such as tunas, sharks and dolphins (Gaevskaya and Nigmatullin, 1981; Naidenova et al., 1985).

BEHAVIOR

Squid behavior was studied during visual observations in the ship’s light field from the deck of the drifting or slowly moving ship in the 0 to 3–5 m layer at night and on the surface during the day (Nigmatullin, 1972, 1987b; Vovk and Nigmatullin, 1972b; Zuyev and Nigmatullin, 1975b; Nesis, 1982b; Nigmatullin and Parfenjuk, 1986; Parfenjuk et al., 1983). It was also studied by SCUBA divers from the anti-shark cage at night light stations in the 0–30 m surface layer (Bazanov, 1986, 1987, 1988; Bazanov and Parfenjuk, 1986), from manned submersibles TINRO-2 and SEVER-2 during day and night at depth to respectively 400 and 1200 m (Sumerin and Gutsal, 1988; Moiseev, 1989, 1992; Moiseev and Kolodnitsky, 1989; Zuyev and Gutsal, 1989; Gutsal, 1989, 1991), and with Doppler hydrolocation (Afanasyev et al., 1983). The Sthenoteuthis squids have the morpho-functional features of an active nektonic swimmer during the whole of postlarval ontogenesis (Zuyev, 1966; Koval and Zhivotovskaya, 1984; Zhivotovskaya and Koval, 1987; Zhivotovskaya, 1988, 1998). Their apparatus for prey capture is well developed (Murzov and Nigmatullin, 1983), as is the brain, particularly the optical lobes (Zuyev, 1975). These features determine behavioral patterns of these squid as high-speed and highly manoeuvrable nektonic animals, mo- mentarily reacting to any change in its surroundings. The color of their bodies may change in a moment and vary from whitish-grey and even almost white to brightly red or dark brown. Their usual color is light or dark brown with a bright luminescent orange spot on the anterior part of the back. They are typical oceanic squid living in a three-dimensional environment. They defi- nitely avoid the bottom even if, in the daytime, in the continental slope area, they descend to the near-bottom layer. In this case they remain 2–3 m away from the bottom while, on the contrary, the shelf-slope-living ommastrephids such as Illex or Todarodes may rest on the bottom (Nesis, 1985; Moiseev, 1989, and pers. comm.). Sthenoteuthis in general are characterized by high cruising speed and particularly by high rush speed. Maximal locomotory activity is inherent in young animals of ML 3–10 cm. During ontogenesis locomotory activity steadily decreases. The cruising speed of middle-sized squid of ML 15–35 cm is approximately 3–10 km h−1, and rush speed, more than 25–35 km h−1 (Afanasyev et al., 1983; Bazanov, Nigmatullin and Parfenjuk, pers. observ.). Migratory speed may also be high. Migrating shoals of squid of ML 25–35 cm were repeatedly observed swimming over periods of 2–5 min at speeds of 20–35 km h−1 (Nigmatullin, pers. observ.). However, it is unclear how long they may sustain such a high speed during horizontal migration. These squid are predators-pursuers and attacking predators, hunting prey by overtak- ing it and often pursuing potential prey over long time periods at high speed. Middle- sized squids often continue to hunt while holding one or two killed prey, usually lanternfishes, in their arm crown. During the night these squid may feed, depending on ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1041 trophic conditions in the area, either quasi-constantly or with two activity peaks, one at dusk and one at dawn (Zuyev et al., 1985). In areas with very low abundance of food organisms, squid are less active during the night. The squid are highly maneuverable during hunting. Sudden stopping may alternate with rush jerks. Swimming at high speed, squid may sharply change both speed and direction, even to the diametrically opposite one. When squid are tightly crowded in the light zone (up to 300–1000 animals within view) or hunting actively and simultaneously, they never collide or even touch one another (Nigmatullin, 1972, 1987b; Vovk and Nigmatullin, 1972b; Bazanov, 1986). Locomotory activity decreases strongly in large squids of ML greater than 45–50 cm. During most of the night, they are passive near the surface and move with slow fin undu- lations, thus minimizing active metabolism. They slowly steal up to potential prey (mostly intermediate-sized fish and squid) and then pounce upon them from a distance of 3–5 m. When an attack fails, they do not pursue it. In danger, they can reach high speeds in a moment (Nigmatullin, 1987b). In the highly productive Arabian Sea, large S. oualaniensis of the giant local form live in a ‘soup’ of lanternfishes; they graze upon their swarms day and night and do not switch to feeding on middle-sized fish as is typical for large squid in other places (Zuyev and Gutsal, 1989; Chesalin, 1994). During the day, at depths more than 200–300 m, squids are much less active than by night at the surface. Here, they generally either ‘hang’ on the spot or move slowly, less than 1–1.5 km h−1, mostly with undulating fins. However, giant S. oualaniensis in the Arabian Sea continue to feed on lanternfishes even during the daytime at depths of 200– 300 m, although less actively than by night (Moiseev, 1989, 1992; Zuyev and Gutsal, 1989). Sthenoteuthis remain obligate shoaling animals throughout their ontogenesis. This is particularly evident when squid density is low. Here squid form swarms of animals of different sizes and in some cases even attempt to join fish of similar size (Nigmatullin, 1972, 1987b). Usually, shoals are formed from animals of the same size without dominant individuals. In the areas of range overlap with related ommastrephid species (Ommastrephes bartramii, Dosidicus gigas), shoals may include animals of two species but of the same size or even of different sizes, but the same in squid of each species (Parfenjuk et al., 1983; Bazanov, 1987; Nigmatullin, pers. observ.). The functions of shoal are various; they may include foraging, defense and migration. The number of squid in a shoal has very broad limits, from 2–4 to more than 200–1000. Shoal size depends on the productivity of the area, on relative abundance of squid of a given size in the area, and on dominant behavior at certain times (day or night) and certain life cycle stages. The abundance of animals, the form of shoals, their composition, and shoal function are highly labile in time and space and may change even over a period of hours (Nigmatullin, 1972, 1987b; Zuyev and Nigmatullin, 1975b; Nigmatullin and Parfenjuk, 1986). Such a high level of individual and social behavioral organization is one of most important prerequisites for ecological progress in Sthenoteuthis squids. 1042 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

Table 2. Equations relating metabolic rates and body weight in the squids Sthenoteuthis.

Stpecies Body weigh Temperature Type of Eequation Sourc (g) (ºC) metabolism S. pteropus 6−16,300 2 −2d8 SWtandar 1.13 0.87 Abolmasova, 1984 --« - -e« AWctiv 3.11 0.80 S. oualaniensis 22−7950 2 −3d0 SWtandar 1.59 0.78 Abolmasova, 1985 --« - -e« AWctiv 4.71 0.75

ENERGY METABOLISM

The study of different features of metabolism in the squids genus Sthenoteuthis has been conducted by the investigators of Departments of Animal Physiology and Ichthyol- ogy of Institute of Biology of the Southern Seas (IBSS) from 1978 to 1990 (Abolmasova, 1985; Abolmasova and Belokopytin, 1987; Abolmasova et al., 1990; Chesalin et al., 1992; Stolbov, 1988; Shchepkin et al., 1981; Shulman and Nigmatullin, 1981; Shulman and Yakovleva, 1981; Shulman et al., 1984, 1992; Yuneva et al., 1994). It has been shown that these squids have very high rate of energy metabolism. The relationship between energy metabolism and body weight of the squids was measured in a specially designed respirometer and the corresponding equations were derived (Abolmasova, 1984, 1985) (Table 2). Research has been conducted on juvenile S. pteropus (average ML 94 mm, average weight 26.6 g) to determine the rate of their metabolism and its dependence on partial pressure of oxygen (Stolbov, 1988b). The oxygen consumption at standard metabolism in S. −1 −1 pteropus was calculated as 460 ml O2 kg h (Shulman et al., 1984), and in S. oualaniensis −1 −1 as 348 ml O2 kg h (Abolmasova and Belokopytin, 1987). The metabolic rate depends on swimming speed and temperature and for S. pteropus (ML between 11–25 cm) at 28ºC and at swimming speed of 1.0, 1.5 and 2.0 total body length (TL) per second increases respectively from 1.4–2.2, 1.7–3.3 to 2.0–4.9 times in comparison with standard metabolism (Abolmasova and Belokopytin, 1987). The optimum swimming speed during horizontal and vertical migrations for these squids was determined as 1–1.5 TL s–1 (20-30 cm s−1) (Abolmasova and Belokopytin, 1987). The level of the energy metabolism was found not to depend on hydrostatic pressure corresponding to the depths of 45 to 100 m (Abolmasova and Stolbov, 1991). Data on oxygen consumption (Abolmasova, 1985; Belokopytin, 1982), weight incre- ments (Zuyev et al., 1985) and food assimilability, accepted as 95% (Boletzky, 1974; LaRoe, 1971; O’Dor et al., 1979), have allowed calculation of values for food assimila- tion, daily food consumption and coefficients of utilization of the consumed food for growth on the basis of balance equation (Shulman et al., 1984). The daily food ration was calculated: for S. pteropus (1–700 g BW) from 45.7 to 7.5% (mean 14.5%); for S. oualaniensis (20–700 g BW) from 19.2 to 7.4% (mean 11.4%) (Abolmasova et al., 1990).

The coefficients of utilization of energy consumed (K1 = P/C) and assimilated (K2 = P/ P+Q) food for growth (P – production, C – ration, Q – metabolism) varied for S. pteropus from 10.2 to 37.2% and 10.8–39.0%, for S. oualaniensis 7.2–34.1% and 7.6–34.9%, respectively. ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1043

BIOCHEMICAL PROPERTIES

Chemical composition of squid tissues (mantle, fins, arms, tentacles) is characterized by a high percentage of water (about 80%), high content of protein (approximately 17%), low contents of lipids (about 1%) and very low glycogen (0.1%) (Ertel’, 1970; Lagunov et al., 1979; Shchepkin et al., 1981). The midgut gland (liver or hepatopancreas) plays a dominant role in the accumulation of protein and lipid reserves (Shulman et al., 1984). Direct relationship was found between the content of dry matter in the liver and its lipids and protein content for both S. oualaniensis (Nikolsky and Shulman, 1980) and S. pteropus (Abolmasova et al., 1990). The absolute content of total lipids and proteins in the liver was found to increase with growth and maturation of squid, but the relative amount of reserve matter decreased (Chesalin et al., 1992; Shulman and Yakovleva, 1981). The amount of dry matter, lipids and proteins in the squid liver more or less depends on total biological productivity of the region in which they live (Abolmasova et al., 1990) and was used to estimate the food supply of S. pteropus in comparison with data on relative abundance of squid and their main food organisms – lanternfishes (Shulman et al., 1992b). Content and composition of total lipids, phospholipids, and fatty acids in squid tissues (liver, mantle, fins, arms, tentacles) have been studied in detail (Abolmasova et al., 1990). Lipids play significant role as structural components of cell membranes. A feature of Sthenoteuthis is a very high content of most polyunsaturated docosahexoenoic fatty acids C . This acid plays an important role in marine animals in maintaining high functional 22:6ω3 activity and adaptive lability of membranes, tissues and whole organism (Shulman and Yakovleva, 1981). The content of this fatty acid in tissues of fast-swimming S. pteropus is higher than in slow-swimming squid Thysanoteuthis rhombus (Yuneva et al., 1994). Also, Sthenoteuthis have high content of cholesterol and its ethers (Abolmasova et al., 1990). At the same time, dry fat-free matter of the squid tissues consists approximately by 85– 90% from proteins, which were found to be the main energy source for energy metabolism. In contrast, many fast moving animals use lipids for this purpose (Shulman et al., 1984; Shulman et al., 1992a). Although on the mobility level as active swimming fishes, which use triacylglycerols as the main sources of energy, squids do not use lipids, but proteins and the products of their catabolism (free amino acids). Analysis of data on oxygen consumption and nitrogen excretion in S. pteropus and S. oualaniensis suggests that all oxygen consumed by squids seems to be utilized for oxidation of proteins. Another remarkable finding is that a considerable proportion of catabo- lized proteins appear to be utilized in anaerobic metabolism since the oxygen consumed is clearly inadequate for its oxidation (Shulman et al., 1992a). It has been shown that hydrocarbons are the main energy sources for mantle muscles work in S. oualaniensis during swimming. Their hydrocarbon metabolism is obligatory aerobic. There is no lactate dehydrogenase, and during periods of anoxy only α-glycero- phosphate and pyruvate is accumulated but not lactate (Hochachka et al., 1975a,b). The role of octopine and lactate dehydrogenases in cephalopod mantle muscle metabolism has been studied in S. oualaniensis by Fields et al. (1976a,b). Activity of peptidhydrolases in muscles after 5 h of autoproteolysis (following the method by Anson at 37°C) is similar in S. pteropus (0.3 µmol g−1 h−1) to 30 species of teleost fishes (0.03–1.75 µmol g−1 h−1) but is higher in the squid Thysanoteuthis rhombus (4.34 µmol g−1 h−1) (Timonina, 1980; L.I. Perova, pers. comm.). 1044 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

The level and distribution of steroid hormones have been investigated in different organs of both sexes of S. pteropus (Nikitina, 1982). The concentration of hydrocortisone in testis of immature, maturing and mature males was respectively 0.4, 0.2 and 0.07 µg g−1, and in nidamental glands of same groups of females 0.163, 0.118 and 0.065 µg g–1. In ovaries of maturing females it was 0.9 mg g–1. The concentration of testosterone has been measured in testis (0.873 µg g−1) and spermatophoric sac (0.653 µg g−1) of mature males, in ovaries of maturing (0.051 µg g−1) and mature (0.560 µg g−1) females and in liver of immature (1.688 µg g−1) and maturing (0.071 µg g−1) squid. The concentration of progesterone has been studied in testis (0.269 µg g−1) and spermatophoric sac (0.049–0.063 µg g−1) of mature males. During the maturation of females the level of progesterone decreased in ovary from 5.70 to 0.0052 µg g−1. In maturing females its concentration was higher in nidamental glands than in ovary (2.50 against 1.30 µg g−1). High concentrations of oestrone were found in the testis (6.625 µg g−1) and spermatophoric sac (2.027 µg g−1) of mature males. In ovaries of mature females its concentration was low (0.497 µg g−1). But in nidamental glands of maturing females the oestrone quantity was extremely high (54.16 µg g−1) and at maturation it decreased to 1.39 µg g−1 (Nikitina, 1982). The catalytic properties and concentration of cholinesterase in the optic ganglia of both species of Sthenoteuthis (among other squid) were analyzed (Grigorjeva, 1987; Epstein, 1992; Rosengart et al., 1994). Unlike shelf-slope Todarodes with one type of cholinesterase, in species of Sthenoteuthis two types of cholinesterases are found with different substrate-inhibitory activity. High activity of Sthenoteuthis cholinesterases in comparison with some other cephalopods testify that these squids have maximal values of behavioral response rates and this was confirmed by observations of their behaviour in natural situations (Nigmatullin, 1972, 1987b; Vovk and Nigmatullin, 1972b; Parfenjuk et al., 1983; Nigmatullin and Parfenjuk, 1986; Bazanov and Parfenjuk, 1986). It is interesting that squid accumulate in their midgut gland substantial quantities of heavy metals usually poisonous for many other animals, particularly copper, iron, silver, zinc and even cadmium. Their concentration may be three orders of magnitude higher than in shallow-water gastropods and bivalves. This situation is the same in S. oualaniensis (for Ag and Zn) or higher (for Cd and Fe) than in Loligo opalescens from Californian coastal waters. This may be connected with copper accumulation as a component of haemocyanin (Martin and Flegal, 1975).

STOCK SIZES AND THE BASELINE OF FISHERY MANAGEMENT STRATEGIES

Studies of squid production and mortality have shown that Sthenoteuthis is a highly productive species. The ratio of annual production to biomass (P/B coefficient) for the adult squids is estimated 8.0–8.5 (Laptikhovsky, 1996). The total instantaneous stock of S. pteropus has been assessed at 4.0–6.5 million t, S. oualaniensis 3–4 million t (Zuyev et al., 1985; Nigmatullin et al., 1991). The minimum and maximum annual production for S. pteropus only have been estimated at 25–45 and 50–90 million t, respectively (Laptikhovsky, 1996). The potential catch of Sthenoteuthis beyond the declared economic zones is estimated 1.0–3.0 million t (Nigmatullin, 1989, 1990; Nigmatullin et al., 1991). Attempts at modeling the population dynamics and development of a biological basis for rational fishery have been made with the Beverton and Holt model (Zuyev et al., 1985). ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1045

These squid are distributed in open areas and are rather scattered; this has impeded their commercial exploitation. The most promising region for a large-scale fishery of S. oualaniensis is the Arabian Sea (Chesalin, 1993, 1994; Gutsal, 1989; Pinchukov, 1994). According to our data the density of squid biomass in this region reaches several tons per km2, a squid stock in this region varies in the range 0.9–1.6 million t and the possible total catch was estimated at 50,000 t (Budnichenko et al., 1993). In the period of winter monsoon a vessel of SRTM type (800–1200 brt) equipped with automated squid-fishing gears, can catch about 6 t of squid per night.

CONCLUSION

Based on results of this review, it is possible to describe general aspects of the biology and life history of Sthenoteuthis spp. Main characteristics of the squid life cycle are shown in Table 3. These squids are abundant oceanic animals, inhabiting open tropical waters of the World Ocean. They possess vast oceanic ranges, which cover all tropical zones and adjacent continental subtropical areas. Quantitative distribution of squids is not uniform; the areas of dense concentrations coincide with dynamically active zones and hydrological fronts. Sthenoteuthis squids make very extensive diurnal vertical migrations ranging from the low mesopelagic to epipelagic layers, therefore they are original integrators of epi- and mesopelagic communities. The squids have a set of special physiological and biochemical adaptations, allowing easy movement between steep gradients in temperature, oxygen content and pressure. Diurnal changes of the ambient temperatures (from 20–30oC at night to 5–15oC at daytime) are important to the optimization of squid metabolism, because of changes in the cost of active metabolism. Probably, this type of behavior enables these squid to maintain relatively high rates of somatic growth after maturation simultaneously with considerable generative metabolism and multiple spawning. They are active nektonic swimmers, voracious predators eating small fishes and invertebrates and, in turn, providing food for large oceanic predators (sharks, tunas, swordfishes, dolphins, sea birds, etc.). Migrations of these squid are connected to migrations of their basic food items (myctophids and other lanternfishes), and through this activity they successfully compete with predatory nektonic fishes. Therefore, squid of genus Sthenoteuthis are key species in tropical oceanic communities. The main flow of matter and energy from zooplankton to higher trophic level passes via these squids. This comparatively young group of animals appeared about 1.5–2 million years ago from the upper Pliocene to late Pleistocene. High fecundity, a short life cycle and high turnover of generations promote successful progressive evolution of these animals. At present there is an active process of sympatric and allopatric speciation within these species, involving adaptation to various environmental conditions, and development of new ecological niches. For example, Sthenoteuthis possesses very complicated intraspecific structures. There is selection within each species for a set of strategies, expressed in opposing tendencies (dwarf and giant forms), and in intermediate (middle-sized forms). In particular, the tendency to gigantism of Sthenoteuthis is expressed in conditions of 1046 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002

)

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Sd ZUYEV ET AL.: WORDWIDE STUDIES ON THE TROPICAL NEKTONIC OCEANIC SQUID, STHENOTEUTHIS 1047 high food supply and at low temperature, whereas the tendency to dwarfism is most obviously expressed in the equatorial zone. Thus, new populations and intraspecific forms are developed, which differ in their size at maturation, life span, places and times of spawning and location of feeding grounds and also in their role in marine communities. They may be a complex of species in status nascendi. A high degree of individual and social behavioral organization is characteristic of Sthenoteuthis squids. This is one of the most important prerequisites for their ecological progress. Due to their high abundance, productivity and food value these squids represent a real resource for fisheries in the nearest future.

ACKNOWLEDGMENTS

We are grateful to many of our friends and colleagues for their help and efforts in working with these squids both at sea and in the laboratory. Special thanks to O. P. Ovcharov, V. N. Nikolsky, V. N. Tyupa, A. M. Amelekhina, G. E. Shulman, G. I. Abolmasova, Yu. S. Belokopytin, A. Ya. Stolbov, A. M. Shchepkina, T. V. Yuneva (IBSS, Sevastopol), A. N. Vovk, R. N. Burukovsky, Yu. M. Froerman, T. S. Dubinina, S. I. Bazanov, A. V. Parfenjuk, R. M. Sabirov, A. S. Shchetinnikov, A. I. Arkhipkin, S. A. Murzov, Yu. A. Alexandronets, V. V. Laptikhovsky, S. E. Prosvirov, A. A. Fetisov, N. M. Toporova, T. A. Simonova (AtlantNIRO, Kaliningrad), M. A. Pinchukov, Yu. V. Korzun, A. G. Ruchkin (YugNIRO, Kerch), S. I. Moiseev, D. K. Gutsal (HYDRONAUT, Sevastopol), Yu. A. Filippova, V. A. Bizikov (VNIRO, Moscow), N. V. Parin, I. V. Nikitina (IO RAN, Moscow) for sampling and biological analysis of the material and great data in their possession. We wish to thank P. Rodhouse and P. Boyle for the opportunity to participate in the CIAC-2000 Symposium and Workshops (July 2000, Aberdeen) and anonymous reviewers for critical reading of the manu- script, valuable comments and great editorial work. This study was supported in part by the Rus- sian Foundation for Basic Research, project No. 00-05-64109 (K.N., Ch.N.).

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ADDRESSES: (G.Z., M.C.) Institute of Biology of the Southern Seas, National Ukrainian Academy of Sciences (IBSS NASU), 2 Nakhimov Ave., Sevastopol 99011, Ukraine. E-mail: . (C.N.) Atlantic Research Institute of Marine Fisheries and Oceanography (AtlantNIRO), 5 Dmitry Donskoy St., Kaliningrad 236000, Russia. E-mail: . (K.N.) Institute of Ocean- ology, Russian Academy of Sciences (IO RAS), 36 Nakhimov Ave., Moscow 117218, Russia. E-mail: .