ISSN 0001-4370, Oceanology, 2007, Vol. 47, No. 4, pp. 531Ð536. © Pleiades Publishing, Inc., 2007. Original Russian Text © A.R. Kosyan, 2007, published in Okeanologiya, 2007, Vol. 47, No. 4, pp. 571Ð576. MARINE BIOLOGY

Morphological Features, Ecology, and Distribution of Poorly Studied Molluscan Genera of the Colinae Subfamily (, ) from the Far Eastern Seas of Russia A. R. Kosyan Severtsov Institute of the Problems of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia e-mail: [email protected] Received January 18, 2007; in final form, February 14, 2007

Abstract—Data on the distribution of six genera of poorly studied buccinids of the Colinae subfamily (Neo- gastropoda, Buccinidae), namely, Röding, 1799; Plicifusus Dall, 1902; Retifusus Dall, 1916; Aulacofusus Dall, 1918; Pararetifusus Kosuge, 1967; and Latisipo Dall, 1916, are presented. These mollusks are widely spread in the North Pacific region dwelling predominantly over loose sediments in a wide range of sea depths. Based on the morphology and contents of their digestive tracts, it is assumed that the representatives of the gen- era studied are predators with diverse diets. It is supposed that the increase in the dwelling depths had no sig- nificant influence on the feeding ecology of the studied. Meanwhile, the lower abundance of preys at greater depths caused the lower population densities and modifications in the proboscis structure of selected taxa. DOI: 10.1134/S0001437007040108

INTRODUCTION allowed us to reach preliminary conclusions about the ecological features of selected poorly studied species. The most diverse group of buccinids in the waters of Russia are the representatives of the Colinae subfam- ily—their share is 16 of 34 genera and 116 of 263 buc- MATERIALS AND METHODS cinid species [5]. The best-studied representative of the In this study, we used the materials of the Zoological Colinae is the numerous Röding, 1798 Institute of the Russian Academy of Sciences (ZIN), the [1, 3]; other species have no commercial value; there- Shirshov Institute of Oceanology of the Russian Academy fore, they didn’t attract the attention of the specialists. of Sciences (SIO), the Zoological Museum of Moscow Among these species, the highest species diversity is State University (ZM MSU), the British of Natural His- characteristic of the Colus Röding, 1799; Plicifusus Dall, tory Museum (BNHM), as well as the materials from a 1902; Retifusus Dall, 1916; Aulacofusus Dall, 1918; private collection kindly presented by D.O. Alekseev Pararetifusus Kosuge, 1967; and Latisipo Dall, 1916 (VNIRO). In all, about 450 specimens representing genera. The bulk of the species of these genera are 33 molluscan species were examined (Table 1). noted in the North Pacific, in particular, in the Russian In the mollusks studied, we measured the shell waters of the Bering Sea, the Sea of Okhotsk, and the length and the lengths of the last whorl and the aperture. Sea of Japan. A series of previously published reviews The morphology of the soft body was studied with the based mostly on the initial identifications of the species use of a tested preparation technique [4]. The exposed contains data about the morphology of the shells and radulae were cleaned of muscles and kept in a solution radulae [2, 8Ð10, 15, 18Ð20], as well as selected infor- of liquid bleach (NaOCl) up to complete removal of the mation about their anatomy [12, 13]. Meanwhile, no soft tissues. Then, they were dried in the open air, information about the ecology of this group is avail- coated with gold, and examined with the help of a Tes- able. can scanning electron microscope. For 30 species (more than 200 specimens), the In the course of an examination of museum collec- stomach and gut contents were studied. tions, we reviewed numerous mollusk samples of the Colus, Plicifusus, Retifusus, Aulacofusus, Parareti- fusus, and Latisipo genera from the region of the Ber- RESULTS AND DISCUSSION ing, Chukchi, and East Siberian seas; the Sea of Japan; Distribution. The genera under consideration fea- the Sea of Okhotsk; and off the Kuril Islands and KurilÐ ture wide habitats in the boreal and higher boreal zones Kamchatka. The external morphology, anatomy, and of the Pacific Ocean. Most of the genera dwell in the the gut contents of the mollusks were studied, which regions within 40°–70° N and 130° EÐ160° W (Table 1).

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Table 1. Geographical distribution and range of dwelling depths of the considered Pacific species and genera of the Colinae subfamily

Genus Geographical distribution Range of dwell- (total number Species studied and their dwelling depths of the representatives ing depths, m of species) of the genus studied

Colus Röding, C. islandicus (Mohr, 1786), 5Ð3006 m Bering Sea, Kamchatka, Sea 5Ð3006 1799 (18 species) C. minor (Dall, 1925), 46Ð260 m of Okhotsk, Pacific coasts of C. kujianus Tiba, 1973, 105Ð2000 m Japan

Aulacofusus A. brevicauda (Deshayes, 1832), 21Ð1000 m Laptev Sea, Bering Sea, Sea 16Ð1000 Dall, A. herendeeni (Dall, 1899), 16Ð920 m of Okhotsk, Kamchatka, 1918 (6 species) A. ombronius (Dall, 1919), 35Ð152 m Kuril Islands A. periscelidus (Dall, 1891), 50Ð200 m

Latisipho Dall, L. hypolispus (Dall, 1891), 40Ð930 m Bering Sea, Sea of Okhotsk, 2Ð1112 1916 (2 species) L. hallii (Dall, 1873), 2Ð1112 m Kamchatka, Alaska

Plicifusus Dall, P. kroeyeri (M¿ller, 1842), 0Ð225 m Circumpolar, Sea of 0Ð2000 1902 (16 species) P. plicatus (A. Adams, 1863), 10Ð287 m Okhotsk, eastern coast of P. croceus (Dall, 1907), 25Ð2000 m Kamchatka, Kuril Islands, P. scissuratus (Dall, 1918), 49Ð400 m* northern part of the Sea of P. elaeodes (Dall, 1907), 80Ð130 m Japan, Pacific coasts of Ja- P. rhyssus (Dall, 1907), 52Ð1530 m pan P. hastarius Tiba, 1980, 7Ð18 m P. bambusus Tiba, 1980, unknown P. olivaceus (Aurivillius, 1885), 103Ð318 m P. oceanodromae (Dall, 1919), 129Ð180 m P. obtusatus Golikov in Golikov et Scarlato, 1985, 53Ð142 m P. torquatus (Petrov, 1982), 142Ð500 m

Retifiisus Dall, R. jessoensis (Schrenck, 1863), 7Ð300 m East Siberian Sea, Chukchi 7Ð920 1916 (9 species) R. frielei (Dall, 1891), 285Ð920 m Sea, Bering Sea, Sea of R. virens (Dall, 1877), 18-430 m Okhotsk, Sea of Japan, Kuril R. yanamii (Yokoyama, 1926), 40Ð100 m Islands, Kamchatka R. roseus (Dall, 1877), 42Ð400 m R. similis (Golikov et Gulbin, 1977), 50Ð300 m R. attenuates (Golikov et Gulbin, 1977), 150Ð414 m R. iturupus (Golikov et Sirenko, 1998), 660Ð920 m R. laticingulatus Golikov et Gulbin, 1977, 129Ð188 m

Pararetifiisus P. tenuis (Okutani, 1966), 400−1500 m Bering Sea, Sea of Okhotsk, 130Ð1500 Kosuge, 1967 P. kantori Kosyan, 2006, 135Ð1400 m Sea of Japan, Kamchatka (3 species) P. kosugei Kosyan, 2006, 130Ð250 m

Note: * The species is first recorded in the fauna of Russia.

Over the vertical, mollusks are encountered over a wide capable of covering vast areas of the seafloor, the find- depth range from 0 to 3000 m (Table 1). The mollusks ings of the representatives of the Colinae genera con- inhabit loose sediments such as broken coquina, peb- sidered are rare, especially as compared to other Far bles, sands, and silts. Despite the application of a trawl Eastern buccinids [6].

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MORPHOLOGICAL FEATURES, ECOLOGY, AND DISTRIBUTION 533

A K

H

D

G

J

B E C F I

Fig. 1. Diversity of the shells of Colinae: A—, B—Mohnia mohnii, C—Pararetifusus tenuis, D—Latisipho hallii, E—Latisipho hypolispus, F—Pararetifusus kantori, G—Aulacofusus brevicauda, H—Retifusus jessoensis, I—Plicifusus kroeyeri, J—Retifusus attenuatus, K—Plicifusus rhyssus. The length of the scale bar is 1 cm.

Morphological features. The shells of the genera type found in species such as R. jessoensis (Schrenk, studied are diverse (Table 1) and extremely variable 1863), R. virens (Dall, 1877), R. yanamii (Yokoyama, within the same genus. Their lengths vary from 7 to 1926), and R. okhotskanus (Tiba, 1980) is characterized 104 mm. A characteristic anatomic feature is the exist- by a central tooth with five or six minor cusps arranged ence of a proboscis, at the end of which the mouth in a fanlike manner. The second type of radular central opening is located. Inside the proboscis, there is a rad- teeth characteristic of R. similis, R. roseus, R. iturupus, ula with a tooth set typical of the Buccinidae: one cen- and R. attenuatus, as well as of all the Pararetifusus tral and two lateral teeth (Fig. 2). The lateral teeth usu- representatives, have three central cusps of equal sizes. ally have three cusps each, though sometimes their The characteristic morphological features of the number may be as great as five. The individuals of the shells and soft bodies of the genera studied are summa- Latisipho, Plicifusus, Colus, and Aulacofusus genera rized in Table 2. feature lateral teeth with smaller median cusps, while The food clots from the stomachs of the mollusks of those of the Retifusus and Pararetifusus genera have all the Plicifusus and Colus genera, along with sand and cusps of equal sizes. The central teeth of the Latisipho, silt particles, also contained nondigested foraminifers, Plicifusus, Colus, and Aulacofusus have three cusps small intact Trochidae, and flat worms of the Kalypto- each; in so doing, the size of the median cusps is sub- rhynchia suborder, as well as fragments of rays of brit- jected to a strong intraspecific variability. For the genus tle stars, bristles of polychaets, and limbs of amphi- Retifusus, two types of central teeth are noted. The first pods. This kind of diet was also described for selected

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A 500 µm C 250 µm E 250 µm

B 500 µm D 50 µm F 100 µm

Fig. 2. Types of the radulae of Colinae: A—Colus islandicus, B—Aulacofusus brevicauda, C—Latisipho hypolispus, D—Parareti- fusus tenuis, E—Plicifusus kroeyeri, F—Retifusus jessoensis.

Pacific species of the genus Neptunea [17]. Most prob- Retifusus jessoensis, R. virens, R. yanamii, and R. frie- ably, the mollusks studied are predators. lei, which are supplied with numerous fanlike sharp minor cusps, most probably are for scraping off soft tis- The suggestion of their predatory character is sues of their prey. proved by the morphological data. For example, for the mollusks of the Colus, Plicifusus, Latisipho, Retifusus, The salivary glands of most of the genera studied are and Pararetifusus genera, the presence of a retractable large and, as in the representatives of the genus Neptu- proboscis, which is typical of predatory gastropods nea, are capable of producing poison [7, 11, 16]. This such as, for example, Neptunea, points to a similar supposition is confirmed by the fact that, among the feeding strategy. An extremely long proboscis that is amphipods that were found in the stomach of Colus jef- significantly greater than the shell length is characteris- freysianus, in addition to small individuals, large indi- tic of all the species of the genus Aulacofusus and of viduals were found, and, in the stomach of a small two species of the genus Colus, namely, C. garacilis P.kroeyeri specimen, fragments of rays of brittle stars (Da Costa, 1778) and C. jeffreysianus (Fischer, 1868) were encountered. The venomous secretion of the sali- (original observations of the author). Amphipods of the vary glands may help to catch prey that large and active. family Corophiidae found in the stomachs of a speci- The presence of poison is also implied by the unusual men of Colus jeffreysianus indicate that these mollusks structure of the salivary ducts of Retifusus roseus and are specialized in feeding on burrowing such as Pararetifusus kosugei. The existence of widenings (sal- bivalves and amphipods. ivary sacs) that seem to serve as temporary reservoirs The structure of the radulae of the representatives of for a great amount of venomous saliva, together with the Plicifusus, Latisipho, Colus, and Aulacofusus gen- the location of the openings of the salivary ducts at the era is similar to that described for Neptunea and Bucci- termination of the proboscis rather than in the rear part num L., 1758, which agrees with the similar diets of of the buccal cavity (as is characteristic of most of the these species. Meanwhile, the radulae of Pararetifusus buccinides studied), allows these mollusks to inject par- and Retifusus are significantly different. The large alyzing poison and then consume the immobilized prey. three-dent teeth of the radulae of Pararetifusus and A similar arrangement of the salivary duct openings most of the species of the Retifusus genus are meant, and the same feeding type were also noted for most probably, for holding their prey and tearing off muricatum (Born, 1778) (, Turbinel- large portions of it. The central teeth of the radulae of lidae) [14].

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Table 2. Morphological features of the Colinae genera studied Genus Colus Aulacofusus Latisipho Plicifusus Retifusus Pararetifusus Feature Range of the 46Ð104 26Ð54 41Ð25 34Ð82 7Ð25 13Ð15 shell size, mm Axial sculpture Incremental Incremental Incremental Axial folds Axial folds Incremental lines of the shell lines lines lines (10Ð20 on the (up to 15 over the last whorl) last whorl) Number of spiral Number of ribs 6Ð16 large spiral 20Ð30 small spi- 30Ð60 small 5Ð18 large spiral 5Ð6 spiral ribs ribs on the penul- strongly varies ribs ral ribs or up to 5 spiral ribs ribs spaced very high timate whorl irregularly ar- ranged ridges Central tooth of 3 cusps, the mid- 3 cusps, the mid- 3 cusps, the mid- 3 cusps, the mid- 5Ð6 small 3 large identical the radula dle of which is dle of which a dle of which is dle of which is or 3 large cusps cusps either longer or bit longer than longer or shorter longer or shorter shorter than the the others than the others than the others others Lateral teeth of 3 cusps, the mid- 3 cusps, the mid- 3 cusps, the mid- 3 cusps, the mid- 3 identical cusps 3 approximately the radula dle of which is dle of which is dle of which is dle of which is identical cusps the smallest the smallest the smallest the smallest Proboscis Short or long Long rolled up Short Short Short Short in rings in the rhynchocoel Salivary ducts Thick, twisted Thick, twisted, Thin, twisted Thin, twisted Thick, straight, Thick, straight, with a layer of may form salivary may form salivary longitudinal sacs sacs muscles in the wall

Thus, we can conclude that the mollusks of the gen- 4. Yu. I. Kantor, Gasteropod Mollusks of the World Ocean: era studied dwell within a significant depth range from Volutopsiinae Subfamily (Nauka, Moscow, 1990) the sublittoral to the bathyal zones and prefer loose sed- [in Russian]. iments; they are predators with a diverse diet. No 5. Yu. I. Kantor and A. V. Sysoev, Catalogue of Mollusks of changes in the feeding strategy were observed over the Russia and Adjacent Countries (KMK, Moscow, 2005) entire vertical range of dwelling depths [in Russian]. 6. A. I. Piskunov, “Summertime Distribution of the Mass Species of Gastropod Mollusks of the Buccinidae Fam- ACKNOWLEDGMENTS ily off the Eastern Sakhalin,” Studies in the Fish Biology and Fishery Oceanography, No. 10, 52Ð59 (1979). The author thanks Dr. I.N. Marin, Prof. Yu.I. Kantor (Severtsov Institute of the Problems of Ecology and 7. U. Anthoni and L. Bohlin, C. Larsen, P. Nielsen, N. H. Nielsen, and C. Christophersen, “The Toxin Tetra- Evolution, Russian Academy of Sciences), and mine from the ‘Edible’ Neptunea antique,” Toxi- Dr. E.M. Krylova (Shirshov Institute of Oceanology of con 27 (7), 717Ð723 (1989). the Russian Academy of Sciences) for helpful critical 8. P. Bouchet and A. Waren, “Revision of the Northeast remarks. This study was supported by the INTAS Sci- Atlantic Bathyal and Abyssal Neogastropoda Excluding entific Foundation (project no. 04-83-3120). Turridae (, Gastropoda),” Bollettino Malaco- logico, Supplemento 1, (1985). REFERENCES 9. A. N. Golikov, B. I. Sirenko, V. V. Gulbin, and E. M. Chaban, “Checklist of Shell-Bearing Gastropods 1. A. N. Golikov, “Gastropod Mollusks of the Neptunea of the Northwestern Pacific,” Ruthenica 11 (2), 153Ð174 (Bolten) Genus,” in Fauna of the USSR. Mollusks (2001). (Nauka, Leningrad, 1963), Vol. 5, Issue 1 [in Russian]. 10. S. Higo, P. Callomon, and Y. Goto, Catalogue and Bibli- 2. A. N. Golikov and B. I. Sirenko, “Prosobranchia Gastro- ography of the Marine Shell-Bearing Mollusca of Japan pod Mollusks of the Continental Slope of the Kuril (Elle Scientific Publications, Osaka, 1999). Island Range,” Ruthenica 8 (2), 91Ð135 (1998). 11. Y. Kawashima, Y. Nagashima, and K. Shiomi, “Toxicity 3. V. N. Goryachev, Gasteropod Mollusks of the Neptunea and Tetramine Contents of Salivary Glands from Carniv- Röding Genus of the Bering Sea (Nauka, Moscow, 1978) orous Gastropods,” Shokuhin Eiseigaku Zasshi 43 (6), [in Russian]. 385Ð388 (2002).

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12. A. R. Kosyan, “Anatomy and Taxonomic Composition 16. A. J. Power B. F. Keegan, and K. Nolan, “The Seasonal- of the Genus Latisipho Dall (Gastropoda: Buccinidae) ity and Role of the Neurotoxin Tetramine in the Salivary from the Russian Waters,” Ruthenica 16 (1-2), 17Ð42 Glands of the Red Whelk Neptunea antiqua (L.),” Toxi- (2006). con 40 (4), 419Ð425 (2002). 13. A. R. Kosyan, “Two New Species of the Genus Parareti- 17. R. Shimek, “The Diets of Alaskan Neptunea,” Veliger 26 fusus Kosuge, 1967 (Buccinidae: Colinae), with Notes (4), 274Ð181 (1984). on the Morphology of Pararetifusus tenuis (Okutani, 18. R. Tiba and S. Kosuge, North Pacific Shells. 7. Genus 1966),” Ruthenica 16 (1-2), 5Ð15 (2006). Plicifusus Dall, 1902 (Occasional Publication of the Institute of Malacology of Tokyo, 1980). 14. A. I. Medinskaya, M. G. Harasewych, and Yu. I. Kantor, 19. R. Tiba and S. Kosuge, North Pacific Shells. 8. Genus “On the Anatomy of Vasum muricatum (Born, 1778) Colus Röding, 1798 (Occasional Publication of the Insti- (Neogastropoda, ),” Ruthenica 5 (2), 131Ð tute of Malacology of Tokyo, 1981). 138 (1996). 20. R. Tiba and S. Kosuge, North Pacific Shells. 18. Genus 15. T. Okutani, Marine mollusks of Japan (Tokai University Mohnia Friele, 1877 (Occasional Publication of the Press, 2000). Institute of Malacology of Tokyo, 1992).

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