Morphology of I.'olutomitra alaskana 49

loose circular muscle penetrated by numerous Beneath this epithelium there is a thin layer of longitudinal and oblique muscle fibers, and an longitudinal muscle fibers and a thick layer of innermost layer of longitudinal muscles arranged circular muscle penetrated by few longitudinal in bundles. The anterior surface of the buccal fibers. The outer part of the esophagus is formed cavity is lined by a cuticularized jaw. The left and by groups of circular muscles, connected to the right margins of the jaw overlap ventrally (Fig. proboscis wall by radial muscle fibers. After 2A, arrow), forming an anteriorly-tapering, leaving the proboscis, the esophagus becomes funnel-shaped enrolled tube that can be pro- narrower and has highly muscular walls truded through the mouth. The posteriorly direc- composed of circular muscle. The ventral channel ted lateral flaps of the jaw (Fig. 2B, If) flank the (Fig. 4C, VC) is lined with non-ciliated cuboidal juncture of the broad muscular esophagus (Fig. epithelium in this region of the esophagus. Within 5A, e) and the narrower buccal pouch (Figs. 4A, the cephalic hemocoel, the esophagus is bp), which contains the buccal mass. The buccal extremely long (while completely extended mass is thin and elongate, extending beyond the esophagus length > shell length) and highly posterior margin of the retracted proboscis and convoluted (Figs. 4 A,B), with adjacent loops completely containing the radular sac. connected to each other by muscle fibers to form The radula is long (4.3mm), narrow (430 a permanently rigid structure. The paired pm) and triserial, containing about 450 rows of salivary glands (Fig. 4A, sg) flank the mid- teeth (n = 1). Each row contains a large rachidian esophagus just behind the small valve of Leiblein tooth flanked by minute lateral teeth. The rachi- situated far anterior of the nerve ring (Fig. 4A, dian tooth (Fig. 2) has a complex form with a vL). Ducts from the salivary glands run laterally single, long, median cusp oriented nearly per- alongside the valve of Leiblein, and become pendicularly to the V-shaped and laterally but- embedded in the walls of the esophagus anterior tressed basal plate. This cusp broadens distally to it (Fig. 4 C-F, dsg). to form a posteriorly pointing, V-shaped cutting Torsion occurs in the posterior portion of the edge. Lateral teeth (Figs. 2D, 3A, It) appear to be valve of Leiblein. In the anterior part of the valve, composed of small (=12pm), posteriorly concave the ventral groove, which is continuous with the basal plates that lack projecting cusps. The ventral channel of the esophagus, is situated odontophore is composed of a pair of short ventrally, and is flanked by two zones of longi- cartilages that do not fuse at their anterior ends tudinal muscles (Fig. 4D, Im). These zones of (Fig. 5B, src). These odontophoral cartilages longitudinal muscles run the entire length of the comprise about Zh of the length of the retracted valve. The folds of the epithelium become pro- proboscis, and are attached along their posterior gressively higher, occupying nearly the entire part to a' muscular rod formed of longitudinal lumen of the valve. These folds have cells with fibers. This rod extends well beyond the end of very long cilia that form a cone-like valve that the proboscis (Fig. 4A, mr) and is connected by runs nearly the entire length of the valve of the short odontophoral retractor muscle (Fig. 4A, Leiblein (Fig. 4 E-G, cv). Posteriorly, the paired om) to the esophagus near the nerve ring (Fig. zones of pale-staining mucous cells (Fig. 4E, mc) 4A, nr). appear at both sides of the longitudinal muscles A long (=I. 1 mm) chitinous shield (Fig. 5, cs) zones. Small supportive cells with very long cilia lines the ventral surface of the buccal pouch, are situated between very tall cells with oval basal which extends far beyond the anteriormost limit nuclei. Within a short span of the valve of of the radula and is nearly long as the buccal Leiblein, the mucous cells (Fig. 4E, mc) are mass. The anterior end of this shield, which has shifted to the dorsal side by zones of "squamous" the form of a shallow gutter, is tapered and cells (Fig. 4E-G, sc) with intensively staining projects beyond the buccal mass into the buccal granulated cytoplasm and moderately long cilia. cavity enclosed by the jaw (Fig. 2 C,D). These cells entirely replace the mucous cells. The Longitudinal sections of the proboscis reveal that clockwise rotation of the primary ventral channel this chitinous shield originates from the cuticular is observed in this part of the valve, indicating the lining of the sublingual pouch (Fig. 5, sp). site of torsion. In all, the channel rotates about A small, unpaired accessory salivary gland, 70". which is completely contained within the Posterior to the valve of Leiblein, the eso- retracted proboscis, runs medially beneath the phagus widens and forms several loops prior to sublingual pouch and opens into the buccal cavity passing through the circumesophageal nervous beneath the chitinous shield by very narrow duct ring (Fig. 4A, nr) . Posterior to the nerve ring, the (about 15pm in diameter) (Fig. 5; dasg) . esophagus becomes greatly convoluted and has The morphology of the esophagus is very thick muscular walls. The posteriormost region of similar to that described for other of the mid-esophagus has extremely thick walls [e.g. Peculator hedleyi (Murdoch, formed of circular muscles that greatly reduce its 1909, see Ponder, 1972 1. That portion of the inner diameter (Fig. 4H). In this region, the anterior esophagus lying within the proboscis is short, narrow gland of Leiblein (Figs. 4 A,H, gL) broad and highly muscular, its thick walls lined joins the muscular esophagus. Posterior to this with tall epithelial cells that bear long cilia. juncture, the esophagus becomes much narrower, FIG. 4. Morphology of the,anterior alimentary system of alaskana Dall. A - Organs of the cephalic haemocoel (scale bar - 0.5 mm); B - Organs of the cephalic haemocoel, partially extended (in the same scale as A); C - Transverse section through anterior esophagus (scale bar - 0.1 mm); D-G - Transverse sections through valve of Leiblein from anterior (D) to posterior (G) (scale bar - 0.5 mm); H - Longitudinal section through posterior end of the muscular mid-esophagus (scale bar - 0.5 mm). Abbreviations: bp - buccal pouch; cv - cone valve of cilia; dsg - duct of salivary gland; gL - gland of Leiblein; Im - longitudinal muscles; mc - mucus cells; mme - muscular part of mid-esophagus; mr - muscular rod; nr - circum- esophageal nerve ring; orm - odontophore retractor muscle; pe - posterior esophagus; pr - proboscis; prm - proboscis retractor muscles; sc - "squamous" cells; sg -salivary gland; vc - ventral channel; vL -valve of Leiblein.

PMC. 4. Mop@onomn nepeAHero oTAena nnqeeapu~enb~oficucreMar Volutomitra alaskana Dall. A - opra~b~TynoeuqHoro reMoqenn (M~CIIJT~~H~~nnHnn - 0.5 MM); B - qacTusHo pacnpaane~bleopra~bl TynonuqHoru reMouenn (B TOM xe M~CUIT~~~, KaK A); C - nonepes~blficpes nepenHem nnqemna (M~CUIT~~H~RnnHnn - 0.1 MM);D-G - nonepesHble cpesbl sepes KnanaH JIefi6nefi~aCnepeAM (D) Ha3aA (G) (M~CUIT~~H~SJIMHMn -0.5 MM);H - np0~0Jlb~blfiCpe3 sepe3 3an~~fiKOHW M~CK~~UCTO~~ sacTn nnqesona (~acm~a6~aanuHnn - 0.5 MM). Co~aqe~un:bp - 6yKKanbHa51 Macca; cv - ~o~ycoen~~brfiKnanaH n3 PeCHHYeK; dsg - npOTOK CJIIOHHofi Xene3bl; gL - XeJle3a JIefi6neit~a;lm - 30Ha ITpOAOnbHbIX MYCKYJlbHblX BOJIOKOH; mC - CJIH3HCTble KneTKM; Inme - MyCKynUCTan 'IaCTb CpenHeW nUUeBOAa; mr - MYCKYJI~H~I~~c~e6ene~; nr - OKOJIO~~OTO~HOe HepBHOe KOnbqO; Orm - PeTpaKTOp OAOHTO@O~~;pe - 3aAH~finMUeBOA; pr - ~060~;prm - PeTpaKTOpbl xo6o~a;SC - UseIU)'fisa~ble" KneTKM; Sg - CJIIOHHa5l Xene3a; VC - BeHTpanbHblfi KaHaJl; VL- Xene3a JIeR6nefi~a. Morphology of Volutomitra alaskana 51 and less muscular (Figs. 4 A,H, pe), and leaves through the mouth and placed against the prey. the cephalic hemocoel to join the stomach. With the protraction of the buccal mass, the chitinous shield slides forward along the ventral DISCUSSION floor of the jaw, its tapered tip lodging near the aperture, or perhaps protruding no more than a few pm beyond it. As the aperture of the jaws The morphology of the foregut of Volutomitra and the rachidian teeth are approximately 40pm alaskana agrees in most regards with those of wide, while the gutter of the chitinous shield is Pecutator hedleyi and marginata slightly narrower, we surmise that the function of (Hutton, 1885) [both described by Ponder, this shield is to provide a gutter or groove through 1972 ] as well as with Volutomitra curta (Strebel, which the cusps of the rachidian teeth can move 1908) and Volutomitra fragillima (Watson, 1882) unimpaired prior to making contact with the prey. [described by Arnaud and van Mol, 19791. The The lateral teeth cannot be protruded through presence of long cilia in the valve of Leiblein, the jaw aperture, but serve to maintain the considered a primitive condition by Arnaud and alignment between the rachidian teeth and the van Mol 11979: 291, appears only in V. alaskana gutter of the chitinous shield. As the individual and V. fragillima, suggesting that V. ccuta may rachidian cusps are protruded and make contact not be congeneric with these two species. with their prey, they first pierce, then draw the Ponder 11972: 324 ] reported the buccal walls integument toward the broader bases of the of Peculator hedleyi to be "covered with a thin teeth, and finally cut through the integument chitinous layer" and noted 11972: 330) a "weak- prior to re-entering the aperture of the jaws. The ly cuticulate oral invagination" in Microvoluta overall effect is to slash or make incisions in the australis, but did not identify these structures as prey. Although the mechanism of radular action jaws. Arnaud and van Mol 11979: 29 1 report jaws is analogous to that of a chain-saw, the depth of to occur in V. fragillima, but do not mention them penetration is limited to the length of the median in their description of V. curta. These authors cusps above the rachidian bases (distance be- also confirm the presence of the chitinous shield tween the arrows in Fig. 2D), approximately in the volutomitrid species they studied, referring 20-25 pm. to it as a chitinous shield or plate [Amaud and The minute oral aperture, small size of the van Mol, 1979: 26, 291 or as a thick cuticular radula, as well as radular morphology preclude plate [Ponder, 1972: 324 I. ingestion of all but the smallest particles of solid Although Carriker [I9431 and Wu [I9651 food, and suggest that volutomitrids are fluid have reported a median dorsal sclerite in certain feeders. Muricidae, the presence of a tubular jaw within It is interesting to note that Cancellarioidea, the order has previously been the only other Neogastropods to have tubular reported only in the Cancellarioidea. The jaw of jaw, were inferred to be, suctorial fluid feeders Volutomitridae, which apparently occur in all [Harasewych and Petit, 1982, 1984, 1986; Petit members of the family, bear considerable and Harasewych, 1986 1. Subsequently, Cancel- similarity to those of Cancellarioidea, especially laria cooperii Gabb, 1865, was documented as of members of the subfamily Admetinae [see feeding on the blood of the Pacific electric ray Oliver, 1982: fig. 4; Harasewych, Petit, 1986: fig. Torpedo californica Ayres [O'Sullivan et. al., 6 I. The jaw of Cancellarioidea [e.g. Petit, 19871. Suctorial feeding, also on the blood of Harasewych, 1986: figs. 9,10 ] also overlap vent- fish, has recently been documented for two rally, but differs in having a long, tubular portion genera within the Marginellidae [Bouchet, anteriorly, and in having the lateral flaps greatly 19891, a family considered to be closely related expanded to envelope the buccal musculature, to Volutomitridae [Ponder, 1973 I. and radula-supporting cuticle [Harasewych, Other features of the anterior alimentary Petit, 1982, 1984, 1986 1. The chitinous shield system of Volutomitridae that are consistent with appears to be ubiquitous within and unique to the the hypothesis of suctorial feeding include: (1) Volutornitridae. the anterior migration of the valve of Leiblein, Other than theauggestion that Volutomitridae which has the effect of reducing the volume of "scrape particles of flesh or may even feed on food in the anterior esophagus, thereby body fluids which are sucked into the proboscis enhancing interaction with salivary secretions by the powerful buccal walls" [Ponder, 1972: and minimizing backflow of fluids posterior to it; 338 1, nothing is known of the diet or feeding of (2) a simplified, elongated, and convoluted mid- this family. No identifiable material was found in esophagus where enzymatic digestion may take the foregut of the specimens of V. alaskana place; and (3) a greatly reduced gland of examined in this study, nor are we aware of any Leiblein. In cancellarioideans, the valve of such reports for other species of Volutornitridae. Leiblein is situated near the rear of the buccal Data on the morphology of the jaw, chitinous mass, the mid-esophagus is long, narrow and shield and radula presented in this paper lead us convoluted, and the gland of Leiblein is absent. to propose the following model for their function The prediction of suctorial feeding in Voluto- during feeding. The tip of the jaw is protruded mitridae awaits empirical observation. However, FJG. 5. Longitudinal section through the anterior portion of the proboscis (A, scale bar - 1 mm) and transverse sections through the anterior part of the odontophore (B, scale bar - 0.25 mm) of Volutomitra alaskana.

Position of the duct of the salivary gland passing in the esophageal wall is indicated by interrupted line.

Abbreviations: cs - chitinous shield; dasg - duct of accessory salivary gland; dsg - duct of salivary gland; j - jaw; e - esophagus; prw - proboscis wall; rd - radular diverti- culum; src - subradular cartilages; sp - sublingual pouch.

PMC. 5. npononbsb~iicpessepes nepenHmm qacTb x060Ta (A, MacIIl~a6HaSlJIHHMR '1 MM)M no- nepes~brRcpes sepes nepenHmm sanb O~OH- ~mpa(B, M~cUIT~~H~S~nMHMn - 0.25 MM) Volutomitra alaskana.

Co~paqesun:cs - XHTHHOB~I~~WMTOK; dasg - IlpOTOK AoI~o~HMT~JI~Ho~~cJI~~HHo~~ XWe- sbr; dsg - npoToK cnm~~oRxenesb~; e - IIMWeBOA; j - YeJllocTb; prw - CTeHKa ~060- Ta; rd - pawnnpsoe maranuqe; src - cy6- pamnnptible XPRWM;sp - cy6panynnp~blfi KapMaH.

the striking similarities of the antei-ior alimentary (Y.K.,unpublished observations), which are nor- systems of Volutomitridae and Cancellarioidea mally lost during the course of development. either represent an extraordinary example of morphological convergence, or indicate that a ACKNOWLEDGMENTS reassessment of the svstematic uosition and rank of these higher taxa is warrant&. Parenthetically, we note the absence of an We thank Dr. Boris I. Sirenko (Zoological operculum in all 24 of the specimens of Voluto- Institute) and Dr. Dmitri L. Ivanov (Zoological mitra alaskana that we were able to examine. Museum of Moscow University) for making avai- This suggests that the.operculum of this species lable the specimens used in this study. Special figured by Cernohorsky [1970: pl. 13, figs. 3,4) thanks are due Mrs. Susann Braden for her was either anomalous, or misattributed. Larval assistance with the Scanning Electron Microsopy. shells 2.5 mm in length that were removed from Dr. Alexandr V. Sysoev read and commented egg capsules do have small transparent opercula on a draft of this manuscript.

REFERENCES

ADAMS H., ADAMS A. 1853. The genera, of Recent poda: Prosobranchia) of the southern Indian Ocean. Molluscs; arranged according to their organization Veliger, 22 (1) : 19-3 1. (Mitridae only). London, 1: 167-181. BAYER F. M. 1971. New and unusual mollusks collected by ARNAUD P.M., van MOL J.-J. 1979. Anatomy, ecology and R/V John Elliott Pillsbury and R/V Gerda in the tropical distribution of the Volutidae and Volutomitridae (Gastro- western Atlantic. Bulletin of Man'ne Science, 21 (1): 11 1 - Morphology of Volutomifraalaskana 53

236. Antarctic Survey Bulletin, 57: 15-20. BOSS K.J. 1982. . In: PARKER S.P., Ed. Synopsis PETIT R.E., HARASEWYCH M.G. 1986. New philippine and classification of living organisms. New York, Cancellariidae (: Cancellariacea) , with notes McGraw-Hill Book Co. Vol. 1: 945-1 166; vol. 2: 1092- on the fine structure and function of the nematoglossan 1096. radula. Veliger, 28(4): 436- 443. BOUCHET Ph. 1989. A marginellid gastropod parasitizes PIWBRY H.A., OWSON A.A. 1954. Systems of the Vo- sleeping fishes. Bulletin of Marine Sciences,4S( 1): 76-84. lutidae. Bulletins of American Paleontology, 35( 152) : CARRIKER M.R. 1943. On the structure and function of the 1-36. proboscis in the common oyster drill Urosalpinw cinerea PONDER W.F. 1972. The morphology of some mitriform Say. Journal of Morphology, 73: 441-506. gastropods with special reference to their alimentary and CERNOHORSKY W.O. 1970. Systematics of the families reproductive systems (Neogastropoda) . Malacologia, Mitridae and Volutomitridae (Mollusca: Gastropoda). 11 (2) : 295-342. Bulletin of the Auckland Institute and Museum, 8: 1-1 90. PONDER W.F. 1973. The origin and evolution of the FISCHER P.H. 1880-1887. Manuel de Conchyliologie et de Neogastropoda. Malacologia, 12 (2) : 295-338. la paleontologic cottchyliologique ou histoire naturelle des PONDER W.F., WAREN A. 1988. Appendix. Classification of mollusques vivant et fossiles. Paris, 1369 p. the and Heterostropha - A list of the GRAY J.E. 1857. Guide to the systematic distribution of family-group names and higher taxa. In: PONDER W.F., Mollusca in the British Museum Part 1. London, 230 p. Ed. Prosobranch phylogeny: Proceedings of a Symposium HARASEWYCH M.G., PETIT R.E. 1982. Notes on the held at the 9th International Malacological Congress, morphology of Cancellaria reticulata (Gastropoda: Can- Edinburgh Malacological Review, Supplement, 4: 288- cellariidae) . Nautilus, 96(3): 104- 1 13. 326. HARASEWYCH M.G., PETIT R.E. 1984. Notes on the THIELE H. 1929. Handbuch der systematischen morphology of Oksonella smithi (Gastropoda: Cancel- Weichtierkunde. Jena, 1154 S. lariidae). Nautilus, 98(1): 37-44. TRYON G.W. 1882. Manual of Conchology, Structural and HARASEWYCH M.G., PETIT R.E. 1986. Notes on the Systematic; with Illustrations of the species. Vol. 4, morphology of Admete viridula (Gastropoda: Cancel- Nassidae, Turbinellidae, Volutidae, Mitridae. lariidae). Nautilus, 100(3): 85-91. Philadelphia, (Mitridae) : 106-276, pls. 2, 32-58. O'SULLIVAN J.B., McCONNAUGHEY R.R., HUBER M.E. WEN2 W. 1943. Handbuch der Palaozoologie. Allgemeiner 1987. A blood-sucking snail: the Cooper's nutmeg, Teil und Prosobranchia Berlin, 6 (1) : 120 1- 1506. Cancellaria cooperi Gabb, parasitizes the California WU, S. K. 1965. Comparative functional studies of the electric ray Torpedo californica Ayres. The Biological digestive system of the muricid gastropods Drupa ricina Bulletin, 172: 362-366. and Morula granulata. Malacologia, 3(2) : 21 1-233. OLIVER, P. G. 1982. A new species of Cancellariid gastropod from Antarctica with a description of the radula. British