Hermania Indistincta Comb. Nov. (Gastropoda: Opisthobranchia: Cephalaspidea) from the Barents Sea – New Species and Genus

ZOOSYSTEMATICA ROSSICA, 24(2): 148–154 25 DECEMBER 2015

Hermania indistincta comb. nov. (Gastropoda: Opisthobranchia: Cephalaspidea) from the Barents Sea – new species and genus for the fauna of the Russian Seas Hermania indistincta comb. nov. (Gastropoda: Opisthobranchia: Cephalaspidea) из Баренцева моря – новый вид и род для фауны морей России

E.M. CHABAN*, I.O. NEKHAEV & P.A. LUBIN

Е.М. ЧАБАН, И.О. НЕХАЕВ, П.А. ЛЮБИН

E.M. Chaban, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg 199034, Russia. E-mail: [email protected] I.O. Nekhaev, Murmansk Marine Biological Institute of Kola Scientific Centre, Russian Academy of Sciences, 17 Vladimirskaya St., Murmansk 183010, Russia. E-mail: [email protected] P.A. Lubin, Research Institute for Problems of Ecology and Mineral Wealth Use of Tatarstan Academy of Sciences, 28 Daurskaya St., Kazan 420087, Russia. E-mail: [email protected]

Hermania indistincta (Ohnheiser et Malaquias, 2013) comb. nov. is recorded for the first time for the Barents Sea and the Russian marine fauna. Based on the morphology of the studied specimens the diagnosis of the genus Hermania Monterosato, 1884 is emended. The taxonomic significance of the spiral shell sculpture in the genus Hermania is discussed. Hermania indistincta (Ohnheiser et Malaquias, 2013) comb. nov. впервые отмечается для Баренцева моря и фауны морей России. На основании морфологии изученных экзем- пляров уточнён диагноз рода Hermania Monterosato, 1884. Обсуждается таксономиче- ское значение спиральной скульптуры раковин видов рода Hermania. Key words: molluscs, new records, Barents Sea, morphology, taxonomy, Cephalaspidea, Philinidae, Hermania indistincta Ключевые слова: моллюски, новые находки, Баренцево море, морфология, таксономия, Cephalaspidea, Philinidae, Hermania indistincta

INTRODUCTION described this species from the Norwegian Sea as Philine indistincta. The taxon Herma- During the expeditions of the Knipo- nia was introduced by Monterosato (1884) vich Polar Research Institute of Marine as a section of the genus Philine Ascanius, Fisheries and Oceanography (PINRO) and 1772 on the basis of a Scaphander-like shell the Murmansk Marine Biological Institute with specific spiral sculpture of Bulla scabra (MMBI) to the Barents Sea several opis- Müller, 1776. Subsequently some malacolo- thobranch molluscs previously unknown gists interpreted the taxonomic rank and for these waters were collected. These status of the name Hermania differently: specimens were identified as Hermania in- as a valid genus (Habe, 1950, 1955; Hori, distincta (Ohnheiser et Malaquias, 2013) 2000; Poppe, 2010) or as a subgenus of comb. nov. Ohnheiser & Malaquias (2013) Philine (Nordsieck, 1972; Martinell, 1981), but mostly as a junior synonym of Philine *Corresponding author. (G.O. Sars, 1878; Pilsbry, 1895; Pruvot-Fol,

1954; Valdés, 2008; Ohnheiser & Malaquias, elongate penial sheath and short convolut- 2013). Recently, Oskars et al. (2015) dem- ed prostate, incurrent duct and ejaculatory onstrated the paraphyly of Philine sensu duct represented by common duct; penial auct. This result returns us to the question papilla developed. of the validity of the taxa which are often listed as synonyms of Philine. Hermania is Hermania indistincta (Ohnheiser one of such taxa. et Malaquias, 2013) comb. nov. In the present paper a philinid species (Figs 1–2) new to the Russian seas is described, its shell sculpture is characterised in greater Philine indistincta Ohnheiser et Malaquias, 2013: detail, and the validity of the genus Herma- 290, 293, figs 10A–H, 11 A–E, 12 A–F. nia is discussed. Material examined. Russia: R/V “Dal- nie Zelentsy”, station 5, Yarnishnaya Bay, MATERIAL AND METHODS 69.130033°N, 36.035233°E, sand, mud, shell rock, 80.5 m depth, 6 specimens, 3 June 2009; All the studied specimens were collect- R/V “Professor Boiko”, station TS1, 69.1744°N, ed during the expeditions of PINRO and 35.1509°E, 44.67 m depth, sand, mud, 3 speci- MMBI on R/V “Dalnie Zelentsy” and R/V mens, 3 June 2008, coll. P.A. Lubin; R/V “Pro- fessor Boiko”, station TS2, 69.183°N, 35.1437°E, “Pr. Boiko” in 2008 and 2009 in the Barents 74 m depth, sand, mud, 1 specimen, 3 June 2008, Sea (Fig. 1). coll. P.A. Lubin. The specimens were fixed first with 4% Description. Shell white, 1.1–3.2 mm formaldehyde and then transferred to 70° high, 0.6–1.6 mm wide, oval-cylindrical, alcohol. The morphology of the shell and narrowed to apex, apex slightly promi- gizzard plates was studied with FEI SEM nent. Aperture with acute angle in upper Quanta-250 scanning electron microscope part, greatly expanded below, with squarish (SEM), the digestive and male copulatory base; aperture height slightly less than shell systems were studied with Opton (Zeiss) height; inner lip forming broad thin callus and Leica DME light microscopes. The on parietal wall. Spiral sculpture consists of studied specimens are kept in the collec- rows of large oval and/or circular deep pits tions of the Zoological Institute, Russian connected to one another by small channels Academy of Sciences. (Figs 2C, D, F, K); rows of wide pits alternate sometimes with rows of narrow pits RESULTS (Fig. 2K); interspaces between rows look like ribs, they carry small and shallow pits Order CEPHALASPIDEA Fischer, 1883 connected to one another, forming second- Family PHILINIDAE Gray, 1850 (1815) order chains. Thin layer of mantle covers shell; spiral sculpture visible through man- Genus Hermania Monterosato, 1884 tle. Foot wide, with small parapodial lobes; Type species: Bulla scabra Müller, 1784, by cephalic shield without any extensions; original designation body uncolored. Diagnosis. Shell scroll-like conical, apex Gizzard elongate cylindrical, surround- blunted; spiral sculpture consists of trans- ed by circular muscle fibers (Fig. 2L). It verse flat ribs divided with chains of deep contains three elongate gizzard plates of pits; chains of shallow pits on the ribs; elon- equal size and shape, with transparent gate gizzard plates equal in size and shape, margins. Inner surface of plates smooth with two longitudinal slits on outer surface; (Fig. 2H); outer surface of each plate with gizzard wall covered with thick sheath of two longitudinal slits (Fig. 2G) and mi- circular muscles, partly reduced at plate crosculpture formed by irregular polygons ends; male copulatory system consists of (Fig. 2I).

Fig. 1. The findings of Hermania indistincta in the Barents Sea.

Male copulatory system consists of 2014: 51). Thompson described the shell elongate penial sheath and thick convo- sculpture of Hermania scabra as “consisting luted prostate (Fig. 2J). Penial sheath con- of spiral rows (approximately 12 per mm) of tains penial papilla and elongated extension tiny oval dots; each dot consists of a raised (bulb). Narrow ejaculatory duct connects oval platform, surrounded by a depressed prostate and penial sheath. “moat”. Where one “moat” joins the next, a Distribution. North and Norwegian tiny kidney-shaped structure is placed, and Seas, 18–20 m, and Southern Barents Sea, the whole effect is very chain-like.” (Thomp- 44–80 m. son, 1976: 140, fig. 75c, as Philine). Both descriptions reflect the real situation but in DISCUSSION different cases, depending on the type of microscope used (light microscope or SEM), This is the first record of Hermania in- angle of view, degree of cleaning of the shell, distincta in Russian waters, and the eastern- and magnification. most record of the species. According to the results of our research, Our research allows us to clarify the the spiral sculpture of the shells of Herma- characteristics of the spiral shell sculpture nia indistincta consists of chains of pits con- for species of the genus Hermania. Herma- nected to one another. The chains of large nia indistincta has external morphology and deep pits alternate with those of small indistinguishable from that of H. scabra, and shallow pits. These double spiral chains the type of Hermania (see Ohnheiser & are clearly visible under the light micro- Malaquias, 2013). Ohnheiser & Malaquias scope (this study: Fig. 2A – for Hermania described the spiral sculpture in both Her- indistincta; Ohnheiser & Malaquias, 2013: mania indistincta (as Philine) and Hermania Fig. 10D – for H. indistincta [as Philine]; scabra (as Philine) as “consisting of trans- Ohnheiser & Malaquias, 2013: Fig. 25E – verse lines of rounded or oval pits connected for Hermania scabra [as Philine]). Ribs with to form chains” (Ohnheiser & Malaquias, chains of large pits are separated by narrow 2013: 290). This description is not suffi- striations with small pits. The double chains cient, as it fits many other species, such as are also visible on a well cleaned shell under Laona quadrata (S.V. Wood, 1839) (Cha- SEM at high magnification (×1000–2000: ban, 2000: 153, as Ossiania Monterosato, Fig. 2K) (Ohnheiser & Malaquias, 2013: 1884; Ohnheiser & Malaquias, 2013: Fig. Fig. 10G – for H. indistincta [as Philine]; 20G, as Philine) or Yokoyamaia ornatissima Fig. 25H – for H. scabra [as Philine]), or at (Yokoyama, 1927) (Chaban & Chernyshev, a viewing angle less than 90° (Ohnheiser &

Fig. 2. Hermania indistincta, light microscope images of the specimen (A, ventral view), male copulatory system (J) and gizzard (L); scanning electron microscope images of the shell (B, ventral view, E, apex), spiral sculpture of the shell (C, D, F, K) and gizzard plates (G, external surface, H, internal surface, I, microsculpture); b – penial bulb, pr – prostate, p sh – penial sheath, sh gr – shallow grooves of the shell. Scale bars: 1 mm (A–B), 500 μm (E, G, H, J, L), 100 μm (C), 50 μm (K, F), 30 μm (D, I).

© 2015 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 24(2): 148–154 152 E. CHABAN ET AL. HERMANIA INDISTINCTA COMB. NOV. FROM THE BARENTS SEA (by Price et al, Praephiline ) (type species of Philine finmarchica spiral striations thick sheath of circular muscles 1:0:1 elongate, lack slits and pores long knobbed prostate; separated ejaculatory duct hammer-shaped Marcus, 1969; & Er. Ev. Chaban & Soldatenko, 2009a, b; Price et al, 2011; Ohnheiser & Malaquias, 2013 (Price et al, 2011; Ohnheiser & Malaquias, Philingwynia ) (type species of Philine monterosati chains of connected pits – 1:1:0:1:1 in form of canoe long prostate; separated ejaculatory duct hammer-shaped Nordsieck, 1972; Bouchet, 1975 (by Chaban & Soldatenko, 2009) or dorsal ornatissima Yokoyamaia Yokoyamaia ) Yokoyamaia (type species of chains of connected pits thick sheath of circular muscles 1:1:0:1:1 elongate, lack slits and pores long prostate; separated ejaculatory duct large conical papilla Chaban & 2014 Chernyshev, (by Thompson, 1976), outer Hermania indistincta external ribs with small shallow chains alternating with deep chains thick sheath of circular muscles, partly reduced at ends of plates 1:1:0:1:1 elongate, with two longitudinal slits on outer surface short prostate, ejaculatory duct not separated hook-shaped, verrucose Ohnheiser& Malaquias, 2013; this study Hermania ) (type species of Hermania scabra ribs with small shallow chains alternating with deep chains thick sheath of circular muscles, partly reduced at ends of plates 1:1:0:1:1 elongate, with two longitudinal slits on outer surface short prostate, ejaculatory duct not separated oval dabble sac with chitinous warts Lemche, 1956; Thompson, 1976; Ohnheiser & Malaquias, 2013 surface (1) of Philine ) (type species Philine aperta long prostate; separated ejaculatory duct hammer-shaped Price et al, 2011; Ohnheiser & Malaquias, 2013 absent three separate muscle strips connected by horny layer 1:0:1 almost triangular plates with two holes on outer features surface ; another its lying on the wall of gizzard is named as Morphological Shell spiral sculpture Gizzard wall Radula Gizzard plates Penis Penial papilla Data from Notes : (1) one surface of the gizzard plate is directed to cavity and named as internal (by Thompson, 1976) or ventral 2013) 2011; Ohnheiser & Malaquias, 2013) surface . and the type species of some genera of Philinidae s. str. 1. Comparative morphology of Hermania indistincta and the type species some genera Philinidae s. str. Table

Malaquias, 2013: Fig. 10F). Only the sim- As a result of comparison of morphology ple chains of large pits are visible on poorly of Hermania scabra and H. indistincta based cleaned shells (Figs 2C) under SEM at low on the literature and our own data, we con- magnification (×500), but traces of the nar- sider Hermania as a valid genus. The previ- row striations could be visible even in this ous diagnosis of Hermania included data on case at high magnification (Figs 2D, F). shell morphology only (Monterosato, 1884: Philine is one of the most morphologi- 147; Nordsieck, 1972: 19). We consider it cally varied genera among cephalaspidean necessary to emend the diagnosis of the ge- opisthobranch molluscs. During the 19th nus (see Results) to include new data ob- and 20th centuries several taxa were sepa- tained by the study of the specimens found rated from Philine and described on the ba- in the Barents Sea. sis of shell morphology as distinct genera In addition to two North Atlantic spe- or subgenera (Monterosato, 1884; Habe, cies Hermania scabra and H. indistincta, 1950; Nordsieck, 1972; Gosliner, 1988), but one more species, Hermania infantilis Habe, these taxa were seldom used subsequent- 1950 from Japan, probably belongs to Her- ly (G.O. Sars, 1878; Pilsbry, 1895; Rud- mania. It was described based on shell mor- é man, 1972; Vald s, 2008; Price et al., 2011; phology (Habe, 1950: 50, Pl. 9, figs 14–16). Ohnheiser & Malaquias, 2013). According Images of the species were also published by to the recent molecular phylogenetic analy- Poppe (2010) from Philippines. The spiral sis of Cephalaspidea (Oskars et al., 2015), sculpture of H. infantilis has spiral ribs and Philinidae s.l. is a polyphyletic group divid- looks like that of H. scabra; also similar are ed into four clades: Philinidae s.str., Laoni- the shapes of the radula with marginal teeth dae Pruvot-Fol, 1954 (reinstated as a valid (1:1:0:1:1) and the fusiform gizzard plates family), “Philinidae” Clade 4 and Philinor- (Habe, 1958). But nothing is known about bidae Oskars, Bouchet et Malaquias, 2015. the morphology of the male copulatory sys- According to this molecular phylogenetic analysis, Philine scabra (type species of tem and about the outer surfaces of the giz- the genus Hermania) belongs to the family zard plates in H. infantilis. Philinidae s.str. The comparison of Herma- nia indistincta and H. scabra with the type ACKNOWLEDGEMENTS species of other genera (valid or listed as We would like to thank Alexey Mirolubov synonyms) of Philinidae s. str. is summa- (Zoological Institute, St Petersburg) for his help rized in Table 1. They are: Philine aperta with the scanning electron microscope images, (Linnaeus, 1767) (type species of Philine As- Pavel Kijashko (Zoological Institute, St Peters- canius, 1772), Yokoyamaia ornatissima (type burg) for useful comments on manuscript, and species of Yokoyamaia Habe, 1950), Philine the anonymous rewievers of the manuscript. monterosati Vayssière, 1875 (type species of Philingwynia Nordsieck, 1972), and Philine REFERENCES finmarchica M. Sars, 1859 (type species of Praephiline Chaban et Soldatenko, 2009). Bouchet Ph. 1975. Opisthobranches de profon- Hermania scabra and H. indistincta have deur de l’Ocean Atlantique. 1. Cephalaspi- a unique set of features (Table 1): spiral dea. Cahiers de biologie marine, 16: 317–365. sculpture with alternating chains of deep Brown H.H. 1933–1934. A study of a tecti- and shallow pits; gizzard plates with paired branch gastropod mollusk, Philine aperta (L.). Transactions of the Royal Society of slits on the outer surfaces; the gizzard wall Edin burgh, 17(1): 179–210. partly reduced at the ends of the plates; a Chaban E.M. 2000. Morphology and systemat- short prostate with the ejaculatory duct not ics of philinids (Opisthobranchia: Philini- separated from the incurrent duct. This set dae) of Northern and Far Eastern seas of of features is not found in any other species Russia. In: Egorova E.N. (Ed.) Mollyuski: of Philinidae s. str. problemy sistematiki, ekologii i filogenii.

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