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Mating and Morphology of the Copulatory Apparatus In ZOOSYSTEMATICA ROSSICA, 22(2): 153–164 25 DECEMBER 2013 Mating and morphology of the copulatory apparatus in Planorbarius corneus (Linnaeus, 1758) (Gastropoda: Pulmonata) Копуляция и морфология копулятивного аппарата у Planorbarius corneus (Linnaeus, 1758) (Gastropoda: Pulmonata) E.V. SOLDATENKO* & A.A. PETROV Е.В. СОЛДАТЕНКО* И А.А. ПЕТРОВ E.V. Soldatenko, Smolensk State University, 4 Przhevalskiy St, Smolensk 214004, Russia. E-mail: [email protected] *Corresponding author. A.A. Petrov, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg 199034, Russia. E-mail: [email protected] This paper examines mating behaviour and copulatory mechanics (including insemination) in Planorbarius corneus (Linnaeus, 1758) and presents a revised description of its copulatory ap- paratus. The taxonomic position of the genus Planorbarius within the Basommatophora is dis- cussed. The study shows that although P. corneus is similar to Planorbella (Seminolina) duryi (Wetherby, 1879) in the structure of the shell, copulatory apparatus, mating behaviour and even mating positions, they have different mechanisms of intromission. The analysis of mor- phology and mating behaviour does not support a close phylogenetic affinity of Planorbarius to the family Bulinidae P. Fischer et Crosse, 1880 and Planorbidae Rafinesque, 1815. В статье приведено описание репродуктивного поведения и механизма копуляции, включая механизм передачи спермы, и уточнено строение копулятивного аппарата у Planorbarius corneus (Linnaeus, 1758). Обсуждается таксономическое положение рода Planorbarius в пределах Basommatophora. Показано, что, несмотря на сходство этого вида с Planorbella (Seminolina) duryi (Wetherby, 1879) по строению раковины, копулятивного аппарата, репродуктивному поведению и даже позе спаривания, механизмы передачи спермы у них несколько различны. Анализ морфологии и репродуктивного поведения не подтверждает близкое филогенетическое родство Planorbarius с представителями се- мейств Bulinidae P. Fischer et Crosse, 1880 и Planorbidae Rafinesque, 1815. Key words: molluscs, morphology, insemination, mating behaviour, Planorbarius corneus Ключевые слова: моллюски, морфология, механизм передачи спермы, процесс копуля- ции, Planorbarius corneus INTRODUCTION the characters of reproductive organs (e.g.: Baker, 1956; Hudec, 1967; Starobogatov This study continues a series of publica- 1967; Hubendick, 1948, 1978; Burch, 1989; tions on mating behaviour and morphology Nordsieck, 1990) and therefore the study of copulatory organs in freshwater molluscs of reproduction in Planorbarius Dumeril, (Soldatenko & Petrov, 2009b, 2012) and 1806 may help resolve the existing disagree- examines Planorbarius corneus (Linnaeus, ment about the taxonomic position of this 1758), one of the most common and larg- genus. The mating process of Planorbarius est members of Palearctic freshwater snails. is of special interest in this regard, because The taxonomy of the basommatophoran the identification of homologies between pulmonates is to a large extent based on the copulatory structures depends heav- © 2013 Zoological Institute, Russian Academy of Scienсes 154 E. SOLDATENKO & A. PETROV. COPULATORY APPARATUS IN PLANORBARIUS CORNEUS ily on correct interpretation of their func- of the ultrapenis. The copulation has been tional role during copulation. Surprisingly studied in several species of Bulinus (Laram- enough, despite the large body size and bergue, 1939; Wu, 1972; Kuma; 1975; Ru- successful attempts to rear P. corneus in dolph, 1979). The snails mate only unilater- the laboratory (Nekrassow, 1928; Precht, ally with distinct stereotypic behaviour and 1936; Bondesen, 1950; Frömming, 1956; the mating process (when the snails do not Kruglov & Frolenkova, 1980; Berezkina & form copulatory chains) lasts 40–120 min. Starobogatov, 1988; Maksimova, 1995), no The passive partner (“female actor”) usu- one has yet been able to observe the whole ally does not stop feeding or moving during complex of mating behaviour, and a few au- intromission. The male actor may deposit a thors who studied the copulation (Hazay, copulatory plug, whose function is unclear 1881; Maksimova & Yakovleva, 1991) did (Rudolph, 1979). not describe the intromission or observe the The second candidate group, the sub- copulatory structures during insemination. family Helisomatinae, and, specifically, the The morphology of copulatory struc- genus Planorbella Haldeman, 1842, have tures in Planorbarius has been studied by both unilateral and simultaneously recip- several authors (Moquin-Tandon, 1855; rocal mating. The duration of copulation is Baudelot, 1863; Taylor, 1900; Germain, approximately 1–2 hours and mating is pre- 1931; Baker, 1945; Hubendick, 1955; ceded by a complex, stereotypic courtship Starobogatov, 1958; Maksimova and Ya- process. During intromission, the partners kovleva, 1991). The phylogenetic interpre- are not firmly attached to each other and tation of this information eventually led penetration can easily be observed directly. to three different views on the taxonomic The mates use the preputial organ to hold position of this genus. Some authors have the partner; the preputial organ may func- placed Planorbarius in the family Planor- tion as a holdfast and probably also as an bidae Rafinesque, 1815, either within the excitatory organ (Abdel-Malek, 1952; Pace, subfamily Helisomatinae F.C. Baker, 1928 1971; Soldatenko & Petrov, 2012). (Baker, 1928, 1945) or within the subfamily A significant number of species in Planorbinae Rafinesque, 1815 (Hubendick, the third candidate group, the subfamily 1978; Glöer, 2002), while others have in- Planorbinae, are specialised forms with long cluded it in the family Bulinidae Fischer & copulatory stylets. Since Planorbarius does Crosse, 1880 (Starobogatov 1967; Maksi- not have a stylet, it seems reasonable to com- mova, 1995; Starobogatov et al., 2004). pare it with those forms in the Planorbinae Recent molecular phylogenetic analyses that have a small cap-shaped stylet (Planor- (Morgan et al., 2002; Jørgensen et al., 2004; bis Geoffroy, 1767) (Soldatenko & Petrov, Walther et al., 2006; Albrecht et al., 2007) 2009a; Soldatenko & Shatrov, 2013) or lack confirmed the separation of Planorbarius a stylet (Biomphalaria Preston, 1910). The from the other genera of Planorboidea, but copulatory apparatuses in these two gen- could not resolve its phylogenetic position era do not have any accessory structures, unambiguously. such as flagellum, preputial organ, prepu- The three possible candidates for being tial gland or accessory duct (Trigwell et al., close phylogenetic relatives of Planorbarius 1997; Soldatenko & Petrov, 2012). Copula- differ from one another both in the struc- tion in both genera is quite similar and can ture of copulatory organs and in mating be both unilateral and reciprocal. The dura- behaviour, providing enough distinction tion of copulation is about 1–2 hours and for comparison with the same characters in intromission is always preceded by shell cir- Planorbarius. The copulatory apparatus in cling. During insemination, the mates are so the first candidate group, the Bulinidae, has closely attached to each other that penetra- a unique morphology, due to the presence tion cannot be directly observed. © 2013 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 22(2): 153–164 E. SOLDATENKO & A. PETROV. COPULATORY APPARATUS IN PLANORBARIUS CORNEUS 155 The aim of this paper is to describe mat- Behavioural study ing behaviour and copulatory mechanics in Planorbarius corneus (Linnaeus, 1758) and Mature individuals of P. corneus were provide new information about its taxo- placed in containers with the water column nomic status. The paper also examines the of 15 cm in groups of 10–12 individuals. morphology of copulatory organs in the Each month the water was heated with flu- snails killed and fixed during intromission orescent tube lamps to 25–28 °C (Duncan, and supplements these data with the de- 1975; Smith, 1981) and was maintained at scription of musculature of the ejaculatory this temperature for a week to induce mat- duct stained with phalloidin-TRITC for ing. Mating pairs were photographed and confocal microscopy. time intervals were recorded for all stages of the mating process. Some individu- als were marked with coloured nail polish MATERIAL AND METHODS to keep track of the formation of mating Collection sites pairs in the containers. Only an approxi- mate estimate was made for the beginning Sexually mature individuals of Planor- of precopulation, because this species does barius corneus were collected by the senior not show any distinct behavioural tran- co-author in 2010–2013 (June through sition from grazing to the pursuit of the October). Collections were made from the prospective partner. The entire precopula- following localities in the European part of tory phase was observed only for one pair, Russia: after both snails in this pair were isolated 1. Smolensk Province, Demidovskiy in separate containers for 9 days. Time in- District, Smolenskoye Poozerye National tervals for the stages of the mating process Park, town Przhevalskoye, channel Sap- are shown in Table 1. scho-Svjatec (N 55°29´59´´ E 31°49´06´´, Two of the mating pairs were separated altitude 154 m), June 2010, July 2011, July during mating to study the mechanism of 2012, July 2013; insemination. In many freshwater mol- 2. Smolensk, a section of the Dubroven- luscs, including Аnisus vortex (Linnaeus, ka river artificially expanded for
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