176 VENUS 68 (3–4), 2010

Spermatophore Transfer in the Dioecious Tidal Snail rhizophorarum (: )

Go Onoda, Tatsujiro Suzuka, Yuka Takeuchi, Toshihiko Konagai and Kiyonori Tomiyama* Department of Earth and Environmental Sciences, Graduate School of Science and Engineering, Kagoshima University, Korimoto, Kagoshima 890-0065, Japan; *[email protected]

Cerithidea rhizophorarum A. Adams, 1855 batillarid species, Batillaria multiformis (Lischke, belonging to the family Potamididae, is a dioecious 1869), co-occur with C. rhizophorarum in this area. tidal snail, occurring throughout the western coasts Observation of copulatory behavior: We of the tropical Pacific Ocean to the northernmost observed copulatory behavior from the middle of part of Honshu Island, Japan. Snail mating can be June to the middle of September. Copulation most categorized as face-to-face mating or shell-mounting frequently started before the lowest tides in daytime. mating (Asami et al., 1998). C. rhizophorarum We observed copulating couples at the lowest tide mates by shell mounting (Wakamatsu & Tomiyama, on June 12, 2006. Whenever we found a pair of C. 2000). Ohtaki et al. (2001) and Takeuchi et al. rhizophorarum in the course of mating on the tidal (2007) observed that C. rhizophorarum shows flat, the male was transferring a spermatophore, and random mating by shell size. When C. thus we recorded the time required for them to rhizophorarum copulates, a male mounts the shell of complete the transfer. a female and inserts its soft body into that of the female (Wakamatsu & Tomiyama, 2000). Even by Results and Discussion dissection of fixed specimens, however, we did not find copulatory organs such as the penis or vagina We obtained direct evidence that C. clearly in males or females. It remained unknown rhizophorarum forms and transfers a spermatophore how the male transfers sperm to the female without to the female partner, in three pairs. Each copulatory organs. In the , sperm transfer spermatophore was spindle-shaped, about 0.5 mm in can be categorized as direct injection of sperm width and 3 mm in length. Each appeared milk- liquid or spermatophore translocation (Tompa, white (Fig. 1). During copulation, the male puts its 1984). It had not been determined whether C. head on the shell of the female. The male adheres rhizophorarum forms a spermatophore. During the strongly to the female shell. Microscope observation field observations on copulatory behavior of this shows the spermatophore to consist of sperm and species, we confirmed spermatophore transfer viscous liquid. The spermatophore slid along the between male-female pairs. In this paper, we report surface of male soft body and entered the female the morphology of spermatophore and the manner body (Fig. 1). A concavity resembling a shallow of spermatophore transfer in C. rhizophorarum. ditch was formed on the surface of the male body for the spermatophore to slide into the female body. Materials and Methods The mechanism by which the male makes the spermatophore slide on the surface of the body is Study site: We conducted field observations of unknown. Muscular peristalsis or ciliary movement copulatory behavior in tidal flats at the mouth of the may contribute to spermatophore sliding. Our Atagogawa River flowing through Kiire-Cho in observation suggests that spermatophore sliding on Kagoshima City (31°23´N, 130°33´E). A small the body surface is necessarily for copulation mangrove forest dominated by Kandelia candel (L.) because C. rhizophorarum lacks a specialized organ Druce and Hibiscus hamabo Sieb. et Zucc covers the to copulate such as the penis or vagina. In the three tidal flats at this site, the northern limit of mangrove pairs, the transfer of the spermatophore took 20, 22 distribution in the West Pacific. Two potamidid and 25 seconds respectively. An earlier study species, Cerithideopsilla djadjariensis (Martin, showed that copulation lasted for 11 to 74 minutes 1899) and C. cingulata (Gmelin, 1791), and one (20 ± 11.0 min: M ± SD; N = 94) (Ohtaki et al., Short Notes 177

Fig. 1. Spermatophore transfer in C. rhizophorarum, which lacks the genital apparatus for copulation. The upper snail is male and the lower is female. A milk-white spindle-shape spermatophore slides from the male to the female across the surface of male soft body.

2001). Interestingly, spermatophore transfer is thorough examinations are necessary to disclose the completed in a short time compared with the sequence of courtship and copulatory behaviors of duration of copulation. Probably the total duration C. rhizophorarum. of copulation, includes the male forming the spermatophore and the female storing it. In this References study, however, we were not able to examine the details of copulatory behavior itself. Further Asami, T., Cowie, R. H. & Ohbayashi, K. 1998. 178 VENUS 68 (3–4), 2010

Evolution of mirror images by sexually asymmetric mating behavior in hermaphroditic フトヘナタリ（腹足綱：フトヘナ snails. The American Naturalist 152: 225–236. タリ科）の精包とその受け渡し Ohtaki, H., Maki, E. & Tomiyama, K. 2001. Seasonal change in the distribution and mating behavior of Cerithidea rhizophorarum 小野田剛・鈴鹿達二郎・武内有加 (Gastropoda: Potamididae). Venus 60: 199– 小長井利彦・冨山清升 210. Takeuchi, M., Ohtaki, H. & Tomiyama, K. 2007. Reproductive behavior of the dioecious tidal フトヘナタリ Cerithidea rhizophorarumが交接の snail Cerithidea rhizophorarum (Gastropoda: 際に♂個体が精包を形成して♀個体に受け渡して Potamididae). American Mallacological Bulletin 23: 81–87. いることがわかり，受け渡し行動を連続写真で示 Tomiyama, K. 1996. Mate choice criteria in a した。精包は乳白色で，大きさは直径約 0.5 mm， protandrous simultaneously hermaphroditic 長さ約 3 mm の紡錘形であった。本種は，交尾の land snail Achatina fulica (Ferussac) (Stylommatophora: Achatinidae). Journal of ための特別な器官をもたず，精包は，♂の頭部の Molluscan Studies 62: 101–111. 軟体部表面を滑走させて♂から♀に受け渡される Tompa, A. S. 1984. Land snails (Stylommatophora). ことがわかった。精包受け渡しに要する時間は 20 In: Tompa, A. S. (ed.), The Mollusca, 7. Reproduction, pp. 47–104. Academic Press, ～25秒程度で，平均 20分間かかっている交接行 London. 動全体からするとごく短い時間であることがわ Wakamatsu, A. & Tomiyama, K. 2000. Seasonal かった。 changes in size distribution of Potamididae (Gastropoda) on mangrove tidal flat. Venus (Japanese Journal of Malacology) 59: 225– 243.

(Accepted November 18, 2009)