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Pair Formation and Reproductive Behavior in the Egg Cowry Ovula Ovum (Gastropoda: Ovulidae) in Southern Kyushu, Japan

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Pair Formation and Reproductive Behavior in the Egg Cowry Ovula Ovum (Gastropoda: Ovulidae) in Southern Kyushu, Japan VENUS 69 (1–2): 49–58, 2010 ©Malacological Society of Japan Pair Formation and Reproductive Behavior in the Egg Cowry Ovula ovum (Gastropoda: Ovulidae) in Southern Kyushu, Japan Kei Kawai* Research Center for the Pacific Islands, Kagoshima University, Korimoto 1-21-24, Kagoshima, 890-8580, Japan Abstract: To clarify the relationship between reproductive behavior and pair formation in the egg cowry Ovula ovum (Linnaeus, 1758), field research was carried out from May 2004 to October 2006 at a small cove in Bonotsu, Minami-Satsuma City, Kagoshima, southern Kyushu, Japan, on the East China Sea, which is a subtropical area. Four types of pair formation by egg cowries were observed: (1) two egg cowries lying in close proximity and spending most of their time feeding on soft corals (common pairs); (2) copulating pairs; (3) one egg cowry lying beside brooding egg cowries; and (4) a female producing egg capsules while a male introduces its penis into the female mantle cavity. There was a significant relationship between the number of pairs and reproductive activities. The distances between the paired individuals were significantly shorter during reproductive periods than during non-reproductive periods. The number of observed pairs was also significantly higher during reproductive periods than during non- reproductive periods. During reproductive periods, egg cowries frequently produced transparent belts from the foot using pedal mucus, which might play an important role in locating a mating partner. Of the pair formations observed, 44% were related to reproductive activities. These observations suggest that pair formation in the egg cowry is closely related to reproductive activities. Keywords: brooding, copulation, mucus trail, subtropical Introduction Distribution patterns represent an important aspect of the ecology of organisms (e.g. Begon et al., 1990). Marine gastropods frequently aggregate in response to various environmental and physiological conditions for many functional reasons (Feare, 1971; Hughes, 1986; Little & Kitching, 1996). The sea slug Placida dendritica forms feeding groups to enhance their feeding and growth (Trowbridge, 1991). Because the dogwhelk Nucella lapillus is unable to maintain a foothold during periods of very low water temperature (approximately 5°C) in intertidal areas, aggregation in winter is used as a defense mechanism to reduce the chance of dislodgement by wave action (Largen, 1967). The marine snail Thais haemastoma is able to attack larger prey when it forages in groups (Brown & Richardson, 1987). The dogwhelk Nucella freycineti aggregates in winter for copulation and in spring for breeding (Kawai & Nakao, 1993). The marine snail T. clavigera produces masses of egg capsules on rocks as a result of breeding aggregation, and these masses may protect the eggs from predators (Abe, 1983). The ovulid gastropod Cyphoma gibbosum tends to aggregate by following mucus trails (Gerhart, 1986), a form of aggregation that may be closely related to the search for mates for the purpose of copulation (Ghiselin & Wilson, 1966; Birkeland & Gregory, 1975). * Corresponding author: [email protected] 50 K. Kawai Reproductive behavior has been well studied in marine snails. For example, Littorina littorea has been found to have the ability to discriminate between male and female mucus trails (Erlandsson & Kostylev, 1995) and to exhibit considerably shorter copulation duration in male- male pairs relative to male-female pairs (Saur, 1990). However, L. saxatilis sometimes exhibits maladaptive copulation behavior (male-male or male-juvenile pairing) (Saur, 1990; Johannesson et al., 1995; Erlandsson & Rolán-Alvarez, 1998). Its reproductive behavior is complex (sexual selection and assortative mating) and is determined by size and ecotype (Erlandsson & Rolán- Alvarez, 1998; Hull, 1998; Erlandsson et al., 1999). Ecotype assortative mating in L. saxatilis promotes reproductive barriers, which have been discussed in connection with parallel speciation (Erlandsson et al., 1999; Johannesson, 2001; Hollander et al., 2005; Panova et al., 2006). Aggregation is closely related to reproductive behavior, and the relationship between aggregation distribution and reproductive behavior is well studied in intertidal areas, but there has been far less research on this relationship in other areas, such as the subtidal and bathyal areas, probably because of difficulties in observation. Soft corals are common in shallow tropical and subtropical regions and possess defenses against predators, such as sclerites, nematocysts, and secondary compounds (Fabricius & Alderslade, 2001). Nonetheless, the ovulid gastropods, which are among the predators that can feed on soft corals, have important functions in the soft coral community. The ovulid gastropod Cyphoma gibbosum has been well studied mainly for its prey preferences among soft corals and aggregating distribution patterns (Birkeland & Gregory, 1975; Lasker & Coffroth, 1988; Lasker et al., 1988; Chiappone et al., 2003). The ovulid gastropod Ovula ovum (Linnaeus, 1758), the egg cowry, is well known as a gastropod that is widely distributed among corals, particularly in the West Pacific and Indian Oceans (Abbott & Dance, 1985). Kawai (2009) studied the life history traits such as growth, reproduction, and mortality of O. ovum. Reproductive activities were observed during most of the season except the coldest water temperature period. This species is frequently reported to aggregate (e.g. Coll et al., 1983), and this behavior has been suggested to serve the purpose of male-female couple formation to mate (e.g. Shirai, 1997). However, there has been little research on how reproductive behavior is related to aggregation in this species. In this study, I investigated the reproduction and pair forming behaviors of the egg cowry in southern Kyushu, Japan and discuss the relationship between these behaviors. Materials and Methods This study was carried out from June 2004 to October 2006 at a small cove in Bonotsu (31°15´N, 130°13´E), Minami-Satsuma City, Kagoshima, southern Kyushu, Japan, on the East China Sea, which is a subtropical area. All observations were carried out during the day by scuba diving. The size of the cove is approximately 100 m by 50 m. The cove bottom at the time these observations were made was covered with many soft corals (mainly Sinularia and Lobophytum species). The lowest water temperature was 15°C, recorded on March 24, 2005, and the highest was 30°C, recorded on August 13, 2004. Egg cowries were observed feeding on the soft corals, where their predominant shell length was found to be 7 to 9 cm. Details of the research area, such as the substratum of the cove and water temperature, and life histories of egg cowries in this area, were previously described in Kawai (2009). Detailed observations of pairing behavior were recorded and the number of pairs was counted in the field. The shell lengths of all egg cowries observed were measured using calipers. The distances between each egg cowry and its nearest neighbor was measured from June 2004 to March 2006 when they were found in close proximity. If the distance was less than 50 cm, the pair was classified as a pair formation. If a group of more than 2 egg cowries was found within a 1 m radius, it was counted as one pair formation and the minimum pair-wise distance among them was Reproductive Behavior in the Egg Cowry 51 measured. Reproductive behavior (copulating and brooding) by egg cowries that formed pairs was determined using Kawai (2009). The reproductive behaviors were continuously observed until October 2006. Sexual maturity was defined in terms of the minimum shell length at which reproductive behaviour (copulating and brooding) was observed. To compare numbers of pairs and pair separation distances in reproductive and non- reproductive seasons, monthly average values were used, which are shown in Fig. 2. The values in May and June, 2005, were omitted from the comparison of pair separation distances because there was no pair formation in these two months. To study the relationship between reproductive activities and pair formation, the number of specific reproductive activities (number of brooding females and copulating pairs) (Kawai, 2009) and the number of pairs formed were compared by collecting data on the same research day. In order to study how long pair formation was maintained and whether pairs subsequently participated in reproductive activity (copulation or brooding), observations were conducted every second day from November 15 to December 21, 2005. When paired egg cowries were found, each individual was identified using methods described in Kawai (2009), whether or not egg cowries had been observed previously, and the behavior at each observation time was recorded and continuously checked to determine whether pairs were maintained. Each observation was ended when the pairing ended. However, if after the pairing ended, the egg cowries were easily found and recognized, each behavior continued to be recorded. Results Pair formation and reproductive behavior The number of egg cowries recorded at each observation in the research area (100 m × 50 m) Fig. 1. Photographs showing (A) common pair formation, (B) copulating pair formation, (C) pair formed by brooding females and another egg cowry, and (D) copulating pair of brooding female and male. 52 K. Kawai varied from 4 to 35 (15.84 ± 1.23: mean ± SE), and a total of 163 pairs was observed. The shell lengths of egg cowries observed during the research
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