VENUS 69 (1–2): 49–58, 2010 ©Malacological Society of Japan

Pair Formation and Reproductive Behavior in the Egg Cowry ovum (: ) 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 (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 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 period ranged from 0.96 cm to 9.8 cm. Most pairs (n = 158; 96.9%) were formed by mature-sized egg cowries (shell length > 7 cm, Fig. 3; Kawai, 2009) – the exceptions being 4 pairs observed in July 2005, and one in August 2005. Four types of pair formation by egg cowries were observed. Common pairs were identified as two egg cowries laying in close proximity that did not show any reproductive activities (n = 116; 71.2%) (Fig. 1A). These pairs spent most of their time feeding on soft corals. Sex of the common pairs was not determined, as identification of the sex was difficult under natural conditions. This type was also occasionally formed by more than two egg cowries (a maximum of 5 egg cowries was observed). Copulating pairs were observed on rocks or soft corals (n = 28; 17.2%) (Fig. 1B).

Fig. 2. Average number of pairs at each observation from June 2004 through March 2006 (A), and average distance between paired individuals (B). Each monthly value was calculated as the average value using each observation. If there were no pair formation in a month, the average distance would be 50 cm (May and June 2005). Standard Error was calculated when the number of research days per month was more than 3. Horizontal bar in each figure indicates the reproductive period from which data referred to in Kawai (2009) were taken. Reproductive Behavior in the Egg Cowry 53

Thirty-eight brooding egg cowries were observed during the research period and eighteen of these were involved in 2 types of pair formation. In the first case, a second egg cowry was present beside the brooding egg cowry (n = 10; 6.1%) (Fig. 1C). In the second case, in which females produced egg capsules, males were seen to have introduced their penises into the female mantle cavities (n = 8; 4.9%) (Fig. 1D). The ratio of lone-brooding females (n = 20) to the total number of brooding females (n = 38) was not significantly different from the ratio of paired brooding females (n = 18) to total brooding females (Binomial test, P > 0.05). Pair formation in egg cowries was observed from June 2004 through February 2005, April 2005, and from July 2005 through March 2006 (Fig. 2A). Reproductive activities were observed from July 2004 through February 2005, and from September 2005 through January 2006 (Kawai, 2009). The median number of pairs observed in the reproductive period (n = 17) was significantly higher than that observed in the non-reproductive period (n = 5) (Mann-Whitney U-test, P < 0.01) (Fig. 3A). The monthly average distance between each individual in a pair was less than approximately 10 cm during the reproductive period; however, the distance was approximately 30 cm during most of the non-reproductive period (Fig. 2B), and the median distance in the reproductive period (n = 17) was significantly shorter than that in the non-reproductive period (n = 3) (Mann-Whitney U-test, P < 0.05) (Fig. 3B). During the reproductive periods, egg cowries frequently produced a transparent belt, called the ‘mucus belt’, from the foot using pedal mucus. The widths and lengths of the mucus belts were approximately 4 to 5 cm and between 1 to 2 and 5 to 6 m. However, the exact length could not be measured since, due to unknown reasons, these belts were frequently fragmented into smaller segments. The mucus belt was not fixed to the substratum and moved freely in the water current. After a while, sand particles adhered to the mucus belt, which subsequently became a narrow string. There were no data obtainable on which sex produced the mucus belts. There was a significant relationship between the number of reproductive activities (number of brooding females and copulating pairs) and the number of pair formations (y = 0.65 x – 0.29: n = 51, r2 = 0.58, P < 0.001) (Fig. 4). Forty-three copulating pairs were observed from June 2004 through October 2006. Copulating egg cowries were measured from approximately 7 cm to 9.5 cm for each sex (Fig. 5), which is the size at sexual maturity and near the observed maximum size in this area, respectively. The relationship between the sizes of copulating males and females was not significant (n = 43, r2 = 0.02, P > 0.05). The ratio (female shell length / male shell length) was 1.02 ± 0.07.

Fig. 3. Average number (± SE) of pairs in reproductive and non-reproductive periods (A) and average distance (± SE) between paired individuals in reproductive and non-reproductive periods (B). 54 K. Kawai

Fig. 4. Relationship between observed number of pairs and reproductive activity (number of brooding individuals and copulating pairs) at each observation.

Fig. 5. Relationship between female shell length (cm) and male shell length (cm) in copulating pairs.

Behavior after pair formation The behavior of 16 pairs was observed from November 15 to December 21 (Table 1). Twelve common pairs (Fig. 1A) were observed at the start of this period. Three pairs remained together until the production of egg capsules was complete, and two females among the three pairs began brooding again after the female had separated from the male. The average time of pair retention was approximately 5 days. However, the other nine pairs separated before participating in reproductive activities, and the average time for the pair to break up was less than 2 days. Four Reproductive Behavior in the Egg Cowry 55

Table 1. Behavior of first and last observed and number of observed pairs for each behavior. First Observed Behavior Common Pair Copulation Last Observed Behavior Separated Brooding Separated Brooding Number of Observed Pairs 9 3 4 0 copulating pairs were observed at the first observation time during this period (Table 1). These pairs did not retain copulating behavior at the next observation (2 days later), but the individuals in these pairs remained in close proximity to one another. These copulating pairs finally separated after 4 days, and brooding behaviors by these females were not observed at this point. However, since observations were not conducted until the end of the reproductive period (January 2006), it is possible that the females may actually have brooded after the observation because observations on common pairs (Table 1) indicated that after pair formation ended, the female alone could produce egg capsules. This observation suggests that 44% [= (4 + 3)/16] of the observed pairs participated in reproductive activities (copulation and brooding).

Discussion

Although the average number of egg cowries recorded during each observation period in the research area (100 m × 50 m) was 15.84, only a few egg cowries were observed during scuba diving in several areas near the research area and in the region to the south of the research area (Yoron Island and Amami Island, Japan and Cebu, ) (Kawai K., unpublished data). This observation suggests that the density of egg cowries generally was very low and that the encounter rate with a mating partner might be correspondingly very low. To facilitate mate location, mucus trails are frequently laid by ovulid gastropods (Gerhart, 1986). Egg cowries produce mucus belts using pedal mucus in this area, and mucus belts were frequently observed during the reproductive period. Therefore, the mucus belts of egg cowries may play a significant role on the pairing of this species. Mate discrimination has previously been observed in marine snails. L. littorea has the ability to discriminate between male and female mucus trails (Erlandsson & Kostylev, 1995) and exhibits considerably shorter copulation durations in male-male pairs relative to those of male-female pairs (Saur, 1990). My observations suggest that once an egg cowry has found another egg cowry, it may remain beside its partner. Nine pairs (56%) did not show any reproductive activities, and the average time of pair retention was less than 2 days (Table 1). However, seven pairs (44%) showed reproductive activities, and they maintained pair formation for 4 to 5 days. This suggests that the maturation levels of individuals might influence the duration of pair retention. The paired individuals existed in close proximity and usually fed on soft corals. The distance between them was less than 10 cm during the reproductive period (Fig. 2B), although paired individuals were not continuously attached to each other. Consequently, egg cowries might assess the maturity and/or sex of potential mating partners when they are side by side. To retain pair status and to recognize each other, paired individuals might sometimes come into contact with each other or produce certain chemicals or pedal mucus for identifying each other. There are many factors that affect mate choice, of which size is one of the important one, because males prefer to mate with large, often more fecund females (Ridley, 1983; Crespi, 1989). Intertidal snails frequently exhibit size-assortative mating (Erlandsson & Rolán-Alvarez, 1998; Hull, 1998; Rolán-Alvarez et al., 1999; Cardoso et al., 2007). However, egg cowries did not exhibit size-assortative mating, indicating that the mating of egg cowries is random relative to size (Fig. 5). Since mucus trails are very important for egg cowries to locate a partner and the rate of pedal mucus production in relation to total energy consumption is generally very high in marine 56 K. Kawai snails [e.g. 23% in Ilyanassa obselata (Edwards & Welsh, 1982), 23 to 29% in Haliotis tuberculata (Peck et al., 1987), and 31% in Patella vulgata (Davies et al., 1990)], the cost of producing mucus in egg cowries might be correspondingly very high. Therefore, since locating a partner is difficult and incurs high energy costs for egg cowries, it may often prove advantageous to mate with any mature individuals encountered, rather than optimal individuals. This could be one of the reasons that egg cowries exhibit random mating. Although pairing success was not high (44%), pair formations are still thought to be closely related to reproductive activities. In this study, 56% of pairs were dissolved before reproduction, which could be a result of maladaptive pairing (e.g. male-male or male-immature female). As described above, egg cowries are highly likely to discriminate between the sexes and maturities of potential partners they encounter. The seminal receptacle and use of stored sperm is widely found in gastropods (e.g. Baur, 1998; Buckland-Nicks et al., 1999). It is also highly likely that female egg cowries are able to store sperm for a time. In fact, females produced egg capsules alone in a lapse after copulation in my observations of pair formation (Table 1), and half of the brooding females produced egg capsules alone in the field observations from June 2004 through March 2006. If females were able to store sperm, females may have copulated with multiple partners and used the sperm of a specific male (e.g. first or last male) for fertilization. Male copulating behavior with brooding females (Fig. 1D) might also represent mate guarding behavior. To determine the details of the mating system in the egg cowry, we will consequently need further field observations and experiments in the future. The observations made during this study found the following: (1) there was a significant relationship between the number of pairs and reproductive activities (Fig. 4); (2) the number of paired individuals was significantly higher during the reproductive periods than during the non- reproductive periods (Fig. 3A); (3) the distances between paired individuals were significantly shorter during the reproductive periods than during the non-reproductive periods (Fig. 3B); (4) most pairs were formed by mature-sized egg cowries; and (5) 44% of the observed pair formations were related to reproductive activities (Table 1). Collectively, these observations suggest that pair formation is a component of the reproductive behavior of this species.

Acknowledgements

This research was carried out as a part of the KURCPI research project titled “Social homeostasis of small islands in an island-zone” and supported by Kagoshima University Research Grants, 2004 and 2005. I am grateful to two anonymous referees, Drs. H. Manabe and K. Yoshino for their critical comments on early drafts and Dr. I. Campbell for his editorial assistance with an earlier version of this manuscript.

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九州南部におけるウミウサギガイのペア形成と繁殖行動

河合 渓

要 約

ウミウサギガイ Ovula ovum（ Linnaeus， 1758）は数個体で集団を形成し，それらの多くは雌雄のペアで あると指摘されているが，その明確な理由が解明されていない。そのため，ウミウサギガイのペア形成 と繁殖行動の関係について鹿児島県南薩摩市坊津の小さな湾内において 2004年 5月から 2006年 10月 まで野外観察を行った。調査地の水温は 8月ごろに最高水温 30°Cを，3月ごろに最低水温 15°Cを示す。 対象とする個体群では殻長 0.9 cm から 9.8 cm の個体が観察され，成熟サイズは約 7 cm，繁殖期間は 低水温期とその後数ヶ月以外ということがすでに報告されている。ペア形成のタイプは大きく 4つのタ イプに分けられる： （1）2個体が近くに位置するペア， （2）交尾を行っているペア， （3）産卵を行ってい るメスの近くに他個体が位置するペア， （4）産卵を行っているメスの上にオス個体が位置し，交尾を行っ ているペア。観察されたペア形成数と繁殖個体数に有意な相関関係が見られた。ペア個体間の距離は繁 殖期間中に短くなっており，ペア個体数は繁殖期間中に有意に多く観察された。また，ペア形成個体の 追跡観察の結果，観察されたペアのうち 44％のペアがなんらかな繁殖行動に関与していた。繁殖期間中 には粘液で形成された透明な帯状物が数 mにわたり形成されており，これがペア形成に大きく関与する 可能性が考えられる。これらの結果はウミウサギガイのペア形成は明らかに繁殖行動と大きく関係して いることを示している。