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Effects of Conspecific Associations on Size at Sex Change in Three Species of Calyptraeid Gastropods

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Effects of Conspecific Associations on Size at Sex Change in Three Species of Calyptraeid Gastropods MARINE ECOLOGY PROGRESS SERIES Vol. 293: 89–97, 2005 Published June 2 Mar Ecol Prog Ser Effects of conspecific associations on size at sex change in three species of calyptraeid gastropods Rachel Collin1,*, Michelle McLellan1, Karl Gruber2, Catherine Bailey-Jourdain1 1Smithsonian Tropical Research Institute, Apartado Postal, 0843-03092, Balboa, Ancon, Panamá 2Bell Museum of Natural History and Department of Ecology, Evolution, and Behavior, University of Minnesota, 1987 Upper Buford Circle, St. Paul, Minnesota 55108-6097, USA ABSTRACT: In marine molluscs, sex change is often labile and is thought to be largely influenced by interactions with conspecifics. Previous studies of calyptraeid gastropods concluded that their social environment influences the timing of protandrous sex change. We conducted field surveys and labo- ratory experiments to examine the effects of conspecifics on size at sex change in 3 Panamanian calyptraeids. Crepidula cf. onyx, C. incurva Broderip, 1834 and Bostrycapulus calyptraeformis (Des- hayes, 1830) vary in densities, sex ratio and mode of development, which suggests that they might respond to associations with conspecifics in different ways. However, our laboratory experiments showed that the response to interactions with conspecifics is generally similar. In all 3 species, indi- viduals raised in isolation pass through a male phase and males raised alone change sex at the same size as males raised with another male. Both C. cf. onyx and C. incurva change sex at a larger size when kept with a female than when kept alone or with another male. The differences in size at sex change between the treatments is small and the treatment effect explains more of the variation in size at sex change in C. cf. onyx, the more solitary species, than in C. incurva, a species that is usually found in pairs. In all species, individuals with high initial growth rates change sex sooner and at a smaller size than those with slower initial growth rates. Growth rates increase significantly during sex change in C. cf. onyx and C. incurva but not in B. calyptraeformis. KEY WORDS: Protandry · Crepidula spp. · Size advantage · Bostrycapulus calyptreaformis Resale or republication not permitted without written consent of the publisher INTRODUCTION including alternate mating strategies for males, accel- erated and delayed sex change, and reversed sex Sex change is widespread among vertebrates and change (e.g. Warner & Swearer 1991, St. Mary 1993, invertebrates. Most species show environmentally Lutnesky, 1994, Munday 2002). Some fishes can make mediated lability in size or age at sex change. How- very fine adjustments in sex allocation in response to ever, the number of factors influencing sex change local social interactions (e.g. Ross et al. 1983, Petersen make it difficult to make precise predictions of the size et al. 2001, Alonzo & Warner 2000b). at which an individual changes sex. Interactions with In contrast to the wide range of behavioral strategies conspecifics have been shown to influence the initia- displayed by sex-changing fishes, most sex-changing tion or delay of sex change in sex-changing fishes (e.g. mollusks seem to employ simple strategies for sex Robertson 1972, Alonzo & Warner 2000a,b, Mackie change (Warner et al. 1996). This simplicity may be 2003, Perry & Grober 2003), shrimp (see e.g. Charnov due to differences between the evolution of reproduc- 1982, Koeller et al. 2000, Chiba et al. 2003), and mol- tive strategies in protandrous (males first) and protog- lusks (e.g. Coe 1953, Hoagland 1978, Charnov 1982, ynous species, differences in the complexity of verte- Soong & Chen 1991, 2003). Studies of protogynous brate versus invertebrate behaviors, or may reflect the (females first) fish species have revealed a surprising relatively large research effort focused on fishes com- diversity of strategies to increase reproductive output, pared to invertebrates. Strategies of sex change in *Email: [email protected] © Inter-Research 2005 · www.int-res.com 90 Mar Ecol Prog Ser 293: 89–97, 2005 protandrous shrimp, which have been more inten- plana) are gregarious and show large differences in sively studied than mollusks, appear to be more vari- size at sex change between solitary and ‘mated’ indi- able, with mixed strategies as well as pure protandry viduals while smaller species with direct development occurring in several groups (e.g. Bauer & VanHoy (C. convexa and C. adunca) are less gregarious and do 1996, Baldwin & Bauer 2003). not show a difference in size at sex change between It is difficult to assess the variability of sex change solitary and mated individuals. The results of Hoag- strategies among mollusks because few groups have land (1978) for C. fornicata, C. plana and C. convexa, a been examined in detail and the conclusions of studies subset of the species examined by Coe (1938), support on the same species often differ. Calyptraeids, protan- the latter’s conclusions. However, C. nivea, Crucibu- drous, filter-feeding limpets, are the most well-studied lum spinosum, and Crepidula norissiarum do not fit the sex-changing mollusks (see e.g. Gould 1917, 1919, pattern (Coe 1938, Warner et al. 1996) and there is no 1952, Coe 1936, 1938, 1953, Hoagland 1978, Collin theoretical expectation that body size or mode of de- 1995, Warner et al. 1996, Chen & Soong 2000). The velopment should be associated with strategies of sex conclusions of these studies are often contradictory, change. and interpretation of many older studies is difficult We examined the lability of sex change in calyp- because they may have employed experimental condi- traeid gastropods with the aim of understanding varia- tions that starved the limpets (e.g. Coe’s [1948] criti- tion in sex allocation strategies among a wider range of cisms of Gould [1947], but see Gould & Hsiao's rebuttal species and to obtain parameters for subsequent use in [1948]), the sample sizes were often low or not re- quantitative models of sex change. We address the ported (e.g. only a single replicate of each density following questions for 3 species (Crepidula cf. onyx, treatment in Hoagland 1978), the experimental design C. incurva and Bostrycapulus calyptraeformis) that was not described (e.g. Coe 1938), or/and the size of display different life histories (Table 1) and gregarious- the limpets in the different treatments were not re- ness in the field: (1) Do individuals raised alone bypass ported (e.g. Coe 1953). Differing results from studies the male stage and develop directly into females? (2) using the same species are common. For example, Coe Do individuals kept alone, or in association with males (1936) stated that there are some ‘true’ males that or, in association with females change sex at different never change, but Hoagland (1978), studying the same sizes? (3) Does growth rate increase during sex species, found no evidence to support this in C. con- change? vexa and thought it unlikely in Crepidula fornicata. Although Gould (1919) reports that small C. plana must be associated with a female to develop into a fully MATERIALS AND METHODS functional male, Coe (1936, 1938) stated that this asso- ciation is not necessary for male development in either Study species and field survey. The 3 calyptraeid C. plana or 6 other species of Crepidula. Some of these species Crepidula cf. onyx, C. incurva Broderip, 1834, conflicting conclusions could be due to differences or and Bostrycapulus calyptraeformis (Deshayes, 1830) vagaries in interpretation of similar results. For exam- examined in this study co-occur commonly in ple, several of these studies report a ‘delayed’ sex muddy–rocky habitats in the intertidal along the Pacific change, which could refer to a delay with respect to coast of Panama. We used field-collected samples to size or to a temporal delay (a distinction that is often survey the natural size frequencies of males and fe- not made clear). males for each species from Playa Venado and Playa Sex change strategies may vary in concert with Chumical (8° 30’ N, 79° 40’ W). The method of sampling mode of development, social behavior, and body size. differed for each species, based on their natural history. Coe (1938) suggested that larger species with plank- Crepidula cf. onyx occurs at Playa Venado in densi- tonic development (Crepidula fornicata, C. onyx and C. ties of 1 or 2 individuals m–2 in the low intertidal (–0.5 Table 1. Crepidula cf. onyx, C. incurva and Bostrycapulus calyptraeformis. Life history differences between the 3 panamanian calyptraeids. Sex ratio: breeding ratio males:males + females Species Development Stacking Max. size (mm) Abundance Sex ratio C. cf. onyx Direct Solitary 34 Uncommon 0.21 C. incurva Planktotrophic 53% in pairs 18 Patchy 0.40 B. calyptraeformis Planktotrophic Solitary or paired 25 Very abundant 0.55 (up to 1000 m–2) Collin et al.: Calyptraeid sex change 91 to –1.0 m). We collected them by carefully examining they also reached a length of 2.0 to 2.5 mm. Juveniles the rocks within an area of about 200 m2 and collecting of each species were transferred to individual 355 ml all the C. cf. onyx during low tide on February 2, 2003. cups which were maintained in the laboratory at room Crepidula incurva occurs patchily in the intertidal temperature. They were fed 10 ml of a mix of algal between –0.5 and –1.0 m. They are usually found cultures (Nannochloropsis sp., Rhodomonas sp., Duna- attached to the shells of other snails, especially Ceri- liella tertiolecta, Isochrysis galbana and Chaetocerus thium sp., which congregate in large numbers in shal- gracilis) daily; the proportion of each alga in the mix low tide pools and below large rocks. We collected C. varied from day to day, but all gastropods were raised incurva from tide pools within an area of 100 m2 by simultaneously and all were fed from the same mix on examining every snail in the pool and collecting all each day.
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