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227 2008 1059 Article-Web 1..13 Mar Biol (2008) 155:623–635 DOI 10.1007/s00227-008-1059-z ORIGINAL PAPER Is Hippolyte williamsi gonochoric or hermaphroditic? A multi-approach study and a review of sexual systems in Hippolyte shrimps Nuxia L. Espinoza-Fuenzalida · Martin Thiel · Enrique Dupre · J. Antonio Baeza Received: 12 March 2008 / Accepted: 29 August 2008 / Published online: 30 September 2008 © Springer-Verlag 2008 Abstract Sexual systems vary considerably among females, which was conWrmed by dissections. No transi- caridean shrimps and while most species are gonochoric, tional individuals were found. Males maintained in the others are described as sequential protandric hermaphro- laboratory molted 1–8 times, and many grew up to reach dites or simultaneous hermaphrodites with an early male sizes observed in only a small fraction of males in the phase. At present, there is confusion about the sexual Weld. No indication of sex change was recorded. Our system exhibited by several species mostly because results indicate that H. williamsi is a sexually dimorphic those studies attempting to reveal their sexual system gonochoric species and emphasizes the importance of draw inferences solely from the distribution of the sexes using several kinds of evidence (size measurements, across size classes. Here we investigated the sexual sys- growth experiments, morphological dissections, and his- tem of the shrimp Hippolyte williamsi from Chile to tological studies) to reveal the sexual system of Hippo- determine if the species is protandric or gonochoric with lyte species. Whether the observed size dimorphism sexual dimorphism (males smaller than females). Mor- between males and females in many species of Hippolyte phological identiWcation and size frequency distribu- is expression of contrasting sexual and natural selection, tions indicated that the population comprised small and whether divergent sexual Wtness functions can con- males, small immature females, and large mature tribute to the evolution of hermaphroditism remains to be revealed in future studies. Communicated by B. Notes. Introduction N. L. Espinoza-Fuenzalida · M. Thiel · E. Dupre · J. A. Baeza Facultad Ciencias del Mar, Sexual systems vary considerably in the Caridea. Most Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile shrimps are gonochoric, with individuals reproducing as e-mail: [email protected] male or female during their entire life (Bauer 2001, 2004). Examples include Rhynchocinetes typus (Thiel and Hinojosa M. Thiel 2003), Macrobrachium rosenbergii (Karplus 2005), Center for Advanced Studies in Arid Systems, CEAZA, Coquimbo, Chile Hippolyte obliquimanus (Terossi et al. 2008), and most e-mail: [email protected] species from the diverse genus Alpheus (Correa and Thiel 2003; Anker et al. 2006). Other species are protandric her- J. A. Baeza maphrodites, in which individuals change from male to Smithsonian Marine Station at Fort Pierce, V 701 Seaway Drive, Fort Pierce, FL 34949, USA female (e.g., Pandalus—Butler 1964, 1980; Ho man 1972, see also review by Bergström 2000). Several variants of J. A. Baeza (&) protandry have been reported, such as mixed protandry Smithsonian Tropical Research Institute, with primary females in Processa edulis (Noël 1976) and Apartado Postal 0843-03092, Balboa, Ancón, Republic of Panama Crangon crangon (Boddeke et al. 1991; Schatte and Sabo- e-mail: [email protected] rowski 2006), or with primary males in Thor manningi 123 624 Mar Biol (2008) 155:623–635 (Bauer and VanHoy 1996). No study so far has reported Buttino 2001; Zupo and Messina 2007) or gonochoric protogyny (female Wrst) among shrimps (e.g., as in the iso- (Cobos et al. 2005). Because the two studies examining the pod Gnorimosphaeroma oregonense—Brook et al. 1994). sexual system of this species were conducted in localities Finally, simultaneous hermaphroditism with an early pro- hundreds of kilometers apart (i.e., Italy and Spain), this tandric phase, i.e. adolescent protandry sensu Ghiselin controversy might well be explained if the two sampled (1974) or protandric simultaneous hermaphroditism sensu populations pertain to two diVerent cryptic species, each Bauer and Holt (1998), where individuals initially mature one with a diVerent sexual system. Data on gender size fre- as males and later become simultaneous hermaphrodites, quency, gonad anatomy, secondary sexual characters and has been described for various species of Lysmata and development in laboratory culture are necessary to deter- might be more common than previously assumed (Baeza mine the sexual system of marine shrimps (e.g. Terossi 2008a). et al. 2008). Interestingly, within the Caridea there is also consider- The aim of the present study was to elucidate the sexual able variation of sexual systems at the generic level. For system of Hippolyte williamsi Schmitt 1924, a small spe- instance, while Thor manningi has been recognized as a cies that inhabits seaweed meadows and seagrass beds of protandric species (Bauer 1986), studies of its congeners, Heterozostera chilensis (0–8 m depth) in northern-central T. dobkini and T. Xoridanus, indicated that they are Chile (González 1992; Stotz and González 1997). Studies gonochoric (Bauer and VanHoy 1996; Bauer 2004). This on the general ecology of this shrimp are lacking. However, variability in gender expression among closely related species preliminary observations indicated that males were smaller suggests that caridean shrimps might be used as models to than females. Although this size diVerence between the test the role of the environment in explaining evolutionary sexes is suggestive of protandry, as reported for its conge- innovations in gender in marine invertebrates. However, at ner Hippolyte inermis (Zupo and Messina 2007; but see present, comparative studies are precluded due to the scar- Cobos et al. 2005), gonochorism cannot be ruled out as an city of information about the sexual system of many species alternative pattern of gender expression (see Terossi et al. in diverse families. 2008). To properly examine the sexual system of H. wil- While the sexual system of most shrimp species is well liamsi, we sampled in diVerent seasons to document the known, for some species the distribution of the sexes population structure and sexual characters. Additionally, among individuals is not clear. For several species there we reared males in the laboratory in three diVerent social is controversy with respect to their sexual system. For environments (in isolation, together with females, or in instance, initial studies on the population structure of Cran- presence of other males), recording possible sex change and gon franciscorum indicated that this species was gonoch- death. oric (Siegfried 1980, 1989). The body size of the males was almost invariably smaller than that of the females, a condi- tion explained at that time by sex-speciWc mortality or Materials and methods migratory behavior (op. cit.). The sexual dimorphism reported for this species might also indicate strong selective Collection and maintenance of shrimps pressures among males (but not females) favoring a small male condition (see review in Baeza and Thiel 2007). On Shrimps were collected with kick nets at low tides from a the other hand, recent studies combining population shallow subtidal sea grass bed of Heterozostera chilensis at dynamics, gonad dissections, and rearing of shrimps in cap- Puerto Aldea (S 30º 17Ј, W 71º 36Ј), Tongoy, Coquimbo, tivity have demonstrated that C. franciscorum is actually Chile, during December 2005, October 2006 and January protandric (Gavio et al. 2006). A similar sexual system 2007. The species was identiWed using d’Udekem d’Acoz (i.e., facultative protandry) has been reported for the conge- (1996, 1997, 2007) and the key of Wicksten (1990), and ner Crangon crangon, where a small proportion of males in our original identiWcation was kindly conWrmed by Sammy the population change sex later in life (Boddeke et al. 1991; De Grave (Oxford University Museum of Natural History, Schatte and Saborowski 2006). accession number of the specimen deposited at the To the best of our knowledge, the caridean family with museum: OUMNH 2007-12-0002). Immediately after col- the highest diversity of sexual systems is the Hippolytidae. lection, shrimp were either preserved in 5% formalin or It contains species that are gonochoric, protandric hermaph- kept alive and placed in large plastic buckets and/or ice rodites and simultaneous hermaphrodites (Bauer 2004; chests (only for samples from 2006 and 2007) to be trans- Bauer and VanHoy 1996; Baeza 2006; Terossi et al. 2008). ported to the seawater laboratories of Universidad Católica Furthermore, there are species whose sexual system del Norte, Coquimbo, Chile. remains controversial such as Hippolyte inermis, which is Shrimps were maintained in 55 L plastic containers with reported either as protandric (Zupo 2000, 2001; Zupo and circulating Wltered seawater at water temperatures ranging 123 Mar Biol (2008) 155:623–635 625 from 12 to 20°C (14–18°C during October–December mediate” individuals, i.e. males with maturing ovaries and/ 2006; 17–20°C in January–February 2007; 14–18°C in or shrimps with both male and female characteristics. For March-April 2007; 12–16°C May–June 2007) and 34.3– instance, individuals carrying embryos beneath the abdo- 34.7 ppt salinity and were fed daily with planktonic micro- men (female character) but with appendices masculinae on algae (Chaetoceros spp.), benthic diatoms (Grammatophora the second pleopods (male characters) would have been
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