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Simultaneous Hermaphroditism in the Marine Shrimp Lysmata Wurdemanni (Caridea: Hippolytidae): an Undescribed Sexual System in the Decapod Crustacea

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Simultaneous Hermaphroditism in the Marine Shrimp Lysmata Wurdemanni (Caridea: Hippolytidae): an Undescribed Sexual System in the Decapod Crustacea Marine Biology (1998) 132: 223±235 Ó Springer-Verlag 1998 R. T. Bauer á G. J. Holt Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea Received: 26 October 1997 / Accepted: 21 April 1998 Abstract Simultaneous hermaphroditism with out- Lysmata spp. may determine the exact form of the sex- crossing, a previously uncon®rmed sexual system in ual system in these species. decapod crustaceans, is documented in the shrimp Lysmata wurdemanni (Gibbes), using time-lapse video observations on mating in pairs of ``female-phase'' (FP) individuals. Copulations between FPs resulted in suc- Introduction cessful spawning and development of embryos. However, female-phase hermaphrodites maintained in Although most species of decapod crustaceans have isolation were unable to self-fertilize spawned eggs. All separate sexes, sequential hermaphroditism in the deca- smaller individuals possessed characters typical of cari- pod Crustacea has been documented in a number of dean males, including male gonopores, appendices species, particularly caridean shrimp (Yaldwyn 1966; masculinae, ejaculatory ducts, and cincinnuli on the ®rst Policansky 1982; Bauer 1986). The form of hermaph- pleopods. However, the gonad of these male-phase (MP) roditism previously described has been protandrous, in individuals was an ovotestis with an undeveloped ovar- which individuals ®rst mature as males and then, with ian portion. FPs, which spawn eggs and incubate increasing age and size, change sex to females. Several embryos, also had male gonopores and an ovotestis variations of protandry are recorded in carideans. In terminating in ejaculatory ducts containing sperm. In some species, such as Pandalus platyceros and Panda- FPs, male pleopod characters were absent or reduced, lopsis dispar (Butler 1964, 1980), as well as Lysmata and a female incubatory character, expanded pleopod seticaudata (Spitschako 1912; Dohrn 1950), all indi- ¯anges, showed a greater relative size. Smaller size viduals are reported to transform from males into classes of the population were composed only of MPs females. However, in other protandric carideans, a while larger size classes consisted of both MPs and FPs. variable proportion of the population mature as ``pri- ``Transitionals,'' individuals with MP characters but an mary'' females without a male phase (Pandalidae: Butler ovotestis containing vitellogenic oocytes, were rare and 1964, 1980; Charnov et al. 1978; BergstsroÈ m 1997; overlapped completely in size with FP and larger MP Crangonidae: Fre chette et al. 1970; Processidae: NoeÈ l individuals. It is suggested that not all MPs transform 1976; Boddeke et al. 1991). Conversely, in the hippolytid into FP hermaphrodites. Social interactions may medi- Thor manningi, the population is composed of 50% ate MP change into FP hermaphrodites in L. wurde- primary males and 50% protandric hermaphrodites manni. The social system of L. wurdemanni and other (Bauer 1986). Primary males and sex changers compose the population of the alpheid Athanas kominatoensis (Nakashima 1987), while a mix of primary females, primary males, and sex changers are found in A. indicus Communicated by N.H. Marcus, Tallahassee (Gherardi and Calloni 1993). R.T. Bauer (&) Simultaneous or synchronous hermaphroditism Department of Biology, University of Southwestern Louisiana, which is functional, i.e, an individual may serve male or Lafayette, Louisiana 70504-2451, USA female at any given time, has not previously been doc- Fax: +318 482-5834 E-mail: [email protected] umented in the order Decapoda, nor in any other malacostracan (Charniaux-Cotton and Payen 1985). G.J. Holt Marine Science Institute, The University of Texas at Austin, Buchanan (1963) reviewed and added to morphological 750 Channelview Drive, Port Aransas, and demographic observations that suggested simulta- Texas 78373, USA neous hermaphroditism in the burrowing thalassinid 224 Calocaris macandreae. Kagwade (1982) concluded, were preserved in 10 to 15% seawater formalin or Davidson's so- on similar grounds, that the hippolytid caridean lution, later washed in water, and stored in 70% ethyl alcohol. From the combined July 1994 sample, some individuals were removed Exhippolysmata ensirostris ®rst passed through a male haphazardly for live work before the rest of the sample was pre- phase and then retained functional testicular tissue and served. All individuals in the July 1995 sample were preserved. Live male ducts in the female phase. However, no mating specimens used for the mating study were mainly collected on 12 observations have been done to con®rm these possible June 1995, with a few specimens taken from the July 1994 sample, cases of synchronous hermaphroditism. along with several reared in the laboratory by one of the authors (GJH) (breeding and rearing techniques given in Riley 1994). Spitschako (1912) illustrated and described the go- Morphometric observations were done on specimens from the nads of the caridean Lysmata seticaudata. In this species, July 1994 sample. Carapace length, a measure of body size, was the gonads are ovotestes, in which the testicular part is measured as the distance from the posterior edge of the eye orbit to well developed in smaller individuals while the ovarian the middorsal posterior edge of the carapace. Appendix masculina length was measured from its base to its tip, spines excluded. part becomes prominent in older, larger (female-phase) Presence or absence of openings (male gonopores) on the coxae of individuals. The species has been described as a pro- the ®fth pereopods was recorded. An ejaculatory duct was dissected tandrous hermaphrodite by various workers such as from the body wall/coxa juncture of the ®fth pereopod, and its Spitschako himself, Dohrn (1950), Berreur-Bonnefant maximum width was measured. The number of coupling hooks (cincinnuli) on the endopod of the ®rst pleopod was counted, as and Charniaux-Cotton (1965), Charniaux-Cotton well as the number of spines on the appendix masculina. Width of (1975), and Charniaux-Cotton and Payen (1985). the ¯ange on the basipod of the second pleopod, narrow in males Berreur-Bonnefant and Charniaux-Cotton demonstrated but expanded in incubating females in carideans (HoÈ glund 1943) with histology that the anterior region of male-phase was measured. Degree of ovarian development in the gonad was individuals of L. seticaudata was the ovarian portion of staged from 1 (no vitellogenic oocytes observed) to 4 (maximum ®lling of ovarian portion with vitellogenic oocytes) as in Bauer an ovotestis while the posterior part of the gonad was (1986); degree of development of incubated embryos was also testicular. Extensive histological study of the gonads and staged from 1 (just spawned) to 4 (near hatching) as in Bauer gametogenesis of L. seticaudata by these authors showed (1986). Measures of carapace length, as well as observations on not only that male ducts are retained in the female phase ovarian condition, incubated embryos, presence or absence of ap- pendices masculinae, and Pleopod 1 cincinnuli were done on but also that spermiogenesis and sperm production specimens from the July 1995 collection for construction of length- continue after the sex change. The possibility of concur- frequency diagrams of population structure. rent male and female sexual function was not addressed. Length-frequency diagrams describing population structure and Reports on Lysmata spp. in which ``females'' are breeding condition were constructed for the 1994 and 1995 sam- ples. ``Male-phase'' (MP) individuals were characterized by the described as mating and producing fertile ospring with occurrence of cincinnuli on the ®rst pleopods (P1), a male character other ``females'' have become frequent in the non- in most carideans (Bauer 1976; Butler 1980), along with a non- refereed literature (Bundy 1983; Riley 1994; Wilkerson vitellogenic gonad. ``Female-phase'' (FP) individuals were those 1994). Fletcher et al. (1995) suggested, on the basis of lacking P1 cincinnuli; ``transitional'' individuals were those with P1 preliminary observations, that L. debelius and L. amboi- cincinnuli which displayed stages 2 to 4 ovarian development in the gonad. nensis are simultaneous hermaphrodites. These anec- Live specimens were maintained in aquaria with seawater at 33 dotal reports and preliminary observations, as well as to 36% s, 25 to 28 °C, and a 14 h light:14 h dark cycle. In mating previous indications of synchronous hermaphroditism in experiments, pairs of female-phase individuals, one in Ovarian the literature, stimulated the present investigation on the Stage 3±4 (near a prespawning molt), were con®ned by a porous partition into a space 21 long ´ 24 wide ´ 15 cm high within a sexual system of L. wurdemanni (Gibbes), the ``red 38 liter aquarium. Individuals chosen for observations on mating cleaning'' or ``peppermint'' shrimp from the Gulf of and spawning carried embryos or had just hatched a brood, i.e. had Mexico. The purpose of this study was to determine if reproduced as females. Activities were recorded with an infrared- female-phase individuals are true simultaneous her- sensitive surveillance camera equipped with an 8 or 12.5 mm lens, connected to a time-lapse video recorder. Day illumination was by maphrodites, capable of mating and reproducing as overhead ¯uorescent lights, that at night by infrared lamps either sex during the same reproductive period. The (880 nm). Videotapes were recorded at 24
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