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Gonochoric sexual system in the caridean shrimps Processa riveroi and P. bermudensis (Decapoda: Processidae) inhabiting a tropical seagrass meadow

Published online by Cambridge University Press:  31 May 2011

Raymond T. Bauer  and
Sara Laporte Conner
Raymond T. Bauer*
Affiliation:
Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504, USA
Sara Laporte Conner
Affiliation:
Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504, USA
*
Correspondence should be addressed to: R.T. Bauer, Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504, USA email: [email protected]
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Abstract

The sexual system of two caridean shrimps (Processa riveroi and P. bermudensis) was investigated, stimulated by reports of male to female sex change (protandry) in Processa edulis from European waters. Shrimps used in the study were obtained from monthly samples taken from March 1982 to February 1983 in a Thalassia–Syringodium seagrass meadow in Puerto Rico. Observations on size, sex, and reproductive condition were used to construct monthly size–frequency distributions and sex-ratios by size-class (SC). Males were smaller than reproductive females, but there was extensive overlap in size between males and immature females. A sex-ratio (SR) analysis by SC of the overall year-long population sample showed an equal or female-biased SR in the smallest SC, a male-biased SR in 1–3 intermediate SC, with larger SC dominated by females incubating embryos. Such a population structure might result from slower growth in males than females and higher mortality in larger males. Observations on and allometric analysis of sexual characters failed to identify transitional individuals (sex-changers) intermediate in reproductive morphology between males and females. Thus, a hypothesis of protandry is rejected, and that of gonochory (separate sexes) is accepted in these two Processa species, revealing possible variation in sexual systems among Processa species.

Keywords

hermaphroditismProcessaprotandryPuerto Ricoseagrass meadowsThalassia
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 3 , May 2012 , pp. 521 - 529
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Al-Adhub, A.H.Y. and Williamson, D. (1975) Some European Processidae (Crustacea, Decapoda, Caridea). Journal of Natural History 9, 693–703.CrossRefGoogle Scholar
Anker, A., Baeza, J.A. and De Grave, S. (2009) A new species of Lysmata (Crustacea, Decapoda, Hippolytidae) from the Pacific coast of Panama, with observations of its reproductive biology. Zoological Studies 48, 682–692.Google Scholar
Baeza, J.A. (2006) Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp. Evolution 60, 1840–1850.Google Scholar
Baeza, J.A. (2009) Protandric simultaneous hermaphroditism is a conserved trait in Lysmata (Caridea: Lysmatidae): implications for the evolution of hermaphroditism in the genus. Smithsonian Contributions to Marine Science 38, 95–110.Google Scholar
Baeza, J.A. (2010) Observations on the sexual system and the natural history of the semi-terrestrial shrimp Merguia rhizophorae (Rathbun, 1900). Invertebrate Biology 129, 266–276.CrossRefGoogle Scholar
Baeza, J.A. and Piatoni, C. (2010) Sexual system, sex ratio, and group living in the shrimp Thor amboinensis (De Man): relevance to resource-monopolization and sex-allocation theories. Biological Bulletin. Marine Biological Laboratory, Woods Hole 219, 151–165.CrossRefGoogle Scholar
Baeza, J.A., Schubart, C.D., Zillner, P., Fuentes, S. and Bauer, R.T. (2009) Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and social monogamy. Biological Journal of the Linnean Society 96, 415–424.CrossRefGoogle Scholar
Bauer, R.T. (1976) Mating behaviour and spermatophore transfer in the shrimp Heptacarpus pictus (Stimpson) (Decapoda: Caridea: Hippolytidae). Journal of Natural History 10, 315–440.CrossRefGoogle Scholar
Bauer, R.T. (1985) Diel and seasonal variation in species composition and abundance of the caridean shrimps (Crustacea, Decapoda) from seagrass meadows in northern Puerto Rico. Bulletin of Marine Science 36, 150–162.Google Scholar
Bauer, R.T. (1986) Sex change and life history pattern in the shrimp Thor manningi (Decapoda: Caridea): a novel case of protandric hermaphroditism. Biological Bulletin. Marine Biological Laboratory, Woods Hole 170, 11–31.CrossRefGoogle Scholar
Bauer, R.T. (1989) Continuous reproduction and episodic recruitment in nine caridean shrimp species inhabiting a tropical seagrass meadow. Journal of Experimental Marine Biology and Ecology 127, 175–187.CrossRefGoogle Scholar
Bauer, R.T. (1991) Analysis of embryo production in a caridean shrimp guild from a tropical seagrass meadow. In Wenner, A.M. and Kuris, A. (eds) Crustacean egg production. Rotterdam: Balkema, pp 181–191.Google Scholar
Bauer, R.T. (2000) Simultaneous hermaphroditism in caridean shrimps: a unique and puzzling sexual system in the Decapoda. Journal of Crustacean Biology 20 (Special Issue No. 2), 116–128.CrossRefGoogle Scholar
Bauer, R.T. (2004) Remarkable shrimps: adaptations and natural history of the carideans. Norman, OK: University of Oklahoma Press.Google Scholar
Bauer, R.T. (2006) Same sexual system but variable sociobiology: evolution of protandric simultaneous hermaphroditism in Lysmata shrimps. Integrative and Comparative Biology 46, 430–438.CrossRefGoogle ScholarPubMed
Bauer, R.T. and Holt, G.J. (1998) Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea. Marine Biology 132, 223–235.CrossRefGoogle Scholar
Bauer, R.T. and Newman, W.A. (2004) Protandric simultaneous hermaphroditism in the marine shrimp Lysmata californica (Caridea: Hippolytidae). Journal of Crustacean Biology 24, 131–139.CrossRefGoogle Scholar
Bauer, R.T. and Thiel, M. (2011) First description of a pure-search mating system and protandry in the shrimp Rhynchocinetes uritai (Decapoda: Caridea). Journal of Crustacean Biology 31, 286–295.CrossRefGoogle Scholar
Bauer, R.T. and VanHoy, R. (1996) Variation in sexual systems (protandry, gonochorism) and reproductive biology among three species of the shrimp genus Thor (Decapoda: Caridea). Bulletin of Marine Science 59, 53–73.Google Scholar
Bergström, B. (2000) The biology of Pandalus. Advances in Marine Biology 38, 1–245.Google Scholar
Berkeley, A.A. (1930) The post-embryonic development of the common pandalids of British Columbia. Contributions to Canadian Biology and Fisheries 6, 115–163.Google Scholar
Blackless, M., Charuvastra, A., Derryck, A., Fausto-Sterling, A., Lauzanne, L. and Lee, E. (2000) How sexually dimorphic are we? Review and synthesis. American Journal of Human Biology 12, 151–166.3.0.CO;2-F>CrossRefGoogle ScholarPubMed
Bodekke, R., Bosschieter, J.R. and Goudswaard, P.C. (1991) Sex change, mating, and sperm transfer in Crangon crangon (L.). In Bauer, R.T. and Martin, J.W. (eds) Crustacean sexual biology. New York: Columbia University Press, pp. 164–182.CrossRefGoogle Scholar
Braga, A.A., López-Greco, L.S., Santos, D.C. and Fransozo, A. (2009) Morphological evidence for protandric simultaneous hermaphroditism in the caridean shrimp Exhippolysmata oplophoroides. Journal of Crustacean Biology 29, 34–41.CrossRefGoogle Scholar
Brandt, F. (1851) Krebse. In von Middendorff, A.T. (ed.) Reise in den aussersten Norden und Osten Sibiriens wahrend der Jahre 1843 und 1844 mitallerhochster Genehmigung auf Veranstaltungder Kaiserlichen Akademie der Wissenschaften zu St. Petersburg ausgefuhrt und in Verbindungmit vielen Gelehrten herausgegeben 2, pp. 77–148.Google Scholar
Butler, T.H. (1964) Growth, reproduction, and distribution of pandalid shrimps in British Columbia. Journal of the Fisheries Research Board of Canada 21, 1403–1452.CrossRefGoogle Scholar
Carpenter, A. (1978) Protandry in the freshwater shrimp, Paratya curvirostris (Heller, 1862) (Decapoda: Atyidae), with a review of the phenomenon of its significance in the Decapoda. Journal of the Royal Society of New Zealand 8, 343–358.CrossRefGoogle Scholar
Chace, F.A. Jr (1972) The shrimps of the Smithsonian–Bredin Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology 98, 1–179Google Scholar
Cobos, V., Díaz, V., García-Raso, J.E. and Manjón-Cabeza, ME. (2005) Insights on the female reproductive system in Hippolyte inermis: is this species really hermaphroditic? Invertebrate Biology 124, 310–320.CrossRefGoogle Scholar
Correa, C. and Thiel, M. (2003a) Mating systems in caridean shrimp (Decapoda: Caridea) and their evolutionary consequences for sexual dimorphism and reproductive biology. Revista Chilena de Historia Natural 76, 187–203.CrossRefGoogle Scholar
Correa, C. and Thiel, M. (2003b) Population structure and operational sex ratio in the rock shrimp Rhynchocinetes typus (Decapoda: Caridea). Journal of Crustacean Biology 23, 849–861.CrossRefGoogle Scholar
De Grave, S. and Fransen, C.H.J.M. (in press) Carideorum catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps. Zoologische Mededellingen, LeidenGoogle Scholar
De Grave, S., Pentcheff, N.D., Ahyong, S.T., Chan, T.-Y., Crandall, K.A., Dworschak, P.C., Felder, D.L., Feldmann, R.M., Fransen, C.H.J.M., Goulding, L.Y.D., Lemaitre, R., Low, M.E.Y., Martin, J.W., Ng, P.K.L., Schweitzer, C.E., Tan, S.H., Tsudy, D. and Wetzer, R. (2009) A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology Supplement 21, 1–114.Google Scholar
De Man, J.G. (1888) Bericht über die von Herrn Dr. J. Brock im indischen Archipel gesammelten Decapoden und Stomatopoden. Archiv für Naturgeschichte 53, 289–600.CrossRefGoogle Scholar
Espinoza-Fuenzalida, N.L., Thiel, M., Dupré, E. and Baeza, J.A. (2008) Is Hippolyte williamsi gonochoric or hermaphroditic? A multi-approach study and a review of sexual systems in Hippolyte shrimps. Marine Biology 155, 623–635.CrossRefGoogle Scholar
Gavio, M.A., Orensanz, J.M. and Armstrong, D. (2006) Evaluation of alternative life history hypotheses for the sand shrimp Crangon franciscorum (Decapoda: Caridea). Journal of Crustacean Biology 26, 295–307.CrossRefGoogle Scholar
Gibbes, L.R. (1850) On the carcinological collections of the cabinets of natural history in the United States: with an enumeration of the species contained therein and descriptions of new species. Proceedings of the third meeting of the American Association for the Advancement of Science. Charleston, SC: Corporation of Charleston, pp. 165–201.Google Scholar
Gould, S.J. (1966) Allometry and size in ontogeny and development. Biological Reviews 41, 587–640.CrossRefGoogle Scholar
Gros, P. (1979) Biologie de Processa nouveli Holthuisi, Al-Adhub et Williamson (Crustacea, Decapoda) dans le secteur nord du Golfe de Gascogne. Annals de l'Institut Océanographique Paris 55, 49–70.Google Scholar
Heller, C. (1862) Neue Crustaceen, gesammelt während der Weltumseglung der k. k. Fregatte Novara. Zweiter vorläufiger Bericht. Verhandllungen der kaiserlich-kongiglichen zoologish-botanischen Gesellschaft in Wien 12, 519–528Google Scholar
Kagwade, P.V. (1982) The hermaphrodite prawn Hippolysmata ensirostris Kemp. Indian Journal of Fisheries 28, 189–194.Google Scholar
Kuris, A.M., Ra'anan, Z., Sagi, A. and Cohen, D. (1987) Morphotypic differentiation of male Malaysian giant prawns, Macrobrachium rosenbergii. Journal of Crustacean Biology 7, 219–237.CrossRefGoogle Scholar
Labat, J.P. and Noël, P.Y. (1987) Kinetical study of size structure and biological cycle of a Mediterranean population of Processa edulis (Decapoda, Caridea). Investigación Pesquera 51 (Supplement 1), 165–176.Google Scholar
Laubenheimer, H. and Rhyne, A.L. (2008) Experimental confirmation of protandric simultaneous hermaphroditism in a caridean shrimp outside of the genus Lysmata. Journal of the Marine Biological Association of the United Kingdom 88, 301–305.CrossRefGoogle Scholar
Leach, W.E. (1815) A tabular view of the external characters of four classes of animals, which Linné arranged under Insecta, with the distribution of the genera comprising three of these classes into orders, and descriptions of several new genera and species. Transactions of the Linnean Society of London 11, 306–400.CrossRefGoogle Scholar
Linnaeus, C. (1758) Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Edition 10, Volume 1. Holmiae: Laurentii Salvii.Google Scholar
Manning, R.B. and Chace, F.A. Jr (1971) Shrimps of the family Processidae from the Northwestern Atlantic Ocean (Crustacea: Decapoda: Caridea). Smithsonian Contributions to Zoology 89, 1–41.Google Scholar
Noël, P. (1973) Cycle biologique et inversion sexuelle du Crustacé Décapode Natantia Processa edulis. Cahiers Biologie Marine 14, 217–227.Google Scholar
Noël, P. (1976) L’évolution des caractères sexuels chez Processa edulis (Risso) (Décapode, Natantia). Vie et Milieu 26, 65–104.Google Scholar
Rankin, W.M. (1900) The Crustacea of the Bermuda Islands, with notes on the collections made by the New York University Expeditions in 1897 and 1898. Annals of the New York Academy of Sciences 12, 521–548.CrossRefGoogle Scholar
Rathbun, M.J. (1902) Descriptions of new decapod crustaceans from the west coast of North America. Proceedings of the United States National Museum 24, 885–905.CrossRefGoogle Scholar
Reverberi, G. (1950) La situazione sessuale di Hippolyte viridis e le condizioni che la reggono. Bollettino di Zoologia 4, 91–94.CrossRefGoogle Scholar
Risso, A. (1816) Histoire naturelle des Crustacés des environs de Nice. Paris: La Librairie Greque-Latine-Allemande.CrossRefGoogle Scholar
Schatte, J.R. and Saborowski, R. (2006) Change of external sexual characteristics during consecutive moults in Crangon crangon L. Helgoland Marine Research 60, 70–73.CrossRefGoogle Scholar
Stimpson, W. (1856) On some Californian Crustacea. Proceedings of the California Academy of Sciences 1, 87–90Google Scholar
Stimpson, W. (1866) Descriptions of new genera and species of Macrurous Crustacea from the coasts of North America. Proceedings of the Chicago Academy of Sciences 1, 46–48.Google Scholar
SYSTAT (2007) SYSTAT version 12. San Jose, CA: SYSTAT Software Inc.Google Scholar
Terossi, M., López Greco, L.S., Mantelatto, F.L. (2008) Hippolyte obliquimanus (Decapoda: Caridea: Hippolytidae): a gonochoric or hermaphroditic shrimp species? Marine Biology 154, 127–135.CrossRefGoogle Scholar
Thiel, M., Chak, S.T.C. and Dumont, C. (2010) Male morphotypes and mating behavior of the dancing shrimp Rhynchocinetes brucei (Decapoda: Caridea). Journal of Crustacean Biology 30, 580–588.CrossRefGoogle Scholar
Wenner, A.M. (1972) Sex ratio as a function of size in marine Crustacea. American Naturalist 106, 321–350.CrossRefGoogle Scholar
Wickler, W. and Seibt, U. (1981) Monogamy in Crustacea and Man. Zeitschrift für Tierpsychologie 57, 215–234.CrossRefGoogle Scholar
Zupo, V. (1994) Strategies of sexual inversion in Hippolyte inermis Leach (Crustacea, Decapoda) from a Mediterranean seagrass meadow. Journal of Experimental Marine Biology and Ecology 178, 131–145.CrossRefGoogle Scholar
Zupo, V., Messina, P., Carcaterra, A., Aflalo, E.D. and Sagi, A. (2008) Experimental evidence of a sex reversal process in the shrimp Hippolyte inermis. Invertebrate Reproduction and Development 52, 93–100.CrossRefGoogle Scholar