Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-24T08:11:02.521Z Has data issue: false hasContentIssue false

Population dynamics, relative growth and sex change of the protandric simultaneous hermaphrodite Exhippolysmata oplophoroides (Caridea: Lysmatidae) close to an upwelling area

Published online by Cambridge University Press:  16 January 2017

Régis A. Pescinelli
Affiliation:
Laboratory of Biology of Marine and Freshwater Shrimp (LABCAM), Department of Biological Sciences, School of Sciences, University of Sao Paulo State (UNESP), Av. Eng. Luiz Edmundo Corrijo Coube, 14-01, 17033-360 Bauru, SP, Brasil
Thiago M. Davanso
Affiliation:
Laboratory of Biology of Marine and Freshwater Shrimp (LABCAM), Department of Biological Sciences, School of Sciences, University of Sao Paulo State (UNESP), Av. Eng. Luiz Edmundo Corrijo Coube, 14-01, 17033-360 Bauru, SP, Brasil
João A. F. Pantaleão
Affiliation:
Laboratory of Biology of Marine and Freshwater Shrimp (LABCAM), Department of Biological Sciences, School of Sciences, University of Sao Paulo State (UNESP), Av. Eng. Luiz Edmundo Corrijo Coube, 14-01, 17033-360 Bauru, SP, Brasil
Abner Carvalho-Batista
Affiliation:
Laboratory of Biology of Marine and Freshwater Shrimp (LABCAM), Department of Biological Sciences, School of Sciences, University of Sao Paulo State (UNESP), Av. Eng. Luiz Edmundo Corrijo Coube, 14-01, 17033-360 Bauru, SP, Brasil
Raymond T. Bauer
Affiliation:
Department of Biology, University of Louisiana at Lafayette, Lafayette, Louisiana 70504-2451, USA
Rogério C. Costa*
Affiliation:
Laboratory of Biology of Marine and Freshwater Shrimp (LABCAM), Department of Biological Sciences, School of Sciences, University of Sao Paulo State (UNESP), Av. Eng. Luiz Edmundo Corrijo Coube, 14-01, 17033-360 Bauru, SP, Brasil
*
Correspondence should be addressed to: R.C. Costa, Laboratory of Biology of Marine and Freshwater Shrimp (LABCAM), Department of Biological Sciences, School of Sciences, University of Sao Paulo State (UNESP), Av. Eng. Luiz Edmundo Corrijo Coube, 14-01, 17033-360 Bauru, SP, Brasil email: [email protected]

Abstract

The present study investigated the population dynamics of Exhippolysmata oplophoroides in an area influenced by upwelling, focusing on reproductive period, sex ratio, growth rate, longevity, mortality, relative growth and size of sex change. We also tested the hypothesis that the appendices internae increased in size with sex change from the male to the simultaneous hermaphrodite phase as possible replacements for the male appendices masculinae, which are reduced or lost at sex change. Population structure was assessed by the distribution of size frequency in three demographic groups: male phase, hermaphrodite phase with, and without embryos. For relative growth analysis, the length of the following structures was measured: carapace, second pleuron, first pereopod, second pereopod, appendices internae of the second to fifth pleopods, and appendix masculina. Smaller size classes were composed only by male-phase individuals. The sex ratio was significantly biased towards the simultaneous hermaphrodite phase. Reproduction was continuous in the population throughout the year. Slower growth rates but higher maximum body sizes than those estimated at other locations in south-eastern Brazil were observed in the population studied. Cooler temperatures and higher nutrient levels associated with upwelling may have produced this pattern of reproduction and growth, similar to that found in more southerly austral latitudes. We also found that sex change influences the relative growth of body structures such as the second pereopods, appendices internae, and appendix masculina, and hypotheses on the adaptive value of such allometric growth are proposed.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baeza, J.A. (2007a) Sex allocation in a simultaneously hermaphroditic marine shrimp. Evolution 61, 23602373.Google Scholar
Baeza, J.A. (2007b) Male mating opportunities affect sex allocation in a protandric-simultaneous hermaphroditic shrimp. Behavioral Ecology and Sociobiology 61, 365370.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 the Marine Sciences 38, 95110.Google Scholar
Baeza, J.A. and Bauer, R.T. (2004) Experimental test of socially mediated sex change in a protandric simultaneous hermaphrodite, the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Behavioral Ecology and Sociobiology 55, 544550.Google Scholar
Baeza, J.A., Braga, A.A., López-greco, L.S., Perez, E., Negreiros-Fransozo, M.L. and Fransozo, A. (2010) Population dynamics, sex ratio and size at sex change in a protandric simultaneous hermaphrodite, the spiny shrimp Exhippolysmata oplophoroides. Marine Biology 157, 26432653.Google Scholar
Baldwin, A.P. and Bauer, R.T. (2003) Growth, survivorship, lifespan, and sex change in the hermaphroditic shrimp, Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). Marine Biology 143, 157166.Google Scholar
Bauer, R.T. (1976) Mating behavior and spermatophore transfer in the shrimp Heptacarpus pictus (Stimpson) (Decapoda: Caridea: Hippolytidae). Journal of Natural History 10, 415440.Google Scholar
Bauer, R.T. (1978) Antifouling adaptations of Caridean shrimps: cleaning of the antennal flagellum and general body grooming. Marine Biology 49, 6982.Google Scholar
Bauer, R.T. (2000) Simultaneous hermaphroditism in caridean shrimps: a unique and puzzling sexual system in the Decapoda. Journal of Crustacean Biology, Special Number 2, 116128.Google Scholar
Bauer, R.T. (2002) Tests of hypotheses on the adaptive value of an extended male phase in the hermaphroditic shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Biological Bulletin 203, 347357.Google 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. (2005) Costs of maleness on brood production in the shrimp Lysmata wurdemanni (Decapoda: Hippolytidae: Caridea), a protandric simultaneous hermaphrodite. Journal of the Marine Biological Society of the United Kingdom 85, 101106.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, 430438.Google Scholar
Bauer, R.T. (2013) Adaptive modification of appendages for grooming (cleaning; antifouling) and reproduction in the Crustacea. In Thiel, M. and Watling, L. (eds) Functional morphology of Crustacea, Vol. 1. New York, NY: Oxford University Press, pp. 337375.Google Scholar
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, 223235.Google 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, 131139.Google Scholar
Berg, A.B.V. and Sandifer, P.A. (1984) Mating behavior of the grass shrimp Palaemonetes pugio Holthuis (Decapoda, Caridea). Journal of Crustacean Biology 3, 417424.Google Scholar
Beverton, R.J.H. and Holt, S.J. (1959) A review of the lifespans and mortality rates of fish in nature and the relation to growth and other physiological characteristics. Ciba Foundation Colloquia on Ageing 5, 142177.Google Scholar
Braga, A.A., López-Greco, L.S. and Fransozo, A. (2009) Morphological evidence for protandric simultaneous hermaphroditism in the caridean Exhippolysmata oplophoroides. Journal of Crustacean Biology 29, 3441.Google Scholar
Cerrato, R.M. (1990) Interpretable statistical tests for growth comparisons using parameters in the von Bertalanffy equation. Canadian Journal of Fisheries and Aquatic Sciences 47, 14161426.Google Scholar
Chacur, M.M. and Negreiros-Fransozo, M.L. (1998) Aspectos biológicos do camarão-espinho Exhippolysmata oplophoroides (Holthuis, 1948) (Crustacea, Caridea, Hippolytidae). Revista Brasileira de Biologia 59, 173181.CrossRefGoogle Scholar
Charnov, E.L. (1982) The theory of sex allocation. Princeton, NJ: Princeton University Press.Google ScholarPubMed
Charnov, E.L., Gotshall, D.W. and Robinson, J.G. (1978) Sex ratio: adaptive response to population fluctuations in Pandalid shrimp. Science 200, 204206.Google Scholar
Costa, R.C., Fransozo, A., Mantelatto, F.L.M. and Castro, R.H. (2000) Occurrence of shrimp species (Crustacea: Decapoda: Natantia: Penaeidea and Caridea) in Ubatuba Bay, Ubatuba, SP, Brazil. Proceedings of the Biological Society of Washington 113, 776781.Google Scholar
De Léo, F.C. and Pires-Vanin, A.M. (2006) Benthic megafauna communities under the influence of the South Atlantic Central Water intrusion onto the Brazilian SE shelf: a comparison between an upwelling and a non-upwelling ecosystem. Journal of Marine Systems 60, 268284.Google Scholar
D'Incao, F. and Fonseca, D.B. (1999) Performance of the von Bertalanffy growth curve in penaeid shrimps: a critical approach. In von Vaupel Klein C. and Schram F.R. (eds). The biodiversity crisis and Crustacea. Proceedings of the Fourth International Crustacean Congress. Amsterdam, the Netherlands. Leiden: Crustacean Issues 12. Rotterdam: A. A. Balkema, pp. 733749.Google Scholar
Fransozo, V., Costa, R.C., Bertini, G. and Cobo, V.J. (2005) Population biology of spine shrimp Exhippolysmata oplophoroides (Holthuis) (Caridea: Alpheoidea: Hippolytidae) in a subtropical region, São Paulo, Brasil. Revista Brasileira de Zoologia 22, 10781084.Google Scholar
Ghiselin, M.T. (1969) The evolution of hermaphroditism among animals. Quarterly Review of Biology 44, 189208.Google Scholar
Hardy, I.C.W. (2002) Sex ratios: concepts and research methods. Cambridge: Cambridge University Press.Google Scholar
Laubenheimer, H. and Rhyne, A. (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, 301305.Google Scholar
Lika, K. (2003) Life historical implications of allocation to growth versus reproduction in dynamic energy budgets. Bulletin of Mathematical Biology 65, 809834.Google Scholar
Mann, K.H. and Lazier, J.R.N. (1996) Dynamics of marine ecosystems: biological–physical interactions in the oceans, 2nd edition. Oxford: Blackwell Science.Google Scholar
Negreiros-Fransozo, M.L., Gonzales-Gordilho, J.I. and Fransozo, A. (2002) First larval stage of Exhippolysmata oplophoroides (Holthuis, 1948) (Decapoda, Caridea, Hippolytidae) obtained in laboratory. Nauplius 10, 6771.Google Scholar
Odebrecht, C. and Djurfeldt, L. (1996) The role of near shore mixing on phytoplankton size structure off Cape Santa Marta Grande, southern Brazil (Spring 1989). Archive of Fishery and Marine Research 43, 217230.Google Scholar
Onaga, H., Fiedler, G.C. and Baeza, A. (2012) Protandric simultaneous hermaphroditism in Parhippolyte misticia (Clark, 1989) (Caridea: Hippolytidae): implications for the evolution of mixed sexual systems in shrimp. Journal of Crustacean Biology 32, 383394.Google Scholar
Pantaleão, J.A.F., Carvalho-Batista, A., Fransozo, A. and Costa, R.C. (2016) The influence of upwelling on the diversity and distribution of marine shrimp (Penaeoidea and Caridea) in two tropical coastal areas of southeastern Brazil. Hydrobiologia 763, 381395.Google Scholar
Pauly, D. (1980) On the interrelationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. ICES Journal of Marine Science 39, 175192.Google Scholar
Sampedro, M.P., Gonzáles-Gurriarán, E., Freire, J. and Muiño, R. (1999) Morphometry and sexual maturity in the spider crab Maja squinado (Decapoda: Majidae) in Galicia, Spain. Journal of Crustacean Biology 19, 578592.Google Scholar
Schaffer, W. (1983) The application of optimal control theory to the general life history problem. American Naturalist 121, 418431.Google Scholar
Silva, E.R., Sancinetti, G.S., Fransozo, A., Azevedo, A. and Costa, R.C. (2014) Biodiversity, distribution and abundance of shrimps Penaeoidea and Caridea communities in a region the vicinity of upwelling in Southeastern of Brazil. Nauplius 22, 111.Google Scholar
Sokal, R.R. and Rohlf, F.J. (1995) Biometry, 3rd edition. New York, NY: W. H. Freeman and Company.Google Scholar
Von Bertalanffy, L. (1938) A quantitative theory of organic growth. Human Biology 10, 181213.Google Scholar
Warner, R.R. (1975) The adaptive significance of sequential hermaphroditism in animals. American Naturalist 109, 6182.Google Scholar
Wickler, W. and Seibt, U. (1981) Monogamy in Crustacea and man. Zeitschrift für Tierpsychologie 57, 215234.Google Scholar
Zar, J.H. (1996) Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall.Google Scholar
Zhang, D. and Lin, J. (2004) Fertilization success without anterior pleopods in Lysmata wurdemanni (Decapoda: Caridea), a protandric simultaneous hermaphrodite. Journal of Crustacean Biology 24, 470473.Google Scholar