Abstract
One of the main goals of sex allocation theory is understanding sex ratio evolution. However, theoretical studies predicting sex ratios in species with unusual sexual systems, such as protandric simultaneous (PS) hermaphroditism, are rare. In PS hermaphrodites, juveniles first develop into functional males that mature into simultaneous hermaphrodites later in life. Here, we report on the sex ratio (males/males + hermaphrodites) in the PS hermaphroditic shrimp Exhippolysmata oplophoroides. A 2-year study demonstrated that hermaphrodites dominated the population in two different bays. This skewed sex ratio may be explained by limited encounter rates among conspecifics. In agreement with this idea, the density of shrimps was extremely low (≤1 shrimp km−2) at the two study sites. Size at sex phase change and sex ratios remained relatively stable through time at the two bays. The stability of these parameters might be explained by the rather steady population structure of this species during the study period. A review of sex ratios in PS hermaphroditic shrimps (Lysmata and Exhippolysmata) revealed considerable variation; some species have male- and others hermaphrodite-skewed sex ratios. The conditions explaining inter- and intra-specific sex ratio variation in protandric simultaneous hermaphroditic species remain to be addressed.
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References
Allen JA (1966) The dynamics and interrelation of mixed population of Caridea found off the North-East coast of England. In: Barnes HB (ed) Some contemporary studies of marine science. Allen and Unwin, London, pp 45–66
Allsop DJ, West SA (2004) Sex ratio evolution in sex changing animals. Evolution 58:1019–1027
Andrade G, Pérez EP (2004) Age and growth of the white shrimp Litopenaeus schmitti in western Venezuela. Interciencia 29:212–218
Anker A, Baeza JA, de Grave S (2009) A new species of Lysmata (Crustacea, Decapoda, Hippolytidae) from the Pacific coast of Panama, with observations on its reproductive biology. Zool Stud 48:682–692
Antezana T, Fagetti E, Lopez MT (1965) Observaciones bioecológicas en decápodos comunes de Valparaíso. Rev Biol Mar Valparaíso 12:1–60
Baeza JA (2007) Sex allocation in a simultaneously hermaphroditic marine shrimp. Evolution 61:2360–2373
Baeza JA (2009) Protandric simultaneous hermaphroditism is a conserved trait in Lysmata (Caridea: Lysmatidae): implications for the evolution of hermaphroditism in the genus. Smithson Contrib Mar Sci 38:95–110
Baeza JA (2010) Molecular systematics of peppermint and cleaner shrimps: phylogeny and taxonomy of the genera Lysmata and Exhippolysmata (Crustacea: Caridea: Hippolytidae). Zool J Linnean Soc. doi:10.1111/j.1096-3642.2009.00605.x
Baeza JA, Anker A (2008) Lysmata hochi n. sp., a new species of hermaphroditic shrimp from the southern Caribbean. J Crustac Biol 28:148–155
Baeza JA, Bauer RT (2004) Experimental test of social mediation of sex change in a protandric sequential hermaphrodite; the marine shrimp Lysmata wurdemanni (Crustacea: Caridea). Behav Ecol Sociobiol 55:544–550
Baeza JA, Piantoni C (2010) Sexual system, sex ratio and group living in the shrimp Thor amboinensis (De Man): relevance to resource-monopolization and sex allocation theories. Biol Bull (Accepted)
Baeza JA, Thiel M (2000) Host use pattern and life history of Liopetrolisthes mitra, an associate of the black sea urchin Tetrapygus niger. J Mar Biol Assoc UK 80:39–45
Baeza JA, Reitz J, Collin R (2007) Protandric simultaneous hermaphroditism and sex ratio in the shrimp Lysmata nayaritensis. J Nat His 41:2843–2850
Baeza JA, Schubart MT, Zillner P, Fuentes S, Bauer RT (2009) Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and pair-living. Biol J Linn Soc 96:415–424
Baldwin AP, Bauer RT (2003) Growth, survivorship, life span, and sex change in the hermaphroditic shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). Mar Biol 143:157–166
Bauer RT (1985) Diel and seasonal variation in species composition and abundance of the caridean shrimps (Crustacea, Decapoda) from seagrass meadows in northern Puerto Rico. Bull Mar Sci 36:150–162
Bauer RT (1989) Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow. J Exp Mar Biol Ecol 127:175–187
Bauer RT (1992) Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Inv Rep Dev 22:193–202
Bauer RT (2000) Simultaneous hermaphroditism in caridean shrimps: a unique and puzzling sexual system in the Decapoda. J Crustac Biol 20(Special No. 2):116–128
Bauer RT (2002) Reproductive ecology of a protandric simultaneous hermaphrodite, the shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). J Crustac Biol 22:742–749
Bauer RT, Holt GJ (1998) Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea. Mar Biol 132:223–235
Bauer RT, Newman WA (2004) Protandric simultaneous hermaphroditism in the marine shrimp Lysmata californica (Caridea: Hippolytidae). J Crustac Biol 24:131–139
Braga AA (2006) Biologia e Ecologia do camarão-espinho Exhippolysmata oplophoroides (Holthuis, 1948) (Caridea: Alpheoidea: Hippolytidae) na Região de Ubatuba, Litoral Norte Paulista. Doctoral thesis, Universidade Estadual Paulista, Botucatu, São Paulo, Brasil
Braga AA, López-Greco LS, Santos DC, Fransozo A (2009) Morphological evidence for protandric simultaneous hermaphroditism in the caridean Exhippolysmata oplophoroides. J Crustac Biol 29:34–41
Chacur MM, Negreiros-Fransozo ML (1998) Aspectos biológicos do camarão-espinho Exhippolysmata oplophoroides (Holthuis, 1948) (Crustacea, Caridea, Hippolytidae). Rev Bras Biol 59:173–181
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton
Charnov EL, Bull JJ (1989) Non-fisherian sex ratios with sex change and environmental sex determination. Nature 338:148–150
Cobos V, Díaz V, García Raso JE, Manjón-Cabeza ME (2005) Insights on the female reproductive system in Hippolyte inermis (Decapoda, Caridea): is this species really hermaphroditic? Invertebr Biol 124:310–320
Collin R (1995) Sex, size, and position: a test of models predicting the size at sex change in the protandrous gastropod Crepidula fornicata. Am Nat 146:815–831
Collin R (2006) Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution 60:735–745
Felder DL (1982) Reproduction of the snapping shrimps Synalpheus fritzmuelleri and S. apioceros (Crustacea: Decapoda: Alpheidae) on a sublittoral reef off Texas. J Crustac Biol 2:535–543
Ford CE Jr (1964) Reproduction in the aggregating sea anemone, Anthopleura elegantissima. Pac Sci 18:138–145
Gallucci V, Amjoun B, Hedgepeth J, Lai HL (1996) Size-based methods of stock assessment of small-scale fisheries. In: Gallucci VF, Saila SB, Gustafson DJ, Rothschild BJ (eds) Stock assessment. Quantitative methods and applications for small-scale fisheries. Lewis, Boca Raton, p 527
García S, Le Reste L (1987) Ciclos vitales, dinámica, explotación y ordenación de las poblaciones de camarones peneidos costeros. Documento Técnico de Pesca No. 203: FAO. Rome, Italy, 180 pp
Haddon M (2001) Modelling and quantitative methods in fisheries. Chapman and Hall/CRC, Boca Raton
Hastings NA, Peacock JB (1975) Statistical distributions—a handbook for students and practitioners. Butterworths, London
Holthuis LB (1980) Shrimps and prawns of the world: an annotated catalogue of species of interest to fisheries. In: FAO Species Catalogue. FAO Fisheries Synopsis 1(125):1–270
Kagwade PV (1982) The hermaphrodite prawn Hippolysmata ensirostris Kemp. Indian J Fish 28:189–194
Laubenheimer H, Rhyne AL (2008) Experimental confirmation of protandric simultaneous hermaphroditism in a Caridean shrimp outside of the genus Lysmata. J Mar Biol Assoc UK 88:301–305
Manríquez PH, Castilla JC (2005) Self-fertilization as an alternative mode of reproduction in the solitary tunicate Pyura chilensis. Mar Ecol Prog Ser 305:113–125
Munday PL, Caley MJ, Jones GP (1998) Bi-directional sex change in a coral-dwelling goby. Behav Ecol Soc 43:371–377
Munday PL, Buston PM, Wagner RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21:89–95
Oh CW, Hartnoll RG (2004) Reproductive biology of the common shrimp Crangon crangon (Decapoda: Crangonidae) in the central Irish Sea. Mar Biol 144:303–316
Parrack M (1979) Aspects of brown shrimp, Penaeus aztecus, growth in the northern Gulf of Mexico. Fish Bull 76:827–836
Premoli MC, Sella G (1995) Sex economy in benthic polychaetes. Ethol Ecol Evol 7:27–48
SAS (2004) SAS/STAT software; version 9.1. SAS Institute, Cary
Sastry AN (1983) Ecological aspects of reproduction. In: Vernberg JJ, Vernberg WB (eds) The biology of Crustacea, vol 8. Academic Press, New York, pp 179–270
Schärer L (2009) Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63:1377–1405
Silliman RP (1969) Comparison between Gompertz and von Bertalanffy curves for expressing growth in weight of fishes. J Fish Res Board Can 26:161–165
Sparre P, Venema SC (1995) Introducción a la evaluación de recursos pesqueros tropicales: Documento Técnico de Pesca No. 306/1. FAO: Rome, Italy, 420 pp
St. Mary CM (1994) Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction. Behav Ecol 5:304–313
Sukumaran KK (1973) On the gonad of the protandric prawn Hippolysmata ensirostris Kemp. Indian J Fish 28:195–198
Sukumaran KK (1982) Observation on the secondary sexual characters of Hippolysmata ensirostris Kemp. Indian J Fish 20:626–629
Sullivan PJ, Lai HL, Gallucci VF (1990) A catch-at-length analysis that incorporates a stochastic model of growth. Can J Fish Aquat Sci 47:184–198
Tomiyama K (1996) Mate-choice criteria in a protandrous simultaneously hermaphroditic land snail Achatina fulica (Fe′russac) (Stylommatophora: Achatinidae). J Moll Stud 62:101–111
Wenner EL, Coon III WP, Sandifer PA, Shealy MH Jr (1991) A comparison of species composition and abundance of decapod crustaceans and fishes from the North and South Edisto Rivers in South Carolina. Charleston, South Carolina: South Carolina Wildlife and Marine Resources Department, Marine Resources Division, Marine Resources Center Technical Report 78
West SA, Herre EA, Sheldon BC (2000) The benefit of allocating sex. Science 290:288–290
Wilson K, Hardy ICW (2002) Statistical analysis of sex ratios: an introduction. In: Hardy ICW (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 48–92
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood Cliffs
Zucker N, Cunningham M, Adams HP (1997) Anatomical evidence for androdioecy in the clam shrimp Eulimnadia texana. Hydrobiologia 359:171–175
Zupo V, Messina P (2007) How do dietary diatoms cause the sex reversal of the shrimp Hippolyte inermis Leach (Crustacea, Decapoda). Mar Biol 151:907–917
Acknowledgments
AF and MLNF thank FAPESP for funding of infrastructure, field trips, and laboratory work (projects #94/4848-4 and #98/3234-6). We appreciate the invaluable help of the NEBECC crew during our field and laboratory activities. JAB is thankful for support from a STRI Marine Postdoctoral Fellowship and a SMSFP Postdoctoral Fellowship. Sampling was conducted according to the Sao Paulo state and Brazilian federal laws. We appreciate the helpful comments by three anonymous referees. This is contribution number 830 from the Smithsonian Marine Station at Fort Pierce.
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Communicated by F. Bulleri.
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Baeza, J.A., Braga, A.A., López-Greco, L.S. et al. Population dynamics, sex ratio and size at sex change in a protandric simultaneous hermaphrodite, the spiny shrimp Exhippolysmata oplophoroides . Mar Biol 157, 2643–2653 (2010). https://doi.org/10.1007/s00227-010-1525-2
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DOI: https://doi.org/10.1007/s00227-010-1525-2