Protandric simultaneous hermaphroditism in parhippolyte misticia (Clark, 1989) (Caridea: Hippolytidae): Implications for the evolution of mixed sexual systems in shrimp

Journal of Crustacean Biology

Volumn 32, Issue 3, 2012, Pages 383-394

  Onaga, Hitoshi ^a   Fiedler, G Curt ^a   Baeza, J Antonio ^b,c,d  

^a UNIVERSITY OF MARYLAND   (United States)

^b OLD DOMINION UNIVERSITY   (United States)

^c SMITHSONIAN MARINE STATION   (United States)

^d Universidad Católica del Norte   (Chile)

Author keywords

Barbouridae; Lysmatidae; mating system; Parhippolyte; sex allocation; sex ratio

Indexed keywords

CARIDEA; CARIDEAN; DECAPODA (CRUSTACEA); EXHIPPOLYSMATA; HIPPOLYTIDAE; LYSMATA;

EID: 84862834998     PISSN: 02780372     EISSN: None     Source Type: Journal    
DOI: 10.1163/193724012X626520     Document Type: Article

References (71)

1. Ahyong, S. T. 2009. New species and new records of hydrothermal vent shrimps from New Zealand (Caridea: Alvinocarididae, Hippolytidae). Crustaceana 82: 775-794.
2. Allen, J. A. 1966. The dynamics and interrelation of mixed population of Caridea found off the North-East coast of England, pp. 45-66. In, H. B. Barnes (ed.), Some Contemporary Studies of Marine Science. Allen and Unwin, London, England.
3. Antezana, T., E. Fagetti, and M. T. Lopez. 1965. Observaciones bioecológicas en decápodos comunes de Valparaíso. Revista de Biología Marina, Valparaíso 12: 1-60.
4. Baeza, J. A. 2006. Testing three models on the adaptive significance of protandric simultaneous hermaphroditism in a marine shrimp. Evolution 60: 1840-1850. (Pubitemid 44808234)
5. -2007a. Male mating opportunities affect sex allocation in a protandric simultaneous hermaphroditic marine shrimp. Behavioral Ecology and Sociobiology 61: 365-370.
6. -2007b. Sex allocation in a simultaneously hermaphroditic marine shrimp. Evolution 62: 2360-2373.
7. -2008. Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlantica, in the tropical eastern Pacific coast. Marine Biology 153: 387-395.
8. -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.
9. -2010a. Sexual system and natural history observations on semiterrestrial shrimp Merguia rhizophorae. Invertebrate Biology 129: 266-276.
10. -2010b. Molecular systematics of peppermint and cleaner shrimps: Phylogeny and taxonomy of the genera Lysmata and Exhippolysmata (Crustacea: Caridea: Hippolytidae). Zoological Journal of the Linnean Society 160: 254-265.
11. 2010c. The symbiotic lifestyle and its evolutionary consequences: Social monogamy and sex allocation in the hermaphroditic shrimp Lysmata pederseni. Naturwissenschaften 97: 729-741.
12. and A. Anker. 2008. Lysmata hochi n. sp., a new species of hermaphroditic shrimp from the southern Caribbean. Journal of Crustacean Biology 28: 148-155. (Pubitemid 351251683)
13. and R. T. Bauer. 2004. Experimental test of social mediation of sex change in a protandric sequential hermaphrodite; the marine shrimp Lysmata wurdemanni (Crustacea: Caridea). Behavioral Ecology and Sociobiology 55: 544-550. (Pubitemid 38517153)
14. and C. Piantoni. 2010. Sexual system, sex ratio and group living in the shrimp Thor amboinensis (De Man): Relevance to resourcemonopolization and sex-allocation theories. Biological Bulletin 219: 151-165.
15. and M. Thiel. 2000. Host use pattern and life history of Liopetrolisthes mitra, an associate of the black sea urchin Tetrapygus niger. Journal of the Marine Biological Association of the United Kingdom 80: 39-45.
16. J. Reitz, and R. Collin. 2008. Protandric simultaneous hermaphroditism and sex ratio in the shrimp Lysmata nayaritensis. Journal of Natural History 41: 2843-2850.
17. J. A. Bolaños, J. E. Hernandez, C. Lira, R. López. 2011. Monogamy does not last long in Pontonia mexicana, a symbiotic shrimp of the Amber pen-shell Pinna carnea from the southeastern Caribbean Sea. Journal of Experimental Marine Biology and Ecology 407: 41-47.
18. C. D. Schubart, P. Zillner, S. Fuentes, and R. T. Bauer. 2009.Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Lysmatidae): The evolutionary origins of pair-living, protandric simultaneous hermaphroditism and species status. Biological Journal of the Linnaean Society 96: 415-424.
19. A. A. Braga, L. S. López-Greco, E. Perez, M. L. Negreiros- Fransozo, and A. Fransozo. 2010. Population dynamics, sex ratio and size at sex change in a protandric-simultaneous hermaphrodite, the spiny shrimp Exhippolysmata oplophoroides.Marine Biology 157: 2643-2653.
20. Baldwin, A. P., and R. T. Bauer. 2003. Growth, survivorship, life span, and sex change in the hermaphroditic shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). Marine Biology 143: 157-166. (Pubitemid 36967332)
21. 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. (Pubitemid 16277828)
22. -1986. Sex change and life history pattern in the shrimp Thor mannigi (Decapoda: Caridea): A novel case of partial protandric hermaphroditism. Biological Bulletin 170: 11-31.
23. -1989. Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical seagrass meadow. Journal of Experimental Marine Biology and Ecology 127: 175-187.
24. -1992. Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebrate Reproduction and Development 22: 193-202.
25. -2000. Simultaneous hermaphroditism in caridean shrimps: A unique and puzzling sexual system in the Decapoda. Journal of Crustacean Biology 20(Spec. No. 2): 116-128.
26. -2002. Reproductive ecology of a protandric simultaneous hermaphrodite, the shrimp Lysmata wurdemanni (Decapoda: Caridea: Hippolytidae). Journal of Crustacean Biology 22: 742-749.
27. -2004. Remarkable Shrimps. Oklahoma University Press, Norman, USA. . 2006. Same sexual system but variable sociobiology: Evolution of protandric simultaneous hermaphroditism in Lysmata shrimps. Integrative and Comparative Biology 46: 430-438.
28. and G. J. Holt. 1998. Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): An undescribed sexual system in the decapod Crustacea. Marine Biology 132: 223-235. (Pubitemid 28488041)
29. and S. Laporte. 2011. Gonochoric sexual system in the caridean shrimps Processa riveroi and P. bermudensis (Decapoda: Processidae) inhabiting a tropical seagrass meadow. Journal of the Marine Biological Association of the United Kingdom. doi:10.1017/S0025315411000622.
30. and W. A. Newman. 2004. Protandric simultaneous hermaphroditism in the marine shrimp Lysmata californica (Caridea: Hippolytidae). Journal of Crustacean Biology 24: 131-139. (Pubitemid 38215641)
31. and R. VanHoy. 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. (Pubitemid 26351541)
32. Becker, J. H. A., and A. S. Grutter. 2005. Client-fish ectoparasite loads and cleaner-shrimp hunger levels affect the cleaning behaviour of the cleanershrimp Urocaridella sp. C. Animal Behavior 70: 991-996. (Pubitemid 41505425)
33. Bergström, B. I. 2000. The biology of Pandalus. Advances in Marine Biology 38: 55-245.
34. Boddeke, R., J. R. Bosschieter, and P. C. Goudswaard. 1991. Sex change, mating, and sperm transfer in Crangon crangon (L.), pp. 164-182.In, R. T. Bauer and J. W. Martin (eds.), Crustacean Sexual Biology. Columbia University Press, New York, USA.
35. Braga, A. A., L. S. López-Greco, D. C. Santos, and A. Fransozo. 2009.Morphological evidence for protandric simultaneous hermaphroditism in the caridean Exhippolysmata oplophoroides. Journal of Crustacean Biology 29: 34-41.
36. 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: 1-179.
37. -1997. The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine Expedition, 1907-1910, Part 7: Families Atyidae, Eugonatonotidae, Rhynchocinetidae, Bathypalaemonellidae, Processidae, and Hippolytidae. Smithsonian Contributions to Zoology 587: 1-106.
38. Charnov, E. L. 1982. The Theory of Sex Allocation. Princeton University Press, Princeton, USA. , and J. J. Bull. 1989. Non-Fisherian sex ratios with sex change and environmental sex determination. Nature 338: 148-150.
39. Christoffersen, M. L. 1987. Phylogenetic relationships of hippolytid genera, with an assignment of new families for the Crangonoidea and Alpheoidea (Crustacea, Decapoda, Caridea). Cladistics 3: 348-362.
40. Clark, J. 1989. Koror misticius, new genus, new species (Decapoda: Hippolytidae), a cave shrimp from Palau. Journal of Crustacean Biology 9: 445-452.
41. De Grave, S. D., N. D. Pentcheff, S. T. Ahyong, T.-Y. Chan, K. A. Crandall, P. C. Dworschak, D. L. Felder, R. M. Feldmann, C. H. J. M. Fransen, L. Y. D. Goulding, R. Lemaitre, M. E. Y. Low, J. M. Martin, P. K. L. Ng, C. E. Schweitzer, S. H. Tan, D. Tshudy, and R. Wetzer. 2009. A classification of living and fossil genera of decapod crustaceans. Raffles Bulletin of Zoology, Supplement 21: 1-109.
42. 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.
43. Espinoza-Fuenzalida, N. L., M. Thiel, E. Dupre, and J. A. Baeza. 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.
44. Felder, D. L. 1982. Reproduction of the snapping shrimps Synalpheus fritzmuelleri and S. apioceros (Crustacea: Decapoda: Alpheidae) on a sublittoral reef off Texas. Journal of Crustacean Biology 2: 535-543.
45. Fiedler, G. C. 1998. Functional, simultaneous hermaphroditism in femalephase Lysmata amboinensis (Decapoda: Caridea: Hippolytidae). Pacific Science 52: 161-169. (Pubitemid 128587651)
46. A. L. Rhyne, R. Segawa, T. Aotsuka, and N. V. Schizas. 2010. The evolution of euhermaphroditism in caridean shrimps: A molecular perspective of sexual systems and systematics. BMC Evolutionary Biology 10: 297. doi:10.1186/1471-2148-10-297.
47. Gavio, M. A., J. M. Orensanz, and D. Amstrong. 2006. Evaluation of alternative life history hypotheses for the sand shrimp Crangon franciscorum (Decapoda: Caridea). Journal of Crustacean Biology 26: 295-307. (Pubitemid 44452877)
48. 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 American Association for the Advancement of Science 3: 167-201.
49. Gordon, I. 1935. On new or imperfectly known Species of Crustacea Macrura. Journal of the Linnean Society, Zoology 39: 307-351.
50. Guérin-Méneville, F. E. 1855. Animales articulados con piés articulados. In, R. de la Sagra (ed.), Historia física política y natural de la isla de Cuba. Segunda Parte. Historia Natural. Tomo VIII (Atlas de Zoologia): 1-371.
51. Holthuis, L. B. 1948. Note on some Crustacea Decapod Natantia from Surinam. Proceedings van de Koninklijke Nederlandsche Akademie van Wetenschappen 51: 1104-1113.
52. Hufnagl, M., A. Temming, and A. Dänhardt. 2010. Hermaphroditism in brown shrimp: Lessons from field data and modelling. Marine Biology 157: 2097-2108.
53. Kingsley, J. S. 1878. Notes on the North American Caridea in the Museum of the Peabody Academy of Science at Salem, Mass. Proceedings of the Academy of Natural Sciences of Philadelphia 1878: 89-98.
54. Lacoursière-Roussel, A., and B. Sainte-Marie. 2009. Sexual system and female spawning frequency in the sculptured shrimp Sclerocrangon boreas (Decapoda: Caridea: Crangonidae). Journal of Crustacean Biology 29: 192-200.
55. Limbaugh, C., H. Pederson, and F. A. Chace Jr. 1961. Shrimps that clean fishes. Bulletin of Marine Science 11: 237-257.
56. Linnaeus, C. 1758. Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. Edition 10. Vol. 1. Laurentii Salvii, Holmiae.
57. Manning, R. B., and F. A. Chace Jr. 1971. Shrimps of the family Processidae from the Northwestern Atlantic Ocean (Crustacea: Decapoda: Caridea). Smithsonian Contributions to Zoology 89: 1-41.
58. Noël, P. 1976. L'évolution des caractères sexuels chez Processa edulis Risso (Décapode, Natantia). Vie Milieu 26: 65-104.
59. Oh, C. W., and R. G. Hartnoll. 2004. Reproductive biology of the common shrimp Crangon crangon (Decapoda: Crangonidae) in the central Irish Sea. Marine Biology 144: 303-316. (Pubitemid 38231386)
60. Olive, P. J. W. 1992. The adaptive significance of seasonal reproduction in marine invertebrates: The importance of distinguishing between models. Invertebrate Reproduction and Development 22: 165-174.
61. 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.
62. Rathbun, M. J. 1900. Results of the Branner-Agassiz expedition to Brazil. I. The decapod and stomatopod Crustacea. Proceedings of the Washington Academy of Sciences 2: 133-156.
63. Rhyne, A. L., and J. Lin. 2006. A western Atlantic peppermint shrimp complex: Redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Sciences 79: 165-204. (Pubitemid 44298557)
64. Risso, A. 1816. Histoire naturelle des Crustacés des environs de Nice. La Librairie Greque-Latine-Allemande, Paris, France.
65. Sastry, A. N. 1983. Ecological aspects of reproduction, pp. 179-270. In, J. J. Vernberg and W. B. Vernberg (eds.), The Biology of Crustacea. Vol. 8.Academic Press, New York, USA.
66. Schatte, J., and R. Saborowski. 2006. Change of external sexual characteristics during consecutive moults in Crangon crangon L. Helgoland Marine Research 60: 70-73. (Pubitemid 43362039)
67. Schmitt, W. L. 1924. The Macrura and Anomura collected by the Williams Galapagos Expedition, 1923. Zoologica, New York 4: 161-171.
68. Spence Bate, C. 1888. Report on the Crustacea Macrura collected by the Challenger during the years 1873-76. Report on the Scientific Results of the Voyage of H.M.S. "Challenger" during the years 1873-76 24: 1-942.
69. Verrill, A. E. 1869. On the parasitic habits of Crustacea. The American Naturalist 3: 239-250.
70. Wilson, K., and I. C.W. Hardy. 2002. Statistical analysis of sex ratios: An introduction, pp. 48-92. In, I. C. W. Hardy (ed.), Sex Ratios: Concepts and Research Methods. Cambridge University Press, Cambridge, England.
71. Zhang, D., and J. Lin. 2007. Effects of density and simulated recruitment and mortality on sex change in a protandric simultaneous hermaphroditic shrimp, Lysmata wurdemanni. Marine Biology 150: 639-645. (Pubitemid 44952963)