Sexual Biology and Mating Behaviour in Decapod Crustaceans: A Case Study with Coral Reef Dwelling Caridean Shrimps

Jump To References Section

Authors

  • Department of Zoology, University of Madras, Guindy Campus, Chennai - 600025 ,IN

DOI:

https://doi.org/10.18311/jer/2023/31247

Abstract

Crustaceans have diversified sexual systems, incorporating various reproductive modalities such as gonochorism and a wide variety of hermaphroditism. In particular, the coral reef- dwelling caridean shrimps, living in symbiosis with other marine invertebrates, have developed unusual sexual systems that have given origin to a range of social systems, including the highly advanced eusociality. Protandric hermaphroditism, common among the caridean shrimps, has also reached a unique sexual condition, known as protandric simultaneous hermaphroditism, in the genus, Lysmata. Similarly, mating systems in the caridean shrimps are highly diverse and divergent. In addition, their occurrence in the coral reef shrimps is correlated to their life style adaptations such as their commensal association with other invertebrates. Other ecological factors like the predation risk from outside of the host animals and differences in the host characteristics may also be the driving forces in determining mating associations. Furthermore, the transition from sexual monogamy to social monogamy under conditions of their symbiotic life led to complex community living in several synalpheid shrimps. Understandably, the existence of various sexual and mating systems in these caridean shrimps has a dependence on the eco- social conditions prevalent in the coral reef biota.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Downloads

Published

2023-05-19

How to Cite

Subramoniam, T. (2023). Sexual Biology and Mating Behaviour in Decapod Crustaceans: A Case Study with Coral Reef Dwelling Caridean Shrimps. Journal of Endocrinology and Reproduction, 27(1), 01–14. https://doi.org/10.18311/jer/2023/31247

Issue

Section

Invited Review Article

 

References

Zhang XG, Siveter DJ, Waloszek D, Maas A. An epipodite- bearing crown-group crustacean from the Lower Cambrian. Nature. 2007; 449(7162):595-8. https://doi. org/10.1038/nature06138 PMid:17914395 DOI: https://doi.org/10.1038/nature06138

Bruce AJ. A report on a small collection of pontoniinid shrimps from the Island of Farquhar (Decapoda, Palaemonidae). Crustaceana. 1974; 27(2):189-203. https://doi.org/10.1163/156854074X00415 DOI: https://doi.org/10.1163/156854074X00415

Bauer RT. Remarkable shrimps: adaptations and natural history of the carideans. Norman: University of Oklahoma Press; 2004.

Subramoniam T. Origin and occurrence of sexual and mating systems in Crustacea: A progression towards communal living and eusociality. Journal of Biosciences. 2013; 38(5):951-69. https://doi.org/10.1007/s12038-013- 9392-x PMid:24296898 DOI: https://doi.org/10.1007/s12038-013-9392-x

Subramoniam T. Sexual biology and reproduction in crustaceans. New York and London: Elsevier/Academic Press; 2016. p. 508.

Dohrn PFR, Holthuis LB. Lysmata nilita, a new species of prawn (Crustacea: Decapoda) from the western Mediterranean. Pubblicazioni della Stazione Zoologica di Napoli. 1950; 22:339-47.

Bauer RT. Sex change and life history pattern in the shrimp Thor manningi (Decapoda: Caridea): A novel case of partial protandric hermaphroditism. Biology Bulletin. 1986; 170(1):11-31. https://doi.org/10.2307/1541377 DOI: https://doi.org/10.2307/1541377

Nakashima Y. Reproductive strategies in a partially protandrous shrimp, Athanas kominatoensis (Decapoda: Alpheidae): Sex change as the best of a bad situation for subordinates. Journal of Ethology. 1987; 5(2):145-59. https://doi.org/10.1007/BF02349947 DOI: https://doi.org/10.1007/BF02349947

Gherardi F, Calloni C. Protandrous hermaphroditism in the tropical shrimp Athanas indicus (Decapoda: Caridea), a symbiont of sea urchins. Journal of Crustacean Biology. 1993; 13(4):675-89. https://doi. org/10.1163/193724093X00246 DOI: https://doi.org/10.1163/193724093X00246

Bauer RT. Simultaneous hermaphroditism in caridean shrimps: A unique and puzzling sexual system in the Decapoda. Journal of Crustacean Biology. 2000; 20(5): 116-28. https://doi.org/10.1163/1937240X-90000014 DOI: https://doi.org/10.1163/1937240X-90000014

Ghiselin MT. A radical solution to the species problem. Systematic Biology. 1974; 23(4):536-44. https://doi. org/10.1093/sysbio/23.4.536 DOI: https://doi.org/10.1093/sysbio/23.4.536

Bauer RT, Newman WA. Protandric simultaneous hermaphroditism in the marine shrimp Lysmata californica (Caridea: Hippolytidae). Journal of Crustacean Biology. 2004; 24(1):131-9. https://doi.org/10.1651/C-2426 DOI: https://doi.org/10.1651/C-2426

Baeza JA. Social monogamy in the shrimp Pontonia margarita, a symbiont of Pinctada mazatlanica, off the Pacific coast of Panama. Marine Biology. 2008; 153(3):387-95. https://doi.org/10.1007/s00227-007-0815-9 DOI: https://doi.org/10.1007/s00227-007-0815-9

Bauer RT, Holt GJ. Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): An undescribed sexual system in the decapod Crustacea. Marine Biology. 1998; 132(2):223- 35. https://doi.org/10.1007/s002270050388 DOI: https://doi.org/10.1007/s002270050388

Baeza JA. The symbiotic lifestyle and its evolutionary consequences: Social monogamy and sex allocation in the hermaphroditic shrimp Lysmata pederseni. Naturwissenschaften. 2010; 97(8):729-41. https:// doi.org/10.1007/s00114-010-0689-4 PMid:20552156 DOI: https://doi.org/10.1007/s00114-010-0689-4

Subramoniam T. Reproductive modes: Invertebrate animals. In: Skinner MK, et al., editors. Encyclopedia of Reproduction. Academic Press; 2018. pp. 32-40. https:// doi.org/10.1016/B978-0-12-809633-8.20533-5 DOI: https://doi.org/10.1016/B978-0-12-809633-8.20533-5

Subramoniam T. Spermatophores and sperm transfer in marine crustaceans. Advances in Marine Biology. 1993; 29:129-214. https://doi.org/10.1016/S0065- 2881(08)60131-5 DOI: https://doi.org/10.1016/S0065-2881(08)60131-5

Hartnoll RG. Mating in the Brachyura. Crustaceana. 1969; 16(2):161-81. https://doi.org/10.1163/156854069X00420 DOI: https://doi.org/10.1163/156854069X00420

Shuster SM, Wade MJ. Mating systems and strategies. Princeton: Princeton University Press; 2003. https://doi. org/10.1515/9780691206882 PMCid:PMC169947 DOI: https://doi.org/10.1515/9780691206882

Emlen ST, Oring LW. Ecology, sexual selection, and the evolution of mating systems. Science. 1977; 197(4300):215-23. https://doi.org/10.1126/science. 327542 PMid: 327542 DOI: https://doi.org/10.1126/science.327542

Baeza JA, Thiel M. The mating system of symbiotic crustaceans. A conceptual model based on optimality and ecological constraints. In: Duffy EJ, Thiel M, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. New York. Oxford Academic; 2007. p. 250-267. https://doi.org/10.1093/acp rof:oso/9780195179927.003.0012 DOI: https://doi.org/10.1093/acprof:oso/9780195179927.003.0012

Bauer RT, Abdalla JH. Male mating tactics in the shrimp Palaemonetes pugio (Decapoda, Caridea): Precopulatory mate guarding vs. pure searching. Ethology. 2001; 107(3):185-99. https://doi. org/10.1046/j.1439-0310.2001. 00636.x DOI: https://doi.org/10.1046/j.1439-0310.2001.00636.x

Bauer RT. Hermaphroditism in caridean shrimps: Mating systems, sociobiology, and evolution, with special reference to Lysmata. In: Duffy JE, Thiel M, editors. Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms. New York: Oxford Academic; 2007. p. 232-248. https://doi.org/10.1093/acp rof:oso/9780195179927.003.0011 PMid:17455015 DOI: https://doi.org/10.1093/acprof:oso/9780195179927.003.0011

Zhang D, Lin J, LeRoy Creswell R. Mating behavior and spawning of the banded coral shrimp Stenopus hispidus in the laboratory. Journal of Crustacean Biology. 1998; 18(3):511-8. https://doi.org/10.1163/193724098X00331 DOI: https://doi.org/10.1163/193724098X00331

Rufino MM, Jones DA. Binary individual recognition in Lysmata debelius (Decapoda: Hippolytidae) under laboratory conditions. Journal of Crustacean Biology. 2001; 21:388-92. https://doi.org/10.1163/20021975-99990139 DOI: https://doi.org/10.1163/20021975-99990139

Wickler W, Seibt, U. Monogamy in Crustacea and man. Zeitschriftfür Tierpsychologie. 1981; 57(34):215- 34. https://doi.org/10.1111/j.1439-0310.1981.tb01924.x DOI: https://doi.org/10.1111/j.1439-0310.1981.tb01924.x

Brusca R, Brusca GJ. Invertebrates. Sinauer Associates Incorporated; 2002.

Bruce AJ. On some pontoniine shrimps from Noumea, New Caledonia. Cahiers de l’Indo-Pacifique. 1980; 2(1):1-39.

Knowlton K. Progressive transmission of grey-scale and binary pictures by simple, efficient, and lossless encoding schemes. Proceedings of the IEEE. 1980; 68(7):885-96. https://doi.org/10.1109/PROC.1980.11754 DOI: https://doi.org/10.1109/PROC.1980.11754

Baeza JA, Gueron R, Simpson L, et al. Population distribution, host-switching, and chemical sensing in the symbiotic shrimp Lysmata pederseni: Implications for its mating system in a changing reef seascape. Coral Reefs. 2016; 35(4):1213-24. https://doi.org/10.1007/s00338- 016-1467-3 DOI: https://doi.org/10.1007/s00338-016-1467-3

Grafen A, Ridley M. A model of mate guarding. Journal of Theoretical Biology. 1983; 102(4):549-67. https://doi. org/10.1016/0022-5193(83)90390-9 DOI: https://doi.org/10.1016/0022-5193(83)90390-9

Correa C, Baeza JA, Hinojosa IA, et al. Male dominance hierarchy and mating tactics in the rock shrimp Rhynchocinetes typus (Decapoda: Caridea). Journal of Crustacean Biology. 2003; 23(1):33-45. https://doi. org/10.1163/20021975-99990313 DOI: https://doi.org/10.1163/20021975-99990313

Kleiman DG. Monogamy in mammals. The Quarterly Review of Biology. 1977; 52(1):39-69. https://doi. org/10.1086/409721 PMid:857268 DOI: https://doi.org/10.1086/409721

Wilson EO. The Insect Societies. Cambridge, MA: Belknap, Harvard Univ Press; 1971.

Subramoniam T. Emergence of eusociality in aquatic environment: Synalpheid shrimps show the way! Indian Journal Geo-Marine Sciences. 2017; 46 (08):1511-8.

Duffy JE. Eusociality in a coral-reef shrimp. Nature. 1996; 381(6582):512-4. https://doi.org/10.1038/381512a0 DOI: https://doi.org/10.1038/381512a0

Toth E, Bauer RT. Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps. Marine Biology. 2007; 151(5):1875-86. https://doi.org/10.1007/s00227-007-0618-z DOI: https://doi.org/10.1007/s00227-007-0618-z

Duffy EJ, Morrison CL, Macdonald KS. Colony defence and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behavioral Ecology and Sociobiology. 2002; 51(5):488-95. https://doi.org/10.1007/s00265-002- 0455-5 DOI: https://doi.org/10.1007/s00265-002-0455-5

Duffy JE. Ecology and evolution of eusociality in spongedwelling shrimp. In Duffy JE, Thiel M, editors. Evolution of Social and Sexual Systems: Crustaceans as Model Systems. London: Oxford University Press; 2007. p. 386- 408. https://doi.org/10.1093/acprof:oso/9780195179927. 003.0018 DOI: https://doi.org/10.1093/acprof:oso/9780195179927.003.0018

Bornbusch SL, Lefcheck JS, Duffy JE. Allometry of individual reproduction and defense in eusocial colonies: A comparative approach to trade-offs in social sponge-dwelling Synalpheus shrimps. PloSOne. 2018; 13(3):e0193305. https://doi.org/10.1371/journal. pone.0193305 PMid: 29538466 PMCid:PMC5851585 DOI: https://doi.org/10.1371/journal.pone.0193305

Andersson M. Sexual selection. Princeton: Princeton University Press; 1994.

Shuster SM. The reproductive behaviour of α-, β-, and γ-male morphs in Paracerceis sculpta, a marine isopod crustacean. Behaviour. 1992; 121(3):231-57. https://doi. org/10.1163/156853992X00381 DOI: https://doi.org/10.1163/156853992X00381

Correa C, Baeza JA, Dupré E, Hinojosa IA, Thiel M. Mating behavior and fertilization success of three ontogenetic stages of male rock shrimp Rhynchocinetes typus (Decapoda: Caridea). Journal of Crustacean Biology. 2000; 20(4):628-40. https://doi.org/10.1163/20021975- 99990086 DOI: https://doi.org/10.1163/20021975-99990086

Thiel M, Chak ST, Dumont CP. Male morphotypes and mating behavior of the dancing shrimp Rhynchocinetes brucei (Decapoda: Caridea). Journal of Crustacean Biology. 2010; 30(4):580-8. https://doi.org/10.1651/09- 3272.1 DOI: https://doi.org/10.1651/09-3272.1

Prakash S, Ajithkumar TT, Bauer R, Thiel M, Subramoniam T. Reproductive morphology and mating behavior in the hingebeak shrimp Rhynchocinetes durbanensis Gordon, 1936 (Decapoda: Caridea: Rhynchocinetidae) in India. Journal of the Marine Biological Association of the United Kingdom. 2016; 96(6):1331-40. https://doi. org/10.1017/S0025315415001083 DOI: https://doi.org/10.1017/S0025315415001083

Ghiselin MT. The evolution of hermaphroditism among animals. The Quarterly Review of Biology. 1969; 44(2):189-208. https://doi.org/10.1086/406066 PMid:4901396 DOI: https://doi.org/10.1086/406066

Atema, J and Steinbach, MA. Chemical communication and social behavior of the lobster Homarus americanus and other decapod Crustacea, In Duffy JE, Thiel M. (Eds.). Evolutionary Ecology of Social and Sexual Systems: Crustaceans as model organisms. Oxford University Press. 2007; 6:115-44. https://doi. org/10.1093/acprof:oso/9780195179927.003.0006 DOI: https://doi.org/10.1093/acprof:oso/9780195179927.003.0006

Bauer RT. Mating behaviour and spermatophore transfer in the shrimp Heptacarpus pictus (Stimpson) (Decapoda: Caridea: Hippolytidae). Journal of Natural History. 1976; 10(4):415-40. https://doi. org/10.1080/00222937600770321 DOI: https://doi.org/10.1080/00222937600770321

Bauer RT. Sex attraction and recognition in the caridean shrimp Heptacarpus paludicola Holmes (Decapoda: Hippolytidae). Marine and Freshwater Behaviour and Physiology. 1979; 6(3):157-74. https://doi. org/10.1080/10236247909378563 DOI: https://doi.org/10.1080/10236247909378563

Bruce AJ. Further information on Apopontonia dubia Bruce (Decapoda, Pontoniinae). Crustaceana. 1983; 45:210-3. https://doi.org/10.1163/156854083X00640 DOI: https://doi.org/10.1163/156854083X00640

Fujino T, Miyake S. Studies on the genus Onycocaris with descriptions of five new species (Crustacea, Decapoda, Palaemonidae). Journal of the Faculty of Agriculture, Kyushu University. 1969; 15(4):403-48. https://doi. org/10.5109/22795 DOI: https://doi.org/10.5109/22795

Bruce AJ. Pontoniine shrimps of Heron Island. Atoll Research Bulletin No. 245; 1981. p. 1-33. https://doi. org/10.5479/si.00775630.245. DOI: https://doi.org/10.5479/si.00775630.245.

Bruce AJ. Re-descriptions of two little-known Indo- West Pacific palaemonid shrimps, Periclimenes calmani Tattersall and P. delagoae Barnard. Journal of Natural History. 1987; 21(6):1415-32. https://doi. org/10.1080/00222938700770891 DOI: https://doi.org/10.1080/00222938700770891

Bruce AJ. The shrimps associated with indo-west pacific echinoderms with the description of a new species in the genus Periclimenes (Crustacea: Pontoniinae). Australian Museum Memoir. 1982; 191:16-8. https://doi.org/10.385 3/j.0067-1967.16.1982.366

Bruce AJ, Coombes KE. The palaemonoid shrimp fauna (Crustacea: Decapoda: Caridea) of the Cobourg Peninsula, Northern Territory. The Beagle, Records of the Museums and Art Galleries of the Northern Territory. 1995; 12:101-44. https://doi.org/10.5962/p.264281 DOI: https://doi.org/10.5962/p.264281

Prakash S, Ajithkumar TT, Subramoniam T. Sexual system and sexual dimorphism in the shrimp Periclimenes brevicarpalis (Schenkel, 1902) (Caridea: Palaemonidae), symbiotic with the sea anemone Stichodactyla haddoni (Saville-Kent, 1893) in the Gulf of Mannar, India. Journal of Crustacean Biology. 2017; 37(3):332-9. https://doi. org/10.1093/jcbiol/rux028 DOI: https://doi.org/10.1093/jcbiol/rux028

Bruce AJ, Svoboda A. Observations upon some pontoniine shrimps from Aqaba, Jordan. Rijksmuseum van Natuurlijke Historie. 1983; 205:3-44.

Gosliner TM, Behrens DW, Williams GC. Coral reef animals of the Indo-Pacific. Monterey: Sea Challengers; 1996.

Bruce AJ. Coral reef shrimps and their color patterns. Endeavour. 1975; 34:23-7. https://doi.org/10.1016/0160- 9327(75)90064-2 DOI: https://doi.org/10.1016/0160-9327(75)90064-2

Bruce AJ. Notes on Some Indo-Pacific Pontoniinae. XIV. Observations on Paratypton siebenrocki Balss. Crustaceana.1969; 17:171-86. https://doi.org/10.1163/ 156854068X00061 61. Bruce AJ, Svoboda A. A report on a small collection of coelenterate-associated pontoniine shrimps from Cebu, Philippines Islands. Asian Marine Biology. 1984; 1:87- 99. DOI: https://doi.org/10.1163/156854068X00061

Bruce AJ. Ctenopontonia cyphastreophila, a new genus and species of coral associated pontoniine shrimp from Eniwetok Atoll. Bulletin of Marine Science. 1979; 29(3):423-35.

Debelius H. Crustacea Guide of the World. Frankfurt, Germany: IKAN; 1999.

Bruce AJ. A report on a small collection of shrimps from the Kenya National Marine Parks at Malindi, with notes on selected species. Zoologische Verhandelingen. 1976; 145(1):1-72. 65. Wirtz P. Crustacean symbionts of the sea anemone Telmatactis cricoides at Madeira and the Canary Islands. Journal of Zoology. 1997; 242(4):799-811. https://doi. org/10.1111/j.1469-7998.1997.tb05827.x 66. Stanton G. Habitat partitioning among associated decapods with Lebrunia danae at Grand Bahama. In: Proceedings of the 3rd International Coral Reef Symposium; 1977. p. 169-75. DOI: https://doi.org/10.1111/j.1469-7998.1997.tb05827.x

Limbaugh C, Pederson H, Chace FA. Shrimps that clean fishes. Bulletin of Marine Science. 1961; 11(2):237-57. 68. Duffy JE. The ecology and evolution of eusociality in sponge-dwelling shrimp. In Kikuchi T, Azuma N, Higashi S, editors. Genes, Behaviour and Evolution in Social Insects, Sapporo: Hokkaido University Press; 2003. p. 217-52.

Morrison CL, Rios R, Duffy JE. Phylogenetic evidence for an ancient rapid radiation of Caribbean spongedwelling snapping shrimps (Synalpheus). Molecular Phylogenetics and Evolution. 2004; 30(3):563-81. https://doi.org/10.1016/S1055-7903(03)00252-5 PMid: 15012939 DOI: https://doi.org/10.1016/S1055-7903(03)00252-5

Toth E, Duffy JE. Coordinated group response to nest intruders in social shrimp. Biology Letters. 2005; 1(1):49-52. https://doi.org/10.1098/rsbl.2004.0237 PMid:17148125 PMCid:PMC1629045 DOI: https://doi.org/10.1098/rsbl.2004.0237

Duffy JE, Morrison CL, Ríos R. Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus). Evolution. 2000; 54(2):503-16. https:// doi.org/10.1111/j.0014-3820.2000.tb00053.x PMid: 10937227 DOI: https://doi.org/10.1111/j.0014-3820.2000.tb00053.x

Rios R, Duffy JE. A review of the sponge-dwelling snapping shrimp from Carrie Bow Cay, Belize, with description of Zuzalpheus, new genus, and six new species. Zootaxa. 2007; 1602:1-89. https://doi.org/10.11646/ zootaxa.1602.1.1 DOI: https://doi.org/10.11646/zootaxa.1602.1.1

Duffy JE, Macdonald KS. Colony structure of the social snapping shrimp Synalpheus filidigitus in Belize. Journal of Crustacean Biology. 1999; 19(2):283-92. https://doi. org/10.2307/1549235 DOI: https://doi.org/10.1163/193724099X00097

Duffy JE. On the frequency of eusociality in snapping shrimps (Decapoda: Alpheidae), with description of a second eusocial species. Bulletin of Marine Science. 1998; 62:387-400.

Didderen K, Fransen CH, De Voogd NJ. Observations on sponge-dwelling colonies of Synalpheus (Decapoda, Alpheidae) of Sulawesi, Indonesia. Crustaceana. 2006; 79:961-75. https://doi.org/10.1163/ 156854006778815937 DOI: https://doi.org/10.1163/156854006778815937

Hultgren KM, Brandt A. Taxonomy and phylogenetics of the Synalpheus paraneptunus-species-complex (Decapoda: Alpheidae), with a description of two new species. Journal of Crustacean Biology. 2015; 35(4):547- 58. https://doi.org/10.1163/1937240X-00002354 DOI: https://doi.org/10.1163/1937240X-00002354