Sexual selection in hermit crabs: A review and outlines of future research

Journal of Zoology

Volumn 270, Issue 4, 2006, Pages 595-605

  Contreras Garduno J ^a   Cordoba Aguilar A ^a  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

Cryptic female choice; Female choice; Hermit crabs; Male male competition; Sexual conflict; Sperm competition

Indexed keywords

COMPETITION (ECOLOGY); COPULATION; CRAB; EGG PRODUCTION; FERTILIZATION (REPRODUCTION); MATE GUARDING; SEXUAL CONFLICT; SEXUAL SELECTION;

ANIMALIA; BIRGUS; DECAPODA (CRUSTACEA); PARAPAGURUS;

EID: 33750980381     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2006.00182.x     Document Type: Review

References (121)

1. Alexander, R.D., Marshall, D.C. & Cooley, J.R. (1997). Evolutionary perspectives on insect mating. In The evolution of mating systems in insects and arachnids: 4-31. Choe, J.C. & Crespi, B.J. (Eds). Cambridge: Cambridge University Press.
2. Andersson, M.R. (1994). Sexual selection. Princeton, NJ: Princeton University Press.
3. Arnqvist, G. (1997). The evolution of animal genitalia: distinguishing between hypotheses by single species studies. Biol. J. Linn. Soc. 60, 365-379.
4. Arnqvist, G. & Nilsson, T. (2000). The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60, 145-164.
5. Asakura, A. (1995). Sexual differences in life history and resource utilization by the hermit crab. Ecology 76, 2295-2313.
6. Bertness, M.D. (1981a). Predation, physical stress and the organisation of a tropical rocky intertidal hermit crab community. Ecology 62, 411-425.
7. Bertness, M.D. (1981b). Pattern and plasticity in tropical hermit crab growth and reproduction. Am. Nat. 117, 2295-2313.
8. Bertness, M.D. (1981c). The influence of shell-type on hermit crab growth rate and clutch size (Decapoda, Anomura). Crustaceana 40, 197-205.
9. Bertness, M.D. (1981d). Interference, exploitation, and sexual components of competition in a tropical hermit crab assemblage. J. Exp. Mar. Biol. Ecol. 49, 189-202.
10. Birkhead, T.R. & Møller, A.P. (1998). Sperm competition and sexual selection. London: Academic Press.
11. Bonduriansky, R. (2001). The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol. Rev. 76, 305-339.
12. Briffa, M. & Elwood, R.W. (2000a). Analysis of the fine scale timing of repeated signals: does shell rapping in hermit crabs signal stamina? Anim. Behav. 59, 159-165.
13. Briffa, M. & Elwood, R.W. (2000b). The power of shell rapping influences rates of eviction in hermit crabs. Behav. Ecol. 11, 288-293.
14. Briffa, M. & Elwood, R.W. (2000c). Cumulative or sequential assessment during hermit crab shell fights: effects of oxygen on decision rules. Proc. Roy. Soc. Lond. Ser. B 267, 2445-2452.
15. Briffa, M. & Elwood, R.W. (2004). Use of energy reserves in fighting hermit crabs. Proc. Roy. Soc. Lond. Ser. B 271, 373-379.
16. Briffa, M. & Elwood, R.W. (2005a). Metabolic consequences of shell choice in Pagurus bernhardus: do hermit crabs prefer cryptic or portable shells. Behav. Ecol. Sociobiol. 59, 143-148.
17. Briffa, M. & Elwood, R.W. (2005b). Rapid change in energy status in fighting animals: causes and effects of strategic decisions. Anim. Behav. 70, 119-124.
18. Briffa, M., Elwood, R.W. & Dick, J.T.A. (1998). Analysis of repeated signals during shell fights in the hermit crab Pagurus bernhardus. Proc. Roy. Soc. Lond. Ser. B 265, 1467-1474.
19. Chapman, T., Arnqvist, G., Bangham, J. & Rowe, L. (2003). Sexual conflict. Trends Ecol. Evol. 18, 41-47.
20. Childress, J.L. (1972). Behavioral ecology and fitness theory in a tropical hermit crab. Ecology 53, 960-964.
21. Christy, J.H. (1987). Female choice and the breeding behavior of the fiddler crab Uca beeberi. J. Crust. Biol. 7, 624-635.
22. Contreras-Garduño, J. (2001). Elección de concha en el cangrejo ermitaño Coenobita compressus: el papel del volumen, el peso y el grosor de la concha. BSc dissertation, Universidad Nacional Autónoma del Estado de México, Mexico.
23. Cordero, C. & Eberhard, W.G. (2003). Female choice of sexually antagonistic male adaptations: a critical review of some current research. J. Evol. Biol. 16, 1-6.
24. Córdoba-Aguilar, A. (1999). Male copulatory sensory stimulation induces female ejection of rival sperm in a damselfly. Proc. Roy. Soc. Lond. Ser. B 266, 779-784.
25. Córdoba-Aguilar, A. & Contreras-Garduño, J. (2003). Sexual conflict. Trends Ecol. Evol. 18, 439-440.
26. Cunningham, E.J.A. & Birkhead, T.R. (1998). Sex roles and sexual selection. Anim. Behav. 56, 1311-1321.
27. Darwin, C. (1871). The descent of man and selection in relation to sex. London: John Murray.
28. Diesel, R. (1988). Male-female association in the spider crab Inachus phalangium: the influence of female reproductive stage and size. J. Crust. Biol. 8, 63-69.
29. Dowds, B.M. & Elwood, R.W. (1983). Shell wars: assessment strategies and the timing of decisions in hermit crab shell fights. Behaviour 85, 1-24.
30. Dowds, B.M. & Elwood, R.W. (1985). Shell wars II: the influence of relative size on decisions made during hermit crab shell fights. Anim. Behav. 33, 649-656.
31. Eberhard, W.G. (1985). Sexual selection and animal genitalia. Harvard: Harvard University Press.
32. Eberhard, W.G. (1996). Sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.
33. Eberhard, W.G. (2004). Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice. Evolution 58, 1947-1970.
34. Elwood, R.W. & Briffa, M. (2001). Information gathering and communication during agonistic encounters: a case study of hermit crabs. In Adv. Study Behav 30, 53-97 Slater, P.J., Rosenblatt, J.S., Snowdon, C.T. & Poper, T.J. (Eds). San Diego: California Academic Press.
35. Elwood, R.W., Gibson, J. & Neil, S. (1987). The amorous Gammarus: size-assortative mating in G. pulex. Anim. Behav. 35, 1-6.
36. Elwood, R.W. & Neil, S.J. (1992). Assessments and decisions: a study of information gathering by hermit crabs. London: Chapman & Hall.
37. Fotheringham, N. (1976). Population consequences of shell utilisation by hermit crabs. Ecology 57, 570-578.
38. Freshney, R. (1987). Culture of animal cells: a manual of basic technique. New York: Allan R. Liss.
39. Gherardi, F. (2004). Resource partitioning between sexes in the "unconventional" hermit crab, Calcinus tubularis. Behav. Ecol. 15, 742-747.
40. Gherardi, F. (2006). Fighting behaviour in hermit crabs: the combined effect of resource-holding potential and resource value in Pagurus longicarpus. Behav. Ecol. Sociobiol. 59, 500-510.
41. Goshima, S., Ito, K., Wada, S., Shimizu, M. & Nakao, S. (1995). Reproductive biology of the stone crab Hapalogaster dentata (Anomura; Lithodidae). Crust. Res. 24, 8-18.
42. Goshima, S., Kawashima, T. & Wada, S. (1998). Mate choice by males of the hermit crabs Pagurus filholi: do males assess ripeness and/or fecundity of females? Ecol. Res. 13, 151-161.
43. Goshima, S., Wada, S. & Ohmori, H. (1996). Reproductive biology of the hermit crab Pagurus nigrofasciata (Anomura: Paguridae). Crust. Res. 25, 86-92.
44. Hamon, M. (1937). Les mécanismes produisant la déhiscence des spermatophores d' Eupagurus prideaux Leach. C. R. Acad. Sci. Paris 204, 1504-1506.
45. Hamon, M. (1939a). La constitution chimique des spermatophores de crustacés supérieurs du groupe des pagurides. C. R. Soc. Biol. Paris 130, 1312-1315.
46. Hamon, M. (1939b). Détermination de la présence de certains acides α aminés dans les spermatophores des pagurides. C. R. Soc. Biol. Paris 131, 109-110.
47. Hazlett, B.A. (1966). Social behavior of the Paguridae and Diogenidae of Curacao. Stud. Fauna Curacao 23, 1-143.
48. Hazlett, B.A. (1968). The sexual behavior of some European hermit crabs. Pubbl. Staz. Zool. Napoli 36, 238-252.
49. Hazlett, B.A. (1970). Tactile stimuli in the social behavior of Pagurus bernhardus (Decapoda, Paguridae). Behaviour 36, 20-40.
50. Hazlett, B.A. (1972). Shell fighting and sexual behavior in the hermit crab genera Paguristes and Calcinus, with comments on Pagurus. Bull. Mar. Sci. 22, 806-823.
51. Hazlett, B.A. (1973). Ethological analyses of reproductive behavior in the marine Crustacea. Pubbl. Staz. Zool. Napoli 39, 677-695.
52. Hazlett, B.A. (1981). The behavioural ecology of hermit crabs. Annu. Rev. Ecol. Syst. 12, 1-22.
53. Hazlett, B.A. (1989). Mating success of male hermit crabs in shell generalist and shell specialist species. Behav. Ecol. Sociobiol. 25, 119-128.
54. Hazlett, B.A. (1996a). Reproductive behaviour of the hermit crab Clibanarius vittatus (Bosc. 1802). Bull. Mar. Sci. 58, 668-674.
55. Hazlett, B.A. (1996b). Precopulatory behaviour of the hermit crabs Diogenes avarus and Clibanarius virescens. Aust. J. Zool. 44, 487-492.
56. Hazlett, B.A. & Baron, L.R. (1989). Influence of shells on mating behavior in hermit crab Calcinus tibicen. Behav. Ecol. Sociobiol. 24, 369-376.
57. Hazlett, B.A. & Rittschof, D. (2000). Predation-reproduction conflict resolution in the hermit crab, Clibanarius vittatus. Ethology 106, 811-818.
58. Helfman, G.S. (1977). Copulatory behaviour of the coconut or robber crab Birgus latro (L.) (Decapoda Anomura, Paguridea, Coenobitidae). Crustaceana 33, 198-202.
59. Hess, G.S. & Bauer, R.T. (2002). Spermatophore transfer in the hermit crab Clibanarius vittatus (Crustace, Anomura, Diogenidae). J. Morphol. 253, 166-175.
60. Hinsch, G.W. (1980). Spermiogenesis in Coenobita clypeatus, I. Sperm structure. Int. J. Invert. Rep. 2, 189-198.
61. Holland, B. & Rice, W.R. (1998). Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52, 1-7.
62. Hosken, D.J. & Stockley, P. (2004). Sexual selection and genital evolution. Trends Ecol. Evol. 19, 87-93.
63. House, C.M. & Simmons, L.W. (2003). Genital evolution and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proc. Roy. Soc. Lond. Ser. B 270, 447-455.
64. Hunter, F.M. & Birkhead, T.R. (2002). Sperm viability and competition in insects. Curr. Biol. 12, 121-123.
65. Imafuku, M. (1986). Sexual discrimination in the hermit crab Pagurus geminus. J. Ethol. 4, 39-47.
66. Imafuku, M. (2002). Ecology of the land hermit crab Coenobita purpureus on kikaijima Island. II. Breeding behavior, food, orientation and environment. Mem. Fac. Sci., Kyoto Univ., Ser. Biol. Kioto. University, Japan 18, 15-34.
67. Imafuku, M. & Ando, T. (1999). Behaviour andmorphology of pagurid hermit crabs (Decapoda, Anomura) that live in tusk shells (Mollusca, Scaphopoda). Crustaceana 72, 129-144.
68. Lemaitre, R. & McLaughlin, P.A. (2003). A new species of Goreopagurus (Decapoda: Anomura: Paguridae) from Tasmania and re-evaluation of sexual tubes in hermit crab systematics. Mem. Mus. Vic. 60, 85-90.
69. Litulo, C. (2005). Population dynamics and reproduction of the hermit crab Calcinus gaimardii (Anomura: Diogenidae) at Inhaca Island, southern Mozambique. J. Nat. Hist. 39, 3359-3367.
70. Litulo, C. & Tudge, C. (2005). Population structure and breeding season of the hermit crab Diogenes brevirostris Stimpson, 1858 (Decapoda, Anomura, Diogenidae) from southern Mozambique. J. Nat. Hist. 39, 2887-2899.
71. Manjón-Cabeza, M.E. & García Raso, J.E. (2000). Reproductive aspects of females of the hermit crab Diogenes pugilator (Crustacea: Decapoda: Anomura) from southern Spain. J. Mar. Biol. Assoc. UK 80, 85-93.
72. Manning, J.T. (1975). Male discrimination and investment in Asellus aquaticus (L.) and A. meridianus Racovitsza (Crustacea: Isopoda). Behaviour 55, 1-14.
73. Mantelatto, F.L.M. & Martinelli, J.M. (2001). Relative growth and sexual dimorphism of the South Atlantic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from Ubatuba, Brazil. J. Nat. Hist. 35, 429-437.
74. Matthews, D.C. (1956). The probable method of fertilization in terrestrial hermit crabs based on a comparative study of spermatophores. Pac. Sci. 10, 303-309.
75. McLaughlin, P.A. (2003). Illustrated keys to families and genera of the superfamiliy Paguroidea (Crustacea: Decapoda: Anomura), with supplemental diagnoses of the genera of the Paguridae. Mem. Mus. Vic. 60, 111-144.
76. Mikkola, K. (1992). Evidence for lock-and key mechanisms in the internal genitalia of the Apomea moths (Lepidoptera, Noctuidae). Syst. Entomol. 17, 145-153.
77. Minouchi, S. & Goshima, S. (1998). Effect of male/female size ratio on mating behavior of the hermit crab Pagurus filholi (Anomura: Paguridae) under experimental conditions. J. Crust. Biol. 18, 710-716.
78. Minouchi, S. & Goshima, S. (2000). The effect of male size and sex ratio on the duration of precopulatory mate guarding in the hermit crab Pagurus filholi. Benthos Res. 55, 37-41.
79. Mouchet, S. (1931). Spermatophores des crustacés décapodes anomoures et brachyoures et castration parasitaire chez quelques Pagures. Ann. Stat. Oceánogr. Salammbo 6, 1-203.
80. Mura, M., Orru, F. & Cau, A. (2006). Reproduction strategies of the deep sea hermit crabs Pagurus alatus and Pagurus excavatus of the central-western Mediterranean sea. Hydrobiologia 557, 51-57.
81. Osorno, J.L., Contreras-Garduño, J. & Macías- García, C. (2005). Long-term costs of using heavy shells in terrestrial hermit crabs and the limit of a shell preference: an experimental study. J. Zool. (Lond.) 266, 377-383.
82. Osorno, J.L., Fernández-Casillas, F. & Rodríguez- Juárez, C. (1998). Are hermit crabs looking for light and large shells?: evidence from natural and field induced shell-exchanges. J. Exp. Mar. Biol. Ecol. 222, 163-173.
83. Parker, G.A. (1970). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525-567.
84. Parker, G.A. (1998). Sperm competition and the evolution of the ejaculates: towards a theory base. In Sperm competition and sexual selection: 3-54. Birkhead, T.R. & Møller, A.P. (Eds). London: Academic Press.
85. Peretti, A.V. (2003). Functional morphology of spermatophores and female genitalia in bothriurid scorpions: genital courtship, coercion and other possible mechanisms. J. Zool. (Lond.) 261, 135-153.
86. Pérez, C. (1930). Asymétrie viscerale et dimorphism des spermatophores chez quelques Pagures. C. R. Acad. Sci. 190, 393-396.
87. Pitnick, S. & Brown, W.D. (2000). Criteria for demonstrating female sperm choice. Evolution 54, 1052-1056.
88. Reyer, H.-U., Frei, G. & Som, C. (1998). Cryptic female choice: frogs reduce clutch size when amplexed by undesired males. Proc. Roy. Soc. Lond. Ser. B 266, 2101-2107.
89. Rondeau, A. & Sainte-Marie, B. (2001). Variable mateguarding time and sperm allocation by male snow crabs (Chionoecetes opilio) in response to sexual competition, and their impact on the mating success of females. Biol. Bull. 201, 204-217.
90. Sato, T., Ashidae, M., Wada, S. & Goshima, S. (2005). Effects of male mating frequency and male size on ejaculate size and reproductive success of female spiny crab Paralithodes brevipes. Mar. Ecol. Prog. Ser. 296, 251-262.
91. Scelzo, M.A., Mantelatto, F.L. & Tudge, C.C. (2004). Spermatophore morphology of the endemic hermit crab Loxopagurus loxochelis (Anomura, Diogenidae) from the southwestern Atlantic-Brasil and Argentina. Invert. Rep. Dev. 46, 1-9.
92. Schuster, S.M. (1981). Sexual selection in the socorro isopod, Thermosphaeroma thermophilium (Cole) (Crustacea: Peracarida). Anim. Behav. 29, 698-707.
93. Simmons, L.W. (2001). Sperm competition and its evolutionary consequences in the insects. Princeton, NJ: Princeton University Press.
94. Simmons, L.W. & Siva-Jothy, M.T. (1998). Sperm competition in insects: mechanisms and the potential for selection. In Sperm competition and sexual selection: 341-434. Birkhead, T.R. & Moller, A.P. (Eds). London: Academic Press.
95. Thornhill, R. (1983). Cryptic female choice and its implications in the scorpionfly Harpobitacus nigriceps. Am. Nat. 122, 765-788.
96. Tudge, C.C. (1991). Spermatophore diversity within and among the hermit crab families, Coenobitidae, Diogenidae, and Paguridae (Paguroidea, Anomura, Decapoda). Biol. Bull. Woods Hole 181, 238-247.
97. Tudge, C.C. (1992). Comparative ultrastructure of hermit crab spermatozoa (Decapoda: Anomura: Paguroidea). J. Crust. Biol. 12, 397-409.
98. Tudge, C.C. (1995). Ultrastructure and phylogeny of the spermatozoa of the infraorders Thalassinidea and Anomura (Decapoda: Crustacea). In Advances in spermatozoal phylogeny and taxonomy. Jamieson, B.G.M., Ausio, J. & Justine, J.-L. (Eds). Mem. Mus. Natn. Hist. Nat. Paris 166: 251-263. Paris, France: Éditions du Muséum.
99. Tudge, C.C. (1996). Spermatophore morphology and spermatozoal ultrastructure of the recently described hermit crab, Strigopagurus boreonotus Forest, 1995 (Decapoda, Anomura, Diogenidae). Bull. Mus. Nat. Hist. Nat. Paris 18, 251-259.
100. Tudge, C.C. (1997). Phylogeny of the Anomura (Decapoda, Crustacea): spermatozoa and spermatophore morphological evidence. Contrib. Zool. Amsterdam 67, 125-141.
101. Tudge, C.C. (1999a). Ultrastructure of the spermatophore lateral ridge in hermit crabs (Decapoda, Anomura, Paguroidea). Crustaceana 72, 77-84.
102. Tudge, C.C. (1999b). Spermatophore morphology in the hermit crab families Paguridae and Parapaguridae (Paguroidea, Anomura, Decapoda). Invert. Reprod. Dev. 35, 203-214.
103. Tudge, C.C. & Jamieson, B.G.M. (1991). Ultrastructure of the mature spermatozoon of the coconut crab Birgus latro (Coenobitidae: Paguroidea: Decapoda). Mar. Biol. 108, 395-402.
104. Tudge, C.C. & Lemaitre, R. (2004). Studies of male sexual tubes in hermit crabs (Crustacea, Decapoda, Anomura, Paguroidea). 1. Morphology of sexual tube in Micropagurus acantholepis (Stimpson, 1858), with comments on function and evolution. J. Morphol. 259, 106-118.
105. Tudge, C.C., Scheltinga, D.M. & Jamieson, B.G.M. (2001). Spermatozoal morphology in the "symmetrical" hermit crab, Pylocheles (Bathycheles) sp. (Crustacea, Decapoda, Anomura, Paguroidea, Pylochelidae). Zoosystema 23, 117-129.
106. Turra, A. (2005). Reproductive behaviour of intertidal hermit crabs (Decapoda, Anomura) in southeastern Brazil. Rev. Bras. Zool. 22, 313-319.
107. Wada, S. (1999). Enviromental factors affecting sexual size dimorphism in the hermit crab Pagurus middendorffii. J. Mar. Biol. Assoc. UK 79, 953-954.
108. Wada, S. (2000). Seasonal growth pattern and the effect of gastropod shells on sexual growth rates in the hermit crab Pagurus middendorffii. Bull. Fac. Fish. Hokkaido Univ. 51, 1-11.
109. Wada, S. (2001). Reproductive characters and population structure of the subtidal hermit crab Pagurus ochotensis (Anomura: Paguridae). Benthos Res. 56, 43-46.
110. Wada, S., Ashidate, M. & Goshima, S. (1997a). Observations of the reproductive behaviour of the spiny king crab Paralithodes brevipes (Anomura: Lithodidae). Crust. Res. 26, 56-61.
111. Wada, S., Goshima, S. & Nakao, S. (1995). Reproductive biology of the hermit crab Pagurus middendorffii Brandt (Decapoda: Anomura: Paguridae). Crust. Res. 24, 23-32.
112. Wada, S., Ishizaki, K., Kitaoka, H. & Goshima, S. (1999b). Shell utilization by hermit crab Pagurus lanuginosus: sexual differences and interspecific comparisons. Benthos Res. 54, 9-16.
113. Wada, S., Kitaoka, H. & Goshima, S. (2000b). Reproduction of the hermit crab Pagurus lanuginosus and comparison of the reproductive traits among sympatric species. J. Crust. Biol. 20, 474-478.
114. Wada, S., Masakazu, A., Yoshino, K., Sato, T. & Goshima, S. (2000a). Effects of sex ratio on egg extrusion frequency and mating behaviour of the spiny crab Paralithodes brevipes (Decapoda: Lithodidae). J. Crust. Biol. 20, 479-482.
115. Wada, S., Ohmori, H., Goshima, S. & Nakao, S. (1997b). Shell-size preference of hermit crabs depends on their growth rate. Anim. Behav. 54, 1-8.
116. Wada, S., Sonoda, T. & Goshima, S. (1996). Temporal size covariation of mating pairs of the hermit crab Pagurus middendorffii (Decapoda: Anomura: Paguridae) during a single breeding season. Crust. Res. 25, 158-164.
117. Wada, S., Tanaka, K. & Goshima, S. (1999a). Precopulatory mate guarding in the hermit crab Pagurus middendorffii: effects of population parameters on male guarding interactions. J. Exp. Mar. Biol. Ecol. 239, 289-298.
118. Wedell, N., Gage, M.J.G. & Parker, G.A. (2002). Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313-320.
119. Williams, J.D. & McDermott, J.J. (2004). Hermit crab biocoenoses: a worldwide review of diversity and natural history of hermit crab associates. J. Exp. Mar. Biol. Ecol. 305, 1-128.
120. Yamanoi, T., Yoshino, K., Kon, K. & Goshima, S. (in press). Delayed copulation as a means of female choice by the hermit crab Pagurus filholi. J. Ethol. in press.
121. Yoshino, K., Ozawa, M. & Goshima, S. (2004). Effects of shell size fit on the efficacy of mate guarding behaviour in male hermit crabs. J. Mar. Biol. Assoc. UK 84, 1203-1208.