Olfactory selectivity in intertidal hermit crabs: aggregation behavior by Pagurus criniticornis (Decapoda, Anomura) in response to simulated predation on the gastropod Cerithium atratum

Abstract

Hermit crabs respond to sensory cues that guide them toward limiting resources in marine and terrestrial environments. We examined the response of the common intertidal hermit crab Pagurus criniticornis (Dana, 1852) to simulated predation events on: (1) their principal shell donor Cerithium atratum (Born, 1778), (2) conspecifics, and (3) a sympatric bivalve; to test for the prevalence of olfactory specificity (i.e., attraction to a preferred gastropod species) or olfactory generality (i.e., attraction to a range of cues). Results showed that crabs were strongly attracted to gastropod baits but not to conspecifics or bivalves possibly reflecting greater motivation to acquire newly liberated resources than those more widely available (e.g., existing shells or food). We then examined the potential drivers of aggregative behavior by comparing the morphology and shell quality of attending individuals to an unbiased population. Although attending crabs were of a similar size and weight to the general population, their shells were of lower quality (adequacy, damage, and encrustation), suggesting that motivation to procure new shells is modulated by existing shell quality. The findings provide a clearer understanding of how hermit crabs acquire new resources and might have implications for the release and redistribution of other limiting resources within coastal environments.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Amaral, A. C. Z., A. E. Migotto, A. Turra & Y. Schaeffer-Novelli, 2010. Araçá: biodiversity, impacts and threats. Biota Neotropica: 10.

  2. Arnott, G. & R. W. Elwood, 2007. Fighting for shells: how private information about resource value changes hermit crab pre-fight displays and escalated fight behaviour. Proceedings of the Royal Society B-Biological Sciences 274: 3011–3017.

    Article  PubMed Central  Google Scholar 

  3. Arnott, G. & R. W. Elwood, 2008. Information gathering and decision making about resource value in animal contests. Animal Behaviour 76: 529–542.

    Article  Google Scholar 

  4. Bach, C. B., B. A. Hazlett & D. Rittschof, 1976. Effects of interspecific competition on fitness of the hermit crab Clibanarius tricolor. Ecology 57: 579–586.

    Article  Google Scholar 

  5. Barnes, D. K. A., 1999. Ecology of tropical hermit crabs at Quirimba Island. Mozambique, Shell characteristics and utilization. Marine Ecology Progress Series 183: 241–251.

    Article  Google Scholar 

  6. Bertness, M. D., 1981a. The influence of shell-type on hermit crab growth rate and clutch size (Decapoda, Anomura). Crustaceana 40: 197–205.

    Article  Google Scholar 

  7. Bertness, M. D., 1981b. Predation, physical stress and the organization of a tropical rocky intertidal hermit crab community. Ecology 62: 411–425.

    Article  Google Scholar 

  8. Bertness, M. D., 1981c. Competitive dynamics of a tropical hermit crab assemblage. Ecology 62: 751–761.

    Article  Google Scholar 

  9. Bertness, M. D. & C. Cunningham, 1981. Crab shell-crushing predation and gastropod architectural defense. Journal of Experimental Marine Biology and Ecology 50: 213–230.

    Article  Google Scholar 

  10. Borjesson, D. L. & W. A. Szelistowski, 1989. Shell selection, utilization and predation in the hermit crab Clibanarius panamensis (Stimpson) in a tropical mangrove estuary. Journal of Experimental Marine Biology and Ecology 133: 213–228.

    Article  Google Scholar 

  11. Briffa, M. & R. W. Elwood, 2000. The power of shell rapping influences rates of eviction in hermit crabs. Behavioral Ecology 11: 288–293.

    Article  Google Scholar 

  12. Briffa, M. & R. W. Elwood, 2001. Motivational change during shell fights in the hermit crab Pagurus bernhardus. Animal Behaviour 62: 505–510.

    Article  Google Scholar 

  13. Brooks, W. R., 1989. Hermit crabs alter sea anemone placement patterns for shell balance and reduced predation. Journal of Experimental Marine Biology and Ecology 132: 109–121.

    Article  Google Scholar 

  14. Buckley, W. J. & J. P. Ebersole, 1994. Symbiotic organisms increase the vulnerability of a hermit crab to predation. Journal of Experimental Marine Biology and Ecology 182: 49–64.

    Article  Google Scholar 

  15. Chase, I. D., M. Weissburg & T. H. Dewitt, 1988. The vacancy chain process: a new mechanism of resource distribution in animals with application to hermit crabs. Animal Behaviour 36: 1265–1274.

    Article  Google Scholar 

  16. Childress, J. R., 1972. Behavioral ecology and fitness theory in a tropical hermit crab. Ecology 53: 960–964.

    Article  Google Scholar 

  17. DeWitt, T. J., A. Sih & D. S. Wilson, 1998. Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13: 77–81.

    CAS  Article  Google Scholar 

  18. Doake, S. & R. W. Elwood, 2011. How resource quality differentially affects motivation and ability to fight in hermit crabs. Proceedings of the Royal Society B-Biological Sciences 278: 567–573.

    CAS  Article  PubMed Central  Google Scholar 

  19. Dominciano, L. C. C., B. S. Sant’’nna & A. Turra, 2009. Are the preference and selection patterns of hermit crabs for gastropod shells species- or site-specific? Journal of Experimental Marine Biology and Ecology 378(1–2): 15–21.

    Article  Google Scholar 

  20. Fotheringham, N., 1976a. Hermit crab shells as a limiting resource (Decapoda, Paguridea). Crustaceana 31: 193–199.

    Article  Google Scholar 

  21. Fotheringham, N., 1976b. Population consequences of shell utilization by hermit crabs. Ecology 57: 570–578.

    Article  Google Scholar 

  22. Forest, J. & M. Saint Laurent, 1967. Campagne de la “Calypso” au large de côtes Atlântiques de l’Amerique du Sud (1961–1962). 6. Crustacés Décapodes: Pagurides. Annales de L’Institute Oceanographique de Monaco, 45.

  23. Gherardi, F., 1991. Relative growth, population structure, and shell-utilization of the hermit crab Clibanarius erythropus in the Mediterranean. Oebalia 17: 181–196.

    Google Scholar 

  24. Gilchrist, S. L., 1984. Specificity of hermit crab attraction to gastropod predation sites. Journal of Chemical Ecology 10: 569–582.

    CAS  Article  PubMed  Google Scholar 

  25. Gilchrist, S. L. & L. G. Abele, 1984. Effects of sampling method on the estimation of population parameters in hermit crabs. Journal of Crustacean Biology 4: 645–654.

    Article  Google Scholar 

  26. Gorman, D., F. Barros & A. Turra, 2015a. What motivates hermit crabs to abandon trapped shells? Assessing the influence of shell value, olfactory attractants and previous experience. Hydrobiologia 743: 285–297.

    Article  Google Scholar 

  27. Gorman, D., C. E. Sikinger & A. Turra, 2015b. Spatial and temporal variation in the predation risk for hermit crabs in a subtropical bay. Journal of Experimental Marine Biology and Ecology 462: 98–104.

    Article  Google Scholar 

  28. Hazlett, B. A., 1981. The behavioral ecology of hermit crabs. Annual Review of Ecology and Systematics 1: 1–22.

    Article  Google Scholar 

  29. Hazlett, B. A., 1996. Comparative study of hermit crab responses to shell-related chemical cues. Journal of Chemical Ecology 22: 2317–2329.

    CAS  Article  PubMed  Google Scholar 

  30. Hazlett, B. A., 1997. The organisation of behaviour in hermit crabs: responses to variation in stimulus strength. Behaviour 134: 59–70.

    Article  Google Scholar 

  31. Hazlett, B. A., 2013. Shell exchange behavior in the Hawaiian hermit crab Calcinus hazletti (Decapoda, Diogenidae). Crustaceana 86(2): 253–257.

    Article  Google Scholar 

  32. Hazlett, B. A. & L. C. Baron, 1989. Influence of shells on mating behavior in the hermit crab Calcinus tibicen. Behavioral Ecology and Sociobiology 24: 369–376.

    Article  Google Scholar 

  33. Hazlett, B. A. & W. Herrnkind, 1980. Orientation to shell events by the hermit crab Clibanarius vittatus (Bose) (Decapoda, Paguridae). Crustaceana 39: 311–314.

    Article  Google Scholar 

  34. Kratt, C. M. & D. Rittschof, 1991. Peptide attraction of hermit crabs Clibanarius vittatus Bosc: roles of enzymes and substrates. Journal of Chemical Ecology 17: 2347–2365.

    CAS  Article  PubMed  Google Scholar 

  35. Laidre, M. E., 2010. How rugged individualists enable one another to find food and shelter: field experiments with tropical hermit crabs. Proceedings of the Royal Society B-Biological Sciences 277: 1361–1369.

    Article  PubMed Central  Google Scholar 

  36. Lau, C. J., 1987. Feeding behavior of the Hawaiian slipper lobster, Scyllarides squammosus, with a review of decapod crustacean tactics on molluscan prey. Bulletin of Marine Science 41: 378–391.

    Google Scholar 

  37. Lepore, M. & S. Gilchrist, 1988. Hermit crab attraction to gastropod predation sites. American Zoologist 28: 93A–93A.

    Google Scholar 

  38. McClintock, T. S., 1985. Effects of shell condition and size upon the shell choice behaviour of a hermit crab. Journal of Experimental Marine Biology and Ecology 88: 271–285.

    Article  Google Scholar 

  39. McLean, R. B., 1974. Direct shell acquisition by hermit crabs from gastropods. Experientia 30: 206–208.

    Article  Google Scholar 

  40. McLean, R. B., 1983. Gastropod shells: a dynamic resource that helps shape benthic community structure. Journal of Experimental Marine Biology and Ecology 69: 151–174.

    Article  Google Scholar 

  41. Mesce, K. A., 1982. Calcium-bearing objects elicit shell selection behavior in a hermit crab. Science 215: 993–995.

    CAS  Article  PubMed  Google Scholar 

  42. Partdridge, B. L., 1980. Background camouflage: an additional parameter in hermit crab shell selection and subsequent behavior. Bulletin of Marine Science 30: 914–916.

    Google Scholar 

  43. Pechenick, J. A. & S. Lewis, 2000. Avoidance of drilled gastropod shells by the hermit crab Pagurus longicarpus at Nahant, Massachusetts. Journal of Experimental Marine Biology and Ecology 253: 17–32.

    Article  Google Scholar 

  44. Pezzuti, J. C. B., A. Turra & F. P. P. Leite, 2002. Hermit crab (Decapoda, Anomura) attraction to dead gastropod baits in an infralittoral algae bank. Brazilian Archives of Biology and Technology 45: 245–250.

    Article  Google Scholar 

  45. Ragagnin, M. N., B. S. Sant’Anna, D. Gorman, C. C. de Castro, A. P. Tschiptschin & T. Turra, 2016. What makes a good home for hermits? Assessing gastropod shell density and relative strength. Marine Biology Research.

  46. Reese, E. S., 1969. Behavioral adaptations of intertidal hermit crabs. American Zoologist 9: 343–355.

    Article  Google Scholar 

  47. Rittschof, D., 1980a. Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites. Journal of Chemical Ecology 6: 103–118.

    Article  Google Scholar 

  48. Rittschof, D., 1980b. Enzymatic production of small molecules attracting hermit crabs to simulated gastropod predation sites. Journal of Chemical Ecology 6: 665–676.

    Article  Google Scholar 

  49. Rittschof, D., C. M. Kratt & A. S. Clare, 1990. Gastropod predation sites: the role of predator and prey in chemical attraction of the hermit crab Clibanarius vittatus. Journal of the Marine Biological Association of the UK 70: 583–596.

    CAS  Article  Google Scholar 

  50. Rittschof, D., D. W. Tsai, P. G. Massey, L. Blanco, G. L. Kueber Jr & R. J. Haas Jr, 1992. Chemical mediation of behavior in hermit crabs: alarm and aggregation cues. Journal of Chemical Ecology 18: 959–984.

    CAS  Article  PubMed  Google Scholar 

  51. Ross, D. M., 1971. Protection of hermit crab (Dardanus spp.) from octopus by commensal sea anemones (Calliacts spp.). Nature 230: 401–402.

    CAS  Article  PubMed  Google Scholar 

  52. Sant’’nna, B. S., L. C. C. Dominciano, S. F. Buozi & A. Turra, 2012. Is shell partitioning between the hermit crabs Pagurus brevidactylus and Pagurus criniticornis explained by interference and/or exploitation competition? Marine Biology Research 8(7): 662–669.

    Article  Google Scholar 

  53. Shumway, S. E., 1978. Osmotic balance and respiration in the hermit crab, Pagurus bernhardus, exposed to fluctuating salinities. Journal of the Marine Biological Association of the UK 58: 869–876.

    Article  Google Scholar 

  54. Small, M. P. & R. W. Thacker, 1994. Land hermit crabs use odors of died conspecifics to locate shells. Journal of Experimental Marine Biology and Ecology 182: 169–182.

    Article  Google Scholar 

  55. Souza, E. C. F., A. Turra, F. P. P. Leite & D. Gorman, 2015. Shell-size relationships in hermit crabs: a comparison of fundamental and realized niches in Pagurus criniticornis (Dana, 1852). Marine Biology Research Bulletin of Marine Science 91: 343–361.

    Article  Google Scholar 

  56. Taylor, P. R., 1981. Hermit crab fitness: the effect of shell condition and behavioral adaptations on environmental resistance. Journal of Experimental Marine Biology and Ecology 52: 205–218.

    Article  Google Scholar 

  57. Thacker, R. W., 1994. Volatile shell investigation cues of land hermit crabs: effect of shell fit, detection of cues from other hermit crab species, and cue isolation. Journal of Chemical Ecology 20: 1457–1482.

    CAS  Article  PubMed  Google Scholar 

  58. Tran, M. V., 2014. The scent of cannibalism: the olfactory basis of cannibalism in hermit crabs. Journal of Experimental Marine Biology and Ecology 457: 8–14.

    Article  Google Scholar 

  59. Tricarico, E. & F. Gherardi, 2006. Shell acquisition by hermit crabs: which tactic is more efficient? Behavioral Ecology and Sociobiology 60(4): 492–500.

    Article  Google Scholar 

  60. Turra, A., 2003. Shell condition and adequacy of three sympatric intertidal hermit crab populations. Journal of Natural History 37: 1781–1795.

    Article  Google Scholar 

  61. Turra, A. & M. R. Denadai, 2001. Desiccation tolerance of four sympatric tropical intertidal hermit crabs (Decapoda, Anomura). Marine and Freshwater Behaviour and Physiology 34: 227–238.

    Article  Google Scholar 

  62. Turra, A. & M. R. Denadai, 2004. Interference and exploitation components in interespecific competition between sympatric, intertidal hermit crabs. Journal of Experimental Marine Biology and Ecology 310: 183–193.

    Article  Google Scholar 

  63. Turra, A. & D. Gorman, 2014. Subjective resource value and shell abandoning behaviour in hermit crabs. Journal of Experimental Marine Biology and Ecology 452: 137–142.

    Article  Google Scholar 

  64. Turra, A. & F. P. P. Leite, 2002. Shell utilization patterns of a tropical intertidal hermit crab assemblage. Journal of the Marine Biological Association of the UK 82: 97–107.

    Google Scholar 

  65. Turra, A., G. B. Jacobucci, F. M. P. Araujo & F. P. P. Leite, 2000. Spatial distribution of four sympatric species of hermit crabs (Decapoda, Anomura). Biodiversity Crisis and Crustacea (eds J. C. V. Klein & F. R. Schram), pp. 261–273.

  66. Turra, A., M. R. Denadai & F. P. P. Leite, 2005. Predation on gastropods by shell-breaking crabs: effects on shell availability to hermit crabs. Marine Ecology Progress Series 286: 279–291.

    Article  Google Scholar 

  67. Vance, R. R., 1972a. The role of shell adequacy in behaviour interactions in hermit crabs. Ecology 53: 1075–1083.

    Article  Google Scholar 

  68. Vance, R. R., 1972b. Competition and mechanisms of coexistence in three sympatric species of intertidal hermit crabs. Ecology 53: 1062–1074.

    Article  Google Scholar 

  69. Wilber Jr, T. P. & W. F. Herrnkind, 1984. Predaceous gastropod regulate new shell supply to salt marsh hermit crabs. Marine Biology 79: 145–150.

    Article  Google Scholar 

Download references

Acknowledgments

Research funding was provided by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) in the form of scholarship grants to E.C.F. Souza (1999/11233-7) and D. Gorman (2013/07576-5). F.P.P. Leite was supported by a fellowship grant provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Fundo de Apoio ao Ensino e à Pesquisa (FAEP-UNICAMP). The Centro de Biologia Marinha of the Universidade de São Paulo (CEBIMar-USP) provided substantial in-kind support. We are grateful to a number of anonymous reviewers whose constructive comments improved earlier versions of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Daniel Gorman.

Additional information

Handling editor: Stuart Jenkins

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Souza, E.C.F., Gorman, D., Leite, F.P.P. et al. Olfactory selectivity in intertidal hermit crabs: aggregation behavior by Pagurus criniticornis (Decapoda, Anomura) in response to simulated predation on the gastropod Cerithium atratum . Hydrobiologia 772, 31–43 (2016). https://doi.org/10.1007/s10750-015-2621-6

Download citation

Keywords

  • Behavior
  • Decapod crustaceans
  • Portable shelters
  • Resource limitation
  • Predation
  • Subjective resource value