What motivates hermit crabs to abandon trapped shells? Assessing the influence of shell value, olfactory attractants, and previous experience
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Abstract
Hermit crabs finding themselves in a trapped shell face a critical decision that will require an assessment of the benefits of abandonment against the increased risks of predation and desiccation. This study investigates factors that influence the rate of shell abandoning by common intertidal hermit crabs. We firstly established that the mud inhabitant, Pagurus criniticornis, exhibits a greater tendency to abandon shells when compared to its neighbors Pagurus brevidactylus and Clibanarius antillensis. We subsequently conducted a series of experiments on this species to assess the relative influence of (1) gastropod shell type, (2) shell adequacy, (3) shell condition, (4) olfactory attractants, (5) previous experience, and (6) shell acclimatization. P. criniticornis abandoned very small shells faster than optimal (well-fitting) specimens and damaged shells faster and more completely than intact specimens. Crabs exposed to olfactory cues (Cerithium atratum) were 15% more likely to abandon their shells than unexposed individuals. Similarly, individuals that had undergone previous abandonment experience and those given longer acclimatization periods (30 vs. 2 days) showed rates of abandonment that were 18 and 28% greater than contrasting treatments. The results can be used to aid our understanding of motivational behavior in invertebrates and other animals that inhabit temporary or ephemeral shelters.
Keywords
White spotwrist Pagurus criniticornis Clibanarius antillensis Pagurus brevidactylus Subjective resource value Shell occupancyNotes
Acknowledgments
This research was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) in an effort to augment our understanding of the behavioral ecology of benthic fauna in the Araçá Bay region of São Sebastião, Brazil. The authors thank Herbert Guariento for assistance with experiments that were conducted at the Laboratory of Aquatic Biology at the Centro Universitário Fundação de Ensino Octávio Bastos. We are grateful to Mark Briffa and two anonymous referees for their insightful comments and suggestions, which helped us to improve the manuscript.
References
- Agrawal, A. A., 2001. Ecology – phenotypic plasticity in the interactions and evolution of species. Science 294: 321–326.PubMedCrossRefGoogle Scholar
- Angel, J. E., 2000. Effects of shell fit on the biology of the hermit crab Pagurus longicarpus (Say). Journal of Experimental Marine Biology and Ecology 243: 169–184.CrossRefGoogle Scholar
- Appel, M. & R. W. Elwood, 2009a. Gender differences, responsiveness and memory of a potentially painful event in hermit crabs. Animal Behaviour 78: 1373–1379.CrossRefGoogle Scholar
- Appel, M. & R. W. Elwood, 2009b. Motivational trade-offs and potential pain experience in hermit crabs. Applied Animal Behaviour Science 119: 120–124.CrossRefGoogle Scholar
- 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.PubMedCentralCrossRefGoogle Scholar
- Asakura, A., 1995. Sexual differences in life history and resource utilization by the hermit crab. Ecology 76: 2295–2313.CrossRefGoogle Scholar
- Bates, D., M. Maechler, B. Bolker & S. Walker, 2014. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7, http://CRAN.R-project.org/package=lme4.
- Billock, W. L. & S. G. Dunbar, 2009. Influence of motivation on behaviour in the hermit crab, Pagurus samuelis. Journal of the Marine Biological Association of the United Kingdom 89: 775–779.CrossRefGoogle Scholar
- Briffa, M., 2013. Plastic proteans: reduced predictability in the face of predation risk in hermit crabs. Biology Letters 9: 20130592.PubMedCentralPubMedCrossRefGoogle Scholar
- Briffa, M. & D. Dallaway, 2007. Inter-sexual contests in the hermit crab Pagurus bernhardus: females fight harder but males win more encounters. Behavioral Ecology and Sociobiology 61: 1781–1787.CrossRefGoogle Scholar
- Briffa, M. & C. Twyman, 2011. Do I stand out or blend in? Conspicuousness awareness and consistent behavioural differences in hermit crabs. Biology Letters 7: 330–332.PubMedCentralPubMedCrossRefGoogle Scholar
- Briffa, M., P. Haskell & C. Wilding, 2008a. Behavioural colour change in the hermit crab Pagurus bernhardus: reduced crypticity when the threat of predation is high. Behaviour 145: 915–929.CrossRefGoogle Scholar
- Briffa, M., S. D. Rundle & A. Fryer, 2008b. Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus. Proceedings of the Royal Society B-Biological Sciences 275: 1305–1311.PubMedCentralCrossRefGoogle Scholar
- Bulinski, K. V., 2007. Shell-selection behavior of the hermit crab Pagurus granosimanus in relation to isolation, competition, and predation. Journal of Shellfish Research 26: 233–239.CrossRefGoogle Scholar
- Calado, R., N. Nogueira & A. dos Santos, 2006. Extended parental care in a hermit crab of the genus Calcinus (Anomura : diogenidae). Journal of the Marine Biological Association of the United Kingdom 86: 121–123.CrossRefGoogle Scholar
- Cama, A., R. Abellana, I. Christel, X. Ferrer & D. R. Vieites, 2012. Moving to the sea: a challenge for an inshore species, the slender-billed gull. Marine Ecology Progress Series 463: 285–295.CrossRefGoogle Scholar
- Chen, P. Z., L. R. Carrasco & P. K. L. Ng, 2014. Post-contest stridulation used exclusively as a victory display in mangrove crabs. Ethology 120: 532–539.CrossRefGoogle Scholar
- Cheng, Y. W. & M. P. Gallinat, 2004. Statistical analysis of the relationship among environmental variables, inter-annual variability and smolt trap efficiency of salmonids in the Tucannon River. Fisheries Research 70: 229–238.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- de la Haye, K. L., J. I. Spicer, S. Widdicombe & M. Briffa, 2011. Reduced sea water pH disrupts resource assessment and decision making in the hermit crab Pagurus bernhardus. Animal Behaviour 82: 495–501.CrossRefGoogle Scholar
- 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.PubMedCentralCrossRefGoogle Scholar
- Dominciano, L. C. C., B. S. Sant’Anna & 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: 15–21.CrossRefGoogle Scholar
- Dowds, B. M. & R. W. Elwood, 1983. Shell wars: assessment strategies and the timing of decisions in hermit crab shell fights. Behaviour 85: 1–24.CrossRefGoogle Scholar
- Drolet, D., J. H. Himmelman & R. Rochette, 2004. Use of refuges by the ophiuroid Ophiopholis aculeata: contrasting effects of substratum complexity on predation risk from two predators. Marine Ecology Progress Series 284: 173–183.CrossRefGoogle Scholar
- Elwood, R. W., 2011. Pain and suffering in invertebrates? Ilar Journal 52: 175–184.PubMedCrossRefGoogle Scholar
- Elwood, R. W. & M. Appel, 2009. Pain experience in hermit crabs? Animal Behaviour 77: 1243–1246.CrossRefGoogle Scholar
- Elwood, R. W. & A. Stewart, 1985. The timing of decisions during shell investigation by the hermit crab, Pagurus bernhardus. Animal Behaviour 33: 620–627.CrossRefGoogle Scholar
- Fotheringham, N., 1976. Hermit crab shells as a limiting resource (Decapoda, Paguridea). Crustaceana 31: 193–199.CrossRefGoogle Scholar
- Gherardi, F., 1996. Gastropod shells or polychaete tubes? The hermit crab Discorsopagurus schmitti’s housing dilemma. Ecoscience 3: 154–164.Google Scholar
- Gherardi, F., 2004. Resource partitioning between sexes in the “unconventional” hermit crab, Calcinus tubularis. Behavioral Ecology 15: 742–747.CrossRefGoogle Scholar
- Gherardi, F. & J. Atema, 2005. Memory of social partners in hermit crab dominance. Ethology 111: 271–285.CrossRefGoogle Scholar
- Gilchrist, S. & L. G. Abele, 1984. Effects of sampling method on the estimation of population parameters in hermit crabs. Journal of Crustacean Biology 4: 645–654.CrossRefGoogle Scholar
- Gorman, D., Sikinger, C.E., Turra, A., In review. Spatial and temporal variation in predation risk in a subtropical estuary. Journal of Experimental Marine Biology and Ecology.Google Scholar
- Hazlett, B. A., 1997. The organisation of behaviour in hermit crabs: responses to variation in stimulus strength. Behaviour 134: 59–70.CrossRefGoogle Scholar
- Hazlett, B. A. & D. Rittschof, 2000. Predation-reproduction conflict resolution in the hermit crab, Clibanarius vittatus. Ethology 106: 811–818.CrossRefGoogle Scholar
- Hazlett, B. A. & D. Rittschof, 2005. Effects of food and shell cues on mating in the hermit crab Clibanarius vittatus. Behaviour 142: 751–759.CrossRefGoogle Scholar
- Houston, A. & J. McNamara, 1999. Models of Adaptive Behaviour: An Approach Based on State. Cambridge University Press, Cambridge.Google Scholar
- Huntingford, F. A., 1992. Assessments and decisions: a study of information gathering by hermit-crabs. In Elwood, R. W. & S. J. Neil (eds), Nature. Chapman and Hall, London: 205.Google Scholar
- Jackson, N. W. & R. W. Elwood, 1989. Memory of information gained during shell investigation by the hermit crab, Pagurus bernhardus. Animal Behaviour 37: 529–534.CrossRefGoogle Scholar
- Katz, J. N. & D. Rittschof, 1993. Alarm investigation responses of hermit-crabs as related to shell fit and crab size. Marine Behaviour and Physiology 22: 171–182.CrossRefGoogle Scholar
- Labonne, J., S. Allouche & P. Gaudin, 2003. Use of a generalised linear model to test habitat preferences: the example of Zingel Asper, an endemic endangered percid of the River Rhone. Freshwater Biology 48: 687–697.CrossRefGoogle Scholar
- Laegdsgaard, P. & C. Johnson, 2001. Why do juvenile fish utilise mangrove habitats? Journal of Experimental Marine Biology and Ecology 257: 229–253.PubMedCrossRefGoogle Scholar
- 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.PubMedCentralCrossRefGoogle Scholar
- Laidre, M. E., 2012. Homes for hermits: temporal, spatial and structural dynamics as transportable homes are incorporated into a population. Journal of Zoology 288: 33–40.CrossRefGoogle Scholar
- Leite, F. P. P., A. Turra & S. M. Gandolfi, 1998. Hermit crabs (Crustacea:Decapoda:Anomura), gastropod shells and environmental structure: their relationship in southeastern Brazil. Journal of Natural History 32: 1599–1608.CrossRefGoogle Scholar
- Mangel, M. & J. Stamps, 2001. Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evolutionary Ecology Research 3: 583–593.Google Scholar
- McClintock, T. S., 1985. Effects of shell condition and size upon the shell choice behavior of a hermit crab. Journal of Experimental Marine Biology and Ecology 88: 271–285.CrossRefGoogle Scholar
- McLean, R. B., 1974. Direct shell acquisition by hermit crabs from gastropods. Experientia 30: 206–208.CrossRefGoogle Scholar
- Mowles, S. L., P. A. Cotton & M. Briffa, 2012. Consistent crustaceans: the identification of stable behavioural syndromes in hermit crabs. Behavioral Ecology and Sociobiology 66: 1087–1094.CrossRefGoogle Scholar
- Pechenik, 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.PubMedCrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Rittschof, D., 1980. Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites. Journal of Chemical Ecology 6: 103–118.CrossRefGoogle Scholar
- Rittschof, D., D. W. Tsai, P. G. Massey, L. Blanco, G. L. Kueber & R. J. Haas, 1992. Chemical mediation of behavior in hermit-crabs: alarm and aggregation cues. Journal of Chemical Ecology 18: 959–984.PubMedCrossRefGoogle Scholar
- Rocha, R. M. D., 1995. Abundance and distribution of sessile invertebrates under intertidal boulders (Sao Paulo, Brazil). Boletim do Instituto Oceanografico 43: 71–88.Google Scholar
- Rodrigues, L.J., Dunham, D.W., Coates, K.A., 2002. Gastropod shells or gastropod tubes? Shelter choice in the hermit crab Calcinus verrilli. In Modern Approaches to the Study of Crustacea: 131–135.Google Scholar
- Rotjan, R. D., J. Blum & S. M. Lewis, 2004. Shell choice in Pagurus longicarpus hermit crabs: does predation threat influence shell selection behavior? Behavioral Ecology and Sociobiology 56: 171–176.CrossRefGoogle Scholar
- Sant’Anna, B. S., L. C. D. 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: 662–669.CrossRefGoogle Scholar
- Scheibling, R. E. & J. Hamm, 1991. Interactions between sea urchins (Strongylocentrotus droebachiensis) and their predators in field and laboratory experiments. Marine Biology 110: 105–116.CrossRefGoogle Scholar
- Sih, A., A. M. Bell, J. C. Johnson & R. E. Ziemba, 2004. Behavioral syndromes: an integrative overview. Quarterly Review of Biology 79: 241–277.PubMedCrossRefGoogle Scholar
- Skilleter, G. A. & C. H. Peterson, 1994. Central of foraging behavior of individuals within an ecosystem context: the clam Macoma balthica and interactions between competition and siphon cropping. Oecologia 100: 268–278.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- Thacker, R. W., 1996. Food choices of land hermit crabs (Coenobita compressus H. Milne Edwards) depend on past experience. Journal of Experimental Marine Biology and Ecology 199: 179–191.CrossRefGoogle Scholar
- Tricarico, E. & F. Gherardi, 2007. Resource assessment in hermit crabs: the worth of their own shell. Behavioral Ecology 18: 615–620.CrossRefGoogle Scholar
- Turra, A., 2003a. Shell condition and adequacy of three sympatric intertidal hermit crab populations. Journal of Natural History 37: 1781–1795.CrossRefGoogle Scholar
- Turra, A., 2003b. História natural, comportamento e ecologia dos caranguejos ermitões (Decapoda, Anomura). Instituto de Biologia. University of Campinas: 175.Google Scholar
- 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 United Kingdom 82: 97–107.Google Scholar
- Turra, A. & M. R. Denadai, 2003. Daily activity of four tropical intertidal hermit crabs from southeastern Brazil. Brazilian Journal of Biology 63: 537–544.CrossRefGoogle Scholar
- Turra, A. & F. P. P. Leite, 2003. The molding hypothesis: linking shell use with hermit crab growth, morphology, and shell-species selection. Marine Ecology Progress Series 265: 155–163.CrossRefGoogle Scholar
- Turra, A. & M. R. Denadai, 2004. Interference and exploitation components in inter-specific competition between sympatric, intertidal hermit crabs. Journal of Experimental Marine Biology and Ecology 310: 183–193.CrossRefGoogle Scholar
- Turra, A. & D. Gorman, 2014. Subjective resource value and shell abandoning behavior in hermit crabs. Journal of Experimental Marine Biology and Ecology 452: 137–142.CrossRefGoogle Scholar
- Turra, A., Jacobucci, G.B., Araujo, F.M.P., Leite, F.P.P., 2000. Spatial distribution of four sympatric species of hermit crabs (Decapoda, Anomura). In Klein, J.C.V., Schram, F.R. (eds), Biodiversity Crisis and Crustacea. Brill Academic Publishers, Leiden: 261–273.Google Scholar
- 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.CrossRefGoogle Scholar
- Vance, R. R., 1972. Role of shell adequacy in behavioral interactions involving hermit crabs. Ecology 53: 1075–1083.CrossRefGoogle Scholar
- White, S. J., R. K. Pipe, A. Fisher & M. Briffa, 2013. Asymmetric effects of contaminant exposure during asymmetric contests in the hermit crab Pagurus bernhardus. Animal Behaviour 86: 773–781.CrossRefGoogle Scholar
- Zuur, A. F., E. N. Ieno, N. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed Effects Models and Extensions in Ecology with R. Springer, New York.CrossRefGoogle Scholar