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Swarms of swift scavengers: ecological role of marine intertidal hermit crabs in California

Marine Biology volume 162, pages 969–977 (2015)Cite this article

Abstract

While marine hermit crabs are well known for being omnivorous filter feeders, less is known about the role they may play as active carrion scavengers in intertidal ecosystems. Prior studies have revealed that intertidal hermit crabs can be attracted to chemical cues from predated gastropods. Yet their attraction is usually assumed to be driven primarily by the availability of new shells rather than by food. We conducted field experiments to assess hermit crabs’ potential role as generalist carrion scavengers on the California Coast, examining their speed of attraction and the size of the aggregations they formed in response to chemical cues from freshly smashed gastropods and mussels, both of which indicated available carrion. Compared to all other marine species, hermit crabs (Pagurus samuelis, P. hirsutiusculus, and P. granosimanus) were the fastest to arrive at the provisioning sites. Hermit crabs also dominated the provisioning sites, accumulating in the largest numbers, with aggregations of up to 20 individuals, which outcompeted all other scavengers for carrion. Notably, hermit crabs arrived equally quickly for both smashed gastropod and mussel, even though the latter does not offer suitable shells for hermit crabs and even though the former only yields shell-related chemical cues over time frames longer than our experiments. These results thus suggest that shell availability is not the only, or even the primary, reason marine intertidal hermit crabs aggregate at carrion sites; they also aggregate to forage, thereby playing an important role as active carrion scavengers in intertidal ecosystems.

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References

  • Barnes D, De Grave S (2000) Ecology of tropical hermit crabs at Quirimba Island, Mozambique: niche width and resource allocation. Mar Ecol Prog Ser 206:171–179. doi:10.3354/meps206171

    Article  Google Scholar 

  • Bertness MD (1981) Predation, physical stress, and the organization of a tropical rocky intertidal hermit crab community. Ecology 62:411–425

    Article  Google Scholar 

  • Bollay M (1964) Distribution and utilization of gastropod shells by the hermit crabs Pagurus samuelis, Pagurus granosimanus, and Pagurus hirsutiusculus at Pacific Grove California. Veliger 6(Suppl.):71–76

    Google Scholar 

  • Bozzano A, Sarda F (2002) Fishery discard consumption rate and scavenging activity in the northwestern Mediterranean Sea. ICES J Mar Sci 59:15–28. doi:10.1006/jmsc.2001.1142

    Article  Google Scholar 

  • Breithaupt T, Theil M (2011) Chemical communication in crustaceans. Springer, New York

    Book  Google Scholar 

  • Britton JC, Morton B (1994) Marine carrion and scavengers. Oceanogr Mar Biol Annu Rev 32:369–434

    Google Scholar 

  • Denny MW, Gaines SD (2007) Encyclopedia of tidepools and rocky shores. University of California Press, Berkeley

    Google Scholar 

  • Denny M, Gaylord B, Helmuth B, Daniel T (1998) The menace of momentum: dynamic forces on flexible organisms. Limnol Oceanogr 43:955–968

    Article  Google Scholar 

  • Gaylord B (1999) Detailing agents of physical disturbance: wave-induced velocities and accelerations on a rocky shore. J Exp Mar Bio Ecol 239:85–124. doi:10.1016/S0022-0981(99)00031-3

    Article  Google Scholar 

  • Gaylord B (2007) Hydrodynamic forces. In: Denny MW, Gaines SD (eds) Encyclopedia of tidepools and rocky shores. University of California Press, Berkeley, pp 277–283

    Google Scholar 

  • Gaylord B, Hale BB, Denny MW (2001) Consequences of transient fluid forces for compliant benthic organisms. J Exp Biol 204:1347–1360

    CAS  Google Scholar 

  • Gherardi F, Atema J (2005) Effects of chemical context on shell investigation behavior in hermit crabs. J Exp Mar Bio Ecol 320:1–7. doi:10.1016/j.jembe.2004.12.022

    Article  CAS  Google Scholar 

  • Gherardi F, Tricarico E (2011) Chemical ecology and social behaviour of Anomura. In: Breithaupt T, Theil M (eds) Chemical communication in crustaceans. Springer, New York, pp 297–312

    Google Scholar 

  • Gilchrist S (1984) Specificity of hermit crab attraction to gastropod predation sites. J Chem Ecol 10:569–582

    Article  CAS  Google Scholar 

  • Hazlett B (1981) The behavioral ecology of hermit crabs. Annu Rev Ecol Syst 12:1–22

    Article  Google Scholar 

  • Holling HC (1957) Pagoo. Houghton Mifflin, Boston

    Google Scholar 

  • King N, Bailey D, Priede I (2007) Role of scavengers in marine ecosystems. Mar Ecol Prog Ser 350:175–178. doi:10.3354/meps07186

    Article  Google Scholar 

  • Kunze J, Anderson DT (1979) Functional morphology of the mouthparts and gastric mill in the hermit crabs Clibanarius taeniatus (Milne Edwards), Clibanarius virescens (Krauss), Paguristes squamosus (McCulloch) and Dardanus setifer (Mile-Edwards) (Anomura: Paguridae). Austrailian J Mar Freshw Res 30:683–722

    Article  Google Scholar 

  • Laidre ME (2007) Vulnerability and reliable signaling in conflicts between hermit crabs. Behav Ecol 18:736–741. doi:10.1093/beheco/arm040

    Article  Google Scholar 

  • Laidre ME (2010) How rugged individualists enable one another to find food and shelter: field experiments with tropical hermit crabs. Proc Biol Sci 277:1361–1369. doi:10.1098/rspb.2009.1580

    Article  Google Scholar 

  • Laidre ME (2011) Ecological relations between hermit crabs and their shell-supplying gastropods: constrained consumers. J Exp Mar Bio Ecol 397:65–70. doi:10.1016/j.jembe.2010.10.024

    Article  Google Scholar 

  • Laidre ME (2012) Niche construction drives social dependence in hermit crabs. Curr Biol 22:R861–R863

    Article  CAS  Google Scholar 

  • Laidre ME (2013a) Foraging across ecosystems: diet diversity and social foraging spanning aquatic and terrestrial ecosystems by an invertebrate. Mar Ecol 34:80–89

    Article  Google Scholar 

  • Laidre ME (2013b) Eavesdropping foragers use level of collective commotion as public information to target high quality patches. Oikos 122:1505–1511

    Google Scholar 

  • Laidre ME, Elwood RW (2008) Motivation matters: cheliped extension displays in the hermit crab, Pagurus bernhardus, are honest signals of hunger. Anim Behav 75:2041–2047

    Article  Google Scholar 

  • McGuire BM, Williams JD (2010) Utilization of partially predated snail shells by the hermit crab Pagurus longicarpus Say, 1817. Mar Biol 157:2129–2142. doi:10.1007/s00227-010-1478-5

    Article  Google Scholar 

  • McLean RB (1974) Direct shell acquisition by hermit crabs from gastropods. Experientia 30:206–208. doi:10.1007/BF01927738

    Article  Google Scholar 

  • Mclean R (1983) Gastropod shells: a dynamic resource that helps shape benthic community structure. J Exp Mar Bio Ecol 69:151–174

    Article  Google Scholar 

  • Morris RH, Abbott DP, Haderlie EC (1980) Intertidal invertebrates of California. Stanford University Press, Stanford

    Google Scholar 

  • Morton B, Yuen W (2000) The feeding behaviour and competition for carrion between two sympatric scavengers on a sandy shore in Hong Kong: the gastropod, Nassarius festivus (Powys) and the hermit crab, Diogenes edwardsii (De Haan). J Exp Mar Bio Ecol 246:1–29

    Article  Google Scholar 

  • Pezzuti J, Turra A, Leite F (2002) Hermit crab (Decapoda, Anomura) attraction to dead gastropod baits in a infralittoral algae bank. Brazilian Arch Biol Technol 45:245–250

    Article  Google Scholar 

  • Prezelin BB (2007) Algal Blooms. In: Denny MW, Gaines SD (eds) Encyclopedia of Tidepools rocky shores. University of California Press, London, pp 30–33

    Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing

  • Ramsay K, Kaiser MJ, Hughes RN (1997) A field study of intraspecific competition for food in hermit crabs (Pagurus bernhardus). Estuar Coast Shelf Sci 44:213–220

    Article  Google Scholar 

  • Reese ES (1969) Behavioral adaptations of intertidal hermit crabs. Am Zool 9:343–355

    Google Scholar 

  • Rittschof D (1980a) Chemical attraction of hermit crabs and other attendants to simulated gastropod predation sites. J Chem Ecol 6:103–118. doi:10.1007/BF00987531

    Article  Google Scholar 

  • Rittschof D (1980b) Enzymatic production of small molecules attracting hermit crabs to simulated gastropod predation sites. J Chem Ecol 6:665–675. doi:10.1007/BF00987677

    Article  Google Scholar 

  • Rittschof D (1992) Chemosensation in the daily lives of crabs. Am Zool 32:363–369

    CAS  Google Scholar 

  • Rittschof D (2007) Hermit crabs. In: Denny MW, Gaines SD (eds) Encyclopedia of tidepools and rocky shores. University of California Press, Berkeley, CA, pp 273–274

    Google Scholar 

  • Rittschof D, Tsai DW, Massey PG et al (1992) Chemical mediation of behavior in hermit crabs: alarm and aggregation cues. J Chem Ecol 18:959–984. doi:10.1007/BF00980056

    Article  CAS  Google Scholar 

  • Schembri PJ (1982) Feeding behaviour of fifteen species of hermit crabs (Crustacea:Decapoda:Anomura) from the Otago region, southeastern New Zealand. J Nat Hist 16:859–878. doi:10.1080/00222938200770691

    Article  Google Scholar 

  • Scully EP (1983) The behavioral ecology of competition and resource utilization among hermit crabs. In: Rebach S, Dunham DW (eds) Studies in adaptation: the behaviour of higher crustacea. Wiley, New York

    Google Scholar 

  • Tran MV (2013) Divergent reactions to olfactory foraging cues between two ecologically similar, sympatric hermit crab species. J Crust Biol 33:512–518. doi:10.1163/1937240X-00002154

    Article  Google Scholar 

  • Tran MV, O’Grady M, Colborn J, Van Ness K, Hill W (2014) Aggression and food resource competition between sympatric hermit crab species. PLoS ONE 9(3):e91823

    Article  Google Scholar 

  • Tricarico E, Gherardi F (2006) Shell acquisition by hermit crabs: Which tactic is more efficient? Behav Ecol Sociobiol 60:492–500. doi:10.1007/S00265-006-0191-3

    Article  Google Scholar 

  • Tricarico E, Bertocchi S, Brusconi S et al (2009) Shell recruitment in the Mediterranean hermit crab Clibanarius erythropus. J Exp Mar Bio Ecol 381:42–46. doi:10.1016/j.jembe.2009.09.001

    Article  Google Scholar 

  • Tricarico E, Breithaupt T, Gherardi F (2011) Interpreting odours in hermit crabs: a comparative study. Estuar Coast Shelf Sci 91:211–215. doi:10.1016/j.ecss.2010.10.039

    Article  Google Scholar 

  • Vermeij G (1987) Evolution and escalation: an ecological history of life, 1st edn. Princeton University Press, Princeton

    Google Scholar 

  • Vermeij GJ (1993) A natural history of shells. Princeton University Press, Princeton

    Google Scholar 

Download references

Acknowledgments

We thank the Bodega Marine Laboratory and the California Department of Fish and Wildlife for permission to conduct this research. We are especially grateful to Jackie Sones, Kitty Brown, and Eric Sanford at Bodega and to Tim Herrlinger at Berkeley for their helpful advice, discussion, and logistical support. We also thank Jennifer Bates and Maryann Davies for assistance with some of the final field experiments. Research was supported by funding from the Miller Institute at Berkeley to M.L.

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Author notes

  1. Mark E. Laidre

    Present address: Department of Biological Sciences, Dartmouth College, Hanover, NH, 03755, USA

  2. Alison L. Greggor

    Present address: Department of Psychology, University of Cambridge, Cambridge, UK

Authors and Affiliations

  1. Department of Integrative Biology, University of California, Berkeley, CA, USA

    Mark E. Laidre & Alison L. Greggor

Authors
  1. Mark E. Laidre
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  2. Alison L. Greggor
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Corresponding author

Correspondence to Mark E. Laidre.

Additional information

Communicated by F. Bulleri.

Electronic supplementary material

Below is the link to the electronic supplementary material.

227_2015_2639_MOESM1_ESM.pdf

Figure S1. Google Earth image of the intertidal study site outside the Bodega Marine Laboratory, with the site divided into four main stretches, each of which contained 20–30 tide pools (PDF 277 kb)

227_2015_2639_MOESM2_ESM.pdf

Figure S2. Number (mean + SE) of gastropods present within the quadrat during each minute of the experiment. (see Figure 2 for details; scale of y-axis same as Figure 2) (PDF 18 kb)

227_2015_2639_MOESM3_ESM.pdf

Figure S3. Number (mean + SE) of brachyuran crabs present within the quadrat during each minute of the experiment (see Figure 2 for details; scale of y-axis same as Figure 2) (PDF 17 kb)

227_2015_2639_MOESM4_ESM.pdf

Figure S4. Number (mean + SE) of gobies present within the quadrat during each minute of the experiment (see Figure 2 for details; scale of y-axis same as Figure 2) (PDF 17 kb)

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Laidre, M.E., Greggor, A.L. Swarms of swift scavengers: ecological role of marine intertidal hermit crabs in California. Mar Biol 162, 969–977 (2015). https://doi.org/10.1007/s00227-015-2639-3

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  • DOI: https://doi.org/10.1007/s00227-015-2639-3

Keywords

  • Hermit Crab
  • Tide Pool
  • Brachyuran Crab
  • Intertidal Ecosystem
  • Carrion Source