Skip to main content
Log in

Alternative camouflage strategies mediate predation risk among closely related co-occurring kelp crabs

  • Plant-Animal Interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Although camouflage is a common predator defense strategy across a wide variety of organisms, direct tests of the adaptive and ecological consequences of camouflage are rare. In this study, we demonstrated that closely related crabs in the family Epialtidae coexist in the same algal environment but use alternative forms of camouflage––decoration and color change––to protect themselves from predation. Decoration and color change are both plastic camouflage strategies in that they can be changed to match different habitats: decoration occurs on a short timescale (hours to days), while color change accompanies molting and occurs on longer timescales (months). We found that the species that decorated the most had the lowest magnitude of color change (Pugettia richii); the species that decorated the least showed the highest magnitude of color change (Pugettia producta), and a third species (Mimulus foliatus) was intermediate in both decoration and color change, suggesting a negative correlation in utilization of these strategies. This negative correlation between color change and decoration camouflage utilization mirrored the effectiveness of these camouflage strategies in reducing predation in different species. Color camouflage primarily reduced predation on P. producta, while decoration camouflage (but not color camouflage) reduced predation on P. richii. These results indicate there might be among-species trade-offs in utilization and/or effectiveness of these two forms of plastic camouflage, with important consequences for distribution of these species among habitats and the evolution of different camouflage strategies in this group.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andraso GM (1997) A comparison of startle response in two morphs of the brook stickleback (Culea inconstans): further evidence for a trade-off between defensive morphology and swimming ability. Evol Ecol 11:83–90

    Article  Google Scholar 

  • Berke SK, Miller M, Woodin SA (2006) Modelling the energy-mortality trade-offs of invertebrate decorating behaviour. Evol Ecol Res 8:1409–1425

    Google Scholar 

  • Berke SK, Woodin SA (2005) Do energy–mortality tradeoffs drive sexual dimorphism in a crabs decoration? (Oregonia gracilis, Brachyura: Majidae). Integr Comp Biol 45:965

    Google Scholar 

  • Booth CL (1990) Evolutionary significance of ontogenetic color change in animals. Biol J Linn Soc 40:125–164

    Article  Google Scholar 

  • Conover WJ (1999) Practical nonparametric statistics, 3rd edn. Wiley, New York

    Google Scholar 

  • Cooper JM, Allen JA (1994) Selection by wild birds on artificial dimorphic prey on varied backgrounds. Biol J Linn Soc 51:433–446

    Article  Google Scholar 

  • Cott HB (1940) Adaptive coloration in animals. Oxford University Press, New York

    Google Scholar 

  • Cummings ME, Partridge JC (2001) Visual pigments and optical habitats of surfperch (Embiotocidae) in the California kelp forest. J Comp Physiol A 187:875–889

    Article  CAS  Google Scholar 

  • Dunn DF (1977) Variability of Epiactis prolifera (Coelenterata, Actiniaria) in the inter tidal zone near Bodega Bay (California, USA). J Nat Hist 11:457–464

    Article  Google Scholar 

  • Endler JA (1978) A predators view of animal color patterns. Evol Biol 11:319–364

    Google Scholar 

  • Fagerstrom T, Larsson S, Tenow O (1987) On optimal defense in plants. Funct Ecol 1:73–82

    Article  Google Scholar 

  • Feltmate BW, Williams DD (1989) A test of crypsis and predator avoidance in the stonefly paragnetina-media (Plecoptera, Perlidae). Anim Behav 37:992–999

    Article  Google Scholar 

  • Garcia TS, Stacy J, Sih A (2004) Larval salamander response to UV radiation and predation risk: color change and microhabitat use. Ecol Appl 14:1055–1064

    Article  Google Scholar 

  • Grossman GD (1986) Food resource partitioning in a rocky intertidal fish assemblage. J Zool Ser B 1:317–356

    Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Hill GE (2000) Energetic constraints on expression of carotenoid-based plumage coloration. J Avian Biol 31:559–566

    Article  Google Scholar 

  • Hines AH (1982) Coexistence in a kelp forest: size, population dynamics, and resource partitioning in a guild of spider crabs (Brachyura: Majidae). Ecol Monogr 52:179–198

    Article  Google Scholar 

  • Hultgren KM (2007) Ecology and evolution of camouflage behavior in the Majoidea (decorator crabs). Doctoral dissertation, University of California, Davis

    Google Scholar 

  • Iampietro PJ (1999) Distribution, diet, and pigmentation of the northern kelp crab, Pugettia producta (Randall) in central California kelp forests. Master’s thesis, California State University, Stanislaus

  • Johannesson K, Ekendahl A (2002) Selective predation favouring cryptic individuals of marine snails (Littorina). Biol J Linn Soc 76:137–144

    Article  Google Scholar 

  • Kicklighter CE, Hay ME (2007) To avoid or deter: interactions among defensive and escape strategies in sabellid worms. Oecologia 151:161–173

    Article  PubMed  Google Scholar 

  • Ko HS (1998) Zoeal development of three species of Pugettia (Decapoda: Majidae), with a key to the known zoeas of the subfamily Epialtinae. J Crustacean Biol 18:499–510

    Article  Google Scholar 

  • Langstroth L, Langstroth L (2000) A living bay. University of California Press, Berkeley

    Google Scholar 

  • Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton

    Google Scholar 

  • Lindquist N, Hay ME (1996) Palatability and chemical defense of marine invertebrate larvae. Ecol Monogr 66:431–450

    Article  Google Scholar 

  • Merilaita S (2001) Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica. Evol Ecol 15:103–116

    Article  Google Scholar 

  • Merilaita S, Tuomi J, Jormalainen V (1999) Optimization of cryptic coloration in heterogeneous habitats. Biol J Linn Soc 67:151–161

    Article  Google Scholar 

  • Morgan SG, Christy JH (1996) Survival of marine larvae under the countervailing selective pressures of photodamage and predation. Limnol Oceanogr 41:498–504

    Article  Google Scholar 

  • Padilla DK, Adolph SC (1996) Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol Ecol 10:105–117

    Article  Google Scholar 

  • Palma AT, Steneck RS (2001) Does variable coloration in juvenile marine crabs reduce risk of visual predation? Ecology 82:2961–2967

    Article  Google Scholar 

  • Patek SN, Oakley TH (2003) Comparative tests of evolutionary trade-offs in a palinurid lobster acoustic system. Evolution 57:2082–2100

    PubMed  CAS  Google Scholar 

  • Peterson CH, Black R (1994) An experimentalists challenge––when artifacts of intervention interact with treatments. Mar Ecol Prog Ser 111:289–297

    Article  Google Scholar 

  • Rathbun MJ (1925) The spider crabs of America. United States National Museum Bulletin. Smithsonian Institution, Washington

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals, and mimicry. Oxford University Press, Oxford

    Google Scholar 

  • Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

    Article  Google Scholar 

  • Stachowicz JJ, Hay ME (1999) Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores. Ecology 80:495–509

    Google Scholar 

  • Stachowicz JJ, Lindquist N (2000) Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts. Oecologia 124:280–288

    Article  Google Scholar 

  • Stepien CA, Glattke M, Fink KM (1988) Regulation and significance of color patterns of the spotted kelpfish, Gibbonsia elegans Cooper, 1864 (Blennioidei, Clinidae). Copeia 1:7–15

    Article  Google Scholar 

  • Thanh PD, Wada K, Sato M, Shirayama Y (2003) Decorating behaviour by the majid crab Tiarinia cornigera as protection against predators. J Mar Biol Assoc UK 83:1235–1237

    Article  Google Scholar 

  • Tollrian R, Harvell CD (1999) The evolution of inducible defenses: current ideas. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

    Google Scholar 

  • Walters KD, Pawlik JR (2005) Is there a trade-off between wound-healing and chemical defenses among Caribbean reef sponges? Integr Comp Biol 45:352–358

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–426

    Article  Google Scholar 

  • Wicksten MK (1983) Camouflage in marine invertebrates. Oceanogr Mar Biol 21:177–193

    Google Scholar 

  • Wicksten MK (1993) A review and a model of decorating behavior in spider crabs (Decapoda, Brachyura, Majidae). Crustaceana 64:314–325

    Article  Google Scholar 

  • Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection—impacts of birds on limpets and algae. Ecology 73:981–991

    Article  Google Scholar 

Download references

Acknowledgements

J. E. Byrnes, A. L. Chaudoin, L. Carney, T. Mai, S. Bryson, and R. C. Coates provided diving assistance during field surveys and tethering experiments. D. Chuang, B. MacElvaine, T. Dillon, and P. L. Reynolds assisted in crab care and photo analysis. This research was conducted in accordance with current U.S. laws. A. R. Hughes, J. M. Davis, and A. Sih, and four anonymous reviewers provided constructive criticism on earlier versions of the manuscript. Financial support was provided by the Center for Population Biology (University of California–Davis) and a National Science Foundation (NSF) predoctoral fellowship to K. M. H., and NSF grant no. OCE 03-51778 to J. J. S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kristin M. Hultgren.

Additional information

Communicated by Pete Peterson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hultgren, K.M., Stachowicz, J.J. Alternative camouflage strategies mediate predation risk among closely related co-occurring kelp crabs. Oecologia 155, 519–528 (2008). https://doi.org/10.1007/s00442-007-0926-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-007-0926-5

Keywords

Navigation