Skip to main content
Log in

Biotic resistance to green crab, Carcinus maenas, in California bays

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The distribution of the introduced European green crab, Carcinus maenas, was investigated in the central California embayments of Bodega Bay Harbor (BBH), Tomales Bay, and Bolinas Lagoon using baited traps and snorkel surveys. Adult green crabs were very spatially limited in all three embayments and occurred primarily in warm, shallow areas that lacked large native Cancer spp. crabs. The green crabs that were found in closest proximity to populations of Cancer spp. exhibited high levels of limb damage and loss; damage was strongly correlated with low ratios of intertidal area: edge, indicative of narrow areas of intertidal that are more easily accessed by large Cancer spp. moving up to forage during periods of tidal inundation. Up to 70% of the green crabs tethered in areas of BBH that are utilized by Cancer spp. experienced limb loss, while those tethered in the marsh, where there are no Cancer spp., were undamaged. The results suggest that the potential distribution of green crabs in the northeastern Pacific will be far less than has been predicted, and that their impacts may be largely attenuated through predation by and competition with native crab species.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abello P, Warman CG, Reid DG, Naylor E (1994) Chela loss in the shore crab Carcinus maenas (Crustacea: Brachyura) and its effect on mating success. Mar Biol 121:247–252

    Article  Google Scholar 

  • Ahyong ST (2005) Range extension of two invasive crab species in eastern Australia: Carcinus maenas (Linnaeus) and Pyromaia tuberculata (Lockington). Mar Pollut Bull 50:460–462

    Article  CAS  Google Scholar 

  • Baltz DM, Moyle PB (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecol Appl 3:246–255

    Article  Google Scholar 

  • Beukema JJ (1991) The abundance of shore crabs Carcinus maenas L. on a tidal flat in the Wadden Sea after cold and mild winters. J Exp Mar Biol Ecol 153:97–114

    Article  Google Scholar 

  • Blackburn TM, Duncan RP (2001) Determinants of establishment success in introduced birds. Nature 414:195–197

    Article  CAS  Google Scholar 

  • Botsford LW, Moloney CL, Hastings A, Largier JL, Powell TM, Higgins K, Quinn JF (1994) The influence of spatially and temporally varying oceanographic conditions on meroplanktonic metapopulations. Deep Sea Res 41:107–145

    Article  Google Scholar 

  • Broekhuyen GJ (1936) On the development, growth, and distribution of Carcinus maenas (L.). Arch Neer Zool 2:257–339

    Article  Google Scholar 

  • Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156

    Article  Google Scholar 

  • Byers JE, Noonburg EG (2003) Scale dependent effects of biotic resistance to biological invasion. Ecology 84:1428–1433

    Article  Google Scholar 

  • Carlton JT (1996) Pattern, process and prediction in marine invasion ecology. Biol Conserv 78:97–106

    Article  Google Scholar 

  • Carlton JT, Cohen AN (2003) Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aestuarii. J Biogeogr 30:1809–1820

    Article  Google Scholar 

  • Cohen AN, Carlton JT, Fountain MC (1995) Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay, California. Mar Biol 122:225–237

    Google Scholar 

  • Crawley MJ, Brown SL, Heard MS, Edwards GR (1999) Invasion-resistance in experimental grassland communities: species richness or species identity? Ecol Lett 2:140–148

    Article  Google Scholar 

  • Cuculescu M, Hyde D, Bowler K (1998) Thermal tolerance of two species of marine crab, Cancer pagurus and Carcinus maenas. J Therm Biol 23:107–110

    Article  Google Scholar 

  • deRivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376

    Article  Google Scholar 

  • Dumas JV, Witman JD (1993) Predation by herring gulls (Larus argentatus Coues) on two rocky intertidal crab species Carcinus maenas (L.) and Cancer irroratus (Say). J Exp Mar Biol Ecol 169:89–101

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen and Co. Ltd., London

    Book  Google Scholar 

  • Glude JB (1955) The effects of temperature and predators on the abundance of the softshell clam Mya arenaria in New England. Trans Am Fish Soc 84:13–26

    Article  Google Scholar 

  • Gray AE, Mulligan TJ, Hannah RW (1997) Food habits, occurrence, and population structure of the bat ray, Myliobatis californica, in Humboldt Bay, California. Environ Biol Fishes 49:227–238

    Article  Google Scholar 

  • Grosholz ED (2005) Recent biological invasion may hasten invasional meltdown by accelerating historical introductions. Proc Natl Acad Sci USA 102:1088–1091

    Article  CAS  Google Scholar 

  • Grosholz ED, Ruiz GM (1995) Spread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California. Mar Biol 122:239–247

    Google Scholar 

  • Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66

    Article  Google Scholar 

  • Grosholz E, Ruiz G (2000) The impact of European green crabs in central California. J Shellfish Res 19:631–632

    Google Scholar 

  • Grosholz ED, Ruiz GM, Dean CA, Shirley KA, Maron JL, Connors PG (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81:1206–1224

    Article  Google Scholar 

  • Grosholz E, Olin P, Williams B, Tinsman R (2001) Reducing predation on Manila clams by nonindigenous European green crabs. J Shellfish Res 20:913–919

    Google Scholar 

  • Hanks RW (1961) Chemical control of the green crab Carcinus maenas (L.). Proc Natl Shellfish Assoc 52:75–86

    Google Scholar 

  • Hines AH, Ruiz GM (1995) Temporal variation in juvenile blue crab mortality: nearshore shallows and cannibalism in Chesapeake Bay. Bull Mar Sci 57:884–901

    Google Scholar 

  • Hoagland P, Jin D (2006) Science and economics in the management of an invasive species. Bioscience 56:931–935

    Article  Google Scholar 

  • Hunt CE, Yamada SB (2003) Biotic resistance experienced by an invasive crustacean in a temperate estuary. Biol Invasions 5:33–43

    Article  Google Scholar 

  • Jamieson GS, Grosholz ED, Armstrong DA, Elner RW (1998) Potential ecological implications from the introduction of the European green crab, Carcinus maenas (Linnaeus), to British Columbia, Canada, and Washington, USA. J Nat Hist 32:1587–1598

    Article  Google Scholar 

  • Jensen GC, McDonald PS, Armstrong DA (2002) East meets west: competitive interactions between green crab Carcinus maenas, and native and introduced shore crab Hemigrapsus spp. Mar Ecol Prog Ser 225:251–262

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Knudson JW (1964) Observations of the reproductive cycles and ecology of the common Brachyura and crablike Anomura of Puget Sound, Washington. Pac Sci 18:3–33

    Google Scholar 

  • Lafferty KD, Kuris AM (1996) Biological control of marine pests. Ecology 77:1989–2000

    Article  Google Scholar 

  • Lake PS, O’Dowd DJ (1991) Red crabs in rain forest, Christmas Island: biotic resistance to invasion by an exotic snail. Oikos 62:25–29

    Article  Google Scholar 

  • Levine JM (2000) Species diversity and biological invasions: relating local process to community pattern. Science 288:852–854

    Article  CAS  Google Scholar 

  • Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invisibility. Oikos 87:15–26

    Article  Google Scholar 

  • Lohrer AM, Whitlatch RB (2002) Interactions among aliens: apparent replacement of one exotic species by another. Ecology 83:719–732

    Article  Google Scholar 

  • Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536

    Article  Google Scholar 

  • Maron JL, Vilá M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Mathews LM, McKnight AE, Avery R, Lee KT (1999) Incidence of autonomy in New England populations of green crabs, Carcinus maenas, and an examination of the effect of claw autonomy on diet. J Crust Biol 19:713–719

    Article  Google Scholar 

  • McVean A, Findlay I (1979) The incidence of autotomy in an estuarine population of the crab Carcinus maenas. J Mar Biolog Assoc U.K. 59:341–354

    Article  Google Scholar 

  • Moller H (1996) Lessons for invasion theory from social insects. Biol Conserv 78:125–142

    Article  Google Scholar 

  • Naeem S, Knops JMH, Tilman D, Howe KM, Kennedy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108

    Article  Google Scholar 

  • Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models: regression, analysis of variance, and experimental designs. Irwin, California

    Google Scholar 

  • Palacios R, Armstrong DA, Orensanz J (2000) Fate and legacy of an invasion: extinct and extant populations of the soft-shell clam (Mya arenaria) in Grays Harbor (Washington). Aquat Conserv Mar Freshw Ecosyst 10:279–303

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pimm SL (1989) Theories predicting success and impact of introduced species. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M, Williamson M (eds) Biological invasions: a global perspective. John Wiley and Sons, Chichester, UK, pp 351–365

  • Reusch TBH (1998) Native predators contribute to invasion resistance to the non-indigenous bivalve Musculista senhousia in southern California, USA. Mar Ecol Prog Ser 170:159–168

    Article  Google Scholar 

  • Robinson JV, Wellborn GA (1988) Ecological resistance to the invasion of a freshwater clam, Corbicula fluminea—fish predation effects. Oecologia 77:445–452

    Article  Google Scholar 

  • Robles C, Sweetham DA, Dittman D (1989) Diel variation of intertidal foraging by Cancer productus in British Columbia. J Nat Hist 23:1041–1049

    Article  Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17(4):170–176

    Article  Google Scholar 

  • Smith LD (1990) Patterns of limb loss in the blue crab, Callinectes sapidus Rathbun, and the effects of autotomy on growth. Bull Mar Sci 46:23–36

    Google Scholar 

  • Smith LD (1992) The impact of limb autotomy on mate competition in blue crabs Callinectes sapidus Rathbun. Oecologia 89:494–501

    Article  Google Scholar 

  • Smith LD (1995) Effects of limb autotomy and tethering on juvenile blue crab survival from cannibalism. Mar Ecol Prog Ser 116:65–74

    Article  Google Scholar 

  • Smith LD, Hines AH (1991) The effect of cheliped loss on blue crab Callinectes sapidus Rathbun foraging rate on soft-shell clams Mya arenaria L. J Exp Mar Biol Ecol 151:245–256

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, New York

    Google Scholar 

  • Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579

    Article  CAS  Google Scholar 

  • Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590

    Article  Google Scholar 

  • Stevens BG, Armstrong DA, Cusimano R (1982) Feeding habits of the Dungeness crab Cancer magister as determined by the index of relative importance. Mar Biol 72:135–145

    Article  Google Scholar 

  • Syrjala SE (1996) A statistical test for a difference between the spatial distributions of two populations. Ecology 77:75–80

    Article  Google Scholar 

  • Thresher RE (1997) Proceedings of the first international workshop on the demography, impacts and management of introduced populations of the European crab, Carcinus maenas. Technical Report 11. Centre for Research on Introduced Marine Pests, Hobart, Tasmania

  • Trowbridge CD (1995) Establishment of the green alga Codium fragile ssp tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. J Ecol 83:949–965

    Article  Google Scholar 

  • Trussell GC (2000) Predator-induced plasticity and morphological trade-offs in latitudinally separated populations of Littorina obtusata. Evol Ecol Res 2:803–822

    Google Scholar 

  • Trussell GC, Nicklin MO (2002) Cue sensitivity, inducible defense, and trade-offs in a marine snail. Ecology 83:1635–1647

    Article  Google Scholar 

  • Trussell GC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci USA 97:2123–2127

    Article  CAS  Google Scholar 

  • Vermeij GJ (1982) Phenotypic evolution in a poorly dispersing snail after arrival of a predator. Nature 299:349–350

    Article  Google Scholar 

  • Visser EP, McDonald PS, Armstrong DA (2004) The impact of yellow shore crabs, Hemigrapsus oregonensis, on early benthic phase Dungeness crabs, Cancer magister, in intertidal oyster shell mitigation habitat. Estuaries 27:699–715

    Article  Google Scholar 

  • Webber JD, Cech JJ Jr (1998) Nondestructive diet analysis of the leopard shark from two sites in Tomales Bay, California. Calif Fish Game 84:18–24

    Google Scholar 

  • Whitlow WL, Rice NA, Sweeney C (2003) Native species vulnerability to introduced predators: testing an inducible defense and a refuge from predation. Biol Invasions 5:23–31

    Article  Google Scholar 

  • Winn RN (1986) Comparative ecology of three cancrid crab species (Cancer anthonyi, C. antennarius and C. productus) in marine subtidal habitats in southern California. Ph.D. dissertation, University of Southern California, Los Angeles

  • Yamada SB (2001) Global invader: the European green crab. Oregon State University, Oregon Sea Grant

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Zimmer Faust RK, Fielder DR, Heck KL Jr, Coen LD, Morgan SG (1994) Effects of tethering on predatory escape by juvenile blue crabs. Mar Ecol Prog Ser 111:299–303

    Article  Google Scholar 

Download references

Acknowledgments

We dedicate this paper to the memory of Eva Mulder, who assisted us with our field work and is greatly missed by all who knew her. We are grateful to the staff of the Bodega Marine Laboratory for providing space and logistical support throughout this study, and thank Mariah Cariss and Tom Wadsworth for field assistance. Statistical consultation was provided by Timothy Miller, Paul Sampson, Christopher Green and Pavel Krivitsky. This research was funded in part by a grant from Washington Sea Grant Program, University of Washington, pursuant to National Ocean and Atmospheric Administration Award no. NA76RG0119, project R/ES-24. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its subagencies. Contribution number 2374, Bodega Marine Laboratory, University of California at Davis. All work conducted in this study complied with the current laws of the United States of America.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gregory C. Jensen.

Additional information

Communicated by J.P. Grassle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jensen, G.C., McDonald, P.S. & Armstrong, D.A. Biotic resistance to green crab, Carcinus maenas, in California bays. Mar Biol 151, 2231–2243 (2007). https://doi.org/10.1007/s00227-007-0658-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0658-4

Keywords

Navigation