Biological Invasions

, Volume 5, Issue 1–2, pp 23–31 | Cite as

Native species vulnerability to introduced predators: testing an inducible defense and a refuge from predation

  • W. Lindsay Whitlow
  • Neil A. Rice
  • Christine Sweeney

Abstract

To manage the impacts of biological invasions, it is important to determine the mechanisms responsible for the effects invasive species have on native populations. When predation by an invader is the mechanism causing declines in a native population, protecting the native species will involve elucidating the factors that affect native vulnerability. To examine those factors, this study measured how a native species responded to an introduced predator, and whether the native response could result in a refuge from predation. Predation by the green crab, Carcinus maenas, has contributed to the decline in numbers of native soft-shell clams, Mya arenaria, and efforts to eradicate crabs have proven futile. We tested how crab foraging affected clam burrowing, and how depth in the sediment affected clam survival. Clams responded to crab foraging by burrowing deeper in the sediment. Clams at shallow depths were more vulnerable to predation by crabs. Results suggest soft-shell clam burrowing is an inducible defense in response to green crab predation because burrowing deeper results in a potential refuge from predation by crabs. For restoring the native clam populations, tents could exclude crabs and protect clams, but when tents must be removed, exposing the clams to cues from foraging crabs should induce the clams to burrow deeper and decrease vulnerability. In general, by exposing potential native prey to cues from introduced predators, we can test how the natives respond, identify whether the response results in a potential refuge, and evaluate the risks to native species survival in invaded communities.

behavior depth Carcinus maenas inducible defense introduced predator invasive species Mya arenaria native species predator avoidance refuge 

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References

  1. Anolt BR and Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76: 2230–2234Google Scholar
  2. Banks PB (2001) Predation-sensitive grouping and habitat use by eastern grey kangaroos: a field experiment. Animal Behavior 61: 1013–1021Google Scholar
  3. Beal BF (1994) Biotic and abiotic factors influencing growth and survival in wild and cultured individuals of the soft-shell clam, Mya arenaria L., in Eastern Maine. PhD thesis, University of Maine, Orono, MaineGoogle Scholar
  4. Beal BF, Lithgow CD, Shaw DP, Renshaw S and Ouellette D (1995) Overwintering hatchery-reared individuals of the soft-shell clam, Mya arenaria L. – a field-test of site, clam size, and intraspecific density. Aquaculture 130: 145–158Google Scholar
  5. Behrens-Yamada S and Boulding EG (1996) The role of highly mobile crab predators in the intertidal zonation of their gastropod prey. Journal of Experimental Marine Biology and Ecology 204: 59–83Google Scholar
  6. Boulding EG (1984) Crab-resistant features of shells of burrowing bivalves: decreasing vulnerability by increasing handling time. Journal of Experimental Marine Biology and Ecology 76: 201–223Google Scholar
  7. Bronmark C and Miner JG (1992) Predator-induced phenotypical change in body morpholgy in crucian carp. Science 258(5086): 1348–1350Google Scholar
  8. Byers JE (1999) The distribution of an introduced mollusc and its role in the long-term demise of a native confamilial species. Biological Invasions 1: 339–352Google Scholar
  9. Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81(5): 1225–1239Google Scholar
  10. Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biological Conservation 78: 97–106Google Scholar
  11. Carlton JT and Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261: 78–82Google Scholar
  12. Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413: 635–639Google Scholar
  13. Checa AG and Cadee GC (1997) Hydraulic burrowing in the bivalve Mya arenaria linnaeus (Myoidea) and associated ligamental adaptations. Journal of Molluscan Studies 63: 157–171Google Scholar
  14. Cohen AN, Carlton JT and Fountain MC (1995) Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay, California. Marine Biology 122: 225–237Google Scholar
  15. Dodson SI, Tollrian R and Lampert W (1997) Daphnia swimming behavior during vertical migration. Journal of Plankton Research 19(8): 969–978Google Scholar
  16. Dow RL (1957) The Maine clam, Mya arenaria. A bulletin of the Department of Sea and Shore Fisheries, State House, Augusta, MaineGoogle Scholar
  17. Ebersole EL and Kennedy VS (1995) Prey preferences of blue crabs Callinectes sapidus feeding on three bivalve species. Marine Ecology Progress Series 118: 167–177Google Scholar
  18. Eggleston DB, Lipcius RN and Hines AH (1992) Density-dependent predation by blue crabs upon infaunal clam species with contrasting distribution and abundance patterns. Marine Ecology Progress Series 85: 55–68Google Scholar
  19. Elner RW(1981) Diet of green crab Carcinus maenas (L.) from Port Herbert, Southwestern Nova Scotia. Journal of Shellfish Research 1: 89–94Google Scholar
  20. Elner RW (1978) The mechanics of predation by the shore crab, Carcinus maenas (L.), on the edible mussel, Mytilus edulis L. Oecolgia 36: 333–344Google Scholar
  21. Fritts TH and Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annual Review of Ecology and Systematics 29: 113–140Google Scholar
  22. Glude JB (1955) The effects of temperature and predators on the abundance of the soft-shell clam, Mya arenaria, in New England. Transactions of the American Fisheries Society 84: 13–26Google Scholar
  23. de Goeij P and Luttikhuizen P (1998) Deep-burying reduces growth in intertidal bivalves: field and mesocosm experiments with Macoma balthica. Journal of Experimental Marine Biology and Ecology 228: 327–337Google Scholar
  24. Grosholz ED, Ruiz GM, Dean CA, Shirley KA, Maron JL and Connors PG (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81: 1206–1224Google Scholar
  25. Grosholz ED and Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biological Conservation 78: 59–66Google Scholar
  26. Grosholz ED and Ruiz GM (1995) Spread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California. Marine Biology 122: 239–247Google Scholar
  27. Hazlett BA (1996) Organisation of hermit crab beaviour: responses to multiple chemical inputs. Behaviour 133: 619–642Google Scholar
  28. Hughes RN and O'Brien N (2001) Shore crabs are able to transfer learned handling skills to novel prey. Animal Behaviour 61: 711–714Google Scholar
  29. Hughes RN and Elner RW (1979) Tactics of a predator, Carcinus maenas, and morphological responses of the prey, Nucella lapillus. Journal of Animal Ecology 48: 65–78Google Scholar
  30. Kitchell JF, Schindler DE, OgutuOhwayo R and Reinthal PN (1997) The Nile perch in Lake Victoria: interactions between predation and fisheries. Ecological Applications 7(2): 653–664Google Scholar
  31. Kolar CS and Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution 16(4): 199–204Google Scholar
  32. Leonard GH, Bertness MD and Yund PO (1999) Crab predation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. Ecology 80: 1–14Google Scholar
  33. Levinton JS (1982) Marine Ecology. Prentice-Hall Inc., New JerseyGoogle Scholar
  34. Lewis DE and Cerrato RM (1997) Growth uncoupling and the relationship between shell growth and metabolism in the soft shell clam Mya arenaria. Marine Ecology Progress Series 158: 177–189Google Scholar
  35. Lodge DM (1993) Biological invasions: lessons for ecology. Trends in Ecology and Evolution 8: 133–137Google Scholar
  36. Maaski H and Guillou J (1999) The role of biotic interactions in juvenile mortality of the cockle (Cerastoderma edule L.): field observations and experiment. Journal of Shellfish Research 18: 575–578Google Scholar
  37. McDonald PS, Jensen GC and Armstrong DA (2001) The competitive and predatory impacts of the nonindigenous crab Carcinus maenas (L.) on early benthic phase Dungeness crab Cancer magister Dana. Journal of Experimental Marine Biology and Ecology 258: 39–54Google Scholar
  38. Meire PM and Ervynck A (1986) Are oystercatchers (Haemoptopus ostralegus) selecting the most profitable mussels (Mytilus edulis)? Animal Behavior 34: 1427–1435Google Scholar
  39. Moody KE and Steneck RS (1993) Mechanisms of predation among large decapod crustaceans of the Gulf of Maine Coast: functional vs. phylogenetic patterns. Journal of Experimental Marine Biology and Ecology 168: 111–124Google Scholar
  40. Nilsson PA (2001) Predator behaviour and prey density: evaluating density-dependent intraspecific interactions on predator functional responses. Journal of Animal Ecology 70: 14–19Google Scholar
  41. Olson MH (1996) Predator–prey interactions in size-structured fish communities: implications of prey growth. Oecologia 108(4): 757–763Google Scholar
  42. Peacor SD and Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proceedings of the National Academy of Sciences 98: 3904–3908Google Scholar
  43. Rangeley RW and Thomas MLH (1987) Predatory behavior of juvenile shore crab Carcinus maenas (L.). Journal of Experimental Marine Biology and Ecology 108: 191–197Google Scholar
  44. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82(2): 523–540Google Scholar
  45. Rejmanek M (2000) Invasive plants: approaches and predictions. Austral Ecology 25: 497–506Google Scholar
  46. Ruiz GM, Carlton JT, Grosholz ED and Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37: 621–632Google Scholar
  47. Skilleter GA (1994) Refuges from predation and the persistence of estuarine clam populations. Marine Ecology Progress Series 109: 29–42Google Scholar
  48. Smith TE, Ydenberg RC and Elner RW (1999) Foraging behaviour of and excavating predator, the red rock crab (Cancer productus Randall) on soft shell clam (Mya arenaria L.) Journal of Experimental Marine Biology and Ecology 238: 185–197Google Scholar
  49. Stachowicz JJ and Hay ME (1999) Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense. Ecology 80(6): 2085–2101Google Scholar
  50. Stephens DW and Krebs JR (1986) Foraging Theory. Princeton University Press, Princeton, New JerseyGoogle Scholar
  51. Tollrian R (1995) Predator-induced morphological defenses – costs, life-history shifts, and maternal effects in Daphnia pulex. Ecology 76(6): 1691–1705Google Scholar
  52. Tollrian R and Dodson SI (1999) Inducible defenses in cladocera: constraints, costs, and multipredator environments. In: Tollrian R and Harvell C (eds) The Ecology and Evolution of Inducible Defenses, pp 177–202. Princeton University Press, Princeton, New JerseyGoogle Scholar
  53. Trussel GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50: 448–454Google Scholar
  54. Trussell GC and Smith LK (2000) Induced defenses in response to an invading crb predator: an explanation of historical and geographic phenotypic change. Proceedings of the National Academy of Sciences, USA 97(5): 2123–2127Google Scholar
  55. Van Dover C and Kirby-Smith WW (1979) Field Guide to Common Marine Invertebrates of Beaufort, NC. Duke University Marine Laboratory, Beaufort, North Carolina, 80 ppGoogle Scholar
  56. van der Veer HW, Feller RJ, Weber A and Witte JIJ (1998) Importance of predation by crustaceans upon bivalve spat in the intertidal zone of the Dutch Wadden Sea as revealed by immunological assays of gut contents. Journal of Experimental Marine Biology and Ecology 231: 139–157Google Scholar
  57. Virnstein RW (1977) The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay. Ecology 58: 119–1217Google Scholar
  58. Welch WR (1968) Changes in abundance of the green crab, Carcinus maenas (L.), in relation to recent temperature changes. Fisheries Bulletin of the US Fish and Wildlife Service 67(2): 337–345Google Scholar
  59. Whitlow WL (2002) Changes in native species after biological invasion: effects of introduced green crabs on native soft-shell clams and an estuarine community. PhD thesis, University of Michigan, Ann Arbor, MichiganGoogle Scholar
  60. Wilson WH (1991) Competition and predation in marine softsediment communities. Annual Review of Ecology and Systematics 21: 221–241Google Scholar
  61. Witte F, Goldschmidt T, Wanink J, Vanoijen M, Goudswaard K, Wittemaas E and Bouton N (1992) The destruction of an endemic species flock – quantitative data on the decline of the Haplochromine cichlids of LakeVictoria. Environmental Biology of Fishes 34(1): 1–28Google Scholar
  62. Zaklan SD and Ydenberg R (1997) The body size – burial depth relationship in the infaunal clam Mya arenaria. Journal of Experimental Marine Biology and Ecology 215: 1–17Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • W. Lindsay Whitlow
    • 2
  • Neil A. Rice
    • 3
  • Christine Sweeney
    • 3
  1. 1.Department of Biology/Environmental StudiesBowdoin CollegeBrunswickUSA
  2. 2.WellsUSA
  3. 3.Wells National Estuarine Research ReserveWellsUSA

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