Biological Invasions

, Volume 3, Issue 4, pp 333–345

Release from Parasites as Natural Enemies: Increased Performance of a Globally Introduced Marine Crab

  • Mark E. Torchin
  • Kevin D. Lafferty
  • Armand M. Kuris
Article

Abstract

Introduced species often seem to perform better than conspecifics in their native range. This is apparent in the high densities they may achieve or the larger individual sizes they attain. A prominent hypothesis explaining the success of introduced terrestrial species is that they are typically free of or are less affected by the natural enemies (competitors, predators, and parasites) they encounter in their introduced range compared to their native range. To test this hypothesis in a marine system, we conducted a global assessment of the effect of parasitism and predation on the ecological performance of European green crab populations. In Europe, where the green crab is native, crab body size and biomass were negatively associated with the prevalence of parasitic castrators. When we compared native crab populations with those from introduced regions, limb loss (an estimator of predation) was not significantly lower in introduced regions, parasites infected introduced populations substantially less and crabs in introduced regions were larger and exhibited a greater biomass. Our results are consistent with the general prediction that introduced species suffer less from parasites compared to populations where they are native. This may partly explain why the green crab is such a successful invader and, subsequently, why it is a pest in so many places.

Carcinus maenas green crab introduced species natural enemies parasites predators global invasion 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abello P,Aagaard A,Warman CG andDepledge MH (1997) Spatial variability in the population structure of the shore crab Carcinus maenas (Crustacea: Brachyura) in a shallow-water, weakly tidal fjord. Marine Ecology Progress Series 147: 97-103Google Scholar
  2. Andrews JD (1980) A review of introductions of exotic oysters and biological planning for new importations. Marine Fisheries Review 42: 1-11Google Scholar
  3. ap Rheinallt T andHughes RN (1985) Handling methods used by the velvet swimming crab Liocarcinus puber when feeding on molluscs and shore crabs. Marine Ecology Progress Series 25: 63-70Google Scholar
  4. Barton DP (1997) Introduced animals and their parasites: the cane toad, Bufo marinus, in Australia. Australian Journal of Ecology 22: 316-324Google Scholar
  5. Beveridge I (1990) Taxonomic revision of Australian Eutetrarhynchidae Guiart (Cestoda: Trypanorhyncha). Invertebrate Taxonomy 4: 785-845Google Scholar
  6. Blaustein AR,Kuris AM andAlió JJ (1983) Pest and parasite speciesrichness problems. American Naturalist 122: 556-566Google Scholar
  7. Bourdon R (1960) Rhizocéphales et isopodes parasites des décapodes marcheurs de la Baie de Quiberon. Bulletin de la Société des Sciences de Nancy 19: 134-153Google Scholar
  8. Bourdon R (1963) Epicarides et Rhizocépales de Roscoff. Cahiers de Biologie Marine 4: 415-434Google Scholar
  9. Bourdon R (1964) Epicarides et Rhizocéphales du Bassin D'Arcachon. Procés-Verbaux de la Société Linnéenne de Bordeaux 101: 1-7Google Scholar
  10. Brattey J,Elner RW,Uhazy LS andBagnall AE (1985) Metazoan parasites and commensals of five crab (Brachyura) species from eastern Canada. Canadian Journal of Zoology 63: 2224-2229Google Scholar
  11. Bush AO,Lafferty KD,Font JM andShostak AW (1997) Parasitology meets ecology: definitions, clarifications, examples and Margolis et al. revisited. Journal of Parasitology 83: 575-583Google Scholar
  12. Buttermore RE,Turner E andMorrice MG (1994) The introduced northern Pacific seastar, Asterias amurensis in Tasmania. Memoirs of the Queensland Museum 36: 21-25Google Scholar
  13. Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81: 1225-1239Google Scholar
  14. Callaway RM andAschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290: 521-523Google Scholar
  15. Calvo-Ugarteburu G andMcQuaid CD (1998) Parasitism and introduced species: epidemiology of trematodes in the intertidal mussels Perna perna and Mytilus galloprovincialis. Journal of Experimental Marine Biology and Ecology 220: 47-65Google Scholar
  16. Carlton JT andGeller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 266: 78-82Google Scholar
  17. Carlton JT,Thompson JK,Schemel LE andNichols aFH (1990) Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. I. Introduction and dispersal. Marine Ecology Progress Series 66: 81-94Google Scholar
  18. Castilho F andBarandela T (1990) Ultrastructural study on the spermatogenesis and spermatozoon of the metacercariae of Microphallus primas (Digenea), a parasite of Carcinus maenas. Molecular Reproduction and Development 25: 140-146Google Scholar
  19. Caullery M andMesnil F (1903) Recherches sur les Fecampia Giard, Turbellaries Rhabdoceles, Parasites internes des crustaces. Annales de la Faculte des Sciences de Marseille 13: 131-168Google Scholar
  20. Ching HL (1991) Lists of larval worms from marine invertebrates of the Pacific Coast of North America. Journal of the Helminthological Society of Washington 58: 57-68Google Scholar
  21. Coe WR (1902) The Nemertean parasites of crabs. American Naturalist 36: 431-450Google Scholar
  22. Comely CA andAnsell AD (1989) The incidence of Carcinonemertes carcinophila (Kolliker) on some decapod crustaceans from the Scottish West Coast. Ophelia 30: 225-233Google Scholar
  23. Cornell HV andHawkins BA (1994) Patterns of parasitoid accumulation on introduced herbivores. In: Hawkins BA andSheehan W (eds) Parasitoid Community Ecology, pp 77-89. Oxford University Press, New YorkGoogle Scholar
  24. Crothers JH (1968) The biology of the shore crab Carcinus meanas (L.) 2. The life of the adult crab. Field Studies 2: 579-614Google Scholar
  25. De Bach P (1974) Biological Control by Natural Enemies. Cambridge University press, LondonGoogle Scholar
  26. Delvinquier BLJ andFreeland WJ (1988) Protozoan parasites of the cane toad, Bufo marinus, in Australia. Australian Journal of Zoology 36: 301-316Google Scholar
  27. Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conservation Biology 2: 31-39Google Scholar
  28. Dumas JV andWitman JD (1993) Predation by herring gulls (Larus argentatus Coues) on two rocky intertidal crab species [Carcinus maenas (L.) and Cancer irroratus Say]. Journal of Experimental Marine Biology and Ecology 169: 89-101Google Scholar
  29. Edwards DC,Conover DO andSutter FI (1882) Mobile predators and the structure of marine intertidal communities. Ecology 63: 1175-1180Google Scholar
  30. Elton CS (1958) The Ecology of Invasions by Animals and Plants. Methuen, LondonGoogle Scholar
  31. Font WF andTate DC (1994) Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolation. Journal of Parasitology 80: 682-688Google Scholar
  32. Gallien L and Bloch F (1936) Recherches sur Lecithomyzon maenadis Bloch & Gallien, copepode parasite de la ponte de Carcinus maenas Pennant. Bulletin Biologique de France et Belgique 70: 36-53Google Scholar
  33. 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
  34. Grisley MS,Boyle PR andKey LN (1996) Eye puncture as a route of entry for saliva during predation on crabs by the octopus Eledone cirrhosa (Lamark). Journal of Experimental Marine Biology and Ecology 202: 225-237Google Scholar
  35. Grosholz ED,Ruiz GM,Dean CA,Shirley KA,Maron JL andConnors PG (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81: 1206-1224Google Scholar
  36. Høeg JT (1995) The biology and lifecycle of the Rhizocephala (Cirripedia). Journal of the Marine Biological Association of the UK 75: 517-550Google Scholar
  37. Høeg J andLűtzen J (1985) Crustacea Rhizocephala. Marine Invertebrates of Scandinavia. Norwegian University Press, OsloGoogle Scholar
  38. Humes AG (1942) The morphology, taxonomy, and bionomics of the nemertean genus Carcinonemertes. Illinois Biological Monographs 18: 1-105Google Scholar
  39. Johnson MW (1957) The copepod Choniosphaera cancrorum parasitizing a new host, the green crab Carcinides maenas. Journal of Parasitology 43: 470-473Google Scholar
  40. Kuris AM andGurney R (1997) Survey of Tasmanian crabs for parasites: a progress report. Proceedings of the first international workshop on the demography, impacts and management of the introduced populations of the European crab, Carcinus maenas. Centre for Research on Introduced Marine Pests. Technical Report 11: 92-94Google Scholar
  41. Kuris AM andLafferty KD (2000) Parasite-host modeling meets reality: adaptive peaks and their ecological attributes. In: Poulin R,Morand S andSkorping A (eds) Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality, pp 9-26. Elsevier Science, AmsterdamGoogle Scholar
  42. Kuris AM,Poinar GO andHess RT (1980) Post-larval mortality of the endoparasitic isopod castrator Portunion conformis (Epicaridea: Entoniscidae) in the shore crab, Hemigrapsus oregonensis, with a description of the host response. Parasitology 80: 211-232Google Scholar
  43. Kuris AM,Ra'anan Z,Sagi A andCohen D (1987) Morphotypic differentiation of male Malaysian giant prawns, Macrobrachium rosenbergii. Journal of Crustacean Biology 7: 219-237Google Scholar
  44. Kuris AM,Blau SF,Paul AJ,Shields JD andWickham DE (1991) Infestation by brood symbionts and their impact on egg mortality of the red king crab, Paralithodes camtschatica, in Alaska: geographic and temporal variation. Canadian Journal of Fisheries and Aquatic Sciences 48: 559-568Google Scholar
  45. Lafferty KD (1999) The evolution of trophic transmission. Parasitology Today 15: 111-115Google Scholar
  46. Lafferty KD andKuris AM (1996) Biological control of marine pests. Ecology 77: 1989-2000Google Scholar
  47. Lampo M andBayliss P (1996) The impact of ticks on Bufo marinus from native habitats. Parasitology 113: 199-206Google Scholar
  48. Last PR andStevens JD (1994) Sharks and Rays of Australia. CSIRO Publications, East Melbourne, AustraliaGoogle Scholar
  49. Le Roux PJ,Branch GM andJoska MAP (1990) On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L.) along the South African Coast. South African Journal of Marine Science 9: 85-93Google Scholar
  50. Lohrer AM,Whitlatch RB,Wada K andFukui Y (2000) Home and away: comparisons of resource utilization by a marine species in native and invaded habitats. Biological Invasions 2: 41-57Google Scholar
  51. Lodge DM (1993) Species invasions and deletions: community effects and responses to climate and habitat change. In: Kareiva PM,Kingsolver JG andHuey RB (eds) Biotic Interactions and Global Change, pp 367-387. Sinauer Associates, Sunderland MassachusettsGoogle Scholar
  52. MacPhail JS,Lord EI andDickie LM (1955) The green crab-A new clam enemy. Fisheries Research Bulletin of Canada, Atlantic Progress Report 63: 3-12Google Scholar
  53. Mathews LM,McKnight AE,Avery R andLee KT (1999) Incidence of autotomy in NewEngland populations of green crabs, Carcinus maenas, and the examination of the effect of claw autotomy on diet. Journal of Crustacean Biology 19: 713-719Google Scholar
  54. Mathieson S,Berry AJ andKennedy S (1998) The parasitic rhizocephalan barnacle Sacculina carcini in crabs of the Forth Estuary, Scotland. Journal of the Marine Biological Association, UK 78: 665-667Google Scholar
  55. McDermott JJ (1998) The western Pacific brachyuran (Hemigrapsus sanguineus: Grapsidae), in its newhabitat along the Atlantic coast of the United States: geographic distribution and ecology. ICES Journal of Marine Science 55: 289-298Google Scholar
  56. McVean A andFindlay I (1979) The incidence of autotomy in an estuarine population of the shore crab Carcinus maenas. Journal of the Marine Biological Association, UK 59: 341-354Google Scholar
  57. Minchin D (1997) The influence of the parasitic cirripede Sacculina carcini on its brachyuran host Carcinus maenas within its home range. In: Thresher R (ed) Proceedings of the First International Workshop on the Demography, Impacts and Management of the Introduced Populations of the European Crab, Carcinus maenas, CSIRO Marine Laboratories, Hobart, Centre for Research on Introduced Marine Pests. Technical Report Number 11Google Scholar
  58. Moreira F (1995) Diet of black-headed gulls Larus ridibundus on emerged intertidal areas in the Tagus estuary (Portugal): predation or grazing? Journal of Avian Biology 26: 277-282Google Scholar
  59. O'Brien J andvan Wyk P (1985) Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. In: Wenner AM (ed) Crustacean Issues 3. Factors in Adult Growth, pp 191-218. A.A. Balkema, Rotterdam, The NetherlandsGoogle Scholar
  60. Pichelin S,Kuris AM andGurney R (1998) Morphological and biological notes on Polymorphus (Profilicollis) sphaerocephalus and Corynosoma stanleyi (Polymorphidae: Acanthocephala). Journal of Parasitology 84: 798-801Google Scholar
  61. Poinar GO Jr andKuris AM (1975) Juvenile Ascarophis (Spirurida: Nematoda) parasitizing intertidal decapod Crustacea in California: with notes on prevalence and effects on host growth and survival. Journal of Invertebrate Pathology 26: 375-382Google Scholar
  62. Rasmussen E (1973) Systematics and the ecology of the Isefjord marine fauna (Denmark). Ophelia 11: 142-165Google Scholar
  63. Settle WH andWilson LT (1990) Invasion by the variegated leafhopper and biotic interactions: parasitism, competition, and apparent competition. Ecology 71: 1461-1470Google Scholar
  64. Smith LD andHines AH (1991) Autotomy in blue crab (Callinectes sapidus Rathbun) populations: geographic, temporal, and ontogenetic variation. Biological Bulletin 180: 416-431Google Scholar
  65. Southward AJ (1950) On the occurence in the Isle of Man of Fecampia erythrocephala Giard, a platyhelminth parasite of crabs. Marine Biological Station at Port Erin, Isle of Man Annual Report 1950: 27-10Google Scholar
  66. Stunkard HW (1956) Studies on the parasites of the green crab, Carcinides maenas. Biological Bulletin 111: 295Google Scholar
  67. Takahashi T andMatsuura S (1994) Laboratory studies on molting and growth of the shore crab, Hemigrapsus sanguineus de Haan, parasitized by a rhizocephalan barnacle. Biological Bulletin 186: 300-308Google Scholar
  68. Thebaud C andSimberloff D (2001) Are plants really larger in their introduced ranges? American Naturalist 157: 231-236Google Scholar
  69. Thompson AB (1985) Analysis of Profilicollis botulus (Acanthocephala: Echinorhynchidae) burdens in the shore crab, Carcinus maenas. Journal of Animal Ecology 54: 595-604Google Scholar
  70. Thresher RE (1997) Introduction. Proceedings of the first international workshop on the demography, impacts and management of the introduced populations of the European crab, Carcinus maenas. Centre for Research on Introduced Marine Pests. Technical Report 11: 1-2Google Scholar
  71. Torchin ME,Lafferty KD andKuris AM (1996) Infestation of an introduced host, the European green crab, Carcinus maenas, by a symbiotic nemertean egg predator, Carcinonemertes epialti. Journal of Parasitology 82: 449-453Google Scholar
  72. Torchin ME,Lafferty KD andKuris AM (2002) Parasites and marine invasions. Parasitology 125 (suppl) (in press)Google Scholar
  73. Van Engel WA Dillon WA,Zwerner D andEldridge D (1965) Loxothylacus panopaei (Cirripedia, Sacculinidae) an introduced parasite on a xanthid crab in Chesapeake Bay, USA Crustaceana 10: 111-112Google Scholar
  74. Wickham DE (1979) Predation by the nemertean Carcinonemertes errans on the eggs of the Dungeness crab Cancer magister. Marine Biology 55: 45-53Google Scholar
  75. Yamaguchi T,Tokunaga S andAratake H (1994) Contagious infection by the rhizocephalan parasite Sacculina sp. in the grapsid crab Hemigrapsus sanguineus (De Haan). Crustacean Research 23: 89-101Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Mark E. Torchin
    • 1
  • Kevin D. Lafferty
    • 2
  • Armand M. Kuris
    • 1
  1. 1.Marine Science Institute and Department of Ecology, Evolution and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA; Author for correspondence (e-mail
  2. 2.US Geological Survey, Western Ecological Research Center, c/o Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA

Personalised recommendations