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Host specificity of Sacculina carcini, a potential biological control agent of the introduced European green crab Carcinus maenas in California

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Abstract

The European green crab, Carcinus maenas, is an introduced marine predator established on the west coast of North America. We conducted laboratory experiments on the host specificity of a natural enemy of the green crab, the parasitic barnacle Sacculina carcini, to provide information on the safety of its use as a possible biological control agent. Four species of non-target, native California crabs (Hemigrapsus oregonensis, H. nudus, Pachygrapsus crassipes and Cancer magister) were exposed to infective larvae of S. carcini. Settlement by S. carcini on the four native species ranged from 33 to 53%, compared to 79% for green crabs. Overall, cyprid larvae tended to settle in higher numbers on individual green crabs than on either C. magister or H. oregonensis. However, for C. magister this difference was significant for soft-shelled, but not hard-shelled individuals. Up to 29% of the native crabs arrested early infections by melanizing the rootlets of the parasite. Most native and green crabs settled on by S. carcini became infected, especially when settled on by >3 cyprids. Infected green crabs died at more than twice the rate of uninfected green crabs. In contrast to green crabs, all infected native crabs died without producing an externa (reproductive sac). At high settlement intensities, infected native crabs frequently exhibited neurological symptoms (twitching, loss of movement) before death. These results indicate that use of S. carcini as a biological control agent could result in the death of native crabs. The magnitude of this effect would be proportional to the density of infected green crabs in the environment and the probability that cyprids would contact native crabs in the wild. Potential benefits of biological control should be assessed in relation to these potential non-target effects.

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References

  • BIP Barratt AA Evans CM Ferguson GM Barker MR McNeill CB Phillips (1997) ArticleTitleLaboratory nontarget host range of the introduced parasitoidsMicroctonus aethiopoides and M hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand Environmental Entomology 26 694–702

    Google Scholar 

  • GH Boettner JS Elkinton CJ Boettner (2000) ArticleTitleEffects of a biological control introduction on three nontarget native species of saturniid moths Conservation Biology 14 1798–1806 Occurrence Handle10.1046/j.1523-1739.2000.99193.x

    Article  Google Scholar 

  • EJ Boone AA Boettcher TD Sherman JJ O’Brian (2003) ArticleTitleCharacterization of settlement cues used by the rhizocephalan barnacle Loxothylacus texanus Marine Ecology Progress Series 252 187–197

    Google Scholar 

  • LE Caltagirone (1981) ArticleTitleLandmark examples in classical biological control Annual Review of Entomology 26 213–232 Occurrence Handle10.1146/annurev.en.26.010181.001241

    Article  Google Scholar 

  • AN Cohen JT Carlton MC Fountain (1995) ArticleTitleIntroduction, dispersal and potential impacts of the green crabCarcinus maenas in San Francisco Bay, California Marine Biology 122 225–237

    Google Scholar 

  • C Combes (2001) Parasitism: The Ecology and Evolution of Intimate Interactions University of Chicago Press Chicago

    Google Scholar 

  • P Drach (1939) ArticleTitleMue et cycle d’intermue chez les Crustacés Décapodes Annales de l’Institut Oceanographique de Monaco 19 103–391

    Google Scholar 

  • H Glenner M Werner (1998) ArticleTitleIncreased susceptibility of recently moulted Carcinus maenas (L.) to attack by the parasitic barnacle Sacculina carcini Thompson 1836 Journal of Experimental Marine Biology and Ecology 228 29–33 Occurrence Handle10.1016/S0022-0981(98)00019-7

    Article  Google Scholar 

  • JB Glude (1955) ArticleTitleThe 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 13–26

    Google Scholar 

  • D Greathead (1995) Benefits and risks of classical biological control H Hokkanen J Lynch (Eds) Biological Control: Benefits and Risks Cambridge University Press Cambridge, England 53–63

    Google Scholar 

  • ED Grosholz GM Ruiz (1996) ArticleTitleSpread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California Marine Biology 122 239–247

    Google Scholar 

  • ED Grosholz GM Ruiz (2003) ArticleTitleBiological invasions drive size increases in marine and estuarine invertebrates Ecology Letters 6 700–705 Occurrence Handle10.1046/j.1461-0248.2003.00495.x

    Article  Google Scholar 

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

    Google Scholar 

  • RW Hanks (1961) ArticleTitleChemical control of the green crab, Carcinus maenas (L.) Proceedings of the National Shellfish Association 52 75–86

    Google Scholar 

  • M Henneman J Memmott (2001) ArticleTitleInfiltration of a Hawaiian community by introduced biological control agents Science 293 1314–1316 Occurrence Handle10.1126/science.1060788 Occurrence Handle11509730 Occurrence Handle1:CAS:528:DC%2BD3MXmtFGjsr0%3D

    Article  PubMed  CAS  Google Scholar 

  • RW Hiatt (1948) ArticleTitleThe biology of the lined shore crab, Pachygrapsus crassipes Randall Pacific Science 2 135–213

    Google Scholar 

  • CP Hickman LS Roberts FM Hickman (1988) Principals of Integrated Zoology Times Mirror/Mosby College Publishers St. Louis, MO

    Google Scholar 

  • JT Høeg (1984a) ArticleTitleA culture system for rearing marine invertebrate larvae and its application to larvae of rhizocephalan barnacles Journal of Experimental Marine Biology and Ecology 84 167–172

    Google Scholar 

  • JT Høeg (1984b) ArticleTitleSize and settling behaviour in male and female cypris larvae of the parasitic barnacle Sacculina carcini Thompson (Crustacea: Cirripedia: Rhizocephala) Journal of Experimental Marine Biology and Ecology 76 145–156

    Google Scholar 

  • JT Høeg (1995) ArticleTitleThe biology and life cycle of the Rhizocephala (Cirripedia) Journal of the Marine Biological Association of the United Kingdom 75 517–550

    Google Scholar 

  • Høeg JT (1997) The epicaridean parasite Portunion maenadis as a biological control agent on Carcinus maenas. In: Thresher RE (ed) Proceedings of the First International Workshop on the Demography, Impacts and Management of the Iintroduced Populations of the European Crab, Carcinus maenas, pp 85–86. CSIRO Centre for Research on Introduced Marine Pests Technical Report 11. Hobart, Tasmania

  • JT Høeg J Lützen (1985) Crustacea Rhizocephala. Marine Invertebrates of Scandinavia Norwegian University Press Oslo

    Google Scholar 

  • JT Høeg J Lützen (1995) ArticleTitleLife cycle and reproduction in the Cirripedia Rhizocephala Oceanography and Marine Biology Annual Review 33 427–485

    Google Scholar 

  • Høeg JT, Werner M and Glenner H (1997) The parasitic castrator Sacculina carcini as a possible control agent of Carcinus maenas: background and results of preliminary work. In: Thresher RE (ed) Proceedings of the First International Workshop on the Demography, Impacts and Management of Introduced Populations of the European Crab, Carcinus maenas , pp 69–75. CSIRO Centre for Research on Introduced Marine Pests Technical Report 11, Hobart

  • FG Howarth (1991) ArticleTitleEnvironmental impacts of classical biological control Annual Review of Entomology 36 485–509 Occurrence Handle10.1146/annurev.en.36.010191.002413

    Article  Google Scholar 

  • GC Jensen PS McDonald DA Armstrong (2002) ArticleTitleEast meets west: competitive interactions between green crab Carcinus maenas, and native and introduced shore crab Hemigrapsus spp Marine Ecology Progress Series 225 251–262

    Google Scholar 

  • AM Kuris (1971) Population interactions between a shore crab and two symbionts. PhD dissertation University of California Berkeley, California

    Google Scholar 

  • AM Kuris KD Lafferty (1992) ArticleTitleModelling crustacean fisheries: effects of parasites on management strategies Canadian Journal of Fisheries and Aquatic Sciences 49 327–336 Occurrence Handle10.1139/f92-037

    Article  Google Scholar 

  • AM Kuris ME Torchin KD Lafferty (2002) ArticleTitle Fecampia erythrocephala rediscovered: prevalence and distribution of a parasitold of the European shore crab, Carcinus maenas Journal of the Marine Biological Association of the United Kingdom 82 955–960 Occurrence Handle10.1017/S0025315402006446

    Article  Google Scholar 

  • KD Lafferty AM Kuris (1996) ArticleTitleBiological control of marine pests Ecology 77 1989–2000

    Google Scholar 

  • SM Louda (2000) Negative ecological effects of the musk thistle biological control agent, Rhinocyllus conicus P Follett J Duan (Eds) Nontarget Effects of Biological Control Kluwer Academic Publishers Boston 215–243

    Google Scholar 

  • SM Louda RW Pemberton MT Johnson PA Follett (2003) ArticleTitleNontarget effects–The Achilles heel of biological control Retrospective analyses to reduce risk associated with biocontrol introductions. Annual Review of Entomology 48 365–396 Occurrence Handle1:CAS:528:DC%2BD3sXnvVyltQ%3D%3D

    CAS  Google Scholar 

  • PS McDonald GC Jensen DA Armstrong (2001) ArticleTitleThe 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 39–54 Occurrence Handle10.1016/S0022-0981(00)00344-0 Occurrence Handle11239624

    Article  PubMed  Google Scholar 

  • REC McFadyen (1998) ArticleTitleBiological controls of weeds Annual Review of Entomology 43 369–393 Occurrence Handle10.1146/annurev.ento.43.1.369 Occurrence Handle15012395 Occurrence Handle1:CAS:528:DyaK1cXktleitQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • Minchin D (1997) The influence of the parasitic cirripede Sacculina carcini on its brachyuran host Carcinus maenas within its home range. In: Thresher RE (ed) Proceedings of the First International Workshop on the Demography, Impacts and Management of the Introduced Populations of the European Crab, Carcinus maenas, pp 76–80. CSIRO Centre for Research on Introduced Marine Pests Technical Report 11. Hobart, Tasmania

  • JW Ropes (1968) ArticleTitleThe feeding habits of the green crab, Carcinus maenas (L.) Fishery Bulletin of the United States Fish & Wildlife Service 67 183–203

    Google Scholar 

  • C Rubiliani Y Turquier G Payen (1982) ArticleTitleRecherche sur l’ontogenèse des rhizocéphales. I. Les stades précoces de la phase endoparasitaire chez Sacculina carcini Thompson Cahiers de Biologie Marine 23 287–297

    Google Scholar 

  • DPA Sands (1998) Guidelines for testing host specificity of agents for biological control of arthropod pests M Zalucki R Drew G White (Eds) Pest Management–Future Challenges: 6th Australia Applied Entomological Research Conference University of Queensland Brisbane 556–560

    Google Scholar 

  • D Secord (2003) ArticleTitleBiological control of marine invasive species: cautionary tales and land-based lessons Biological Invasions 5 117–131 Occurrence Handle10.1023/A:1024054909052

    Article  Google Scholar 

  • D Simberloff P Stiling (1996a) ArticleTitleHow risky is biological control Ecology 77 1965–1974

    Google Scholar 

  • D Simberloff P Stiling (1996b) ArticleTitleRisks of species introduced for biological control Biological Conservation 78 185–192 Occurrence Handle10.1016/0006-3207(96)00027-4

    Article  Google Scholar 

  • RR Sokal FJ Rohlf (1981) Biometry Freeman New York

    Google Scholar 

  • DR Strong RW Pemberton (2000) ArticleTitleBiological control of invading species–risk and reform Science 288 1969–1970 Occurrence Handle10.1126/science.288.5473.1969 Occurrence Handle10877714 Occurrence Handle1:CAS:528:DC%2BD3cXkt1Gluro%3D

    Article  PubMed  CAS  Google Scholar 

  • MB Thomas AJ Willis (1998) ArticleTitleBiocontrol–risky but necessary Trends in Ecology and Evolution 13 325–329

    Google Scholar 

  • JN Thompson (1994) The coevolutionary process The University of Chicago Press Chicago

    Google Scholar 

  • Thresher RE (1996) Environmental tolerances of larvae of the European parasitic barnacle, Sacculina carcini (Rhizocephala: Sacculinidae): implications for use as a biological control agent against the introduced European crab, Carcinus maenas, CSIRO Centre for Research on Introduced Marine Pests. Hobart, Tasmania

  • RE Thresher M Werner JT Hoeg I Svane H Glenner NE Murphy C Wittwer (2000) ArticleTitleDeveloping the options for managing marine pests: specificity trials on the parasitic castrator, Sacculina carcini, against the European crab, Carcinus maenas, and related species Journal of Experimental Marine Biology and Ecology 254 37–51 Occurrence Handle10.1016/S0022-0981(00)00260-4 Occurrence Handle11058725

    Article  PubMed  Google Scholar 

  • ME Torchin KD Lafferty AM Kuris (1996) ArticleTitleInfestation of an introduced host, the European green crab, Carcinus maenas, by a symbiotic nemertean egg predator,Carcinonemertes epalti Journal of Parasitology 82 449–453 Occurrence Handle8636851 Occurrence Handle1:STN:280:DyaK283jslyktw%3D%3D

    PubMed  CAS  Google Scholar 

  • ME Torchin KD Lafferty AM Kuris (2001) ArticleTitleRelease from parasites as natural enemies: increased performance of a globally introduced marine crab Biological Invasions 3 333–345 Occurrence Handle10.1023/A:1015855019360

    Article  Google Scholar 

  • A Veillet (1945) ArticleTitleRecherches sur le parasitisme des crabes at des galathées par les Rhizocéphales et les Epicarides Annales de l’Institut Océanographique de Monaco 22 193–341

    Google Scholar 

  • G Walker (1987) ArticleTitleFurther studies concerning the sex ratio of the larvae of the parasitic barnacle, Sacculina carcini Thompson Journal of Experimental Marine Biology and Ecology 106 151–163 Occurrence Handle10.1016/0022-0981(87)90153-5

    Article  Google Scholar 

  • G Walker (1988) ArticleTitleObservations on the larval development of Sacculina carciniM (Crustacea: Cirripedia: Rhizocephala) Journal of the Marine Biological Association of the United Kingdom 68 377–390 Occurrence Handle10.1017/S0025315400043277

    Article  Google Scholar 

  • Walton WC (1997) Attempts at physical control of Carcinus maenas within coastal ponds of Martha’s Vineyard, MA (northeastern coast of North America). In: Proceedings of the First International Workshop on the Demography, Impacts and Management of Introduced Populations of the European Crab, Carcinus maenas, 64–65. CSIROCentre for Research on Introduced Marine Pests Technical Report 11, Hobart, Tasmania

  • S Yamada (2001) Global Invader: The European Green Crab. Sea Grant Communications Corvalis Oregon 140

    Google Scholar 

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Authors and Affiliations

  1. Marine Science Institute, University of California, Santa Barbara, CA, 93106, USA

    Jeffrey H. R Goddard

  2. Marine Science Institute and Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, 93106, USA

    Mark E Torchin, Armand M Kuris & Kevin D. Lafferty

  3. Western Ecological Research Center, US Geological Survey, Marine Science Institute, University of California, Santa Barbara, CA, 93106, USA

    Kevin D. Lafferty

Authors
  1. Jeffrey H. R Goddard
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  2. Mark E Torchin
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  3. Armand M Kuris
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  4. Kevin D. Lafferty
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Correspondence to Kevin D. Lafferty.

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Goddard, J.H.R., Torchin, M.E., Kuris, A.M. et al. Host specificity of Sacculina carcini, a potential biological control agent of the introduced European green crab Carcinus maenas in California. Biol Invasions 7, 895–912 (2005). https://doi.org/10.1007/s10530-003-2981-0

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  • DOI: https://doi.org/10.1007/s10530-003-2981-0

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