Biological Invasions

, Volume 7, Issue 6, pp 885–894 | Cite as

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

  • Mark E. Torchin
  • James E. Byers
  • Todd C. Huspeni
Article

Abstract

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.

Keywords

Batillaria attramentaria Batillaria cumingi Cerithidea californica fish parasites invasion ecology local extinctions non-indigenous species trematodes 

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References

  1. Adachi, N, Wada, K 1998Distribution of two gastropods, Batillaria multiformis and B. cumingi (Batillariidae) at a co-occuring areaVenus(Japanese Journal of Malacology)57115120Google Scholar
  2. Andrews, JD 1980A review of introductions of exotic oysters and biological planning for new importationsMarine Fisheries Review42111Google Scholar
  3. Augustine, L, Muller-Parker, G 1998Selective predation by the mosshead sculpin Clinocottus globiceps on the sea anemone Anthopleura elegantissima and its two algal symbiontsLimnology and Oceanography43711715Google Scholar
  4. Barrett EM (1963) The California oyster industry. California Department Fish and Game, Fish Bulletin 123:2–103Google Scholar
  5. Barse, AM, Secor, DH 1999An exotic nematode parasite of the American eelFisheries24611CrossRefGoogle Scholar
  6. Behrens Yamada, S, Sankurathri, CS 1977Direct development in the intertidal gastropod B. zonalisVeliger20179Google Scholar
  7. Bonnot, P 1935The California oyster industryCalifornia Fish and Game216580Google Scholar
  8. Bush, AO, Lafferty, KD, Font, JM, Shostak, AW 1997Parasitology meets ecology: definitions, clarifications, examples and Margolis et al. revisitedJournal Parasitology83575583Google Scholar
  9. Byers, JE 1999The distribution of an introduced mollusc and its role in the long-term demise of a native confamilial speciesBiological Invasions1339352CrossRefGoogle Scholar
  10. Byers, JE 2000aCompetition between two estuarine snails: implications for invasions of exotic speciesEcology8112251239Google Scholar
  11. Byers, JE 2000bDifferential susceptibility to hypoxia aids estuarine invasionMarine Ecology Progress Series203123132Google Scholar
  12. Byers, JE, Goldwasser, L 2001Exposing the mechanism and timing of impact of non-indigenous species on native speciesEcology8213301343Google Scholar
  13. Carlton, JT 1975Extinct and endangered populations of the endemic mud snail Cerithidea californica in Northern CaliforniaBulletin of the American Malacological Union416566Google Scholar
  14. Ching, HL 1991Lists of larval worms from marine invertebrates of the Pacific Coast of North AmericaJournal of Helminthological Society Washington585768Google Scholar
  15. Crivelli, AJ 1983The destruction of aquatic vegetation by carpHydrobiologia1063742CrossRefGoogle Scholar
  16. Font, WF, Tate, DC 1994Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolationJournal of Parasitology80682688PubMedGoogle Scholar
  17. Freeland, WJ 1983Parasites and the coexistence of animal host speciesAmerican Naturalist121223236CrossRefGoogle Scholar
  18. Harada, M, Suguri, S 1989Surveys on cercariae in brackish water snails in Kagawa Prefecture, Shikoku, JapanJapanese Journal of Parasitology38388391Google Scholar
  19. Hayward, CJ, Iwashita, M, Crane, JS, Ogawa, K 2001First report of the invasive eel pest Pseudodactylogyrus biniin North America and in wild American eelsDiseases of Aquatic Organisms445360PubMedGoogle Scholar
  20. Heyneman, DH, Lim, K, Jeyarasasingam, U 1972Antagonism of Echinostoma liei (Trematoda: Echinostomatidae) against the trematodes Paryphostomum segregatum and Schistosoma mansoniParasitology65223233PubMedGoogle Scholar
  21. Holmes, JC, Bethel, WM 1972

    Modification of intermediate host behavior by parasites

    Canning, EUWright, CA. eds. Behavioral Aspects of Parasite TransmissionAcademic PressLondon123149
    Google Scholar
  22. Holmes, JC, Minchin, D 1995Two exotic copepods imported into Ireland with Pacific oyster Crassostrea gigas (Thunberg)Irish Naturalist’s Journal251720Google Scholar
  23. Holt, RD 1984Spatial Heterogeneity, indirect interactions, and the coexistence of prey speciesAmerican Naturalist124377406CrossRefGoogle Scholar
  24. Holt, RD, Lawton, JH 1994The ecological consequences of shared natural enemiesAnnual Review of Ecology and Systematics25495520CrossRefGoogle Scholar
  25. Huspeni, TC, Lafferty, KD 2004Using larval trematodes that parasitize snails to evaluate a salt-marsh restoration projectEcological Applications14795804Google Scholar
  26. Ito, J 1988A subsequent monograph of cercariae in JapanJapanese Journal of Parasitology37269322Google Scholar
  27. Kuris, AM 1974Trophic interactions: similarity of parasitic castrators to parasitoidsQuarterly Review of Biology49129148CrossRefGoogle Scholar
  28. Kuris, AM 1997

    Host behavior modification an evolutionary perspective

    Beckage, NE. eds. Parasites and Pathogens Effects on Host Hormones and BehaviorChapman HallNew York293315
    Google Scholar
  29. Kuris, AM, Warren, J 1980Echinostome cercarial penetration and metacercarial encystment as mortality factors for a second intermediate host, Biomphalaria glabrataJournal of Parasitology66630635PubMedGoogle Scholar
  30. Lafferty, KD 1991Effects of parasitic castration on the salt marsh snail, Cerithidea californicaUniversity of CaliforniaSanta BarbaraPhD dissertation.Google Scholar
  31. Lafferty, KD 1992Foraging on prey that are modified by parasitesAmerican Naturalist140854867CrossRefGoogle Scholar
  32. Lafferty, KD 1993Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californicaMarine Ecology Progress Series96229237Google Scholar
  33. Lafferty, KD 1999The evolution of trophic transmissionParasitology Today15111115CrossRefPubMedGoogle Scholar
  34. Lafferty, KD, Morris, AM 1996Altered behavior of parasitized killifish increases susceptibility to predation by final bird hostsEcology7713901397Google Scholar
  35. Lim, HK, Heyneman, D 1972Intramolluscan intertrematode antagonism: a review of factors influencing the host-parasite system and its possible role in biological controlAdvances in Parasitology10191268PubMedGoogle Scholar
  36. Llewellyn, J 1965

    The evolution of parasitic platyhelminths

    Taylor, AER eds. Evolution of ParasitesBlackwell Scientific PublicationsOxford4778
    Google Scholar
  37. Martin, WE 1972An annotated key to the cercariae that develop in the snail Cerithidea californicaBulletin of Southern California Academy of Science713943Google Scholar
  38. Martin, WE, Adams, JE 1961Life cycle of Acanthoparyphium spinulosum Johnston, 1917 (Echinostomatidae: Trematoda)Journal of Parasitology47777782PubMedGoogle Scholar
  39. Minchella, DJ, Scott, ME 1991Parasitism: a cryptic determinant of animal community structureTrends in Ecology and Evolution6250254CrossRefGoogle Scholar
  40. Mitchell, AJ, Salmon, MJ, Huffman, DG, Goodwin, AE, Brant, TM 2000Prevalence and pathogenicity of a heterophyid trematode infecting the gills of an endangered fish, the fountain darter, in two central Texas spring-fed riversJournal of Aquatic Animal Health12283289CrossRefGoogle Scholar
  41. Morris, RH, Abbott, DP, Haderlie, EC 1980Intertidal Invertebrates of CaliforniaStanford University PressStanford, CaliforniaGoogle Scholar
  42. Osmanov SO (1971) Parasites of fishes of Uzbekistan. Tashkent: FAN (in Russian)Google Scholar
  43. Ozawa, T 1996A new species of Batillaria (Gastropoda: Batillariidae) from JapanVenus(Japanese Journal of Malacology)55189197Google Scholar
  44. Park, T 1948Experimental studies of interspecific competition. I. Competition between populations of flour beetles Tribolium confusum Duval and T. castaneum HerbstEcological Monographs18265307Google Scholar
  45. Price, PW, Westoby, M, Rice, B 1988Parasite-mediated competition: some predictions and testsAmerican Naturalist131544555CrossRefGoogle Scholar
  46. Ruiz, GM, Fofonoff, P, Hines, AH, Grosholz, ED 1999Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactionsLimnology and Oceanography44950972Google Scholar
  47. Rybakov, AV, Lukomskaya, OG 1988On the life cycle of Acanthoparyphium macracanthum sp.n Trematoda, Echinostomatidae.Parazitologiya22224229Google Scholar
  48. Schall, JJ 1992Parasite-mediated competition in Anolis lizardsOecologia925864CrossRefGoogle Scholar
  49. Secord, D, Kareiva, P 1996Perils and pitfalls in the host specificity paradigmBioScience46448453Google Scholar
  50. Shimura, S, Ito, J 1980Two new species of marine cercariae from the Japanese intertidal gastropod, Batillaria cumingi(Crosse)Japanese Journal of Parasitology29369375Google Scholar
  51. Shoop, WL 1988Trematode transmission patternsJournal of Parasitology744659PubMedGoogle Scholar
  52. Sousa, WP 1983Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasitesJournal of Experimental Marine Biology and Ecology73273296CrossRefGoogle Scholar
  53. Sousa, WP 1990

    Spatial scale and the processes structuring a guild of larval trematode parasites

    Esch, GWBush, AOAho, JM eds. Parasite Communities: Patterns and ProcessesChapman and HallNew York4167
    Google Scholar
  54. Torchin, ME, Lafferty, KD, Kuris, AM 2001Release from parasites as natural enemies: increased performance of a globally introduced marine crabBiological Invasions3333345CrossRefGoogle Scholar
  55. Torchin, ME, Lafferty, KD, Kuris, AM 2002Parasites and marine invasionsParasitology124137151CrossRefPubMedGoogle Scholar
  56. Torchin, ME, Lafferty, KD, Dobson, AP, McKenzie, VJ, Kuris, AM 2003Introduced species and their missing parasitesNature421628630CrossRefPubMedGoogle Scholar
  57. Whitlatch RB (1972) The ecology, life history and feeding biology of Batillaria zonalis. Masters thesis, University of the PacificGoogle Scholar
  58. Whitlatch, RB 1974Studies on the population ecology of the salt marsh gastropod Batillaria zonalisVeliger174755Google Scholar
  59. Whitlatch, RB, Obrebski, S 1980Feeding selectivity and coexistence in two deposit feeding gastropodsMarine Biology58219225CrossRefGoogle Scholar
  60. Yamaguti, S 1971Synopsis of digenetic trematodes of vertebratesKeigaku Publishing CompanyTokyo, JapanGoogle Scholar
  61. Yamaguti, S 1975A synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval formsKeigaku Publishing CompanyTokyo, JapanGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Mark E. Torchin
    • 1
  • James E. Byers
    • 1
  • Todd C. Huspeni
    • 1
  1. 1.Marine Science Institute and Department of Ecology, Evolution and Marine BiologyUniversity of CaliforniaSanta BarbaraUSA
  2. 2.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  3. 3.Department of ZoologyUniversity of New HampshireDurhamUSA

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