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Resistance of an invasive gastropod to an indigenous trematode parasite in Lake Malawi

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Abstract

Successful establishment and spread of biological invaders may be promoted by the absence of population-regulating enemies such as pathogens, parasites or predators. This may come about when introduced taxa are missing enemies from their native habitats, or through immunity to enemies within invaded habitats. Here we provide field evidence that trematode parasites are absent in a highly invasive morph of the gastropod Melanoides tuberculata in Lake Malawi, and that the invasive morph is resistant to indigenous trematodes that castrate and induce gigantism in native M. tuberculata. Since helminth infections can strongly influence host population abundances in other host-parasite systems, this enemy release may have provided an advantage to the invasive morph in terms of reproductive capacity and survivorship.

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References

  • Abd el-Kader Saad AI, Abed GH (1995) Studies on the life cycle of Haplorchis pumilio (Looss, 1896) with morphological redescription of larval and adult stages. J Egypt Soc Parasitol 25:795–806

    CAS  Google Scholar 

  • Albon SD, Stien A, Irvine RJ, Langvatn R, Ropstad E, Halvorsen O (2002) The role of parasites in the dynamics of a reindeer population. Proc R Soc B 269:1625–1632

    Google Scholar 

  • Ballabeni P (1995) Parasite-induced gigantism in a snail: A host adaptation? Funct Ecol 9:887–893

    Article  Google Scholar 

  • Ben-Ami F, Heller J (2005) Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail. Melanoides tuberculata. J Evol Biol 18:138–46

    Article  PubMed  CAS  Google Scholar 

  • Byers JE, Goldwasser L (2001) Exposing the mechanism and timing of impact of nonindigenous species on native species. Ecology 82:1330–1343

    Article  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Dillon RT (2000) The ecology of freshwater molluscs. Cambridge University Press, Cambridge, United Kingdom

    Google Scholar 

  • Dzikowski R, Levy MG, Poore MF, Flowers JR, Paperna I (2004) Use of rDNA polymorphism for identification of heterophyidae infecting freshwater fishes. Dis Aquat Org 59:35–41

    Article  PubMed  CAS  Google Scholar 

  • Ebert D (1994) Virulence and local adaptations of a horizontally transmitted parasite. Science 265:1084–1086

    Article  PubMed  Google Scholar 

  • Ebert D (1998) Experimental evolution of parasites. Science 282:1432–1435

    Article  PubMed  CAS  Google Scholar 

  • Ebert D, Carius HJ, Little T, Decaestecker E (2004) The evolution of virulence: When parasites cause host castration and gigantism. Am Nat 164(Supp 5):S19–S32

    Article  PubMed  Google Scholar 

  • Erpenbeck D, Breeuwer JAJ, van der Velde HC, van Soest RWM (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol 141:377–386

    Article  Google Scholar 

  • Evers BN, Madsen H, McKaye KM, Stauffer JR (2006) The schistosome intermediate host, Bulinus nyassanus, is a ‘preferred’ food for the cichlid fish, Trematocranus placodon, at Cape Maclear, Lake Malawi. Ann Trop Med Parasitol 100:75–85

    Article  PubMed  CAS  Google Scholar 

  • Fredensborg BL, Mouritsen KN and Poulin R (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Mar Ecol Prog Ser 290:109–117

    Article  Google Scholar 

  • Fromme AE, Dybdahl MF (2006) Resistance in introduced populations of a freshwater snail to native range parasites. J Evol Biol 19:1948–1955

    Article  Google Scholar 

  • Genner MJ, Michel E (2003) Fine-scale habitat associations of soft-sediment gastropods at Cape Maclear, Lake Malawi. J Molluscan Stud 69:325–328

    Article  Google Scholar 

  • Genner MJ, Michel E, Erpenbeck D, de Voogd N, Witte F, Pointier J-P (2004) Camouflaged invasion of Lake Malawi by an oriental gastropod. Mol Ecol 13:2135–2141

    Article  PubMed  CAS  Google Scholar 

  • Genner MJ, Todd JA, Michel E, Erpenbeck D, Joyce DA, Jimoh A, Piechocki A, Pointier J-P (2007) Amassing diversity in an ancient lake: Evolution of a morphologically diverse parthenogenetic gastropod assemblage in Lake Malawi. Mol Ecol 16:517–530

    Article  PubMed  Google Scholar 

  • Gérard C, Le Lannic J (2003) Establishment of a new host-parasite association between the introduced invasive species Potamopyrgus antipodarum (Smith) (Gastropoda, Prosobranchia, Hydrobiidae) and Sanguinicola sp. Plehn (Trematoda, Sanguinicolidae) in Europe. J Zool 261:213–216

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Heller J, Farstay V (1990) Sexual and parthenogenetic populations of the freshwater snail Melanoides tuberculata in Israel. Isr J Zool 37:75–87

    Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Krakau M, Thieltges DW, Reise K (2006) Native parasites adopt introduced bivalves of the North Sea. Biol Invasions 8:919–926

    Article  Google Scholar 

  • Lively CM, Dybdahl MF (2000) Parasite adaptation to locally common host genotypes. Nature 405:679–681

    Article  PubMed  CAS  Google Scholar 

  • Lively CM, Dybdahl MF, Jokela J, Osnas E, Delph LF (2004) Host sex and local adaptation by parasites in a snail-trematode interaction. Am Nat 164:S6–S18

    Article  PubMed  Google Scholar 

  • Lo CT, Lee KM (1996) Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). J Parasitol 82:347–350

    Article  PubMed  CAS  Google Scholar 

  • MacNeil C, Dick JTA, Hatcher MJ, Terry RS, Smith JE, Dunn AM (2003) Parasite-mediated predation between native and invasive amphipods. Proc R Soc London B 270:1309–1314

    Article  Google Scholar 

  • Mahdy OA, Shaheed IB (2001) Studies on metacercarial infection among Tilapia species in Egypt. Helminthologia 38:35–42

    Google Scholar 

  • Minchella DJ (1985) Host life history variation in response to parasitism. Parasitology 90:205–216

    Article  Google Scholar 

  • Mouritsen KN, Jensen KT (1994) The enigma of gigantism: Effect of larval trematodes on growth, fecundity, egestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). J Exp Mar Biol Ecol 181:53–66

    Article  Google Scholar 

  • Navajas M, Cotton D, Kreiter S, Gutierrez J (1992) Molecular approach in spider mites (Acari: Tetranychidae): preliminary data on ribosomal DNA sequences. Exp Appl Acarol 15:211–218

    Article  PubMed  CAS  Google Scholar 

  • Newey S, Thirgood S (2004) Parasite-mediated reduction in fecundity of mountain hares. Proc R Soc London B 271:S413–S415

    Google Scholar 

  • Prenter J, MacNeil C., Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Samadi S, Balzan C, Delay B, Pointier J-P (1997) Local distribution and abundance of thiarid snails in recently colonized rivers from the Caribbean area. Malacol Rev 30:45–52

    Google Scholar 

  • Scholz T, Aguirre-Macedo ML, Salgado-Maldonado G (2001) Trematodes of the family Heterophyidae (Digenea) in Mexico: a review of species and new host and geographical records. J Nat Hist 35:1733–1772

    Article  Google Scholar 

  • Seeley RH (1986) Intense natural selection caused a rapid morphological transition in a living marine snail. Proc Nat Acad Sci USA 83:6897–6901

    Google Scholar 

  • Sorensen RE, Minchella DJ (2001) Snail-trematode life history interactions: past trends and future directions. Parasitology 123:S3–S18

    Article  PubMed  Google Scholar 

  • Sommerville C (1982) The life history of Haplorchis pumilio (Looss, 1896) from cultured tilapias. J Fish Dis 5:233–241

    Article  Google Scholar 

  • Strauss SY, Webb CO, Saamin N (2006) Exotic taxa less related to native species are more invasive. Proc Nat Acad Sci USA 103:5841–5845

    Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  PubMed  CAS  Google Scholar 

  • Torchin ME, Byers JE, Todd C (2005) Differential parasitism of native and introduced snails: replacement of a parasite fauna. Biol Invasions 7:885–894

    Article  Google Scholar 

  • Umadevi K, Madhavi R (1997) Effects of light and temperature on the emergence of Haplorchis pumilio cercariae from the snail host, Thiara tuberculata. Acta Parasitol 42:12–17

    Google Scholar 

  • Wang JJ, Chung LY, Lee JD, Chang EE, Chen ER, Chao D, Yen CM (2002) Haplorchis infections in intermediate hosts from a clonorchiasis endemic area in Meinung, Taiwan, Republic of China. J Helminthol 76:185–188

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Department of Fisheries for support during our research programme. We also thank Alan Smith, Paul Nichols, Kate Jones and Tom Woolford for assistance surveying molluscs, Jan van Arkel for photography, and C. van Oosterhout and one anonymous reviewer for helpful comments. This work was primarily funded by European Commission Marie Curie Fellowship HPMF-CT-2000–79.

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Correspondence to Martin J. Genner.

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Genner, M.J., Michel, E. & Todd, J.A. Resistance of an invasive gastropod to an indigenous trematode parasite in Lake Malawi. Biol Invasions 10, 41–49 (2008). https://doi.org/10.1007/s10530-007-9105-1

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  • DOI: https://doi.org/10.1007/s10530-007-9105-1

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