Skip to main content
Log in

The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe

Biological Invasions Aims and scope Submit manuscript

Cite this article

Abstract

Several freshwater mussel species represent some of the most problematic invasive species and have considerably altered ecosystems worldwide. Their invasion potential has been partially attributed to their free-living larvae, which have a high dispersal capability. We investigated the invasion potential of Anodonta (Sinanodonta) woodiana, a species of East Asian unionid mussel established worldwide despite having an obligatory parasitic stage (glochidium), which must encyst on host fish. The invasion success of A. woodiana has been attributed to the success of worldwide introductions of its sympatric fish hosts. We experimentally found, however, that A. woodiana is a broad host generalist, which can complete its development on all eight fish species tested, both coinvasive and native. Subsequently, we used a data on the occurrence and relative abundance of potential hosts in river habitats in the Czech Republic to project scenarios of the effect of host availability on A. woodiana invasion. We found that host availability does not constitute a major limit for A. woodiana to colonise most aquatic habitats in Central Europe. In addition, we investigated seasonal dynamics of A. woodiana reproduction and did not detect any limitations of its reproduction by ambient water temperatures typical of a Central European lowland river. Consequently, we predict that A. woodiana may further increase the speed and range of its invasion and we discuss possible consequences to native habitats and communities, especially to the endangered species of unionid mussels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Bakke TA, Harris PD, Cable J (2002) Host specificity dynamics: observations on gyrodactylid monogeneans. Int J Parasitol 32:281–308

    Article  PubMed  Google Scholar 

  • Barnhart MC, Haag WR, Roston WN (2008) Adaptations to host infection and larval parasitism in Unionoida. J N Am Benthol Soc 27:370–394

    Article  Google Scholar 

  • Bauer G (2001) Framework and driving forces for the evolution of naiad life histories. In: Bauer G, Wachtler K (eds) Ecology and evolution of the freshwater mussels Unionoida. Springer, Berlin, pp 233–255

    Chapter  Google Scholar 

  • Bauer G, Hochwald S, Silkenat W (1991) Spatial distribution of freshwater mussels: the role of host fish and metabolic rate. Freshw Biol 26:377–386

    Article  Google Scholar 

  • Bean MG, Bonner TH (2010) Spatial and temporal distribution of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in the Rio Grande (Rio Bravo del Norte). J Aquat Anim Health 22:182–189

    Article  PubMed  Google Scholar 

  • Benson AJ (2011) Sinanodonta woodiana. USGS nonindigenous aquatic species database. http://nas.er.usgs.gov/queries/FactSheetaspx?speciesID=2824. Accessed 18 Jan 2011

  • Beran L (1997) First record of Sinanodonta woodiana (Mollusca: Bivalvia) in the Czech Republic. Acta Soc Zool Bohem 61:1–2

    Google Scholar 

  • Beran L (2008) Expansion of Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae) in the Czech Republic. Aquat Invasions 3:91–94

    Article  Google Scholar 

  • Blazek R, Gelnar M (2006) Temporal and spatial distribution of glochidial larval stages of European unionid mussels (Mollusca: Unionidae) on host fishes. Folia Parasit 53:98–106

    Google Scholar 

  • Bogan AE (1993) Freshwater bivalve extinctions (Mollusca: Unionoida): a search for causes. Am Zool 33:599–609

    Google Scholar 

  • Brouder MJ, Hoffnagle TL (1997) Distribution and prevalence of the Asian fish tapeworm, Bothriocephalus acheilognathi, in the Colorado River and tributaries, Grand Canyon, Arizona, including two new host records. J Helminth Soc Wash 64:219–226

    Google Scholar 

  • Cappelletti C, Cianfanelli S, Beltrami ME, Ciutti F (2009) Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae): a new non-indigenous species in Lake Garda (Italy). Aquat Invasions 4:685–688

    Article  Google Scholar 

  • Cianfanelli S, Lori E, Bodon M (2007) Non-indigenous freshwater molluscs and their distribution in Italy. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution and threats. Springer, Dordrecht, pp 103–121

    Chapter  Google Scholar 

  • Corsi I, Pastore AM, Lodde A, Palmerini E, Castagnolo L, Focardi S (2007) Potential role of cholinesterases in the invasive capacity of the freshwater bivalve, Anodonta woodiana (Bivalvia: Unionacea): a comparative study with the indigenous species of the genus, Anodonta sp. Comp Biochem Phys C 145:413–419

    Google Scholar 

  • Darrigran G (2002) Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biol Invasions 4:145–156

    Article  Google Scholar 

  • Djajasasmita M (1982) The occurrence of Anodonta woodiana Lea, 1837 in Indonesia (Pelecypoda, Unionidae). Veliger 25:175

    Google Scholar 

  • Douda K (2010) Effects of nitrate nitrogen pollution on Central European unionid bivalves revealed by distributional data and acute toxicity testing. Aquat Conserv 20:189–197

    Article  Google Scholar 

  • Dudgeon D, Morton B (1983) The population dynamics and sexual strategy of Anodonta woodiana (Bivalvia, Unionacea) in Plover Cove Reservoir, Hong-Kong. J Zool 201:161–183

    Article  Google Scholar 

  • Dudgeon D, Morton B (1984) Site selection and attachment duration of Anodonta woodiana (Bivalvia, Unionacea) glochidia on fish hosts. J Zool 204:355–362

    Article  Google Scholar 

  • Froufe E, Magyary I, Lehoczky I, Weiss S (2002) mtDNA sequence data supports an Asian ancestry and single introduction of the common carp into the Danube Basin. J Fish Biol 61:301–304

    Article  CAS  Google Scholar 

  • Fukuhara S, Nagata Y, Yamada T (1986) Glochidium parasitic period, host-fish and parasitic site of Anodonta woodiana in small pond. Venus 45:43–52

    Google Scholar 

  • Galbraith HS, Vaughn CC (2009) Temperature and food interact to influence gamete development in freshwater mussels. Hydrobiologia 636:35–47

    Article  CAS  Google Scholar 

  • Graf DL (2007) Palearctic freshwater mussel (Mollusca: Bivalvia: Unionoida) diversity and the comparatory method as a species concept. P Acad Nat Sci Phila 156:71–88

    Article  Google Scholar 

  • Haag WR, Berg DJ, Garton DW, Farris JL (1993) Reduced survival and fitness in native bivalves in response to fouling by the introduced zebra mussel (Dreissena polymorpha) in western Lake Erie. Can J Fish Aquat Sci 50:13–19

    Article  Google Scholar 

  • Higgins SN, Vander Zanden MJ (2010) What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecol Monogr 80:179–196

    Article  Google Scholar 

  • Holt RD, Dobson AP, Begon M, Bowers RG, Schauber EM (2003) Parasite establishment in host communities. Ecol Lett 6:837–842

    Article  Google Scholar 

  • Hruška J (1992) The freshwater pearl mussel in south Bohemia: evaluation of the effect of temperature on reproduction, growth and age structure of the population. Arch Hydrobiol 126:181–197

    Google Scholar 

  • Jansen W, Bauer G, Zahner-Meike E (2001) Glochidial mortality in freshwater mussels. In: Bauer G, Wachtler K (eds) Ecology and evolution of the freshwater mussels Unionoida. Springer, Berlin, pp 185–211

    Chapter  Google Scholar 

  • Johnson LE, Padilla DK (2010) Geographic spread of exotic species: ecological lessons and opportunities from the invasion of the zebra mussel Dreissena polymorpha. Biol Conserv 78:23–33

    Article  Google Scholar 

  • Jurajda P, Slavik O, White S, Adamek Z (2010) Young-of-the-year fish assemblages as an alternative to adult fish monitoring for ecological quality evaluation of running waters. Hydrobiologia 644:89–101

    Article  Google Scholar 

  • Karatayev AY, Burlakova LE, Padilla DK (1997) The effects of Dreissena polymorpha (Pallas) invasion on aquatic communities in eastern Europe. J Shellfish Res 16:187–203

    Google Scholar 

  • Karatayev AY, Boltovskoy D, Padilla DK, Burlakova LE (2007a) The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: parallels, contrasts, potential spread and invasion impacts. J Shellfish Res 26:205–213

    Article  Google Scholar 

  • Karatayev AY, Padilla DK, Minchin D, Boltovskoy D, Burlakova LE (2007b) Changes in global economies and trade: the potential spread of exotic freshwater bivalves. Biol Invasions 9:161–180

    Article  Google Scholar 

  • Keller RP, Drake JM, Lodge DM (2007) Fecundity as a basis for risk assessment of nonindigenous freshwater Molluscs. Conserv Biol 21:191–200

    Article  PubMed  Google Scholar 

  • Kiss A (1995) The propagation, growth and biomass of the Chinese huge mussel (Anodonta woodiana woodiana Lea, 1834) in Hungary. Dissertation, University of Agricultural Sciences of Gödöllo

  • Kohlmann K, Gross R, Murakaeva A, Kersten P (2003) Genetic variability and structure of common carp (Cyprinus carpio) populations throughout the distribution range inferred from allozyme, microsatellite and mitochondrial DNA markers. Aquat Living Resour 16:421–431

    Article  Google Scholar 

  • Konečná M, Reichard M (2011) Seasonal dynamics in population characteristics of European bitterling Rhodeus amarus in a small lowland river. J Fish Biol 78:227–239

    Article  PubMed  Google Scholar 

  • Kraszewski A (2007) The continuing expansion of Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae) in Poland and Europe. Folia Malac 15:65–69

    Google Scholar 

  • Kraszewski A, Zdanowski B (2007) Sinanodonta woodiana (Lea, 1834) (Mollusca)—a new mussel species in Poland: occurrence and habitat preferences in a heated lake system. Pol J Ecol 55:337–356

    Google Scholar 

  • Lee KA, Klasing KC (2004) A role for immunology in invasion biology. Trends Ecol Evol 19:523–529

    Article  PubMed  Google Scholar 

  • Leung B, Drake JM, Lodge DM (2004) Predicting invasions: propagule pressure and the gravity of Allee effects. Ecology 85:1651–1660

    Article  Google Scholar 

  • Lucas MC, Baras E (2001) Migration of freshwater fishes. Blackwell Science, Malden

    Book  Google Scholar 

  • Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clark SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mollusks. Bioscience 54:321–330

    Article  Google Scholar 

  • Mackie GL (1984) Bivalves. In: Tompa AS, Verdonk NH, van den Biggelaar JAM (eds) The Mollusca vol. 7: reproduction. Academic Press, London, pp 351–418

    Google Scholar 

  • McNichols KA, Mackie GL, Ackerman JD (2011) Host fish quality may explain the status of endangered Epioblasma torulosa rangiana and Lampsilis fasciola (Bivalvia: Unionidae) in Canada. J N Am Benthol Soc 30:60–70

    Article  Google Scholar 

  • Paunovic M, Csányi B, Simic V, Stojanovic BCP (2006) Distribution of Anodonta (Sinanodonta) woodiana (Rea, 1834) in inland waters of Serbia. Aquat Invasions 1:154–160

    Article  Google Scholar 

  • Popa OP, Kelemen BS, Murariu D, Popa LO (2007) New records of Sinanodonta woodiana (Lea, 1834) (Mollusca: Bivalvia: Unionidae) from Eastern Romania. Aquat Invasions 2:265–267

    Article  Google Scholar 

  • Poulin R (1992) Determinants of host-specificity in parasites of freshwater fishes. Int J Parasitol 22:753–758

    Article  PubMed  CAS  Google Scholar 

  • Pou-Rovira Q, Araujo R, Boix D, Clavero M, Feo C, Ordeix M, Zamora L (2009) Presence of the alien chinese pond mussel Anodonta woodiana (Lea, 1834) (Bivalvia, Unionidae) in the Iberian Peninsula. Graellsia 65:67–70

    Article  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 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reichard M, Ondrackova M, Przybylski M, Liu H, Smith C (2006) The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evol Biol 19:788–796

    Article  PubMed  CAS  Google Scholar 

  • Reichard M, Przybylski M, Kaniewska P, Liu H, Smith C (2007) A possible evolutionary lag in the relationship between freshwater mussels and European bitterling. J Fish Biol 70:709–725

    Article  Google Scholar 

  • Reichard M, Polacik M, Tarkan AS, Spence R, Gaygusuz O, Ercan E, Ondrackova M, Smith C (2010) The bitterling-mussel coevolutionary relationship in areas of recent and ancient sympatry. Evolution 64:3047–3056

    PubMed  Google Scholar 

  • Rogers CL, Dimock RV (2003) Acquired resistance of bluegill sunfish Lepomis macrochirus to glochidia larvae of the freshwater mussel Utterbackia imbecillis (Bivalvia: Unionidae) after multiple infections. J Parasitol 89:51–56

    Article  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sárkány-Kiss A, Sirbu I, Hulea O (2000) Expansion of the adventive species Anodonta woodiana (Lea, 1834) (Mollusca, Bivalvia, Unionoidea) in central and eastern Europe. Acta Oecol Univ Sibiu 7:49–57

    Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176

    Article  Google Scholar 

  • Sousa R, Antunes C, Guilhermino L (2008a) Ecology of the invasive Asian clam Corbicula fluminea (Muller, 1774) in aquatic ecosystems: an overview. Ann Limnol-Int J Lim 44:85–94

    Article  Google Scholar 

  • Sousa R, Nogueira AJA, Gaspar M, Antunes C, Guilhermino L (2008b) Growth and extremely high production of the non-indigenous invasive species Corbicula fluminea (Müller, 1774): possible implications for ecosystem functioning. Estuar Coast Shelf S 80:289–295

    Article  Google Scholar 

  • Sousa R, Gutierrez JL, Aldridge DC (2009) Non-indigenous invasive bivalves as ecosystem engineers. Biol Invasions 11:2367–2385

    Article  Google Scholar 

  • Stoeckel JA, Schneider DW, Soeken LA, Blodgett KD, Sparks RE (1997) Larval dynamics of a riverine metapopulation: implications for zebra mussel recruitment, dispersal, and control in a large-river system. J N Am Benthol Soc 16:586–601

    Article  Google Scholar 

  • Strayer DL (1999) Effects of alien species on freshwater mollusks in North America. J N Am Benthol Soc 18:74–98

    Article  Google Scholar 

  • Strayer DL (2008) Freshwater mussel ecology: a multifactor approach to distribution and abundance. University of California Press, Berkley

    Google Scholar 

  • Strayer DL (2009) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Front Ecol Environ 7:135–141

    Article  Google Scholar 

  • Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128

    Article  PubMed  CAS  Google Scholar 

  • Trdan RJ, Hoeh WR (1982) Eurytopic host use by two congeneric species of freshwater mussel (Pelecypoda, Unionidae, Anodonta). Am Midl Nat 108:381–388

    Article  Google Scholar 

  • Treasurer JW, Hastie LC, Hunter D, Duncan F, Treasurer CM (2006) Effects of (Margaritifera margaritifera) glochidial infection on performance of tank-reared Atlantic salmon (Salmo salar). Aquaculture 256:74–79

    Article  Google Scholar 

  • Vaughn CC, Hakenkamp CC (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol 46:1431–1446

    Article  Google Scholar 

  • Vaughn CC, Taylor CM (1999) Impoundments and the decline of freshwater mussels: a case study of an extinction gradient. Conserv Biol 13:912–920

    Article  Google Scholar 

  • Vaughn CC, Taylor CM (2000) Macroecology of a host-parasite relationship. Ecography 23:11–20

    Article  Google Scholar 

  • von Proschwitz T (2008) The Chinese giant mussel Sinanodonta woodiana (Lea, 1834) (Bivalvia, Unionidae): an unwelcome addition to the Swedish fauna. Basteria 72:307–311

    Google Scholar 

  • Wachtler K, Dreher-Mansur MC, Richter T (2001) Larval types and early postlarval biology in naiads (Unionoida). In: Bauer G, Wachtler K (eds) Ecology and evolution of the freshwater mussels Unionoida. Springer, Berlin, pp 93–125

    Chapter  Google Scholar 

  • Wang N, Augspurger T, Barnhart MC, Bidwell JR, Cope WG, Dwyer FJ, Geis S, Greer IE, Ingersoll CG, Kane CM, May TW, Neves RJ, Newton TJ, Roberts AD, Whites DW (2007) Intra- and interlaboratory variability in acute toxicity tests with glochidia and juveniles of freshwater mussels (Unionidae). Environ Toxicol Chem 26:2029–2035

    Article  PubMed  CAS  Google Scholar 

  • Ward JM, Ricciardi A (2007) Impacts of Dreissena invasions on benthic macroinvertebrate communities: a meta-analysis. Divers Distrib 13:155–165

    Article  Google Scholar 

  • Watters GT (1992) Unionids, fishes, and the species-area curve. J Biogeogr 19:481–490

    Article  Google Scholar 

  • Watters GT (1997) A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Lea, 1834) (Bivalvia:Unionidae). Veliger 40:152–156

    Google Scholar 

  • Watters GT, O’Dee SH (2000) Glochidial release as a function of water temperature: beyond bradyticty and tachyticty. Proceedings of the conservation, captive care, and propagation of freshwater mussels symposium. Ohio Biological Survey, Ohio, pp 135–140

Download references

Acknowledgments

The authors thank to Matej Polačik, David Strayer and an anonymous reviewer for their helpful comments on the manuscript. The research was funded by grants awarded by the Ministry of Environment of the Czech Republic (MZP 0002071101), Czech University of Life Sciences Prague (CIGA 42110/1313/3104), and the Grant Agency of the Czech Academy of Sciences (KJB600930802). KD and MR conceived the study, analysed the data and drafted the manuscript; KD designed and performed the experimental work; OS analyzed host availability and MV analysed histological data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. Douda.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Douda, K., Vrtílek, M., Slavík, O. et al. The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe. Biol Invasions 14, 127–137 (2012). https://doi.org/10.1007/s10530-011-9989-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-011-9989-7

Keywords

Navigation