Skip to main content
SpringerLink
Log in

Long-term population fluctuations of the exotic New Zealand mudsnail Potamopyrgus antipodarum and its introduced aporocotylid trematode in northwestern France

  • INVASIVE SPECIES II
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Long-term studies of invasive populations are rare, which is unfortunate because important aspects of their dynamics may only be detected over long term. For instance, invasive populations can experience substantial population declines, or even crashes, sometime after their introduction and invasion. Potamopyrgus antipodarum (Caenogastropoda) is a successful invader, and is rarely parasitized in introduced areas. In France, the snail is parasitized as first intermediate host by only one trematode species (Aporocotylid sp. I), native to the snail’s home range, New Zealand. Here, we examined the dynamics of the molluscan assemblage in a French stream on a 14-year interval (2000–2004 and 2009–2013), focusing on this introduced host-parasite association. Overall, P. antipodarum was numerically dominant (90.80%) among molluscs, also including sphaeriid clams (9.12%) and pulmonate snails (0.08%). However, during the last monitoring period, we found a substantial population decline of P. antipodarum, potentially driven by environmental change, such as decreased water temperature and depth, and possibly competitive interactions with sphaeriids, which became numerically dominant (56.34%). P. antipodarum was the only mollusc found infected and only by Aporocotylid sp. I. Interestingly, despite low monthly prevalence (from 0 to 1.52%) and snail host population decline, the P. antipodarum-aporocotylid relationship appeared to be persistent over time.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alonso, A. & P. Castro-Díez, 2008. What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia 614: 107–116.

    Article  Google Scholar 

  • Alonso, A. & P. Castro-Díez, 2012. The exotic aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca): state of the art of a worldwide invasion. Aquatic Sciences 74: 375–383.

    Article  CAS  Google Scholar 

  • Bennett, D. M., T. L. Dudley, S. D. Cooper & S. S. Sweet, 2015. Ecology of the invasive New Zealand mud snail, Potamopyrgus antipodarum (Hydrobiidae), in a mediterranean-climate stream system. Hydrobiologia 746: 375–399.

    Article  CAS  Google Scholar 

  • Blanc, A. & C. Gérard, 2001. Etude préliminaire de la malacofaune de deux hydrosystèmes interconnectés dans une zone humide. International Journal of Limnology 37: 277–280.

    Article  Google Scholar 

  • Boycott, A. E., 1936. The habitats of freshwater mollusca in Britain. Journal of Animal Ecology 5: 116–186.

    Article  Google Scholar 

  • Bush, A. O., K. D. Lafferty, J. M. Lotz & A. W. Shostak, 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583.

    Article  PubMed  CAS  Google Scholar 

  • Clément, J.-C., G. Pinay & P. Marmonier, 2002. Seasonal dynamics of denitrification along toposequences in three different riparian wetlands. Journal of Environmental Quality 31: 1025–1037.

    Article  PubMed  Google Scholar 

  • Collado, G. A., 2014. Out of New Zealand: molecular identification of the highly invasive freshwater mollusk Potamopyrgus antipodarum (Gray, 1843) in South America. Zoological Studies 53: 70.

    Article  Google Scholar 

  • Cross, W. F., C. V. Baxter, K. C. Donner, E. J. Rozi-Marshall, T. A. Kennedy, R. O. Hall, H. A. Wellard Kelly & R. S. Rogers, 2011. Ecosystem ecology meets adaptive management: food web response to a controlled flood on the Colorado River, Glen Canyon. Ecological Applications 21: 2016–2033.

    Article  PubMed  Google Scholar 

  • Dahl, A. & L. B. Winter, 1993. Life-history and growth of the prosobranch snail Potamopyrgus jenkinsi in Lake Esrom, Denmark. Verhandlungen des Internationalen Verein Limnologie 25: 582–586.

    Google Scholar 

  • Dillon, R. T., 2004. The Ecology of Freshwater Molluscs. Cambridge University Press, Cambridge.

    Google Scholar 

  • Dorgelo, J., 1987. Density fluctuations in populations (1982–1986) and biological observations of Potamopyrgus jenkinsi in two trophically differing lakes. Hydrobiological Bulletin 21: 95–110.

    Article  Google Scholar 

  • Dorgelo, J., H. G. van der Geest & E. R. Hunting, 2014. Dynamics of natural populations of the detritivorous mudsnail Potamopyrgus antipodarum (Gray) (Hydrobiidae) in two interconnected Lakes differing in trophic state. SpringerPlus 3: 736.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dudgeon, D., 1983. The effects of water fluctuations on a gently shelving marginal zone of Plover Cove Reservoir, Hong Kong. Archiv für Hydrobiologie 65: 163–196.

    Google Scholar 

  • Dussart, G. B. J., 1976. The ecology of freshwater mollusks in North West England in relation to water chemistry. Journal of Molluscan Studies 42: 181–198.

    Google Scholar 

  • Dussart, G. B. J., 1977. The ecology of Potamopyrgus jenkinsi (Smith) in North West England with a note on Marstoniopsis scholtzi (Schmidt). Journal of Molluscan Studies 43: 208–216.

    Google Scholar 

  • Dussart, G. B. J., 1979. Sphaerium corneum (L.) and Pisidium spp. Pfeiffer – the ecology of freshwater bivalve molluscs in relation with water chemistry. Journal of Molluscan Studies 45: 19–34.

    Google Scholar 

  • Fenchel, T., 1975. Factors determining the distribution patterns of mud snails (Hydrobiidae). Oecologia 20: 1–17.

    Article  PubMed  Google Scholar 

  • Gaino, E., F. Scoccia, T. Lancioni & A. Ludovisi, 2008. The invader mudsnail Potamopyrgus antipodarum in the Tiiber River basin (Central Italy). Italian Journal of Zoology 75: 1–9.

    Article  Google Scholar 

  • Gangloff, M. M., 1998. The New Zealand mud snail in Western North America. Aquatic Nuisance Species Digest 2: 25–30.

    Google Scholar 

  • Gérard, C., 1997. Importance du parasitisme dans la communauté de Gastéropodes de l’étang de Combourg (Bretagne, France). Parasite 4: 49–54.

    Article  Google Scholar 

  • Gérard, C., 2001. Structure and temporal variation of trematode and gastropod communities in a freshwater ecosystem. Parasite 8: 275–287.

    Article  PubMed  Google Scholar 

  • Gérard, C. & G. B. J. Dussart, 2003. Invader and invaded – colonization by, and of, Potamopyrgus antipodarum Gray (Mollusca, Hydrobiidae). BCPC Symposium Proceedings NO. 80: Slugs & Snails: Agricultural, Veterinary & Environmental Perspectives: 281–286.

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

    Article  Google Scholar 

  • Gérard, C. & V. Poullain, 2005. Variation in the response of the invasive species Potamopyrgus antipodarum (Smith) to natural (cyanobacterial toxin) and anthropogenic (herbicide atrazine) stressors. Environmental Pollution 138: 28–33.

    Article  PubMed  CAS  Google Scholar 

  • Gérard, C., A. Blanc & K. Costil, 2003. Potamopyrgus antipodarum (Mollusca: Hydrobiidae) in continental aquatic gastropod communities: impact of salinity on trematode parasitism. Hydrobiologia 493: 167–172.

    Article  Google Scholar 

  • Gérard, C., A. Carpentier & J.-M. Paillisson, 2008. Long-term dynamics and community structure of freshwater gastropods exposed to parasitism and other environmental stressors. Freshwater Biology 53: 1–21.

    Article  Google Scholar 

  • Gérard, C., V. Poullain, E. Lance, A. Acou, L. Brient & A. Carpentier, 2009. Ecological impacts of toxic cyanobacteria on community structure and microcystin bioaccumulation of freshwater molluscs. Environmental Pollution 157: 609–617.

    Article  PubMed  CAS  Google Scholar 

  • Gérard, C., O. Miura, J. Lorda, T. H. Cribb, M. J. Nolan & R. F. Hechinger, 2017. A native-range source for a persistent trematode parasite of the exotic New Zealand mudsnail (Potamopyrgus antipodarum) in France. Hydrobiologia 785: 115–126.

    Article  CAS  Google Scholar 

  • Glöer, P. & C. Meier-Brook, 1994. Süsswassermollusken. Deutscher Jugendbund für Naturbeobachtung, Hamburg.

    Google Scholar 

  • Gray, J. E., 1843. Fauna of New Zealand: materials towards a fauna of New Zealand, Auckland Island, and Chatham Islands. In Dieffenbach, E. (ed.), Travels in New Zealand: with Contributions to the Geography, Geology, Botany, and Natural History of that Country (Volume 2). John Murray, London: 177–295.

    Google Scholar 

  • Gruau, G., A. Dia, G. Olivié-Lauquet, M. Davranche & G. Pinay, 2004. Controls on the distribution of rare earth elements in shallow groundwater. Water Research 38: 3576–3586.

    Article  PubMed  CAS  Google Scholar 

  • Hall, R. O., M. F. Dybdahl & M. C. Vanderloop, 2006. Extremely high secondary production of introduced snails in rivers. Ecological Applications 16: 1121–1131.

    Article  PubMed  Google Scholar 

  • Haynes, A. & B. Taylor, 1984. Food finding and food preference in Potamopyrgus jenkinsi. Archiv für Hydrobiologie 100: 479–491.

    Google Scholar 

  • Hechinger, R. F., 2012. Faunal survey and identification key for the trematodes (Platyhelminthes: Digenea) infecting Potamopyrgus antipodarum (Gastropoda: Hydrobiidae) as first intermediate host. Zootaxa 3418: 1–27.

    Google Scholar 

  • Holopainen, I. J. & P. M. Jónasson, 1989. Bathymetric distribution and abundance of Pisidium (Bivalvia: Sphaeriidae) in Lake Esrom, Denmark from 1954 to 1988. Oikos 55: 324–334.

    Article  Google Scholar 

  • Hoy, M., B. L. Boese, L. Taylor, D. Reusser & R. Rodriguez, 2012. Salinity adaptation of the invasive New Zealand mud snail (Potamopyrgus antipodarum) in the Columbia River estuary (Pacific Northwest, USA): physiological and molecular studies. Aquatic Ecology 46: 249–260.

    Article  CAS  Google Scholar 

  • Hughes, R. N., 1996. Evolutionary ecology of parthenogenentic strains of the prosobranch snail, Potamopyrgus antipodarum (Gray) (=P. jenkinsi (Smith)). Molluscan Reproduction in Malacological Review 6: 101–113.

    Google Scholar 

  • Jacobsen, R. & V. E. Forbes, 1997. Clonal variation in life-history traits and feeding rates in the gastropod, Potamopyrgus antipodarum: performance across a salinity gradient. Functional Ecology 11: 260–267.

    Article  Google Scholar 

  • Jurkiewicz-Karnkowska, E. & J. Zbikowski, 2004. Long-term changes and spatial variability of mollusc communities in selected habitats within the dam reservoir (Włocławek reservoir, Vistula River, Central Poland). Polish Journal of Ecology 52: 491–503.

    Google Scholar 

  • Kolar, C. S. & D. M. Lodge, 2001. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16: 199–204.

    Article  Google Scholar 

  • Kerans, B. L., M. F. Dybdahl, M. M. Gangloff & J. E. Jannot, 2005. Potamopyrgus antipodarum: distribution, density, and effects on native macroinvertebrate assemblages in the Greater Yellowstone Ecosystem. Journal of the North American Benthological Society 24: 123–138.

    Article  Google Scholar 

  • Kilgour, B. & G. Mackie, 1988. Factors affecting the distribution of sphaeriid bivalves in Britannia Bay of the Ottawa River. Nautilus 102: 73–77.

    Google Scholar 

  • Korniushin, A. V., 2007. Non-unionid freshwater bivalves (Sphaeriidae, Corbiculidae, Dreissenidae) of North American fauna. Vestnik zoologii 41: 13–22.

    Google Scholar 

  • Kubíková, L., O. Simon & K. Fricová, 2011. The occurrence of Pisidium species (Bivalvia: Sphaeriidae) in oligotrophic springs of the Blanice River catchment (Czech Republic) in relation to ecological conditions. Biologia 66: 299–307.

    Article  Google Scholar 

  • Lafferty, K. D., 1993. Effects of parasitic castration on growth, reproduction and population dynamics of the marine snail Cerithidea californica. Marine Ecology Progress Series 96: 229–237.

    Article  Google Scholar 

  • Lefebvre, S., P. Marmonier & G. Pinay, 2004. Stream regulation and nitrogen dynamics in sediment interstices: comparison of natural and straightened sectors of a third-order stream. River Research and Applications 20: 499–512.

    Article  Google Scholar 

  • Lenth, R., 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software 69: 1–33.

    Article  Google Scholar 

  • Levri, E. P., R. M. Dermott, S. J. Lunnen, A. A. Kelly & T. Ladson, 2008. The distribution of the invasive New Zealand mud snail (Potamopyrgus antipodarum) in Lake Ontario. Aquatic Ecosystem Health & Management 11: 412–421.

    Article  Google Scholar 

  • Lucas, A., 1965. Progrès récents en Europe d’une espèce envahissante : Hydrobia jenkinsi (E. A. Smith), mollusque gastéropode. PhD Thesis, University of Rennes.

  • McKenzie, V. J., W. E. Hall & R. P. Gulranick, 2013. New Zealand mud snail (Potamopyrgus antipodarum) in Boulder Creeck, Colorado: environmental factors associated with fecundity of a parthenogenic invader. Canadian Journal of Zoology 91: 30–36.

    Article  CAS  Google Scholar 

  • McMillan, N., 1990. The history of alien freshwater mollusca in North-West England. Naturalist 115: 123–132.

    Google Scholar 

  • Moffitt, C. M. & C. A. James, 2012a. Response of New Zealand mudsnails Potamopyrgus antipodarum to freezing and near-freezing fluctuating water temperatures. Freshwater Science 31: 1035–1041.

    Article  Google Scholar 

  • Moffitt, C. M. & C. A. James, 2012b. Dynamics of Potamopyrgus antipodarum infestations and seasonal water temperatures in a heavily used recreational watershed in intermountain North America. Aquatic Invasions 7: 193–202.

    Article  Google Scholar 

  • Moore, J. W., D. B. Herbst, W. N. Heady & S. M. Carlson, 2012. Stream community and ecosystem responses to the boom and bust of an invading snail. Biological Invasions 14: 2435–2446.

    Article  Google Scholar 

  • Mouthon, J. & M. Daufresne, 2008. Population dynamics and life cycle of Pisidium amnicum (Müller) (Bivalvia: Sphaeriidae) and Valvata piscinalis (Müller) (Gastropoda: Prosobranchia) in the Saône river, a nine-year study. International Journal of Limnology 44: 241–251.

    Article  Google Scholar 

  • Múrria, C., N. Bonada & N. Prat, 2008. Effects of the invasive species Potamopyrgus antipodarum (Hydrobiidae, Mollusca) on community structure in a small Mediterranean stream. Fundamental and Applied Limnology/Archiv für Hydrobiologie 171: 131–143.

    Article  CAS  Google Scholar 

  • Negovetich, N. J. & G. W. Esch, 2008. Life history cost of trematode infection in Helisoma anceps using mark-recapture in Charlie’s pond. Journal of Parasitology 94: 314–325.

    Article  PubMed  CAS  Google Scholar 

  • Neiman, M., 2006. Embryo production in a parthenogenetic snail (Potamopyrgus antipodarum) is negatively affected by the presence of other parthenogens. Invertebrate Biology 125: 45–50.

    Article  Google Scholar 

  • Neiman, M., D. Warren, B. Rasmussen & S. Zhang, 2013. Complex consequences of increased density for reproductive output in an invasive freshwater snail. Evolutionary Ecology 27: 1117–1127.

    Article  Google Scholar 

  • Newcombe, R. G., 1998. Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics in Medicine 17: 857–872.

    Article  PubMed  CAS  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Core Team, 2017. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-131.

  • R Core Team, 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Ricklefs, R. E. & G. L. Miller, 2005. Ecologie (4ème Edition). Editions De Boeck.

  • Schreiber, E. S. G., A. Glaister, G. P. Quinn & P. S. Lake, 1998. Life-history and population dynamics of the exotic snail Potamopyrgus antipodarum (Prosobranchia: Hydrobiidae) in lake Purrumbete, Victoria, Australia. Marine and Freshwater Research 49: 73–78.

    Article  Google Scholar 

  • Siegismund, H. R. & J. Hylleberg, 1987. Dispersal-mediated coexistence of mud snails (Hydrobiidae) in an estuary. Marine Biology 94: 395–402.

    Article  Google Scholar 

  • Simberloff, D. & L. Gibbons, 2004. Now you see them, now you don’t! – Population crashes of established introduced species. Biological Invasions 6: 161–172.

    Article  Google Scholar 

  • Simberloff, D., 2013. Invasive Species: What Everyone Needs to Know. Oxford University Press, Oxford.

    Google Scholar 

  • Sousa, R., M. Ilarri, A. T. Souza, C. Antunes & L. Guilhermino, 2011. Rapid decline of the greater European peaclam at the periphery of its distribution. International Journal of Limnology 47: 211–219.

    Article  Google Scholar 

  • Städler, T., M. Frye, M. Neiman & C. M. Lively, 2005. Mitochondrial haplotypes and the New Zealand origin of clonal European Potamopyrgus, an invasive aquatic snail. Molecular Ecology 14: 2465–2473.

    Article  PubMed  CAS  Google Scholar 

  • Strayer, D. L., V. T. Eviner, J. M. Jeschke & M. L. Pace, 2006. Understanding the long-term effects of species invasions. Trends in Ecology & Evolution 21: 645–651.

    Article  Google Scholar 

  • Strzelec, M. & W. Serafinski, 1996. Population ecology of Potamopyrgus antipodarum (Gray, 1843) in a recently colonized area: Upper Silesia (Southern Poland) (Gastropoda: Prosobranchia: Hydrobiidae). Malakologische Abhandlungen Staatlichen Museum für Tierkunde Dresden 18: 75–82.

    Google Scholar 

  • Tibbets, T. M., A. C. Krist, R. O. Hall Jr. & L. A. Riley, 2010. Phosphorus-mediated changes in life history traits of the invasive New Zealand mudsnail (Potamopyrgus antipodarum). Oecologia 163: 549–559.

    Article  PubMed  Google Scholar 

  • Torchin, M. E., K. D. Lafferty, A. P. Dobson, V. J. McKenzie & A. M. Kuris, 2003. Introduced species and their missing parasites. Nature 421: 628–630.

    Article  PubMed  CAS  Google Scholar 

  • Vaughn, C. C. & C. C. Hakenkamp, 2001. The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46: 1431–1446.

    Article  Google Scholar 

  • Wallace, C., 1978. Notes on the distribution of sex and shell characters in some australian populations of Potamopyrgus (Gastropoda : Hydrobiidae). Journal of the Malacological Society of Australia 4: 71–76.

    Article  Google Scholar 

  • Wallace, C., 1985. On the distribution of the sexes of Potamopyrgus jenkinsi (Smith). Journal of Molluscan Studies 51: 290–296.

    Google Scholar 

  • Wilke, T., M. Haase, R. Hershler, H. P. Liu, B. Misof & W. Ponder, 2013. Pushing short DNA fragments to the limit: phylogenetic relationships of ‘hydrobioid’ gastropods (Caenogastropoda: Rissooidea). Molecular Phylogenetics and Evolution 66: 715–736.

    Article  PubMed  Google Scholar 

  • Winterbourn, M. J., 1970. Population studies on the New Zealand freshwater gastropod, Potamopyrgus antipodarum (Gray). Proceedings of the Malacological Society of London 39: 139–149.

    Google Scholar 

  • Zbikowski, J. & E. Zbikowska, 2009. Invaders of an invader – Trematodes in Potamopyrgus antipodarum in Poland. Journal of Invertebrate Pathology 101: 67–70.

    Article  PubMed  Google Scholar 

  • Zielske, S., M. Glaubrecht & M. Haase, 2011. Origin and radiation of rissooidean gastropods (Caenogastropoda) in ancient lakes of Sulawesi. Zoologica Scripta 40: 221–237.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Valérie Briand for bibliographical assistance.

Author information

Authors and Affiliations

  1. Ecosystèmes, Biodiversité, Evolution (UMR ECOBIO 6553), Université de Rennes, 35042, Rennes, France

    Claudia Gérard

  2. IGEPP, Université de Rennes 1, Avenue du Général Leclerc, 35042, Rennes, France

    Maxime Hervé

  3. Scripps Institution of Oceanography-Marine Biology Research Division, University of California, San Diego, La Jolla, CA, 92093, USA

    Ryan F. Hechinger

Authors
  1. Claudia Gérard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maxime Hervé
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryan F. Hechinger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudia Gérard.

Ethics declarations

Conflict of interest

All of the authors read and approved the paper that has not been published previously nor is it being considered by any other peer-reviewed journal. The authors declare that there are no conflicts of interest.

Additional information

Guest editors: John E. Havel, Sidinei M. Thomaz, Lee B. Kats, Katya E. Kovalenko & Luciano N. Santos / Aquatic Invasive Species II

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Table

Physicochemical characteristics of the French stream “Le Petit Hermitage” measured in May 2003 (DOCX 17 kb)

Supplementary Fig.

Relative size-frequency distributions of P. antipodarum in different months from June 2000 to September 2004 (a) and from April 2009 to May 2013 (b) in the French stream “Le Petit Hermitage” (size classes in mm, relative abundance from 0 to 100% with 10%-step graduation). Sample size is indicated for each month (PDF 110 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gérard, C., Hervé, M. & Hechinger, R.F. Long-term population fluctuations of the exotic New Zealand mudsnail Potamopyrgus antipodarum and its introduced aporocotylid trematode in northwestern France. Hydrobiologia 817, 253–266 (2018). https://doi.org/10.1007/s10750-017-3406-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-017-3406-x

Keywords

Search

Navigation