, Volume 817, Issue 1, pp 253–266 | Cite as

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

  • Claudia Gérard
  • Maxime Hervé
  • Ryan F. Hechinger


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.


Invasive Potamopyrgus antipodarum Introduced aporocotylid Long-term population dynamics Decline Abiotic parameters Sphaeriids 



We thank Valérie Briand for bibliographical assistance.

Compliance with ethical standards

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.

Supplementary material

10750_2017_3406_MOESM1_ESM.docx (17 kb)
Supplemental Table Physicochemical characteristics of the French stream “Le Petit Hermitage” measured in May 2003 (DOCX 17 kb)
10750_2017_3406_MOESM2_ESM.pdf (110 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)


  1. Alonso, A. & P. Castro-Díez, 2008. What explains the invading success of the aquatic mud snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca)? Hydrobiologia 614: 107–116.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. Boycott, A. E., 1936. The habitats of freshwater mollusca in Britain. Journal of Animal Ecology 5: 116–186.CrossRefGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 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.CrossRefPubMedGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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
  11. Dillon, R. T., 2004. The Ecology of Freshwater Molluscs. Cambridge University Press, Cambridge.Google Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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
  15. 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
  16. 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
  17. 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
  18. Fenchel, T., 1975. Factors determining the distribution patterns of mud snails (Hydrobiidae). Oecologia 20: 1–17.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Gangloff, M. M., 1998. The New Zealand mud snail in Western North America. Aquatic Nuisance Species Digest 2: 25–30.Google Scholar
  21. Gérard, C., 1997. Importance du parasitisme dans la communauté de Gastéropodes de l’étang de Combourg (Bretagne, France). Parasite 4: 49–54.CrossRefGoogle Scholar
  22. Gérard, C., 2001. Structure and temporal variation of trematode and gastropod communities in a freshwater ecosystem. Parasite 8: 275–287.CrossRefPubMedGoogle Scholar
  23. 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.Google Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefPubMedGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. Glöer, P. & C. Meier-Brook, 1994. Süsswassermollusken. Deutscher Jugendbund für Naturbeobachtung, Hamburg.Google Scholar
  31. 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
  32. 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.CrossRefPubMedGoogle Scholar
  33. Hall, R. O., M. F. Dybdahl & M. C. Vanderloop, 2006. Extremely high secondary production of introduced snails in rivers. Ecological Applications 16: 1121–1131.CrossRefPubMedGoogle Scholar
  34. Haynes, A. & B. Taylor, 1984. Food finding and food preference in Potamopyrgus jenkinsi. Archiv für Hydrobiologie 100: 479–491.Google Scholar
  35. 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
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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
  39. 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.CrossRefGoogle Scholar
  40. 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
  41. Kolar, C. S. & D. M. Lodge, 2001. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16: 199–204.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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
  44. Korniushin, A. V., 2007. Non-unionid freshwater bivalves (Sphaeriidae, Corbiculidae, Dreissenidae) of North American fauna. Vestnik zoologii 41: 13–22.Google Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. Lenth, R., 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software 69: 1–33.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. Lucas, A., 1965. Progrès récents en Europe d’une espèce envahissante : Hydrobia jenkinsi (E. A. Smith), mollusque gastéropode. PhD Thesis, University of Rennes.Google Scholar
  51. 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.CrossRefGoogle Scholar
  52. McMillan, N., 1990. The history of alien freshwater mollusca in North-West England. Naturalist 115: 123–132.Google Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. 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.CrossRefGoogle Scholar
  61. Newcombe, R. G., 1998. Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics in Medicine 17: 857–872.CrossRefPubMedGoogle Scholar
  62. 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.Google Scholar
  63. R Core Team, 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
  64. Ricklefs, R. E. & G. L. Miller, 2005. Ecologie (4ème Edition). Editions De Boeck.Google Scholar
  65. 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.CrossRefGoogle Scholar
  66. Siegismund, H. R. & J. Hylleberg, 1987. Dispersal-mediated coexistence of mud snails (Hydrobiidae) in an estuary. Marine Biology 94: 395–402.CrossRefGoogle Scholar
  67. Simberloff, D. & L. Gibbons, 2004. Now you see them, now you don’t! – Population crashes of established introduced species. Biological Invasions 6: 161–172.CrossRefGoogle Scholar
  68. Simberloff, D., 2013. Invasive Species: What Everyone Needs to Know. Oxford University Press, Oxford.Google Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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
  73. 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.CrossRefPubMedGoogle Scholar
  74. 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.CrossRefPubMedGoogle Scholar
  75. Vaughn, C. C. & C. C. Hakenkamp, 2001. The functional role of burrowing bivalves in freshwater ecosystems. Freshwater Biology 46: 1431–1446.CrossRefGoogle Scholar
  76. 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.Google Scholar
  77. Wallace, C., 1985. On the distribution of the sexes of Potamopyrgus jenkinsi (Smith). Journal of Molluscan Studies 51: 290–296.Google Scholar
  78. 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.CrossRefPubMedGoogle Scholar
  79. 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
  80. Zbikowski, J. & E. Zbikowska, 2009. Invaders of an invader – Trematodes in Potamopyrgus antipodarum in Poland. Journal of Invertebrate Pathology 101: 67–70.CrossRefPubMedGoogle Scholar
  81. Zielske, S., M. Glaubrecht & M. Haase, 2011. Origin and radiation of rissooidean gastropods (Caenogastropoda) in ancient lakes of Sulawesi. Zoologica Scripta 40: 221–237.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Claudia Gérard
    • 1
  • Maxime Hervé
    • 2
  • Ryan F. Hechinger
    • 3
  1. 1.Ecosystèmes, Biodiversité, Evolution (UMR ECOBIO 6553)Université de RennesRennesFrance
  2. 2.IGEPP, Université de Rennes 1RennesFrance
  3. 3.Scripps Institution of Oceanography-Marine Biology Research DivisionUniversity of California, San DiegoLa JollaUSA

Personalised recommendations