, Volume 829, Issue 1, pp 189–204 | Cite as

No evidence for a genetic impoverishment of the indigenous amphipod Gammarus roeselii (Gervais, 1835) due to the invasion of Dikerogammarus villosus (Sowinsky, 1894) in Lake Constance

  • René GergsEmail author
  • Isabelle Gemmer
  • Meike Koester
  • Karl-Otto Rothhaupt
  • Jasminca Behrmann-Godel
Primary Research Paper


The replacement of native species by invasive species is one of the most critical threats to the biodiversity of aquatic systems today. However, little is known about potential effects of species invasions on the genetic diversity of indigenous species in cases where the latter coexist with the invader. Here we present an example of the indigenous amphipod Gammarus roeselii, which has been partly replaced by the invasive Dikerogammarus villosus in Lake Constance (C-Europe) and now mostly exists in small, isolated populations. We compared the genetic diversity, population structure, indicators for bottlenecks and migrations rates of G. roeselii before and after the invasion event from samples collected between 1999 and 2013. We expected a genetic impoverishment in the reduced and segregated populations of G. roeselii. However, no genetic measure on G. roeselii differed temporally or spatially over the investigated period, which indicates that D. villosus has not yet had an impact on G. roeselii at the genetic scale. Hence, even though a decline in population size of G. roeselii was found in Lake Constance, our results on the genetic scale contribute to recent findings that the overall impact of D. villosus on native species is not as strong as often discussed.


Microsatellites Genetic diversity Invasive species Displacement Coexistence Variability 



We thank all former members of the Cooperative Research Centre (CRC) 454 “Littoral Ecology of Lake Constance” who contributed to the benthic sampling program, especially Christian Fiek, and Karen Brune for editing the English language of the manuscript. This study was funded by the German Research Foundation (DFG) by the CRC 454 and the Project GE2219/3-1.

Supplementary material

10750_2018_3831_MOESM1_ESM.pdf (541 kb)
Supplementary material 1 (PDF 540 kb)


  1. Alp, M., I. Keller, A. M. Westram & C. T. Robinson, 2012. How river structure and biological traits influence gene flow: a population genetic study of two stream invertebrates with differing dispersal abilities. Freshwater Biology 57: 969–981.CrossRefGoogle Scholar
  2. Bacela-Spychalska, K., M. Grabowski, T. Rewicz, A. Konopacka & R. Wattier, 2013. The ‘killer shrimp’ Dikerogammarus villosus (Crustacea, Amphipoda) invading Alpine lakes: overland transport by recreational boats and scuba-diving gear as potential entry vectors? Aquatic Conservation: Marine and Freshwater Ecosystems 23: 606–618.CrossRefGoogle Scholar
  3. Baumgärtner, D., 2004. Principles of macroinvertebrate community structure in the littoral zone of Lake Constance. PhD thesis.Google Scholar
  4. Berthier, K., N. Charbonnel, M. Galan, Y. Chaval & J. F. Cosson, 2006. Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Molecular Ecology 15: 2665–2676.CrossRefGoogle Scholar
  5. Bij de Vaate, A. & A. G. Klink, 1995. Dikerogammarus villosus Sowinsky (Crustacea: Gammaridae) a new immigrant in the Dutch part of the Lower Rhine. Lauterbornia 20: 51–54.Google Scholar
  6. Bij de Vaate, A., K. Jazdzewski, H. A. M. Ketelaars, S. Gollasch & G. van der Velde, 2002. Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59: 1159–1174.CrossRefGoogle Scholar
  7. Bijlsma, R. & V. Loeschcke, 2012. Genetic erosion impedes adaptive responses to stressful environments. Evolutionary Applications 5: 117–129.CrossRefGoogle Scholar
  8. Bollache, L., S. Devin, R. Wattier, M. Chovet, J.-N. Beisel, J. C. Moreteau & T. Rigaud, 2004. Rapid range extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France: potential consequences. Archiv für Hydrobiologie 160: 57–66.CrossRefGoogle Scholar
  9. Bruijs, M. C. M., B. Kelleher, G. van der Velde & A. Bij de Vaate, 2001. Oxygen consumption, temperature and salinity tolerance of the invasive amphipod Dikerogammarus villosus: indicators of further dispersal via ballast water transport. Archiv für Hydrobiologie 152: 633–646.CrossRefGoogle Scholar
  10. Busch, J. D., P. M. Waser & J. A. DeWoody, 2007. Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Molecular Ecology 16: 2450–2462.CrossRefGoogle Scholar
  11. Carlsson, J., 2008. Effects of microsatellite null alleles on assignment testing. Journal of Heredity 99: 616–623.CrossRefGoogle Scholar
  12. Carroll, S. P., 2007. Natives adapting to invasive species: ecology, genes, and the sustainability of conservation. Ecological Research 22: 892–901.CrossRefGoogle Scholar
  13. Casellato, S., G. La Piana, L. Latella & S. Ruffo, 2006. Dikerogammarus villosus (Sowinsky, 1894) (Crustacea, Amphipoda, Gammaridae) for the first time in Italy. Italian Journal of Zoology 73: 97–104.CrossRefGoogle Scholar
  14. Chapuis, M.-P. & A. Estoup, 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621–631.CrossRefGoogle Scholar
  15. Cobben, M. M. P., O. Mitesser & A. Kubisch, 2017. Evolving mutation rate advances the invasion speed of a sexual species. BMC Evolutionary Biology 17: 150.CrossRefGoogle Scholar
  16. Cornuet, J. M. & G. Luikart, 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001–2014.PubMedPubMedCentralGoogle Scholar
  17. Coutellec, M.-A., A.-L. Besnard & T. Caquet, 2013. Population genetics of Lymnaea stagnalis experimentally exposed to cocktails of pesticides. Ecotoxicology 22: 879–888.CrossRefGoogle Scholar
  18. DAISIE, 2017. European invasive alien species gateway [available on internet at]. Accessed June 2017.
  19. Development Core Team, R., 2013. R: a language and environment for statistical computing, Vol. vol. R Foundation for Statistical Computing, Vienna.Google Scholar
  20. Dick, J. T. A. & D. Platvoet, 2000. Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proceedings of the Royal Society of London, Series B 267: 977–983.CrossRefGoogle Scholar
  21. Do, C., R. S. Waples, D. Peel, G. M. Macbeth, B. J. Tillett & J. R. Ovenden, 2013. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources 14: 209–214.CrossRefGoogle Scholar
  22. Ellegren, H. & N. Galtier, 2016. Determinants of genetic diversity. Nature Reviews Genetics 17: 422–433.CrossRefGoogle Scholar
  23. Ellner, S. P., 2013. Rapid evolution: from genes to communities, and back again? Functional Ecology 27: 1087–1099.CrossRefGoogle Scholar
  24. Frankham, R., 2005a. Genetics and extinction. Biological Conservation 126: 131–140.CrossRefGoogle Scholar
  25. Frankham, R., 2005b. Stress and adaptation in conservation genetics. Journal of Evolutionary Biology 18: 750–755.CrossRefGoogle Scholar
  26. Frankham, R., J. D. Ballou & D. A. Briscoe, 2004. A primer of conservation genetics. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  27. Fraser, D. J., M. M. Hansen, S. Ostergaard, N. Tessier, M. Legault & L. Bernatchez, 2007. Comparative estimation of effective population sizes and temporal gene flow in two contrasting population systems. Molecular Ecology 16: 3866–3889.CrossRefGoogle Scholar
  28. Gallardo, B., M. Clavero, M. I. Sánchez & M. Villà, 2016. Global ecological impacts of invasive species in aquatic ecosystems. Global Change Biology 22: 151–163.CrossRefGoogle Scholar
  29. Garza, J. C. & E. G. Williamson, 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10: 305–318.CrossRefGoogle Scholar
  30. Gemmer, I. & R. Gergs, 2013. Characterization of the first twelve microsatellite loci for the amphipod Gammarus roeselii (Crustacea: Amphipoda). Conservation Genetics Resources 5: 955–957.CrossRefGoogle Scholar
  31. Gergs, R. & K. O. Rothhaupt, 2015. Invasive species as driving factors for the structure of benthic communities in Lake Constance, Germany. Hydrobiologia 746: 245–254.CrossRefGoogle Scholar
  32. Gergs, R., L. Schlag & K. O. Rothhaupt, 2013. Different ammonia tolerance may facilitate spatial coexistence of Gammarus roeselii and the strong invader Dikerogammarus villosus. Biological Invasions 15: 1783–1793.CrossRefGoogle Scholar
  33. Gherardi, F., 2007. Biological invasions in inland waters: an overview. In Gherardi, F. (ed.), Biological invaders in inland waters: Profiles, distribution, and threats. Invading nature—Springer series in invasion ecology. Springer, New York: 3–25.Google Scholar
  34. Gilbert, K. J. & M. C. Whitlock, 2015. Evaluating methods for estimating local effective population size with and without migration. Evolution 69: 2154–2166.CrossRefGoogle Scholar
  35. Gollasch, S. & S. Nehring, 2006. National checklist for aquatic alien species in Germany. Aquatic Invasions 1: 245–269.CrossRefGoogle Scholar
  36. Goudet, J., 2005. Hierfstat, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes 5: 184–186.CrossRefGoogle Scholar
  37. Grabowski, M., K. Bacela & A. Konopacka, 2007. How to be an invasive gammarid (Amphipoda: Gammaroidea)—comparison of life history traits. Hydrobiologia 590: 75–84.CrossRefGoogle Scholar
  38. Hanselmann, A. J., 2011. A review of spatio-temporal patterns of the colonisation of Lake Constance with alien macrozoobenthos. Lauterbornia 72: 131–148.Google Scholar
  39. Hellmann, C., F. Schöll, S. Worischka, J. Becker & C. Winkelmann, 2017. River-specific effects of the invasive amphipod Dikerogammarus villosus (Crustacea: Amphipoda) on benthic communities. Biological Invasions 19: 381–398.CrossRefGoogle Scholar
  40. Hesselschwerdt, J., J. Necker & K. M. Wantzen, 2008. Gammarids in Lake Constance: habitat segregation between the invasive Dikerogammarus villosus and the indigenous Gammarus roeselii. Fundamental and Applied Limnology 173: 177–186.CrossRefGoogle Scholar
  41. IGKB, 2004. Der Bodensee Zustand-Fakten-Perspektiven. Internationale Gewässerschutzkommission für den Bodensee, Stuttgart, Germany [available on internet at]. Accessed Jan 2004.
  42. Jensen, J. L., A. J. Bohonak & S. T. Kelley, 2005. Isolation by distance, web service. BMC Genetics 6: 13. v.13.23 [available on internet at].
  43. Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.CrossRefGoogle Scholar
  44. Jombart, T., S. Devillard & F. Balloux, 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 94.CrossRefGoogle Scholar
  45. Jorde, P. E. & N. Ryman, 2007. Unbiased estimator for genetic drift and effective population size. Genetics 177: 927–935.CrossRefGoogle Scholar
  46. Keller, L. & D. M. Waller, 2002. Inbreeding effects in wild populations. Trends in Ecology & Evolution 17: 230–241.CrossRefGoogle Scholar
  47. Keller, L. F., K. J. Jeffrey, P. Arcese, M. A. Beaumont, W. M. Hochachka, J. N. M. Smith & M. W. Bruford, 2001. Immigration and the ephemerality of a neutral population bottleneck: evidence from molecular markers. Proceedings of the Royal Society B-Biological Sciences 268: 1387–1394.CrossRefGoogle Scholar
  48. Koester, M. & R. Gergs, 2014. No evidence for intraguild predation of Dikerogammarus villosus (Sowinsky 1894) at an invasion front in the Untere Lorze, Switzerland. Aquatic Invasions 9: 489–497.CrossRefGoogle Scholar
  49. Leuven, R. S. E. W., G. van der Velde, I. Baijens, J. Snijders, C. van der Zwart, H. J. R. Lenders & A. bij de Vaate, 2009. The river Rhine: a global highway for dispersal of aquatic invasive species. Biological Invasions 11: 1989–2008.CrossRefGoogle Scholar
  50. Luikart, G. & J. M. Cornuet, 1998. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology 12: 228–237.CrossRefGoogle Scholar
  51. Luikart, G., F. W. Allendorf, J.-M. Cornuet & W. B. Sherwin, 1998a. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238–247.CrossRefGoogle Scholar
  52. Luikart, G., W. B. Sherwin, B. M. Steele & F. W. Allendorf, 1998b. Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Molecular Ecology 7: 963–974.CrossRefGoogle Scholar
  53. MacNeil, C., D. Platvoet, J. T. A. Dick, N. Fielding, A. Constable, N. Hall, D. Aldridge, T. Renals & M. Diamond, 2010. The Ponto-Caspian “killer shrimp”, Dikerogammarus villosus (Sowinsky, 1894), invades the British Isles. Aquatic Invasions 5: 441–445.CrossRefGoogle Scholar
  54. MacNeil, C., J. T. A. Dick, D. Platvoet & M. Briffa, 2011. Direct and indirect effects of species displacements: an invading freshwater amphipod can disrupt leaf-litter processing and shredder efficiency. Journal of the North American Benthological Society 30: 38–48.CrossRefGoogle Scholar
  55. Martens, A. & K. Grabow, 2008. Risk of spreading of non-indigenous Amphipods due to overland transport of recreation boats. Lauterbornia 62: 41–44.Google Scholar
  56. Mörtl, M., 2004. Biotic interactions in the infralittoral of Lake Constance. PhD thesis.Google Scholar
  57. Mürle, U., A. Becker & P. Rey, 2004. Dikerogammarus villosus (Amphipoda) new in Lake Constance. Lauterbornia 49: 77–79.Google Scholar
  58. Palstra, F. P. & D. E. Ruzzante, 2008. Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology 17: 3428–3447.CrossRefGoogle Scholar
  59. Paradis, E., 2010. pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26: 419–420.CrossRefGoogle Scholar
  60. Piry, S., G. Luikart & J. M. Cornuet, 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity 90: 502–503.CrossRefGoogle Scholar
  61. Piscart, C., B. J. Kefford & J. N. Beiseld, 2011. Are salinity tolerances of non-native macroinvertebrates in France an indicator of potential for their translocation in a new area? Limnologica 41: 107–112.CrossRefGoogle Scholar
  62. QGIS Development Team, 2014. QGIS geographic information system. Version 2.4. Open source geospatial foundation project [available on internet at].
  63. Rewicz, T., M. Grabowski, C. MacNeil & K. Bacela-Spychalska, 2014. The profile of a ‘perfect’ invader—the case of killer shrimp, Dikerogammarus villosus. Aquatic Invasions 9: 267–288.CrossRefGoogle Scholar
  64. Ricciardi, A. & H. J. MacIsaac, 2000. Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology and Evolution 15: 62–65.CrossRefGoogle Scholar
  65. Sala, O. E., F. S. Chapin II, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-sanwald, L. F. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oestergeld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker & D. H. Wall, 2000. Global diversity scenarios for the year 2100. Science 287: 1770–1774.CrossRefGoogle Scholar
  66. Shama, L. N. S., K. B. Kubow, J. Jokela & C. T. Robinson, 2011. Bottlenecks drive temporal and spatial genetic changes in alpine caddisfly metapopulations. BMC Evolutionary Biology 11: 278.CrossRefGoogle Scholar
  67. Smith, T. B. & L. Bernatchez, 2008. Evolutionary change in human-altered environments. Molecular Ecology 17: 1–8.CrossRefGoogle Scholar
  68. Strauss, S. Y., J. A. Lau & S. P. Carroll, 2006. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecology Letters 9: 357–374.CrossRefGoogle Scholar
  69. Suarez, A. V. & N. D. Tsutsui, 2008. The evolutionary cosequences of biological invasions. Molecular Ecology 17: 351–360.CrossRefGoogle Scholar
  70. van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  71. Vellend, M., L. J. Harmon, J. L. Lockwood, M. M. Mayfield, A. R. Hughes, J. P. Wares & D. F. Sax, 2007. Effects of exotic species on evolutionary diversification. Trends in Ecology & Evolution 22: 481–488.CrossRefGoogle Scholar
  72. Vilas, R., C. Bouza, M. Vera, A. Millán & P. Martínez, 2010. Variation in anonymous and EST-microsatellites suggests adaptive population divergence in turbot. Marine Ecology Progress Series 420: 231–239.CrossRefGoogle Scholar
  73. Waples, R. S. & C. Do, 2008. ldne: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources 8: 753–756.CrossRefGoogle Scholar
  74. Wessels, M., 1998. Geological history of the Lake Constance area. Archiv für Hydrobiologie/Advances in Limnology 53: 1–12.Google Scholar
  75. Westram, A. M., J. Jokela & I. Keller, 2013. Hidden biodiversity in an ecologically important freshwater amphipod: differences in genetic structure between two cryptic species. PLoS ONE 8: e69576.CrossRefGoogle Scholar
  76. Wetherill, G. B. & D. W. Brown, 1991. Statistical process control. Chapman and Hall, New York.CrossRefGoogle Scholar
  77. Wilson, G. A. & B. Rannala, 2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177–1191.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • René Gergs
    • 1
    • 2
    Email author
  • Isabelle Gemmer
    • 1
  • Meike Koester
    • 1
    • 3
  • Karl-Otto Rothhaupt
    • 4
  • Jasminca Behrmann-Godel
    • 4
  1. 1.Institute for Environmental SciencesUniversity of Koblenz-LandauLandauGermany
  2. 2.German Environment AgencyBerlinGermany
  3. 3.Institute of Natural SciencesUniversity of Koblenz-LandauKoblenzGermany
  4. 4.Limnological InstituteUniversity of KonstanzConstanceGermany

Personalised recommendations