Biological Invasions

, Volume 18, Issue 7, pp 1967–1988

The bad and the super-bad: prioritising the threat of six invasive alien to three imperilled native crayfishes

Original Paper

Abstract

Multiple species invasions and limited resources for management require prioritisation of deleterious effects of invaders on imperilled native species. This study prioritises the threat of six non-indigenous crayfish species (NICS) to three indigenous crayfish species (ICS) in southwestern Germany, a European region with high diversity of crayfish species and freshwater habitats. Using multivariate statistical analyses and niche-based species distribution models, the (1) contemporary and potential range overlap, (2) habitat overlap, and (3) rate of spread of the nine species were assessed. Predicted and contemporary range overlap with ICS was consistently the highest for the alien signal crayfish. Environmental niches of ICS tended to be associated with cooler temperatures (except for white-clawed crayfish), lower Human Influence Index, and higher terrain slope than that of alien Orconectes and Procambarus species, but were mostly similar to that of signal crayfish. Habitat overlap was found to be the highest between signal crayfish and ICS. In contrast to Orconectes and Procambarus species, signal crayfish also invade headwaters, where the most ICS populations occur. Range expansion during the past 15 years was the highest for signal crayfish, followed by Orconectes species. Because of the great potential to invade as-yet isolated refuge areas and spread at a high rate, signal crayfish is of the highest concern for conservation of ICS and should be primarily targeted by prevention and control measures. However, it merely represents the ‘worst of the worst’, since all NICS of North American origin are natural reservoirs of crayfish plague, a fatal disease of ICS.

Keywords

Aquatic invaders Risk assessment Crustacea Distribution models Habitat association 

Supplementary material

10530_2016_1141_MOESM1_ESM.pdf (420 kb)
Supplementary material 1 (PDF 419 kb)
10530_2016_1141_MOESM2_ESM.pdf (1.1 mb)
Supplementary material 2 (PDF 1106 kb)

References

  1. Aguirre-Gutiérrez J, Carvalheiro LG, Polce C, van Loon EE, Raes N, Reemer M, Biesmeijer JC (2013) Fit-for-purpose: species distribution model performance depends on evaluation criteria—Dutch hoverflies as a case study. PLoS ONE 8:e63708CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alderman DJ (1996) Geographical spread of bacterial and fungal diseases of crustaceans. Bull Off Int Epizoot 15:603–632CrossRefGoogle Scholar
  3. Alderman DJ, Polglase JL, Frayling M (1987) Aphanomyces astaci pathogenicity under laboratory and field conditions. J Fish Dis 10:385–393CrossRefGoogle Scholar
  4. Araújo MB, Guisan A (2006) Five (or so) challenges for species distribution modelling. J Biogeogr 33:1677–1688CrossRefGoogle Scholar
  5. Bezdek JC (1981) Pattern recognition with fuzzy objective function algoritms. Plenum Press, New YorkCrossRefGoogle Scholar
  6. Bohman P, Edsman L (2011) Status, management and conservation of crayfish in Sweden: results and the way forward. Freshw Crayfish 18:19–26CrossRefGoogle Scholar
  7. Buřič M, Kouba A, Kozák P (2009) Spring mating period in Orconectes limosus: the reason for movement. Aquat Sci 71:473–477CrossRefGoogle Scholar
  8. Capinha C, Leung B, Anastácio P (2011) Predicting worldwide invasiveness for four major problematic decapods: an evaluation of using different calibration sets. Ecography 34:448–459CrossRefGoogle Scholar
  9. Capinha C, Larson ER, Tricarico E, Olden JD, Gherardi F (2013) Effects of climate change, invasive species, and disease on the distribution of native European crayfishes. Conserv Biol 27:731–740CrossRefPubMedGoogle Scholar
  10. CBD (2011) Aichi biodiversity targets. Convention on biological diversity. http://www.cbd.int/sp/targets/. Accessed 19 December 2011
  11. Chucholl C (2011) Disjunct distribution pattern of Procambarus clarkii (Crustacea, Decapoda, Astacida, Cambaridae) in an artificial lake system in Southwestern Germany. Aquat Invasions 6:109–113CrossRefGoogle Scholar
  12. Chucholl C (2012) Understanding invasion success: life-history traits and feeding habits of the alien crayfish Orconectes immunis (Decapoda, Astacida, Cambaridae). Knowl Manag Aquat Ecosyst 404:04CrossRefGoogle Scholar
  13. Chucholl C (2013) Feeding ecology and ecological impact of an alien “warm-water” omnivore in cold lakes. Limnologica 43:219–229CrossRefGoogle Scholar
  14. Chucholl C (2014) Predicting the risk of introduction and establishment of an exotic aquarium animal in Europe: insights from one decade of Marmorkrebs (Crustacea, Astacida, Cambaridae) releases. Manag Biol Invasions 5:309–318CrossRefGoogle Scholar
  15. Chucholl C, Dehus P (2011) Flusskrebse in Baden-Württemberg. Fischereiforschungsstelle Baden-Württemberg (FFS), LangenargenGoogle Scholar
  16. Chucholl C, Schrimpf A (2015) The decline of endangered stone crayfish (Austropotamobius torrentium) in southern Germany is related to the spread of invasive alien species and land-use change. Aquat Conserv Mar Freshw Ecosyst. doi:10.1002/aqc.2568 Google Scholar
  17. Chucholl C, Morawetz K, Groß H (2012) The clones are coming—strong increase in Marmorkrebs [Procambarus fallax (Hagen, 1870) f. virginalis] records from Europe. Aquat Invasions 7:511–519CrossRefGoogle Scholar
  18. Chucholl C, Mrugała A, Petrusek A (2015) First record of an introduced population of the southern lineage of white-clawed crayfish (Austropotamobiusitalicus”) north of the Alps. Knowl Manag Aquat Ecosyst 416:10CrossRefGoogle Scholar
  19. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  20. Clarke K, Warwick R (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, PlymouthGoogle Scholar
  21. COM (2008) Towards an EU strategy on invasive species. Communication from the Commission to the Council, the European Parliament, the European Economic and Social Committee and the Committee of the Regions, BrusselsGoogle Scholar
  22. Council of the European Communities (2014) Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off J Eur Commun L317/35Google Scholar
  23. D’Antonio C, Meyerson LA, Denslow J (2001) Exotic species and conservation—research needs. In: Soulé ME, Orians GH (eds) Conservation biology: research priorities for the next decade. Island press, Washington, pp 59–80Google Scholar
  24. DAISIE (2012) European invasive alien species gateway. http://www.europe-aliens.org/. Accessed 1st February 2012
  25. Dana ED, García-de-Lomas J, González R, Ortega F (2011) Effectiveness of dam construction to contain the invasive crayfish Procambarus clarkii in a Mediterranean mountain stream. Ecol Eng 37:1607–1613CrossRefGoogle Scholar
  26. Diéguez-Uribeondo J (2006) The dispersion of the Aphanomyces astaci-carrier Pacifastacus leniusculus by humans represents the main cause of disappearance of the indigenous crayfish Austropotamobius pallipes in Navarra. Bull Fr Peche Piscicult 380–381:1303–1312CrossRefGoogle Scholar
  27. Dörr AJM, Scalici M (2013) Revisiting reproduction and population structure and dynamics of Procambarus clarkii eight years after its introduction into Lake Trasimeno (Central Italy). Knowl Manag Aquat Ecosyst 408:10CrossRefGoogle Scholar
  28. Dunoyer L, Dijoux L, Bollache L, Lagrue C (2014) Effects of crayfish on leaf litter breakdown and shredder prey: are native and introduced species functionally redundant? Biol Invasions 16:1545–1555CrossRefGoogle Scholar
  29. Elith J, Leathwick JR (2009) The contribution of species distribution modelling to conservation prioritization. In: Possingham HP, Moilanen A, Wilson KA (eds) Spatial conservation prioritization: quantitative methods and computational tools. Oxford University Press, Oxford, pp 70–93Google Scholar
  30. Elith J, Graham CH, Anderson RP et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  31. Elith J, Kearney M, Phillips SJ (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342CrossRefGoogle Scholar
  32. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57CrossRefGoogle Scholar
  33. Feria TP, Faulkes Z (2011) Forecasting the distribution of Marmorkrebs, a parthenogenetic crayfish with high invasive potential, in Madagascar, Europe, and North America. Aquat Invasions 6:55–67CrossRefGoogle Scholar
  34. Filipová L, Petrusek A, Matasová K, Delaunay C, Grandjean F (2013) Prevalence of the crayfish plague pathogen Aphanomyces astaci in populations of the signal crayfish Pacifastacus leniusculus in France: evaluating the threat to native crayfish. PLoS ONE 8:e70157CrossRefPubMedPubMedCentralGoogle Scholar
  35. Firn J, Martin TG, Chadès I, Walters B, Hayes J, Nicol S, Carwardine J (2015) Priority threat management of non-native plants to maintain ecosystem integrity across heterogeneous landscapes. J Appl Ecol. doi:10.1111/1365-2664.12500 Google Scholar
  36. Füreder L (ed) (2009) Flusskrebse: Biologie, Ökologie, Gefährdung. Veröffentlichungen des Naturmuseums Südtirol, 6, Folio-Verlag, Bozen, WienGoogle Scholar
  37. Gallardo B, Ermgassen PS, Aldridge DC (2013) Invasion ratcheting in the zebra mussel (Dreissena polymorpha) and the ability of native and invaded ranges to predict its global distribution. J Biogeogr 40:2274–2284CrossRefGoogle Scholar
  38. 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, vol 2. Springer, Dordrecht, pp 3–25CrossRefGoogle Scholar
  39. Gil-Sanchez JM, Alba-Tercedor J (2002) Ecology of the native and introduced crayfishes Austropotamobius pallipes and Procambarus clarkii in southern Spain and implications for conservation of the native species. Biol Conserv 105:75–80CrossRefGoogle Scholar
  40. Hänfling B, Edwards F, Gherardi F (2011) Invasive alien Crustacea: dispersal, establishment, impact and control. Biocontrol 56:573–595CrossRefGoogle Scholar
  41. Holdich DM, Pöckl M (2007) Invasive crustaceans in European inland waters. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Invading nature—springer series in invasion ecology, vol 2. Springer, Dordrecht, pp 29–75CrossRefGoogle Scholar
  42. Holdich DM, Reynolds JD, Souty-Grosset C, Sibley PJ (2009) A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl Manag Aquat Ecosyst 11:394–395Google Scholar
  43. Holdich DM, James J, Jackson C, Peay S (2014) The North American signal crayfish, with particular reference to its success as an invasive species in Great Britain. Ethol Ecol Evol 26:232–262CrossRefGoogle Scholar
  44. Huber M, Schubart C (2005) Distribution and reproductive biology of Austropotamobius torrentium in Bavaria and documentation of a contact zone with the alien crayfish Pacifastacus leniusculus. Bull Fr Peche Piscicult 376–377:759–776CrossRefGoogle Scholar
  45. Hulme PE (2015) Invasion pathways at a crossroad: policy and research challenges for managing alien species introductions. J Appl Ecol. doi:10.1111/1365-2664.12470 Google Scholar
  46. Jackson MC, Jones T, Milligan M, Sheath D, Taylor J, Ellis A, England J, Grey J (2014) Niche differentiation among invasive crayfish and their impacts on ecosystem structure and functioning. Fresh Biol 59:1123–1135CrossRefGoogle Scholar
  47. Jussila J, Kokko H, Kortet R, Makkonen J (2013) Aphanomyces astaci PsI-genotype isolates from different Finnish signal crayfish stocks show variation in their virulence but still kill fast. Knowl Manag Aquat Ecosyst 411:10CrossRefGoogle Scholar
  48. Justo-Hanani R, Dayan T, Tal A (2010) The role of regulatory decision-making on nonindigenous species introductions. Biol Invasions 12:2815–2824CrossRefGoogle Scholar
  49. Karatayev AY, Burlakova LE, Padilla DK, Mastitsky SE, Olenin S (2009) Invaders are not a random selection of species. Biol Invasions 11:2009–2019CrossRefGoogle Scholar
  50. Keller NS, Pfeiffer M, Roessink I, Schulz R, Schrimpf A (2014) First evidence of crayfish plague agent in populations of the marbled crayfish (Procambarus fallax forma virginalis). Knowl Manag Aquat Ecosyst 414:15CrossRefGoogle Scholar
  51. Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05CrossRefGoogle Scholar
  52. Kozubíková E, Filipová L, Kozák P, Ďuriš Z, Martín MP, Diéguez-Uribeondo J, Oidtmann B, Petrusek A (2009) Prevalence of the crayfish plague pathogen Aphanomyces astaci in invasive American crayfishes in the Czech Republic. Conserv Biol 23:1204–1213CrossRefPubMedGoogle Scholar
  53. Kozubíková-Balcarová E, Beran L, Ďuriš Z, Fischer D, Horká I, Svobodová J, Petrusek A (2014) Status and recovery of indigenous crayfish populations after recent crayfish plague outbreaks in the Czech Republic. Ethol Ecol Evol 26:299–319CrossRefGoogle Scholar
  54. Lampert W, Sommer U (1999) Limnoökologie. Georg Thieme Verlag, StuttgartGoogle Scholar
  55. Larson ER, Olden JD, Usio N (2010) Decoupled conservatism of Grinnellian and Eltonian niches in an invasive arthropod. Ecosphere 1:16CrossRefGoogle Scholar
  56. Larson ER, Abbott CL, Usio N, Azuma N, Wood KA, Herborg LM, Olden JD (2012) The signal crayfish is not a single species: cryptic diversity and invasions in the Pacific Northwest range of Pacifastacus leniusculus. Freshw Biol 57:1823–1838CrossRefGoogle Scholar
  57. LGL (2012) Amtliches Topografisch-Kartografisches Informationssystem. Landesamt für Geoinformation und Landentwicklung Baden-Württemberg (LGL), StuttgartGoogle Scholar
  58. Light T (2003) Success and failure in a lotic crayfish invasion: the roles of hydrologic variability and habitat alteration. Freshw Biol 48:1886–1897CrossRefGoogle Scholar
  59. Light T, Erman DC, Myrick C, Clarke J (1995) Decline of the Shasta Crayfish (Pacifastacus fortis Faxon) of Northeastern California. Conserv Biol 9:1567–1577CrossRefGoogle Scholar
  60. Lodge DM, Deines A, Gherardi F, Yeo DCJ, Arcella T, Baldridge AK et al (2012) Global introductions of crayfishes: evaluating the impact of species invasions on ecosystem services. Annu Rev Ecol Evol Syst 43:449–472CrossRefGoogle Scholar
  61. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s worst invasive alien species. A selection from the Global Invasive Species Database. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)Google Scholar
  62. Manenti R, Bonelli M, Scaccini D, Binda A, Zugnoni A (2014) Austropotamobius pallipes reduction vs. Procambarus clarkii spreading: management implications. J Nat Conserv 22:586–591CrossRefGoogle Scholar
  63. Markovic D, Freyhof J, Wolter C (2012) Where are all the fish: potential of biogeographical maps to project current and future distribution patterns of freshwater species. PLoS ONE 7:e40530CrossRefPubMedPubMedCentralGoogle Scholar
  64. McCarthy JM, Hein CL, Olden JD, Vander Zanden M (2006) Coupling long-term studies with meta-analysis to investigate impacts of non-native crayfish on zoobenthic communities. Freshw Biol 51:224–235CrossRefGoogle Scholar
  65. McGeoch MA, Butchart SHM, Spear D, Marais E, Kleynhans EJ, Symes A et al (2010) Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Divers Distrib 16:95–108CrossRefGoogle Scholar
  66. Nakata K, Goshima S (2003) Competition for shelter of preferred sizes between the native crayfish species Cambaroides japonicus and the alien crayfish species Pacifastacus leniusculus in Japan in relation to prior residence, sex difference, and body size. J Crustac Biol 23:897–907CrossRefGoogle Scholar
  67. Nakata K, Goshima S (2006) Asymmetry in mutual predation between the endangered japanese native crayfish and the North American invasive crayfish : a possible reason for species replacement. J Crustac Biol 26:134–140CrossRefGoogle Scholar
  68. Nakazato T, Warren DL, Moyle LC (2010) Ecological and geographic modes of species divergence in wild tomatoes. Am J Bot 97:680–693CrossRefPubMedGoogle Scholar
  69. Nyström P (1999) Ecological impact of introduced and native crayfish on freshwater communities: European perspectives. Crustac Issues 11:63–85Google Scholar
  70. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259CrossRefGoogle Scholar
  71. Primak RB (2011) Endangered and threatened species. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Los Angeles, pp 189–193Google Scholar
  72. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  73. Quinn A, Gallardo B, Aldridge DC (2013) Quantifying the ecological niche overlap between two interacting invasive species: the zebra mussel (Dreissena polymorpha) and the quagga mussel (Dreissena rostriformis bugensis). Aquat Conserv Mar Freshw Ecosyst. doi:10.1002/aqc.2414 Google Scholar
  74. Ramalho RO, Anastácio PM (2015) Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hydrobiologia 746:135–146CrossRefGoogle Scholar
  75. Reynolds J, Souty-Grosset C (eds) (2012) Management of freshwater biodiversity. Crayfish as bioindicators. Cambridge University Press, CambridgeGoogle Scholar
  76. Riegel JA (1959) The systematics and distribution of crayfishes in California. Calif Fish Game 45:29–50Google Scholar
  77. Římalová K, Douda K, Štambergová M (2014) Species-specific pattern of crayfish distribution within a river network relates to habitat degradation: implications for conservation. Biodivers Conserv 23:3301–3317CrossRefGoogle Scholar
  78. Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R et al (2000) Biodiversity scenario for the year 2100. Science 287:1770–1774CrossRefPubMedGoogle Scholar
  79. Schrimpf A, Chucholl C, Schmidt T, Schulz R (2013) Crayfish plague agent detected in populations of the invasive North American crayfish Orconectes immunis (Hagen, 1870) in the Rhine River, Germany. Aquat Invasions 8:103–109CrossRefGoogle Scholar
  80. Schweng E (1973) Orconectes limosus in Deutschland insbesondere im Rheingebiet. Freshw Crayfish 1:79–87Google Scholar
  81. Shine C, Kettunen M, ten Brink P, Genovesi P, Gollasch S (2009) Technical support to EU strategy on invasive species (IAS)—recommendations on policy options to control the negative impacts of IAS on biodiversity in Europe and the EU. Final report for the European Commission. Institute for European Environmental Policy (IEEP), BrusselsGoogle Scholar
  82. Söderbäck B (1991) Interspecific dominance relationship and aggressive interactions in the freshwater crayfishes Astacus astacus (L.) and Pacifastacus leniusculus (Dana). Can J Zool 69:1321–1325CrossRefGoogle Scholar
  83. Souty-Grosset C, Holdich DM, Noel PY, Reynolds JD, Haffner P (eds) (2006) Atlas of crayfish in Europe. Museum national d‘Histoire naturelle, ParisGoogle Scholar
  84. Souty-Grosset C, Hardy V, Raimond R, Ollivier L (2010) Land use in headwaters and the distribution of native white-clawed crayfish, Austropotamobius pallipes (Lereboullet), in a stream from the Poitou-Charentes Region, France. Freshw Crayfish 17:29–34Google Scholar
  85. Tilmans M, Mrugała A, Svoboda J, Engelsma MY, Petie M, Soes DM et al (2014) Survey of the crayfish plague pathogen presence in the Netherlands reveals a new Aphanomyces astaci carrier. J Invertebr Pathol 120:74–79CrossRefPubMedGoogle Scholar
  86. Troschel J, Dehus P (1993) Distribution of crayfish species in the Federal Republic of Germany, with special reference to Austropotamobius pallipes. Freshw Crayfish 9:390–398Google Scholar
  87. Twardochleb LA, Olden JD, Larson ER (2013) A global meta-analysis of the ecological impacts of nonnative crayfish. Freshw Sci 32:1367–1382CrossRefGoogle Scholar
  88. Usio N, Nakajima H, Kamiyama R, Wakana I, Hiruta S, Takamura N (2006) Predicting the distribution of invasive crayfish (Pacifastacus leniusculus) in a Kusiro Moor marsh (Japan) using classification and regression trees. Ecol Res 21:271–277CrossRefGoogle Scholar
  89. Weinländer M, Füreder L (2012) Associations between stream habitat characteristics and native and alien crayfish occurrence. Hydrobiologia 693:237–249CrossRefGoogle Scholar
  90. Weinländer M, Bou-Vinals A, Füreder L (2014) Landscape analyses offer a promising tool for managing native and alien crayfish species. Freshw Crayfish 20:27–40CrossRefGoogle Scholar
  91. Westman K, Savolainen R, Julkunen M (2002) Replacement of the native crayfish Astacus astacus by the introduced species Pacifastacus leniusculus in a small, enclosed Finnish lake: a 30-year study. Ecography 25:53–73CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Fisheries Research Station Baden-WürttembergLangenargenGermany

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