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.
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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:e63708
Alderman DJ (1996) Geographical spread of bacterial and fungal diseases of crustaceans. Bull Off Int Epizoot 15:603–632
Alderman DJ, Polglase JL, Frayling M (1987) Aphanomyces astaci pathogenicity under laboratory and field conditions. J Fish Dis 10:385–393
Araújo MB, Guisan A (2006) Five (or so) challenges for species distribution modelling. J Biogeogr 33:1677–1688
Bezdek JC (1981) Pattern recognition with fuzzy objective function algoritms. Plenum Press, New York
Bohman P, Edsman L (2011) Status, management and conservation of crayfish in Sweden: results and the way forward. Freshw Crayfish 18:19–26
Buřič M, Kouba A, Kozák P (2009) Spring mating period in Orconectes limosus: the reason for movement. Aquat Sci 71:473–477
Capinha C, Leung B, Anastácio P (2011) Predicting worldwide invasiveness for four major problematic decapods: an evaluation of using different calibration sets. Ecography 34:448–459
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 27:731–740
CBD (2011) Aichi biodiversity targets. Convention on biological diversity. http://www.cbd.int/sp/targets/. Accessed 19 December 2011
Chucholl C (2011) Disjunct distribution pattern of Procambarus clarkii (Crustacea, Decapoda, Astacida, Cambaridae) in an artificial lake system in Southwestern Germany. Aquat Invasions 6:109–113
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 404:04
Chucholl C (2013) Feeding ecology and ecological impact of an alien “warm-water” omnivore in cold lakes. Limnologica 43:219–229
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 5:309–318
Chucholl C, Dehus P (2011) Flusskrebse in Baden-Württemberg. Fischereiforschungsstelle Baden-Württemberg (FFS), Langenargen
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
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 7:511–519
Chucholl C, Mrugała A, Petrusek A (2015) First record of an introduced population of the southern lineage of white-clawed crayfish (Austropotamobius “italicus”) north of the Alps. Knowl Manag Aquat Ecosyst 416:10
Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143
Clarke K, Warwick R (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Primer-E, Plymouth
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, Brussels
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 L317/35
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 59–80
DAISIE (2012) European invasive alien species gateway. http://www.europe-aliens.org/. Accessed 1st February 2012
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 37:1607–1613
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 380–381:1303–1312
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 408:10
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 16:1545–1555
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 70–93
Elith J, Graham CH, Anderson RP et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151
Elith J, Kearney M, Phillips SJ (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57
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 6:55–67
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:e70157
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
Füreder L (ed) (2009) Flusskrebse: Biologie, Ökologie, Gefährdung. Veröffentlichungen des Naturmuseums Südtirol, 6, Folio-Verlag, Bozen, Wien
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 40:2274–2284
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 3–25
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 105:75–80
Hänfling B, Edwards F, Gherardi F (2011) Invasive alien Crustacea: dispersal, establishment, impact and control. Biocontrol 56:573–595
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 29–75
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 11:394–395
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 26:232–262
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 376–377:759–776
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
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 59:1123–1135
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 411:10
Justo-Hanani R, Dayan T, Tal A (2010) The role of regulatory decision-making on nonindigenous species introductions. Biol Invasions 12:2815–2824
Karatayev AY, Burlakova LE, Padilla DK, Mastitsky SE, Olenin S (2009) Invaders are not a random selection of species. Biol Invasions 11:2009–2019
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 414:15
Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05
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 23:1204–1213
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 26:299–319
Lampert W, Sommer U (1999) Limnoökologie. Georg Thieme Verlag, Stuttgart
Larson ER, Olden JD, Usio N (2010) Decoupled conservatism of Grinnellian and Eltonian niches in an invasive arthropod. Ecosphere 1:16
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 57:1823–1838
LGL (2012) Amtliches Topografisch-Kartografisches Informationssystem. Landesamt für Geoinformation und Landentwicklung Baden-Württemberg (LGL), Stuttgart
Light T (2003) Success and failure in a lotic crayfish invasion: the roles of hydrologic variability and habitat alteration. Freshw Biol 48:1886–1897
Light T, Erman DC, Myrick C, Clarke J (1995) Decline of the Shasta Crayfish (Pacifastacus fortis Faxon) of Northeastern California. Conserv Biol 9:1567–1577
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 43:449–472
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)
Manenti R, Bonelli M, Scaccini D, Binda A, Zugnoni A (2014) Austropotamobius pallipes reduction vs. Procambarus clarkii spreading: management implications. J Nat Conserv 22:586–591
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:e40530
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 51:224–235
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 16:95–108
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 23:897–907
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 26:134–140
Nakazato T, Warren DL, Moyle LC (2010) Ecological and geographic modes of species divergence in wild tomatoes. Am J Bot 97:680–693
Nyström P (1999) Ecological impact of introduced and native crayfish on freshwater communities: European perspectives. Crustac Issues 11:63–85
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Modell 190:231–259
Primak RB (2011) Endangered and threatened species. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Los Angeles, pp 189–193
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
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
Ramalho RO, Anastácio PM (2015) Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hydrobiologia 746:135–146
Reynolds J, Souty-Grosset C (eds) (2012) Management of freshwater biodiversity. Crayfish as bioindicators. Cambridge University Press, Cambridge
Riegel JA (1959) The systematics and distribution of crayfishes in California. Calif Fish Game 45:29–50
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 23:3301–3317
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R et al (2000) Biodiversity scenario for the year 2100. Science 287:1770–1774
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 8:103–109
Schweng E (1973) Orconectes limosus in Deutschland insbesondere im Rheingebiet. Freshw Crayfish 1:79–87
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), Brussels
Söderbäck B (1991) Interspecific dominance relationship and aggressive interactions in the freshwater crayfishes Astacus astacus (L.) and Pacifastacus leniusculus (Dana). Can J Zool 69:1321–1325
Souty-Grosset C, Holdich DM, Noel PY, Reynolds JD, Haffner P (eds) (2006) Atlas of crayfish in Europe. Museum national d‘Histoire naturelle, Paris
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 17:29–34
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 120:74–79
Troschel J, Dehus P (1993) Distribution of crayfish species in the Federal Republic of Germany, with special reference to Austropotamobius pallipes. Freshw Crayfish 9:390–398
Twardochleb LA, Olden JD, Larson ER (2013) A global meta-analysis of the ecological impacts of nonnative crayfish. Freshw Sci 32:1367–1382
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 21:271–277
Weinländer M, Füreder L (2012) Associations between stream habitat characteristics and native and alien crayfish occurrence. Hydrobiologia 693:237–249
Weinländer M, Bou-Vinals A, Füreder L (2014) Landscape analyses offer a promising tool for managing native and alien crayfish species. Freshw Crayfish 20:27–40
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 25:53–73
Acknowledgments
I thank S. Blank (Fisheries Research Station Baden-Wuerttemberg) for his invaluable assistance with handling the FiAKa database. A. Brinker, T. Basen (both Fisheries Research Station BW), one anonymous reviewer, and Z. Faulkes (University of Texas Rio Grande Valley) are thanked for helpful comments on the manuscript. I also acknowledge the following persons (in alphabetical order) for kindly providing crayfish records: J. Abele, S. Bauer, R. Biss, A. Fichtner, S. Hemmerle, J. Jilg, U. Junghans, B. Kappus, F. Künemund, G. Maier, M. Martens, A. Megerle, F. Pätzold, P. Pfeiffer, S. Phillipson, P. Rudolph, F. Sauter, D. Schmid, W. Sitter, K. Strauß, P. Weisser, F. Wendler, C. Wenzel, and S. Werner. I gratefully acknowledge the financial support received from the fisheries levy of Baden-Wuerttemberg. The views expressed in this article are those of the author and not necessarily of his parent organisation.
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Chucholl, C. The bad and the super-bad: prioritising the threat of six invasive alien to three imperilled native crayfishes. Biol Invasions 18, 1967–1988 (2016). https://doi.org/10.1007/s10530-016-1141-2
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DOI: https://doi.org/10.1007/s10530-016-1141-2