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Multifaceted implications of the competition between native and invasive crayfish: a glimmer of hope for the native’s long-term survival

Abstract

Biological invasions represent a complex phenomenon driven by multiple factors. In this study, a real-time invasion process between a native (Pontastacus leptodactylus) and an invasive (Faxonius limosus) crayfish species was investigated in the Lower Danube (South-East Europe) through an interdisciplinary approach, by measuring various ecological, genetic, physiological and biometric endpoints. The results revealed that the prolonged competition in old invaded sites of the river (at least a decade) either drove the native species to extinction, or, unexpectedly, allowed its survival as highly fragmented populations. However, for the latter situation, several biological and ecological traits differed in the remnant populations: increased trophic position and elemental imbalance for two major macronutrients (C:N molar ratio), low growth, as strongly contracted trophic niche widths and low overlap degree with the invasive crayfish. The data suggest that the prolonged competition induced potential resource partitioning between species, potentially driving their coexistence, as the development of larger and heavier claws within the native males’ population. On the contrary, in more recently invaded sectors of the Lower Danube (3 years), the trophic niche of the native species was significantly larger compared to old invaded sites and characterised by high level of niche overlap, indicating almost identical diet with the invasive crayfish, but characterised by the lowest trophic position compared to other invasion sectors. The genetic diversity of the native crayfish populations was strongly reduced in the invaded sectors of the river, but without signs of genetic bottleneck, which may be explained by a drift-mutational equilibrium reached as a consequence of diminishing population size. Our findings suggest strong coexistence potential in the future for both species in the Lower Danube.

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References

  • Adegboye D (1981) The ‘Crayfish Condition Factor’ a tool in crayfish research. Freshw Crayfish 5:154–172

    Google Scholar 

  • Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715

    Article  Google Scholar 

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Université de Montpellier II, Montpellier

  • Bøhn T, Amundsen PA, Sparrow A (2008) Competitive exclusion after invasion? Biol Invasions 10:359–368

    Google Scholar 

  • Bolnick DI, Svanbäck R, Araújo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci 104:10075–10079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brandner J, Cerwenka AF, Schliewen UK, Geist J (2013) Bigger is better: characteristics of round gobies forming an invasion front in the Danube River. PLoS ONE 8:e73036

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buřič M, Hulák M, Kouba A, Petrusek A, Kozák P (2011) A successful crayfish invader is capable of facultative parthenogenesis: a novel reproductive mode in decapod crustaceans. PLoS ONE 6:e20281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byers JE (2000) Competition between two estuarine snails: implications for invasion of exotic species. Ecology 81:1225–1239

    Article  Google Scholar 

  • Canales-Delgadillo JC, Scott-Morales L, Korb J (2012) The influence of habitat fragmentation on genetic diversity of a rare bird species that commonly faces environmental fluctuations. J Avian Biol 43:168–176

    Article  Google Scholar 

  • Carroll SP, Loye LE, Dingle H, Mathieson M, Famula TR, Zalucki MP (2005) And the beak shall inherit—evolution in response to invasion. Ecol Lett 8:944–951

    Article  PubMed  Google Scholar 

  • Cattau CE, Fletcher RJ, Kimball RT, Miller CW, Kitchens WM (2018) Rapid morphological change of a top predator with the invasion of a novel prey. Nat Ecol Evol 2:108–115

    Article  PubMed  Google Scholar 

  • Christensen V, Walters CJ (2004) Ecopath with ecosim: methods, capabilities and limitations. Ecol Model 172:109–139

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1997) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    Google Scholar 

  • Cross WF, Benstead JP, Rosemond AD, Wallace JB (2003) Consumer-resource stoichiometry in detritus-based streams. Ecol Lett 6:721–732

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Filipová L, Lieb DA, Grandjean F, Petrusek A (2011) Haplotype variation in the spiny-cheek crayfish Orconectes limosus: colonization of Europe and genetic diversity of native stocks. Freshw Sci 30:871–881

    Google Scholar 

  • Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynolds RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14(2):245–253

    Article  Google Scholar 

  • Fitzsimons JD, Jonas JL, Claramunt RM, Williston B, Williston G, Marsden JE, Ellrott BJ, Honeyfield DC (2007) Influence of egg predation and physical disturbance on lake trout Salvelinus namaycush egg mortality and implications for life-history theory. J Fish Biol 71(1):1–16

    Article  Google Scholar 

  • Fox BJ, Taylor JE, Fox MD, Williams C (1997) Vegetation changes across edges of rainforest remnants. Biol Conserv 82:1–13

    Article  Google Scholar 

  • Gherardi F, Aquiloni L, Diéguez-Uribeondo J, Tricarico E (2011) Managing invasive crayfish: is there a hope? Aquat Sci 73:185–200

    Article  Google Scholar 

  • Girdner SF, Ray AM, Buktenica MW, Hering DK, Mack JA, Umek JW (2018) Replacement of a unique population of newts (Taricha granulosa mazamae) by introduced signal crayfish (Pacifastacus leniusculus) in Crater Lake, Oregon. Biol Invasions 20:721–740

    Article  Google Scholar 

  • Glon MG, Reisinger LS, Pintor M (2018) Biogeographic differences between native and non-native populations of crayfish alter species coexistence and trophic interactions in mesocosms. Biol Invasions 20:3475–3490

    Article  Google Scholar 

  • González AL, Kominoski JS, Danger M, Ishida S, Iwai N, Rubach A (2010) Can ecological stoichiometry help explain patterns of biological invasions? Oikos 119:779–790

    Article  Google Scholar 

  • Gross R, Koiv K, Pukk L, Kaldre K (2017) Development and characterization of novel tetranucleotide microsatellite markers in the noble crayfish (Astacus astacus) suitable for highly multiplexing and for detecting hybrids between the noble crayfish and narrow-clawed crayfish (A. leptodactylus). Aquaculture 472:50–56

    Article  CAS  Google Scholar 

  • Guzzo MM, Haffner GD, Legler ND, Rush SA, Fisk AT (2013) Fifty years later: trophic ecology and niche overlap of a native and non-indigenous fish species in the western basin of Lake Erie. Biol Invasions 15:1695–1711

    Article  Google Scholar 

  • Harrisson KA, Pavlova A, Amos JN, Radford JQ, Sunnucks P (2014) Does reduced mobility through fragmented landscapes explain patch extinction patterns for three honeyeaters? J Anim Ecol 83:616–627

    Article  PubMed  Google Scholar 

  • Henttonen P, Huner JV (1999) The introduction of alien species of crayfish in Europe: a historical introduction. In: Gherardi F, Holdich DM (eds) Crayfish in Europe as alien species: how to make the best of the bad situation?. Balkema, Rotterdam, pp 13–22

    Google Scholar 

  • Hudina S, Hock K, Zganec K et al (2012) Changes in population characteristics and structure of the signal crayfish at the edge of its invasive range in a European river. Int J Limnol 48:3–11

    Article  Google Scholar 

  • Huey RB, Gilchrist GW, Hendry AP (2005) Using invasive species to study evolution: case studies with Drosophila and Salmon. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland, pp 139–164

    Google Scholar 

  • Iacarella JC, Dick JTA, Ricciardi A (2015) A spatio-temporal contrast of the predatory impact of an invasive freshwater crustacean. Divers Distrib 21:803–812

    Article  Google Scholar 

  • Jackson MC, Britton JR (2014) Divergence in the trophic niche of sympatric freshwater invaders. Biol Invasions 16:1095–1103

    Article  Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602

    Article  PubMed  Google Scholar 

  • Jackson MC, Jackson AL, Britton JR, Donohue I, Harper D, Grey J (2012) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PlosOne 7:e31757

    Article  CAS  Google Scholar 

  • Jackson MC, Evangelista C, Zhao T, Lecerf A, Britton R, Cucherousset J (2017) Between-lake variation in the trophic ecology of an invasive crayfish. Freshw Biol 62:1501–1510

    Article  Google Scholar 

  • Kamran M, Moore PA (2015) Comparative homing behaviors in two species of crayfish, Fallicambarus oodiens and Orconectes rusticus. Ethology 121:775–784

    Article  Google Scholar 

  • Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110

    Article  Google Scholar 

  • Kokko H, Koistinen L, Harlioğlu MM, Makkonen J, Aydin H, Jussila J (2012) Recovering Turkish narrow clawed crayfish (Astacus leptodactylus) populations carry Aphanomyces astaci. Knowl Manag Aquat Ecosyst 404:12

    Article  Google Scholar 

  • Kozák P, Buřič M, Policar T, Hamáčková J, Lepičová A (2007) The effect of inter-and intra-specific competition on survival and growth rate of native juvenile noble crayfish Astacus astacus and alien spiny-cheek crayfish Orconectes limosus. Hydrobiologia 590:85–94

    Article  Google Scholar 

  • Kušar D, Vrezec A, Ocepek M, Jenčič V (2013) Aphanomyces astaci in wild crayfish populations in Slovenia: first report of persistent infection in a stone crayfish Austropotamobius torrentium population. Dis Aquat Organ 103:157–169

    Article  CAS  PubMed  Google Scholar 

  • Larsson J, Jansman HA, Segelbacher G, Hoglund J, Koelewijn HP (2008) Genetic impoverishment of the last black grouse (Tetrao tetrix) population in the Netherlands: detectable only with a reference from the past. Mol Ecol 17:1897–1904

    Article  PubMed  Google Scholar 

  • Lele SF, Pârvulescu L (2019) Crayfish chelae usage suggests predominantly ambidextrous habitude. Crustaceana 92:257–267

    Article  Google Scholar 

  • Lodge DM, Deines A, Gherardi F, Yeo DC, Arcella T, Baldridge AK, Barnes MA, Chadderton WL, Feder JL, Gantz CA, Howard GW (2012) Global introductions of crayfishes: evaluating the impact of species invasions on ecosystem services. Annu Rev Ecol Evol Syst 43:449–472

    Article  Google Scholar 

  • Makkonen J, Jussila J, Kortet R, Vainikka A, Kokko H (2012) Differing virulence of Aphanomyces astaci isolates and elevated resistance of noble crayfish Astacus astacus against crayfish plague. Dis Aquat Organ 102:129–136

    Article  CAS  PubMed  Google Scholar 

  • Martín-Torrijos L, Llach MC, Pou-Rovira Q, Diéguez-Uribeondo J (2017) Resistance to the crayfish plague, Aphanomyces astaci (Oomycota) in the endangered freshwater crayfish species, Austropotamobius pallipes. Plos One 12:e0181226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messager ML, Olden JD (2019) Phenotypic variability of rusty crayfish (Faxonius rusticus) at the leading edge of its riverine invasion. Freshw Biol 64:1196–1209

    Article  CAS  Google Scholar 

  • Moyle PB, Light T (1996) Biological invasions of freshwater: empirical rules and assembly theory. Biol Cons 78:149–161

    Article  Google Scholar 

  • Nyström P, Svensson O, Lardner B, Brönmark C, Granéli W (2001) The influence of multiple introduced predators on a littoral pond community. Ecology 81:1023–1039

    Article  Google Scholar 

  • Olden JD, McCarthy JM, Maxted JT, Fetzer WW, Vander Zanden MJ (2006) The rapid spread of rusty crayfish (Orconectes rusticus) with observations on native crayfish declines in Wisconsin (USA) over the past 130 years. Biol Invasions 8:1621–1628

    Article  Google Scholar 

  • Olsson K, Nyström P, Stenroth P, Nilsson E, Svensson M, Granéli W (2008) The influence of food quality and availability on trophic position, carbon signature, and growth rate of an omnivorous crayfish. Can J Fish Aquat Sci 65:2293–2304

    Article  CAS  Google Scholar 

  • Olsson K, Stenroth P, Nyström P, Granéli W (2009) Invasions and niche width: does niche width of an introduced crayfish differ from a native crayfish? Freshw Biol 54:1731–1740

    Article  Google Scholar 

  • Ooue K, Ishiyama N, Ichimura M, Nakamura F (2019) Environmental factors affecting the invasion success and morphological responses of a globally introduced crayfish in floodplain waterbodies. Biol Invasions 21:2639–2652

    Article  Google Scholar 

  • Panteleit J, Keller NS, Makkonen J, Martín-Torrijos L, Pîrvu M, Patrulea V, Preda C, Diéguez-Uribeondo J, Schrimpf A, Pârvulescu L (2018) Hidden sites in the distribution of the crayfish plague pathogen Aphanomyces astaci in Eastern Europe: relicts of genetic groups from older outbreaks? J Invertebr Pathol 157:117–124

    Article  PubMed  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pârvulescu L, Schrimpf A, Kozubíková E, Cabanillas Resino S, Vrålstad T, Petrusek A, Schulz R (2012) Invasive crayfish and crayfish plague on the move: first detection of the plague agent Aphanomyces astaci in the Romanian Danube. Dis Aquat Organ 98:85–94

    Article  PubMed  Google Scholar 

  • Pârvulescu L, Pîrvu M, Moroşan LG, Zaharia C (2015) Plasticity in fecundity highlights the females’ importance in the spiny-cheek crayfish invasion mechanism. Zoology 118:424–432

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pintor LM, Sih A (2009) Differences in growth and foraging behavior of native and introduced populations of an invasive crayfish. Biol Invasions 11:1895–1902

    Article  Google Scholar 

  • Puky M, Schád P (2006) Orconectes limosus colonises new areas fast along the Danube in Hungary. Knowl Manag Aquat Ecosyst 380(381):919–926

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Article  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rebrina F, Skejo J, Lucić A, Hudina S (2015) Trait variability of the signal crayfish (Pacifastacus leniusculus) in a recently invaded region reflects potential benefits and trade-offs during dispersal. Aquat Invasions 10:41–50

    Article  Google Scholar 

  • Reisinger LS, Elgin AK, Towle KM, Chan DJ, Lodge DM (2017) The influence of evolution and plasticity on the behavior of an invasive crayfish. Biol Invasions 19:815–830

    Article  Google Scholar 

  • Rodriguez LF (2006) Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939

    Article  Google Scholar 

  • Schrimpf A, Pârvulescu L, Copilaş-Ciocianu D, Petrusek A, Schulz R (2012) Crayfish plague pathogen detected in the Danube Delta—a potential threat to freshwater biodiversity in southeastern Europe. Aquat Invasions 7:503–510

    Article  Google Scholar 

  • Sjödin H, Ripa J, Lundberg P (2018) Principles of niche expansion. Proc R Soc B 285(1893):20182603

    Article  PubMed  PubMed Central  Google Scholar 

  • Solarz SL, Newman RM (2001) Variation in hostplant preference and performance by the milfoil weevil, Euhrychiopsis lecontei Dietz, exposed to native and exotic watermilfoils. Oecologia 126:66–75

    Article  PubMed  Google Scholar 

  • Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374

    Article  PubMed  Google Scholar 

  • Strauss A, White A, Boots M (2012) Invading with biological weapons: the importance of disease-mediated invasions. Funct Ecol 26:1249–1261

    Article  Google Scholar 

  • Streissl F, Hödl W (2002) Growth, morphometrics, size at maturity, sexual dimorphism and condition index of Austropotamobius torrentium Schrank. Hydrobiologia 477:201–208

    Article  Google Scholar 

  • Svanbäck R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc Lond B Biol 274:839–844

    Article  Google Scholar 

  • van der Wal JE, Dorenbosch M, Immers AK, Forteza CV, Geurts JJ, Peeters ET, Koese B, Bakker ES (2013) Invasive crayfish threaten the development of submerged macrophytes in lake restoration. PLoS ONE 8:e78579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Vander-Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464

    Article  CAS  Google Scholar 

  • Watterson GA (1984) Allele frequencies after a bottleneck. Theor Popul Biol 26:387–407

    Article  Google Scholar 

  • Wauters LA, Tosi G, Gurnell J (2002) Interspecific competition in tree squirrels: do introduced grey squirrels (Sciurus carolinensis) deplete tree seeds hoarded by red squirrels (S. vulgaris)? Behav Ecol Sociobiol 51:360–367

    Article  Google Scholar 

  • Woodworth BL, Atkinson CT, LaPointe DA, Hart PJ, Spiegel CS, Tweed EJ, Henneman C, LeBrun J, Denette T, DeMots R, Kozar KL, Triglia D, Lease D, Gregor A, Smith T, Duffy D (2005) Host population persistence in the face of introduced vector-borne disease: Hawaii amakihi and avian malaria. Proc Natl Acad Sci 102:1531–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was funded by a grant from the Romanian National Authority for Scientific Research and Innovation (UEFISCDI) Project Number PN-II-RU-TE-2014-4-0785. We would like to thank Mišel Jelić for sharing information about microsatellite primers, Britta Wahl-Ermel for generating the microsatellite raw data and Lenuţa Novăcescu for help provided during field sampling campaigns.

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LP and OP conceived the study. OP, MP, LP and SFL provided field samples collection. KT and AS provided genetic data and population genetic analyses. OP provided samples preparation for stable isotope, nutrient mass, JPZ performed stable isotope and elemental analyses, OP, RS and JIJ performed statistical analyses. AA, CS and OIS measured the RNA/DNA ratio (growth rate). MP and SFL measured biometric parameters. OP, KT and LP led the writing of the manuscript. All authors contributed and approved publication.

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Correspondence to Lucian Pârvulescu.

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10530_2019_2136_MOESM1_ESM.xls

Supplementary material Annex 1: Sampling sites abbreviation, geographic location (latitude and longitude), taxonomic composition of macroinvertebrates within each sampling site, cover degree by macrophytes and presence/absence of riparian trees on the river shores. (XLS 25 kb)

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Pacioglu, O., Theissinger, K., Alexa, A. et al. Multifaceted implications of the competition between native and invasive crayfish: a glimmer of hope for the native’s long-term survival. Biol Invasions 22, 827–842 (2020). https://doi.org/10.1007/s10530-019-02136-0

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Keywords

  • Pontastacus leptodactylus
  • Faxonius limosus
  • Biological invasions
  • Invasive species
  • Populations genetics
  • Stable isotopes