Skip to main content
SpringerLink
Log in

Trophic ecology of invasive marbled and spiny-cheek crayfish populations

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

North American cambarid crayfish have been highly successful in establishing and spreading across Europe and are now over-invading earlier arrivals in many water bodies. Parthenogenetic marbled crayfish (Procambarus virginalis), which originated from aquarium stocks, are relatively recent invaders and have established in lakes previously invaded by spiny-cheek crayfish (Faxonius limosus). However, the feeding ecology of marbled crayfish and consequential impacts on the non-native species’ coexistence are largely unexplored. By combining laboratory experiments with stable isotope analyses of field samples, we were able to (1) determine food preferences of both species under controlled conditions and (2) explore their trophic niches in three lakes where both species co-occur. In the food-choice laboratory experiments, the two species showed similar food preferences and consumption rates. Consistently, the stable isotope analyses (δ13C and δ15N) highlighted the intermediate trophic position of both species. Marbled crayfish and spiny-cheek crayfish occupied a wide range of trophic positions corresponding to a very generalist diet. However, marbled crayfish were more relying on arthropod prey than spiny-cheek crayfish which fed more on mollusks. This is the first work providing evidence for trophic plasticity of marbled crayfish in lake food webs. Our results suggest that the addition of marbled crayfish increases grazing pressure on macrophytes and macrophyte-dependent organisms and the allochthonous detritus decomposition in ecosystems already invaded by spiny-cheek crayfish. Since both species are listed as invasive alien species of EU concern, further assessments of potentially endangered food organisms are needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alp M, Cucherousset J, Buoro M et al (2016) Phenological response of a key ecosystem function to biological invasion. Ecol Lett 19:519–527

    PubMed  Google Scholar 

  • Andriantsoa R, Tönges S, Panteleit J et al (2019) Ecological plasticity and commercial impact of invasive marbled crayfish populations in Madagascar. BMC Ecol 19:8

    PubMed  PubMed Central  Google Scholar 

  • Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234

    Google Scholar 

  • Baldridge AK, Lodge DM (2014) Long-term studies of crayfish-invaded lakes reveal limited potential for macrophyte recovery from the seed bank. Freshw Sci 33:788–797

    Google Scholar 

  • Bobeldyk AM, Lamberti GA (2008) A decade after invasion: evaluating the continuing effects of rusty crayfish on a Michigan river. J Great Lakes Res 34:265–275

    Google Scholar 

  • Bubb DH, O'Malley OJ, Gooderham AC et al (2009) Relative impacts of native and non-native crayfish on shelter use by an indigenous benthic fish. Aquat Conserv 19:448–455

    Google Scholar 

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453

    CAS  Google Scholar 

  • Charnov EL (1976) Optimal foraging, the marginal value theorem. Theor Popul Biol 9:129–136

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Chucholl C (2013a) Feeding ecology and ecological impact of an alien ‘warm-water’omnivore in cold lakes. Limnologica 43:219–229

    Google Scholar 

  • Chucholl C (2013b) Invaders for sale: trade and determinants of introduction of ornamental freshwater crayfish. Biol Invasions 15:125–141

    Google Scholar 

  • Chucholl C (2015) Marbled crayfish gaining ground in Europe: the role of the pet trade as invasion pathway. In: Kawai T, Faulkes Z, Scholtz G (eds) Freshwater crayfish: a global overview. CRC Press, Boca Raton, pp 83–114

    Google Scholar 

  • 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

    Google Scholar 

  • Chucholl C, Pfeiffer M (2010) First evidence for an established Marmorkrebs (Decapoda, Astacida, Cambaridae) population in Southwestern Germany, in syntopic occurrence with Orconectes limosus (Rafinesque, 1817). Aquat Invasions 5:405–412

    Google Scholar 

  • Chucholl C, Wendler F (2017) Positive selection of beautiful invaders: long-term persistence and bio-invasion risk of freshwater crayfish in the pet trade. Biol Invasions 19:197–208

    Google Scholar 

  • Correia AM (2003) Food choice by the introduced crayfish Procambarus clarkii. Ann Zool Fenn 40:517–528

    Google Scholar 

  • Cribari-Neto F, Zeileis A (2010) Beta Regression in R. J Stat Softw 34:24

    Google Scholar 

  • Doherty-Bone TM, Dunn AM, Liddell C et al (2018) Transformation of detritus by a European native and two invasive alien freshwater decapods. Biol Invasions 20:1799–1808

    PubMed  PubMed Central  Google Scholar 

  • Dorn NJ, Volin JC (2009) Resistance of crayfish (Procambarus spp.) populations to wetland drying depends on species and substrate. J N Am Benthol Soc 28:766–777

    Google Scholar 

  • Dunoyer L, Dijoux L, Bollache L et al (2014) Effects of crayfish on leaf litter breakdown and shredder prey: are native and introduced species functionally redundant? Biol Invasions 16:1545–1555

    Google Scholar 

  • Ercoli F, Ruokonen TJ, Hämäläinen H et al (2014) Does the introduced signal crayfish occupy an equivalent trophic niche to the lost native noble crayfish in boreal lakes? Biol Invasions 16:2025–2036

    Google Scholar 

  • Fischer D, Pavluvčík P, Sedláček F et al (2009) Predation of the alien American mink, Mustela vison on native crayfish in middle-sized streams in central and western Bohemia. Folia Zool 58:45–56

    Google Scholar 

  • Gherardi F (2007) Understanding the impact of invasive crayfish. In: Gherardi F (ed) Biological invaders in inland waters: profiles, distribution, and threats. Springer, Dordrecht, pp 507–542

    Google Scholar 

  • Gherardi F, Acquistapace P (2007) Invasive crayfish in Europe: the impact of Procambarus clarkii on the littoral community of a Mediterranean lake. Freshw Biol 52:1249–1259

    Google Scholar 

  • Glon M, Larson E, Pangle K (2016) Comparison of 13C and 15N discrimination factors and turnover rates between congeneric crayfish Orconectes rusticus and O. virilis (Decapoda, Cambaridae). Hydrobiologia 768:51–61

    CAS  Google Scholar 

  • Gutekunst J, Andriantsoa R, Falckenhayn C et al (2018) Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nat Ecol Evol 2:567–573

    PubMed  Google Scholar 

  • Haddaway NR, Wilcox RH, Heptonstall RE et al (2012) Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS ONE 7:e32229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haertel Borer SS, Zak D, Eckmann R et al (2005) Population density of the crayfish, Orconectes limosus, in relation to fish and macroinvertebrate densities in a small mesotrophic lake–implications for the lake's food web. Int Rev Hydrobiol 90:523–533

    Google Scholar 

  • Hendrix AN, Loftus WF (2000) Distribution and relative abundance of the crayfishes Procambarus alleni (Faxon) and P. fallax (Hagen) in southern Florida. Wetlands 20:194–199

    Google Scholar 

  • Hill AM, Lodge DM (1994) Diel changes in resource demand: competition and predation in species replacement among crayfishes. Ecology 75:2118–2126

    Google Scholar 

  • Holdich DM (2002) Crayfish in Europe–an overview of taxonomy, legislation, distribution, and crayfish plague outbreaks. In: Holdich DM, Sibley PJ (eds) Management & conservation of crayfish. Environment Agency, Bristol, pp 15–34

    Google Scholar 

  • Hossain MS, Kubec J, Kouba A et al (2019) Still waters run deep: marbled crayfish dominates over red swamp crayfish in agonistic interactions. Aquat Ecol 53:97–107

    CAS  Google Scholar 

  • Hubbell SP (2005) Neutral theory in community ecology and the hypothesis of functional equivalence. Funct Ecol 19:166–172

    Google Scholar 

  • Hudina S, Galić N, Roessink I et al (2011) Competitive interactions between co-occurring invaders: identifying asymmetries between two invasive crayfish species. Biol Invasions 13:1791–1803

    Google Scholar 

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

    PubMed  Google Scholar 

  • Jackson MC, Evangelista C, Zhao T et al (2017) Between-lake variation in the trophic ecology of an invasive crayfish. Freshw Biol 62:1501–1510

    Google Scholar 

  • Jackson MC, Grey J, Miller K et al (2016) Dietary niche constriction when invaders meet natives: evidence from freshwater decapods. J Anim Ecol 85:1098–1107

    PubMed  Google Scholar 

  • Jackson MC, Jones T, Milligan M et al (2014) Niche differentiation among invasive crayfish and their impacts on ecosystem structure and functioning. Freshw Biol 59:1123–1135

    Google Scholar 

  • James J, Thomas J, Ellis A et al (2016) Over-invasion in a freshwater ecosystem: newly introduced virile crayfish (Orconectes virilis) outcompete established invasive signal crayfish (Pacifastacus leniusculus). Mar Freshw Behav Phys 49:9–18

    Google Scholar 

  • Johnston K, Robson BJ, Fairweather PG (2011) Trophic positions of omnivores are not always flexible: evidence from four species of freshwater crayfish. Aust Ecol 36:269–279

    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

    Google Scholar 

  • Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05

    Google Scholar 

  • Kreps TA, Larson ER, Lodge DM (2016) Do invasive rusty crayfish (Orconectes rusticus) decouple littoral and pelagic energy flows in lake food webs? Freshw Sci 35:103–113

    Google Scholar 

  • Larson ER, Twardochleb LA, Olden JD (2017) Comparison of trophic function between the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii. Limnology 18:275–286

    CAS  Google Scholar 

  • Linzmaier SM, Goebel LS, Ruland F et al (2018) Behavioral differences in an over-invasion scenario: marbled vs. spiny-cheek crayfish. Ecosphere 9:e02385

    Google Scholar 

  • Lipták B, Veselý L, Ercoli F et al (2019) Trophic role of marbled crayfish in a lentic freshwater ecosystem. Aquat Invasions 14:299–309

    Google Scholar 

  • Marten M, Werth C, Marten D (2004) The Marbled crayfish (Cambaridae, Decapoda) in Germany—another neozoan in the Rhein basin. Lauterbornia 50:17–23

    Google Scholar 

  • Martin AL, Moore PA (2007) Field observations of agonism in the crayfish, Orconectes rusticus: shelter use in a natural environment. Ethology 113:1192–1201

    Google Scholar 

  • Mathers KL, Chadd RP, Dunbar MJ et al (2016) The long-term effects of invasive signal crayfish (Pacifastacus leniusculus) on instream macroinvertebrate communities. Sci Total Environ 556:207–218

    CAS  PubMed  Google Scholar 

  • McCutchan JH, Lewis WM, Kendall C et al (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    CAS  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of δ15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    CAS  Google Scholar 

  • Momot WT (1995) Redefining the role of crayfish in aquatic ecosystems. Rev Fish Sci 3:33–63

    Google Scholar 

  • Nentwig W, Bacher S, Kumschick S et al (2018) More than “100 worst” alien species in Europe. Biol Invasions 20:1611–1621

    Google Scholar 

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

    Google Scholar 

  • Ottonello D, Salvidio S, Rosecchi E (2005) Feeding habits of the European pond terrapin Emys orbicularis in Camargue (Rhône delta, Southern France). Amphibia-Reptilia 26:562–565

    Google Scholar 

  • Parkyn SM, Collier KJ, Hicks BJ (2001) New Zealand stream crayfish: functional omnivores but trophic predators? Freshw Biol 46:641–652

    Google Scholar 

  • Parnell AC, Phillips DL, Bearhop S et al (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399

    Google Scholar 

  • Phillips DL, Inger R, Bearhop S et al (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 92:823–835

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Google Scholar 

  • Post DM, Layman CA, Arrington DA et al (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    PubMed  Google Scholar 

  • Post DM, Pace ML, Hairston NG (2000) Ecosystem size determines food-chain length in lakes. Nature 405:1047–1049

    CAS  PubMed  Google Scholar 

  • Poulin B, Lefebvre G, Crivelli A (2007) The invasive red swamp crayfish as a predictor of Eurasian bittern density in the Camargue, France. J Zool 273:98–105

    Google Scholar 

  • Quezada-Romegialli C, Jackson AL, Hayden B et al (2018) tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol Evol 9:1592–1599

    Google Scholar 

  • Reynolds J, Souty-Grosset C, Richardson A (2013) Ecological roles of crayfish in freshwater and terrestrial habitats. Freshw Crayfish 19:197–218

    Google Scholar 

  • Roth BM, Hein CL, Vander Zanden MJ (2006) Using bioenergetics and stable isotopes to assess the trophic role of rusty crayfish (Orconectes rusticus) in lake littoral zones. Can J Fish Aquat Sci 63:335–344

    Google Scholar 

  • Ruokonen T, Kiljunen M, Karjalainen J et al (2012) Invasive crayfish increase habitat connectivity: a case study in a large boreal lake. Knowl Manag Aquat Ecosyst 407:08

    Google Scholar 

  • Ruokonen TJ, Karjalainen J, Hämäläinen H (2014) Effects of an invasive crayfish on the littoral macroinvertebrates of large boreal lakes are habitat specific. Freshw Biol 59:12–25

    Google Scholar 

  • Russell JC, Caut S, Anderson SH et al (2015) Invasive rat interactions and over-invasion on a coral atoll. Biol Conserv 185:59–65

    Google Scholar 

  • Russell JC, Sataruddin NS, Heard AD (2014) Over-invasion by functionally equivalent invasive species. Ecology 95:2268–2276

    PubMed  Google Scholar 

  • Sargeant BL, Gaiser EE, Trexler JC (2010) Biotic and abiotic determinants of intermediate-consumer trophic diversity in the Florida everglades. Mar Freshw Res 61:11–22

    CAS  Google Scholar 

  • Scholtz G, Braband A, Tolley L et al (2003) Ecology: Parthenogenesis in an outsider crayfish. Nature 421:806–806

    CAS  PubMed  Google Scholar 

  • Seebens H, Blackburn TM, Dyer EE et al (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:14435

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siesa ME, Padoa-Schioppa E, Ott J et al (2014) Assessing the consequences of biological invasions on species with complex life cycles: impact of the alien crayfish Procambarus clarkii on Odonata. Ecol Indic 46:70–77

    Google Scholar 

  • Souty-Grosset C, Holdich DM, Noël PY et al (2006) Atlas of crayfish in Europe. Muséum national d'Histoire naturelle, Paris

    Google Scholar 

  • Stenroth P, Holmqvist N, Nyström P et al (2006) Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment, and season. Can J Fish Aquat Sci 63:821–831

    CAS  Google Scholar 

  • Stites AJ, Taylor CA, Kessler EJ (2017) Trophic ecology of the North American crayfish genus Barbicambarus Hobbs, 1969 (Decapoda: Astacoidea: Cambaridae): evidence for a unique relationship between body size and trophic position. J Crustacean Biol 37:263–271

    Google Scholar 

  • Stock BC, Jackson AL, Ward EJ et al (2018) Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6:e5096

    PubMed  PubMed Central  Google Scholar 

  • Taylor CA, Soucek DJ (2010) Re-examining the importance of fish in the diets of stream-dwelling crayfishes: implications for food web analyses and conservation. Am Midl Nat 163:280–293

    Google Scholar 

  • Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci 101:10854–10861

    CAS  PubMed  Google Scholar 

  • Trudeau A (2018) Impact of lake characteristics on foraging niches, size structure, and abundance of Eurasian perch (Perca fluviatilis): a comparative study across German gravel pit lakes. Albrecht Daniel Thaer-Institute of Agricultural and Horticultural Sciences. Master thesis. Humboldt University of Berlin, Berlin

  • Usio N, Townsend CR (2002) Functional significance of crayfish in stream food webs: roles of omnivory, substrate heterogeneity and sex. Oikos 98:512–522

    Google Scholar 

  • Vadeboncoeur Y, Vander Zanden MJ, Lodge DM (2002) Putting the lake back together: reintegrating benthic pathways into lake food web models. Bioscience 52:44–54

    Google Scholar 

  • van der Wal JE, Dorenbosch M, Immers AK et al (2013) Invasive crayfish threaten the development of submerged macrophytes in lake restoration. PLoS ONE 8:e78579

    PubMed  PubMed Central  Google Scholar 

  • VanArman PG (2011) Role of native crayfish, Procambarus alleni (Faxon) and Procambarus fallax (Hagen), in everglades food webs: a literature review and conceptual model. Fla Sci 74:100–125

    Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404

    Google Scholar 

  • Vogt G, Dorn NJ, Pfeiffer M, et al. (2018) In-depth investigation of the species problem and taxonomic status of marbled crayfish, the first asexual decapod crustacean. bioRxiv:356170

Download references

Acknowledgements

We thank Michael Pfeiffer and Christoph Chucholl for sharing their knowledge on crayfish and helping us in the field. We further thank Larissa Goebel for taking care of the crayfish and assisting us during the study. Finally, we thank Sofia Schütt, Robert Nikolaus, Alban Sagouis and Jorrit Lucas for their help during sampling and Ashley Trudeau for her support in the lab. Furthermore, we would like to thank Robert Arlinghaus for providing additional data. SL and JJ were financially supported by IGB and the Deutsche Forschungsgemeinschaft (DFG; JE 288/9-1, JE 288/9-2). CM was funded by the German Federal Ministry of Education and Research BMBF within the Collaborative Project ‘Bridging in Biodiversity Science—BIBS’ (Funding Number 01LC1501A-H). SM was jointly financed by the German Federal Ministry of Education and Research (BMBF) and the German Federal Agency for Nature Conservation (BfN) with funds granted by the German Federal Ministry for the Environment, Nature Conservation and Nuclear Safety (BMU; Grant Number: 01LC1320A; www.baggersee-forschung.de).

Author information

Authors and Affiliations

  1. Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 310, 12587, Berlin, Germany

    Stefan M. Linzmaier, Camille Musseau, Sven Matern & Jonathan M. Jeschke

  2. Department of Biology, Chemistry, Pharmacy, Institute of Biology, Freie Universität Berlin, Königin-Luise-Str. 1-3, 14195, Berlin, Germany

    Stefan M. Linzmaier, Camille Musseau & Jonathan M. Jeschke

  3. Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Königin-Luise-Str. 2-4, 14195, Berlin, Germany

    Stefan M. Linzmaier, Camille Musseau & Jonathan M. Jeschke

  4. Devision for Integrative Fisheries Management, Albrecht Daniel Thaer-Institute of Agriculture and Horticulture, Faculty of Life Science, Humboldt-Universität zu Berlin, Philippstr. 13, Haus 7, 10155, Berlin, Germany

    Sven Matern

Authors
  1. Stefan M. Linzmaier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camille Musseau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sven Matern
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan M. Jeschke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefan M. Linzmaier.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Appendix

Appendix

See Tables 4, 5 and Fig. 4.

Table 4 Pairwise comparisons of posterior trophic positions and Post’s (2002) α (littoral reliance)
Full size table
Table 5 Posterior trophic position estimates and posterior alpha (α) estimates for marbled crayfish (M) and spiny-cheek crayfish (S) populations from Bayesian Models with two different sets of trophic discrimination factors (median and [95% credibility interval]) and parametric trophic position estimates (± standard deviation) according to Post (2002)
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Linzmaier, S.M., Musseau, C., Matern, S. et al. Trophic ecology of invasive marbled and spiny-cheek crayfish populations. Biol Invasions 22, 3339–3356 (2020). https://doi.org/10.1007/s10530-020-02328-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-020-02328-z

Keywords

Search

Navigation