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Comparison of trophic function between the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii

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Abstract

Impacts of invasive species may manifest most strongly if these organisms are highly distinct functionally from the native species they often replace. Yet, should we expect functional differences between native and invasive species of generalist organisms like freshwater crayfish? Some existing evidence has pointed to native and invasive crayfish species as ecologically equivalent. We contribute to this literature by comparing the trophic niches of the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii, by applying carbon and nitrogen stable isotope analyses to replicated allopatric (alone) and sympatric (together) lake populations in western Washington State, USA, where P. clarkii has been recently introduced and P. leniusculus is presumed native. Our study corrected for potential inherent differences in lake food webs as a consequence of lake abiotic or biotic characteristics using random effects in linear mixed effects models. We found that although overall trophic niche size or area of these species was not significantly different, P. leniusculus was significantly higher in trophic position than P. clarkii when also accounting for the effects of body size, sex, and lakes as random effects. This pattern of increased trophic position of P. leniusculus over P. clarkii was conserved over time in one sympatric lake for which we had data over multiple years. Cumulatively, our findings point to trophic differences between the globally cosmopolitan crayfishes P. leniusculus and P. clarkii, particularly when accounting for the ways that ecosystem context can affect food web structure of communities and the trophic resources available to these consumers.

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References

  • Alberti M, Booth D, Hill K, Coburn B, Avolio C, Coe S, Spirandelli D (2007) The impact of urban patterns on aquatic ecosystems: an empirical analysis in Puget lowland sub-basins. Landsc Urban Plan 80:345–361

    Article  Google Scholar 

  • Alp M, Cucherousset J, Buoro M, Lecerf A (2016) Phenological response of a key ecosystem function to biological invasion. Ecol Lett. doi:10.1111/ele.12585

    PubMed  Google Scholar 

  • Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst 42:411–440

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Bondar CA, Bottriell K, Zeron K, Richardson JS (2005) Does trophic position of the omnivorous signal crayfish (Pacifastacus leniusculus) in a stream food web vary with life history stage or density? Can J Fish Aquat Sci 62:2632–2639

    Article  Google Scholar 

  • Bortleson GC, Dion NP, McConnell JB, Nelson LM (1976) Reconnaissance data on lakes in Washington. Washington Department of Ecology, Tacoma

    Google Scholar 

  • Bouchard RW (1977) Distribution, systematic status and ecological notes on five poorly known species of crayfishes in western North America (Decapoda: Astacidae and Cambaridae). Freshw Crayfish 3:409–423

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Carolan JV, Mazumder D, Dimovski C, Diocares R, Twining J (2012) Biokinetics and discrimination factors for δ13C and δ15N in the omnivorous freshwater crustacean, Cherax destructor. Mar Freshw Res 63:878–886

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Collins NC, Harvey HH, Tierney AJ, Dunham DW (1983) Influence of predatory fish density on trapability of crayfish in Ontario lakes. Can J Fish Aquat Sci 40:1820–1828

    Article  Google Scholar 

  • Comte L, Cucherousset J, Olden JD (2016) Global test of Eltonian niche conservatism of nonnative freshwater fish species between their native and introduced ranges. Ecography. doi:10.1111/ecog.02007

    Google Scholar 

  • Dorn NJ, Mittelbach GG (2004) Effects of a native crayfish (Orconectes virilis) on the reproductive success and nesting behavior of sunfish (Lepomis spp.). Can J Fish Aquat Sci 61:2135–2143

    Article  Google Scholar 

  • Dorn NJ, Wojdak JM (2004) The role of omnivorous crayfish in littoral communities. Oecologia 140:150–159

    Article  PubMed  Google Scholar 

  • Edwards BA, Jackson DA, Somers KM (2013) Linking temporal changes in crayfish communities to environmental changes in boreal Shield lakes in south-central Ontario. Can J Fish Aquat Sci 71:21–30

    Article  Google Scholar 

  • Ercoli F, Ruokonen TJ, Hämäläinen H, Jones RI (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

    Article  Google Scholar 

  • Ercoli F, Ruokonen TJ, Erkamo E, Jones RI, Hämäläinen H (2015) Comparing the effects of introduced signal crayfish and native noble crayfish on the littoral invertebrate assemblages of boreal lakes. Freshw Sci 34:555–563

    Article  Google Scholar 

  • Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Chang Biol 22:151–163

    Article  PubMed  Google Scholar 

  • Gamradt SC, Kats LB (1996) Effect of introduced crayfish and mosquitofish on California newts. Conserv Biol 10:1155–1162

    Article  Google Scholar 

  • Geiger W, Alcorlo P, Baltanas A, Montes C (2005) Impact of an introduced crustacean on the trophic webs of Mediterranean wetlands. In: Capdevila-Argüelles L, Zilletti B (eds) Issues in bioinvasion science. Springer, Heidelberg, pp 49–73

    Chapter  Google Scholar 

  • Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Freshw Behav Physiol 39:175–191

    Article  Google Scholar 

  • Glon MG, Larson ER, Pangle KL (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

    Article  CAS  Google Scholar 

  • Gutiérrez-Yurrita PJ, Sancho G, Bravo MA, Baltanás A, Montes C (1998) Diet of the red swamp crayfish Procambarus clarkii in natural ecosystems of the Doñana National Park temporary fresh-water marsh (Spain). J Crustac Biol 18:120–127

    Article  Google Scholar 

  • Hansen GJ, Vander Zanden MJ, Blum MJ, Clayton MK, Hain EF, Hauxwell J, Izzo M, Kornis MS, McIntyre PB, Mikulyuk A, Nilsson E, Olden JD, Papeş M, Sharma S (2013) Commonly rare and rarely common: comparing population abundance of invasive and native aquatic species. PLoS One 8:e77415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanshew BA, Garcia TS (2012) Invasion of the shelter snatchers: behavioural plasticity in invasive red swamp crayfish, Procambarus clarkii. Freshw Biol 57:2285–2296

    Article  Google Scholar 

  • Harvey GL, Moorhouse TP, Clifford NJ, Henshaw AJ, Johnson MF, Macdonald DW, Reid I, Rice S (2011) Evaluating the role of invasive aquatic species as drivers of fine sediment-related river management problems: the case of the signal crayfish (Pacifastacus leniusculus). Prog Phys Geogr 35:517–533

    Article  Google Scholar 

  • Hauser CE, McCarthy MA (2009) Streamlining ‘search and destroy’: cost-effective surveillance for invasive species management. Ecol Lett 12:683–692

    Article  PubMed  Google Scholar 

  • Hobbs HH, Jass JP, Huner JV (1989) A review of global crayfish introductions with particular emphasis on two North American species (Decapoda, Cambaridae). Crustaceana 56:299–316

    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, 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. Freshw Biol 59:1123–1135

    Article  Google Scholar 

  • James J, Slater FM, Vaughan IP, Young KA, Cable J (2014) Comparing the ecological impacts of native and invasive crayfish: could native species’ translocation do more harm than good? Oecologia 178:309–316

    Article  PubMed  Google Scholar 

  • James J, Davidson KE, Richardson G, Grimstead C, Cable J (2015) Reduced aggression and foraging efficiency of invasive signal crayfish (Pacifastacus leniusculus) infested with non-native branchiobdellidans (Annelida: Clitellata). Parasit Vectors 8:1–9

    Article  Google Scholar 

  • Johnson BL, Willacker JJ, Eagles-Smith CA, Pearl CA, Adams MJ (2014) Invasive crayfish as vectors of mercury in freshwater food webs of the Pacific Northwest. Environ Toxicol Chem 33:2639–2645

    Article  CAS  PubMed  Google Scholar 

  • Jussila J, Ruokonen TJ, Syväranta J, Kokko H, Vainikka A, Makkonen J, Korter R (2015a) It takes time to see the menu from the body: an experiment on stable isotope composition in freshwater crayfishes. Knowl Manag Aquat Ecosyst 416:25

    Article  Google Scholar 

  • Jussila J, Vrezec A, Makkonen J, Kortet R, Kokko H (2015b) Invasive crayfish and their invasive diseases in Europe with the focus on the virulence evolution of the crayfish plague. In: Canning-Clode J (ed) Biological invasions in changing ecosystems: vectors, ecological impacts, management and predictions. De Gruyter Open, Berlin, pp 183–211

    Google Scholar 

  • Kobayashi R, Maezono Y, Miyashita T (2011) The importance of allochthonous litter input on the biomass of an alien crayfish in farm ponds. Popul Ecol 53:525–534

    Article  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

    Article  Google Scholar 

  • Kumschick S, Gaertner M, Vilà M, Essl F, Jeschke JM, Pyšek P, Ricciard A, Bacher S, Blackburn TM, Dick JTA, Evans T, Hulme PE, Kühn I, Mrugata A, Pergl J, Rabitsch W, Richardson DM, Sendek A, Winter M (2015) Ecological impacts of alien species: quantification, scope, caveats, and recommendations. Bioscience 65:55–63

    Article  Google Scholar 

  • Larson ER, Olden JD (2012) Using avatar species to model the potential distribution of emerging invaders. Glob Ecol Biogeogr 21:1114–1125

    Article  Google Scholar 

  • Larson ER, Olden JD (2013) Crayfish occupancy and abundance in lakes of the Pacific Northwest, USA. Freshw Sci 32:94–107

    Article  Google Scholar 

  • Larson ER, Olden JD, Usio N (2010) Decoupled conservatism of Grinnellian and Eltonian niches in an invasive arthropod. Ecosphere 1:1–13 (Article16)

    Article  Google Scholar 

  • Larson ER, Olden JD, Usio N (2011) Shoreline urbanization interrupts allochthonous subsidies to a benthic consumer over a gradient of lake size. Biol Lett 7:551–554

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Layman CA, Quattrochi JP, Peyer CM, Allgeier JE (2007) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett 10:937–944

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lodge DM, Stein RA, Brown KM, Covich AP, Bronmark C, Garvey JE, Klosiewski SP (1998) Predicting impact of freshwater exotic species on native biodiversity: challenges in spatial scaling. Aust J Ecol 23:53–67

    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, Jerde CL, Peters BW, Peters JA, Sargent LW, Turner CR, Wittmann ME, Zeng Y (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 

  • Machida Y, Akiyama YB (2013) Impacts of invasive crayfish (Pacifastacus leniusculus) on endangered freshwater pearl mussels (Margaritifera laevis and M. togakushiensis) in Japan. Hydrobiologia 720:145–151

    Article  Google Scholar 

  • Magoulick DD (2014) Impacts of drought and crayfish invasion on stream ecosystem structure and function. River Res Appl 30:1309–1317

    Article  Google Scholar 

  • Magoulick DD, Piercey GL (2016) Trophic overlap between native and invasive stream crayfish. Hydrobiologia 766:237–246

    Article  Google Scholar 

  • Matsuzaki SS, Usio N, Takamura N, Washitani I (2009) Contrasting impacts of invasive engineers on freshwater ecosystems: an experiment and meta-analysis. Oecologia 158:673–686

    Article  PubMed  Google Scholar 

  • Matsuzaki SS, Sakamoto M, Kawabe K, Takamura N (2012) A laboratory study of the effects of shelter availability and invasive crayfish on the growth of native stream fish. Freshw Biol 57:874–882

    Article  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15 N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Moore JW, Carlson SM, Twardochleb LA, Hwan JL, Fox JM, Hayes SA (2012) Trophic tangles through time? Opposing direct and indirect effects of an invasive omnivore on stream ecosystem processes. PLoS One 7:e50687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller KW (2001) First record of the red swamp crayfish, Procambarus clarkii (Girard, 1852) (Decapoda, Cambaridae), from Washington state, USA. Crustaceana 74:1003–1007

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nilsson E, Solomon CT, Wilson KA, Willis TV, Larget B, Vander Zanden MJ (2012) Effects of an invasive crayfish on trophic relationships in north-temperate lake food webs. Freshw Biol 57:10–23

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: community ecology package. R package version 2.4-0. http://CRAN.R-project.org/package=vegan. Accessed 8 Jan 2016

  • Olden JD, Larson ER, Mims MC (2009) Home-field advantage: native signal crayfish (Pacifastacus leniusculus) out consume newly introduced crayfishes for invasive Chinese mystery snail (Bellamya chinensis). Aquat Ecol 43:1073–1084

    Article  Google Scholar 

  • Olden JD, Ray L, Mims MC, Horner-Devine MC (2013) Filtration rates of the non-native Chinese mystery snail (Bellamya chinensis) and potential impacts on microbial commuties. Limnetica 32:107–120

    Google Scholar 

  • Olsen TM, Lodge DM, Capelli GM, Houlihan RJ (1991) Mechanisms of impact of an introduced crayfish (Orconectes rusticus) on littoral congeners, snails, and macrophytes. Can J Fish Aquat Sci 48:1853–1861

    Article  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 

  • Parnell A, Jackson A (2013) siar: stable isotope analysis in R. R package version 4.2. http://CRAN.R-project.org/package=siar. Accessed 8 Jan 2016

  • Pearl CA, Adams MJ, McCreary B (2013) Habitat and co-occurrence of native and invasive crayfish in the Pacific Northwest, USA. Aquat Invasions 8:171–184

    Article  Google Scholar 

  • Peters JA, Lodge DM (2013) Habitat, predation, and coexistence between invasive and native crayfishes: prioritizing lakes for invasion prevention. Biol Invasions 15:2489–2502

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-128. http://CRAN.R-project.org/package=nlme. Accessed 8 Jan 2016

  • Pintor LM, Sih A, Bauer ML (2008) Differences in aggression, activity and boldness between native and introduced populations of an invasive crayfish. Oikos 117:1629–1636

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org. Accessed 8 Jan 2016

  • Reisinger LS, Petersen I, Hing JS, Davila RL, Lodge DM (2015) Infection with a trematode parasite differentially alters competitive interactions and antipredator behaviour in native and invasive crayfish. Freshw Biol 60:1581–1595

    Article  Google Scholar 

  • Renai B, Gherardi F (2004) Predatory efficiency of crayfish: comparison between indigenous and non-indigenous species. Biol Invasions 6:89–99

    Article  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 

  • 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

    Article  Google Scholar 

  • Stenroth P, Holmqvist N, Nyström P, Berglund O, Larsson P, Granéli W (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

    Article  CAS  Google Scholar 

  • Syväranta J, Lensu A, Marjomäki TJ, Oksanen S, Jones RI (2013) An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. PLoS One 8:e56094

    Article  PubMed  PubMed Central  Google Scholar 

  • Twardochleb LA, Olden JD (2016) Human development modifies the functional composition of lake littoral invertebrate communities. Hydrobiologia. doi:10.1007/s10750-016-2727-5

    Google Scholar 

  • Twardochleb LA, Olden JD, Larson ER (2013) A global meta-analysis of the ecological impacts of nonnative crayfish. Freshw Sci 32:1367–1382

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Usio N, Suzuki K, Konishi M, Nakano S (2006) Alien vs. endemic crayfish: roles of species identity in ecosystem functioning. Archiv für Hydrobiol 166:1–21

    Article  CAS  Google Scholar 

  • Usio N, Nakata K, Kawai T, Kitano S (2007) Distribution and control status of the invasive signal crayfish (Pacifastacus leniusculus) in Japan. Jpn J Limnol 68:471–482

    Article  Google Scholar 

  • Usio N, Imada M, Nakagawa M, Akasaka M, Takamura N (2013) Effects of pond draining on biodiversity and water quality of farm ponds. Conserv Biol 27:1429–1438

    Article  PubMed  Google Scholar 

  • Vander Zanden MJ, Casselman JM, Rasmussen JB (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467

    Article  CAS  Google Scholar 

  • Vander Zanden MJ, Clayton MK, Moody EK, Solomon CT, Weidel BC (2015) Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLoS One 10:e0116182

    Article  PubMed  PubMed Central  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Evol Syst 33:475–505

    Article  Google Scholar 

  • Wood KA, Hayes RB, England J, Grey J (2016) Invasive crayfish impacts on native fish diet and growth vary with fish life stage. Aquat Sci. doi:10.1007/s00027-016-0483-2

    Google Scholar 

  • Yokomizo H, Possingham HP, Thomas MB, Buckley YM (2009) Managing the impact of invasive species: the value of knowing the density-impact curve. Ecol Appl 19:376–386

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the University of Washington School of Aquatic and Fishery Sciences and H. Mason Keeler Endowed Professorship to Julian Olden, as well as the Oregon Zoo Future for Wildlife Grants Program. Francis Lin and Kerry Ung provided field assistance through sponsorship by the American Fisheries Society Hutton Junior Fisheries Biology Program. Thomas Pool contributed to additional field sampling, and Mariana Tamayo helped compile lake attribute data. This manuscript was improved by comments from several anonymous reviewers.

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Correspondence to Eric R. Larson.

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Larson, E.R., Twardochleb, L.A. & Olden, J.D. Comparison of trophic function between the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii . Limnology 18, 275–286 (2017). https://doi.org/10.1007/s10201-016-0505-8

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