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The influence of evolution and plasticity on the behavior of an invasive crayfish

Biological Invasions volume 19, pages 815–830 (2017)Cite this article

Abstract

Invasion success can be enhanced by evolution and behavioral plasticity, but the importance of these processes for most invasions is not well understood. Previous research suggests there is a genetic basis for differences in growth rate between native and invaded range rusty crayfish (Orconectes rusticus). We hypothesized that invaded range O. rusticus achieve faster growth by allocating more time to foraging and less to defense. We conducted a laboratory experiment to test the effects of range (native or invaded) and plasticity (as induced by exposure to predators) on crayfish behavior. We collected O. rusticus adults and eggs from both ranges, hatched eggs in the lab, and reared juveniles in common conditions either with or without predatory fish. We then quantified adult and juvenile crayfish activity in an experiment with and without predatory fish. In support of our hypothesis, invaded range adults displayed reduced antipredator behavior compared to native range adults. Further, invaded range juveniles were more active than native range juveniles without predators, but all juveniles were inactive with predators. In addition, invaded range juveniles had greater plasticity in behavior than native range juveniles. These results suggest that activity level in the absence of predators has diverged in the invaded range. Because active crayfish consume more prey, this change in behavior may be responsible for rapid growth in the invaded range of O. rusticus, a trait that contributes to the strong ecological impacts of this invasive crayfish.

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References

  • Baldridge AK, Smith LD (2008) Temperature constraints on phenotypic plasticity explain biogeographic patterns in predator trophic morphology. Mar Ecol Prog Ser 365:25–34

    Article  Google Scholar 

  • Baldridge AK, Lodge DM (2013) Intraguild predation between spawning smallmouth bass (Micropterus dolomieu) and nest-raiding crayfish (Orconectes rusticus): implications for bass nesting success. Freshw Biol 58:2355–2365

    Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants—a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Boschung HT, Williams JD, Gotshall DW, Caldwell DK, Caldwell MC, Nehring C, Verner J (1983) The Audubon Society field guide to North American fishes, whales, and dolphins. Alfred A. Knopf, New York

    Google Scholar 

  • Bossdorf O, Prati D, Auge H, Schmid B (2004) Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353

    Article  Google Scholar 

  • Bruski CA, Dunham DW (1987) The importance of vision in agonistic communication of the crayfish Orconectes rusticus: an analysis of bout dynamics. Behaviour 103:83–107

    Article  Google Scholar 

  • Burton OJ, Phillips BL, Travis JMJ (2010) Trade-offs and the evolution of life-histories during range expansion. Ecol Lett 13:1210–1220

    Article  PubMed  Google Scholar 

  • Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40

    Article  Google Scholar 

  • Colautti RI, Barrett SCH (2013) Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342:364–366

    Article  CAS  PubMed  Google Scholar 

  • Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017

    Article  PubMed  Google Scholar 

  • Cousyn C, De Meester L, Colbourne JK, Brendonck L, Verschuren D, Volckaert F (2001) Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proc Natl Acad Sci 98:6256–6260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox GW (2004) Alien species and evolution. Island Press, Washington, DC

    Google Scholar 

  • Crawley MJ (1987) What makes a community invasible? In: Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell Scientific Publications, Oxford, pp 429–453

    Google Scholar 

  • Cripps MG, Hinz HL, McKenney JL, Price WJ, Schwarzlander M (2009) No evidence for an ‘evolution of increased competitive ability’ for the invasive Lepidium draba. Basic Appl Ecol 10:103–112

    Article  Google Scholar 

  • Crispo E (2010) The evolution of phenotypic plasticity in response to anthropogenic disturbance. Evol Ecol Res 12:47–66

    Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flory SL, Long FR, Clay K (2011) Invasive Microstegium populations consistently outperform native range populations across diverse environments. Ecology 92:2248–2257

    Article  PubMed  Google Scholar 

  • Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 58:831–833

    Article  Google Scholar 

  • Garvey JE, Stein RA, Thomas HM (1994) Assessing how fish predation and interspecific prey competition influence a crayfish assemblage. Ecology 75:532–547

    Article  Google Scholar 

  • Ghalambor ACK, Mckay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. Univeristy of Chicago Press, Chicago

    Google Scholar 

  • Hay WP (1896) The crawfishes of the state of Indiana. In: 20th annual report of the Department of Geology and Natural Resources of Indiana

  • Hendry AP (2016) Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J Hered 107:25–41

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hill AM, Sinars DM, Lodge DM (1993) Invasion of an occupied niche by the crayfish Orconectes rusticus—potential importance of growth and mortality. Oecologia 94:303–306

    Article  Google Scholar 

  • Huey RB, Gilchrist GW, Hendry AP (2005) Using invasive species to study evolution: case studies of drosophila and salmon. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Kuznetsova A, Bruun Brockhoff P, Bojesen Christensen RH (2015) lmerTest: tests in linear mixed effects models. R package version 2.0-29. http://CRAN.R-project.org/package=lmerTest

  • Lamarque LJ, Delzon S, Lortie CJ (2011) Tree invasions: a comparative test of the dominant hypotheses and functional traits. Biol Invasions 13:1969–1989

    Article  Google Scholar 

  • Lodge DM, Taylor CA, Holdich DM, Skurdal J (2000) Nonindigenous crayfishes threaten North American freshwater biodiversity: lessons from Europe. Fisheries 25:21–25

    Article  Google Scholar 

  • Lodge DM, Deines A, Gherardi F, Yeo DCJ, 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 YW (2012) Global introductions of crayfishes: evaluating the impact of species invasions on ecosystem services. Ann Rev Ecol Evol Syst 43:449–472

    Article  Google Scholar 

  • Peters B (2010) Evaluating strategies for controlling invasive crayfish using human and fish predation. MS Thesis, Biological Sciences, University of Notre Dame, Notre Dame

  • Phillips BL, Brown GP, Shine R (2010) Life-history evolution in range-shifting populations. Ecology 91:1617–1627

    Article  PubMed  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 

  • 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 

  • Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc B 270:1433–1440

    Article  PubMed  PubMed Central  Google Scholar 

  • Roth BM, Tetzlaff JC, Alexander ML, Kitchell JF (2007) Reciprocal relationships between exotic rusty crayfish, macrophytes, and Lepomis species in northern Wisconsin lakes. Ecosystems 10:74–85

    Article  Google Scholar 

  • Roughgarden J (1971) Density-dependent natural selection. Ecology 52:453–468

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Evol Syst 32:305–332

    Article  Google Scholar 

  • Sargent LW, Lodge DM (2014) Evolution of invasive traits in nonindigenous species: increased survival and faster growth in invasive populations of rusty crayfish (Orconectes rusticus). Evol Appl 7:949–961

    Article  PubMed  PubMed Central  Google Scholar 

  • Sargent LW, Baldridge AK, Vega-Ross M, Towle KM, Lodge DM (2014) A trematode parasite alters growth, feeding behavior, and demographic success of invasive rusty crayfish (Orconectes rusticus). Oecologia 175:947–958

    Article  PubMed  Google Scholar 

  • Savolainen R, Westman K, Pursiainen M (1997) Fecundity of Finnish noble crayfish, Astacus, and signal crayfish, Pacifastacus leniusculus (Dana), females in various natural habitats and in culture in Finland. Freshw Crayfish 11:319–338

    Google Scholar 

  • Shine R, Brown GP, Phillips BL (2011) An evolutionary process that assembles phenotypes through space rather than through time. Proc Natl Acad Sci 108(14):5708–5711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skurdal J, Hessen DO, Garnas E, Vollestad LA (2011) Fluctuating fecundity parameters and reproductive investment in crayfish: driven by climate or chaos? Freshw Biol 56:335–341

    Article  Google Scholar 

  • Sol D, Lefebvre L (2000) Behavioural flexibility predicts invasion success in birds introduced to New Zealand. Oikos 90:599–605

    Article  Google Scholar 

  • Stein RA (1977) Selective predation, optimal foraging, and the predator-prey interaction between fish and crayfish. Ecology 58:1237–1253

    Article  Google Scholar 

  • Stein RA, Magnuson JJ (1976) Behavioral response of crayfish to a fish predator. Ecology 57:751–761

    Article  Google Scholar 

  • Taylor CA (2000) Systematic studies of the Orconectes juvenilis complex (Decapoda: Cambaridae), with descriptions of two new species. J Crust Biol 20:132–152

    Article  Google Scholar 

  • Thoma RF, Jezerinac RF (2000) Ohio crayfish and shrimp atlas. The Ohio State University Press, Clumbus

    Google Scholar 

  • United States Geological Survey (2015) Nonindigenous aquatic species database. Washington, DC http://nas.er.usgs.gov/queries/speciesmap.aspx?SpeciesID=214

  • van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    Article  PubMed  Google Scholar 

  • Wilson KA, Magnuson JJ, Lodge DM, Hill AM, Kratz TK, Perry WL, Willis TV (2004) A long-term rusty crayfish (Orconectes rusticus) invasion: dispersal patterns and community change in a north temperate lake. Can J Fish Aquat Sci 61:2255–2266

    Article  Google Scholar 

  • Wooster D, Sih A (1995) A review of the drift and activity responses of stream prey to predator presence. Oikos 73:3–8

    Article  Google Scholar 

  • Wright TF, Eberhard JR, Hobson EA, Avery ML, Russello MA (2010) Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethol Ecol Evol 22:393–404

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Tracy Arcella and Iris Petersen for help with crayfish collection and raising juveniles. We also appreciate helpful comments on the manuscript from two anonymous reviewers. We are grateful to the University of Wisconsin’s Trout Lake Research Station for providing space for experiments. Funding for this research was provided by the University of Notre Dame Environmental Research Center and National Science Foundation Grant award #0504495 to the Global Linkages of Biology, Environment, and Society graduate training program at the University of Notre Dame. This is a publication of the Notre Dame Environmental Change Initiative and is Great Lakes Environmental Research Laboratory Contribution No. 1829.

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  1. Lindsey S. Reisinger

    Present address: Institute for Great Lakes Research, Central Michigan University, Mount Pleasant, MI, 48859, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Notre Dame, 100 Galvin Life Sciences Center, Notre Dame, IN, 46556, USA

    Lindsey S. Reisinger, Ashley K. Elgin, Kevin M. Towle & David J. Chan

  2. Environmental Change Initiative and Department of Biological Sciences, University of Notre Dame, 100 Galvin Life Sciences Center, Notre Dame, IN, 46556, USA

    David M. Lodge

  3. National Oceanic and Atmospheric Administration, Great Lakes Environmental Research Laboratory, 4840 S State Rd, Ann Arbor, MI, 48108, USA

    Ashley K. Elgin

  4. Atkinson Center for a Sustainable Future and Department of Ecology and Evolutionary Biology, Cornell University, 200 Rice Hall, Ithaca, NY, 14853, USA

    David M. Lodge

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Correspondence to Lindsey S. Reisinger.

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Reisinger, L.S., Elgin, A.K., Towle, K.M. et al. The influence of evolution and plasticity on the behavior of an invasive crayfish. Biol Invasions 19, 815–830 (2017). https://doi.org/10.1007/s10530-016-1346-4

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  • DOI: https://doi.org/10.1007/s10530-016-1346-4

Keywords

  • Invasive species
  • Feeding
  • Predation
  • Foraging rate
  • Antipredator behavior
  • Behavioral plasticity