Divergence in foraging and predator avoidance behavior across the geographic range of native and non-native crayfish

Abstract

There is growing evidence that species’ traits may diverge during biological invasions; however, we still lack a general understanding of how the invasion process affects behavior. We used a biogeographic approach to compare foraging and antipredator behavior across a reciprocal invasion (in which each species invaded the native range of the other) of virile (Faxonius virilis) and rusty crayfish (F. rusticus). We hypothesized that the invasion process would select for individuals that invest more in foraging and less in defense than their native counterparts. We used laboratory experiments to examine crayfish boldness, activity, and foraging voracity and mesocosm experiments to examine antipredator behavior in response to fish. Non-native virile crayfish (Indiana, USA) were less bold, active and voracious than native virile crayfish (Wisconsin, USA), and they exhibited more antipredator behavior. Non-native rusty crayfish (Wisconsin) were more active in mesocosms and exhibited less antipredator behavior than native rusty crayfish (Indiana). Combined, these findings suggest a growth/mortality trade-off. Counter to our hypothesis, relative investment in foraging versus predator avoidance differed across regions and was not consistently associated with native or invasive populations. Thus, the substantial divergence in behavior we observed may by driven by local adaptation.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Baldridge, A. K. & L. D. Smith, 2008. Temperature constraints on phenotypic plasticity explain biogeographic patterns in predator trophic morphology. Marine Ecology Progress Series 365: 25–34.

    Google Scholar 

  2. Bassar, R. D., M. C. Marshall, A. López-Sepulcre, E. Zandonà, S. K. Auer, J. Travis, C. M. Pringle, A. S. Flecker, S. A. Thomas, D. F. Fraser, D. N. Reznick, A. Lopez-Sepulcre, E. Zandona, S. K. Auer, J. Travis, C. M. Pringle, A. S. Flecker, S. A. Thomas, D. F. Fraser & D. N. Reznick, 2010. Local adaptation in Trinidadian guppies alters ecosystem processes. Proceedings of the National Academy of Sciences of the United States of America 107: 3616–3621.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Bates, D., M. Maechler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Google Scholar 

  4. Biro, P. A. & J. A. Stamps, 2008. Are animal personality traits linked to life-history productivity? Trends in Ecology and Evolution 23: 361–368.

    PubMed  PubMed Central  Google Scholar 

  5. Biro, P. A., M. V. Abrahams, J. R. Post & E. A. Parkinson, 2006. Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. Journal of Animal Ecology 75: 1165–1171.

    PubMed  PubMed Central  Google Scholar 

  6. Biro, P. A., M. V. Abrahams & J. R. Post, 2007. Direct manipulation of behaviour reveals a mechanism for variation in growth and mortality among prey populations. Animal Behaviour 73: 891–896.

    Google Scholar 

  7. Biro, P. A., B. Adriaenssens & P. Sampson, 2014. Individual and sex-specific differences in intrinsic growth rate covary with consistent individual differences in behaviour. Journal of Animal Ecology 83: 1186–1195.

    PubMed  PubMed Central  Google Scholar 

  8. Blanckenhorn, W. U., 2005. Behavioral causes and consequences of sexual size dimorphism. Ethology 111: 977–1016.

    Google Scholar 

  9. Boschung, H. T., J. D. Williams, D. W. Gotshall, D. K. Caldwell, M. C. Caldwell, C. Nehring & J. Verner, 1983. The Audubon Society field guide to North American fishes, whales, and dolphins. Alfred A, Knopf.

    Google Scholar 

  10. Brodin, T. & F. Johansson, 2004. Conflicting selection pressures on the growth/predation-risk trade-off in a damselfly. Ecology 85: 2927–2932.

    Google Scholar 

  11. Burton, O. J., B. L. Phillips & J. M. J. Travis, 2010. Trade-offs and the evolution of life-histories during range expansion. Ecology Letters 13: 1210–1220.

    Google Scholar 

  12. Capellini, I., J. Baker, W. L. Allen, S. E. Street & C. Venditti, 2015. The role of life history traits in mammalian invasion success. Ecology Letters 18: 1099–1107.

    PubMed  PubMed Central  Google Scholar 

  13. Chuang, A. & C. R. Peterson, 2016. Expanding population edges: theories, traits, and trade-offs. Global Change Biology 22: 494–512.

    Google Scholar 

  14. Chucholl, C., H. B. Stich & G. Maier, 2008. Aggressive interactions and competition for shelter between a recently introduced and an established invasive crayfish: orconectes immunis vs. O. limosus. Fundamental and Applied Limnology 172: 27–36.

    Google Scholar 

  15. Clobert, J., A. Oppliger, G. Sorci, B. Ernade, J. Swallow & T. Garland, 2000. Trade-offs in phenotypic traits: endurance at birth, growth, survival, predation and susceptibility to parasitism in a lizard, Lacerta vivipara. Functional Ecology 14: 675–684.

    Google Scholar 

  16. Colautti, R. I. & J. A. Lau, 2015. Contemporary evolution during invasions: evidence for differentiation, natural selection, and local adaptation. Molecular Ecology 24: 1999–2017.

    Google Scholar 

  17. Crandall, K. A. & S. De Grave, 2017. An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. Journal of Crustacean Biology 37: 615–653.

    Google Scholar 

  18. Dick, J. T. A., C. Laverty, J. J. Lennon, D. Barrios-O’Neill, P. J. Mensink, J. Robert Britton, V. Médoc, P. Boets, M. E. Alexander, N. G. Taylor, A. M. Dunn, M. J. Hatcher, P. J. Rosewarne, S. Crookes, H. J. MacIsaac, M. Xu, A. Ricciardi, R. J. Wasserman, B. R. Ellender, O. L. F. Weyl, F. E. Lucy, P. B. Banks, J. A. Dodd, C. MacNeil, M. R. Penk, D. C. Aldridge, & J. M. Caffrey, 2017. Invader Relative Impact Potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. Journal of Applied Ecology 54:1259–1267.

  19. Dmitriew, C. M., 2011. The evolution of growth trajectories: what limits growth rate? Biological Reviews 86: 97–116.

    Google Scholar 

  20. Eberly, W. R., 1955. Summary of the distribution of Indiana crayfishes, including new state and county records. Proceedings of the Indiana Academy of Science 64: 281–283.

    Google Scholar 

  21. Englund, G. & J. J. Krupa, 2000. Habitat use by crayfish in stream pools: influence of predators, depth and body size. Freshwater Biology 43: 75–83.

    Google Scholar 

  22. Fortino, K. & R. P. Creed, 2007. Abiotic factors, competition or predation: what determines the distribution of young crayfish in a watershed? Hydrobiologia 575: 301–314.

    Google Scholar 

  23. Garvey, J. E., R. A. Stein & H. M. Thomas, 1994. Assessing how fish predation and interspecific prey competition influence a crayfish assemblage. Ecology 75: 532–547.

    Google Scholar 

  24. Gherardi, F., B. Renai, P. Galeotti & D. Rubolini, 2006. Nonrandom mating, mate choice, and male-male competition in the crayfish Austropotamobius italicus, a threatened species. Archiv für Hydrobiologie 165: 557–576.

    Google Scholar 

  25. Gherardi, F., K. M. Mavuti, N. Pacini, E. Tricarico & D. M. Harper, 2011. The smell of danger: chemical recognition of fish predators by the invasive crayfish Procambarus clarkii. Freshwater Biology 56: 1567–1578.

    Google Scholar 

  26. Giraudoux, P., 2017. pgirmess: data analysis in ecology. R package version 1.6.7

  27. Glon, M. G., L. S. Reisinger & L. M. Pintor, 2018. Biogeographic differences between native and non-native populations of crayfish alter species coexistence and trophic interactions in mesocosms. Biological Invasions 20: 3475–3490.

    Google Scholar 

  28. Godin, J.-G. J. & S. A. Smith, 1988. A fitness cost of foraging in the guppy. Nature 333: 69–71.

    Google Scholar 

  29. Hendry, A. P., T. J. Farrugia & M. T. Kinnison, 2008. Human influences on rates of phenotypic change in wild animal populations. Molecular Ecology 17: 20–29.

    Google Scholar 

  30. Hierro, J. L., J. L. Maron & R. M. Callaway, 2005. A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. Journal of Ecology 93: 5–15.

    Google Scholar 

  31. Hill, A. M. & D. M. Lodge, 1994. Diel changes in resource demand—competition and predation in species replacement among crayfishes. Ecology 75: 2118–2126.

    Google Scholar 

  32. Hudson, C. M., G. P. Brown & R. Shine, 2017. Evolutionary shifts in anti-predator responses of invasive cane toads (Rhinella marina). Behavioral Ecology and Sociobiology 71: 1–9.

    Google Scholar 

  33. Iacarella, J. C., J. T. A. Dick & A. Ricciardi, 2015. A spatio-temporal contrast of the predatory impact of an invasive freshwater crustacean. Diversity and Distributions 21: 803–812.

    Google Scholar 

  34. Iles, D. T., R. Salguero-Gómez, P. B. Adler & D. N. Koons, 2016. Linking transient dynamics and life history to biological invasion success. Journal of Ecology 104: 399–408.

    Google Scholar 

  35. Juette, T., J. Cucherousset & J. Cote, 2014. Animal personality and the ecological impacts of freshwater non-native species. Current Zoology 60: 417–427.

    Google Scholar 

  36. Kolar, C. S. & D. M. Lodge, 2001. Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16: 199–204.

    Google Scholar 

  37. Kuznetsova, A., P. B. Brockhoff & R. H. B. Christensen, 2016. lmerTest: tests in linear mixed effects models. R package version 2.0-33.

  38. Lenth, R. V., 2016. Least-squares means: the R package lsmeans. Journal of Statistical Software 69: 1–33.

    Google Scholar 

  39. Lodge, D. M., M. W. Kershner, J. E. Aloi & A. P. Covich, 1994. Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75: 1265–1281.

    Google Scholar 

  40. Martin III, A. L. & P. A. Moore, 2010. The influence of reproductive state on the agonistic interactions between male and female crayfish (Orconectes rusticus). Behaviour 147: 1309–1325.

    Google Scholar 

  41. Maupin, J. L. & S. E. Riechert, 2001. Superfluous killing in spiders: a consequence of adaptation to food-limited environments? Behavioral Ecology 12: 569–576.

    Google Scholar 

  42. Palkovacs, E. P. & D. M. Post, 2009. Experimental evidence that phenotypic divergence in predator foraging traits drives ecological divergence in prey communities. Ecology 90: 300–305.

    Google Scholar 

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

  44. Peters, J. A. & D. M. Lodge, 2013. Habitat, predation, and coexistence between invasive and native crayfishes: prioritizing lakes for invasion prevention. Biological Invasions 15: 2489–2502.

    Google Scholar 

  45. Phillips, B. L., 2009. The evolution of growth rates on an expanding range edge. Biology Letters 5: 802–804.

    PubMed  PubMed Central  Google Scholar 

  46. Phillips, B. L., G. P. Brown & R. Shine, 2010. Life-history evolution in range-shifting populations. Ecology 91: 1617–1627.

    PubMed  Google Scholar 

  47. Pintor, L. M. & A. Sih, 2009. Differences in growth and foraging behavior of native and introduced populations of an invasive crayfish. Biological Invasions 11: 1895–1902.

    Google Scholar 

  48. Pintor, L. M., A. Sih & M. L. Bauer, 2008. Differences in aggression, activity and boldness between native and introduced populations of an invasive crayfish. Oikos 117: 1629–1636.

    Google Scholar 

  49. Reale, D., D. Garant, M. M. Humphries, P. Bergeron, V. Careau & P. Montiglio, 2010. Personality and the emergence of the pace-of-life syndrome concept at the population level. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 4051–4063.

    Google Scholar 

  50. Reisinger, L. S., A. K. Elgin, K. M. Towle, D. J. Chan & D. M. Lodge, 2017. The influence of evolution and plasticity on the behavior of an invasive crayfish. Biological Invasions 19: 815–830.

    Google Scholar 

  51. Ricciardi, A., 2007. Are modern biological invasions an unprecedented form of global change? Conservation Biology 21: 329–336.

    Google Scholar 

  52. Roth, B. M., J. C. Tetzlaff, M. L. Alexander & J. F. Kitchell, 2007. Reciprocal relationships between exotic rusty crayfish, macrophytes, and Lepomis species in northern Wisconsin lakes. Ecosystems 10: 74–85.

    Google Scholar 

  53. Roughgarden, J., 1971. Density-dependent natural selection. Ecology 52: 453–468.

    Google Scholar 

  54. Sargent, L. W. & D. M. Lodge, 2014. Evolution of invasive traits in nonindigenous species: increased survival and faster growth in invasive populations of rusty crayfish (Orconectes rusticus). Evolutionary Applications 7: 949–961.

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  56. Segev, U., L. Burkert, B. Feldmeyer & S. Foitzik, 2017. Pace-of-life in a social insect: behavioral syndromes in ants shift along a climatic gradient. Behavioral Ecology 28: 1149–1159.

    Google Scholar 

  57. Sih, A., 1992. Prey uncertainty and the balancing of antipredator and feeding needs. American Naturalist 139: 1052–1069.

    Google Scholar 

  58. Simon, T. P., 2001. Checklist of the crayfish and freshwater shrimp (decapoda) of Indiana. Proceedings of the Indiana Academy of Science 110: 104–110.

    Google Scholar 

  59. Skurdal, J., D. O. Hessen, E. Garnas & L. A. Vollestad, 2011. Fluctuating fecundity parameters and reproductive investment in crayfish: driven by climate or chaos? Freshwater Biology 56: 335–341.

    Google Scholar 

  60. Stamps, J. A., 2007. Growth-mortality tradeoffs and “personality traits” in animals. Ecology Letters 10: 355–363.

    Google Scholar 

  61. Start, D. & B. Gilbert, 2017. Predator personality structures prey communities and trophic cascades. Ecology Letters 20: 366–374.

    Google Scholar 

  62. Stein, R. A., 1976. Sexual dimorphism in crayfish chelae: functional significance linked to reproductive activities. Canadian Journal of Zoology 54: 220–227.

    Google Scholar 

  63. Strauss, R. E., 1979. Reliability estimates for Ivlev’s electivity index, the forage ratio, and a proposed linear index of food selelction. Transactions of the American Fisheries Society 108: 344–352.

    Google Scholar 

  64. Strobbe, F., M. A. McPeek, M. De Block & R. Stoks, 2011. Fish predation selects for reduced foraging activity. Behavioral Ecology and Sociobiology 65: 241–247.

    Google Scholar 

  65. Taugbol, T. & J. Skurdal, 1992. Growth, mortality and moulting rate of noble crayfish, Astacus astacus L., juveniles in aquaculture experiments. Aquaculture and Fisheries Management 23: 411–420.

    Google Scholar 

  66. Taylor, C. A., G. A. Schuster, & D. B. Wylie, 2015. Field guide to crayfishes of the midwest. Illinios Natural Hisotry Survey Manual.

  67. Thoma, R. F. & R. F. Jezerinac, 2000. Ohio crayfish and shrimp atlas. Ohio Biological Survey, Columbus.

    Google Scholar 

  68. U.S. Geological Survey, 2016. National Water Information System data available on the World Wide Web (USGS Water Data for the Nation), accessed (June 13, 2019), [available on internet at http://waterdata.usgs.gov/nwis/].

  69. Van Petegem, K. H. P., J. Boeye, R. Stoks & D. Bonte, 2016. Spatial selection and local adaptation jointly shape life-history evolution during range expansion. The American Naturalist 188: 485–498.

    Google Scholar 

  70. Whitney, K. D. & C. A. Gabler, 2008. Rapid evolution in introduced species, “invasive traits” and recipient communities: challenges for predicting invasive potential. Diversity and Distributions 14: 569–580.

    Google Scholar 

  71. Williams, M., J. Zalasiewicz, P. K. Haff, C. Schwagerl, A. D. Barnosky & E. C. Ellis, 2015. The anthropocene biosphere. The Anthropocene Review 2: 196–219.

    Google Scholar 

  72. Wilson, K. A., J. J. Magnuson, D. M. Lodge, A. M. Hill, T. K. Kratz, W. L. Perry & T. V. Willis, 2004. A long-term rusty crayfish (Orconectes rusticus) invasion: dispersal patterns and community change in a north temperate lake. Canadian Journal of Fisheries and Aquatic Sciences 61: 2255–2266.

    Google Scholar 

  73. Wolf, M., G. S. Van Doorn, O. Leimar & F. J. Weissing, 2007. Life-history trade-offs favour the evolution of animal personalities. Nature 447: 581–584.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Wright, T. F., J. R. Eberhard, E. A. Hobson, M. L. Avery & M. A. Russello, 2010. Behavioral flexibility and species invasions: the adaptive flexibility hypothesis. Ethology Ecology & Evolution 22: 393–404.

    Google Scholar 

Download references

Acknowledgements

For help with crayfish collection and husbandry, we thank 2016 Central Michigan University (CMU) Great Lakes Summer Research Program students, students in the Pintor Lab at The Ohio State University (OSU), the University of Wisconsin-Madison’s Trout Lake Station Staff, and Y Guy and R Zhu. In addition, we are grateful to the CMU Biological Station staff for assistance with mesocosm setup and maintenance and R Clark for assistance with fabrication of experimental equipment. This work was supported by OSU School of Environment and Natural Resources; the Ohio Agricultural Research and Development Center; and CMU Institute for Great Lakes Research. This manuscript is contribution 136 to CMU’s Institute for Great Lakes Research.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Lindsey S. Reisinger.

Additional information

Publisher's Note

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

Handling editor: Andrew Dzialowski

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Reisinger, L.S., Glon, M.G. & Pintor, L.M. Divergence in foraging and predator avoidance behavior across the geographic range of native and non-native crayfish. Hydrobiologia 847, 803–818 (2020). https://doi.org/10.1007/s10750-019-04139-3

Download citation

Keywords

  • Growth-mortality trade-off
  • Invasive species
  • Evolution
  • Plasticity
  • Predation
  • Competition