Biological Invasions

, Volume 21, Issue 5, pp 1737–1749 | Cite as

Population density contributes to the higher functional response of an invasive fish

  • Rebecca A. Paton
  • Jenilee Gobin
  • Anna C. Rooke
  • Michael G. FoxEmail author
Original Paper


Invasive species often have higher functional responses than native analogs. A better understanding of the functional response of invasive species could help explain the effect of these species on native prey communities, and aid in the development of tools for predicting invasion impact. We investigated the role of population density and location along the invasion pathway in determining the functional response of an invasive fish. We used invasive round goby (Neogobius melanostomus) collected from the Trent-Severn Waterway in Ontario, Canada to test for differences in the functional response of fish from high and low density sites, and from different locations along the invasion pathway. We also compared the functional response of round goby with that of northern logperch (Percina caprodes), a native species occupying the same niche. The density of the invasive predator population influenced its functional response, with attack rate being significantly higher for fish from high-density sites compared to fish from low-density sites. Functional response of individuals living at the invasion front was not significantly different from those living in established areas. The higher functional response of round goby compared to its native analog was associated with shorter handling time. Patterns in functional response curves were not explained by differences in diet among wild populations. Our research demonstrates that population density influences the functional response of an invasive species, and therefore should be accounted for when evaluating the functional response of a potential invader.


Aquatic invasive species Intraspecific competition Laurentian Great Lakes Spatial sorting Spatio-temporal gradient 



We thank C. May and S. Blair for assisting with field collections, and E. Nol and two anonymous reviewers for helpful comments on an earlier version of this manuscript. This research was funded by a National Science and Engineering Canada Undergraduate Student Research Award to RAP and a National Science and Engineering Canada Discovery Grant to MGF.


Funding was provided by National Science and Engineering Research Council (CA) (Grant No. 46681).


  1. Abrams PA (2015) Why ratio dependence is (still) a bad model of predation. Biol Rev 90:794–814. CrossRefGoogle Scholar
  2. Alexander ME, Dick JTA, Weyl OLF, Robinson TB, Richardson DM (2014) Existing and emerging high impact invasive species are characterized by higher functional responses than natives. Biol Lett 10:20130946. CrossRefGoogle Scholar
  3. Balshine S, Verma A, Chant V, Theysmeyer T (2005) Competitive interactions between round gobies and logperch. J Great Lakes Res 31:68–77. CrossRefGoogle Scholar
  4. Barrios-O’Neill D, Dick JTA, Emmerson MC, Ricciardi A, MacIssac HJ, Alexander ME, Bovy HC (2014) Fortune favours the bold: a higher predator reduces the impact of a native but not an invasive intermediate predator. J Anim Ecol 83:693–701. CrossRefGoogle Scholar
  5. Barrios-O’Neill D, Dick JTA, Emmerson MC, Ricciardi A, MacIssac HJ (2015) Predator-free space, functional responses and biological invasions. Funct Ecol 29:377–384. CrossRefGoogle Scholar
  6. Beddington JR (1975) Mutual interference between parasites or predators and its effect on searching efficiency. J Anim Ecol 44:331–340CrossRefGoogle Scholar
  7. Bergstrom MA, Mensinger AF (2009) Interspecific resource competition between the invasive round goby and three native species: logperch, slimy sculpin, and spoonhead sculpin. Trans Am Fish Soc 138:1009–1017. CrossRefGoogle Scholar
  8. Bolker BM (2007) Ecological models and data in R. Princeton University Press, OxfordGoogle Scholar
  9. Bollache L, Dick JTA, Farnsworth KD, Montgomery WI (2008) Comparison of the functional responses of invasive and native amphipods. Biol Lett 4:166–169. CrossRefGoogle Scholar
  10. Byers JE, Reichard S, Randall JM, Parker IM, Smith CS, Lonsdale WM, Atkinson IAE, Seastedt TR, Williamson M, Chornesky E, Hayes D (2002) Directing research to reduce the impacts of nonindigenous species. Conserv Biol 16:630–640CrossRefGoogle Scholar
  11. Cosner C, DeAngelis DL, Ault JS, Olson DB (1999) Effects of spatial grouping on the functional response of predators. Theor Popul Biol 56:65–75. CrossRefGoogle Scholar
  12. Crowley PH, Martin EK (1989) Functional responses and interference within and between year classes of a dragonfly population. J N Am Benthol Soc 8:211–221CrossRefGoogle Scholar
  13. DeAngelis DL, Goldstein RA, O’Neill RV (1975) A model for tropic interaction. Ecology 56:881–892CrossRefGoogle Scholar
  14. DeLong JP (2014) The body-size dependence of mutual interference. Biol Lett 10:20140261. CrossRefGoogle Scholar
  15. Dick JTA, Gallagher K, Avlijas S, Clarke HC, Lewis SE, Leung S, Minchin D, Caffrey J, Alexander ME, Maguire C, Harrod C, Reid N, Haddaway NR, Farnsworth KD, Ricciardi R (2013) Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biol Invasions 15:837–846. CrossRefGoogle Scholar
  16. Dick JTA, Alexander ME, Jeschke JM, Ricciardi R, MacIsaac HJ, Kumschick S, Wehl OLF, Dunn AM, Hatcher MJ, Paterson RA, Farnsworth KD, Robinson TB (2014) Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biol Invasions 16:735–753. CrossRefGoogle Scholar
  17. Dick JTA, Alexander ME, Ricciardi R, Laverty C, Downey PO, Xu M, Jeschke JM, Saul W-C, Hill MP, Wasserman R, Barrios-O’Neill D, Weyl OLF, Shaw RH (2017) Functional responses can unify invasion ecology. Biol Invasions. Google Scholar
  18. Dubs DOL, Corkum LD (1996) Behavioral interactions between round gobies (Neogobius melanostomus) and mottled sculpins (Cottus bairdi). J Great Lakes Res 22:838–844. CrossRefGoogle Scholar
  19. Gutowsky LFG, Fox MG (2011) Occupation, body size and sex ratio of round goby (Neogobius melanostomus) in established and newly invaded areas of an Ontario river. Hydrobiologia 671:27–37. CrossRefGoogle Scholar
  20. Gutowsky LFG, Fox MG (2012) Intra-population variability of life-history traits and growth during range expansion of the invasive round goby, Neogobius melanostomus. Fish Manag Ecol 19:78–88. CrossRefGoogle Scholar
  21. Haddaway NR, Wilcox RH, Heptonstall REA, Griffiths HM, Mortimer RJG, Christmas M, Dunn AM (2012) Predatory functional response and prey choice identify predation differences between native/invasive and parasitised/unparasitised crayfish. PLoS ONE 7:e32229. CrossRefGoogle Scholar
  22. Hansen GJA, Vander Zanden MJ, Blum MJ, Clayton MK, Hain EF, Hauxwell J, Izzo M, Kornis MS, McIntyre PB, Mikulyuk A, Nilsson E, Olden JD, Papes M, Sharma S (2013) Commonly rare and rarely common: comparing population abundance of invasive and native aquatic species. PLoS ONE 8:e77415. CrossRefGoogle Scholar
  23. Hassell MP, Varley GC (1969) New inductive population model for insect parasites and its bearing on biological control. Nature 223:1133–1137. CrossRefGoogle Scholar
  24. Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506. CrossRefGoogle Scholar
  25. Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European pine sawfly. Can Entomol 91:293–320CrossRefGoogle Scholar
  26. Howard BR, Barrios-O’Neill D, Alexander ME, Dick JTA, Therriault TW, Robinson TB, Coté I (2018) Functional responses of a cosmopolitan invader demonstrate intraspecific variability in consumer resource dynamics. PeerJ 6:e5634. CrossRefGoogle Scholar
  27. Iacarella JC, Dick JT, Ricciardi A (2015) A spatio-temporal contrast of the predatory impact of an invasive freshwater crustacean. Divers Distrib 21:803–812. CrossRefGoogle Scholar
  28. Iltis C, Spataro T, Wattier R, Médoc V (2018) Parasitism may alter functional response comparisons: a case study on the killer shrimp Dikerogammarus villosus and two non-invasive gammarids. Biol Invasions 20:619–632. CrossRefGoogle Scholar
  29. Janssen J, Jude DJ (2001) Recruitment failure of mottled sculpin Cottus bairdi in Calumet Harbor, Southern Lake Michigan, induced by the newly introduced round goby Neogobius melanostomus. J Great Lakes Res 27:319–328. CrossRefGoogle Scholar
  30. Jude DJ, Reider RH, Smith GW (1992) Establishment of gobiidae in the Great Lakes Basin. Can J Fish Aquat Sci 49:416–421. CrossRefGoogle Scholar
  31. Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, Oxford, pp 178–196Google Scholar
  32. Kulhanek SA, Ricciardi A, Leung B (2011) Is invasion history a useful tool for predicting the impacts of the world’s worst aquatic invasive species? Ecol Appl 21:189–202. CrossRefGoogle Scholar
  33. Lauer TE, Allen PJ, McComish TS (2004) Changes in mottled sculpin and johnny darter trawl catches after the appearance of round gobies in the Indiana waters of Lake Michigan. Trans Am Fish Soc 133:185–189. CrossRefGoogle Scholar
  34. Laverty C, Green KD, Dick JTA, Barrios-O’Neill D, Mensink PJ, Médoc V, Spataro T, Caffrey JM, Lucy FE, Boets P, Britton JR, Peg J, Gallagher C (2017) Assessing the ecological impacts of invasive species based on their functional responses and abundances. Biol Invasions 19:1653–1665. CrossRefGoogle Scholar
  35. Leung B, Lodge DM, Finnoff D, Shogre JF, Lewis MA, Lamberti G (2002) An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species. Proc R Soc Lond B 269:2407–2413. CrossRefGoogle Scholar
  36. Mack RN, Simberloff D, Lonsdale MW, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710.;2 CrossRefGoogle Scholar
  37. Masson L, Brownscombe JW, Fox MG (2016) Fine scale spatio-temporal life history shifts in an invasive species at its expansion front. Biol Invasions 18:775–792. CrossRefGoogle Scholar
  38. Médoc V, Albert H, Spataro T (2015) Functional response comparisons among freshwater amphipods: ratio-dependence and higher predation for Gammarus pulex compared to the non-natives Dikerogammarus villosus and Echinogammarus berilloni. Biol Inv 17:3625–3637. CrossRefGoogle Scholar
  39. Médoc V, Thuillier L, Spataro T (2018) Opportunistic omnivory impairs our ability to predict invasive species impacts from functional response comparisons. Biol Invasions 20:1307–1319. CrossRefGoogle Scholar
  40. Myles-Gonzalez E, Burness G, Yavno S, Rooke A, Fox MG (2015) To boldly go where no goby has gone before: boldness, dispersal tendency, and metabolism at the invasion front. Behav Ecol 26:1083–1090. CrossRefGoogle Scholar
  41. Novak M, Wolf C, Coblentz KE, Shepard ID (2017) Quantifying predator dependence in the functional response of generalist predators. Ecol Lett 20:761–769. CrossRefGoogle Scholar
  42. Papacostas KJ, Rielly-Carroll EW, Gerogian SE, Long DJ, Princiotta SD, Quattrini AM, Reuter KE, Freestone AL (2017) Biological mechanisms of marine invasions. Mar Ecol Prog Ser 565:251–268. CrossRefGoogle Scholar
  43. Paterson RA, Dick JTA, Pritchard DW, Ennis M, Hatcher MJ, Dunn AM (2015) Predicting invasive species impacts: a community module functional response approach reveals context dependencies. J Anim Ecol 84:453–463. CrossRefGoogle Scholar
  44. Perkins LB, Nowak RS (2013) Invasion syndromes: hypotheses on relationships among invasive species attributes and characteristics of invaded sites. J Arid Land 5:275–283. CrossRefGoogle Scholar
  45. Phillips BL, Brown GP, Travis JM, Shine R (2008) Reid’s paradox revisited: the evolution of dispersal kernels during range expansion. Am Nat 172:S34–S48. CrossRefGoogle Scholar
  46. Phillips BL, Brown GP, Shine R (2010a) Life-history evolution in range-shifting populations. Ecology 91:1617–1627. CrossRefGoogle Scholar
  47. Phillips BL, Brown GP, Shine R (2010b) Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. J Evol Biol 23:2595–2601. CrossRefGoogle Scholar
  48. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs associated with non-indigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  49. Pritchard DW (2014) Frair: functional response analysis in R. R package version 0.5.
  50. Pritchard DW, Paterson RA, Bovy HC, Barrios-O’Neill D (2017) Frair: an R package for fitting and comparing consumer functional responses. Methods Ecol Evol 8:1528–1534. CrossRefGoogle Scholar
  51. R Development Core Team (2017) R: a language and environment for statistical computing. Vienna, Austria. Retrieved from
  52. Raby GD, Gutowsky LF, Fox MG (2010) Diet composition and consumption rate in round goby (Neogobius melanostomus) in its expansion phase in the Trent River, Ontario. Environ Biol Fishes 89:143–150. CrossRefGoogle Scholar
  53. Ricciardi A (2003) Predicting the impacts of an introduced species from its invasion history: an empirical approach applied to zebra mussel invasions. Freshw Biol 48:972–981. CrossRefGoogle Scholar
  54. Ricciardi A, Cohen J (2007) The invasiveness of an introduced species does not predict its impact. Biol Invasions 9:309–315. CrossRefGoogle Scholar
  55. Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383. CrossRefGoogle Scholar
  56. Schröder A, Kalinkat G, Arlinghaus R (2016) Individual variation in functional response parameters is explained by body size but not behavioral types in a poeciliid fish. Oecologia 182:1129–1140. CrossRefGoogle Scholar
  57. Skalski GT, Gilliam JF (2001) Functional responses with predator interference: viable alternatives to the Holling type II model. Ecology 82:3083–3092CrossRefGoogle Scholar
  58. South J, Dick JTA, McCard M, Barrios-O’Neill D, Anton A (2017) Predicting predatory impact of juvenile invasive lionfish (Pterois volitans) on a crustacean prey using functional response analysis: effects of temperature, habitat complexity and light regimes. Environ Biol Fishes 100:1155–1165. CrossRefGoogle Scholar
  59. Taylor NG, Dunn AM (2018) Predatory impacts of alien decapod Crustacea are predicted by functional responses and explained by differences in metabolic rate. Biol Invasions. Google Scholar
  60. Toscano BJ, Griffen BD (2014) Trait-mediated functional responses: predator behavioral type mediates prey consumption. J Anim Ecol 83:1469–1477. CrossRefGoogle Scholar
  61. Welcomme RL (1988) International introductions of inland aquatic species. FAO Fisheries Technical Paper, vol 294, pp 1–318Google Scholar
  62. Xu M, Mu X, Dick JTA, Fang M, Gu D, Luo D, Zhang J, Luo J, Hu Y (2016) Comparative functional responses predict the invasiveness and ecological impacts of alien herbivorous snails. PLoS ONE 11:e0147017. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologyTrent UniversityPeterboroughCanada
  2. 2.Environmental and Life Sciences Graduate ProgramTrent UniversityPeterboroughCanada
  3. 3.School of the EnvironmentTrent UniversityPeterboroughCanada

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