Skip to main content
Log in

Fine scale spatio-temporal life history shifts in an invasive species at its expansion front

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

Abstract

The dynamic shifts in life history traits by non-native populations at an invasion front may be driven by a combination of phenotypic plasticity and micro-evolutionary processes, allowing for appropriate responses to changes in biotic and abiotic factors associated with range expansion. The temporal and spatial scale at which these shifts occur, however, is largely unexplored. We examined the age-specific life-history responses of female round goby (Neogobius melanostomus) across a fine spatial scale by comparing traits of individuals at the expanding front of an invasive pathway with those of individuals living at the previous year’s front. Females in the new front were younger, exhibited higher body condition index and fecundity, and greater reproductive allocation than those living at the previous year’s front. No difference in back-calculated length at age or in seasonal growth increment was found between occupants of the old and new fronts. Age-specific differences in reproductive investment were observed; age-1 females from the new front exhibited greater reproductive effort but similar reproductive allocation, whereas age-2 females showed greater reproductive allocation in the new front, but similar reproductive effort. These age-specific differences may be related to differences in population density and other biotic factors encountered during ontogeny, or to micro-evolutionary processes. Our results demonstrate that fine scale changes in energy allocation towards reproduction through increases in reproductive allocation and fecundity occur at the invasion front, highlight how quickly those shifts can occur at the expansion front, and suggest that such changes in newly colonised areas facilitate range expansion.

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

Access this article

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bagenal TB, Tesgh FW (1978) Age and growth. In: Bagenal TB (ed) Methods for the assessment of fish production in fresh waters, HBP Handbook No. 3. Blackwell Scientific Publication, Oxford, pp 101–136

    Google Scholar 

  • Baker HG (1965) Characters and modes of origins of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–172

    Google Scholar 

  • Belichon S, Clobert J, Massot M (1996) Are there differences in fitness components between philopatric and dispersing individuals? Acta Oecol 17:503–517

    Google Scholar 

  • Bøhn T, Sandlund OT, Amundsen PA, Primicerio R (2004) Rapidly changing life history during invasion. Oikos 106:138–150. doi:10.1111/j.0030-1299.2004.13022.x

    Article  Google Scholar 

  • Bonte D, Van Dyck H, Bullock JM et al (2012) Costs of dispersal. Biol Rev Camb Philos Soc 87:290–312. doi:10.1111/j.1469-185X.2011.00201.x

    Article  PubMed  Google Scholar 

  • Brandner J, Cerwenka AF, Schliewen UK, Geist J (2013) Bigger is better: characteristics of round gobies forming an invasion front in the Danube river. PLoS One. doi:10.1371/journal.pone.0073036

    Google Scholar 

  • Brownscombe JW, Fox MG (2012) Range expansion dynamics of the invasive round goby (Neogobius melanostomus) in a river system. Aquat Ecol 46:175–189. doi:10.1007/s10452-012-9390-3

    Article  Google Scholar 

  • Brownscombe JW, Masson L, Beresford DV, Fox MG (2012) Modeling round goby Neogobius melanostomus range expansion in a Canadian river system. Aquat Invasions 7:537–545. doi:10.3391/ai.2012.7.4.010

    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. doi:10.1111/j.1461-0248.2010.01505.x

    Article  PubMed  Google Scholar 

  • Charlebois PM, Marsden JE, Goettel RG et al (1997) The round goby Neogobius Melanostomus (Pallas), a review of European and North American literature. Illinois-Indiana Sea Grant Progr Illinois Nat Hist Surv INHS, Spec Publ 20:76

    Google Scholar 

  • Clarke A (1987) Temperature, latitude and reproductive effort. Mar Ecol Prog Ser 38:89–99. doi:10.3354/meps038089

    Article  Google Scholar 

  • Corkum LD, Sapota MR, Skora KE (2004) The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biol Invasions 6:173–181. doi:10.1023/B:BINV.0000022136.43502.db

    Article  Google Scholar 

  • Cotto O, Kubisch A, Ronce O (2014) Optimal life-history strategy differs between philopatric and dispersing individuals in a metapopulation. Am Nat 183:384–393. doi:10.1086/675064

    Article  PubMed  Google Scholar 

  • Crivelli AJ, Mestre D (1988) Life history patterns of pumpkinseed, Legornis gibbosus, introduced into the Camargue, a mediterranean wetland. Arch Hydrobiol 13(1):449–466

    Google Scholar 

  • Danylchuk AJ, Fox MG (1994) Seasonal reproductive patterns of pumpkinseed (Lepomis gibbosus) populations with varying body size characteristics. Can J Fish Aquat Sci 51:490–500

    Article  Google Scholar 

  • DeMaster DP (1978) Calculation of the average age of sexual maturity in marine mammals. J Fish Res Board Canada 35:912–915

    Article  Google Scholar 

  • Dibattista JD, Feldheim KA, Gruber SH, Hendry AP (2007) When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. J Evol Biol 20:201–212. doi:10.1111/j.1420-9101.2006.01210.x

    Article  CAS  PubMed  Google Scholar 

  • Dytham C, Travis JMJ, Mustin K, Benton TG (2014) Changes in species’ distributions during and after environmental change: which eco-evolutionary processes matter more? Ecography 37:1210–1217. doi:10.1111/ecog.01194

    Article  Google Scholar 

  • Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18:524–535. doi:10.1111/j.1420-9101.2005.00887.x

    Article  CAS  PubMed  Google Scholar 

  • Feiner ZS, Aday DD, Rice JA (2012) Phenotypic shifts in white perch life history strategy across stages of invasion. Biol Invasions 14:2315–2329. doi:10.1007/s10530-012-0231-z

    Article  Google Scholar 

  • Fox MG (1994) Growth, density, and interspecific influences on pumpkinseed sunfish life histories. Ecology 75:1157–1171

    Article  Google Scholar 

  • Fox MG, Copp GH (2014) Old world versus new world: life-history alterations in a successful invader introduced across Europe. Oecologia 174:435–446. doi:10.1007/s00442-013-2776-7

    Article  PubMed Central  PubMed  Google Scholar 

  • Fox MG, Crivelli AJ (1998) Body size and reproductive allocation in a multiple spawning centrarchid. Can J Fish Aquat Sci 55:737–748. doi:10.1139/f97-269

    Article  Google Scholar 

  • Fox MG, Vila-Gispert A, Copp GH (2007) Life-history traits of introduced Iberian pumpkinseed Lepomis gibbosus relative to native populations. Can differences explain colonization success? J Fish Biol 71:56–69. doi:10.1111/j.1095-8649.2007.01683.x

    Article  Google Scholar 

  • French JRP, Jude DJ (2001) Diets and diet overlap of nonindigenous gobies and small benthic native fishes co-inhabiting the St. Clair River, Michigan. J Great Lakes Res 27:300–311. doi:10.1016/S0380-1330(01)70645-4

    Article  Google Scholar 

  • Gadgil M, Solbrig OT (1972) The Concept of r- and K-selection: evidence from wild flowers and some theoretical considerations. Am Nat 106:14–31. doi:10.1086/282748

    Article  Google Scholar 

  • 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. doi:10.1007/s10750-011-0701-9

    Article  Google Scholar 

  • 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. doi:10.1111/j.1365-2400.2011.00831.x

    Article  Google Scholar 

  • Gutowsky LFG, Brownscombe JW, Fox MG (2011) Angling to estimate the density of large round goby (Neogobius melanostomus). Fish Res 108:228–231. doi:10.1016/j.fishres.2010.12.014

    Article  Google Scholar 

  • Hirshfield MF (1980) An experimental analysis of reproductive effort and cost in the Japanese medaka, Oryzias latipes. Ecology 61:282–292

    Article  Google Scholar 

  • Hirshfield MF, Tinkle DW (1975) Natural selection and the evolution of reproductive effort. Proc Natl Acad Sci USA 72:2227–2231. doi:10.1073/pnas.72.6.2227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hôrková K, Kováč V (2014) Different life-histories of native and invasive Neogobius melanostomus and the possible role of phenotypic plasticity in the species’ invasion success. Knowl Manag Aquat Ecosyst 412(1):1–11. doi:10.1051/kmae/2013081

    Article  Google Scholar 

  • Jurajda P, Cerný J, Polačik M et al (2005) The recent distribution and abundance of non-native Neogobius fishes in the Slovak section of the River Danube. J Appl Ichthyol 21:319–323. doi:10.1111/j.1439-0426.2005.00688.x

    Article  Google Scholar 

  • Kipp R, Ricciardi A (2012) Impacts of the Eurasian round goby (Neogobius melanostomus) on benthic communities in the upper St. Lawrence River. Can J Fish Aquat Sci 69:469–486. doi:10.1139/f2011-139

    Article  Google Scholar 

  • Kipp R, Hébert I, Lacharité M, Ricciardi A (2012) Impacts of predation by the Eurasian round goby (Neogobius melanostomus) on molluscs in the upper St. Lawrence River. J Great Lakes Res 38:78–89. doi:10.1016/j.jglr.2011.11.012

    Article  Google Scholar 

  • Kornis MS, Mercado-Silva N, vander Zanden MJ (2012) Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. J Fish Biol 80:235–285. doi:10.1111/j.1095-8649.2011.03157.x

    Article  CAS  PubMed  Google Scholar 

  • Krakowiak PJ, Pennuto CM (2008) Fish and macroinvertebrate communities in tributary streams of Eastern Lake Erie with and without round gobies (Neogobius melanostomus, Pallas 1814). J Great Lakes Res 34:675–689. doi:10.3394/0380-1330-34.4.675

    Article  Google Scholar 

  • L’avrinčíková M, Kováč V (2007) Invasive round goby Neogobius melanostomus from the Danube mature at small size. J Appl Ichthyol 23:276–278. doi:10.1111/j.1439-0426.2007.00851.x

    Article  Google Scholar 

  • Lederer AM, Janssen J, Reed T, Wolf A (2008) Impacts of the Introduced Round Goby (Apollonia melanostoma) on Dreissenids (Dreissena polymorpha and Dreissena bugensis) and on Macroinvertebrate Community between 2003 and 2006 in the Littoral Zone of Green Bay, Lake Michigan. J Great Lakes Res 34:690–697. doi:10.3394/0380-1330-34.4.690

    Article  Google Scholar 

  • Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967

    Article  Google Scholar 

  • Lucek K, Sivasundar A, Seehausen O (2014) Disentangling the role of phenotypic plasticity and genetic divergence in contemporary ecotype formation during a biological invasion. Evolution 68:2619–2632. doi:10.1111/evo.12443

    Article  PubMed  Google Scholar 

  • MacInnis AJ, Corkum LD (2000) Fecundity and reproductive season of the round goby Negobius melanosomus in the upper Detroit river. Trans Am Fish Soc 129:136–144. doi:10.1577/1548-8659(2000)129<0136

    Article  Google Scholar 

  • Masson G, Valente E, Fox MG, Copp GH (2014) Thermal influences on life-history traits and reproductive effort of introduced pumkinseed sunfish Lepomis Gibbosus in the River Moselle Basin (Northeastern France). River Res Applic. doi:10.1002/rra

    Google Scholar 

  • Michel MJ, Chevin LM, Knouft JH (2014) Evolution of phenotype-environment associations by genetic responses to selection and phenotypic plasticity in a temporally autocorrelated environment. Evolution (NY) 68:1374–1384. doi:10.1111/evo.12371

    Article  Google Scholar 

  • Minns CK, Moore JE, Seifried KE (2004) Nutrient load and budgets in the Bay of Quinte, Lake Ontario, 1972–2001. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2694, GLLFAS, Fisheries and Ocean Canada, Burlington, ON

  • Olden JD, Leroy Poff N, Bestgen KR (2006) Life-history strategies predict fish invasions and extirpations in the Colorado River Basin. Ecol Monogr 76:25–40. doi:10.1890/05-0330

    Article  Google Scholar 

  • Pauchard A, Shea K (2006) Integrating the study of non-native plant invasions across spatial scales. Biol Invasions 8:399–413. doi:10.1007/s10530-005-6419-8

    Article  Google Scholar 

  • Phillips BL (2009) The evolution of growth rates on an expanding range edge. Biol Lett 5:802–804. doi:10.1098/rsbl.2009.0367

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Polačik M, Janáč M, Vassilev M, Trichkova T (2012) Morphometric comparison of native and non-native populations of round goby Neogobius melanostomus from the River Danube. Folia Zool 61:1–8

    Google Scholar 

  • Quinn TP, Kinnison MT, Unwin MJ (2001) Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern, rate, and process. Genetica 112–113:493–513. doi:10.1023/A:1013348024063

    Article  PubMed  Google Scholar 

  • Raby GD, Gutowsky LFG, 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. doi:10.1007/s10641-010-9705-y

    Article  Google Scholar 

  • Radinger J, Wolter C (2014) Patterns and predictors of fish dispersal in rivers. Fish Fish 15:456–473. doi:10.1111/faf.12028

    Article  Google Scholar 

  • Ray WJ, Corkum LD (2001) Habitat and site affinity of the round goby. J Great Lakes Res 27:329–334. doi:10.1016/S0380-1330(01)70648-X

    Article  Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993. doi:10.1111/j.1461-0248.2006.00950.x

    Article  PubMed  Google Scholar 

  • Ridgway MS, Shuter BT, Post EE (1991) The relative influence of body size and territorial behaviour on nesting asynchrony in male smallmouth bass, Micropterus dolomieui (Pisces: Centrarchidae). J Anim Ecol 60:665–681

    Article  Google Scholar 

  • Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242. doi:10.1016/j.tree.2014.02.003

    Article  PubMed  Google Scholar 

  • Roche KF, Janač M, Jurajda P (2013) A review of Gobiid expansion along the Danube–Rhine corridor– geopolitical change as a driver for invasion. Knowl Manag Aquat Ecosyst. doi:10.1051/kmae/2013066

    Google Scholar 

  • Rodriguez MA (2002) Restricted movement in stream fish: the paradigm is incomplete, not lost. Ecology 83:1–13

    Article  Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B 273:2453–2459. doi:10.1098/rspb.2006.3597

    Article  PubMed Central  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Sapota MR, Skóra KE (2005) Spread of alien (non-indigenous) fish species Neogobius melanostomus in the Gulf of Gdansk (south Baltic). Biol Invasions 7:157–164. doi:10.1007/s10530-004-9035-0

    Article  Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176

    Article  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 108:5708–5711. doi:10.1073/pnas.1018989108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Skalski GT, Gilliam JF (2000) Modeling diffusive spread in a heterogeneous population: a movement study with stream fish. Ecology 81:1685–1700

    Article  Google Scholar 

  • Snyder D (1983) Fish eggs and larvae. In: Nielsen L, Johnson D (eds) Fisheries techniques. American Fisheries Society, Bethesda, pp 165–197

    Google Scholar 

  • Stearns SC, Koella JC (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40:893–913. doi:10.2307/2408752

    Article  Google Scholar 

  • Taborsky B (2006) The influence of juvenile and adult environments on life-history trajectories. Proc R Soc B 273:741–750. doi:10.1098/rspb.2005.3347

    Article  PubMed Central  PubMed  Google Scholar 

  • Tesch FW (1968) Age and growth. Richer WE Methods for assessment of fish production in fresh waters. Blackwell Scientific, Oxford, pp 93–123

    Google Scholar 

  • Tomczak MT, Sapota MR (2006) The fecundity and gonad development cycle of the round goby (Neogobius melanostomus, Pallas, 1811) from the Gulf of Gdańsk. Oceanol Hydrobiol Stud XXXV:353–367

    Google Scholar 

  • Trippel EA, Harvey HH (1987) Reproductive responses of five white sucker (Catostomus commersoni) populations in relation to lake acidity. Can J Fish Aquat Sci 44:1018–1023

    Article  Google Scholar 

  • Verhoeven KJF, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc Biol Sci 278:2–8. doi:10.1098/rspb.2010.1272

    Article  PubMed Central  PubMed  Google Scholar 

  • Weeks SC (1993) Phenotypic plasticity of life-history traits in clonal and sexual fish (Poeciliopsis) at high and low densities. Oecologia 93:307–314

    Article  Google Scholar 

  • Winemiller KO, Rose KA (1992) Patterns of life-history diversification in north american fishes: implications for population regulation. Can J Fish Aquat Sci 49:2196–2218. doi:10.1139/f92-242

    Article  Google Scholar 

  • Zenni RD, Simberloff D (2013) Number of source populations as a potential driver of pine invasions in Brazil. Biol Invasions 15:1623–1639. doi:10.1007/s10530-012-0397-4

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. In: Gail M, Krickeberg K, Samet JM et al (eds) Statistics for Biology and Health. Springer, New York

    Google Scholar 

Download references

Acknowledgments

We thank Gérard Masson for his suggestions on study design and laboratory analysis procedures, and Dirk Algera for his assistance during field collection and laboratory analysis. We also thank two anonymous reviewers for helpful comments and suggestions on an earlier draft of this manuscript. This research was supported by a Discovery Grant from the Natural Science and Engineering Research Council (#46680-2007) and a grant from the Ontario Invasive Species Centre Partnership Fund (#2011-12) to MGF.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laurence Masson.

Appendix

Appendix

See Appendices A and B.

Appendix A Mean gonadosomatic index (GSI), Mean fecundity (count of eggs per g of soma) fecundity and Fulton’s condition index (K) of “ready to spawn” female round goby sampled from each site of the old (OF, 2010) and new (NE, 2011) invasion fronts during the reproductive season (period 1, 16–20 May/1–3 June, 2, 13–15 June/28–29 June, 3, 8-11 July/26–27 July)
Appendix B Mean total length (mm) at age and of female round goby samples from each site of the old (OF) and new fronts (NF) in the Otonabee River during the spawning season of 2011

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Masson, L., Brownscombe, J.W. & Fox, M.G. Fine scale spatio-temporal life history shifts in an invasive species at its expansion front. Biol Invasions 18, 775–792 (2016). https://doi.org/10.1007/s10530-015-1047-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-1047-4

Keywords

Navigation