Skip to main content
SpringerLink
Log in

Temporal and ontogenetic changes in the trophic signature of an invasive marine predator

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Many successful invasive species have generalist diets, but the extent to which they can track changing resources has seldom been documented. Stable isotope analysis was used to measure dietary shifts with ontogeny and over time in relation to changes in prey availability for Indo-Pacific lionfish (Pterois sp.). These are invasive predators that are well established throughout the western North Atlantic and Caribbean where they have caused significant decreases in native reef fish populations in some areas. Samples and observations were made off New Providence Island, Bahamas during the summers of 2008 and 2010. Lionfish δ15N and δ13C values increased only weakly with body length, suggesting that processes other than growth also contribute to stable isotope variability. The trophic niche of lionfish changed significantly between years, concomitant with large changes in native fish prey abundance and community structure. The trophic niche of large lionfish expanded, increasing in trophic diversity at the population level and showing lower individual trophic similarity, while that of small lionfish remained similar in size but shifted towards more 15N-enriched and 13C-depleted prey sources. The ability of lionfish to modify their diet over time may have facilitated their expansion and persistence at high densities in some areas despite local prey depletion.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Albins, M. A., 2012. Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biological Invasions 15: 29–43.

    Article  Google Scholar 

  • Albins, M. A., 2015. Invasive Pacific lionfish Pterois volitans reduce abundance and species richness of native Bahamian coral-reef fishes. Marine Ecology Progress Series 522: 231–243.

    Article  Google Scholar 

  • Albins, M. A. & M. A. Hixon, 2008. Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Marine Ecology Progress Series 367: 233–238.

    Article  Google Scholar 

  • Araujo, M. S., D. I. Bolnick & C. A. Layman, 2011. The ecological causes of individual specialisation. Ecology Letters 14: 948–958.

    Article  PubMed  Google Scholar 

  • Arrington, D. A. & K. O. Winemiller, 2002. Preservation effects on stable isotope analysis of fish muscle. Transactions of the American Fisheries Society 131: 337–342.

    Article  CAS  Google Scholar 

  • Barbour, A. B., M. L. Montgomery, A. A. Adamson, E. Díaz-Ferguson & B. R. Silliman, 2010. Mangrove use by the invasive lionfish Pterois volitans. Marine Ecology Progress Series 401: 291–294.

    Article  Google Scholar 

  • Bearhop, S., C. E. Adams, S. Waldron, R. A. Fuller & H. Macleod, 2004. Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73: 1007–1012.

    Article  Google Scholar 

  • Benkwitt, C. E., 2013. Density-dependent growth in invasive Lionfish (Pterois volitans). PLoS ONE 8: e66995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benkwitt, C. E., 2014. Non-linear effects of invasive lionfish density on native coral-reef fish communities. Biological Invasions 17: 1383–1395.

    Article  Google Scholar 

  • Benkwitt, C. E., 2016a. Central-place foraging and ecological effects of an invasive predator across multiple habitats. Ecology 97: 2729–2739.

    Article  PubMed  Google Scholar 

  • Benkwitt, C. E., 2016b. Invasive lionfish increase activity and foraging movements at greater local densities. Marine Ecology Progress Series 558: 255–266.

    Article  Google Scholar 

  • Bolnick, D. I., R. Svanback, J. A. Fordyce, L. H. Yang, J. M. Davis, C. D. Hulsey & M. L. Forister, 2003. The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161: 1–28.

    Article  PubMed  Google Scholar 

  • Brown, J. H. & B. A. Maurer, 1986. Body size, ecological dominance and Cope’s rule. Nature 324: 248–250.

    Article  Google Scholar 

  • Buchheister, A. & R. J. Latour, 2010. Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Canadian Journal of Fisheries and Aquatic Sciences 67: 445–461.

    Article  CAS  Google Scholar 

  • Byron, D., K. Heck & M. A. Kennedy, 2014. Presence of juvenile lionfish in a Northern Gulf of Mexico nursery habitat. Gulf of Mexico Science 32: 75–77.

    Article  Google Scholar 

  • Callicó Fortunato, R. & E. Avigliano, 2014. Presence of genus Pterois (Oken, 1817) (Scorpaeniformes, Scorpaenidae): extension of invasive range in Caribbean Sea and first published record for Los Frailes Archipelago. Journal of Fisheries Sciences 8: 88–91.

    Google Scholar 

  • Caut, S., E. Angulo & F. Courchamp, 2008. Dietary shift of an invasive predator: rats, seabirds and sea turtles. Journal of Applied Ecology 45: 428–437.

    Article  PubMed  Google Scholar 

  • Chapman, L. J., W. C. Mackay & C. W. Wilkinson, 1989. Feeding flexibility in Northern pike (Esox lucius): fish versus invertebrate prey. Canadian Journal of Fisheries and Aquatic Sciences 46: 666–669.

    Article  Google Scholar 

  • Charnov, E. L., 1976. Optimal foraging, the marginal value theorem. Theoretical Population Biology 9: 129–136.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, K. R. & R. M. Warwick, 2001. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd ed. PRIMER-E, Plymouth: 172.

    Google Scholar 

  • Claydon, J. A. B., M. C. Calosso & S. B. Traiger, 2012. Progression of invasive lionfish in seagrass, mangrove and reef habitats. Marine Ecology Progress Series 448: 119–129.

    Article  Google Scholar 

  • Cocheret de la Morinière, E., B. J. A. Pollux, I. Nagelkerken, M. A. Hemminga, A. H. L. Huiskes & G. van der Velde, 2003a. Ontogenetic dietary changes of coral reef fishes in the mangrove–seagrass–reef continuum: stable isotopes and gut-content analysis. Marine Ecology Progress Series 246: 279–289.

    Article  Google Scholar 

  • Cocheret de la Morinière, E., B. J. A. Pollux, I. Nagelkerken & G. van der Velde, 2003b. Diet shifts of Caribbean grunts (Haemulidae) and snappers (Lutjanidae) and the relation with nursery-to-coral reef migrations. Estuarine, Coastal and Shelf Science 57: 1079–1089.

    Article  Google Scholar 

  • Côté, I. M., S. J. Green, J. A. Morris, J. L. Akins & D. Steinke, 2013. Diet richness of invasive Indo-Pacific lionfish revealed by DNA barcoding. Marine Ecology Progress Series 472: 249–256.

    Article  Google Scholar 

  • Curtis, J. S., K. R. Wall, M. A. Albins & C. D. Stallings, 2017. Diet shifts in a native mesopredator across a range of invasive lionfish biomass. Marine Ecology Progress Series 573: 215–228.

    Article  Google Scholar 

  • Dahl, K. A. & W. F. Patterson III, 2014. Habitat-specific density and diet of rapidly expanding invasive red lionfish, Pterois volitans, populations in the Northern Gulf of Mexico. PLoS ONE 9: e105852.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dahlgren, C., P. R. Kramer, J. Lang & K. D. Sherman, 2014. New Providence and Rose Island, Bahamas Coral Reef Report Card.

  • Damijan, D., 2006. Intraspecific exploitation competition as cause for density dependent breeding success in the white stork. Waterbirds: The International Journal of Waterbird Biology 29: 391–394.

    Article  Google Scholar 

  • Dance, M. A., W. F. Patterson Iii & D. T. Addis, 2011. Fish community and trophic structure at artificial reef sites in the Northeastern Gulf of Mexico. Bulletin of Marine Science 87: 301–324.

    Article  Google Scholar 

  • Darling, E. S., S. J. Green, J. K. O’Leary & I. M. Côté, 2011. Indo-Pacific lionfish are larger and more abundant on invaded reefs: a comparison of Kenyan and Bahamian lionfish populations. Biological Invasions 13: 2045–2051.

    Article  Google Scholar 

  • Davenport, S. R. & N. J. Bax, 2002. A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Canadian Journal of Fisheries and Aquatic Sciences 59: 514–530.

    Article  Google Scholar 

  • Davis, J. P., K. A. Pitt, B. Fry & R. M. Connolly, 2015. Stable isotopes as tracers of residency for fish on inshore coral reefs. Estuarine, Coastal and Shelf Science 167: 368–376.

    Article  CAS  Google Scholar 

  • DeNiro, M. J. & S. Epstein, 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495–506.

    Article  CAS  Google Scholar 

  • Deniro, M. J. & S. Epstein, 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341–351.

    Article  CAS  Google Scholar 

  • Duffy, J. E., B. J. Cardinale, K. E. France, P. B. McIntyre, E. Thébault & M. Loreau, 2007. The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecology Letters 10: 522–538.

    Article  PubMed  Google Scholar 

  • Eby, L. A., W. J. Roach, L. B. Crowder & J. A. Stanford, 2006. Effects of stocking-up freshwater food webs. Trends in Ecology and Evolution 21: 576–584.

    Article  PubMed  Google Scholar 

  • El-Sabaawi, R. W., M. Trudel, D. L. Mackas, J. F. Dower & A. Mazumder, 2012. Interannual variability in bottom-up processes in the upstream range of the California Current system: an isotopic approach. Progress in Oceanography 106: 16–27.

    Article  Google Scholar 

  • Elton, C. S., 1927. Animal Ecology. Macmillan Co., New York.

    Google Scholar 

  • Evangelista, C., A. Boiche, A. Lecerf & J. Cucherousset, 2014. Ecological opportunities and intraspecific competition alter trophic niche specialization in an opportunistic stream predator. Journal of Animal Ecology 83: 1025–1034.

    Article  PubMed  Google Scholar 

  • Falk-Petersen, J., P. Renaud & N. Anisimova, 2011. Establishment and ecosystem effects of the alien invasive red king crab (Paralithodes camtschaticus) in the Barents Sea – a review. ICES Journal of Marine Science 68: 479–488.

    Article  Google Scholar 

  • Fanelli, E., E. Azzurro, M. Bariche, J. E. Cartes & F. Maynou, 2015. Depicting the novel Eastern Mediterranean food web: a stable isotopes study following Lessepsian fish invasion. Biological Invasions 17: 2163–2178.

    Article  Google Scholar 

  • Ferreira, C. E. L., O. J. Luiz, S. R. Floeter, M. B. Lucena, M. C. Barbosa, C. R. Rocha & L. A. Rocha, 2015. First record of invasive lionfish (Pterois volitans) for the Brazilian Coast. PLoS ONE 10: e0123002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fogg, A. Q., E. R. Hoffmayer, W. B. Driggers, M. D. Campbell, G. J. Pellegrin & W. Stein, 2013. Distribution and length frequency of invasive lionfish (Pterois sp.) in the Northern Gulf of Mexico. Gulf and Caribbean Research. https://doi.org/10.18785/gcr.2501.08.

    Article  Google Scholar 

  • France, R. L., 1995. Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Marine Ecology Progress Series 124: 307–312.

    Article  Google Scholar 

  • Gardner, P. G., T. K. Frazer, C. A. Jacoby & R. P. E. Yanong, 2015. Reproductive biology of invasive lionfish (Pterois spp.). Frontiers in Marine Science. https://doi.org/10.3389/fmars.2015.00007.

    Article  Google Scholar 

  • Goering, J., V. Alexander & N. Haubenstock, 1990. Seasonal variability of stable carbon and nitrogen isotope ratios of organisms in a North Pacific Bay. Estuarine, Coastal and Shelf Science 30: 239–260.

    Article  CAS  Google Scholar 

  • Goubault, M., Y. Outreman, D. Poinsot & A. M. Cortesero, 2005. Patch exploitation strategies of parasitic wasps under intraspecific competition. Behavioral Ecology 16: 693–701.

    Article  Google Scholar 

  • Green, S. J. & I. M. Côté, 2009. Record densities of Indo-Pacific lionfish on Bahamian coral reefs. Coral Reefs 28: 107–107.

    Article  Google Scholar 

  • Green, S. J. & I. M. Côté, 2014. Trait-based diet selection: prey behaviour and morphology predict vulnerability to predation in reef fish communities. Journal of Animal Ecology 83: 1451–1460.

    Article  PubMed  Google Scholar 

  • Green, S. J., J. L. Akins, A. Maljkovic & I. M. Côté, 2012. Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE 7: e32596.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green, S. J., N. K. Dulvy, A. M. L. Brooks, J. L. Akins, A. B. Cooper, S. Miller & I. M. Côté, 2014. Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecological Applications 24: 1311–1322.

    Article  PubMed  Google Scholar 

  • Griffen, B. D., M. Vogel, L. Goulding & R. Hartman, 2015. Energetic effects of diet choice by invasive Asian shore crabs: implications for persistence when prey are scarce. Marine Ecology Progress Series 522: 181–192.

    Article  Google Scholar 

  • Hackerott, S., A. Valdivia, C. E. Cox, N. J. Silbiger & J. F. Bruno, 2017. Invasive lionfish had no measurable effect on prey fish community structure across the Belizean Barrier Reef. PeerJ 5: e3270.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hare, J. A. & P. E. Whitfield, 2003. An Integrated Assessment of the Introduction of Lionfish (Pterois volitans/miles Complex) to the Western Atlantic Ocean. NOAA Technical Memorandum NOS NCCOS, Vol. 2: 21.

  • Harrison, X. A., L. Donaldson, M. E. Correa-Cano, J. Evans, D. N. Fisher, C. E. D. Goodwin, B. S. Robinson, D. J. Hodgson & R. Inger, 2018. A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6: e4794.

  • Hayden, B., A. Massa-Gallucci, C. Harrod, M. O’Grady, J. Caffrey & M. Kelly-Quinn, 2014. Trophic flexibility by roach Rutilus rutilus in novel habitats facilitates rapid growth and invasion success. Journal of Fish Biology 84: 1099–1116.

    Article  CAS  PubMed  Google Scholar 

  • Hempson, T. N., N. A. J. Graham, M. A. MacNeil, D. H. Williamson, G. P. Jones & G. R. Almany, 2017. Coral reef mesopredators switch prey, shortening food chains, in response to habitat degradation. Ecology and Evolution. https://doi.org/10.1002/ece3.2805.

    Article  PubMed  PubMed Central  Google Scholar 

  • Herzka, S. Z. & G. J. Holt, 2000. Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Canadian Journal of Fisheries and Aquatic Sciences 57: 137–147.

    Article  Google Scholar 

  • Hin, V. & A. M. Roos, 2019. Evolution of size-dependent intraspecific competition predicts body size scaling of metabolic rate. Functional Ecology 33: 479–490.

    Article  PubMed  Google Scholar 

  • Holdridge, E. M., C. Cuellar-Gempeler & C. P. terHorst, 2016. A shift from exploitation to interference competition with increasing density affects population and community dynamics. Ecology and Evolution 6: 5333–5341.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hughes, N. F., 1986. Changes in the feeding biology of the Nile perch, Lates niloticus (L.) (Pisces: Centropomidae), in Lake Victoria, East Africa since its introduction in 1960, and its impact on the native fish community of the Nyanza Gulf. Journal of Fish Biology 29: 541–548.

    Article  Google Scholar 

  • Hurtubia, J., 1973. Trophic diversity measurement in sympatric predatory species. Ecology 54: 885–890.

    Article  Google Scholar 

  • Hutchinson, G. E., 1957. Concluding remarks. Cold Spring Harbour Symposium on Quantitative Biology 22: 415–427.

    Article  Google Scholar 

  • Ingeman, K. E., 2016. Lionfish cause increased mortality rates and drive local extirpation of native prey. Marine Ecology Progress Series 558: 235–245.

    Article  Google Scholar 

  • Ingeman, K. E. & M. S. Webster, 2015. Native prey mortality increases but remains density-dependent following lionfish invasion. Marine Ecology Progress Series 531: 241–252.

    Article  Google Scholar 

  • Jackson, A. L., R. Inger, A. C. Parnell & S. Bearhop, 2011. Comparing isotopic niche widths among and within communities: SIBER – Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80: 595–602.

    Article  PubMed  Google Scholar 

  • Jackson, M. C., I. Donohue, A. L. Jackson, J. R. Britton, D. M. Harper & J. Grey, 2012. Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS ONE 7: e31757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jennings, S., S. P. R. Greenstreet, L. Hill, G. Piet, J. K. Pinnegar & K. J. Warr, 2002. Long-term trends in the trophic structure of the North Sea fish community: evidence from stable-isotope analysis, size-spectra and community metrics. Marine Biology 141: 1085–1097.

    Article  Google Scholar 

  • Jørgensen, S. E. & Y. M. Svirezhev, 2004. Chapter 9 – Thermodynamics of Ecological Networks Towards a Thermodynamic Theory for Ecological Systems. Pergamon, Oxford: 221–241.

    Book  Google Scholar 

  • Kadye, W. T. & A. J. Booth, 2012. Detecting impacts of invasive non-native sharptooth catfish, Clarias gariepinus, within invaded and non-invaded rivers. Biodiversity and Conservation 21: 1997–2015.

    Article  Google Scholar 

  • Lamb, K. & P. K. Swart, 2008. The carbon and nitrogen isotopic values of particulate organic material from the Florida Keys: a temporal and spatial study. Coral Reefs 27: 351–362.

    Article  Google Scholar 

  • Layman, C. A. & J. E. Allgeier, 2012. Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in The Bahamas. Marine Ecology Progress Series 448: 131–141.

    Article  Google Scholar 

  • Layman, C. A., D. A. Arrington, C. G. Montaña & D. M. Post, 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42–48.

    Article  PubMed  Google Scholar 

  • Layman, C. A., M. S. Araujo, R. Boucek, C. M. Hammerschlag-Peyer, E. Harrison, Z. R. Jud, P. Matich, A. E. Rosenblatt, J. J. Vaudo, L. A. Yeager, D. M. Post & S. Bearhop, 2012. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews of the Cambridge Philosophical Society 87: 545–562.

    Article  PubMed  Google Scholar 

  • Marques, T. S., N. R. F. Lara, L. A. B. Bassetti, C. I. Piña, P. B. Camargo & L. M. Verdade, 2013. Intraspecific isotopic niche variation in broad-snouted caiman (Caiman latirostris). Isotopes in Environmental and Health Studies 49: 325–335.

    Article  CAS  PubMed  Google Scholar 

  • Marra, P. P., K. A. Hobson & R. T. Holmes, 1998. Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282: 1884–1886.

    Article  CAS  PubMed  Google Scholar 

  • McKinney, M. L. & J. L. Lockwood, 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution 14: 450–453.

    Article  CAS  PubMed  Google Scholar 

  • McMahon, K. W., L. Ling Hamady & S. R. Thorrold, 2013. A review of ecogeochemistry approaches to estimating movements of marine animals. Limnology and Oceanography 58: 697–714.

    Article  CAS  Google Scholar 

  • Minagawa, M. & E. Wada, 1984. Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48: 1135–1140.

    Article  CAS  Google Scholar 

  • Montoya, J. P., 2007. Natural abundance of 15N in marine planktonic ecosystems. In Michener, R. & K. Lajtha (eds), Stable Isotopes in Ecology and Environmental Science, 2nd ed. Blackwell Publishing Ltd., Oxford: 176–201.

    Chapter  Google Scholar 

  • Morillo-Velarde, P. S., P. Briones-Fourzán, L. Álvarez-Filip, S. Aguíñiga-García, A. Sánchez-González & E. Lozano-Álvarez, 2018. Habitat degradation alters trophic pathways but not food chain length on shallow Caribbean coral reefs. Scientific Reports 8: 4109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris, J. A., 2009. The biology and ecology of the invasive Indo-Pacific lionfish. PhD Thesis, North Carolina State University, Raleigh, North Carolina, 168 pp.

  • Morris, J. A. & J. L. Akins, 2009. Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian Archipelago. Environmental Biology of Fishes 86: 389–398.

    Article  Google Scholar 

  • Muñoz, R. C., C. A. Currin & P. E. Whitfield, 2011. Diet of invasive lionfish on hard bottom reefs of the Southeast USA: insights from stomach contents and stable isotopes. Marine Ecology Progress Series 432: 181–193.

    Article  Google Scholar 

  • Nahon, S., S. Séité, J. Kolasinski, P. Aguirre & I. Geurden, 2017. Effects of euthanasia methods on stable carbon (δ13C value) and nitrogen (δ15N value) isotopic compositions of fry and juvenile rainbow trout Oncorhynchus mykiss. Rapid Communications in Mass Spectrometry 31: 1742–1748.

    Article  CAS  PubMed  Google Scholar 

  • Nurkse, K., J. Kotta, H. Orav-Kotta & H. Ojaveer, 2016. A successful non-native predator, round goby, in the Baltic Sea: generalist feeding strategy, diverse diet and high prey consumption. Hydrobiologia 777: 271–281.

    Article  CAS  Google Scholar 

  • Nuttall, M. F., M. A. Johnston, R. J. Eckert, J. A. Embesi, E. L. Hickerson & G. P. Schmahl, 2014. Lionfish (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) records within mesophotic depth ranges on natural banks in the Northwestern Gulf of Mexico. BioInvasions Records 3: 111–115.

    Article  Google Scholar 

  • O’Farrell, S., S. Bearhop, R. A. R. McGill, C. P. Dahlgren, D. R. Brumbaugh & P. J. Mumby, 2014. Habitat and body size effects on the isotopic niche space of invasive lionfish and endangered Nassau grouper. Ecosphere. https://doi.org/10.1890/ES14-00126.1.

    Article  Google Scholar 

  • O’Reilly, C. M., R. E. Hecky, A. S. Cohen & P. D. Plisnier, 2002. Interpreting stable isotopes in food webs: recognizing the role of time averaging at different trophic levels. Limnology and Oceanography 47: 306–309.

    Article  Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens & H. Wagner, 2016. Vegan: Community Ecology Package. R package version 2.3-4 [available on internet at http://CRAN.R-project.org/package=vegan]. Accessed 15 Feb 2014.

  • Pagani-Núñez, E., C. A. Barnett, H. Gu & E. Goodale, 2016. The need for new categorizations of dietary specialism incorporating spatio-temporal variability of individual diet specialization. Journal of Zoology 300: 1–7.

    Article  Google Scholar 

  • Parnell, A. & A. L. Jackson, 2013. SIAR: stable isotope analysis in R. R package version 4.2 [available on internet at http://CRAN.R-project.org/package=siar]. Accessed 23 March 2014.

  • Peake, J., A. K. Bogdanoff, C. A. Layman, B. Castillo, K. Reale-Munroe, J. Chapman, K. Dahl, W. F. Patterson III, C. Eddy, R. D. Ellis, M. Faletti, N. Higgs, M. A. Johnston, R. C. Muñoz, V. Sandel, J. C. Villasenor-Derbez & J. A. Morris, 2018. Feeding ecology of invasive lionfish (Pterois volitans and Pterois miles) in the temperate and tropical western Atlantic. Biological Invasions 20: 2567–2597.

    Article  Google Scholar 

  • Peck, D. R., L. Faulquier, P. Pinet, S. Jaquemet & M. Le Corre, 2008. Feral cat diet and impact on sooty terns at Juan de Nova Island, Mozambique Channel. Animal Conservation 11: 65–74.

    Article  Google Scholar 

  • Pimiento, C., J. C. Nifong, M. E. Hunter, E. Monaco & B. R. Silliman, 2015. Habitat use patterns of the invasive red lionfish Pterois volitans: a comparison between mangrove and reef systems in San Salvador, Bahamas. Marine Ecology 36: 28–37.

    Article  Google Scholar 

  • Post, D. M., C. A. Layman, D. A. Arrington, G. Takimoto, J. Quattrochi & C. G. Montana, 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179–189.

    Article  PubMed  Google Scholar 

  • R Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna [available on internet at https://www.R-project.org/]. Accessed 10 June 2015.

  • Radabaugh, K. R., D. J. Hollander & E. B. Peebles, 2013. Seasonal δ13C and δ15N isoscapes of fish populations along a continental shelf trophic gradient. Continental Shelf Research 68: 112–122.

    Article  Google Scholar 

  • Ribeiro, F., R. L. Orjuela, M. F. Magalhães & M. J. Collares-Pereira, 2007. Variability in feeding ecology of a South American cichlid: a reason for successful invasion in Mediterranean-type rivers? Ecology of Freshwater Fish 16: 559–569.

    Article  Google Scholar 

  • Ricciardi, A. & J. B. Rasmussen, 1998. Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Canadian Journal of Fisheries and Aquatic Sciences 55: 1759–1765.

    Article  Google Scholar 

  • Robertson, D. R. & K. W. Kaufmann, 1998. Assessing early recruitment dynamics and its demographic consequences among tropical reef fishes: accommodating variation in recruitment seasonally and longevity. Australian Journal of Ecology 23: 226–233.

    Article  Google Scholar 

  • Rocha, L. A., C. R. Rocha, C. C. Baldwin, L. A. Weigt & M. McField, 2015. Invasive lionfish preying on critically endangered reef fish. Coral Reefs 34: 803–806.

    Article  Google Scholar 

  • Ruffino, L., J. C. Russell, B. Pisanu, S. Caut & E. Vidal, 2011. Low individual-level dietary plasticity in an island-invasive generalist forager. Population Ecology 53: 535–548.

    Article  Google Scholar 

  • Sale, P. F., 2004. Connectivity, recruitment variation, and the structure of reef fish communities. Integrative and Comparative Biology 44: 390–399.

    Article  PubMed  Google Scholar 

  • Schmidt, S. N., J. D. Olden, C. T. Solomon & M. J. V. Zanden, 2007. Quantitative approaches to the analysis of stable isotope food web data. Ecology 88: 2793–2802.

    Article  PubMed  Google Scholar 

  • Schofield, P. J., 2009. Geographic extent and chronology of the invasion of non-native lionfish (Pterois volitans [Linnaeus 1758] and P. miles [Bennett 1828]) in the Western North Atlantic and Caribbean Sea. Aquatic Invasions 4: 473–479.

    Article  Google Scholar 

  • Schofield, P. J., 2010. Update on geographic spread of invasive lionfishes (Pterois volitans [Linnaeus, 1758] and P. miles [Bennett, 1828]) in the Western North Atlantic Ocean, Caribbean Sea and Gulf of Mexico. Aquatic Invasions 5: S117–S122.

    Article  Google Scholar 

  • Smith, N. S., S. J. Green, J. L. Akins, S. Miller & I. M. Côté, 2017. Density-dependent colonization and natural disturbance limit the effectiveness of invasive lionfish culling efforts. Biological Invasions 19: 2385–2399.

    Article  Google Scholar 

  • Tamburello, N. & I. M. Côté, 2015. Movement ecology of Indo-Pacific lionfish on Caribbean coral reefs and its implications for invasion dynamics. Biological Invasions 17: 1639–1653.

    Article  Google Scholar 

  • Tillberg, C. V., D. A. Holway, E. G. Lebrun & A. V. Suarez, 2007. Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proceedings of the National Academy of Sciences of the United States of America 104: 20856–20861.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tilley, A., J. López-Angarita & J. R. Turner, 2013. Diet reconstruction and resource partitioning of a Caribbean marine mesopredator using stable isotope Bayesian modelling. PLoS ONE 8: e79560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tornabene, L. & C. C. Baldwin, 2017. A new mesophotic goby, Palatogobius incendius (Teleostei: Gobiidae), and the first record of invasive lionfish preying on undescribed biodiversity. PLoS ONE 12: e0177179.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trégarot, E., M. Fumaroli, A. Arqué, C. Hellio & J.-P. Maréchal, 2015. First records of the red lionfish (Pterois volitans) in Martinique, French West Indies: monitoring invasion status through visual surveys. Marine Biodiversity Records 8: e1.

    Article  Google Scholar 

  • Turner, T. F., M. L. Collyer & T. J. Krabbenhoft, 2010. A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91: 2227–2233.

    Article  PubMed  Google Scholar 

  • Villéger, S., J. Ramos Miranda, D. Flores Hernandez, A. Sosa Lopez & D. Mouillot, 2008. Stable trophic structure across coastal nekton assemblages despite high species turnover. Marine Ecology Progress Series 364: 135–146.

    Article  Google Scholar 

  • Vizzini, S. & A. Mazzola, 2003. Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Marine Biology 142: 1009–1018.

    Article  CAS  Google Scholar 

  • Ward-Paige, C. A., M. J. Risk & O. A. Sherwood, 2005. Reconstruction of nitrogen sources on coral reefs: δ15N and δ13C in gorgonians from Florida Reef Tract. Marine Ecology Progress Series 296: 155–163.

    Article  CAS  Google Scholar 

  • Weidel, B. C., S. R. Carpenter, J. F. Kitchell & M. J. Vander Zanden, 2011. Rates and components of carbon turnover in fish muscle: insights from bioenergetics models and a whole-lake 13C addition. Canadian Journal of Fisheries and Aquatic Sciences 68: 387–399.

    Article  CAS  Google Scholar 

  • Whitfield, P. E., J. A. Hare, A. W. David, S. L. Harter, R. C. Muñoz & C. M. Addison, 2007. Abundance estimates of the Indo-Pacific lionfish Pterois volitans/miles complex in the Western North Atlantic. Biological Invasions 9: 53–64.

    Article  Google Scholar 

  • Wyatt, A. S. J., A. M. Waite & S. Humphries, 2012. Stable isotope analysis reveals community-level variation in fish trophodynamics across a fringing coral reef. Coral Reefs 31: 1029–1044.

    Article  Google Scholar 

  • Zuur, A. F., E. N. Ieno & C. S. Elphick, 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3–14.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Stuart Cove’s Dive Bahamas for generously donating logistic support for fieldwork in the Bahamas, and Lad Akins and many volunteers with the Reef Environmental Education Foundation for assistance with collecting lionfish for this study. We also thank Amber Richmond, Christine Konrad, Dickson Wong, Melissa Englouen, and Roxanne-Liana Francisca for their help in processing samples for SIA.

Funding

LMC was supported by Scholarships from the National Council for Research and Technology of Mexico (CONACyT; Grant Number 311409) and Simon Fraser University (SFU), as well as through a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to IMC.

Author information

Author notes

  1. Luis Malpica-Cruz

    Present address: Instituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja California, 22860, Ensenada, Baja California, Mexico

Authors and Affiliations

  1. Earth to Ocean Research Group, Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6, Canada

    Luis Malpica-Cruz & Isabelle M. Côté

  2. ECOCIMATI A.C., 22800, Ensenada, Baja California, Mexico

    Luis Malpica-Cruz

  3. Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada

    Stephanie J. Green

Authors
  1. Luis Malpica-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephanie J. Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabelle M. Côté
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luis Malpica-Cruz.

Ethics declarations

Conflict of interest

All authors declare that they have no conflicts of interest.

Ethical approval

All national and institutional guidelines concerning the care and use of animals were followed.

Additional information

Handling editor: Michael Power

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Malpica-Cruz, L., Green, S.J. & Côté, I.M. Temporal and ontogenetic changes in the trophic signature of an invasive marine predator. Hydrobiologia 839, 71–86 (2019). https://doi.org/10.1007/s10750-019-03996-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-03996-2

Keywords

Search

Navigation