Skip to main content
SpringerLink
Log in

Two is better than one: combining gut content and stable isotope analyses to infer trophic interactions between native and invasive species

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

Abstract

Two complementary approaches are commonly used for analysing trophic interactions that allow inferences about consumed and assimilated resources: gut content (GCA) and stable isotope (SIA) analyses. We used these methods to assess the trophic ecology of a native (Pontastacus leptodactylus) and an invasive species (Faxonius limosus) of crayfish in the Lower Danube (Romania) by calculating five frequently used metrics (i.e. trophic position, omnivory index, elemental imbalance for C:N ratio, trophic niche width and overlap). The SIA approach indicated significantly different trophic niche widths between the crayfish species and potential resource partitioning that triggered lower niche overlap, aspects not depicted by GCA. The latter approach suggested higher omnivory indices and elemental imbalance for macronutrients, potentially because of high incidences of basal resources with low nitrogen content in the foreguts of both species. Although, as indicated by GCA, the two species seem to feed largely on the same resources, SIA suggested that the ingested food items were assimilated with differing efficiencies. These findings are of importance for studies of invasion biology, where the replacement of native species by invasive taxa is underpinned by mechanisms that should be explored by using the most appropriate approach.

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

References

  • 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 

  • Beatty, S. J., 2006. The diet and trophic positions of translocated, sympatric populations of Cherax destructor and Cherax cainii in the Hutt River, Western Australia: evidence of resource overlap. Marine and Freshwater Research 57: 825–835.

    Article  CAS  Google Scholar 

  • Bøhn, T. & P. A. Amundsen, 2001. The competitive edge of an invading specialist. Ecology 82: 2150–2163.

    Article  Google Scholar 

  • Bøhn, T., P. A. Amundsen & A. Sparrow, 2008. Competitive exclusion after invasion? Biological Invasions 10: 359–368.

    Article  Google Scholar 

  • Brabrand, Å. & B. Faafeng, 1993. Habitat shift in roach (Rutilus rutilus) induced by pikeperch (Stizostedion lucioperca) introduction: predation risk versus pelagic behaviour. Oecologia 95: 38–46.

    Article  PubMed  Google Scholar 

  • Brunner, E. & M. L. Puri, 2001. Nonparametric methods in factorial designs. Statistical Papers 42: 1–52.

    Article  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2001. Kullback-Leibler information as a basis for strong inference in ecological studies. Wildlife Research 28: 111–119.

    Article  Google Scholar 

  • Christensen, V. & C. J. Walters, 2004. Ecopath with ecosim: methods, capabilities and limitations. Ecological Modelling 172: 109–139.

    Article  Google Scholar 

  • Cleveland, A. & W. Montgomery, 2003. Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomacentridae: Stegastes dorsopunicans and S. planifrons). Marine Biology 142: 35–44.

    Article  CAS  Google Scholar 

  • Cross, W. F., J. P. Benstead, A. D. Rosemond & J. B. Wallace, 2003. Consumer-resource stoichiometry in detritus-based streams. Ecology Letters 6: 721–732.

    Article  Google Scholar 

  • Davis, A. M., M. L. Blanchette, B. J. Pusey, T. D. Jardine & R. G. Pearson, 2012. Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river. Freshwater Biology 57: 2156–2172.

    Article  CAS  Google Scholar 

  • Eloranta, A. P., R. Knudsen & P. A. Amunsen, 2013. Niche segregation of coexisting Arctic charr (Salvelinus alpinus) and brown trout (Salmo trutta) constrains food web coupling in subarctic lakes. Freshwater Biology 58: 207–221.

    Article  Google Scholar 

  • Ercoli, F., T. J. Ruokonen, H. Hamalainen & R. I. Jones, 2014. Does the introduced signal crayfish occupy an equivalent trophic niche to the lost native noble crayfish in boreal lakes? Biological Invasions 16: 2025–2036.

    Article  Google Scholar 

  • Filipová, L., D. A. Lieb, F. Grandjean & A. Petrusek, 2011. Haplotype variation in the spiny-cheek crayfish Orconectes limosus: colonization of Europe and genetic diversity of native stocks. Freshwater Science 30: 871–881.

    Google Scholar 

  • Fitzsimons, J. D., J. L. Jonas, R. M. Claramunt, B. Williston, G. Williston, J. E. Marsden, B. J. Ellrott & D. C. Honeyfield, 2007. Influence of egg predation and physical disturbance on lake trout Salvelinus namaycush egg mortality and implications for life-history theory. Journal of Fish Biology 71: 1–16.

    Article  Google Scholar 

  • Franssen, N. R. & K. B. Gido, 2006. Use of stable isotopes to test literature-based trophic classifications of small-bodied stream fishes. The American Midland Naturalist 156: 1–10.

    Article  Google Scholar 

  • González, A. L., J. S. Kominoski, M. Danger, S. Ishida, N. Iwai & A. Rubach, 2010. Can ecological stoichiometry help explain patterns of biological invasions? Oikos 119: 779–790.

    Article  Google Scholar 

  • Gotelli, N.J., E.M. Hart & A.M. Ellison, 2015. Co-occurrence analysis. EcoSim R.

  • Guzzo, M. M., G. D. Haffner, N. D. Legler, S. A. Rush & A. T. Fisk, 2013. Fifty years later: trophic ecology and niche overlap of a native and non-indigenous fish species in the western basin of Lake Erie. Biological Invasions 15: 1695–1711.

    Article  Google Scholar 

  • Higgins, J. J. & S. Tashtoush, 1994. An aligned rank transform test for interaction. Nonlinear World 1: 201–211.

    Google Scholar 

  • Ho, C. T., S. J. Kao, C. F. Dai, H. L. Hsieh, F. K. Shiah & R. Q. Jan, 2007. Dietary separation between two blennies and the Pacific gregory in northern Taiwan: evidence from stomach content and stable isotope analyses. Marine Biology 151: 729–736.

    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. & J. R. Britton, 2014. Divergence in the trophic niche of sympatric freshwater invaders. Biological Invasions 16: 1095–1103.

    Article  Google Scholar 

  • Jackson, M. C., A. L. Jackson, J. R. Britton, I. Donohue, D. 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 

  • Jackson, M. C., T. Jones, M. Milligan, D. Sheath, J. Taylor, A. Ellis, J. England & J. Grey, 2014. Niche differentiation among invasive crayfish and their impacts on ecosystem structure and functioning. Freshwater Biology 59: 1123–1135.

    Article  Google Scholar 

  • Jackson, M. C., C. Evangelista, T. Zhao, A. Lecerf, R. Britton & J. Cucherousset, 2017. Between-lake variation in the trophic ecology of an invasive crayfish. Freshwater Biology 62: 1501–1510.

    Article  Google Scholar 

  • Johnson, P. T. J., J. D. Olden, C. T. Solomon & M. J. Vander Zanden, 2009. Interactions among invaders: community and ecosystem effects of multiple invasive species in an experimental aquatic system. Oecologia 159: 161–170.

    Article  PubMed  Google Scholar 

  • Jones, J. I. & S. Waldron, 2003. Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes. Freshwater Biology 48: 1396–1407.

    Article  Google Scholar 

  • Kadye, W. T. & A. J. Booth, 2012. Integrating stomach content and stable isotope analyses to elucidate the feeding habits of non-native sharptooth catfish Clarias gariepinus. Biological Invasions 14: 779–795.

    Article  Google Scholar 

  • Lauridsen, R. B., F. K. Edwards, M. J. Bowes, G. Woodward, A. Hildrew, A. T. Ibbotson & J. I. Jones, 2012. Consumer–resource elemental imbalances in a nutrient-rich stream. Freshwater Science 31: 408–422.

    Article  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 87: 545–562.

    Article  PubMed  Google Scholar 

  • Levins, R., 1968. Evolution in Changing Environments: Some Theoretical Explorations. (MPB-2). Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Magoulick, D. D. & G. L. Piercey, 2016. Trophic overlap between native and invasive stream crayfish. Hydrobiologia 766: 237–246.

    Article  Google Scholar 

  • Marufu, L. T., T. Dalu, C. Phiri & T. Nhiwatiwa, 2017. Diet composition changes in tigerfish of Lake Kariba following an invasion by redclaw crayfish. Annales de Limnologie-International Journal of Limnology 53: 47–56.

    Article  Google Scholar 

  • Marufu, L. T., T. Dalu, P. Crispen, M. Barson, R. Simango, B. Utete & T. Nhiwatiwa, 2018. The diet of an invasive crayfish, Cherax quadricarinatus (Von Martens, 1868), in Lake Kariba, inferred using stomach content and stable isotope analyses. BioInvasions Records 7: 121–132.

    Article  Google Scholar 

  • Merritt, R. W. & K. W. Cummins (eds), 1996. An Introduction to the Aquatic Insects of North America. Kendall/Hunt, Dubuque, Iowa.

    Google Scholar 

  • Moore, J. W. & B. X. Semmens, 2008. Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11: 470–480.

    Article  PubMed  Google Scholar 

  • Olden, J. D., J. M. McCarthy, J. T. Maxted, W. W. Fetzer & M. J. Vander Zanden, 2006. The rapid spread of rusty crayfish (Orconectes rusticus) with observations on native crayfish declines in Wisconsin (USA) over the past 130 years. Biological Invasions 8: 1621–1628.

    Article  Google Scholar 

  • Olsson, K., P. Nyström, P. Stenroth, E. Nilsson, M. Svensson & W. Granéli, 2008. The influence of food quality and availability on trophic position, carbon signature, and growth rate of an omnivorous crayfish. Canadian Journal of Fisheries and Aquatic Sciences 65: 2293–2304.

    Article  CAS  Google Scholar 

  • Olsson, K., P. Stenroth, P. Nyström & W. Granéli, 2009. Invasions and niche width: does niche width of an introduced crayfish differ from a native crayfish? Freshwater Biology 54: 1731–1740.

    Article  Google Scholar 

  • Parnell, A. C., D. L. Phillips, S. Bearhop, B. X. Semmens, E. J. Ward, J. Moore, A. L. Jackson, J. Grey, D. J. Kelly & R. Inger, 2013. Bayesian stable isotope mixing models. Environmetrics 24: 387–399.

    Google Scholar 

  • Pârvulescu, L., M. Pîrvu, L. G. Moroşan & C. Zaharia, 2015. Plasticity in fecundity highlights the females’ importance in the spiny-cheek crayfish invasion mechanism. Zoology 118: 424–432.

    Article  PubMed  Google Scholar 

  • Phillips, B. L. & R. Shine, 2006. An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proceedings of the Royal Society B: Biological Sciences 273: 1545–1550.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pianka, E. R., 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4: 53–74.

    Article  Google Scholar 

  • Puky, M. & P. Schád, 2006. Orconectes limosus colonises new areas fast along the Danube in Hungary. Knowledge and Management of Aquatic Ecosystems 381: 919–926.

    Article  Google Scholar 

  • R Core Team, 2017. R: a language and environment for statistical analyses. Austria, Vienna.

    Google Scholar 

  • Rasmussen, J. B., 2010. Estimating terrestrial contribution to stream invertebrates and periphyton using a gradient-based mixing model for δ13C. Journal of Animal Ecology 79: 393–402.

    Article  PubMed  Google Scholar 

  • Rebrina, F., J. Skejo, A. Lucić & S. Hudina, 2015. Trait variability of the signal crayfish (Pacifastacus leniusculus) in a recently invaded region reflects potential benefits and trade-offs during dispersal. Aquatic Invasions 10: 41–50.

    Article  Google Scholar 

  • Richter, S. J., 1999. Nearly exact tests in factorial experiments using the aligned rank transform. Journal of Applied Statistics 26: 203–217.

    Article  Google Scholar 

  • Roth, B. M., C. L. Hein & M. J. Vander Zanden, 2006. Using bioenergetics and stable isotopes to assess the trophic role of rusty crayfish (Orconectes rusticus) in lake littoral zones. Canadian Journal of Fisheries and Aquatic Sciences 63: 335–344.

    Article  Google Scholar 

  • Rybczynski, S. M., D. M. Walters, K. M. Fritz & B. R. Johnson, 2008. Comparing trophic position of stream fishes using stable isotope and gut contents analyses. Ecology of Freshwater Fish 17: 199–206.

    Article  Google Scholar 

  • Sharma, C. M. & R. Borgstrøm, 2008. Shift in density, habitat use, and diet of perch and roach: an effect of changed predation pressure after manipulation of pike. Fisheries Research 91: 98–106.

    Article  Google Scholar 

  • Sjödin, H., J. Ripa & P. Lundberg, 2018. Principles of niche expansion. Proceedings of the Royal Society B: Biological Sciences 285: 20182603.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stenroth, P., N. Holmqvist, P. Nystrom, O. Berglund, P. Larsson & W. Graneli, 2006. Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment, and season. Canadian Journal of Fisheries and Aquatic Sciences 63: 821–833.

    Article  CAS  Google Scholar 

  • Svanbäck, R. & D. I. Bolnick, 2006. Intraspecific competition drives increased resource use diversity within a natural population. Proceedings of the Royal Society B: Biological Sciences 274: 839–844.

    Article  PubMed Central  Google Scholar 

  • Syväranta, J., A. Lensu, T. J. Marjomäki, S. Oksanen & R. I. Jones, 2013. An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from isotope data. PLoS ONE 8: e56094.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Therry, L., E. Lefevre, D. Bonte & R. Stoks, 2014. Increased activity and growth rate in the non-dispersive aquatic larval stage of a damselfly at an expanding range edge. Freshwater Biology 59: 1266–1277.

    Article  Google Scholar 

  • Vander Zanden, M. J., G. Cabana & J. B. Rasmussen, 1997. Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences 54: 1142–1158.

    Article  Google Scholar 

  • Vander Zanden, M. J., J. Casselman & J. B. Rasmussen, 1999. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401: 464–467.

    Article  CAS  Google Scholar 

  • Webb, C. O., D. D. Ackerly, M. A. McPeek & M. J. Donoghue, 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33: 475–505.

    Article  Google Scholar 

  • Weber, M., 1999. The aim and structure of ecological theory. Philosophy of Science 66: 71–93.

    Article  Google Scholar 

  • Whitledge, G. W. & C. F. Rabeni, 1997. Energy sources and ecological role of crayfishes in an Ozark stream: insights from stable isotopes and gut analysis. Canadian Journal of Fisheries and Aquatic Sciences 54: 2555–2563.

    Article  Google Scholar 

  • Wobbrock, J. O., L. Findlater, D. Gergle & J. J. Higgins, 2011. The aligned rank transform for nonparametric factorial analyses using only ANOVA procedures. In: Proceedings of the SIGCHI Conference on Human Factors in Computing Systems, Vancouver, British Columbia. ACM Press, New York, pp. 143–146.

  • Woodward, G. & A. G. Hildrew, 2002. Food web structure in riverine landscapes. Freshwater Biology 47: 777–798.

    Article  Google Scholar 

  • Zambrano, L., E. Valiente & M. J. Vander Zanden, 2010. Food web overlap among native axolotl (Amblystoma mexicanum) and two exotic fishes: carp (Cyprinus carpio) and tilapia (Oreochromis niloticus) in Xochimilco, Mexico City. Biological Invasions 12: 3061–3069.

    Article  Google Scholar 

  • Závorka, L., M. Buoro & J. Cucherousset, 2018. The negative ecological impacts of a globally introduced species decrease with time since introduction. Global Change Biology 24: 4428–4437.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by a grant from the Romanian National Authority for Scientific Research and Innovation (UEFISCDI) project number PN-II-RU-TE-2014-4-0785. We are grateful to three anonymous reviewers who provided valuable comments on this manuscript.

Author information

Authors and Affiliations

  1. Department of Biology-Chemistry, Faculty of Chemistry, Biology, Geography, West University of Timisoara, 300115, Timisoara, Romania

    Octavian Pacioglu & Lucian Pârvulescu

  2. National Institute of Research and Development for Biological Sciences, 060031, Bucharest, Romania

    Octavian Pacioglu

  3. Institute for Environmental Sciences, University of Koblenz-Landau, Fortstraße 7, 76829, Landau, Germany

    Jochen P. Zubrod & Ralf Schulz

  4. Eußerthal Ecosystem Research Station, University of Koblenz-Landau, Birkenthalstraße 13, 76857, Eußerthal, Germany

    Jochen P. Zubrod

  5. School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS, UK

    J. Iwan Jones

Authors
  1. Octavian Pacioglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jochen P. Zubrod
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ralf Schulz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Iwan Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lucian Pârvulescu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Octavian Pacioglu.

Additional information

Handling editor: Andrew Dzialowski

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pacioglu, O., Zubrod, J.P., Schulz, R. et al. Two is better than one: combining gut content and stable isotope analyses to infer trophic interactions between native and invasive species. Hydrobiologia 839, 25–35 (2019). https://doi.org/10.1007/s10750-019-03990-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-03990-8

Keywords

Search

Navigation