Skip to main content
SpringerLink
Log in

Variation in δ13C and δ15N trophic enrichment factors among Hyalella azteca amphipods from different lakes

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

Abstract

Stable isotopes are a powerful tool used to study the diets of animals because they provide information on food assimilated over an extended period. However, trophic enrichment factors used to reconstruct diets sometimes vary substantially, even among animals from the same trophic level. The goal of this study was to verify if trophic enrichment factors vary among animals as similar as Hyalella azteca amphipods from different lakes. We compared the carbon and nitrogen isotopic compositions of amphipods from different lakes fed on leaf detritus and on periphyton. Amphipods showed significant differences in their trophic enrichment factors among treatments (about 3.0‰ for carbon and nitrogen). The trophic enrichment factor of carbon was more affected by the food type, whereas the trophic enrichment factor of nitrogen was more affected by lake of origin. We estimated that amphipods had a tissue turnover of 25 days for carbon and 34 days for nitrogen. Our study showed that animals from different lakes can exhibit substantial variation in their trophic enrichment factors. This strengthens the view that trophic enrichment factors specific to a study system should be used whenever possible to reconstruct the in situ diet of consumers.

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

Similar content being viewed by others

References

  • Agresti, A., 2011. Categorical data analysis, 2nd ed. John Wiley & Sons, Hoboken.

    Google Scholar 

  • Anderson, N. H. & K. W. Cummins, 1979. Influences of diet on the life histories of aquatic insects. Journal of the Fisheries Research Board of Canada 36: 335–342.

    Article  Google Scholar 

  • Bärlocher, F., 1985. The role of fungi in the nutrition of stream invertebrates. Botanical Journal of the Linnean Society 91: 83–94.

    Article  Google Scholar 

  • Bärlocher, F., 1992. Effects of drying and freezing autumn leaves on leaching and colonization by aquatic hyphomycetes. Freshwater Biology 28: 1–7.

    Article  Google Scholar 

  • Bärlocher, F. & B. Kendrick, 1973. Fungi in the diet of Gammarus pseudolimnaeus (Amphipoda). Oikos 26: 295–300.

    Article  Google Scholar 

  • Boecklen, W. J., C. T. Yarnes, B. A. Cook & A. C. James, 2011. On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution, and Systematics 42: 411–440.

    Article  Google Scholar 

  • Bond, A. L. & A. W. Diamond, 2011. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21: 1017–1023.

    Article  PubMed  Google Scholar 

  • Bosley, K. L., D. A. Witting, R. C. Chambers & S. C. Wainright, 2002. Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Marine Ecology Progress Series 236: 233–240.

    Article  Google Scholar 

  • Bousfield, E. L., 1996. A contribution to the reclassification of neotropical freshwater hyalellid amphipods (Crustacea: Gammaridea, Talitroidea). Bolletino del Museo Civico di Storia Naturale di Verona 20: 175–224.

    Google Scholar 

  • Braun, A., K. Auerswald, A. Vikari & H. Schnyder, 2013. Dietary protein content affects isotopic carbon and nitrogen turnover. Rapid Communications in Mass Spectrometry 27: 2676–2684.

    Article  CAS  PubMed  Google Scholar 

  • Caut, S., E. Angulo & F. Courchamp, 2008. Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Functional Ecology 22: 255–263.

    Article  Google Scholar 

  • Caut, S., E. Angulo & F. Courchamp, 2009. Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46: 443–453.

    Article  CAS  Google Scholar 

  • Cerling, T. E., L. K. Ayliffe, M. D. Dearing, J. R. Ehleringer, B. H. Passey, D. W. Podlesak, A.-M. Torregrossa & A. G. West, 2007a. Determining biological tissue turnover using stable isotopes: the reaction progress variable. Oecologia 151: 175–189.

    Article  PubMed  Google Scholar 

  • Cerling, T. E., G. J. Bowen, J. R. Ehleringer & M. Sponheimer, 2007b. The reaction progress variable and isotope turnover in biological systems. In Dawson, T. E. & R. T. W. Siegwolf (eds.), Stable Isotopes as Indicators of Ecological Change. Academic Press, New York: 163–171.

    Chapter  Google Scholar 

  • Cooper, W. E., 1965. Dynamics and production of a natural population of a fresh-water amphipod, Hyalella azteca. Ecological Monographs 35: 377–394.

    Article  Google Scholar 

  • Cothran, R. D., K. A. Henderson, D. Schmidenberg & R. A. Relyea, 2013. Phenotypically similar but ecologically distinct: differences in competitive ability and predation risk among amphipods. Oikos 122: 1429–1440.

    Google Scholar 

  • Crawley, K. R., G. A. Hyndes & M. A. Vanderklift, 2007. Variation among diets in discrimination of δ13C and δ15N in the amphipod Allorchestes compressa. Journal of Experimental Marine Biology and Ecology 349: 370–377.

    Article  CAS  Google Scholar 

  • Cummins, K. W. & M. J. Klug, 1979. Feeding ecology of stream invertebrates. Annual Review of Ecology and Systematics 10: 147–172.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dionne, K., 2009. Structure d’une communauté d’amphipodes Hyalella azteca et sa consommation des détritus organiques selon la saison dans la zone littorale d’un lac boréal. M. Sc. thesis, Université du Québec à Rimouski, Rimouski (Québec, Canada).

  • Dionne, K., 2015. Coexistence d’un complexe d’espèces cryptiques à des échelles locales et régionales. Ph. D. thesis, Université du Québec à Rimouski, Rimouski (Québec, Canada).

  • Dionne, K., F. Charles & C. Nozais, 2014. Feeding rates of amphipods in boreal lakes: is there a seasonal shift independent of temperature and photoperiod? Hydrobiologia 730: 167–177.

    Article  CAS  Google Scholar 

  • Dionne, K., R. Vergilino, F. Dufresne, F. Charles & C. Nozais, 2011. No evidence for temporal variation in a cryptic species community of freshwater amphipods of the Hyalella azteca species complex. Diversity 3: 390–404.

    Article  Google Scholar 

  • Dodds, W. K., S. M. Collins, S. K. Hamilton, J. L. Tank, S. Johnson, J. R. Webster, K. S. Simon, M. R. Whiles, H. M. Rantala, W. H. McDowell, S. D. Peterson, T. Riis, C. L. Crenshaw, S. A. Thomas, P. B. Kristensen, B. M. Cheever, A. S. Flecker, N. A. Griffiths, T. Crowl, E. J. Rosi-Marshall, R. El-Sabaawi & E. Marti, 2014. You are not always what we think you eat: selective assimilation across multiple whole-stream isotopic tracer studies. Ecology 95: 2757–2767.

    Article  Google Scholar 

  • Fry, B., 2006. Stable Isotope Ecology. Springer, New York.

    Book  Google Scholar 

  • Fry, B. & C. Arnold, 1982. Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54: 200–204.

    Article  Google Scholar 

  • Gaye-Siessegger, J., U. Focken, S. Muetzel, H. Abel & K. Becker, 2004. Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138: 175–183.

    Article  PubMed  Google Scholar 

  • Glon, M. G., E. R. Larson & K. L. Pangle, 2016. Comparison of 13C and 15N discrimination factors and turnover rates between congeneric crayfish Orconectes rusticus and O. virilis (Decapoda, Cambaridae). Hydrobiologia 768: 51–61.

    Article  CAS  Google Scholar 

  • Goedkoop, W., N. Åkerblom & M. H. Demandt, 2006. Trophic fractionation of carbon and nitrogen stable isotopes in Chironomus riparius reared on food of aquatic and terrestrial origin. Freshwater Biology 51: 878–886.

    Article  CAS  Google Scholar 

  • Graça, M. A., 2001. The role of invertebrates on leaf litter decomposition in streams – a review. International Review of Hydrobiology 86: 383–393.

    Article  Google Scholar 

  • Hargrave, B. T., 1970. The utilization of benthic microflora by Hyalella azteca (Amphipoda). Journal of Animal Ecology 39: 427–437.

    Article  Google Scholar 

  • Haubert, D., R. Langel, S. Scheu & L. Ruess, 2005. Effects of food quality, starvation and life stage on stable isotope fractionation in Collembola. Pedobiologia 49: 229–237.

    Article  CAS  Google Scholar 

  • Hobbie, E. A., S. A. Macko & H. H. Shugart, 1999. Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118: 353–360.

    Article  Google Scholar 

  • Hobbie, E. A., N. S. Weber & J. M. Trappe, 2001. Mycorrhizal vs saprotrophic status of fungi: the isotopic evidence. New Phytologist 150: 601–610.

    Article  CAS  Google Scholar 

  • Hobson, K. A. & R. G. Clark, 1992a. Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94: 181–188.

    Article  Google Scholar 

  • Hobson, K. A. & R. G. Clark, 1992b. Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94: 189–197.

    Article  Google Scholar 

  • Hogg, I. D., C. Larose, Y. de Lafontaine & K. G. Doe, 1998. Genetic evidence for a Hyalella species complex within the Great Lakes – St. Lawrence River drainage basin: implications for ecotoxicology and conservation biology. Canadian Journal of Zoology 76: 1134–1152.

    Article  Google Scholar 

  • Jennings, S. & J. van der Molen, 2015. Trophic levels of marine consumers from nitrogen stable isotope analysis: estimation and uncertainty. ICES Journal of Marine Science 72: 2289–2300.

    Article  Google Scholar 

  • Kaufman, M. R., R. R. Gradinger, B. A. Bluhm & D. M. O’Brien, 2008. Using stable isotopes to assess carbon and nitrogen turnover in the Arctic sympagic amphipod Onisimus litoralis. Oecologia 158: 11–22.

    Article  PubMed  Google Scholar 

  • Macko, S. A., W. Y. Lee & P. L. Parker, 1982. Nitrogen and carbon isotope fractionation by two species of marine amphipods: laboratory and field studies. Journal of Experimental Marine Biology and Ecology 63: 145–149.

    Article  Google Scholar 

  • MacNeil, C., J. T. A. Dick & R. W. Elwood, 1997. The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): problems and perspectives concerning the functional feeding group concept. Biological Reviews 72: 349–364.

    Article  Google Scholar 

  • Mancinelli, G., 2012. On the trophic ecology of Gammaridea (Crustacea: Amphipoda) in coastal waters: a European-scale analysis of stable isotopes data. Estuarine Coastal and Shelf Science 114: 130–139.

    Article  CAS  Google Scholar 

  • Martínez del Rio, C. & R. Anderson-Sprecher, 2008. Beyond the reaction progress variable: the meaning and significance of isotopic incorporation data. Oecologia 156: 765–772.

    Article  PubMed  Google Scholar 

  • Matthews, B. & A. Mazumder, 2008. Detecting trophic-level variation in consumer assemblages. Freshwater Biology 53: 1942–1953.

    Article  Google Scholar 

  • McCutchan Jr., J. H., W. M. Lewis Jr., C. Kendall & C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102: 378–390.

    Article  CAS  Google Scholar 

  • Michener, R. & K. Lajtha, 2007. Stable Isotopes in Ecology and Environmental Science, 2nd ed. Blackwell Scientific, Oxford.

    Book  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 and Cosmochimica Acta 48: 1135–1140.

    Article  CAS  Google Scholar 

  • Passey, B. H., T. F. Robinson, L. K. Ayliffe, T. E. Cerling, M. Sponheimer, M. D. Dearing, B. L. Roeder & J. R. Ehleringer, 2005. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. Journal of Archeological Science 32: 1149–1470.

    Article  Google Scholar 

  • Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.

    Article  Google Scholar 

  • Phillips, D. L., R. Inger, S. Bearhop, A. L. Jackson, J. W. Moore, A. C. Parnell, B. X. Semmens & E. J. Ward, 2014. Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92: 823–835.

    Article  Google Scholar 

  • Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718.

    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, 2014. R: A language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. URL http://www.R-project.org/.

  • Rounick, J. S. & M. J. Winterbourn, 1986. Stable carbon isotopes and carbon flow in ecosystems. BioScience 36: 171–177.

    Article  CAS  Google Scholar 

  • Smith, G.K., 2013. The coexistence of ecologically similar species. Ph.D. thesis, The University of Texas at Austin, Austin (Texas, USA).

  • Sokal, R. R. & F. J. Rohlf, 2012. Biometry, 4th ed. W.H. Freeman and Company, New York.

    Google Scholar 

  • Spence, K. & J. Rosenheim, 2005. Isotopic enrichment in herbivorous insects: a comparative field-based study of variation. Oecologia 146: 89–97.

    Article  PubMed  Google Scholar 

  • Stephenson, R. L., F. C. Tan & K. H. Mann, 1986. Use of stable carbon isotope ratios to compare plant material and potential consumers in a seagrass bed and a kelp bed in Nova Scotia, Canada. Marine Ecology Progress Series 30: 1–7.

    Article  CAS  Google Scholar 

  • Tieszen, L. L., T. W. Boutton, K. G. Tesdahl & N. A. Slade, 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57: 32–37.

    Article  Google Scholar 

  • Vander Zanden, M. J. & J. B. Rasmussen, 2001. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.

    Article  CAS  Google Scholar 

  • Vander Zanden, M. J., M. K. Clayton, E. K. Moody, C. T. Solomon & B. C. Weidel, 2015. Stable isotope turnover and half-life in animal tissues: a literature synthesis. PLOS ONE 10: e0116182.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanderklift, M. A. & S. Ponsard, 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136: 169–182.

    Article  PubMed  Google Scholar 

  • Vergilino, R., K. Dionne, C. Nozais, F. Dufresne & C. Belzile, 2012. Genome size differences in Hyalella cryptic species. Genome 55: 134–139.

    Article  PubMed  Google Scholar 

  • Wellborn, G. A. & R. D. Cothran, 2007. Niche diversity in crustacean cryptic species: complementarity in spatial distribution and predation risk. Oecologia 154: 175–183.

    Article  PubMed  Google Scholar 

  • Weston, D. P., H. C. Poynton, G. A. Wellborn, M. J. Lydy, B. J. Blalock, M. S. Sepulveda & J. K. Colbourne, 2013. Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca. Proceedings of the National Academy of Sciences 110: 16532–16537.

    Article  CAS  Google Scholar 

  • Witt, J. D. S., D. L. Threloff & P. D. N. Hebert, 2006. DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Molecular Ecology 15: 3073–3082.

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama, H., A. Tamaki, K. Harada, K. Shimoda, K. Koyama & Y. Ishihi, 2005. Variability of diet-tissue isotopic fractionation in estuarine macrobenthos. Marine Ecology Progress Series 296: 115–128.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank F. St-Pierre for his help during fieldwork and experiments, R. Vergilino for fruitful discussions and M. Babin and C. Renault for stable isotope analyses. We thank B. Beisner, M. Leibold and G. Winkler, anonymous reviewers and the associate editor K. Kovalenko for their comments that greatly improved our text, and C. Riley for English revision. We thank the Réserve faunique Duchénier for access to the Lake France and Lake des Baies. This work was supported by a grant to CN and a scholarship to KD from the Natural Sciences and Engineering Research Council of Canada and by a scholarship to KD from EnviroNord. This study is a contribution to the research programs of the Centre d’études nordiques and the Centre sur la science de la biodiversité du Québec. The experiments described herein comply with the current laws of Canada.

Author Contributions

KD and CN conceived and designed the experiments. KD conducted fieldwork, performed the experiments and prepared the samples for the stable isotope analyses. KD analysed the data. KD, CN and FD wrote the manuscript. The experiments described herein comply with the current laws of Canada.

Author information

Authors and Affiliations

  1. Département de Biologie et centre d’études nordiques, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, QC, G5L 3A1, Canada

    Kaven Dionne

  2. Département de biologie, chimie et géographie, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, QC, G5L 3A1, Canada

    France Dufresne & Christian Nozais

Authors
  1. Kaven Dionne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. France Dufresne
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Nozais
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kaven Dionne.

Additional information

Handling editor: Katya E. Kovalenko

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 477 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dionne, K., Dufresne, F. & Nozais, C. Variation in δ13C and δ15N trophic enrichment factors among Hyalella azteca amphipods from different lakes. Hydrobiologia 781, 217–230 (2016). https://doi.org/10.1007/s10750-016-2846-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2846-z

Keywords

Search

Navigation