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Biochemical tracers reveal intra-specific differences in the food webs utilized by individual seabirds

  • Physiological Ecology - Original Paper
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Abstract

Food web structure regulates the pathways and flow rates of energy, nutrients, and contaminants to top predators. Ecologically and physiologically meaningful biochemical tracers provide a means to characterize and quantify these transfers within food webs. In this study, changes in the ratios of stable N isotopes (e.g., δ15N), fatty acids (FA), and persistent contaminants were used to trace food web pathways utilized by herring gulls (Larus argentatus) breeding along the shores of the St Lawrence River, Canada. Egg δ15N values varied significantly among years and were used as an indicator of gull trophic position. Temporal trends in egg δ15N values were related to egg FA profiles. In years when egg δ15N values were greater, egg FA patterns reflected the consumption of more aquatic prey. Egg δ15N values were also correlated with annual estimates of prey fish abundance. These results indicated that temporal changes in aquatic prey availability were reflected in the gull diet (as inferred from ecological tracer profiles in gull eggs). Analysis of individual eggs within years confirmed that birds consuming more aquatic prey occupied higher trophic positions. Furthermore, increases in trophic position were associated with increased concentrations of most persistent organic contaminants in eggs. However, levels of highly brominated polybrominated diphenyl ether congeners, e.g, 2,2′,3,3′,4,4′,5,5′,6,6′-decabromoDE (BDE-209), showed a negative relationship with trophic position. These contrasting findings reflected differences among contaminant groups/homologs in terms of their predominant routes of transfer, i.e., aquatic versus terrestrial food webs. High trophic level omnivores, e.g., herring gulls, are common in food webs. By characterizing ecological tracer profiles in such species we can better understand spatial, temporal, and individual differences in pathways of contaminant, energy, and nutrient flow.

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References

  • Addis PB (2005) Omega-3 fatty acid content of Lake Superior fish. Minnesota Sea Grant report, http://www.seagrant.umn.edu/fish/omega3.pdf

  • Arts MT, Ackman RG, Holub BJ (2001) “Essential fatty acids” in aquatic ecosystems: a crucial link between diet and human health and evolution. Can J Fish Aquat Sci 58:122–137

    Article  CAS  Google Scholar 

  • Ballschmiter K, Bacher R, Mennel A, Fischer R, Riehle U, Swerev M (1992) The determination of chlorinated biphenyls, chlorinated dibenzodioxins, and chlorinated dibenzofurans by GC-MS. J High Resolut Chromatogr 15:260–270

    Article  CAS  Google Scholar 

  • Bearhop S, Phillips RA, Thompson DR, Waldron S, Furness RW (2000) Variability in mercury concentrations of great skuas Catharacta skua: the influence of colony, diet and trophic status inferred from stable isotope signatures. Mar Ecol Prog Ser 195:261–268

    Article  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    PubMed  CAS  Google Scholar 

  • Chen D, Mai B, Song J, Sun Q, Luo Y, Luo X, Zeng EY, Hale RC (2007) Polybrominated diphenyl ethers in birds of prey from Northern China. Environ Sci Technol 41:1828–1833

    Article  PubMed  CAS  Google Scholar 

  • Dalsgaard J, St John M, Kattner G, Muller-Navarra DC, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340

    Article  PubMed  Google Scholar 

  • Elliott JE, Noble DG, Norstrom RJ, Whitehead PE, Simon M, Pearce PA, Peakall DB (1992) Patterns and trends of organic contaminants in Canadian seabird eggs, 1968–90. In: Livingstone D, Walker CH (eds) Persistent pollutants in marine ecosystems. Pergamon Press, Oxford

    Google Scholar 

  • Ewins PJ, Weseloh DV, Groom JH, Dobos RZ, Mineau P (1994) The diet of herring gulls (Larus argentatus) during winter and early spring on the lower Great Lakes. Hydrobiologia 279/280:39–55

    Article  Google Scholar 

  • Fox GA, Allan LJ, Weseloh DV, Mineau P (1990) The diet of herring gulls during the nesting period in Canadian waters of the Great Lakes. Can J Zool 68:1075–1085

    Article  Google Scholar 

  • Gaston AJ, Woo K, Hipfner JM (2003) Trends in forage fish populations in northern Hudson Bay since 1981, as determined from the diet of nestling thick-billed murres, Uria lomvia. Arctic 56:227–233

    Google Scholar 

  • Gauthier LT, Hebert CE, Weseloh DVC, Letcher RJ (2008) Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982–2006. Environ Sci Technol 42:1524–1530

    Article  PubMed  CAS  Google Scholar 

  • Gilbertson M (1974) Pollutants in breeding herring gulls in the lower Great Lakes. Can Field Nat 88:273–280

    Google Scholar 

  • Gorke M, Brandl R (1986) How to live in colonies: spatial foraging strategies of the black-headed gull. Oecologia 70:288–290

    Article  Google Scholar 

  • Great Lakes Institute for Environmental Research (2008) Standard operating procedure for the analysis of total recoverable mercury in biological tissues (vegetables and animals) by atomic absorption spectrometry vapor generation (AAS-VG). SOP 01-002, University of Windsor, Windsor

  • Hebert CE, Sprules WG (2002) The relevance of seabird ecology to Great Lakes management. J Great Lakes Res 28:91–103

    Article  Google Scholar 

  • Hebert CE, Norstrom RJ, Weseloh DV (1999a) A quarter century of environmental surveillance: the Canadian Wildlife Service’s Great Lakes Herring Gull Monitoring Program. Environ Rev 7:147–166

    Article  CAS  Google Scholar 

  • Hebert CE, Shutt JL, Hobson KA, Weseloh DVC (1999b) Spatial and temporal differences in the diet of Great Lakes Herring Gulls (Larus argentatus): evidence from stable isotope analysis. Can J Fish Aquat Sci 56:323–338

    Article  Google Scholar 

  • Hebert CE, Hobson KA, Shutt JL (2000) Changes in food web structure affect rate of PCB decline in herring gull (Larus argentatus) eggs. Environ Sci Technol 34:1609–1614

    Article  CAS  Google Scholar 

  • Hebert CE, Shutt JL, Ball RO (2002) Plasma amino acid concentrations as an indicator of protein availability to breeding herring gulls (Larus argentatus). Auk 119:185–200

    Article  Google Scholar 

  • Hebert CE, Arts MT, Weseloh DVC (2006) Ecological tracers can quantify food web structure and change. Environ Sci Technol 40:5618–5623

    Article  PubMed  CAS  Google Scholar 

  • Hebert CE, Weseloh DVC, Idrissi A, Arts MT, O’Gorman R, Gorman OT, Locke B, Madenjian CP, Roseman EF (2008) Restoring piscivorous fish populations in the Laurentian Great Lakes causes seabird dietary change. Ecology 89:891–897

    Article  PubMed  Google Scholar 

  • Hobson KA (1995) Reconstructing avian diets using stable-carbon and nitrogen isotope analysis of egg components: patterns of isotopic fractionation and turnover. Condor 97:752–762

    Article  Google Scholar 

  • Hobson KA, Hughes KD, Ewins PJ (1997) Using stable-isotope analysis to identify endogenous and exogenous sources of nutrients in eggs of migratory birds: applications to Great Lakes contaminants research. Auk 114:467–478

    Google Scholar 

  • International Joint Commission (1987) Revised Great Lakes Water Quality Agreement of 1978. International Joint Commission, Windsor

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecol Monogr 74:211–235

    Article  Google Scholar 

  • Jardine TD, Kidd KA, Fisk AT (2006) Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology. Environ Sci Technol 40:7501–7511

    Article  PubMed  CAS  Google Scholar 

  • Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol Oceanogr 49:1784–1793

    CAS  Google Scholar 

  • Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27

    Article  Google Scholar 

  • Klindt RM (2006) 2005 Lake St Lawrence warmwater fisheries assessment. In New York State Department of Environmental Conservation Annual Report, Bureau of Fisheries Lake Ontario Unit and St Lawrence River Unit to the Great Lakes Fishery Commission’s Lake Ontario Committee. Watertown

  • Koussoroplis A-M, Lemarchand C, Bec A, Desvilettes C, Amblard C, Fournier C, Berny P, Bourdier G (2008) From aquatic to terrestrial food webs: decrease of the docosahexaenoic acid/linoleic acid ratio. Lipids 43:461–466

    Article  PubMed  CAS  Google Scholar 

  • Lazar R, Edwards RC, Metcalfe CD, Gobas FAPC, Haffner GD (1992) A simple, novel method for the quantitative analysis of coplanar (non-ortho substituted) polychlorinated biphenyls in environmental samples. Chemosphere 25:493–504

    Article  CAS  Google Scholar 

  • Lindberg P, Sellström U, Häggberg L, de Wit CA (2004) Higher brominated diphenyl ethers and hexabromocyclododecane found in eggs of peregrine falcons (Falco peregrinus) breeding in Sweden. Environ Sci Technol 38:93–96

    Article  PubMed  CAS  Google Scholar 

  • Marth P, Martens D, Schramm K-W, Schmitzer J, Oxynos K, Kettrup A (2000) Environmental specimen banking. Herring gull eggs and breams as bioindicators for monitoring long-term and spatial trends of chlorinated hydrocarbons. Pure Appl Chem 72:1027–1034

    Article  CAS  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between 15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Mineau P, Fox GA, Norstrom RJ, Weseloh DV, Hallett D, Ellenton JA (1984) Using the Herring Gull to monitor levels and effects of organochlorine contamination in the Canadian Great Lakes. In: Nriagu JO, Simmons MS (eds) Toxic contaminants in the Great Lakes. Wiley, Toronto, pp 425–452

    Google Scholar 

  • Morris RD, Black JE (1980) Radio telemetry and herring gull foraging patterns. J Field Ornithol 51:110–118

    Google Scholar 

  • Napolitano GE (1998) Fatty acids as trophic and chemical markers in freshwater ecosystems. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 21–44

    Google Scholar 

  • Nisbet ICT, Montoya JP, Burger J, Hatch JJ (2002) Use of stable isotopes to investigate individual differences in diets and mercury exposures among common terns Sterna hirundo in breeding and wintering grounds. Mar Ecol Prog Ser 242:267–274

    Article  CAS  Google Scholar 

  • Oxynos K, Schmitzer J, Kettrup A (1993) Herring gull eggs as bioindicators for chlorinated hydrocarbons (contribution to the German Federal Environmental Specimen Bank). Sci Total Environ 139–40:387–398

    Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Skjervold H (1992) How should the new discoveries influence future food production? In: Lifestyle diseases and the human diet. As-Trykk, Norway

  • StatSoft (2005) STATISTICA data analysis software system, version 7.1. StatSoft, Tulsa

  • Thompson RM, Hemberg M, Starzomski BM, Shurin JB (2007) Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. Ecology 88:612–617

    Article  PubMed  Google Scholar 

  • United States Environmental Protection Agency (2001) Great Lakes ecosystem report 2000. Great Lakes National Program Office, Chicago. http://www.epa.gov/glnpo/rptcong/2001/

  • Wanless S, Harris MP, Redman P, Speakman JR (2005) Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea. Mar Ecol Prog Ser 294:1–8

    Article  Google Scholar 

  • Weseloh DVC, Pekarik C, de Solla SR (2006) Spatial patterns and rankings of contaminant concentrations in herring gull eggs from 15 sites in the Great Lakes and connecting channels, 1988–2002. Environ Monit Assess 113:265–284

    Article  PubMed  CAS  Google Scholar 

  • Wood AG, Naef-Daenzer B, Prince PA, Croxall JP (2000) Quantifying habitat use in satellite-tracked pelagic seabirds: application of kernel estimation to albatross locations. J Avian Biol 31:278–286

    Article  Google Scholar 

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Acknowledgements

Environment Canada’s Chemicals Management Plan and the Ontario Ministry of the Environment provided support for this research. K. Hobson’s laboratory conducted the stable isotope analyses. M. Drebenstedt, R. Ferguson, A. Idrissi, and B. Joyce assisted with the FA analyses. The Great Lakes Institute for Environmental Research at the University of Windsor conducted the Hg and organochlorine analyses. Cynthia Pekarik and Tania Havelka, CWS-Ontario Region, provided database support. Suggestions from R. O’Gorman, K. Keenleyside, and two anonymous reviewers improved the manuscript. All research completed as part of this study complied with Environment Canada’s Animal Care and Use guidelines.

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Authors and Affiliations

  1. Environment Canada, Wildlife and Landscape Science Directorate, National Wildlife Research Centre, Ottawa, ON, K1A 0H3, Canada

    Craig E. Hebert, Lewis T. Gauthier & Robert J. Letcher

  2. Environment Canada, Canadian Wildlife Service, Ontario Region, Downsview, Toronto, ON, M3H 5T4, Canada

    D. V. Chip Weseloh

  3. Environment Canada, Water Science and Technology Directorate, National Water Research Institute, Burlington, ON, L7R 4A6, Canada

    Michael T. Arts

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  1. Craig E. Hebert
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  2. D. V. Chip Weseloh
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  3. Lewis T. Gauthier
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  4. Michael T. Arts
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  5. Robert J. Letcher
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Correspondence to Craig E. Hebert.

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Communicated by Dag Olav Hessen.

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Hebert, C.E., Weseloh, D.V.C., Gauthier, L.T. et al. Biochemical tracers reveal intra-specific differences in the food webs utilized by individual seabirds. Oecologia 160, 15–23 (2009). https://doi.org/10.1007/s00442-009-1285-1

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  • DOI: https://doi.org/10.1007/s00442-009-1285-1

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