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Stable Isotopes Indicate the Extent of Freshwater Feeding by Cormorants

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Stable Isotopes Indicate the Extent of Freshwater Feeding by Cormorants Journal of Stable isotopes indicate the extent of freshwater feeding Applied Ecology 0888\ 25\ by cormorants Phalacrocorax carbo shot at inland 64Ð73 _sheries in England STUART BEARHOP\ DAVID R[ THOMPSON\ SUSAN WALDRON$\ IAN C[ RUSSELL%\ GAVIN ALEXANDER& and ROBERT W[ FURNESS Ornithology Group\ Graham Kerr Building\ Institute of Biomedical and Life Sciences\ University of Glasgow\ Glasgow G01 7QQ\ UK^ $Scottish Universities Research and Reactor Centre "SURRC#\ East Kilbride\ Glasgow G64 9QF\ UK^ %Centre for the Environment\ Fisheries and Aquaculture Science "CEFAS#\ Lowestoft Laboratory\ Pake_eld Road\ Lowestoft\ Suffolk NR22 OHT\ UK^ and &Institute of Terrestrial Ecology\ Banchory\ Aberdeenshire AB20 3BY\ UK Summary 0[ The numbers of cormorants Phalacrocorax carbo feeding at English freshwater _sheries during winter have increased rapidly over the last 19 years\ causing concern among _shery managers and anglers[ 1[ In order to assess the extent of freshwater feeding\ stable isotope ratios of carbon and nitrogen "d02C and d04N# in feathers of wild cormorants from inland freshwater _sheries were compared with those in the feathers of piscivorous birds with marine diets "captive {marine!fed| cormorants\ free!ranging shags Phalacrocorax aristotelis# and freshwater diets "juvenile goosanders Mergus merganser#[ 2[ Isotope signatures of feathers represent the diet at the time of growth[ Feathers grown at di}erent times of the year were taken from wild cormorants^ each feather type therefore represented the diet over a di}erent temporal scale[ 3[ Isotopic analyses of feathers indicated that\ when shot\ nearly all of the cormorants had been feeding entirely on freshwater prey[ The mean d02C value of primary feathers growing when birds were shot was Ð11=1-\ indicative of an entirely freshwater diet[ 4[ The move to freshwater habitats from coastal breeding grounds occurred over several months\ but once established cormorants appear to have fed at freshwater sites throughout the autumn and winter[ 5[ The suitability of using a two!source isotopic mixing model in order to quantify the extent of freshwater feeding in piscivorous birds is discussed[ 6[ Although the results indicate long!term residency and feeding in freshwater systems\ they do not indicate whether birds were feeding regularly at the sites at which they were shot\ or the composition of the diet[ It is recommended that further studies using telemetry and multiple isotope analyses be carried out in order to address these issues[ Key!words] carbon!02\ feather\ fractionation factor\ mixing model\ nitrogen!04[ Journal of Applied Ecology "0888# 25\ 64Ð73 Introduction the last 19 years has led to increasing con~ict between these birds and freshwater _shery interests "Staub + The rapid increase in numbers of cormorants Phal! Ball 0883^ Suter 0884^ van Eerden + Gregersen 0884#[ acrocorax carbo "L[# throughout most of Europe over In Britain and Ireland\ cormorant numbers have increased at a much slower rate than on the continent "Gibbons\ Reid + Chapman 0883# but problems have Correspondence] Stuart Bearhop "fax] 9030 2294860^ e! mail] sbearhopÝudcf[gla[ac[uk#[ arisen\ particularly during winter when numbers of Þ 0888 British %ICEFAS is an Executive Agency of the Ministry of Agric! cormorants feeding on inland freshwater _sheries are Ecological Society ulture Fisheries and Food[ highest "Russell et al[ 0885#[ This pattern appears to 64 65 be due largely to seasonal movement of cormorants of dietary inputs and trophic relationships[ In the case Freshwater feeding from predominantly marine breeding areas into fresh! of nitrogen\ the ratio of 04Nto03N "conventionally by cormorants water wintering areas "MacDonald 0876^ Callaghan\ expressed as d04N# exhibits a stepwise 04N enrichment Kirby + Bell 0883^ Kirby\ Gilburn + Sellers 0884^ of about 3- at each trophic level "Schoeninger + Kirby\ Holmes + Sellers 0885^ Russell et al[ 0885# DeNiro 0873^ Hobson + Welch 0881^ Hobson\ Piatt but probably also to the arrival of some birds from + Pitocechelli 0883# due to preferential excretion of continental breeding areas to winter in England "van the lighter isotope "Peterson + Fry 0876#[ For carbon\ Eerden + Munstermann 0884^ Kirby\ Gilburn + Sel! the ratio of 02Cto01C "conventionally expressed as lers 0884^ Russell et al[ 0885#[ In the British Isles\ cor! d02C# also shows a tendency to increase with trophic morants feed almost exclusively on _sh\ eating a wide level\ but to a lesser degree than in the case of nitrogen range of species when feeding in freshwater systems[ "Rau et al[ 0872^ Fry + Sherr 0873^ Hobson + Welch Roach Rutilis rutilis "L[#\ perch Perca ~uviatilis L[\ 0881#[ However\ the d02C value is distinctly di}erent bream Abramis brama "L[# and carp Cyprinus carpio between marine and freshwater:terrestrial animals[ L[ are the most common prey species\ but brown trout Signatures of marine animals are typically 6- more Salmo trutta L[\ rainbow trout Oncorhynchus mykiss 02C!enriched relative to those from freshwater equi! "Walbaum# and salmon S[ salar L[ are also taken valents "Craig 0842^ Chisholm\ Nelson + Schwartz regularly\ with eels Anguilla anguilla "L[# being con! 0871^ Fry\ Scanlan + Parker 0872#[ This disparity is a sumed less commonly "Russell et al[ 0885#[ Cor! consequence of a fundamental isotope ratio di}erence morants show a habitat preference for large lowland between bicarbonate "the source of carbon _xed in freshwater bodies\ so their predation particularly con! marine food chains# and carbon dioxide "the source of cerns freshwater _shery managers and anglers in sou! carbon _xed in freshwater and terrestrial food chains^ thern England "Callaghan\ Kirby + Bell 0883#[ Craig 0842^ Chisholm\ Nelson + Schwartz 0871^ Fry\ The Ministry of Agriculture\ Fisheries and Food Scanlan + Parker 0872#[ The 6- di}erential has been "MAFF# issues licences to permit the shooting of a used to estimate the proportion of dietary protein limited number of cormorants at freshwater _sheries derived from marine vs[ freshwater:terrestrial foods in England as an aid to scaring\ with the intention of of birds "Hobson 0876\ 0889^ Hobson + Sealy 0880#\ reducing serious damage to these _sheries[ Analyses and was also applied by Mizutani et al[ "0889# in a of stomach contents indicate that these birds have study of cormorant diets in Japan[ an almost exclusively freshwater diet at the time of The use of stable isotopes also overcomes some shooting "I[C[ Russell\ unpublished data#[ However\ of the biases normally associated with conventional this does not provide an indication of any temporal dietary analyses "e[g[ assessed via analysis of stomach variation in the diet[ Some studies have found cor! contents\ regurgitates\ pellets or by direct observation# morants to be highly mobile in winter "Feare 0877^ as the isotopic signature represents assimilated as YJsou 0884#\ and this impression is supported by opposed to ingested food[ Conventional dietary infor! counts of birds at inland waters and roosts\ which mation\ if it is not collected regularly over an extended show considerable short!term variations "Russell et al[ period\ is likely only to re~ect short!term diet^ in 0885#[ It is clear that some cormorants move between addition\ analyses of stomach contents\ regurgitates di}erent freshwater feeding sites and some birds roost or pellets are known to be biased towards particular inland while feeding in estuaries during the day "Feare types of prey "Hobson\ Piatt + Pitocechelli 0883^ Rus! 0877#[ However\ in England there are individuals that sell et al[ 0885#[ have been shown to exhibit a degree of site _delity Typical proteins used in the study of seabirds and "Kirby\ Holmes + Sellers 0885#\ but detailed infor! trophic relationships have been bone collagen extracts mation on movements is lacking[ For instance\ it is and muscle "e[g[ Hobson 0889\ 0882^ Hobson + Sealy not known whether large numbers of birds regularly 0880^ Hobson + Welch 0881^ Hobson\ Piatt + Pito! switch between freshwater and marine habitats\ cor! cechelli 0883#\ but the d02C and d04N signatures of respondingly consuming a mixture of marine and feather keratin have also been used to infer trophic freshwater _sh\ or whether those cormorants that status and dietary sources "Mizutani et al[ 0889^ move inland feed largely\ or exclusively\ on freshwater Thompson + Furness 0884^ Thompson\ Furness + _sh throughout the winter\ having selected the inland Lewis 0884#[ Additionally\ multiple isotope analyses habitat[ In this study we investigated this question by of feathers have been used to infer the breeding origins analysis of stable isotopes of carbon and nitrogen in of migratory songbirds "Chamberlain et al[ 0886^ the feathers of cormorants shot "under MAFF Hobson + Wassenaar 0886#[ Thus\ knowledge of the licences# at freshwater _sheries in England during the pattern and timing of moult makes it possible to inves! winter[ tigate aspects of diet of an individual bird over the Stable isotope ratios in proteins of consumers re~ect period of its moult "Thompson + Furness 0884#[ Cor! Þ 0888 British those in their diets in such a predictable manner morants show a relatively complex and extended Ecological Society\ Journal of Applied "DeNiro + Epstein 0867\ 0870^ Peterson + Fry 0876# moult\ with feather growth occurring through most Ecology\ 25\ that measurements of protein stable isotope signature of the year "Cramp + Simmons 0866^ Johnsgard 64Ð73 can be a powerful analytical tool in the understanding 0882#[ This allows inferences from stable
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