Journal of Stable isotopes indicate the extent of freshwater feeding Applied 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\ \ 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 isotope 66 ratios of the diet of individual birds over a period of ASSESSMENT OF DIETARY {END!POINTS| AND S[ Bearhop et al[ several months prior to feather sampling[ We used DIETÐFEATHER FRACTIONATION di}erent feathers from cormorants shot under licence In order to calibrate the isotope ratio expected from at inland freshwater _sheries and compared their iso! a particular diet\ moulted feathers were collected from tope signatures with those of feathers taken from cap! eight captive cormorants[ These birds had been taken tive cormorants\ fed exclusively on a marine _sh diet\ from a marine cormorant colony at the chick stage marine feeding shags Phalacrocorax aristotelis "L[# "before feathers had grown# and reared in captivity at and freshwater feeding goosanders Mergus merganser MAFF|s Central Science Laboratories\ Worplesdon\ L[\ in order to assess the extent of their freshwater UK\ where they had been maintained exclusively on feeding[ marine _sh "sprat Sprattus sprattus "L[## for at least a year prior to sampling[ Isotope ratios were also measured in a sample of 09 sprats to determine the food to feather fractionation occurring[ A further Materials and methods measure of food to feather fractionation and isotope ratios was derived for the shag\ a closely related sea! FEATHERS SAMPLED FROM WILD bird with an exclusively marine _sh diet[ Growing CORMORANTS FOR ISOTOPE ANALYSIS ~ight feathers were clipped from 01 adult shags caught Cormorants shot in England under MAFF licences in at nests in Foula\ Shetland\ during July 0885\ and 01 two winters "0883Ð84 and 0884Ð85# were collected for sandeels Ammodytes marinus Raitt\ their sole breeding a variety of post!mortem studies and stored at Ð19 >C[ season prey at this colony "Furness 0889#\ were Birds with known location and date of shooting were collected[ The sandeels had been dropped by shags weighed\ and sexed by internal examination[ One wing returning to feed chicks at the same colony[ Addition! from each bird was removed and sent to the University ally\ both the captive cormorant and shag feathers of Glasgow for examination of moult and feather should indicate the signals that would be expected preparation for stable isotope determinations[ Only from an entirely marine diet[ It should be noted that 02 bird wings with no juvenile plumage and in which at the d C values of marine prey show considerable least one primary feather was in active growth were variation\ and as such there is no single {end!point| selected\ giving a sample of 10 birds shot between operating in marine food webs[ It is therefore impor! December and February at freshwater _sheries in tant that studies of this nature are carried out at a local England[ Stomach analyses were undertaken by the scale\ and that all of the major dietary components can Centre for the Environment\ Fisheries and Aqua! be assessed[ To provide a freshwater isotope signal culture Science "CEFAS#[ Cormorants were assigned and a third measure of fractionation\ eight salmon one of three geographical categories depending on parr from the River Dee\ Aberdeenshire\ UK\ and where they were shot "Hampshire including the River freshly grown ~ight feathers from 09 juvenile goos! Test\ n  6^ the lower Severn catchment including the anders from the same river were collected[ On the River Wye\ n  7^ Lancashire and Cumbria\ n  5#[ River Dee goosander diet has been shown to be com! Three distinct samples were taken from each wild posed predominantly of salmon parr "Alexander cormorant] growing primary feathers greater than 0884#[ These birds were shot as part of another study\ 8 cm long "clearly evident from their short length and under licence from the Scottish O.ce Agriculture\ presence of a waxy sheath at the base#^ recently re! Environment and Fisheries Department[ grown primary feathers "identi_ed as such from their colour\ lack of abrasion and location adjacent to\ and SAMPLE PREPARATION on the body side of\ a currently growing feather#^ and Feather samples were washed in 9=14 M sodium a sample of 7Ð09 lesser coverts[ Cormorant primary hydroxide solution to remove surface contamination\ feathers take approximately 0 month to grow "Cramp rinsed in distilled water\ dried in an oven at 49 >C to + Simmons 0866#[ Thus\ adjacent primaries would constant weight\ and then ground to a _ne powder indicate diets in successive months although there using an impactor mill "Glen Creston Ltd[\ Stanmore\ would be some overlap[ Because the isotopic signature Middlesex\ UK# operating at liquid nitrogen tem! of a feather sample is indicative of the diet at the time perature[ Whole salmon parr\ sandeels and sprats of feather growth "Hobson + Clark 0881#\ the aim were also dried and then ground in the same way[ was to use the growing primaries to indicate diet in Lipids were extracted from _sh samples using a the days immediately before the bird was shot\ the Soxhlet apparatus with re~uxing chloroform\ then newly grown primaries to indicate the diet about 1Ð samples were re!dried to remove solvent[ 7 weeks before the bird was shot\ and the lesser coverts Þ 0888 British to indicate the diet averaged over the period JuneÐ Ecological Society\ ISOTOPE ANALYSIS Journal of Applied November[ According to Cramp + Simmons "0866# 02 04 Ecology\ 25\ body feathers\ including lesser coverts\ are replaced All d C and d N analyses were carried out by con! 64Ð73 during these months[ tinuous ~ow isotope ratio mass spectrometry "CF! 67 IRMS# using a Finnigan Tracer Mat isotope ratio male and female wild cormorants in mean isotopic 02 Freshwater feeding mass spectrometer coupled to a Carlo Erba C:N:S signatures for growing feathers "d C] t08  9=06\ 04 by cormorants analyser "Thermoquest\ Hemel Hempstead\ UK#[ P  9=78^ d N] t08  9=61\ P  9=37#\ for newly 02 04 Each sample was loaded into a miniature tin cup "3 grown feathers "d C] t08  0=34\ P  9=06^ d N] 02 × 5 mm# for combustion[ A typical run comprised a t08  9=87\ P  9=23# or for lesser coverts "d C] 04 reference sample\ followed by duplicate analyses of t08  9=85\ P  9=24^ d N] t08  9=57\ P  9=49#\ so two standards\ and then 7Ð09 samples[ This sequence data for both sexes were pooled[ Neither were there was repeated throughout the run\ allowing a cor! signi_cant di}erences between isotopic signatures for rection to be made for drift\ if necessary[ One of the any given feather type and the area where a bird was standards used was an internal laboratory carbon shot\ nor any signi_cant relationships between fea! standard "graphite#\ the value of which had been ascer! thers and date of shooting "Table 1#\ so data were tained against international standards by closed tube pooled for all collection dates and sites[ Carbon iso! combustion "Stuermer\ Peters + Kaplan 0867#^ the tope ratios in the shags\ sprat!fed cormorants\ san! other was an IAEA!nitrogen standard\ IAEA!N!1[ deels and sprats "Table 0# were all within the range of These standards were chosen for their d02C and d04N values reported in the literature for marine vertebrates values\ which were similar in magnitude to the "Chisholm\ Nelson + Schwartz 0871^ Mizutani et al[ samples[ Isotope ratios are expressed in parts per 0889^ Hobson\ Piatt + Pitocechelli 0883^ Thompson thousand "-#\ according to the following equation] + Furness 0884#[ The growing feathers of wild cor! morants indicated a strong freshwater dietary in~u! Rsample dX  −0 × 0999 ence\ with a mean d02C signature of Ð11=1- "Table 0#\ $0Rstandard1 % although the d02C of goosanders\ which feed exclus! 04 02 where X is Nor C and R is the corresponding ratio ively on freshwater prey\ was more positive "mean Ð 04 03 02 01 02 N: Nor C: C[ Rstandard for C is PDB "Pee Dee 19=6-^ Table 0#\ suggesting a weaker freshwater 04 belemnite# and for N is atmospheric nitrogen "AIR#[ in~uence[ 02 04 Each d C and d N measurement was made in trip! The fractionation of isotopes from _sh to predator licate and a value was derived by discarding the out! feather was remarkably consistent despite the very lying datum and taking the mean of the remaining di}erent _sh signatures "Fig[ 0#\ averaging 1=2- for two[ This procedure was found to give the highest d02C and 3=1- for d04N[ Applying these fractionation repeatability for triplicate measures "r  9=83 for factors to the mean d02C and d04N values for growing 02 04 02 d C^ r  9=85 for d N^ Godley et al[ 0887#[ d C feathers from wild cormorants indicates an isotope measurements were precise and accurate to 2 9=1-\ signature for their _sh prey of Ð13=4- for d02C and 04 and d N measurements were precise and accurate to 02=4- for d04N "Fig[ 0#\ which are within ranges 2 9=3-[ reported for freshwater _sh in other studies "Estep + Vigg 0874^ Mizutani et al[ 0889^ Fry 0880^ Hesslein Results et al[ 0880#[ Isotope values for cormorant feathers\ shag feathers\ The mean d02C values of the three feather types goosander feathers and all _sh are presented in from the wild cormorants were signi_cantly di}erent

Table 0[ There were no signi_cant di}erences between "Fig[ 1^ one!way ANOVA F1\59  55\ P ³ 9=992#\ as

Table 0[ Summary statistics for carbon and nitrogen isotopes

d02C"-# d04N"-#

Sample n Mean "SD# Range Mean "SD# Range

Cormorant Growing feathers 10 Ð11=1 "1=83# Ð15=6 to Ð06=0 06=6 "1=90# 04=5Ð11=3 Freshly grown feathers 10 Ð19=0 "2=88# Ð15=1 to Ð02=2 07=0 "0=86# 04=2Ð11=2 Lesser coverts 10 Ð07=5 "1=88# Ð13=6 to Ð02=4 05=3 "0=76# 01=4Ð08=6 Captive cormorant Moulted feathers 7 Ð03=8 "9=38# Ð04=2 to Ð03=1 05=3 "9=14# 05=0Ð05=6 Sprat Whole _sh 09 Ð06=4 "9=51# Ð07=4 to Ð05=2 00=4 "9=43# 09=8Ð01=2 Shag Growing feathers 01 Ð04=4 "9=34# Ð05=5 to Ð03=7 00=4 "9=46# 09=3Ð01=4 Sandeel Whole _sh 01 Ð06=4 "9=64# Ð07=8 to Ð05=4 6=8 "9=84# 4=8Ð8=2 Þ 0888 British Goosander Ecological Society\ Growing feathers 7 Ð19=6 "0=70# Ð11=3 to Ð05=6 00=3 "0=00# 09=9Ð02=9 Journal of Applied Salmon parr Ecology\ 25\ Whole _sh 7 Ð12=0 "0=40# Ð13=4 to Ð19=2 6=1 "9=61# 5=3Ð7=1 64Ð73 68 Table 1[ Comparisons between feather isotope signatures of wild cormorants shot in three di}erent areas and relationships S[ Bearhop et al[ between the date that birds were shot and feather isotope signatures Area "ANOVA# Date "product moment correlation coe.cient#

Sample d02C d04N d02C d04N

Growing primary F1\07  9=03\ P  9=76 F1\07  0=77\ P  9=07 r00  9=0\ P  9=61 r00  9=32\ P  9=04

Freshly grown primary F1\07  1=28\ P  9=01 F1\07  9=63\ P  9=38 r00  9=15\ P  9=3 r00  9=03\ P  9=56

Lesser coverts F1\07  9=53\ P  9=43 F1\07  9=80\ P  9=31 r00  9=22\ P  9=2 r00  9=03\ P  9=56

Fig[ 0[ Mean carbon and nitrogen isotope signatures in feathers "bars represent 20 SD# of piscivorous birds with single!species _sh diet and in their food _sh[ The open circle indicates the predicted mean isotopic signature of food _sh of wild cormorants as derived from growing feathers\ calculated from the mean food to feather fractionation values of the three examples[

Fig[ 1[ Mean carbon and nitrogen isotope signatures "bars represent 20 SD# in three feather types of 10 wild cormorants shot at freshwater _sheries in winter\ the feathers of captive cormorants fed sprats and the feathers of wild shags eating sandeels[

were the d04N values "Fig[ 1^ one!way ANOVA Although sprat!fed captive cormorants seemed to be 04 F1\59  3=71\ P ³ 9=91#\ with growing feathers having at a higher trophic level "mean d N  05=3-^ signi_cantly di}erent carbon values from both coverts Table 0# than shags "mean d04N  00=4-^ Table 0# Þ 0888 British and freshly grown feathers "StudentÐNeumanÐKeuls feeding on sandeels\ their d02C values were similar Ecological Society\ 04 02 Journal of Applied test#[ The d N values of lesser coverts were sig! "captive cormorant mean d C  Ð03=8-\ shag mean 02 Ecology\ 25\ ni_cantly di}erent from those of growing and freshly d C  Ð04=4-^ Table 0#[ Wild cormorants showed 64Ð73 grown primaries "StudentÐNeumanÐKeuls test#[ much greater individual variation in isotope signature 79 than either shags or sprat!fed cormorants "Fig[ 1#\ Discussion Freshwater feeding consistent with a more varied diet[ Data on the diet The isotope data do not _t the hypothesis that cor! by cormorants of wild cormorants in this study are presented in morants move freely between freshwater and marine Table 2[ The d02C signatures in covert samples indi! habitats through the winter[ They do strongly support cated a higher intake of marine _sh than did newly the hypothesis that birds moving to freshwater habi! grown or growing primaries\ suggestive of a dietary tats for the winter normally remain there\ feeding shift from marine _sh or a mixture of marine and entirely on freshwater _sh throughout this period\ freshwater _sh in summer to freshwater _sh in winter although extreme cold may force a move to the coast "Fig[ 1#[ due to icing of inland waters[ Most cormorants of the There were no signi_cant correlations between car! P[ c[ carbo subspecies\ in the British Isles\ nest in small bon and nitrogen isotope ratios of individual birds coastal colonies\ returning to their nest sites in late from growing feathers\ newly grown feathers or March and dispersing to nearby wintering areas in 02 coverts[ However\ the d C values for growing primar! August "Cramp + Simmons 0866^ Gibbons\ Reid + ies\ newly grown primaries and coverts from each Chapman 0883#[ Numbers moving into freshwaters individual were all correlated with each other from coastal colonies increase from August to Feb! "P ³ 9=94 in each pairwise comparison#[ This implies ruary "Kirby\ Gilburn + Sellers 0884^ Russell et al[ that although the diets of individual birds within the 0885#\ with freshwater _sheries near to rivers being sample of 10 was variable over the 5!month period favoured "Callaghan\ Kirby + Bell 0883#\ suggesting before they were shot\ there was no tendency to switch that birds may use rivers as a route inland[ The iso! back to marine habitats after the move into fresh! topic data support this scenario[ Coverts indicated water[ that about half of the _sh taken in the 5 months 02 The frequency distributions of d C values for the JuneÐNovember were from freshwater\ and growing three feather types indicated that the signatures of primary feathers suggested that\ for most birds\ all the growing primaries were consistent\ with all birds feed! _sh taken in the weeks immediately before they were ing predominantly on freshwater _sh at the time of shot "i[e[ during DecemberÐFebruary# were from growth\ and that 05 of the 10 were probably feeding freshwater[ If birds had fed entirely on marine _sh exclusively on freshwater _sh "Fig[ 2#[ Newly grown while breeding "including during JuneÐAugust# and primaries also indicated predominantly freshwater moved to freshwater habitats on dispersal from their feeding\ but with _ve birds having moved from marine colonies in AugustÐSeptember\ then they would exhi! feeding to freshwater feeding between growth of the bit a signal that suggested 49) of _sh consumed were previous primaries and those currently in growth from freshwater over JuneÐNovember[ Individual "Fig[ 2#[ Coverts\ because they integrate dietary iso! variation in this proportion would _t with variation tope signal over a period of about 5 months rather in the timing of movement from marine to freshwater than over the short period indicated by individual habitats\ as is indicated by the continued rise in num! primary feathers\ showed a unimodal distribution\ bers of cormorants inland between August and Feb! with four individuals feeding almost entirely on mar! ruary "Kirby\ Gilburn + Sellers 0884#[ The small stan! ine _sh\ six almost entirely on freshwater _sh\ and 00 dard deviations for d02C seen in the shags and captive feeding on a mixture "Fig[ 2#[ cormorants\ which are stenophagus "either naturally

Table 2[ Diet of wild cormorants at the time of shooting\ based on macroscopic examination of stomach contents[ Scienti_c names of species not already mentioned in the text are grayling Thymallus thymallus "L[#\ pike Esox lucius L[\ bleak Alburnus alburnus "L[#\ minnow Phoxinus phoxinus "L[#

Hampshire "incl[ River Test# Lower Severn area "incl[ River Wye# Lancashire and Cumbria

Species n Species n Species n

Grayling 6 Roach 17 Carp 2 Pike 0 Bleak 16 Roach 1 Bream 0 Perch 1 Rainbow trout 1 Salmon parr 1 Pike 0 Pike 0 Cyprinid 0 Þ 0888 British Minnow 0 Ecological Society\ Gudgeon 0 Journal of Applied Salmonid 0 Ecology\ 25\ 64Ð73 Not identi_ed to species 70 S[ Bearhop et al[

Fig[ 2[ Frequency distribution of carbon isotope signatures for three feather types from 10 wild cormorants\ categorized as marine "d02C −01 to −05^ mean d02C for shags  −04=4-#\ mixed "d02C −05 to −19# or freshwater "d02C −19 to −15^ mean d02C for goosanders  −19=6-#[

or arti_cially#\ when compared with those of the wild freshwater _sh they are feeding on[ Our estimate that cormorants "Table 0#\ also support this[ However\ _sh consumed by cormorants during growth of cur! even when feeding within a single habitat type\ wild rently growing primaries had a mean d02C of Ð13=4- cormorants take a variety of prey species "Russell et al[ _ts very well with published values for freshwater _sh 0885# and it would be expected that a species with a "Estep + Vigg 0874^ Mizutani et al[ 0889^ Fry 0880^ variable diet would have increased variation in the Hesslein et al[ 0880#\ and this again suggests that most isotopic signatures of its tissues compared with a spec! cormorants were feeding in freshwater habitats pre! ies with a monotonous diet "Mizutani\ Fukuda + ceding the date they were shot[ However\ extreme Kabaya 0881#[ values for di}erent freshwater _sh species in di}erent Inland breeding is becoming increasingly common systems can vary by up to 00- "Hobson + Welch in British cormorants[ During 0874Ð76 around 0299 0884^ France + Steedman 0885#[ In addition to this\ in of the 00 699 pairs nesting in the British Isles bred our study wild cormorants may have been consuming inland "Lloyd\ Tasker + Partridge 0880#\ and this stocked _sh\ such as rainbow trout\ fed on arti_cial _gure was still rising in 0884 "Russell et al[ 0885#[ diets "of marine origin#\ although these _sh only Additionally\ it has been suggested that between 4) occurred in the diet of birds from the Lancashire and and 09) of the British wintering population may be Cumbria area "Table 2#[ Further\ cormorants are gen! birds of the subspecies P[ c[ sinensis\ originating from erally thought to be opportunistic feeders "Russell mainland Europe "Russell et al[ 0885#\ where inland et al[ 0885# but it is worth considering that some birds breeding is common[ Six of the birds had covert d02C may feed preferentially on particular prey species[ All signatures indicative of exclusively freshwater feeding of these could help account for some of the variability from June to November\ suggesting that these birds in isotopic signatures of feathers[ Thus\ it is di.cult may have come from freshwater breeding sites[ It is to establish a d02C {end!point| for freshwater feeding\ also worth noting that the d04N signatures of growing as this will vary with the system in which the bird is and freshly grown primaries were signi_cantly more feeding and the species of freshwater _sh consumed[ enriched than those observed in lesser coverts and In previous studies of marine vs[ fresh! marine!fed cormorants[ This suggests that the fresh! water:terrestrial feeding\ the approach has been to set water bodies that these cormorants are feeding on may up a mixing model based on marine and freshwater have additional nitrogen inputs\ for example from isotopic end!points\ in order to quantify the pro! agricultural run!o} or sewage treatment plants[ portions of marine and freshwater:terrestrial feeding The generally accepted di}erence in d02C values "Chisholm\ Nelson + Schwartz 0871^ Hobson 0876^ between freshwater and marine ecosystems is 6- Hobson 0889^ Hobson + Sealy 0880#[ In the present "Craig 0842^ Chisholm\ Nelson + Schwartz 0871^ Fry\ study a mixing model would be inappropriate[ We Scanlan + Parker 0872^ Peterson + Fry 0876#[ Our did not have access to cormorants fed entirely on data for cormorant feathers appear to support this\ freshwater _sh\ which could have provided a fresh! with the sprat!fed cormorant feathers "mean d02CÐ water end!point[ The goosanders used here were of 03=8-^ Table 0# and growing primaries from wild cor! limited use as indicators of a purely freshwater diet as Þ 0888 British morants "mean d02C Ð11=1-^ Table 0# di}ering by their mean carbon signature "Ð19=6-^ Table 0# was Ecological Society\ 02 02 Journal of Applied 6=2-[ However\ individual cormorants had d C sig! more {marine| "greater C!enrichment# than that of Ecology\ 25\ natures as low as Ð15=6- "Table 0#\ suggesting that the growing cormorant feathers "Ð11=1-^ Table 0#[ 64Ð73 there is a relatively wide range of d02C values in the Although goosander prey "salmon parr# had d02C 71 values "Table 0# similar to those found in adult Paci_c valuable or sport _sh[ Neither can we be certain that Freshwater feeding salmon Oncorhynchus spp[ "Kline et al[ 0889\ 0882#\ the birds were feeding regularly at the particular wat! by cormorants they tended to be higher than d02C values found in erbodies where they were shot rather than at other other freshwater _sh "Chisholm\ Nelson + Schwartz freshwater sites[ These factors could in~uence man! 0871^ Hobson 0889^ Kline et al[ 0889^ Mizutani et al[ agement strategies adopted on the basis of these 0889^ Rosenfeld + Ro} 0881^ Hobson + Welch 0884#[ results[ More detailed analyses using multiple isotopes It is possible that this disparity is linked to the num! "Ehrlinger + Rundel 0878# could be used to create bers of anadromous _sh in the catchment[ Adult sal! {_ngerprints| for prey species from di}erent inland mon "that have undertaken the bulk of their growth freshwaters to help clarify this situation[ In particular\ at sea and therefore most of the carbon in their tissues d76Sr has been shown recently to be a very sensitive will be of marine origin# migrate upstream to spawn marker in distinguishing salmon fry stocks from and then die\ introducing a 02C!enriched carbon di}erent freshwater catchments "Kennedy et al[ 0886#[ source into the system\ which is re~ected in d02C! Additionally\ satellite and radiotelemetry studies enrichment in the tissues of the biota[ In the River could be used in order to establish how much move! Dee\ where the goosanders and salmon were sampled ment there is between di}erent inland sites[ from\ there is an annual salmon run "Anonymous 0885#[ Findings similar to these have been reported by Kline et al[ "0889\ 0882# for di}erent freshwater Acknowledgements catchments in Alaska\ in which migratory Paci_c sal! We thank CEFAS "MAFF# for supplying the wild mon contributed substantial amounts of marine car! cormorant feathers and the diet data\ Dr I[ Inglis bon to freshwater systems[ "MAFF\ CSL# for making available a sample of sprats Another approach to quantifying the freshwater and feathers from captive!reared cormorants\ and input to diet might have been to take the 6- di}er! T[ Fallick "SURRC\ East Kilbride#[ Iso! ential between marine and freshwater reservoirs and topic analyses were carried out by Julie Dougans subtract it from the more reliable marine end!point within the Life Sciences Community Stable Isotope 02 "as de_ned by the captive cormorant feather d C Facility\ SURRC\ East Kilbride\ which is funded by 02 signature#[ However\ the di}erence between the d C a consortium of Scottish Universities and the Natural signatures of marine and freshwater animals can Environmental Research Council[ Stuart Bearhop is depart from 6-[ Other studies report di}erences funded by a University of Glasgow Scholarship\ and between the estimated marine and freshwater endpo! Brendan Godley made helpful comments on the ints of 09=0- in the muscle of marbled murrelets Bra! manuscript[ chyramphus marmoratus "Hobson 0889# and 7=0- in the muscle of northern saw!whet owls Aegolius acad! icus "Hobson + Sealy 0880#[ Furthermore\ the d02C References signatures of feathers from wild cormorants ranged from Ð15=6- to Ð02=2- "Table 0#[ A captive cor! Alexander\ G[ "0884# Foraging ecology of goosander "Mergus 02 merganser# and the red!breasted merganser "M[ serrator# morant fed entirely on marine _sh with a d CofÐ ducklings in north east Scotland[ PhD thesis[ University of 04=2- "extreme negative value for captive cor! Aberdeen\ Aberdeen\ UK[ morants^ Table 0# is no less {marine| than a wild cor! Anonymous "0885# Scottish Salmon and Sea Trout Catches morant with a d02C of Ð02=2- "extreme positive value 0884[ Statistical bulletin no[ FIS:0885:0[ SOAEFD\ Fresh! for freshly grown feathers of wild cormorants^ water Fisheries Laboratory\ Montrose\ UK[ Callaghan\ D[A[\ Kirby\ J[S[ + Bell\ M[C[ "0883# An Assess! Table 0#[ It follows therefore that a bird with the mean ment of Cormorant Phalacrocorax carbo Occupancy and 02 d C for growing feathers "Ð11=1-^ Table 0# would Impact at Stillwater Game Fisheries in England and Wales[ not necessarily have less freshwater prey in its diet Report to the Association of Stillwater Game Fishery than one with a d02C of Ð15=6- "extreme negative Managers[ WWT\ Slimbridge\ UK[ value for growing feathers^ Table 0#[ Thus\ there Chamberlain\ C[P[\ Blum\ J[D[\ Holmes\ R[T[\ Xiahong Feng\ Sherry\ T[W[ + Graves\ G[R[ "0886# The use of appears to be a wide range of potential freshwater isotope tracers for identifying populations of migratory end!points for a given species further complicating birds[ Oecologia\ 098\ 021Ð030[ the mixing model approach[ Clearly\ estimates of the Chisholm\ B[S[\ Nelson\ D[E[ + Schwartz\ H[P[ "0871# relative contributions of marine and freshwater pro! Stable!carbon isotope ratios as a measure of marine versus tein would vary considerably depending on which terrestrial protein in ancient diets[ Science\ 105\ 0020Ð0021[ Craig\ H[ "0842# The geochemistry of stable!carbon isotopes[ values are chosen as end!points[ Geochimica et Cosmochimica Acta\ 2\ 42Ð81[ We can conclude from the isotopic data presented Cramp\ S[ + Simmons\ K[E[L[ "0866# Birds of the Western here that most cormorants shot under licence on fresh! Palearctic\ Vol[ 0[ Oxford University Press\ Oxford\ UK[ waters in winter in England are feeding almost entirely DeNiro\ M[J[ + Epstein\ S[ "0867# In~uence of diet on the Þ 0888 British on freshwater prey at the time of shooting and in the distribution of carbon isotopes in animals[ Geochimica et Ecological Society\ Cosmochimica Acta\ 31\ 384Ð495[ Journal of Applied preceding period[ Thus\ there is potential for con~ict DeNiro\ M[J[ + Epstein\ S[ "0870# In~uence of diet on the Ecology\ 25\ with freshwater _sheries[ However\ we do not know distribution of nitrogen isotopes in animals[ Geochimica et 64Ð73 to what extent these birds are feeding on commercially Cosmochimica Acta\ 34\ 230Ð240[ 72 van Eerden\ M[R[ + Gregersen\ J[ "0884# Long term changes using d02C and d04N analysis[ Marine Ecology Progress S[ Bearhop et al[ in the north!west European population of cormorants Series\ 73\ 8Ð07[ Phalacrocorax carbo sinensis in Western Europe[ Ardea\ Hobson\ K[A[ + Welch\ H[E[ "0884# Cannibalism and tro! 72\ 0Ð8[ phic structure in a high Arctic lake^ insights from stable! van Eerden\ M[R[ + Munstermann\ M[J[ "0884# Sex and age isotope analysis[ Canadian Journal of Fisheries and Aquatic dependent distribution in wintering cormorants Phal! Science\ 41\ 0084Ð0190[ acrocorax carbo sinensis in Western Europe[ Ardea\ 72\0Ð Hobson\ K[A[\ Piatt\ J[F[ + Pitocechelli\ J[ "0883# Using 8[ stable isotopes to determine seabird trophic relationships[ Ehrlinger\ J[R[ + Rundel\ P[W[ "0878# Stable isotopes] Journal of Animal Ecology\ 52\ 675Ð687[ history\ units and instrumentation[ Stable Isotopes in Eco! Johnsgard\ P[A[ "0882# Cormorants\ Darters\ and Pelicans logical Research "eds P[W[ Rundel\ J[R[ Ehrlinger + K[A[ of the World[ Smithsonian Institution Press\ Washington\ Nagy#\ pp[ 190Ð107[ Springer!Verlag\ New York[ DC[ Estep\ M[L[F[ + Vigg\ S[ "0874# Stable carbon and nitrogen Kennedy\ B[P[\ Folt\ C[L[\ Blum\ J[D[ + Chamberlain\ C[P[ isotope tracers of trophic dynamics in natural populations "0886# Natural isotope markers in salmon[ Nature\ 276\ and _sheries of the Lahontan lake system\ Nevada[ Can! 655[ adian Journal of Fisheries and Aquatic Science\ 31\ 0601Ð Kirby\ J[S[\ Gilburn\ A[S[ + Sellers\ R[M[ "0884# Status\ 0608[ distribution and habitat use by Cormorants Phalacrocorax Feare\ C[J[ "0877# Cormorants as predators at freshwater carbo wintering in Great Britain[ Ardea\ 72\ 82Ð091[ _sheries[ Institute of Fisheries Management Annual Study Kirby\ J[S[\ Holmes\ J[S[ + Sellers\ R[M[ "0885# Cormorants Course\ 07\ 07Ð31[ Phalacrocorax carbo as _sh predators] an appraisal of their France\ R[ + Steedman\ R[ "0885# Energy provenance for conservation and management in Great Britain[ Biological juvenile lake trout in small Canadian Shield lakes as shown Conservation\ 64\ 080Ð088[ by stable isotopes[ Transactions of the American Fisheries Kline\ T[C[\ Goering\ J[J[\ Mathisen\ O[A[\ Poe\ P[H[ + Society\ 014\ 401Ð407[ Parker\ P[L[ "0889# Recycling of elements transported Fry\ B[ "0880# Stable isotope diagrams of freshwater food upstream by runs of Paci_c salmon] I d04N and d02C webs[ Ecology\ 65\ 1182Ð1186[ evidence in Sashin creek\ Southeastern Alaska[ Canadian Fry\ B[ + Sherr\ E[ "0873# d02C measurements as indicators Journal of Fisheries and Aquatic Science\ 36\ 025Ð033[ of carbon ~ow in marine and freshwater systems[ Con! Kline\ T[C[\ Goering\ J[J[\ Mathisen\ O[A[\ Poe\ P[H[\ tributions to Marine Science\ 16\ 02Ð36[ Parker\ P[L[ + Scanlan\ R[S[ "0882# Recycling of elements Fry\ B[\ Scanlan\ R[S[ + Parker\ P[L[ "0872# 02C:01C ratios transported upstream by runs of Paci_c salmon[ II[ d04N in marine food webs of the Torres Strait\ Queensland[ and d02C evidence in the Kvichak river watershed\ Bristol Journal of Australian Marine and Freshwater Research\ 23\ bay\ Southwestern Alaska[ Canadian Journal of Fisheries 696Ð604[ and Aquatic Science\ 49\ 1249Ð1254[ Furness\ R[W[ "0889# A preliminary assessment of the quan! Lloyd\ C[\ Tasker\ M[L[ + Partridge\ K[ "0880# The Status tities of Shetland sandeels taken by seabirds\ seals\ preda! of Seabirds in Britain and Ireland[ Poyser\ London\ UK[ tory _sh and the industrial _shery in 0870Ð72[ Ibis\ 021\ MacDonald\ R[A[ "0876# The breeding population and dis! 194Ð106[ tribution of the cormorant in Ireland[ Irish Birds\ 2\ 394Ð Gibbons\ D[W[\ Reid\ J[B[ + Chapman\ R[A[ "0883# The 305[ New Atlas of Breeding Birds in Britain and Ireland] 0877Ð Mizutani\ H[\ Fukuda\ M[ + Kabaya\ Y[ "0881# 02C and 04N 80[ Poyser\ London\ UK[ enrichment factors of feathers of 00 species of adult birds[ Godley\ B[J[\ Thompson\ D[R[\ Waldron\ S[ + Furness\ Ecology\ 62\ 0280Ð0284[ R[W[ "0887# The trophic status of marine turtles as deter! Mizutani\ H[\ Fukuda\ M[\ Kabaya\ K[ + Wada\ E[ "0889# mined by stable isotope analysis[ Marine Ecology Progress Carbon isotope ratio of feathers reveals feeding behaviour Series\ 055\ 166Ð173[ of cormorants[ Auk\ 096\ 399Ð326[ Hesslein\ R[H[\ Capel\ M[J[\ Fox\ D[E[ + Hallard\ K[A[ Peterson\ B[J[ + Fry\ B[ "0876# Stable isotopes in ecosystem "0880# Stable isotopes of sulfur\ carbon and nitrogen as studies[ Annual Review of Ecology and Systematics\ 07\ indicators of trophic level and _sh migration in the lower 182Ð219[ Mackenzie river basin\ Canada[ Canadian Journal of Fish! Rau\ G[H[\ Mearns\ A[J[\ Young\ D[R[\ Olson\ R[J[\ Schafer\ eries and Aquatic Science\ 37\ 1147Ð1154[ H[A[ + Kaplan\ I[R[ "0872# Animal 02C:01C correlates Hobson\ K[A[ "0876# Use of stable!carbon isotope analysis with trophic level in pelagic food webs[ Ecology\ 53\ 0203Ð to estimate marine and terrestrial protein content in gull 0207[ diets[ Canadian Journal of Zoology\ 54\ 0109Ð0102[ Rosenfeld\ J[S[ + Ro}\ J[C[ "0881# Examination of the car! Hobson\ K[A[ "0889# Stable isotope analysis of marbled mur! bon base in southern Ontario streams using stable relets] evidence for freshwater feeding and determination isotopes[ Journal of the American Benthological Society\ of trophic level[ Condor\ 81\ 786Ð892[ 00\ 0Ð09[ Hobson\ K[A[ "0882# Trophic relationships among high Arc! Russell\ I[C[\ Dare\ P[J[\ Eaton\ D[R[ + Armstrong\ J[D[ tic seabirds] insights from tissue!dependent stable isotope "0885# Assessment of the Problem of Fish!Eating Birds in models[ Marine Ecology Progress Series\ 84\ 6Ð07[ Inland Fisheries in England and Wales[ Report to the Min! Hobson\ K[A[ + Clark\ R[G[ "0881# Assessing avian diets istry of Agriculture\ Fisheries and Food[ MAFF Project using stable isotopes[ II[ Factors in~uencing diet!tissue VC 9093[ Directorate of Fisheries Research\ Lowestoft[ fractionation[ Condor\ 83\ 078Ð086[ Schoeninger\ M[J[ + DeNiro\ M[J[ "0873# Nitrogen and car! Hobson\ K[A[ + Sealy\ S[G[ "0880# Marine protein con! bon isotopic composition of bone collagen from marine tributions to the diet of Northern saw!whet owls on the and terrestrial animals[ Geochimica et Cosmochimica Acta\ Queen Charlotte Islands] a stable isotope approach[ Auk\ 37\ 514Ð528[ 097\ 326Ð339[ Staub\ E[ + Ball\ R[ "0883# Effects of Cormorant Predation Hobson\ K[A[ + Wassenaar\ L[I[ "0886# Linking the breeding on Fish Populations of Inland Waters[ Working document Þ 0888 British and wintering grounds of neotropical migrant songbirds for the 07th session of EIFAC\ and Report of the EIFAC Ecological Society\ using stable hydrogen isotopic analysis of feathers[ Oec! Working Party Held in Starnberg\ 14Ð29 July Journal of Applied ologia\ 098\ 031Ð037[ 0882[ EIFAC:XVIII:83:Inf[7 Rev[ May 0883[ EIFAC\ Ecology\ 25\ Hobson\ K[A[ + Welch\ H[E[ "0881# Determination of tro! Starnberg\ Germany[ 64Ð73 phic relationships within a high Arctic marine food web Stuermer\ D[H[\ Peters\ K[E[ + Kaplan\ I[R[ "0867# Source 73 indicators of humic substances and proto!kerogen[ Stable Thompson\ D[R[\ Furness\ R[W[ + Lewis\ S[A[ "0884# Diets 04 02 Freshwater feeding isotope ratios\ elemental compositions and electron spin and long!term changes d N and d C values in northern resonance spectra[ Geochimica et Cosmochimica Acta\ 31\ fulmars Fulmarus glacialis from two northeast Atlantic by cormorants 878Ð886[ colonies[ Marine Ecology Progress Series\ 014\ 2Ð00[ Suter\ W[ "0884# The e}ect of predation by wintering cor! YJsou\ P[ "0884# Individual migration strategies in cor! morants Phalacrocorax carbo on grayling Thymallus thy! morants Phalacrocorax carbo passing through or win! mallus and trout "Salmonidae# populations] two case studies tering in western France[ Ardea\ 72\ 156Ð163[ from Swiss rivers[ Journal of Applied Ecology\ 21\ 18Ð35[ Thompson\ D[R[ + Furness\ R[W[ "0884# Stable!isotope ratios of carbon and nitrogen in feathers indicate seasonal Received 01 November 0886^ revision received 17 November dietary shifts in northern fulmars[ Auk\ 001\ 382Ð387[ 0887

Þ 0888 British Ecological Society\ Journal of Applied Ecology\ 25\ 64Ð73