Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies

Mar Biol (2008) 155593ndash598

DOI 101007s00227-008-1048-2

ORIGINAL PAPER

DiVerences in stable isotopes in blood and feathers of seabirds are consistent across species age and latitude implications for food web studies

Petra Quillfeldt middot Leandro Bugoni middot Rona A R McGill middot Juan F Masello middot Robert W Furness

Received 29 April 2008 Accepted 20 August 2008 Published online 12 September 2008copy The Author(s) 2008 This article is published with open access at Springerlinkcom

Abstract Stable isotopes of growing feathers and bloodboth represent assimilated diet and both tissues are used tostudy the diet and foraging distribution of marine and ter-restrial birds Although most studies have assumed thatboth tissues represent a diVerence of one trophic level todiet the enrichment factors of blood and feathers maydiVer especially where endogenous reserves are used asprecursors during feather synthesis In this study we com-pare carbon and nitrogen stable isotopes of blood andsimultaneously growing feathers of Wve species of Procel-lariiformes representing Wve genera diVerent geographicalregions and diVerent life stages (chicks and adults) In allspecies feathers were enriched in 15N and 13C comparedwith blood Isotopic values of carbon and nitrogen werecorrelated in diVerent tissues growing simultaneously for mostspecies analyzed suggesting that mathematical correctionscould be used to compare diVerent tissues Our resultsimply that more care needs to be taken when comparingstable isotope signatures across studies assuming diVerenttissues are equivalent indicators of trophic ecology

Introduction

Recent developments in our knowledge about the naturaldistribution of stable isotopes in marine food webs have pro-vided us with a useful tool to study movements and the tro-phic level at which seabirds feed which can be appliedwhen more direct studies are impossible (eg Cherel et al2005a 2006 Quillfeldt et al 2005 Bearhop et al 2006Gladbach et al 2007) In particular carbon stable isotoperatios can reXect foraging locations (reviewed in Rubensteinand Hobson 2004) while nitrogen isotope ratios becomeenriched in 15N with trophic level by approximately 30ndash50permil (Minagawa and Wada 1984 Owens 1987) and 15Ncan thus indicate trophic position and be used to infer die-tary composition (eg Hobson and Welch 1992 Hobsonet al 2000 Forero et al 2005) Depending on the tissue cho-sen dietary information spanning diVerent temporal scalescan also be obtained (Hobson and Clark 1992a)

The stable isotope approach is especially useful for stud-ies of diet and foraging areas outside the breeding seasonwhen pelagic birds are not usually accessible for samplingusing traditional methods (Barrett et al 2007) A number ofstudies have made use of the fact that the molting period isin this time and thus feathers grown by adult seabirds reX-ect the diet in the interbreeding period (eg Nisbet et al2002 Quillfeldt et al 2005 Cherel et al 2006 Gladbachet al 2007) To assess diet and foraging areas during thebreeding season on the other hand several tissues can besampled non-destructively including blood and feathersamples of chicks and adults However due to the speciWcmetabolic processes involved in tissue synthesis diVerenttissues may diVer in their isotopic enrichment factor rela-tive to the diet (eg Hobson and Clark 1992a)

As noted by several authors (Bearhop et al 2000aCherel et al 2005a b) diVerences in isotopic discrimination

Communicated by R Lewison

P Quillfeldt (amp) middot J F MaselloMax-Planck-Institut fuumlr Ornithologie Vogelwarte Radolfzell Schlossallee 2 78315 Radolfzell Germanye-mail petraquillfeldtgmxde

L Bugoni middot R W FurnessInstitute of Biomedical and Life Sciences Graham Kerr Building University of Glasgow Glasgow G12 8QQ UK

R A R McGillScottish Universities Environmental Research Centre East Kilbride Glasgow G75 0QF UK

123

594 Mar Biol (2008) 155593ndash598

among tissues are a potential problem when comparingdiVerent tissue types Temporal studies comparing theblood (representing the breeding season) and feathers (rep-resenting the interbreeding season) of adult seabirds aredependent on the assumption that isotope analyses of thetwo tissues provide directly comparable dietary proxiesHowever most researchers working in the Weld of isotopeecology are aware that the enrichment factors of blood andfeathers may diVer when endogenous reserves are used asprecursors during feather synthesis (Cherel et al 2005a) orwhen blood contains 15N-depleted uric acid (Bearhop et al2000b) Thus most studies have limited their analysis toeither blood or feathers but have assumed both tissues torepresent a diVerence of one trophic level to diet A fewstudies have directly compared feather and blood isotopevalues (eg Podlesak et al 2005 Bearhop et al 2006)mainly on the assumption that the inXuence of tissue spe-ciWc fractionation is small compared to the eVect theyaimed to measure

The aim of this study is to compare the carbon and nitro-gen stable isotope values of blood and simultaneouslygrowing feathers of Wve species of Procellariiformes inorder to test for diVerences in isotopic tissue discriminationbetween tissues We also hope that by testing the basis ofassumptions that are often made in dietary studies regard-ing the equivalence of diVerent tissues we can help clarifyif blood or feather is the optimal tissue to sample We alsoconsider the limitations of extrapolating diVerent-tissue sta-ble isotope comparisons within temporal studies or betweenstudies using feather and studies using blood

Materials and methods

Study site species and sampling

Species abbreviations used in Fig 1 and sampling loca-tions are listed in Table 1 for sample sizes see Table 2

Great shearwaters PuYnus gravis Atlantic Yellow-nosed albatrosses Thalassarche chlororhynchos and Spec-tacled petrels Procellaria conspicillata were sampled in the

Southwestern Atlantic Ocean oV the Brazilian coastonboard Wshing vessels from February to June 2006 Birdsscavenging discards were attracted to the vessel andtrapped with a cast net as described by Bugoni et al(2008b) Blood was collected from the tarsal vein using a2-ml disposable syringe and needle Growing body feath-ers ie still with blood in the calamus from the breast anddorsum were collected and stored dry in sealed plastic bagsThis sample includes immature as well as breeding andnon-breeding adults

Trindade petrels Pterodroma arminjoniana were sam-pled in breeding colonies of Trindade Island (c 20deg30Sndash29deg19W) where there is a population estimated at 1130breeding pairs (Luigi et al 2008) Blood and growing feath-ers were collected from December 2006 to April 2007 and

Table 1 Species abbreviations used in Fig 1 and sampling locations of the Procellariifor-mes included in the present study

Species Abbreviation Age and sample location

Atlantic Yellow-nosed albatross Thalassarche chlororhynchos

AYA Adults and immatures (at sea SW Atlantic)

Spectacled petrel Procellaria conspicillata SPP Adults and immatures (at sea SW Atlantic)

Great shearwater PuYnus gravis GRS Adults and immatures (at sea SW Atlantic)

Trindade petrel Pterodroma arminjoniana TRP Breeding adults (colonies Trindade Island)

Trindade petrel Pterodroma arminjoniana TRP Chicks (colonies Trindade Island)

Thin-billed prion Pachyptila belcheri TBP Chicks (colonies New Island Falkland Islands)

Fig 1 Carbon and nitrogen stable isotopes (means sect SE) of seabirdblood and growing feathers representing similar time periods Forsample sizes see Table 2

AYA SPP GRS TRP TRP TBP

δ13

C

-20

-18

-16

-14

(chicks) (chicks)

δ15

N

12

14

16

18 BloodFeathers

123

Mar Biol (2008) 155593ndash598 595

preserved in the same way described above Four adultswere sampled during chick feeding stage whereas 14 wereprospecting birds but both groups were sampled over thesame time period despite diVerences in breeding stage asthe species nests throughout the year (Luigi et al 2008)During the prospecting period (ie before the pre-layingexodus which lasts usually 2 months) adults are frequentlyin Wnal moult stage with some growing body feathers stillpresent (Luigi et al 2008) Chicks were sampled followingthe same procedure and full grown or growing body feath-ers of the deWnitive plumage were collected One chick was40-days-old and others were 70ndash100 days old so close toXedging which occurs about the 95th to 100th day (Luigiet al 2008) The half-life of isotope turnover of avianwhole blood has been determined to be 114 days for quail(Hobson and Clark 1992a) and so represents the same timewindow as growth of new body feathers as these feathersare 20ndash30 mm long and growth rate of feathers in birds var-ies from 25 to 10 mm per day (Langston and Rohwer1996)

Feather and blood samples from chicks of Thin-billedprions Pachyptila belcheri were collected as part of ongo-ing studies of their breeding biology at New Island NatureReserve Falkland Islands (eg Quillfeldt et al 2003 20062007a b c) The present study includes samples collectedfrom 40-day-old chicks during the breeding seasons 2004ndash2005 (N = 7) and 2005ndash2006 (N = 10) Birds were capturedby hand and blood samples (02ndash04 ml) were collectedfrom the brachial vein using heparinized capillaries within2 min from burrow opening to the end of blood samplingBlood samples were immediately transferred to 05-mltubes and kept on ice until centrifugation Plasma (used forhormone analyses eg Quillfeldt et al 2006 2007c) andblood cells (used in the present analysis) were stored frozenin separate 05-ml tubes at iexcl20degC Undertail covert feath-ers of chicks were collected shortly before Xedging by gen-tle pulling and placed in individual sealed plastic bags TheWrst tail feathers of chicks including the tail coverts startto emerge after 3 weeks of age (eg Strange 1980 ldquoat

22 days the sheaths of the rectrices can be felt protrudingrdquo)therefore the distal parts of these feathers represent themiddle of the nestling growth period of 50ndash56 days Thehalf-life of isotope turnover of avian red blood cells was298 days in crows Corvus brachyrhynchos (Hobson andClark 1993) and 109 days for Yellow-rumped warblersDendroica coronata (Podlesak et al 2005) The red bloodcell samples collected from Thin-billed prion chicks there-fore represented the diet ingested ca 2ndash4 weeks before thesampling at 20 days ie at the same time as the analyzedfeather parts

Sample preparation and stable isotope analysis

Feathers were cut into small fragments using stainless steelscissors and whole blood and red blood cells (RBC) werefreeze-dried and ground Carbon and nitrogen isotopeanalyses were carried out on 065ndash07 mg aliquots ofhomogenized powder weighed into tin cups

Carbon and nitrogen isotope ratios were measuredsimultaneously by continuous-Xow isotope ratio mass spec-trometry (CF-IRMS) using a Costech Elemental Analyser(EA) linked to a Thermo Finnigan Delta Plus XP MassSpectrometer Two laboratory standards were analyzed forevery ten unknown samples allowing any instrument driftover a typical 14-h run to be corrected Stable isotope ratioswere expressed in notation as parts per thousand (permil)deviation from the international standards V-Pee Deebelemnite (carbon) and AIR (nitrogen) according to thefollowing equation X = [(RsampleRstandard) iexcl 1] pound 1000where X is 15N or 13C and R is the corresponding ratio 15N14N or 13C12C Based on internal standards (tryptophan)the analytical precision (sect 1 SD) was estimated as sect018permiland sect017permil for 15N and 13C respectively

Data analysis

Statistical tests were performed in Sigma Stat 203 All testsused pair-wise data for each individual carried out sepa-

Table 2 Carbon stable isotopes (means sect SE) of seabird blood and growing feathers representing similar time periods and individual diVerencesbetween the simultaneously sampled tissues (means sect SE)

Species Age 13C

Blood Feathers Paired diVerences

Pair-wise test Correlation

Thalassarche chlororhynchos Adults (N = 15) iexcl168 sect 01 iexcl155 sect 02 13 sect 01 t = 171 P lt 0001 R = 0894 P lt 0001

Procellaria conspicillata Adults (N = 21) iexcl171 sect 01 iexcl160 sect 01 11 sect 01 t = 132 P lt 0001 R = 0807 P lt 0001PuYnus gravis Adults (N = 15) iexcl169 sect 01 iexcl154 sect 01 14 sect 01 t = 180 P lt 0001 R = 0749 P = 0001

Pterodroma arminjoniana Adults (N = 18) iexcl175 sect 01 iexcl159 sect 02 15 sect 02 t = 77 P lt 0001 R = 0036 P = 0888

Pterodroma arminjoniana Chicks (N = 15) iexcl183 sect 01 iexcl172 sect 01 12 sect 02 t = 71 P lt 0001 R = 0080 P = 0776

Pachyptila belcheri Chicks (N = 17) iexcl199 sect 02 iexcl190 sect 02 09 sect 01 t = 139 P lt 0001 R = 0912 P lt 0001

123

596 Mar Biol (2008) 155593ndash598

rately for each species and age group Sample sizes aregiven in Table 2

Results

In all species and age groups the feathers were enriched in15N and 13C compared with blood (Table 2 Fig 1) ThediVerences ranged between 04 and 15permil for 15N andbetween 09 and 16permil for 13C (Table 2 Fig 1) In all spe-cies except Trindade petrels the 15N and 13C values offeathers and blood samples were highly correlated in indi-viduals (Table 2 Table 3)

Discussion

Our study shows diVerences between the carbon and nitro-gen stable isotopes of blood and simultaneously growingfeathers of Wve species of Procellariiformes representingWve genera We found that feathers were consistentlyenriched in 15N and 13C compared with blood in all species

This is in line with previous studies that reported diVer-ences in isotope values between blood and feathers (egHobson and Clark 1992b Bearhop et al 2000a Cherelet al 2005a b) However the present approach is novel inthat it used simultaneously collected samples from wildbirds in their natural habitat and exhibiting their naturalforaging behaviors In contrast previous studies did notsample the same individuals simultaneously (eg Cherelet al 2005a Bearhop et al 2000a for simultaneously sam-pled hydrogen see Langin et al 2007) Further studies withsimultaneous sampling to our knowledge have been car-ried out only in captive birds thus far (Hobson and Clark1992b Cherel et al 2005b but see Bugoni et al 2008a)

The most likely explanation for increased 15N and 13Cisotope enrichment in feathers compared to blood are meta-bolic diVerences These may be found in the diVerent pro-tein sources (several proteins in blood keratin in feathers)

and diVerences would also appear if endogenous reservesare used as precursors during feather synthesis (eg Cherelet al 2005a) For example a large diVerence between 15Nenrichment factors of whole blood and feathers may indi-cate that most amino acids available for keratin synthesisare provided by endogenous reserves Conversely almostidentical and low 15N enrichment factors in whole bloodand feathers may suggest a dietary origin of feather aminoacids (Cherel et al 2005a)

The presence of uric acid which is 15N depleted (Peter-sen and Fry 1987) has also been suggested as a cause ofisotopic diVerences between blood and feathers Bearhopet al (2000b) found that uric acid removal in Great skuaStercorarius skua blood increased the measured 15N by12permil while 13C was not aVected As Cherel et al (2005a)pointed out the eVect of uric acid is likely to be minimalbecause of the small amount of uric acid in blood com-pared to protein (Garcia-Rodriguez et al 1987 Boismenuet al 1992) Higher values might be found however intimes of high protein turnover such as during growth inchicks (Bearhop et al 2000b and references therein) In thepresent study both the nitrogen and carbon isotope ratioswere lower in blood than in feathers indicating that uricacid is not the only source for the observed diVerencebetween tissues In Thin-billed prions blood cells ratherthat whole blood were analyzed and as uric acid is presentin the plasma it should not interfere with the measurementsin this case In fact we found that the diVerence between15N of blood and feathers was smallest in Thin-billed pri-ons (04permil) and the diVerence was statistically signiWcant(P = 0021) rather that highly signiWcant (P lt 0001) as inall other species Thus when the separation of plasma ispossible this may be a good way to exclude uric acid as anerror source and allow better comparison between bloodand feathers from the same species

In four of Wve species in this study 15N and 13C valuesof feathers and blood samples from individual birds werehighly correlated There was one exception of this patternIn Trindade petrels we observed a correlation only for

Table 3 Nitrogen stable isotopes (means sect SE) of seabird blood and growing feathers representing similar time periods and individual diVer-ences between the simultaneously sampled tissues (means sect SE)

Species Age 15N

Blood Feathers Paired diVerences

Pair-wise test Correlation

Thalassarche chlororhynchos Adults (N = 15) 160 sect 04 171 sect 04 11 sect 02 t = 62 P lt 0001 R = 0765 P lt 0001

Procellaria conspicillata Adults (N = 21) 143 sect 02 155 sect 02 12 sect 01 t = 97 P lt 0001 R = 0819 P lt 0001PuYnus gravis Adults (N = 15) 148 sect 03 163 sect 03 15 sect 02 t = 62 P lt 0001 R = 0765 P lt 0001

Pterodroma arminjoniana Adults (N = 18) 113 sect 02 121 sect 02 08 sect 01 t = 52 P lt 0001 R = 0709 P lt 0001

Pterodroma arminjoniana Chicks (N = 15) 113 sect 01 120 sect 02 07 sect 02 t = 40 P = 0001 R = 0278 P = 0316

Pachyptila belcheri Chicks (N = 17) 121 sect 02 125 sect 02 03 sect 01 t = 25 P = 0021 R = 0859 P lt 0001

123

Mar Biol (2008) 155593ndash598 597

adults and only for nitrogen It is tempting to suggest thatthis may have resulted from a large variation in foragingareas over a short time as the Trindade petrel is the onlytropical species in our dataset In tropical species foragingoccurs over vast oceanic areas and thus there may be moreshort-term variation in diet as well as individual metabolicdiVerences (eg in the use of internal stores during feathergrowth) Foraging trips by Trindade petrel parents varyfrom hours to weeks (Luigi et al 2008) which could sug-gest that chicks use both diet and endogenous stores fortissue formation depending on feeding frequencies Thusthe lack of intertissue correlations of carbon and nitrogenisotope values could reveal individual diVerences accordingto nutritional status

In the present study the diVerence between blood andsimultaneously grown feathers was remarkably similaracross Wve species of Procellariiformes representing Wvegenera (Fig 1) despite diVerences in ecology and geo-graphical regions It was also in the range of the diVerencefound for captive King Aptenodytes patagonicus and Rock-hopper Eudyptes chrysocome penguins where Cherel et al(2005b) found diVerence of 15 and 17permil for 15N andbetween 09 and 11 permil for 13C

In deciding which tissue type is more reliable both tis-sue types have error sources In blood variable content ofuric acid and lipids is of concern but this may be avoided ifred blood cells can be used rather than whole blood whichmay also be beneWcial in many studies because red bloodcells sample a much longer time window than plasma (egPodlesak et al 2005) In feathers the variable use of endog-enous reserves during feather growth has to be taken intoaccount especially of certain amino acids such as sulphur-containing amino acids (cysteine and methionine) that areabundant in keratin but may be scarce in recently ingestedfood such that feather stable isotopes may also be biasedFor chicks the role of stored reserves is not usually a majorconcern although this needs to be conWrmed in speciesundergoing mass recession during the growth of the feath-ers as is the case in Procellariiformes The best solutionmay be the analysis of both blood and growing feather sothat the two together give a better indication than eithertissue alone

We suggest that future studies consider the following (i)Sample both tissues if possible to overcome limitations ofeach (ii) Use similar tissues to compare temporal patternswhen possible eg compare moult feathers with regrowthsin the breeding season (iii) RBC may be preferable towhole blood or plasma by avoiding uric acid eVects onnitrogen isotope ratios (iv) Correlation between isotopicvalues of diVerent tissues of similar age should beaddressed which could provide arithmetic corrections andmake comparisons across tissues viable (v) More researchis needed on metabolic diVerences between chick and

adults as well as studies addressing diVerences in chick andadult diets in the nesting period (vi) Avoid preserving tis-sues with preservatives containing the stable isotopes to beanalyzed such as ethanol or heparin for determination of SIof carbon in blood

Acknowledgments We are grateful to the following organizationsthat facilitated Weldwork New Island Conservation Trust ProjetoAlbatroz captain and crew of Wshing vessel lsquoAna Amaralrsquo and theBrazilian Navy NERC funded the isotope analysis We would like toacknowledge Wnancial support by DFG Germany (Qu 1481-V) andNew Island Conservation Trust Fieldwork at New Island was ap-proved by the Falkland Islands Government (Environmental PlanningOYce) and in Brazil by environmental agency (IBAMA) through per-mits No 0128931BR No 2032006 No 020010059812005 No0232006 No 0402006 and No 12821 and International AnimalHealth CertiWcate No 0975ndash06 The Scottish Executive-Rural AVairsDirectorate also kindly provided us the permit POAO 200791 to im-port samples into Scotland LB received a CAPES Scholarship

Open Access This article is distributed under the terms of the Crea-tive Commons Attribution Noncommercial License which permits anynoncommercial use distribution and reproduction in any mediumprovided the original author(s) and source are credited

References

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Bearhop S Teece MA Waldron S Furness RW (2000b) InXuence oflipid and uric acid on 13C and 15N values of avian blood impli-cations for trophic studies Auk 117504ndash507 doi1016420004-8038(2000)117[0504IOLAUA]20CO2

Bearhop S Phillips RA McGill R Cherel Y Dawson DA Croxall JP(2006) Stable isotopes indicate sex-speciWc and long-term indi-vidual foraging specialisation in diving seabirds Mar Ecol ProgSer 311157ndash164 doi103354meps311157

Boismenu C Gauthier G Larochelle J (1992) Physiology of prolongedfasting in Greater Snow Geese (Chen caerulescens atlantica)Auk 109511ndash521

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Bugoni L Neves TS Peppes FV Furness RW (2008b) An eVectivemethod for trapping scavenging seabirds at sea J Field Ornithol79(3)308ndash313 doi101111j1557-9263200800178x

Cherel Y Hobson KA Bailleul FR Groscolas R (2005a) Nutritionphysiology and stable isotopes new information from fastingand molting penguins Ecology 862881ndash2888 doi10189005-0562

Cherel Y Hobson KA Hassani S (2005b) Isotopic discrimination be-tween food and blood and feathers of captive penguins Implica-tions for dietary studies in the wild Physiol Biochem Zool78106ndash115 doi101086425202

Cherel Y Phillips RA Hobson KA McGill R (2006) Stable isotopeevidence of diverse species-speciWc and individual wintering

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Forero MG Gonzalez-Solis J Hobson KA Doncazar JA BertellottiM Blanco G et al (2005) Stable isotopes reveal trophic segrega-tion by sex and age in the southern giant petrel in two diVerentfood webs Mar Ecol Prog Ser 296107ndash113 doi103354meps296107

Garcia-Rodriguez T Ferrer M Carrillo JC Castroviejo J (1987)Metabolic responses of Buteo buteo to long-term fasting andrefeeding Comp Biochem Physiol A 87381ndash386 doi1010160300-9629(87)90139-3

Gladbach A McGill RAR Quillfeldt P (2007) Foraging areas ofWilsonrsquos storm-petrel Oceanites oceanicus in the breeding andinter-breeding period determined by stable isotope analysis PolarBiol 301005ndash1012 doi101007s00300-007-0258-2

Hobson KA Clark RG (1992a) Assessing avian diets using stableisotopes I Turnover of 13C in tissues Condor 94181ndash188doi1023071368807

Hobson KA Clark RG (1992b) Assessing avian diets using stable iso-topes II Factors inXuencing diet-tissue fractionation Condor94189ndash197 doi1023071368808

Hobson KA Clark RG (1993) Turnover of 13C in cellular and plasmafractions of blood implications for nondestructive sampling inavian dietary studies Auk 110638ndash641

Hobson KA Welch HE (1992) Determination of trophic relationshipswithin a high Arctic marine food web using 13C and 15N analy-sis Mar Ecol Prog Ser 849ndash18 doi103354meps084009

Hobson KA Sirois J Gloutney ML (2000) Tracing nutrient allocationto reproduction with stable isotopes a preliminary investigationusing colonial waterbirds of Great Slave Lake Auk 117760ndash774doi1016420004-8038(2000)117[0760TNATRW]20CO2

Langin KM Reudink MW Marra PP Norris DR Kyser TK RatcliVeLM (2007) Hydrogen isotopic variation in migratory bird tissuesof known origin implications for geographical assignment Oec-ologia 152449ndash457 doi101007s00442-007-0669-3

Langston NE Rohwer S (1996) Molt-breeding tradeoVs in albatrosseslife story implications for big birds Oikos 76498ndash510 doi1023073546343

Luigi G Bugoni L Fonseca-Neto FP Teixeira DM (2008) Biologia econservaccedilatildeo do petrel-de-trindade Pterodroma arminjoniana nailha da Trindade Atlacircntico sul In Mohr LV Castro JWA CostaPMS Alves RJV (eds) Ilhas oceacircnicas brasileiras da pesquisa aomanejo vol 2 Ministeacuterio do Meio Ambiente Brasiacutelia

Minagawa M Wada E (1984) Stepwise enrichment of 15N along foodchains further evidence and the relation between 15N and animal

age Geochim Cosmochim Acta 481135ndash1140 doi1010160016-7037(84)90204-7

Nisbet ICT Montoya JP Burger J Hatch JJ (2002) Use of stables iso-topes to investigate individual diVerences in diets and mercuryexposures among Common terns Sterna hirundo in breeding andwintering grounds Mar Ecol Prog Ser 242267ndash274 doi103354meps242267

Owens NJP (1987) Natural variation in 15N in the marine environmentAdv Mar Biol 24389ndash451 doi101016S0065-2881(08)60077-2

Petersen BJ Fry B (1987) Stable isotopes in ecosystem studies Annu RevEcol Syst 18293ndash320 doi101146annureves18110187001453

Podlesak DW McWilliams SR Hatch KA (2005) Stable isotopes inbreath blood feces and feathers can indicate intra-individualchanges in the diet of migratory songbirds Oecologia 142501ndash510 doi101007s00442-004-1737-6

Quillfeldt P Masello JF Strange IJ (2003) Breeding biology of theThin-billed prion Pachyptila belcheri at New Island FalklandIslands in the poor season 20022003 egg desertion breedingsuccess and chick provisioning Polar Biol 26746ndash752doi101007s00300-003-0544-6

Quillfeldt P McGill RAR Furness RW (2005) Diet and foraging areasof Southern Ocean seabirds and their prey inferred from stableisotopes review and case study of Wilsonrsquos storm-petrel MarEcol Prog Ser 295295ndash304 doi103354meps295295

Quillfeldt P Masello JF Strange IJ Buchanan KL (2006) Begging andprovisioning of Thin-billed prions Pachyptila belcheri is relatedto testosterone and corticosterone Anim Behav 711359ndash1369doi101016janbehav200509015

Quillfeldt P Strange IJ Masello JF (2007a) Sea surface temperaturesand behavioural buVering capacity in Thin-billed prions Pachyp-tila belcheri breeding success provisioning and chick beggingJ Avian Biol 38298ndash308

Quillfeldt P Strange IJ Segelbacher G Masello JF (2007b) Male andfemale contributions to provisioning rates of Thin-billed prionsPachyptila belcheri in the South Atlantic J Ornithol 148367ndash372 doi101007s10336-007-0138-0

Quillfeldt P Poisbleau M Chastel O Masello JF (2007c) Corticoste-rone in Thin-billed prion Pachyptila belcheri chicks diel rhythmtiming of Xedging and nutritional stress Naturwissenschaften94919ndash925 doi101007s00114-007-0275-6

Rubenstein DR Hobson KA (2004) From birds to butterXies animalmovement patterns and stable isotopes Trends Ecol Evol 19256ndash263 doi101016jtree200403017

Strange I (1980) The Thin-billed prion Pachyptila belcheri at NewIsland Falkland Islands Gerfaut 70411ndash445

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