TheAuk 114(3):467-478, 1997
USING
STABLE-ISOTOPE
ANALYSIS
TO IDENTIFY
ENDOGENOUS
AND EXOGENOUS
SOURCES OF NUTRIENTS
IN EGGS OF
MIGRATORY
BIRDS: APPLICATIONS
TO GREAT LAKES
CONTAMINANTS
RESEARCH
KEITH A. HOBSON,TM KIMBERLEYD. HUGHES?AND PETERJ. EWINS3
•Canadian
WildlifeService,
115Perimeter
Road,Saskatoon,
Saskatchewan
S7N OX4,Canada;
2Department
of Biology,
Universityof Saskatchewan,
Saskatoon,SaskatchewanS7N OWO,Canada; and
'•Canadian
WildlifeService,
Environmental
Canada,4905DufferinStreet,Toronto,
OntarioM3H 5T4, Canada
ABSTR^CT.--Stable-isotope
analyses (carbon [13C/12C]and sulfur [•4S/32S])were performedon eggsof two migratoryfish-eatingbirds,CaspianTerns(Sternacaspia)
andDoublecrestedCormorants(Phalacrocorax
auritus)collectedfrom Lake Ontario, Canada, to examine
the extentto whichnutrientreservesacquiredon marinewinteringgroundsare transferred
to eggslaid on freshwaterbreeding grounds.In order to establishisotopicpatternstypical
of eggsof birds usingmarine and freshwaterC-3 biomes,eggsof Herring Gulls (Larusargentatus),a year-roundresidenton the Great Lakes,and thoseof CaspianTernsand Herring
Gulls, breedingresepectivelyin the Gulf Coastof Texasand Atlantic Coastof Canada,were
analyzedisotopically.Individualeggcomponents
showeddistinctisotopevaluesthatwere
similarfor both migratoryand nonmigratorybirdsbreedingin a freshwaterbiomeand significantlylighterthanthosebreedingin a marinebiome.Hence,thereappearedto be little
evidencefor significantnutrienttransferbetweenthe two biomes.The intermediateisotope
valuesshownfor eggcomponents
of Herring Gullsbreedingon the AtlanticCoastsuggest
nutrient input from terrestrialas well as marine sources.Our resultsindicatethe utility of
stable-isotope
analysisfor tracingendogenous
and exogenous
contributionsto reproduction
in birds and further validatethe useof migratorybirds as indicatorsof breedingareacontaminant levels and their effects on the Great Lakes. Received16 October1996, accepted14
February1997.
HIGH LEVELS
OF CONTAMINANTS
present in
eggs of Double-crestedCormorants(Phalacrocoraxauritus)and Herring Gulls (Larusargentatus)havebeenlinkedto thelow reproductive
successshown by these speciesin the Great
Lakesin the early 1970s(Gilbertson1974,We-
birds as indicatorsof local contaminantexposure on the Great Lakesbreedinggroundsseldomhasbeenquestionedfor two reasons.First,
spatialpatternsof contaminantlevelsin the
eggsof thesebirdswere similarto thosein fish
(Sunset al. 1991), sediments(Frank et al. 1977,
selohet al. 1983).Thesespecies,
togetherwith 1979), and eggs of other piscivorousbirds
CaspianTerns(Sternacaspia)
havebeenstudied (Bishopet al. 1992a,b;Yamashitaet al. 1993;
extensivelyin the Great Lakes Basin as part of
the Great
Lakes
colonial
waterbird
contami-
Pettit et al. 1994a,b). Second,in the 1970s and
1980s,the Great Lakesecosystemwas one of
nantsmonitoringprograminitiatedin 1971by
the Canadian Wildlife Service (Mineau et al.
1984;Governmentof Canada1991;Bishopet al.
1992a,b;Pettitet al. 1994a,b).Over the past20
years, however, contaminant levels have
dropped substantiallyand breeding populationshaveincreaseddramatically(Mineau et al
the most contaminatedfreshwatersystemsin
the world, and levels generally were much
higher than thoseat wintering groundselsewhere (Nriagu and Simmons1984).Therefore,
the contribution
of contaminants
from winter-
ing groundsto eggslaid in theGreatLakeswas
thoughtto be minimal.
1984; Ewins et al 1994b; Weseloh et al 1994,
Levels of most persistentcontaminantsin
1995).During this time, the use of migratory fish and bird speciesin the Great Lakeshave
declinedto a plateausincethe mid-1980s(Mi4Send correspondenceto Canadian Wildlife Ser- neauet al. 1984,Borgmannand Whittle 1991).
vice, 115 Perimeter Road, Saskatoon, Saskatchewan Small but detectabletemporalfluctuationsin
S7N 0X4, Canada.E-mail:[email protected] residuelevelsremainin bird eggs(Bishopet al.
467
468
HOBSON,
HUGHES,
ANDEWINS
[Auk,Vol. 114
1992a,b; Pettit et al. 1994a,b). These fluctua- gen (Fry and Sherr 1988, Michener and Schell
tions probablyare due to many different fac- 1994). The occurrenceof isotopicallydistinct
tors, includingvariation in local feedingcon- inputs to varioussystemsalso forms the basis
ditions,availabilityof foragefish (Ewinset al. for usingstable-isotope
measurements
to trace
1994b), and the influence of weather-induced sourcesof pollutantsin food webs(seeMacko
changesthat might affect ratesof contaminant and Ostrom 1994).
uptake in biota (Smith 1995).The contribution
Dietary shifts in birds from terrestrial or
of endogenousnutrients,and hencelipophilic freshwaterC-3 to marineecosystems
(andvice
persistent contaminants from wintering versa)influenceisotopicsignaturesin a variety
grounds,is anotherpotential sourceof varia- of tissues (Hobson 1987, 1990; Mizutani et al.
tion influencing temporal trends in contami- 1990;Thompsonand Furness1995).Bird eggs
nant levelsin eggsof thesemigratoryspecies. are particularly amenableto this type of analHowever,techniquesfor tracing the origin of ysisbecausenutrientsrequiredfor eggproducnutrient input into eggs from endogenousre- tion are derivedfrom the diet of the laying feservesacquiredon the wintering groundshave male (von Schirndinget al. 1982,Schaffnerand
been unavailableuntil recently.In this study, Swart 1991, Hobson 1995, Jarman et al. 1996).
we evaluatetheuseof stable-isotope
analysisof In their recentexaminationof seabirdeggsand
eggsfor tracing nutrient transferbetweenbi- marineprey,Jarmanet al. (1996)suggestedthat
omesand henceof the relative importanceof the combined use of contaminant and stableendogenousand exogenous
nutrientresources isotope analysesof egg proteins and lipids
to reproduction.
couldprovide informationon the allocationof
Stable-isotope
analysisof tissuescanprovide endogenous
versusexogenous
lipid reservesto
valuable information on the diets of individuals
eggs. This, together with the isotopicinvestiand populations(von Schirndinget al. 1982; gationsof Hobson(1995) using captive-raised
Hobson, 1987, 1990; Mizutani et al. 1990; birds,clearlysuggeststhatstableisotopicanalSchaffnerand Swart 1991;Hobsonand Sealy ysesof variouseggcomponentscanprovidein1991; Hobson et al. 1994). This approachis formationon the sourceof nutrientsin eggprobasedon the premisethat stable-isotope
ratios duction.Our objectivewas to test the hypothof various elements in a consumer's tissues ulesis that migratory birds wintering in marine
timatelyare relatedto thosein its diet (DeNiro areasacquirebody-nutrientreservesthat ultiand Epstein1978,1981).Conventionalmethods mately are transferredto their eggs laid on
of diet analysisprovide a relativelyshort-term freshwaterbreedinggrounds.
and detailedassessment
of dietary intake.StaMATERIALS AND METHODS
ble-isotopeanalysiscomplementsthesemethods by allowing time-integrateddietary estimates and the evaluation
of assimilated
versus
ingesteddietary contributions(Tieszenet al.
1983, Hobson 1993). Stable-isotopeanalysis
alsomaybe particularlyusefulin determining
the origin of nutrients in consumertissuesin
cases where accessto isotopically distinct
sourcesof food occurs.Using this approach,
the relative
contributions
of terrestrial
and ma-
Studysitesandcollections.--Eggs
of two migratory,
fish-eatingcolonial waterbirdswere selected:Double-crestedCormorant and Caspian Tern. Both speciesmigrate from their wintering groundsin the Atlantic and Gulf Coast states (and the Carribean Ba-
sin, in the caseof terns)and arrive in April to breed
in the Great Lakes in Canada (L'Arriv•e and Blokpoel 1988, Dolbeer 1991, Weselohand Ewins 1994).
For comparativepurposes,we alsoanalyzedeggsof
rine protein to consumerdietshavebeenestab- CaspianTernsbreedingin a marineenvironmentof
lished for both modern and ancient food webs
because •3C abundance in marine food webs
coastalTexas.Stable-isotopevaluesfor the eggsof
Herring Gulls,oneof the few nonmigratory,colonial
fish-eating birds that breed on the Great Lakes
typicallyis enrichedoverthat of terrestrialC-3
(Moore 1976, Gilman
food webs (Chisholmet al. 1982,Schoeninger
and DeNiro 1984; Hobson and Collier 1984;
Hobson1987,1990;Mizutani et al. 1990).Other
elementswith stable-isotopevalues that are
typically enrichedin marine versusterrestrial
foodwebsincludesulfur,hydrogen,andnitro-
et al. 1977, Weseloh 1984), were
comparedwith thoseof nonmigratoryHerring Gulls
collected from a marine environment
on the Atlantic
Coastof Canada.In general,a transferof marine-derived nutrientsto eggslaid in a freshwateror terrestrial C-3 biomewould be indicatedby a substantial
enrichmentof •3Cor uS valuesabovethoseexpected
July1997]
Isotope
Tracers
ofEggNutrients
469
from nonmigratory birds that feed exclusivelyin
to sulfateby nitric-aciddigestion,nitrate fusion,and
barium precipitation,followed by thermal decomEggs of Double-crestedCormorants, Caspian positionto sulfur dioxidebeforebeinganalyzedusTerns,and Herring Gulls were collectedfrom Pigeon ing the VG OPTIMA massspectrometer.
Island, Lake Ontario (44ø04'N,76ø33'W).In addition,
Stable-isotope
concentrations
wereexpressed
in 8
CaspianTerneggswere collectedfrom nestson spoil notationas the deviationfrom standardsin partsper
islands in the Laguna Madre of Texas(26ø21'N, thousand (%0) accordingto the following relation97ø18'W),andHerringGull eggswerecollectedfrom ship:
these latter areas.
two islands located on the Atlantic
coast of Canada:
8X = [(/ ...... /n .......d)- 1] X 1000,
(1)
Kent Island (44ø35'N,66ø45'W)in the Bayof Fundy,
and Gull Island (47ø16'N,52ø46'W)in Witless Bay, where X is •C or 34Sand R is the correspondingratio
Newfoundland.
•C/•2C or •4S/,•2S.Rm,aara
values for •3C and •4Scor-
One eggper nestwascollectedfrom freshlycompleted clutches.Although no attemptwas made to
randomize collection,samplingwas opportunistic
and likely unbiased because observers walked
throughoutcoloniesduring collections.Egg "freshness"was determinedby the appearanceof newly
deposited calcium carbonateresidue around the
shelland by flotation.Thus,all eggscollectedprobably were within the first 10 daysof incubation.Each
egg was wrapped in aluminum foil and frozen at
respond to the Pee Dee Belemnite(PDB) standard
and Canyon Diabolo standard,respectively.Using
laboratory internal standardsfor organic material,
analyticalerror was estimatedto be -+ 0.3%0for •C
samplesrun on the Robo Prep, _+0.1%ofor carbon-
selectednestscontainingearly clutches(14 May
1993) and from each of six nestscontaininglate
clutches(10 June1993).CaspianTerneggsalsowere
nificance
ates run on the VG OPTIMA, and _+0.3%0for sulfur
samples.
Statistical
analyses.--Simultaneous
comparisons
of
mean8•3Cand 8•4Svaluesin eggyolk amongspecies
and siteswere performedusing a multivariateanal-20øC within six h of collection. Within Lake Ontarysis of variance(MANOVA) and Wilks' Lambdaas
io, HerringGull eggswerecollectedon 27 April 1994 the teststatistic.Mean 8•3Cvaluesfor yolk lipid and
(n = 7) and 14 May 1993 (n = 5), and CaspianTern eggshellcarbonatewere comparedamong species
eggswere collectedon 5 May 1994(n = 12) and 14 and sites using a one-way analysis of variance
May 1994 (n = 4). Becauseno significant difference (ANOVA). For all egg components,Tukey multiple
in stable-isotoperatiosbetweencollectiondateswas range test was used to identify the sourceof variaobservedfor anyeggcomponent,
valueswerepooled tion when significant differenceswere detected
within species.To examine the influence of the amongspeciesand sites.Unlessstatedotherwise,all
referto this test.Statisticalanalamountof time spenton freshwaterbreedingareas testsof significance
to changesin isotoperatios,oneDouble-crested
Cor- yses were conductedusing SAS version 6.04 (SAS
moranteggwascollectedfrom eachof 10 randomly 1985). All tests were two-tailed, and statisticalsig-
collectedfrom the Gulf of Texason 10 May 1993 (n
= 10), and Herring Gull eggs were collectedfrom
Kent Island on 6 June1993 (n = 5) and from Gull Island on May 23, 1994 (n = 12).
Stable-isotope
analysis.--Eggshell,albumen, and
yolk sampleswereseparatedby hand;subsamples
of
yolk were obtaind with a syringe.Eggshellswere
rinsedin distilledwater,allowedto dry at roomtemperature (after shell membraneswere removed), and
powdered using a mortar and pestle. Yolk was similarly powderedafter freezedrying. Yolk lipids were
removedfrom a subsampleof yolksusingthe method of Bligh and Dyer (1959).
Powderedlipid-free yolk (hithertoreferredto as
yolk), yolk lipid, and eggshellsamplesfor stable-carbon isotopeanalysiswere placedin tin cupsand introducedinto a EuropaRoboPrep combustionsystem interfacedwith a EuropaTracermatcontinuous-
was defined
as P < 0.05.
RESULTS
Marine-freshwater
comparison.--Stable-carbon
isotope values differed among egg components, with eggshell carbonatesshowing the
mostenrichedand yolk lipids the mostdepleted values (Table 1). Overall, significantdifferencesamongall speciesandsitesweredetected
in valuesof 813Cand 834Sin yolk (MANOVA,
Wilks' Lambda F = 55.42, df = 10 and 104, P <
0.0001), and in values of 81•Cin yolk lipids
(ANOVA, F = 38.31, df = 6 and 61, P < 0.0001)
and eggshellcarbonates(ANOVA, F = 49.56,df
= 5 and 53, P < 0.0001). Furthermore, these dif-
ferencesfit a consistentpattern; i.e. egg com-
ponentsof CaspianTernsfrom coastalTexas
were significantlymore enrichedin •C and 34S
flow isotope-ratiomassspectrometer.
Eggshellcar- than thosespecies,includingCaspianTerns,
bonateswere reacted with phosphoricacid under that bred at Lake Ontario (Tukey teststhroughvacuumto evolveCO2for directisotopicanalysisus- out;Table1, Fig. 1). Herring Gulls breedingoff
tended to show intermediate
ing a VG OPTIMA massspectrometer.
Yolksamples Newfoundland
for stable-sulfurisotopeanalysiswere decomposed valuesof 8•C and 8•4Sbetweenthosebreeding
470
HOBSON,
HUGHES,
ANDEWINS
[Auk,Vol.114
TABLE
1. Stable-isotope
analysis(2 -+SD,rangeandnumberof eggsanalyzedin parentheses)
of eggcomponents.
Withincolumns,
meanswith thesameletterarenotsignificantly
different(P > 0.05;Tukeytest).
ForDouble-crested
Cormorants,
earlyandlateclutches
areindicated
by E andL, respectively.
Species
Yolk8•3C(%o)a
Yolklipid 8•3C(%o) Carbonate8•3C(%0)
Yolk8•4S(%o)a
Lake Ontario
Double-crested
Cormorant E
Double-crested
Cormorant L
CaspianTern
Herring Gull
-22.8
_+ 1.2 ^"
-25.3
(-21.1 to -24.7, 10)
-23.9
(-22.9
-25.0
(-23.0
-24.0
(-22.0
+_ 0.7 Bc
_+ 0.9"
-25.7
to -25.0, 6)
_+1.2c
to -27.2, 16)
_+1.0•c
to -25.3, 12)
_+ 0.6 "c
-27.0
-21.8 _+0.6^
(-21.0 to -22.6, 5)
_+ 0.5"
4.4 _+ 0.5"
(-10.5 to -11.9, 10)
-11.4
(-25.1 to -26.7, 6)
(3.5 to 5.0, 10)
+ 0.4 B
4.9 + 0.2 B
(-10.6 to -12.6, 6)
_+ 1.5 c
-11.6
(4.6 to 5.2, 6)
_+ 0.8 B
5.0 + 0.6 B
(-25.0 to -30.8, 13) (-10.7 to -12.9, 16)
-26.2
+ 0.7 Bc
-11.0
(-25.5 to -27.0, 12)
New
Herring Gull
-11.2
(-23.7 to -27.1, 10)
-23.2
(4.1 to 6.2, 13)
+_ 0.8"
4.6 +_ 0.5"
(-9.9 to -12.3, 12)
(3.8 to 5.2, 12)
Brunswick
+_ 0.6 ^
-9.4
-22.6 to -24.0, 5)
_+ 2.3 ^
(-6.4 to -11.4, 5)
--
Newfoundland
Herring Gull
-21.7 _+1.3^
(-19.8 to -24.1, 12)
-25.6
ñ 0.7 •c
Coastal
Caspian Tern
-18.6 +_1.0ø
(-16.3 to -19.5, 10)
10.7 ñ 2.0 ^
(-24.6 to -27.1, 12)
-21.2
--
(7.9 to 13.7, 8)
Texas
_+ 1.3 TM
-5.4
(-18.4 to -23.3, 10)
-+ 1.5 TM
16.0 + 1.3 t•
( 3.0 to -7.6, 10)
(15.0to 17.7,10)
"Lipids removed.
in LakeOntarioandCaspianTernsbreedingin Wilks' Lambda F = 60.33, df = 2 and 17, P <
the Gulf of Texas(Table1, Fig. 1). Significant 0.0001). No differenceswere detected for •3C
differences were detected in •sC and •34 S valvaluesin yolk lipids of HerringGull eggsfrom
uesin yolk of HerringGull eggscollectedfrom Lake Ontario versus Newfoundland. However,
Lake Ontario and Newfoundland (MANOVA, differences
weresignificantbetweenmeanyolk
TERRESTRIAL
C-3
MARINE
FRESHWATER
20.0
TEXAS
COAST
18.0
LU
Z
16.0
NEWFOUNDLAND
14,0
12,0
10,0
8.0
LAKE ONTARIO
6.0
LEGEND:
LU •
ß CATE
o HEGU
4,0
2.0
I* OCCOI
0.0
-28.0
•26.0
-24.0
-22.0
-20.0
-18,0
-16.0
(•13C
(%0)
F•G.1. Stablecarbon-andsulfur-isotope
values(œ_+SD)of lipid-removed
eggyolkof birdsfromLake
Ontario,Newfoundland
andtheTexascoast.CATE,CaspianTern;HEGU,HerringGull;DCCO,Double-crested Cormorant.
July1997]
•3C
Isotope
Tracers
ofEggNutrients
values for these two sites and New Bruns-
wick (ANOVA, F = 33.64, df = 2 and 26, P <
0.0001).Significantdifferencesalso were detectedin •3C valuesin eggshellcarbonates
of
HerringGull eggscollectedfrom LakeOntario
471
cantlydifferentfromeggsof HerringGulls(not
shown in Table 1). There were no significant
differences
in valuesof g•3Cin eggshellcarbonatesamongspeciesfoundin Lake Ontario.
and New Brunswick (ANOVA, F = 4.80, df = 1
DISCUSSION
and 15, P = 0.045).
LakeOntariocomparison.--For
speciesbreedStable-isotope
valuesin freshwater
versusmarine
ing on Lake Ontario, the isotope signatures environments.--Thedistinct isotopic segrega-
weretypicalof C-3 freshwaterbiomes(Table1,
Fig. 1). Generally,Double-crestedCormorant
eggsshowedmore enriched•C valuesthan
did CaspianTerneggs.Marginallysignificant
tion in egg componentsamongCaspianTerns
breedingin the marine environmentof Texas
and Double-crestedCormorantsand Caspian
Ternsbreedingon Lake Ontario provideslittle
differences were detected in • C and •34 S in
evidencefor significanttransferof endogenous
yolk between early versuslate-laid Double- reservesfrom marine wintering sitesby corcrested Cormorant eggs (MANOVA, Wilks' morantsand ternsto their eggslaid in a fresh-
Lambda F = 4.11, df = 2 and 13, P = 0.042),
waterecosystem.
Theisotopicevidence
forthis
with late-laideggsshowing•C and •S valuessimilarto thosefor HerringGulls andCaspian Ternson LakeOntario.The resultsof the
MANOVA and Tukeytests(denotedby superscriptsin Table1) may not agreebecausethe
formertest,which is morerigorous,compares
is based on inferencesfrom our investigation
means
for
two
different
variables
simulta-
neously(e.g.•3C and •S valuesin yolk), and
the lattertestcomparesmeansfor onevariable
acrossall sitessampled.No significantdifferenceswere found betweenearly and late-laid
cormoranteggsin •C of yolk lipids and eggshellcarbonates.
Consequently,
for thepurpose
of interspecificcomparisonson Lake Ontario,
thesetwo groupswere pooled for both egg
components(seebelow).
Overall, significantdifferencesoccurredin
•3C and •4S values in yolk among species
breeding on Lake Ontario (MANOVA, Wilks'
Lambda F = 3.78, df = 6 and 72, P = 0.0025;
not shown in Table 1). When •C
and •4S val-
ues were analyzed separatelyamongspecies,
early laid Double-crestedCormoranteggswere
significantlymoreenrichedin valuesof •3C in
yolk than were valuesof •C in CaspianTern
eggs. No significant differencesoccurred in
valuesof •4S amongLakeOntariospecies.Sig-
involvingstableisotopesof two elementsand
of three egg components.
Our use of several
eggcomponents
wasbasedon aninterestin evidencefor mobilizationof both proteinsand
lipids from endogenousreserves.Although
birdsmightbe expectedto synthesizeeggproteins directly from their diet, systematicdeclinesin somaticprotein in responseto protein
demandsduring egg productionhave been
demonstrated in waterfowl (Alisauskas and
Ankney1992;seealsoHoustonet al. 1995,Williams 1996). In such cases,the occurrenceof
carbonor sulfur from proteinsoriginatingin
body reservesthat were in turn derivedfrom
areasseparatefrom the breedinggroundsis
possible.Lipid-nutrientstorageprior to reproduction has been demonstrated
in waterfowl
(Alisauskasand Ankney 1992;but seePerrins
1996),and it was this componentof eggsthat
we assumedwouldhavethegreatestlikelihood
of providingisotopicevidencefor transferbetween marine and freshwatersystemsby migratingbirds. Our g•3Canalysisof shell carbonatewasperformedto testwhethercarbon
isotopevaluesof eggshellare directlyrelated
to isotopevaluesin localfoods.Unlikecalcium
nificant differences also were found for •C
that may be mobilizedfrom medullarybone
valuesin lipid amongeggsof CaspianTerns, duringshellformation,carbonfor the calcium
HerringGulls,andDouble-crested
Cormorants carbonatefraction of shell is derived directly
(pooled)in LakeOntario (ANOVA,F = 8.41,df from plasmathroughthe metabolismof re= 2 and 38, P = 0.0009);upon furtherinvesti- cently assimilatedfood (Simkiss and Tyler
gation, only lipid values in eggs of Double- 1958).
Theaverageg•3Cvaluesof eggyolk, yolklipcrested Cormorants (pooled) and Caspian
for birdsbreeding
Ternsweresignificantly
different,whereasval- ids, andeggshellcarbonates
ues for both of thesespecieswere not signifi- on Lake Ontario were -24.1, -26.2, and
472
HOBSON,
HUGHES,
ANDEWINS
[Auk, Vol. 114
-11.3%o, respectively,and the differencebetween these values and the respectivevalues
for eggsof CaspianTernsbreedingon the Gulf
coastof Texas(Table1) were remarkablyconsistent,rangingfrom 5.0 to 5.9%0.This isotopic
sulfur occurringspecificallyin protein pathways involving sulfur-bearing amino acids
(e.g.cystein)comparedwith carbonthat occurs
in all amino acids.As such,seasonalchangesin
stable-carbonand sulfur isotopevalues may
difference between marine and freshwater endnot necessarilybe correlated.
points is consistentwith carbon-isotopegraIt is alsopossiblethat diets of breedingcordients previouslymeasuredbetweenprimary morants changedseasonally(see below). Anproductionin each of thesebiomes(Fry and other variable complicatinginterpretationof
Sherr 1988, Schaffner and Swart 1991). How- the cormorantdatais that the entirepopulation
ever, considerable variation in •3C values of bi- doesnot winter consistentlyin marineenvironota in freshwatersystemsalsohavebeendoc- ments.Most of the recoveriesof juvenileDouumented (France 1995, Hecky and Hesslein ble-crestedCormorants(72%,age 1 to 2 years)
1995). Nevertheless, our inferences based on
banded
on Lake Ontario
in 1986 occurred
dur-
•C values are corroboratedby •4S analyses ing the winter months on the mid-Atlantic
and, for all egg componentsthat we examined, Coast and the Gulf Coast portions of Florida,
there was no isotopicevidencefor significant Mississippi, and Louisiana (Weseloh and
transfer of nutrients
from marine to freshwater
locations.Further support for this inference
was provided by the similar carbonand sulfur
isotopevaluesfor Lake Ontario Herring Gull,
Caspian Tern, and Double-crestedCormorant
eggs, becauseHerring Gulls were resident
year-round and were expectedto provide an
Ewins 1994). The remainder of the recoveries
occurredfarther inland in Mississippi,Louisiana, and Texas, where Double-crested Cormo-
rants have been observedincreasinglyin the
last 20 yearsfeedingat freshwaterlakes(Campoet al. 1993) and fish farms (Glahn and Stickley 1995, Jacksonand Jackson1995). If these
entirely non-marine signal.
patternsare typical of adults,then most DouWe also were interestedin determining if ble-crestedCormorantswould be expectedto
there was evidencefor changesin the isotope have endogenousreserveswith isotopic sigsignaturesof egg componentsbetween birds natures characteristicof a marine biome prior
laying eggsshortlyafter arrival and thoselay- to arriving on the breeding grounds,provided
ing eggslater.A shift towardisotopicallylight- that few reserveswere acquiredduring migraer isotopevaluesof eggcomponents
laterin the tory stopoversin freshwaterhabitats(Hobson
seasonmight indicatethat birds had mobilized and Clark 1992).
nutrients from wintering grounds into their
Further evidencethat cormorantsbreeding
eggs. Our comparisonof stable-isotoperatios in the 1990s in eastern Lake Ontario did not
in early Double-crestedCormoranteggs and draw markedly on endogenousreservesaccuthose laid four weeks later indicated a slight mulated on their wintering groundsis providbut significantdecreasein •'•C and a slightin- ed by a contaminant marker. Mirex released
creasein •34Svaluesin yolk only. It is difficult until 1978 at Oswego,New York and the Nito know whether the •3C changesprovide ev- agara River (Kaiser 1978) still is detected conidence for a transfer of marine-derived
nutrisistentlyand at relativelyhigh levelsin wildlife
entsfrom winteringgroundsbecauseeventhe tissuessampledfrom Lake Ontario compared
early eggsshowed8•3C(and 834S)
valuestypical with the other Great Lakes (International Joint
of the local food web (described below). Al- Commission1985,Struger et al. 1993, Ewins et
though isotopicvalues of componentsof cor- al. 1994b). Mirex concentrations in Doublemorant eggs varied among individuals (Table crestedCormoranteggscollectedfrom Pigeon
1), we detected no isotopic overlap between Islandin 1990rangedfrom 0.475to 0.607•g/g
cormorant eggs and those of Caspian Terns (Canadian Wildlife Serviceunpubl. data). In
breeding exclusivelyin the marine biome of the southeasternUnited States in the early
coastalTexas.Enrichment in yolk 8•4Svalues 1970s,mirex was used to controlthe spreadof
for late clutchesactually was oppositeto the fire ants (Committeefor Agricultural Science
trend expectedif marine-derivedreserveshad and Technology1976).Sinceits ban in the Unitbeenusedprimarilyin earlyclutches.
Bulkpro- ed States in 1978 (Environmental Protection
tein sources for carbon and sulfur differ, with
Agency1977),however,mirex levelsin wildlife
July1997]
Isotope
Tracers
ofEggNutrients
tissueshavedroppeddramatically.Reportsof
organochlorines
in avian tissuesin manyparts
Ontario.
wintered
were estimated
473
Such an enrichment
is consistent with
a more benthic- or inshore-baseddiet among
of the southern United States indicate that mithe bird speciesthat we examined(e.g.Ewins
rex is detectedinfrequently(White et al. 1980, et al. 1994b,France 1995, Hecky and Hesslein
1983),is found at relativelylow concentrations 1995).However,Kiriluk et al. (1995)did not excompared with piscivorous species on the tract lipids from their samplesprior to isotope
GreatLakes(King et al. 1987),or generallyfalls analysis.Becauselipids are isotopicallylighter
in •3C than in other tissues, Kiriluk et al's •3C
below the limit of detection,usually0.1 •g/g
wet weight (King and Kynitsky 1986).Within valuesmay be biasedtoward more negative
the last 10 years,few contaminantsstudiesin values compared with ours (Monteiro et al.
theseregionshavereportedsignificantlevelsof 1991,Sholto-Douglas
et al. 1991).
mirex in bird tissues.Therefore,the comparaIn LakeOntario,observeddifferencesamong
tively high levelsof mirex for both early and speciesin •C valuesin eggsmaybe relatedto
late cormorant eggs at Lake Ontario in the differencesin diet andforaginglocationduring
1990sprovide further support that these mi- egg formation.Basedon analysesof regurgigratory birds readily accumulateorganochlo- tatedpellets,Double-crested
Cormorants,Casrineson the breedinggroundsand largelyuse pian Terns,and Herring Gulls foragingin Lake
nutrientsacquiredthere for eggproduction.
Ontario consumea wide variety of prey items.
The possibilitythat somecormorantsmay Double-crestedCormorantsand CaspianTerns
not have wintered exclusivelyin a marine bi- arepiscivores
with dietsdominatedby shallow
omecouldequallybe appliedto CaspianTerns and warmwater fish (Ewins et al. 1994b), but
(R. Pierotti pers. comm.). However, without cormorantsappearto havea more varied diet,
dealingexclusively
with markedindividualsor taking more benthic prey species,such as
using extremelylarge samplesizes,it is im- brown bullhead (Ictalurus nebulosus),white
possible to know whether we have encom- sucker (Catostomuscommersoni),snails, and
passedindividualswinteringin marinebiomes crayfish.Herring Gulls on the Great Lakes are
exclusively.
Further,we were interestedin de- opportunisticpredators,feedingprimarily on
termining if there was positive isotopicevi- fish but also on terrestrial items including
dencefor a marinecontributionto eggslaid at small mammals, refuse, and plant material
freshwaterbreedinggroundsand so obtained (Foxet al 1990,Ewins et al. 1994a).Using the
a minimum estimate for this effect. The absence
diet-tissueisotope fractionationfactors estiof this effectin our data doesnot precludethe matedby Hobson(1995),the •3C dietaryvalpossibility that some individuals may have uesfor CaspianTernsbreedingin coastalTexas
inland.
Stable-isotope
ratiosand diet.--Although we
did not make direct isotopicmeasurements
of
food-webcomponentsin eachof the threeareas
where eggswere obtained,otherisotopicstudies provide data for comparisonwith our resuits.In orderto link isotopicmeasurements
of
egg componentswith the expecteddiet of laying females,it is necessaryto apply diet-tissue
isotopefractionationfactorsfor eachtissueof
interest(HobsonandClark 1992).Applyingthe
appropriate fractionationfactors derived by
Hobson(1995)betweencarnivoredietsandegg
yolk, yolk lipid, andeggshellcarbonates
to the
averageegg componentvaluesreportedabove,
we estimateddietary •3C valuesto be -24.1,
- 22.8,and - 22.5%o,respectively.Thesevalues
are typicallyenrichedby about2%0compared
with thoseobtainedby Kiriluk et al. (1995)for
componentsof the pelagic food web of Lake
to be
-18.5,
-17.8,
and
- 17.0%o
basedoneggyolk,yolklipid, andeggshell carbonates,respectively.These values
were similar to •C values found for fish (œ=
-17.0%o) and benthic filter-feeders (œ =
- 18.2%0) at offshoreareasin the Gulf of Mexico
(seeFry and Sherr1988).Fry et al. (1977)examined
•C
values
in coastal
surface
sedi-
mentsfrom the Upper LagunaMadre region
closeto our CaspianTern colonyand obtained
evidencefor carbonderivedfrom both seagrass
and plankton. The derived •3C valuesfor the
diets of laying CaspianTernsin this area are
entirely consistentwith the enriched•3C values(range- 12.5to - 17.2%o)measuredby Fry
et al. (1977) for this inshorecoastalarea, providing additional evidencethat these birds
may preferentiallybe feedinginshore.
In our study,Herring Gull eggsfrom New-
foundland
andNewBrunswick
originally
were
474
HOBSON,
HUGHES,
ANDEWINS
[Auk,Vol. 114
chosen
to establish
isotopevaluesfor eggsthat thisisotopeactuallyis moreusefulthancarbon
weretypicalof gullsfeedingin a marinebiome. in delineatingsourcesof nutrientsto birds
However,for both carbonand sulfur, gulls movingbetweenterrestrialand marinebiomes.
from thesetwo regionsshowedstable-isotope Previously,this isotopewas more difficult to
valuesfor bothisotopesthatwereintermediate measure compared with carbon, a situation
betweenthoseexpectedfor gulls feedingin that has changedwith the adventof continumarine and terrestrial or freshwater C-3 food
ous-flowisotoperatio massspectrometers.
Conclusions.--Our
study has demonstrated
webs(Dickson1986,Hobson1987,this study).
approachcanbe usedto
As a resultof thelargedeclineof northerncod how a stable-isotope
(Gadusmorhua)stocks off the coast of New- gaininsightinto the originsof nutrientsfrom
birdsareformed.In
foundland(Hutchinsand Myers 1994),and a whicheggsof piscivorous
subsequentmoratoriumimposedon the Ca- addition, we have illustrated how this technadianfishingindustryin 1992,fishoffalthat niquecanbe usedas an aid in the interpreta-
hadbeenreadilyavailable
to breeding
Herring
tion of contaminant
data derived from the anal-
Gulls is no longerabundant(but see Pierotti ysisof bird eggsin freshwaterandmarinesysand Annett 1987). Consequently,Herring temsand, moreimportantly,how one might
Gulls,nowmorethanever,maybe depending usethe isotopetechniqueto evaluateevidence
on refuseas a dietarysourcein Newfoundland for the transfer of nutrients and stored contamThisstudyadds
(J.W.Chardinepers.comm,G.Foxpers.comm; inantsbetweenthesesystems.
to therapidlyexpandsee also Pierotti and Annet 1990). Additional yet anotherapplication
isotopicstudiesdesignedto monitorchanges ing field of using stable-isotopeand contamitogetherin ecosystem-level
studin the dietsof gullsin coastalareaswouldbe nantanalyses
valuable (e.g. Pierotti and Annett 1987).Her- ies (e.g. Spies et al 1989, Broman et al 1992,
ring Gulls also show considerable
individual Rolff et al 1993, Kidd et a11995, Muir et a11995,
variation in prey selectionor specialization Jarmanet al 1996).
(Pierotti and Annette 1990, 1991),and this was
ACKNOWLEDGMENTS
reflectedin the rangeof isotopesignatures
in
eggsof Herring Gulls in Newfoundlandand
analyseswereperformedat thelabNew Brunswick(Table1). Clearly,stable-iso- Stable-isotope
oratoriesof C. van KesselandL. Wassenaar,
Departtope analysisof eggsrepresentsa new and ef- mentof SoilScience,Universityof Saskatchewan
and
fectivemeansof determiningdietary differ- the NationalHydrologyResearch
Institute,respecencesamonglayingfemaleswithinandamong tively.We thankG. Parryand R. Georgefor assispopulations.
tancewith the preparation
of isotopesamples.
We
Stable-sulfur
isotope
ratios.--Theuse of a sec- also thank C. Weseloh,L. Benner, and M. Miller for
with eggcollections
fromLakeOntario;J.
ond element,sulfur, complemented
the use of assistance
N. Garrity
carbonin identifyingsourcesof nutrientsin the Chardinefor thosefromNewfoundland;
components
of eggs.To date,no studieshave for thosefrom New Brunswick;andL. Laack(United
investigated
the relationshipbetweenstable- StatesFish and Wildlife Service)for collectionsof
CaspianTern eggsfrom Texas.T. Custerprovided
sulfurisotopevaluesin dietaryandvariousegg technicaladvice,and M. Moraprovidedadviceon
components.However, •3•Svalues determined contaminants
in thesouthern
UnitedStates.
Funding
for theeggsof birdsbreedingonLakeOntario was providedby EnvironmentCanadaGreat Lakes
were typical of those found in freshwaterbi- programsand the Prairieand NorthernWildlife Reomesin temperateregions,and little fraction- searchCentre(CanadianWildlifeService)in Saska-
ationbetweendiet and eggsis expected(Nriagu 1968, Nriagu and Coker 1976, Fry 1988,
Krouse1988).Similarly,the highly enriched
•3•Svaluesdeterminedfor CaspianTerneggs
from a coastal marine area are consistent with
valuesfoundin othermarinefood webs(Jackson and Gough 1988, Michenerand Schell
1994).Thelargedifference
in •3•Svaluesof sulphates derived from terrestrial and marine
sources(seeNriagu et al. 1991)suggeststhat
toon.Previousdrafts of the manuscriptwere improvedby C. Weseloh,D. Stewart,C. Hebert,R. Kir-
iluk,L. Shutt,andM. Gloutney.
Wearegratefulto R.
Pierotti and E C. Schaffner for constructive reviews
and suggestions.
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