The Auk 116(4):994-1000, 1999
PLASMA
LIPID
METABOLITES
CHANGE
OVER
PROVIDE
SEVERAL
WESTERN
INFORMATION
ON MASS
DAYS IN CAPTIVE
SANDPIPERS
TONY D. WILLIAMS,• CHRISTOPHERG. GUGLIELMO,OLIVER EGELER,AND
CHRISTOPHER
J. MARTYNIUK
Department
of Biological
Sciences,
SimonFraserUniversity,8888 UniversityDrive,Burnaby,
British Columbia V5A 1S6, Canada
ABSTRACT.--Individual
quality is often assessed
usinga staticmeasureof body condition,
suchas size-corrected
body mass.Plasmametabolites
havethe potentialto provideinformationonthedynamicsof physiological
stateandthusmaybebettermeasures
ofindividual
performancecapacity(and fitness).We studiedrelationships
betweenrate of masschange
and circulatinglevelsof triglycerides,glycerol,and ]•-hydroxybutyrate
in captiveWestern
Sandpipers(Calidrismauri).The rate of masschangeoveroneand two daysprior to blood
samplingwas positivelyrelatedto residualtriglyceride(controllingfor body massat sampling) and negativelyrelatedto residualglyceroland residual]•-hydroxybutyrate.
The relationshipbetweenmetabolitelevel and masschangewas still apparentover a seven-day
intervalfor glycerol,but not for the othertwo metabolites.
In a stepwisemultipleregression
of masschangeovertwo days(controllingforbodymass),only]•-hydroxybutyrate
andglycerol were enteredin the model at P < 0.15. Analysisof group meansfor sevensampling
eventsshowedthat body-masschangein a groupof individualswasrelatedto meancirculatinglevelsof eachmetabolite,i.e. to a characteristic
metaboliteprofile.Thus,it maybe
feasibleto employthesemetabolites
to assess
habitatqualitybasedon animalperformance
(e.g.at migratorystopoversites),or to understandthe effectsof climaticor anthropogenic
factorsonthehealthandsurvivalof animals.Received
19May1998,accepted
8 February
1999.
INDIVIDUALQUALITY(variationin body condition or "health") is a widely usedconceptin
behavioraland ecologicalstudies.Body condition perhapsis most simply definedas the
degree to which an organism'sphysiological
state influencesits performance(e.g. production or activity;Brown1996),which,in turn, is
assumedto be positivelyrelatedto fitness(sensu Arnold 1983). Traditionally, measuresof
conditionhavebeenbasedon someaspectof
body composition,such as nutrient reserves.
More recently,studieshaveattemptedto usea
wide range of physiologicalmeasuresof conditionthatarenot directlybasedonnutrientreserves,includingplasmametabolites(Andersson and Gustaffson 1995, Dawson and Borto-
lotti 1997), glucocorticoids(Wingfield et al.
1992),hematocrit(Piersmaet al. 1996),andimmune-systemfunction (Lochmiller et al. 1993,
Ots and H6rak 1996).
In almostall cases,compositional,morphological, or physiologicalindicesof body condition or quality provide only a staticassessE-mail:
tdwillia@sfu.ca
994
mentof the individualat a singlepointin time,
usually the time of capture.This might be a
majorproblemif two individuals(or two sampledpopulations)areundergoingrapidchanges in condition.For example,two individuals
couldhavethe sameconditionindex or body
massat capture,leadingto the conclusion
that
they are of equal quality (and predictedfitness).However,one individual might be on a
trajectoryof rapid massloss,whereasthe mass
of a secondindividual might be constantor increasingover time. In reality, the former individualwouldbe of lowerqualitythanthelatter
individual. Physiologicalindicesof condition
or quality are muchmorevaluableif theyprovide informationon the dynamicsor rate and
directionof changein conditionovertime.
Recently,Jenni-Eiermann
andJenni(1994)reportedthat severalplasmametabolites(in particular, triglyceride and J3-hydroxybutyrate)
couldpredictindividualmasschangeoverseveral hoursin captiveGardenWarblers(Sylvia
borin),whicharesmallmigratorypasserines.
In
this paper,we showthat plasmalipid metabolites (triglycerides,glycerol,and J3-hydroxybutyrate) can provide information on rates of
October1999]
LipidMetabolites
andMassChange
995
TABLE1. Detailsof bodymass(œ-+SE)in experimentalWesternSandpipersat thestartandendof sampling
periods.Masschangein birdsfrom samples5 to 7 wasexperimentally
inducedvia short-termfooddeprivation.
Body
mass
(g)
Sample
Date
No.
No.
Start
End
Rate(g/ day)
days
birds
1
2
3
4
18 January
20 February
3 April
12 July
25.2 _+1.1
33.1 _+1.4
34.2 _+0.9
34.2 _+1.5
25.9 _+1.2
34.0 _+1.6
31.7 _+0.8
29.8 ñ 1.1
0.31 _+0.11
0.13 +_0.08
0.36 _+0.08
-2.16 +_0.32
2
7
7
2
13
17
16
14
5
6
7
3 & 29 November
4 November
30 November
22.6 _+ 0.6
21.1 _+ 0.7
23.0 _+ 0.7
20.1 _+ 0.5
23.7 _+ 0.5
25.1 _+ 0.8
-2.41 _+ 0.27
1.31 _+ 0.24
2.13 _+ 0.20
1
2
1
12
6
6
lite levels).Time fromcaptureto bloodsamplingwas
lessthan 3 min in all cases.Blood(up to 200 •L) was
collectedin heparinizedcapillarytubes,transferred
to 0.6-mLEppendorftubes,and centrifugedat 5,000
rpm (2,200 x g) for 10 min. Plasmawas storedat
-20øC until furtheranalysis.Wepresentpooleddata
fromthe two experimentson plasmametabolitecontats or relative to different climatic conditions
centrationsandbody massat the time of bloodsamor anthropogenicdisturbances.
plingrelativeto therateof masschangebeforesampling at intervalsof one,two, and sevendays.
METHODS
Metabolite
assays.--Plasma
triglyceridesand glycerol weremeasuredwith enzymaticendpointassays
Experimental
protocoL--Juvenile
WesternSandpip- (WakoDiagnostics,
Richmond,andSigma),andplaserswerecapturedin mistnetsduringsouthwardmi- ma [B-hydroxybutyrate
wasmeasuredby enzymahc
grationin August1994and 1995at BoundaryBayin
assay(Sigma).Wefollowedmanufacturers'
protocols
British Columbia, Canada (49ø10'N, 123ø05'W).Anexceptthat the assayswere modifiedfor use with
imal handling protocolsconformedwith Canadian
small volumesof plasma(5 •L) using96-well microCommitteefor Animal Care guidelines,and birds
plates,with assaysbeingread on a Biotek340i miwere captured and maintained under permits from
croplatereader.Sampleswere assayedin triplicate.
Canadian Wildlife Service, Environment Canada,
Becausethe triglycerideassayalso measuredfree
and SimonFraserUniversityAnimal CareCommittee. Birds were maintainedin groupsof 12 to 16 in glycerol,true plasmatriglyceridelevelswere calcuoutdoorpens(3 x 6 m) on naturaldaylengths,with latedby subtractingglycerolfrom total triglyceride.
food (Clark'strout chow)and water providedad li- Assayswere validatedusing referencevaluesfrom
bitum.Infraredheatinglampswereprovidedduring normal and abnormal human control sera (Wako).
winter months,and experimentsbegana minimum Coefficientsof variationbetweenassayswere 6.2%(n
ofthreemonthsaftercapture.Masschangeandplas- = 11), 8.1% (n = 5), and 18.1%(n = 8) for triglycerrespectively.
ma metabolitedata were obtainedfrom two experi- ide, glycerol,and [B-hydroxybutyrate,
Small
volumes
of
plasma
precluded
us
from assaymentalgroupsof sandpipersfor a totalof sevensamin somesamples,sosampling periods(seeTable1): (1) naturalmasschange ing forall threemetabolites
(n = 17birds,4 sampleperiods),in whichbirdswere ple sizesvary.
Statisticalanalysis.--All plasma metabolite data
weighed at either two or sevendays beforeblood
sampling; and (2) experimentallyinduced mass were distributednon-normally(Shapiro-Wilk'stest,
change(n = 12 birds, 3 sampleperiods),in which P < 0.05), so we transformedthe data using
masschangewas inducedby short-termfood dep- In(metabolite + 0.5). Data were analyzed in two
rivation(24h) andre-feeding.Thebirdsin group2 ways. First, at the level of the individual, we comwere differentfrom thosein group1, and we sam- pared rates of masschangewith plasma levelsof
pled their blood after one or two days of mass each of the three metabolites over three time interchange.Birdswerecapturedoneat a timeandsam- vals (one, two, and sevendays) using multiple repled indoorsawayfrom the penssuchthat individ- gressionanalysis(to controlfor the effectof body
uals not being sampled were left undisturbed to massat the time of sampling).To avoid pseudorefeed, bathe,etc. For all birds, blood was sampled plicationwe randomlyselecteda singlerecord for
mass changein captive WesternSandpipers
(Calidrismauri)overtime periodsup to at least
two days(48h). We alsoillustratehow plasma
metaboliteprofiles may be used to determine
mass-changetrajectoriesof different sample
populationsof birds, e.g. from differenthabi-
from the brachial vein between 0930 and 1130 PST
each individual
(to control for possiblediurnal variationin metabo-
of the seventotal samplingperiods.Second,in a
bird for each time interval from one
996
WILLIAMS
ETAL.
[Auk,Vol.116
population
levelanalysis,
wecompared
themean .,_, 4
rateof masschangefor eachsamplingperiodwith
"•
Triglyceride
mean plasmametabolitelevelsfor the sevensam-
plingperiodsusingSpearman
rankcorrelation.
We
considered
thatthissecond
analysis
moreclosely
ap-
proximated
thesituation
thatwouldoccur
in the
fieldwheredatawouldbeobtained
fromseveral
•
0
groupsof individuals(e.g. at differenttimesor in
differenthabitats)
with a variableandunknownpe-
-4
riod of masschangeprior to captureandbloodsampling.Wehad a prioriexpectations
of directionalre-
4
lationships
betweenmetabolites
andmasschange,
so
we used one-tailed
-0.50
-0.'15
0.•0
Glycerol
statistical tests. All values are
ßß ß
given as ϖ SE unlessotherwisestated.
ß
'
RESULTS
Absolutebody mass and the rate of mass
changevariedwidely amongsamplingperiods;data on body massat the start and end of
-0.35
theperiodofmasschange,
rateofmasschange,
andthetimeintervalfor eachsampling
period
4
0.•0
0.35
B-OH-butyrate
aregivenin Table1. Plasma•3-hydroxybutyrate
concentrations
were negativelycorrelatedwith
triglyceride(r = -0.53, n = 50, P < 0.001)and
positivelycorrelatedwith glycerol(r = 0.43,n
= 50, P < 0.002) amongindividual birds. Plasma triglyceride and glycerol concentrations
were not significantlycorrelated(r = 0.11, n =
-4
-2.0
210
66, P > 0.30). Plasmatriglyceridelevelswere
Residual In(metabolite + 0.05)
positivelyrelatedto body massat the time of
blood sampling(F = 65.5, df = 1 and 37, r2 =
FIG. 1. Relationshipbetweenindividual rate of
0.64,P < 0.001),whereasplasma•3-hydroxy- body-mass
changewithin two daysof bloodsambutyratelevelswerenegativelyrelatedto body plingandlevelsof plasmatriglyceride(n = 20),glycmass (F = 5.70, df = 1 and 31, r2 = 0.21, P <
erol(n = 20)and[3-hydroxybutyrate
(n = 19)in cap0.01). Regressionequationsfor theserelation- tive WesternSandpipers.Metabolite concentrations
shipswere:
(mmolper L) areresidualsfromtheregression
with
triglyceride= 0.06(mass)- 1.12
(1)
body mass.
and
•3-hydroxybutyrate
= -0.04(mass)+ 1.96. (2) 0.80).Theequation
fortherelationship
between
mass
change
and
mass-corrected
triglyceride
Plasmaglycerolconcentration
was independent of body massfor our dataset(F = 0.04,df for the two-dayinterval,for whichwe had the
= 1 and 37, P > 0.80). Nonetheless,we con- largestsamplesize,was:
trolledfor body massin subsequent
analyses masschange= 7.61(triglyceride)
- 0.05. (3)
for all threeplasmametabolites(whichdid not
affectany of our resultsor conclusions).
Masschangeovertwo dayswasnegativelyreRates of mass changein individual birds lated to plasmaglycerol(F = 27.98,df = 1 and
were positivelyrelated to plasmatriglyceride 19, r2 = 0.61,P < 0.001;Fig. 1) and •3-hydroxyat thetimeof bloodsamplingfor theone-day butyrate(F = 26.71,df = 1 and 18, r2 = 0.61,P
(F = 3.93,df = 1 and 10, P = 0.04)and thetwo- < 0.001;Fig. 1). The equations
for therelationday(F = 12.09,df = 1 and19,P < 0.01;Fig.1) shipsbetweenmasschangeandmass-correctsamplingintervals,but not for masschange ed metabolite concentrations for these data
over sevendays(F = 0.07, df = 1 and 13, P > were:
October
1999]
LipidMetabolites
andMassChange
mass
change
= -7.77(glycerol)
- 1.34 (4)
and
997
•.. 0.3
+
mass
change
= -1.74([•-hydroxybutyrate)
• •
-o.3o.
(5) [ o.o
Plasma
glycerol
levels
were
also
negatively
re- • '•
lated
tomass
change
over
one
day(F= 9.37,
df •
= 1 and 10, r2 = 0.51,P < 0.025),and this relationshipwasstill apparentoversevendays(F
= 24.71,df = 1 and13,r2 = 0.67,P < 0.001).
Thelevelof [•-hydroxybutyrate
wassimilarly
•
rs= 0.857
-0.3
0.3
•..
relatedto masschangeoveroneday(F = 4.22, .• +
(F = 0.23,df = 1 and12,P > 0.60).
'•
df
=1aand
9,P=0.035)
but
not
over
seven
days
•-- 0.0
In
stepwise
multiple
regression
of mass
•=
change
overtwodays
inwhich
residual
tri- •
glyceride,
glycerol,
and[•-hydroxybutyrate
-•
wereenteredas independent
variables
(con-
r•= -0.786
-0.3
trolling
forbodymass),
only[•-hydroxybuty•.. 1.5
rate (partial r2 = 0.54,P < 0.001)and glycerol
•
(partialr2 = 0.10,P < 0.05)enteredintothe
+
model
atP<
(nmeans
=20).
Analysis
of0.15
group
forthe
seven
sam-•--•
pling
periods
showed
asimilar
overall
pattern• .• 0.0
totheanalysis
attheindividual
level(Fig.2): • •
rate
ofmass
change
was
positively
correlated
•
withtheresidual
level
ofplasma
triglyceride
(r• _•'-1.5
= 0.857,P < 0.025) and negativelycorrelated
with residuallevelsof plasmaglycerol(rs =
-0.786, P < 0.05)and plasma[•-hydroxybuty-
-3
-0.898
-1.5
0.0
1.5
3
Rateofmass
change
(g.d
-1)
rate (rs = -0.898, P < 0.01).
FIG.2. Relationship
betweenaverage
rateofmass
changein captiveWesternSandpipers
andmeanlevDISCUSSION
elsof plasmatriglyceride,
glycerol,and13-hydroxybutyratefor eachsamplingevent(n = 7). Metabolite
(mmolper L) areresidualsfromthe
Jenni-Eiermann
andJenni(1994)showedthat concentrations
with bodymass.Numbersreferto samplasmametabolitescouldprovideinformation regression
on ratesof body-mass
changeovera fewhours plingevents(seeTable1).
in a small migratory passerine.Our results
with WesternSandpipers
extendthistechnique
using plasmameand clearly demonstratethat certain plasma cess,and conditionassessed
metabolitescanbe usedto provideinformation tabolitesshouldthereforebe directlyrelatedto
on ratesof masschangebeforea captureand an organism'sperformance.Plasmatriglycerbloodsamplingeventin individualbirdsover ides increasedwith increasingmass gain,
ina periodof at leasttwo days.Lengthsof stayat whereasglyceroland [•-hydroxybutyrate
stopoversitesduringmigrationaveragethree creasedwith increasingmassloss,consistent
functioning
of these
to four daysin the WesternSandpiper(War- with knownphysiological
nock and Bishop1997),so analysisof plasma metabolites.During fat deposition,triglycermetabolitescan predictmasschangefor bio- idesincreasein theplasmaowingto transport
eitherdilogicallyrelevanttimeintervalsin thisspecies. of lipidsto peripheraladiposetissue,
or indiIn addition,rateof masschange,whichlargely rectlyfrom the gut (asportomicrons)
reflectsrate of fat deposition(Lindstr6m and rectlyvia the liver asverylow-densitylipoproPiersma1993,C. Guglielmounpubl.data),is a teins (Robinson1970,Ramenofsky1990).Durvery important predictor for migratory suc- ing massloss(i.e. when birds are in negative
998
WILLIAMS
ETAL.
energy balance),glyceroland free fatty acids
(FFA) are releasedinto the plasmaduring lipolysisof triglycerides
in adiposetissue,and
hydroxybutyrate(a ketone body) is synthe-
sizedfrom FFA,replacingglucoseasthe principal fuel for respirationin sometissues(Ramenofsky 1990, Horton et al. 1993). Thus,
glyceroland •3-hydroxybutyrate
increasein the
plasmaduringmassloss,whichis indicativeof
lipid catabolismand glucoseshortage(JenniEiermann and Jenni1994).
Althoughwe report an experimentalstudy
using captive birds provided with artificial
food, we seeno reasonwhy the samegeneral
relationship(s)
betweenmasschangeandplasma metabolite
levels should not occur in free-
[Auk, Vol. 116
stantaneous
(i.e.short-term)masschange,
then
we would have predictedmore consistentrelationships between metabolites and mass
changeregardlessof the time interval used
(giventhatmasschangewaslinear).In fact,of
the threemetabolites
measured,only glycerol
wasstill relatedto masschangeoverthelonger
(sevenday)interval.Thissuggests
thatcertain
metabolitesindeed"integrate"informationon
physiologicalstateover severaldays,in addition to reflectingshort-termchangesin mass.
For example, in long-term-fastingpenguins,
concentrationsof plasma •3-hydroxybutyrate
andureaincrease
throughout
stageII offasting
(protein sparing; Cherel et al. 1988b), even
thoughmasslossis constantat thistime (Cher-
livingbirds,because
masschanges
in captivity el et al. 1988a).Thus, in this caseabsolutemeandin the wild shouldinvolvea commonphys- tabolite concentrations reflect both the rate and
iologicalmechanism
andthusgiveriseto sim- the duration of massloss.Somesupportexists
ilar changes
in plasmabiochemistry
(Cherelet for this interpretation
of our datain that glycal. 1988a).However,our data shouldbe extrap- erolwasthe onlymetabolitewe measuredthat
olatedto free-livingbirdswith caution,partic- was not related to body mass at the time of
ularly with regardto masschangeoverthelon- bloodsampling;i.e. plasmaglycerolappeared
ger seven-dayinterval. Plasma levels of all to be lessdependenton the bird'scurrentphysthree metabolitesreflectedmasschangeover iologicalstatethan weretriglycerideand •3-hyoneand two days,but theserelationshipswere droxybutyrate.
lessconsistentover the seven-dayinterval.It is
Anotherpotentialdifferencebetweenour expossiblethat plasmametaboliteprofilessimply perimentalstudyandthat for free-livingbirds
reflectinstantaneous
ratesof masschange,or is that someof our birdsgainedand lostmass
changeoververy shorttime intervals(i.e.one- at relativelyhigh rates (up to 2 g per day).
half to oneday).Assumingthatmasschangeis Zwarts et al. (1990) predicted maximum rates
linear, any relationshipbetween changesin of increase in mass of 4 to 5% of "winter" mass
massoverlongertime intervalswouldthenbe per day,using data on fat depositionfrom 42
due to the effectof the singlemost-recent
day. studiesof shorebirds.This would represent1.1
Our experimentalprotocolmeant that mass g per day for a 22.7-gWesternSandpiperSimchangein our birdswasmoreor lessconstant ilarly, Lindstr/Sm(1991)gavea range of maxiand linear;e.g.masschangeovertwo daysbe- mum fat depositionratesof 2.6 to 4.3% of lean
forebloodsamplingwashighlycorrelatedwith mass,i.e. 0.59 to 0.98 g per day for a 22.7-g
masschangetwo days after sampling(T. D. WesternSandpiper Maximum rates of fat deWilliams unpubl. data). This may not be the positionreportedfor congeneric
Semipalmated
caseundercertaincircumstances
in free-living Sandpipers(C. pusilla)are 1.1 to 1.26g per day
birds (e.g.with markeddiurnalfluctuations
in (Lank 1983,White 1985).However,in our study
mass in small passerines;Meijer et al. 1994, the relationshipbetweenmasschangeoverthe
Witter et al. 1995), althoughseveralstudies seven-dayinterval and plasma glycerol ocsuggestthat rapid massgainduringfat depo- curredover a range of masschangesof +1 g
sition is approximatelylinear and constantin per day,whichis within therangereportedfor
migratoryshorebirds
overseveraldays(Zwarts field studies.Furthermore,for the populationet al. 1990,Lindstr/Sm1991).Thus,the relation- level analysis,the relationshipbetweenrate of
shipbetweenglycerolandmasschangethatwe masschangeand plasmametaboliteswas still
reportfor the seven-dayintervalmay be an ar- apparentwithin the range of _+1.5g per day,
tifact of our particular experimentaldesign. especiallyfor plasmatriglyceride(seeFig. 2).
However,we do not believethat this is entirely
Similaritiesand important differencesexist
the case.If metabolitelevelsreflectedonly in- betweenour studyand that of Jenni-Eiermann
October
1999]
LipidMetabolites
andMassChange
999
andJenni(1994).In thelatterstudy,•-hydroxy- the time of bloodsampling.Usingconventional
butyrate and triglyceridetogetherexplained measuresof condition,birds in sample4 would
asbeingin bet61%of the total variationin body-masschange, likely havebeencharacterized
with partial r2-values
of 51%and 44%,respec- ter conditionthanbirdsin sample1. However,
tively. Jenni-Eiermann
and Jenni(1994:table4) birds in sample4 were on a steeptrajectoryof
did not find a significantrelationship
between masslosscomparedwith birds in sample1,
masschangeand plasmaglycerolin a multiple which were maintainingmore or lessconstant
regressionanalysis.Variation in rate of mass mass.This differencein masschangewasclearchangein captiveWesternSandpipersovertwo ly revealedby the metaboliteprofilesof these
ofbirds,with birdsin sample4 bedayswas significantlyrelatedto plasmalevels twosamples
by high •-hydroxybutyrate
of all threemetabolites,
but glyceroland •-hy- ing characterized
droxybutyratewere betterat explainingvaria- and glycerollevelsand low triglyceridelevels
tion (each61%) than was triglyceride(40%).In comparedwith birdsin sample1 (Fig. 2). The
profilesto comparethe
the multiple regressionanalysis,•-hydroxy- useof suchmetabolite
stateand mass-change
trajectory
butyratewasenteredfirstinto themodel sug- physiological
of birdsmightrepgestingthat it was the singlebestpredictorof of differentsubpopulations
masschangeovertwodays,whichis consistent resentthemostusefulapplicationof thistechand management,
for exwith the finding of Jenni-Eiermann
and Jenni niqueto conservation
thehealthof populations
in
(1994).It is unclearwhetherthe differencebe- amplein assessing
factween our results and thoseof Jenni-Eiermann relationto habitatqualityor anthropogenic
andJenni(1994)with regardto glycerolreflects tors. However, studiesthat examinethe factors
a species-specific
effector suggests
thatdiffer- that influencevariabilityin the levelsof these
ent metabolitesare more or lessuseful in pre- metabolitesin free-living birds (e.g. time of
dicting masschangeover varying time inter- day,tidal cycle,and temperature)are needed.
vals(hoursversusdays;seeabove).NevertheLITERATURE CITED
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