246
ShortCommunications
value of fat reserves and the trade-off
between
starvationand predation.Acta Biotheoretica
38:
37-61.
METCALFE,
N. B. 1984.The effectof mixed-species
flockingon the vigilanceof shorebirds:Who do
theytrust?Animal Behaviour32:986-993.
PIERCE,V., AND T. C. GRUBB,JR. 1981. Laboratory
studies of foraging in deciduouswoodland
birds. Auk 98:307-320.
Popp,J. W. 1988. Scanningbehaviorof finchesin
mixed-species
groups.Condor90:510-512.
PRAVOSUDOV,V. V. 1986. Individual
differences in
foraging and storingbehaviorin SiberianTits
Parus cinctus Bodd. and Willow
Tits Parus mon-
[Auk,Vol. 116
non-breedingseason:A review. Current Ornithology14:189-234.
PULLIAM,n. R., AND T. CARACO.1984. Living in
groups:Is there an optimal group size?Pages
122-147in Behavioural
ecology,an evolutionary
approach(J. R. Krebsand N. B. Davies,Eds.).
Blackwell Scientific Publications, London.
SASVARI,
L. 1992. Great Tits benefit from feeding in
mixed-speciesflocks:A field experiment.Animal Behaviour
43:289-296.
SMITH,S.M. 1991.The Black-capped
Chickadee:
Behavioral ecologyand natural history. Cornell
UniversityPress,Ithaca,New York.
WAITE,T. A. 1987a.Vigilancein the White-breasted
Nuthatch:Effectsof dominanceand sociality.
tanusBald.SovietJournalof Ecology4:60-64.
Auk 104:429-434.
PRAVOSUDOV,
V. V., ANDT. C. GRUBB,
JR.1995.Vigi- WAITE,T. A. 1987b.Dominance-specific
vigilancein
lance in the Tufted Titmousevariesindepenthe Tufted Titmouse: Effect of social context.
dently with air temperatureand conspecific
Condor 89:932-935.
group size. Condor97:1064-1067.
PRAVOSUDOV,
V. V., AND T. C. GRUBB,JR. 1997. En- Received
13 November
1997,accepted
9 June1998.
ergy managementin passerinebirds duringthe AssociateEditor:J. Ekman
TheAuk 116(1):246-252, 1999
MaintenanceEnergy Costsof Two Partially FolivorousTropical Passerines
CARLOSBOSQUE,L3M. ANDREINA PACHECO,• AND RODNEY B. SIEGEL2
•Universidad
Sim6nBolivar,
Departamento
deBiologœa
deOrganismos,
Apartado
89000,
Caracas1080, Venezuela;and
2University
of California,Department
ofAvianSciences,
Davis,California95616,USA
In homeotherms, residual variation of mainte-
suchastheirlow metabolizable
energyowingto the
nance-energycostsaround allometric curvescan be
contentof difficult-to-digestfiber and to the high
content of secondarycompounds(McNab 1978,
relatedto factorsindependentof body mass,suchas
food habits (McNab 1986), taxonomic affiliation
(Bennettand Harvey 1987),season(Kendeighet al.
1977),habitattype (Hubert and Dawson1974),climate (Weathers1979),and body composition
(Daan
et al. 1990).Foodhabitsare importantbecausethe
rate of energyacquisitionmight limit the rate of energy expenditure (McNab 1986, Weiner 1992). For
mammals,McNab(1978,1986)hypothesized
thatthe
processingof food with low metabolizableenergy
content,includingthe leavesof woody plants,requires a low basal metabolicrate (BMR). Hence,arborealmammalsthatmeetlargeportionsof theirenergyrequirementfrom leaveshavelowerBMRsthan
predicted from allometricequations(McNab 1978,
1980a).Someof the reductionof BMR in folivorous
mammalsseemsto be relatedto propertiesof leaves,
1986).
Food habits also influence rates of maintenance
en-
ergy expenditurein birds (McNab 1988),but the re-
lationshipbetweenfolivory and avian BMR is not
fully understood.To a large extent,this is because
little is knownabouttheenergetics
of folivorousspecies. Here, we report on the maintenanceenergy
costsand thermalresponseto ambienttemperature
of two speciesof passerines
that regularlyinclude
leavesand otherplant tissuesin their diets.Passerinesare of interestbecauseof their high mass-specific energyexpenditure,becausetheir smallbody
sizeconstrains
theuseof greentissuesof plants,and
becausefolivory is particularlyscarceamongthem
(Morton 1978, Parra 1978). Characteristics
intrinsic
to leaves should also affect avian consumers;there-
fore, it is of interestto determineif folivory is correlated with reduced BMR in birds, as it is in mamE-mail:
carlosb@usb.ve
mals.
January1999]
ShortCommunications
We studiedtwo speciesof cardinalids,theGrayish
Saltator(Saltatorcoerulescens;
47.0 + SD of 2.6 g; n =
6) andtheOrinocanSaltator(S.orenocensis;
32.7_+2.1
g; n = 4) from the centralfloodplains(llanos)of Venezuela.Both speciesare generalizedarborealherbivores at our study site, feeding mostly on fruits,
leaves,and otherplant tissues.
GrayishSaltatorsfeedalmostexclusively
on plant
tissuethroughouttheyear.Theirdiet is largelymade
up of fruit (35.6%of feedingobservations),
mature
leavesof woodyplants(27.7%),and flowers(16.6%).
Mostof the restof the diet (20%)is madeup of a variety of other plant tissues(leaf buds,flowerbuds,
tendrils,and the skin of seedpods).Insectsaccount
for only 0.1% of feeding observations(Rodriguez
1994). Orinocan Saltatorsalso consumemostly plant
tissue throughoutthe year but are less folivorous
than Grayish Saltators.Nevertheless,during the
rainy seasonmatureleavesaccountfor 19.5%of feeding observations
and leaf buds a further 2.3%. The
restof the diet is madeup of flowersand flowerbuttons (34.5%), fruits (28.7%), and seeds (14.9%). Li-
chensandinsectsare consumedoccasionally
(Garcfa
1994).Bothspecies
havesimpleguts,andgiventheir
small body size and brief mean retentiontime of digesta(59 min for GrayishSaltatorand 80 min for OrinocanSaltator),it is likely that the bulk of their energy requirementsis extracted from cell solubles
rather than from fiber fermentation (Garcia 1994,
Rodriguez1994).Other speciesof saltatorsare also
known to regularly include leaves,buds, and fruits
in their diets (Jenkins1969, Munson and Robinson
1992);however,none that has been studied in more
detail is exclusivelyor obligatorilyfolivorous.
In this work, we comparemaintenanceenergy
costsof both speciesof saltatorwith thoseexpected
from allometricequations.We expected,by analogy
with arboreal folivorous mammals, that BMRs
wouldbe lowerthanpredictedfor passerines
of their
to leavesunder caged conditions(Garcfa 1994, Rod-
rfguez1994).Birdswerefastedfor 4 to 6 h beforethe
experiments.Becauseenoughtime elapsedbetween
thelastfeedingandtheexperimental
measurements
for birds to haveemptiedtheir gutsseveraltimes,we
concluded
thatbirdswereunderpostabsorptive
conditions. Sex of the birds was unknown, and no in-
dividualwasmoltingduringthe experiments.
We measured
oxygenconsumption
(902) of six
GrayishSaltatorsand four OrinocanSaltatorsin relation to ambienttemperature(Ta)during the nonactive phasewith an open-flowApplied Electrochemistrymodel S-3A analyzer as describedin
Weatherset al. (1980).Birds were weighedto the
nearest0.01 g beforebeing placedin a dark, 15.2-L
metabolicchamberthrough which air was drawn
with a flow rate of approximately
0.762L. min • for
GrayishSaltatorsand 0.658 L - min-• for Orinocan
Saltators.The chamberwasplacedin a thermostatically controlledtemperaturecabinetthat allowedus
to regulateambienttemperature.
Thesystemwasallowedto equilibratefor at least1 h beforethebeginning of measurements.
Effluentair wasrun through
tubescontainingsilicagel and sodalime granulesto
removeH20 and CO2beforemeasuringoxygenconcentration.We recordedonly the loweststabilized
readingsof the presumablyinactiveindividuals.At
the endof eachrun, we openedthe metabolicchamber and measuredcloacalbody temperature(Tb)
with a thermocoupleaccurate to 0.1øC and reweighedthe bird. We usedthe averageof the initial
and final body massesof eachbird to calculateits
specificmetabolicrate.Ambienttemperaturein the
chamberwas continuouslymonitoredwith Cu-Cn
thermocouples
connectedto a CampbellScientific
CR21data logger.Not everybird wasrun over the
whole ambienttemperaturerange.Ratesof oxygen
consumptionwere calculated according to Hill
(1972)and expressedunder STPconditions.
Foreachspecies,
therelationship
between
902and
size.
Methods.--We
247
mist netted
saltators
at Fundo
Pe-
Towasexaminedby themethodof YaegerandUltsch
cuarioMasaguaral(Gu•rico State,8ø34'N,67ø35'W), (1989).Thismethodfitstwo straightsegments
to the
a cattle ranch in the seasonal savannahs of Venezuedata and determinesthe point wheretheyintercept.
la, from Juneto August 1995.Vegetationis a mosaic Thispoint canbe considered
the lower criticaltemof open savannaand gallery forest.Rainfall averages peraturewhere the shift from metabolicregulation
1,400 to 1,500 mm annually and is largely concen-
tratedin a singlerainy seasonthat lastsfrom May to
November.Temperaturevariesonly slightlyduring
the year;averagemonthlyminimumand maximum
temperatures are 19.0 and 37.7øC, respectively
(Troth 1979).
During the experimentalperiod,birds were kept
for one to four daysin individual cagesin a room
exposedto naturalphotoperiod.Duringthisperiod,
birds were offered cultivated (papaya and guava)
and wild fruits that are regularly includedin their
natural diet (i.e. Annonajahni and Momordicacharantia).Saltatorsreadily adapt to cagesand maintain
their bodymasson a diet of fruit, whichtheyprefer
of oxygen consumptionto metabolicconformation
occurs.We estimated"wet" thermal conductance
by
calculatinga mean conductancefrom individual
conductances
obtained
byapplying
C = 902 / (T• To)to eachmeasurement
of oxygenconsumption
and
body temperaturebelow thermoneutrality(McNab
1980b).
Weconsidered
BMRastheaverage
of •O2
values within the thermoneutralzone. To compare
measuredoxygenconsumption
rateswith expectations from allometricequations,we used an energy
equivalentof I watt (W) to 0.05mL O2. s-L All birds
were releasedunharmed.at the end of the experiments.
Results
for Grayish
Saltators.--Based
on the method
248
ShortCommunications
41
ture at nightfell within the rangerecordedfor other
passerines(seePrinzingeret al. 1991)ß
Basalmetabolicratewas 1ß489_+0ß04mL O2 ßg-•
4O
ßh • (n = 14),or 0ß3887
W ßind • for a 47.0-gbirdß
Thisvalueis 64ß4%
of thatexpectedfrombodymass
for passerines
during the night periodas predicted
by Aschoffand Pohl (1970) and 63ß6%of that ex-
39
38
•.•
[Auk,Vol. 116
pectedfor passerines
during summernights(calculatedfrom Kendeighet al. 1977)ßBMRmeasuredfor
theGrayishSaltatorfellbelowthe95%confidence
in-
37
o
tervalof the standardregression
of BMR andbody
38
10
2•
3•
4•
massfor birds (Reynoldsand Lee 1996)ß
Thermal conductancewas 0ß116_+ 0ß002mL O2
5O
ßg-• ßh-• ßøC-•,whichis 18.9%higherthanexpected
frombodymassfor passerines
duringtherestphase
(ißeß
0ß098mL O2 ßg • ßh • ßøC •; Aschoff1981)ßEx-
3.5
T
trapolatedbody (= ambient)temperatureat a rate of
metabolismequal to zero (i.eß46.9øC;Fig. lB) was
considerably
higherthan recordedbody temperatures.
o_ 2.0
I-.
•
1.5
O
1.0
Results
for OrinocanSaltators.--The
two linesfitted
byYaeger
andUltsch's
(1989)method,
•'O2= 1.83+
0.06T•and•'O• = 2ß91- 0.04T•,intercepted
at T• =
10.9øC,whichis not biologicallymeaningfulß
Therefore,on thebasisof visualinspectionwe dividedthe
datasetin pointsaboveandbelow25øCandfittedby
leastsquaresa line to eachsubset(Fig.2B).The line
to theleft (•'O• = 3ß925- 0.080T•;n = 11, r = 0ß74,
U,I
>-
0.5
x
0.0
10
20
30
40
P = 0ß009)
andthelineto theright(•'O• = 1.540+
50
0.006T•; n = 9, r = 0ß102,P = 0ß794)intersected at
27.7øC, which we considered to be the lower limit of
AMBIENT TEMPERATURE(øC)
F•c. 1. Body temperature(A) and oxygenconsumption (B) in relation to ambient temperatureof
thermoneutrality.
Averagenightlybodytemperature
of individuals
within
the thermoneutral
zone was
body
six postabsorptiveGrayish Saltatorsduring their 38.8øC_+0ß269(n = 6).As in theformerspecies,
nonactivephase.The two linesin the lowerfigure temperatureof Orinocan Saltatorsvaried signifiwerefittedby themethodofYeagerandUltsch(1989; cantly with ambienttemperature,even within the
thermoneutral zone (Tb = 32ß4+ 0.198T•;n = 20, r =
seetext for equations).Eachsymbolrepresents
one
0ß774,P < 0.001;Fig. 2A). Averagebodytemperature
individual
bird.
at nightalsofell within the rangerecordedfor other
passerines(seePrinzingeret al. 1991)ß
Basalmetabolicrate was 1ß715-+ 0ß064mL O• ßg •
of Yeagerand Ultsch(1989),we fitted two linesto the
ßh • (n = 6), or 0ß3136
W. ind • for a 32.7-gbirdßThis
valueis 67ß9%
of that expectedfrombodymassfor
0.078T•;n = 22, r = 0.790,P < 0.001) and the line to passerines
duringthe night periodas predictedby
theright(•O2 = 1.941- 0.015Ta;
n = 18,r = 0.296, Aschoffand Pohl(1970)and 65ß4%of that expected
P = 0.233)intersected
at 27.1øC.
Thispointmarksthe for passerines
during summernightsas calculated
shiftfrommetabolicconformation
to metabolicreg- from Kendeighet al. (1977)ßBMR of the Orinocan
dataset(Fig.lB). Thelineto theleft(•O 2= 3.657-
ulation
and can be considered
to be the lower limit
Saltator also fell below the 95% confidence interval
of thermoneutrality.
Averagenightlybody temper- of thestandardregression
ofBMRandbodymassfor
ature of individuals
within
the thermoneutral
zone
birds (Reynoldsand Lee 1996).
Thermal
conductance
of Orinocan
Saltators was
was39.4 _+SEof 0.141øC(n = 14).GrayishSaltators
maintaineda high but variablebody temperature
(Fig. 1A). Althoughbirds clearlycouldthermoregulate,theirbodytemperature
wasnotcontrolled
precisely,and it varied significantlywith ambienttem-
0ß143_+0ß004mL O• ßg • ßh • ßøC •, whichis 23ß9%
higherthanexpectedfrombodymassfor passerines
during the rest phase(ißeß
0ß115mL O• ßg-• ßh •
ßøC-•;Aschoff1981)ßAs for GrayishSaltators,ex-
perature (T b = 36.4 + 0.091T•; n = 40, r = 0.617, P
< 0.001). Not even within the thermoneutralzone
trapolatedbody (= ambient)temperatureat a rate of
metabolismequal to zero (ißeß49.1øC;Fig. 2B) was
was there a clear indication
considerably
higherthan recordedbody tempera-
that birds maintained
a
constantbody temperature.Averagebody tempera-
tures.
January1999]
ShortCommunications
41
real species,particularlythosethat rely extensively
40
on fiber fermentation (McNab 1978). Microtine ro-
dentsof smallbodymassthat feedheavilyon leaves
of woodyplants,and that probablydigestcell solublesonly,havehigh basalrates(McNab1986).Furthermore,in mammalsit appearsthat BMR is reducedonly in specieswhosedietsconsistof at least
39
38
37
38
20 to 30% leaves(McNab 1978:figure 6). In contrast,
BMRsare considerablyreducedin small birds (e.g.
35
•m
0
34
33
•
249
I .........
10
, .......
20
30
40
50
10
20
30
40
50
3.5
0 2.0
I'-
Q.
'--'
1.5
t.•
1.0
•-
0.5
0.0
AMBIENT TEMPERATURE(øC)
FIG. 2. Body temperature(A) and oxygenconsumption(B) in relationto ambienttemperatureof
four postabsorptive
OrinocanSaltatorsduringtheir
nonactivephase.The two lines of the lower figure
werefittedby dividingthedatasetintopointsbelow
and above25øC(seetext for equations).
Eachsymbol
representsoneindividual bird.
saltatorsand mousebirds)
that are incapableof fiber
fermentation
andthatincorporate
leavesin theirdiet
to a moderateextentonly.
The interactionbetweenfood quality and digestive physiologymight influencemetabolicratesof
homeotherms
becausedigestiveand absorptiveprocessesmight limit ratesof energyacquisition,thus
settingan upperceilingto the energybudgetof organisms(e.g. Weiner 1992, Velosoand Bozinovic
1993). In particular, McNab (1978, 1986) proposed
that theuseof a poorfoodsourceby mammalianarborealfolivoresmight requirethem to have a low
basalrate of metabolism.He posedthreenonexclusive explanationsto interpret the correlationbetweenfolivoryand reducedBMRin mammals.First,
leavesmight have a low metabolizable
energycontent becausethey are rich in fiber,whichis difficult
to digest.Limitationson the maximumbulk of energy-dilutefood that canbe processed
daily by the
digestivetractmightlimit energyintakein folivores.
Second, the low basal rates of folivorous mammals
may be an adaptationto reducethe intakeof toxic
secondary
compounds
presentin thegreentissuesof
plants. Reduced intake of secondarycompounds
may reducedose-relatednegativeeffectsand the
costs of detoxification. Third, arboreal mammalian
folivores,particularlylargerspecies,are rathersedentaryandhavea lowproportionof musclemassrelative to body mass.In mammals,low basal ratesof
metabolism
are
correlated
with
reduced
muscle
mass.
Discussion.--Inaccordancewith expectations, Explanationsproposedby McNab in relation to
both speciesof saltatorhad substantiallylower mammalsmightalsoapplyto folivorousbirds.First,
with thedigestionof fiber(and
BMRsthan predictedfrom their body size.Thisre- difficultiesassociated
ductionof restingmetabolismshouldcontributeto
an economyof daily energyexpenditure.Other ar-
of soluble cell contents contained
within
fibrous cell
walls) determinethat metabolizableenergy of foborealfolivores
alsohavelowBMRs.Speckled
Mouse- liagerankslowestamongbird foods(Karasov1990).
birds (Coliusstriatus;50 to 55 g) and Blue-naped Likewise,limitationsof tract volumeand processing
Mousebirds(Urocoliusmacrourus;
51.3 g), two par- rate of energy-dilutefoliage are known to limit intially folivorousspeciesof tropical and temperate take rates in folivorousbirds (Kenward and Sibly
Africa, feed on leaves, buds, and fruit and have
1977). Second,folivorous birds are known to limit in-
BMRsthat are 75 and 63%,respectively,
of expected
(BartholomewandTrost1970,Prinzinger1988).Furthermore,mousebirds
areableto entertorpor,animportant energy-savingmechanism(Bartholomew
and Trost1970,Prinzingeret al. 1981).Likewise,the
take in order to reduceingestionof toxic plant secondarymetabolites(Jakubaset al. 1993),and detoxificationcostsmightbe a substantialportionof their
energyand nutrientbudget(Guglielmoet al. 1996).
Third, in birds small muscle mass in associationwith
sedentaryhabitsmightalsobe correlatedwith a low
isthocomus
hoazin;
598g) of theNeotropics
hasa BMR basal rate of metabolism (McNab 1988, 1994). Few
that is 69.8%of expected(Grajal1991).In mammals, data exist on time budgetsof arboreal folivorous
reductionof BMR is highestin medium-sizedarbo- birds,but it is of interestthat the obligatorilyfoli-
obligate folivorous, fiber-fermentingHoatzin (Op-
250
ShortCommunications
vorous Hoatzin has a thickened callus of skin on the
[Auk,Vol. 116
reduced metabolicrates. At this point, we cannot
tip of the sternumthat helpsit to maintaina sitting discern the effects of diet and latitude on our results.
posturefor 70 to 80%of the day (Strahl1988).In our However,the fact that saltatorsspend77 to 80% of
study site,nonbreedingindividualsof both species their time sitting, singing,and preeningsuggests
of saltatorremain motionlessfor major portions of that, under sucha relaxedtime budget,it is unlikely
their time budget.GrayishSaltatorsand Orinocan that theywouldbe forcedto forageor to spendconSaltatorspendabout50 and 42% of daylighthours, siderableportionsof timeexposedto unfavorablerarespectively,sitting and a further 30 and 35% en- diative environments. The fact that BMR is reduced
gagedin low-coststaticactivitiessuchas preening in otherarborealfolivores,includingtemperatespeand singing(Garcfa1994,Rodriguez1994).
cies,suggests
that diet is important.
A considerableportion of the diet of saltatorsis
Amongfolivorousbirds, it appearsthat only the
madeup of fruitsandotherplanttissues.Dataonthe morearborealspecieshavereducedmetabolicrates.
energetics
of frugivoresis scant,but it appearsthat The ground-dwellingfolivorousgrouseand ptarfrugivoryin birds is alsoassociated
with low BMR migan (Tetraoninae)of temperate latitudes have
(McNab 1988).However,this is not well established metabolicrates that are similar to or higher than
becausethreespeciesof highlyfrugivorousNeotrop- those expectedfrom considerationsof body mass
ical manakins(Pipridae)haveBMRsthat correspond alone (see Weathers1979, McNab 1988). Likewise,
to theirbodysize(VleckandVleck1979).Neverthe- flightless,forb-eatingratitesand largelyterrestrial,
less,severalof the conditionsthat apply to folivory grass-feedinganseriforms do not have reduced
mightalsoapplyto frugivory.Fruit hasa highwater BMRs(seeMcNab 1988).To someextent,thispattern
content and a considerableportion of indigestible is similarto that foundin mammalsin which only
seeds;hence,metabolizable
energyof wholefruits the moresedentaryarborealspecieshavelow basal
per unit of freshmassis quitelow (Karasov1990), rates.In contrast,theconsumptionof grassandforbs
and processing
by the digestivetractmightlimit in- by terrestrialherbivorousmammalsis associated
takein highlyfrugivorousspecies
(LeveyandGrajal with highbasalrates(McNab1978,1986).Furtherre1991).Similarly,secondary
metabolitesof fruit pulp search is needed to unravel the effects of latitude, focan limit intake in frugivores(Izhaki and Safriel livory, and arborealhabitson the metabolicratesof
1989,CipolliniandStiles1993).Perhapsthelowbas- birds.
al ratesin saltatorsare associatedwith folivory in
Acknowledgments.--We
are grateful to Sr. Tom•s
combination
with frugivory.
Blohmfor permissionto work at Hato Masaguaral
Neitherspecies
of saltatorfully balancedheatloss- and for his unrestrictedsupport of our activities.
es through an increasein metabolismas ambient Kako provided logisticalsupport in many ways.
temperature decreased(their body temperatures MAP was partially supported by ECONATURA
droppedin a seeminglycontrolledmanner).The de- while at HatoMasaguaral.Travelexpenses
of RBSto
creasein Tbbetween 34 and 13øCTathat we estimat- Venezuela
werecoveredby a Jastro-Shields
Graduate
ed from the regressionequationswas 1.9øCin the ResearchFellowshipfrom the Universityof CaliforGrayishSaltator(from 39.5 to 37.6øC)and 4.1øCin nia. WesWeatherskindly allowedthe useof the oxthe OrinocanSaltator(from 39.1to 35.0øC).This con- ygen analyzer.Researchon saltatorsat Hato Masatrolled decreasein Tb, although moderate,should guaral was initiated by M. A. Garciaand A. Rodricontributeto an economyof energyexpenditureand guez.Suggestions
by reviewersgreatlyimprovedthe
also couldbe consideredan adaptationto saveen- manuscript.All birds were captured and handled
ergy.A moderatedecrease
in Tbwith fallingTa,con- underpermissionsfrom PROFAUNA(Ministeriodel
trolledhypothermia,is knownfor approximately
40 Ambiente y RecursosNaturales Renovables)issued
other speciesof birds, includingmousebirds(Prin- to M. A. Garcia and A. Rodriguez.
zinger et al. 1991).Failureto increaseheat productionenoughto balanceheatlossalsohastheeffectof
LITERATURE CITED
loweringthe slopeof the line to the left of the lower
criticaltemperature(Figs.lB and2B),whichcoupled ASCHOFF,J. 1981. Thermal conductance in mammals
with a combination
of physicaland chemicaltherand birds: Its dependenceon body size and cirmoregulation(McNab 1980b),shouldaccountfor the
cadian phase.ComparativeBiochemistryand
highextrapolated
bodytemperatures
atanestimated
Physiology69A:611-619.
ASCHOFF,J., AND H. POHL. 1970. Der Ruheumsatz
rate of metabolismequalto zerofor both species.
Tropical birds seem to have reduced BMRs for
von V6gelen als Funktion der Tageszeitund der
their body size,particularlyspeciesthat regularly
K6pergr6sse.Journalftir Ornithologie111:3847.
foragein the sun(Weathers1979,1997).Latitude,or
factorsassociatedwith it (e.g.lower massof meta- BARTHOLOMEW, G. g., AND C. H. TROST. 1970. Tembolicallyactivetissue;Renschand Rensch1956 in
peratureregulationin the SpeckledMousebird,
Colius striatus. Condor 72:141-146.
Daan et al. 1990),might be a confoundingfactorin
the interpretationof our findingthat saltatorshave BENNETT,P. g., AND P. H. HARVEY. 1987. Active and
January1999]
ShortCommunications
restingmetabolismin birds:Allometry,phylogeny and ecology.Journalof Zoology (London)
213:327-363.
CIPOLLINI, M. L., AND E. W. STILES. 1993. Fruit rot,
antifungal defense,and palatability of fleshy
fruits for frugivorousbirds. Ecology74:751-762.
DIAN,
S., D. MASMAN, AND A. GROENEWOLD. 1990.
251
dar Waxwings. American Naturalist 138:171189.
MCNAB,B. K. 1978.Energeticsof arborealfolivores:
Physiologicalproblemsand ecologicalconsequencesof feeding on an ubiquitousfood supply. Pages153-162in The ecologyof arborealfo-
livores(G. G. Montgomery,Ed.). Smithsonian
Institution Press,Washington,D.C.
with body compositionand energyexpenditure MCNAB,B K. 1980a.Foodhabits,energeticsand the
populationbiology of mammals.AmericanNatin nature.AmericanJournalof Physiology259:
Avian
basal
metabolic
rates: Their
association
uralist
R333-R340.
116:106-124.
GARCIA,M. A. 1994.La dietay la eficienciadigestiva MCNAB,B. K. 1980b.On estimatingthermalconductancein endotherms.Physiological
Zoology53:
del LechoseroPechiblanco(Saltatororenocensis).
Thesis, Universidad
Sim6n Bolivar, Caracas,
144-156.
MCNAB, B. K. 1986. The influence of food habits on
Venezuela.
theenergeticsof eutherianmammals.Ecological
GRAJAL,
A. 1991.The nutritionalecologyand digesMonographs56:1-19.
tive physiologyof the Hoatzin (Opisthocomus
hoazin),a folivorousbird with foregut fermen- MCNAB, B. K. 1988. Food habits and basal rate of metabolism in birds. Oecologia77:343-349.
tation.Ph.D.dissertation,Universityof Florida,
MCNAB,B. K. 1994. Energy conservationand the
Gainesville.
evolution of flightlessnessin birds. American
GUGLIELMO,C. G., W. H. KARASOV,AND W. J. JAKUNaturalist
144:628-642.
BAS.1996.Nutritional costsof a plant secondary
MORTON,
E.
S.
1978.Avian arborealfolivores:Why
metaboliteexplain selectiveforagingby Ruffed
not?
Pages
123-130 in The ecologyof arboreal
Grouse.Ecology77:1103-1115.
folivores(G. G. Montgomery,
Ed.). Smithsonian
HILL, R. W. 1972.Determinationof oxygenconsumpInstitution
Press,
Washington,
D.C.
tion by use of paramagneticoxygenanalyzer.
MUNSON, E. S., AND W. D. ROBINSON.1992. Extensive
Journalof Applied Physiology33:261-263.
folivory by Thick-billedSaltators(SaltatormaxHULBERT,A. J., AND t. J. DAWSON.1974. Standard
ilIosus)in southernBrazil. Auk 109:917-919.
metabolismand body temperatureof peramePARRA,R. 1978.Comparisonof foregut and hindgut
loid marsupialsfrom different environments.
fermentationin herbivores.Pages153-162 in
ComparativeBiochemistryand Physiology47A:
The ecologyof arborealfolivores(G. G. Mont583-590.
gomery, Ed.). SmithsonianInstitution Press,
IZHAKI,I., ANDU. N. SAFRIEL.
1989.Why are thereso
Washington,D.C.
few exclusivelyfrugivorousbirds?Experiments
PRINZINGER,
R. 1988.Energymetabolism,body-temof fruit digestibility.Oikos54:23-32.
peratureandbreathingparameters
in nontorpid
JAKUBAS,W. J., W. H. KARASOV,AND C. G. GUGLIELMO. 1993. Ruffed
Grouse tolerance
and biotrans-
Blue-naped Mousebirds Urocolius macrourus.
Journalof ComparativePhysiology157B:801-
formation of the plant secondarymetabolite
806.
coniferylbenzoate.Condor95:625-640.
PRINZINGER,R., R. GOPPEL,A. LORENZ, AND E. KULJENKINS,
R. 1969.Ecologyof threespeciesof saltators
ZER.1981.Bodytemperatureand metabolismin
in CostaRicawith specialreferenceto their fruthe Red-backed Mousebird (Colius castanotus)
givorousdiet. Ph.D. dissertation,Harvard Uniduring fasting and torpor. Comparative Bioversity,Cambridge,Massachusetts.
chemistryand Physiology69A:689-692.
KARASOV,
W. H. 1990. Digestion in birds: Chemical PRINZINGER,R., A. PREllMAR,AND E. SCHLEUCHER.
and physiologicaldeterminantsand ecological
1991. Body temperaturein birds. Comparative
implications.Studiesin Avian Biology13:391Biochemistryand Physiology99A:499-506.
458.
KENDEIGH, S.C., V. R. DOL'NIK, AND V. M. GAVRILOV.
1977.Avian energetics.Pages127-204 in Graniv-
RENSCH,I., AND B. RENSCH.1956. Relative organ-
massebeitropischen
warmbluetern.Zoologischer Anzeiger 156:106-124.
orousbirdsin ecosystems
(J.PinowskyandS.C. REYNOLDS,
P.S., ANDR. M. LEEIII. 1996.PhylogeKendeigh,Eds.). CambridgeUniversity Press,
neticanalysisof avianenergetics:
Passerines
and
Cambridge,United Kingdom.
nonpasserines
do not differ.AmericanNaturalKENWARD, R. E., AND R. M. SIBLY. 1977. A Wood Pi-
geon (Columbapalumbus)feeding preferenceexplained by a digestivebottle-neck.Journalof
Applied Ecology14:815-826.
LEVEY,D. J., ANDA. GRAJAL.
1991.Evolutionaryimplicationsof fruit-processinglimitationsin Ce-
ist 147:735-759.
RODRIGUEZ,
A. 1994. Dieta y comportamientoalimentario del LechoseroAjicero (SaltatorcoeruIescens).
Thesis, Universidad Sim6n Bolivar. Caracas, Venezuela.
STRAHL,S, D. 1988.The socialorganizationand be-
252
ShortCommunications
haviour of the Hoatzin (Opisthocomus
hoazin)in
central Venezuela.
Ibis 130:483-502.
TROTH,R. G. 1979.Vegetationaltypeson a ranchin
[Auk, Vol. 116
WEATHERS,W. W., C. J. SHAFIRO,AND L. B. ASTHEI-
MER. 1980. Metabolic responses of Cassin's
Finches (Carpodacuscassini) to temperature.
ComparativeBiochemistryand Physiology65A:
the central llanos of Venezuela.Pages17-30 in
Vertebrateecologyin the northernNeotropicis
235-238.
(J. E Eisenberg,Ed.). SmithsonianInstitution WEINER,J. 1992. Physiologicallimits to sustainable
Press,Washington,D.C.
energybudgetsin birds and mammals:EcologVELOSO,C., ANDE BOZINOvlC.1993. Dietary and diical implications.Trendsin Ecologyand Evolugestiveconstraintson basalenergy metabolism
in a small herbivorousrodent. Ecology74:20032010.
VLECK, C. E.M., AND D. VLECK. 1979. Metabolic rate
in five tropicalbird species.Condor81:89-91.
WEATHERS,
W. W. 1979. Climatic adaptation in avian
standardmetabolicrate. Oecologia42:81-89.
tion 7:384-388.
YEAGER,
D., ANDG. R. ULTSCH.1989.Physiological
regulationand conformation:A BASICprogram
for the determinationof criticalpoints.Physiological Zoology 62:888-907.
WEATHERS,
W. W. 1997.Energeticsand thermoregulationby smallpasserines
of the humid,lowland Received11 November1997, Accepted22 April 1998.
tropics.Auk 114:341-353.
Associate
Editor:M.E. Murphy
TheAuk 116(1):252-256,1999
Low ExtrapairPaternityin the CactusFinch (Geospizascandens)
KENNETH PETREN,• g. ROSEMARYGRANT, AND PETERg. GRANT
Department
of Ecology
andEvolutionary
Biology,
PrincetonUniversity,
Princeton,
NewJersey
08544,USA
Severalinvestigationsof Darwin's fincheshaverelied upon observationsof adults at the nestfor identifying parents.Theseincludeestimationsof heritable variation and covariation (Grant and Grant 1989,
en by brachialvein puncturefrom nestlingsat day 8
and from adults capturedin mist nets. Nearly all
males on the island throughoutthe study period
were sampled. The largest number of potential
1994), lifetime reproductive successand genetically
effective population sizes (Grant and Grant 1992),
and the evolutionaryresponseto selection(Grant
and Grant 1995). Studies of other emberizids and
breeders was present in 1993 (68 males and 27 females), when 90% of the males and 93% of the femaleswere sampled.
Prior to puncture with a 30.5-gaugehypodermic
cardinalids(relatedsparrows,finches,andbuntings) needle,the areawas cleanedwith alcohol,and a drop
in the temperatezone have shownthat simply ob- of 0.5M EDTA was placed over the vein. Blood was
servingadults at the nest is not sufficientto be sure transferred to EDTA-soakedfilter paper, air dried,
of correctlyidentifying biologicalparents(Westneat and storedin drierite at ambient(field) temperatures
and Webster1994).Extrapair copulationssometimes beforebeingtransferredto the laboratoryand stored
result in fertilizationsand the rearing of nonpaternal at - 80øC.
offspring.To determinewhetherthis occursin Darwin'sfinches,we undertooka studyof microsatellite
DNA variation in a socially monogamous,multibrooded species,the CactusFinch (Geospiza
scandens),on the GalapaRosisland of Daphne Major
(0ø15'S,90ø13'W).The frequencyof polygyny has
neverexceeded5% in this population(seeBoarand
Grant 1984, Gibbs and Grant 1987, Grant and Grant
Eight microsatelliteloci developedin the Medium
Ground-Finch(Geospizafortis)
wereusedto testparentagein G,scandens.
Laboratorytechniques
usedfor
genomiclibrary screeningand geneticscreeningof
individual birds generally followed those of Prim-
mer et al. (1995).Detailedmethodsand primer sequencesare availableelsewhere(Petren1998).Measuresof variation at theseeight loci and exclusion
1996 for breeding characteristicsand population probabilities are given in Table 1. We found no evidata).
denceof "null" alleles(Callen et al. 1993)in the pedMethods.--Bloodsamples were taken from 248
igree.
birds in 1988to 1996.A singledrop of bloodwastakResultsanddiscussion.--All159 offspringhad one
allelein commonwith thematernalparent(with the
E-mail: petren@princeton.edu
exceptionof the Z-linked locus).Therefore,mater-