246 ShortCommunications [Auk,Vol. 116

value of fat reserves and the trade-off between non-breedingseason: A review. Current Orni- starvationand predation.Acta Biotheoretica38: thology14:189-234. 37-61. PULLIAM,n. R., AND T. CARACO.1984. Living in METCALFE,N. B. 1984.The effectof mixed- groups:Is there an optimal group size?Pages flockingon the vigilanceof shorebirds:Who do 122-147in Behaviouralecology, an evolutionary they trust? Behaviour32:986-993. approach(J. R. Krebs and N. B. Davies, Eds.). PIERCE,V., AND T. C. GRUBB,JR. 1981. Laboratory Blackwell Scientific Publications, London. studies of foraging in deciduous woodland SASVARI,L. 1992. Great Tits benefit from feeding in . Auk 98:307-320. mixed-speciesflocks: A field experiment.Ani- mal Behaviour 43:289-296. Popp,J. W. 1988. Scanningbehavior of finchesin SMITH,S. M. 1991.The Black-cappedChickadee: Be- mixed-speciesgroups. Condor 90:510-512. havioral ecologyand natural history. Cornell PRAVOSUDOV,V. V. 1986. Individual differences in UniversityPress, Ithaca, New York. foraging and storingbehavior in SiberianTits WAITE,T. A. 1987a.Vigilance in the White-breasted Parus cinctus Bodd. and Willow Tits Parus mon- Nuthatch:Effects of dominanceand sociality. tanusBald. Soviet Journal of Ecology4:60-64. Auk 104:429-434. PRAVOSUDOV,V. V., AND T. C. GRUBB,JR. 1995. Vigi- WAITE,T. A. 1987b.Dominance-specific vigilance in lance in the Tufted Titmousevaries indepen- the Tufted Titmouse: Effect of social context. dently with air temperatureand conspecific Condor 89:932-935. group size. Condor 97:1064-1067. PRAVOSUDOV,V. V., AND T. C. GRUBB,JR. 1997. En- Received13 November1997, accepted 9 June 1998. ergy managementin passerinebirds during the AssociateEditor: J. Ekman

TheAuk 116(1):246-252, 1999

MaintenanceEnergy Costsof Two Partially FolivorousTropical

CARLOSBOSQUE, L3 M. ANDREINA PACHECO,• AND RODNEY B. SIEGEL2 •UniversidadSim6n Bolivar, Departamento deBiologœa deOrganismos, Apartado 89000, Caracas1080, Venezuela;and 2Universityof California,Department of AvianSciences, Davis, California 95616, USA

In homeotherms, residual variation of mainte- suchas their low metabolizableenergy owing to the nance-energycosts around allometric curves can be content of difficult-to-digestfiber and to the high relatedto factorsindependent of body mass,such as content of secondary compounds(McNab 1978, food habits (McNab 1986), taxonomic affiliation 1986). (Bennettand Harvey 1987),season (Kendeigh et al. Food habits also influence rates of maintenance en- 1977),habitat type (Hubert and Dawson1974), cli- ergy expenditurein birds (McNab 1988),but the re- mate (Weathers1979), and body composition(Daan lationshipbetween folivory and avian BMR is not et al. 1990).Food habits are important becausethe fully understood.To a large extent,this is because rate of energyacquisition might limit the rate of en- little is knownabout the energetics of folivorousspe- ergy expenditure (McNab 1986, Weiner 1992). For cies. Here, we report on the maintenanceenergy mammals,McNab (1978,1986)hypothesized that the costsand thermalresponse to ambienttemperature processingof food with low metabolizableenergy of two speciesof passerinesthat regularlyinclude content,including the leavesof woody ,re- leavesand other tissuesin their diets.Passer- quires a low basal metabolicrate (BMR). Hence,ar- ines are of interestbecause of their high mass-spe- borealmammals that meet large portions of theiren- cific energyexpenditure, because their small body ergyrequirement from leaveshave lower BMRs than sizeconstrains the use of greentissues of plants,and predicted from allometricequations (McNab 1978, becausefolivory is particularly scarceamong them 1980a). Someof the reduction of BMR in folivorous (Morton 1978, Parra 1978). Characteristicsintrinsic mammalsseems to be relatedto propertiesof leaves, to leaves should also affect avian consumers;there- fore, it is of interestto determineif folivory is cor- related with reduced BMR in birds, as it is in mam- E-mail: [email protected] mals. January1999] ShortCommunications 247

We studiedtwo speciesof cardinalids,the Grayish to leavesunder caged conditions(Garcfa 1994, Rod- Saltator(Saltator coerulescens; 47.0 + SD of 2.6 g; n = rfguez1994). Birds were fasted for 4 to 6 h beforethe 6) and theOrinocan Saltator (S. orenocensis; 32.7 _+2.1 experiments.Because enough time elapsedbetween g; n = 4) from the centralfloodplains (llanos) of Ven- the lastfeeding and the experimentalmeasurements ezuela.Both speciesare generalizedarboreal herbi- for birds to haveemptied their guts severaltimes, we vores at our study site, feeding mostly on fruits, concludedthat birds were under postabsorptive con- leaves,and otherplant tissues. ditions. Sex of the birds was unknown, and no in- GrayishSaltators feed almostexclusively on plant dividual was moltingduring the experiments. tissuethroughout the year.Their diet is largelymade We measuredoxygen consumption (902) of six up of fruit (35.6%of feedingobservations), mature GrayishSaltators and four OrinocanSaltators in re- leavesof woodyplants (27.7%), and flowers(16.6%). lation to ambienttemperature (Ta) during the non- Mostof the restof the diet (20%)is madeup of a va- active phase with an open-flowApplied Electro- riety of other plant tissues(leaf buds, flower buds, chemistrymodel S-3A analyzer as describedin tendrils,and the skin of seedpods). account Weatherset al. (1980).Birds were weighedto the for only 0.1% of feeding observations(Rodriguez nearest0.01 g beforebeing placedin a dark, 15.2-L 1994). Orinocan Saltatorsalso consumemostly plant metabolicchamber through which air was drawn tissue throughoutthe year but are less folivorous with a flow rate of approximately0.762 L. min • for than Grayish Saltators.Nevertheless, during the GrayishSaltators and 0.658 L - min-• for Orinocan rainy seasonmature leaves account for 19.5%of feed- Saltators.The chamberwas placedin a thermostati- ing observationsand leaf buds a further 2.3%. The cally controlledtemperature cabinet that allowedus restof the diet is madeup of flowersand flowerbut- to regulateambient temperature. The systemwas al- tons (34.5%), fruits (28.7%), and seeds (14.9%). Li- lowedto equilibratefor at least1 h beforethe begin- chensand insectsare consumedoccasionally (Garcfa ning of measurements.Effluent air wasrun through 1994).Both species have simple guts, and given their tubescontaining silica gel and sodalime granulesto small body size and brief mean retentiontime of di- removeH20 and CO2before measuring oxygen con- gesta(59 min for GrayishSaltator and 80 min for Or- centration.We recordedonly the loweststabilized inocanSaltator), it is likely that the bulk of their en- readingsof the presumablyinactive individuals. At ergy requirementsis extracted from cell solubles the end of eachrun, we openedthe metaboliccham- rather than from fiber fermentation (Garcia 1994, ber and measured cloacalbody temperature(Tb) Rodriguez1994). Other speciesof saltatorsare also with a thermocoupleaccurate to 0.1øC and re- known to regularly include leaves,buds, and fruits weighedthe . We usedthe averageof the initial in their diets (Jenkins1969, Munson and Robinson and final body massesof eachbird to calculateits 1992);however, none that has been studied in more specificmetabolic rate. Ambient temperature in the detail is exclusivelyor obligatorilyfolivorous. chamberwas continuouslymonitored with Cu-Cn In this work, we comparemaintenance energy thermocouplesconnected to a CampbellScientific costsof both speciesof saltatorwith thoseexpected CR21 data logger.Not everybird was run over the from allometricequations. We expected,by analogy whole ambienttemperature range. Rates of oxygen with arboreal folivorous mammals, that BMRs consumption were calculated according to Hill wouldbe lowerthan predictedfor passerinesof their (1972)and expressedunder STP conditions. size. Foreach species, the relationship between 902 and Methods.--We mist netted saltators at Fundo Pe- Towas examined by the methodof Yaegerand Ultsch cuarioMasaguaral (Gu•rico State,8ø34'N, 67ø35'W), (1989).This method fits two straightsegments to the a cattle ranch in the seasonal savannahs of Venezue- data and determinesthe point wherethey intercept. la, from Juneto August 1995.Vegetation is a mosaic This point canbe consideredthe lower criticaltem- of open savannaand gallery forest.Rainfall averages peraturewhere the shift from metabolicregulation 1,400 to 1,500 mm annually and is largely concen- of oxygen consumptionto metabolicconformation trated in a singlerainy seasonthat lastsfrom May to occurs.We estimated"wet" thermal conductanceby November.Temperature varies only slightlyduring calculatinga mean conductancefrom individual the year;average monthly minimum and maximum conductancesobtained by applying C = 902 / (T• - temperatures are 19.0 and 37.7øC, respectively To)to eachmeasurement of oxygenconsumption and (Troth 1979). body temperaturebelow thermoneutrality(McNab During the experimentalperiod, birds were kept 1980b).We considered BMR as the averageof •O2 for one to four days in individual cagesin a room values within the thermoneutralzone. To compare exposedto naturalphotoperiod. During thisperiod, measuredoxygen consumption rates with expecta- birds were offered cultivated (papaya and guava) tions from allometricequations, we used an energy and wild fruits that are regularly includedin their equivalentof I watt (W) to 0.05mL O2 . s-L All birds natural diet (i.e. Annonajahni and Momordicachar- were releasedunharmed .at the end of the experi- antia).Saltators readily adapt to cagesand maintain ments. their body masson a diet of fruit, whichthey prefer Resultsfor GrayishSaltators.--Based on the method 248 ShortCommunications [Auk, Vol. 116

41 ture at night fell within the rangerecorded for other passerines(see Prinzinger et al. 1991)ß 4O Basalmetabolic rate was 1ß489_+ 0ß04 mL O2 ßg-• ßh • (n = 14), or 0ß3887W ßind • for a 47.0-gbirdß 39 Thisvalue is 64ß4%of thatexpected from body mass for passerinesduring the night periodas predicted 38 by Aschoffand Pohl (1970) and 63ß6%of that ex- pectedfor passerinesduring summernights (calcu-

•.• 37 latedfrom Kendeighet al. 1977)ßBMR measuredfor o theGrayish Saltator fell belowthe 95% confidence in-

38 tervalof the standardregression of BMR and body 10 2• 3• 4• 5O massfor birds (Reynoldsand Lee 1996)ß Thermal conductancewas 0ß116_+ 0ß002mL O2

3.5 ßg-• ßh -• ßøC-•, which is 18.9%higher than expected T frombody massfor passerinesduring the restphase (ißeß0ß098 mL O2 ßg • ßh • ßøC •; Aschoff1981)ß Ex- trapolatedbody (= ambient)temperature at a rate of metabolismequal to zero (i.eß46.9øC; Fig. lB) was considerablyhigher than recordedbody tempera- tures. o_ 2.0 I-. Resultsfor OrinocanSaltators.--The two linesfitted

• 1.5 byYaeger and Ultsch's (1989) method, •'O 2 = 1.83+ 0.06T•and •'O• = 2ß91- 0.04T•,intercepted at T• = 10.9øC,which is not biologicallymeaningfulß There- O 1.0 fore,on thebasis of visualinspection we dividedthe U,I dataset in pointsabove and below 25øC and fittedby >- 0.5 x leastsquares a line to eachsubset (Fig. 2B). The line to the left (•'O• = 3ß925- 0.080T•;n = 11, r = 0ß74, 0.0 10 20 30 40 50 P = 0ß009)and the line to theright (•'O• = 1.540+ 0.006T•; n = 9, r = 0ß102,P = 0ß794)intersected at AMBIENT TEMPERATURE(øC) 27.7øC, which we considered to be the lower limit of F•c. 1. Body temperature(A) and oxygencon- thermoneutrality.Average nightly body temperature of individuals within the thermoneutral zone was sumption (B) in relation to ambient temperatureof six postabsorptiveGrayish Saltatorsduring their 38.8øC_+ 0ß269 (n = 6). As in theformer species, body nonactivephase. The two linesin the lowerfigure temperature of Orinocan Saltatorsvaried signifi- werefitted by themethod of Yeagerand Ultsch (1989; cantly with ambienttemperature, even within the seetext for equations).Each symbol represents one thermoneutral zone (Tb = 32ß4+ 0.198T•;n = 20, r = individual bird. 0ß774,P < 0.001;Fig. 2A). Averagebody temperature at night alsofell within the rangerecorded for other passerines(see Prinzinger et al. 1991)ß Basalmetabolic rate was 1ß715-+ 0ß064mL O• ßg • of Yeagerand Ultsch(1989), we fitted two linesto the ßh • (n = 6), or 0ß3136W. ind • for a 32.7-gbirdß This dataset (Fig. lB). Theline to theleft (•O 2= 3.657- valueis 67ß9%of that expectedfrom body massfor 0.078T•;n = 22, r = 0.790, P < 0.001) and the line to passerinesduring the 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.This point marks the for passerinesduring summernights as calculated shiftfrom metabolicconformation to metabolicreg- from Kendeighet al. (1977)ßBMR of the Orinocan ulation and can be considered to be the lower limit Saltator also fell below the 95% confidence interval of thermoneutrality.Average nightly body temper- of thestandard regression of BMRand body mass for ature of individuals within the thermoneutral zone birds (Reynoldsand Lee 1996). was 39.4 _+SE of 0.141øC(n = 14). GrayishSaltators Thermal conductance of Orinocan Saltators was maintaineda high but variablebody temperature 0ß143_+ 0ß004 mL O• ßg • ßh • ßøC •, whichis 23ß9% (Fig. 1A). Althoughbirds clearlycould thermoreg- higherthan expected from body massfor passerines ulate,their body temperature was not controlled pre- during the rest phase(ißeß 0ß115 mL O• ßg-• ßh • cisely,and it varied significantlywith ambienttem- ßøC-•; Aschoff 1981)ß As for GrayishSaltators, ex- perature (T b = 36.4 + 0.091T•; n = 40, r = 0.617, P trapolatedbody (= ambient)temperature at a rate of < 0.001). Not even within the thermoneutralzone metabolismequal to zero (ißeß49.1øC; Fig. 2B) was was there a clear indication that birds maintained a considerablyhigher than recordedbody tempera- constantbody temperature.Average body tempera- tures. January1999] ShortCommunications 249

41 real species,particularly those that rely extensively 40 on fiber fermentation (McNab 1978). Microtine ro-

39 dentsof smallbody mass that feedheavily on leaves of woodyplants, and that probablydigest cell solu- 38 blesonly, have high basalrates (McNab 1986).Fur- 37 thermore,in mammalsit appearsthat BMR is re-

38 ducedonly in specieswhose diets consist of at least 20 to 30% leaves(McNab 1978:figure 6). In contrast, 35 •m BMRs are considerablyreduced in small birds (e.g. 0 34 saltatorsand )that are incapableof fiber

33 I ...... , ...... fermentationand that incorporateleaves in theirdiet 10 20 30 40 50 to a moderateextent only. The interactionbetween food quality and diges- • 3.5 tive physiologymight influencemetabolic rates of homeothermsbecause digestive and absorptivepro- cessesmight limit ratesof energy acquisition,thus settingan upper ceilingto the energybudget of or- ganisms (e.g. Weiner 1992, Veloso and Bozinovic 1993). In particular, McNab (1978, 1986) proposed 0 2.0 that the useof a poorfood source by mammalianar- I'- Q. boreal folivoresmight requirethem to have a low

'--' 1.5 basalrate of metabolism.He posedthree nonexclu- sive explanationsto interpret the correlationbe-

t.• 1.0 tweenfolivory and reducedBMR in mammals.First, leavesmight have a low metabolizableenergy con- tent becausethey are rich in fiber,which is difficult •- 0.5 to digest.Limitations on the maximumbulk of en- ergy-dilutefood that can be processeddaily by the 0.0 10 20 30 40 50 digestivetract might limit energyintake in folivores. Second, the low basal rates of folivorous mammals AMBIENT TEMPERATURE(øC) may be an adaptationto reducethe intake of toxic FIG. 2. Body temperature(A) and oxygen con- secondarycompounds present in thegreen tissues of sumption(B) in relationto ambienttemperature of plants. Reduced intake of secondarycompounds four postabsorptiveOrinocan Saltators during their may reducedose-related negative effects and the costs of detoxification. Third, arboreal mammalian nonactivephase. The two lines of the lower figure werefitted by dividingthe dataset into pointsbelow folivores,particularly larger species, are rathersed- and above25øC (see text for equations).Each symbol entaryand have a low proportionof musclemass rel- ative to body mass.In mammals,low basal rates of representsone individual bird. metabolism are correlated with reduced muscle

mass. Discussion.--Inaccordance with expectations, Explanationsproposed by McNab in relation to both speciesof saltatorhad substantiallylower mammalsmight also apply to folivorousbirds. First, BMRsthan predictedfrom their body size.This re- difficultiesassociated with the digestionof fiber(and ductionof restingmetabolism should contribute to of soluble cell contents contained within fibrous cell an economyof daily energyexpenditure. Other ar- walls) determine that metabolizableenergy of fo- borealfolivores also have low BMRs.Speckled Mouse- liage rankslowest among bird foods(Karasov 1990). birds (Coliusstriatus; 50 to 55 g) and Blue-naped Likewise,limitations of tract volumeand processing Mousebirds( macrourus; 51.3 g), two par- rate of energy-dilute foliage are known to limit in- tially folivorousspecies of 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 take in to reduceingestion of toxic plant sec- (Bartholomewand Trost1970, Prinzinger 1988). Fur- ondarymetabolites (Jakubas et al. 1993),and detox- thermore,mousebirds are ableto entertorpor, an im- ificationcosts might be a substantialportion of their portant energy-savingmechanism (Bartholomew energyand nutrient budget (Guglielmoet al. 1996). and Trost1970, Prinzinger et al. 1981).Likewise, the Third, in birds small muscle mass in associationwith obligate folivorous, fiber-fermenting Hoatzin (Op- sedentaryhabits might alsobe correlatedwith a low isthocomushoazin; 598 g) of the Neotropicshas a BMR basal rate of metabolism (McNab 1988, 1994). Few that is 69.8%of expected(Grajal 1991). In mammals, data exist on time budgetsof arboreal folivorous reductionof BMR is highestin medium-sizedarbo- birds, but it is of interestthat the obligatorilyfoli- 250 ShortCommunications [Auk, Vol. 116 vorous Hoatzin has a thickened callus of skin on the 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 saltatorsspend 77 to 80% of study site, nonbreedingindividuals of both species their time sitting, singing,and preeningsuggests of saltator remain motionlessfor major portions of that, under sucha relaxedtime budget,it is unlikely their time budget.Grayish Saltators and Orinocan that theywould be forcedto forageor to spendcon- Saltatorspend about 50 and 42% of daylighthours, siderableportions of time exposedto unfavorablera- respectively,sitting and a further 30 and 35% en- diative environments. The fact that BMR is reduced gagedin low-coststatic activities such as preening in otherarboreal folivores, including temperate spe- and singing(Garcfa 1994, Rodriguez 1994). cies,suggests that diet is important. A considerableportion of the diet of saltatorsis Amongfolivorous birds, it appearsthat only the madeup of fruits and otherplant tissues.Data on the morearboreal species have reduced metabolic rates. energeticsof frugivoresis scant,but it appearsthat The ground-dwellingfolivorous grouse and ptar- frugivoryin 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 becausethree species of highlyfrugivorous Neotrop- those expectedfrom considerationsof body mass ical manakins(Pipridae) have BMRs that correspond alone (see Weathers1979, McNab 1988). Likewise, to theirbody size (Vleck and Vleck 1979). Neverthe- flightless,forb-eating ratites and largelyterrestrial, less,several of the conditionsthat apply to folivory grass-feedinganseriforms do not have reduced mightalso apply to frugivory.Fruit hasa highwater BMRs(see McNab 1988).To someextent, this pattern content and a considerableportion of indigestible is similar to that foundin mammalsin which only seeds;hence, metabolizable energy of whole fruits the more sedentaryarboreal species have low basal per unit of freshmass is quitelow (Karasov1990), rates.In contrast,the consumptionof grassand forbs and processingby the digestivetract might limit in- by terrestrialherbivorous mammals is associated takein highlyfrugivorous species (Levey and Grajal with high basalrates (McNab 1978,1986). Further re- 1991).Similarly, secondary metabolites of fruit pulp search is needed to unravel the effects of latitude, fo- can limit intake in frugivores(Izhaki and Safriel livory, and arborealhabits on the metabolicrates of 1989,Cipollini and Stiles1993). Perhaps the low bas- birds. al rates in saltatorsare associatedwith folivory in Acknowledgments.--Weare grateful to Sr. Tom•s combinationwith frugivory. Blohmfor permissionto work at Hato Masaguaral Neitherspecies of saltatorfully balancedheat loss- 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 seeminglycontrolled manner). The de- while at Hato Masaguaral.Travel expenses of RBSto creasein T bbetween 34 and 13øCT a that we estimat- Venezuelawere covered by a Jastro-ShieldsGraduate ed from the regressionequations was 1.9øCin the ResearchFellowship from the Universityof Califor- GrayishSaltator (from 39.5 to 37.6øC)and 4.1øCin nia. WesWeathers kindly allowedthe use of the ox- the OrinocanSaltator (from 39.1 to 35.0øC).This con- ygen analyzer.Research on saltatorsat Hato Masa- trolled decreasein Tb, although moderate,should guaral was initiated by M. A. Garcia and A. Rodri- contributeto an economyof energyexpenditure and guez.Suggestions by reviewersgreatly improved the also could be consideredan adaptationto saveen- manuscript.All birds were captured and handled ergy.A moderatedecrease in Tb with falling Ta,con- under permissionsfrom PROFAUNA(Ministerio del trolledhypothermia, is knownfor approximately40 Ambiente y RecursosNaturales Renovables)issued other speciesof birds, includingmousebirds (Prin- to M. A. Garcia and A. Rodriguez. zinger et al. 1991).Failure to increaseheat produc- tion enoughto balanceheat loss also has the effect of LITERATURE CITED loweringthe slopeof the line to the left of the lower criticaltemperature (Figs. lB and2B), which coupled ASCHOFF,J. 1981. Thermal conductance in mammals with a combinationof physicaland chemicalther- and birds: Its dependenceon body size and cir- moregulation(McNab 1980b),should account for the cadian phase.Comparative Biochemistry and highextrapolated body temperatures at an estimated Physiology69A:611-619. rate of metabolismequal to zero for both species. ASCHOFF,J., AND H. POHL. 1970. Der Ruheumsatz Tropical birds seem to have reduced BMRs for von V6gelen als Funktion der Tageszeitund der their body size, particularlyspecies that regularly K6pergr6sse.Journal ftir Ornithologie111:38- foragein the sun (Weathers1979, 1997). Latitude, or 47. factorsassociated with it (e.g. lower massof meta- BARTHOLOMEW, G. g., AND C. H. TROST. 1970. Tem- bolicallyactive tissue;Rensch and Rensch1956 in peratureregulation in the SpeckledMousebird, Daan et al. 1990),might be a confoundingfactor in striatus. Condor 72:141-146. the interpretationof our findingthat saltatorshave BENNETT,P. g., AND P. H. HARVEY. 1987. Active and January1999] ShortCommunications 251

restingmetabolism in birds:Allometry, phylog- dar Waxwings. American Naturalist 138:171- eny and ecology.Journal of Zoology (London) 189. 213:327-363. MCNAB,B. K. 1978. Energeticsof arborealfolivores: CIPOLLINI, M. L., AND E. W. STILES. 1993. Fruit rot, Physiologicalproblems and ecologicalconse- antifungal defense,and palatability of fleshy quencesof feeding on an ubiquitousfood sup- fruits for frugivorousbirds. Ecology74:751-762. ply. Pages153-162 in The ecologyof arborealfo- DIAN, S., D. MASMAN, AND A. GROENEWOLD. 1990. livores (G. G. Montgomery,Ed.). Smithsonian Avian basal metabolic rates: Their association Institution Press,Washington, D.C. with body compositionand energyexpenditure MCNAB,B K. 1980a.Food habits, energetics and the in nature.American Journal of Physiology259: populationbiology of mammals.American Nat- R333-R340. uralist 116:106-124. GARCIA,M. A. 1994.La dieta y la eficienciadigestiva MCNAB,B. K. 1980b.On estimatingthermal conduc- del LechoseroPechiblanco (Saltator orenocensis). tancein endotherms.Physiological Zoology 53: Thesis, Universidad Sim6n Bolivar, Caracas, 144-156. Venezuela. MCNAB, B. K. 1986. The influence of food habits on GRAJAL,A. 1991.The nutritionalecology and diges- the energeticsof eutherianmammals. Ecological tive physiologyof the Hoatzin (Opisthocomus Monographs56:1-19. hoazin),a folivorousbird with foregut fermen- MCNAB, B. K. 1988. Food habits and basal rate of me- tation. Ph.D. dissertation,University of Florida, tabolism in birds. Oecologia77:343-349. Gainesville. MCNAB, B. K. 1994. Energy conservationand the GUGLIELMO,C. G., W. H. KARASOV,AND W. J. JAKU- of flightlessnessin birds. American BAS.1996. Nutritional costsof a plant secondary Naturalist 144:628-642. metaboliteexplain selectiveforaging by Ruffed MORTON,E. S. 1978.Avian arborealfolivores: Why Grouse.Ecology 77:1103-1115. not? Pages123-130 in The ecologyof arboreal HILL, R. W. 1972.Determination of oxygenconsump- folivores(G. G. Montgomery,Ed.). Smithsonian tion by use of paramagneticoxygen analyzer. InstitutionPress, Washington, D.C. MUNSON, E. S., AND W. D. ROBINSON.1992. Extensive Journalof Applied Physiology33:261-263. HULBERT,A. J., AND t. J. DAWSON. 1974. Standard folivory by Thick-billedSaltators (Saltator max- ilIosus)in southernBrazil. Auk 109:917-919. metabolism and body temperature of perame- PARRA,R. 1978. Comparisonof foregut and hindgut loid marsupialsfrom different environments. fermentationin herbivores.Pages 153-162 in ComparativeBiochemistry and Physiology47A: 583-590. The ecologyof arborealfolivores (G. G. Mont- gomery, Ed.). SmithsonianInstitution Press, IZHAKI,I., ANDU. N. SAFRIEL.1989. Why are thereso Washington,D.C. few exclusivelyfrugivorous birds? Experiments PRINZINGER,R. 1988.Energy metabolism, body-tem- of fruit digestibility.Oikos 54:23-32. peratureand breathing parameters in nontorpid JAKUBAS,W. J., W. H. KARASOV,AND C. G. GUGLIEL- Blue-naped Mousebirds Urocolius macrourus. MO. 1993. Ruffed Grouse tolerance and biotrans- Journalof ComparativePhysiology 157B:801- formation of the plant secondarymetabolite 806. coniferylbenzoate. Condor 95:625-640. PRINZINGER,R., R. GOPPEL,A. LORENZ, AND E. KUL- JENKINS,R. 1969.Ecology of threespecies of saltators ZER.1981. Body temperature and metabolismin in CostaRica with specialreference to their fru- the Red-backed (Colius castanotus) givorousdiet. Ph.D. dissertation,Harvard Uni- during fasting and torpor. Comparative Bio- versity,Cambridge, Massachusetts. chemistryand Physiology69A:689-692. KARASOV,W. H. 1990. Digestion in birds: Chemical PRINZINGER,R., A. PREllMAR,AND E. SCHLEUCHER. and physiologicaldeterminants and ecological 1991. Body temperaturein birds. Comparative implications.Studies in Avian Biology13:391- Biochemistryand Physiology99A:499-506. 458. RENSCH,I., AND B. RENSCH.1956. Relative organ- KENDEIGH, S.C., V. R. DOL'NIK, AND V. M. GAVRILOV. massebeitropischen warmbluetern. Zoologisch- 1977.Avian energetics.Pages 127-204 in Graniv- er Anzeiger 156:106-124. orousbirds in ecosystems(J. Pinowsky and S.C. REYNOLDS,P.S., AND R. M. LEEIII. 1996. Phyloge- Kendeigh,Eds.). Cambridge University Press, neticanalysis of avianenergetics: Passerines and Cambridge, United Kingdom. nonpasserinesdo not differ. AmericanNatural- KENWARD, R. E., AND R. M. SIBLY. 1977. A Wood Pi- ist 147:735-759. geon (Columbapalumbus) feeding preferenceex- RODRIGUEZ,A. 1994. Dieta y comportamientoali- plained by a digestivebottle-neck. Journal of mentario del LechoseroAjicero (Saltatorcoeru- Applied Ecology14:815-826. Iescens).Thesis, Universidad Sim6n Bolivar. Ca- LEVEY,D. J., ANDA. GRAJAL.1991. Evolutionary im- racas, Venezuela. plicationsof fruit-processinglimitations in Ce- STRAHL,S, D. 1988. The socialorganization and be- 252 ShortCommunications [Auk, Vol. 116

haviour of the Hoatzin (Opisthocomushoazin) in WEATHERS,W. W., C. J. SHAFIRO,AND L. B. ASTHEI- central Venezuela. Ibis 130:483-502. MER. 1980. Metabolic responses of Cassin's TROTH,R. G. 1979.Vegetational types on a ranchin Finches (Carpodacuscassini) to temperature. the central llanos of Venezuela.Pages 17-30 in ComparativeBiochemistry and Physiology65A: Vertebrateecology in the northern Neotropicis 235-238. (J. E Eisenberg,Ed.). SmithsonianInstitution WEINER,J. 1992. Physiologicallimits to sustainable Press,Washington, D.C. energybudgets in birds and mammals:Ecolog- VELOSO,C., AND E BOZINOvlC.1993. Dietary and di- ical implications.Trends in Ecologyand Evolu- gestiveconstraints on basal energy metabolism tion 7:384-388. in a small herbivorousrodent. Ecology74:2003- 2010. YEAGER,D., AND G. R. ULTSCH.1989. Physiological VLECK, C. E.M., AND D. VLECK. 1979. Metabolic rate regulationand conformation:A BASICprogram in five tropicalbird species.Condor 81:89-91. for the determinationof criticalpoints. Physio- WEATHERS,W. W. 1979. Climatic adaptation in avian logical Zoology 62:888-907. standardmetabolic rate. Oecologia42:81-89. WEATHERS,W. W. 1997.Energetics and thermoregu- lationby smallpasserines of the humid,lowland Received11 November1997, Accepted22 April 1998. tropics.Auk 114:341-353. AssociateEditor: M.E. Murphy

TheAuk 116(1):252-256, 1999

Low ExtrapairPaternity in the CactusFinch (Geospizascandens)

KENNETH PETREN,• g. ROSEMARYGRANT, AND PETERg. GRANT Departmentof Ecologyand Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA

Severalinvestigations of Darwin's fincheshave re- en by brachialvein puncturefrom nestlingsat day 8 lied upon observationsof adults at the nestfor iden- and from adults capturedin mist nets. Nearly all tifying parents.These include estimations of herita- males on the island throughoutthe study period ble variation and covariation (Grant and Grant 1989, were sampled. The largest number of potential 1994), lifetime reproductive successand genetically breeders was present in 1993 (68 males and 27 fe- effective population sizes (Grant and Grant 1992), males), when 90% of the males and 93% of the fe- and the evolutionaryresponse to selection(Grant males were sampled. and Grant 1995). Studies of other emberizids and Prior to puncture with a 30.5-gaugehypodermic cardinalids(related sparrows, finches, and buntings) needle,the area was cleanedwith alcohol,and a drop in the temperatezone have shownthat simply ob- of 0.5M EDTA was placed over the vein. Blood was serving adults 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 beforebeing transferredto the laboratoryand stored result in fertilizationsand the rearing of nonpaternal at - 80øC. offspring.To determinewhether this occursin Dar- Eight microsatelliteloci developedin the Medium win's finches,we undertooka studyof microsatellite Ground-Finch(Geospizafortis) were used to testpar- DNA variation in a socially monogamous,multi- entagein G,scandens. Laboratory techniques used for brooded species,the Cactus Finch (Geospizascan- genomiclibrary screeningand geneticscreening of dens),on the GalapaRosisland of Daphne Major individual birds generally followed those of Prim- (0ø15'S,90ø13'W). The frequencyof polygyny has mer et al. (1995).Detailed methodsand primer se- neverexceeded 5% in this population(see Boar and quencesare availableelsewhere (Petren 1998). Mea- Grant 1984, Gibbs and Grant 1987, Grant and Grant suresof variation at theseeight loci and exclusion 1996 for breeding characteristicsand population probabilities are given in Table 1. We found no evi- data). denceof "null" alleles(Callen et al. 1993)in the ped- Methods.--Bloodsamples were taken from 248 igree. birds in 1988to 1996.A singledrop of bloodwas tak- Resultsand discussion.--All159 offspring had one allelein commonwith the maternalparent (with the E-mail: [email protected] exceptionof the Z-linked locus).Therefore, mater-