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Maintenance Energy Costs of Two Partially Folivorous Tropical 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-species groups:Is there an optimal group size?Pages flockingon the vigilanceof shorebirds:Who do 122-147in Behaviouralecology, an evolutionary they trust?Animal 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 birds. 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 storing behaviorin SiberianTits WAITE,T. A. 1987a.Vigilance in the White-breasted Parus cinctus Bodd. and Willow Tits Parus mon- Nuthatch:Effects of dominanceand sociality. tanusBald. SovietJournal 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 Passerines 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 plants,re- leavesand other plant 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 the OrinocanSaltator (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 feeding observations),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). Insects 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 bird. 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
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