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Energetics of Toucans, a Barbet, and a Hornbill: Implications for Avian Frugivory

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Energetics of Toucans, a Barbet, and a Hornbill: Implications for Avian Frugivory The Auk 118(4):916-933, 2001 ENERGETICS OF TOUCANS, A BARBET, AND A HORNBILL: IMPLICATIONS FOR AVIAN FRUGIVORY BRIAN K. MCNAB 1 Departmentof Zoology,University of Florida,Gainesville, Florida 32611, USA ABSTRACT.--Rateof oxygenconsumption was measuredin eight speciesof toucans,one barbet, and one hornbill to examinefactors that influencetheir energyexpenditures. Basal rate of metabolismin thosespecies, supplemented with measurementsfrom three wood- peckersand three mousebirds,is correlatedwith body massand either food habitsor cli- mate:temperate acorn- and insect-eatingspecies have basal rates that are -70% greaterthan tropicalfruit-eating species. The temperate,insect- or acorn-eatingspecies are woodpeckers, so level of basal rate is also correlated with familial affiliation. The toucans, barbet, and horn- bill havebasal rates similar to thoseof frugivorouspigeons and bats,which collectivelyare low by avianstandards. The effectsof climate,food habits,and family affiliationon basal rates in endothermsare difficult to separate,given the restricteddata set available.Earlier conclusionsthat the basalrates of birds greatlyexceed those of mammalsare confounded by characterinteractions that influencedependence of basalrate on body mass.The largest toucanshowed a remarkableability to reduceenergy expenditureat low ambienttemper- atureswithout reducingcore body temperature,possibly as a result of peripheralvasocon- striction.Received 7 June1999, accepted16 April 2001. BIRDS HAVE BASAL rates of metabolism that at low latitudesto high levelsof solarradiation; vary with many factors,including body mass. McNab (1988a)suggested that the basalrate of They are describedas having higher basal rates birds is correlated with food habits; McNab than mammals,with passerineshaving higher and Bonaccorso (1995) showed that basal rate basal rates than other birds (Lasiewski and in insectivorous birds is correlated with for- Dawson 1967,Aschoff and Poh11970),and they aging style; and McNab (2000) demonstrated have a circadian rhythm in which the rate is that the basalrate of frugivorouspigeons in the highest,even when inactive,during the normal South Pacific is correlated with island size. period of activity (Aschoffand Pohl 1970). A Here I present data on temperatureregula- recent analysisby Reynoldsand Lee (1996) ar- tion and rate of metabolismof eight speciesof gued that passerinesdo not havehigher basal toucansthat belongto five of the six genera,on rates than other birds, a conclusionfirst sug- one speciesof African ground-barbet(Trachy- gestedby Prinzingerand Hanssler(1980), al- phonusdarnaudiO, and on Blyth's Hornbill (Ac- though the data used by Reynolds and Lee erosplicatus), a member of the palaeotropical were not stipulated and potentially included family Bucerotidae.The toucan family Ram- measurements that do not meet strict standards phastidaeis limited in distributionto the Neo- for basal rate (McNab 1997). Nevertheless, tropics, which along with woodpeckers(Pici- much interspecificvariation is found in basal dae), honeyguides (Indicatoridae), jacamars rate, even when body size, taxonomy,and time (Galbulidae), puffbirds (Bucconidae),and bar- of day are taken into consideration.Although bets (Capitonidae) constitutethe order Picifor- the extent to which that residual variation in- mes.Recent analyses, however, have suggested cludesmeasurement error is unclear, the larg- that New World barbetsconstitute a subfamily est proportion is correlatedwith the natural (Capitoninae) of the Ramphastidae (Prum history of the speciesstudied. Thus, Weathers 1988), whereas African barbets are placed in (1979) showed that latitude (and climate) has the family Lybiidae and Asian barbets in the an effect on basal metabolic rate in birds; Ellis family Megalaimidae (Sibley and Ahlquist (1980, 1984) demonstrated that basal rate is cor- 1990). related with plumage color in speciesexposed Toucans are of special interest becauseof their commitmentto frugivory (Remsenet al. 1993), although large speciesalso opportunis- E-mail: [email protected] tically prey on birds and mammals (Skutch 916 October2001] EnergeticsofAvian Frugivores 917 1983, Boinski 1987, Mitchell et al. 1991). Pro- Zoo) occursin southeasternBrazil to Paraguay and pensity for carnivory in sometoucans is most northern Argentina. (8) Red-Billed Toucan (Ram- marked in the highlands,which may compen- phastostucanus; one male and one female studied at satefor a reducedfruit availability(Galetti et the Parque Ambiental y Zoo16gicoGustavo Rivera) al. 2000). African ground-barbetsfeed on fruit occursprincipally in the tropical lowlands of South America north of the Amazon River. (9) Toco Toucan and insects (Short and Horne 1980). Hornbills, (Ramphastostoco; one male and one female borrowed traditionally placedin the order Coraciiformes, from the Lowry Park Zoo) lives in South America representan ecotypeconvergent with toucans, from the Guianasand Brazil southto Paraguayand large arborealspecies, such as A. plicatus,being northern Argentina. (10) Blyth'sHornbill (Acerospli- highly frugivorous(Kemp 1995). catus;one male and one female,semicaptives studied Thesedata permit an examinationof effectof at Christensen ResearchInstitute, Madang, Papua body size,food habits,behavior, and climateon New Guinea) inhabits Burma east to Sulawesi, New energeticsof tropical nonpasserinefrugivores Guinea, the BismarckArchipelago, and the Solomon through a comparison of toucan energetics Islands, although some of its distribution east of with those of the barbet, hornbill, and three New Guinea may be due to human transport (D. W. Steadman pers. comm.). mousebirds (Bartholomew and Trost 1970, Somecaptive individuals used in this study were Prinzinger et al. 1981, Prinzinger 1988). Tou- caughtin the wild, whereasothers were the product cans are also compared with woodpeckers of captivebreeding. They ate a variety of fruits with (Kendeighet al. 1977, Weatherset al. 1990), the protein and vitamin supplements and lived under only other piciformsthat have had their ener- the local natural photoperiod and temperaturere- geticsmeasured. In addition,I comparethe en- gimes. Measurements in Venezuela occurred in Au- ergy expenditures of those frugivores with gust and December, in Papua New Guinea in July, those of frugivorous pigeons (McNab 2000) and in Florida in fall or spring. and fruit bats belongingto the family Ptero- Experimentaltechniques.--Measurements of rate of metabolism,as oxygenconsumption, occurred in an podidae (Bonaccorsoand McNab 1997,McNab open system.Room air was suckedthrough a cham- and Armstrong 2001, McNab and Bonaccorso ber, the size of which varied with the size of a bird: 2001). a 329 L hollow-walled chamber was connected to a thermoregulatedwater bath; a 2 and a 44 L chamber, METHODS the temperaturesof which were regulatedby placing the chamber into the hollow-walled chamber; or a 15 Birds.--! studied 10 speciesof birds. They were (1) and a 27 L chamberwas placed a temperature-con- D'Arnaud's Ground-Barbet (Trachyphonusdarnaudii; trolled refrigerator.The barbet was measuredin a 2 one male and one female borrowedfrom the Lowry L chamber, most toucans in the 15 or 44 L chamber, Park Zoo, Tampa, Florida), a speciesthat occursin and the Toco Toucan both in the 44 and 329 L cham- EastAfrica from the Sudanto Tanzaniain dry brush bers. Hornbills were confined in the 27 L chamber country. (2) Saffron Toucanet(Baillonius bailloni; one during measurements.After being removedfrom the male and one female borrowed from the Central chamber, air was sequentially scrubbedof CO2 (by Florida Zoological Park, Lake Monroe, Florida) lives indicating soda lime) and water (by indicating silica in the Atlantic rainforest of Brazil. (3) Groove-Billed gel). The air stream then went to a flowmeter and to Toucanet(Aulacorhynchus sulcatus; one male and one an Applied ElectrochemistryS3A-II OxygenAnalyz- female studied at the ParqueAmbiental y Zoo16gico er, the outputsof which went to a stripchartrecorder. Gustavo Rivera, Falc6n, Venezuela) occurs in north- The flow rates varied with chamber size: flow rates ern Colombia and Venezuela. (4) Emerald Toucanet were 0.6 to 0.9 L min • in the 2 L chamber, 1.0 to 1.5 (Aulacorhynchusprasinus; one male and one female L mint in the 15 L chamber, 4.1 to 6.6 L mint in the borrowedfrom the Lowry Park Zoo) lives in south- 27 L chamber, 2.1 to 2.7 L min -• in the 44 L chamber, ern Mexico and Central America south to Venezuela, and 4.5 to 9.0 L min -t in the 329 L chamber. Those Colombia, Ecuador, and Peru. (5) Spot-Billed Tou- rates were high enoughto ensurean adequatemix- canet (Selenideramaculirostris; two males and one fe- ture of air in the chamber,as was demonstratedby male borrowed from the Lowry Park Zoo) is found independence of the calculated rate of metabolism in Brazil south of the Amazon to northeastArgen- from flow rate. tina. (6) Black-NeckedAra•ari (Pteroglossusaracari; To minimize the influence of activity, minimal one male and one female studied at the ParqueAm- rates of metabolism that lasted ---2 min were used; biental y Zoo16gicoGustavo Rivera) lives from Ven- individual runs usually lasted 2-3 h. The experi- ezuela and the Guianas souththrough southernBra- mentsreported here representeda total of 1,572h of zil. (7) Red-BreastedToucan (Ramphastosdicolorus; measurements;usually two experimentswere run at one male and one femaleborrowed from Lowry Park the same time. The cloacal temperature and body 918 BRIANK. MCNAB [Auk, Vol. 118 mass of the birds were measured at the terminus
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