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Home , Hirundo, Pacific swallow, Petrochelidon, Tachycineta, Tree swallow

FIELD METABOLISM OF TREE DURING THE BREEDING SEASON

JOSEPHB. WILLIAMS Departmentof Physiology,College of Medicine,University of Arizona, Tucson,Arizona 85724 USA

ABSTRACT.--Iused doubly labeled water to study the field metabolic rate (FMR) of Tree Swallows( bicolor) on Kent Island, New Brunswick,Canada, during the breeding season.I testedthe hypothesisthat aeriallyforaging have higher energyrequirements than other species. For incubatingfemale swallows,carbon dioxide productionaveraged 201.4 + 15.8 ml CO2/ h. While feeding 5 young, male and female swallowsexpired CO2at a rate of 211.6 + 23.3 and 231.0 + 26.4 ml CO2/h, respectively.During this period malesworked at similar levels to females,but the power consumptionof females that fed young was significantly higher than incubatingfemales. For both parentstogether, the meannumber of visitsto the nest/h was correlatedwith CO2production: ml CO2/h = 201.6 + 2.49 (visits/h). On Kent Island, Tree Swallows had a higher FMR than Savannah Sparrows (Passerculus sandwichensis),suggesting that aerial-foragingbirds have a higher FMR than ground-foraging species.For 7 speciesof hirundines, energy expenditurewas associatedpositively with body mass;log(kJ/d) = 1.34 + 0.53 log(body mass,g). This relationshipdiffered from one for specieswhich use alternative foraging modes (ground foraging and flycatching, n = 11), log(kJ/d) = 0.89 + 0.75log(body mass, g). Aerial foragersexpend from 16-38%more energy/ day than do other of similar size that spend lesstime flying. ReceivedI September1987, accepted8 June1988.

ENERGYrequirements during flight are rela- higher energy requirements than ground-for- tively high (Bergerand Hart 1974, Pennycuick aging species.By an allometric analysis,I tested 1975), and aerial feeding presumablyrequires the idea that, in general, hirundines have a more energy than other foraging modes.As a higher FMR than other birds that use alterna- consequence,birds that foragein flight, suchas tive foraging modeswhich require lesstime in swallows, may exhibit relatively high rates of flight. daily energy expenditure (DEE; Mugaas and METHODS King 1981,Kavanau 1987). This hypothesisgains indirectsupport from time-energybudget (TEB) Studyarea and species.--Thisstudy was conducted studieswhere subtle differencesin flight time at the Bowdoin Scientific Research Station on Kent result in substantial variation in estimates of Island, New Brunswick, Canada (66ø46'W, 44ø35'N), energy expenditure (Utter and Le Febvre 1973, during the summersof 1981 and 1982. The island contains 2 grassy fields (10.7 and 4.0 ha) in which Bryant and Westerterp 1983). about 100 Tree nest boxes have been erected. However, aerial insectivores have wing The boxeswere painted white with the entrance fac- shapeswhich may decreasethe cost of flight ing north, away from prevailing winds. The fields, (Hails 1979). An alternative hypothesisis that dominated by Agrostisstolonifera and Festucarubra, aerially foraging speciesexpend less energy provided nesting habitat for about 100 pairs of Sa- during flight than other species,and as a con- vannah Sparrows(Williams 1987). sequence,the overall field metabolicrate (FMR) The breeding biology of Tree Swallows on Kent may be equivalent to similar-sizedbirds which Island has been describedby Paynter (1954) and that use alternative foraging modes. of Savannah Sparrows,by Dixon (1978). Both species I usedthe doubly labeled water (DLW) meth- are migratory;both lay eggsin early June. Swallows nest in boxes;sparrows construct well-hidden open- od to estimatethe FMR of Tree Swallows (Tachy- cup nests,usually on the ground. The femalesof both cinetabicolor) during the breeding seasonsof speciesincubate unassistedby the male. Although 1981and 1982.I comparedtheir FMR with pub- male swallows may bring food to their incubating lished values for Savannah Sparrows (Passer- mates (Kuerzi 1941), I did not observe this behavior. culus sandwichensis;Williams 1987) to test the Modal clutchsize for swallowsvaried from 5-6 eggs hypothesis that aerial-foraging species have depending on the year (Winn 1949, Paynter 1954); 706 The Auk 105: 706-714. October 1988 October1988] FieldMetabolism ofTree Swallows 707

TABLE1. CO2 production,energy use, and water flux rates for incubatingfemale Tree Swallowson Kent Island, New Brunswick, Canada.

Mean Waterflux (ml/d) Date mass(g) ml CO2/h kJ/d In Out Taa FMR/BMR 1981 17-18 June 25.3 193.3 114.1 14.0 14.3 11.8 3.4 17-18 June 22.5 191.7 113.2 18.8 18.4 11.8 3.8 7-8 June 22.2 181.6 107.2 17.5 18.3 11.0 3.6 15-16 June 21.8 202.1 119.3 16.4 17.2 9.0 4.1 12-13 June 23.1 201.9 119.2 19.4 19.5 I 1.0 3.9 19-20 June 24.5 230.1 135.9 13.6 13.9 10.5 4.2 1982 8-9 June 19.9 206.2 121.7 16.4 15.9 13.5 4.6 7-8 June 20.6 185.4 109.5 13.7 13.8 10.3 4.0 3-4 June 23.2 219.9 129.8 14.7 15.2 9.0 4.2 Mean 22.6 201.4 118.9 16.1 16.3 10.9 4.0 (SD) (+-1.7) (_+15.8) (+-9.3) (+-2.2) (+2.1) (-+1.4) (+-0.4) Mean air temperaturefor experimentalperiod.

SavannahSparrows usually lay 4 eggs.In both species, on Tree Swallows followed Williams (1987). Birds were femalesbrood the young until they are about5 days captured late in the afternoon at nest boxesand in- old, and in both speciesmales and femalesjointly jectedin the pectoralmuscle with 0.10 ml tritiated provide food for the young (Quinney 1986,Williams water (1 # Ci/g body mass)mixed with 97 atom % 1987).Nestling swallowsfledge fully featheredand oxygen-18.After an hour equilibrationperiod (Wil- are able to after 19-20 days in the nest, whereas liams and Nagy 1984), injected individuals were sparrowsleave the nest in 8-9 days and acquirethe markedwith white paint on the tip of the tail, banded ability to fly 7-10 days later. with a numbered aluminum band, and released. Lab- First-year female swallows, distinguishablefrom oratory proceduresfor the distillation of water from older females by plumage coloration (Winn 1949), blood samplesand for the assayof tritium followed may produce smaller clutches(De Steven 1978) and Williams (1987).Water sampleswere analyzed for 280 were excludedfrom this study. content by Dr. Ken Nagy at the University of Cali- Laboratorymetabolism.--Oxygen consumption (•o2) fornia, LosAngeles. Water influx and effiux were cal- of adult Tree Swallowswas measuredby meansof a culatedusing equations6 and 5, respectively,of Nagy closed-circuitmanometric system (Williams and Prints (1975), and rates of CO2 production using equation 8. 1986). In brief, 4 stainlesssteel chambers (2,000 ml) Backgroundlevels of isotopesobtained from unin- were wrapped with • inch copper tubing through jected conspecificswere subtractedfrom all values which a mixture of water and methanol was circulated prior to calculations.Validation studieshave shown with a refrigerated bath. Temperature,as measured reasonableagreement (-+10%) between gravimetric by a 38-gaugethermocouple and a BaileyThermom- measurementof CO2production and CO2production eter (Model 12), could be controlled to within -+0.1øC. as estimatedby DLW (Williams and Nagy 1984,Wil- During each trial, expired CO2 and H20 vapor were liams 1985). removed using Ascariteand Drierite, thus a decrease The factor of 24.6 J/ml CO2 was used to convert in pressure within the chamber was a result of O2 metabolicrates from units of CO2 to units of energy uptake.As birds consumed02, I restoredthe pressure (Williams and Nagy 1985).To convert O2 consump- in the chamber by infusion of O2 with a calibrated tion to heat production, I used20.08 J/ml O2(Schmidt- glasssyringe. The walls of eachchamber were coated Nielsen 1979). with flat black paint to minimize reflectedthermal Nine birds that were feeding nestlingseluded re- radiation. Birds were equilibrated 1-2 h before ex- capture after 24 h and were not re-bled until the perimentation. Experimentswere performed during following morning. For theseindividuals, I subtract- daylight hours (1000-1800) and each trial lasted 60 ed CO2 production during the secondnight period min.I correctedall Vo2values to STPD. Williams and from their total CO2 production (seeWilliams 1987). Prints (1986) and Obst et al. (1987) have shown close I assumed an R.Q. of 0.75 and that mean ambient air agreement(5-8% difference)between measurements temperature at night was a reasonableestimate of the of•o• asgiven by this method and •'o• as determined thermal environment(Mugaas and King 1981). with an open-flow system. All femalesthat were injectedwhile incubatinghad Fieldmetabolism.--The field protocolfor using DLW laid 5 or 6 eggs.To determinewhen injectedfemales 708 JOSEPHB. WILLIAMS [Auk, Vol. 105 resumed incubation, I placed a thermocouple in the 250 nest and continuously monitored nest temperature with a Linearstrip-chart recorder. Only I female(12- 200 13 June 1981; Table I) failed to return to the box by nightfall (2-3 h after injection).She resumedincu- 150 bationat daybreakthe next morning.All femaleswere recapturedat night in their nestboxes approximately 100 24-30 h after injection. For adultstending young, I injectedone of 50 a pair during the late afternoon.Thefollowing day, o the visits of both parents were recorded for 6 l-h -lO o lO 20 3o 40 periodsspaced throughout the day. All birds included Temperoture(øC) in this analysisfed chicks,although the variability in visitation frequencywas high. Broodsof 3 and 7 were Fig. I. Laboratory metabolism of Tree Swallows constructedby addingor subtractingequal aged young on Kent Island, NewBrunswick. to broods of 5 or 6. During both years, periods of inclement weather at times impeded swallows from feeding young, and some nestlingsdied. Thus, sam- the nighttime basalmetabolism (BMR) of 59.5 ple sizesfor broodmanipulation experiments are low. ml O2/h, or 1.19 kJ/h. I measuredair temperature(Ta) and relative humid- Below30øC, •o2 increased as Ta declined: ml ity (RH) continuouslywith a Weathermeasurehy- O2/h = 195.5 - 3.77 (Ta, øC) (n = 40, r 2 = 0.93, grothermographplaced in a standardweather instru- P < 0.0001). At a metabolic rate of zero, this ment shelter (Stevensonscreen). Each instrument was calibrateddaily with a Baileythermometer and a sling equation extrapolatesto 53.5øCsuggesting that psychrometer,respectively. Twice each day, at 0700 heat transfer from swallows in metabolism h and 1900 h, I recorded fog conditions and precip- chambers is not constant below their lower crit- itation (mm H20). Fogwas scoredas present or absent ical temperature(Ttc). The heat transfer coeffi- at each of the observation times. Precipitation was cient, calculatedas the slope of the regression measuredwith a standard rain gauge and recorded line for metabolismbelow the T•c,was 3.5 J/g. daily. During experimentalperiods, at 2 h intervals, I measuredirradiance (W/m 2)with a LiCor 185A pyra- Fieldmetabolism.--For incubating females, CO2 riometer calibrated against an Eppley pyranometer. productionaveraged 201.4 _+15.8 ml CO2/h or Wind speedwas measured I m abovethe groundwith 118.9kJ/d (Table 1). Carbon dioxide production a hand-held anemometer (Dwyer Model No. 460) was unrelated to Ta, wind, or solar irradiance. which was previously calibratedagainst a pitot tube in the laboratory. The ratio of FMR to BMR averaged4.0. Data were analyzedby meansof a SPSS/PCstatis- Body massof femalesdeclined from the in- tical package(Norusis 1984). Means are presented+ 1 cubation period (mean mass = 22.6 _+ 1.7, n = SD unless otherwise indicated. 9) to the nestling period (mean mass= 19.3 + 1.4, n = 18; t = 5.23, P < 0.01). While feeding RESULTS 5 young,male and femaleswallows expired CO2 at an averagerate of 211.6 and 231.0 ml CO2/ During June and July, the weather on Kent h, respectively(Table 2). ExpiredCO2 translated Island is cool and moist, with frequent fog into 124.9 kJ/d for males and 136.4 kJ/d for (Cunningham 1942,McCain 1975).Fog covered females. During this period, males worked at the island at 1 of the 2 observationperiods on similar levels to females (t = 1.4, P = 0.18), but 13 and 14 days in June and July of 1981, re- power consumptionof femalesfeeding young spectively.Similar valuesfor 1982 were 8 and wassignificantly higher than that of incubating 12 days.Rain fell on 30 daysin 1981and on 21 females (t = 3.0, P < 0.01). daysin 1982.Temperatures averaged about 1 IøC Combining all data, males expired CO2 at a in Juneand 13øCin July for both years. rate of 213.6 + 22.1 ml CO2/h (n = 7) and fe- Laboratorymetabolism.--The resting metabolic males at a rate of 229.7 + 28.9 ml CO2/h (n = rate (RMR) of post-absorptiveTree Swallows 18), valueswhich are statisticallyindistinguish- during the day averaged79.3 + 12.6 ml O2/h able (t = 1.33, P > 0.10). (Fig. 1; n = 12; mean mass = 21.6 _+ 1.9 g). For males and females together, the mean ReducingRMR by 25%(Aschoff and Pohl 1970, numberof visits/hour correlatedwith CO2pro- Calder and King 1974) yields an estimatefor duction(Fig. 2): ml CO•/h = 201.6 + 2.49 (visit/ October1988] FieldMetabolism of Tree Swallows 709

TABLE2. Ratesof CO2 production,energy use, and water flux for Tree Swallowsfeeding young on Kent Island, New Brunswick (1981 and 1982).

Mean Waterflux (ml/d) body mass Nestling FMR/ Date (g) age (d) ml CO2/h kJa/d Influx Effiux BMR Brood size = 3

Males 7-8 July 1982 21.2 4 200.0 118.1 20.3 20.8 4.2 Females 3-4 July 1982 16.6 14 195.9 115.7 22.3 21.7 5.2 26-27 July 1982 21.5 14 286.0 168.9 26.5 26.4 5.9 1-3 July 1982 19.7 15 202.4 119.5 15.3 16.2 4.6 19-21 July 1982 17.1 15 190.9 112.7 14.1 14.5 5.0 25-26 July 1982 19.0 15 228.0 134.6 20.0 20.0 5.3 Mean 18.8 12.8 217.2 128.3 19.8 19.9 5.0 (SD) (+2.0) (+36.1) (_+21.3) (+4.6) (+4.2) (+0.6)

Brood size = 5

Males 24-26 June 1981 20.3 2 209.7 123.8 10.6 11.2 4.6 23-24 June 1981 20.2 3 216.9 128.1 20.8 20.9 4.8 25-26 June 1982 22.5 6 230.4 136.0 19.5 19.6 4.5 29 June to 1 July 1981 18.9 13 172.7 102.0 15.1 15.3 4.1 1-3 July 1982 18.1 14 228.3 134.8 20.8 20.9 5.6 Mean 20.0 7.6 211.6 124.9 17.4 17.6 4.7 (SD) (+1.7) (+5.6) (+23.3) (+13.8) (_+4.4) (+4.2) (+0.6) Females 3-4 July 1981 20.0 2 195.8 115.6 12.4 13.1 4.3 24-26 June 1981 20.3 3 214.9 126.9 13.6 14.1 4.7 25-26 June 1981 19.2 4 258.8 152.8 21.1 21.3 6.0 18-19 June 1981 22.3 5 217.2 128.2 24.9 24.9 4.3 23-24 June 1981 19.5 5 260.9 154.0 27.0 26.6 5.9 10-12 July 1981 18.4 7 236.5 139.6 16.3 16.4 5.7 24-25 June 1981 19.6 11 220.1 129.9 18.6 18.7 5.0 24-25 June 1981 17.7 12 275.2 162.5 17.1 16.8 6.9 5-7 July 1982 19.0 15 198.0 116.9 18.2 18.2 4.6 30 June to 1 July 1982 18.7 15 217.7 128.5 20.4 20.5 5.2 30 June to 1 July 1982 19.0 15 246.2 145.4 20.8 20.9 5.6 Mean 19.4 8.5 231.0 136.4 19.1 19.2 5.3 (SD) (+1.2) (+5.1) (+26.4) (+15.6) (+4.4) (_+4.2) (_+0.8)

Brood size = 7

Males 3-5 July 1982 18.1 14 236.9 139.9 16.4 16.5 5.8 Females 23-24 June 1982 20.1 4 253.9 149.9 30.7 30.3 5.6 21-22 June 1982 20.4 7 235.8 139.2 21.0 21.5 5.1 Mean 20.3 5.5 244.9 144.6 25.9 25.9 5.4 (SD) (+0.2) (_+2.1) (+12.8) (+7.6) (+6.9) (+6.2) (+0.4) 24.6 J of heat/ml CO2(Williams and Nagy 1985). 710 JOSEPHB.WILLraMS [Auk,Vol.-105

300 35

Tree Swallows 30

25o

c 20 200

•0 •50 150 5 10 15 20 25 CO2 Production(ml/h) Average Visits / h Fig. 3. Water influx as a function of CO2produc- Fig. 2. Field metabolismas a function of the av- tion for Tree Swallowswith nestlingson Kent Island, erage visits/h of Tree Swallows on Kent Island, New New Brunswick. Brunswick.Squares represent birds feeding 3 nest- lings;circles, birds feeding 5 nestlings;triangles, birds feeding 7 nestlings. _+1.7 ml O•/(massø-67.h);sparrows = 12.1 +_1.3 ml O2/(massø-67-h);t = 3.3, P < 0.01), but below the TNZ, they consumedO2 at a higher rate h) (n = 25, r• = 0.21, P < 0.02). Nest visitation thansparrows (ANCOVA, ts•ope, = 5.3, P < 0.01). was unrelated to nestling age for either sex For swallows,ml O2/(mass0.•7.h)= 25.9 - 0.51 (males r• = 0.04, P > 0.5, females r2 = 0.02, P > (Ta,øC) (n = 40, r2 = 0.91,P < 0.001);for spar- 0.6). Males averaged7.4 visits/h (SD = 5.0, n = rows, ml O•/(massø.•7.h)= 19.6 - 0.26 (Ta,øC) 7), and females, 9.1 visits/h (SD = 5.6, n = 18). (n = 25, r2 = 0.64, P < 0.001). At an air tem- Waterinflux and effiux.--In general,water in- peratureof 11.5øC,the mean air temperature flux equaled effiux indicating that birds bal- duringDLW measurements,mass independent anced water intake againstwater losses(Tables laboratorymetabolism for swallowswas 20.1 ml 1 and 2). For incubating females,water influx O•/(massø'•?.h)and for sparrowswas 16.7 ml averaged 16.1 +_ 2.2 ml H20/d (Table 1), and O•/(massø.e•.h),a 16.9% difference. The plum- increased to 20.1 _+ 5.0 ml H20/d during the agethickness of swallowsmay be lessthan that chickrearing period (Table2). Water influx cor- of sparrows,which resultsin greaterheat loss. relatedwith CO2production for birdswith nest- During incubation, female Tree Swallows ex- lings (Fig. 3). Water influx (ml/d) = -1.71 + pend lessenergy than when they feed young. 0.09 (ml CO2/h) (n = 25, r• = 0.30, P < 0.001). Common House-Martins(Delichon urbica), Bank Solar irradiancepositively influenced water in- Swallows( riparia), and EuropeanStar- flux, ml H20/d = 14.3 + 0.02 (W/m 2) (Fig. 4; n lings (Sturnusvulgaris) show the samediminu- = 25, r2 = 0.29, P < 0.001). tion in FMR during incubation,and also nest

DISCUSSION 35

Aschoffand Pohl (1970) predicteda BMR of •0 0 1.24 kJ/h for a 21.6 g passefinein its night •, phase.This is within 4% of the value that I have • 25 estimatedrows on Kentfor TreeIsland Swallows. had a restingSavannah metabolicSpar- =• g 20 rateof 86.0 + 8.8ml Odh or 1.73 kJ/h (Williams • •5 o unpubl.; n = 13, mean mass= 18.9 + 1.3). Be- • o o causeTree Swallows were slightly heavier than •0 SavannahSparrows (t = 5.5, P < 0.001), I cal- 1 O0 200 300 400 500 600 culated mass independent measurementsof Irradiance(W/m 2) metabolismby dividing •o• bymass ø.• (Heus- Fig.4. Water influx as a function of irradiance for ner 1985). In the TNZ, swallows had a lower Tree Swallows with nestlings on Kent Island, New metabolicrate than sparrows(swallows = 10.1 Brunswick. October1988] FieldMetabolism of Tree Swallows 711

50- 5 11 40- o

30-

•II 0Tree Swallows ß Say. Sparrows

I I I I o 0 5 10 15 20 25 TreeSwallows SovonnohSparrows Visits to Nest/h Fig. 5. Massindependent field metabolismfor Tree Fig. 6. Mass independent field metabolism as a Swallows and Savannah Sparrows while feeding function of nest visitation rate for Tree Swallows and youngßThe open bar representsmale swallows,bar SavannahSparrows. Elevations but not slopesare sta- with diagonal lines representsfemale swallows, bar tisticallydifferent. For swallows,ml CO2mass ø'67 x h with cross-hatchingrepresents male sparrows, and = 27.7 + 0.34 (visits/h) (ta = 0.26, P = 0.003); for bar with vertical lines representsfemale sparrowsß sparrows,ml CO2mass ø-67 x h = 16.4 + 0.52 (visits/ Lines above bars indicate 95% confidence intervals; h) (r• = 0.24, P < 0.001). numbersabove bars,sample sizeß differencesto the increasedthermoregulatory in cavitiesor boxes(Westerterp and Bryant 1984); costsof swallows. However, swallows spend a Ricklefs and Williams 1984). Savannah Spar- substantialproportion of their day flying, and rows on Kent Island build an open-cup nestand heat producedas a by-productof this activity only the femaleincubates. The FMR of sparrow may substitutefor the heat required for ther- femaleswas equivalent during the incubation tooregulation(Tucker 1968, Palandino and King and early nestling periods(Williams 1987). 1984).Consequently the differencein thermo- Female Tree Swallowsweigh lessduring the regulatory costsbetween swallows and spar- nestling period than during the incubationpe- rows is reduced.Thus, the increasedflight time riod (seealso Westerterp and Bryant 1984,Rick- of swallowsis, to a large extent,responsible for lefs and Williams 1984, Williams 1987). Mass their higher FMR. loss may reflect physiologicalstress from in- The difference in FMR between sparrowsand creasedactivity while adultsfeed their young swallows is not directly attributable to the fact (Hussell 1972).However, knowledge of the time that swallowsfed an additionalnestling. MIFMR when weight declinesis critical in interpreting was higher for swallowsthan for sparrowsper this pattern (Freed 1981). Female swallows lose nest visit (Fig. 6; ANCOVA, ts•ope= 1.82, NS, mass during the incubation period (Williams t,•w•o• = 325.3, P < 0.001). Moreover, when unpubl.). Changes in body massduring incu- sparrowsfed 6 nestlings,their FMR was lower bation in hirundinesmostly reflectchanges in than for swallows that fed 5 (Williams 1987). lipid reserves(Jones 1987) and suggestthat the Hirundines may, in general, have a higher incubation period may be energetically stress- FMR than other birds. I have plotted FMR (kJ/ ful for female Tree Swallows on Kent Island. d) as a function of body massfor 7 speciesof Female sparrows(18.3 g) weigh slightly less aerially foraging birds during the nestling pe- than male (20.0 g) or female (19.4 g) swallows riod (Fig. 7). With the exceptionof Cliff Swal- during the nestling period (ANCOVA, F = 5.2, lows (Withers 1977), all the data refer to DLW P < 0.005). While provisioning 5 young, mass measurementsof FMR. Log(kJ/d) = 1.34 + 0.53 independent values of field metabolism log(bodymass, g) describesthe relationship(r • (MIFMR) (Heusner 1985) for Tree Swallows ex- = 0.78, P < 0.01). For comparison,I plotted the ceededvalues for SavannahSparrows that tend- FMR of 11species of birdsthat are either ground- ed 4 young (Fig. 5; ANCOVA, F = 31.1, P < foraging insectivores,flycatchers, or picivores 0.001).The MIFMR of male swallowswas higher also during the nestling period (Fig. 7). Six of than in malesparrows by 25.6%,and the MIFMR these studies used the DLW method. I combined of female swallows was higher than female flycatchersand ground foragersbecause the for- sparrowsby 38.8%.I attributea portion of these agingroutine of flycatchersoften entails no more 712 JOSEPHB. WILLIAMS [Auk, Vol. 105

500 tios are among the highest thus far reported,

0 aerial farager• ß which may indicate that Kent Island is ener- ß other foragem getically stressfulfor swallows.It would be in- teresting to know if the survival rate of Tree 1 oo Swallows on Kent Island was lower than for

50 swallows from other populations. The influence of weather on the FMR of birds varies. Favorable weather conditions, such as warm, calm days, were associatedwith higher 10 10 20 50 100 levelsof energyexpenditure in CommonHouse- BodyMass (g) Martins (Bryant and Westerterp 1983). Fair weather also was correlatedpositively with a Fig. 7. Field metabolism as a function of body larger number of flying .Thus, house- massfor hirundines (open circles)and other birds of martins spent more time foraging. However, similar size (closedtriangles). Lines are statistically different. (See Appendix for speciesand sources.) foul weathersuch as strong winds causeda sig- nificant increase in the FMR of Black-legged Kittiwakes (Rissa tridactyla; Gabrielsen et al. flight time than the routineof ground-foraging 1987). For Tree Swallows, I found no relation- species(Ettinger and King 1980).The line which ship between FMR and weather. Water influx describesthese data, log(kJ/d) = 0.89 + 0.75 was positively related with irradiance, which log(body mass, g) (r• = 0.87, P < 0.001), lies suggeststhat the foraging successof swallows below the line for aerial foragers (ANCOVA, was higher on clear days, when insectswere t•op•= 1.1, NS, t•,•vatio,= 9.9, P < 0.001). Thus, presumablymore abundant. aerial foragersexpend from 16 to 38% more en- ergy than similar-sizedspecies that employ al- ACKNOWLEDGMENTS ternativeforaging modes. Walsberg (1983) found a statisticallyinsignificant (10%) differencebe- I thank Bob Ricklefs for his continued guidance tween the DEE of aerial foragers (humming- throughoutthe courseof this study.Glen Walsberg, Pat Mock, Stephanie Brown, Paul Tatnet, and C. J. birds and swallows) and that of other birds. Hails generouslycommented on a penultimatever- Powers and Nagy (unpubl.) found a FMR of 32 sion of the manuscript.Dr. Chuck Huntington pro- kJ/d for Anna's Hummingbirds (Calypteanna), vided logisticalhelp while I wason Kent Island, and a value intermediatebetween predictionsof the StephanieBrown, Linda Williams, Ann Kronchie,and 2 equations.These birds were not feedingyoung. Rachel Bereson assisted in the field. P. J. Mock, D. When Tree Swallows fed their chicks more fre- Powers,K. Nagy, and Wes Weathersprovided un- quently, their CO2production increased. Swal- publisheddata. Funds for this projectwere provided lows often spendmore time flying when insects by NSF grant DEB80-21732administered by R. E. are abundant (Bryant and Westerterp 1983). Ricklefs,and by a grant from the JohnStauffer Char- itable Trust. Feeding frequency also was related positively to FMR in CommonHouse-Martins (Bryant and Westerterp1983) and SavannahSparrows (Wil- LITERATURE CITED lianas1987). The number of visits each parent ASCHOFF,J., & H. POHL 1970. Rhythmic variations Tree Swallow made to the nest was unrelated in energy metabolism.Fed. Proc.29: 1541-1552. to nestling age (see also Lombardo 1987). BAKKEN,G. S. 1980. The use of standard operative Drent and Daan (1980) speculatedthat an en- temperaturein the study of thermal energetics ergeticplateau exists approximately equal to 4.0 of birds. Physiol.Zool. 53: 108-119. times BMR for optimal reproductive perfor- BERGER,M., & J. S. HART. 1974. Physiologyand en- mance. Above this level, birds accrue serious ergeticsof flight. Pp. 260-415 in Avian biology, physiological consequences. When raising vol. 4 (D. S. Farner and J. R. King, Eds.). New York, Academic Press. young,Savannah Sparrows and other smallpas- BRYANT,D.g. 1979. Reproductivecosts in the house serines work at levels near 3.0 times BMR (Wil- martin ( urbica). J. Animal Ecol. 48: 655- liams 1987). In contrast, FMR/BMR ratios for 676. Tree Swallows during the nestling period ex- -, C. J. HAILS,& P. TATNER.1984. Reproductive ceededthe hypotheticallimit, apparentlywith- energeticsof two tropical species.Auk 101: out immediate adverseconsequences. These ra- 25-37. October1988] FieldMetabolism ofTree Swallows 713

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Starlings(Sturnus vulgaris) during the nesting , & K. A. NAG¾. 1984. Validation of the dou- cycle. Auk I01: 707-715. bly-labeledwater techniquefor measuringen- ROSENBERG,N., B. BLAD,& S. VERMA. 1983. Pp. 1- ergy metabolismin SavannahSparrows. Physiol. 495 in Microclimate.New York, John Wiley and Zool. 57: 325-328. Sons. , & ---. 1985. Water flux and energetics SCHMIDT-NIELSEN,K. 1979. Animal physiology.New of nestingSavannah Sparrows in the field. Phys- York, CambridgeUniv. Press. iol. Zool. 58: 515-525. TUCKER,V.A. 1968. Respiratoryexchange and evap- , & A. PPaNTS.1986. Energeticsof growth in orativewater lossin the flying Budgerigar.J. Exp. nestling Savannah Sparrows:a comparisonof Biol. 48: 67-87. double-labeledwater and laboratoryestimates. U•rER,J. M. 1971. Daily energyexpenditure of free- Condor 88: 74-83. living Purple Martins (Prognesubis) with a com- W•NN, H. 1949. Nestling mortality rate of the Tree parison of two northern populationsof mock- Swallow. Bowdoin Sci. Sta. Bull. II: 19-20. ingbirds (Minus polyglottus).Ph.D. dissertation. W•TH•RS,P. C. 1977. Energeticaspects of reproduc- New Brunswick,New Jersey,Rutgers Univ. tion by the . Auk 94: 718-725. --, & E. A. LE FEBVRE.1973. Daily energy ex- penditureof PurpleMartins ( subis) during the breeding season:estimates using D2•80 and APPENDIX. Speciesand sourcesfor aerial and other time budgetmethods. Ecology 54: 597-604. foragers(see Fig. 7). WALSB•RG,G. E. 1977. Ecologyand energeticsof contrastingsocial systemsin Phainopeplanitens For hirundines (open circles),species and sources (Aves:Ptilogonatidae). Univ. Calif. BerkeleyPubl. are: (Ripariariparia), 12.9 g, Westerterp Zool. 108: 1-63. and Bryant 1984; (Hirundotahitica), 1978, Brood size and the use of time and 13.9g, Bryantet al. 1984;House Martin, 18.1g, Hails energyby the Phainopepla.Ecology 59: 147-153. and Bryant 1979;European Swallow (Hirundirustica), 19.1 g, Westerterp and Bryant 1984; Tree Swallow, --. 1983. Avianecologicalenergetics.AvianBiol. 8: 161-220. 19.7 g, this study; Cliff Swallow (Petrochelidonpyr- rhonota),24.6 g, Withers 1977;, 49.0 g, WESTERTERP,K. R., & D. M. BRYANT.1984. Energetics Utter and Le Febvre 1983. of free-existence in swallows and martins (hir- Forother birds (closed triangles), species and sources undinidae)during breeding: a comparativestudy are:Willow Flycatcher(Epidonax traillii), 12.6 g, Ettin- using doublelabeled water. Oecologia62: 376- ger and King 1980;Savannah Sparrow, 17.0 g, Wil- 381. liamsand Nagy 1985;Savannah Sparrow, 19.3 g, Wil- W•LLL•VtS,J. B. 1985. Validation of the doubly-la- liams 1987;Yellow-eyed Junco (Junco phaeonotus), 19.5 beledwater techniquefor measuringenergy me- g, WesWeathers, pers. com.; Phainopepla (Phainopepla tabolismin starlingsand sparrows.Comp. Bio- nitens),24.0 g, Walsberg1978; Western (Sialia chem.Physiol. 80A: 349-353. mexicanius),27.5 g, P. J. Mock, pers. com.; White- 1987. Field metabolismand food consump- crownedSparrow (Zonotrichia leucophrys), 28.7 g, Hub- bard 1978; Blue-throated Bee Eater (Meropsviridis), tion of SavannahSparrows during the breeding 33.9 g, Bryant et al. 1984;Mockingbird (Mimuspoly- season. Auk 104: 277-289. glottos),46.7 g, Utter 1971;Starling, 75.5 g, Ricklefs --, & H. HANSELL.1981. Bioenergeticsof captive and Williams 1985;Pied Kingfisher(Ceryle rudis), 76.0 Belding'sSavannah Sparrows (Passerculus sand- g, Reyer and Westerterp1985. wichensisbeldingi). Comp. Biochem.Physiol. 69A: 783-787.