THE ENERGETIC SIGNIFICANCE OF HUDDLING BEHAVIOR IN COMMON BUSHTITS (PSALTRIPARUS MINIMUS)

SUSAN B. CI-IAPLIN 1 Departmentof Biology,Occidental College, Los Angeles, California 90041 USA

AnSTRACT.--Thedaily energeticsof a very small ,the CommonBushtit (Psaltri- parusminimus), were examinedby measuring24-h existencemetabolism, activity, and noc- turnal metabolicrate. Bushtitsconsumed 80% of their body mass(5.5 g) in mealwormsper day at 20øC.A lower energy intake than this resulted in marked weight loss (0.543.8 g), slighthypothermia upon exposure to 10øCfor 4 h (To= 38.6øC),and a higherdiurnal activity level than well-fedbirds. Birdshoused in pairsor largergroups spent portions of the day perchingtogether and spentall of the nocturnalperiod huddled in a tight mass.These were alsoless active diumally than isolatedindividuals and had lower nocturnalmetabolism; the metabolismof paired birds was 79% of that of singleindividuals at 20øC.The energy savingsgained by the gregariousnature of this diminutive ,reflected by the dimin- ished cost to an individual of being a member of a flock, may be integral to its survival during periodsof food scarcityor inclementweather. Received10 August1981, accepted12 December 1981.

THE North American Common Bushtit [Psal- 1921, Bent 1946). Such gregarious behavior triparusminimus (Paridae)] is one of the small- may be a strategy for ameliorating the roost est passerine species(5.5 g) in the world. It microclimate. Thus, for bushtits, at least part rangesfrom coastalsouthern British Columbia of the solution to the problem of excessiveheat to northern M•xico and may encounter loss in the cold may be found in their social subfreezingtemperatures on winter nights in behavior. The purposesof this study were: (1) parts of its range (Bent 1946, Smith 1972). to determine the energeticsignificance of the Bushtits' diminutive size and consequenthigh huddling behavior in bushtits, and (2) to mea- rate of heat loss make the maintenance of a sure the extent to which bushtits use nocturnal constantbody temperature on cold nights po- hypothermia or reduce their activity to limit tentially energeticallyexpensive. Some small their energy expenditures. ((15 g) parid species,such as the Black-capped Chickadee(Parus atricapillus) and Willow and METHODS Siberian tits (P. montanusand P. cinctus), con~ Six bushtits were captured in mist nets during serveenergy at low temperaturesby nocturnal November 1974 and six more in June 1975 in a syc- hypothermia (Haftorn 1972, Chaplin 1976, amore-oakgrove outsidethe Moore Laboratoryof Grossmanand West 1977). Other species,such Zoologyat OccidentalCollege, Los Angeles,Califor- as Long-tailed Tits (Aegithaloscaudatus) and nia (34ø latitude). They were weighed immediately bushtits, which are ecologicalequivalents on after capture (• = 5.54 g + 0.07 SE in November and different continents (Austin and Smith 1972), ß = 5.51 g + 0.04 SE in June), color-bandedfor in- huddle together when exposedto cold (Miller dividual recognition, and placed in a 0.5-m3 wire screencage supplied with perchesand with cedar 1921, Bent 1946, Lack and Lack 1958, Smith shavingson the floor. The birds were fed mealworm 1972).Bushtits are extremelygregarious during (Tenebriomolitor) larvae and pupae ad libitum and the nonbreeding season.They may travel in were suppliedwith drinking water (which they were flocks of 20-70 birds in the daytime, and all never observedto use) from a dish on the cagefloor. enter the same tree to roost at night (Miller The cage was placed in a walk-in environmental chamber regulated at a constant 20 + 2øC and a 12L:12D photoperiod. The chamber had a one-way view port through which the birds were observedat • Present address:Division of BiologicalSciences, intervalsduring the day and at night with the aid of University of Missouri, Columbia, Missouri 65211 a low intensity red bulb near the cage. USA. In order to calculatethe energy expendituresand

424 The Auk 99: 424-430.July 1982 JvL¾1982] Daily Energeticsof Bushtits 425 energy intake of single and grouped individuals, I hoveringattempts. Active metabolism was estimated measuredbasal metabolismand cloacalbody tem- at 2.0 times BMR, becausethe birds were hopping peraturesat night over a 10-30øCtemperature range, aroundthe cageabout 50-75% of the time. In addi- amount of food eaten and feces produced per day, tion, it was assumedthat birds were usually in an amountof activity during the light period, and body absorptivecondition during the light period, be- weightchanges over a 24~hperiod. Nocturnal resting causethey were fed at frequent intervals and thus metabolism was measuredby an open-flow system, probably had an R.Q. of 1.0. Hence, the energy utilizing a Gelman pump to push air through a col- equivalentof metabolicexpenditure during this pe- umn of drierite to the metabolism chamber (500 cc/ riod would be 21.31joules/cc O2 (Gordon1977). Diur- min for one in the chamber, 700 cc/min for two nal metabolicexpenditure was then calculatedas fol- birds). A 4-1 double-lipped paint can with a wire lows: screenfloor over a layer of mineral oil was used as Diurnal Expenditure = Energy expended in ac- the metabolic chamber. Air exiting the chamber tivity + Energy expended passed through a column of a drierite-ascaritemix at rest (3:1) before entering the sample cell of a Beckman D.E. (joules)= [activity(h). (MRra'2.0) E-2 paramagnetic oxygen analyzer at 100 cc/min. + rest(h)'(MRr•' 1.2)] Birds were taken from their cageat the beginning of '21.31. the nocturnalperiod, weighed, and placed individ- ually or in pairs in the metabolic chamber, which Nocturnal metabolism was calculated from the MR- was then placed in a temperature-controlled incu- Ta regressioncurve as follows: bator set at one of the test temperatures.Incubator Nocturnal Expenditure (jotdes) = MR7,•' 12 h.21.31. and metabolic-chamber temperatures were moni- tored over the next 3-4 h with a YSI telethermometer. Adding the diurnal and nocturnalexpenditures then Readingsof oxygencontent of exit air were taken at gives the total predicteddaily expenditureat a par- 30-min intervals for the first 2-3 h of the experiment ticular temperature. and at 10-min intervals during the last hour. Birds Ingestion and egestion of single birds were mea- were then removed from the chamber, and cloacal or sured concurrentlywith activity and converted to esophagealtemperature was takenas quicklyas pos- energeticterms to give an estimate of daily energy sible (30-60 s) by insertinga 40-gaugeYSI thermistor expenditure by measurementof existencemetabo- probe to a standarddepth (0.7 cm into the cloacaor lism. Approximately 1.5 g of medium-sized meal- 2.0 cm into the esophagus).The bird was weighed worms were presentedto a bird at regular intervals again before being returnedto the cage.The highest four times a day, and the feedingperiods were noted sustainedreading of oxygenconcentration of exit air on the activity record. Mealworms were weighed to (correctedto STP and for N2 expansionafter CO2 and the nearest 0.1 g before each feeding, and all meal- H20 vapor removal) was used to calculate oxygen worms and remnants remaining from the previous consumptionin cc O•'g •.h • accordingto the ap- feedingwere alsoweighed. The bird was.weighed propriate formulae in Depocas and Hart (1957). at the beginning of the feedingtrial (0800)and again Activity of single and grouped birds (n = 5) was 24 h later. A large sheet of glassinepaper placed in recordedcontinuously for 24 h at 20øCin a 0.25-m3 the bottom of the cage permitted easy removal of cage via a treadle-activatedmicroswitch connected feces, which generally accumulateddirectly under to an Esterline-Angusevent recorder.When inactive, the treadle perch. After removing feeding remnants the birds tended to perch on the treadle rather than (heads and exoskeletons),I placed the fecesin a vac- the side of the cage, causinga downward deflection uum drying oven at 45øCand weighed them to the in the re•ord. Thus, one could calculate the number nearest0.1 g after 24 h. The dessicatingenvironment of minutes spentat rest from the activity record.The and small mass involved (<0.5 g) insured that the sum of minutes of pen markings(treadle movement) samples dried very rapidly and that there was no divided by the total 720-min light period gave the masslost to bacterial decay. percentageof activity per day. The energy ingested and that remaining in the Diurnal metabolism was estimated from the activ- feces were determined in the following way. Three ity record by using the assumptionsthat diurnal samplesof 1.0 g of mealwormswere weighed, dried metabolism of resting birds is approximately20% to a constant mass, reweighed, and then ignited in higher than nocturnalbasal metabolism (Aschoff and a Parr adiabatic bomb calorimeter to determine the Pohl 1970) and that diurnal metabolism of active energy value of mealworms.The total mass of in- birds is 1.70-2.0 times the nocturnal basal metabo- gested mealworms mtdtiplied by their percentage lism at a specifictemperature (Brenner 1965, Hains- dry weight (32.3) and energy equivalent (25.87 kJ/g worth et al. 1977, Beuchat et al. 1979). Bushtits were dry weight) yielded the total ingested energy. The very active throughout the day, but their activity total dry mass of feces multiplied by their energy consistedalmost entirely of short-distancehops from equivalent(13.98-17.92 kJ/g dry weight) yielded the one side of the cageto the other rather than flight or total egestedenergy. The difference of ingestedand 426 Sus^N B. CHAPLIN [Auk, Vol. 99

15 ber and June. This might be expected,because the average monthly temperature in June was 18.9øC and that for November was 16.8øC 12 (NOAA 1974-1975). Thus, the data were com- ee MR=-0.36T a ß 14.64 bined to give one linear regressionof metab- olism on temperature: M = 0.36T(• + 14.64. This regression extrapolatesto 40.7øC at zero metabolism,which is approximatelythe body temperature measured after birds were ex- posed to 25 and 30øC:• = 40.2 + 0.8øCSE (n = O 6. 7). Body temperature of bushtits exposed to MR= - 0.32T a + 12.3 o 10øCfor 4 h averaged38.6 _+1.6øC SE (n = 8) and was not significantlylower than that of

o birds at thermoneutrality. Oxygen consumptionof two bushtits in the same chamber was markedly lower than that of single bushtits, when compared on a per 0 10 2o 3o gram basis (Fig. 1). Attempts to measureme- TaøC tabolism of more than two birds in the same Fiõ. 1. Relationship of nocturnal metabolism, chamber always resulted in highly spurious measuredas oxygen consumption,and temperature results. The birds never settled down and cer- in single (0) and paired (C)) bushtits. The standard tainly did not huddle, even after 3-4 h. At 10øC error of the regression(s,.•) for the single bushtits the metabolic rate of paired birds was signifi- was 0.18 and for paired bushtits was 0.11. cantly lower than that of isolated birds (P • 0.05, Mann-Whitney test). There were no significantdifferences at higher temperatures. egestedenergy, metabolizedenergy, was compared The metabolism of a pair of birds as a function with the predicteddiurnal metabolicexpenditure cal- of ambient temperature was described by the culated as described above. If the results of these equation: M = 0.32T• + 12.30. Although the two calculations were similar, one could then exam- slope of the pair regressionwas less than that ine the relative importance of each of the compo- of single birds, the two regressionlines were nents of daily expenditureto the bird's energybud- not significantlydifferent by a t-test of slopes. getand comparecosts of daily maintenancefor single, Nevertheless, these results suggestthat chem- paired, or multiple-caged individuals. ical thermogenesis(heat production) of a par- ticular individual is less at all ambient tem- RESULTS peratureswhen that individual is a member of Nocturnal metabolism.--The lowest rate of a group than when it is alone. Thus, some de- oxygen consumption of bushtits was 3.96 cc gree of energy conservationis obtained by O2'g •'h -• at 30øC, which closely approxi- huddling. mates the resting standard metabolism pre- Diurnal metabolism.--Bushtits,like their par- dicted for a 5.5-g bird (4.14 cc O2'g-•'h -•) by id relatives chickadees and titmice, are con- the Aschoff-Pohlmetabolism-weight regression stantly active in their natural environment. In equation (Aschoff and Pohl 1970). It was as- captivity a bushtit kept singly in a cage large sumed that metabolism at this temperature enough to permit flight made continuous representedthe basalrate, as 30øCis probably short-distancehops around the cage, usually in the bushtit's thermoneutral zone based on calling continuouslyas it moved. Only after similar findings in other speciesof this size feeding did the birds perch for any length of living in roughly the sameclimate [e.g. Verdin time. As a consequenceof this behavior, five (Auriparusfiaviceps), Goldstein 1974; Anna's singly caged bushtits were active an average Hummingbird (Calypteanna), Lasiewski1963]. of 55% (_+8% SE) of the light period. Adding There was no significantdifference between otherbirds to the cageseemed to calmthis fer- the basal rates of metabolism or slopesof the vent searchingbehavior and reduce the activ- MR-T,, regressionof birds capturedin Novem- ity time, even though the likelihood of acti- JuLY 1982] Daily Energeticsof Bushtits 427

SINGLE BUSHTITS TRIAL I G2' B2'

B2 G2 5 BUSHTITS• * DAY,[,

• O0 t 10I 12I 14I 16I 1•00,OFF TIME Fig. 2. Daily activityrecords of singly-housedand groupedbushtits. * indicatesfeeding times. ß indi- catestimes of lightson and off in the environmentalchamber. In Trial1 for singlebushtits, both individuals (G2 and B2) were given enoughfood for them to maintaintheir weight. In Trial 2 for the samebirds, one feedingperiod was skipped,and the daily intake was inadequateto maintainweight. vating the perch microswitch was increased to calculate these data had a mean mass of 5.5 with multiple birds per cage.Five birds in a g and maintainedthat mass +0.2 g over the cage together activated the perch only next 24 h. The calculateddaily metabolicex- 43.5% + 5.3 SE of the daytime(mean of 4 con- penditurefor a single5.5-g bird, 26.5 kJ (Table tinuousdays of recording).The most notable 1), based on the assumptionsgiven in the decreasein activityin groupedbirds tookplace methods, was less than the energy metabo- afterfeeding. Whereas single birds perchedfor lized. Thus, the estimated metabolic expendi- 10-20 min after eating most of the mealworms ture maybe too conservativebut is still useful introduced,grouped birds often perchedfor to predict the energeticconsequences of tem- 30-50 min, especiallyduring the middle of the perature,food supply, or amountof activityon light period (1200)(Fig. 2). In fact, even at the the individual's energy balance. moderate temperature of the feeding experi- In four feeding trials insufficientfood was ment (20øC),the birds sat closetogether on the (inadvertently)presented during the light pe- perch, and some exhibited a typical sleeping riod, and the birds lost 0.5-0.8 g. In two cases, posture. the samebirds maintained their weight during Daily energetics.--Bushtitskept at a constant a feedingexperiment 3-4 daysearlier, and this 20øC consumed a mean of 35.17 kJ + 1.26 SE serendipitous experiment provided an inter- mealworms per day and metabolized 31.40 estingcomparison with the normalenergy bal- kJ + 1.26 SE of that intake. The six birds used ance situation (Table 2). As a group, the four

TABLE1. Estimateddaily energyexpenditures of birds housedsingly vs. in pairs for individualsweighing 5.5 g kept under 12L:12Dand 20øCconditions. See text for explanationof calculations.

Mnocturnal Mcliuraal mactivitu minactivitu Total 0= con- Time Time energy sumption active inactive expended (ccO• 'g-•. h-•) kJ (h) kJ (h) kJ (kJ) Singly 7.44 9.88 6.50 11.05 5.50 5.61 26.50 Paired 5.90 7.83 5.50 7.41 6.50 5.32 20.56 428 SUSANB. CHAPLIN [Auk, Vol. 99

TAnrE2. Metabolizedenergy compared with estimateddaily expenditurefor two birds fed an amount of foodadequate to maintainweight (+0.1 g) in onetrial andan inadequateamount of foodin anothertrial.

Energy intake in kJ (measured) Energy expenditure in kJ Feces (calculated) + Food urine Metabolized M,oc M,•ct M,.es, Total Adequate food B-2 (5.3--5.2) 24.45 3.10 21.35 8.54 9.29 5.07 22.90 G-2 (5.7-5.8) 38.27 4.48 33.79 9.29 10.17 5.27 24.73 Inadequate food B-2 (5.5-5.0) 20.31 2.68 17.63 8.50 14.15 2.14 25.04 G-2 (5.8-5.0) 20.31 2.93 17.38 8.75 15.03 1.93 25.71

birds ingested and metabolized less energy presumably, the cost further decreasesas the than they required for daily maintenance,and rate of heat loss decreasesin larger groups of someof them alsoexpended more energy diur- huddling individuals. The diurnal costsfor a nally than those individuals fed an adequate memberof a groupmight alsobe reducedbe- amount by having a higher percentageof ac- low thoseof a singleindividual, perhapsby a tivity per day (79% vs. 55%) (Fig. 2). Thesetwo reductionin activity time and by daytime hud- factorsalone probablyaccounted for the large dling behavior. Although a single individual energydeficit and marked weight lossin these may be able to balanceits energybudget under birds. The extent to which these individuals used the conditionsof adequatefood or moderate nocturnal hypothermia and decreasedmetab- temperaturesused in this study, the real en- olism to balance their energy budget was not ergeticadvantage of this contactsocial behav- tested. Body temperaturesof birds exposedto ior is to increasethe survival time during pe- 10øC, however, even of individuals weighing riods of inclement or cold weather or low food less than normal, were only 2-3øC lower than availability. The two bushtits fed an inade- daytime body temperatures.Hence, decreased quate amount of food (Table 2) metabolized nocturnal metabolism seems to be a less im- only 17.6 and 17.4kJ/day and lost0.5-0.8 g but portant avenue of energy conservation in could have almost maintained their weight bushtits, at least during short-term cold ex- during that period by having just one other posure. bird in the cage. Their expenditures would then have been approximately20.6 kJ/day(Ta- DISCUSSION ble 1), comparedto the 25.0 and 25.7 kJ/day estimated from their daily activity record. Communal roosting or decreasedindividual Brenner (1965) found that the survival time of distance (sensuHediger 1950) is not uncom- singly housed Starlings at 4øC was extended mon among small birds, especiallyduring un- from 1 day to 3 by placingthem in groupsof seasonably cold weather (L6hrl 1955, Kos- four. kimies 1961, Grubb 1973, White et al. 1975, The gregariousbehavior of a flockof bushtits Meservy and Kraus 1976,Beal 1978,McNicholl is importantnot only for nocturnalenergy con- 1979). The physiological,especially the ener- servationbut perhapsfor reductionof daytime getic, advantageof this behavior, however, has expendituresand maximization of energy ac- been demonstratedonly for Starlings(Sturnus quisition as well. Searchintensity for food by vulgaris; Brenner 1965), which, at a body an individual could be reducedby its being a weight of 70-80 g, should be consideredlarge member of a flock the individuals of which .Communal roostingenables bush- communicate information about the location tits to reduce both their nocturnal maintenance and density of resourcesand the presenceof cost and their diurnal inactive cost. The noc- predators(Murton 1971). Flock foraging is the turnal cost at 20øC for a member of a pair of typical mode of feeding among parid species bushtitsis 79% of that of a single bird, and, who are often the leaders of mixed insectivore- JULY1982] DailyEnergetics of Bushtits 429 speciesflocks (Gibb 1954; Morse 1970, 1978; heat loss(slope of singlebird metabolism-tem- Austin and Smith 1972). The constancyin size peratureregression, Fig. 1) was almostexactly of bushtit flocksthroughout the nonbreeding that predicted for a 5.5-g bird, 0.37 cc season,however, and the high degreeof relat- O2'g •.h •.C ø •, by the Lasiewskiet al. (1967) ednessof their membersare unusualamong the conductance-weightregression. Verdins, Black- Paridae, and Ervin (1977)suggests that these cappedChickadees, and some Old World tit- characteristicsstrengthen flock cohesiveness mouse speciesall have a conductiveheat loss and may be valuable in the exploitationof lo- that is lower than predictedfor their body mass cally abundant but patchy resources.It has and denserplumage than other birds of similar been demonstratedthat flock foraging enables size, 10.7-11.5% of body mass(Hissa and Pa- individuals to forage more efficiently, i.e. lokangas 1970, Goldstein 1974, Chaplin un- greater energy is consumedfor the cost nec- publ. data). These speciesare continuallyex- essaryto obtain it, and less energy is devoted posed to severe cold during the winter, to detectionof predators(Murton 1971, Cody however, whereas bushtits rarely encounter 1974, Powell 1974). This may mean that less freezingtemperatures, especially in the south- energy is expendeddaily, and thus, in turn, ern part of their range, where this study was lessfood is required for maintenance.The en- conducted. Nevertheless, the extent to which ergetic savings obtained by the social nature huddling behavior can ameliorate the local of this species,in fact, reinforcestheir social- microenvironmentis impressiveand obvious- ity. The diminished costof being a member of ly is integral to survivalduring suddeninclem- a flock translatesinto the supportof more in- ent weather. dividuals by the resourcesin a given area. ACKNOWLEDGMENTS Thus, there is positive feedback for mainte- nanceof a flockthat roostsand foragestogether This studywas greatlyfacilitated by supportfrom to minimize their individual costs. White et al. the Departmentof Biologyat OccidentalCollege, Los Angeles,California and the generousloan of equip- (1975)described a similar responsein Sociable ment from M. L. Morton. Carol A. Beuchat assisted Weavers (Philetairussocius) in their winter des- with collectionof someof the data. I am grateful to ert environment. S. J. Chaplin, S. Haftorn, G. C. West, and anony- The necessityof such a social strategy to a mous reviewers for constructive comments on the bird as small as the bushtit is obvious when manuscript. one realizesthat a single individual must con- sume about 80% of its body weight daily in LITERATURE CITED energy-rich insectsjust to maintain itself at ASCHO•, J., & H. POHL.1970. Rhythmic variations 20øC and probably close to or greater than in energymetabolism. Fed. Proc. 29: 1541-1552. 100% of its body weight at lower temperatures. AUSTIN,G. T., & E. L. SMITH. 1972. Winter foraging The burden on food acquisition may make ex- ecologyof mixed insectivorousbird flocksin oak istenceat low temperaturesuntenable for sin- woodland in southern Arizona. Condor 74: 17- gle individuals as smallas bushtits. 24. Communal roosting may represent one of BEAL,K. G. 1978. Temperature-dependentreduction of individual distancein captive House Spar- the first lines of defenseagainst cold in many rows. Auk 95: 195-196. species.Bushtits, however, do not appear to BENT, A. C. 1946. Life histories of North American utilize other energy conservationstrategies to jays, crows and titmice. U.S. Natl. Mus. Bull. the same extent as their parid relatives.They 191: 438-455. do not roost in holes or old nests, as do chick- BEUCHAT, C. A., S. B. CHAPLIN, • M. L. MORTON. adees, titmice, and Verdins (Bent 1946, Gold- 1979. Ambient temperatureand the daily ener- stein1974), although they do roostcommunally geticsof two speciesof hummingbirds,Calypte in dense branches as shelter from radiative and anna and Selasphorousrufus. Physiol. Zool. 52: convectiveheat loss (Bent 1946). Their body 280-295. BRENNER,F. J. 1965. Metabolism and survival time temperaturefalls only slightly upon exposure of grouped Starlings at various temperatures. to coldor followingmarked weight loss.Thus, Wilson Bull. 77: 388-395. they do not appear to utilize energy savings CHAPLIN,S. B. 1976. The physiologyof hypothermia gained by hypothermiaor torpor as do chick- in the Black-cappedChickadee, Parus atricapil- adeesand titmice (Haftore 1972,Chaplin 1976). lus. J. Comp. Physiol. 112:335-344. They apparentlydo not have any denser than COD¾,M. L. 1974. Optimization in ecology. Science normalplumage to retard heat loss;conductive 183: 1156-1164. 430 SUSANB. CHAPLIN [Auk, Vol. 99

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