168 SHORT COMMUNICATIONS

negatively correlated with hatch date in Black characteristicsand body reservesof neonateRoss ’ Brant. Ecology 72:496-502. and Lesser Snow Geese. Condor 97:970-984. SEDINGER, J. S., P. L. FLINT, AND M. S. LINDBERG. WEBB, D. R. 1987. Thermal tolerance of avian em- 1995. Environmental influence on life history bryos: a review. Condor 89:874-898 traits: growth, survival, and fecundity in Black WILSON,S. F., AND N. A. M. VERBEEK. 1995. Patterns Brant (Branta bernicla). Ecology 76:2404-2414. of Wood Duck nest temperaturesduring egg-lay- SLATTERY, S. M., AND R. T. ALISAUSKAS. 1995. Egg ing and incubation. Condor 97:963-969.

The Condor 100:168-171 0 The CooperOrnithological Society 1998

NOCTURNAL VARIATION IN BODY TEMPERATURE OF GFUFFON ’

OFER BAHAT~ AND ITZHAK CHOSHNIAK Departmentof Zoology, Tel-Aviv University,Ramat-Aviv 69978,

DAVID C. HOUSTON Applied OrnithologyUnit, Graham Kerr Building, Glasgow University,Glasgow, G12 8QQ, Scotland, U.K.

Abstract. The variation in body temperatureover periods of food deprivation as a result of irregular 24 hr was measured by implanting temperaturemea- feeding or food shortage (Hatch 1970, Larochelle et suring radio transmittersin the abdominal cavity of six al. 1982, Chaplin et al. 1984). captive Griffon Vultures (Gypsfulvus). Body temper- Griffon Vultures (of the genus ) are a group of ature was measured when the were under three large birds which might be particularly expected to different feeding regimes: within 24 hr of feeding have developedadaptations for conservingenergy. Be- (while digesting), 2-3 days after feeding (post-absorp- ing obligatory ,they are totally dependent tive state), and 9.5-10.5 days after feeding (food de- on finding dead , which are an unpredictable prived). For all birds, nocturnalbody temperaturewas and irregular food supply (Houston 1974). Radio te- significantly lower than diurnal body temperature.The lemetry tracking in Israel has shown that Eurasian decline in body temperatureat night was significantly Griffon Vultures (Gypsfulvus) regularly withstandpe- greaterin food-deprivedbirds, which at 10.5days post- riods of 7 to 10 days between successive feedings (Ba- feeding had drovved bv 4-6°C. We suavestthat this is hat et al. 1993). We examined the hypothesis that in an adaptationtdpeduce energy requirem&ts of Griffon order to decrease the metabolism needed for mainte- Vultures during periods of food shortage. nance during a prolonged fast, the Eurasian Griffon reducesthe gradient between ambient temper- Key words: ambient temperature,body core tem- ature (T,) and Tb by decreasingits T,. We also inves- perature, daily temperature variation, food depriva- tigated the daily T, variation of Griffon Vultures and tion, GrifSonVulture, Gyps fulvus. consideredwhether the extent of nocturnaldrop in T, is influenced by their plane of nutrition. Birds usually show a daily variation in body core tem- perature (T,,), with maximum temperaturesoccurring METHODS during the period of activity and minimum tempera- Four immature (between 2 and 4 years old) and two tures occurring during the period of inactivity (Calder adult birds (over 6 years old) were used in this study. and King 1974, Aschoff 1982). In small diurnal birds, All were hatched in captivity or had been in captivity the nocturnal drop in T, is known to be greater in pe- for over 3 years and were accustomedto handling. riods of food shortage (Stuebe and Ketterson 1982, Birds were kept in individual outdoor cages (2 X 4 X Hohtola et al. 1991, Waite 1991) or exposure to cold 2 m) at the Zoological Garden, Tel-Aviv University. stress conditions (Saarela et al. 1989, 1991). In these Experiments were done between 29 July and 13 Sep- situations,nocturnal drop in T, is commonly used to tember 1993 (summer), when ambient temperature(T,) conserve energy (Reinertsen 1983). Nocturnal drop in ranged from 18.7”C to 35.2”C. Average (? SD) T, dur- Tb also has been demonstratedin several species of ing the experimentswas 21.0 5 3.3”C. The birds were birds of prey, which are often exposed to extensive not exposed to T, exceeding the limits of their ther- moneutral zone (Bahat 1995), therefore exposure to heat or cold stresswas avoided. All birds were exposed ‘Received 17 October 1996. Accepted 7 October to natural light/dark cycles. 1997. T, was measuredby implanted transmitters(model * Current address: Faculty of Aerospace Engineer- TM-Disc, Mini-Mitter, Sunriver, Oregon). Each trans- ing, Technion-Israel Institute of Technology, Haifa mitter weighed 13.5 g, measured34 mm in length and 32000, Israel, e-mail: [email protected] 18 mm in diameter, and had a 6 month battery life. SHORT COMMUNICATIONS 169

The transmitterswere implanted in the abdominalcav- RESULTS ity through a 3-cm-long incision in the abdominalskin The six experimental Griffon Vultures showed various under general anesthesia,using a combination of Xy- degreesof variation in T, between day and night, de- lazine (average dose of 0.66 mg.kg-i) and Ketamine pending upon the durationof food deprivation(Fig. 1). (average dose of 10 mg.kg-I). The incision was su- Figure 1A shows that while digesting food, birds had tured and two weeks were allowed for recovery. Each an averageT, variation of 1.8 ? 0.4”C, and their max- transmitter was calibrated in a controlled temperature imum T, range was 36.6-40.6”C, with average maxi- bath prior to the implantation and after the end of the mum T, of 39.7 ? 0.8”C and average minimum T, of experiment, at 1°C intervals from 33°C to 43°C. Mea- 37.9 2 0.8”C. Figure 1B shows that when birds were surementaccuracy was 5 0.2”C. A regressionequation in the post-absorptivestate, their average T, variation was calculatedfrom the calibration curve to transform increasedto 2.5 2 O&C, and maximum T, range was the pulse repetition frequency into body temperature 35.5-40.4”C, (average maximum T, of 39:3 +.8”C, data. Calibration regressioncoefficients (r*) varied be- average minimum T, of 36.8 5 0.7”C). Figure 1C in- tween 0.9924.999. Comparative calibrations of each dicate; that food deprived birds showed still greater transmitterbefore and after the experimentsshowed no average T, variation of 3.0 2 0.7”C, with a maximum significant drift in the transmitter data. T, (in the T, range of 35.3-39.9”C. shade) was measured using a copper-constantan2.4 There was a significant increasein the maximum T, mm gauge thermocouplewith a Wescor TH-65 digital variation shown by birds as they were in more ad- thermometer with measurementaccuracy of ? O.l”C. vanced stages of food deprivation (ANOVA, F,,5 = All average T, data in this paper are given 2 SD. 19.1, P < 0.001). This was not the result of a change Birds were supplied with drinking water ad libitum, in the averagemaximum daily Ts, which did not differ and Turkey meat was provided as food during the pe- significantlybetween birds in different feeding regimes riod of experiments.T, of the birds was recordedevery (F2,5 = 0.58). However there was a significantdecrease hour through a 24-hr period. Three different experi- in T, at night, with the average minimum T, dropping ments were done: First, body temperature was mea- to lower levels when birds were deprived of food for suredin the 24-hr period following feeding. Birds were 10 days (F2,5 = 29.8, P < 0.001). allowed to eat ad libitum. Griffon Vultures have large If we consider the effect of T, on the average T,, crops, which can hold up to 1.5 kg, and it takes ap- there was a significant correlation (r = 0.93) only proximately 34 hr for this quantity of food to pass when birds were deprived of food (F2,5 = 9.1, P < through the alimentary tract (Houston and Cooper 0.01) (Fig. 2). Birds, therefore, reacted to food depri- 1975). The 24 hr period following feeding therefore vation by increased T, variation, which resulted from representsthe period during which digestion occurred. a greater nocturnal decreasein T,. Second, birds were monitored from 48 to 72 hr after having been fed. This period covers the post-absorp- DISCUSSION tive state, when digestion is no longer taking place. Body temperaturevariation in Griffon Vultures under Finally, birds were deprived of food for up to 10 days outdoor ambient temperaturesmaintained a rhythmic until their next feeding, and temperaturereadings were circadian pattern and showed a diurnal cycle. T, fell taken from birds at the end of this period-that is from at night in all conditions,but more so when birds were birds that had not received any food for 9.5 to 10.5 deprived of food. days. We call this the food deprivation state. The av- Circadian cycles comparable to those observed in erage (t SD) body mass of the six birds in the post- the Griffon Vulture have been described in other rap- absorptive state was 6,580 5 890 g, and in food de- torial scavengers:among Old World vultures, T, in prived birds it was 5,730 ? 790 g. Each was wild African White-backed Vultures (Gyps africanus) weighed daily without handling, using a wooden perch (averagebody mass 5.3 kg) between dawn and midday which covered a portable, battery powered weighing differed by approximately 2°C (Houston 1973). device (model B50-E Shekel Inc., Israel, accuracy i- Among New World vultures, T, in a 5 8). (Coragypsatrums) (body massapproximately 2,000 g) There are important ethical considerationsinvolved fasted for 36 hr and kept at T, range of 15-35°C in any experiment in which animals are deprived of showed a T, range of 5.3”C, between 37.7-43.O”C be- food for long periods. We do not considerthat depriv- tween day and night (Larochelle et al. 1982). A T, ing Griffon Vultures of food for 10 days presentedan variation of 4°C (between 38.0-34.O”C) was reported unnatural situation or resulted in any distress, as this for a single male (2,230 g) ( species withstands long intervals between feeding in aura) fed ad libitum and kept in constantT, of 15°C the wild; even in captivity, when provided with food (Heath 1962). T, in five Turkey Vultures (body mass every day, Griffon Vultures will voluntarily avoid food 1,530-2,590g) fed daily and kept under winter con- for several days (Bahat, unpubl. data). In the present ditions varied 0.4-2.6”C, from 39-40°C in the after- experiment, all birds were in good condition and at noon down to near 38°C in the early morning, regard- their normal body massbefore each feeding trial. They less of the T, (Hatch 1970). An average Tb of 39.7”C were continuously observed and we planned to ter- (range 38.0-41.7”C) was found in six Turkey Vultures minate a trial immediately if any of them had shown at a T, range of 1l-40°C (Arad and Bernstein 1988). signs of discomfort or distress.Therefore, we consider Considering the fact that the thermoneutral zones this period of food deprivationto be a perfectly normal (TNZ) of Black and Turkey Vultures are between 25- experience for this speciesand one for which it is ap- 40°C and 26-40°C respectively (Larochelle et al. parently adapted. 1982, Arad and Bernstein 1988), the measurements 170 SHORT COMMUNICATIONS

y = 0.18x + 33.32

39

38 38

36

35 6 12 18 24 351 15 20 25 30

Ambient temperature( ‘C)

FIGURE 2. Effect of ambient temperature on aver- age body temperature of six food deprived Griffon Vultures (9.5-10.5 days following last feeding).

mentioned above for the two species were made while the birds were exposed to T, values below their lower critical T, (T,,). Some vultures at the lower ambient temperatures might have been cold stressed. One might expect that under these conditions, birds would drop their T, as much as possible in order to reduce the difference between T, and T, to a minimum. Conse- quently, one might anticipate that Black and Turkey 6 Ii Ii 24 Vultures which are kept only in their TNZ, would show a reduced degree of nocturnal drop in T,. 41 Nocturnal drop in T, also has been found among C nonscavenging raptors: in Red-tailed Hawks (Buteo ju- maicensis), a nocturnal decrease in T, of up to 1.8”C has been measured in the summer in birds deprived of food (Chaplin et al. 1984). When fed ad libitum, their T, variation was only 0.8”C. In winter, these birds had a maximum T, variation of 3.2”C during fast and a T, variation of 2.O”C when fed ad libitum. In all seasons, the range of T, variation in Red-tailed Hawks primar- ily was affected by food deprivation; changes in T, had a smaller effect (Chaplin et al. 1984). The Griffon Vulture, although 20% heavier than the African White-backed Vulture, more than three times heavier than the Black and the Turkey Vultures, and near- ly six times heavier than the Red-tailed Hawk, has a greater Tb variation than any of these other species. In 8 11 1; 24 order to assess the magnitude of energy conserved by nocturnal drop in T,, of Griffon Vultures, we used the 1 dark 1 light 1 dark 1 data on T, changes which were obtained in this study, together with a specific heat capacity of the body of 3.35 J.g-’ ‘C-l (Hart 1951, Schmidt-Nielsen 1990). For a Time of day (hour) 6,580 g Griffon Vulture (average body mass in the pres- ent experiment), the amount of heat needed to increase FIGURE 1. Average daily body temperature varia- Tb by 1°C is 22.0 Jg’ “C-I. The amount of heat needed tions in Griffon Vultures under different feeding con- to increase Tb by 1.8”C (average nocturnal drop in T, in ditions. (A) values for birds while digesting food. (B) digesting vultures) is 39.6 J.g-’ “Cm’. An increase in T,, values for birds in the post-absorptive state. (C) values of 2.YC (average nocturnal drop in Tb in post-absorptive for birds following 10 days of food deprivation. state) requires 55.1 J.g-’ ‘C-‘, and an increase in Tb of SHORT COMMUNICATIONS 171

3.o”C (nocturnaldrop in T, in food deprived vultures) A companion to physiology. Cambridge reauires66.1 J.ai “C-I. Thus. bv lowering its bodv tem- Univ. Press, Cambridge. perature.3.O”C is responseto f&d depriv&on, a Griffon BAHAT,0. 1995. Physiological adaptationsand for- Vulture may savea considerableamount of energy.How- aging ecology of an obligatory carrion eater-the ever, there is a cost, in that energy will need to be ex- Griffon Vulture (Gyps fulvus). Ph.D. diss., Tel- pendedto raiseTb in the early morning,although Griffon Aviv University, Tel-Aviv, Israel. Vulturescan reducethis costunder natural conditions by BAHAT,O., A. KAPLAN,Y. BAIDAIZ,L. KAPLAN,I. CHOSH- using solarradiation (Bahat 1995). NIAK,AND D. HOUSTON.1993. Radio-trackinga ju- As Griffon Vulturesrange from extreme arid deserts venile Griffon Vulture (Gypsfihs) in the north of to high and cold mountainousareas, and as this species Israe-preliminary results.Isr. J. Zool. 39:47. is mostly nonmigratory,it is exposed to a very wide CALDER.W. A., AND J. R. KING. 1974. Thermal and range of T,. Furthermore,as it nestsand roostson open caloric relations of birds, p. 259-413. In D. S. cliff ledgesand only rarely in caves(cave nestingis typ- Famer and J. R. King leds.1. Avian bioloav,I- vol. 4. Academic Press, New York. ical in the Turkey Vulture, Hatch 1970), it is fully ex- CHAPLIN,S. B., D. A. DIESEL,AND J. A. KASPAIUE.1984. posed to T, effects. In view of the unpredictablenature Body temperatureregulation in Red-tailed Hawks of its food supply as an obligatory carrion feeder, the and Great Homed Owls: responsesto air tempera- abilitv of the Griffon Vulture to lower its T, regularlvand ture and food deprivation.Condor 86:175-181. minimize the temperaturedifference between-T, and T,, HATCH,D. E. 1970. -Energy conserving and heat dis- and consequentlyits heat loss, is an importantenergy- sinatina mechanismsof the Turkey Vulture. Auk saving adaptationto endure long periods of starvation. 8?:llly-124. AlthoughGriffon Vulturesshow a nocturnaldrop in body HART, J. S. 1951. Calorimetric determination of av- temperatureeven when recently fed, this cycle of tem- erage body temperatureof small mammals and its peraturevariation is subjectedto environmentalinfluence: variation with environmental conditions. Can. J. T, furtherinfluences the deviationof Tb from T, but only Zool. 29:224-233. under conditionsof food deprivation.We suggestthat HEATH,J. E. 1962. Temperature fluctuations in the body temperaturevariation in the Griffon Vulture is al- Turkey Vulture. Condor 64~234-235. ways presentbut is furthershaped by changesof T, when HOHTOLA,E., R. HISSA,A. PY~RNIL;~,H. RINTAMAKI, a bird is deprivedof food. By regularlyreducing the dif- AND S. SAARELA.1991. Nocturnal hypothermiain ferencebetween T,, and T,, and by reducingheat produc- fasting JananeseQuail: the effect of ambient tem- tion, Griffon Vultures save energy otherwise used for pera&e. Physiol. and Behav. 49:563-567. thermoregulation.Accordingly, this substantialenergy HOUSTON,D. C. 1973. The ecology of Serengeti vul- savingenables the Griffon Vulture to cope with regular tures. Ph.D. diss., Oxford Univ., Oxford. periods of food shortagewithout decreasingits activity HOUSTON,D. C. 1974. Food searchingin griffon vul- level. The maintenanceof foraging activity is very im- tures. E. Afr. Wildl. J. 12:63-77. portant for this speciesbecause it is totally dependent Houston, D. C., and J. E. Cooper. 1975. The digestive upon finding carcasseswhich are searchedfor over ex- tract of the Whiteback Griffon Vulture and its role tensive areasand regularlyover periodsof severaldays. in disease transmissionamong wild ungulates.J. Therefore, keeping a continual daily foraging activity, Wildl. Dis. 11:306-313. while minimizing nocturnalenergy expenditure, is a ma- LAROCHELLE,J., J. DELSON,AND K. SCHMIDT-NIELSEN. jor adaptationto the scavengingway of life of this spc- 1982. Temperature regulation in the Black Vul- ties. ture. Can. J. Zool. 60:491-494. REINERTSEN,R. E. 1983. Nocturnal hypothermia and We are most grateful to I. Horowitz and his staff for its energetic significancefor small birds living in the invaluable help in the surgical proceduresfor im- the a&c and subarctic regions. A review. Polar planting body temperature measuring radio-transmit- Res. 1:269-284. ters. We are -grateful to G. Mandel, who took part in SAARELA,S., B. KLAPPER,AND G. HELDMAIER.1989. Thermogenic capacity of Greenfinches and Sis- the telemetrv. work. We thank Y. Yom-Tov, U. Marder, and all the staff of the Zoological Garden, Tel-Aviv kins, p. 115-122. In C. Beth and R. E. Reinertsen University, for their important help throughoutthe pe- [eds.], Physiology of cold adaptationin birds. Ple- riod of physiological experiments (1990-1994). We num Press, New York. are grateful to R. Dmi’el for letting us use transmitters SAARELA,S., B. KLAPPER,AND G. HELDMAIER.1991. Seasonalchanges in circadian rhythm of thermo- and receiving equipment from his laboratory. We are regulation in Greenfinchesand Siskins at different grateful to J. A. Gessamanfor his advice concerning ambient temneratures. D. 573-579. In E. Riklis the implantation of temperature measuring transmit- [ed.], Photobiology. Plenum Press, New York. ters. Finally, we thank the Israeli Ministry of Science SCHMIDT-NIELSEN,K. 1990. Animal physiology: ad- for financial support(grant no. 4101-l-92). antation and environment, 4th ed. Cambridge Univ. Press, Cambridge. LITERATURE CITED STUEBE.M. M.. AND E. D. KETTERSON. 1982. A study of fasting in Tree Sparrows(Spizella arborea) and ARAD,Z., AND M. BERNSTEIN.1988. Temperaturereg- Dark-eyed Juncos (Bunco hyemalis): ecological ulation in Turkey Vultures. Condor 90:913-919. implications. Auk 99:299-308. ASCHOFF,J. 1982. The circadianrhythm of body tem- WAITE, T A. 1991. Nocturnal hypothermia in Gray perature as a function of body size, p. 173-188. Jays (Perisoreus canadensis) wintering in interior In C. R. Taylor, K. Johansen,and L. Bolis [eds.], Alaska. Omis Stand. 22:107-110.