sign in sign up
<<
Home , Kingfisher, Laughing kookaburra, Puerto Rican tody, Tody

The Condor 0(0):1–6 c The Cooper Ornithological Society 2008

BODY TEMPERATURE AND ACTIVITY PATTERNS OF FREE-LIVING LAUGHING : THE LARGEST IS HETEROTHERMIC

, , , CHRISTINE E. COOPER1 2 4,GERHARD KORTNER2,MARK BRIGHAM2 3, AND FRITZ GEISER2 1Environmental Biology, Curtin University of Technology, PO Box U1987, , Western , Australia 2Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, N.S.W., Australia 3Department of Biology, University of Regina, Regina, SK S4S 0A2, Canada

Abstract. We show that free-ranging Laughing Kookaburras (Dacelo novaeguineae), the largest kingfishers, ◦ are heterothermic. Their minimum recorded body temperature (Tb) was 28.6 C, and the maximum daily Tb range was 9.1◦C, which makes kookaburras only the second coraciiform and the only member of the Alcedinidae known to be heterothermic. The amplitude of nocturnal body temperature variation for wild, free- living kookaburras during winter was substantially greater than the mean of 2.6◦C measured previously for captive kookaburras. Calculated metabolic savings from nocturnal heterothermia were up to 5.6 ± 0.9 kJ per night. There was little effect of ambient temperature on any of the calculated Tb-dependent variables for the kookaburras, although ambient temperature did influence the time that activity commenced for these diurnal . Kookaburras used endogenous metabolic heat production to rewarm from low Tb, rather than relying on passive rewarming. Rewarming rates (0.05 ± 0.01◦Cmin−1) were consistent with those of other avian species. Captivity can have major effects on thermoregulation for birds, and therefore the importance of field studies of wild, free-living individuals is paramount for understanding the biology of avian temperature regulation.

Key words: Alcedinidae, , heterothermia, temperature telemetry, torpor. Temperatura Corporal y Patrones de Actividad de Individuos Silvestres de Dacelo novaeguineae: El Mart´ın Pescador de Mayor Tamano˜ es Heterotermico´ Resumen. Mostramos que Dacelo novaeguineae, el mart´ın pescador de mayor tamano˜ corporal, es het- ◦ erotermico.´ La temperatura corporal m´ınima (Tb) registrada para esta especie fue de 28.6 C y el rango maximo´ de variacion´ diaria fue de 9.1◦C, lo que hace a esta especie la segunda especie conocida como heterotermica´ dentro de los coraciiformes y la unica´ dentro de la familia Alcedinidae. La amplitud de la variacion´ de la temperatura corporal nocturna para individuos silvestres de D. novaeguineae durante el invierno fue substancialmente mayor que la media de 2.6◦C medida anteriormente en individuos de la misma especie en cautiverio. El ahorro metabolico´ resultante de la heterotermia nocturna fue de hasta 5.6 ± 0.9 kJ por noche. Hubo poca influencia de la temperatura ambiental sobre cualquier variable dependiente de la Tb de D. novaeguineae, aunque la temperatura ambiental influyo´ sobre el horario en que comenzo´ la actividad en estas aves diurnas. Los individuos de D. novaeguineae utilizaron la produccion´ de calor metabolico´ endogeno´ para aumentar la Tb baja, en vez de depender de un recalen- tamiento pasivo. Las tasas de recalentamiento (0.05 ± 0.01◦Cmin−1) fueron consistentes con las reportadas para otras especies de aves. El cautiverio puede tener efectos importantes sobre la termorregulacion´ en las aves, por lo que los estudios de campo con individuos silvestres son de extrema importancia para entender la biolog´ıa de la regulacion´ de la temperatura en las aves.

INTRODUCTION and regulated below that of normothermic Tb, resulting in an increased nycthemeral T rhythm (McKechnie and Lovegrove The majority of birds are considered to be homeothermic en- b 2002). Heterothermic responses include hibernation and daily dotherms, maintaining a high and stable body temperature (T ) b torpor, which are distinct from obligate hypothermia, which by means of endogenous heat production. However, there is a usually results from an inability to maintain physiological ther- considerable energetic cost of sustaining a high T , especially b moregulation (McKechnie and Lovegrove 2002, Schleucher at low ambient temperature (T ), when T –T differentials are a b a and Prinzinger 2006). large. One strategy by which this energetic demand may be re- Heterothermia occurs more commonly in than duced is heterothermy, during which rest-phase T is reduced b birds (Geiser et al. 2006). Worldwide, only 29 of 138 avian families within 11 of 30 orders are known to contain species that are heterothermic (McKechnie and Lovegrove 2002). Het- Manuscript received 25 January 2007; accepted 30 September 2007 erothermia appears to be more common in small species that 4E-mail: [email protected] inhabit regions with harsh or unpredictable climates and those

The Condor, Vol. 0, Issue 0, pages 1–6. ISSN 0010-5422, electronic ISSN 1938-5422. c 2008 by The Cooper Ornithological Society. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.com/reprintInfo.asp. DOI: 10.1525/cond.2008.8327

1 2 CHRISTINE E. COOPER ET AL.

with diets that are temporally and spatially patchy (Hiebert to a national standard. Temperature transmitters were then im- 1993, McKechnie and Lovegrove 2002). Heterothermia has planted into the abdominal cavities of the kokaburras under been studied in few species, particularly under free-living general anesthesia (oxygen-isoflurane). Kookaburras were re- conditions. Quantitative data on heterothermy in free-living turned to their sites of capture several hours after recovery birds have been obtained for only a few species of caprimulgi- from anesthesia. Measurement of Tb commenced two weeks forms (Brigham et al. 2000, 2006, Kortner¨ et al. 2000, 2001), after surgery to reduce any possible effects of capture, surgery, the White-backed (Colius colius; McKechnie et al. or anesthesia on Tb regulation. 2004), and a (Dolby et al. 2004). Several studies sug- Remote logger-receiver systems were used to monitor Tb gest that captivity substantially influences the use, depth and nightly (Kortner¨ and Geiser 1998) by recording transmitter duration of facultative hypothermia in many birds and mam- pulse-intervals every 10 minutes. Ambient air temperature (Ta) mals (Geiser et al. 2000, Geiser and Ferguson 2001, Kortner¨ 1 m above ground level was recorded (±1◦C) simultaneously et al. 2001, Dolby et al. 2004). For many species, captive in- via a temperature sensor connected to each data logger. Kook- dividuals have reduced amplitude in Tb oscillation compared aburras were tracked to roost sites at dusk and logging systems to their wild, free-living counterparts. This may be due to a set up within signal range and left running overnight. If a kook- ready supply of food but may also be a consequence of not aburra returned to the same roost site for consecutive nights, fully adjusting to captive conditions (Kortner¨ et al. 2001). the logging system was left running continuously for up to a Laughing Kookaburras (Dacelo novaeguineae)arethe week before downloading the data. Monitoring continued un- largest (360 g) members of the kingfisher family (order Coraci- til transmitter signals could no longer be located. There was iformes, family Alcedinidae). Kookaburras are diurnally ac- no evidence of a systematic change in Tb data throughout the tive birds that inhabit woodland and open forest throughout study; we thus assumed that transmitter calibration did not eastern Australia. They have also been introduced to Western drift during the period of data collection. Australia and , where they are well established. Un- We analyzed the data using a custom-written analysis pro- like other Australian kingfishers, family groups of kookaburras gram in Visual Basic 6.0 (Microsoft Corporation, Redmond, are sedentary and territorial year-round. They feed mostly on Washington), where the pulse intervals were converted to tem- , as well as small reptiles, birds, and mammals perature (◦C) using the calibration curve for each transmit- (Schodde and Tideman 1997). ter. Temperature variables calculated (Fig. 1) were: minimum In captivity, kookaburras exhibit low-amplitude, daily Tb Tb (Tbmin), mean nocturnal Tb (Tb night), Tb when arriving at ◦ ◦ oscillation, with Tb varying from 37.2 to 39.7 C (Buttemer the roost (Tbarrival), and Tb when leaving the roost (Tb active), et al. 2003). However, year-round territory maintenance and along with the associated Ta and time of day. On nights when a seasonally variable diet presumably place free-living kook- kookaburras changed roost sites, Tbarrive could not be deter- aburras under energetic stress during winter in cold climates. mined, as the Tb recording commenced only after moving the The purpose of our study was to measure nocturnal Tb and ac- tivity patterns of free-living kookaburras during winter to de- termine whether their thermoregulatory patterns differed from those of captive .

METHODS Temperature-sensitive radio-transmitters were used to measure Tb for five wild, free-living kookaburras near Armidale, New South Wales (30˚30S, 151◦39W). Kookaburras were captured in mist nets or a raptor trap and assigned identification num- bers. The Tb of three kookaburras was monitored during July, August, and early September in 2003 (A03 for 34 nights, B03 for 49 nights, and C03 for 64 nights), and two kookaburras were monitored during June and July in 2004 (A04 for 12 FIGURE 1. Body temperature of a Laughing (Dacelo nights and B04 for 19 nights). novaeguineae) during its nocturnal rest phase. Time between sun- Transmitters (Sirtrack Wildlife Tracking Solutions, Have- set and sunrise is indicated by a thick dark bar along the x-axis. lock North, ; ∼3.5 g) were coated with a biolog- Thin bars indicate the calculation of various temperature variables; = = ically inert wax (paraffin-Elvax, Minimitter Company, Inc., Tb night mean nocturnal body temperature, Tbmin minimum body temperature, Tbarrive = body temperature when arriving at the roost Sunriver, Oregon) and calibrated in a water bath at Ta from = ◦ ◦ ◦ site, Tbactive body temperature when leaving the roost site. Cooling 15 to 50 Cin5 increments. The temperature in the water and arousal rates were calculated as the slope of the regression of bath was measured to ±0.1◦C with a thermometer traceable body temperature on time during cooling and arousal. KOOKABURRA BODY TEMPERTURE 3

logger to the new roost site. The range in Tb was calculated by subtracting Tbmin from Tbarrival,asTb arrival was always the highest Tb recorded at the roost. Unless stated otherwise, all Tb characteristics refer to mean Tb for at least 20 minutes (i.e., ≥3 readings). Cooling and arousal rates were calculated from the slopes of the regressions of Tb on time during pe- riods of cooling after arriving at the roost and arousal before leaving the roost, respectively. We estimated energy savings resulting from heterothermy from metabolic rates (VO2calc) calculated using the equation Tb = 20.1 × [VO2calc –C× (Tb –Ta)]/(m× SH) after Withers et al. (1990) and Cooper and FIGURE 2. Nightly body temperature oscillation for a wild, free- Withers (2004); T is the change in T (◦Cmin−1; calculated living (Dacelo novaeguineae). Breaks in the b b data occur when the bird was out of transmitter range. The region from a 50 minute running average), C is thermal conductance −1 ◦ −1 within the dashed border represents the body temperature variation (0.139 ml O2 min C; Buttemer et al. 2003), m is body mass of captive kookaburras (Buttemer et al. 2003). (g, when captured), SH is the specific heat of tissues (3.47 J −1◦ −1 g C ), and 1 ml O2 is assumed to be equivalent to 20.1 J. 2 We assumed that kookaburras did not exhibit metabolic inhi- ship between Ta and Tbarrive (C03: F1,62 = 18.2, R = 0.23, 2 bition at the onset of the Tb reduction. We compared VO2calc P < 0.001; B04: F1,12 = 18.3, R = 0.60, P = 0.001). ◦ for actual Tb to VO2calc for kookaburras maintaining a constant Mean nighttime Tb ranged from 34.8 ± 0.4 C (A03: Ta = ◦ ◦ ◦ ◦ normothermic resting Tb of 37.2 C (Buttemer et al. 2003). En- 2.2 ± 1.1 C) to 37.6 ± 4.8 C (B04: Ta = 4.0 ± 0.6 C). The ergy savings were calculated for each kookaburra for the night relationship between Ta night and Tb night, although weak, they attained their lowest mean nightly Tb. was significant for two kookaburras (B03: F1,46 = 6.2, P = 2 2 0.02, R = 0.12; C03: F1,60 = 21.8, P < 0.001, R = 0.27). All kookaburras exhibited nightly variation in T , with the STATISTICAL ANALYSIS b mean difference between Tbarrive and Tbminranging from 3.6 ± All statistical analyses were conducted using statistiXL 1.6 0.3◦Cto6.8± 0.3◦C (Fig. 2). The smallest variation for a single (statistiXL, Nedlands, Australia). Temperature values are pre- overnight measurement was 0.3◦C, and the largest was 9.1◦C. sented as means ± SE for each individual, unless stated oth- Mean Tbmin occurred between 00:50 ± 40 min and 02:02 ± erwise. Relationships between T and T were determined by ◦ ◦ b a 21 min. Mean Tbminranged from 32.5 ± 0.5 C to 36.0 ± 0.3 C; least squares regression, and data for individual kookaburras ◦ the lowest individual Tb recorded was 28.6 C (A04). There were compared using ANOVA. Mean values for time of day was a significant, albeit weak relationship between Tbminand were calculated using circular descriptive statistics, with time 2 Ta for two kookaburras (B03: F1,46 = 6.3, P = 0.01, R = values presented as mean ± 95% confidence limits. Differ- 2 0.12; C03 : F1,62 = 12.9, P = 0.001, R = 0.17). ences between VO2calc for kookaburras with actual Tb and The mean minimal nocturnal VO2calc for all five kook- normothermic T were assessed using a paired t-test. Signifi- b aburras (for the night when Tbmin was lowest for each bird) cance was determined at α ≤ 0.05. −1 was 287 ± 11 ml O2 h for an average resting period of 12.2 ± 1.1 hr. Mean nocturnal VO2calc for kookaburras, if they ◦ had maintained a normothermic resting Tb of 37.2 C, was cal- RESULTS −1 culated to be 310 ± 10 ml O2 h —significantly higher than The mean body mass of the kookaburras we captured was 348 the VO2calc for the actual Tb (t4 = 8.1, P < 0.001). The calcu- ± 16 g (range: 311–386 g). Sex of the birds could not be deter- lated mean savings resulting from nocturnal heterothermia was mined. Individuals differed with respect to when they initiated 280 ± 46 ml O2 (5.6 ± 0.9 kJ, assuming 1 ml O2 is equivalent roosting (F4,155 = 6.3, P < 0.001). Initial roosting time of in- to 20.1 J) per night (i.e., 12.2 hours). dividual kookaburras varied from 17:05 ±1 hr 36 min to 18:11 Kookaburras roosted for 11 hr 18 min ± 21minto13 ±9 min and ranged from 4.7 ± 10.2 min to 43.8 ± 4.8 min after hr 7 min ± 11 min per night. Roosting duration was signif- sunset. Roost arrival time was significantly affected by Ta for icantly influenced by Ta night for only one kookaburra (C03: 2 2 only one individual (B04: F1,11 = 6.7, P = 0.02, R = 0.38). F1,55 = 17.8, P = 0.001, R = 0.24). Activity commenced Mean Tb when roosting commenced (i.e., Tbarrive) ranged between 05:41 ± 25 min and 06:15 ± 29 min, from 34.2 from 39.1 ± 0.5◦C to 39.9 ± 0.2◦C, with corresponding mean ± 0.1 min to 38.3 ± 4.8 min before sunrise (Fig. 3). The ◦ ◦ Ta of 6.2 ± 0.9 C and 8.4 ± 0.4 C, respectively. time activity commenced did not differ among individuals There was no significant difference for Tbarrive among (time: F4,166 = 1.0, P = 0.43; time after sunrise: F4,162 = birds, although Taarrive did differ (F4,165 = 2.5, P = 0.04). 0.7 P = 0.60). Time of departure from the roost in relation to Only two individuals showed a significant positive relation- sunrise was positively associated with Ta for four of the five 4 CHRISTINE E. COOPER ET AL.

the roost, presumably reduce thermoregulatory costs (Reebs 1986). We observed this for kookaburras, with roost depar- ture times significantly influenced by Ta, and birds leaving the roost earlier before sunrise on warmer days. Therefore, even for larger birds such as kookaburras, there appears to be an energetic advantage to remaining in a roost longer when en- vironmental conditions are unfavorable (Everding and Jones 2006). In addition, kookaburras prey mainly on invertebrates and small birds, reptiles and mammals, which are presumably less active during cold periods. Therefore, there may be little energetic advantage in becoming active early on cold morn- ings, so kookaburras remain in their roost later when Ta is low. Environmental factors generally have a stronger influence on the time at which birds leave a foraging site in the evening than on their arrival at the roost due to differences in foraging FIGURE 3. Body temperature of a Laughing Kookaburra (Dacelo novaeguineae), demonstrating rewarming prior to leaving the roost location and interactions en route to the roost site (Davis and site. Rewarming occurs prior to sunrise and increasing ambient tem- Lussenhop 1970, Swingland 1976). This appears to also be the perature and must therefore be due to endogenous heat production, case for kookaburras. Arrival time at the roost in the evening not passive rewarming. The vertical dashed lines represent sunset and was generally not related to Ta, and was much more variable sunrise. between individual kookaburras than departure time in the morning. kookaburras (P ≤ 0.009). Mean Tb active ranged from 37.1 ± Maximum nocturnal Tb variation (Tb range) for heterother- ◦ ◦ ◦ 0.4 Cto39.0 ± 0.2 C, at Ta active of 1.2 ± 1.3 C and 2.3 ± mic birds shows a weak but statistically significant (F1,56 = ◦ 2 0.7 C, respectively. There was no difference for Ta active among 8.0, P = 0.007, R = 0.12) negative allometric relationship: ◦ individual birds (F4,163 = 0.4, P = 0.83); however, Tb active did Tb range( C) = –3.7 (± 1.3) log10 m (g) + 17.6 (± 2.3); differ among individuals (F4,169 = 11.3, P < 0.001). There was where m = body mass (where Tb range is the greatest recorded no relationship between Tb active and Ta active for any individu- for a species; data from McKechnie and Lovegrove 2002). als. Mean cooling rates from Tbarrive to Tbminranged from 0.9 Kookaburras conform to this relationship, with their maxi- ◦ −1 ◦ −1 ◦ ± 0.1 Chr to 2.2 ± 1.1 Chr and were always slower than mum nocturnal Tb reduction of 9.1 C being 112% of that arousal rates from Tbminto Tb active, which ranged from 1.7 ± predicted (Fig. 4A). Associated with this is a weak but sig- ◦ −1 ◦ −1 2 0.1 Chr to 3.6 ± 1.1 Chr . There was no significant effect nificant (F1,82 = 17.7, P < 0.001, R = 0.18) positive allo- ◦ of Ta on either cooling or arousal rates for any kookaburra. metric relationship; Tbmin ( C) = 5.2 (± 1.2) log10 m + 18.2 (± 1.9, where Tbmin is the lowest recorded for a species; data from McKechnie and Lovegrove 2002) for avian T . DISCUSSION bmin Kookaburras also conform to this relationship (Fig. 4B), with a ◦ The daily range in Tb that we measured for free-living kook- Tbminof 28.6 C that is 91% of that predicted from body mass. aburras shows unequivocally that kookaburras, the largest Birds with body mass >80g have not been reported to allow ◦ kingfishers, are heterothermic. Their extent of Tb reduction Tb to fall below 20 C (data from McKechnie and Lovegrove meets most definitions of torpor (Reinertsen 1996, McKechnie 2002), suggesting that there is an upper mass limit for the oc- and Lovegrove 2002, Schleucher and Prinzinger 2006). We currence of deep (<20◦C) torpor. Larger birds (>80g), such demonstrate here that wild kookaburras exhibit greater am- as kookaburras and Tawny Frogmouths (Podargus strigoides; plitude of Tb oscillation than measured previously for captive Kortner¨ et al. 2001) are, however, capable of significant, al- individuals (Buttemer et al. 2003). though less substantial, reductions in Tb. Body mass appears Roosting times for kookaburras are comparable to those to be an important factor determining the extent of nocturnal of other diurnal birds (Everding and Jones 2006), occurring hypothermia for birds; although presumably other ecological, during the dark phase of the day, for an average of about physiological and phylogenetic factors also influence avian 12 hr each night. For many birds, roost arrival and depar- Tbmin(Brigham et al. 2006). ture times are related to environmental factors such as day Kookaburras are the second coraciiform species and length, light intensity, cloud cover and Ta (Swingland 1976, the only member of the Alcedinidae known to employ het- Brodsky and Weatherhead 1984, Reebs 1986, Everding and erothermy. The other heterothermic coraciiform species, the Jones 2006). During inclement weather, late departures and Puerto Rican ( mexicanus), weighs only 5–7g and ◦ ◦ early arrivals, which result in longer periods of inactivity in exhibits a Tb range from 23.5 –42.9 C (Merola-Zwartjes and KOOKABURRA BODY TEMPERTURE 5

to be heterothermic, which appears to be a facultative response that presumably helps them balance their energy budgets. We found little effect of Ta on any of the calculated Tb variables for the kookaburras, with <30% of the variation in Tb attributed to Ta. Thus, we argue that Ta has a relatively minor impact on Tb, presumably due to the comparatively large size of kookaburras and their nocturnal huddling behavior, which reduces thermal conductance. Presumably, Ta has greater im- pact on Tb patterns of smaller birds with a larger surface area to volume ratio, and thus greater thermal conductance (Merola- Zwartjes and Ligon 2000). Kookaburras used endogenous metabolic heat production to rewarm from low Tb rather than relying on passive rewarming from increasing Ta or solar radiation, as arousal to normothermic Tb and commencement of activity occurred be- fore sunrise and before Ta began to rise (Fig 3). This confirms that the heterothermic response of these birds is an actively regulated, controlled process, and not simply an inability to meet thermoregulatory demands at low Ta. Nocturnal birds FIGURE 4. Allometric relationship for (A) avian maximum noctur- such as Tawny Frogmouths (Kortner¨ et al. 2000, 2001) and nal body temperature (Tb) oscillation and (B) minimum body temper- Australian Owlet-Nightjars (Agotheles cristatus; Brigham ature. Data from McKechnie and Lovegrove (2002). The Laughing Kookaburra (Dacelo novaeguineae) is indicated with a dark square et al. 2000) are also capable of using endogenous heat pro- and the (Todus mexicanus; Merola-Zwartjes and duction to arouse from torpor at night, but may exploit solar Ligon 2000), with a dark triangle. radiation and increased Ta to arouse from morning torpor, thus reducing the energetic costs of arousal. For kookaburras Ligon 2000). The minimum Tb predicted for a tody by the allo- and other diurnal birds (Hiebert 1993), waiting to passively metric equation generated from McKecknie and Lovegrove’s rewarm would require a substantial delay in activity and pre- ◦ (2002) dataset is 22.2˚C. The tody’s actual Tbmin of 23.5 C sumably reduce foraging success, especially for ectothermic clearly conforms to the relationship and is 106% of that pre- prey that rely on basking to attain high activity levels. The dicted (Fig. 4B). overall mean warming rate during arousal of kookaburras was ◦ ◦ Kookaburras had a Tbarrive (39.1 –39.9 C) that was com- 75% of that predicted based on body mass by the equation ◦ parable to the mean active-phase Tb (39.7 C) of captive indi- logR = 0.44 – 0.63 M, where R = rewarming rate and M = viduals (Buttemer et al. 2003). However, the overnight drop body mass (McKechnie and Wolf 2004; Fig. 5). However, ◦ in Tb for the wild, free-living kookaburras (up to 9.1 C with a kookaburras conform to this relationship, falling well within mean reduction range of 3.6◦–6.8◦C) was substantially greater the 95% prediction limits (Cooper and Withers 2006). than the mean of 2.6◦C measured for captive kookaburras (Buttemer et al. 2003; Fig. 2), despite similar Ta variation in the two studies. Captivity appears to have a substantial effect on the occurrence, depth and duration of torpor in a number of birds and mammals (Geiser et al. 2000, Geiser and Ferguson 2001, Kortner¨ et al. 2001, Dolby et al. 2004), although there is a paucity of Tb data for wild endotherms. For example, wild Tawny Frogmouths exhibit nightly temperature fluctuations ◦ of up to 9 C, while mean nocturnal Tb fluctuation in cap- tive individuals is only 0.4◦C (Bech and Nicol 1999, Kortner¨ et al. 2001). Presumably, captive birds are less energy limited than free-living birds and have a lower propensity to enter torpor. Captive birds may also not feel sufficiently secure to use heterothermy due to decreased responsiveness at low Tb. Comparison of captive and wild kookaburras indicates that FIGURE 5. Relationship between log body mass and log rewarming rate for 13 bird species (white circles; data from McKechnie and kookaburras are capable of maintaining homeothermy, even at Wolf 2004) and the Laughing Kookaburra (Dacelo novaeguineae; low Ta (Buttemer et al. 2003) if they have access to sufficient black square; this study). The solid line is the regression line, and the energy. However, wild kookaburras clearly have the capacity dashed lines, the 95% prediction limits for the regression. 6 CHRISTINE E. COOPER ET AL.

The costs of rewarming, along with low cooling rates, EVERDING S. E., AND D. N. JONES. 2006. Communal roosting in a sub- reduce the advantages of heterothermy for larger birds. How- urban population of Torresian Crows (Corvus orru). Landscape and Urban Planning 74:21–33. ever, our results suggest that even moderate drops in Tb have GEISER F. , AND C. FERGUSON. 2001. Intraspecific differences in be- an impact on a kookaburra’s daily energy budget. Given the haviour and physiology: effects of captive breeding on patterns of common occurrence of heterothermy, these energy savings torpor in feathertail gliders. Journal of Comparative Physiology B must outweigh any potential costs, such as possible increased 171:569–576. predation risk associated with low Tb for kookaburras. GEISER F.,J.C.HOLLOWAY,G.KORTNER¨ ,T.A.MADDOCKS,C.TURBILL, Captivity can have major effects on thermoregulation by AND R. M. BRIGHAM. 2000. Do patterns of torpor differ between free-ranging and captive mammals and birds?, p. 95–101. In G. birds, and therefore the importance of field studies of wild, Heldmaier, and M. Klingenspor [EDS.], Life in the cold: Eleventh free-living individuals is paramount for understanding the bi- International Hibernation Symposium. Springer, Berlin, Germany. ology of avian temperature regulation. Our study shows that GEISER F. , G . K ORTNER¨ ,T.A.MADDOCKS, AND M. R. BRIGHAM. 2006. the largest member of the Alcedinidae, a family not previously Torpor in Australian birds. Proceedings of the 23rd International known to have species capable of heterothermy, displays shal- Ornithological Congress, Acta Zoologica Sinica. 52S:405–408. HIEBERT S. M. 1993. Seasonality of daily torpor in a migratory hum- low nocturnal torpor. It would be interesting to investigate how mingbird, p. 25–32. In C. Carey, G. L. Florant, B. A. Wunder, and ∼ others of the 100 intermediately sized members of the family, B. Horwitz [EDS.], Life in the cold: ecological, physiological and especially small sedentary species, deal physiologically with molecular mechanisms. Westview Press, Boulder, CO. inclement weather and limited food supply in the wild. KORTNER¨ G., AND F. G EISER. 1998. Ecology of natural hibernation in the marsupial mountain pygmy-possum (Burramys parvus). Oecologia 113:170–178. ACKNOWLEDGMENTS KORTNER¨ G.,R.M.BRIGHAM, AND F. G EISER. 2000. Winter torpor in a large bird. Nature 407:318. We thank Rebecca Drury for her assistance with collection and prepara- KORTNER¨ G.,R.M.BRIGHAM, AND F. G EISER. 2001. Torpor in free- tion of the data, and two anonymous reviewers who provided constructive ranging Tawny Frogmouths (Podargus strigoides). Physiological comments on the manuscript. and Biochemical Zoology 74:789–797. MCKECHNIE A.E.,G.KORTNER¨ , AND B. G. LOVEGROVE. 2004. Rest- phase thermoregulation in free-ranging White-backed Mouse- LITERATURE CITED birds. Condor 106:144–150. MCKECHNIE A. E., AND B. G. LOVEGROVE. 2002. Avian facultative BRIGHAM,R.M.,G.KORTNER¨ ,T.A.MADDOCKS, AND F. G EISER. 2000. hypothermic responses: a review. Condor 104:705–724. Seasonal use of torpor by free-ranging Australian Owlet-nightjars. MCKECHNIE A. E., AND B. O. WOLF. 2004. The energetics of the re- Physiological and Biochemical Zoology 73:613–620. warming phase of avian torpor. Life in the cold: evolution, mech- BRIGHAM,R.M.,C.WOODS,J.E.LANE,Q.E.FLETCHER, AND F. anisms, adaptation and application. Twelfth International Hiber- GEISER. 2006. Ecological correlates of torpor use among five nation Symposium. Biological Papers of the University of Alaska caprimulgiform birds. Proceedings of the 23rd International Or- 27:265–273. nithological Congress, Acta Zoologica Sinica 52S:401–404. MEROLA-ZWARTJES M, AND J. D. LIGON. 2000. Ecological energetics BRODSKY,L.N.,AND P. J. W EATHERHEAD. 1984. Behavioural ther- of the Puerto Rican Tody: heterothermy, torpor and intra-island moregulation in wintering Black Ducks: roosting and resting. variation. Ecology 81:990–1003. Canadian Journal of Zoology 62:1223–1226. REEBS S. G. 1986. Influence of temperature and other factors on the BUTTEMER,W.A.,S.C.NICOL, AND A. SHARMAN. 2003. Thermoen- daily roosting times of Black-billed Magpies. Canadian Journal ergetics of pre-moulting and moulting kookaburras (Dacelo no- of Zoology 64:1614–1619. vaeguineae): they’re laughing. Journal of Comparative Physiology REINERTSEN R. E. 1996. Physiological and ecological aspects of hy- B 173:223–230. pothermia, p 125–157. In C. Carey [ED.], Avian energetics and COOPER C. E., AND P. C . W ITHERS. 2004. Patterns of body temperature nutritional ecology. Chapman and Hall, New York. and torpor in the numbat Myrmecobius fasciatus (Marsupialia SCHLEUCHER E., AND R. PRINZINGER. 2006. Heterothermia and tor- Myrmecobiidae). Journal of Thermal Biology 29:277–284. por in birds: highly specialized physiological ability or just deep COOPER C. E., AND P. C . W ITHERS. 2006. Numbats and aardwolves— “nocturnal hypothermia”?—The limitations of terminology. Pro- how low is low? A re-affirmation of the need for statistical rigour ceedings of the 23rd International Ornithological Congress, Acta in evaluating regression predictions. Journal of Comparative Phys- Zoologica Sinica. 52S:393–396. iology B 176:223–629. SCHODDE R., AND S. C. TIDEMAN. 1997. Reader’s Digest Complete DAV I S G. J., AND J. F. LUSSENHOP. 1970. Roosting of Starlings (Sturnus Book of Australian Birds. Readers Digest, . vulgaris): a function of light and time. Behaviour 18:362– SWINGLAND I. R. 1976. The influence of light intensity on the roosting 365. times of the Rook (Corvus frugilegus). Animal Behaviour 24:154– DOLBY A.S.,J.G.TEMPLE,L.E.WILLIAMS,E.K.DILGER,K.M. 158. STECHLER, AND V. S . D AV I S . 2004. Facultative rest-phase hypother- WITHERS P.C.,K.C.RICHARDSON, AND R. D. WOOLER. 1990. mia in free-ranging White-throated Sparrows. Condor 106:386– Metabolic physiology of euthermic and torpid honey possums 390. Tarsipes rostratus. Australian Journal of Zoology 37:685–693.