Seasonal Variations in Thermal Energetics of Australian Silvereyes (Zosterops Lateralis)

J. Zool., Lond. (2000) 252, 327±333 # 2000 The Zoological Society of London Printed in the United Kingdom

Seasonal variations in thermal energetics of Australian silvereyes (Zosterops lateralis)

Tracy A. Maddocks and Fritz Geiser Zoology, School of Biological Sciences, University of New England, Armidale NSW 2351, Australia (Accepted 26 October 1999)

Abstract Most Australian birds do not migrate over long distances and therefore have to cope with seasonal changes in weather and food availability. We investigated whether the small (11 g) silvereye Zosterops lateralis changes its thermal tolerance from winter to summer. Body mass and body temperature of silvereyes exhibited little seasonal variability. However, metabolic rates (MR) and thermal conductance showed signi®cant changes. Below the thermoneutral zone (TNZ), winter-acclimatized birds had signi®cantly lower resting MR and thermal conductance than summer-acclimatized birds. Within the TNZ (~27.0±33.6 8C -1 -1 winter; ~25.4±33.5 8C summer) basal MR of winter-acclimatized birds (2.30 0.29 mL O2 g h ) was -1 -1 signi®cantly lower than that of summer-acclimatized birds (2.88 0.43 mL O2 g h ). The average daily MR also differed signi®cantly between summer and winter largely due to a greater reduction of MR at night and the decreased conductance. Our study shows that small passerines such as silvereyes exhibit seasonal variability in physiology and thermal energetics, even when they live in areas with a relatively mild climate, to help overcome seasonal changes in weather conditions and food availability.

Key words: birds, thermal energetics, season, metabolic rate, body temperature, Zosterops lateralis

INTRODUCTION seasonal changes in climate and less harsh winter conditions than many areas in the northern hemisphere, Seasonal changes in climate represent potential increases weather conditions are highly unpredictable and may in energetic stress for small diurnal birds. During make acquiring food dif®cult and/or energetically de- summer they are exposed to hot temperatures which manding. Moreover, in contrast to many birds from the may result in dehydration and heat stress. During northern hemisphere, most Australian birds are winter, conditions may be even more unfavourable as nomadic or sedentary and do not migrate over long the interacting problems of inclement weather, long distances (Ford, 1989). To survive changing environ- nights and restricted food supplies, and high energetic mental conditions, small birds living in Australia costs for thermoregulation may push them to their therefore require some survival mechanisms and/or energetic limit. To cope with these stressors, many birds seasonal acclimatization, although these are likely to be exhibit seasonal changes in their physiology. In less pronounced than in species from the northern passerines, such changes have been investigated pri- hemisphere. marily in species from North America and Europe, with Although seasonal changes in physiology seem likely the major physiological changes involving body mass in Australian birds, little is known about the subject. (BM), metabolic rate (MR) and insulation (Hart, 1962; The only information available is restricted to seasonal Mugaas & Templeton, 1970; Dawson & Carey, 1976; changes in basal MR (BMR) of Australian scrubwrens Dawson et al., 1983; Swanson, 1991; Cooper & (Ambrose & Bradshaw, 1988) and resting MR (RMR) Swanson, 1994; Saarela, Klapper & Heldmaier, 1995). of honeyeaters (Collins & Briffa, 1983). There is no Nevertheless, seasonal adjustments might also be detailed information that encompasses seasonal varia- required in small passerines living in the less climatically tion of BM, RMR, BMR and conductance, nor how stressful areas such as Australia due to their small size diurnal variations in body temperature (T b) and MR and high energy requirements. Although most of the change with season. Australian continent experiences relatively minor We were interested in whether the silvereye (Zosterops lateralis), an Australian passerine, exhibits seasonal *All correspondence to: Tracy Maddocks. acclimatization in morphology and/or thermal ener- E-mail: [email protected] getics. Australian silvereyes have a wide distribution, 328 T. A. Maddocks and F. Geiser which extends from Queensland to Tasmania and west mercury thermometer in a waterbath over a Ta range of to Western Australia (Blakers, Davies & Reilly, 1985). 30±50 8C. The transmitters were implanted intraperito- They are resident to the extent that some individuals are neally under Iso¯urane anaesthesia. Animals were present throughout their range in all seasons and thus allowed at least 7 days to recover before any experi- are annually exposed to ¯uctuations in temperature and ments were performed. The transmitter signal was food availability. Silvereyes are known to signi®cantly received with a ferrite rod antenna placed under each reduce MR and T b at night in winter (Maddocks & chamber and multiplexed to a receiver. Geiser, 1997, 1999). To determine whether they exhibit Ambient temperature (Ta) was measured to the seasonal acclimatization, we investigated the seasonal nearest 0.1 8C with a calibrated Cu-Constantan thermo- changes in BM, MR, Tb and thermal conductance over couple inserted 1 cm into the respirometry chamber. a range of ambient temperatures (T a). We also deter- Thermocouple output was ampli®ed by a digital mined whether daily ¯uctuations of MR and T b change thermometer (Omega DP116). Measurements of Tb and with season. Ta were taken simultaneously with MR every 12 mins. Analog outputs from the ¯owmeter, oxygen analyser, transmitter receiver and digital thermometer were inter- MATERIALS AND METHODS faced via a 14 bit analog to digital converter card to a computer. Data acquisition and processing were per- Nine silvereyes were captured with mist nets near formed with software written by B. Lovegrove, T. Ruf Armidale, NSW, Australia (30832'S, 151839'E) in June and G. KoÈrtner. MR values were calculated for STP (winter) 1995. As some of these birds were used in conditions according to equation 3a of Withers (1977) another experiment and were not available for summer assuming an RQ of 0.85. measurements, a further 4 birds were captured in During MR measurements, birds were post-absorptive September. After capture, birds were weighed to the (at least 2 h since last possible meal) and food and water nearest 0.1 g. They were housed outdoors in wooden were not available. RMR were determined over a range cages, where they were exposed to natural photoperiod of Ta from 3 to 26 8C which is approximately the range and temperature ¯uctuations. Water and food (arti®cial between average daily minimum in winter and average nectar and insect replacements, apple and Tenebrio daily maximum in summer in the Armidale area. Birds larvae) were available in excess and supplied fresh daily. were placed in the respirometry chambers at approx. Winter measurements were carried out during August 15:00 and kept at constant Ta for periods of 16±18 h. and the ®rst week in September (Ta range approx. 0 to The photoperiod within the cabinet was adjusted with a 13 8C; Bureau of Meteorology, 1988), and summer timer to coincide with the natural photoperiod at that measurements during December and January (Ta range time of year (approx. L11:D13 winter; L14:D10 approx. 13 to 27 8C; Bureau of Meteorology, 1988). MR summer). was measured as the rate of oxygen consumption using Measurements of oxygen consumption were used to open ¯ow respirometry. The respirometry chamber (1L determine RMR, BMR and average daily MR (ADMR) glass jar ®tted with a perch) was positioned within a during winter and summer. MR values were calculated temperature-controlled cabinet ( 0.5 8C). Birds could as the mean of at least 3 low consecutive readings (i.e. not see each other during measurement periods. Air over at least a 36 min interval) at each Ta. The means of -1 ¯ow rates of about 300 mL min through the chambers the corresponding readings of Tb and Ta were also were controlled with rotameters and measured with a calculated. mass ¯owmeter (FMA 5606, Omega Engineering Inc. For MR measurements within the thermoneutral Stamford, USA). Oxygen content of the air entering and zone (TNZ), animals were placed in respirometry leaving the metabolic chamber was measured using a chambers at approx. 16:00 and kept for a maximum of single channel oxygen analyser (Ametek Applied 8 h. Measurements were taken over a Ta range of 25 to Electrochemistry Oxygen Analyser S-3A/1, Pittsburgh). 40 8C to determine the TNZ. Starting at 25 8C the Ta Solenoid valves switched channels in 3 min intervals, was progressively increased in steps of 2 8C every hour which permitted the measurement of up to 3 animals until a sharp rise in MR and Tb was observed. If an and a reference in succession, each channel was mea- acute rise was evident for 1 individual, all birds being sured once every 12 min. Birds were weighed before and measured at that time were removed because the after each testing period and a constant rate of mass loss removal of 1 would disturb the others. Therefore, for was assumed for calculation of mass-speci®c MR. All some individuals, data above TNZ may be lacking due individuals survived and remained healthy during the to premature termination of the experiment. BMR was course of the experimental period. determined for each individual as the lowest MR value Implanted temperature-sensitive transmitters (Mini- over 36 min during the scotophase. The lower critical Ta mitter model X-M, in modi®ed, smaller capsule) were (Tlc) of the TNZ, at which RMR begins to increase with used to measure T b ( 0.1 8C). The wax-paraf®n coated decreasing Ta, was determined by calculating the Ta of transmitters weighed 1.1±1.3 g and measured 1268mm the RMR/BMR intersect of each individual using the and were smaller than silvereye eggs (17613 mm). RMR vs. Ta regression line below the TNZ. The upper Several days after batteries were replaced, transmitters critical Ta (Tuc) was determined by calculating the Ta were calibrated to the nearest 0.1 8C against a precision of the RMR/BMR intersect using the RMR vs. Ta Seasonal thermal energetics of silvereyes 329

(a)

Fig. 1(a). Daily ¯uctuation of metabolic rate (MR), body temperature (Tb) and conductance of Zosterops lateralis at ambient temperature (Ta)168C during winter. Animals were measured at a constant Ta for a period of 16±18 h. Values shown are mean sd of n = 9 (MR), n =4(Tb and conductance). Dark bar indicates period of darkness. regression line above the TNZ of pooled data as there squares, and the slopes and elevations were compared was insuf®cient data above the TNZ to calculate Tuc for using an analysis of covariance. Differences were con- each individual. sidered signi®cant at the 5% level (P < 0.05). The ADMR was calculated for each individual integrating total MR at each Ta measured. An average for both the photophase and scotophase was deter- RESULTS mined, which was then multiplied by the duration of the phase for each season (L11:D13 winter; L14:D10 The BM of silvereyes varied little seasonally. The summer). Data were converted to kJ (1L O2 = 20.08 kJ; average BM during winter (11.22 0.96 g, n = 9) did not Schmidt-Nielsen, 1997). For each measurement Ta was differ signi®cantly (P = 0.26) from the average summer also averaged, and data for each season were grouped BM (10.90 1.04 g, n = 9). according to Ta. For each group, Ta data were then Daily oscillations of MR, T b and conductance were rounded to the nearest 0.1 8C. Mass-speci®c thermal triggered by the light phase both during winter (Fig. 1a) conductance was calculated using the equation: and summer (Fig. 1b). The three variables decreased Conductance = MR/(Tb±Ta) (Lasiewski, Weathers & signi®cantly immediately after the light was switched off Bernstein, 1967). (approx. 17:30 winter; 18:50 summer), but then gradu- Data are presented as mean sd of the number of ally increased throughout the scotophase. A signi®cant individuals measured (n). Sample variances were tested and rapid increase of MR, Tb and conductance occurred for homogeneity using F max test. Paired observations when the light was switched on (approx. 06:25 winter; were compared using a paired or pooled Student's t-test. 04:50 summer). Linear regressions were ®tted using the method of least RMR was negatively correlated with Ta during both 330 T. A. Maddocks and F. Geiser

(b)

Fig. 1(b). Daily ¯uctuation of metabolic rate (MR), body temperature (Tb) and conductance of Zosterops lateralis at ambient temperature (Ta)168C during summer. Animals were measured at a constant Ta for a period of 16±18 h. Values shown are mean sd of n = 9 (MR), n =4(Tb and conductance). Dark bar indicates period of darkness.

2 2 the scotophase (r = 0.92, P < 0.001; r = 0.87, P < 0.001; ever, the Tlc for winter- and summer-acclimatized birds Fig. 2) and photophase (r2 = 0.73, P < 0.001; r2 = 0.67, did not differ signi®cantly (P = 0.20). Within the TNZ, -1 -1 P < 0.001) during winter and summer, respectively. BMR of winter birds (2.30 0.29 mL O2 g h , n =8) However, winter RMRs were signi®cantly lower than was signi®cantly lower (P = 0.006) than that of summer -1 -1 those measured during summer for both photophase birds (2.88 0.43 mL O2 g h , n = 9 ) (Fig. 2). (P = 0.02) and scotophase (P < 0.001). Between Ta 3 8C Below the TNZ, the scotophase Tb in both seasons and 26 8C during winter, RMR ranged from 7.77 0.67 was more or less stable until Ta declined below 5 8C, and -1 -1 -1 -1 mL O2 g h (n = 9) to 5.06 0.82 mL O2 g h (n =9) thus was not correlated with Ta (P = 0.53 winter; -1 during the photophase, and from 5.58 0.32 mL O2 g P = 0.13 summer) (Fig. 3). The mean Tb of birds both -1 -1 -1 h (n = 9) to 2.60 0.30 mL O2 g h (n = 9) during the below (36.92 0.95 8C, n = 5, winter; 37.6 0.87 8C, scotophase. This is a decrease in MR of up to 49.4% n = 4, summer) and within the TNZ (38.41 0.75 8C, from photo- to scotophase in winter. During summer n = 4, winter; 39.9 8C, n = 2, summer) were indistinguish- -1 -1 the RMR ranged from 9.46 0.87 mL O2 g h (n =7) able (P = 0.07 and P = 0.13, respectively) (Fig. 3). -1 -1 to 5.84 0.88 mL O2 g h (n = 9) during the photo- Thermal conductance below the TNZ during the -1 -1 phase, and from 7.35 0.58 mL O2 g h (n =8) to scotophase was signi®cantly lower in winter than in -1 -1 3.26 0.55 mL O2 g h (n = 9) during the scotophase. summer (P = 0.001) (Fig. 4). Thermal conductance was This is a decrease in MR of up to 44.4 % from photo- to a signi®cant linear function of Ta during winter scotophase in summer. (P < 0.001), though not in summer (P = 0.73). The The TNZ extended over about 7±8 8C, ranging mean thermal conductance within the TNZ during -1 -1 -1 from 27.0 2.4 8C to 33.6 8C during winter and from winter (0.38 0.10 mL O2 g h 8C , n = 4) was not 25.4 1.9 8C to 33.5 8C during summer (Fig. 2). How- signi®cantly higher (P = 0.33) than the mean for summer Seasonal thermal energetics of silvereyes 331

Fig. 2. Mass-speci®c metabolic rate of resting Zosterops later- Fig. 3. Body temperature (Tb)ofZosterops lateralis as a alis over a range of ambient temperature (T ) during the a function of ambient temperature (Ta) during summer (closed scotophase. Measurements were taken in summer (closed symbols) and winter (open symbols) during the scotophase. symbols) and in winter (open symbols), and each point Each point represents a measurement for one individual. The represents a measurement for one individual. Dashed and dashed and broken lines represent the lower critical and upper broken lines represent the lower critical and upper critical critical temperatures (Tlc and Tuc) of the thermoneutral zone temperatures (Tlc and Tuc) of the thermoneutral zone (TNZ) (TNZ) for winter and summer, respectively. Below the TNZ for summer and winter, respectively. Below the TNZ the MR the Tb showed no relationship to Ta in either summer showed a negative linear relationship with T (summer: a (P = 0.13) or winter (P = 0.53). Within the TNZ, Tb for winter 2 MR = 8.5070.22 Ta, P < 0.001, r = 0.87; winter: MR = 6.62 birds (38.4 0.75 8C) was lower, but not signi®cantly, than 2 70.16 Ta, P < 0.001, r = 0.92). Within the TNZ (25.4±33.5 8C summer birds (39.9 1.3 8C). summer; 27.0±33.6 8C winter) the BMR was 2.88 0.43 mL O2 -1 -1 -1 g h in summer-acclimatized birds and 2.30 0.29 mL O2 g -1 winter. This phenomenon of controlled reduction of Tb h in winter-acclimatized birds. by several degrees for energy conservation at night is not uncommon, and has been recorded for many small -1 -1 -1 (0.29 mL O2 g h 8C , n = 2) (Fig. 4). However, due to passerines from North America and Europe (Mugaas & the low sample size, these results within the TNZ must Templeton, 1970; West, 1972; Pohl & West, 1973; be viewed with caution. Reinertsen & Haftorn, 1983; Berger & Phillips, 1993; ADMR differed signi®cantly between summer and Saarela et al., 1995). However, our study is the ®rst to winter largely due to the greater reduction of MR at demonstrate the seasonal change of thermal energetics night and the decreased conductance in winter (Fig. 5). in an Australian passerine. Altering thermoregulatory As winter RMRs were lower than summer RMRs, and patterns with season should maximize energy use and the duration of the scotophase during winter is longer increase the probability of survival. (i.e. winter 13 h, summer 10 h), the ADMR in winter Seasonal acclimatization by birds commonly involves was reduced. At Ta 6.3 8C, 15.8 8C and 24.9 8C winter- altering a number of morphological and physiological acclimatized birds used signi®cantly less energy per day variables, including BM, MR, Tb and conductance. than summer-acclimatized birds (P = 0.0001, P = 0.008, Increases in BM in winter are largely due to an increase and P = 0.002, respectively) (Fig. 5). in the amount of fat stores (Marsh & Dawson, 1989). Increased fat stores are common for avian winter acclimatization, as fat can be used to help ful®l the high DISCUSSION energy demand that is required for thermoregulation, because it can function as a high energy content reserve Our study demonstrates that silvereyes undergo distinct during foraging restrictions (Dawson & Marsh, 1986), daily ¯uctuations in MR, Tb and conductance on a and, especially when stored subcutaneously, also regular basis during both winter and summer. These increases insulation. Seasonal changes in BM appear to ¯uctuations, especially that of MR, are more pro- be common for ground foraging birds, however, tree nounced in winter than in summer resulting, together foraging species (such as silvereyes) show less change with decreases in conductance, in lower ADMR during (Rogers, 1987; Blem, 1990). This may be because the 332 T. A. Maddocks and F. Geiser

140 summer winter 120

100

60 ADMR (kJ /day) ADMR (kj/day)

0 6.3 15.8 24.9 Ambient temperature (°C) Fig. 4. Thermal conductance of Zosterops lateralis as a func- Fig. 5. Average daily metabolic rate (ADMR, kJ/day) of tion of ambient temperature (Ta) during the scotophase in Zosterops lateralis during summer (open) and winter (solid). summer (closed symbols) and winter (open symbols). Each Energy consumption was calculated for each individual using point represents a measurement for one individual. Dashed total MR at each ambient temperature (Ta) measured. Data and broken lines represent the lower critical and upper critical were converted to kJ and an average for both the photophase temperatures (Tlc and Tuc) of the thermoneutral zone (TNZ) and scotophase was determined, which was then multiplied by for winter and summer, respectively. Below the TNZ, conduc- the duration of the phase for each season (L11:D13 winter; tance values and Ta showed a positive linear relationship in L14:D10 summer). For each measurement Ta was also aver- 2 winter (conductance = 0.170 + 0.002Ta, P < 0.001, r = 0.72), aged, and data for each season were grouped according to Ta. though not in summer (conductance = 0.232 70.0003Ta, For each group, Ta data were then rounded to the nearest P = 0.73, r2 = 0.01). 0.1 8C. Summer energy consumption was 27%, 10.6% and 11.4

% greater than winter energy consumption at Ta 6.3 8C, food supply is more predictable for tree foraging birds 15.8 8C and 24.9 8C, respectively. (Rogers, 1987; Rogers & Smith, 1993). Like some other small passerines (West, 1972; Cooper & Swanson, acclimatized silvereyes were up to 21.5% lower than 1994), the silvereyes in our study did not signi®cantly summer-acclimatized birds. Winter reduction in RMR increase BM during winter, indicating that altering fat has been recorded for a number of small passerines stores during seasonal acclimatization is of minor con- from the northern hemisphere, from areas that experi- sequence and may re¯ect the limitations imposed by ence extremely cold winters (Dawson & Carey, 1976; their small body size and requirements for locomotion. Saarela et al., 1995), and also those that have relatively Seasonal effects on BMR also differs widely among mild winters (Swanson, 1991; Cooper & Swanson, small birds. The silvereyes displayed an elevated BMR 1994). Thus, it appears that RMR reduction in winter is in summer which may be related to increased energy a common adaptation in small passerines. The low demands for reproductive organs. However, other RMR of silvereyes coupled with the extended period of similar-sized passerines elevate BMR in winter (Pohl & hypometabolism in winter accrues signi®cant savings in West, 1973; Swanson, 1991), or show no signi®cant the ADMR (kJ/day) when compared to summer- change (Dawson & Carey, 1976). A reduced BMR in acclimatized birds. Thus, the reduction of scotophase winter, such as that displayed by silvereyes, lowers MR in winter allows for better use of energy reserves for energy requirements for maintenance and may enhance maintaining Tb over the longer scotophase. However, individual survival over winter (Feist & White, 1989). the overall nightly energy consumption for the period of Silvereye MR changes include not only a seasonal the scotophase (winter 13 h; summer 10 h) in winter change in BMR, but also a more pronounced nocturnal birds is greater than in summer. Nocturnal decreases in decrease in winter RMR which results in a lower MR were, to some extent, due to decreases in conduc- ADMR in comparison to summer. RMR during the tance. This reduction in conductance lowers the amount scotophase, in comparison to photophase, decreased by of heat lost to the environment, and as such, reduces the up to 49% in winter and by 44% in summer, which is energy required to maintain a stable Tb. The greater particularly advantageous during the long winter nights reduction of conductance at night in comparison to when thermoregulatory responses are most likely to be daytime values in winter (42%) compared to summer most costly. Moreover, scotophase RMR of winter- (30%), re¯ects the greater reduction in MR which allows Seasonal thermal energetics of silvereyes 333 extended availability of energy reserves. Moreover, in Dawson, W. R., Marsh, R. L., Buttemer, W. A. & Carey, C. conjunction with RMR, winter-acclimatized birds had (1983). Seasonal and geographic variation of cold resistance in signi®cantly lower thermal conductances when com- house ®nches Carpodacus mexicanus. Physiol. Zool. 56: 353± 369. pared to summer-acclimatized birds, though their Tbs Dawson, W. R. & Marsh, R. L. (1986). Winter fattening in the did not differ signi®cantly. This is probably due to the American gold®nch and the possible role of temperature in its better insulating plumage that birds tend to acquire in regulation. Physiol. Zool. 59: 357±368. winter (Marsh & Dawson, 1989), which would reduce Feist, D. D. & White, R. G. (1989). Terrestrial mammals in cold. the thermal conductance. In Advances in comparative and environmental physiology: 327± In conclusion, our ®ndings of seasonal acclimatiza- 354. Wang, L. C. H. (Ed.). Heidelberg: Springer-Verlag. tion in Australian silvereyes show that even for birds Ford, H. A. (1989). Ecology of Birds: an Australian Perspective. Chipping Norton: Surrey Beatty and Sons. exposed to a relatively mild climate, changes in thermal Hart, J. S. (1962). Seasonal acclimatization in four species of small energetics are used to overcome potential energetic wild birds. Physiol. Zool. 35: 224±235. constraints. It suggests that such adaptations are com- Lasiewski, R. C., Weathers, W. W. & Bernstein, M. H. (1967). monly used by small passerines and other birds, and not Physiological responses of the giant hummingbird, Patagona just in species that inhabit areas of harsh, cold climates. gigas. Comp. Biochem. Physiol. 23: 797±813. Maddocks, T. A. & Geiser, F. (1997). 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