Nocturnal heterothermy and torpor in the Malachite Sunbird (Nectarinia famosa)
Downs, Colleen T
ABSTRACT.-Heterothermy in birds occurs in species that are generally small and whose diet fluctuates. This study of thermoregulation of Malachite Sunbirds (Nectarina famosa) showed that they have circadian fluctuations in T^sub b^ and VO^sub 2^, as in most birds. Of special importance was the high degree of restphase hypothermy and exhibition of torpor at ambient temperatures of 10 deg C and lower. These patterns are significant because they have not been described in detail for a passerine species. Surgically implanted minimitters were used to measure T^sub b^ continuously and without disturbing the birds. Minimum VOZ during rest phase was 1.70 (mL O^sub 2^ g^sup -1^ h^sup -1^) at 25 deg C. As ambient temperature decreased, VO^sub 2^, minimum during the rest phase did not increase to maintain T^sub b^. No birds remained normothermic during scotophase. At 5 deg C, that resulted in torpor in Malachite Sunbirds with a decrease of 15 deg C in T^sub b^. Birds increased T^sub b^ to active-phase levels with the onset of light. It was difficult to define limits and ranges of physiological parameters associated with observed heterothermy. Individuals showed similar responses; however, those differed with ambient temperature. Malachite Sunbirds conserved energy nocturnally by reducing metabolic rate and, concomitantly, T^sub b^. This plasticity in T^sub b^ shows that daily variations in T^sub b^ of homeotherms are biologically important. Furthermore, this heterothermy (particularly nocturnal hypothermia and torpor) in a small avian species would be important in an unpredictable environment where food resources fluctuate to prevent an energy deficit.
RESUMEN.-La heterotermia ocurre en aves de tamano corporal pequeno que presentan una dieta fluctuante. Este estudio sobre la termorregulacion de Nectarina famosa mostro que, como en la mayoria de las aves, esta especie presenta una fluctuation circadiana de la T^sub b^ y VO^sub 2^. De especial importancia fueron las observaciones sobre el alto grado de hipotermia en la fase de descanso y la exhibicion de torpor a una temperatura menor o igual a 10 deg C. Estos patrones son de interes ya que no se han descrito previamente en detalle para aves paserinas. Se utilizaron medidores implantados quirurgicamente para medir la T^sub b^ en forma continua sin perturbar a las aves. El valor minimo de VO^sub 2^ registrado durante la fase de descanso fue de 1.70 (mLO^sub 2^ g^sup -1^ h^sup -1^) a 25 deg C..
Con la disminucion de la temperatura ambiental, el valor de VO^sub 2^ minimo durante la fase de descanso no aument6 para mantener la T^sub b^. Ningun ave permaneci6 normotermica durante la escotofase. A 5 deg C esta especie entro en torpor con una disminucion de 15 deg C en la T^sub b^. Las aves incrementaron la T^sub b^ a niveles correspondientes a la fase activa con la presencia de luz. Fue dificil definir los If mites y rangos de los parimetros fisiologicos asociados con la heterotermia observada. Los individuos mostraron respuestas similares, pero estas variaron con la temperatura ambiental. N. famosa conserva energia durante la noche reduciendo la tasa metabolica y, concomitantemente, la T^sub b^. Esta plasticidad en la T^sub b^ muestra que su variacion diaria en homeotermos es biologicamente importante. Esta heterotermia (hipotermia nocturna y torpor) debiera ser importante para aves de pequeno tamano corporal para prevenir un deficit de energia en ambientes impredecibles donde los recursos alimenticios fluctuan.
Torpor is polyphyletic and evolved independently in many bird species when environmental conditions required a reduction of high endothermic metabolism for survival (Geiser 1998). Birds use a variety of thermoregulatory and behavioral options to maintain a positive energy balance (Reinertsen 1996). Small homeotherms have higher energetic demands with increased cold (Withers 1992). That requires physiological adjustments in body temperature (Tb) and metabolic rate to minimize energy loss.
Many bird species (especially small birds) exhibit nocturnal hypothermia that is characterized by a fall of T^sub b^ at night of 5 deg C (Whittow 1976, Prinzinger et al. 1991, Refinetti and Menaker 1992, Geiser 1998). The benefit of that plasticity in T^sub b^ is energy savings accrued by reduction in metabolic rate (Reinertsen 1996, Maddocks and Geiser 1997). Those changes in T^sub b^ have been categorized as “nocturnal hypothermia” or “torpor.” Reduction in T^sub b^ is less in nocturnal hypothermia than torpor, although both are characterized by the same physiological patterns: decreased T^sub b^ during entry phase, followed by a period of low T^sub b^, and then a spontaneous arousal (Reinertsen 1996). “Hypothermia” has been defined as any core temperature below the set range specified for normal active state of the species, whereas “torpor” is a state of inactivity and reduced responsiveness (Commission for Thermal Physiology of IUPS 1987). Hypothermia is usually described when there is shallow depression of T^sub b^ (30-38 deg C) and a reduction in metabolic rate (Reinertsen 1996, Maddocks and Geiser 1997). Torpor is characterized by far greater depression of T^sub b^ (4-30 deg C) and metabolic rate (Reinertsen 1996, Maddocks and Geiser 1997).
Yet torpor (following the definitions above) has not been described in passerine birds, although several species (nine families) display nocturnal hypothermia (e.g. manakins, sunbirds, honeyeaters, and silvereyes; Reinertsen 1996, Maddocks and Geiser 1997). Passerines usually do not enter hypothermia at ambient temperatures >20 deg C and do not let T^sub b^ fall below 30 deg C (Reinertsen 1996, Maddocks and Geiser 1997).
Sunbirds (Order Passeriformes, Family Nectariniidae) are small (
Malachite Sunbirds (Nectarinia famosa; 15-21 g) experience a range of ambient temperatures from 0 to 35 deg C, with daily fluctuation as great as 20 deg C. (Skead 1967, Maclean 1993). We investigated thermoregulation in this nectarivorous passerine, and tested specifically for nocturnal hypothermy and torpor.
Methods.-Five adult male Malachite Sunbirds were captured near Creighton, KwaZulu-Natal, South Africa (29 deg 50’40″S, 29 deg 40’28″E) under permit from the KwaZulu-Natal Wildlife during September-October 1999 using mist nets. Birds were color banded for identification and transferred to the School of Botany and Zoology, University of Natal, Pietermaritzburg, South Africa, where they were housed individually in cages (1 x 0.35 x 0.5 m) and kept in a constant-environment room (25 deg C, 12 h light, 12 h dark). Twice a day, birds were fed a sugarprotein mixture (Downs and Perrin 1996). Water and fruit flies (Drosophila sp.) were made available ad libitum. Cages were cleaned daily. All experiments were conducted during December 1999.
Body temperature was measured using temperature-sensitive radio transmitters (Mini-mutter Model XM in a modified smaller capsule; Mini Mitter Company Inc., Bend, Oregon). The wax-coated telemeters (1.1-1.3 g) were calibrated with a mercury thermometer (0.05 deg C) over a range of 5-42 deg C. These were surgically implanted into the peritoneal cavity of the birds under inhalation anaesthesia (Isoflorane; induction 2.5% in O^sub 2^; maintenance 2.0% in O^sub 2^;O^sub 2^ flow rate, ~1.0 L min^sup -1^). Birds were given a recovery period of three days before they were weighed and placed individually in perspex respirometers (10.5 x 13.5 x 21.5 cm). Birds were placed in respirometers between 1500 and 1600 h. Oxygen consumption (VO^sub 2^) and T^sub b^ were recorded from 1600 to 0700 h the following morning, after which birds were returned to their cages and fed. That was repeated for a range of ambient temperatures (5-30 deg C). The sequence of ambient temperatures was as follows: 25, 20, 15, 10, 5, 28, and 33 deg C. At 33 deg C, birds were removed from the respirometers at 2045 h to avoid excessive heat stress because birds had shown increased evaporative water loss. Birds were food-deprived during measurements, but were fed just prior to the experiment; they naturally do not feed during the dark period (onset of dark was at 1800 h). During the active phase, O^sub 2^ consumption did not include flight because respirometers were large enough to allow birds to only perch and change position.
Respirometers, together with a control respirometer, were placed in a sound-proof temperature cabinet (1 m^sup 3^) with light-dark photoperiods set the same as the constant-environment room. Radio signals from telemeters were detected by antennae surrounding each respirometer. VO^sub 2^ (using a flowthrough system) and T^sub b^ were measured simultaneously and recorded on computer using a system designed by B. G. Lovegrove. Detailed description of the O^sub 2^ and temperature setup, measurements, and calibrations are presented elsewhere (Boix-Hinzen and Lovegrove 1998, Lovegrove et al. 2001, McKechnie and Lovegrove 2001). Air was drawn through the respirometers at flow rates chosen to maintain
VO^sub 2^ and T^sub b^ were recorded every 6 min for each bird-that is, 10 measurements per hour. VO^sub 2^ was corrected for standard temperature and pressure and expressed as a mass-specific value (Lovegrove et al. 2001, McKechnie and Lovegrove 2001). Mean hourly VO^sub 2^ and T^sub b^ values were calculated using each value for all individuals (n = 5). Minimum and maximum mean hourly VO^sub 2^ and T^sub b^ values were determined using those mean values.
STATISTICA (Statsoft, Tulsa, Oklahoma) software was used for all statistical analyses. All values recorded for each individual were used in tests using repeated-measures ANOVA.
Results.-Mean daily body mass of the five birds on any experimental day ranged from 16.20 (SE +/0.40) to 16.76 g (SE +/- 0.24) during experimental trial days. There was no significant difference in daily body mass of individuals between different trials at the various ambient temperatures (repeated-measures ANOVA F = 1.57, df = 7 and 21, P > 0.05).
During the night (rest phase, or “scotophase”), none of the Malachite Sunbirds remained normothermic. In response to ambient temperature change, all Malachite Sunbirds showed similar changes in T^sub b^ and VO^sub 2^, as shown by the small standard error (Figs. 1 and 2). All birds showed similar circadian changes in T^sub b^ and VO^sub 2^ (Figs. 1-3). Some of those changes are illustrated in Figure 4 for individual 5.
With onset of dark, all T^sub b^ decreased to a level where VO^sub 2^ was 1.2-1.6x greater than the mean minimum VO^sub 2^ (Table 2) with Tb then maintained at that level for 5-6 h (i.e. there was a single bout of decreased T^sub b^. Thereafter, T^sub b^ increased rapidly back to normothermic levels with onset of light, or active phase. The greatest changes in T^sub b^ occurred at ambient temperatures
As a consequence of patterns observed at each ambient temperature, it was difficult to generalize limits and ranges of T^sub b^, minimum VO^sub 2^, or hypothermictorpor bout length. Malachite Sunbirds, however, showed a similar response among individuals at each ambient temperature.
Malachite Sunbirds showed nocturnal hypothermy. At ambient temperatures >10 deg C, Malachite Sunbirds showed heterothermy with controlled restphase hypothermia, whereas at 5-10 deg C they went into torpor. Although mean values of minimum resting T^sub b^ showed a broad range (from 26.77 to 39.56 deg C over the range of ambient temperatures tested, with lower values measured at the lower range of ambient temperature), there was little individual variation at particular ambient temperatures (Table 1, Figs. 1 and 3). Consequently, T^sub b^ is illustrated showing mean minimum rest phase (Beta) and mean maximum active phase (alpha) values of the five birds at the respective ambient temperatures (Fig. 1), and for each temperature showing mean hourly rates (Fig. 3). The lowest T^sub b^ recorded in a particular individual was 25.37 deg C at an ambient temperature of 5 deg C. Mean values of T^sub b^ during active phase showed less variation compared with rest phase, and maximum mean hourly values ranged from 41.26 to 43.34 deg C over the range of ambient temperatures tested (Table 1, Figs. 1 and 4).
Cooling rates showing the linear decrease of Tb at onset of scotophase were calculated for each ambient temperature (Fig. 1). As expected, cooling rates were greatest at lower ambient temperatures (Table 3).
Heating rate (Table 4) was greatest at onset of light with a 4-5 deg C increase in T^sub b^ within an hour, especially at lower ambient temperatures (Fig. 3). However, at 5 and 10 deg C, that heating rate was slow initially and took several hours. Heating at light onset rapidly reached active-phase levels of T^sub b^.
As with T^sub b^ at different ambient temperatures, VO^sub 2^ decreased to a minimum level with onset of dark and was then maintained at that level for most of the rest phase. Thereafter it increased linearly back to normothermic levels with a rapid elevation at onset of light. The lowest minimum mean resting VO^sub 2^ was 1.70 mL O^sub 2^ g^sup -1^ h^sup -1^ at 25 deg C (Fig. 2, values are shown as mean SE because there was little individual variation; n = 5), which is 90% of expected passerine values (Withers 1992). Minimum resting VO^sub 2^ did not increase linearly with decreased ambient temperature as is expected for an endotherm (Table 2, Figs. 2-4). Therefore, it was difficult to describe a thermoneutral zone. However, there was no significant difference in resting VO^sub 2^ between 25 and 33 deg C (Scheffe test, P > 0.05). At lower ambient temperatures, Malachite Sunbirds’ VO^sub 2^ values decreased to levels 1.3-1.7x greater than minimum resting VO^sub 2^ (Table 2, Figs. 2-4).
Active-phase metabolic rate increased linearly with change in ambient temperature. Maximum active-phase VO^sub 2^ was 8.75 mL O^sub 2^ g^sup -1^ h^sup -1^ at 5 deg C; however, birds showed greatest reduction between active and rest phase at that value (Table 2). Percentage reduction in metabolic rate between active and rest phase ranged from 51.8-68.1% at temperatures
Energy conservation was determined during scotophase by calculating an hourly energy consumption. All VO^sub 2^ values were multiplied by 20.083 x 10^sup 3^ kJ after Schmidt-Nielsen (1990). Because no birds remained normothermic, reduction in hourly energy at each ambient temperature was calculated as maximum active-phase energy required to maintain normothermic levels minus hourly minimum energy value, then expressed as a fraction of maximum active-phase energy and converted to a percentage. Trends in energy conservation are shown in Figure 5, which shows that nocturnal hourly energy savings were ~60% at each ambient temperature during scotophase. However, at lower ambient temperatures, nocturnal energy savings accrued were not sufficient to offset energy loss. For example, total nocturnal energy expended at 5 deg C was 83% greater than that at 25 deg C.
Minimal thermal conductance (C^sub min;^ Aschoff 1981) was calculated for each VOz and Tb measured simultaneously. This showed circadian fluctuation as well as decreased levels at lower ambient temperatures. During scotophase, there was no significant difference in thermal conductance
Discussion.-Heterothermy in birds occurs in species that are generally small and whose diet fluctuates (Geiser 1998). Malachite Sunbirds have circadian fluctuations in T^sub b^ and VO^sub 2^ as in most birds. Of special importance was the high degree of rest-phase hypothermy and exhibition of torpor at ambient temperatures of =
Individual Malachite Sunbirds showed similar patterns of change in T^sub b^ and VO^sub 2^ at each ambient temperature. However, those patterns differed between respective ambient temperatures. With decreased ambient temperatures, they decreased both T^sub b^ and VO^sub 2^ during resting phase only. There was an initial period of linear cooling, followed by a period of T^sub b^ maintained at that low value, then increased T^sub b^ near the arousal period. They decreased VO^sub 2^ at onset of scotophase to values slightly higher than minimum mean resting VO^sub 2^ at 25 deg C, accumulating nocturnal energy savings of ~60%, compared to birds that maintain normothermic T^sub b^. Although there were great differences in active and resting T^sub b^ at ambient temperatures
At ambient temperatures >25 deg C, circadian responses of Malachite Sunbirds were similar to Silvereyes (Zosterops lateralis; Maddocks and Geiser 1997) and Lesser Double-collared Sunbirds (Nectarina chalybea; Leon and Nicolson 1997). However, neither of those species showed the unique regulated and exaggerated depression of T^sub b^ and VO^sub 2^ (i.e. torpor) found in Malachite Sunbirds at lower ambient temperatures. Level of controlled heterothermy shown by Malachite Sunbirds indicates very advanced thermoregulatory ability.
At low ambient temperatures, most bird species increase heat production to achieve thermal balance (Dawson and O’Connor 1996, Maddocks and Geiser 1997). However, others such as hummingbirds and mousebirds decrease Tb passively as a consequence of decreased VO^sub 2^ during scotophase (Dawson and Hudson 1970, McKechnie and Lovegrove 2001). Degree of cooling is primarily determined by body mass, surface area, and conductance, and follows a Newtonian cooling curve (Dawson and Hudson 1970). McKechnie and Lovegrove (2001) observed that this nocturnal heterothermia was inconsistent with those described for typical avian torpor bouts (Lyman et al. 1982) in White-backed Mousebirds (Colius colius) because T^sub b^ decreased through the night, increasing at the end of scotophase. Rate of cooling in Malachite Sunbirds was an immediate response to decreased VO^sub 2^, which then plateaued in a maintenance phase. Sunbirds did not abandon temperature regulation. Both White-backed Mousebirds and Malachite Sunbirds generated endogenous heat at the end of scotophase even when T^sub b^ was
Increase in T^sub b^ at the end of scotophase, sometimes described as “arousal from hypothermia,” results in T^sub b^ being raised back to daytime values. This warm up is a function of heat production and heat loss (Reinertsen 1996). Birds rewarm themselves by endogenous heat production (Geiser 1998). At temperatures >5 deg C, Malachite Sunbirds showed a dramatic increase in metabolic rate during arousal. Of particular interest is ability of birds to raise T^sub b^ from resting-phase to active-phase levels in a short period of time. Those were accompanied by dramatic increases in O^sub 2^ consumption over relatively short periods, suggesting involvement of a heat-generating mechanism. However, at Y5 deg C, heating occured over several hours and in two phases. The daily cycle of T^sub b^ is clearly keyed to photoperiod and that requires further investigation. Malachite Sunbirds show some additional form of heat generation because VO^sub 2^ increased greatly. Nonshivering thermogenesis in birds is controversial because its mechanisms, sites, and mediators are not as detectable as in mammals (Dawson and O’Connor 1996).
The level of energy storage in birds is related to body mass. The lower the energy storage in birds (e.g. Hummingbirds [Hainsworth et al. 1977] and Willow Tits [Parus montanus; Reinertsen and Haftorn 1983]), the greater necessity that overnight energy expenditure needs to be reduced, with concomitant effects on magnitude of change of T^sub b^. Amount of energy saved is dependent on T^sub b^, ambient temperature, duration of lowered T^sub b^, and body mass. That results in energy savings of 85% in hummingbirds (Kruger et al. 1982). In Malachite Sunbirds, the energy savings accrued differed at the respective ambient temperatures but were as much as 60% higher than if birds remained normothermic at each respective ambient temperature. Although savings may be far less in other species, it may affect survival or foraging requirements (Reinertsen 1996). It therefore appears that many avian species, including some passerines, use that mechanism of hypothermy to reduce energy deficits, especially during exposure to more demanding nocturnal ambient temperatures. Furthermore, Malachite Sunbirds do not have a crop for food storage (Mbatha and Downs 2002).
Malachite Sunbirds show adaptive heterothermy-in particular, controlled rest-phase hypothermia and torpor. Their plasticity in T^sub b^ and VO^sub 2^ permitted energy savings compared to birds trying to maintain normothermic levels, although that varied with ambient temperature. This heterothermy, particularly nocturnal hypothermia or torpor, would be particularly important in reducing energy deficits in an unpredictable environment where food resources and daily ambient temperatures fluctuate.
Acknowledgments..-The KwaZulu-Natal Conservation Services gave permission for bird capture and maintenance. We thank Dale Forbes and Robyn Van Dyk for assistance with bird netting. We are grateful to Kelly Brookes, Kwezi Mzilikazi, and Jaishree Raman for their excellent technical support. We thank Dr. Barry Lovegrove for use of measurement equipment, and Dr. Rob Slotow for comments on the manuscript.
ASCHOFF, J. 1981. Thermal conductance in mammals and birds: Its dependence on body size and circadian phase. Comparative Biochemistry and Physiology A 69:611-619.
BARTHOLOMEW, G. A., T. R. HOWELL, AND T. J. CADE. 1957. Torpidity in the White-throated Swift, Anna’s Hummingbird and Poor-will. Condor 59: 145-155.
BECH, C., A. S. ABE, J. F STEFFENSEN, M. BERGER, AND J. E. P. W. BICUDO. 1994. Multiple nightly torpor bouts in hummingbirds. Pages 323-328 in Intergrative and Cellular Aspects of Autonomic Functions: Temperature and Osmoregulation (K. Pleschka and R. Gerstberger, Eds.). John Libbey Eurotext, Paris, France.
BICUDO, J. E. P. W. 1996. Physiological correlates of daily torpor in hummingbirds. Pages 293-311 in Animals and Temperature, Phenotypic and Evolutionary Adaptation (I. A. Johnston and A. E Bennett, Eds.). Cambridge University, Cambridge, United Kingdom.
BOIX-HINZEN, C., AND B. G. LOVEGROVE. 1998. Circadian metabolica and thermoregulatory patterns of Red-Billed Wood-Hoopoes (Phoeniculus purpureus): The influence of huddling. Journal of Zoology (London) 244:33-41.
CHEKE, R. A. 1971. Temperature rhythms in African montane sunbirds. Ibis 113:500-506. COMMISSION FOR THERMAL PHYSIOLOGY OF THE IN
TERNATIONAL UNION OF PHYSIOLOGICAL SCIENCES. 1987. Glossary of terms for physiology, 2nd ed. Pflugers Archiv 410:567-587.
DAWSON, W. R., AND J. W. HUDSON. 1970. Birds. Pages 223-310 in Comparative Physiology of Thermoregulation, Invertebrates and Nonmamma
lian Vertebrates, vol. 1 (G. C. Whittow, Ed.). Academic Press, New York.
DAWSON, W R., AND T. P O’CONNOR. 1996. Energetic features of avian thermoregulatory responses. Pages 85-124 in Avian Energetics and Nutritional Ecology (C. Carey, Ed.). Chapman and Hall, New York.
DOWNS, C. T., AND M. R. PERRIN. 1996. Sugar preferences of some southern African nectarivorous birds. Ibis 138:455-459.
GEISER, F. 1998. Evolution of daily torpor and hibernation in birds and mammals: Importance of body size. Clinical and Experimental Pharmacology and Physiology 25:736-740.
HAINSWORTH, F. R., B. G. COLLINS, AND L. L. WOLF. 1977. The function of torpor in hummingbirds. Physiological Zoology 50:215-222.
KRUGER, K., R. PRINZINGER, AND K. L. SCHUCHMANN. 1982. Torpor and metabolism in hummingbirds. Comparative Biochemistry and Physiology A 73: 679-689.
LEON, B., AND S. W. NICOLSON. 1997. Metabolic rate and body temperature of an African sunbird, Nectarina chalybea: Daily rhythm and the effect of ambient temperature. South African Journal of Zoology 32:31-36.
LOVEGROVE, B. G., J. RAMAN, AND M. R. PERRIN. 2001. Heterothermy in elephant shrews, Elephantulus spp. (Macroscelididea): Daily torpor or hibernation. Journal of Comparative Physiology B 171:1-10.
LYMAN, C. P., J. S. WILLIS, A. MALAN, AND L. C. H. WANG. 1982. Hibernation and Torpor in Mammals and Birds. Academic Press, New York.
MACLEAN, G. L. 1993. Roberts’ Birds of Southern Africa, 6th ed. John Voelcker Bird Book Fund, Cape Town, South Africa.
MADDOCKS, T. A., AND F. GEISER. 1997. Energetics, thermoregulation and nocturnal hypothermia in Australian Silver-eyes. Condor 99:104-112.
MBATHA, K. R., AND C. T. DOWNS. 2002. Nectar passage and gut morphology in the Malachite Sunbird and the Black-capped Lory: Implications for feeding. Ostrich 73:in press.
McKECHNIE, A. E., AND B. G. LOVEGROVE. 2001. Thermoregulation and the energetic significance
of clustering behavior in the White-backed Mousebird (Colius colius). Physiological and Biochemical Zoology 74:238-249.
PRINZINGER, R., I. LUBBEN, AND K. L. SCHUCHMANN. 1989. Energy metabolism and body temperature in 13 sunbird species (Nectariniidae). Comparative Biochemistry and Physiology A 92:393402.
PRINZINGER, R., A. PRESSMAR, AND E. SCHLEUCHER. 1991. Body temperature in birds. Comparative Biochemistry and Physiology A 99:499-506.
PRINZINGER, R., T. SCHAFER, AND K. L. SCHUCHMANN. 1992. Energy metabolism, respiratory quotient and breathing parameters in two convergent small bird species: The Fork-tailed Sunbird Aethopyga christinae (Nectariniidae) and the Chilean hummingbird Sephanoides sephanoides (Trochilidae). Journal of Thermal Biology 17:7179.
REFINETTI, R., AND M. MENAKER. 1992. The circadian rhythm of body temperature. Physiology and Behaviour 51:613-637.
REINERTSEN, R. E. 1996. Physiological and ecological aspects of hypothermia. Pages 125-157 in Avian Energetics and Nutritional Ecology (C. Carey, Ed.). Chapman and Hall, New York.
REINERTSEN, R. E., AND S. HAFTORN. 1983. Nocturnal hypothermia and metabolism in the Willow Tit, Parus montanus, at 63 deg N. Journal of Comparative Physiology B 151:109-118.
SCHMIDT-NIELSEN, K. 1990. Animal Physiology: Adaptation and Environment, 4th ed. Cambridge University Press, New York.
SKEAD, C. J. 1967. The Sunbirds of Southern Africa. A. A. Balkema, Cape Town, South Africa. WITHERS, P. C. 1992. Comparative Animal Physiolo
gy. Saunders, Sydney, Australia.
WHITTOW, G. C. 1976. Regulation of body temperature. Pages 146-173 in Avian Physiology, 3rd ed. (P. D. Sturkie, Ed.). Springer-Verlag, Berlin, Germany.
Received 01 September 2000, accepted 12 August 2001.
Associate Editor: W. H. Karasov
COLLEEN T. DOWNS1 AND MARK BROWN
School of Botany and Zoology, University of Natal, Private Bag X01, Scottsville, Pietermaritzburg
3209, South Africa
1 E-mail: email@example.com
Copyright American Ornithologists’ Union Jan 2002
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