Effect of environmental temperature on body temperature and metabolic heat production in a heterothermic rodent, Spermophilus tereticaudus
Department of Biology, Arizona State University, Tempe, AZ 85287-1501, USA
* e-mail: wooden{at}asu.edu
Accepted 25 April 2002
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Summary |
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Key words: thermoregulation, heat transfer, heterothermy, metabolic heat production, body temperature, round-tailed ground squirrel, Spermophilus tereticaudus
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Introduction |
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Endothermic homeothermy also imposes a large energetic burden on the
animal. At rest within the animal's thermoneutral zone, maintenance of the
metabolic machinery necessary for increased activity and thermogenic capacity
results in a basal metabolic rate that is 8-10 times higher than the standard
metabolic rate of a similar-sized ectotherm
(Bennett and Ruben, 1979;
Else and Hulbert, 1981
). When
exposed to air temperatures below the thermoneutral zone, these animals
further increase metabolic rate, as much as eightfold above basal metabolic
rate, to maintain a constant TB
(Hinds et al., 1993
). The
energetic requirements for an endothermic homeotherm to maintain such a
constant TB is a function of the animal's thermal
conductance and the temperature gradient that must be overcome. Small and
poorly insulated animals have the highest area-specific thermal conductances
and, therefore, are most likely to experience conditions in which the
energetic demand of maintaining a constant TB exceeds
supply (e.g. extreme thermal conditions, limited resource availability,
inadequate ability to acquire or process sufficient resources).
Instability of body temperature due to exposure has mostly been studied in
humans and domestic animals (Keller,
1955; Hamilton,
1968
; Edholm,
1978
; Hayward,
1983
; Clark and Edholm,
1985
; Reinertsen,
1996
). For these species as well as other non-domesticated forms
(e.g. Neotoma lepida, Dipodomys merriami; K. M. Wooden, personal
observation), hypothermia of more than 2 °C results in the loss of
coordinated locomotory performance, impairment of physiological function and
loss of consciousness. Hypothermia of more than 5 °C often results in
death. Thus, for many small and poorly insulated animals, survival mechanisms
have evolved that allow them temporarily to abandon tight thermoregulatory
control. Through hibernation, torpor or estivation, these animals reduce
thermoregulatory demand, lower metabolic rate and realize substantial
energetic savings. However, because the TB of most
endothermic homeotherms is tightly coupled to physiological function, allowing
TB to drop also leaves these animals inactive and unable
to respond readily to external stimuli (Schmidt-Nielsen, 1990;
Reinertsen, 1996
).
At least one species of bird (Todus mexicanus,
Mercola-Zwartjes and Ligon,
2000) and several species of mammal (Bradypus cuculliger,
Wislocki, 1933
; Bradypus
griseus, Britton and Atkinson,
1961
; Pipistrellus hesperus,
Bradley and O'Farrell, 1969
;
Myotis thysanodes, Myotis lucifugus,
Studier and O'Farrell, 1972
;
Eptesicus fugcus, Hirshfeld and
O'Farrell, 1976
; Antrozous pallidus, Myotis californicus,
Pipistrellus hesperus, Plecotus townsendii,
Nelson et al., 1977
;
Heterocephalus glaber, Buffenstein
and Yahav, 1991
; Nycticeius humeralis, Lasiurus
intermedius, Genoud,
1993
; Geogale aurita,
Stephenson and Racey, 1993
;
Murina leucogaster ognevi, Choi
et al., 1997
; Spermophilus tereticaudus,
Hudson, 1964
;
Wooden and Walsberg, 2000
)
can, however, maintain normal activity and display no pathological effects
over changes in TB as large as 14 °C. Of these
species, the energetics of this phenomenon has only been studied in the Puerto
Rican today (Todus mexicanus)
(Mercola-Zwartjes and Ligon,
2000
). T. mexicanus remains fully alert, responsive to
external stimuli and capable of flight at body temperatures ranging from 28 to
42 °C. When exposed to an air temperature (Tair) of 15
°C, the body temperature of this species ranges between 32 and 33.4
°C. By lowering TB by only 1.4 °C from 33.4 to 32
°C, this species reduces energetic cost by 28 %. At a
Tair of 30 °C, T. mexicanus maintains an
active-phase TB of only 36.7 °C. This allows them to
expend 33 % less energy for thermoregulation than that required to maintain
the TB reported for other coraciforms of 40 °C
(Prinzinger et al., 1991
).
Our current study addresses the energetics and thermoregulatory ability of
a mammal, the round-tailed ground squirrel (Spermophilus
tereticaudus), that like T. mexicanus relaxes thermoregulatory
limits without becoming inactive. This diurnal rodent inhabits the most barren
areas of the Sonoran and Mohave Deserts, where daytime air temperature ranges
from less than 5 °C in the winter months to 50 °C during the summer
(K. M. Wooden, unpublished data). S. tereticaudus has a very sparse
coat (Walsberg, 1988) and
consequently a very high thermal conductance
(Wooden and Walsberg, 2000
).
Metabolic rate at rest within the thermoneutral zone is approximately 60 % of
that predicted by mass, and this species remains active and alert over body
temperatures ranging from 30 to 42 °C
(Hudson, 1964
;
Wooden and Walsberg, 2000
).
The primary questions addressed by this study are as follows. (i) How does
Tair affect metabolic heat production and
TB? (ii) How much control over TB does
this species have at a given Tair? (iii) How do changes in
TB relate to changes in metabolic heat production? (iv)
Are there energetic savings associated with changes in
TB?
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Materials and methods |
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Within 1 week of capture, all animals were drinking water freely and began gaining mass. At this time, temperature transmitters were inserted into the abdominal cavity and positioned just below the liver (anesthesia, metofane). The incision (approximately 2 cm long) was closed with silk sutures. We began the experimental procedures when all animals had fully recovered from the surgery (2 weeks). Mean body mass during the experimental procedures was 131.4±2.1 g (mean ± S.E.M., N=11).
Procedures
We conducted two studies using the same animals. In both studies,
measurements were taken from post-absorptive animals resting quietly for at
least one 99 % equilibration period of the chamber
(Lasiewski et al., 1966). The
regime of temperature exposure was randomized, and no animal was used on
consecutive days. Studies conducted during the active phase of the animals'
daily cycle were completed between 08:00 h and 17:00 h. Those conducted during
the animal's resting phase were completed between 20:00 h and 05:00 h. The
first study measured metabolic heat production (MHP) and
TB during the active phase, over short-term (approximately
1 h) exposure to air temperatures ranging from 10 to 45 °C. Values of MHP
are the mean of the first 5 min following at least 45 min under the
experimental conditions. Values of TB reported were taken
immediately following metabolic measurements. The second study measured the
same variables over longer periods of exposure to air temperatures below the
thermoneutral zone (during both the active and resting phases of the animals)
to determine the thermoregulatory ability of this species and to quantify
energetic costs. In this study, animals were exposed to air temperatures of
10, 20 and 30 °C for 8 h. Active- and resting-phase measurements were
taken on different days. Measurements of TB were taken
every 20 min. Values reported are the 8 h average TB,min
and TB,max (TB,min and
TB,max are the means of the lowest and highest
TB maintained within 0.2 °C for at least 1 h,
respectively). Metabolic measurements were recorded every 10 min over the 8 h
period. Values reported are the 8 h average maximum and minimum (maximum and
minimum measurements are 5 min averages taken 30 min into the hours in which
the minimum and maximum body temperatures were maintained).
Body temperature
We measured TB (±0.1°C) using temperature
transmitters (AVM Corp., model SM-1) implanted into the abdominal cavity of
the animals and a radiotelemetry receiver (AVM Corp., model LA12-Q). We
converted transmitter output into TB by timing 100 pulses
with a digital stopwatch. Both prior to implantation and after removal from
the animal, we calibrated the transmitters (±0.1°C) in water baths
whose temperatures were measured with a type-T (copperconstantan)
thermocouple (Omega Scientific, model HH23 thermometer, calibrated against ice
baths and mercury thermometers traceable to the NIST). There was no measurable
difference in transmitter calibrations before and after the experiments.
Metabolic rate
Measurements of metabolic rate were made using 800 ml respirometry chambers
constructed of transparent acrylic plastic. Air temperature was regulated by
placing these chambers into a temperature-controlled room. Animals were
exposed to fluorescent lighting that allowed normal vision but was thermally
insignificant (irradiance <3 W m-2) for measurements taken
during their active phase. During the resting phase, measurements were made in
total visual darkness, and subjects were monitored under infrared light using
a CCD camera (Magnavox 18MC205T), Metabolic rate was determined from rates of
CO2 production and O2 consumption. Influent air was
scrubbed of CO2 and dried by an air purifier (Puregas CDA1) before
being sent through rotameters (Omega FL3402C-HRV, calibrated against a
soap-film flowmeter). Flow rates were adjusted so that there was an
approximately 1 % reduction in oxygen concentration, measured at a downstream
oxygen analyzer (Applied Electrochemistry, S-3A). At the lowest flow rate
used, the entire respiratory apparatus equilibrated in 19 min
(Lasiewski et al., 1966). A
150 ml min-1 subsample of gas was dried with anhydrous calcium
sulfate and passed to a CO2 analyzer (LiCor, 6252) which has a
resolution of 1 p.p.m. The analyzer was calibrated daily with both
CO2-free air and a calibration gas known to contain 2840 p.p.m.
CO2. Instrument signals were recorded on a Campbell CR21x
datalogger and averaged at 1 min intervals. Carbon dioxide production was
calculated using equation 3 of Walsberg and Wolf
(1995
) and corrected to STP
(0°C, 101 kPa).
This calculation and subsequent conversion to units of energy requires
knowledge of the respiratory exchange ratio (RER). Carbon dioxide production
and oxygen consumption were recorded and averaged simultaneously using a
Campbell CR21x datalogger. The O2 concentration of air entering and
leaving the chamber was determined from a 50 ml min-1 subsample of
effluent air from the chamber using an Applied Electrochemistry S3a oxygen
analyzer. The oxygen analyzer was calibrated daily, as described by Walsberg
and Wolf (1995), against the
general atmosphere.
Thermal conductance
Total conductance (C) was calculated at ambient temperatures below
thermoneutrality by using the following equation derived, for biological
application, from Fourier's law of heat flow by Burton
(1934):
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Statistical analyses
Statistical analyses were performed using StatView 5.0 for Macintosh.
Analyses were accomplished using a repeated-measures analysis of variance
(ANOVA) followed by a post-hoc multiple-comparison test (Tukey type)
for pairwise comparisons among groups. All reported values are significant at
P<0.05. Values are given as means ±1 S.E.M.
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Results |
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Long-term exposure
There was no difference in body temperature or metabolic heat production
between studies conducted during the active and resting phases of the animals'
daily cycle (P<0.05). Therefore, reported values are for studies
conducted during the active phase only. All animals remained awake and rested
quietly for the entire 8 h at each temperature. At every air temperature,
animals maintained (within 0.2°C), for at least 1 h, significantly
different minimum (TB,min) and maximum
(TB,max) body temperatures (10°C,
F2,16=19.462, P<0.0001; 20°C,
F2,16=43.423, P<0.0001; 30°C,
F2,16=152.726, P<0.0001)
(Fig. 3). There was no apparent
pattern to the direction of TB changes, the number of
times an animal changed TB or the duration for which a
given TB was maintained. TB,min was
constant across all air temperatures at 31.2°C (P<0.05). The 8
h average and TB,max increased from 32.5 and 33.6°C at
10°C to 34.4 and 36.3°C at 30°C respectively (8 h average,
F2,16=36.362, P<0.0001;
TB,max, F2,16=55.697,
P<0.0001). MHP was lower at TB,min than at
TB,max across all air temperatures (10°C,
F2,16=20.584, P<0.0001; 20°C,
F2,16=46.362, P<0.0001; 30°C,
F2,16=106.302, P<0.0001)
(Fig. 4). As
Tair decreased, the MHP corresponding to
TB,min increased from 0.46 W at 30°C to 2.43 W at
10°C (F2,16=213.354, P<0.0001) and that
corresponding to TB,max increased from 0.86 W at 30°C
to 3.23 W at 10°C (F2,14=290.658,
P<0.0001). Mean total thermal conductance across all conditions
was 0.146±0.004 W°C-1 (N=9;
P<0.05).
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Discussion |
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We found that the TB of S. tereticaudus is
much more variable and dependent upon Tair than that of
typical rodents. Within 45 min of exposure to air temperatures ranging from 10
to 45°C, mean body temperatures ranged from 32.1°C to 40.4°C
respectively (Fig. 1). These
animals, however, remained alert and responsive at all body temperatures. One
individual experienced changes in body temperature ranging from 27.8°C at
10°C to 41.0°C at 45°C. The thermal conductance for S.
tereticaudus remained constant under both short-term and long-term
exposure to air temperatures below the thermoneutral zone at approximately
0.14 W°C-1. This value is the same as that from our previous
study in which we found that the thermal conductance of S.
tereticaudus was 45% higher than predicted by Aschoff's
(1981) allometric equation and
was the highest reported of 17 species of rodents ranging in mass from 100 to
200 g as measured during the active phase of their daily cycle
(Wooden and Walsberg,
2000
).
S. tereticaudus can both estivate and enter torpor when
circumstances do not permit the maintenance of energetic balance
(Hudson, 1964); however, they
are commonly found above ground and active year-round
(Dengler, 1967
;
Drabek, 1973
;
Vorhies, 1945
; K. M. Wooden,
personal observation). This diurnal rodent must survive high air temperatures
in the summer and arid conditions throughout most of the year. In an arid
desert environment when Tair is high, allowing
TB to rise above Tair is advantageous
as it maintains the driving force
(TBTair) for non-evaporative
heat loss and conserves body water by eliminating the need for evaporative
cooling. Similarly, when Tair exceeds
TB, a rise in TB reduces the rate of
heat influx (TairTB) and
conserves both the water and energy required to eliminate the incoming heat
through active evaporative cooling. In winter and early spring, S.
tereticaudus faces air temperatures that drop below 5°C (K. M.
Wooden, unpublished data). By allowing TB to drop when
Tair is low (Fig.
1), non-torpid individuals may conserve body water in two ways.
First, as oxygen requirements for metabolic heat production are reduced,
ventilation rate and respiratory water loss should decrease. Second, as body
temperature is lowered, exhaled air is cooler (carrying less water vapor per
unit volume) and transcutaneous water loss presumably decreases as a result of
lowered skin temperature.
Inhabiting the most barren habitats of the Sonoran Desert also subjects
S. tereticaudus to periods of several months in which the only
available vegetation may be creosote bush (Larrea tridentata). This
plant contains toxic phenols (Rhoades and
Cates, 1976; Mabry et al.,
1977
), and dependence upon it as a primary food source may
severely limit energy, nutrient and water intake
(Karasov, 1989
;
Meyer and Karasov, 1989
). By
reducing the gradient between TB and
Tair, S. tereticaudus, in addition to conserving
water, also reduces the energetic cost required to maintain
TB. We estimated the MHP required to achieve a
TB of 37°C using equation 1, setting C=0.14
W°C-1 and TB=37°C. By lowering
TB at air temperatures below the thermoneutral zone,
S. tereticaudus realizes a short-term energetic saving ranging from
0.63 W (18%) at 10°C to 0.43 W (43%) at 30°C
(Fig. 2). It is important to
note that this lowering of TB does not reflect an
inability to generate sufficient heat because the animal is demonstrably
capable of higher rates of heat production
(Fig. 2). Rather, this implies
a controlled mechanism for reducing energetic demand.
The results of long-term exposure to air temperatures between 10 and 30°C offer additional evidence of an ability to adjust energetic expenditure through body temperature regulation. During long-term exposure to air temperatures of 10, 20 and 30°C, animals again demonstrate the ability to generate sufficient heat to raise TB at 20 and 30°C well above that typical of other rodents (37°C) (Fig. 4). By averaging body temperatures over 8 h of 32.5°C at 10°C, 33.5°C at 20°C and 34.4°C at 30°C rather than 37°C, these animals potentially realize long-term energetic savings of 1.1 W (28%), 0.69 W (28%) and 0.35 W (34%) respectively (Fig. 4).
During the 8 h of exposure to each temperature, individuals also demonstrated the ability to vary their body temperature over time by as much as 9.0°C. The occurrences of a minimum and maximum body temperatures at each Tair (during which TB did not vary by more than 0.2°C for at least 1 h) occurred randomly both within the runs of individual animals and among animals. At all air temperatures studied, animals allowed TB,min to drop to a mean of 31.2°C (Fig. 3). The TB,min was significantly lower than the average TB in all cases and correlates to additional energetic savings of 0.41 W (10%) at 10°C, 0.34 W (14%) at 20°C and 0.20 W (20%) at 30°C from that projected to maintain a TB of 37°C (Fig. 4).
Our data show that S. tereticaudus did not maintain a TB typical of other rodents at any air temperature below their thermoneutral zone. We estimate (as described above) that these animals, even at their maximum body temperatures, expended 0.71 W (18%) at 10°C, 0.32 W (13%) at 20°C and 0.16 W (16%) less energy than would be required if they maintained a TB of 37°C. Although these animals did not maintain body temperatures comparable with those other rodents, at each Tair, the maximum body temperature maintained was significantly higher (2.7°C at 10°C, 4.4°C at 20°C and 4.4°C at 30°C) than TB,min (Fig. 3). The reason for this variation in TB at a given Tair is unknown. However, these animals realized a significant energetic savings of 0.8 W (25%) at 10°C, 0.71 W (33%) at 20°C and 0.40 W (47%) at 30°C by maintaining the minimum rather than the maximum TB (Fig. 4).
With respect to avian and mammalian thermoregulation, S.
tereticaudus and the Puerto Rican tody
(Mercola-Zwartjes and Ligon,
2000) are unusual: both species have independently evolved to
remain alert, responsive and active over a very broad range of body
temperatures. This adaptation provides a mechanism to reduce energetic costs
to levels below those required in other birds and mammals. In the light of the
current hypotheses regarding the costs and benefits of homeothermy, this gives
rise to several interesting questions. Are there costs, relative to other
birds and mammals, associated with this adaptation? What mechanisms allow for
the maintenance of physiological function over such a broad range of body
temperatures? Why have not all birds and mammals lowered energetic costs by
expanding their thermoregulatory limits? We suggest that further investigation
at the tissue, cellular and biochemical levels, using these species as models
of comparison, might significantly advance our understanding of mammalian and
avian physiology.
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aschoff, J. (1981). Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp. Biochem. Physiol. 69A,611 -619.
Avery, R. A. (1979). Lizards: a study in thermoregulation. The Institute of Biology's Studies in Biology 109. Baltimore: University Park Press.
Bartholomew, G. A. (1977). Body temperature and energy metabolism. In Animal Physiology: Principles and Adaptations (ed. M. S. Gordon), pp.364 -449. New York: Macmillan.
Bennett, A. F. and Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science 206,649 -654.[Medline]
Block, B. A., Finnerty, J. R., Stewart, A. F. R. and Kidd, J. (1993). Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260,210 -213.[Medline]
Bradley, W. G. and O'Farrell, M. M. (1969). Temperature relations of the western pipistrelle (Pipistrellus hesperus). In Physiological Systems of Semi-arid Environments (ed. C. C. Hoff and M. L. Reidesel), pp.85 -96. Albuquerque: University of New Mexico Press.
Britton, S. W. and Atkinson, W. E. (1961). Poikilothermism in the sloth. J. Mammal. 34, 94-99.
Buffenstein, R. and Yahav, S. (1991). Is the naked mole-rat Heterocephalus glaber an endothermic yet poikilothermic mammal? J. Therm. Biol. 16,227 -232.
Burton, A. C. (1934). The application of the theory of heat flow to the study of energy metabolism. J. Nutr. 7,497 -533.
Burton, A. C. and Edholm, O. G. (1955). Man in Cold Environment. London: Edward Arnold.
Choi, I., Cho, Y., Oh, Y. K., Jung, N. and Shin, H. (1997). Behavior and muscle performance in heterothermic bats. Physiol. Zool. 71,257 -266.
Clark, R. P. and Edholm, O. G. (1985). Responses to cold. In Man and His Thermal Environment, pp. 155-172. London: Edward Arnold.
Cossins, A. R. and Bowler, K. (1987). Temperature Biology of Animals. New York: Chapman & Hall.
Crompton, A. W., Taylor, C. R. and Jagger, J. A. (1978). Evolution of homeothermy in mammals. Nature 272,333 -336.[Medline]
Dengler, W. F. (1967). Contributions toward the life history of Citellus tereticaudus in Arizona. MS thesis, Arizona State University.
Drabek, C. M. (1973). Home range and daily activity of the round-tailed ground squirrel, Spermophilus tereticaudus neglectus. Am. Midl. Nat. 89,287 -293.
Edholm, O. G. (1978). Man hot and cold. In The Institute of Biology's studies in Biology 97. London: Edward Arnold.
Else, P. L. and Hulbert, A. J. (1981). Comparison of the `mammalian machine' and the `reptile machine': energy production. Am. J. Physiol. 240, R3-R9.[Medline]
Genoud, M. (1993). Temperature regulation in subtropical tree bats. Comp. Biochem. Physiol. 104A,321 -331.
Hamilton, J. B. (1968). The effect of hypothermic states upon reflex and central nervous system activity. Yale J. Biol. Physiol. 9, 327-332.
Hayes, J. P. and Garland, T., Jr (1995). The evolution of endothermy: Testing the aerobic capacity model. Evolution 49,836 -847.
Hayward, J. S. (1983). The physiology of immersion hypothermia. In The Nature and Treatment of Hypothermia (ed. R. S. Pozos and L. E. Wittmers), pp.3 -19. Minneapolis: University of Minnesota.
Heinrich, B. (1977). Why have some animals evolved to regulate a high body temperature? Am. Nat. 111,623 -640.
Hensel, H., Brück, K. and Raths, P. (1973). Homeothermic organisms. In Temperature and Life (ed. H. Precht, J. Christophersen, H. Hensel and W. Larcher), pp. 503-761. New York: Springer-Verlag.
Hill, R. W. and Wyse, G. A. (1989). Animal Physiology. New York: Harper & Row.
Hinds, D. S., Baudinette, R. V., MacMillen, R. E. and Halpern,
E. A. (1993). Maximum metabolism and the aerobic factorial
scope of endotherms. J. Exp. Biol.
182, 41-56.
Hirshfeld, J. R. and O'Farrell, M. J. (1976). Comparisons of differential warming rates and tissue temperatures in some species of desert bats. Comp. Biochem. Physiol. 55A, 83-87.
Hudson, J. W. (1964). Temperature regulation in the round-tailed ground squirrel, Citellus tereticaudus. Ann. Acad. Sci. Fenn., Ser. A 15,219 -233.
Karasov, W. H. (1989). Nutritional bottleneck in a herbivore, the desert wood rat (Neotome lepida). Physiol. Zool. 62,1351 -1382.
Keller, A. D. (1955). Hypothermia in the unanesthetized poikilothermic dog. In Physiology of Induced Hypothermia (ed R. D. Dripps), pp.61 -79. Washington: National Academy of Sciences.
Kleiber, M. (1961). The Fire of Life. New York: John Wiley and Sons.
Lasiewski, R. C., Acosta, A. L. and Bernstein, M. H. (1966). Evaporative water loss in birds. I. Characteristics of the open flow method of determination and their relation to estimates of thermoregulatory ability. Comp. Biochem. Physiol. 19,445 -457.
Mabry, T. J., DiFeo, D. R., Jr, Sakakibara, M., Bohnstedt, C. F., Jr and Seigler, D. (1977). The natural products chemistry of Larrea. In Creosote Bush: Biology and Chemistry of Larrea in the New World Deserts (ed. T. J. Mabry, J. H. Hunziker and D. R. DiFeo, Jr), pp. 115-133. Stroudsburg: Dowden, Hutchinson & Ross.
McNab, B. K. (1978). The evolution of homeothermy in the phylogeny of mammals. Am. Nat. 112, 1-21.
Mercola-Zwartjes, M. and Ligon, J. D. (2000). Ecological energetics of the Puerto Rican Tody: heterothermy, torpor and intra-island variation. Ecology 81,990 -1003.
Meyer, M. W. and Karasov, W. H. (1989). Antiherbivore chemistry of Larrea tridentata: effects on woodrat (Neotoma lepida) feeding and nutrition. Ecology 70,953 -961.
Nelson, Z. C., Hirshfeld, J. R., Schreiwes, D. O. and O' Farrell, M. M. (1977). Flight muscle contraction in relation to ambient temperaturein some species of desert bats. Comp. Biochem. Physiol. 56A,31 -36.
Prinzinger, R., Preßmar, A. and Schleucher, E. (1991). Body temperature in birds. Comp. Biochem. Physiol. 99A,499 -506.
Reinertsen, R. E. (1996). Physiological and ecological aspects of hypothermia. In Avian Energetics and Nutritional Ecology (ed. C. Carey), pp.125 -157. New York: Chapman & Hall.
Rhoades, D. F. and Cates, R. G. (1976). Towards a general theory of plant antiherbivore chemistry. Recent Adv. Phytochem. 10,168 -213.
Schmidt-Neilsen, K. (1990). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press. pp. 276-282.
Somero, G. N., Dahlhoff, E. and Lin, E. E. (1996). Stenotherms and eurytherms: mechanisms establishing thermal optima and tolerance ranges. In Animals and Temperature: Phenotypic and Evolutionary Adaptation (ed. I. A. Johnston and A. F. Bennett), pp. 53-78. Cambridge: Cambridge University Press.
Stephenson, P. J. and Racey, P. A. (1993). Reproductive energetics of the Tenrecidae (Mammalia: Insectivora). I. The large-eared tenrec, Geogale aurita. Physiol. Zool. 66,643 -663.
Studier, E. H. and O'Farrell, M. J. (1972). Biology of Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). I. Thermoregulation. Comp. Biochem. Physiol. 41A,567 -596.
Vorhies, C. T. (1945). Water requirements of desert animals in the southwest. Ariz. Agr. Exp. Stat. Tech. Bull. 107,486 -525.
Walsberg, G. E. (1988). Consequences of skin and fur properties for solar heat gain and ultraviolet irradiance in two mammals. J. Comp. Physiol. B 158,213 -221.[Medline]
Walsberg, G. E. and Wolf, B. O. (1995).
Variation in the respiratory quotient of birds and implications for indirect
calorimetry using measurements of carbon dioxide production. J.
Exp. Biol. 198,213
-219.
Wislocki, G. B. (1933). Location of the testes and body temperature in mammals. Q. Rev. Biol. 8, 385-396.
Withers, P. C. (1992). Comparative Animal Physiology. Orlando: Saunders College Publishing. pp.160 -162.
Wooden, K. M. and Walsberg, G. E. (2000).
Effect of wind and solar radiation on metabolic heat production in a small
desert rodent, Spermophilus tereticaudus. J. Exp.
Biol. 203,879
-888.