Body temperature and locomotor capacity in a heterothermic rodent
School of Life Sciences, Arizona State University, Tempe, AZ 85287-4601, USA
* Author for correspondence (e-mail: wooden{at}asu.edu)
Accepted 23 September 2003
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Summary |
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Key words: body temperature, thermoregulation, heterothermy, locomotor capacity, sprint speed, limb cycling frequency, force production, round-tailed ground squirrel, Spermophilus tereticaudus
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Introduction |
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Although endothermic homeothermy is one of the most significant
evolutionary alterations involving the relationship between an animal and its
environment, it comes with several tradeoffs to the animal. Endothermic
homeothermy may offer profound ecological advantages, yet imposes a large
energetic burden on the animal (Bennett and
Ruben, 1979; Else and Hulbert,
1981
). Endothermic homeothermy may also provide a steady state for
physiological and biochemical functions, yet restricts the range of body
temperatures over which the animal can remain active or even survive
(Hochachka and Somero,
1984
).
Under most circumstances, endothermic homeotherms are able to maintain
Tb. However, when 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), these animals typically respond in one of two
ways. Some birds and mammals enter a state of torpor or hibernation, lowering
their energetic demand by temporarily, yet substantially, reducing
Tb. The Tb of most endothermic
homeotherms, however, is tightly coupled to physiological function, and
allowing Tb to drop also leaves these animals inactive and
unable to respond readily to external stimuli
(Schmidt-Nielsen, 1990;
Reinertsen, 1996
). Most other
birds and mammals have no such mechanism by which to lower their energetic
demand. For these animals, hypothermia leads to the pathological impairment of
physiological function. Complex functions such as coordinated locomotor
performance usually become impaired at a drop in Tb of as
little as 2°C. A drop in Tb of greater than 5°C
commonly leads to widespread physiological impairment and often death
(Keller, 1955
;
Hamilton, 1968
;
Edholm, 1978
;
Hayward, 1983
;
Clark and Edholm, 1985
;
Reinertsen, 1996
).
Although the inability to maintain Tb results in either
the suppression or loss of physiological function for most birds and mammals,
some species appear to remain alert, responsive and active over changes in
Tb of as much as 14°C (see references in
Wooden and Walsberg, 2002). By
regulating Tb over such a wide range, these species can
reduce thermoregulatory costs to levels below those required in other birds
and mammals and thus reduce their overall energetic demand
(Mercola-Zwartjes and Ligon,
2000
; Wooden and Walsberg,
2002
). These species, however, do not enter a torpid state or
display any pathological effects with such large changes in body temperature
as other birds and mammals do. This raises some very interesting questions. Do
these species actually maintain physiological function across this wide range
of body temperatures? Is strict homeothermy necessary to maintain
physiological function by birds and mammals? Why cannot all birds and mammals
lower energetic costs by expanding their thermoregulatory limits?
One of the first signs that an endothermic homeotherm is unable to maintain
Tb is the loss of coordinated locomotor performance.
Although coordinated locomotor ability among these heterothermic species
appears to be maintained over this broad range of body temperatures, this has
not yet been quantified. Many investigators have shown that the effects of
changes in Tb on the locomotor performance of mammals are
similar to those of poikilothermic animals and can be attributed to losses of
function at the muscle (Cullingham et al.,
1960; Close and Hoh,
1968
; Ranatunga,
1977
,
1980
,
1982
,
1984
,
1998
;
Buller et al., 1984
;
Huey and Kingsolver, 1989
;
Bennett, 1990
;
Faulkner et al., 1990
;
Johnston et al., 1990
;
Marsh, 1990
;
Rall and Woledge, 1990
;
Rome, 1990
;
Rome et al., 1990
;
Marden, 1995
;
Xiang et al., 1996
),
peripheral nervous system (PNS; Chatfield
et al., 1948
; Paintal,
1965
; Miller and Irving,
1967
; Jensen,
1972
; MacDonald,
1981
; Montgomery and
MacDonald, 1990
) and/or central nervous system (CNS;
Brooks et al., 1955
;
Roots and Prosser, 1962
;
Hamilton, 1968
;
Friedlander et al., 1976
;
Budnick et al., 1981
;
Oro and Haghighi, 1992
;
MacKenzie et al., 1995
).
Therefore, these birds and mammals should also face a cost to locomotor
ability associated with the relaxation of thermoregulatory limits.
Spermophilus tereticaudus, a small desert rodent, inhabits the
most barren habitats of the Sonoran and Mohave deserts, where daytime air
temperature ranges from less than 5°C in the winter months to as much as
50°C during the summer (K. M. Wooden, unpublished data).
Tb of S. tereticaudus is much more variable and
dependent upon air temperature than that of typical rodents. The
Tb of alert and active animals can drop as low as
27.8°C within 45 min of exposure to an air temperature of 10°C. The
same period of exposure at an air temperature of 45°C can cause
Tb to rise to as much as 41.0°C
(Wooden and Walsberg, 2002).
S. tereticaudus lowers energetic expenditure as much as 50% through
this relaxation of thermoregulatory limits
(Wooden and Walsberg, 2002
).
This species also remains active, alert and responsive across this range of
body temperatures (Hudson,
1964
; Wooden and Walsberg,
2000
,
2002
). In the present study,
we test the hypothesis that this species does experience a significant loss in
locomotor capacity associated with the relaxation of thermoregulatory
limits.
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Materials and methods |
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Body temperature measurements
We measured Tb (±0.1°C) using temperature
transmitters (Mini Mitter, XM-FH; Mini Mitter Co., Inc., Bend, OR, USA;
accurate to 0.1°C) surgically implanted into the abdominal cavity of the
animals. Transmitters are 1.5 cm-longx1 cm-wide cylinders coated with
medical grade silicon rubber (Sylgard). They weigh approximately 1.5 g, or
less than 2% of body mass. Transmitter output was received with an AM radio
and converted 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 (copper-constantan) thermocouple
(model HH23 thermometer, calibrated against ice baths and mercury thermometers
traceable to the NIST; Omega Scientific, Tarzana, CA, USA). There was no
measurable difference in transmitter calibrations before and after the
experiments.
Surgical procedures
Surgery was performed under aseptic conditions. Animals were anesthetized
using metophane. Transmitters were sterilized by immersion in Cidex solution
(Advanced Sterilization Products, Miami, FL, USA) and rinsed with saline
solution prior to implantation. Transmitters were positioned between the liver
and stomach through an incision approximately 1.5 cm wide in the lateral
abdominal wall. The abdominal wall was closed using 4.0 silk sutures. The
dermis and epidermis were closed using surgical staples. Animals were allowed
to recover for 7-10 days and had returned to, at minimum, their mass at the
time of capture prior to experimental use. Mean body mass during the
experimental procedures was 131.4±2.1 g (mean ±
S.E.M., N=21).
Experimental procedures
We tested all animals at body temperatures of 30-32°C, 36-38°C and
40-42°C, randomizing the sequence of temperature exposure for each animal.
We brought the animals to the desired Tb by placing them
in a walk-in environmental chamber for 30-60 min. The environmental chamber
was set at 10°C to achieve a Tb of 30-32°C, at
35°C to achieve a Tb of 36-38°C and at 45°C to
achieve a Tb of 40-42°C. Experiments were conducted on
a 5 m-longx10 cm-wide track at room temperature (23°C). One side
wall of the track was made of clear acrylic plastic and the other side wall
was made of plywood with markings every centimeter. The track was lined with a
short-napped carpet to maximize traction. A darkened box at the end of the
track served as a target refuge into which the animals could escape from the
sound of compressed air hissing out of a plastic tube at the beginning of the
track. For three days prior to the start of the experiments, animals were run
on the track to familiarize them with the track and accustom them to the
procedure. All experimental procedures were completed between 08:00 h and
17:00 h, and no animal was used for more than one experimental condition per
day or on consecutive days. All animals were tested three times in one day at
each Tb and the results reported are the maximum values
that an individual achieved.
Sprint speed and limb cycling frequency
Animals were video taped (Panasonic camera model 456) at a rate of 60
frames s-1 as they ran along the track. Framing rates were measured
continuously by simultaneously recording a digital stopwatch. Upon removal
from the environmental chamber, animals were immediately placed on the track,
Tb was taken and the animal was stimulated to run by the
sound of compressed air hissing out of a plastic tube at the beginning of the
track and the sight of a darkened refuge at the end of the track.
Tb was taken again at the end of each run and the animal
was returned to the environmental chamber for a minimum of 30 min as it
awaited its next trial at that Tb range. Frame-by-frame
analysis of the films was performed with a Desktop Editor video cassette
recorder (Panasonic Model AG-1980). Results reported from this experiment
include maximum sprint speed (m s-1) achieved over any 1 m section
of track and limb cycling frequency for at least four strides over that same
portion of the run.
Force production
Upon removal from the environmental chamber, animals were placed into a
nylon harness fitted around the body and secured snugly with VelcroTM.
The harness was constructed to fit over the torso and not interfere with limb
motion or respiration. As soon as the animal was placed on the track, body
temperature was taken and the harness was attached to a thin wire that ran
over pulleys and connected to 5 m of fine-linked chain, piled vertically below
the pulley, on the floor. The animal was stimulated to start pulling by the
sound of compressed air hissing out of a plastic tube at the beginning of the
track and the sight of a darkened refuge at the end of the track. As the
animal proceeded down the track, it lifted a greater length of chain (greater
mass) off the floor. Each animal was video-taped and the maximum distance the
animal was able to move itself down the track was recorded. Maximum distance
pulled equaled the maximum length of chain lifted and was determined as the
point at which any further attempt to progress forward resulted in the weight
of the chain pulling the animal backwards. The opposing force was the weight
of the chain lifted, calculated as the product of the maximum number of links
of chain lifted and the mass of each link. Self-lubricating ball-bearing
pulleys were used to minimize frictional resistance. A chain with links that
were 1.2 cm long and weighed 0.92 g provided sufficient opposing force for
most animals. Several of the larger animals, however, required a chain with
links that were 2.2 cm long and had a mass of 2.56 g. In each case, the
resolution of the weight of a single link to the weight lifted was less than
1%. Body temperature was again measured and compared with that prior to the
run. At the beginning and end of each day, calculated forces at various
intervals along the track were compared with those measured by a force
displacement transducer (model FT03; Grass, West Warwick, RI, USA) calibrated
against known weights. The calculated force differed from that measured by the
force transducer by less than 1%. Results reported are the individual's
maximum force exerted.
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. Values presented are means ±
S.E.M. (N=21).
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Results |
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|
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Mean Tb during measurements of force production was 30.8±0.2°C, 36.9±0.1°C and 40.6±0.1°C for trials at individual body temperatures in the range of 30-32°C, 36-38°C and 40-42°C, respectively. In each trial, animals moved forward along the track with all feet firmly grasping the carpeted floor. Animals continued to move away from the hissing sound at the beginning of the track and towards the darkened box at the end of the track until they were unable to move forward any further. At this point, all animals held the carpet firmly so as not to be pulled backwards. Body mass was correlated with force production (r2=0.8 at Tb=30-32°C, r2=0.7 at Tb=36-38°C and r2=0.6 at Tb=40-42°C. Therefore, we removed the mass effect and report the mass-specific force production as 0.13±0.0004 N g-1, 0.12±0.0005 N g-1 and 0.12±0.0006 N g-1 for trials at individual body temperatures ranging from 30°C to 32°C, 36°C to 38°C and 40°C to 42°C, respectively (Fig. 3).
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Discussion |
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Our results show no thermal dependence for sprint speed, limb cycling
frequency or maximum force production across the range of body temperatures
studied. We found that sprint speed at body temperatures ranging from 30°C
to 35°C, like that of lizards, shows no thermal dependence
(Marsh and Bennett, 1985;
Kaufmann and Bennett, 1989
;
Xiang et al., 1996
). One
striking difference, however, is that the performance of this mammalian
species is maintained at body temperatures up to
41°C whereas the
sprint speed of lizards commonly declines above 35°C. One possible
explanation for these findings is the one that has been used to explain the
low thermal dependence of whole-animal locomotion in lizards despite the high
thermal dependence of the isolated muscle fibers. Farley
(1997
) demonstrated that
maximum sprint speed in lizards is limited by something other than the maximum
mechanical power output of the muscular system. If maximum exertion of all
muscle fibers is not required to attain maximum sprint speed at higher
temperatures, then performance may be maintained at lower body temperatures by
greater muscle fiber output or the recruitment of additional muscle
fibers.
Maximum performance in activities such as lifting a load, however, requires
the simultaneous recruitment of all fibers in the relevant muscles and thus
the maximum mechanical power output of the muscular system
(Rome, 1990). Activities such
as this should, therefore, be as temperature dependant as isolated muscles
with temperature coefficients of
1.5-4.0
(Rome, 1990
). In the present
study, ground squirrels lifted a progressively heavier load to the point that
the load overwhelmed the mechanical power output of the muscular system. These
animals were most certainly utilizing the maximum power output of the muscles
and, therefore, should not be able to compensate through motor unit
recruitment at varying temperatures. Our findings, however, show that maximum
force production in this species is also temperature independent over a range
of
10°C. Perhaps in this species, like that of another heterothermic
mammal (Murina leucogaster), the neuro-muscular system is less
temperature dependent at these temperatures than in other animals, allowing
for the maintenance of whole-animal performance across a broader range of body
temperatures (Choi et al.,
1997
).
The results of our study suggest the need for further investigation at the
tissue and cellular levels to explain how this mammal can maintain
whole-animal performance across such a broad range of body temperatures and
avoid any significant loss of locomotor capabilities associated with either a
decrease of 7-8°C or a rise of 3-4°C in body temperature from typical
mammalian values. A popular view regarding the evolution of endothermic
homeothermy is that birds and mammals expend large amounts of energy to
maintain high and stable body temperatures so as to be able to remain active
over a broad range of environmental conditions
(Crompton et al., 1978;
Block et al., 1993
). This
hypothesis suggests that homeothermy allows for the maintenance of activity
over varying environmental conditions by providing greater biochemical
stability, greater enzyme specialization and, consequently, improved metabolic
efficiency (Heinrich, 1977
;
Avery, 1979
;
Hochachka and Somero,
1984
).
Our results argue against the view that strict homeothermy is required to maintain activity over a broad range of environmental conditions. S. tereticaudus maintains its capacity for intense activity over environmental temperatures ranging from at least 5°C to 50°C and does so over a wide range of body temperatures (30-42°C). Similarly, the ability to maintain neuro-muscular activity over such a broad range of body temperatures together with the energetic savings provided by changes in body temperature argue against the need for homeothermy to render biochemical stability and metabolic efficiency.
In summary, the temperature independence of locomotor performance and the
associated reduction in energy expenditure characteristic of this mammal
raises significant questions regarding our understanding of the evolution and
physiology of the mammalian mode of thermoregulation. If some species, such as
round-tailed ground squirrels, can realize large energetic benefits by
allowing body temperature to vary by 12°C without accruing costs in
their capacity for intense activity, why do not all birds and mammals do
this?
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Acknowledgments |
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References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Avery, R. A. (1979). Lizards - A Study in Thermoregulation. 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. (1990). Thermal dependence of locomotor capacity. Am. J. Physiol. 259,R253 -R258.[Medline]
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]
Brooks, C. M., Koizumi, K. and Malcolm, J. L.
(1955). Effects of changes in temperature on reactions of spinal
cord. J. Neurophysiol.
18,205
-216.
Budnick, B., McKeown, K. L. and Wiederholt, W. C. (1981). Hypothermia-induced changes in rat short latency somatosensory evoked potentials. Electroenceph. Clin. Neurophysiol. 51,19 -31.[CrossRef][Medline]
Buller, A. J., Kean, J. C., Ranatunga, K. W. and Smith, J. A. (1984). Temperature dependence of isometric contractions of cat fast and slow skeletal muscles. J. Physiol. 355, 25-31.[Abstract]
Burton, A. C. and Edholm, O. G. (1955). Man in Cold Environment. London: Edward Arnold.
Chatfield, P. O., Battista, A. F., Lyman, C. P. and Garcia, J.
P. (1948). Effects of cooling on nerve conduction in a
hibernator (golden hamster) and non-hibernator (albino rat). Am. J.
Physiol. 155,179
-185.
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.
Close, R. and Hoh, J. F. Y. (1968). Influence of temperature on isometric contractions in rat skeletal muscles. Nature 217,1179 -1180.[Medline]
Cossins, A. R. and Bowler, K. (1987). Temperature Biology of Animals. New York: Chapman and Hall.
Cullingham, P. J., Lind, A. R. and Morton, R. J. (1960). The maximal isometric tension developed by mammalian muscle, in situ, at different temperatures. Quart. J. Exp. Physiol. 45,142 -156.
Crompton, A. W., Taylor, C. R. and Jagger, J. A. (1978). Evolution of homeothermy in mammals. Nature 272,333 -336.[Medline]
Djawdan, M. and Garland, T., Jr (1988). Maximal running speeds of bipedal and quadrupedal rodents. J. Mamm. 69,765 -772.
Edholm, O. G. (1978). Man - Hot and Cold. 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]
Farley, C. T. (1997). Maximum speed and
mechanical power output in lizards. J. Exp. Biol.
200,2189
-2195.
Faulkner, J. A., Zerba, E. and Brooks, S. V. (1990). Muscle temperature of mammals: cooling impairs most functional properties. Am. J. Physiol. 259,R259 -R265.[Medline]
Friedlander, M. J., Kotchabhakdi, N. and Prosser, C. L. (1976). Effects of cold and heat on behavior and cerebellar function in goldfish. J. Comp. Physiol. 112, 19-45.
Hamilton, J. B. (1968). The effect of hypothermic states upon reflex and central nervous system activity. Yale J. Biol. Physiol. 9, 327-332.
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. Natr. 111,623 -640.[CrossRef]
Hill, R. W. and Wyse, G. A. (1989). Animal Physiology. New York: Harper and Row.
Hochachka, P. W. and Somero, G. N. (1984). Biochemical Adaptations. Princeton: Princeton University Press.
Hudson, J. W. (1964). Temperature regulation in the round-tailed ground squirrel, Citellus tereticaudus. Ann. Acad. Sci. Fenn. Ser. A 15,219 -233.
Huey, R. B. (1982). Temperature, physiology, and the ecology of reptiles. In Biology of the Reptilia vol. 12 (ed. C. Gans and F. H. Pough), pp. 25-91. New York: Academic Press.
Huey, R. B. and Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4,131 -135.[CrossRef]
Jensen, D. W. (1972). The effect of temperature on transmission at the neuromuscular junction of the sartorius muscle of Rana pippins. Comp. Biochem. Physiol. A 41,685 -695.[CrossRef][Medline]
Johnston, I. A., Fleming, J. D. and Crockford, T. (1990). Thermal acclimation and muscle properties in cyprinid fish. Am. J. Physiol. 259,R231 -R236.[Medline]
Kaufmann, J. S. and Bennett, A. F. (1989). The effect of temperature and thermal acclimation on locomotor performance in Xantusia vigilis, the desert night lizard. Physiol. Zool. 62,1047 -1058.
Keller, A. D. (1955). Hypothermia in the unanesthetized dog. In Physiology of Induced Hypothermia (ed. R. D. Dripps), pp.61 -79. Washington: National Academy of Sciences.
Macdonald, J. A. (1981). Temperature compensation in the peripheral nervous system: Antarctic vs temperate poikilotherms. J. Comp. Physiol. 142,411 -418.
MacKenzie, M. A., Vingerhoets, D. M., Colon, E. J., Pinckers, A. J. L. G. and Notermans, S. L. H. (1995). Effect of steady hypothermia and normothermia on multimodality evoked potentials in human poikilothermia. Arch. Neurol. 52, 52-58.[Abstract]
Marden, J. H. (1995). Evolutionary adaptation of contractile performance in muscle of ectothermic winter-flying moths. J. Exp. Biol. 198,2087 -2094.[Medline]
Marsh, R. L. (1990). Deactivation rate and shortening velocity are determinants of contractile frequency. Am. J. Physiol. 259,R223 -R230.[Medline]
Marsh, R. L. and Bennett, A. F. (1985). Thermal dependence of isotonic contractile properties of skeletal muscle and sprint performance of the lizard Dipsosaurus dorsalis. J. Comp. Physiol. B 155,541 -551.[Medline]
McNab, B. K. (1978). The evolution of homeothermy in the phylogeny of mammals. Am. Nat. 112, 1-21.[CrossRef]
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.
Miller, L. K. and Irving, L. (1967).
Temperature-related nerve function in warm- and cold-climate muskrats.
Am. J. Physiol. 213,1295
-1298.
Montgomery, J. C. and MacDonald, J. A. (1990). Effects of temperature on nervous system: implications for behavioral performance. Am. J. Physiol. 259,R191 -R196.[Medline]
Oro, J. and Haghighi, S. S. (1992). Effects of altering core temperature on somatosensory and motor evoked potentials in rats. Spine 17,498 -503.[Medline]
Paintal, A. S. (1965). Effects of temperature on conduction velocity in single vagal and saphenous myelinated nerve fibers of the cat. J. Physiol. 180, 20-49.[Medline]
Rall, J. A. and Woledge, R. C. (1990). Influence of temperature on mechanics and energetics of muscle contraction. Am. J. Physiol. 259,R197 -R203.[Medline]
Ranatunga, K. W. (1977). Changes produced by chronic denervation in the temperature-dependent isometric contractile characteristics of rat fast and slow twitch skeletal muscles. J. Physiol. 273,255 -262.[Abstract]
Ranatunga, K. W. (1980). Influence of temperature on isometric tension development in mouse fast-and slow-twitch skeletal muscles. Exp. Neurol. 70,211 -218.[Medline]
Ranatunga, K. W. (1982). Temperature dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle. J. Physiol. 329,465 -483.[Medline]
Ranatunga, K. W. (1984). The force-velocity relation of rat fast-and slow-twitch muscles examined at different temperatures. J. Physiol. 351,517 -529.[Abstract]
Ranatunga, K. W. (1998). Temperature dependence of mechanical power output in mammalian (rat) skeletal muscle. Exp. Physiol. 83,371 -376.[Abstract]
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 and Hall.
Rome, L. C. (1990). Influence of temperature on muscle recruitment and muscle function in vivo. Am. J. Physiol. 259,R210 -R222.[Medline]
Rome, L. C., Funke, R. P. and Alexander, R. M. (1990). The influence of temperature on muscle velocity and sustained performance in swimming carp. J. Exp. Biol. 154,163 -178.[Abstract]
Roots, B. I. and Prosser, C. L. (1962). Temperature acclimation and the nervous system in fish. J. Exp. Biol. 39,617 -629.[Medline]
Schmidt-Nielsen, K. (1990). Animal Physiology: Adaptation and Environment, pp.276 -282. Cambridge: Cambridge University Press.
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.
Wooden, K. M. and Walsberg, G. E. (2002). Effect of environmental temperature on body temperature and metabolic heat production in a heterothermic rodent, Spermophilus tereticaudus. J. Exp. Biol. 205,2099 -2105.[Medline]
Xiang, J., Weiguo, D. and Pingyue, S. (1996). Body temperature, thermal tolerance, and influence of temperature on sprint speed and food assimilation in adult grass lizards, Takydromus septentrionalis. J. Therm. Biol. 21,155 -161.[CrossRef]
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