Individual variation in metabolic traits of wild nine-banded armadillos (Dasypus novemcinctus), and the aerobic capacity model for the evolution of endothermy
Department of Biological Sciences, University of New Orleans, New Orleans, LA 70148, USA
e-mail: pboily{at}uno.edu
Accepted 1 July 2002
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Summary |
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Key words: armadillo, Dasypus novemcinctus, endothermy, aerobic capacity, thermoregulation
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Introduction |
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An important model that explains the evolution of endothermy and its
associated elevated BMR is the aerobic capacity model, originally outlined by
Bennett and Ruben (1979). This
model argues that natural selection favored individuals with a high aerobic
capacity because of its associated benefits to predator avoidance, prey
capture and other performance characteristics that directly affect fitness.
Selection for increased aerobic capacity would indirectly result in increased
BMR, reflecting the energetic costs required to sustain the physiological
machinery necessary to support a high aerobic capacity. A fundamental
assumption of this model is that aerobic capacity and BMR are functionally
linked. Previous studies have demonstrated that aerobic capacity and BMR in
vertebrates are generally weakly correlated at the intraspecific level, and
similar correlation analyses conducted at the interspecific level have
provided only mixed support for the model (for a review, see
Hayes and Garland, 1995
).
The nine-banded armadillo Dasypus novemcintus is an excellent
subject in which to test the aerobic capacity model because, compared with
most eutherian mammals, armadillos and other members of the order Xenarthra
exhibit an atypical endothermy characterized by low and variable metabolic
rates and body temperatures (Eisenberg,
1981; Johansen,
1961
; Schmidt-Nielsen et al.,
1978
). The main objective of the present study was to use
measurements of BMR and cold-induced peak metabolic rate (PMR) obtained from
wild nine-banded armadillos to investigate the assumption that aerobic
capacity and BMR are functionally linked at the intraspecific level.
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Materials and methods |
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Experimental procedures
On the morning following capture, at approximately 07:30 h, the two animals
were restrained with a towel while a calibrated thermocouple was inserted into
the rectum to a depth of 15 cm and secured in place by taping it to the tail.
Animals were placed individually in rectangular Plexiglas chambers (25 cm wide
x 25 cm high x 50 cm long) in which a small fan on the lid
prevented gas stratification. Chambers were connected to an open-flow
respirometry system (described by Knopper
and Boily, 2000) and placed in a modified freezer. The freezer had
an electrical heater controlled by a computerized data-acquisition system
(Sable Systems) that maintained the air temperature inside the chambers at
30±0.5°C, which is within the thermoneutral zone of armadillos
(Johansen, 1961
;
McNab, 1980
). A system of
solenoid valves alternated the flow pattern of the respirometry system so that
each chamber was sampled for 45 min. Each chamber was sampled three times,
yielding 2.25 h of observations per individual. There was no significant
difference between the two chambers for any of the measurements. Animals were
allowed to acclimate to the chamber for 1 h before starting the measurements.
Data (gas concentrations, rectal temperatures, chamber temperatures) were
averaged (10 readings) and recorded at 10 s intervals. Airflow (dried,
CO2-free ambient air) through the system was controlled with a
mass-flow controller and ranged from 2 to 4.51 min-1 STPD,
depending on animal size. The animals were visually monitored at regular
intervals, and they always appeared to be resting or sleeping. Once BMR
measurements had been completed, animals were returned to their crates until
measurements of PMR.
A cold-exposure protocol using a heliox mixture (21% O2:79% He)
as the environmental gas was selected to measure PMR. Heliox was used to
accelerate heat loss from the animal while reducing the risk of peripheral
cold injuries (Rosenmann and Morrison,
1974). Although cold-induced protocols may underestimate PMR in
some mammals (Seeherman et al.,
1981
; but see Chappell and
Bachman, 1995
), they do not require the repetitive training
associated with exercise protocols, which is impractical for sampling numerous
wild individuals. Cold-induced PMR is therefore a method widely used to
estimate the aerobic capacity of endotherms (e.g.
Dutenhoffer and Swanson, 1996
;
Sparti, 1992
). For many
mammalian species, measurements of PMR using cold-exposure protocols are
highly correlated with measurements obtained using exercise protocols
(Chappell and Bachman, 1995
;
Hayes and Chappell, 1990
). At
approximately 14:00 h, the first animal was placed in a chamber after securing
a rectal thermocouple, as described above. Heliox was mixed from pressurized
tanks of pure gases using a proportional gas mixer calibrated with an
electronic bubble flow meter (model 730, Humonics Inc., Rancho Cordova, CA,
USA). The chamber was flushed with heliox for approximately 10 min at a rate
of 151 min-1 (STPD) at room temperature (20-25°C) before being
transferred to a cold (-20°C) freezer. Data were averaged (five readings)
and recorded at 5 s intervals until the animal's metabolic rate was obviously
declining or when its rectal temperature fell below 28°C. The animal was
then returned to its crate for recovery, and the procedure was repeated on the
second animal. The order in which the animals were used had no significant
effect on the results.
Data analyses
Because armadillos are seasonal breeders, producing one litter a year
during the spring, the body mass of the individuals originally sampled
(N=87) was not normally distributed, forming three distinct groups
probably related to age (Loughry and
McDonough, 1996): 0.5-1 kg (<1 year old), 2-3.35 kg (1 year
old) and more than 3.5 kg (adults). All analyses were limited to adults
because they formed the majority (80%) of individuals sampled, and all
measured traits were normally distributed within this group. Of these adults,
reliable measurements of metabolic rates and body temperature were obtained
from 47 individuals (N=22 for 1998, N=25 for 1999), seven of
which had clipped ears in 1999 and therefore may also have been used in 1998;
these animals were removed from the dataset, leaving a sample size of 18
individuals for 1999 and of 40 for the two years combined (15 males, 25
females). The reproductive biology of armadillos of the genus Dasypus
is unique among vertebrates because females give birth to sets of monozygotic
siblings, quadruplets in the case of D. novemcinctus
(McBee and Baker, 1982
). The
likelihood that some of the individuals sampled were clonal siblings is small,
as a parallel study (P. Boily, P. A. Prodöhl and P. G. O'Neil,
unpublished data), conducted on 75% of the 87 individuals initially sampled,
identified only three sets of twins, none of which was part of the final
sample used for the purpose of the present study.
Instantaneous O2 and CO2 concentrations were
calculated according to Bartholomew et al.
(1981). Rates of O2
consumption (
O2)
and CO2 production
(
CO2) were
calculated according to Withers
(2001
). For each individual,
the lowest continuous 10 min periods of
O2 and
CO2 were used as
measurements of BMR, and they were significantly correlated with each other
(r=0.98, P<0.0001), with a mean respiratory quotient (RQ)
of 0.81±0.05 (mean ± S.D., N=40). The highest
continuous 2 min periods of
O2 and
CO2 were used as
measurements of PMR, and they were significantly correlated with each other
(r=0.79, P<0.0001), with a mean RQ of 1.00±0.20
(N=40). Large errors in measurements of
O2 obtained by
using heliox mixed on-site as an environmental gas can occur as a result of
minute changes in the composition of the gas entering the chamber (see
Appendix). However, measurements of
CO2 during
periods of high metabolic demand can overestimate PMR because the rate of
CO2 excretion can exceed the rate of CO2 production as a
result of the buffering of lactic acid by bicarbonates
(Seeherman et al., 1981
;
McArdle et al., 1986
). Despite
these independent potential sources of error associated with each measurement
of gas exchange, statistical analyses yielded consistent results whether
O2 or
CO2 was used as
a measure of PMR. For simplicity and ease of comparison with previous studies,
all statistical analyses presented are those using
O2 as a measure
of BMR and PMR.
Analyses of correlation were used to test for relationships between
physiological variables. Mass-independent BMR and PMR were obtained by
performing regression analyses for each variable as a function of body mass,
calculating the residual for each data point, and adding the overall mean to
the residual of each data point. This method, described in detail by Packard
and Boardman (1988), yields
mass-independent variables that have the same mean as their whole-animal
values. Analyses of variance were used to test for differences in whole-animal
and mass-independent physiological variables between years and sexes;
identical results were obtained when mass was used as a covariate in analyses
of covariance (ANCOVA). All values are presented as the mean ± 1
S.D.
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Results |
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PMR was significantly correlated with BMR (Fig. 2), both as whole-animal (r=0.62, P<0.001) and as mass-independent (r=0.45, P<0.005) values. The aerobic scope, calculated as the ratio of PMR to BMR, ranged from 4.6 to 10.3 (7.3±1.5) and was higher (F=19.86, P<0.001) for males (8.4±1.2) than for females (6.6±1.9) but did not differ significantly between sampling years and was not related to body mass.
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Compared with allometric predictions, the mean mass-independent BMR
(13.0±2.3 ml O2 min-1) was 60% of that predicted
for eutherian mammals of similar mass (4.2 kg; 21.7 ml O2
min-1; Lovegrove,
2000). Assuming a Q10 of 3, mass-independent
BMR would rise to 20.4 ml O2 min-1, or 94% of the
predicted value, if body temperature were 38°C instead of the observed
mean of 33.9±0.74°C (Fig.
3). The mean mass-independent PMR (93.3±21.7 ml
O2 min-1) was 26% of the value predicted for eutherian
mammals of similar mass (4.2 kg; 362 ml O2 min-1;
Taylor et al., 1981
). Assuming
a Q10 of 3, mass-independent PMR would rise to 174 ml
O2 min-1, or 57% of the predicted value, if body
temperature were 38°C instead of the observed mean of
32.5±1.93°C (Fig.
3). Rectal temperatures obtained during BMR measurements ranged
from 32.7 to 35.3°C and were higher (F=13.89,
P<0.001) in 1999 (34.1±0.69°C) than in 1998
(33.3±0.84°C). These rectal temperatures were positively correlated
with whole-animal (r=0.81, P<0.001) and mass-independent
(r=0.63; P<0.001) BMR and with body mass
(r=0.56, P<0.001).
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A typical example of temporal changes in chamber temperature, rectal
temperature, CO2
and
O2 of an
armadillo during cold-exposure for measurements of PMR is depicted in
Fig. 4. Shortly after the
chamber was transferred to the precooled freezer, the gas (heliox) temperature
inside the metabolic chamber quickly dropped below 0°C and gradually
leveled to temperatures between -5 and -10°C. The rectal temperature of
the animal increased, reaching a peak value 25.6±10.8 min following the
start of cold-exposure, and then gradually declined. Values of
O2 and
CO2 also
increased quickly, but their peak values generally occurred after the peak in
rectal temperature, on average (for
O2)
71.7±43.1 min (N=40) following the start of cold-exposure and
up to 127 min after the peak rectal temperature occurred
(Fig. 5). A few individuals
(N=3) did not exhibit an increase in rectal temperature during
cold-exposure but had a constant rectal temperature that eventually declined,
indicating a state of hypothermia. Rectal temperatures measured when PMR
occurred were lower (paired t-test) by 2.54±1.77°C than
their peak values (t=8.51, P<0.001) and by
1.30±2.02°C than their thermoneutral values measured at BMR
(t=3.74, P<0.001). Rectal temperatures measured when PMR
occurred ranged from 28.8 to 35.9°C, did not differ between sampling years
and were not correlated with whole-animal (P=0.55) or
mass-independent (P=0.13, N=37,
Fig. 3) PMR. However, peak
rectal temperatures were significantly correlated with whole-animal
(r=0.66, P<0.001) and mass-independent (r=0.60,
P<0.001) PMR. Rectal temperatures obtained during BMR measurements
were positively correlated with peak rectal temperatures during cold-exposure
(r=0.63, P<0.001), but not with rectal temperatures
measured when PMR occurred during cold-exposure (P=0.98).
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Discussion |
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The investigation of the selective forces that led to the evolution of
species with metabolic rates that deviate substantially from interspecific
allometric predictions has been the subject of numerous studies. For instance,
species with low metabolic rates have been associated with low
(Mueller and Diamond, 2001) or
unpredictable (Lovegrove,
2000
) environmental productivity, with burrowing or fossorial
habits (McNab, 1979
) and with
low food quality or availability (McNab,
1986
). Although the last two associations apply directly to
armadillos, they could be the result of the confounding effect of phylogeny
(e.g. Elgar and Harvey, 1987
).
Using phylogenetically independent analyses, Lovegrove
(2001
) observed that armored
mammals, such as armadillos, have low metabolic rates compared with
non-armored mammals and proposed that their slow metabolic physiology results
from a weak selective pressure to increase locomotor performance (and thus for
a high aerobic capacity) because body armor substantially reduces predation
risk without the need for fast escape mechanisms. The appeal of this
hypothesis is its relationship to the aerobic capacity model
(Bennett and Ruben, 1979
),
which proposes that BMR is subject to two opposing selection forces, one to
increase aerobic capacity, which increases BMR, the other to maximize energy
conservation, which reduces BMR. Thus, for mammals that do not require a high
aerobic capacity to escape predators or to catch prey, the selective force for
energy conservation would dominate and lead to low metabolic rates (BMR and
PMR). This is entirely consistent with the biology of the nine-banded
armadillo, which feeds mostly on invertebrates and has a very low predation
risk (McBee and Baker, 1982
).
The hypothesis of Lovegrove
(2001
) can also be expanded
explain the low metabolic rates of non-armored mammals that have other
predation defense mechanisms and do not require a high locomotor performance
to catch prey. For instance, spotted (Spilogale putorius) and striped
(Mephitis mephitis) skunks use a musk spray for defense, feed mostly
on invertebrates and plants and have BMRs 30% lower than predicted
(Knudsen and Kilgore,
1990
).
The observed differences in metabolic rates and rectal temperatures between
sampling years may be related to rainfall. Nine-banded armadillos generally
feed on soil invertebrates and, during periods of drought, food availability
may be substantially limited by a lower abundance of soil invertebrates and by
soil that is harder to dig into. Thus, a reduced food supply could lead to a
temporary metabolic depression, which would be consistent with the observation
that metabolic rates, body masses and rectal temperatures were lower in 1998,
when rainfall was considerably below normal values, than in 1999. Such a
decrease in food availability caused by a drought can be further amplified by
the fact that low water availability can directly cause a decrease in food
intake and in body mass in the nine-banded armadillo
(Greegor, 1975).
Basal metabolic rates did not differ between male and female armadillos,
but males had a significantly higher PMR and, as a consequence, a higher
aerobic scope. Typically, female nine-banded armadillos give birth in the
early spring (around March), nurse until late spring (around May) and mate in
the summer (July), but gestation does not start until late fall because the
embryo remains in a state of suspended development until November, when
implantation occurs (McBee and Baker,
1982). Because they were sampled in the summer, it is unlikely
that any female was either lactating or gestating, and these potentially
confounding factors can therefore be eliminated. The ecological significance
of this observation or the mechanism involved in generating this difference
between sexes is unclear. The only comparable observation of which I am aware
is that of Chappell and Bachman
(1995
), who observed that BMR
of the Belding's ground squirrels (Spermophilus beldingi) did not
differ between sexes but that females had a higher PMR than males (by
approximately 7%); the authors did not discuss the potential significance of
their observation.
The observation that the nine-banded armadillo exhibits an increase in body
temperature during cold-exposure is not new; Johansen
(1961) originally described
this unusual response over 40 years ago. In a detailed study using direct and
indirect calorimetry, Mercer and Hammel
(1989
) concluded the armadillo
actively regulates its core temperature at elevated levels during
cold-exposure. A possible adaptive advantage of this unusual response is that
regulating core temperature at an elevated level during cold-exposure could
lead to an increase in PMR because of the Q10 effect and,
thus, increase cold-tolerance. If this is the case, then PMR should occur when
core temperatures are at or near their peak, but this was not the case.
Indeed, PMR occurred up to 100 min after peak rectal temperature, when rectal
temperatures had dropped on average by 2.4°C from peak values. The other
puzzling observation was that PMR was correlated with peak rectal temperature
but not with rectal temperature measured when PMR occurred. This apparent
disassociation between the timing of peak core temperature and peak metabolic
rate could be the result of three errors. First, rectal temperature can be
misleading if there is regional heterothermy. This is unlikely because rectal
temperatures in the armadillo are highly correlated with core temperatures
measured at other sites (Mercer and
Hammel, 1989
; F. M. Knight and P. Boily, unpublished data).
Second, errors in measurements of gas exchange rates could have been involved.
The use of heliox as a respiratory gas can cause errors in
O2 if baseline
O2 concentration changes during an experiment (see Appendix), and
CO2 during
periods of high metabolic demand can overestimate metabolic rates because of
the excess CO2 excretion rate resulting from the buffering of
lactic acid. This is also unlikely because the sources of errors for
measurements of
O2 and
CO2 are
independent and yet nearly identical results were obtained for
O2 and
CO2. Third, the
effects of exercise may have caused these results, because armadillos can
become very active during sustained cold-exposure
(Johansen, 1961
), and maximum
exercise metabolic rates can exceed peak rates of thermogenesis
(Seeherman et al., 1981
; but
see Chappell and Bachman,
1995
). This is the most likely hypothesis, but cannot be tested
with the data collected during this study. While I have no evidence to provide
a satisfactory explanation for the apparent disassociation between the timing
of peak core temperature and metabolic rates, it should be noted that the
animals were not necessarily hypothermic at the time when PMR was measured
because rectal temperatures were, on average, only 1.2°C below
thermoneutral levels at the time when PMRs were observed.
In conclusion, the results obtained during this study are consistent with the existence of a functional relationship between basal and peak metabolic rates and, therefore, support the aerobic capacity model for the evolution of endothermy. In addition, this study confirmed that the nine-banded armadillo exhibits low and variable metabolic rates that may have evolved because the presence of a body armor reduced predation risk and thus the need for a high aerobic capacity, resulting in a unbalanced selection strongly favoring energy-conservation mechanisms.
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Appendix |
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![]() | (A1) |
![]() | (A2) |
The results show that minute changes (0.25%) in either of the gas flow
rates during an experiment can lead to large errors (10%) in the observed
O2
(Table 2). Such errors are
proportional to the changes occurring in the flow rates of either of the gases
during an experiment; if the flow rate of one gas changes by 1% during the
course of an experiment, the error in observed
O2 will be
approximately 40%. The critical factor involved is not the accuracy of flow
rate measurements, but rather the stability of flow rates over time. Further,
while a linear drift in O2 concentration during an experiment can
be corrected by measuring the O2 concentration of the circulating
gas at the beginning and end of an experimental trial, non-linear fluctuations
cannot be corrected unless the O2 concentration of the inflowing
gas is continuously measured. Preliminary trials using the same procedures as
those used in the present study, in which heliox was circulated through an
empty chamber, gas pressures were regulated at 345 kPa using dual-stage
regulators and gas temperatures varied by less than 0.1°C, indicated that
baseline O2 concentration typically fluctuated non-linearly by
0.06% over a 80 min interval (Fig.
6). Such fluctuations would lead to errors in
O2 calculations
of up to 16%. However, because the baseline concentration of CO2 in
the gas mixture entering the chamber is constant (0%), errors in
CO2 are equal to
errors in FRT, i.e. the potential error in
CO2 is 0.25% if
the flow rate of either gas varies by 0.25% during an experiment.
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Acknowledgments |
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References |
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---|
Bartholomew, G. A., Vleck, D. and Vleck, C. M. (1981). Instantaneous measurements of oxygen consumption during pre-flight warm-up and post-flight cooling in sphingid and saturniid moths. J. Exp. Biol. 90,17 -32.
Bennett, A. F. and Ruben, J. A. (1979). Endothermy and activity in vertebrates. Science 206,649 -654.[Medline]
Blaxter, K. (1989). Energy Metabolism in Animals and Man. Cambridge: Cambridge University Press.
Chappell, M. A. and Bachman, G. C. (1995). Aerobic performance in Belding's ground squirrels (Spermophilus beldingi): variance, ontogeny, and the aerobic capacity model of endothermy. Physiol. Zool. 68,421 -442.
Dutenhoffer, M. S. and Swanson, D. L. (1996). Relationship of basal to summit metabolic rate in passerine birds and the aerobic capacity model for the evolution of endothermy. Physiol. Zool. 69,1232 -1254.
Eisenberg, J. F. (1981). The Mammalian Radiations: An Analysis of Trends in Evolution, Adaptation and Behavior. Chicago: University of Chicago Press.
Elgar, M. A. and Harvey, P. H. (1987). Basal metabolic rates in mammals: allometry, phylogeny and ecology. Funct. Ecol. 1,25 -36.
Greegor, D. H., Jr (1975). Renal capabilities of an argentine desert armadillo. J. Mammal. 56,626 -632.
Hayes, J. P. (1989). Altitudinal and seasonal effects on aerobic metabolism of deer mice. J. Comp. Physiol. B 159,453 -459.[Medline]
Hayes, J. P. and Chappell, M. A. (1990). Individual consistency of maximal oxygen consumption in deer mice. Funct. Ecol. 4,495 -503.
Hayes, J. P. and Garland, T. D., Jr (1995). The evolution of endothermy: testing the aerobic capacity model. Evolution 49,836 -847.
Johansen, K. (1961). Temperature regulation in the nine-banded armadillo (Dasypus novemcinctus). Physiol. Zool. 34,126 -144.
Knopper, L. D. and Boily, P. (2000). The energy budget of captive Siberian hamsters, Phodopus sungorus, exposed to photoperiod changes: mass loss is caused by a voluntary decrease in food intake. Physiol. Biochem. Zool. 73,517 -522.[Medline]
Knudsen, K. L. and Kilgore, D. L. (1990). Temperature regulation and basal metabolic rate in the spotted skunk, Spilogale putorius. Comp. Biochem. Physiol. 97A, 27-33.
Lovegrove, B. G. (2000). The zoogeography of mammalian metabolic rate. Am. Nat. 156,201 -219.[Medline]
Lovegrove, B. G. (2001). The evolution of body armor in mammals: plantigrade constraints of large body size. Evolution 55,1464 -1473.[Medline]
Loughry, W. J. and McDonough, C. M. (1996). Are road kills valid indicators of armadillo population structure? Am. Midl. Nat. 135,53 -59.
McArdle, W. D., Katch, F. I. and Katch, V. L. (1986). Exercise Physiology: Energy, Nutrition, and Human Performance. Second edition. Philadelphia: Lea & Febiger.
McBee, K. and Baker, R. J. (1982). Dasypus novemcinctus. Mammal species 162, 1-9.
McNab, B. K. (1979). The influence of body size on the energetics and distribution of fossorial and burrowing mammals. Ecology 60,1010 -1021.
McNab, B. K. (1980). Energetics and the limits to a temperate distribution in armadillos. J. Mammal. 61,606 -627.
McNab, B. K. (1986). The influence of food habits on the energetics of eutherian mammals. Ecol. Monogr. 56,1 -19.
Mercer, J. B. and Hammel, H. T. (1989). Total calorimetry and temperature regulation in the nine-banded armadillo. Acta Physiol. Scand. 135,579 -589.[Medline]
Mueller, P. and Diamond, J. (2001). Metabolic
rate and environmental productivity: well-provisioned animals evolved to run
and idle fast. Proc. Natl. Acad. Sci. USA
98,12550
-12554.
Packard, G. C. and Boardman, T. J. (1988). The misuse of ratios, indices, and percentages in ecophysiological research. Physiol. Zool. 61,1 -9.
Robinson, W. R., Peters, R. H. and Zimmermann, J. (1983). The effects of body size and temperature on metabolic rates of organisms. Can. J. Zool. 61,281 -288.
Rosenmann, M. and Morrison, P. (1974). Maximum
oxygen consumption and heat loss facilitation in small homeotherms by
He-O2. Am. J. Physiol.
226,490
-495.
Schmidt-Nielsen, K., Bolis, L. and Taylor, C. R. (1978). Comparative Physiology: Primitive Mammals. Cambridge: Cambridge University Press.
Seeherman, H. J., Taylor, C. R., Maloiy, G. M. O. and Armstrong, R. B. (1981). Design of the mammalian respiratory system. II. Measuring maximum aerobic capacity. Respir. Physiol. 44, 11-23.[Medline]
Sparti, A. (1992). Thermogenic capacity of shrews (Mammalia, Soricida) and its relationship with basal rate of metabolism. Physiol. Zool. 65, 77-96.
Storrs, E. E. (1987). Armadillo. In The UFAW Handbook on the Care and Management of Laboratory Animals. Sixth edition (ed. T. B. Poole), pp.229 -239. New York: Churchill-Livingstone.
Taylor, C. R., Maloiy, G. M. O., Weibel, E. R., Langman, V. A., Kamau, J. M. Z., Seeherman, H. J. and Heglund, N. C. (1981). Design of the mammalian respiratory system. III. Scaling maximum aerobic capacity to body mass: wild and domestic mammals. Respir. Physiol. 44,25 -37.[Medline]
Withers, P. C. (1992). Comparative Animal Physiology. Fort Worth: Saunders College Publishing.
Withers, P. C. (2001). Design, calibration and calculation for flow-through respirometry systems. Aust. J. Zool. 49,445 -461.