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Metabolic scope and conductance in response to cold of some dasyurid marsupials and Australian rodents
Camp. Bin&m. Physinf. Vol 71A. pp. 59 to 64. 1982 Printed tn Great Britain. All rights reserved
Copyright
0300-9629 82.010059-06503.00’0 0 1982 Pergaman Press Ltd
METABOLIC SCOPE AND CONDUCTANCE IN RESPONSE TO COLD OF SOME DASYURID MARSUPIALS AND AUSTRALIAN RODENTS TERENCEJ. DAWSONand WILLIAMR. DAWSON* School of Zoology, University of New South Wales, Kensington 2033, N.S.W., Australia (Receiwd
14 May 1981)
Abstract-l. The metabolic response to cold of two small dasyurid marsupials, Phigale gilesi and Ihsyuroides byrnei, was compared with that of two Australian rodents, Notom~~ cerainus and Psuedomys gracilicaudatus. 2. The mean resting body temperatures in the thermoneutral zone were 36.2 + 0.98”C (mean + SD) for the marsupials and 37.2 k 0.67”C for the eutherians. 3. The standard metabolic rates (SMR) were 2.22 + 0.17 W kg-o.75 and 3.27 k 0.27 W kg-“.75, respectively for the marsupials and eutherians, these being close to predicted values. 4. The characteristics of heat loss, conductances, were similar in the two groups. 5. In response to severe cold, the marsupials attained levels of summit metabolism at least matching those of the eutherians. 6. The metabolic scope of the marsupials was 8-9 times SMR compared with +-5 times SMR for the eutherians, indicating that the lower SMR of marsupials has not restricted their abilities for chemical thermoregutation. -
however, do make extensive use of torpor (Dawson & Wolfers, 1978; Wallis, 1979), as do small eutherians, both thereby avoiding some of the energetic and thermoregulatory difficulties in cold environments. Small homeothermic animals have problems in the cold because they potentially have high rates of heat loss. This arises because the volume of heat producing tissue and the animals’ surface area, through which heat is lost, vary with different exponents of body mass, 1.0 and 0.67 respectively. Therefore as mass decreases the surface available for heat loss declines relatively less rapidly. This problem is compounded by the constraints on the amount of insulation that a small mammal can carry, the level of insulation being largely determined by fur thickness (Scholander et al., 1950). Maintenance of similar body temperatures in the face of a high heat loss should require an equivalently high heat production by small marsupials or any small mammals. It is here that marsupials may have problems, for many birds and mammals appear unable to sustain metabolic rates in the cold that exceed about 3-4 times SMR (Gelineo, 1964). Were small marsupials such as dasyurids to follow this pattern, their lower SMR would be accompanied by absolute metabolic capabilities that would limit their cold tolerance relative to that of their eutherian counterparts. This possibility led us to attempt to define the metabolic scope of these animals.
INTRODUCTION The basic concern of this study is the metabolic capabilities of marsupials relative to those of other mammals, with the thermogenic responses to cold being the specific topic of investigation. Conjecture has occurred regarding this aspect of the physiology of marsupials since the pioneering work of Martin (1902). Martin, prompted by earlier studies of Sutherland {1897), examined the body temperatures and metabolic rates of marsupials and eutherians, as well as of monotremes. Marsupials were reported to have body temperatures and metabolic rates intermediate between those of eutherians and monotremes; the metabolic rates of the marsupials were less than one third of those of the eutherians. For some five decades Martin’s work was cited as demonstrating that marsupials represented an intermediate level of homeothermic development, below the “advanced” eutherians but better than the “very primitive” monotremes. The notion of marsupials as “primitive” mammals became entrenched (Johansen, 1962). The situation has been much clarified over the past decade. The minimal resting metabolic rate or standard metabolic rate (SMR) of marsupials has been demonstrated to vary with the 0.75 power of body mass in the same manner as in eutherians, but. at any mass, the level is about 70% of the corresponding eutherian level (Dawson & Hulbert, 1969, 1970; MacMillen & Nelson, 1969). The thermoregulatory abilities of a variety of marsupials, especially those of some of the larger macropodids, also have been examined and, generally have been shown to be similar to those of eutherians (Dawson, 1973a; Dawson et al., 1974). Smaller species, such as many of the dasyurids,
MATERIAL& METHODS The dasyurids examined were the Paucident Planigale P/aniga/r gi/esi and the Kowari. ksyuroidcs hymei. Both these species are found in semiarid and arid regions, P. gilesi coming from Western N.S.W. and D. byrnei from southwestern Qld. The rodents were the Fawn Hoppingmouse, Notomys cercinus, and the Eastern Chestnut Mouse, Pse~d~~~s gra~j~i~uudat~~. The N. ce~~~i~u~came from southwestern Queensland and the P. ~ruei~i~u~~af;~s
* Permanent address: Division of Biological Sciences. University of Michigan, Ann Arbor, MI 38109, U.S.A. 59
60
TERENCEJ. DAWSONand WILLIAMR. DAWSON
from the central coast of N.S.W. Animals had been kept in an unheated animal house for several months prior to the experiments, which were carried out during winter and early spring (June-September). The only exception involved three planigales, which were wild caught in September. The temperature of the animal house followed outside ambient; usual daily maxima were 1621°C with minima of 8 14°C. Nest material or nest boxes were provided. Animals were fasted overnight only in experiments at the highest temperatures, i.e. in the thermoneutral zone. Fasting prior to low temperature experiments occasionally led to torpor in the marsupials. Metabolic responses to various temperatures were tested in either of two temperature controlled cabinets, which operated down to - 3’ and - 20°C. respectively. To enable the animals to rest undisturbed in a normal posture, body temperature was not monitored continuously. Temperatures were measured with copper-constantan thermocouples. Body temperatures, taken as deep rectal temperature, were obtained at the beginning and end of the experiments. The basic gas measuring system used the positive pressure. open circuit technique. Air was passed through a small perspex chamber containing the animal, at a rate measured by a calibrated dry gas meter. Oxygen consumption and carbon dioxide production were determined using a Beckman F3 paramagnetic analyser and a Beckman model 864 infrared gas analyser. respectively. The oxygen analyser was cd&rated manometrically before each experiment and the carbon dioxide analyser was calibrated using standard gases. Oxygen consumption and carbon dioxide production were calculated as dry gas at STP. Heat production was estimated from oxygen consumption and RQ, which varied between 0.84 and 0.71. using the appropriate conversion factors (Brody. 1945). Whole body conductances, uncorrected for heat loss by evaporation or changes in T,, were measured by the formula: (in W m z Cm I)
conductance
heat production (T, - T,)
1surface area
Surface area was calculated using the equation S.A. (in m’) = 0.10 kg”‘. The Meeh factor adopted, 0.10, was one considered appropriate for general comparative estimates of total surface area. although this is slightly lower than the
Table
Mass N
g
1. Standard
metabolic
L C
1.1 5 118 i: 12 - 10.3 5 118 + 14 Notr~nt~s ~wrinu.s 32.0 5 32.5 I: 3.0 -0.2 5 32.1 i. 1.4 5 33.1 +_ 3.2 -13.1 Pwurlot~~~~.s yrclcilicurrtlatus 31.9 5 79.8 k 6.9 -0.7 5 15.6 +- 8.5 5 81.2 & 11.3 -10.6
rate and metabolic
TId> c
value obtained for small marsupials in the study of Dawson & Hulbert (1970). To obtain good base line readings for SMR measurements, all species were placed in the chambers for some 46 hr. starting at 09:OO hr. Reported measurements were taken over two, 20min periods in the latter part of the exposure, but before 15:30 hr. Preliminary experiments indicated that after approximately 16:OO hr, oxygen consumption could start to increase as the animals became more restless. The same pattern was followed during cold exposures, except experiments were terminated if oxygen consumption noticeably declined. In these cases. the oxygen consumption reported was that obtained before the decline. Because of concern about the limited number of planigales, these tiny dasyurids were examined at less extreme temperatures and for shorter periods, the exposure period before data collection being 3 hr.
RESULTS Values for body temperatures
responses rodents
02 Consumption 1 kg-r hrr’
to cold exposure
of small
Heat production W kg-‘.”
MRiSMR
--
36.8 * 0.5 35.8 k 0.9 35.2 & 1.3
1.28 +- 0.12 8.89 t 0.42 10.98 2 2.00
2.32 f 0.12 15.4 f 1.46 19.0 f 2.30
6.6 & 0.6 8.2 t: 1.0
& 0.8 + 0.8
35.6 & 1.0 36.2 & 1.6 37.1 rt 0.5
0.65 k 0.06 4.05 + 0.46 5.80 + 0.53
2.12 2 0.17 13.2 + 1.66 18.6 & 2.08
f 0.9 * 1.5 i 1.0
37.0 + 0.7 36.9 f 0.8 34.2 + 2.6
1.44 + 0.14 6.06 + 0.24 8.85 ) 0.85
* 1.3 * 2.4 f 2.9
37.4 + 0.6 36.2 + 0.2 29.4 + 4.0
1.05 + 0.05 3.27 -i: 0.16 4.03 5 0.46
* Time to data indicates the time to the beginning Values are means + SD.
and metabolic
rates
for the four species at thermoneutral temperatures and two low temperatures are summarised in Table 1, The data in thermoneutral conditions for body temperature and metabolic rate of the marsupials and eutherians follow a conventional pattern. The overall mean body temperatures of the marsupials was 36.2 + 0.98’C as opposed to a group mean for the two eutherians of 37.2 rt: 0.67”C (P < 0.02). The SMR for the marsupials and eutherians in the mass-independent units of W kg-0.75, were 2.22 + 0.17 and 3.27 + 0.29 respectively (P c 0.001). These values are close to the predicted ones for the SMR, of 2.35 W kg-o.75 (Dawson & Hulbert, 1970) and 3.34 W kg-o.75 (Kleibet, 1961) respectively for marsupials and eutherians. The marsupial values are 687,, of the eutherian ones. The responses to cold environments are interesting. but difficult to interpret, unless the time course of experiments is kept in mind. With the exception of the tiny planigales, all species maintained body temperature down to about O’C, and even some of the larger marsupials
Time to data* min
and
Conductance Wm-2’C-I
245 f 95 189 + 53 132 k 41
4.9 i 1.32 4.3 2 0.47 4.4 i 0.57
6.2 1. 0.8 8.8 & 1.0
336 + 64 290 i 35 225 i 57
4.3 i 1.00 3.2 + 0.33 3.4 + 0.34
3.42 k 0.33 14.1 f 0.58 21.0 f 0.45
4.1 & 0.2 6.1 + 0.5
291 4 64 288 i 58 150 + 28
5.3 + 0.83 2.9 i 0.14 3.4 2 0.16
3.12 k 0.17 9.6 k 0.42 12.0 + 1.54
3.1 & 0.2 3.8 & 0.5
255 + 69 251 rL_68 113 + 59
4.8 + 1.02 2.2 * 0.18 2.5 * 0.36
of data collection.
-
Metabolic scope and conductance male planigales (11.5-12.5 g) maintained T,, at a T, close to 0°C for periods in excess of 3 hr. Below zero, - 10 to - 13°C. the picture changed and only D. byrnei maintained Tb for the test period of 4 hr. Of the eutherians the small hopping mouse N. cervinus performed well and body tem~rature was reasonably maintained for some 3 hr, whereas the larger P. gracilicaudatus was unable to maintain Tb more than 1: hr at - 10°C. Reasons for the differing thermoregulatory capacities are suggested by the data on metabolic responses. Pseudomys gracilicaudatus had the lowest maximum metabolic rate both in mass-specific and rn~s-independent terms. The pattern of metabolic response to cold varied between the marsupials and eutherians (Table 1). While the marsupials started with a lower basal heat production their maximum metabolic responses were similar to that of N. ceroinus, the eutherian with the better thermogenic capacity of the two species tested. It should also be noted that the value for D. byrnei was probably submaximal because T, was maintained to the end of the experiment. This pattern is best appreciated by the ratio of maximum metabolic rate to SMR. In both marsupials the relative increase, 8-9 times, was significantly higher than in either of the eutherians, and was double that of P. ~ru~i~~caadafl~s. For the maintenance of body temperature in a cold environment, the reduction of heat loss is the other important variable apart from increased heat production. The variation in conductance at different air temperatures is shown in Table 1. The general pattern which emerged for all species was consistent with that for homeotherms generally. In the thermoneutral zone, conductance was elevated as thermoregulatory vasomotor and pilomotor adjustment occurred. Conductance was minimal around zero but increased at the lowest temperatures, particularly well below freezing, This effect presumably resulted partially from increased shivering, which may break up the air boundary layer. Possibly more important in these results could be an increased blood flow to the periphery to
I
4
0 001
I
I
I
0 01
01
IO
Body
I 100
nwss. kg
Fig. 1. Conductance values for the marsupials and rodents compared with the relationships between conductance (converted to W m -’ Y-l) and mass previously obtained for eutherians and marsupials by Herreid & Kessel (1967) and MacMillen & Nelson (1969) respectively. Data for PhascoIarctos cinereus (Degabriele & Dawson, 1979) is also included. 0 P. gilesi; m D. byrnei; o N. cervinus; l P. graciliccwfntus; A P. cinereus.
61
give protection against freezing of the tissues, i.e. frost bite. No large differences were seen between the minimal conductance levels of the two groups of mammals (Fig. l), although the values from the marsupials tended to be higher. The planigales with their very short fur had a high conductance. The P. ~rl~~~i~~alldatus, which had the smallest metabolic scope, had the lowest conductance, that is the highest total body insulation. DISCUSSION
The pattern of difference between marsupials and eutherians which is evident in resting, thermoneutrai body temperatures, together with that in standard metabolic rates is in agreement with that found in many of the studies undertaken in the past decade following the primary studies of Dawson & Hulbert (1969, 1970) and MacMiIlen & Nelson (1969). Few studies have actually compared eutherians and marsupials directly, although Dawson & Hulbert (1970) examined rabbits to reinforce their results. This general lack of direct comparative study has enabled the perpetuation of the idea that the difference in SMR between the two groups could be due to a Qlo effect associated with differences in body temperature (Kinnear & Shield, 1975). When marsupials and eutherians are treated similarly as in the current experiments the data do not support this proposition and it is probably time that the idea was laid to rest. It may be argued that comparisons of the metabolic status of various groups of homeotherms based on the SMR are not particularly valid, because the conditions under which the SMR is determined are rather artificial and rarely related to the animal’s activities in the real world. However there is ample evidence that other levels of physiological activity in marsupials are related to the SMR. These include normal maintenance, nitrogen and energy requirements (Brown & Main, 1967: Hume. 1974) and water requirements (Denny & Dawson, 1975). Also, most importantly. the maximal sustained metabolic responses to cold in some groups of birds and mammals consistently appear to be about quadruple the SMR (Gelineo, 1964). Therefore such maximal responses could be limited in absolute terms in those groups with low SMR (Dawson, 1973b). Data on bandicoots (Hulbert & Dawson, 1974) suggest that this may be also true for marsupials, but other studies have argued against a limiting relationship between metabolic capability and SMR for marsupials. Baudinette et al. (1976) have in fact proposed that the metabolic scope of dasyurids in response to exercise may be greater than that of eutherians. The relationship between metabolic responses to cold and the energy expenditure during exercise is unclear because, for large mammals such as the red kangaroo, an increase in metabolic rate during sustained exercise representing at least 20 times the SMR is possible (Dawson & Taylor, 1973). While several workers have dealt with this problem, no concensus as yet exists concerning what is maximum metabolic activity and how it should be assessed. Hart (1971) reviewed much of the initial work, particularly that dealing with small mammals, and he recognised at least two different levels of maximum metabolic ac-
62
TERENCEJ. DAWSONand WILLIAMR. DAWSON
tivity, peak metabolic effort and summit metabolism. The first of these, peak metabolic effort (Hart, 1957), is the highest rate of oxygen consumption that can be sustained for a short time, some 3-20 minutes. This may be attained by exposure to extreme cold under conditions where heat loss initially exceeds heat production, or by the addition of exercise to a submaximal cold exposure. This latter test is made on the assumption that heat production due to shivering and that due to exercise, are in the short term, interchangeable. Some doubt exists about whether peak rates obtained by these two procedures are comparable, but they seem similar, at least in small rodents. Peak metabolic effort appears to be 7 times SMR in small mammals (Hart, 1971), but is obviously higher in exercise in larger cursorial species. Summit metabolism is the other measure of metabolic scope used for comparative purposes (Gelineo, 1964), and this is the highest metabolic rate that can be sustained in the cold by a sedentary animal. Some doubt exists about the appropriate time scale for measurements of summit metabolism, but a period of at least several hours is now accepted. Over a range of homeotherms it seems that most species have a summit metabolism 3-4 times basal (Gelineo, 1964) although a few northern hemisphere mammals from cold climates have been reported to exceed this figure in winter (Rosenmann et al., 1975). Some small birds which reside in the boreal winter of the northern hemisphere also have exceptional metabolic capabilities but it has also been noted that they have a high SMR (Dawson & Carey, 1976). In our examination of the metabolic capabilities of marsupials, we were primarily interested in maximum metabolic responses, sustainable by homeothermic animals over an extended period in severe cold. We have thus been concerned with an approximation of summit metabolism, rather than in peak effort. In this regard two cold test temperatures were used to characterise responses more completely. The three larger species were able to maintain Tb for the test time of approx. 5 hr at the temperatures near 0°C. However, even the planigales, with the exception of a 7.7 g female maintained Tb for their test period near freezing for 3 hr. Below freezing, the responses of D. byrnei and the rodents differed. Dasyuroides byrnei maintained Tb for the test period of 4 hr, whereas neither of the eutherians could do so for this interval. The summit metabolism of the eutherians therefore develops between the two cold test temperatures and approx. 3-5 times their SMR; N. ceruinus reached a level 6 times SMR but could not maintain it. The dasyurids therefore have a higher summit metabolism relative to their SMR, some 8-9 times SMR, one Kowari actually maintained a metabolic level 10.4 times SMR. The dasyurids, then, are not restrained in their response to cold stress by their initially low SMR. This is further indicated by data derived from Dawson & Wolfers (1978), Fig. 2, where a P. gilesi maintained oxygen consumption l@ll times SMR for many hours. The true relative metabolic capabilities are appreciated by consideration of the data in the mass independent terms of W kg-o.75 (Table 1). In this comparison the marsupials have rates of heat production approximating that of N. cercinus and substantially exceeding
1
20
I
Lights
off I
0.
l *
.
.
. 2
i
.*
C,O-
l
E
a
z
l .
0..
-
. _.=
*.
l**e
.
:
. .
8
mm... k 5- ------
--
..**
. Pred
cond
P +
.
3
-6
0”_
J
. . . . . ...’
0” __----
IO
2
- - SMR0,33X
0 16
20
24
04
06
12
16
Time. hr
Fig. 2. Oxygen consumption (0) and conductance (m) of a P. clilesi (wt 9.4 g) in the cold (14.5”C) for 24 hr. The olanigale was inactive and curled up while the lights were on but was active and feeding for much of the night period. Food, Tenebrio sp larvae, was available ad lib. Values arc hourly means. The SMR for this animal at a Tai, of 33 C is indicated, as is the predicted minimum conductance value from MacMillen & Nelson (1969).
that of P. gracilicaudatus. However, N. ceruinus could not maintain this rate whereas D. byrnei could. How then do these small dasyurids manage this metabolic scope? Rodents rely heavily on nonshivering thermogenesis (NST) in their responses to cold (Hart, 1971) and since these experiments were carried out in winter and the animals were kept in unheated quarters NST might be functional. One explanation for the large metabolic scope of the dasyurids could be a greater capacity for NST, but this appears unlikely. Reports of NST in marsupials are as yet conflicting. Reynolds & Hulbert (1982) suggest that it is absent and even those studies reporting NST in marsupials are equivocal because the doses of noradrenaline required to elicit a response are far greater than those needed for rodents (Nicol, 1978; Wallis, 1979). It is possible that the dasyurids rely primarily on shivering for their regulatory heat production. In this regard it is interesting that the maximum sustained rates of heat production in exercise and cold thermogenesis are both approximately 8-9 times SMR in dasyurids (Baudinette et al., 1976; R. E. MacMillen & T. J. Dawson, unpublished data). An interesting parallel to this discussion of the metabolic capabilities of dasyurids and other marsupials is their very low resting heart rates (Kinnear & Brown. 1967). These are much lower than those of eutherians, lower even than would be expected from their lower SMR. On the other hand. marsupials compensate for these low heart rates by having a much larger heart stroke volume (Dawson & Needham, 1981). If, as Baudinette (1978) has reported, marsupials and eutherians have similar maximal heart rates, then maximal cardiac outputs may be greater in marsupials. This would be quite consistent with the data indicating the high sustained aerobic capacity of marsupials and it is conceivable that marsupials are superior to eutherians of comparable size in aerobic capacity. It had been suggested that low metabolic rates in marsupials might be compensated for by a lower rate
Metabolic scope and conductance
of heat loss than seen in eutherians (Dawson, 1973b). While this option appears used by larger marsupials (Dawson. 1973a; Degabriele & Dawson, 1979), it is not available for smaller species (Fig, 1). MacMillen & Nelson (1969) failed to find a difference between their data for dasyurid conductance and the predictions for eutherians by Herreid & Kessel (1967), and the pattern noted in the current study did not differ markedly from these previous estimates. In small mammals conductan~ through the core to skin surface is high, because of the high rate of heat transfer through tissue (about 10 times that through fur) and the very small distances involved. As animals become larger however this situation may change and marked adjustments can be made by the utilization of mechanisms such as countercurrent arrangements (Dawson & Fanning, 1981). There are also obvious constraints on the amount of fur a small mammal can carry. Combined with these factors there is the additional problem with the variation of the effective surface area for heat loss. The conductances given in Table 1, and Fig. 1 are minimum conductances and represent the conditions when the animals are inactive and curled up into a ball; the Meeh factor for a sphere is 0.047, about half the measured total surface. When a small mammal is active the effective surface area approximates the total surface and heat flow is doubled (Fig. 2), greatly increasing the metabolic heat requirement. Given these circumstances, if a small dasyurid or any other small animal is to remain homeothermic over a wide temperature range, it must have a large metabolic capacity. In marsupials with their low SMR this means a large functional metabolic scope. Whether this is a feature of marsupials in general or a specific adaptation to small size such as may occur in some groups of shrews, has yet to be determined. ~cknowled~e~e~rs-The authors wish to thank F. D. Fanning for his technical assistance and B. Fox and D. Read for providing animals. The work was supported by a grant from the Australian Research Grants Committee. W. R. Dawson was in receipt of a Visiting Professorship from the University of New South Wales and received some support from the Horace H. Rackham School of Graduate Studies, the University of Michigan.
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and
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Copyright
0300-9629 82.010059-06503.00’0 0 1982 Pergaman Press Ltd
METABOLIC SCOPE AND CONDUCTANCE IN RESPONSE TO COLD OF SOME DASYURID MARSUPIALS AND AUSTRALIAN RODENTS TERENCEJ. DAWSONand WILLIAMR. DAWSON* School of Zoology, University of New South Wales, Kensington 2033, N.S.W., Australia (Receiwd
14 May 1981)
Abstract-l. The metabolic response to cold of two small dasyurid marsupials, Phigale gilesi and Ihsyuroides byrnei, was compared with that of two Australian rodents, Notom~~ cerainus and Psuedomys gracilicaudatus. 2. The mean resting body temperatures in the thermoneutral zone were 36.2 + 0.98”C (mean + SD) for the marsupials and 37.2 k 0.67”C for the eutherians. 3. The standard metabolic rates (SMR) were 2.22 + 0.17 W kg-o.75 and 3.27 k 0.27 W kg-“.75, respectively for the marsupials and eutherians, these being close to predicted values. 4. The characteristics of heat loss, conductances, were similar in the two groups. 5. In response to severe cold, the marsupials attained levels of summit metabolism at least matching those of the eutherians. 6. The metabolic scope of the marsupials was 8-9 times SMR compared with +-5 times SMR for the eutherians, indicating that the lower SMR of marsupials has not restricted their abilities for chemical thermoregutation. -
however, do make extensive use of torpor (Dawson & Wolfers, 1978; Wallis, 1979), as do small eutherians, both thereby avoiding some of the energetic and thermoregulatory difficulties in cold environments. Small homeothermic animals have problems in the cold because they potentially have high rates of heat loss. This arises because the volume of heat producing tissue and the animals’ surface area, through which heat is lost, vary with different exponents of body mass, 1.0 and 0.67 respectively. Therefore as mass decreases the surface available for heat loss declines relatively less rapidly. This problem is compounded by the constraints on the amount of insulation that a small mammal can carry, the level of insulation being largely determined by fur thickness (Scholander et al., 1950). Maintenance of similar body temperatures in the face of a high heat loss should require an equivalently high heat production by small marsupials or any small mammals. It is here that marsupials may have problems, for many birds and mammals appear unable to sustain metabolic rates in the cold that exceed about 3-4 times SMR (Gelineo, 1964). Were small marsupials such as dasyurids to follow this pattern, their lower SMR would be accompanied by absolute metabolic capabilities that would limit their cold tolerance relative to that of their eutherian counterparts. This possibility led us to attempt to define the metabolic scope of these animals.
INTRODUCTION The basic concern of this study is the metabolic capabilities of marsupials relative to those of other mammals, with the thermogenic responses to cold being the specific topic of investigation. Conjecture has occurred regarding this aspect of the physiology of marsupials since the pioneering work of Martin (1902). Martin, prompted by earlier studies of Sutherland {1897), examined the body temperatures and metabolic rates of marsupials and eutherians, as well as of monotremes. Marsupials were reported to have body temperatures and metabolic rates intermediate between those of eutherians and monotremes; the metabolic rates of the marsupials were less than one third of those of the eutherians. For some five decades Martin’s work was cited as demonstrating that marsupials represented an intermediate level of homeothermic development, below the “advanced” eutherians but better than the “very primitive” monotremes. The notion of marsupials as “primitive” mammals became entrenched (Johansen, 1962). The situation has been much clarified over the past decade. The minimal resting metabolic rate or standard metabolic rate (SMR) of marsupials has been demonstrated to vary with the 0.75 power of body mass in the same manner as in eutherians, but. at any mass, the level is about 70% of the corresponding eutherian level (Dawson & Hulbert, 1969, 1970; MacMillen & Nelson, 1969). The thermoregulatory abilities of a variety of marsupials, especially those of some of the larger macropodids, also have been examined and, generally have been shown to be similar to those of eutherians (Dawson, 1973a; Dawson et al., 1974). Smaller species, such as many of the dasyurids,
MATERIAL& METHODS The dasyurids examined were the Paucident Planigale P/aniga/r gi/esi and the Kowari. ksyuroidcs hymei. Both these species are found in semiarid and arid regions, P. gilesi coming from Western N.S.W. and D. byrnei from southwestern Qld. The rodents were the Fawn Hoppingmouse, Notomys cercinus, and the Eastern Chestnut Mouse, Pse~d~~~s gra~j~i~uudat~~. The N. ce~~~i~u~came from southwestern Queensland and the P. ~ruei~i~u~~af;~s
* Permanent address: Division of Biological Sciences. University of Michigan, Ann Arbor, MI 38109, U.S.A. 59
60
TERENCEJ. DAWSONand WILLIAMR. DAWSON
from the central coast of N.S.W. Animals had been kept in an unheated animal house for several months prior to the experiments, which were carried out during winter and early spring (June-September). The only exception involved three planigales, which were wild caught in September. The temperature of the animal house followed outside ambient; usual daily maxima were 1621°C with minima of 8 14°C. Nest material or nest boxes were provided. Animals were fasted overnight only in experiments at the highest temperatures, i.e. in the thermoneutral zone. Fasting prior to low temperature experiments occasionally led to torpor in the marsupials. Metabolic responses to various temperatures were tested in either of two temperature controlled cabinets, which operated down to - 3’ and - 20°C. respectively. To enable the animals to rest undisturbed in a normal posture, body temperature was not monitored continuously. Temperatures were measured with copper-constantan thermocouples. Body temperatures, taken as deep rectal temperature, were obtained at the beginning and end of the experiments. The basic gas measuring system used the positive pressure. open circuit technique. Air was passed through a small perspex chamber containing the animal, at a rate measured by a calibrated dry gas meter. Oxygen consumption and carbon dioxide production were determined using a Beckman F3 paramagnetic analyser and a Beckman model 864 infrared gas analyser. respectively. The oxygen analyser was cd&rated manometrically before each experiment and the carbon dioxide analyser was calibrated using standard gases. Oxygen consumption and carbon dioxide production were calculated as dry gas at STP. Heat production was estimated from oxygen consumption and RQ, which varied between 0.84 and 0.71. using the appropriate conversion factors (Brody. 1945). Whole body conductances, uncorrected for heat loss by evaporation or changes in T,, were measured by the formula: (in W m z Cm I)
conductance
heat production (T, - T,)
1surface area
Surface area was calculated using the equation S.A. (in m’) = 0.10 kg”‘. The Meeh factor adopted, 0.10, was one considered appropriate for general comparative estimates of total surface area. although this is slightly lower than the
Table
Mass N
g
1. Standard
metabolic
L C
1.1 5 118 i: 12 - 10.3 5 118 + 14 Notr~nt~s ~wrinu.s 32.0 5 32.5 I: 3.0 -0.2 5 32.1 i. 1.4 5 33.1 +_ 3.2 -13.1 Pwurlot~~~~.s yrclcilicurrtlatus 31.9 5 79.8 k 6.9 -0.7 5 15.6 +- 8.5 5 81.2 & 11.3 -10.6
rate and metabolic
TId> c
value obtained for small marsupials in the study of Dawson & Hulbert (1970). To obtain good base line readings for SMR measurements, all species were placed in the chambers for some 46 hr. starting at 09:OO hr. Reported measurements were taken over two, 20min periods in the latter part of the exposure, but before 15:30 hr. Preliminary experiments indicated that after approximately 16:OO hr, oxygen consumption could start to increase as the animals became more restless. The same pattern was followed during cold exposures, except experiments were terminated if oxygen consumption noticeably declined. In these cases. the oxygen consumption reported was that obtained before the decline. Because of concern about the limited number of planigales, these tiny dasyurids were examined at less extreme temperatures and for shorter periods, the exposure period before data collection being 3 hr.
RESULTS Values for body temperatures
responses rodents
02 Consumption 1 kg-r hrr’
to cold exposure
of small
Heat production W kg-‘.”
MRiSMR
--
36.8 * 0.5 35.8 k 0.9 35.2 & 1.3
1.28 +- 0.12 8.89 t 0.42 10.98 2 2.00
2.32 f 0.12 15.4 f 1.46 19.0 f 2.30
6.6 & 0.6 8.2 t: 1.0
& 0.8 + 0.8
35.6 & 1.0 36.2 & 1.6 37.1 rt 0.5
0.65 k 0.06 4.05 + 0.46 5.80 + 0.53
2.12 2 0.17 13.2 + 1.66 18.6 & 2.08
f 0.9 * 1.5 i 1.0
37.0 + 0.7 36.9 f 0.8 34.2 + 2.6
1.44 + 0.14 6.06 + 0.24 8.85 ) 0.85
* 1.3 * 2.4 f 2.9
37.4 + 0.6 36.2 + 0.2 29.4 + 4.0
1.05 + 0.05 3.27 -i: 0.16 4.03 5 0.46
* Time to data indicates the time to the beginning Values are means + SD.
and metabolic
rates
for the four species at thermoneutral temperatures and two low temperatures are summarised in Table 1, The data in thermoneutral conditions for body temperature and metabolic rate of the marsupials and eutherians follow a conventional pattern. The overall mean body temperatures of the marsupials was 36.2 + 0.98’C as opposed to a group mean for the two eutherians of 37.2 rt: 0.67”C (P < 0.02). The SMR for the marsupials and eutherians in the mass-independent units of W kg-0.75, were 2.22 + 0.17 and 3.27 + 0.29 respectively (P c 0.001). These values are close to the predicted ones for the SMR, of 2.35 W kg-o.75 (Dawson & Hulbert, 1970) and 3.34 W kg-o.75 (Kleibet, 1961) respectively for marsupials and eutherians. The marsupial values are 687,, of the eutherian ones. The responses to cold environments are interesting. but difficult to interpret, unless the time course of experiments is kept in mind. With the exception of the tiny planigales, all species maintained body temperature down to about O’C, and even some of the larger marsupials
Time to data* min
and
Conductance Wm-2’C-I
245 f 95 189 + 53 132 k 41
4.9 i 1.32 4.3 2 0.47 4.4 i 0.57
6.2 1. 0.8 8.8 & 1.0
336 + 64 290 i 35 225 i 57
4.3 i 1.00 3.2 + 0.33 3.4 + 0.34
3.42 k 0.33 14.1 f 0.58 21.0 f 0.45
4.1 & 0.2 6.1 + 0.5
291 4 64 288 i 58 150 + 28
5.3 + 0.83 2.9 i 0.14 3.4 2 0.16
3.12 k 0.17 9.6 k 0.42 12.0 + 1.54
3.1 & 0.2 3.8 & 0.5
255 + 69 251 rL_68 113 + 59
4.8 + 1.02 2.2 * 0.18 2.5 * 0.36
of data collection.
-
Metabolic scope and conductance male planigales (11.5-12.5 g) maintained T,, at a T, close to 0°C for periods in excess of 3 hr. Below zero, - 10 to - 13°C. the picture changed and only D. byrnei maintained Tb for the test period of 4 hr. Of the eutherians the small hopping mouse N. cervinus performed well and body tem~rature was reasonably maintained for some 3 hr, whereas the larger P. gracilicaudatus was unable to maintain Tb more than 1: hr at - 10°C. Reasons for the differing thermoregulatory capacities are suggested by the data on metabolic responses. Pseudomys gracilicaudatus had the lowest maximum metabolic rate both in mass-specific and rn~s-independent terms. The pattern of metabolic response to cold varied between the marsupials and eutherians (Table 1). While the marsupials started with a lower basal heat production their maximum metabolic responses were similar to that of N. ceroinus, the eutherian with the better thermogenic capacity of the two species tested. It should also be noted that the value for D. byrnei was probably submaximal because T, was maintained to the end of the experiment. This pattern is best appreciated by the ratio of maximum metabolic rate to SMR. In both marsupials the relative increase, 8-9 times, was significantly higher than in either of the eutherians, and was double that of P. ~ru~i~~caadafl~s. For the maintenance of body temperature in a cold environment, the reduction of heat loss is the other important variable apart from increased heat production. The variation in conductance at different air temperatures is shown in Table 1. The general pattern which emerged for all species was consistent with that for homeotherms generally. In the thermoneutral zone, conductance was elevated as thermoregulatory vasomotor and pilomotor adjustment occurred. Conductance was minimal around zero but increased at the lowest temperatures, particularly well below freezing, This effect presumably resulted partially from increased shivering, which may break up the air boundary layer. Possibly more important in these results could be an increased blood flow to the periphery to
I
4
0 001
I
I
I
0 01
01
IO
Body
I 100
nwss. kg
Fig. 1. Conductance values for the marsupials and rodents compared with the relationships between conductance (converted to W m -’ Y-l) and mass previously obtained for eutherians and marsupials by Herreid & Kessel (1967) and MacMillen & Nelson (1969) respectively. Data for PhascoIarctos cinereus (Degabriele & Dawson, 1979) is also included. 0 P. gilesi; m D. byrnei; o N. cervinus; l P. graciliccwfntus; A P. cinereus.
61
give protection against freezing of the tissues, i.e. frost bite. No large differences were seen between the minimal conductance levels of the two groups of mammals (Fig. l), although the values from the marsupials tended to be higher. The planigales with their very short fur had a high conductance. The P. ~rl~~~i~~alldatus, which had the smallest metabolic scope, had the lowest conductance, that is the highest total body insulation. DISCUSSION
The pattern of difference between marsupials and eutherians which is evident in resting, thermoneutrai body temperatures, together with that in standard metabolic rates is in agreement with that found in many of the studies undertaken in the past decade following the primary studies of Dawson & Hulbert (1969, 1970) and MacMiIlen & Nelson (1969). Few studies have actually compared eutherians and marsupials directly, although Dawson & Hulbert (1970) examined rabbits to reinforce their results. This general lack of direct comparative study has enabled the perpetuation of the idea that the difference in SMR between the two groups could be due to a Qlo effect associated with differences in body temperature (Kinnear & Shield, 1975). When marsupials and eutherians are treated similarly as in the current experiments the data do not support this proposition and it is probably time that the idea was laid to rest. It may be argued that comparisons of the metabolic status of various groups of homeotherms based on the SMR are not particularly valid, because the conditions under which the SMR is determined are rather artificial and rarely related to the animal’s activities in the real world. However there is ample evidence that other levels of physiological activity in marsupials are related to the SMR. These include normal maintenance, nitrogen and energy requirements (Brown & Main, 1967: Hume. 1974) and water requirements (Denny & Dawson, 1975). Also, most importantly. the maximal sustained metabolic responses to cold in some groups of birds and mammals consistently appear to be about quadruple the SMR (Gelineo, 1964). Therefore such maximal responses could be limited in absolute terms in those groups with low SMR (Dawson, 1973b). Data on bandicoots (Hulbert & Dawson, 1974) suggest that this may be also true for marsupials, but other studies have argued against a limiting relationship between metabolic capability and SMR for marsupials. Baudinette et al. (1976) have in fact proposed that the metabolic scope of dasyurids in response to exercise may be greater than that of eutherians. The relationship between metabolic responses to cold and the energy expenditure during exercise is unclear because, for large mammals such as the red kangaroo, an increase in metabolic rate during sustained exercise representing at least 20 times the SMR is possible (Dawson & Taylor, 1973). While several workers have dealt with this problem, no concensus as yet exists concerning what is maximum metabolic activity and how it should be assessed. Hart (1971) reviewed much of the initial work, particularly that dealing with small mammals, and he recognised at least two different levels of maximum metabolic ac-
62
TERENCEJ. DAWSONand WILLIAMR. DAWSON
tivity, peak metabolic effort and summit metabolism. The first of these, peak metabolic effort (Hart, 1957), is the highest rate of oxygen consumption that can be sustained for a short time, some 3-20 minutes. This may be attained by exposure to extreme cold under conditions where heat loss initially exceeds heat production, or by the addition of exercise to a submaximal cold exposure. This latter test is made on the assumption that heat production due to shivering and that due to exercise, are in the short term, interchangeable. Some doubt exists about whether peak rates obtained by these two procedures are comparable, but they seem similar, at least in small rodents. Peak metabolic effort appears to be 7 times SMR in small mammals (Hart, 1971), but is obviously higher in exercise in larger cursorial species. Summit metabolism is the other measure of metabolic scope used for comparative purposes (Gelineo, 1964), and this is the highest metabolic rate that can be sustained in the cold by a sedentary animal. Some doubt exists about the appropriate time scale for measurements of summit metabolism, but a period of at least several hours is now accepted. Over a range of homeotherms it seems that most species have a summit metabolism 3-4 times basal (Gelineo, 1964) although a few northern hemisphere mammals from cold climates have been reported to exceed this figure in winter (Rosenmann et al., 1975). Some small birds which reside in the boreal winter of the northern hemisphere also have exceptional metabolic capabilities but it has also been noted that they have a high SMR (Dawson & Carey, 1976). In our examination of the metabolic capabilities of marsupials, we were primarily interested in maximum metabolic responses, sustainable by homeothermic animals over an extended period in severe cold. We have thus been concerned with an approximation of summit metabolism, rather than in peak effort. In this regard two cold test temperatures were used to characterise responses more completely. The three larger species were able to maintain Tb for the test time of approx. 5 hr at the temperatures near 0°C. However, even the planigales, with the exception of a 7.7 g female maintained Tb for their test period near freezing for 3 hr. Below freezing, the responses of D. byrnei and the rodents differed. Dasyuroides byrnei maintained Tb for the test period of 4 hr, whereas neither of the eutherians could do so for this interval. The summit metabolism of the eutherians therefore develops between the two cold test temperatures and approx. 3-5 times their SMR; N. ceruinus reached a level 6 times SMR but could not maintain it. The dasyurids therefore have a higher summit metabolism relative to their SMR, some 8-9 times SMR, one Kowari actually maintained a metabolic level 10.4 times SMR. The dasyurids, then, are not restrained in their response to cold stress by their initially low SMR. This is further indicated by data derived from Dawson & Wolfers (1978), Fig. 2, where a P. gilesi maintained oxygen consumption l@ll times SMR for many hours. The true relative metabolic capabilities are appreciated by consideration of the data in the mass independent terms of W kg-o.75 (Table 1). In this comparison the marsupials have rates of heat production approximating that of N. cercinus and substantially exceeding
1
20
I
Lights
off I
0.
l *
.
.
. 2
i
.*
C,O-
l
E
a
z
l .
0..
-
. _.=
*.
l**e
.
:
. .
8
mm... k 5- ------
--
..**
. Pred
cond
P +
.
3
-6
0”_
J
. . . . . ...’
0” __----
IO
2
- - SMR0,33X
0 16
20
24
04
06
12
16
Time. hr
Fig. 2. Oxygen consumption (0) and conductance (m) of a P. clilesi (wt 9.4 g) in the cold (14.5”C) for 24 hr. The olanigale was inactive and curled up while the lights were on but was active and feeding for much of the night period. Food, Tenebrio sp larvae, was available ad lib. Values arc hourly means. The SMR for this animal at a Tai, of 33 C is indicated, as is the predicted minimum conductance value from MacMillen & Nelson (1969).
that of P. gracilicaudatus. However, N. ceruinus could not maintain this rate whereas D. byrnei could. How then do these small dasyurids manage this metabolic scope? Rodents rely heavily on nonshivering thermogenesis (NST) in their responses to cold (Hart, 1971) and since these experiments were carried out in winter and the animals were kept in unheated quarters NST might be functional. One explanation for the large metabolic scope of the dasyurids could be a greater capacity for NST, but this appears unlikely. Reports of NST in marsupials are as yet conflicting. Reynolds & Hulbert (1982) suggest that it is absent and even those studies reporting NST in marsupials are equivocal because the doses of noradrenaline required to elicit a response are far greater than those needed for rodents (Nicol, 1978; Wallis, 1979). It is possible that the dasyurids rely primarily on shivering for their regulatory heat production. In this regard it is interesting that the maximum sustained rates of heat production in exercise and cold thermogenesis are both approximately 8-9 times SMR in dasyurids (Baudinette et al., 1976; R. E. MacMillen & T. J. Dawson, unpublished data). An interesting parallel to this discussion of the metabolic capabilities of dasyurids and other marsupials is their very low resting heart rates (Kinnear & Brown. 1967). These are much lower than those of eutherians, lower even than would be expected from their lower SMR. On the other hand. marsupials compensate for these low heart rates by having a much larger heart stroke volume (Dawson & Needham, 1981). If, as Baudinette (1978) has reported, marsupials and eutherians have similar maximal heart rates, then maximal cardiac outputs may be greater in marsupials. This would be quite consistent with the data indicating the high sustained aerobic capacity of marsupials and it is conceivable that marsupials are superior to eutherians of comparable size in aerobic capacity. It had been suggested that low metabolic rates in marsupials might be compensated for by a lower rate
Metabolic scope and conductance
of heat loss than seen in eutherians (Dawson, 1973b). While this option appears used by larger marsupials (Dawson. 1973a; Degabriele & Dawson, 1979), it is not available for smaller species (Fig, 1). MacMillen & Nelson (1969) failed to find a difference between their data for dasyurid conductance and the predictions for eutherians by Herreid & Kessel (1967), and the pattern noted in the current study did not differ markedly from these previous estimates. In small mammals conductan~ through the core to skin surface is high, because of the high rate of heat transfer through tissue (about 10 times that through fur) and the very small distances involved. As animals become larger however this situation may change and marked adjustments can be made by the utilization of mechanisms such as countercurrent arrangements (Dawson & Fanning, 1981). There are also obvious constraints on the amount of fur a small mammal can carry. Combined with these factors there is the additional problem with the variation of the effective surface area for heat loss. The conductances given in Table 1, and Fig. 1 are minimum conductances and represent the conditions when the animals are inactive and curled up into a ball; the Meeh factor for a sphere is 0.047, about half the measured total surface. When a small mammal is active the effective surface area approximates the total surface and heat flow is doubled (Fig. 2), greatly increasing the metabolic heat requirement. Given these circumstances, if a small dasyurid or any other small animal is to remain homeothermic over a wide temperature range, it must have a large metabolic capacity. In marsupials with their low SMR this means a large functional metabolic scope. Whether this is a feature of marsupials in general or a specific adaptation to small size such as may occur in some groups of shrews, has yet to be determined. ~cknowled~e~e~rs-The authors wish to thank F. D. Fanning for his technical assistance and B. Fox and D. Read for providing animals. The work was supported by a grant from the Australian Research Grants Committee. W. R. Dawson was in receipt of a Visiting Professorship from the University of New South Wales and received some support from the Horace H. Rackham School of Graduate Studies, the University of Michigan.
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and
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