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The ecological significance of thermoregulatory responses to heat stress shown by two populations of an Australian murid, Rattus fuscipes
Cmp.
Biochm.
Physiol., 1973, Vol. 44A, pp. 1129to 1140.Pergamon Press. Printed in Great Britain
THE ECOLOGICAL SIGNIFICANCE OF THERMOREGULATORY RESPONSES TO HEAT STRESS SHOWN BY TWO POPULATIONS OF AN AUSTRALIAN MURID, RATTUS FUSCIPES B. G. COLLINS Department of Pharmacy, Western Australian Institute of Technology, Western Australia 6102
Bentley,
(Received 22 June 1972) Abstract-1. Both populations of Rattusfusci~es thermoregulate well at ambient temperatures below their lower critical temperatures, being assisted by low thermal conductances that vary directly with ambient temperature. 2. All animals remain normothermic when subjected to temperatures within their thermoneutral zones, although they become hypertheqmic at higher temperatures. Evaporative cooling is less effective as a means of delaying lethal hyperthermia than in other Australian Rut&s species. 3. The two populations of R. fuscipes studied show minor differences in thermoregulatory ability which correlate well with differences in their environments. 4. The absence of R. fuscapes from relatively hot parts of northern Australia, whilst being abundant in cooler, southern areas, can be explained in terms of the thermoregulatory physiology of this species. INTRODUCTION
THE PAUCITY of published information regarding the abilities of members of the Muridae, one of the largest rodent families, to withstand heat stress has been discussed by Collins (1972) and Collins & Bradshaw (1972). The above authors have referred especially to a lack of information for Australian murids which is rather surprising in view of the existence of extreme macro-environmental temperatures in many parts of Australia where murids are found (Troughton, 1965; Ride, 1970; Gentilli, 1971). One of the most widespread of the Australianmurid groups is the R&us genus (Ride, 1970). The apparent restriction of certain species to cooler southern areas of the continent, while others such as R. vdlotist*mus, R. lutreolus, R. tunneyi and R. rattus are capable of surviving in hotter, northern areas, suggests that members of the genus may show differences between their physiological and/or behavioural responses to environmental heat stress which correlate with their geographical distributions. Investigations aimed at testing this hypothesis for R. lutreolus, R. vdlotidmu-s and R. rattat have been reported previously (Collins, 1972; Collins & Bradshaw, 1972). The results of similar studies on two geographically isolated 1129
B. G.
1130
COLLINS
populations of R.fuscipes, a species restricted to the coastal and foothill regions of south-western and south-eastern Australia, are discussed in the present paper. MATERIALS
AND METHODS
c011ectio?t and ??Iaintenance of a?u*mls Twenty members of two geographically isolated populations of Rattus fumpes located near Jurien Bay and Way&i&up River, Western Australia, respectively (Fig. l), were trapped and taken immediately to the laboratory. They were housed in individual wire
j \----Jurien
Bay
Western
Australia
L
FIG. 1. Known distribution of R. fusczpes within Western Australia (based upon personal observations, and records kept by the West Australian Museum). Bach symbol signifies the collection of at least one specimen in that particular area. mesh cages (30 x 30 x 30 cm) in an environmental room which had an ambient temperature of 25 f l”C, a relative humidity that varied between 48 and 65%, and a photoperiod’ that extended from 0800 to 2000 hr. All rata were subsequently maintained on ad lib. regimes of standard rat cubes (Wesfeeds Pty. Ltd.) and tap water. No data were collected from the animals until they had been kept in the laboratory for at least 4 weeks. Carbon diox& productian and pulmocutaneous
water loss
Rates of carbon dioxide production and pulmocutaneoua water loss were measured simultaneously in the light for 24-hr post-absorptive rats, using the gravimetric method described in detail by Collins & Bradshaw (1972). All measurements were made during the time between 1100 and 1700 hr, a period found to be one of minimal activity and body temperatures for members of both populations.
TIiERMORECX7LATORY
RESPONSES TO HEAT SlXESS IN RATTUS
FUSCIPES
1131
Air which had been dried and freed of CO8 by passage through drierite and ascarite absorbents was passed into each respirometer containing a rat at a constant rate of 800 ml/mm. Similar absorbents were used to remove pulmocutaneous water and metabolic COs from air leaving the respirometer, with weight changes in the absorbents being measured to the nearest 0-l mg over 15-min test periods at a particular ambient temperature. The ambient temperature within each respirometer was measured by means of a standard mercury thermometer, and maintained at a suitable level (+ O*Z’C) by means of a thermostatically controlled water-bath. Breuthing rate Breathing rates were measured simultaneously with carbon dioxide outputs and puhnocutaneous water losses. Counts were made for several 2%set intervals at each ambient temperature, and the means calculated. Body temperature Rectal temperatures of post-absorptive rats were measured under conditions similar to those already described for the determination of carbon dioxide production and pulmocutaneous water loss. The only essential difference was that rata were removed from the respirometers after 1 hr at a particular ambient temperature, and their temperatures measured immediately by means of rectal thermistor probes connected to a Yellow Springs International telethermometer. Each probe was inserted to a depth of 7 cm into the rectum. Skin structure Samples of thoracic and abdominal akin were removed from the ventral surfaces of several members of each population, then fixed in 10% form01 saline. Sections were cut at 6 p and stained with haematoxylin and eosin. RESULTS
On the following pages, the Waychinicup River population of R. fusci$es is referred to as R. furcipes (W.R.) and the Jurien Bay population as R.fuscipes (J.B.).
Members of both populations of R. fuscipes respond to ambient temperatures between approximately 10 and 30°C by assuming upright, hunched postures and flufKng their fur. No visible shivering occurs, and the animals are usually quite calm. At higher ambient tempera~res, the rats tend to lie on their ventral surfaces for much of the time, with their fur noticeably less fluffed, although they become more restless as the temperature rises, exhibit sporadic licking of the front paws, thorax and abdomen, and frequently shift position. Most animals exhibit marked drooling at temperatures in excess of approximately 39”C, but none seem capable of increasing the frequency of licking beyond that shown at lower temperatures. Metabolic responsesto chatrgesin ambient temperu&re The influence of ambient temperature upon rates of CO, production for the two populations is shown in Fig. 2. Both populations exhibit thermo-neutral zones, with the respective lower critical temperatures (TLC) and upper critical temperatures (Tut), defined by solving simultaneous regression equations fitted to 37
1132
B. G. COLLINS
data by the method of least squares (Simpson et al., 1960), being almost identical (R.fk.rcz~ (W.R.): TLC = 28*1”C, Z’uc = 329°C; R.furcipes (J.B.): TLC = 28*6”C, Tu, = 3298°C).
4.0R.
fwcipes (WR)
2.0--.. 7
z. 0.0 s.
4’0R. fuscipes(JB)
fA)
OC
FIG. 2. Variations in metabolic rates (M) caused by changes in ambient temperature (Td. The symbols TLC and Tut indicate the lower and upper critical temperatures, respectively. Regression lines drawn on the graphs have been fitted by the method of least squares, with lines (a), (b) and (c) corresponding to the following equations: R. fuccipa (W.R.) (a) M = -O*OSST&+2.56, (b) M = -0+02T~+1*07, (c) M = O*lOOT* -2.29; R.fwcipes (J.B.) (a) M = -O*065TA +2*97, (b) M = -O+06TA+1.28, (c) M = 0+48T,-0.49.
Both populations show regression of CO, production on ambient temperature (Z’,) at temperatures below the appropriate TLC’s, although there is no significant difference between the two regression coefficients ([email protected] (W.R.): /3 = - 0.055 ; R. fuscipes (J.B.): /3 = -0.065 ; P> O-05, using the method of Simpson et al., 1960). Each regression line extrapolates to zero CO, production at a T, that is well in excess of the mean normothermic body temperature (R. fusc$xs (W.R.): 46*5”C vs. 37~5°C; R. fusczjws (J.B.): 45~7°C vs. 36~4°C). Correction of the regression lines to allow for the dissipation of metabolic heat associated with pulmocutaneous water loss (Collins & Bradshaw, 1972) appreciably improves the relationship between predicted and actual body temperatures (R. fuscz$es (W.R.): 40.6”C vs. 37~5°C; R. jkcz$es (J.B.): 39~3°C vs. 37.4”C). Thermal conductances for both populations at a number ofT,‘s, calculated by the method of Morrison et al. (1959) and indicated in Table 1, decrease as the . Ta’s are reduced below the appropriate TLc’s. The mean metabolic rates for the two populations within their thermoneutral zones are not significantly different (R. jksdpes (W.B.): l*OO+O~lS S.D. ml CO, $222) iV = 6; R. fusczpes (J.B.): 1.09 + O-16 S.D. ml CO, (g hr)-l, N = 10; .
.
At Ta’s in excess of the appropriate T,,, each population shows regression of CO, production on T,, although there is no significant difference between
TABLE
FOR BOTH POPULATIONS OF R. fuscipes AT AMBIENT RESPECTIVE LOWRRCRITICAL TEMPERATURES
~-THERMAL CONDUCTANCRS TRMPRRATURRSRRLOWTHE
Ambient temperature (“C)
1133
HEAT STRESS IN RATTVSFVSCIPES
THRRMORRGULATORYRESPONSESTO
Thermal conductance (ml COs/g hr “C)*
R. fuscipes (W.R.)
R. fuscipes (J.B.)
11.6
0.083
-
13.0 17.1
0.089
0.076 -
18.5 22.5
0.104
0.082 -
23.0 27.5
0.138
0.090 0.106
* Conductances have been calculated after the manner outlined by Morrison et nI. (1959). As mean values of TB and metabolic rate have been used at each Td, standard deviations are not available.
regression coefficients for the two groups (R. fuscipes (W.R.): (J.B.): p = 0449; P> 0.05).
b = 0.100;
R.fuscipes
&eathirzg rates Breathing rates for R. fuscipes are illustrated in Fig. 3. The rates for both populations are influenced by changes in T, in a manner that approximates the variations in carbon dioxide production shown in Fig. 2. 200.
. .
.
T ;100._ E
..
. .
.*
. .
.
R . fvscipes
$ 20% =.
f ~IOO-•' 0 G R. 0
*
IO
a. ..*
. .:..., . l
. . . . . .* . .
fuscipss (JB), I IS
:T;r 1 Gc ..>’ . . ::. .
1. .:,. >.
::
: .
*
(WR 1 I
I
.
.
I 20
I
II L .
1 T,, 1 '. n ' . *. .* ' a....: ,:*., . . .. *.' *. *.* . * I 25
II 30
I 35
I 40
45
FIG. 3. Weight-relative breathing rates for rata maintained at a variety of ambient temperatures. TLC and T,, have the same meanings as in Fig. 2. The arrow projecting from each baseline represents the Td at which a pronounced increase in the log of weight-relative pulmocutaneous water loss commences.
Pulmocutaneous water losses Semi-log plots of weight-relative pulmocutaneous water loss (PWL) against TA for both populations demonstrate distinct changes in gradient (points of
1134
B. G. COLLINS
inf’lexion) in the vicinity of the thermo-neutral zones (Fig. 4). Neither population shows significant regression of log PWL on T, at temperatures below its point of inflexion. At higher ambient temperatures, however, significant regression occurs for both populations, although there is no significant difference between regression coefficients (R. jkcz$rs (W.R.): j? = 0.091; R. furciper (JR): ,!I= 0.054; P> O-05). 30.0 20.0
Rhsctbes (WI?) _
T*I
.:/’
-I
OC
FIG. 4. Weight-relative puhnocutaneous water losses (PWL) at a variety of ambient temperatures (TJ. Symbols as in Fig. 2. Letters (a) and (b) correspond to the following regression equations: R. fuscipes (W.R.) (a) log PWL = O-165 + O.OOZT,, (b) log PWL = - 2*284+0*091 TA; R. fuscz$es (J.B.) (a) log PWL = 0~160+O~O09TA, (b) log PWL = -1.171 +O.O54T,.
Both populations show relationships between log PWL per ml CO, expired and T, (Fig. 5) that resemble those illustrated in Fig. 4. Although the plots in Fig. 5 would suggest otherwise, there is no statistically significant difference between regression coefficients for TA’s above the points of inflexion (R. fuscz$es (W.R.): j? = 0.062; R. fusczpes (J.B.): p = O-042; P> 0.05). Neither population is able to achieve values of PWL which permits its members to dissipate more heat than is generated by metabolism at high ambient temperatures (equality of metabolic heat production and evaporative heat loss is represented in Fig. 5 by the horizontal dashed lines, providing the assumptions outlined by Collins (1972) are made). Regulation of body temperature The body temperatures ( TB) shown for both populations in Fig. 6 are relatively constant at Ta’s below the appropriate Tut’s, with mean values not being significantly different (R. jhctpes (W.R.): 37*5”C; R. fuscipes (J.B.): 37*4”C; P> 0.05).
THERMOREGULATORY
RESPONSES
TO
HEAT
STRESS
IN
R4TTU.S
FUSClPES
1135
FIG. 5. Pulmoeutaneous water losses per ml COs expired at a variety of ambient temperatures. Horizontal dashed lines indicate equality of metabolic heat production and evaporative heat dissipation. Other symbols as in Fig. 4. Letters (a) and (b) correspond to the following regression equations: R. fumipes (W.R.): (a) log PWL = -O*306+0.018TA, (b) log PWL = -1*388+O*062TA; R.fuscipes (J.B.) (a) log PWL = - 0.300 + 0.023 TA, (b) log PWL = - 0.085 f 0.042TA. 45 f
T “E
‘C
40. y
_
* .
.*
*. * *
I
432
.. : .
.
hm
i
.._**
*
*.
*
i .* *
* ,
T l.c
TUC
40:
3510
. . I I5
.*. . I 20
. ..a
*. I 25 7. A’
..*_ ***
I
I .
. 30 DC
FIG. 6. Relationships between ambient and body temperatures. Open circles represent body temperatures for rats experiencing lethal ambient temperatures. Other symbols as in Fig. 3.
Hyperthermia occurs at Ta’s above the Tuck, with neither population being able to achieve equality of TA and TB. Although no systematic attempt was made
1136
B. G. COLLINS
to investigate lethal temperatures for either population, Ta’s in excess of 40°C as shown in Fig. 6.
several animals died at
Structure of the skin There is no evidence of sweat glands in any of the thoracic and abdominal skin samples, although each shows the existence of sebaceous glands and a corrugated epidermis. DISCUSSION
Physiblogi~al responses to heat stress The evidence presented in Fig. 6 clearly demonstrates the ability of each R. fuscz$es population to maintain a relatively constant body temperature when exposed to ambient temperatures between approximately 10°C and its TLC. Despite the significant TB- T_k differentials that exist within this TA range, both populations are able to minimize the increases in metabolic heat production that are needed to offset heat losses to the environment (Fig. 2); This is made possible by the extremely efficient insulation exhibited by the rats. frhe mean conductance (C) indicated by the regression of metabolic rate on T, for R. fusci$es (W.R.) is only 52.2 per cent, and that for R. fuscajks (J.B.) 65.8 per cent, of values calculated on the basis of body weight (W) according to the empirical equation C = 1~02W-“*ws ml 0, (g hr “C)-l (modified after Herreid & Kessel, 1%7).] When conductances at temperatures below the TLC’s are calculated from the relationship (Morrison et al., 1959) ‘=
metabolic rate T B- T A
rather than from regression coefficients, it is seen that values for each R. fuscipes population vary directly with the ambient temperature (Table 1). This response, which is also exhibited by several other rodents reported in the literature (MacMillen & Lee, 1970; Wunder, 1970; Collins, 1972; Collins & Bradshaw, 1972), must facilitate thermoregulation when the rats are exposed to low ambient temperatures. It is suggested that increased peripheral vasoconstriction, and possibly piloerection, is mainly responsible for those reductions in conductance which occur, although hunching of the rats at low temperatures could alter the surface area exposed to the environment sufficiently to cause significant changes in conductance. The failure of both R. fuscipes populations to conform to Newton’s law of cooling (Scholander et al., 1950) is apparent, as neither shows good correlation between measured TB and the TB obtained by extrapolation of the regression line relating metabolic rate and TA to zero metabolism. Although better agreement is obtained when metabolic rates are corrected for heat losses associated with the evaporation of pulmocutaneous water, neither population exhibits the same agreement that is shown by R. lutreolus (Collins, 1972), R. vdloskim and R. rattus (Collins & Bradshaw, 1972) when similar corrections are made. It is suggested
THERMOREGULATORY
RESPONSES
TO
HEAT
STRESS
IN
RATTVS
FUSCIPES
1137
that the inferior position of R. fuxipes, particularly the Jurien Bay population, can be adequately explained in terms of its greater change in conductance at Ta’s below the TLC. Unlike R. aillosiwimus (Collins & Bradshaw, 1972) and R. Zutreolus (Collins, 1972), R. fuscipes remains normothermic at T,‘s within the thermo-neutral zone. This occurs despite the occurrence of basal metabolic rates for R. fusc;Pes which do not show the depression, when compared with values predicted on the basis of body weights (Morrison et al., 1959), that are typical of most other nocturnally active, diurnally fossorial rodents (Carpenter, 1966; McNab, 1966; MacMillen & Lee, 1970; Collins, 1972; Collins & Bradshaw, 1972). The metabolic rate for R. fuscipes (W.R.) is only 94 per cent, and that for R. fuscipes (J.B.) 103 per cent of the predicted values. It issuggested that the pronounced increase in pulmocutaneous water loss which occurs for each R. fuscipes population at Ta’s in excess of those corresponding roughly with the appropriate TLC is probably responsible for the avoidance of hyperthermia. Both populations of R. fusczipes become hyperthermic at ambient temperatures in excess of their TUC’s. The Waychinicup River population is at least as adept at limiting hyperpthermia as is the Jurien Bay population, under relatively dry laboratory conditions at Ta’s below approximately 39°C although in doing so it clearly dissipates more water and shows a greater elevation of metabolic rate (Figs. 2, 4 and 5). Nevertheless, neither population is able to dissipate sufficient body heat by evaporative cooling to avoid lethal hyperthermia at higher T,‘s. In this regard each is therefore more akin to Notomys dexis and N. cerwinus (MacMillen & Lee, 1970), small hopping mice that inhabit hot, arid regions of Central Australia, than it is to other Rattus species, most of which can evaporate sufficient water to equalize T, and TB, and limit hyperthermia, at comparable ambient temperatures. Some of the investigations reported earlier in this paper were aimed at determining what factors were responsible for the enhanced PWL associated with high Ta’s. Although neither population shows an increase in breathing rate that is comparable with those demonstrated by animals such as the marsupial Trichosurus vulpecula (Dawson, 1969), the evidence available (Fig. 3) suggests that faster breathing could contribute significantly to the enhanced PWL’s which occur at high Ta’s. It would seem unlikely, however, that the initial increases in PWL at TA’s below the appropriate TvC’ s can be explained in terms of hyper-ventilation. Rats that are subjected to high TA’s invariably show signs of moisture on their pelage. The onset of licking for each population of R. fusctpes occurs at an TA which corresponds roughly with that at which the pronounced increase in log PWL commences, and undoubtedly contributes to this moistening of the fur. Licking is so sporadic, however, even at high Ta’s, that this response cannot be advanced as the sole non-pulmonary means of dissipating water. This view is supported by the observation that parts of the pelage which are never licked become quite moist. Histological evidence indicates that it is most unlikely that sweating could contribute significantly to PWL. However, matting of the pelage beneath the chin, particularly at T,‘s above 39°C when the PWL is relatively high, suggests that
1138
B. G. COLLINS
drooling makes a significant contribution. Moisture on other parts of the pelage which are not licked must, presumably, be due to a fairly pronounced insensible cutaneous water loss. Ecological ctmshhrations The two populations of R. fuscipes considered in the present paper were chosen so as to represent the northern and southern limits of the species in south-western Australia. As such, they occupy areas which experience quite different macroclimates (Table 2) Both populations of R. fuscz$es are fossorial, and spend most of the daytime in their burrows. Although no attempt has been made to measure burrow climatic conditions, it would seem reasonable to assume that maximum burrow temperatures would be lower than those above-ground, and humidities would be higher, whatever the season might be (Carpenter, 1966; MacMillen & Lee, 1970). If this is true, then R. ficscipes (J.B.) should seldom be subjected to Ta’s in excess of about 3O”C, or R. fuscipes (W.R.) to more than approximately 24”C, at the hottest times of the year. This means that both populations should experience peak burrow temperatures which generally do not promote enhanced PWL as a means of limiting hyperthermia (Figs. 4 and 5). The high humidities which probably prevail in the burrows should therefore not significantly influence thermoregulation by the rats. It is not difficult to envisage the problems that R.@cz$es (W.R.) would face if transferred to conditions such as those experienced at Jurien Bay. In order to remain normothermic at the prevailing Ta’s, it would need to increase its PWL, a response that could be difficult under burrow conditions. Failure to increase evaporative cooling might lead to lethal hyperthermia, whilst any increase in water loss could be troublesome in a habitat which receives significantly less rainfall than occurs at Waychinicup River. Minimum T,‘s would generally occur at night when rats of either population were above ground. Enhanced metabolism resulting from exercise and the uptake of food would help to offset heat loss to the environment, although members of each population would be aided by having low conductances. It is significant that R. fuscipes (W.R.), the population that would experience the lowest minimum T,‘s, has the lowest conductance (Table 1). R. fwcz$es is particularly abundant in south-eastern and south-western Australia, yet it is noticeable that the species does not extend into areas with macro-environmental temperatures much above 32°C (Troughton, 1965; Ride, 1970; Gentilli, 1971). Although it would be foolish to suggest that inadequate physiological responses by R. fuscipes to heat stress are the sole reasons for its limited distribution, one must be impressed by the fact that both of the populations investigated so far exhibit responses which are decidedly inferior to those shown by Rattus species which successfully occupy northern, hotter parts of the Australian continent (Robinson & Morrison, 1957; Collins, 1972; Collins & Bradshaw, 1972).
0.37
19.0
Mean daily minimum temperature (“C)
Mean rainfall (in.)
32.X
Mean daily maximum temperature (“C)
O-78
13.2
Mean daily minimum temperature (“C)
Mean rainfall (in.)
26.1
Jan.
Mean daily maximum temperature (“C)
Parameter
0.37
19.3
32-l
0.78
13.7
25.2
Feb.
0.74
17.2
29.9
l-49
12-S
23.9
Mar.
* Figures have been calculated from meteorological Melbourne.
Jurien Bay
Waychinicup River
Population
3.48
12.4
23.7
3.25
8-9
18.2
May
5.80
11.2
20.6
4.35
8.4
16.4
June
4.05
9.3
19.3
4.96
7-1
15-S
July
2.42
8.5
19.7
4.80
6.6
15.6
Aug.
1.13
8.7
21.7
3.25
7-2
16.6
Sept.
0.30
13.7
27.2
1.45
10-4
21.8
Nov.
0.18
16.6
29.9
l-57
12.2
23.9
Dec.
20.70
32.78
Total
Bureau of Meteorology,
0.72
11.1
24.7
3.49
9.1
19.4
Oct.
wm3 COLLECTED*
data provided by the Commonwealth
l-14
151
27.2
2.61
11.4
20.7
Apr.
TABLE 2-M~cxo-CLIMATIC DATA FOR BOTH AReAs IN WHICH Ruttusfwcipes
1140
B. G. COLLINS
Acknowledgements-I would like to thank Dr. S. D. Brad&w for his encouragement and advice during the course of the experimental work upon which this paper is based. Particular thanks are also due to Mr. E. Cockett for able technical assistance. Mr. J. Bannister, of the Western Australian Museum, has kindly furnished me with information on the known distribution of R. fuscipes within Western Australia. REFERENCES CARPENTERR. E. (1966) A comparison of thermoregulation and water metabolism in the kangaroo rats Dipodomys agilis and Dipodomys merriami. Univ. C&if. pubi. 2001. 78, l-36. COLLINS B. G. (1972) Physiological responses to temperature stress by an Australian murid, Rattus lutreolus. J. Mammal. (In press.) COLLINS B. G. & BRADSXAWS. D. (1972) Studies on the metabolism, thermoregulation and evaporative water losses of two species of Australian rats, Rattus tiUosi.~timusand Rattus rattus. Physiol. Zoiil. (In press.) DAWSONT. J. (1969) Temperature regulation and evaporative water loss in the brush-tailed possum Trichosurus vulpecuha. Comp. Biochem. Physiol. 28, 401-407. GENTILLI J. (1971) Climates of Australia and New Zealand. In World Survey of Climatology, Vol. 13. Elsevier, New York. HERREID C. F. & KEPSHLB. (1967) Thermal conductance in birds and mammals, Comp. Biochem. Physiol. 21, 405414. MACMILLBN R. E. & Lxx A. K. (1970) Energy metabolism and p&no-cutaneous water loss of Australian hopping mice. Comp. Biochem. Physiol. 35, 355-369. MCNAB B. K. (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47, 712-733. MORRISONP. R., RYSER F. A. & DARE A. R. (1959) Studies on the physiology of the masked shrew (Sorex cinereus). Physiol. Z&l. 32, 256-271. RIDE W. D. L. (1970) A Guide to Natiue Mammals of Australia. Oxford University Press, Melbourne. ROBINSONK. W. & MORRISONP. R. (1957) The reactions to hot atmospheres of various species of Australian marsupials and placental animals. J. cell. camp. Physiol. 49,455478. SCHOLAND~~ P. F., HOCK R., WATERSV., JOHNSONF. & IRVINGL. (1950) Heat regulation in some arctic and tropical mammals and birds. Biol. Bull. 99, 237-258. SIMPSONG. G., L~WONTINR. C. & ROE A. (1960) Q uantitatiue Zoology. Harcourt, Brace & World, New York. TROUGHTONE. (1965) Furred Animals of Australia. Angus & Robertson, Sydney. WIJNDER B. A. (1970) Temperature regulation and the effects of water restriction on Merriam’s chipmunk, Eutamias merriami. Comp. B&hem. Physiol. 33, 385403. Key Word regulation.
In&x-Thermoregulation;
heat
stress;
Rattus
fuscipes;
temperature
Biochm.
Physiol., 1973, Vol. 44A, pp. 1129to 1140.Pergamon Press. Printed in Great Britain
THE ECOLOGICAL SIGNIFICANCE OF THERMOREGULATORY RESPONSES TO HEAT STRESS SHOWN BY TWO POPULATIONS OF AN AUSTRALIAN MURID, RATTUS FUSCIPES B. G. COLLINS Department of Pharmacy, Western Australian Institute of Technology, Western Australia 6102
Bentley,
(Received 22 June 1972) Abstract-1. Both populations of Rattusfusci~es thermoregulate well at ambient temperatures below their lower critical temperatures, being assisted by low thermal conductances that vary directly with ambient temperature. 2. All animals remain normothermic when subjected to temperatures within their thermoneutral zones, although they become hypertheqmic at higher temperatures. Evaporative cooling is less effective as a means of delaying lethal hyperthermia than in other Australian Rut&s species. 3. The two populations of R. fuscipes studied show minor differences in thermoregulatory ability which correlate well with differences in their environments. 4. The absence of R. fuscapes from relatively hot parts of northern Australia, whilst being abundant in cooler, southern areas, can be explained in terms of the thermoregulatory physiology of this species. INTRODUCTION
THE PAUCITY of published information regarding the abilities of members of the Muridae, one of the largest rodent families, to withstand heat stress has been discussed by Collins (1972) and Collins & Bradshaw (1972). The above authors have referred especially to a lack of information for Australian murids which is rather surprising in view of the existence of extreme macro-environmental temperatures in many parts of Australia where murids are found (Troughton, 1965; Ride, 1970; Gentilli, 1971). One of the most widespread of the Australianmurid groups is the R&us genus (Ride, 1970). The apparent restriction of certain species to cooler southern areas of the continent, while others such as R. vdlotist*mus, R. lutreolus, R. tunneyi and R. rattus are capable of surviving in hotter, northern areas, suggests that members of the genus may show differences between their physiological and/or behavioural responses to environmental heat stress which correlate with their geographical distributions. Investigations aimed at testing this hypothesis for R. lutreolus, R. vdlotidmu-s and R. rattat have been reported previously (Collins, 1972; Collins & Bradshaw, 1972). The results of similar studies on two geographically isolated 1129
B. G.
1130
COLLINS
populations of R.fuscipes, a species restricted to the coastal and foothill regions of south-western and south-eastern Australia, are discussed in the present paper. MATERIALS
AND METHODS
c011ectio?t and ??Iaintenance of a?u*mls Twenty members of two geographically isolated populations of Rattus fumpes located near Jurien Bay and Way&i&up River, Western Australia, respectively (Fig. l), were trapped and taken immediately to the laboratory. They were housed in individual wire
j \----Jurien
Bay
Western
Australia
L
FIG. 1. Known distribution of R. fusczpes within Western Australia (based upon personal observations, and records kept by the West Australian Museum). Bach symbol signifies the collection of at least one specimen in that particular area. mesh cages (30 x 30 x 30 cm) in an environmental room which had an ambient temperature of 25 f l”C, a relative humidity that varied between 48 and 65%, and a photoperiod’ that extended from 0800 to 2000 hr. All rata were subsequently maintained on ad lib. regimes of standard rat cubes (Wesfeeds Pty. Ltd.) and tap water. No data were collected from the animals until they had been kept in the laboratory for at least 4 weeks. Carbon diox& productian and pulmocutaneous
water loss
Rates of carbon dioxide production and pulmocutaneoua water loss were measured simultaneously in the light for 24-hr post-absorptive rats, using the gravimetric method described in detail by Collins & Bradshaw (1972). All measurements were made during the time between 1100 and 1700 hr, a period found to be one of minimal activity and body temperatures for members of both populations.
TIiERMORECX7LATORY
RESPONSES TO HEAT SlXESS IN RATTUS
FUSCIPES
1131
Air which had been dried and freed of CO8 by passage through drierite and ascarite absorbents was passed into each respirometer containing a rat at a constant rate of 800 ml/mm. Similar absorbents were used to remove pulmocutaneous water and metabolic COs from air leaving the respirometer, with weight changes in the absorbents being measured to the nearest 0-l mg over 15-min test periods at a particular ambient temperature. The ambient temperature within each respirometer was measured by means of a standard mercury thermometer, and maintained at a suitable level (+ O*Z’C) by means of a thermostatically controlled water-bath. Breuthing rate Breathing rates were measured simultaneously with carbon dioxide outputs and puhnocutaneous water losses. Counts were made for several 2%set intervals at each ambient temperature, and the means calculated. Body temperature Rectal temperatures of post-absorptive rats were measured under conditions similar to those already described for the determination of carbon dioxide production and pulmocutaneous water loss. The only essential difference was that rata were removed from the respirometers after 1 hr at a particular ambient temperature, and their temperatures measured immediately by means of rectal thermistor probes connected to a Yellow Springs International telethermometer. Each probe was inserted to a depth of 7 cm into the rectum. Skin structure Samples of thoracic and abdominal akin were removed from the ventral surfaces of several members of each population, then fixed in 10% form01 saline. Sections were cut at 6 p and stained with haematoxylin and eosin. RESULTS
On the following pages, the Waychinicup River population of R. fusci$es is referred to as R. furcipes (W.R.) and the Jurien Bay population as R.fuscipes (J.B.).
Members of both populations of R. fuscipes respond to ambient temperatures between approximately 10 and 30°C by assuming upright, hunched postures and flufKng their fur. No visible shivering occurs, and the animals are usually quite calm. At higher ambient tempera~res, the rats tend to lie on their ventral surfaces for much of the time, with their fur noticeably less fluffed, although they become more restless as the temperature rises, exhibit sporadic licking of the front paws, thorax and abdomen, and frequently shift position. Most animals exhibit marked drooling at temperatures in excess of approximately 39”C, but none seem capable of increasing the frequency of licking beyond that shown at lower temperatures. Metabolic responsesto chatrgesin ambient temperu&re The influence of ambient temperature upon rates of CO, production for the two populations is shown in Fig. 2. Both populations exhibit thermo-neutral zones, with the respective lower critical temperatures (TLC) and upper critical temperatures (Tut), defined by solving simultaneous regression equations fitted to 37
1132
B. G. COLLINS
data by the method of least squares (Simpson et al., 1960), being almost identical (R.fk.rcz~ (W.R.): TLC = 28*1”C, Z’uc = 329°C; R.furcipes (J.B.): TLC = 28*6”C, Tu, = 3298°C).
4.0R.
fwcipes (WR)
2.0--.. 7
z. 0.0 s.
4’0R. fuscipes(JB)
fA)
OC
FIG. 2. Variations in metabolic rates (M) caused by changes in ambient temperature (Td. The symbols TLC and Tut indicate the lower and upper critical temperatures, respectively. Regression lines drawn on the graphs have been fitted by the method of least squares, with lines (a), (b) and (c) corresponding to the following equations: R. fuccipa (W.R.) (a) M = -O*OSST&+2.56, (b) M = -0+02T~+1*07, (c) M = O*lOOT* -2.29; R.fwcipes (J.B.) (a) M = -O*065TA +2*97, (b) M = -O+06TA+1.28, (c) M = 0+48T,-0.49.
Both populations show regression of CO, production on ambient temperature (Z’,) at temperatures below the appropriate TLC’s, although there is no significant difference between the two regression coefficients ([email protected] (W.R.): /3 = - 0.055 ; R. fuscipes (J.B.): /3 = -0.065 ; P> O-05, using the method of Simpson et al., 1960). Each regression line extrapolates to zero CO, production at a T, that is well in excess of the mean normothermic body temperature (R. fusc$xs (W.R.): 46*5”C vs. 37~5°C; R. fusczjws (J.B.): 45~7°C vs. 36~4°C). Correction of the regression lines to allow for the dissipation of metabolic heat associated with pulmocutaneous water loss (Collins & Bradshaw, 1972) appreciably improves the relationship between predicted and actual body temperatures (R. fuscz$es (W.R.): 40.6”C vs. 37~5°C; R. jkcz$es (J.B.): 39~3°C vs. 37.4”C). Thermal conductances for both populations at a number ofT,‘s, calculated by the method of Morrison et al. (1959) and indicated in Table 1, decrease as the . Ta’s are reduced below the appropriate TLc’s. The mean metabolic rates for the two populations within their thermoneutral zones are not significantly different (R. jksdpes (W.B.): l*OO+O~lS S.D. ml CO, $222) iV = 6; R. fusczpes (J.B.): 1.09 + O-16 S.D. ml CO, (g hr)-l, N = 10; .
.
At Ta’s in excess of the appropriate T,,, each population shows regression of CO, production on T,, although there is no significant difference between
TABLE
FOR BOTH POPULATIONS OF R. fuscipes AT AMBIENT RESPECTIVE LOWRRCRITICAL TEMPERATURES
~-THERMAL CONDUCTANCRS TRMPRRATURRSRRLOWTHE
Ambient temperature (“C)
1133
HEAT STRESS IN RATTVSFVSCIPES
THRRMORRGULATORYRESPONSESTO
Thermal conductance (ml COs/g hr “C)*
R. fuscipes (W.R.)
R. fuscipes (J.B.)
11.6
0.083
-
13.0 17.1
0.089
0.076 -
18.5 22.5
0.104
0.082 -
23.0 27.5
0.138
0.090 0.106
* Conductances have been calculated after the manner outlined by Morrison et nI. (1959). As mean values of TB and metabolic rate have been used at each Td, standard deviations are not available.
regression coefficients for the two groups (R. fuscipes (W.R.): (J.B.): p = 0449; P> 0.05).
b = 0.100;
R.fuscipes
&eathirzg rates Breathing rates for R. fuscipes are illustrated in Fig. 3. The rates for both populations are influenced by changes in T, in a manner that approximates the variations in carbon dioxide production shown in Fig. 2. 200.
. .
.
T ;100._ E
..
. .
.*
. .
.
R . fvscipes
$ 20% =.
f ~IOO-•' 0 G R. 0
*
IO
a. ..*
. .:..., . l
. . . . . .* . .
fuscipss (JB), I IS
:T;r 1 Gc ..>’ . . ::. .
1. .:,. >.
::
: .
*
(WR 1 I
I
.
.
I 20
I
II L .
1 T,, 1 '. n ' . *. .* ' a....: ,:*., . . .. *.' *. *.* . * I 25
II 30
I 35
I 40
45
FIG. 3. Weight-relative breathing rates for rata maintained at a variety of ambient temperatures. TLC and T,, have the same meanings as in Fig. 2. The arrow projecting from each baseline represents the Td at which a pronounced increase in the log of weight-relative pulmocutaneous water loss commences.
Pulmocutaneous water losses Semi-log plots of weight-relative pulmocutaneous water loss (PWL) against TA for both populations demonstrate distinct changes in gradient (points of
1134
B. G. COLLINS
inf’lexion) in the vicinity of the thermo-neutral zones (Fig. 4). Neither population shows significant regression of log PWL on T, at temperatures below its point of inflexion. At higher ambient temperatures, however, significant regression occurs for both populations, although there is no significant difference between regression coefficients (R. jkcz$rs (W.R.): j? = 0.091; R. furciper (JR): ,!I= 0.054; P> O-05). 30.0 20.0
Rhsctbes (WI?) _
T*I
.:/’
-I
OC
FIG. 4. Weight-relative puhnocutaneous water losses (PWL) at a variety of ambient temperatures (TJ. Symbols as in Fig. 2. Letters (a) and (b) correspond to the following regression equations: R. fuscipes (W.R.) (a) log PWL = O-165 + O.OOZT,, (b) log PWL = - 2*284+0*091 TA; R. fuscz$es (J.B.) (a) log PWL = 0~160+O~O09TA, (b) log PWL = -1.171 +O.O54T,.
Both populations show relationships between log PWL per ml CO, expired and T, (Fig. 5) that resemble those illustrated in Fig. 4. Although the plots in Fig. 5 would suggest otherwise, there is no statistically significant difference between regression coefficients for TA’s above the points of inflexion (R. fuscz$es (W.R.): j? = 0.062; R. fusczpes (J.B.): p = O-042; P> 0.05). Neither population is able to achieve values of PWL which permits its members to dissipate more heat than is generated by metabolism at high ambient temperatures (equality of metabolic heat production and evaporative heat loss is represented in Fig. 5 by the horizontal dashed lines, providing the assumptions outlined by Collins (1972) are made). Regulation of body temperature The body temperatures ( TB) shown for both populations in Fig. 6 are relatively constant at Ta’s below the appropriate Tut’s, with mean values not being significantly different (R. jhctpes (W.R.): 37*5”C; R. fuscipes (J.B.): 37*4”C; P> 0.05).
THERMOREGULATORY
RESPONSES
TO
HEAT
STRESS
IN
R4TTU.S
FUSClPES
1135
FIG. 5. Pulmoeutaneous water losses per ml COs expired at a variety of ambient temperatures. Horizontal dashed lines indicate equality of metabolic heat production and evaporative heat dissipation. Other symbols as in Fig. 4. Letters (a) and (b) correspond to the following regression equations: R. fumipes (W.R.): (a) log PWL = -O*306+0.018TA, (b) log PWL = -1*388+O*062TA; R.fuscipes (J.B.) (a) log PWL = - 0.300 + 0.023 TA, (b) log PWL = - 0.085 f 0.042TA. 45 f
T “E
‘C
40. y
_
* .
.*
*. * *
I
432
.. : .
.
hm
i
.._**
*
*.
*
i .* *
* ,
T l.c
TUC
40:
3510
. . I I5
.*. . I 20
. ..a
*. I 25 7. A’
..*_ ***
I
I .
. 30 DC
FIG. 6. Relationships between ambient and body temperatures. Open circles represent body temperatures for rats experiencing lethal ambient temperatures. Other symbols as in Fig. 3.
Hyperthermia occurs at Ta’s above the Tuck, with neither population being able to achieve equality of TA and TB. Although no systematic attempt was made
1136
B. G. COLLINS
to investigate lethal temperatures for either population, Ta’s in excess of 40°C as shown in Fig. 6.
several animals died at
Structure of the skin There is no evidence of sweat glands in any of the thoracic and abdominal skin samples, although each shows the existence of sebaceous glands and a corrugated epidermis. DISCUSSION
Physiblogi~al responses to heat stress The evidence presented in Fig. 6 clearly demonstrates the ability of each R. fuscz$es population to maintain a relatively constant body temperature when exposed to ambient temperatures between approximately 10°C and its TLC. Despite the significant TB- T_k differentials that exist within this TA range, both populations are able to minimize the increases in metabolic heat production that are needed to offset heat losses to the environment (Fig. 2); This is made possible by the extremely efficient insulation exhibited by the rats. frhe mean conductance (C) indicated by the regression of metabolic rate on T, for R. fusci$es (W.R.) is only 52.2 per cent, and that for R. fuscajks (J.B.) 65.8 per cent, of values calculated on the basis of body weight (W) according to the empirical equation C = 1~02W-“*ws ml 0, (g hr “C)-l (modified after Herreid & Kessel, 1%7).] When conductances at temperatures below the TLC’s are calculated from the relationship (Morrison et al., 1959) ‘=
metabolic rate T B- T A
rather than from regression coefficients, it is seen that values for each R. fuscipes population vary directly with the ambient temperature (Table 1). This response, which is also exhibited by several other rodents reported in the literature (MacMillen & Lee, 1970; Wunder, 1970; Collins, 1972; Collins & Bradshaw, 1972), must facilitate thermoregulation when the rats are exposed to low ambient temperatures. It is suggested that increased peripheral vasoconstriction, and possibly piloerection, is mainly responsible for those reductions in conductance which occur, although hunching of the rats at low temperatures could alter the surface area exposed to the environment sufficiently to cause significant changes in conductance. The failure of both R. fuscipes populations to conform to Newton’s law of cooling (Scholander et al., 1950) is apparent, as neither shows good correlation between measured TB and the TB obtained by extrapolation of the regression line relating metabolic rate and TA to zero metabolism. Although better agreement is obtained when metabolic rates are corrected for heat losses associated with the evaporation of pulmocutaneous water, neither population exhibits the same agreement that is shown by R. lutreolus (Collins, 1972), R. vdloskim and R. rattus (Collins & Bradshaw, 1972) when similar corrections are made. It is suggested
THERMOREGULATORY
RESPONSES
TO
HEAT
STRESS
IN
RATTVS
FUSCIPES
1137
that the inferior position of R. fuxipes, particularly the Jurien Bay population, can be adequately explained in terms of its greater change in conductance at Ta’s below the TLC. Unlike R. aillosiwimus (Collins & Bradshaw, 1972) and R. Zutreolus (Collins, 1972), R. fuscipes remains normothermic at T,‘s within the thermo-neutral zone. This occurs despite the occurrence of basal metabolic rates for R. fusc;Pes which do not show the depression, when compared with values predicted on the basis of body weights (Morrison et al., 1959), that are typical of most other nocturnally active, diurnally fossorial rodents (Carpenter, 1966; McNab, 1966; MacMillen & Lee, 1970; Collins, 1972; Collins & Bradshaw, 1972). The metabolic rate for R. fuscipes (W.R.) is only 94 per cent, and that for R. fuscipes (J.B.) 103 per cent of the predicted values. It issuggested that the pronounced increase in pulmocutaneous water loss which occurs for each R. fuscipes population at Ta’s in excess of those corresponding roughly with the appropriate TLC is probably responsible for the avoidance of hyperthermia. Both populations of R. fusczipes become hyperthermic at ambient temperatures in excess of their TUC’s. The Waychinicup River population is at least as adept at limiting hyperpthermia as is the Jurien Bay population, under relatively dry laboratory conditions at Ta’s below approximately 39°C although in doing so it clearly dissipates more water and shows a greater elevation of metabolic rate (Figs. 2, 4 and 5). Nevertheless, neither population is able to dissipate sufficient body heat by evaporative cooling to avoid lethal hyperthermia at higher T,‘s. In this regard each is therefore more akin to Notomys dexis and N. cerwinus (MacMillen & Lee, 1970), small hopping mice that inhabit hot, arid regions of Central Australia, than it is to other Rattus species, most of which can evaporate sufficient water to equalize T, and TB, and limit hyperthermia, at comparable ambient temperatures. Some of the investigations reported earlier in this paper were aimed at determining what factors were responsible for the enhanced PWL associated with high Ta’s. Although neither population shows an increase in breathing rate that is comparable with those demonstrated by animals such as the marsupial Trichosurus vulpecula (Dawson, 1969), the evidence available (Fig. 3) suggests that faster breathing could contribute significantly to the enhanced PWL’s which occur at high Ta’s. It would seem unlikely, however, that the initial increases in PWL at TA’s below the appropriate TvC’ s can be explained in terms of hyper-ventilation. Rats that are subjected to high TA’s invariably show signs of moisture on their pelage. The onset of licking for each population of R. fusctpes occurs at an TA which corresponds roughly with that at which the pronounced increase in log PWL commences, and undoubtedly contributes to this moistening of the fur. Licking is so sporadic, however, even at high Ta’s, that this response cannot be advanced as the sole non-pulmonary means of dissipating water. This view is supported by the observation that parts of the pelage which are never licked become quite moist. Histological evidence indicates that it is most unlikely that sweating could contribute significantly to PWL. However, matting of the pelage beneath the chin, particularly at T,‘s above 39°C when the PWL is relatively high, suggests that
1138
B. G. COLLINS
drooling makes a significant contribution. Moisture on other parts of the pelage which are not licked must, presumably, be due to a fairly pronounced insensible cutaneous water loss. Ecological ctmshhrations The two populations of R. fuscipes considered in the present paper were chosen so as to represent the northern and southern limits of the species in south-western Australia. As such, they occupy areas which experience quite different macroclimates (Table 2) Both populations of R. fuscz$es are fossorial, and spend most of the daytime in their burrows. Although no attempt has been made to measure burrow climatic conditions, it would seem reasonable to assume that maximum burrow temperatures would be lower than those above-ground, and humidities would be higher, whatever the season might be (Carpenter, 1966; MacMillen & Lee, 1970). If this is true, then R. ficscipes (J.B.) should seldom be subjected to Ta’s in excess of about 3O”C, or R. fuscipes (W.R.) to more than approximately 24”C, at the hottest times of the year. This means that both populations should experience peak burrow temperatures which generally do not promote enhanced PWL as a means of limiting hyperthermia (Figs. 4 and 5). The high humidities which probably prevail in the burrows should therefore not significantly influence thermoregulation by the rats. It is not difficult to envisage the problems that R.@cz$es (W.R.) would face if transferred to conditions such as those experienced at Jurien Bay. In order to remain normothermic at the prevailing Ta’s, it would need to increase its PWL, a response that could be difficult under burrow conditions. Failure to increase evaporative cooling might lead to lethal hyperthermia, whilst any increase in water loss could be troublesome in a habitat which receives significantly less rainfall than occurs at Waychinicup River. Minimum T,‘s would generally occur at night when rats of either population were above ground. Enhanced metabolism resulting from exercise and the uptake of food would help to offset heat loss to the environment, although members of each population would be aided by having low conductances. It is significant that R. fuscipes (W.R.), the population that would experience the lowest minimum T,‘s, has the lowest conductance (Table 1). R. fwcz$es is particularly abundant in south-eastern and south-western Australia, yet it is noticeable that the species does not extend into areas with macro-environmental temperatures much above 32°C (Troughton, 1965; Ride, 1970; Gentilli, 1971). Although it would be foolish to suggest that inadequate physiological responses by R. fuscipes to heat stress are the sole reasons for its limited distribution, one must be impressed by the fact that both of the populations investigated so far exhibit responses which are decidedly inferior to those shown by Rattus species which successfully occupy northern, hotter parts of the Australian continent (Robinson & Morrison, 1957; Collins, 1972; Collins & Bradshaw, 1972).
0.37
19.0
Mean daily minimum temperature (“C)
Mean rainfall (in.)
32.X
Mean daily maximum temperature (“C)
O-78
13.2
Mean daily minimum temperature (“C)
Mean rainfall (in.)
26.1
Jan.
Mean daily maximum temperature (“C)
Parameter
0.37
19.3
32-l
0.78
13.7
25.2
Feb.
0.74
17.2
29.9
l-49
12-S
23.9
Mar.
* Figures have been calculated from meteorological Melbourne.
Jurien Bay
Waychinicup River
Population
3.48
12.4
23.7
3.25
8-9
18.2
May
5.80
11.2
20.6
4.35
8.4
16.4
June
4.05
9.3
19.3
4.96
7-1
15-S
July
2.42
8.5
19.7
4.80
6.6
15.6
Aug.
1.13
8.7
21.7
3.25
7-2
16.6
Sept.
0.30
13.7
27.2
1.45
10-4
21.8
Nov.
0.18
16.6
29.9
l-57
12.2
23.9
Dec.
20.70
32.78
Total
Bureau of Meteorology,
0.72
11.1
24.7
3.49
9.1
19.4
Oct.
wm3 COLLECTED*
data provided by the Commonwealth
l-14
151
27.2
2.61
11.4
20.7
Apr.
TABLE 2-M~cxo-CLIMATIC DATA FOR BOTH AReAs IN WHICH Ruttusfwcipes
1140
B. G. COLLINS
Acknowledgements-I would like to thank Dr. S. D. Brad&w for his encouragement and advice during the course of the experimental work upon which this paper is based. Particular thanks are also due to Mr. E. Cockett for able technical assistance. Mr. J. Bannister, of the Western Australian Museum, has kindly furnished me with information on the known distribution of R. fuscipes within Western Australia. REFERENCES CARPENTERR. E. (1966) A comparison of thermoregulation and water metabolism in the kangaroo rats Dipodomys agilis and Dipodomys merriami. Univ. C&if. pubi. 2001. 78, l-36. COLLINS B. G. (1972) Physiological responses to temperature stress by an Australian murid, Rattus lutreolus. J. Mammal. (In press.) COLLINS B. G. & BRADSXAWS. D. (1972) Studies on the metabolism, thermoregulation and evaporative water losses of two species of Australian rats, Rattus tiUosi.~timusand Rattus rattus. Physiol. Zoiil. (In press.) DAWSONT. J. (1969) Temperature regulation and evaporative water loss in the brush-tailed possum Trichosurus vulpecuha. Comp. Biochem. Physiol. 28, 401-407. GENTILLI J. (1971) Climates of Australia and New Zealand. In World Survey of Climatology, Vol. 13. Elsevier, New York. HERREID C. F. & KEPSHLB. (1967) Thermal conductance in birds and mammals, Comp. Biochem. Physiol. 21, 405414. MACMILLBN R. E. & Lxx A. K. (1970) Energy metabolism and p&no-cutaneous water loss of Australian hopping mice. Comp. Biochem. Physiol. 35, 355-369. MCNAB B. K. (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47, 712-733. MORRISONP. R., RYSER F. A. & DARE A. R. (1959) Studies on the physiology of the masked shrew (Sorex cinereus). Physiol. Z&l. 32, 256-271. RIDE W. D. L. (1970) A Guide to Natiue Mammals of Australia. Oxford University Press, Melbourne. ROBINSONK. W. & MORRISONP. R. (1957) The reactions to hot atmospheres of various species of Australian marsupials and placental animals. J. cell. camp. Physiol. 49,455478. SCHOLAND~~ P. F., HOCK R., WATERSV., JOHNSONF. & IRVINGL. (1950) Heat regulation in some arctic and tropical mammals and birds. Biol. Bull. 99, 237-258. SIMPSONG. G., L~WONTINR. C. & ROE A. (1960) Q uantitatiue Zoology. Harcourt, Brace & World, New York. TROUGHTONE. (1965) Furred Animals of Australia. Angus & Robertson, Sydney. WIJNDER B. A. (1970) Temperature regulation and the effects of water restriction on Merriam’s chipmunk, Eutamias merriami. Comp. B&hem. Physiol. 33, 385403. Key Word regulation.
In&x-Thermoregulation;
heat
stress;
Rattus
fuscipes;
temperature