The circadian rhythm of body temperature of four marsupials

J

Pergamon PII: S0306-4565(!37)000260

therm. Biol. Vol. 22, No. 415, pp. 301-307, 1997 10 1997 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0306-4565/97 $17.00 + 0.00

THE CIRCADIAN RHYTHM OF BODY TEMPERATURE OF FOUR MARSUPIALS ROBERT T. GEMMELL,’

SCOTT J. TURNER’

and WILLIAM

J. KRAUSE2

‘Department of Anatomical Sciences, The University of Queensland, Brisbane, Queensland, 4072, Australia and zDepartment of Pathology and Anatomical Sciences, The University of Missouri, Columbia, MO 65212, U.S.A. (Received I I September

1996; accepted in revised form 1 I June 1997)

Abstract-The 24-h pattern of body temperature of the brushtail possum Trichosurus vulpeculu, the northern brown bandicoot Isoodon macrourus, the South American opossum Didelphis marsupialis and the Virginian opossum Dideiphis virginiana was determined with temperature transmitters (Titley Electronics, Balhna, NSW). Although all four species exhibited a circadian rhythm with a peak at midnight and a nadir at noon, the profile of D. virginiana was not as defined as those of the other three species, with one D. virginiana not showing a definitive 24-h rhythm. The mean body temperatures of the possum, bandicoot, and the two opossums were 37.4, 36.2, 35.5

and 35.4”C, respectively. The mean 24-h body temperatures had a range of 35.0 to 39.O’C in eutherian species. This range was 35.4 to 37.4”C in the four marsupial species. 0 1997 Elsevier Science Ltd. All rights reserved.

INTRODUCTION

virginiana

(Treagust

bandicoot

Isoodon

et

al.,

1979) but not the and the opossum Didelphis marsupialis. There are difficulties in comparing body temperatures obtained from various marsupial species by different research workers. Variation can occur due to differences in the methodology of maintaining the animals and in the equipment for measuring temperatures. The present study allows direct comparison between marsupials from three families, a Phalangerid, Peramelid and two Didelphids. The 24-h profile for body temperature was obtained for the brushtail possum T. vulpecula, the northern brown bandicoot Zsoodon macrourus, the South American D. marsupialis and the Virginian opossum D .virginiana. The form of the temperature profile of the four marsupial species was compared as was the mean body temperature over 24 h to ascertain if differences occur between marsupial species.

Rectal thermocouples have been used to obtain body temperature measurements from restrained animals usually during the daylight hours. These single values represented the mean of a period of rest or were simply a stable or plateau value obtained during the day or night. With the advent of small temperature transmitters which can be placed in the body cavity of an animal, continuous monitoring of the body temperature of free-ranging animals can be achieved. The results of studies using these transmitters have shown that the body temperature of many mammals varies throughout the day and night. Earlier reports of body temperature obtained by rectal probes demonstrated that marsupials had mean body temperatures 2 to 3°C lower than generally found in eutherians (Dawson and Hulbert, 1970). Evidence that marsupials have thermoregulatory abilities that are equal to or superior to eutherians is now available (McCarron and Dawson, 1989). However, the view that marsupials have a lower body temperature than eutherians has persisted (Tyndale-Biscoe, 1973; McCarron and Dawson, 1989). Temperature transmitters have been used to obtain the 24 h body temperature profile in several species including the possum Trichosurus vulpecula (Halse and Rose, 1988) and the opossum Didelphis

macrourus

MATERIAL

AND METHODS

The six female and two male brushtail possums, used in this study were from the captive breeding colony, housed at the Native Animal Facility, Pinjarra Hills, Brisbane, Australia. They were adult animals, the females weighing about 1800 g and the males 2000 g. The possums were T. vulpeculu,

301

R. T. Gemmell c’i ~1.

302 housed

in

fully

enclosed

yards

each

measuring

11 C. Lights were on at 7.00 am and off at 5.00 pm.

2 x IO m. The yards were open to the environment

Each pen contained

and the possums were fed ad libitum on fruit and vegetables (Gemmell ef u/.. 1987; Gemmell, 1995).

animals were fed ad libitum on dog food (Lab-canine

Body

temperatures

were

year, the range of ambient 35 C. The possums

obtained temperature

remained

during the day and foraged enclosure

during

throughout

the

was from 5 to

in their nesting

boxes

in the open section of the

the night.

Day length

was IO h in

the winter and I4 h in the summer. The

two

male

and

one

female

bandicoots.

Facility, (Gemmell.

1982). They

were

The five male Virginian were trapped

adult

animals.

the

Green

Research weighed

and

were

open

contained were

fed

ad

Running

temperatures

Ration,

were

was

Provincial

Traders

Body temperatures the range

made

fed on dog

available food

20 C. The bandicoots

the Dog

Pty. Ltd.. Queensland).

were obtained

of ambient

and

(Drimeat

during the winter.

temperature remained

was from

5 to

in their nests during

the day and foraged in the enclosure

during the night.

Day length

and I4 h in the

was IO h in the winter

summer. The five South

American

opossums,

LI. MUTSU-

Department

pens measuring

to

the

of

of Columbia.

2500 g. The opossums

libitum

were

I x 3 x 3 m

environment.

on

were

dog

obtained

of ambient

The transmitters were supplied Australia.

Each

food

pen

(Lab-canine

during

temperature

and receivers

the

of receivers

Regal 2000. The transmitters

Ballina, model

used,

melting

point

wax

transmitters

and

with batteries, weighed

were

NSW.

GPI

Regal

I .5 x I .O x 0.5 cm. were coated

5 g. The

5 to

used in this study

were

were

autumn,

was from

by Titley Electronics,

The transmitters

types

mately

pialis, were part of a colony imported from southern Central America 3 years ago. The female opossum

(Missouri

Lab Chow, Purina Mills, Richmond, All had free access to water. Body

the range 30’ c.

two

Missouri

at the Charles

a small box filled with straw. The animals

Diet-5006, Indiana).

water

D. @$ttiu~.

12 miles south

about

Richmond.

of Columbia,

enclosures

Area

located

housed in fully enclosed

female weighing 1200 g and the males 2000 g. The bandicoots were housed in a 3 x 6 m outside yard. bandicoots

opossums.

in the environs

and then held in outside

They

colony, housed at the Native Animal Pinjarra Hills. Brisbane. Australia

breeding

Diet-5006, Lab Chow, Purina Mills. Indiana). All had free access to water.

Conservation)

I. IIIUUOUI’IIJ,used in this study were from the captive

a small box filled with straw. The

and

IO and approxi-

with a high

approximately

calibrated

in a water

weighed 2000 g and the four males about 2500 g. The

bath prior to be being placed in the marsupials. They were inserted into the abdominal cavity of

opossums

the anaesthetised

were held indoors

at room temperature

of

marsupial

via a midline

38 I. macrourus

i

34L 12

24

12

24

12

24

12

24

12

24

12

24

12

Hours Fig. 1. The body temperature of an adult with the peak temperatures at night and 7 days was 36.0-C with a range of 34.5 to The bar along the

bandicoot over 7 days. A definite circadian rhythm was present the troughs at mid-day. The mean body temperature over the 37.2’C. The environmental temperature varied from 12 to 22°C. X-axis indicated the period of darkness.

incision

Marsupial

body

303

temperature

40 T. vulpe~~ula 39

36

36

2 0

12

24

I

1

12

24

Hours Fig. 2. The profile of mean body temperature for a possum over 24 h. The mean and standard deviation was calculated from 6 days of temperature recording. The mean body temperature was 37.3”C with a range of 36.2 to 38.8”C. The 24-h profile was drawn twice to display the temperature during the night. The environmental temperature varied from 10 to 21°C. The bar along the X-axis indicated the period of darkness.

in the abdomen.

The marsupials

with a Halothaneoxygen

were anaesthetised

gas mixture.

The marsu-

a series of beeps. These beeps were recorded every hour. With the use of the calibration beeps could be converted

pials were returned to their respective enclosure. Each transmitter transmitted at a set frequency in the

ings were initiated

150 mHz band, the temperature

of the transmitter.

being translated

into

36r

0

into temperature.

for 3 min curve the Record-

about one week after the insertion

I. macrourus

12

24

12

24

Hours Fig. 3. The profile of mean body temperature for a bandicoot over 24 h. The mean and standard deviation was calculated from 7 days of temperature recording. The mean body temperature was 36.4”C with a range of 34.2 to 38.6”C. The 24-h profile was drawn twice to display the temperature during the night. The environmental temperature varied from 12 to 22°C. The bar along the X-axis indicated the period of darkness.

304

R. T. Gemmell

er nl.

D. marsupialis 36

37

34

33 0

24

12

24

12

Hours Fig. 4. The profile of mean body temperature for a South American opossum over 24 h. The mean and standard deviation was calculated from 7 days of temperature recording. The mean body temperature was 36.0’ C with a range of 35.0 to 37. I C. The 24-h profile was drawn twice to display the temperature during the night. The environmental temperature was maintained at 21 C. The bar along the X-axis indicated the period of darkness.

Results mean

and

were

obtained

standard

for

deviation

at least

six days.

was calculated

of the 24 h. The 24-h profile was presented the temperature

during

the night.

RESULTS

The

for each

to display

The

displayed

body

temperature

a similar circadian

body temperature

occurring

of

all

eight

rhythm,

during the night and the

D. virginiana

36

e!

=I tii t P E F

35

34

32

S 0

12

24

12

possums

with the peak

24

Hours Fig. 5. The profile of mean body temperature for a Virginian opossum over 24 h. The mean and standard deviation was calculated from 7 days of temperature recording. The mean, body temperature was 35.l”C with a range of 33.8 to 36.3”C. The 24-h profile was drawn twice to display the temperature during the night. The environmental temperature varied from 6 to 21°C. The bar along the X-axis indicated the period of darkness.

Marsupial body temperature nadir during the day. The rhythm of all eight possums was very definite and did not change dramatically over the days of recording. Similarly, the body temperature of the three bandicoots also showed a very definite rhythm with the highest temperatures during the night (Fig. 1). The 24 h body temperature of the five D. marsupialis showed a definite rhythm. The 24 h body temperature of the five Virginian opossums did not show a definite pattern as observed with the possums and bandicoots. Virginian opossums 1, 2, 3 and 4 showed some pattern with the higher temperatures during the night. However, Virginian opossum 5 did not show any definite pattern of body temperature. Falls in body temperature to around 30°C were observed in Virginian opossums 1, 2 and 5. These falls were noticed about 2.00 pm. In the other two Virginian opossums the lowest body temperatures were between 32 and 33°C. This variation in the consistency of the 24 h body temperature profile is displayed in the figures of the mean body temperature data (Figs 2 - 5). The standard deviations in the possum (Fig. 2), bandicoot (Fig. 3) and the South American opossum (Fig. 4) data are far smaller than that for the Virginian opossum (Fig. 5). In the eight possums, three bandicoots and five South American opossums the rise in body temperature in the evening was achieved in about 5 h and the decline took place over about 10 h (Figs 2 - 4). The rise in body temperature occurred over 5 h in Virginian opossum 3 and in Virginian opossums 1,2 and 4 there was no difference in the rate of increase or decrease (Fig. 5). The mean body temperatures of the possum, bandicoot, South American opossum and Virginian opossum was 37.4”C, 36.2”C, 35.5”C and 35.4”C, respectively. Although the mean body temperature of the possum varied from 36.4 to 384°C the mean value of 37.4”C is greater than that for the bandicoot, which in turn is greater than that of the two opossum species (Table 1). Body temperatures were obtained for possums throughout the year. However no correlation was observed between the ambient temperature and the mean body temperature of the possum. DISCUSSION

The resting body temperature for the brushtail possum was previously reported as 36.2 f 0.5 with a range of 35.4 to 368°C (Dawson and Hulbert, 1970). The temperatures were measured with copperconstantan thermocouples inserted into the rectums of the possums, the animals being housed in restraining cages. Measurements were made during the day. In the present study, the 24 h body temperature profile obtained with transmitters

305

Table 1. The mean 24-h body temperatures of the brushtail possum, Trichosurus vulpecula, the bandicoot, Isoodon macrourus and the opossum, Didelphis virginiana

Mean body temperature f”ct

Range (“C)

I

36.4

35.6 to 37.6

2 3 4 5 6 7 8

36.9 37.0 37.3 37.3 37.8 38.0 38.4

35.0 36.0 35.9 36.2 36.7 37.7 37.9

I

36.0

34.5 to 37.2

2 3

36.3 36.4

34.5 to 38.1 34.2 to 38.6

2 3

35.8 35.0 35.5

33.2 to 38.4 31.5 to 38.8 32.4 to 38.1

4 5

36.0 35.2

33.4 to 39.1 32.8 to 38.1

2

35.1 35.3

29.9 to 37.9 31.5 to 38.1

3 4 5

35.3 35.7 35.8

32.5 to 37.5 33.7 to 37.6 30.4 to 38.6

Marsupial Possum

to to to to to to to

39.5 38.4 38.8 38.8 39.3 38.5 39.2

Bandicoot

South American

opossum

I

Virginian opossum

I

that the body temperature is at its lowest during the day. The range of body temperatures for the eight possums of this study was from 35.0 to 39.6”C. The lower value for the range was from 35.0 to 37.9”C and the mean low body temperature was 36.4”C (SD + 1.0, N = 8). Thus the value obtained by Dawson and Hulbert (1970) of 36.2”C was similar to the mean low body temperature obtained with transmitters possums during the day. Halse and Rose (1988) reported a clear diurnal rhythm in body temperature in the brushtail possum using transmitters inserted into the abdominal cavity. The temperature of one possum reached 38.3”C and that of another fell to 34.3”C. Maximum temperatures occurred during the active periods of the night and the minimum temperature, termed T basal by the authors occurred, during the day. They reported a T basal of 35.4 f O.“C for mainland possums and 34.7 + 0.6”C for Tasmanian possums. It could not be determined whether the significant difference recorded between Tasmanian and mainland possums was due to sub-specific differences, simple environmental adaptation or random variation. Unfortunately this study did not provide the mean body temperature of the possum over 24 h and the value obtained for T basal or the mean low body

demonstrated

R. T. Gemmell

306

35.4 and 34.7’C which were lower than 364”C, the value obtained in the present study. temperature

was

Although

the pattern

of the Halse and Rose (1988) paper that obtained

in Fig. 1

of body temperature

was similar

to

in this study there was a drift in the

basal levels which were not present

in the recordings

from this study (Fig. 1). Temperature transmitters allow measurements to be made in unrestrained animals still

throughout

difficult

the day and night. however

to compare

normally

temperature

been shown

In laboratory

when it is

macropods

to allow their body temperature

at high environmental

temperatures

have to rise

(McCarron

and

for the bandicoot.

I. macrourus was reported by Dawson and Hulbert (1970) as 34.7 _+ 0.9 and a range of 33.7 to 35.8-C. with

the temperatures

copper-constantan

Common

were measured

thermocouples Table

animals

the

measurements

being

housed being

in

made

during the day. The range of body temperatures for the three bandicoots of this study was from 34.2 to 38.6”C. The lower value for the range was from 34.2 temperature

to 34.5”C and the mean low body was 34.3”C (SD + 1.5, N = 3). Thus

the value obtained was

similar

The

to

by Dawson

the

mean

with transmitters mean

Virginian

minimum

opossum

and Hulbert

low

body

from bandicoots body

temperature

has been reported

be 34.4’ C and the mean maximum

(1970)

temperature during of the

previously

to

body temperature

was 36. I C when held at 2 I ‘C (Treagust

et ai., 1979).

The

transmitters

measurements

implanted

in

were

the

made

peritoneal

with cavity.

The

mean

minimum

Dawson. 1989). The resting body temperature

As with the possum.

the

cages,

during the day

such as reproductive

studies,

rectum,

obtained

cycles (Peters and Rose, 1979) can also influence body temperature.

into

the day.

to increase

low and other factors

the

restraining

temperature

24 h body

profiles. As shown in Fig. I movement can cause body

it is

cr crl

inserted

body temperature was 30.6 + 0.8 C and maximum body temperature was mean

the 38.2 _+ 0.4”C in this study. Although the minimum and maximum values differ, the mean body temperature of 35.2 k 0.4 ‘C was similar 35.4 k O.&C obtained in this study.

2. The mean 24-h body temperature

of some mammals

Mean body temperature

name

MotlorrenW., Platypus. Ovnirhor/2~~nc,12u.s mutimrs Echidna. Trrc/t~$~.~.s rrcukntus (2)

(I )

32.

( C)

I (range 29.2-34.6) 32.0

Marsupial

Sugar glider, Peruuru.s hrwiceps (3) Opossum. Didelphis r*irginiana (4) Didelphis

virginiana

Didelphis

nmrsupialis

(5) (6)

Tasmanian devil. Sarcophi/w harrisii Bandicoot. Isoodon rmuwuru.~ (8) Antechinus. Antechinus stuarrii (9) Possum. Tric~hosurus wlpecula ( IO) Trichosurus wlprcula (I I ) Bettong. Bet/ongia gaimurdi ( 12)

(7)

34.9 (range 35.1 (range 35.4 (range 35.5 (range

33.3-36.5) 33.8-36.3)

35.3 (range

32.0-38.0)

36.2 (range

36.0-36.4)

35.1-35.8) 35.0-36.0)

36.5 36.1 37.4 (range

36.4-38.4)

37.4 (range

36.6-38.3)

Eutheriutl

Hedgehog. Erinrrceus europuvus ( I3 Human (14) Hamster. Criwfux cr/c’c’ms ( 15) Beaver. CU,S/W canadrnsis (I 6) Tree shrew. Tupaia hrlangrri (I 7) Monkey (I 8) Rat (19) Rabbit (20) Sheep (21)

I

36.0 (range

35-37.0)

36.5-37.4 36.6-37.1 36.6-37.5 37.0 (range

35-41.0) 37.2 (range 36.3-37.3) 37.0-37.8 38.7-39.2 38.8-39.3

(I) Grigg et rrl. (1992b). (2) Grigg rr rrl. (1992a). (3) Dawson and May (1984). (4) Treagust et (I[. (1979). (5) Gemmell at cd..this paper, (6) this paper. (7) Guiler and Heddle (1974). (8) Gemmell CI crl.. this paper, (9) Kortner and Geiser (1995). (IO) Halse and Rose ( 1988). ( I I) Gemmell and Cepon (I 993). (I 2) Rose PI al. ( 1990). ( 13) Fowler (l988), (14) Refinetti and Menaker (1992a). (15) Retinetti ( 1994). (16) Dyck and MacArthur (1992). (17) Refinetti and Menaker (1992b). (18) Honnebier LJ/ al. (1992). (19) Gordon (1994). (20) Varosi (J/ trl. (1990). (21) Mohr and Krzyywanek (1995).

to that of

Marsupial body temperature Whereas

the 24-h profile of body temperature

for

the possum, bandicoot and South American opossum were relatively constant from day to day, that of the Virginian opossum standard deviations

varied as illustrated by the large around the mean values or was

not even present in the case of one of the five animals. As well in both

opossums,

the body

temperature

could fall precipitously by several degrees. thus the range of body temperature was greater in the opossum er

al.

than in the possum (1979)

opossums

reported

exhibited

ever McManus

or bandicoot.

that

all

prominent

Treagust

four

Virginian

daily rhythms.

How-

(1969) stated that there were no daily

fluctuations in body temperature in the animal. He obtained a mean body temperature of 357°C with a range of 33.8 to 36.3”C for the Virginian is possible

that the opossum

a control

of body

opossum.

It

does not have as precise

temperature

as the possum

and

bandicoot. The use of the same temperature recording equipment to obtain body temperatures from the four marsupial

species

comparison. temperature is higher Similar mammals

in the present

The

possum

study

has

a

than that of the bandicoot than

variation

that

of the

two

allows

higher

which in turn

opossum

has been obtained

for body

species.

with eutherian

(Table 2).

Acknowledgements~The authors thank Alan his technical expertise and assistance.

Blowers

for

REFERENCES

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