Camp. Biochem. Physiol. Vol. I IOA. No. I. pp. 65-69, 1995 Copyright I@’ 1995 Elsevier Science Ltd Pergamon

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The thermal biology of the white-tailed rat Mystromys albicaudatus, a cricetine relic in southern temperate African grassland

Colleen T. Downs and M. R. Perrin

Department of Zoology & Entomology, University of Natal, Pietermaritzburg, Private Bag X01, Scottsville, 3209, South Africa

This study examines the hypothesis that Mystromys albicaudatus, a cricetine relic in southern Africa, has thermal characteristics typical of a rodent adapted to a cold temperature regime. Metabolic rate (oxygen consumption) of M. afbicaudatus was measured using open-flow respirometry at ambient temperatures ranging from S’C to 3S’C. Lowest specific oxygen consumption was 1.352 f 0.089 ml 0, g-‘hr-’ (n = 8; body mass = 93.78 + 6.27 g) at 25’C, equivalent to 121.8% of the predicted value of Kleiber (1975), 128.8% of the value predicted for eutherians and 113.7% of the value predicted for cricetidae (Hayssen and Lacy, 1985).

Key words: Mystromys; Thermal biology; Metabolic rate.

Comp. Biochem. Physiol. IlOA, 65-69, 1995.

Introduction

The white-tailed rat Mystromys albicaudatus is the only cricetine rodent in Africa (Meester et al., 1986) and is endemic to southern African (De Graaff, 1981) south of latitude 25” (Dean, 1978). It is confined to highveld and montane grassland where it occurs in pure grassveld types as well as in bankenveld, southern tall grassveld and Natal sour sandveld grass types (Acocks, 1953). Mystromys albicaudatus is nocturnal and occupies burrows (De Graaff, 1981) but its habits are poorly known. In the laboratory, it eats a wide variety of plant foods, but has a preference for insects and seeds (Perrin and Maddock, 1983).

Present-day populations of M. albicaudatus are fragmented, and they are in need of stricter conservation (Dean, 1978). The main distribu- tional area is within the temperature grassland area, but there is a relict population in the ______ Correspondence to: C. T. Downs, Dept. of Zoology &

Entomology, University of Natal, Pietermaritzburg, Private Bag X01. Scottsville, 3209, South Africa. Fax 0331-2605105; e-mail: Downs@,gate2.cc.unp.ac.za

Received 25 November 1993; revised 22 July 1994; accepted 2 August 1994.

southwestern Cape. Brain (1985) has speculated that the relict population was linked to the main population during past times of cold-induced grassland expansion and that it is isolated today because of the current warm interglacial period. Mystromys albicaudatus, which is k selected (Dean, 1978), may have survived the coloniz- ation of Africa by the r selected murids (Perrin, 1980) owing to its complex gastric anatomy and symbiotic microflora (Maddock and Perrin, 1981, 1983; Perrin and Maddock, 1983) and/or because of its ability to persist in cold temperate grasslands in southern Africa.

We postulated that M. albicaudatus exhibits thermal characteristics typical of a rodent adapted to cold temperature regimes. These include a higher than expected basal metabolic rate (BMR), and a broad thermoneutral zone (TNZ) at lower temperatures compared with desert-adapted rodents (Downs and Perrin, 1990). Consequently, the main aims of this study were: (1) to determine changes in meta- bolic rate in relation to ambient temperature (T,); and (2) to quantify the degree of tempera- ture regulation above and below the TNZ.

65

66 C. T. Downs and M. R. Perrin

together with conductance, evaporative water loss and heat production, of M. albicaudatus.

Materials and Methods

Animals were housed individually in standard laboratory rodent cages in a constant environ- ment (CE) room at 25°C with a 12 L: 12 D photoperiod. Each was supplied with rat cubes, supplemented with mixed seeds and carrots, with water available ad libitum.

Evaporative water loss (EWL), thermal con- ductance, body temperature (Tb) and oxygen consumption ( 1’02) of adult M. albicaudatus were measured between T, = 5 and 35°C during the day when the nocturnally active M. albicau- datus were inactive. Measurements were made on post-absorptive animals after they had been equilibriated to the experimental T, (&- 2°C) for 3 hr. During this period, each animal was placed in a 5 1 plastic container covered with a wire mesh grid. An artificial burrow (370 ml) was available in each container. At T, = 5°C the equilibration period was reduced to 1 hr. Each subject was then placed in a glass, cylindrical metabolism chamber (1730 ml) for 45 min. A flow-through respirometry system was used to record oxygen consumption and evaporative water loss simultaneously at each experimental temperature. Room air was dried over silica-gel before entering the chamber and again before entering the oxygen analyser (Amtek S-3A/l, Applied Electrochemistry, Pittsburgh). Flow rates were controlled and measured using a mercury flowmeter (Tube RSI, Float Hi-Den Air, Glass Precision Engineering) at 15.0-15.5 mmHg, then converted to ml min-’ air 760 mmHg. Carbon dioxide was removed from the excurrent air before entering the O2 analyser over a column of soda lime. A data logger (chart recorder, Model RYT) running at 2 mm min-’ recorded 1/O> continuously.

Mean percent oxygen concentration recorded regularly for 5 min intervals during a 30 min period was calculated as efflux. Recordings were ignored if animals were active. Influx and efflux rates were corrected to STP, for flow rate, and used to calculate VO, using the equations of Depocas and Hart (1957) and Hill (1972). Values were converted to specific 1/02 (ml O2 g-’ hr-‘).

A gravimetric method was used to determine EWL where the increase in mass (measured to 0.1 mg) of the silica-gel drying column used to dry excurrent air, was used to calculate re- sidual water content of incurrent air during calibration, and evaporative water loss of each rat while in the chamber. Values were con- verted to specific evaporative water loss (mg

H,O gg’ hr-I). Measurements were discarded if the animals urinated in the respirometer chamber.

A copper-constan thermocouple connected to a digital display thermometer (51 K/J Fluke, John Fluke MFG. Co., Everett, Washington) measured the temperature of the respirometer chamber and rectal T,, of the rats. The probe was inserted 20-25 mm into the rectum of each subject after they had been removed from the metabolism chamber. Handling was kept to a minimum.

Dry thermal conductance (C,) was calculated according to the equation of Dawson and Schmidt-Nielsen (1966). Minimal thermal con- ductance (C,,“), including EWL, was calculated using the formula of Scholander et al. (1950).

3- (6)

(4) (6)

2-

(3) (4) z 1

I- (4) $ - *

I (7)

5 10 15 20 25 30 35

Ambient temperature (“C)

Fig. I. Change in specific oxygen consumption, body temperature and evaporative water loss with change in ambient temperature of M. ulbicaudutus (mean + SE, n in

parentheses).

Thermal biology of Myslromys albicuudutus 61

Results

The change in specific VO, with change in T, for M. albicaudatus is illustrated in Fig. 1. Lowest specific VO, was 1.352 + 0.089 ml O2 g-’ hr’ (n = 8, body mass = 93.78 +_ 6.27 g) (all values mean f SE) at 25°C equivalent to 121.8% using the Kleiber equation (1975), 128.81% of the value predicted for eutherians and 113.72% of the value predicted for species of the family cricetidae (Hayssen and Lacy, 1985). Experimental values were significantly different from values predicted by Kleiber and for eutherians (t = 2.68; d.f. = 14; P < 0.05; t = 3.26; d.f. = 14; P < 0.05) but not signifi- cantly different to predicted values for cricetids (t = 1.83; d.f. = 14; P > 0.05). The regression equation for change of VO, with T,, below 25°C is as follows:

VO, = 4.4779 - O.l147T,

(I’ = 0.53, D.F. = 36).

This yields an x-axis intercept value of 39.03”C and a y-axis intercept of 3.31. The exact limits of the TNZ were not determined; however, values of VO, at 25°C and 30°C were not significantly different (P > O.OS), suggesting a broad TNZ in this range.

Body temperatures ranged from a mean mini- mum of 32.83 + 0.77”C at 5°C (n = 8) to a mean maximum of 38.34 & 0.23 at 35°C (n = 7) (Fig. 1). Mean Tb values showed little variation between Ta = 5 and 25°C and were not signifi- cantly different (P > 0.05), but increased above T, = 25°C. At T, = 35°C blood-vessels in the ears and toes were prominently dilated.

There was a regular increase in EWL from Ta = 5 to 30°C with a steep increase at 35°C where values were significantly greater (P < 0.05) (Fig. 1). Values of 2.34 J mg-’ Hz0 and 20.1 J ml-’ 0, were used to convert EWL and VO, to thermal units. Maximal heat loss through evaporative cooling was 31.5% at T, = 35°C.

Dry thermal conductance values rose sharply above T, = 30°C and were significantly different (P < 0.05) from values at lower T,s where the rate was low and values obtained not signifi- cantly different (P > 0.05) from one another (Fig. 2). C,i, values (Fig. 2) showed similar trends, increasing above Ta = 30°C with no significant difference among values (P > 0.05) at lower Tas.

Discussion

The change in EWL with increasing Ta was minimal in M. albicaudatus but increased rapidly above T, = 35°C. At high T.,s, EWL

4

(7)

(7) s

T

(8)

E

(8)

f

T

(3)

i

(5)

(6)

i

(4)

i

(4)

rf (6)

I

0 0 5 10 15 M 25 30 35

Ambient tempera,ure ("C)

Fig. 2. Dry thermal conductance and C,,,,, values of M. albicaudutus in relation to 7” (mean f SE, n in

parentheses).

effected cooling and off-loaded 31.5% of the heat load. However, this was insufficient to prevent a steep rise in T,,. This indicated that M. albicaudatus was unable to regulate Tb at high Tds, suggesting that it is a cold-adapted species. Mystromys albicaudatus shows the typical en- dothermic response of increasing oxygen con- sumption linearly above 30°C and below 25’C. There was some variation in Tb but such ranges in T,, (from 32.83”C to 38.34C) are common in rodents that show a controlled daily circadian rhythm in Tb (Lovegrove et al., 1991). However, below Ta = 15°C Tb was constant. Insulation was maximal here, and heat generated from increased metabolic rate at these low Tds was necessary to prevent further decrease in T,. None of the experimental animals became tor- pid at low temperatures. Further experiments are required using minimitters to prevent errors caused by handling the subjects.

Thermal conductance is a measure of the ease with which heat leaves or enters a body (Scholander et al., 1950). Below 25”C, dry ther- mal conductance values were low and stable, reducing heat loss and conserving energy, which is typical of rodents, whether cold- or hot adapted. At low T,s, heat production was the most significant factor affecting thermoregu- lation. Increased thermal conductance above

68 C. T. Downs and M. R. Perrin

30°C facilitated heat loss, preventing hyper- thermia.

Mystromys albicaudatus is the single represen- tative of the subfamily Cricetinae in the southern African subregion. Its northern tem- perate relatives (including the voles and hamsters) are generally considered to be “cold- adapted”. A relatively low and broad TNZ suggests that M. albicaudatus has maintained thermal characteristics typical of cold-adapted rodents and that there has been no adaptive shift in TNZ with increased temperature regimes in Africa. The lower critical tempera- tures of Microtus pennsyhanicus (Kurta and Ferkin, 1991) M. breweri (Kurta and Ferkin, 1991) and M. montanus (Tomasi. 1985) are 3-4°C higher than that of M. albicaudatus, but are broad. Avoidance of T,s above the TNZ is essential to prevent increased EWL and hyper- thermia. so M. albicaudatus remains inactive diurnally in the thermally buffered micro- environment of a burrow. The thermal charac- teristics of M. albicaudatus reduce energetic costs when they are active nocturnally.

The minimum oxygen consumption at 25°C for M. albicaudatus is a relatively low limit of thermoneutrality compared with several southern African rodents occurring in mesic grassland habitats (Haim and Fourie, 1980). Other southern African rodents with similar low TNZ ranges are Tatera afra (Duxbury and Perrin, 1992) and Otomys irroratus (Haim and Fairall, 1987). The latter is said to have a thermal biology suited to its preferred wetland habitat (Haim and Fairall, 1987). Winter accli- mated Saccostomus campestris, one of two species of Cricetomyinae rodents found in the southern African subregion, has a TNZ between 28 and 30°C (Haim et al., 1991).

Mass specific determined BMR values were generally higher than predicted values using Kleiber’s equation (1975) or that of Hayssen and Lacy (1985). Similarly, M. montanus (Tomasi, 1985) and M. pennq~loanicus (Kurta and Furkin, 1991) had higher than predicted metabolic rates, while M. brenleri had a meta- bolic rate close to that predicted by Kleiber (Kurta and Ferkin, 199 1). The slope of the curve below the TNZ of the latter two species was similar to that of M. albicaudatus. Generally. Microtus (Packard, 1968: Wunder. 1985; Tomasi, 1985) and Clethrionomys (Grodzinski. 1985) species have higher than predicted meta- bolic rates. Vogel (1980) theorized that in- creased BMR values are an adaptation to living in cold climates and that such animals are poor thermoregulators. This suggests that BMR val- ues in M. albicaudatus are primitive as they are elevated above values expected for body size. However, there is a trend towards BMR values

approaching expected BMR values which may represent adaptation to the warmer thermal environment climate that they inhabit. A coun- ter explanation is that M. albicaudatus, because of its higher mass-independent metabolic rates and its ability to thermoregulate efficiently, is a “power” strategist (Gnaiger, 1987) with high rates of energy intake, and consequently comparatively higher BMR, than “frugal” strategists (Szarski, 1983; Koteja, 1987). Many species with lower than expected BMR values are xeric inhabitants (Downs and Perrin, 1990) and so are obligate “frugal” strategists.

Some other southern African “cold adapted” rodents, including Saccostomus campestris (Ellison and Skinner, 1992) increase metab- olism at low Tas with some individuals having spontaneous bouts of torpor. Ellison and Skinner (1992) found that S. campestris only enter torpor when acclimated to T,s lower than those experienced in their burrows. Therefore, they proposed that torpor was a rare occur- rence. The capacity for torpor in M. albicauda- tus needs to be investigated. However, reduction or avoidance of cold exposure by decreasing the duration of individual activity bouts, and max- imizing the use of thermally buffered burrows probably reduce the necessity for torpor.

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