Metabolic rate and thermal conductance in a mycophagous marsupial, Bettongia gaimardi

Randy Rose
Zoology Department, University of Tasmania
GPO Box 252C Hobart, Tasmania, AUSTRALIA 7005
Correspondence should be addressed to: Randy Rose, PhD.

Submitted for publication: March 7, 1997


Keywords: Metabolic rate, thermal conductance, mycophagous, marsupial, Bettongia gaimardi.


Title Page Abstract Introduction Materials and Methods Results
Discussion Conclusions Acknowledgements References Table of Contents
Figure 1 Figure 2 Figure 3


ABSTRACT

    Tasmanian mammals live in the coolest part of Australia; as such they tend to have denser fur, lower conductance and higher body temperatures. The Tasmanian Bettong Bettongia gaimardi is a highly mycophagous species eating underground (hypogean) fungi. Although fungi are not usually regarded as nutritious food, recent evidence suggests that bettongs survive well on this diet. Correspondingly, they have a high basal metabolic rate of 0.46 ml O2 g-1 hr-1 that is above that predicted for marsupials and many eutherians of this size. The metabolic rate of cold-adapted bettongs was not significantly different from normal animals. Conductance was found to be low at 0.55 J. g. hr-1.oC-1 but became significantly greater at 30-35oC. The thermoneutral zone was also surprisingly low being between 10 - 20o C. Coupled with a high fecundity and growth rate, this species is well adapted to its fungivorous life-style.


INTRODUCTION

Tasmania is an island, south-east of mainland Australia; it is much cooler having summer temperatures usually between 20 - 12o C (mean maximum and minimum) and winter temperatures that vary from 12 - 5o C at sea-level; temperatures rarely exceed 35o C nor go below 0o C (1). Compared with mainland Australia, Tasmanian mammals tend to be larger and have higher body temperatures due to increased metabolic rates and better insulation (2-4).

The Tasmanian bettong is an endemic rat-kangaroo (see Figure 1) that is the largest of the four species in this genus (5); it lives at altitudes between sea-level and 1000 metres (6). It has a mean body temperature (Tb) of 37.4oC (range 36.6 to 38.1) at 20o C ambient temperature (Ta) that varies daily in a sinusoidal way typical of nocturnal mammals; its Tb increases below 5o C and above 30 oC Ta (4). The Tb of the female bettong varied throughout the oestrous cycle, there being a significant increase just after oestrus (7) . Recently, we measured resting metabolic rates of bettongs to be 0.51 O2 g-1h-1 (8)

Bettongs and other rat-kangaroos are extensively mycophagous, eating large numbers of the fruiting bodies of hypogean fungus (5, 9). These fungi are high in nitrogen and lipid but are deficient or imbalanced in some essential amino acids eg. lysine and methionine (10). Much of the nitrogen and carbohydrate in the sporocarps of the fungus Elaphomyces granulatus were found to be unavailable to a mycophagous ground squirrel (11). A pure fungus diet being too poor to sustain growth or reproduction in the squirrel. More recently, it has been shown that hypogeal fungus is of marginal nutritional value for small mammals with simple stomachs (12)Furthermore it was shown that much of the high levels of fungal nitrogen were in non-protein form or associated with cell walls and may be of either low nutritional value or protected from digestive enzymes. However by microbial fermentation, bettongs and some other rat-kangaroos are able to synthesise those amino acids lacking in the diet in their extensive sacculated foregut (10-12). Recently, it was suggested that hypogeous sporocarps are a primary food source of high nutritional value to the Tasmanian bettong(9). In addition, bettongs are able to supplement their diet with Acacia gum exudate, high in carbohydrate (14)

The basal metabolism of marsupials is approximately 70% of similar sized eutherian mammals (15), although there are species differences related to the life style of the animal, (16-18).

The equation in (19) based on the metabolic rates of 32 marsupials allows a calculation that a 1.6 kg bettong would have a basal metabolic rate of 0.36 mls O2 g-1h- 1

It is difficult to predict whether the metabolic rate of the Tasmanian bettong will differ from similar sized mainland marsupials. If the diet is poor, one would expect the animal to conserve energy with a low metabolic rate. In addition, being larger and better furred than mainland species it would have better insulation and lower conductance again leading to a prediction of a lower metabolic rate. Living in a cool environment one would also expect its thermoneutral zone to be lower: this will be determined by measuring metabolic rate over a range of ambient temperatures.

We have also shown that bettongs respond to an infusion of nor-adrenalin with an increase in metabolic rate (8) indicative of 'non-shivering thermogenesis'. However, it is not known whether bettongs change their metabolic response when cold-adapted: an experiment was designed to test this.


MATERIALS AND METHODS

Animals

Five bettongs (1.5 - 1.9 kg) were trapped and held in the outdoor breeding colony at the University of Tasmania. Their husbandry has been described (20); they were fed on apples, bread and solid dog food supplemented with seeds. Prior to experimentation they were housed inside with 12 hours light and 12 hours of dark. The experiments were carried out during spring/summer 1995/96. Two bettongs were male, the other three were females without pouch young.

Four of these bettongs were later cold-adapted in a cold room at 5oC for one week and their metabolic rate at 20oC was recorded.

Measurements

Metabolic rates were measured in a perspex chamber (20 litres) totally enclosed within a water bath. The temperature of this bath could be varied between 0o C and 35o C. The air passing into the chamber was varied with a flowmeter that had been calibrated prior to the experiment. The air passed through a one metre long copper pipe that was coiled within the water bath so that the air entering the chamber was nearly at the same temperature as the water. A sub-sample of air leaving the chamber passed through drying tubes containing Silica gel and indicating soda lime before entering the oxygen analyser (AMETEK S-3A/11, 2-channels). Similarly, a sub-sample of air entering the chamber was passed though the drying tubes and into a separate channel of the oxygen analyser. The difference between the percentage oxygen of the air entering and leaving the chamber could be read directly on the analyser or from a pen recorder. The flow rate was 4 litres per minute for most experiments although at high and low temperatures this was increased to 5.5 litres. Calculations of the metabolic rate were made using equations from 21 (in 22)

Measurements were obtained during the day between 1100 - 1500 hours when the animals would normally be at rest. In the first experiment, food was not removed overnight but the bettongs had not eaten for between 6 - 10 hours before the experiment. In an additional experiment metabolic rates were obtained at Ta 20o C for the same 5 animals starved overnight; these animals would not have eaten for at least 24 hours. All animals were left in the chamber until their metabolic rate stabilised for 15 minutes.

The three female bettongs had temperature transmitters implanted for a previous experiment (7) and these animals were used for the measurement of thermal conductance (C) which was estimated using the equation:

C (J. gm. hr-1. ¡C-1) = Metabolic Rate (O2. g¨1 .h-1) x 20.1

          (Tb - Ta) . Surface area

Surface Area in cm2 = 10.7 Weight in grams2/3 (from 23). Evaporative water loss was not calculated in this experiment.

Statistical Analysis: Analysis of variance was chosen to analyse the changes in metabolic rate and conductance with ambient temperature changes. A student's t-test was used to compare the cold-adapted bettongs with normal ones at 20¡C Ta.


RESULTS

Figure 2 illustrates the change in resting metabolic rate with changing ambient temperature. Metabolic rates were lowest between 10 - 20o C which can be termed the thermoneutral zone. The lower critical temperature below which the metabolic rate increased is thus 10o C. Metabolic rates were highest at the extremes of Ta; 1.38 ± 0.38 (Mean ± sem) at 35oC and 1.00 ± 0.07 at 2o C. Panting occurred at the highest temperature (35o C) as noted by rapid shallow breathing and moisture accumulating in the tube leading to the drying column. A 'wet patch' at the base of the tail indicated that sweating occurred also at 35o C.

At 20oC ambient temperature the resting metabolic rate was 0.59 ± 0.09 O2 g-1 h-1 compared with the basal metabolic rate measured in post-absorptive bettongs at thermoneutrality that was 0.46 ± 0.05 O2 g-1 h-1. The metabolic rate of the 4 cold-adapted bettongs measured at 20oC was 0.55 ± 0.09 O2 g-1 h-1 not significantly different from the results obtained prior to cold adaptation (p=0.24, t=1.29, df=7). ANOVA showed that there were significant differences in metabolic rates (df=7,32; F=5.786; p=0.0002) at the extremes of temperature compared with 10-25oC.

Thermal Conductance

This was measured to be 0.55 ± 0.04 J. gm. hr-1. oC-1 in post-absorptive adult bettongs at 20o C. Figure 3 illustrates the variation in thermal conductance over the range of ambient temperatures. Little difference occurred in the conductance between 2-25oC Ta, but the post hoc tests showed that it increased significantly at 30 and 35oC (df=4; F=18.08; p=0.0001).


DISCUSSION

If hypogeous fungi are poor quality food they should lead to a low metabolic rate in the animals that feed predominantly on them: this did not occur in the Tasmanian bettong.

A direct relationship exists between basal metabolic rate and body weight0.75 of marsupials (23): the values obtained from post-absorptive bettongs at 20o C are above the regression line. The value of 0.46± 0.05 ml O2 .g-1 .h-1 is similar to that found in the related species Potorous tridactylus (0.45) (24). This converts (using an RQ of 0.8) to a metabolic rate of 253.5 kJ. kg-0.75 . day-1 which again is higher than the average value of 203.7 for marsupials in (23). Measurents of daily heat production in the brush tail bettong (Bettongia penicillata.) resulted invalues of 238-279 kJ. kg-0.75. day-1 (25).

A detailed list of metabolic rates for mammals: of 11 marsupials with body weights between 1-2 kg has been published (19), none had metabolic rates above 0.46 O2. g-1. h-1. Interestingly, only 3 out of 16 eutherian mammals (1-2 kg) had metabolic rates above this value.

The metabolic rates obtained in this study were similar to those from (26, 8). Metabolic rates of Tasmanian bettongs in the field have been calculated by measuring CO2 production using the doubly-labelled water method (27); the value obtained of approximately 0.8 ml CO2 g-1 h-1 (if one uses a respiratory quotient of 0.8) converts to 0.64 ml O2 g-1 h-1; only slightly higher than the values obtained at rest in thermoneutrality (0.59) in the present study.

Along with its relatively high metabolic rate, bettongs also have a high body temperature of between 36.6o C - 38.3o C; mean ± sem = 37.36o C ± 0.59 (4, 7). Two other Tasmanian mammals (Trichosurus vulpecula and Potorous tridactylus ) were found to have body temperatures approximately 1 Co above that recorded for their sub- species on mainland Australia (3).

Basal rates of metabolism in marsupials (and eutherians) are principally correlated with body mass, food habits and activity (28) . Marsupials that are specialist feeders upon invertebrates, fruits or the leaves of woody plants have low metabolic rates even by marsupial standards. In contrast, eutherians that feed on other vertebrates or herbs have high metabolic rates - "but no marsupials with these habits (dasyurids and macropodids) have high basal rates" (28). Furthermore, it has been stated that a high metabolic rate leads to high rates of reproduction (28). If one assumes that eating fungus coupled with microbial fermentation in the gut is a similar ecological niche to that of herbivorous kangaroos then the bettongs in this study appear to comply with McNab's hypothesis: they have both a high metabolic rate and high fecundity. In common with other bettongs, Bettongia gaimardi, breeds throughout the year and virtually always have a young in the pouch (29). Rat-kangaroos are more fecund than their larger relatives, the kangaroos, even when body size is taken into account (30) In addition, the Tasmanian bettong has the fastest growth rate of any macropodid marsupial for which we have information (5,31- 32): presumably the high metabolic rate and nutritious food source make this possible.

If mycophagy were a poor nutrient source or one in which essential nutrients are unavailable one might expect bettongs to conserve energy and have evolved a lower metabolic rate. The results from this work do not support that hypothesis but do support work which concludes that hypogean fungi are a rich source of food for the bettong (9).

It is interesting that thermoneutrality in this species occurred between 10-20o C, considerably lower than found in other marsupials including the related potoroo Potorous tridactylus (20-30o C) and the rufous bettong Aepyprymnus rufescens (25-35o C), (24- 25). Bettongs are strictly nocturnal (20), sleeping during the day in a well-constructed nest lined with dry grass. A nest that has just been vacated feels warm to the touch (5). In Tasmania, night temperatures are invariably low and it may be that this bettong is adapted to relatively low ambient temperatures. This is corroborated by the fact that far more oxygen was consumed at higher temperatures (30-35o C) than at low temperature (2-10o C). Considerable differences were found between metabolic rates measured during the day and night in the brush-tailed bettong Bettongia penicillata (25)

Given that the metabolic rate is higher than predicted, one likely corollary is that bettongs have low conductance and high insulation. This appears to correlate with the fact that at lower Ta., the bettong does not markedly increase its metabolic rate until 2oC nor is there much change in thermal conductance at lower temperatures. Previously (4) it was shown that body temperature demonstrated little change between ambient temperatures of 5-30oC. Although the fur of bettongs is relatively short (backfur is approximately 30 mm), it is quite dense. The thermal conductance in adult bettongs at 20o C is 50% lower than the values obtained for a range of perameloid marsupials ('bandicoots') (16) but similar to the minimum value found for the tammar wallaby Macropus eugenii (33). It has been found that fur from a Tasmanian bandicoot, Perameles gunnii, had higher insulation and fur depth than 6 mainland species(16). Also the echidna (Tachyglossus aculeatus) in Tasmania had much lower conductance values than mainland forms from Victoria and Queensland (2). The fact that the metabolic rate of the cold-adapted animals was little different from the non-adapted animals is further corroboration of low conductance.


CONCLUSIONS

The Tasmanian Bettong Bettongia gaimardi is a highly mycophagous species eating underground (hypogean) fungi. Although fungi are not usually regarded as nutritious food, bettongs survive well on this diet. Correspondingly, they have a high basal metabolic rate of 0.46 ml O2 g-1 hr-1 that is above that predicted for marsupials and many eutherians of this size. Conductance was found to be low at 0.55 J. g. hr-1. oC-1 but became significantly greater at 30-35¡C. The thermoneutral zone was also surprisingly low being between 10 - 20¡ C. Coupled with a high fecundity and growth rate, this species is well adapted to its fungivorous life-style.


ACKNOWLEDGEMENTS

This work was supported by a grant from the Australian Research Commission. A Jones assisted with the measurements of metabolic rate and S. Nicol and A Hulbert made comments upon the manuscript.


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