Energetic aspects of adaptation in the Indian desert gerbil Meriones hurrianae Jerdon

Journal of Arid Environments (1982) 5,69-75

Energetic aspects of adaptation in the Indian desert gerbil Meriones hurrianae Jerden

S. P. Goyal, P. K. Ghosh & Ishwar Prakash" Accepted 28 April 1981 Basal metabolic rate (BMR), evaporative water loss (EWL) within the thermoneutral zone and minimal thermal conductance (C) of the Indian desert gerbil Meriones hurrianae jerdon, were 0·79 cm ' 02/g/h, 1·89 mg H 20/cm 3 02 and 0·110 cm' 02/g/h/"C respectively. Below the thermoneutral zone, gerbils regulated their body temperature within the normal limits of homeotherms. The relatively high body temperature (38'7"C) recorded within the thermoneutral zone is, presumably, the result of an adaptive mechanism for reducing evaporative water loss. The gerbil's low BMR, low conductance (67 and 92 per cent of the values predicted on body weight basis respectively) and its comparatively high body temperature are considered to be physiological means of avoiding overheating.

Introduction The Indian desert gerbil Meriones hurrianae jerdon is the most abundant of 17 species and sub-species of rodents in the Rajasthan desert of north-western India. The ecology and life-history of this species have been studied in detail by Prakash, Gupta et al. (1971). Certain behavioural and physiological components of its water use have been discussed by Ghosh (1975). However, the energetic aspects of the gerbil's adaptation to the desert environment have not previously been studied. The present study was undertaken to examine its basal metabolic rate, conductance and evaporative water loss under different thermal regimes.

Material and methods Animals Gerbils were trapped at the Central Research Farm, Jodhpur (26°18'N, 73°01'E) and maintained separately in galvanized-iron mesh cages on a diet of pearl millet (Pennisetum typhoides). Eight adult M. hurrianae (4 males and 4 females), having an average body weight 69·78 (± 5·41 S.E.) g were used. The animals were provided with drinking water for 3 months prior to and also during the experimental period.

Oxygen consumption and basal metabolic rate The rate of oxygen consumption of the experimental animals (n = 8) was determined within the thermoneutral zone (TNZ) (30-35°C) (Goyal, Ghosh & Prakash, unpublished observations) by the closed-circuit method of Visscher, Brown et al. (1950) as modified by McLaren, Asplund et al. (1964). The details of oxygen consumption • Division of Animal Studies, Central Arid Zone Research Institute, Jodhpur 342003, India. 0140-1963/82/010069+07 $02.00/0

© 1982 Academic Press Inc. (London) Limited

70

S. P. GOYAL. P. K. GHOSH & I. PRAKASH

measurement have been discussed elsewhere (Ghosh, Goyal et al., 1979). All O 2 consumption values were corrected for standard temperature, pressure and dry gas.

Body and skin temperature Rectal (body) temperature (To) was measured to the nearest 0·1 ·C at the end of each experiment with a thermistor probe attached to an Atkins telethermometer. The temperatures of the skin on the inner side of the ear, the ventral and dorsal body surfaces, the inner sides of the fore and hind limbs and of the tail were measured by additional thermistors connected to the telethermometer.

Evaporative water loss Evaporative water loss (EWL) was determined gravimetrically at different ambient temperatures (T A ) , viz. 27, 33,36 and 37·C. The number of animals used at each of these temperatures were 4,8, 5 and 5 respectively. Air passing through tubes containing silica gel and calcium chloride was metered through the animal chamber (containing a layer of light liquid paraffin to minimize moisture loss from urine and faeces). The air flow through the animal chamber was maintained at a constant rate of 600 cm 3jmin. The air leaving the animal chamber passed through two gas absorption tubes which were weighed to 0·05 mg. Correction was made for the water-vapour content of the incoming air by estimating a mean value from control runs before and after the actual experiments. All measurements of EWL were made on post-absorptive animals. After allowing an animal I h to adjust at each T A' the EWL from that animal was measured over the next hour at that T A' Determinations were made at 15-min intervals, and a mean of the two lowest values obtained for each animal at each TAwas used to estimate EWL. EWL was expressed as mg H 20jcm 3 O 2 consumed during that period.

Results Body and skin temperature Within the TNZ of these animals, body temperature (To) was maintained at 38'7 ±0·34·C (S.E.) (Fig. 1). The rectal temperature rose when T A exceeded 36·C. After an hour's exposure to T A40 and 41 ·C, the rectal temperature of the animals reached about 40· 5 ·C. The skin temperature of different parts of the body, recorded at T Awithin the TNZ, are shown in Fig. I. Except in the tail region, they were generally high.

Figure 1. Rectal temperature and skin temperatures of various body regions of Meriones hurrianae recorded within its thermoneutral zone. Vertical lines represent ranges, horizontal lines, mean values, and boxes, standard errors of the means.

ADAPTATION IN MERIONES HURRJANAE

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Figure 2. Relationship between evaporative water loss and environmental temperature in Meriones hurrianae <.____.) and Dipodomys merriami <0--- 0; Schmidt-Nielsen, 1964). ·Values adapted from Ghosh (1975).

Oxygen consumption Within the TNZ, the gerbil's metabolic rate was 67·13 per cent of the expected value (Table I).

Evaporative water loss Evaporative water losses (gjlOO gjh) at different ambient temperatures are shown in Fig. 2. A conspicuous rise in water loss was observed above 37 DC.Between 27 and 37 DC, the mean EWL increased from 0'13±0'001 (5.£.) to 0·34±0·019 (5.E.) g/IOOg/h with a QIO of 2·6. Between 37 and 44 DC, however, EWL increased to 3·04 g/IOO g/h with a high QIO value. The curve (Fig. 2) showing EWL and T A suggests that T A does not influence EWL in a uniform manner, although certain temperatures appear to be more critical than others. Comparatively low Ql0 values found for the intermediate temperature range 27-37 DC indicate a thermal range within 'which the gerbils are relatively insensitive to temperature changes. This zone of thermal insensitivity apparently coincides with the thermal regime usually encountered by the animals in nature.

Discussion Desert rodents, in general, have significantly lower basal metabolic rates (Celino, 1964; Hudson, 1964; McNab, 1966; Schmidt-Nielsen, 1972) than those predicted on the basis of body weight (Kleiber, 1961). In the present study, the BMR for the Indian desert gerbil was 33 per cent lower than the predicted value (0'79 ± 0·043 (5.E.) em? 02/g/h, d.

34

42

51

108·5

70 69

Notomys cervinus

Acomys cahirinus

Acomys russatus

Gerbillus pyramidum

Meriones unguiculatus Meriones hurrianae

2/g/h

1·40 0·79

0·75

0·80

1·10

1·22

1·40

cm 3 0

Il9·10 67·13

77-55

62·88

82·36

86·65

97·93

%

Basal metabolic rate (Mb ) 2/g/hj"C

onor

0·140

0·102

0·199"

0·140"

0·232

0·292

cm 3 0

119·82 92·00t

IlI·56

90·37

95·50

137·39

167·65

%

Minimal thermal conductance (C)

Abbreviations: M. % = 100 X mean/3·4 W- O' 2 S , C % = 100 X mean/I·02 W- O' S I , T, = lowerlimit of thermoneutral zone. .. In these cases values of To were computed from the respective TA/To curves at T A = 30·C. t Values adopted from Ghosh et al. (1979).

32

Notomys cervinus

Species

Body weight (g)

Table 1. Energetic parameters of Meriones hurrianae and some other murid desert rodents

38·2 36·lt

38·7

37·0

37·0

38·5

Reference MacMillen & Lee (1970) - MacMillen & Lee (1970) - Shkolnik & Borut (1969) - Shkolnik & Borut (1969) 30 Robinson & Henrickson (1961) 30 Robinson (1959) 30 Present study

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73

ADAPTATION IN MERIONES HURRIANAE

1·18 cm' 02/g/h). The BMR of M. hurrianae, as reported here, corresponds with the lowest value reported for Acomys russatus by Shkolnik & Borut (1969) (Table 1). Its crepuscular habit makes the Indian desert gerbil susceptible to overheating. Presumably, it avoids lethal body temperatures by reducing its metabolic rate. This ensures that, while the actual impact of high T A on the body is reduced, the gerbil's need for evaporative cooling is also minimized. Similar observations have been made on the Mongolian gerbil M. unguiculatus (Robinson, 1959) and on some Spermophilus spp. (Hudson, Deavers et al., 1972). The low minimal conductance of the gerbil's pelage (92 per cent of expected value), which is, nevertheless, comparatively higher than that of other desert rodents, would seem to be part of an adaptation mechanism to combat hyperthermia (Table 1). The rate of EWL is obviously of great significance to small desert mammals. From Fig. 2 it appears that at high temperatures M. hurrianae is comparatively more efficient than the North American kangaroo rat (Dipodomys merriami) in reducing moisture loss through EWL. Furthermore, the observation that M. hurrianae significantly increases EWL at T A > 37·C only indicates a relatively high upper critical temperature. Within the thermoneutral zone, only about one-quarter of the total body heat lost by M. hurrianae can be accounted for as EWL, the rest being dissipated by radiation, conduction and convection (i.e. dry heat loss). About one-third of the water lost by the gerbil through EWL is generated within the animal's body in the course of metabolism. It is possible that the gerbil's normally high To is responsible for the relatively high dry heat loss in this species. Scholander, Hock et al, (1950) have reported high dry heat loss responses in several species of tropical mammals. Apparently, in all these species, increased EWL occurs as T A crosses threshold values which may be different for different species. A meaningful comparison between animal species based on EWL should result by relating water loss to oxygen consumption. Published EWL data for different rodent species and for M. hurrianae have been presented in Table 2 for purposes of Table 2. Comparison of evaporative water lossof Meriones hurrianae and other desert rodents within their thermoneutral zones

Water loss mg/g/h

mg H 20/cm 3 O 2 consumed

Perognathus spp.

1·56

0·50

Dipodomys merriami Dipodomys merriami Dipodomys spectabilis

1·20 0·903 0·79

0·54 0·80 0·57

Peromyscus crinitus

\·60

\·05

3·\7

2·34 \·60 2·2\ \·70 1·98 \·66

0·83 \·50 2·04 \·05 0·76 1·96 \·99

Schmidt-Nielsen & SchmidtNielsen (1950) Schmidt-Nielsen (1964) Carpenter (1966) Schmidt-Nielsen & SchmidtNielsen (1950) Schmidt-Nielsen & SchmidtNielsen (1950) Chew (\955) MacMillen (\965) Lee (1963) MacMillen & Lee (1970) MacMillen & Lee (\970) Shkolnik & Borut (1969) Shkolnik & Borut (1969)

3·95 \·50

1·15 \·89

MacMillen & Lee (1970) Present study

Species

Peromyscus maniculatus Peromyscus eremicus N eotoma lepida Notomys alexis Notomys ceroinus Acomys cahirinus Acomys russatus Leggadina hermannsburgensis Meriones hurrianae

Reference

74

S. P. GOYAL, P. K. GHOSH & I. PRAKASH

comparison. The observed high EWL in M. hurrianae, compared with that of other desert rodent species, would suggest that it places primary reliance on EWL for the maintenance of homeostasis while reducing water loss through the excretory routes (Gaur & Ghosh, 1971). Observed high body temperature within the TNZ may be due to the fact that the animal cannot afford to achieve rates of EWL sufficient to ensure a lower To. The relatively high To may help M. hurrianae to restrict EWL better than does Dipodomys merriami. The higher T R and skin temperature (Fig. 1) of M. hurrianaepresumably help the animal by reducing the gradient between the hot environment and its body. The higher abdominal skin temperature in comparison to that of the dorsal region (Fig. 1) may help the animals in reducing heat gain from the soil during day time. The gerbil's tendency to salivate at high ambient temperatures is presumably an emergency physiological defence mechanism against excessive heat, as has been suggested by Hainsworth & Stricker (1969). A similar adaptive mechanism has been reported for other desert rodents (Kirmiz, 1962; Schmidt-N ielsen, 1964; McNab, 1966) and in tortoises (Cloudsley-Thompson, 1970). The gerbil has a relatively high lethal body temperature (43·C). High lethal temperatures have also been reported for the desert ground squirrel Citellus tereticaudus (Hudson, 1964) and for certain species of birds (42--45 ·C) (Kendeigh, 1944; Dawson, 1954).

Ecological significance The levels of metabolic rate and conductance of a rodent depend, to a large extent, on two ecological factors, viz. its micro- and macro-environments (McNab, 1970; Kinnear & Shield, 1975). A decrease in the value of the metabolic rate and conductance of M. hurrianae are apparently of considerable adaptive significance especially in the light of the following facts: (a) The temperature inside the gerbil burrow during the summer ranges from 30 to 35·C (Goyal, unpublished observation). Thus, the gerbil does not experience the full heat load of the summer day. Its relatively comfortable micro-environment minimizes the chances of body over-heating and reduces the need for evaporative and convective cooling. (b) Sharma & Joshi (1975) had estimated that one gerbil excavates 61,500 kg of soiljdayjkm 2 during the summer. The internal and external heat load on the gerbil's body during this work alone should be sufficient to upset the rodent's thermoregulatory system. It seems probable that the gerbil avoids overheating by a combination of lowered heat production and increased heat loss (Table 1). We wish to express our sincere thanks to Professor T. J. Dawson of the University of New South Wales, Australia, and to Professor Brian K. McNab of the University of Florida, U. S.A. for their many helpful suggestions and valuable criticism. We are also grateful to Dr H. S. Mann, Director of this Institute, for providing the necessary facilities for this work.

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ADAPTATION IN MERIONES HURRIANAE

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