J . Zool., Lond . (1990) 222. 215-233

The effect of diet on water and energy turnover rates of four GevbiZZuvus species in captivity

COLLEEN T . DOWNS AND M . R . PERRIN

Department of Zoology and Entomology. University of Natal. P.O. Box 375. Pietermaritzburg. Natal 3200. RSA

(Accepted 31 October 1989)

(With 3 figures in the text)

The effects of diets differing in energy and water content on the energy turnover rates and water flux of four Gerbillurus species have been examined in the laboratory . Gerbillurus tytonis. a dune species. had higher than predicted daily energy expenditure (DEE) and high water turnover rates (WTR) for a small desert mammal . The large Gerbillurus setzeri. which occurs on gravel plains. has slightly lower than predicted DEE and lower WTR than the other gerbil species studied . The GerbiNurus species examined have DEE and WTR that are affected by the protein content and potential water yield of food eaten . The importance ofdiet selection for water and energy budgets are discussed as adaptive strategies employed for survival and reproduction within the southern African arid zone .

Contents Page

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216 Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216

Water deprivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 216 Energy and water balance measurements . . . . . . . . . . . . . . . . . . . . 216 Total body water determinations . . . . . . . . . . . . . . . . . . . . . . 217 Energy and water budgets . . . . . . . . . . . . . . . . . . . . . . . . . . 218 Statistical tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218

Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 218 Water deprivation trials . . . . . . . . . . . . . . . . . . . . . . . . . . 218 Energy and water budgets . . . . . . . . . . . . . . . . . . . . . . . . . . 219 Tritium-determined water turnover rates . . . . . . . . . . . . . . . . . . . . Comparison of tritium and gravimetric techniques . . . . . . . . . . . . . . . . Urine production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Faecal water loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Water budgets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Comparison of tritium-dilution and gravimetric techniques . . . . . . . . . . . . Water intake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Water efflux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Diet selection and physiological water conservation: their effects on water flux . . . . Reproduction and habitat selection: their relation to water flux . . . . . . . . . . Energy budgets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

222 222 224 224 226 226 227 228 228 229 229 230

Water and energy turnover rates: their relationship . . . . . . . . . . . . . . . . 230 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231

215 0952-8369/90/010215+ 19 $03.00 0 1990 The Zoological Society of London

216 C O L L E E N T . D O W N S A N D M . R. PERRIN

Introduction

Determination of water flux and energy expenditure partly define the adaptations and geographical distribution of desert rodents. Daily energy expenditure (DEE) and water turnover rates (WTR) of free-living mammals integrate the costs of thermoregulation, diet, activity, metabolism and reproduction (Karasov, 198 I ) . Laboratory conditions cannot quantify absolute metabolic rates precisely (Mullen. 1980). but can be used to elucidate physiological adaptations that enhance survival, and to validate field results.

The Gerhillurus species, G. puehu paehu. G. tj*totiis, G. seceri and G. twllinus tiallinus occur in arid areas where surface water is absent (Downs & Perrin, 1989). Gerhillurus tytonis is restricted to the dunes of the Namib Desert whereas G. setxri occurs only on the adjacent gravel plains. Both species rely on food for their supply of water as metabolic and preformed water. Water loss is a combination of urinary, faecal and pulmocutaneous water loss and the ability of gerbils to minimize water loss. behaviourally and physiologically (see Schmidt-Nielsen, 1964, 1975 for reviews). determines the minimum water flux necessary to remain in water balance. Because the Gcrhillurus species are diurnally fossorial and inactive. they avoid costly evaporative cooling.

The objectives of this comparative study on the four species of Gerhillurus were to:

I . Determine the effects of diets differing in energy and water content on water and energy flux. 2. Compare gravimetric and tritium-dilution techniques to determine daily energy expenditure (DEE) and water turnover rates (WTR) in the laboratory (since this is useful for the validation of the tritium technique used in the field on wild animals). 3. Compare water and energy budgets. in relation to species-specific habitat preferences.

Materials and methods

Gerbils were live-trapped during June 1986 and March 1987 in South West Africa/Namibia and in the Northern Cape. GerM1uru.s tyt0ni.s were collected at Gobabeb (23 34’ S, 15 03’ E), G. p . paebn at Swakopmund (22 42‘ S. 14 3 1 ’ E). G. . w t x r i at Rossing (22 24‘ S. I4 59’ E) and G. r . Lw//inus near Kenhardt (29 38’ S. 21 59’ E). In the laboratory, gerbils were housed individually or in pairs in aquaria with sand, in a constant environment room with a 12: 12 L : D photoperiod. relative humidity of 75% and a temperature of 25 C ( & 1 C). Gerbils were provided with w-ater l id lihitzcrii and mixed birdseed supplemented with mealworms (Tenehrio niolitor larvae), and vegetables.

Water clcprir*atioti

Effects of incremental water deprivation were investigated in 3 stages and by subjecting study animals to 3 different diet treatments, namely mealworms, sunflower seeds or millet seed. For the first 4 days (stage I) , animals were provided with water and carrot in addition to the test diet. Water was then removed (stage 2) and 4 days later. the remaining source of supplementary water (carrots) was stopped (stage 3). Individuals were weighed daily. From day 13. animals received their regular laboratory diet. During each feeding trial, 3 or 4 individuals of each species were kept in metabolic cages (145 mm x 185 mm x 100 mm) for urine collection. (A gauze ( 1 mm’) separator prevented faeces from contaminating the urine which was collected under liquid paraffin).

Energj. and water halance tiieasurettient.7

DEE and WTR determinations for G . p . ptreha. G. rytoriis and C. serzeri were done in the laboratory using the 3 feeds previously used in the water deprivation trials (Table I). For G. I ‘ . alli in us, only WTR was

WATER AND ENERGY RATES I N FOUR CAPTIVE GERBILLURUS SPECIES 217

TABLE I The composition of the dfereni experimental diet foods

Yo of Energy" EA' Potential H20 Food item wet mass (kJg-I) Fatb Proteinb Ashb Carbohydrateb (kJg-l) (mlg-I) - Sunflower seeds 3.73 29.76 45.43 30.35 3.71 20.50 2856 0.7311 Mealworms 5567 25.68 4042 44.38 2.76 12.44 11.38 0.8752 Milletd 0.0 18.0 2.69 10.0 1.0 84.0 17.5ge 0,5335' Carrots 89.47 16.50 1.30 13.25 10.67 74.78 1.74 0.9455

~~~

Gross energy content (dry mass) Percentage of dry mass Energy assimilated per g wet mass eaten if 100% assimilation efficiency Using Withers (1982) Calculated using Schmidt-Nielsen (1975) energy values for fat, carbohydrates and protein

determined. Animals were deprived of free water but fed carrots as a source of water. For a week before each feeding trial, regular diets were supplemented with the test diet and carrots. Individuals were weighed, their reproductive condition noted, and injected intraperitoneally with 0.5 ml tritiated water (0.1 mCi/ml) before being placed in a metabolic cage. During experimentation, animals were provided with known quantities of food ad lib. Uneaten food and faeces were removed daily and oven-dried at 60 "C to constant mass, before being separated and weighed. Control samples of feeds and carrots were monitored to determine a desiccation correction factor.

Further WTR data using the tritium-dilution technique were obtained for different individuals of each species subjected to the 3 diet regimes; these animals were weighed before and after experimentation.

On day 7 of each WTR trial, animals were anaesthetized with 0.05 ml Saffan (Glaxovet) injected intramuscularly. Blood samples were taken by cardiac puncture. Each animal was immediately reinjected with 0.5 ml tritiated water and kept without food or water for 3 h when a second blood sample was taken. Sealed blood samples were immediately stored at -4 "C. Additional blood samples were taken from control animals which were injected with 0.5 ml tritiated water for the first time at the end of a feeding trial, and blood samples obtained 3 h later. Animals were then returned to their vivaria live.

Water was removed from each blood sample under vacuum. Specific activity of each water sample was determined using 20 pl mixed with 5 ml scintillation cocktail (Beckmann, Ready Solve HP/B) which was then read on a Beckmann liquid scintillation counter (Model LS3801) to 2% error.

Water content of each diet was obtained by desiccating weighed fresh samples to constant mass at 60 "C. Energy content of feeds and faeces was determined by bomb calorimetry while dietary protein content was determined using the Kjeldahl method (Grodzinski & Wunder, 1975). Dietary fat content was determined using the Soxhlet method with diethyl ether as the solvent (Grodzinski & Wunder, 1975).

Total body water determinations

Several newly-caught and laboratory-maintained animals of each species were weighed and then killed using ether. Total body water (TBW) content (expressed as a percentage of wet body mass) was calculated after the animals had desiccated to constant mass at 60 "C. Carcasses were ground in a mill before determining fat content. TBW of wild animals was obtained from specimens collected during March 1988. Gerbils were preserved in 75% alcohol for I week after capture and then desiccated to constant mass. Laboratory white mice, Mus musculus, were used to validate the technique.

218 C O L L E E N T. D O W N S A N D M. R. P E R R I N

Daily energy intake (DEI) of the 4 species was determined gravimetrically as the difference between gross energy intake (GEI) and faecal energy (FE) per day. DEI was assumed to approximate daily energy expended (DEE). An energy budget was calculated using the equation from Buffenstein (1985) which assumes that daily energy assimilated (DEA) approximates energy expended plus changes in energy stored in the body where:

DEA = GEI -(FE+ U ) + ME.

Energy content of urine ( U ) was ignored in these calculations as it constitutes about 1% of total energy ingested (Grodzinski & Wunder. 1975). Metabolizable energy (ME) is the energy flux in fat stores. As subjects were non-breeding adults. i t was assumed that mass changes resulted from fat deposition or mobilization (Buffenstein. 1985). DEA was calculated using Jagosz. Gorecki & Pozzi-Cabaj (1979) values of 23.36 KJg-' of Pat mobilized and 33.9 KJg- ' of fat deposited to give a maximal energy intake estimate. Assimilation efficiency was calculated as DEE!GEI and expressed as a percentage.

Water intake was calculated as the sum of preformed water intake and metabolic water yield from consumption of food including carrots. Metabolic water was calculated assuming that 1.071.0.396 and 0.556 mi HIO is produced per gram of fat. protein and carbohydrate. respectively (Schmidt-Nielsen, 1975).

Estimated actual water turnover rates were calculated from specific activity changes of tritium between initial equilibration and final blood sample collection over time (Lifson & McClintlock, 1966). However, equilibration-specific-activity values (calculated as the specific activity of samples obtained after the second injection of tritium and 3 h equilibration. minus the specific activity of samples obtained after the initial injection of tritium) were lower than specific activity equilibration values obtained 3 h after an initial injection of tritium. When a standard tritium sample is used for all animals for all diet trials, there is a positive correlation betueen the natural logarithm of equilibration specific activity values determined after an initial injection of the isotope. and the log of body mass. Consequently, an equation was derived where:

Ln I = 12,9-(1,7 xlog body mass) R?=75.5%

(for a tritium solution with an activity of 70000 per 0.5 ml. where I is the equilibration specific activity). Consequently WTRs and TBWs for all animals were calculated using the final mass of individuals with

equilibration values derived using the above equation. The standard equations for k (the rate constant), total body water and specific WTR were used in calculations (Macfarlane & Howard, 1972; Nagy & Costa, 1980).

Stcrtistical tests

Students' t-tests. analysis of variance and standard regressions were done using Minitab5 and Statgraphics software packages. A probability of less than 0.05 was accepted as statistically significant.

Results

Water depriizt ion trials

The experimental diets differed in protein content and potential water yield (Table I). Figures 1 to 3 show thc changes in mass of gerbils fed different diets. and the effects of gradual reduction of supplementary water over time. Each species maintained mass on each diet if supplementary water was available (free water or carrots). When supplementary water was removed, average body mass of each of the four species declined, particularly on sunflower or millet seed diets. Table I1 shows the percentage decrease of initial body mass for each species at the end ofeach trial. Final masses of G. t?,tonis, G. p . paeba and G. setzeri were significantly lower than their initial body masses (P<0.05) on the sunflower seed diet.

WATER A N D ENERGY RATES I N FOUR CAPTIVE G E R B I L L U R U S SPECIES 219

110-

100-

I 5 90- : l a : . ln . D o 2 8 0 -

'C - 7 0 -

0

- m .- c

60 - Water and carrots

. . v v v T ~ Z ~ ~ . - 7 .

q q v v . . ~

0 0

I . 0

Carrots only No waterkarrot

Days 1 G. tytonis n=5 v G. paeba n=5 oG. vallinus n=5- G. setzeri n=5

FIG. 1. Changes in body mass with water deprivation on a mealworm diet

110-

- 6 100- I i 1 ! s. I

5 go-

2 80-

ln ln

- m .- c .E - 7 0 -

6 0 . Water and carrots Carrots only

0 v n . ' O D

V 7

. T I

a Q

I

No waterkarrot

Days I G. tytonis n=6 v G. paeba n=5 DG. vallinus n=5 7 G. setzeri n=5

FIG. 2. Changes in body mass with water deprivation on a sunflower seed diet.

Energy and water budgets

Components of the energy budgets for different diets for G. p . paeba, G. tytonis and G. setzeri are shown in Tables I11 and IV. Statistical comparison between species and diets is shown in Table V.

Gerbillurus tytonis had a higher water intake (ml/g/day) than G . p . paeba and G. setzeri, when fed sunflower seed or mealworms, and WTRs were highest for each species when fed mealworms. Water intake rates were assumed to equal water loss if the animals were in water balance. However, changes in mass could affect actual water assimilated. WTRs were recalculated to give values if change in mass was due to (i) fat mobilization, or (ii) dehydration. However, the correct

220 COLLEEN T. DOWNS A N D M . R . P E R R I N

v

Water and carrots

5 0 0 1 2 3

8 0

x D

Carrots only No waterlcarrot

4 5 6 7 8 9 10 Days

1G. tytonis n=12 7 G. paeba n=12 0 G. vallinus n= 12 G. setzeri n=9

FIG. 3 . Changes in body mass with water deprivation on a millet seed diet.

partitioning of weight loss to either of these factors is not possible unless the degree of dehydration is monitored. The gravimetrically-determined specific water intake values, together with recalculated water intake values if changes in mass were caused by fat mobilization and/or dehydration of each species on each diet, are shown in Tables 111 and IV.

Each species showed an initial decrease in mass when fed sunflower seeds and carrots, particularly G. setzeri. This change can be attributed to dehydration or fat mobilization. The assumption that DEI was equivalent to DEE was thus invalid. DEE was therefore recalculated assuming all changes in mass were due to fat mobilization to derive a maximum DEA.

It was necessary to establish whether or not differences in energy budget components were a true reflection of differences in mean body mass for each species. To allow comparison between species, the expected DEE value for small granivorous rodents was calculated (in kJ) using the equation of Grodzinski & Wunder (1975). Percentage actual DEE of predicted DEE (Grodzinski & Wunder, 1975) was 148, 112 and 93 for G . tJ9tonis. G. p . paeha and G. setzeri, respectively, when fed sunflower seeds and carrots. Gerhillur~s p . paebu and G . setzeri had DEE values close to the expected values.

TABLE I 1 The percentage initial body mass oJ'rhe.four Cerbillurus species at the

end of the narer deprirarion rrials

Percentage initial mass (%)

Diet G. 1ytoni.c G. p . paeba G. selzeri G. L'. rallinus

Sunflower seeds 73.19** 80.60** 82.54** 90.67 Mealworms 86.70 90.53 94.1 1 86.33 Millet seed 8764 81.51 9 I .96 85.12

__

** Indicate significant difference (P<0.05) between initial and final body mass

WATER A N D ENERGY RATES I N FOUR CAPTIVE GERBILLURUS SPECIES 22 1

TABLE 111 The energy and waterparameters of three Gerbillurus species when deprived of

drinking water and fed a diet of mealworms supplemented with carrots ~~

G. tytonis G. p . paeba G. setzeri

Parameter X S.D. X S.D. X S.D.

No. of animals 6 6 6 Initial mass (g) 30.5 5.22 27.91 3.65 43.72 15.61 Final mass (8) 29.77 3.06 24.88 2.47 40.01 9.78 GEI (kJ/g/day) 2.31 0.95 1.74 0.76 1.45 0.97 DEE (kJ/g/day) 2.10 0.86 1.63 0.73 1.39 0.90 DEA (kJ/g/day) 1.99 0.48 1.98 0.34 1.64 1.44 F E x (kJ/g/day) 20.51 10.91 11.22 5.26 12.46 8.65 AE(%) 91.09 2.85 92.68 5.13 90.00 12.13 WTR (ml/day) 16.33 4.89 8.74 3.44 10.89 4.17 WTR (ml/kg/day) 554.1 200.6 348.0 157.3 295.5 177.6 WTR* (ml/kg/day) 587.5 199.8 374.1 147.1 322.3 183.0 WTR** (ml/kg/day) 585.5 199.5 372.4 147.7 320.5 182.6

Data expressed per gram dry mass. WTR-water turnover rate assuming this equals water intake. WTR*-assuming all changes in mass are due to fat mobilization/deposition. WTR**-assuming all loss in mass is due to dehydration. G E I 4 r o s s energy intake. DEE-Daily energy expenditure. DEA-Daily energy assimilated. FE-Faecal energy. AE-Assimilation efficiency

TABLE IV The energy and water parameters of three GerbiUurus species when deprived of drinking water andfeda diet of sunflower seedssupplemented with carrots

G. tytonis G. p. paeba G. sefzeri

Parameter X S.D. X S.D. X S.D.

No. of animals 6 8 6 Initial mass (8) 30.5 5.49 28.08 3.68 38.33 7.53 Final mass (g) 31.06 3.61 25.89 3.13 34.00 7.95 GEI (kJ/g/day) 2.72 0.73 2.00 0.57 1.54 0.82 DEE (kJ/g/day) 2.56 0.74 2.07 1.16 1.48 0.79 DEA (kJ/g/day) 2.47 0.62 2.31 1.07 1.61 0.88

AE (YO) 91.95 11.84 95.40 3.62 95.76 2.55 WTR (ml/day) 10.76 3.09 6.04 2.18 7.47 3.24

FE x (kJ/g/day) 15.71 7.31 8.76 6.93 6.50 4.71

WTR (ml/kg/day) 365.4 115.1 230.7 87.4 233.5 83.8 WTR* (ml/kg/day) 378.2 113.8 253.5 87.4 254.0 71.7 WTR** (ml/kg/day) 377.4 114.0 252.1 87.2 253.5 72.3

Data expressed per gram dry mass. WTR-water turnover rate assuming this equals water intake. WTR*-assuming all changes in mass are due to fat mobilization/deposition. WTR**-assuming all loss in mass is due to dehydration. G E I 4 r o s s energy intake. DEE-Daily energy expenditure. DEA-Daily energy assimilated. FE-Faecal energy. AE-Assimilation efficiency

222 C O L L E E N T . D O W N S A N D M. R . P E R R I N

T A B L E V Results qfanu1ni.r of variance 0fenerg.1. and wafer partimeters for rhree Gerbillurus species

Interspecific Intraspecific

Mealworm and carrot Significant differences between diets

significant difference significant difference betweea G. tytonis G. p . paeba G. setzeri

Sunflower seed and carrot -___

____-~ GEI (kJ,'g day) G. r.v/onis G. setzeri G. tyronis G. p . paebu G. setzeri - - -

DEE (kJig;day) G. tj.ronis G. setzeri G. p . paebu G. setzeri - - - G. rxronrs

G. p . paebu DEA (kJ:g!day) - - G. r!.rotii.c G. seceri FE x 10-~' (kJ,g/day) G. p . paeba G. p. paeba

G. se/:eri G. ryroriis G. setzeri G. /?xronis - - - - AE ( 0 0 )

WTR (nil day) G. p . paeba G. p . paeba

WTR (nil g day) G. p . paeha G. p . paebu

WTR* (nil. g. day) G. p . paeha G. p . paebn

G. serzeri G. ryronis G. setzeri G. r~./onis

G. seneri G. ijroni.s G. serzeri G. trronis

G . sei:eri G. rytonis G. serxri G. tjroiiis

*** __ *** - - ***

*** *** ***

*** *** -

*** *** - WTR** (ml g day) G. p . paeba G. p. purho

G. serieri G. rytoni.~ G. serzeri G. /jroni.s *** *** -

Data expressed per gram dry mass. WTR-water turnover rate assuming this equals water intake. WTR*-assuming all changes in m a s are due to fat mobi1ization;deposition. WTR**-assuming all loss in mass is due to dehydration. GEI- Gross energy intake. DEE-Daily energy expenditure. DEA-Daily energy assimilated. FE-Faecal energy. AE-- Assimilation efficiency. *** (significant difference at P < 0.05).

Percentage DEE of predicted DEE values were 120, 87 and 94 for G . tytonis, G . p . paeha and G . set:eri. respectively, when fed mealworms and carrots. Subjects exhibited a less marked initial decrease in mass compared to those fed sunflower seed. Gerbillurus tytonis and G . p . paeha subsequently increased in body mass but G . setzericontinued to lose body mass. AE values of each species were high and similar on mealworm/carrot diets. In addition, G.p.paehu and G . tytonis had similar DEA values.

Tritium-determined water turnover rates

Table VI shows laboratory WTRs of the four Gerhillurus species on diets differing in protein and water content, using the tritium-dilution technique. Significant intraspecific and interspecific differences for each diet are shown in Table VII.

Conzpur ison of t ri t iuiii and grar itne t r ic techn i y ues

Percentage hod) \t.ater

Table VI shows percentage body water content obtained using the tritium technique, for each species on each diet. No significant differences were noted among diets ( P > 0.05) for each species, hou ever, there were significant differences among species on each diet trial. Percentage body water was positive11 correlated with body mass (r'=91.20%, d$ = 185) where:

% Body water= 145,547- 1.593 Log mass.

WATER A N D ENERGY RATES I N FOUR CAPTIVE G E R B I L L U R U S SPECIES

TABLE VI Water turnover in four Gerbiiiurus species in the laboratory on diets difering in protein and water content

223

BM TBW K Water flux Species N (g) YO final wt. x (ml/kg/day) (ml/kg 042/day)* ml/day

Mealworm G. rytonis 7 33.3k3.06 70.35k 1.471 15.71 298.1 f44.5 509.6k48.9 8.44k0.8 and G. p. paeba 5 27.9k2.1 73.43f 1.417 14.07 231.2k 13.55 355.0k30.3 6.66f0.19 carrots G. v . vallinus 10 37.652.17 67.45f0.842 18.20 225.53k58.39 455.7k51.1 6.63f0.56

G. setzeri 4 32,853.01 70.73k 1.740 11.79 200.53f49.29 385.3k 107.8 6.38+ 1 59 Sunflower G. tytonis 10 32.95 1.35 70.38k0.76 13.07 220.5f15.9 468.4k52.8 7.2350.61 seeds and G. p. paeba 20 27,250.95 74.01 k0.681 8.92 150.8f7.94 213.2+ 14.2 4.06f0.21 carrots G. v . vallinus 6 47.4 k 4.43 64.12 f 1.462 6.73 103.5 k 7.68 420.1 k 58.6 447 k 0.46

G. setzeri 12 41.8k2.35 64.77k0.984 7.45 115.01 k23.66 359.8k77.4 4.76k0.98 Millet G. tytonis 7 36.9f1.84 67.61k0.96 8.31 136.99f 14.9 314.9k35.1 4.93k0.50 and G. p.paeba 8 29,452.57 72.80k1.622 6.14 105.6f8.97 206.9k38.1 2,9650.16 carrots G. v . oallinus 8 40.35 1.28 66.68k0.653 10.97 173.4k 18.17 515.4k72.6 7.18k0.88

G. setzeri 3 294751.69 71.99+1.103 5.91 102.17k4.68 172.0k16.5 3.04k0.14

Mean+S.E.; N, number of animals; BM, body mass; TBW, total body water; K, water turnover fraction per day; * water flux using body mass expressed to 0.82 (Macfarlane & Howard, 1972).

Percentage body water values of wild animals, determined gravimetrically, are shown in Table VIII. The effects of 70% alcohol fixation on total body water were found to be negligible when laboratory white mice were used to validate the technique. Gravimetrically-determined percentage body water values were similar to those obtained for animals in the laboratory using the tritium- dilution technique (Table VI).

Water flux

Tritium and gravimetric techniques showed similar trends of water flux among the species for each diet treatment. However, gravimetrically determined water turnover rates were generally greater than tritium-derived values by a factor of two. Table IX compares values determined using

TABLE VII Inter- and intraspecijic comparison of the Gerbiiiurus species on the three diet regimes

Water flux (ml/g/day)

Interspecific comparison Intraspecific comparison

Diet Significantly different* Species Significant difference*

Mealworm and G. tytonis and G. setzeri G. tytonis All 3 diets carrot

Sunflower G. tytonis and G . setzeri G . p . paeba Mealworm and carrots seed and G.p.paeba G. u. uallinus No diet carrot

Millet seed No spp. and carrot

G. setzeri Mealworm and carrots

* Significant difference (P< 0.05)

224 C O L L E E N T. D O W N S A N D M. R. P E R R I N

TABLE V I I I Grat.i~nc~tricu/lv dcverniined percenluge hod). water q/' bi.ild aninial.v

caught during March I988

Faecal water loss (mlj'g of body mass) Mass (g)

Species I1 x f S.E. X * S.E.

G ri / o t i / y 8 j; 2 4 0 3 k 2 2 4 6#37+0960

G p pueha 5 j j 2358+420 6968k5036

G I I ul/rnii\ 1 ; 26 8 64 55 G ieIzeri 2 j; 35 30+44O 6 7 9 3 k 4 2 0

Mus muscuht 2 jj' 2092+154 6570+2182 (alcohol treatment)' 2 M u \ ti1usc uluc 2 j'j 2 2 3 4 i 0 7 2 6 4 0 0 k 2 0 4 (control treatment)** I

5 .

1

3 - -

* Alcohol t r e a t m e n t d e a d animals stored in 70"/;1 alcohol for 7

* * Control t r e a t m e n t d e a d animals placed only into oven at days before being placed in an oven at 60 c for 7 days

60 C for 7 days.

both techniques in the laboratory. Results from regression analysis between the data collected for the two techniques are shown in Table X.

C'riiie production

Urine volumes recorded for the Gerhillirrrrs species on mealworm or sunflower seed diets are shown in Table XI. Medians are included because daily individual variation on each diet trial was high.

Fueid \ iatCr loss

Table XI1 summarires faecal water loss of gerbils on different diets and includes faecal water loss ( % wet weight), faecal production (g,day,g of body mass), and specific faecal water loss (ml/g of body mass, day).

TABLE IX Cotnpurisori c!f water .flus using grarinie/ric and tritium-

dihrrioii te4lnique.s

Tritium WTRGravimetric WTR ( ' X )

Species Mealworm and carrot Sunflower and carrot

G. rytonis 53.80 60.4 I G. p . paeho 66.44 65.28 G. serxri 67.75 49. I5

WATER A N D ENERGY RATES IN FOUR CAPTIVE GERBZLLURUS SPECIES

TABLE X Results of linear regression analysis between gravimetric and tritium-dilution techniques

for individuals when both techniques were used simultaneously

225

Diet Intercept Slope R2(%) Prob. level d.J ______

Mealworm and carrot 148.1 k32.94 0.124k0.076 15.95 0.0005 15

Sunflower and carrot 195.1 k41.24 0.0195+0.152 0.14 0.00049 13 0,1254

0.89996 Both 174.45k21.28 0.074f0.058 5.41 0.0000 29

0.2163

TABLE XI Urine production ofthe four Gerbillurus species on mealworm and carrot, and

sunflower seed and carrot diets

Urine production (ml/day)

Mealworm and carrot Sunflower seed and carrot

n X Median S.E. X n X Median S.E. %

G. tytonis 17 0.988 1,100 0,108 13 0.119 0.080 0.033 G.p. paeba 8 0.264 0.240 0.071 14 0,081 0.050 0,018 G. u. vallinus 7 0.460 0.190 0,216 12 0.293 0,235 0.066 G. setzeri 12 0.762 0,425 0.174 11 0.058 0.020 0.019

TABLE XI1 Faecal production and faecal water loss of the Gerbillurus

Mealworms Sunflower seeds

G. tytonis G. paeba G. vallinus G. setzeri G. tytonis G. paeba G. vallinus G. setzeri B

Faecal production 0,0114 0.06 - 0.007 0.009 0.005 - 0.004 (g/day/g of body mass) (6) (6) (6) (6) (8) (6)

A Faecal water loss 45.94 59.01 62.57 41.89 37.36 35.38 43.00 37.01 (% wet faecal mass) (8) (2) (3) (2) (3) (2) (4) (3)

B 50.64 - 51.78 53.66 37.21 28.75 32.37 39.10

(6) - (4) (5 ) (4) (2) (3)

B Faecal water loss 0.01 17 0.0051 - 0.0869 0.0053 0.0021 - 0.0026 (ml/g of body)

A = Diet supplemented with water and carrot B =Diet supplemented only with carrot, no drinking water Sample sizes in parentheses

22h C O L L E E N T . D O W N S A N D M. R. P E R R I N

Water budgets

Avenues of water intake and water loss which make up the water budget, together with actual water flux, are shown in Table XIII.

TABLE XI11 A sunimarj of the ti'iiter hudgrrs Of'Gerbillurus species crssumitig water intake equals

w~rter loss

Water loss

Faecal Urinary EWL WTR Diet Species (ml gBM day) (ml g d a j ) (mllgiday) (ml/g/day)

Mealworms G. g.ro~is 0.01 17 0.0297 0.257 0,298 and G. p. paeha 0.005 I OW95 0.216 0.23 I carrot G. ser-eri 0.0087 0.232 0,169 0,201

Sunflower G . r~.ronr.s 0,0053 0.0036 0.212 0.221 seed and G. p. paeha 0.0021 0.0030 0,146 0,151 carrot G. .retxri 0,0026 0.0014 0.111 0.115

Mean values: EWL, calculated evaporative water loss; WTR, water turnover rate using tritium-dilution technique: BM, body mass

Discussion

The abilitb to survive indefinitely without free water is characteristic of desert rodents that reduce water loss through urine concentration, reduced faecal and evaporative water loss and low metabolic rates (Blackwell & Pivoruni, 1978: Deavers & Hudson, 1979). Comparison of DEEs and WTRs of G. p . ymha, G. tj*tonis and G . setzeri, on diets differing in energy and water content, allows conclusions to be drawn regarding adaptive strategies for coping with changing environmental circumstances and physiological mechanisms in reducing water loss.

Recent studies on energy and water budgets of xeric-adapted rodents have examined the effect of diet on energy and water turnover rates. Foods vary in their relative concentrations of preformed and metabolic water, while the assimilation and digestibility of particular foods affect water yield and faecal water loss (Withers, 1982). Diets with similar water content but having incremental nitrogen loads (Grubbs, 1980). the effectiveness of arthropods and succulent vegetation as water sources (Karasov. 1981), and differences in preformed water content and digestive assimilation efficiency (Withers, 1982). are factors known to affect energy and water balance of desert rodents. This study examined these factors, particularly the relationship between energy and water balance. and differences in preformed water, by investigating diets differing in potential water yield and protein content. Buffenstein (1985) found that G. p . puebu maintained water balance on millet seed, however. on bran. a fibrous, low-digestibility diet, water deficiency occurred owing to increased faecal water loss. In this study, the fibre content of different diets was low and AE high.

Several desert rodents, including Gerhillirspusilliis (Buffenstein, 1984), Dipodomys rnerriumi and D. ri'eserti (Yousef et ul., 1974). survive indefinitely on a diet of dry seeds in the laboratory. However. other desert rodents. particularly omnivores and insectivores, including Peromyscus municulutus (Jameson, 1952), Onychomjss torridus (Schmidt-Nielsen & Haines, 1964; Whitford &

WATER AND ENERGY RATES IN FOUR CAPTIVE GERBILLURUS SPECIES 221

Conley, 1971) are dependent on arthropods and/or succulent vegetation for water and cannot survive on dry seed diets. The feeds used in this study differed in composition; millet seed had a lower protein content than sunflower seed yet both had lower water yields than mealworms. The Gerbillurus species maintained body mass when fed mealworms but were unable to maintain body mass on a diet of millet or sunflower seeds without supplementary water.

Comparison of tritium-dilution and gravimetric techniques

Urine-c,oncentrating abilities of desert rodents, and their tolerance of water deprivation, have been examined in the laboratory to assess their independence of water and efficiency of water usage (MacMillen & Hinds, 1983). However, the biological significance of these results is restricted, since free-living animals are never exposed to such extremes, or utilize metabolic and/or preformed water. Development of the tritium-dilution technique for estimating total body water content (Pace et al., 1947; Hollemann & Dieterich, 1975) and water turnover rates (Lifson & McClintlock, 1966; Macfarlane & Howard, 1972; Nagy, 1975), allows assessment of energy and water relations of both laboratory and wild animals.

The water turnover constant, k, defines theamount of body water turned over per day. This is an accurate index of WTR (Grubbs, 1980) which varies with diet, temperature and size in an expected manner, but is affected by a body mass function. WTR is expressed: (i) specifically (i.e. per gram of body mass); or (ii) as a function ofmass expressed to a power (the power function 0.82 (Macfarlane & Howard, 1972) is generally used). The biological significance of many of these expressions is dubious, however, they are applied routinely. When comparing WTR (either intra- or interspecifically), seasonal and dietary effects must be considered.

Good correspondence between laboratory-determined gravimetric and tritiated WTRs has been obtained (Lee & Lifson, 1960; Hulbert & Dawson, 1974; Green & Dunsmore, 1978). However, Grenot et al. ( I 984) found that the tritium-dilution technique underestimated WTRs by about 2444, whereas Grubbs (1980) found that it overestimated WTRs. In this study, the tritium- dilution determined values were lower than values determined using the gravimetric method, however, both methods showed similar trends in water flux. The gravimetric data are questioned, because of inaccuracies in the quantification of amount of food eaten. Inaccuracies in the measurement of actual amount of food eaten would further contribute to discrepancies.

It was assumed that water intake reflected WTRs when rates were determined using the tritium- dilution technique. The WTRs of G. tytonis showed a decrease with potential water yield of the diet but WTR was higher on a diet with greater protein content but with similar water yield to other diet regimes. Each species had higher WTRs on the insect diet, which emphasizes the effect of diet on WTR. The WTR of G. p. paeba increased 1.5 times when changed from a sunflower to a mealworm diet. Gerbillurus setzeri and G. p. paeba reduced their WTR by a factor of 2 when feeding on millet seeds rather than mealworms. Although the DEE of G . p. paeba was slightly lower than predicted by body mass (Grodzinski & Wunder, 1975) and the WTR greater on the mealworm diet, animals were in positive energy and water balance as there was no change in body mass. Increased WTRs may have been a result of excess water supply or increased urinary water loss to cope with higher protein levels. The WTRs of G. setzeri were lower on each diet trial compared to the other gerbil species. This could be partly the result of reduced surface to volume ratio and lower mass-specific metabolic rate of G. setzeri owing to its large body size which causes lower evaporative water loss.

228 COLLEEN 7. DOWNS AND M . R . P E R R I N

Wuter intake

In a review of the water relations of rodents, Fyhn (1979) showed that water consumption correlated poorly with body mass, despite the positive relationships found by Hudson (1962) and Chew (1965). Fyhn (1979) also found that, within a given habitat, there were large differences in water requirements for different species, although water needs generally decreased with increase in aridity of the macro-environment.

Water intake of G. p . paeha was higher on a millet seed and carrot diet than that observed by Buffenstein (1985) when animals were provided with millet and water. GerbiElurus p . paeha (Withers, Louw & Henschel, 1980) and G. tj.tonis (Maiga, 1984) had high water intakes in the laboratory. Rodents that do not drink in the wild may develop a dependancy on drinking water in the laboratory (Boice, 1972). In the current study WTRs of G. ryronis on each diet were higher than other desert rodents of similar body mass. GerbiNus gfeadowi, a small nocturnal rodent of the Indian Desert, has a high WTR for its body mass, owing to its small size and consequent large difference between total water loss and metabolic production (Ghosh, 1975).

Water qflus

Investigation of varying dietary protein and water content on faecal water content, urinary output and its concentration are essential for understanding the water budgets of Gerbillurus species. Desert-dwelling granivores may balance water budgets in two fundamentally different ways: by reducing the rate of metabolism and/or by increasing urine concentration (McNab, 1979). Most species use a combination of the two, with the balance being reflected in differences in food selection (McNab, 1979). Renal concentrating abilities are of major importance in water conservation in Gerhillurus species.

Urine osmolality, changes in body mass and water fluxes are often monitored to define water balance status (Grubbs, 1980) but emphasis is often placed on urine osmolality rather than urine volume. Urine concentration reflects either the solute load of the diet or the water conserving abilities of a diet low in water yield, while urine osmolality is generally used as an indicator of urinary water loss. This study shows that, on an arthropod diet, the animals concentrate urine maximally but produce increased volumes of urine compared to those on a granivorous diet, high in protein but low in water yield. The major physiological response an animal can achieve to remain in water balance is to lower urinary water loss (Grubbs, 1980). Data regarding the composition of the urine on the different diets, together with information about kidney structure, will be presented elsewhere (Downs & Perrin. In prep.).

Gerhillurus species have a faecal water content similar to those of other desert rodents (Carpenter, 1966; MacMillen & Lee, 1967. 1970; Buffenstein, 1985). Rodents consuming seeds have high assimilation efficiencies (AE), reduced faecal output and consequently lower faecal water loss (Withers e f a/., 1980). High AE is essential for the maintenance of a positive water balance, especially for desert rodents as they could not survive indefinitely on a diet low in preformed water if AE was less than 85% because faecal water loss alone would prohibit water balance (Withers, 1982). The assimilation efficiencies of all species studied here were high on both the mealworm and sunflower seed diets.

When water budgets were compiled for each Gerbi//urus species on each diet, combined urinary and faecal water losses were seen to constitute a small proportion of total water loss; the main water loss was evaporative water loss.

WATER A N D ENERGY RATES IN FOUR CAPTIVE G E R B I L L U R U S SPECIES 229

Diet selection and physiological water conservation: their efects on wateryux

For animals dependant on water intake from food, diet selection, composition and availability adjust to determine water intake. Haines et al. (1974) and Morton (1980) show that for some desert insectivores, exploitation of insect food removes the need for efficient physiological water conservation. Degen et al. (1986) suggest that omnivores survive in arid zones through diet selection and not physiological adaptation. However, diets comprised principally of arthropods, although high in water yield, have a correspondingly high nitrogenous waste production. To minimize water loss, these animals require efficient urinary concentrating abilities and it is reasoned that they inhabit desert areas, through physiological adaptations and diet selection.

Stomach content analyses of three of the Gerbillurus species (Table XIV) indicate that they are omnivorous and opportunistic. Leaves of the succulent Trianthema hereoensis (Seely & Louw, 1980) and invertebrate remains (Downs & Perrin, 1989) have been found in burrows, suggesting that gerbils select food items high in potential water yield.

Previous studies have used WTR as an estimate of the overall state of water economy. Generally, animals with extremely low WTRs are assumed to be the most ‘desert-adapted’ in terms of water economy. This must be particularly true when food resources are at a minimum and inhibit diet selection. However, minimum WTRs are deceptive as animals may only seldom be strict granivores, at which times water intake may be low, permitting existence but preventing reproduction.

Reproduction and habitat selection: their relation to waterpux

Christian (1979) suggested that seasonality of reproduction in G. p . paeba is determined by periods of increased ‘water’ availability. Resource availability and diet selection therefore influence water- and energy-acquisition necessary for reproduction. Water scarcity will cause selection for foods high in digestibility (Buffenstein, 1985) and animals may require all water intake for maintenance, and breed only when water availability increases.

Knowledge of water flux in the field and water conserving abilities in the laboratory may be poor predictors of habitat selection and distribution in desert rodents (Karasov, 1983). Rodents indirectly dependant on water, which rely on arthropods, are seldom faced with water stress if arthropod densities are stable and/or sufficiently high. The Namib Desert is unique in receiving small but regular amounts of precipitation in the form of fog so that insects found there exhibit behavioural and physiological adaptations to maximize intake of fog water (Louw & Seely, 1972).

TABLE XIV Resulfs of stomach content analysis

Percentage

seed invertebrates plant unknown

*G.p.paeba 8.0 53.6 35.0 2.7 *G. tytonis 4.3 52.0 41.0 3.4 **G. serzeri 10.0 50.0 40.0 -

* Mean values (Boyer, pers. comm.) ** Mean values obtained during March 1988, gravel

plains near Gobabeb (n = 5)

230 COLLEEN T. DOWNS A N D M . R . PERRIN

Arthropod population densities have been extensively studied in the dunes, and studies are currently in progress on the population densities on the gravel plains (Seely, pers comm.). Gerbillurus tytonis is confined to the dunes whereas G. setzeri occurs only on the gravel plains, and it is speculated that differences in their WTR may reflect differences in insect availability in these habitats.

Energ!. h udge ts

Typically, desert rodents (Yousef & Johnson, 1975; Haim & Borut, 1986) have reduced metabolic rates. Withers et al. (1980) and Buffenstein ( 1985), however, found that G.p.paeba had a higher than predicted DEE for a granivorous rodent of its body size when fed on air-dried seed, suggesting that it supplements its diet with arthropods. In this study, G.p.paebaand G. tytonis had DEEs greater than expected values, suggesting high metabolic rates relative to body size. When fed sunflower seeds or mealworms, G. set-eri had a DEE 93% of the predicted value. This lower DEE contributes to a lower WTR than G. tytonis and G. p . paeba.

McNab (1980) suggested that desert rodents with higher than predicted DEE values do not have the ability to become torpid. Even when starved, or deprived of water, Gerhillurus species have never exhibited torpor in the laboratory (pers. obs.). Petrontjvcus collinus (Withers et al., 1980), which also occur in the arid zones of southern Africa, have a low WTR and DEE, and can also go into torpor. but, unlike Gerbi/lurzts species, these mice are strict granivores.

Water and eiiergj. turnocer rates: their relationship

When animal species are dependant on diet for water intake, it is necessary to establish whether differences in water flux reflect differences in metabolic rate or water conserving abilities. Water and energy turnover rates can be linked if animals rely solely on their food as a water source (Yousef et al., 1974). Desert-dwelling. strictly insectivorous animals (Haines et ul., 1974; Morton, 1980) which show little evidence of adaptations to reduce water loss, and desert-dwelling granivorous rodents (Glenn, 1970). have water flux patterns that directly reflect energy usage patterns. An understanding of an animal's ability to survive on different diets is impossible ifwater and energy budgets are not examined simultaneously. The ratio of WTR/DEE (using the WTR determined from the tritium-dilution technique) can be used as an index of water economy (Withers rt al.. 1980) and energy balance. When fed mealworms, G. p. paeba and G. tytonis exhibited the same ratio value of 0.142 ml H20 kJ-', with G. setreri only slightly higher with a value of 0.144. All four species maintained body mass on this diet without supplementary water or succulent material. The equivalent ratios on the sunflower seed diet were 0.073,0.086 and 0.078 for G. p . puehu. G. tytonis and G. setreri, respectively, i.e. almost half the values recorded on the previous diet. Ratios were similar for the different gerbil species for each diet regime, emphasizing first. the relationship between DEE and WTR. and secondly, the similar response of the gerbils to different diets. The WTRs primarily paralleled DEE but were secondarily affected by the potential uater yield of the different diets. This required efficient water balance control, particularly plasticity, in renal concentrating ability.

For each unit of energy ingested, carnivorous dasyurids ingest approximately five times more water than granivorous rodents (Haines et al., 1974). The former show no specific adaptations to reduce water loss and WTR is directly parallel to metabolic rate. Water turnover rates of gerbils, however. do not necessarily reflect metabolic rate as they are compounded by the abilities of the

WATER A N D ENERGY RATES IN FOUR CAPTIVE GERBILLURUS SPECIES 23 1

gerbils to produce highly concentrated urine, and the differing potential water yield of the dietary items eaten. Low WTR on the sunflower seed diet is a consequence of a lower water intake, and to remain in water balance, gerbils have reduced water loss, particularly urinary water loss. The WTR/DEE ratios for the Gerbillurus species are all higher than the 0.04 value that Withers et al. (1 980) found for desert rodents.

Summary

In the laboratory, Gerbillurus species showed high WTRs but good urine concentrating abilities that would allow versatility in WTR, depending on the protein content and potential water yield of the diet. Insect diets, or supplements of succulent plant material, are important for the maintenance of water balance. The dune species, G. tyronis, had a higher WTR than the allopatric gravel plain species G . setzeri, with the other two species showing intermediate values. For free- living gerbils, diet selection and resource availability will determine WTR and maintenance of water balance.

The FRD of CSIR and the University of Natal Research Fund are thanked for funding this study. Laura- Jane Fielden, Colin Sapsford and Tony Bowland are thanked for their constructive discussions, while Bernard Cebekhulu is thanked for his assistance with caring for the animals.

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