(Myotis lucifugus) during pregnancy and lactation

Water balance of free-ranging little brown bats (Myotis lucifugus) during pregnancy and lactation ALLENKURTA'AND GARYP. BELL^ Department of Biology, Boston University, Boston, MA 02215, U. S.A.

KENNETHA. NAGY Laboratory of Biomedical and Environmental Sciences, University of California, Los Angeles, CA 90024, U.S.A. AND

THOMASH. KUNZ

Can. J. Zool. Downloaded from www.nrcresearchpress.com by 70.81.128.66 on 05/04/15 For personal use only.

Department of Biology, Boston University, Boston, MA 02215, U.S.A. Received October 21, 1988 KURTA,A., BELL,G. P., NAGY,K. A., and KUNZ,T. H. 1989. Water balance of free-ranging little brown bats (Myotis lucifugus) during pregnancy and lactation. Can. J. Zool. 67: 2468 -2472. This study provides the first measurements of daily water flux in free-ranging bats during pregnancy and lactation. We used the wash-out rate of tritiated water from the body water pool to calculate daily water flux in 10 pregnant and 14 lactating little brown bats (Myotis lucifugus). Average water influx was 6.16 f 0.47 (SE) mL/day during pregnancy and 6.91 f 0.37 mL/ day during lactation; average efflux was 6.27 f 0.44 and 7.07 f 0.36 mL/day during pregnancy and lactation, respectively. Using data from the literature, we partitioned daily flux into major components. Our calculations indicated that most (>62 %) water influx was preformed water in the insect diet. Drinking water represented 23 -26% of daily influx. Although previous studies indicated that evaporative losses greatly exceeded urinary losses in laboratory-maintained M. lucifugus, urinary and evaporative losses were comparable in our free-ranging bats. Urinary losses represented 46% of water efflux during pregnancy and 35% during lactation. Over 80% of all water efflux occurs during the 8-h night. KURTA,A., BELL,G. P., NAGY,K. A., et KUNZ,T. H. 1989. Water balance of free-ranging little brown bats (Myotis lucifugus) during pregnancy and lactation. Can. J. Zool. 67 : 2468 -2472. On trouvera ici les ksultats d'une etude originale sur le flux hydrique quotidien de chauves-souris au cours de la grossesse et de la lactation. Nous avons utilise le taux d'klimination d'eau tritike B partir du pool hydrique total chez 10 femelles enceintes et 14 femelles noumcikres du Vespertilion brun (Myotis lucifigus) pour calculer le flux hydrique quotidien. L'influx hydrique moyen a 6t6 kvaluk 5 6,16 f 0,47 mL/jour (erreur type) au cours de la grossesse et B 6,91 f 0,37 mL/jour au cours de la lactation; l'blimination moyenne est de 6,27 f 0,44 chez les femelles enceintes et de 7,07 +_ 0,36 mL/jour chez les femelles nourricikres. Nous avons d6tennine les principales composantes du flux quotidien B partir des donnees de la litterature : nos calculs indiquent que la plus grande partie ( > 62 %) de l'influx hydrique provient d'eau dbja pksente dans les insectes consomm6s. L'eau bue reprbsente 23 -26% de l'influx quotidien. Bien que des btudes antkrieures aient indique que les pertes d'eau par evaporation semblent exceder considerablement les pertes d'eau dans l'urine chez des M. lucifugus gardes en laboratoire, les ksultats de notre etude indiquent que les pertes d'eau dans l'urine sont comparables aux pertes d'eau par bvaporation chez les chauves-souris libres. Les pertes d'eau dans l'urine constituent 46% de l'klimination pendant la grossesse et 35 % durant la lactation. Plus de 80% de toute l'elimination d'eau se produit durant les 8 h de la nuit. [Traduit par la revue]

Introduction The water economy of mammals has been examined in a number of species, with emphasis on compartmentalization of water loss and the adaptive role of kidney structure (e.g., Chew 1965; MacMillen 1972; Geluso 1978). Such studies provide valuable insight toward understanding water relations in mammals, particularly desert forms, but most measurements have been on animals confined to the laboratory. Water flux, however, is generally correlated with metabolic rate (Macfarlane and Howard 1972), and the metabolic rate of freeranging mammals is generally greater than that of animals in captivity (Nagy 1987). In addition, laboratory conditions (temperature, humidity, diet, etc .) are frequently quite different from those that an animal experiences in the wild. Consequently, a thorough understanding of mammalian water balance requires the quantification of water flux under field conditions. 1Present address: Department of Biology, Eastem Michigan University, Ypsilanti, MI 48 197, U. S.A. 'Present address: The Nature Conservancy, Santa Rosa Plateau Preserve, 221 15 Tenaja Road, Mumeta, CA 92362, U.S.A. Printed in Canada 1 ImprimC au Canada

Bats are particulary intriguing mammals in which to investigate water flux, for a number of reasons. Their small size, large naked flight membranes, and warm roosts presumably lead to high rates of evaporative water loss at rest (Bassett 1980). In flight, water loss is even greater (Carpenter 1986). Moreover, many bats depend on high-protein diets, such as insects, and consequently face high urea loads. Although bats are the second largest group of mammals, only two previous studies (Helversen and Reyer 1984; Bell et al. 1986) have quantified water flux of bats in the field, and both studies used only nonreproductive individuals. In the present paper we provide the first measurements of daily water influx and efflux in free-ranging bats during pregnancy and lactation. Myotis lucifugus is a small (7 - 11 g) insectivorous bat which is widely distributed across North America (Barbour and Davis 1969). Kurta et al. (1989) recently reported field measurements of metabolic rate for M. lucifugus, made with the doubly labeled water technique. This method uses the differential and Oxygen in the water pool to calculate carbon dioxide production (Nagy 1980). The doubly labeled water technique also a l l ~ w sthe separate calculation of water influx and efflux, using the wash-out rate

KURTA ET AL.

of the hydrogen isotope alone (Nagy and Costa 1980). In the present paper, we present water flux data for the 24 M. lucifugus whose energy expenditure is summarized by Kurta et al. (1989). In addition, we use the extensive ecological and physiological data base of M. lucifugus (see Fenton and Barclay 1980) to partition daily flux into major components.


Methods Field and laboratory protocol Fieldwork was carried out at five M. lucifugus maternity colonies in southern New Hampshire and northern Massachusetts (U. S.A.) between 9 May and 23 July 1986. Bats were captured by hand from their maternity roosts at approximately 13:00. Each bat was weighed to the nearest 0.0 1 g and marked with a numbered plastic band. Using a calibrated glass syringe we injected each bat intraperitoneally with 24 pL of sterile water containing 95 at. % of '"0and 32 pCi (1 Ci = 37 Bq) of 3H per microlitre. We allowed 1 h for equilibration of the isotopes with the body water pool; preliminary analyses indicated that equilibration was complete within 45 min (Kunz and Nagy 1988). During equilibration, bats were housed in small wooden cages that simulated the normal roost environment and minimized physiological stress (Kunz and Kurta 1988). After equilibration, a small (40 -60 pL) blood sample was taken from a vein in either the wing or tail membrane before the bat was released inside its home roost. Injected bats were recaptured 24 or 48 h after injection; upon recapture, each bat was weighed and bled a second time. Blood samples were flame-sealed in heparinized microhematocrit tubes and transported on ice to the laboratory. Blood samples were vacuum distilled, and the resulting water was later analyzed for isotope activity. Tritium activity was measured using a toluene Triton-X-100 - PPO scintillation cocktail and a Beckrnan 230 liquid scintillation counter; '"0was measured by proton activation analysis (Wood et al. 1975). Details of laboratory procedures are given by Nagy (1983) and Kunz and Nagy (1988). Water influx and efflux were calculated from the wash-out rate of tritium, using the equations of Lifson and McClintock (1966) as modified by Nagy (1975, 1983). In general, we estimated total body water (TBW) from '"0dilution space. However, leaks occurred during the injection of four individuals and made the estimate of their TBW, based on '"0dilution, unreliable. In calculating water flux for these four bats, we assumed that their percent body water content was equal to the mean value of the other bats. We also compared estimates of TBW obtained with '"0 and those obtained by desiccation, using an additional 42 adult female M. lucifugus. These bats were injected with '"0-enriched water, and blood samples were drawn after 45 min. The blood was later distilled and '"0activity was determined and used to calculate TBW. The bats were sacrificed after bleeding; the carcasses were then dried to constant mass at 60°C, and TBW was determined gravimetrically. Water loss while day-roosting was estimated, for both pregnant and lactating M. lucifugus, on the basis of the decrease in average body mass. A group of bats was removed from the roost near dawn (about 04:30) and sacrificed; gut contents were removed, and the bats were weighed to the nearest 1 mg. A similar sample was taken at dusk (about 20:30). The difference in mean body mass between morning and evening samples was taken as an estimate of average water loss (including evaporative, urinary, and milk water, but excluding fecal water) during the day-roosting period. This procedure slightly overestimates actual water loss because a small portion of the mass loss is attributable to solids in the milk or urine. Conversion factors and diet composition On average, insects contain about 70 % water, 17.8 % protein, 4.6 % fat, 2.2% carbohydrate, 3.8% chitin, and 1.5 % ash (Kurta et al. 1989). We assumed that M. lucifugus assimilated 95 % of ingested protein, fat, and carbohydrate, and that chitin was totally indigestible (Altman and Dittmer 1968). Thus, 0.07 g of dry feces is produced for each gram of ingested insects. One gram of metabolized protein, fat, or carbohydrate yields 862, 1400, or 830 mL C 0 2 , respectively (Bra-

2469

field and Llewellyn 1982). Thus, 0.75 g of protein is metabolized for each litre of CO, produced from an insect diet. Metabolism of 1 g of protein yields 5.7 mmol of urea (Brafield and Llewellyn 1982); consequently, each litre of C 0 2 produced by M. lucifugus also indicates the production of 4.28 mmol of urea which must be excreted. One gram of metabolized protein, fat, or carbohydrate will also yield 0.425, 1.08, or 0.556 mL of metabolic water, respectively (Brafield and Llewellyn 1982; Robbins 1983). Based on these standard equivalents and the composition of an insect diet, given earlier, 0.583 mL of metabolic water are produced for each litre of C 0 2 produced by M. lucifugus.

Results We obtained water flux data from 10 pregnant and 14 lactating M. lucifugus (Table 1). Mean body mass was 9.02 0.28 (SE) g during pregnancy and 7.88 f 0.14 g during lactation. Percent body water at injection, measured by ''0 dilution space, was 69.3 0.6 % during pregnancy and 68.5 0.6 % during lactation. Percent body water did not differ between reproductive conditions (t = 0.94; df = 18; p = 0.36). Average water influx was 6.16 f 0.47 mL/day for pregnant females and 6.9 1 0.37 mL/day for lactating M. lucifugus. Water efflux averaged 6.27 f 0.44 and 7.07 f 0.36 mL/day during pregnancy and lactation, respectively. Mass-specific rates are given in Table 1. Water influx (t = 1.27; df = 22; p = 0.22) and efflux (t = 1.42; df = 22; p = 0.17) did not differ significantly between pregnancy and lactation on a whole-animal basis. On a mass-specific basis, however, both influx (t = 2.61; df = 22; p = 0.02) and efflux (t = 2.87; df = 22; p = 0.001) were significantly greater during lactation. For pregnant M. lucifugus, influx and efflux were not significantly different (paired t = 1-48; df = 9; p = 0.17), indicating that the bats were in approximate water balance in the field. During lactation, however, efflux was significantly greater than influx (paired t = 3.01; df = 13; p = 0.01); on average, efflux exceeded influx by 0.16 f 0.05 mL/day . The difference between influx and efflux during lactation is probably related to slight changes in body mass that occurred between injection and recapture. Lactating M. lucifugus lost an average of 0.28 f 0.08 g of body mass between injection and recapture, and the difference between influx and efflux was highly correlated with the changes in body mass (r = 0.97; df = 12; p = 0.0001). Although the observed mass (water) loss during lactation may be caused partially by disturbance, the amounts are quite small, and M. lucifugus normally loses body mass during lactation (Burnett and Kunz 1982). We compared TBW obtained with ''0 dilution and by desiccation, using 42 pregnant M. lucifugus. Body mass of these females averaged 9.30 f 0.16 g . Using ''0 dilution space, we calculated that TBW was 6.41 f 0.13 mL H20 (68.8 f 0.4% of body mass at injection) compared with 6.32 f 0.12 mL (67.9 f 0.3 %) obtained by drying. The difference between the two techniques is small but significant (paired t = 3.26; df = 41 ; p = 0.002). Apparent ''0 dilution space overestimated TBW by 0.09 f 0.03 mL, or 1.4% of TBW obtained by drying; this percent error is similar to values (0.4- 1.6%) previously reported for other vertebrates (Crum et al. 1985; Nagy 1980). The slight error in determining TBW suggests that our measurements of water flux may also be overestimated by 1.4%. Results of the diurnal mass loss measurements are shown in Table 2. If mass loss is equivalent to water loss, then pregnant

+

+

+

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CAN. J. ZOOL. VOL. 67, 1989

TABLE1. Body mass, water flux, and metabolic rate of free-ranging Myotis lucifugus

Reproductive condition

Water flux (mL/day)

Body mass (8)

In

Water flux (mL - kg-' .day-')

Out

In -

Pregnant Lactating

9.02 (0.28) 7.88 (0.14)

6.16 (0.47) 6.91 (0.37)

-

6.27 (0.44) 7.07 (0.36)

-

Out

c02 production &/day)

702 (5 1) 899 (45)

1.22 (0.04) 1.04 (0.06)

~dicted insect consumption @/day)

-

691 (56) 878 (45)

5.5 -

6.7 -


NOTE:Carbon dioxide production was measured simultaneously with water flux (from Kurta et al. 1989). Estimates of insect consumption are those needed to satisfy energy demands, including tissue and milk production (fmm Kurta et al. 1989). Numbers in parentheses indicate standard error.

TABLE2. Mass loss by Myotis lucifugus in the day-roost Reproductive condition Pregnant Lactating

Body mass (g) Morning

Evening

9.47 (0.33) 8.45 (0.14)

8.62 (0.24) 7.10 (0.12)

TABLE3. Daily water budgets for Myotis lucifugus Pregnant

Mean body mass loss (8)

% change in body mass

1.06

-11.2

-

-

1.35

- 16.0

-

-

NOTE:N = 11 for pregnant females in the morning and n = 12 for every other group (total 47). Bats were captured at about 04:30 and at 20:30. Body masses were measured after removal of gut contents. Difference in body mass between morning and evening was attributed to loss of water thmugh evaporation and in the urine and milk. Numbers in parentheses indicate standard error.

M. lucifugus lost 1.06 mL of H 2 0 and lactating females lost 1.35 mL during the day-roosting period. The higher diurnal loss by lactating females agrees with their greater daily water flux as measured by tritium turnover (Table 1). Higher flux during lactation is presumably related to milk export.

Discussion Daily water flux of free-ranging M. lucifugus is quite high, amounting to 100%of total body water during pregnancy and 130%during lactation. Daily flux for free-ranging M. lucifugus is three to five times greater than that reported for captive nonreproductive M. lucifugus (Coutts et al. 1973; O'Farrell et al. 197 1). To date, water turnover has been measured in only two other species of free-ranging bats, neither of which was pregnant or lactating. The 13-g insectivorous Macrotus californicus has a mean flux of about 200 mL .kg-' day-' (Bell et al. 1986), and the 12-g nectarivorous Anoura caudifer has a water turnover of 1 165 mL .kg-' . day-' (Helversen and Reyer 1984). Averaging our influx and efflux rates for M. lucifugus (Table 1) yields 696 and 888 mL .kg-' day-' during pregnancy and lactation, respectively. The extremely high flux reported for A. caudifer is probably related to the high water content of its nectar diet. The much lower values found in M. californicus may reflect adaptations to desert conditions (see Bell et al. 1986). Water influx Total water influx was 6.16 mL/day during pregnancy and 6.91 mL/day during lactation (Table 1). Pregnant M. lucifigus consume 5.5 g of insects per day on average, whereas lactating females ingest 6.7 g (Table 1; Kurta et al. 1989). If insects are 70%water, then preformed water intake is 3.85 and 4.69 mL/ day during pregnancy and lactation, respectively (Table 3).

Water influx Preformed Metabolic Drinking Total Water efflux Urinary Fecal Milk Evaporative Total -

Lactating

mL/day

%

mL/day

%

3.85 0.71 1.60 6.16

62.5 11.5 26.0 100.0

4.69 0.60 1.62 6.91

67.9 8.7 23.4 100.0

2.91 0.58

46.4 9.3

2.78 6.27

44.3 100.0

2.47 0.74 1.85 2.01 7.07

34.9 10.5 26.2 28.4 100.0

-

-

-

-

-

NOTE:See text for calculation details.

Average C 0 2 production by these free-ranging bats is 1.22 L/ day during pregnancy and 1.04L/day during lactation (Table 1 ; Kurta et al. 1989). If 0.583 mL of metabolic water is produced for every litre of C 0 2 (see Methods), then pregnant M. lucifugus gain 0.71 mL/day from metabolic water and lactating females 0.60 mL/day (Table 3). Metabolic water production by pregnant M. lucifugus slightly exceeds that of lactating females, despite the latter's greater insect consumption (Table l), because much of the additional food intake by lactating M. lucifugus is exported as milk and not metabolized to C 0 2 and water (Kurta et al. 1989). Assuming preformed, metabolic, and drinking water are the only major sources of input, we then estimated the amount of drinking water by subtraction. Pregnant M. lucifugus drank 1.60 mL/day and lactating females, 1.62 mL/day; these amounts are equivalent to 26.0 and 23.4% of total influx during pregnancy and lactation, respectively (Table 3). Water eflux Water efflux values were 6.27 and 7.07 mL/day for pregnant and lactating bats, respectively (Table I). The major routes of water loss are through the urine and feces, pulmocutaneous evaporation, and milk export. For simplicity we ignored the small amount of water associated with changes in body mass between injection and recapture. Based on the composition of an insect diet and data from the literature, we made reasonable estimates of urinary, fecal, and milk losses and then calculated daily evaporative water loss (EWL) by subtraction. Carbon dioxide production by free-ranging M. lucifugus is shown in Table 1 . If 0.75 g of protein is metabolized for every

KURTA ET AL.

247 1

assistance: A. Brooke, C. Diaz, B. Flint, M. Gruchacz, K. Klinghammer, and A. Rodriguez-Duran. We are grateful to D. Amos, F. Carr, B. T. Hunter, G. Niemela, and J. Twitchell, and to the Town of Harrisville, New Hampshire, for allowing access to bat colonies under their care. J. E. Bassett provided constructive criticism. Boston University's Sargent Camp provided accommodations and logistical support. This study was funded by National Science Foundation grant BSR8314821 to T.H.K. and K.A.N., and by a contract (DE-AC0376-5F00012) between the Ecological Research Division of the U.S. Department of Energy and the University of California (K.A.N.).

Acknowledgments The following people provided field or laboratory

KUNZ,T. H., and KURTA, A. 1988. Capture methods and holding devices. In Ecological and behavioral methods for the study of


litre of C 0 2 produced (see Methods), then pregnant M. lucifigus metabolize 0.92 g proteinlday, on average, whereas lactating females metabolize 0.78 g proteinlday. One gram of metabolized protein typically yields 5.7 mmol of urea (Brafield and Llewellyn 1982). Based on field measurements of M. lucifigus in New Mexico (Geluso and Studier 1979), we assumed that average urine concentration of M. lucifigus in New England was 2400 mosmol1L. If 75 % of total osmolarity is attributable to urea (Carpenter 1969; Vogel and Vogel 1972), then M. lucifigus needs 2.9 1 and 2.47 mL H20/day for urinary purposes during pregnancy and lactation, respectively (Table 3). These amounts are probably conservative because the urine concentration of free-ranging M. lucifigus in arid New Mexico may be greater than that of M. lucifigus in New England (Bassett 1982). Myotis lucifigus produces 0.07 g of dry feces for every gram of ingested insects (see Methods). If insectivorous bat feces are 60% water (Bassett and Studier 1988; Rumage 1979), then fecal water losses are 0.58 and 0.74 mL1day during pregnancy and lactation, respectively (Table 3). On average, lactating M. lucifigus export 1.85 mL H20/day in milk (Kunz et al. 1983; Kurta et al. 1989). By subtraction, we calculated that EWL equals 2.78 mL1day during pregnancy and 2.01 mL1day during lactation (Table 3). Evaporative losses represent 28 -44 % of total water efflux and are comparable to urinary losses (Table 3). Based on laboratory observations of M. lucifigus, Bassett (1980) suggested that as much as 90% of total water efflux was evaporative in nature. However, urine production should be much higher in the field than in the laboratory because of the greater food (protein) intake of free-ranging bats (Kurta et al. 1989). In addition, EWL should be much lower in the field because of water-conserving behaviors such as clustering and the use of enclosed roost sites; in the laboratory, bats are generally caged singly and have no opportunity to select an optimal microclimate (Bassett 1980; J. E. Bassett , personal communication). Although the day-roosting period for M. lucifigus represents about 65% (15 - 16 h) of the bat's daily time budget (Kurta et al. 1989), day-roosting water losses are only 15 - 19% of daily water efflux (Table 2). Greater water losses during the 8-h night are probably related to two main factors. First, EWL during foraging flight is much greater than when at rest (e.g., Carpenter 1969), and M. lucifigus averages about 4 h of flight each night (Kurta et al. 1989). In addition, most digestive activity and, hence, urinary and fecal losses, probably take place at night. Almost two-thirds of the prey captured by M. lucifigus each night is consumed in the postsunset foraging period (Anthony and Kunz 1977). Myotis lucifigus begins to void feces within 35 min of ingesting prey (Buchler 1975), and urine flow increases markedly after a meal (Bassett and Wiebers 1979). Bassett's (1980) laboratory measurements suggest that EWL alone over a 16-h day-roosting period would be at least 1.O1 mL; this approximates the combined evaporative and urinary losses actually observed in pregnant M. lucifigus in the field (1.06 mL, Table 2). Again, much of the difference between our field observations and the laboratory measurements of Bassett (1980) may be related to free-ranging bats' ability to cluster and to select a favorable microclimate, thereby reducing EWL.

ALTMAN, P. L., and DITTMER, D. S. 1968. Metabolism. Federation of American Societies for Experimental Biology, Bethesda, MD. ANTHONY, E. L. P., and KUNZ,T. H. 1977. Feeding strategies of the little brown bat, Myotis lucifigus, in southern New Hampshire. Ecology, 58: 775 -786. BARBOUR, R. W., and DAVIS,W. H. 1969. Bats of America. University Press of Kentucky, Lexington. J. E. 1980. Control of postprandial water loss in Myotis BASSETT, lucifigus lucifigus. Comp. Biochem. Physiol. A, 65: 497 -500. 1982. Habitat aridity and intraspecific differences in the urine concentrating ability of insectivorous bats. Comp. Biochem. Physiol. A, 72: 703 -708. BASSETT, J. E., and STUDIER, E. H. 1988. Methods for determining water balance in bats. In Ecological and behavioral methods for the study of bats. Edited by T. H. Kunz. Smithsonian Institution Press, Washington, DC. pp. 373 - 386. BASSETT, J. E., and WIEBERS, J. E. 1979. Urine concentration dynamics in the post-prandial and fasting Myotis lucifigus lucifigus. Comp. Biochem. Physiol. A, 64: 373 -379. BELL,G. P., BARTHOLOMEW, G. A., and NAGY,K. A. 1986. The role of energetics, water economy, foraging behavior, and geothermal refugia in the distribution of the bat, Macrotus califomicus. J. Comp. Physiol. B, 156: 44.1 -450. BRAFIELD, A. E., and LLEWELLYN, M. J. 1982. Animal energetics. Blackie, London. BUCHLER, E. R. 1975. Food transit time in Myotis lucifigus (Chiroptera: Vespertilionidae). J . Mammal. 56: 252 -253. BURNETT, C. D., and KUNZ,T. H. 1982. Growth rates and age estimation in Eptesicus fiscus and comparison with Myotis lucifigus. J. Mammal. 63: 33-41. CARPENTER, R. E. 1969. Structure and function of the kidney and the water balance of desert bats. Physiol. Zool. 42: 288 -302. 1986. Flight physiology of intermediate-sized fruit bats (Pteropodidae). J . Exp. Biol . 120: 79 - 103. CHEW,R. M. 1965. Water metabolism in mammals. In Physiological marnrnalogy. Edited by V. H. Mayer and R. G. Van Gelder. Academic Press, New York. pp. 44- 170. COUTTS, R. A., FENTON, M. B., and GLEN,E. 1973. Food intake by captive Myotis lucifigus and Eptesicusfiscus (Chiroptera: Vespertilionidae). J. Mammal. 54: 985 -990. CRUM,B. G., WILLIAMS, J. B., and NAGY,K. A. 1985. Can tritiated water-dilution space accurately predict total body water in chukar partridges? J. Appl. Physiol. 59: 1383 - 1388. FENTON, M. B., and BARCLAY, R. M. R. 1980. Myotis lucifigus. Mamm. Species, 142: 1 -8. GELUSO, K. N. 1978. Urine concentrating ability and renal structure of insectivorous bats. J. Mammal. 59: 3 12 -323. GELUSO,K. N., and STUDIER, E. H. 1979. Diurnal fluctuation in urine concentration in the little brown bat, Myotis lucifigus, in a natural roost. Comp. Biochem. Physiol. A, 62: 471 -473. HELVERSEN, 0 . v., and REYER,H.-U. 1984. Nectar intake and energy expenditure in a flower visiting bat. Oecologia, 63: 178 - 184.


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bats. Edited by T. H. Kunz. Smithsonian Institution Press, Washington, DC. pp. 1 -24. KUNZ,T. H., and NAGY,K. A. 1988. Methods for energy budget analysis. In Ecological and behavioral methods for the study of bats. Edited by T. H. Kunz. Srnithsonian Institution Press, Washington, DC. pp. 277 - 302. KUNZ,T. H., STACK,M. H., and JENNESS, R. 1983. A comparison of milk composition in Myotis lucifugus and Eptesicus fuscus (Chiroptera: Vespertilionidae) . Biol . Reprod. 28: 229 -234. KURTA,A,, BELL, G. P., NAGY,K. A., and KUNZ,T. H. 1989. Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Phy siol . Zool . 62 : 804 - 8 1 8. LIFSON,N., and MCCLINTOCK, R. 1966. Theory and use of the turnover rates of body water for measuring energy and material balance. J. Theor. Biol. 12: 46-74. MACFARLANE, W. V., and HOWARD,B. 1972. Comparative water and energy economy of wild and domestic animals. Symp. Zool. Soc. (London), 31: 26 1 -296. MACMILLEN,R. R. 1972. Water economy of nocturnal desert rodents. Symp. Zool. Soc. (London), 31: 147 - 174. NAGY,K. A. 1975. Water and energy budgets of free-living animals: measurement using isotopically labeled water. In Environmental physiology of desert organisms. Edited by N. F. Hadley . Dowden, Hutchinson & Ross, Inc., Stroudsberg, PA. pp. 227 -245. 1980. COz production in animals: analysis of potential errors in the doubly labeled water method. Am. J. Physiol. 238: R454 -R465.

1983. The doubly labeled water (3HH180)method: a guide to its use. University of California at Los Angeles, Publ. No. 12- 1417. 1987. Field metabolic rate and food requirement scaling in mammals and birds. Ecol. Monogr. 57: 1 1 1 - 127. NAGY,K. A., and COSTA,D. P. 1980. Water flux in animals: analysis of potential errors in the tritiated water method. Am. J . Phy siol . 238: R466 -R473. O'FARRELL,M. J., STUDIER,E. H., and EWING,W. G. 1971. Energy utilization and water requirements of captive Myotis thysanodes and Myotis lucifugus (Chiroptera). Comp. Biochem. Physiol. A, 39: 549-552. ROBBINS,C. T. 1983. Wildlife feeding and nutrition. Academic Press, New York. RUMAGE, W. T., 111. 1979. Seasonal changes in dispersal pattern and energy intake of Myotis lucifugus. M .A. thesis, Boston University, Boston. r Konzentrationism der VOGEL,V., and VOGEL,W. 1972. ~ b e das Nieren zweier Fledermausarten (Rhinopoma hardwickei und Rhinolophusferrumequinum) mit unterschliedlich langer Nierenpapille. Z. Vgl. Physiol. 76: 358-371. WOOD,R. A., NAGY,K. A., MACDONALD, N. A., WAKAKUWA, R. J., and KAAZ,H. 1975. Determination of S. T., BECKMAN, oxygen- 2 8 in water contained in biological samples by charged particle activation. Anal. Chem. 47: 646 -650.


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