Seasonal daily, daytime and night-time field metabolic rates in Arabian babblers (Turdoides squamiceps)
1 Department of Life Sciences, Ben-Gurion University of the Negev,
Beer-Sheva 84105, Israel
2 Desert Animal Adaptations and Husbandry, Wyler Department of Dryland
Agriculture, Jacob Blaustein Institute for Desert Research, Ben-Gurion
University of the Negev, Beer-Sheva 84105, Israel
3 Department of Zoology, George S. Wise Faculty of Life Sciences, Tel-Aviv
University, Tel-Aviv 69978, Israel
* Author for correspondence (e-mail: degen{at}bgumail.bgu.ac.il)
Accepted 14 August 2002
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Summary |
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Daily and daytime energy expenditure rates were higher during the breeding season than during either summer or winter, but there was no difference among seasons in night-time energy expenditure rates. Thus, our hypothesis was supported. The daytime field metabolic rates in summer and winter nonbreeding babblers were 3.92x and 4.32x the resting metabolic rate (RMR), respectively, and in breeding babblers was 5.04x RMR, whereas the night-time field metabolic rates ranged between 1.26x RMR and 1.35x RMR in the three seasons. Daily and daytime water-influx rates were highest in winter, intermediate during the breeding season and lowest in summer, but there was no difference among seasons in night-time water-influx rate. Daytime water-influx rate was greater than night-time water-influx rate by 2.5-fold in summer, 3.9-fold in the breeding season and 6.75-fold in winter.
Seasonal patterns of daily and daytime energy expenditure were similar, as were seasonal patterns of daily and daytime water influx. Daily and daytime energy expenditure and water-influx rates differed among seasons whereas night-time rates of both did not. Daily and daytime field metabolic rates of babblers were highest during the breeding season, whereas daily and daytime water-influx rates were highest in winter.
Key words: Arabian babbler, Turdoides squamiceps, doubly labelled water, daily field metabolic rate, daytime field metabolic rate, night-time field metabolic rate, water-influx rate
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Introduction |
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Dietary selection and food intake influence metabolic rates
(McNab, 1988). Some small
birds have to forage during the day in order to accumulate sufficient body
energy reserves to survive the night
(King, 1972
;
Chaplin, 1974
;
Blem, 1976
). Consequently,
overnight energy demands of birds are important in assessing their ability to
survive. Most previous studies monitored changes in body mass and used them as
an indication of energy use (Webster,
1989
; Chan, 1994
).
In some studies, time activity budgets were used to calculate time energy
budgets, and basal or resting metabolic rates were assumed for night roosting
(Carmi-Winkler et al.,
1987
).
In the present study, we determined the daily, daytime and night-time
metabolic rates of free-living Arabian babblers (Turdoides squamiceps
Cretzsch; Timaliidae; adult body mass=65-85 g) in summer and winter in
nonbreeding adults and in spring in breeding adults. The Arabian babbler
inhabits the Arava, part of the Great Rift, an extreme desert of Israel
(Zahavi, 1990). This diurnal
bird lives in groups of mixed sex, is terrestrial and is active throughout the
day (Wright et al., 2001
). It
is an omnivore that eats invertebrates and fruits and, at least at our study
site, appears not to drink (Anava et al.,
2000
). In earlier studies, we found no difference in the daily
field metabolic rate of nonbreeding babblers during winter and summer
(Anava et al., 2000
), but
breeding babblers had higher daily metabolic rates than nonbreeding babblers
(Anava et al., 2001a
). We
hypothesized that the daytime metabolic rate of breeding babblers would be
higher than the summer and winter daytime metabolic rates of nonbreeding
babblers, but that the night-time metabolic rate would be similar in the
breeding, summer and winter seasons.
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Materials and methods |
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The study was carried out during 1997. There were approximately 13 h light
and 11 h dark in summer, 11 h light and 13 h dark in winter and 12 h light and
12 h dark in spring (breeding period). There is a period of 10-20 min of dim
light at sunrise and at sunset. The groups of babblers at the reserve have
been observed continually for over 30 years
(Zahavi, 1990;
Wright et al., 2001
) and there
were more than 20 groups on the site at the time of the study. The legs of all
babblers were colour banded, which allowed for quick individual
identification. The birds foraged on their own in the wild; however, they were
accustomed to the presence of observers within 2-3 m without showing signs of
fear.
Doubly labelled water measurements
Measurements of field metabolic rate and water influx in Arabian babblers
were made for nonbreeding adults in winter (JanuaryFebruary) and summer
(JulyAugust) and for breeding adults in spring (MarchMay).
Tritiated-water space measurements (as an estimate of total body water volume)
were made concomitantly but not on the same individuals that were used for
doubly labelled water measurements. In each season, 12 adult babblers (six
males and six females) were captured using traps in which the doors were
triggered shut when the birds walked in; mealworms were used as bait. For
tritiated-water space measurements, the birds were weighed and then a 100-200
µl blood sample was taken by pricking the basilic vein, located on the
ventral surface of the wing, and collecting blood with microhematocrit tubes.
These samples were used to measure background radioactivity levels. Each bird
was then injected intramuscularly with 0.5 ml of sterile isotonic avian saline
containing 1.85 MBq of tritium. The birds were kept without food or water for
45-60 min to allow for equilibration of the isotope with body fluids
(Degen et al., 1981), after
which time they were weighed again and another 100-200 µl blood sample was
collected. The mean of the two weighings was used in subsequent calculations.
Blood samples were refrigerated and then micro-distilled to dryness to obtain
pure water (Wood et al.,
1975
). The specific activity of tritium was determined in
duplicate samples by liquid scintillation spectrometry (Kontron; Munchenstein,
Switzerland) in which each sample contained 20 µl of distillate in 5 ml
scintillation fluid (Amersham, UK). Samples were counted for 10 min, and
counts were corrected for quenching using a series of quenched standards.
Tritiated water space was estimated from the dilution of tritium in the body
fluids (Nagy and Costa, 1980
;
Degen et al., 1981
).
We developed a technique in which doubly labelled water measurements were
made without touching the babblers (Anava
et al., 2000). Birds were trained to walk onto a large platform
balance (Moznei-Shekel, Kibbutz Keshet, Israel; model B-2-P, 104; -0.2 g), at
which time they were weighed. Furthermore, isotopes were delivered to birds in
a unique manner. 50 µl water containing 95 atoms % 18O (Yeda,
Rehovot, Israel) and 4.625 MBq tritium (Nuclear Research Centre, Negev,
Beer-Sheva, Israel) was injected into a cricket. The cricket was then fed to a
babbler at between 09:00 h and 11:00 h, and the isotopes were allowed to
equilibrate with body water, which usually occurred within an hour
(Degen et al., 1981
). The
following morning, the babblers were observed, weighed and a fresh excreta
sample from each babbler was collected from the ground into a glass vial
immediately after the sample was excreted. Samples were also collected that
evening and the following morning, at which time the birds were weighed.
Excreta samples were refrigerated and then micro-distilled under vacuum
until dryness (Wood et al.,
1975) to obtain pure water. Tritium levels were determined as
above, except that 50 µl (rather than 20 µl) of distillate was analysed.
Levels of 18O specific activity were measured in triplicate by an
autogamma counting system (Packard, Downers Grove, IL, USA) after converting
18O to
-emitting 18F by cyclotron-generated
proton activation (Wood et al.,
1975
). Excreta samples from three non-injected birds were treated
similarly to measure background levels of 18O and tritium.
Water fluxes were calculated from the decline in specific activity of
tritium over time (Nagy and Costa,
1980; Degen et al.,
1981
; Degen,
1997
), and rates of CO2 production were estimated from
the decline in specific activity of tritium and 18O over time
(Lifson and McClintock, 1966
;
Nagy, 1980
). For calculation
of water flux, we used equation 2 of Nagy
(1980
), which assumes that
total body water changes linearly over the time of measurement. These
calculations require knowledge of the total body water volume of the animal.
For this, we used the mean value determined from the tritiated-water space
measurements for each sex and within each season. The excreta samples were
collected within 30 min of the babblers descending from the tree to start
daytime activity and 30 min before they ascended the tree for roosting. The
two morning samples allowed calculations of daily rates. The morning and
evening samples allowed calculations of daytime rates, as both samples were
taken during daytime activity. Total daytime rates were then calculated by
multiplying hourly rates by the hours of daytime activity. The
night-to-morning fluid samples included daytime activity at both ends and thus
would overestimate night-time rates. As a result, total night-time rates were
calculated as the total daily rate minus the total daytime rate.
CO2 production rate was converted to energy expenditure by assuming
that 25.7 J of heat energy are produced for each ml of CO2
(Anava et al., 2000
).
For comparisons of field metabolic rate and water-influx rate among seasons, we used a two-way analysis of covariance (ANCOVA) using body mass as a covariate factor. We accepted P<0.05 as the minimum level for significance. Values are presented as means ± S.E.M.
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Results |
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Daily and daytime energy expenditure rates during the breeding season were significantly higher than during either summer or winter, but there was no difference in night-time energy expenditure rate among seasons. Daytime energy expenditure rate was significantly greater than night-time energy expenditure rate: by 3.04-fold in summer, 3.43-fold in winter and 3.74-fold in the breeding season (Table 1).
Daily and daytime water-influx rates were highest in winter, intermediate during the breeding season and lowest in summer, but there was no difference in night-time water-influx rates among seasons. Daytime water-influx rate was significantly greater than the night-time rate: by 2.5-fold in summer, 3.9-fold in the breeding season and 6.75-fold in winter (Table 2).
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Discussion |
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The doubly labelled water method follows the decline over time in
concentrations of oxygen and hydrogen isotopes after introducing the isotopes
into an animal and allowing them to equilibrate with body fluids. The rate of
decline of the hydrogen isotope estimates water flux, and the difference in
decline of isotope concentrations is used to estimate CO2
production rate (Lifson and McClintock,
1966; Kam and Degen,
1997a
).
Fluid samples are required to measure the rate of decline of the isotopes;
blood, urine, faeces, saliva and respiratory water have been used. All have
proven to provide reliable and similar results. For example, following the
administration of tritium in humans, the specific activity of water obtained
from either urine or sweat was the same as that of body water
(Pinson and Langham, 1957).
Urine and blood were used in small mammals
(Lifson et al., 1975
), and
urine and saliva were used in humans, with accurate results
(Schoeller and van Santen,
1982
). Calculations of CO2 production rates using
doubly labelled water gave similar results regardless of whether fluid was
taken from blood or faeces in reindeer (Rangifer tarandus tarandus)
(Gotaas et al., 1997
).
Furthermore, faecal samples collected off the ground were used to measure
water flux in free-living blesbok (Damaliscus dorcas phillipsi) and
impala (Aepyceros melampus melampus)
(Fairall and Klein, 1984
;
Klein and Fairall, 1986
).
In general, the weighing of animals and collection of fluid samples for
doubly labelled water measurements entail their capture, placing them in bags
and pricking their blood vessels for blood samples. However, these procedures
can stress the animals and affect measurements of energy expenditure. The
present study eliminated these stressful procedures. The method was tested on
two babblers in the laboratory. Daily energy expenditure and water influx
measured by the doubly labelled water method described above, were, on
average, 4.0% and 4.6% higher, respectively, than the values obtained by the
balance method (Anava, 1998).
These differences in methods were acceptable and similar to others reported in
validation studies for avian species
(Nagy, 1980
;
Williams, 1985
;
Speakman and Racey, 1988
),
indicating that the method could be used to estimate metabolic rate and water
flux in free-living birds. Furthermore, the delivery of isotopes orally and
the use of urine for fluid samples, as adapted in this study, gave accurate
results of energy expenditure in humans
(Schoeller and van Santen,
1982
).
Field metabolic rate and water influx
The daily energy expenditure of nonbreeding Arabian babblers in winter,
124.7 kJ day-1, and in summer, 127.0 kJ day-1, were
similar, but daily energy expenditure of breeding babblers, 150.1 kJ
day-1 for a 72.5 g babbler, was significantly greater than the
expenditure of nonbreeding adults. This is in agreement with a number of
studies that have shown that the breeding season is the most costly in terms
of energy expenditure in avian species
(Tatner, 1990;
Tinbergen and Dietz, 1994
).
However, the daily energy costs of the breeding babblers were relatively low
when compared with other breeding passerines. Allometric equations of Masman
et al. (1989
) and Nagy
(1987
) predict that a 72.5 g
breeding passerine bird should expend 219.9 kJ day-1 and 195.9 kJ
day-1, respectively. In the present study, energy expenditure of
breeding Arabian babblers was 68-77% of these values.
The resting metabolic rate (RMR) of Arabian babblers was reported as 26.9 J
g-1 h-1 (Anava et
al., 2001b), which, when compared with the phylogenetically
adjusted equation for basal metabolic rate (BMR) in birds, is only 73% of the
value predicted for a bird of its body mass (Reynolds and Lee, 1966;
Williams, 1999
). Using this
RMR value, the daily field metabolic rate of Arabian babblers ranged between
2.70x RMR in nonbreeding adults and 3.22x RMR in breeding adults.
As BMR is lower than RMR (Degen,
1997
), field metabolic rates as a multiple of BMR would be higher
than as a multiple of RMR. It is likely, therefore, that for breeding birds it
would fall somewhere between the predicted values of 3.2x BMR
(Daan et al., 1991
) and
4.0x BMR (Drent and Daan,
1980
).
Night-time field metabolic rates per hour were similar between breeding and
nonbreeding babblers, which supported our hypothesis, and ranged between
1.26x RMR and 1.35x RMR. Tinbergen and Dietz
(1994) found that night-time
field metabolic rate in the 17.7 g breeding great tit (Parus major)
was 1.9x BMR. BMR is slighly lower than RMR, and therefore the ratio to
BMR would be slightly lower than the ratio to RMR but, most likely, still
higher than that for breeding Arabian babblers. The night-time field metabolic
rate was 47% of the daily field metabolic rate for nonbreeding babblers in
both summer and winter. The value during the breeding season was 42%, which
was lower than the 62% reported for breeding great tits
(Tinbergen and Dietz, 1994
).
Thus, the energy expended at night-time, as a percentage of total daily energy
expenditure, was greater in the great tit than in the Arabian babblers.
Daytime field metabolic rate was greater in breeding than nonbreeding
babblers, which also supports our hypothesis. The daytime field metabolic rate
in nonbreeding summer and winter babblers was 3.92x RMR and 4.32x
RMR, respectively, and in breeding babblers was 5.04x RMR. Furthermore,
daytime field metabolic rates were approximately 3.20x night-time field
metabolic rates in nonbreeding babblers and 3.74x night-time field
metabolic rates in breeding babblers.
Patterns of seasonal daily and daytime water-influx rates of the babblers
differ from those of daily energy expenditure. Water-influx rate was highest
in winter, intermediate during breeding and lowest in summer. These
differences in water influx were associated mainly with preformed water of the
diet and not energy intake, as the birds shifted diets among seasons. In
winter, babblers consume more fruit and less insects than in summer
(Anava et al., 2000). A higher
water influx in avian species during winter than in summer owing to a dietary
shift was also reported in Negev desert chukars (Alectoris chukar)
and sand partridges (Ammoperdix heyi)
(Alkon et al., 1985
;
Kam et al., 1987
). The
night-time water-influx rate was similar between breeding and nonbreeding
babblers, approximately 0.0070 ml g-1 h-1, and ranged
between 27% and 55% of the daily water-influx rate in nonbreeding winter and
summer babblers, respectively. The water-influx rate during the daytime was
higher than the night-time rate by 2.48x in summer, 3.92x in the
breeding season and 6.75x in winter.
In summary, seasonal patterns of daily and daytime energy expenditure were similar, as were seasonal patterns of daily and daytime water influx. Daily and daytime energy expenditure and water-influx rates differed among seasons, whereas night-time rates of both did not. Daily and daytime field metabolic rates of babblers were highest during the breeding season, whereas daily and daytime water-influx rates were highest in winter.
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Acknowledgments |
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References |
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---|
Alkon, P. U., Degen, A. A., Pinshow, B. and Shaw, P. J. (1985). Phenology, diet, and water turnover rates of Negev desert chukars. J. Arid Environ. 9, 51-61.
Anava, A. (1998). Seasonal water and energy fluxes in Arabian babblers (Turdoides squamiceps), a passerine that inhabits extreme deserts. PhD thesis. Ben-Gurion University of the Negev, Beer Sheva, Israel.
Anava, A., Kam, M., Shkolnik, A. and Degen, A. A. (2000). Seasonal field metabolic rate and dietary intake in Arabian babblers (Turdoides squamiceps) inhabiting extreme deserts. Funct. Ecol. 14,607 -613.
Anava, A., Kam, M., Shkolnik, A. and Degen, A. A. (2001a). Effect of group size on field metabolic rate of Arabian babblers provisioning nestlings. Condor 103,376 -380.
Anava, A., Kam, M., Shkolnik, A. and Degen, A. A. (2001b). Heat production and body temperature of Arabian babblers (Turdoides squamiceps): a bird from hot desert habitats. J. Arid Environ. 48,59 -67.
Blem, C. R. (1976). Patterns of lipid storage and utilization in birds. Am. Zool. 16,671 -684.
Bryant, D. M. (1988). Energy expenditure and body mass changes as measures of reproductive costs in birds. Funct. Ecol. 2,23 -34.
Carmi-Winkler, N., Degen, A. A. and Pinshow, B. (1987). Seasonal time-energy budgets of free-living chukars in the Negev Desert. Condor 89,594 -601.
Chan, K. (1994). Winter body mass and overnight energetics of a south temperate passerine. Auk 111,721 -723.
Chaplin, S. B. (1974). Daily energetics of the black-capped chickadee, Parus atricapillus, in winter. J. Comp. Physiol. 89,321 -330.
Daan, S., Masman, D., Dijkstra, C. and Kenagy, G. J. (1991). Daily energy turnover during reproduction in birds and mammals: its relationship to basal metabolic rate. Proc. Int. Ornithol. Cong. 20,1976 -1988.
Degen, A. A. (1997). Ecophysiology of Small Desert Mammals. Berlin: Springer-Verlag.
Degen, A. A., Pinshow, B., Alkon, P. U. and Arnon, H.
(1981). Tritiated water for estimating total body water and water
turnover rate in birds. J. Appl. Physiol.
51,1183
-1188.
Drent, R. H. and Daan, S. (1980). The prudent parent: energetic adjustments in avian breeding. Ardea 68,225 -252.
Fairall, N. and Klein, D. R. (1984). Protein intake and water turnover: a comparison of two equivalently sized African antelope the blesbok Damaliscus dorcas and impala Aepyceros melampus. Can. J. Anim. Sci. 64 (Suppl.),212 -214.
Gotaas, G., Milne, E., Haggarty, P. and Tyler, N. J. C.
(1997). Use of feces to estimate isotopic abundance in doubly
labeled water studies in reindeer in summer and winter. Am. J.
Physiol. 273,R1451
-R1456.
Kam, M. and Degen, A. A. (1997a). Energy budget
in free-living animals: a novel approach based on the doubly labeled water
method. Am. J. Physiol.
272,R1336
-R1343.
Kam, M. and Degen, A. A. (1997b). Energy requirements and the efficiency of utilization of metabolizable energy in free-living animals: evaluation of existing theories and generation of a new model. J. Theor. Biol. 184,101 -104.
Kam, M., Degen, A. A. and Nagy, K. A. (1987). Seasonal energy, water and food consumption of Negev chukars and sand partridges. Ecology 68,1029 -1037.
King, J. R. (1972). Adaptive periodic fat storage by birds. Proc. Int. Ornithol. Cong. 15,200 -217.
Klein, D. R. and Fairall, N. (1986). Comparative foraging behaviour and associated energetics of impala and blesbok. J. Appl. Ecol. 23,489 -502.
Lifson, N., Little, W. S., Levitt, D. G. and Henderson, R.
M. (1975). D218O method for
CO2 output in small mammals and economic feasibility in man.
J. Appl. Physiol. 39,657
-664.
Lifson, N. and McClintock, R. (1966). Theory of use of the turnover rates of body water for measuring energy and material balance. J. Theor. Biol. 180,803 -811.
Masman, D., Dijkstra, C., Daan, S. and Bult, A. (1989). Energetic limitation of avian parental effort: field experiments in the kestrel. J. Evol. Biol. 2, 435-455.
McNab, B. K. (1988). Food habits and the basal rate of metabolism in birds. Oecologia 77,343 -349.
Nagy, K. A. (1980). CO2 production
in animals: analysis of potential errors in the doubly labeled water method.
Am. J. Physiol. 238,R466
-R473.
Nagy, K. A. (1987). Field metabolic rate and food requirement scaling in mammals and birds. Ecol. Monogr. 57,111 -128.
Nagy, K. A. and Costa, D. P. (1980). Water flux
in animals: analysis of potential errors in the tritiated water method.
Am. J. Physiol. 238,R454
-R465.
Pinson, E. A. and Langham, W. H. (1957).
Physiology and toxicology of tritium in man. J. Appl.
Physiol. 10,108
-126.
Reynolds, P. and Lee, R., III (1996). Phylogenetic analysis of avian energetics: passerines and nonpasserines do not differ. Am. Nat. 147,735 -759.
Rozin, P. (1976). The selection of foods by rats, humans, and other animals. Adv. Study Behav. 6, 21-76.
Schoeller, D. A. and van Santen, E. (1982).
Measurement of energy expenditure in humans by doubly labeled water method.
J. Appl. Physiol. 53,955
-959.
Speakman, J. R. (1997). Doubly Labelled Water. London: Chapman & Hall.
Speakman, J. R. and Racey, P. A. (1988). Validation of the doubly labelled water technique for measurement of energy expenditure in insectivorous bats. Physiol. Zool. 61,514 -527.
Speakman, J. R., Racey, P. A. and Burnett, A. M. (1991). Metabolic and behavioral consequences of the procedures of the doubly labelled water technique on white (MFI) mice. J. Exp. Biol. 157,123 -132.[Abstract]
Stern, E., Gradus, Y., Meir, A., Krakover, S. and Tsoar, H. (1986). Atlas of the Negev. Jerusalem: Keterpress Enterprises.
Tatner, P. (1990). Energetic demands during brood rearing in the wheatear Oenanthe oenanthe. Ibis 132,423 -435.
Tinbergen, J. M. and Dietz, M. W. (1994). Parental energy expenditure during brood rearing in the great tit (Parus major) in relation to body mass, temperature, food availability and clutch size. Funct. Ecol. 8, 563-572.
UNESCO (1977). MAB, Technical Note 7 In Map of the World Distribution of Arid Lands, pp.1 -7. Paris: UNESCO.
Webster, M. D. (1989). Overnight mass loss by wintering verdins. Condor 91,983 -985.
Williams, J. B. (1985). Validation of the doubly labeled water technique for measuring energy metabolism in starlings and sparrows. Comp. Biochem. Physiol. 80A,349 -353.
Williams, J. B. (1999). Heat production and evaporative water loss of dune larks from the Namib Desert. Condor 101,432 -438.
Wood, R. A., Nagy, K. A., MacDonald, N. S., Wakakua, S. I., Beckman, R. J. and Kaaz, H. (1975). Determination of oxygen-18 in water contained in biological samples by charged activation. Analyt. Chem. 47,646 -650.[Medline]
Wright, J., Berg, E., de Kort, S. R., Khazin, V. and Maklakov, A. A. (2001). Cooperative sentinel behaviour in the Arabian babbler. Anim. Behav. 62,973 -979.
Zahavi, A. (1990). Arabian babblers: The quest for social status in a cooperative breeder. In Cooperative Breeding in Birds (ed. P. B. Stacy and W. D. Koenig), pp.105 -130. Cambridge: Cambridge University Press.
Zurowski, K. L. and Brigham, R. M. (1994). Does use of doubly labeled water in metabolic studies alter activity levels of common poorwills. Wilson Bull. 106,412 -415.