Heterothermy and the water economy of free-living Arabian oryx (Oryx leucoryx)
1 National Wildlife Research Center, PO Box 1086, Taif, Saudi
Arabia
2 Department of Evolution, Ecology and Organismal Biology, Ohio State
University, 1735 Neil Avenue, Columbus, OH 43210, USA
* Author for correspondence (e-mail: ostrowski{at}nwrc-sa.org)
Accepted 31 January 2003
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Summary |
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Key words: Arabian oryx, desert, heterothermy, Oryx leucoryx, thermoregulation, water saving
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Introduction |
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Diurnal variation in Tb has been reported in a number
of large ruminants, including the dromedary camel (Camelus
dromedarius), Grant's gazelle (Gazella granti), Thomson's
gazelle (Gazella thomsonii), fringe-eared oryx (Oryx beisa
callotis) and Cape eland (Taurotragus oryx)
(Schmidt-Nielsen et al., 1957;
Taylor and Lyman, 1967
;
Taylor, 1969
,
1970
), but these studies were
also done on captive animals, so our knowledge about use of heterothermy and
its physiological significance among free-living ungulates remains limited
(Parker and Robbins, 1985
). In
these studies, fluctuations in Tb were often as much as
47°C when captive ungulates were deprived of drinking water but
only 12°C when hydrated, suggesting that hydration state influences
the use of heterothermy.
Because measurements of Tb have been made in captivity,
where opportunities for behavioural thermoregulation by individuals may be
limited, the extent to which, and under what circumstances, heterothermy is
used by ungulates in their natural environment remains unclear, despite
statements to the contrary (Willmer et
al., 2000; Randall et al.,
2002
). Investigations on free-ranging mule deer (Odocoileus
hemionus; Sargeant et al.,
1994
) and black wildebeest (Connochaetes gnou;
Jessen et al., 1994
), both
inhabitants of semi-arid areas, and on springbok (Antidorcas
marsupialis; Mitchell et al.,
1997
) and Cape eland (Fuller et
al., 1999
), both occurring in arid habitats, did not find that
these species routinely employed heterothermy, despite daily variation in air
temperature (Ta) of >15°C in some cases. Because
Tb of Cape eland was relatively invariant when they were
allowed to seek shade, Fuller et al.
(1999
) argued that the
heterothermy observed by Taylor and Lyman
(1967
) was "probably an
experimental artefact occurring in animals denied access to behavioural
thermoregulation".
The Arabian oryx (Oryx leucoryx), a desert antelope (body mass,
80100k g) that once ranged throughout most of the Arabian peninsula,
was extirpated from the wild by 1972
(Henderson, 1974). In 1990,
Arabian oryx were reintroduced into Mahazat as-Sayd, a large protected area
160 km north-east of Taif, Saudi Arabia. Captive-reared animals survived and
reproduced without supplemental food and water; the population has increased
significantly over the past decade and now numbers more than 450 individuals
(Ostrowski et al., 1998
;
Treydte et al., 2001
). Arabian
oryx can live without access to drinking water in arid and hyperarid deserts
(Williams et al., 2001
),
including the Rub al-Khali, one of the driest regions in the world
(Meigs, 1953
). Survival of
oryx in such harsh areas is noteworthy when one considers its large size, its
inability to shelter in burrows and that herbivory is typically associated
with high rates of water turnover (Nagy
and Peterson, 1988
). Arabian oryx have one of the lowest
mass-specific water-influx rates among ungulates living in hot environments:
76.9% below allometric prediction in summer
(Nagy and Peterson, 1988
;
Williams et al., 2001
;
Ostrowski et al., 2002
).
In the present study, we tested the hypothesis that heterothermy is a mechanism employed by free-ranging Arabian oryx in their natural environment. We found that their mean daily Tb varied by 4.1±1.7°C during summer, the first documentation of heterothermy in a free-living ungulate, but only by 1.5±0.6°C during winter. We used data on heterothermy of Arabian oryx during summer and winter to estimate their daily heat storage and concomitant water savings.
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Materials and methods |
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Characterized by hot summers and mild winters, the arid climate of this region has an annual mean rainfall of 96±41 mm (N=11 years). The mean daily maximum (Ta,max) and minimum (Ta,min) air temperatures are 42.4°C and 26.6°C, respectively, in June, the hottest month, and 23.8°C and 11.5°C, respectively, in January (National Wildlife Research Center, unpublished report). During 1998, 1999, 2000 and 2001, annual rainfall was 79 mm, 34 mm, 45 mm and 136 mm, respectively. Weather data were measured continuously at an automatic meteorological recording station situated within the protected area. Solar radiation was measured using a pyranometer (Li-Cor, Lincoln, NB, USA).
The sparse vegetation of Mahazat as-Sayd is dominated by perennial grasses,
including Panicum turgidum, Lasiurus scindicus, Stipagrostis spp. and
Ochthochloa compressa
(Mandaville, 1990). Small
acacia (Acacia spp.) and maeru trees (Maerua crassifolia),
sporadically distributed along dry wadis (water courses), provide shade for
the oryx.
Handling of oryx
We darted six wild-born Arabian oryx [Oryx leucoryx (Pallas,
1777); three males and three females] with a mixture of 4.9 mg
ml1 etorphine (M99; C-Vet, Leyland, UK; mean dose,
4.2±0.4 mg) and 50 mg ml1 xylazine (Rompun; Bayer,
Leverkusen, Germany; dose, 25 mg), a combination of drugs that induced
anaesthesia within 10 min (Machado et al.,
1983). All animals were sexually mature and >3 years old,
judging from wear on their teeth (Ancrenaz
and Delhomme, 1997
). After oryx were anaesthetized, we weighed
them (±0.5 kg) using a Salter scale attached to a tripod and moved them
to a truck. Mean body mass was 92.9±4.26 kg (range, 88.999.1
kg). Using aseptic procedures, we sutured temperature-sensitive
radio-transmitters (model IMP/400 equipped with a S4 thermistor; Telonics,
Mesa, AZ, USA), embedded in synthetic resin and coated with paraffin and
beeswax (3.3 cmx9.7 cm; 8590 g), into a fold of the omentum. We
injected each individual with 1 g of long-acting amoxycillin intramuscularly,
attached a second radio-transmitter around its neck, and reversed the
anaesthetic with 9 mg diprenorphine (M50-50; C-Vet; 12 mg
ml1) and 10 mg atipamezole (Antisedan; Orion, Espoo,
Finland; 5 mg ml1). Experimental animals were ambulatory
within 2 min following drug reversal and were released, on average,
42.2±5.8 min after they were darted. Radio-transmitters affixed to
collars were long-range and motion-sensitive (MOD-400/ S11 sensor; Telonics),
with a faster pulse rate when animals were active. Our experimental protocol
was approved by the National Commission for Wildlife Conservation and
Development, Riyadh, Saudi Arabia.
Temperature-sensitive radio-transmitters
We calibrated (±0.1°C) temperature-sensitive radio-transmitters
in a temperature-controlled water bath against a mercury thermometer with a
certificate traceable to the US National Institute of Standards and
Technology. We determined the interpulse interval of these radio-transmitters
using a digital data processor (TDP-2; Telonics) connected to a portable
multichannel receiver (TR-2; Telonics) over a temperature range of
3246°C. After log transformation of temperatures and interpulse
intervals, we derived least-squares linear regression equations relating
interpulse interval to Tb; all regressions had an
r2 of >0.995. We surgically removed two
radio-transmitters 22 months after implantation to check for deviations in
calibration. Between 32°C and 46°C, the change from our initial
calibrations of these two transmitters was 0.1°C and
0.2°C. We concluded that temperature-sensitive radio-transmitters
provided an accurate measurement of oryx Tb.
Data collection
Beginning 30 days after implanting radio-transmitters, we used a hand-held
antenna (range, 600800 m) to record Tb every 30 min
for a total of 828 h during the day and 81 h at night, with measurement
periods equally distributed among six oryx. We monitored
Tb of oryx from 17 May 1998 to 29 September 2001. Daytime
was considered to be between 06.00 h and 19.00 h, and night-time between 19.30
h and 05.30 h. We also measured Ta (±0.1°C) in
the shade at the same intervals with an electronic thermometer (Type T; Omega
Engineering, Stamford, CT, USA) and a 38-gauge copperconstantan
thermocouple, 30 cm above ground. When oryx were in deep shade,
Ta crudely approximates to operative temperature (Bakken,
1976,
1992
). To document oryx shading
behaviour, we monitored their movements by radiotracking them at long distance
from our vehicle using the radio signal from their neck collar. When visible
through binoculars, oryx were described every 15 min as resting in shade,
standing outside of shade or active (walking, feeding or interacting). During
the night, we classified behaviour as active or inactive based on differences
in pulse interval of radio-collar signals. At night, some oryx were sensitive
to our presence, even at long distance. Observations of behaviour were
terminated and Tb data were eliminated if we suspected
that oryx were more active because of our presence. Hence, total night-time
observations were fewer than those in daytime.
Calculation of water savings
To calculate water savings as a result of hyperthermia, we assumed that
oryx had a uniform body and surface temperature, a reasonable approximation at
the high Tas experienced by animals during summer in this
study. Skin temperature was probably lower than Tb in
winter but, because the heat of vaporization of water is only 0.7% higher at
30°C than at 38°C (Kleiber,
1975), errors are probably small because of this assumption. We
used the following equation:
W=
TbCpMb/Hv,
where W is water saved (in litres) per time interval,
Tb is the difference between Tb
observed and mean Tb (in °C), Cp is the
specific heat of tissue (3.48 kJ kg1deg.1;
Taylor, 1970
;
International Union of Physiological
Sciences Thermal Commission, 1987
), Mb is mean
body mass (in kg), and Hv is the heat of vaporization of water
(2404 kJ litre1 at 38°C;
Kleiber, 1975
;
Schmidt-Nielsen, 1998
).
Because of the complexity of heat exchange of an animal with its
environment (Porter and Gates,
1969), we recognize the limitations of our simplifying assumptions
involved in estimating water savings. However, given that we computed water
savings only when Tb>Tb,mean, and
given that Ta exceeded Tb,mean in
summer only for an average of 4 h per day, our estimates of water savings are
conservative.
Data analysis
To test for differences between mean daily Tb and daily
variation in Tb
(Tb,maxTb,min), we used a
repeated-measures two-way analysis of variance [ANOVA; with season
(winter/summer) and time of day (night/day) as fixed factors and individuals
as a random factor (model type III)]. We investigated the relationship between
total heat storage, expressed as
Cp(Tb,maxTb,
min)Mb, and Ta with linear
regression. We tested for differences in Ta between
seasons by comparing half-hour means with a Wilcoxon matched pairs signed-rank
test.
For each season, the proportion of time spent in shade per 24 h-day was
calculated for each animal. The effect of climate on behaviour was examined by
correlating activity with Ta, Ta,max
and Ta,min. All proportions were arcsine transformed prior
to analyses (Zar, 1996). To
determine if animals were resting in shade when their Tb
was decreasing, and if they were active in sun when their
Tb was increasing, we used a binomial test
(Ho; P=0.5). Means ± 1 S.D. are reported.
We assumed statistical significance at P<0.05
(Zar, 1996
).
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Results |
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Body temperature
With data from summer and winter combined, mean body temperature
(Tb) was 38.4±1.3°C; it did not vary
significantly between seasons or between day and night
(F1,59=1.1, P=0.30). However, the daily variation
in Tb,
(Tb,maxTb,min), was
significantly higher in summer (4.13±1.7°C;
F1,56=148.9, P<0.0001) than in winter
(1.5±0.6°C).
During summer, Tb,max and Tb,min averaged 40.5±0.66°C and 36.5±1.16°C, respectively, during day and 39.8±0.20°C and 38.1±0.36°C during night. Tb,min occurred around 08.30 h, which is 3 h later than Ta,min. Tb,max occurred near 18.30 h, shortly before sunset, and decreased during the night (Fig.2). Mean Tb was 38.3±0.44°C during day and 38.8±0.16°C during night. The largest change in Tb during one day was 7.5°C, from 34.5°C to 42.0°C (in July), in a male that weighed 99.1 kg, the heaviest oryx in our cohort.
|
During winter, the mean Tb,max and Tb,min were 39.2±0.29°C and 37.5±0.51°C, respectively, during day, and 39.2±0.22°C and 37.9±0.18°C during night. Tb,min occurred around 07.00 h, 3060 min after sunrise. Tb increased until 18.00 h and monotonically decreased during the night (Fig.2). Mean Tb was 38.3±0.59°C during the day and 38.5±0.22°C during the night. The largest change in Tb during one day was 2.5°C, from 36.6°C to 39.1°C in February, in a female that weighed 89.7 kg. During the summer, mean Tb,max was significantly higher (t=290.4, d.f.=57, P<0.001), and mean Tb,min significantly lower (t=159, d.f.=57, P<0.001) than during winter. There was no statistically significant correlation (P>0.5) between mean Ta and Tb in summer or winter. However, there was a significant correlation between the total heat stored and the amplitude of variation in Ta during the day in summer (Fig.3A; F1,24=4.9, P=0.03, r2=0.17) and in winter (F1,20=22.2, P<0.001, r2=0.53). There was also a correlation between the total heat stored and Ta,max and Ta,min during the summer (Fig.3B,C; F1,24=14.4, P<0.001, r2=0.37 and F1,24=242.8, P<0.001, r2=0.91, respectively) and between total heat stored and Ta,max during the winter (Fig.3B; F1,20=9.0, P=0.007, r2=0.32). There was no correlation between total amount of heat stored and Ta,min in winter (Fig.3C; F1,20=0.1, P=0.78, r2=0.04).
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Behavioural thermoregulation
To search for correlations between behaviour and changes in
Tb, we recorded oryx activity between 06.00 h and 08.30 h,
when Tb was typically decreasing, and between 08.30 h and
18.30 h, when Tb was increasing. During summer, between
06.00 h and 08.00 h, animals were more frequently active outside shade than
resting under shade (Fig.4A;
P<0.001, N=20). During periods when
Tb was increasing, animals were resting under shade more
frequently than active outside shade
(Fig.4A; P<0.001,
N=20). In winter, there was no relationship between behaviour and
Tb
(Fig.4B).
|
Shading pattern
During summer, when diurnal Ta was >35°C, oryx
sought shade as early as 06.30 h, typically under the dense foliage of maeru
trees. They stayed in the shade, on average, for 9 h 21 min and began foraging
at around 18.30 h. Time spent in the shade by oryx was positively correlated
with mean Ta (rs=0.70,
P<0.01, N=20), Ta,max
(rs=0.67, P<0.01, N=20) and
Ta,min (rs=0.65, P<0.01,
N=20). Shading time was also positively correlated with
Tb,max (rs=0.77, P<0.01,
N=20). During winter, time spent in the shade was not correlated with
any of the variables we measured.
Water savings by heat storage
The gradient between the temperature of the animal's surface and
Ta drives heat flux
(Gates, 1962), but often the
approximation TbTa is used
(McNab, 1980
;
McClure and Porter, 1983
;
Parker and Robbins, 1985
).
During summer, TbTa was
positive in late afternoon, night and early morning. During the morning, as
Ta approached Tb, the outward flow of
heat was reduced. Then, between 09.00 h and 17.30 h,
TbTa was negative, indicating
heat flow to the animals from their environment
(Fig.5). During winter,
Tb of animals was always higher than
Ta. Heat storage was 112.1 kJ h1 in
summer versus 36.9 kJ h1 in winter, and the rate of
heat gain was also higher in summer (tslope=10.3, d.f.=21,
P<0.001; bsummer=44.9,
r2=0.98; bwinter=16.3,
r2=0.84).
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Assuming mean Tb=38.4°C, Tb,max=40.48°C and body mass=92.9 kg, heat storage was 672.4 kJ day1 in summer and 258.6 kJ day1 in winter. To dissipate this amount of heat by evaporation would require 0.28 litres H2O day1 in summer and 0.11 litres H2O day1 in winter.
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Discussion |
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In a vanguard study, Schmidt-Nielsen et al.
(1957) showed that the camel
(N=2; mean body mass=260 kg), under penned conditions and deprived of
drinking water, varied its rectal Tb from 3.5°C to
6.2°C and as much as 2.8°C above mean Tb during
summer. If we calculate heat storage for the camel as we have done for oryx,
then camels stored approximately 2500 kJ day1 and
potentially saved approximately 1 litre H2O day1.
With a daily variation in core Tb of 1.57.5°C,
and a potential water saving of 0.28 litres H2O
day1 during summer, the Arabian oryx, which is about a third
the size of a camel and therefore has a larger surface-to-volume ratio,
appears to employ heterothermy in the wild as effectively as does the
legendary domestic camel.
Although studies on free-ranging Cape eland and springbok failed to find
heterothermy (Mitchell et al.,
1997; Fuller et al.,
1999
), these studies were conducted when climatic conditions were
moderate (Ta<35°C) and over short periods (<2
months; Fuller et al., 1999
).
Had we measured Tb of Arabian oryx only during winter, we
would have found variation of <1.5±0.6°C day1.
During summer, arid-zone antelopes are often exposed to
Tas of >40°C, a temperature above the mean
Tb for bovid ungulates, and do not have access to drinking
water. Under such conditions, these species may also use heterothermy to limit
evaporative water losses.
The extent to which hydration state influences heterothermy remains
uncertain. In captivity, at Ta>35°C, the variation
in rectal Tb increased for camels, Grant's gazelles,
Thomson's gazelles and fringe-eared oryx when they were water-deprived
compared with when they were hydrated
(Schmidt-Nielsen et al., 1957;
Taylor, 1970
). However, Cape
eland, African buffalo (Syncerus caffer) and wildebeest did not
significantly elevate rectal Tb when water-deprived
(Taylor and Lyman, 1967
;
Taylor, 1970
). Because
free-living Arabian oryx have a remarkably low rate of water influx during
summer, on average 1310 ml H2O day1
(Williams et al., 2001
), it
could be that they are somewhat dehydrated at this time. In support of this
idea, they have higher haematocrit, plasma protein concentration and plasma
osmolality during summer than during winter (S. Ostrowski, unpublished data).
Hydration state during summer may influence use of heterothermy by oryx.
During summer, oryx stored 112.1 kJ h1 of heat during the
day and dissipated this heat by non-evaporative means at night. They defended
their Tb by evaporative cooling, primarily panting, only
when Tb approached 41.542°C (S. Ostrowski,
unpublished data). Between 06.00 h and 08.30 h, Tb
continued to decline despite the fact that Ta and solar
radiation were increasing and oryx were active during this period, a pattern
that was also observed for the camel
(Schmidt-Nielsen et al.,
1957), red kangaroo (Megaleia rufa;
Brown and Dawson, 1977
) and
Cape eland (Fuller et al.,
1999
). Allowing Tb to decrease to a lower
level would presumably permit oryx to store additional heat during the hot
part of the day, as is also suggested by the correlation between
Ta,min and total heat storage
(Fig. 3C). In winter, oryx also
increased their Tb during the day, storing 36.9 kJ
h1. However, Tb,min was higher in winter
than in summer despite the fact that the gradient between
Tb and Ta was larger, suggesting that
they limit the decrease in Tb during winter.
During winter, Tb of oryx always exceeded
Ta, indicating that heat stored in their body was
endogenous (Fig.5). Williams et
al. (2001) reported that oryx
during spring, with a mean body mass of 89.0 kg, had a mean field metabolic
rate of 920 kJ h1. The fact that oryx stored 258.6 kJ during
the 12.5 h that Tb was higher than
Tb,mean suggests that, during winter days, a modest 2.2%
of heat production was stored, assuming that oryx were in energy balance. Our
results indicate that, during winter, oryx adjust their thermoregulatory
behaviour and attendant water savings to a decrease in
Ta.
Our estimates of water savings as a result of heat storage indicate that
this is an important mechanism in the water economy of Arabian oryx. Our
calculations show that they saved 0.28 litres H2O
day1 and 0.11 litres H2O day1
in summer and winter, respectively, when we used mean Tb
in our calculations. The mass-corrected water-influx rate of oryx in summer is
22.7 ml H2O day1 kg0.922, where
0.922 is the slope of the allometric relationship between water influx (ml
day1) and body mass (kg) among large ungulates in hot
environments (Ostrowski et al.,
2002). If oryx maintained a constant Tb of
38.4°C, their water-influx rate would have to increase 19% (to 27 ml
H2O day1 kg0.922) to offset
water losses.
Our use of mean Tb in our calculation of water savings assures that our estimate is a conservative one. Given that oryx allowed their Tb to decline to a mean of 36.5°C during summer, one could argue that heat storage was 1293.2 kJ day1 (4.0°Cx3.48 kJ kg1 deg.1x92.9 kg) and that water savings were 0.538 litres day1.
Although Arabian oryx avoid solar radiation during the day in summer, they
still depend on heterothermy at this time. Our calculations of water savings
as a result of heterothermy, coupled with their low daily water-influx rate
(Ostrowski et al., 2002),
suggest that oryx can not obtain sufficient preformed water during summer to
maintain homeothermic Tb without disrupting their
hydration state. Contrary to what was suggested for the Cape eland
(Fuller et al., 1999
),
behavioural thermoregulation in the oryx does not result in homeothermy.
An endangered species, the Arabian oryx has been the focus of
re-introduction projects throughout the Middle East
(Stanley Price, 1989;
Ostrowski et al., 1998
).
Formerly, this species was distributed over much of the Arabian peninsula, but
now the only viable free-living herds occur in the desert of central Saudi
Arabia and the western Rub al-Khali or Empty Quarter. Current models of
climate change attributable to global warming predict that the Arabian
peninsula may experience as much as a 5°C increase in mean
Ta over this century; night-time mean
Ta,min may increase proportionately more than daytime
Ta,max values
(Mitchell and Hulme, 2000
).
Our data highlight the importance of minimum night-time Ta
to daytime heat storage of oryx and their attendant water conservation. If
night-time Ta increases as models predict, this will
undoubtedly impact the ability of oryx to live in some areas, a major concern
for conservationists.
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Acknowledgments |
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References |
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Ancrenaz, M. and Delhomme, A. (1997). Teeth eruption as a means of age determination in captive oryx Oryx leucoryx (Bovidae, Hippotraginae). Mammalia 61,135 -138.
Bakken, G. S. (1976). A heat transfer analysis of animals: unifying concepts and the application of metabolism chamber data to field ecology. J. Theor. Biol. 60,337 -384.[Medline]
Bakken, G. S. (1992). Measurement and application of operative and standard operative temperatures in ecology. Am. Zool. 32,194 -216.
Bartholomew, G. A. (1964). The roles of physiology and behaviour in the maintenance of homeostasis in the desert environment. In Homeostasis and Feedback Mechanisms. Symposia of The Society of Experimental Biology, volume17 (ed. G. M. Hughes), pp.7 -29. Cambridge: Cambridge University Press.
Brown, G. D. and Dawson, T. J. (1977). Seasonal variations in the body temperatures of unrestrained kangaroos (Macropodidae: Marsupialia). Comp. Biochem. Physiol. A 56, 59-67.[Medline]
Fuller, A., Moss, D. G., Skinner, J. D., Jessen, P. T., Mitchell, G. and Mitchell, D. (1999). Brain, abdominal and arterial blood temperatures of free-ranging eland in their natural habitat. Pflügers Arch. 438,671 -680.[CrossRef][Medline]
Gates, D. M. (1962). Energy Exchange in the Biosphere. New York: Harper and Row.
Henderson, D. S. (1974). Were they the last Arabian oryx? Oryx 12,347 -350.
International Union of Physiological Sciences Thermal Commission (1987). Glossary of terms of thermal physiology. Pflügers Arch. 410,567 -587.[Medline]
Jessen, C., Laburn, H. P., Knight, M. H., Kuhnen, G., Goelst, K.
and Mitchell, D. (1994). Blood and brain temperature
of free-ranging black wildebeest in their natural environment. Am.
J. Physiol. 267,R1528
-R1536.
Jessen, C. (2001). Temperature Regulation in Humans and Other Mammals. Berlin: Springer-Verlag.
Kleiber, M. (1975). The Fire of Life. Huntington, NY: Krieger Publishing Company.
Langman, V. A. and Maloiy, G. M. O. (1989). Passive obligatory heterothermy of the giraffe (abstract). J. Physiol. Lond. 415,89P .
Machado, C. R., Furley, C. W. and Hood, H. (1983). Observation of the use of M99, Immobilon and xylazine in the Arabian oryx (Oryx leucoryx). J. Zoo Anim. Med. 14,107 -110.
Mandaville, J. P. (1990). Flora of Eastern Saudi Arabia. London: Kegan Paul International.
McClure, P. A. and Porter, W. (1983). Development of insulation in neonatal cotton rats (Sigmodon hispidus). Physiol. Zool. 56, 18-32.
McNab, B. K. (1980). On estimating thermal conductance in endotherms. Physiol. Zool. 53,145 -156.
Meigs, P. (1953). World distribution of arid and semi-arid homoclimates. Arid Zone Res. 1, 203-210.
Mitchell, T. and Hulme, M. (2000). A country by country analysis of past and future warming rates. Tyndall Center Working Paper no. 1. Tyndall Center Publication, Norwich, UK.
Mitchell, D., Maloney, S. K., Laburn, H. P., Knight, M. H., Kuhnen, G. and Jessen, C. (1997). Activity, blood temperature and brain temperature of free-ranging springbok. J. Comp. Physiol. B 167,335 -343.[CrossRef][Medline]
Nagy, K. A. and Peterson, C. C. (1988). Scaling of water flux rate in animals. Univ. California Public. Zool. 120,1 -172.
Ostrowski, S., Bedin, E., Lenain, D. M. and Abuzinada, A. H. (1998). Ten years of Arabian oryx conservation breeding in Saudi Arabia achievements and regional perspectives. Oryx 32,209 -222.
Ostrowski, S., Williams, J. B., Bedin, E. and Ismail, K. (2002). Water flux and food consumption of free-leaving oryx (Oryx leucoryx) in the Arabian desert during summer. J. Mammal. 83,665 -673.
Parker, K. L. and Robbins, C. T. (1985). Thermoregulation in ungulates. In Bioenergetics of Wild Herbivores (ed. R. J. Hudson and R. G. White), pp.161 -182. Boca Raton, FL: CRC Press.
Porter, W. P. and Gates, D. M. (1969). Thermodynamic equilibria of animals with environment. Ecol. Monogr. 39,227 -244.
Randall, D., Burggren, W. and French, K. (2002). Eckert Animal Physiology. New York: W. H. Freeman & Co.
Sargeant, G. A., Eberhardt, L. E. and Peek, J. M. (1994). Thermoregulation by mule deer (Odocoileus hemionus) in arid rangelands of southcentral Washington. J. Mammal. 75,536 -544.
Schmidt-Nielsen, K. (1998). Animal Physiology: Adaptation and Environment. Cambridge: Cambridge University Press.
Schmidt-Nielsen, K., Schmidt-Nielsen, B., Jarnum, S. A. and Houpt, T. R. (1957). Body temperature of the camel and its relation to water economy. Am. J. Physiol. 188,103 -112.[Medline]
Stanley Price, M. R. (1989). Animal Re-introduction: the Arabian oryx in Oman. Cambridge: Cambridge University Press.
Taylor, C. R. (1969). The eland and the oryx. Sci. Am. 220,88 -97.[Medline]
Taylor, C. R. and Lyman, C. P. (1967). A comparative study of the environmental physiology of an East African antelope, the eland, and the Hereford steer. Physiol. Zool. 40,280 -295.
Taylor, C. R. (1970). Strategies of temperature
regulation: effect on evaporation in East African ungulates. Am. J.
Physiol. 219,1131
-1135.
Treydte, A. C., Williams, J. B., Bedin, E., Ostrowski, S., Seddon, P. J., Marshall, E. A., Waite, T. A. and Ismail, K. (2001). In search of the optimal management strategy for Arabian oryx. Anim. Conserv. 4,239 -249.[CrossRef]
Walsberg, G. (2000). Small mammals in hot deserts: some generalizations revisited. Bioscience 50,109 -120.
Williams, J. B., Ostrowski, S., Bedin, E. and Ismail, K.
(2001). Seasonal variation in energy expenditure, water flux and
food consumption of Arabian oryx Oryx leucoryx. J. Exp.
Biol. 204,2301
-2311.
Willmer, P., Stone, G. and Johnson, I. (2000). Environmental Physiology of Animals. Magden, USA: Blackwell Science.
Zar, J. H. (1996). Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall.
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