Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation
UNM Biology Department, MSC03-2020, 1 University of New Mexico, Albuquerque, NM 87131-0001, USA
* Author for correspondence (e-mail: aemckech{at}unm.edu)
Accepted 16 October 2003
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Summary |
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Key words: acclimation, cutaneous evaporative water loss, respiratory evaporative water loss, water vapour diffusion resistance, thermoregulation, Zenaida asiatica mearnsii
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Introduction |
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Current data provide limited insight into the variation in REWL and CEWL
associated with phylogenetic position, environmental temperature and
acclimation period. In most avian species investigated to date, CEWL has been
found to represent at least 50% of total evaporative water loss (TEWL) at
moderate air temperatures (Ta)
(Bernstein, 1971;
Lasiewski et al., 1971
;
Dawson, 1982
;
Webster and Bernstein, 1987
;
Webster and King, 1987
;
Wolf and Walsberg, 1996
;
Tieleman and Williams, 2002
).
Considerably less attention has been focused on the relative importance of
respiratory and cutaneous evaporative heat loss in response to high air
temperatures (Ta
35°C). The limited data available
on the relative contributions of CEWL and REWL to TEWL at high
Ta values reveal considerable variation among taxa
(Wolf and Walsberg, 1996
). For
instance, in the few members of the Columbiformes (pigeons and doves)
examined, CEWL represented more than 40% of TEWL at 35°C
Ta
45°C
(Webster and King, 1987
;
Withers and Williams, 1990
;
Hoffman and Walsberg, 1999
). In
contrast, in passerine birds the relative contribution of cutaneous
evaporation decreases with increasing Ta
(Dawson, 1982
;
Wolf and Walsberg, 1996
;
Tieleman and Williams, 2002
).
In verdins (Auriparus flaviceps: Passeriformes: Remizidae), for
example, the contribution of CEWL decreased from ca. 60% of TEWL at
Ta=35°C to ca. 15% at
Ta=50°C (Wolf and
Walsberg, 1996
). Tieleman and Williams
(2002
) observed similar
decreases in the relative contribution of CEWL with increasing
Ta in four species of larks (Passeriformes:
Alaudidae).
An understanding of factors other than taxonomic affiliation that influence
patterns of TEWL partitioning is critical for understanding avian
thermoregulation and water balance at high environmental temperatures. Of
particular interest are potentially adaptive changes in CEWL in response to
acclimatization, acclimation and/or short-term changes in evaporative cooling
requirements. Tieleman and Williams
(2002) found little evidence
for changes in CEWL/TEWL of larks following thermal acclimation. However,
other researchers have found large changes in the role of cutaneous
evaporation with acclimation. Adult rock doves acclimated to high
Ta values from hatching exhibited elevated rates of CEWL
compared to non-acclimated doves, and dissipated virtually their entire heat
load cutaneously at Ta=60°C
(Marder and Arieli, 1988
;
Ophir et al., 2002
). Evidence
that CEWL can be adjusted over much shorter time scales is provided by Hoffman
and Walsberg (1999
), who found
that mourning doves (Zenaida macroura) responded within minutes to
experimental inhibition of REWL by increasing CEWL by 72% at
Ta=35°C. Nevertheless, the periods over which changes
in CEWL associated with thermal acclimation occur remain relatively
unknown.
We investigated the effect of short-term (days to weeks) thermal acclimation on the partitioning of TEWL in western white-winged doves (Zenaida asiatica mearnsii). We also examined the interactions between modes of evaporative water loss, body temperature, skin temperature and metabolic rate, in an attempt to provide an integrative view of how heat-acclimated and non-heat-acclimated doves respond to high levels of heat stress. We chose white-winged doves for this study because they winter in southern Mexico under moderate environmental conditions, but breed during the summer in the Sonoran Desert of the southwestern United States and northwestern Mexico, where they frequently experience environmental temperatures approaching or exceeding 50°C (B. O. Wolf and A. E. McKechnie, personal observation).
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Materials and methods |
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Measurements of evaporative water loss, O2 consumption and
CO2 production
We measured the respiratory and cutaneous components of evaporative water
loss in a 14.6 l metabolic chamber, constructed from 5 mm-thick glass. During
measurements, the bird perched on a stainless steel wire mesh screen placed at
a height that allowed for normal perching postures. Any faeces produced fell
through the mesh into a 2 cm layer of mineral oil, preventing evaporation.
REWL and CEWL were partitioned using a chamber that was divided into upper
(4.3 l) and lower (10.3 l) compartments by a 1 mm-thick aluminum partition. A
80 mmx120 mm rectangle was cut from the partition, and a piece of 0.25
mm-thick stretchable latex membrane (Semantodontics Dental Dam, Phoenix, AZ,
USA) secured over the opening using an aluminum frame bolted to the partition.
The bird's head and neck protruded through a hole punched through the
membrane. The diameter of the hole was slightly less than the diameter of the
bird's neck, and provided a snug fit. An illustration of a similar chamber may
be found in Wolf and Walsberg
(1996). Tieleman and Williams
(2002
) suggested that the
flow-through mask system they used to measure REWL and CEWL in four species of
lark was an improvement over the partitioned chamber system used by previous
investigators and in the present study, on the grounds that cutaneous losses
from the head and neck are included in the respiratory component measured in
the upper compartment. However, this source of error is small and can be
minimized by making corrections to REWL and CEWL measurements based on the
surface area of the head and neck that protrude into the upper chamber
(Wolf and Walsberg, 1996
; see
below).
The experimental air temperature (Ta) was controlled by placing the metabolism chamber in an insulated 200 l environmental chamber. The Ta within the environmental chamber was regulated using a temperature-controlled circulator (Model 1187, VWR Scientific Products, West Chester, PA, USA), which pumped fluid through copper tubing. Air within the environmental chamber was mixed using a small electric fan. Ta within the metabolism chamber was measured using a 21-gauge Cu-Cn thermocouple and a TC-1000 thermocouple meter (Sable Systems, Las Vegas, NV, USA).
Dry, CO2-free air (dewpoint = -73°C) produced using a FTIR
Purge Gas Generator (Whatman, Newton, MA, USA) flowed through the chamber at
flow rates of 6-10 l min-1, chosen to maintain dewpoints below
1°C in the chamber during all measurements. Flow rates into the lower
compartment of the chamber were regulated using a FMA-series mass flow
controller (Omega, Bridgeport, NJ, USA), and flow rates into the upper chamber
by a FMA-series mass flow controller and model 246B mass flow controller (MKS
Instruments, Andover, MA, USA) plumbed in parallel. The mass flow controllers
were calibrated using a 1 l soap bubble flowmeter
(Baker and Pouchot, 1983).
Because the partition between the upper and lower compartments was not
completely airtight, we controlled flow rates to the upper and lower
compartments so as to ensure that no pressure gradient existed between them.
During all measurements, we maintained CO2 concentrations of <20
p.p.m. in the lower compartment, indicating that leakage between the
compartments was negligible.
Dry, CO2-free control air and excurrent air from the upper and lower compartments of the metabolism chamber were sequentially sampled using a TR-RM8 Respirometer Multiplexer (Sable Systems). The partial pressure of water vapour and carbon dioxide concentration in sampled air was measured using a LI-7000 CO2/H2O analyzer (Li-Cor, Lincoln, NE, USA), calibrated daily using dry, CO2-free air and a span gas for water vapour generated using a LI-610 portable dew point generator (Li-Cor) and a certified span gas containing 1020.0 p.p.m. CO2 (Matheson Tri-Gas, Houston, TX, USA). Dewpoint temperatures of the air samples were well below those of the ambient environment, ensuring that no condensation occurred within the sampling system. After the sample left the LI-7000 CO2/H2O analyzer, water vapour and CO2 were scrubbed using a Drierite® and Ascarite® column. The fractional O2 concentration was then determined using a FC-1B oxygen analyzer (Sable Systems). Output from the CO2/H2O and oxygen analyzers, and the thermocouple meter, was digitized using a Universal Interface II (Sable Systems) and recorded on a personal computer using Datacan V data acquisition software (Sable Systems), with a sampling interval of 1 s.
Measurements of skin and body temperature
Body temperature (Tb) was measured by inserting a
36-gauge Cu-Cn Teflon-coated thermocouple (Physitemp, Clifton, NJ, USA)
approximately 1.5 cm into the cloaca, at which depth a slight withdrawal did
not result in a decrease in the Tb reading. The
thermocouple wire was secured to the feathers immediately behind the cloaca by
a small piece of adhesive tape. Skin temperature (Tskin)
was measured dorsally, by attaching a similar thermocouple to the skin between
the scapulars using cyanoacrylic adhesive.
Experimental protocol
REWL, CEWL, oxygen consumption
(O2) and carbon
dioxide production
CO2) were
measured at Ta=34.8±0.5, 40.0±0.5 and
45.9±0.4°C (means ± 95% confidence intervals). For
convenience, we refer to these experimental Ta values as
35, 40 and 45°C, respectively. Measurements at each Ta
were carried out during separate 2-3 day periods. At each experimental
Ta, measurements were made in five cool-acclimated and
five heat-acclimated doves, in random order. All measurements were made in
darkness on fed doves, during the active-phase of their circadian cycle.
Typically, each set of measurements lasted 2 h, and data recorded during the
first 30 min of each run were not included in the analyses. In a few cases,
cool-acclimated doves exhibited rapid, apparently uncontrolled increases in
Tb at Ta>45°C, and in such
cases we removed the bird prior to the end of the 2 h period. For each bird,
the interval between each set of measurements was at least 3 days.
Because REWL and CEWL were measured sequentially, there was a time lag of 5
min between the respective measurements. However, 99% equilibrium times for
the two compartments, calculated using the relevant equation in Lasiewski et
al. (1966), were 7-14 min.
Since the equilibrium times (and hence the periods over which gas measurements
were integrated) were greater than the time lag between the REWL and CEWL
measurements, the data are essentially equivalent to simultaneous
measurements. Moreover, we only used EWL data that were stable during the
entire measurement period.
Data analysis
We calculated REWL and CEWL from the water vapour partial pressure in
excurrent air from the upper and lower compartments respectively. We corrected
these measurements for the surface area of the head and neck in the upper
compartment by subtracting a surface-area specific estimate of CEWL from the
head and neck from the measured REWL, following Wolf and Walsberg
(1996). The surface area of
the head and neck in the upper compartment averaged 2.5% of the total skin
surface area, estimated from the equation provided by Walsberg and King
(1978
). We calculated
whole-body water vapour diffusion resistance (rv) as
rv=(
'v(Tskin)-
va)/CEWL,
where
'v(Tskin) is the saturation water vapour
density at skin temperature (g cm-3),
va is the
water vapour density of the air in the metabolism chamber (g cm-3),
and CEWL is surface area-specific cutaneous evaporative water loss (g
cm-2 s-1) (Webster
et al., 1985
). Although the effective evaporative surface area
could conceivably have varied slightly through postural adjustments, we
assumed that it remained constant during all measurements. We also assumed
that the dorsal Tskin measurements were representative of
the entire skin surface. During the experiments, the water vapour partial
pressure in the chamber varied from 0.097 kPa to 0.616 kPa, corresponding to
dewpoints of -22.9°C and 0.1°C. It is unlikely that these low levels
of ambient humidity affected any properties of the skin that potentially
determine rv, such as the hydration state of surface skin
layers.
O2 was
calculated using the relevant equation in Withers
(1977
) and
CO2 using
equation 3 in Walsberg and Wolf
(1995
). Respiratory exchange
ratios were calculated as
CO2/
O2
and gas exchange measurements were converted to metabolic rates using thermal
equivalence data from table 4-2 in Withers
(1992
). This approach assumes
that only carbohydrates and lipids are metabolized, and a maximum error of 6%
is associated with protein metabolism
(Walsberg and Wolf, 1995
).
We subjectively examined all data, and discarded any traces of gas exchange
and/or EWL that were not stable. For each bird at each Ta,
we used the lowest value recorded over 1 min, representing a mean of 60
measurements. All values are presented as means ± 95% confidence
intervals. We compared data using t-tests and repeated-measures analyses of
variance (RM-ANOVA; Zar,
1999). Unless otherwise stated, the sample size for each
experimental group was five doves.
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Results |
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The REWL of heat-acclimated doves increased from 1.9±0.2 mg g-1 h-1 at Ta=35°C to 4.3±0.6 mg g-1 h-1 at Ta=45°C, whereas REWL in cool-acclimated doves increased from 1.9±0.5 mg g-1 h-1 at Ta=35°C to 8.3±1.9 mg g-1 h-1 at Ta=45°C (Fig. 1B). REWL did not differ between the two groups at Ta=35°C or 40°C, but was significantly higher in cool-acclimated doves at Ta=45°C (t=3.951; P=0.002).
The CEWL of heat-acclimated doves increased from 3.6±1.2 mg g-1 h-1 (64% of TEWL) at Ta=35°C to 15.0±2.1 mg g-1 h-1 (78% of TEWL) at Ta=45°C, and the CEWL of cool-acclimated doves increased from 2.7±0.7 mg g-1 h-1 at Ta=35°C to 7.8±3.4 mg g-1 h-1 at Ta=45°C. CEWL in heat-acclimated doves was significantly higher than that of cool-acclimated doves at Ta=40°C (t=6.337; P<0.001) and at Ta=45°C (t=3.517; P=0.003), but not at Ta=35°C (Fig. 1C). At Ta=35°C, 40°C and 45°C, the mean CEWL in heat-acclimated doves was equivalent to 136%, 187% and 192%, respectively, of the corresponding rates in cool-acclimated doves (Fig. 1C). Surface area-specific CEWL increased from 1.4±0.4 mg cm-2 h-1 at Ta=35°C to 4.1±1.7 mg cm-2 h-1 at Ta=45°C in the cool-acclimated doves, and from 1.9±0.6 mg cm-2 h-1 at Ta=35°C to 7.7±1.0 mg cm-2 h-1 at Ta=45°C in the heat-acclimated doves.
The contribution of CEWL to TEWL did not vary significantly between the three experimental Ta values in cool-acclimated doves (RM-ANOVA, F2,4=3.119; P=0.100), although CEWL/TEWL decreased slightly with increasing Ta (Fig. 2). In contrast, the contribution of CEWL increased significantly with increasing Ta in the heat-acclimated doves (RM-ANOVA, F2,4=13.281; P=0.003) from 64±7% of TEWL at Ta=35°C to 78±2% of TEWL at Ta=45°C (Fig. 2). The contribution of CEWL to TEWL did not differ between the cool- and heat-acclimated groups at Ta=35°C (t=1.614; P=0.09), but was significantly greater in heat-acclimated doves at Ta=40°C (t=7.833; P<0.001) and Ta=45°C (t=5.593; P<0.001; Fig. 2).
|
Metabolic rate
Metabolic rates did not show significant variation between the three
experimental Ta values in either the cool-(RM-ANOVA,
F2,4=0.480; P=0.636) or heat-acclimated groups
(RM-ANOVA, F2,4=1.139; P=0.367;
Fig. 3). The mean metabolic
rate for cool-acclimated doves was 7.1±0.5 mW g-1, and the
mean metabolic rate for heat-acclimated doves was 6.3±0.8 mW
g-1. At Ta=45°C, the mean metabolic rate of
the cool-acclimated doves was significantly higher (t=2.726;
P=0.013) than that of the heat-acclimated doves
(Fig. 3).
|
Body temperature and skin temperature
Our sample sizes for Tb were in some cases smaller than
those for EWL and metabolic rate because doves sometimes initially struggled
and dislodged the thermocouples shortly after being placed in the metabolism
chamber. The mean Tb of cool-acclimated doves was
significantly higher than that of the heat-acclimated doves
(Table 1) at both
Ta=40°C (t=4.314; P=0.004) and
Ta=45°C (t=2.537; P=0.019). This
observation is consistent with the doves' behavior upon removal from the
metabolic chamber at the termination of the measurements at
Ta=45°C. Whereas heat-acclimated doves showed no
indication of panting or gular flutter, all five cool-acclimated doves
exhibited pronounced panting behavior.
|
Whole-body water vapour diffusion resistance
In both the heat- and cool-acclimated doves, rv
decreased significantly with increasing Ta
(Fig. 4). In the
heat-acclimated doves, mean rv decreased by 78% from
172±78 s cm-1 (N=3) at
Ta=35°C to 38±8 s cm-1
(N=5) at Ta=45°C.
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Discussion |
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Another way that partitioning of evaporative losses affects thermoregulation and water balance is through the increased heat loads associated with panting and gular flutter. At Ta=45°C, cool-acclimated doves had REWL rates that were approximately double those of heat-acclimated doves, and metabolic rates 35% greater than those of heat-acclimated doves, suggesting that a reliance on respiratory heat loss is more energetically costly than cutaneous heat loss. However, an analysis of the relative energetic costs and benefits of different patterns of evaporative water loss partitioning requires a complete understanding of the mechanisms responsible for adaptive decreases in skin water vapour diffusion resistance. Changes in the physical properties of the skin and/or the circulatory system may entail longer-term energetic costs associated with structural changes in the epidermis that are currently unquantified.
The Tb values we observed in heat-acclimated
white-winged doves were similar to those reported by Marder and Arieli
(1988) for heat-acclimated
rock doves (Columba livia) at 30°C > Ta
> 60°C. At Ta=45°C, the mean
Tb of cool-acclimated white-winged doves
(42.9±0.4°C) was slightly lower than that observed in
non-acclimated C. livia (43.4±0.7°C;
Marder and Arieli, 1988
).
The increases that we observed in the CEWL of heat-acclimated doves
primarily resulted from decreases in whole-body water vapour diffusion
resistance (Fig. 4). Whole-body
water vapour diffusion resistance rv is the sum of skin
(rvs), plumage (rvc) and boundary
layer (rva) resistances. Of these resistances, however,
the plumage and boundary layer comprise a small fraction of the total
resistance, and that of the skin (rvs) comprises 75-94% of
rv (Webster et al.,
1985). Hence, the lower rv values that we
observed in heat-acclimated doves primarily reflect changes in the resistance
of the skin. Two broad categories of mechanisms can potentially lead to
changes in skin resistance to water vapour diffusion
(Webster et al., 1985
). The
first category includes structural changes affecting the permeability of the
skin, and the second includes mechanisms affecting peripheral blood supply.
The available evidence suggests that mechanisms from both these categories may
be involved in increasing avian CEWL in response to thermal acclimation. Lipid
bodies in the epidermis are the major determinant of skin permeability to
water in vertebrates (Hadley,
1989
) and several studies have demonstrated that
acclimation-induced changes in avian CEWL correspond with changes in epidermal
lipid structure and abundance (Menon et al.,
1988
,
1989
,
1996
). The epidermis of
heat-acclimated rock doves included modified areas of greater thickness and
different intracellular structure compared to non-acclimated and
cold-acclimated birds (Peltonen et al.,
1998
). Recently, Haugen et al.
(2003
) attributed
acclimation-induced variation in the CEWL of hoopoe larks (Alaemon
alaudipes) to differences in the lipid composition of the epidermis.
These authors found that CEWL was negatively correlated with the proportion of
ceramides in the stratum corneum. Hoopoe larks acclimated to
Ta=35°C exhibited higher proportions of ceramides,
lower proportions of free fatty acids and sterols, and reduced CEWL compared
to larks acclimated to Ta=15°C
(Haugen et al., 2003
).
Ultrastructural changes permit more rapid water vapour diffusion across the
avian epidermis, but a second critical component of acclimation-induced
increases in CEWL appears to be an increased supply of water to the epidermis.
In rock doves, increased skin capillary hydrostatic pressure, rather than
increased blood flow per se, appears to be an important driving force
behind acclimation-induced elevated CEWL
(Ophir et al., 2002). The
inhibition of ß-adrenergic receptors or the stimulation of
2-adrenergic receptors (by propanolol and clonidine
administration, respectively) led to increased arterial blood flow and
decreased venous blood flow in heat-acclimated doves, measured using laser
Doppler flowmetry (Ophir et al.,
2002
). These authors argued that in heat-acclimated rock doves,
increased hydrostatic pressure in the skin microvasculature is achieved by
adrenergic control of arterial and venous blood flow, and results in elevated
water outflow from capillaries leading to elevated CEWL. These adjustments in
epidermal water supply presumably occur over shorter time scales than
structural changes in skin permeability, and may well be responsible for rapid
adjustments in CEWL such as those reported by Hoffman and Walsberg
(1999
) in mourning doves. In
the present study, we did not investigate the mechanism(s) responsible for
increased CEWL in heat-acclimated white-winged doves. At best, we can
speculate that similar mechanisms to those discussed above led to higher
CEWL/TEWL. Our data do reveal, however, that the differences in skin
resistance between cool- and heat-acclimated white-winged doves were
approximately constant at all three experimental Ta values
(Fig. 4).
Ecological and evolutionary implications
As in other Columbiforme species
(Webster and King, 1987;
Withers and Williams, 1990
;
Hoffman and Walsberg, 1999
), a
large proportion of TEWL in Z. a. mearnsii occurred cutaneously. The
CEWL/TEWL ratios we observed in cool-acclimated Z. a. mearnsii were
similar to the ratios exhibited by mourning doves Z. macroura housed
indoors at Ta=30°C
(Hoffman and Walsberg, 1999
).
The CEWL/TEWL ratios in heat-acclimated Z. a. mearnsii are among the
highest recorded (Wolf and Walsberg,
1996
), and are comparable to the ratios observed in Australian
Spinifex pigeons (Geophaps plumifera;
Withers and Williams, 1990
).
In the latter study, CEWL represented 70-80% of TEWL at all
Ta values between 0°C and 40°C
(Withers and Williams, 1990
).
Our data, together with recent data on TEWL partitioning in mourning doves
(Hoffman and Walsberg, 1999
)
and four species of larks (Tieleman and
Williams, 2002
), support the view that avian patterns of TEWL
partitioning exhibit considerable taxonomic variation
(Wolf and Walsberg, 1996
).
Differences in the relative importance of CEWL appear to be particularly
pronounced between Columbiformes and Passeriformes
(Wolf and Walsberg, 1996
).
Our data suggest that in addition to taxonomic differences in patterns of
TEWL partitioning, there may be variation in the phenotypic plasticity of
these patterns. Tieleman and Williams
(2002) investigated changes in
the partitioning of TEWL in response to thermal acclimation in four species of
larks, namely hoopoe larks Alaemon alaudipes, Dunn's larks
Eremalauda dunni, skylarks Alauda arvensis and woodlarks
Lullula arborea. CEWL in A. alaudipes was 22% lower in
individuals acclimated to Ta=35°C for 3 weeks than in
individuals acclimated to Ta=15°C, but no differences
were evident in any of the other species
(Tieleman and Williams, 2002
).
On the basis of these results, Tieleman and Williams
(2002
) concluded that
acclimatization plays a minor role in determining CEWL.
Extrapolating physiological data collected in the laboratory to field conditions is potentially problematic and often speculative. For instance, the variable ambient water vapour pressures experienced by wild birds may affect TEWL partitioning, and patterns of partitioning in active birds are probably different from those of resting birds. Nevertheless, our data suggest that in free-ranging Z. a. mearnsii, CEWL varies in response to thermal acclimatization, and that the relative importance of REWL and CEWL at any particular time of year reflects the preceding thermal conditions. Moreover, we argue that the ability of Z. a. mearnsii to tolerate high Ta values, together with the high radiative heat loads associated with foraging in the open during mid-summer in the Sonoran Desert, is at least partly dependent on thermal acclimatization earlier in the season.
Currently data on the partitioning of TEWL at Ta
35°C are available for 12 species from four avian orders (Galliformes,
Anseriformes, Columbiformes and Passeriformes; reviewed in
Wolf and Walsberg, 1996
).
Hence, there are currently too few data to generate hypotheses concerning the
phylogenetic distribution of patterns of TEWL partitioning, or the evolution
of these patterns. The observation that in Z. a. mearnsii the
relative contributions of REWL and CEWL vary in response to short-term thermal
acclimation has important implications for future work. Firstly, measurements
of REWL and CEWL need to account for the possible influence of thermal
acclimation prior to the measurements. Secondly, data used for comparative
analyses to need to be carefully selected to ensure that taxonomic variation
in TEWL partitioning is not confounded by the effects of
acclimation/acclimatization. A related issue concerns comparing data from
species in which TEWL partitioning is sensitive to thermal acclimation to data
from species in which it is not.
In summary, our data provide evidence of plasticity in the partitioning of avian evaporative water losses in response to short-term thermal acclimation. The capacity of white-winged doves, and possibly other species, to alter TEWL partitioning over relatively short time scales has important implications for thermoregulation and water balance at high environmental temperatures. Our data also reveal that the degree of plasticity in the partitioning of TEWL varies greatly between avian taxa.
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Acknowledgments |
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References |
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