Phenotypic flexibility in cutaneous water loss and lipids of the stratum corneum
1 Department of Evolution, Ecology and Organismal Biology, 318 W. 12th
Avenue, Columbus, OH 43210, USA
2 Zoological Laboratory, University of Groningen, PO Box 14, 9750 AA Haren,
The Netherlands
Author for correspondence (e-mail:
williams.1020{at}osu.edu)
Accepted 11 July 2003
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Summary |
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Key words: cutaneous water loss, stratum corneum, ceramide, free fatty acid, lipid, hoopoe lark, Alaemon alaudipes
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Introduction |
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The sum of evaporative water loss from respiratory passages and from skin -
total evaporative water loss (TEWL) - is the major avenue of water loss to the
environment, especially for small species of birds in which TEWL is five times
greater than urinary/fecal water loss
(Bartholomew, 1972;
Dawson, 1982
;
Williams and Tieleman, 2000
).
There exists substantial evidence that TEWL is reduced in species of birds
that live in deserts, with mesic species having rates of TEWL nearly double
those of species from deserts (Williams,
1996
; Williams and Tieleman,
2000
; Tieleman et al.,
2003
).
Early investigators assumed that most evaporative water loss took place
across respiratory passages and that cutaneous water loss (CWL) played a minor
role in thermoregulation (Mount,
1979; Bartholomew and Cade,
1963
). Subsequent work has shown that CWL can equal or exceed
evaporation from respiratory passages at moderate Tas
(Dawson, 1982
;
Tracy and Walsberg, 2001
;
Webster and King, 1987
;
Wolf and Walsberg, 1996
). In a
study on larks, Tieleman and Willliams
(2002
) found that CWL
accounted for 50-70% of TEWL at 25°C and that surface-area-specific CWL
was about 30% lower in arid species compared with ones living in mesic
environments. They hypothesized that natural selection has equipped resident
desert birds with a mechanism(s) that reduces water loss through the skin, at
least at moderate Tas, as a water conservation
mechanism.
Natural selection could be responsible for reduced TEWL and CWL found in
desert larks (Bennett, 1997;
Feder et al., 2000
;
Williams and Tieleman, 2001
;
Tieleman et al., 2003
). We
know that the magnitude of TEWL is a heritable trait, at least in mammals
(Furuyama and Ohara, 1993
),
and, by inference, we assume that rates of CWL are influenced by heritable
factors. Hence, it could be that phenotypes with a stronger barrier to water
vapor diffusion have been selected in deserts. Alternatively, phenotypic
plasticity, including reversible phenotypic flexibility (acclimation;
Piersma and Lindstrom, 1997
)
and developmental plasticity (Pigliucci,
2001
), can lead to covariation between physiological traits and
environmental variables. Studies on the relative importance of phenotypic
plasticity and genetic variation in the production of phenotypic traits among
birds are few. Williams and Tieleman
(2000
) tested whether hoopoe
larks (Alaemon alaudipes) acclimated to 15°C or 35°C for 3
weeks altered their TEWL; they found that those acclimated to 35°C had a
TEWL 23% lower than the 15°C group. This acclimation experiment was
repeated the following year and also included skylarks (Alauda
arvensis) and woodlarks (Lullula arborea), from The Netherlands,
and Dunn's larks (Eremalauda dunni), from the Arabian desert. Results
showed that skylarks, woodlarks and Dunn's larks did not change their TEWL
significantly with acclimation temperature, but that hoopoe larks did, the
latter finding being consistent with previous results; mass-specific TEWL for
hoopoe larks was 22% lower in the 35°C group
(Tieleman and Williams, 2002
).
In all experiments, TEWL was consistently lower in desert species, and
acclimation could not account for the magnitude of differences
(Tieleman and Williams,
2002
).
Tieleman and Williams
(2002) also showed that
changes in TEWL were attributable to changes in CWL and not respiratory water
loss (RWL). CWL in the hoopoe lark decreased by 22% in the 35°C-acclimated
group but did not decrease for the other three species. These results suggest
that hoopoe larks alter the permeability of their skin in response to
acclimation to temperature but that the other three species do not.
The skin of birds is composed of a thicker (120 µm) vascularized dermis
and a thin (13-22 µm) non-vascular epidermis that has two layers: (1) a
viable layer composed of the stratum transitivum, stratum intermedium and the
mitotically active stratum basale and (2) an outer layer of cornified
non-living cells (corneocytes) embedded in a lipid matrix called the stratum
corneum (SC; Lucas and Stettenheim,
1972). The lipid layers of the SC constitute 10-15% of its dry
mass (Gray and Yardley, 1975
)
and primarily consist of cholesterol, ceramides (amides of fatty acids with
hydroxylated long-chain amines) and free fatty acids
(Elias and Friend, 1975
;
Wertz et al., 1986
;
Menon and Menon, 2000
). In the
SC of mammals, ceramides account for as much as 50% of the total lipids
(Raith and Neubert, 2000
).
From work mostly on mammals, but also a few domestic species of birds,
evidence has accumulated that the SC forms the barrier to water vapor
diffusion from the animal to the environment
(Blank, 1953
;
Blank et al., 1984
;
Golden et al., 1987
;
Warner et al., 1988
;
Elias and Menon, 1991
;
Peltonen et al., 2000
).
Haugen et al. (2003) have
shown that free fatty acids, cholesterol and ceramides are the major
constituents of SC in wild larks (skylarks, woodlarks, hoopoe larks and Dunn's
larks) from mesic, semi-arid and arid environments. They reported that CWL was
reduced among larks inhabiting deserts, but their data did not support the
hypothesis that birds from desert environments have larger quantities of
lipids per unit dry mass of the SC compared with larks from more mesic
environments. Instead, larks in arid environments had a higher proportion of
ceramides, especially the more polar fractions 4-6, and a smaller proportion
of free fatty acids in their SC, an adjustment that apparently reduced CWL.
This implies that subtle changes in the ratios of lipid classes alter the
movement of water vapor through the skin. They proposed that desert birds have
higher proportions of ceramides in their SC and lower proportions of free
fatty acids because this combination allows the lipid lamellae to exist in a
more highly ordered crystalline phase and, consequently, creates a tighter
barrier to water vapor diffusion (Bouwstra
et al., 2003
).
Given that hoopoe larks adjust their CWL when acclimated to 35°C
compared with individuals acclimated to 15°C but that skylarks, woodlarks
and Dunn's larks do not (Tieleman and
Williams, 2002), we predicted that hoopoe larks acclimated to
35°C would alter the lipid composition of their SC, resulting in a
decrease in CWL, but that skylarks, woodlarks and Dunn's larks would not. In
particular, in light of the results of Haugen et al.
(2003
), we hypothesized that
hoopoe larks acclimated to 35°C would increase the proportions of polar
ceramide content and decrease the proportions of free fatty acids in their SC
compared with individuals acclimated to 15°C but that skylarks, woodlarks
(both mesic species) and Dunn's larks (another desert species) would not alter
ratios of lipid classes in their SC with acclimation.
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Materials and methods |
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Environments
Birds in The Netherlands were captured during the breeding season in the
province of Drenthe (52°52' N, 06°20' E), where rainfall
averages 750 mm per year and mean maximum Ta in July is
21.7°C (Tieleman et al.,
2003). In Saudi Arabia, birds were captured in late spring in
Mahazat as Sayd, a reserve in the Arabian Desert (22°15' N,
41°50' E), where average yearly rainfall is 90 mm and maximum
Ta in July is 40.2°C (National Wildlife Research
Center, unpublished).
Acclimation
In order to assess the flexibility in lipids of the SC as a result of
acclimation, we randomly assigned individuals to one of two groups
(N=8 in each group). In each group, half of the individuals from each
species were housed for 3 weeks in a room with a constant
Ta of 15±2°C (12 h:12 h L:D), a temperature
that is below the thermal neutral zone of all four species and close to the
Ta experienced by skylarks and woodlarks in The
Netherlands during the breeding season, and the other half were housed for 3
weeks in a room with a constant Ta of 35±2°C
(12 h:12 h L:D), which mimicked the Ta of the Arabian
desert during spring. Each treatment group contained equal proportions of
males and females and was similar in mean body mass. Humidity was not
controlled in rooms where birds were housed but was recorded with a relative
humidity probe (Vaisala, Woburn, MA, USA) or with a dew point hygrometer (M4;
General Eastern, Woburn, MA, USA). The absolute humidity was 5-7 g
m-3 in the 15°C rooms and 9-12 g m-3 in the 35°C
rooms (Tieleman et al.,
2003).
Cutaneous water loss
For measuring CWL [mg H2O cm-2 day-1] at
25°C, we followed the protocol of Tieleman and Williams
(2002). In brief, we measured
RWL and CWL simultaneously by placing a bird fitted with a plastic mask in a
metabolism chamber into which dry, CO2-free outside air was drawn.
Steel metabolic chambers had an airtight Plexiglas lid and were water-jacketed
to control Ta by a circulating water bath (RTE-140;
Neslab, Portsmouth, NH, USA; +0.2°C). Birds were placed on a
wire-mesh platform over a layer of mineral oil to trap excrement, excluding it
as a source of water in measurements. We measured the water vapor density of
air entering the chamber (
v-in) by routing air before and
after experiments around the chamber and through the dewpoint hygrometer. Air
pulled through the mask contained all respiratory gases and was routed through
polytetrafluroethylene (PTFE) tubing, a dew point hygrometer, columns of
Drierite and ascarite (to remove H2O and CO2), a
previously calibrated Brooks mass flow controller (model 5850E;
Levy, 1964
) and a vacuum pump.
Chamber volume and flow rates used are reported in Tieleman and Williams
(2002
). We calculated the flow
rate through the dew point hygrometer
(
e1) by adjusting the value
recorded at the mass flow controller for H2O and CO2
added (Tieleman and Williams,
2002
), the latter estimated assuming a respiratory quotient (RQ)
of 0.71 (King and Farner,
1961
). In practice, these adjustments were less than 1%. To
calculate RWL, we used the equation of Tieleman and Williams
(2002
). Air was also drawn
from the chamber through a second exit port and passed along a second train
identical to the first except that air from the vacuum pump was vented to the
room. Calculation of CWL was complicated by the fact that air within the
chamber that contained water vapor from the skin was exiting through two
ports. We calculated flow rate of air leaving the chamber by summing the flow
rates from the mask (
e1)
and from the chamber (
e2)
and determined CWL using the equation CWL=(
v-chamber -
v-in)(
e1+
e2).
After a 2-3 h equilibration period, we recorded the dew points of inlet,
chamber and mask air, the temperature of the dew point hygrometers and the
Ta in the chamber using a data logger model (21X or CR23X;
Campbell Scientific, Logan, UT, USA). When, during the third hour of
measurements, the traces for dew points were stable for at least 10 min, we
noted these times and used these data for calculations. Validated by Tieleman
and Williams (2002
), this
system measures water loss from the skin, including the head and neck,
together with water lost from the eyes. CWL measurements were taken for each
bird before and after the 3-week acclimation period.
Separation of stratum corneum
After the final determination of CWL, we determined the mass of each bird,
sacrificed it, plucked its feathers and removed its skin. We pinned the skin
to a thin sheet of Teflon and dipped it in distilled water at 65°C for 3
min and then gently peeled the epidermis from the dermis
(Wertz et al., 1986;
Haugen, 2003
). Next, we placed
the epidermis in a vial containing 0.5% trypsin in phosphate-buffered saline
(pH 7.4; 370 mOsm) and placed it in a refrigerator (4°C) overnight. The
following day, we rinsed the intact SC tissue with distilled H2O to
remove epithelial cells, re-immersed the remaining tissue in fresh 0.5%
trypsin solution and allowed it to stand at 38±2°C for 3 h. After a
final rinse in distilled H2O, we separated SC tissue from the
solvent by filtering and froze it at -80°C under an atmosphere of argon.
Thereafter, we lyophilized the SC tissue to dryness (12 h), sealed it in a
test tube, again under an atmosphere of argon, and then stored it at -80°C
pending further analysis. In preliminary trials, we confirmed that 12 h of
lyophilization was adequate to completely dry the sample by repeatedly
weighing samples during the drying process
(Haugen, 2003
).
Identification of lipids
After transport to the USA, we re-lyophilized the SC tissue, weighed it to
determine dry mass and extracted the lipids with a chloroform:methanol series
of 2:1, 1:1 and 1:2 v/v for 2 h at each step
(Law et al., 1995). Chemicals
and tissues were placed in covered glass funnels equipped with Teflon
stopcocks and pre-extracted cotton plugs. We combined extracts and evaporated
the mixture under nitrogen. To prepare the lipid residue for thin layer
chromatography (TLC), we dissolved the extracted lipids in 200 µl
chloroform:methanol 2:1 containing the antioxidant butylated hydroxytoluene
(50 mg l-1).
We separated classes of lipids using analytical TLC on 20 cmx20 cm
glass plates coated with silicic acid (0.25 mm thick; Adsorbosil-Plus 1;
Alltech Associates, Deerfield, IL, USA;
Downing, 1968). Identification
of lipids was achieved by comparison of their chromatographic properties with
known standards. To prepare our plates, we placed them in chromatographic
tanks with a mixture of chloroform:methanol (2:1) until the solvent reached
the top, thereby removing any contaminants, activated them in an oven at
110°C and scored the adsorbent into 6 mm-wide lanes
(Wertz et al., 1986
). Using a
Teflon-tipped Hamilton syringe (#80055; Hamilton, Reno, NV, USA), we pipetted
5 µl of either lipid extract from the SC or a mixture of lipid standards
onto a pre-absorbent area on the lower portion of the plate. We ran each
sample in triplicate and used the mean value of these determinations in our
analyses. Our standard lipid mixture included non-hydroxy fatty acid ceramides
(a sphingosine base with a mixture of octadecanoic and
cis-15-tetracosenoic acids as the N-acyl fatty acid groups),
cholesterol and stearic acid (a free fatty acid), all purchased from Sigma (St
Louis, MO, USA), and dissolved in chloroform:methanol (2:1) in concentrations
from 0.625 mg ml-1 to 10 mg ml-1.
Two solvent systems were employed to separate lipids of different polarities. For the more non-polar lipids, such as cholesterol and free fatty acids, we developed plates to the top in tanks of hexane, followed by toluene, followed by a mixture of hexane:ethyl ether:acetic acid (70:30:1), run to 12 cm from the bottom. For the more polar lipids, including the six classes of ceramides, plates were developed twice with a mixture of chloroform:methanol:acetic acid solution (190:9:1) followed by development with a mixture of hexane:ethyl ether:acetic acid (70:30:1).
We visualized bands of lipids by spraying plates with a charring agent (a
solution of 3% cupric acetate in 8% phosphoric acid) and then placing the
plate on a 20 cmx20 cm polished aluminum hotplate that was slowly heated
to 220°C, carbonizing all lipids
(Wertz et al., 1986).
Bands of lipids were quantified using photodensitometry
(Downing, 1968). We scanned
each lane on plates with a Hewlett Packard scanner and the computer software
tnimage
(http://entropy.brni-jhu.org/tnimage.html)
to determine areas of charred regions. At the same time, we scanned lanes that
contained a series of known concentrations of standards in order to establish
standard curves (Vecchini et al.,
1995
; Johnson,
2000
).
Although analytical TLC is a standard procedure, we wanted to estimate our
error in using the method to quantify concentrations of lipids. To do so, we
pipetted known concentrations of cholesterol, ranging from 4.2 mg
ml-1 to 14.3 mg ml-1, onto plates, in triplicate, and
followed our protocol for determining lipid concentrations
(Haugen, 2003). We averaged
values for the three lanes for each trial and compared these results with the
known concentration. Calculated as (observed - actual/actual)x100, the
mean error was ±0.82%, indicating that our method provides a reasonable
estimate of quantities of lipids (Haugen
et al., 2003
).
Even though bands on chromatograms coincided with known classes of lipids,
we wanted to confirm our identification of lipids. Using our lipid extracts
from the SC of larks, we ran preparative TLC on 0.5-mm silica gel plates,
again divided into 6-mm lanes, using the same mobile phase as described
earlier. After spraying the plate with an ethanol solution of
8-hydroxy-1,3,6-pyrenetrisulfonic acid tri-sodium salt (10 mg per 100 ml),
lipid bands were visualized by viewing under ultraviolet light. Then, bands
were scraped off into a glass dish, mixed with a solution of
chloroform:methanol (2:1) to extract lipids, which were subsequently eluted
for analysis (Wertz et al.,
1986). For free fatty acids and sterols, we added a
trimethylsilylation reagent
[pyridine:hexamethyldisilazane:trimethylchlorosilane (9:3:1); Supelco,
Bellefonte, PA; Bleton et al.,
2001
] to prepare the lipids for gas chromatography-mass
spectrometry (GC-MS). Analyses were carried out on a Finnigan Trace GC-MS with
a 30 mx0.32 mm i.d. fused silica column and with a 0.25 µm XTI-5 film
of 5% diphenyl:95% dimethyl polysiloxane (Restek, Bellefonte, PA). We verified
ceramide bands using electrospray ionization tandem mass spectrometry on a
Bruker Esquire LC/MS-MS system in positive ion mode
(Raith and Neubert, 2000
).
Statistics
All statistical analyses were performed using SPSS version 11.0 with the
null hypothesis rejected at P<0.05. We used General Linear Model
procedure for analysis of variance when comparing lipid quantities for each
group of lipids from the SC of larks. Our model included lipid class as a
dependent factor and both species and acclimation treatment as fixed factors.
After testing for the significance of the two-way interaction term, we removed
it when insignificant and tested for the significance of the fixed factors.
For comparisons of lipid concentrations among species, we performed analysis
of variance (ANOVA) followed by a Tukey's test to identify significant
differences between species. To search for correlations, we calculated
Spearman's rho. Means are in units of mg lipid g-1 dry mass of SC
±1 S.E.M., unless otherwise specified. All proportions were
arcsine transformed prior to statistical analyses. N=8 for each
species; N=8 for each group. Experiments were carried out in The
Netherlands under license #DEC2425, in Ohio under ILACUC permit #00A0161 and
in Saudi Arabia with permission from the National Commission for Wildlife
Research and Development.
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Results |
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Among-species comparisons - lipid quantities
We investigated differences in quantities of lipid classes (mg
g-1 dry mass SC) among species that were exposed to the different
acclimation temperatures. There was no significant interaction between species
and treatment for any of the lipid classes (all P>0.05), although
the interaction term for percent total ceramides and for amount of cholesterol
in the SC were nearly significant (Fig.
1; P=0.06 for both). With the interaction term removed,
we found significant effects for species for free fatty acids, free sterols,
total ceramides, ceramide 1 and ceramide 3 (F=24.5,
P<0.001; F=32.4, P<0.001; F=6.7,
P<0.001; F=15.2, P<0.001; F=3.6,
P<0.02, respectively). A post-hoc test showed that hoopoe
larks and Dunn's larks, both desert species, had significantly lower
quantities of free fatty acids, cholesterol and ceramide 1 per unit dry mass
of SC than did skylarks and woodlarks from The Netherlands. We did not find an
effect of treatment in any species. However, for hoopoe larks, the 95%
confidence intervals for total ceramides, ceramide 3 and ceramide 4/5 for the
treatments did not overlap.
|
Among-species comparisons - lipid proportions
Because proportions of lipid classes seem to be important in water barrier
formation (Haugen et al.,
2003), we also investigated the effect of acclimation on the
proportion of each lipid class in the SC. With proportion of lipids as the
dependent factor and species and acclimation treatment as fixed factors in our
model, we found no significant interaction between species and treatment for
any of the lipid classes (Fig.
2; all P>0.05). When we removed the interaction term,
we found significant differences between the species in proportions of free
fatty acids, free sterols and total ceramides
(Fig. 2; F=8.1,
P<0.001; F=4.1, P=<0.02; F=19.6,
P<0.001, respectively). Ceramides 2, 3, 4/5 and 6 were
significantly different among species (F=13.6, P<0.001;
F=6.2, P<0.001; F=16.4, P<0.001;
F=4.2, P<0.01). Post-hoc tests revealed that the
two desert species - Dunn's and hoopoe larks - formed homogeneous subsets for
reduced proportions of free fatty acids and free sterols, while also forming a
homogeneous subset for increased proportions of total ceramides when compared
with the two mesic species - woodlarks and skylarks. Hoopoe larks and Dunn's
larks had higher proportions of ceramides 2, 3, 4/5 and 6 in their SC than did
woodlarks and skylarks. We found no significant effect of treatment in any of
our comparisons.
|
CWL and lipids within hoopoe larks
Because we elucidated differences in CWL relative to acclimation
Ta in hoopoe larks, but not other species, we explored
changes among lipids in the SC of hoopoe larks between treatment groups.
Hoopoe larks acclimated to 35°C had significantly higher concentrations of
total ceramide per unit dry mass of SC (F=30.6, P<0.001)
and higher concentrations of polar ceramides: ceramides 3, 4/5 and 6
(F=6.4, P<0.03; F=17.7, P<0.001;
F=5.8, P<0.04, respectively). Hoopoe larks in the
35°C group also had significantly higher proportions of total ceramide in
their SC (F=6.6, P<0.03) and higher proportions of
ceramide 3 (F=6.5, P<0.03). Proportions of ceramide 4/5
were not significantly higher in the 35°C group (F=4.3,
P<0.06). We note that the SC of hoopoe larks acclimated to
15°C contained ceramide that totaled 32.4% of the lipids that we measured,
but the SC of birds acclimated to 35°C contained ceramide that totaled
40.8%, a significant increase for the latter of 26% (F=30.6,
P<0.001). Hence, as CWL was reduced in the 35°C group, the
proportion of total ceramide in the SC increased.
Correlations between CWL and lipids
We found a significant correlation with CWL and both % total ceramide
(Fig. 3; r=-0.58,
P<0.03, N=14) and % ceramide 4 (r=-0.61,
P<0.03, N=14).
|
Correlations among lipids in the SC
Using all species, we found that both % free fatty acids and % free sterols
were negatively correlated with % total ceramide
(Fig. 4; r=-0.86,
P<0.001, N=50; r=-0.35, P=0.013,
N=50, respectively). With values for individuals of each species
averaged, % free fatty acids again correlated negatively with % total
ceramides (r=-0.995, P=0.005, N=4). However, there
was no significant correlation between % free sterols and % total ceramides
(r=-0.93, P=0.07, N=4). The percentage of free
fatty acids in the SC was also negatively correlated with the percentage of
ceramides for fractions 2-6 (r=-0.52, P<0.001,
N=50; r=-0.34, P=0.016, N=50;
r=-0.78, P<0.001, N=50; r=-0.49,
P<0.001, N=50, respectively).
|
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Discussion |
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Given that hoopoe larks adjust their CWL when acclimated to 35°C
compared with individuals acclimated to 15°C, but skylarks, woodlarks and
Dunn's larks do not (Tieleman and
Williams, 2002), we predicted that hoopoe larks acclimated to
35°C would increase the proportions of polar ceramides and decrease the
proportions of free fatty acids in their SC compared with individuals
acclimated to 15°C, but that skylarks, woodlarks (two mesic species) and
Dunn's larks (another desert species) would not. Hoopoe larks in the 35°C
group had significantly higher proportions of total ceramide in their SC and
higher proportions of ceramide 3. Hence, as CWL was reduced in the 35°C
group, the proportion of total ceramide in the SC increased, in partial
agreement with our hypothesis. We did not find a significant decrease in the
proportion of free fatty acids, although the % of free fatty acids declined by
10.9%. Hence, we think that by adjusting lipid synthesis towards more polar
ceramides and less free fatty acids, hoopoe larks can alter the permeability
of their skin to water.
When comparing hoopoe larks acclimated to 15°C and 35°C, the 35°C group had a 19.2% decrease in total evaporative water loss and an 18.9% decrease in CWL, which corresponded with a 25.9% increase in the proportion of total ceramides in the SC. We did not see any significant changes in amounts or proportions of lipids in the SC among species that did not alter their CWL in response to acclimation. Why Dunn's larks do not adjust their CWL to acclimation temperature is not known, but it is noteworthy that hoopoe larks are permanent residents in the extreme arid regions in the Arabian Peninsula, including the Rub `al Khali, whereas Dunn's larks emigrate from arid regions during severe drought.
In summary, the proportion of ceramides and free fatty acids in the stratum
corneum in larks affects the rate of water loss through the skin. The lower
CWL and TEWL rates found in species of larks
(Williams and Tieleman, 2001;
Tieleman and Williams, 2003; Haugen et
al., 2003
; Tieleman et al.,
2003
) can be partially explained by a difference in the proportion
of total ceramides to free fatty acids in the SC, where an increased
proportion of ceramides causes a decrease in the water flux across the skin.
Hoopoe larks acclimated to 35°C had an 18.9% decrease in CWL compared with
the group acclimated to 15°C, which was due to a change in the lipid
composition in the SC. Specifically, it seems that an increase in the
proportion of the more polar ceramides and a decrease in the proportion of
free fatty acids caused a tighter barrier to water vapor in the skin of hoopoe
larks.
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Acknowledgments |
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Footnotes |
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References |
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