Cutaneous water loss and lipids of the stratum corneum in house sparrows Passer domesticus from arid and mesic environments
Department of Evolution, Ecology and Organismal Biology, Aronoff Laboratory, 318 W 12th Avenue, Columbus, OH 43210, USA
* Author for correspondence (e-mail: munoz-garcia.1{at}osu.edu)
Accepted 26 July 2005
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Summary |
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Although CWL was lower in sparrows from Arabia, and lipid composition of their SC differed, we could not detect differences between rates of water loss through non-living skin attached to glass vials (46.0±15.7 mg H2O cm-2 day-1 for sparrows in Saudi Arabia; 45.8±27.2 mg H2O cm-2 day-1 for sparrows in Ohio). These results suggest that biological control mechanisms interact with layers of lipids in the stratum corneum to adjust CWL to the environment.
Key words: cutaneous water loss, lipid, house sparrow, Passer domesticus, stratum corneum, desert
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Introduction |
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Total evaporative water loss, the sum of cutaneous water loss (CWL) and
respiratory water loss, is reduced in birds living in deserts compared to
those from mesic environments (Williams,
1996; Williams and Tieleman,
2000
). Evidence thus far indicates that this reduction in total
evaporative water loss cannot be explained by a decrease in respiratory water
loss (Tieleman et al., 1999
;
Tieleman and Williams, 1999
).
Exploring the idea that natural selection has influenced CWL in desert birds,
Tieleman and Williams (2002
)
measured CWL of four species of larks, two from mesic and two from arid
environments, and found that CWL was reduced in larks from arid
environments.
CWL is a function of the water vapor gradient between skin and air, and the
total resistance to vapor diffusion through skin, feathers and boundary layer
(Webster and King, 1987;
Wolf and Walsberg, 1996
;
Williams and Tieleman, 2001
).
Resistance across the skin contributes 70-95% of the total resistance
(Webster et al., 1985
).
Tieleman and Williams (2002
)
suggested that reduced CWL observed in desert larks could be achieved by
increasing resistance through the skin, and they proposed that changes in the
lipid content of the stratum corneum (SC) would serve this purpose.
The epidermis of the skin of birds consists of four layers, all derived
mitotically from the cells in the basal layer. Cells of the stratum basale,
the innermost layer, have a large Golgi apparatus that apparently synthesizes
lipids (Menon et al., 1986).
Cells of the stratum intermedium, the layer above basal cells, form
multigranular bodies (MGB), homologous to the lamellar bodies of mammals
(Landmann, 1980
;
Menon et al., 1986
). MGB are
membrane-bounded organelles about 0.5 µm in diameter that contain lipids,
mainly glycosphingolipids, cholesterol and phospholipids, which are thought to
be stacked in layers called lamellae
(Elias and Menon, 1991
). In
the stratum transitivum, it is thought that lamellae inside the MGB
deteriorate and MGB coalesce to form membrane-free neutral lipid droplets, at
least under normal circumstances
(Landmann, 1986
;
Elias and Menon, 1991
). At the
stratum transitivum-stratum corneum interface, lipid droplets are apparently
extruded into the intercellular spaces of the SC, creating the barrier to
water vapor diffusion (Scheuplein and
Blank, 1971
; Elias et al.,
1981
; Blank et al.,
1984
; Grubauer et al.,
1989
; Elias and Menon,
1991
; Menon and Menon,
2000
).
The SC consists of flattened, dead corneocytes embedded in a matrix of
lipids (Elias and Friend, 1975;
Menon, 2002
;
Wertz, 2000
). The main lipid
classes found in the SC of birds are cholesterol, free fatty acids, ceramides
(a molecule of sphingosine linked to a fatty acid) and cerebrosides (a
ceramide bound to a sugar; Menon et al.,
1986
; Wertz et al.,
1986
). If the SC is the barrier to water vapor diffusion, and if
the layer of dead corneocytes and lipids forms this barrier, it would seem
that the barrier properties would be the same even when skin is removed from
the bird.
Few studies have explored the association between the lipid composition of
the SC and CWL in birds. Working with eight species of larks along an
environmental gradient from mesic to arid, Haugen et al.
(2003a) found that larks
living in arid environments have a reduced CWL, a higher proportion of
ceramides, and a smaller proportion of free fatty acids in their SC. They
concluded that reduced CWL observed in desert larks was associated with
changes in ratios of lipid classes in the SC.
Acclimation experiments on single species suggest that CWL is associated
with the type and arrangement of lipids in the SC. Menon et al.
(1989) found that zebra
finches (Taeniopygia guttata) that were water-deprived for 45 days
reduced their transepidermal water loss by 50% compared to control birds. This
decrease was associated with changes in the lipid composition of the SC. When
birds were rehydrated, changes were apparently reversed
(Menon et al., 1989
). Haugen
et al. (2003b
) found that
Hoopoe larks Alaemon alaudipes L. acclimated to 35°C increased
the proportion of polar ceramides and decreased the proportion of free fatty
acids in the SC with respect to individuals acclimated to 15°C, and that
these changes in lipid composition were associated with a reduction in
CWL.
Transepidermal water loss is thought to be a passive diffusion process
influenced by the type and arrangement of lipids in the SC
(Pinnagoda, 1994;
Wilson and Maibach, 1994
;
Hoffman and Walsberg, 1999
).
If evaporation through the skin is a passive process, then rates of water loss
through the skin of a living bird, and rates of water loss through the same
skin removed from the bird, ought to be nearly the same. Although the physical
properties of the SC do influence CWL, biological mechanisms may also operate
in the live animal, enhancing the water barrier
(Elias, 2004
). Most of these
processes involve the creation of gradients of ions across the SC that
influence water permeation through lipid layers. For example, changes in the
pH and calcium gradient across the SC alter the permeability of the skin, and
affect barrier recovery after disruption
(Menon et al., 1994
;
Bernard et al., 2003
; Fluhr et
al.,
2004a
,b
).
Despite the variety of biological mechanisms known to modify the performance
of the permeability barrier in the skin, no studies have attempted to separate
the contribution of physical and biological factors in the formation of the
epidermal water barrier.
In this study we compared CWL of populations of house sparrows, one living in deserts (Saudi Arabia) and one living in a mesic environment (Ohio), and related CWL to lipid composition of the SC. We hypothesized that desert sparrows would have a lower CWL and that this reduction would be associated with changes in the lipids of the SC. We attempted to separate the physical properties of the barrier to water vapor diffusion from biological properties active in a living bird. We found that desert sparrows had a reduced CWL compared with sparrows from Ohio. Further, desert sparrows had larger concentrations of ceramides and cerebrosides in their SC and the proportion of cholesterol was lower in their SC. Despite this variation in lipid composition of the SC, when we measured water permeation through the dead skin in both groups of sparrows, we detected no differences between desert and mesic individuals. We concluded that water loss through the skin is not simply a passive process but rather an interaction between living cells of the epidermis and the non-living layers of the stratum corneum.
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Materials and methods |
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House sparrows in North America, members of the subspecies P. d.
domesticus, were introduced at the end of the 19th century from England
(Summers-Smith, 1988). House
sparrows in Saudi Arabia, P. d. indicus, are apparently native to the
area, although they depend on humans for access to water
(Cramp and Perrins, 1994
). The
population of house sparrows that we studied in west-central Saudi Arabia had
daily access to water, and probably would not be able to survive without it.
These two subspecies have been isolated from one another for about 5000 years
(Summers-Smith, 1988
).
Measurement of metabolic rate and evaporative water losses
We measured oxygen consumption, respiratory water loss and CWL using an
open-flow mask system, during November and December of 2003
(Gessaman, 1987;
Tieleman and Williams, 2002
).
We removed food from the cages of birds 2-3 h prior to measurements to ensure
postabsorptive conditions. Dissection of specimens at the end of measurements
confirmed that the digestive tract was empty. In Ohio, measurements were made
at night; in Saudi Arabia they were made during either the day or night.
Because we did not find significant differences between measurements made
during the day or night in Saudi Arabia, we pooled results (t=1.04,
d.f.=11, P>0.33).
Birds were placed in a water-jacketed steel metabolic chamber (29.5
cmx21.5 cmx28 cm) that had a Plexiglas lid rendered airtight by a
rubber gasket. We controlled the temperature of the air in the chamber using a
Neslab circulating water bath (model RTE-140) set at 30.0°C, a temperature
within the thermoneutral zone of sparrows
(Hudson and Kimzey, 1966).
Sparrows stood on a wire mesh platform over a layer of mineral oil that
trapped feces, eliminating them as a source of water in our measurements. We
quantified CWL and respiratory water loss separately using a plastic mask
system (Tieleman and Williams,
2002
). The mask covered the bill and nares, but did not cover the
eyes or head of the bird, so evaporation from these areas contributed to
CWL.
In our system, air coursed through Drierite®, soda lime and
Drierite® to remove water and CO2, then into the chamber. Air
was drawn through the mask, then routed to a dewpoint hygrometer (EdgeTech,
model 2001-C1-S3, Milford, MA, USA, in Ohio; General Eastern, model M4,
Woburn, MA, USA, in Saudi Arabia), columns of Drierite® and ascarite, a
mass-flow controller (Tylan, model FC 260, Billerica, MA, USA, in Ohio;
Brooks, model 5850, Hatfield, PA, USA, in Saudi Arabia), set at 600 ml
min-1, both calibrated with a bubble meter
(Levy, 1964), and into an
oxygen analyzer (Applied Electrochemistry S3A-II, Naperville, IL, USA).
Another air stream exited the chamber itself, and was directed through a
second circuit identical to the first at a flow rate of 400 ml
min-1, except that air was vented to the room after passing through
the dewpoint hygrometer and the vacuum pump. We verified that all respiratory
gases were captured by the mask by directing air from the chamber to the
oxygen analyzer: the fraction of O2 in chamber air was always
identical to inlet air.
Oxygen consumption, calculated using equation 4a of Withers
(1977), was converted to kJ
day-1 using 20.08 J ml-1 O2
(Schmidt-Nielsen, 1997
). To
estimate respiratory water loss, we used the equation
RWL=(
mask-
chamber)
(V'e1), where
chamber is absolute
humidity (g m-3) of air leaving the mask corrected to standard
temperature and pressure (STP),
mask is the
absolute humidity of air in the chamber (g m-3, STP),
and V'e1 is the flow rate of air leaving the mask
(Tieleman and Williams, 2002
).
To calculate V'e1, we assumed a respiratory quotient
of 0.71 (King and Farner,
1961
). CWL was determined as
CWL=(
chamber-
in)(V'e1+V'e2),
where
in is the absolute humidity of the air entering the
chamber (STP), and V'e2 is the flow rate of the
air leaving the chamber (Tieleman and
Williams, 2002
). After 2-3 h, when traces of O2
consumption were stable, we recorded oxygen consumption, dewpoint
temperatures, and temperature of the air in the dewpoint hygrometers. We
averaged data for oxygen consumption and dewpoint temperatures from traces
that remained stable for at least 10 min.
Dewpoint hygrometers were factory calibrated against a primary standard traceable to the National Institute of Standards and Technology, less than 1 year prior to measurements. However, to confirm the accuracy of dewpoint hygrometers at the time of measurements, compressed air was routed through a column of Drierite® to remove water, then through a Brooks mass-flow controller (model 5850E), calibrated with a bubble meter, at a rate of 1000 ml min-1. To saturate this air stream with water, we bubbled air through a 25 cm high column of distilled water at 20°C. Next we bubbled air through a water jacketed chamber filled with distilled water controlled at 12°C by a Neslab circulating water bath. Wet saturated air exited the chamber was directed to a dewpoint hygrometer. Air temperature into the chamber, measured with a thermocouple, was 12.0°C, whereas dewpoint temperatures were 11.7°C (General Eastern) and 11.3°C (EdgeTech), a deviation of 1-3% for General Eastern and 3-6% for our EdgeTech dewpoint hygrometer. These measurements were made in August 2005.
We also validated our ability to predict water loss from a bird using dewpoint hygrometry. Dry air was pushed through a mass-flow controller set at 1000 ml min-1. Air was then directed into a 125 ml sealed flask partially filled with about 75 ml of distilled water. Air exited the flask to a dewpoint hygrometer. We wanted to estimate the error using our system to calculate evaporative water loss. To do so, we calculated water loss gravimetrically, weighing the water in the flask when the system reached equilibrium and 2-3 h after, and compared the mass difference with the total evaporative water loss obtained from the dewpoint temperature using the equations given above. The average error was 0.86±1.96% (N=5 trials).
Passive water loss through skin removed from sparrows
To estimate the passive permeability barrier of the skin attributable to
the non-living SC, apart from active processes maintained by the living bird,
we affixed skin of the ventral apterium to a glass vial (surface area of
skin=2.13 cm2) filled with a solution of phosphate-buffered saline
(PBS; Na2HPO4 7H2O,
NaH2PO4 H2O monobasic, and NaCl in distilled
water, pH 7.4, 370 mOsm). Skin was glued to the edges of the vial with
cyanoacrylate glue. We ensured a complete seal of our preparation by turning
the vial upside down and examining for leaks. We then placed the vial in a
sealed container over a layer of Drierite® to ensure a low and constant
water vapor pressure. The container and contents were then set in an incubator
at 36°C, a temperature selected because it is near skin temperature of a
desert bird. An uncovered vial filled with PBS was also placed in the same
container and used as a control. After 8 h, a period previously determined for
rates of water loss from the vial to stabilize, we recorded the weight of the
vials using a balance (Metler, model AB204; 0.1 mg). We re-weighed the vials
2-3 h after the initial weighing.
Separation and identification of skin lipids
To isolate and quantify lipids of the SC of the sparrows, we weighed birds,
killed them, plucked their feathers and removed their skin
(Wertz et al., 1986; Haugen et
al.,
2003a
,b
).
We pinned the skin to a thin sheet of Teflon®, and immersed it into a
distilled water bath at 65°C for 3 min. Then, we gently peeled the
epidermis from the dermis. The epidermis was incubated at 4°C overnight in
a solution of 0.5% trypsin in PBS, allowing us to separate the SC from the
rest of the epidermis. The following day, we rinsed the SC with distilled
water, and reimmersed it in fresh 0.5% trypsin solution for 3 h at 38°C.
We then rinsed the SC with distilled water over a fine mesh of silk cloth to
remove any remaining feathers, and then froze the SC at -20°C in an
atmosphere of argon or nitrogen. Thereafter, we freeze-dried the SC for 12 h,
and stored it in a test tube at -20°C, again in an atmosphere of argon or
nitrogen.
After determining dry mass of the SC (±0.01 mg), weextracted lipids
with a mixture of chloroform:methanol 2:1, 1:1 and 1:2 v/v for 2 h, each step
containing 50 mg l-1 of the antioxidant butylated hydroxytoluene
(BHT; Law et al., 1995). We
then combined extracts and dried the solution using a stream of nitrogen with
an evaporimeter (N-EVAP, model 11155-O, Organomation Associates, Inc., Berlin,
MA, USA).
Lipid classes were separated using analytical thin layer chromatography (TLC) on 20 cmx20 cm glass plates coated with silicic acid (0.25 mm thick; Adsorbosil-Plus 1, Altech, Deerfield, IL, USA). We removed contaminants from the plates by developing them with a mixture of chloroform:methanol (2:1, v/v) to the top, and thereafter activated plates in an oven at 110°C for 30 min. Then, we divided each plate into 29 6 mm-wide lanes. We prepared a series of five standards of known concentration, each containing nonhydroxy fatty acid ceramides (a sphingosine base with a mixture of octodecanoic and cis-15-tetracosenoic acids as the N-acyl fatty acid groups), galactocerebrosides, cholesterol, and a mixture of free fatty acids. We dissolved standards in chloroform:methanol (2:1, v/v) in concentrations ranging from 0.30 mg ml-1 to 10 mg ml-1. Previous work indicated that this range covered concentrations of lipids found in our TLC plates. A duplicate series of standards was run on each plate. To prepare our samples for TLC, we re-dissolved the extracted lipids in 200 µl of chloroform:methanol (2:1, v/v) containing BHT. We pipeted 5 µl of each lipid extract in triplicate in the pre-adsorbent area of the plates using a Teflon-tipped Hamilton syringe. Two solvent systems were used, one for polar lipids, such as ceramides and cerebrosides, and another for non-polar lipids, free fatty acids and cholesterol. To separate ceramides and cerebrosides, we developed plates with a mixture of chloroform:methanol:acetic acid (190:9:1, v/v) to the top, followed by development with hexane:ethyl ether:acetic acid (70:30:1, v/v) run to 12 cm from the bottom. For sparrows, this procedure yielded four bands of ceramides and three bands of cerebrosides. Cholesterol and free fatty acids were separated by development with hexane to the top of the plate, followed by toluene to the top, and finally a development with hexane:ethyl ether:acetic acid run to 12 cm from the bottom. We visualized bands of lipids by spraying the plates with a solution of 3% cupric acetate in 8% phosphoric acid, and then placing the plates on a 20 cmx20 cm aluminum hotplate slowly raised to 220°C over the course of 2 h.
To quantify the concentration of lipid classes, we scanned the plates with
a Hewlett Packard scanner, and measured the amount of each class by
photodensitometry using the computer software TN-Image (T. J. Nelson, 2003:
Shareware software available at
http://entropy.brni-jhu.org/tnimage.html).
Because Haugen et al.
(2003a,b
)
found that proportions of the main lipid classes in the SC changed along an
aridity gradient, we also calculated percentages of lipids as the amount (mg)
divided by the sum of the total amount of the four lipid classes analyzed.
To validate our ability to measure the quantity of lipids in solution, we followed the same protocol but used known concentrations of cholesterol as our unknown. The average error, calculated as [(observed-actual/actual)x100], was -0.88±4.47% (N=8).
Statistics
All statistical tests were performed using SPSS 12.0. We rejected the null
hypothesis at P>0.05. Values are means ± 1 S.D.
We tested for differences between means using a two-tailed t-test for
independent samples. Concentrations of cholesterol and free fatty acids were
not normally distributed (Kolmogorov-Smirnov test, KS=0.18,
P<0.04, and KS=0.20, P<0.01, respectively). We
log-transformed these variables to normalize the data (KS=0.10,
P>0.15, and KS=0.09, P>0.15). Percentages were logit
transformed [ln(Y/1-Y);
Zar, 1996] prior to analyses
to normalize data. We performed regressions using a general linear model. To
test for differences between regressions for lipids from desert and mesic
sparrows, we first tested for the significance of the interaction term. If the
interaction was not significant, we removed it from the model, and tested for
differences in intercepts assuming a common slope.
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Results |
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Oxygen consumption
Desert sparrows consumed oxygen at a lower rate than did Ohio sparrows:
56.9±5.9 ml h-1 for sparrows in Saudi Arabia,
64.8±6.0 ml h-1 for birds in Ohio (t=-2.7, d.f.=17,
P<0.02). Heat production was 27.5±3.0 kJ day-1
for sparrows from Saudi Arabia, and 31.3±3.3 kJ day-1 for
birds from Ohio. Mass-specific metabolic rates were not significantly
different between groups: 1.37±0.14 kJ g-1 day-1
(Saudi Arabia) and 1.32±0.18 kJ g-1 day-1 (Ohio;
t=0.65, d.f.=17, P>0.5).
Respiratory water loss
Respiratory water loss was 0.97±0.23 and 1.25±0.32 g
H2O day-1 for sparrows from Saudi Arabia and from Ohio,
respectively, values that differed significantly (t=-2.5, d.f.=20,
P<0.02). When these values were expressed per unit body mass,
however, we did not detect significant differences: 48±12 mg
H2O g-1 day-1 (Saudi Arabia), 54±16 mg
H2O g-1 day-1 (Ohio); t=-0.997,
d.f.=20, P>0.3 (Fig.
1A).
|
Passive water loss through non-living skin
In vials covered with skin, water loss was 46.0±15.7 mg
H2O cm-2 day-1 for sparrows from Saudi Arabia
(N=12), and 45.8±27.2 mg H2O cm-2
day-1 for sparrows from Ohio (N=11), values that were not
significantly different (d.f.=21, P>0.9). The rate of water loss
in the uncovered vial was 456.4±37.1 mg cm-2
day-1 in Saudi Arabia, and 440.5±59.0 mg cm-2
day-1 in Ohio (t=0.77, d.f.=16; P>0.45). When
compared with an open vial, a free water surface, skin-covered vials lost
10.1% and 10.4% as much water in Saudi Arabia and Ohio, respectively.
Lipids in the stratum corneum
For both groups of sparrows, our procedure using TLC revealed distinct
bands of lipids corresponding to standards of cholesterol, free fatty acids,
ceramides and cerebrosides. The ceramides that separated into bands were named
in order of increasing polarity (ceramides 1-4), as were the cerebrosides 1-3
(Fig. 2).
|
|
Because it is thought that subtle changes in the proportions of lipid
classes in the SC can influence the fluidity of the lipid layer and therefore
water permeation (Haugen et al.,
2003a,b
;
Bouwstra et al., 2003
), we also
expressed lipid classes as a percentage of the total lipids extracted. Desert
sparrows had a significantly lower proportion of cholesterol and ceramide 2
than mesic birds (Table 2).
|
CWL and lipids
CWL did not vary with the quantity of total lipids in the SC in either
group of sparrows (r2<0.06, P>0.27, for all
cases). However, among sparrows from Ohio, CWL was positively correlated with
the percentage of free fatty acids (r2=0.50,
P<0.01), and it varied negatively with the percentage of total
ceramides, ceramide 3 and total cerebrosides (r2=0.46,
P<0.02; r2=0.36, P<0.04;
r2=0.39, P<0.04, respectively;
Fig. 3). There were no
significant correlations between CWL and percentages of the different lipid
classes in sparrows from Saudi Arabia, but this may not be surprising since
variation tended to be lower in desert sparrows.
|
Correlations among lipids in the SC
Given that adjustments in the relative proportions of lipids in the SC may
have important consequences for barrier function, we explored covariation
between the percentages of the various lipids in the SC; proportions of some
classes of lipids were significantly correlated in both groups
(Table 3). Interestingly,
variation in lipids among individuals was low for desert sparrows. In general,
free fatty acids are negatively correlated with the rest of the lipid classes
in the SC.
|
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Discussion |
---|
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In order to compare house sparrows with other birds, we compiled data for CWL from the literature (Table 4). As one might expect, amongst 21 species of birds, CWL (mg H2O cm-2 day-1) varied positively with body mass (Mb, in g) as described by CWL=0.011Mb+11.946 (r2=0.98, P<0.01). However, to our surprise, we found that surface-specific CWL (mg H2O cm-2 day-1) also varied with body mass: CWL=11.44+7.93logMb (r2=0.45, P<0.001; Fig. 4). Larger birds tend to lose more water per unit surface area than do small birds. Therefore, expressing CWL on a surface-specific basis does not standardize comparisons for interspecific data sets. Using analysis of covariance (ANCOVA) with Mb as a covariate, we could not find any significant difference between desert and non-desert birds (P>0.45). These data suggest that large birds, having a smaller surface to volume ratio, need higher rates of water loss for thermoregulation than birds of smaller size, a hypothesis in need of testing.
|
|
|
The lipid composition of the SC of house sparrows differed from that found
in other species of birds. In pigeons and chickens, free fatty acids comprised
about 20-30% of the dry weight of the SC
(Menon et al., 1986;
Wertz et al., 1986
). The
percentage of free fatty acids in our samples exceeded 55% in both desert and
mesic house sparrows. Sphingolipids accounted for about 25% of the dry mass of
the SC in pigeons, with ceramides and cerebrosides accounting for equal
proportions (Menon et al.,
1986
). The percentage of sphingolipids in the SC in both
populations of sparrows was around 40%. Moreover, in our samples almost two
thirds of the sphingolipids were cerebrosides. A high proportion of
glucosylceramides apparently precludes the formation of lamellae in the
intercellular spaces of the SC in mammals
(Holleran et al., 1993
;
Proksch et al., 1993
). This
effect is not caused by a decrease in ceramides, so it does not imply a
negative association between these two lipid classes. In fact, we found a
positive relationship between ceramides and cerebrosides in house sparrows
(Table 3). Cerebrosides can be
cleaved to form ceramides by glycosidases
(Wertz and Downing, 1989
).
Therefore, accumulation of cerebrosides could lead to a mobilization of a
higher amount of ceramides whenever it is necessary by increasing the activity
of this enzyme.
The high concentration of glycosphingolipids within the SC of desert
sparrows seems counterintuitive because in mammals an increase in
glycosphingolipids decreases barrier function of skin
(Holleran et al., 1993). Birds
in general are thought to have a less competent barrier than mammals, and they
typically have higher concentrations of glycosphingolipids in their SC
(Elias and Menon, 1991
). So
how can we reconcile desert sparrows having lower water loss, yet at the same
time higher concentrations of cerebrosides in their SC? We propose a model to
explain our results, based on requirements for thermoregulation and for water
conservation (Fig. 5).
|
Experimental work on birds partially supports predictions of the model.
Menon et al. (1989) found that
cerebrosides in water-stressed zebra finches represented 5.9% of the epidermal
lipid dry mass, compared with 8.7% in the controls, and 9.9% in rehydrated
birds. In addition, water-deprived zebra finches showed fewer lipid droplets
in the corneocytes, more intercellular lamellae in their SC, and a higher
number of MGB when compared to control birds. These changes led to an
enhancement of the permeability barrier through the skin; water-deprived zebra
finches exhibited a 50% reduction of their trans-epidermal water loss.
Peltonen et al. (1998
,
2000
) found that
cold-acclimated pigeons (Columba livia L.) substituted the amorphous
lipoid material of the intercellular spaces in the SC by lipid lamellae, a
response similar to that found in zebra finches under xeric stress.
Unfortunately, they did not report any values for CWL. Heat acclimated pigeons
did not show lamellar material in the SC (Peltonen et al.,
1998
,
2000
), a result consistent
with the idea that effective theromoregulation by CWL requires more
cerebrosides. Desert birds without access to water should be selected to
maintain high concentrations of ceramides in their SC and rely on respiratory
water loss to control body temperature
(Tieleman and Williams, 2002
).
In eight species of larks, the proportion of ceramides in the SC increases
with the aridity of the environment
(Haugen et al., 2003a
).
Although we found that the lipid composition of the SC differs in desert
house sparrows, this alteration by itself does not seem to make the physical
permeability barrier more effective when compared to their mesic counterparts.
If only passive diffusion through the skin were acting on water loss rates in
house sparrows, we would predict differences in water loss rates through the
dead skin of the sparrows from desert and mesic populations. However, water
evaporation rate through the non-living epidermis attached to vials was not
significantly different between the two populations. If passive diffusion were
the only factor accounting for evaporation through the skin of the sparrows,
birds in Saudi Arabia would lose 3.24 g day-1, whereas sparrows in
Ohio would evaporate 3.73 g day-1. Live animals lose 28.7% and
35.4% of these values, respectively. Therefore, biological factors operating
in the live animal influence CWL significantly. According to our model,
activation of the metabolic machinery would produce a reduction of water loss
through the skin (Fig. 5).
Forexample, pH is lower in the upper layers of the SC than in the lower SC
(Elias, 2004). Most of the
enzymes that convert lipids in the multigranular bodies to those lipid classes
that form the permeability barrier have a maximum activity within a pH of 4-6.
It is likely that active processes are responsible for creating and
maintaining this pH gradient, allowing regulation of the biochemical
properties of the SC. Consistent with the idea that there is a metabolic cost
in maintaining the barrier to vapor diffusion, we found a negative correlation
between surface-specific CWL and oxygen consumption in desert house sparrows
(Fig. 6).
In conclusion, CWL in house sparrows living in a desert environment was reduced compared to mesic house sparrows, and this decrease in CWL was responsible for the reduction of total evaporative water loss in desert house sparrows when compared to the mesic population. We found an alteration of the lipid composition in the SC, yet we did not find any significant difference in the properties of the physical barrier in both populations. Thus, biological control mechanisms must play a crucial role enhancing the permeability barrier. The balance between requirements for thermoregulation by evaporative means and water conservation might have played an important role in the evolution of the composition of the skin in desert species.
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References |
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