Body wiping behaviors associated with cutaneous lipids in hylid tree frogs of Florida
Department of Zoology, University of Florida, Gainesville, FL 32611-8525, USA
* Author for correspondence (e-mail: tbarbeau{at}fmarion.edu)
Accepted 29 March 2005
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Summary |
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Key words: evaporative water loss, gland, Hylidae, integument, lipid, tree frog, wiping behavior
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Introduction |
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Some frogs, however, deviate from this pattern and exhibit specialized
adaptations to reduce dehydration in arid environments
(Table 1). Such adaptations
include uricotelism, increased water uptake through the ventral skin patch,
and skin resistance to EWL attributable to lipid secretions from cutaneous
glands (Toledo and Jared,
1993). Arboreal species, in particular, have been shown to have
comparatively low rates of EWL (Wygoda,
1984
). Examples include South American (Phyllomedusa
sauvagei) and Australian (Litoria caerulea) hylid tree frogs,
which secrete lipids from specialized cutaneous glands and spread them over
the body by complex self-wiping movements to form an effective barrier to EWL
(Blaylock et al., 1976
;
Christian et al., 1988
).
Remarkably, the resulting EWL in P. sauvagei is similar to that of
some desert-dwelling reptiles (Shoemaker
et al., 1972
).
|
The Indian tree frog Polypedates maculatus engages in similar
wiping movements involving lipid secretions from cutaneous mucous glands.
These secretions, however, provide a lower reduction in EWL than do those of
phyllomedusine or Australian tree frogs. Therefore, wiping behaviors might
have evolved before such secretions provided a significant water barrier and
are possibly more widespread among arboreal or xerophilic frogs than
previously considered (Lillywhite et al.,
1997; Lillywhite and Mittal,
1999
).
The phylogenetic origin of wiping behaviors might have evolved from
movements involved in removal of debris or shedding skin from the body
(Blaylock et al., 1976). Wiping
might also aid in the spread of mucous gland secretions that are necessary for
respiration, thermoregulation and cutaneous water balance
(Lillywhite, 1971
).
Comparative descriptions of anuran self-wiping behaviors provide important
insights into their evolution and ecophysiological significance
(Lillywhite et al., 1997
).
Wiping behaviors associated with cutaneous lipids have been documented in relatively few species of amphibians. In this study we investigated and compared self-wiping behaviors in Florida tree frogs (family Hylidae). We also examined these frogs for the presence of an extra-epidermal layer of mucus and lipid secretions, and we describe the morphology of the epidermis, dermis and cutaneous glands. Lastly we determined rates of total EWL in unrestrained frogs during bouts of water deprivation and wiping. The species of tree frogs included Hyla andersonii, H. avivoca, H. chrysoscelis, H. cinerea, H. femoralis, Hyla gratiosa and H. squirella.
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Materials and methods |
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Observations of skin secretions
To evoke cutaneous glands to secrete their contents onto the dorsal skin
surfaces of frogs, we stroked the dorsal skin surfaces of frogs using a blunt
metal probe or, in separate tests, injected epinephrine into the dorsal lymph
sac (0.15 µg g-1 body mass). These methods have been used
previously to study glandular secretions in tree frogs
(Lillywhite et al., 1997).
Secretions were collected by gently pressing a glass slide against the
dorsal skin surface. Slides were air-dried, stained with Hematoxylin and Eosin
(H&E), and examined microscopically to confirm that secretions were not
contaminated with epidermal cells. Periodic Acid Schiff (PAS) was used to
identify mucopolysaccharides, neutral mucosubstances, hyaluronic acid and
sialomucins. Alcian Blue at a pH 1.0 (AB-1) was used to identify sulfated
glycoproteins, and at a pH of 2.5 (AB-2.5) to identify nonsulfated and
sulfated glycoproteins. Sudan Black B (SBB) and Oil Red O (ORO) were used to
identify lipids (Presnell and Schreibman,
1997). Duplicate slides were treated with chloroform:methanol (2:1
v/v) to extract lipids prior to staining with SBB. The duplicate slides did
not stain with SBB, indicating that the stain effectively detected lipids in
experimental slides.
Wiping behavior and evaporative water loss
To evoke possible grooming behaviors, we dropped plant debris and water
droplets onto the dorsal body surfaces of resting and active frogs, and we
observed their responses for 15 min. Grooming movements that dislodged debris
were considered distinct from wiping behaviors that spread glandular
secretions. We then conducted systematic observations of wiping behavior.
First, we observed wiping behaviors of frogs during 10 h trial periods when
they had ad libitum access to water. We monitored the mass of each
animal by weighing at the beginning (0 h), middle (5 h) and end (10 h) of each
trial. Wiping behaviors of individual frogs were observed for 15 min
immediately after each weighing for a total of 45 min of observation of each
frog. A total of 10 trials were repeated for each individual for a total of
450 min of observation of wiping behavior per individual per species. Each
trial was conducted approximately 12-14 h apart, and frogs were provided free
access to water between trials.
A second set of observations was conducted on individuals subjected to repetitive trials of moderate dehydration (<35% of standard body mass loss) to examine whether dehydration stress influenced the frequency or pattern of wiping behavior. With the exception of water deprivation, each dehydration trial was identical in procedure, length of time and repetition to the free water trials. At the start of each dehydration trial, bladder water was expressed from each frog, and access to water was withheld for a total of 10 h. Calculations of EWL (mg cm-2 h-1) were based on losses of body mass relative to standard mass during each 10 h trial.
Partly to account for size differences among species, we converted rates of
EWL measured during dehydration trials to surface area-specific rates of EWL
for each frog. Surface areas of frogs were estimated from the general equation
in Talbot and Feder (1992),
assuming an average exposure of two-thirds of the total body surface area to
EWL (Withers et al., 1984
). We
recognize that a small component of these measurements reflects pulmonary
water losses, and we use such data solely to assess whether dehydration stress
and wiping reduced EWL in frogs, and to contrast the temporal patterns of
integrated (total) EWL among the species studied.
Histology
Skin biopsies were sampled from five individuals each of H. andersonii,
H. avivoca, H. chrysoscelis, H. cinerea, H. femoralis, H. gratiosa, H.
squirella, P. hypochondrialis and R. utricularia. Frogs were
euthanized with chloroform hydrochloride gas. Pieces of skin (5 mmx5 mm)
were excised from the dorsal midline between the shoulders (three samples) and
from the abdomen (two samples). One skin sample from each region was rinsed in
Ringer's solution and fixed in 10% neutral buffered formalin, while a second
skin sample was fixed in Opti-freeze solution and flash-frozen in isopentane
(2-methylbutane) immersed in liquid nitrogen. Formalin-fixed skin samples were
dehydrated in ethanol, embedded in paraffin, serially sectioned at 6 µm,
mounted onto glass slides, and stained with H&E, PAS, AB-1 and AB-2.5.
Frozen skin sections were serially sectioned at 10 µm, mounted on glass
slides, air-dried and stained with ORO or SBB. Lipids were extracted from
control skin sections prior to staining for lipids using chloroform:methanol
(2:1 v/v) for 15 min. These negative control sections showed little or no
reaction to ORO or SBB.
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Statistical analyses
The total number of wiping movements exhibited by all species under the
conditions of normal hydration and dehydration were compared with a paired
t-test. For each type of wiping movement, analysis of variance
(ANOVA) was performed to compare the number of wiping movements among species.
Differences in surface area-specific rates of EWL among trials for each
species were determined with one-way repeated measures ANOVA, following which
time effects were tested by Helmert contrasts. The total number of wiping
movements and rates of EWL were compared among species using ANOVA, and
significant ANOVAs were followed by Scheffe's pairwise contrasts. Thickness of
the epithelium, stratum corneum, stratum spongiosum, and total skin and
diameter of glands, were compared among species with ANOVA followed by
Student-Newman-Keuls post hoc tests. Gland density was compared among
species with Kruskal-Wallace non-parametric analyses followed by Mann-Whitney
U-pairwise contrasts. All data were analyzed using SPSS 7.5 software
and P set a priori at 0.05, unless otherwise specified.
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Results |
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In all species examined, slides with air-dried secretions stained positively with PAS, AB-2.5 and AB-1. Dried secretions stained dark blue to black for lipids with SBB, whereas duplicate slides with secretions subjected to lipid extraction prior to staining demonstrated a weak or negative reaction to SBB or to ORO.
Description of body wiping movements
Variable wiping behaviors were observed in Florida tree frogs. The most
common behavior involved wiping of the dorsal head by the front limbs (head
wipe). The wipe progressed, in a caudal to cranial direction, over the eye
orbit (the eyes momentarily closed), the snout and the nostril before the hand
returned to a resting position on the substrate
(Fig. 1A,B). It was not unusual
for animals to wipe one side of the head several times in succession and then
immediately wipe the opposite side of the head with the other forelimb, once
or several times, in the same manner.
Another behavior observed was the wiping of the ventral surface of the chin with the forelimbs (ventral-lateral chin wipe). As with the dorsal head wipe, this wipe was often immediately repeated with the same or opposite forelimb several times.
Wiping behaviors involving the hind limbs were also observed in all species. One of these behaviors was the wiping of the dorsal back surface with the hind foot (dorsal wipe). The wipe progressed over the back in a caudal to cranial direction, before the hind foot extended laterally off the body at the thoracic region and returned to a resting position (Fig. 1C). This wipe was typically repeated several times with singular, alternating movements of the left and right hind limbs. The hind limbs were also involved in wiping of the lateral body surfaces (lateral wipe) in all species. Similarly to the dorsal back wipe, this wipe was often repeated several times with singular, alternating movements of the hind limbs.
Another wiping behavior observed was a brief wiping of the eyes with one of the front limbs (eye flick). This movement typically was not repeated with the same or opposite limb; however it often preceded a sequence of seating movements associated with a water-conserving posture (WCP; Fig. 1D).
When debris was dropped on the heads of frogs, they would quickly `flick' off the debris with a forelimb, but this behavior appeared distinct from head-wiping and was seen only occasionally. After such flicking movements, individuals promptly assumed a WCP.
Each species appeared to engage in a different repertoire of wiping movements during normal hydration and dehydration trials. Hyla cinerea exhibited the highest number of head-wiping movements compared to the other species (P=0.0001), whereas H. gratiosa and H. squirella exhibited an intermediate number of wiping movements compared to H. femoralis and H. chrysoscelis (P=0.008 and P=0.001, respectively). The number of head wipes in H. avivoca was similar to all species except H. cinerea. Although the number of dorsal wiping movements was similar among species, H. squirella exhibited the highest number of lateral wiping movements (P=0.0001). The number of ventral-lateral chin-wiping movements was similar among H. avivoca, H. gratiosa and H. squirella; however, H. cinerea, H. chrysoscelis and H. femoralis did not exhibit this wiping movement. Hyla gratiosa engaged in more eye-flicking movements (P=0.024) than H. avivoca, but H. femoralis exhibited a similar number of wiping movements to the aforementioned two (Table 2).
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During normal hydration trials, frogs typically were active and displayed wiping behaviors within the first 5-10 min of each observation period, after which they became quiescent in a WCP for the remaining time. During dehydration trials, frogs typically displayed wiping behaviors within several minutes after weighing, following which they displayed a WCP for the remaining time. However, several individuals of H. cinerea displayed exploratory or escape behaviors during the final minutes of several observation periods, suggesting that these individuals were stressed by the trial. The mean number of wiping movements exhibited by all species during dehydration trials (52.8) was significantly higher (P<0.025) than those under normal hydration (34.8). This difference partly reflects the relatively higher frequency of wiping movements observed during the first 5 min of the dehydration trials.
Rates of surface area-specific EWL, body water deficit and rehydration
Body water deficits incurred among all species during dehydration cycles
ranged between 4.0 and 26.9% of standard body mass, with H. gratiosa
averaging one-half to one-third the deficit displayed by the other species.
Following access to water, rehydration levels among species ranged from 103.5
to 124.7% of standard body mass (Table
3).
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Frogs were subjected to repetitive trials of dehydration to determine if acclimation to dehydration stress affected rates of EWL over time. Rates of EWL were similar among trials for H. cinerea and H. femoralis, but different among trials for H. avivoca (Fig. 2A, P<0.001), H. gratiosa (Fig. 2B, P<0.001), H. squirella (Fig. 2C, P<0.001) and H. chrysoscelis (Fig. 2D, P<0.001). Overall, the rates of EWL fluctuated considerably over time for all species examined, and no discernable trend in EWL was evident.
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Skin morphology
For all species examined, the epidermis was organized into several layers
and exhibited an outermost stratum corneum (Sc) of flattened, keratinized
epithelial cell layers (Fig.
3A). Directly above the Sc of most species was a thin coat of
sulfated and nonsulfated glycoproteins, indicated by a turquoise color when
stained with AB-1 and AB-2.5, respectively. This extra-epidermal mucous coat
was confirmed by the staining of extra-epidermal skin secretions. For most
species, neutral glycoproteins, hyaluronic acid or sialomucins were detected
by PAS. Beneath the Sc was the stratum intermedium layer consisting of
eosinophilic epithelial cell layers. Lower epithelial cells of this layer were
cuboidal in shape with cells appearing more flattened near the Sc. This layer
was eosinophilic with H&E, and stained positively for lipids with SBB in
P. hypochondrialis and H. andersonii. The basal layers of
the epidermis were composed of a stratum germinativum of a single layer of
columnar epithelial cells bordered below by an innermost basement membrane
(BM) of collagenous fibers (Fox,
1994).
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The basal portion of granular glands often extended into the SC layer, whereas the mucous glands were found in the upper SS beneath the basement membrane. The inner wall of mucous glands was lined with cuboidal or columnar epithelial cells having eosinophilic nuclei. The gland collar and duct typically were filled with cuboidal myoepithelial cells. The lumen of these glands was often empty and contained few if any granules. Granular glands were round or elliptical in shape, sometimes with an enlarged basal region. The inner wall of these glands was lined with flattened myoepithelial cells with eosinophilic nuclei. The gland collar and duct were filled with cuboidal epithelial cells, similar to that in mucous glands. The lumen of granular glands was relatively large and usually filled with heterogenous granular secretory material. Often, the basal portion of the gland contained more secretory material than apical regions (Fig. 3A).
Histochemical differences were observed between granular and mucous glands. Secretory mucus was located within the lumen or apical region of the mucous gland. In the granular glands of all species except H. cinerea and H. gratiosa, mucous and lipid secretions were associated with the secretory granules and often concentrated at the basal region of the gland. Both types of glands contained nonsulfated glycoproteins; however, sulfated glycoproteins were found predominantly in mucous glands whereas neutral glycoproteins, hyaluronic acid or sialomucins were found predominantly in granular glands. In P. hypochondrialis, sulfated and nonsulfated glycoproteins were found only in granular glands while neutral mucosubstances were found in mucous glands. In R. utricularia these mucosubstances were detected only in the mucous glands, with the exception of sulfated and nonsulfated mucins in the ventral granular glands of R. utricularia. In all species, the secretory material in mucous glands stained positively for neutral glycoproteins and for non-sulfated glycoproteins, but did not demonstrate lipids with either ORO or SBB staining.
The lumen and periphery of dorsal granular glands stained positively for lipids with SBB in H. andersonii, H. femoralis, H. chrysoscelis and H. squirella (Fig. 3B). Dorsal granular glands in H. andersonii and H. avivoca stained positively for lipids with ORO. In P. hypochondrialis, lipid glands unique to this genus stained positively for lipids with SBB and with ORO, but granular glands did not show similar lipids. Granular glands in H. cinerea, H. gratiosa and R. utricularia did not stain positively for lipids with SBB or ORO. Control slides of skin sections rinsed in chloroform:methanol showed little or no reaction to lipid staining.
Glands differed in diameter and density among species. Diameter of the granular glands did not differ among Florida tree frogs, but among all species granular glands were larger in R. utricularia, smaller in P. hypochondrialis and H. squirella, and of intermediate size in the other hylids (Table 4, P=0.04). For Florida tree frogs, mucous glands were larger in H. gratiosa and smaller in the other tree frogs (P=0.02). For all species combined, mucous glands were larger in P. hypochondrialis and smaller in H. femoralis and H. avivoca (Table 4, P<0.001). Density of granular glands was similar among species but the density of mucous glands was greater in H. femoralis than in H. cinerea and P. hypochondrialis (Table 5, P=0.002).
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Discussion |
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Most species of the Florida hylids we studied engage in frequent wiping of
the head, back and lateral body surfaces compared to the ventral surfaces and
eyes. The surfaces wiped more frequently are those that are more exposed to
EWL when individuals are positioned in a WCP. With the exception of three
species that displayed a low frequency (<10% of total wipes observed) of
ventral-lateral chin wiping, wiping of other ventral surfaces is absent. In
natural environments, several of these species occupy plant or tree cavity
microhabitats wherein the frogs insert the posterior body into a protective
depth of a cavity and conceal the ventral body surface with a WCP, while the
anterior surfaces of head and back remain exposed
(Neil, 1951;
Goin, 1958
;
Boughton, 1997
). To the extent
that skin secretions containing lipids reduce EWL, wiping behaviors that
spread these secretions over skin regions subjected to evaporative exposure
should provide a further selective advantage.
No visible skin secretions are expelled from glands prior to tactile
stimulation, whereupon the skin becomes visibly wet at the region of contact.
This pattern of secretion is similar to that shown in P. maculatus
(Lillywhite et al., 1997) but
distinct from that of phyllomedusine frogs, which appear to expel secretions
prior to the wiping event (Blaylock et al.,
1976
). Thus, one function of wiping might be to stimulate
secretion from cutaneous glands
(Lillywhite et al., 1997
).
After completing a sequence of wiping movements, most frogs become
quiescent in a WCP. This behavior is probably necessary to prevent the
physical disruption of the dried extra-epidermal layer of secretions that
cover the skin (Lillywhite and Mittal,
1999).
Frogs that exhibit self-wiping behaviors accompanied by lipid secretions
are associated with arboreal habitats and are subject to dehydrating
conditions (Blaylock et al.,
1976; Christian et al.,
1988
; Lillywhite et al.,
1997
). Although Florida tree frogs occupy mesic habitats, they are
active in microenvironments that are subject to seasonal or periodic aridity.
Moreover, Hyla cinerea, H. femoralis and H. squirella have
been observed basking on exposed vegetation during the day
(Einem and Ober, 1956
;
Lee, 1969
;
McComb and Noble, 1981
;
Ritke and Babb, 1991
).
Hyla femoralis are often heard calling from high in the canopy of
upland forested areas and are infrequently found on the ground except during
periods of rainfall or reproduction (T.R.B., personal observation). Hyla
gratiosa inhabit comparatively drier upland regions away from water
except during the reproductive season
(Farrell and MacMahon, 1969
;
Layne et al., 1989
). Compared
to the other Florida hylids, H. cinerea is typically found on
vegetation closely associated with permanent or temporary water bodies
(Wright and Wright, 1949
;
Neil, 1951
;
Goin, 1958
;
Farrell and MacMahon, 1969
).
The relatively higher EWL measured in H. cinerea reflects the
association with aquatic vegetation, whereas the lower EWL measured in H.
gratiosa corresponds with drier arboreal environments that are used by
this species.
There are subtle distinctions in wiping behaviors associated with lipid
secretions among arboreal frogs. Phyllomedusine species tend to exhibit more
elaborate patterns of wiping compared to the Florida hylids. Polypedates
maculatus engages in complex wiping behavior but, similar to Florida tree
frogs, exhibits a higher EWL than phyllomedusine tree frogs. These wiping
behaviors might have evolved in the absence of lipid secretions and possibly
served other functions, such as grooming, shedding skin or spreading
secretions that maintain a moist integument for respiration and
thermoregulation (Lillywhite,
1971; Lillywhite and Licht,
1974
). The comparatively simple body wiping behaviors shown in
Florida tree frogs, associated with lipid secretions, may represent an early
stage of the more advanced wiping behaviors seen in waterproof species.
Cutaneous lipids
An important discovery in this study was that Florida tree frogs, like some
other arboreal anurans, have lipoid skin secretions that form an
extra-epidermal layer and appear to be spread by stereotypical wiping
behaviors (Blaylock et al.,
1976; McClanahan et al.,
1978
). The release of secretions and initiation of wiping
behaviors can be elicited by tactile stimuli such as brief handling, massaging
or gentle probing of skin surfaces. Tactile stimuli are possibly perceived by
the frogs as predatory, and the resulting secretions and wiping behaviors
could serve a defensive function. However, we did not examine the secretions
for bioactive amines, peptides or alkaloids associated with defensive
responses (Esparmer, 1994
).
Similarly to P. maculatus
(Lillywhite et al., 1997
;
Lillywhite and Mittal, 1999
),
the skin secretions in Florida tree frogs contain both mucosubstances and
lipids that reduce EWL (Wygoda,
1984
,
1988
;
Toledo and Jared, 1993
),
whereas the rates of EWL we measured are comparatively higher than those of
so-called waterproof species (Blaylock et
al., 1976
; Lillywhite et al.,
1997
; Withers et al.,
1984
; Wygoda,
1984
).
There is considerable variation, and no distinct trend, in rates of EWL
over time in the Florida tree frogs subjected to moderate dehydration. These
results indicate an absence of acclimation to prolonged dehydration. Such
acclimation most likely would be demonstrated by a gradual but consistent
decrease in rates of EWL over the 10 dehydration trials. The variation
observed in rates of EWL over time might be attributable to several factors,
including the influences of activity and posture as well as possible changes
in the cutaneous water barrier. Generally, the rates of EWL observed in the
Florida hylids are within the range of measurements reported in studies of
non-waterproof tree frogs (Wygoda,
1984; Lillywhite et al.,
1997
). Whereas these data cannot provide estimates of skin
resistance, they provide an index of the moderate waterproofing related to
wiping and skin secretions, and they indicate an absence of acclimation during
periods of water deprivation.
The presence of extra-epidermal lipids and wiping behaviors represent a combination of traits that appear to be convergent among several distantly related genera of arboreal frogs. Clearly there is a wide range of reduced EWL associated with lipid secretions in arboreal frogs. Therefore, an extra-epidermal lipid layer may aid in reducing EWL as in P. maculatus and evidently Florida hylids, but not necessarily lead to tight waterproofing as in the phyllomedusine species.
In P. hypochondrialis, lipids are detected with SBB and ORO
staining in specialized lipid glands. In H. andersonii, H. chrysoscelis,
H. femoralis and H. squirella, SBB indicates that lipids are
present in the dorsal granular glands, but these are extracted from tissue on
control slides that are treated with chloroform-methanol prior to staining.
This result suggests the presence of phospholipids because polar lipids
dissolve readily in chloroform-methanol
(Withers et al., 1984). Lipids
are also detectable with ORO in the dorsal granular glands of H.
andersonii and H. avivoca. Unbound lipid secretory material
would likely be extracted from tissue during staining with ORO because it is
an alcohol-based stain. Therefore, the positive reaction to ORO in the
granular glands of these species indicates the presence of bound lipids, or
lipids that are bound to structural elements within the gland. These might be
neutral lipids, such as fatty acids, esters, cholesterol or triglycerides.
The size and density of dorsal granular glands are similar among Florida
tree frog species, which suggests the relative quantities of mucus and lipids
(when present) are also similar among species. According to Withers et al.
(1984), the polar and neutral
cutaneous lipids found in the waterproof arboreal frogs Litoria
gracilenta and Phyllomedusa hypochondrialis are also present in
some non-waterproof species. Like Litoria and Phyllomedusa,
Florida tree frogs secrete these lipids onto the skin, and likely spread them
with wiping behaviors to form the extra-epidermal layer. Despite these
similarities, skin resistance to EWL in Florida tree frogs appears
significantly lower than that of L. gracilenta and P.
hypochondrialis (Wygoda,
1984
; Christian et al.,
1988
; Buttemer, 1990). What could account for the clear disparity
in the protective capacity of these lipids associated with wiping behaviors?
Variable rates of EWL may be attributable to quantitative or qualitative
differences of the lipids that are present in the extra-epidermal skin
secretions of arboreal frogs. Further, it is likely that the relatively simple
body-wiping behaviors observed in Florida tree frogs do not spread lipids
adequately over the entire body to form a complete barrier to EWL.
The quantity of lipids secreted onto the skin of Florida tree frogs might
also be influenced by the dilution of these lipids with mucus or other
proteinaceous secretory products. Lipids are combined with mucus within mucous
and granular glands, and therefore might be diluted when secreted onto the
skin surfaces. Conceivably, a thinner and less concentrated extra-epidermal
lipid layer might confer the comparatively moderate skin resistance to EWL
shown in these species. The dilution of secretory lipids is considered a
factor contributing to the relatively modest skin resistances demonstrated in
other non-waterproof arboreal frogs
(Lillywhite et al., 1997). A
specialized gland is dedicated to lipid production in the phyllomedusines, and
therefore a larger quantity and concentration of lipids are likely to result
in a higher resistance to CWL in these species. Further investigation is
required to determine how lipid chemistry and quantity of secreted products
might influence EWL rates in arboreal frogs.
Strikingly similar traits are shared among arboreal frogs inhabiting arid
or seasonally arid environments. The present study demonstrates that glandular
secretion of lipids spread over the body by wiping behaviors is part of a
suite of characters that are more widespread among arboreal frogs than
previously known. The occurrence of these characters among different genera of
arboreal frogs on several continents likely represents evolutionary
convergence of function in response to dehydration stress
(Shoemaker et al., 1987;
Christian et al., 1988
;
Lillywhite et al., 1997
).
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Acknowledgments |
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