Mechanical properties of the integument of the common gartersnake, Thamnophis sirtalis (Serpentes: Colubridae)
1 Department of Biological Sciences, Old Dominion University, Norfolk, VA
23529, USA
2 Advanced Materials and Processing Branch, NASA Langley Research Center,
Hampton, VA 23681, USA
* Author for correspondence at present address: Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA (e-mail: grivera{at}clemson.edu)
Accepted 28 May 2005
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Summary |
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Key words: integument, skin, biomechanics, feeding, snake, Thamnophis sirtalis
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Introduction |
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The evolution of snakes has involved considerable morphological change,
including body elongation and the loss of limbs
(Greene, 1997). Morphological
adaptations of the skull and cephalic musculature, associated with the ability
to ingest large-bodied prey, have been investigated extensively
(Gans, 1961
;
Rieppel, 1980
;
Cundall, 1995
;
Lee et al., 1999
;
Cundall and Greene, 2000
). In
addition, recent studies have examined the mechanics of post-cranial prey
transport (Moon, 2000
;
Kley and Brainerd, 2002
). In
order for slender-bodied organisms such as snakes to evolve a macrophagous
feeding system, the esophagus, stomach, abdominal musculature and overlying
integument must be modified to allow for considerable distension when
accommodating large, intact prey (Gans,
1974
; Arnold, 1983
;
Singh and Mittal, 1989
;
Mullin, 1996
;
Cundall and Greene, 2000
).
However, although it is evident that macrophagy in snakes requires highly
compliant postcranial skin, the mechanical properties and morphological
correlates of the ophidian integument have received limited attention,
particularly in the context of feeding. Only one previous study
(Jayne, 1988
) has examined the
mechanical properties of the ophidian integument. However, that study focused
on the relevance of integumentary mechanics to locomotion. Jayne
(1988
) conducted tensile tests
on skin samples by applying loads parallel to the longitudinal body axis for
six species of snakes. Given the likely anisotropic behavior of ophidian skin,
Jayne's results, although significant in the context of locomotion, provide
few insights into the behavior of skin when stretched in the circumferential
direction, as would occur during feeding.
The skin of snakes is unusual among vertebrate integuments in possessing
folds of intersquamous skin between longitudinally oriented scale rows
(Savitzky et al., 2004). The
apparent function of these folds is to permit the maximum circumference of the
snake to increase, allowing large-diameter prey to pass from the oral cavity
into the stomach (Gans, 1952
,
1974
;
Mullin, 1996
). Snakes feeding
on large prey typically possess a larger number of dorsal scale rows in
prepyloric regions of the body than in postpyloric regions
(Gans, 1974
;
Mullin, 1996
; but see
Shine, 2002
). The greater
number of scale rows and the associated folds of skin anterior to the pylorus
allow undigested food to be accommodated more easily. Postpyloric regions
require less circumferential stretch because food passing through the pylorus
has been reduced in bulk.
Thamnophis sirtalis, the common gartersnake, belongs to the
colubrid subfamily Natricinae and has an extensive distribution, extending
between both coasts of North America
(Rossman et al., 1996).
Typically a habitat and prey generalist, its diet consists of both small- and
large-diameter prey, including earthworms, fishes, amphibians, mammals and
birds. Earthworms and amphibians typically constitute the largest proportion
of the diet (Gregory, 1978
;
Rossman et al., 1996
). In a
Michigan population, earthworms were found to constitute 80% of the diet,
while amphibians accounted for 15%
(Carpenter, 1952
).
Thamnophis sirtalis, like most snakes, has a resting body
circumference that increases from the head toward the mid-body and then
decreases toward the tail. Thus, within the prepyloric region of the trunk,
which must accommodate undigested prey, the most anterior sections have the
narrowest circumference. We hypothesize that, in response to the variation in
body circumference and size of the food bolus, the skin should vary in its
ability to stretch circumferentially in different regions along the length of
the body. Such regional variation in the mechanical properties of skin that is
subjected to different forces has been described in other taxa. Swartz et al.
(1996) found that the skin of
bat wings, which functions as the primary producer of lift and thrust during
flight, varied in mechanical properties among the three regions of the wing
membrane and suggested that this variation reflected the distinct role of each
region during flight. In addition, we hypothesize that the biomechanical
properties of the skin will change in association with the position of the
pylorus, which separates prepyloric skin subjected to large food boluses from
postpyloric skin that overlies the region of the digestive track in which prey
has been reduced markedly in size. To test these hypotheses, we examined
regional variation in the mechanical properties of the skin of T.
sirtalis along the longitudinal body axis.
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Materials and methods |
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Each individual snake was weighed to the nearest 0.001 g using a
top-loading electronic balance and was then euthanized by an intracardiac
injection of sodium pentobarbital. SVL was measured to the nearest millimeter,
and ventral scales were counted following the method described by Dowling
(1951). A midventral incision
was made along the length of the body. At both the anterior and posterior ends
of the incision, a circumferential cut was made through the skin, completely
detaching the body skin from that of the head and tail. To separate the skin
from the body, the anterior edge was gently pulled caudally until the complete
skin of the body was removed. The skin was spread on a flat surface, and
transverse sections were cut using a razor blade. Nine circumferential strips
of skin were prepared, each spanning 10 ventral scales. The excised strips
were centered at increments of 10% of the ventral scale count (VSC); the
initial strip of skin was excised at 10% and the final strip at 90% of the
VSC. These regions were designated ai, with
a being the most anterior and i the most posterior
(Fig. 1). Each excised strip
was divided into equally wide anterior and posterior samples, and the edges of
each sample were straightened using a razor blade to form smooth edges
parallel to the direction of subsequent loading and extension and
corresponding to the transverse body axis. For each individual snake, the
anterior sample from each region was subjected to a uniaxial tensile test, and
the posterior sample was preserved for histological preparation.
|
Determination of skin thickness
Skin thickness was measured from histological sections in order to quantify
the cross-sectional area of samples subjected to mechanical tests. Samples
were manually extended in the circumferential direction until taut. Samples
were then pinned in this stretched condition to a vinyl sheet, fixed in 10%
phosphate-buffered formalin and stored in 70% ethanol. For future morphometric
analyses, including the quantification of dorsal scale rows, digital
photographs of each fixed sample were taken.
For each individual snake, one subsample was removed from each of the nine
regional samples. Each subsample was longitudinally centered within the sample
and incorporated dorsal scale rows four through six of the right side. These
scale rows were selected because they displayed relatively uniform scale
dimensions and similar quantities of intersquamous skin (i.e. skin between the
scales). Within each subsample, each of the three dorsal scale rows contained
no fewer than two complete scales. Subsamples were prepared for histology
using a Shandon Hypercenter XP automatic tissue processor (Pittsburgh, PA,
USA). Subsamples were dehydrated through an ethanol series, cleared in xylene,
embedded in a synthetic paraffin-polymer medium (Paraplast Plus; Oxford
Labware/Sherwood Medical Co., St Louis, MO, USA) and serially sectioned at a
thickness of 10 µm using a Leitz 1512 rotary microtome. Approximately 2 mm
of tissue per subsample was sectioned from posterior to anterior. Sections
were mounted on subbed slides, stained with iron gallein and counterstained
with eosin (Presnell and Schreibman,
1997).
The stained sections were examined with a Nikon Optiphot compound microscope, and digital photographs were taken of the sections using an attached digital camera (Nikon Coolpix 990). After processing the digital images in Photoshop (version 6.0; Adobe Systems, Inc., San Jose, CA, USA), skin thickness was measured using SigmaScan Pro image analysis software (version 5.0; SPSS, Inc., Chicago, IL, USA), using the image of a stage micrometer for calibration. In order to obtain these measurements, serial sections were examined and the anterior progression of the posterior-most scale belonging to the fifth scale row was followed. This series revealed a transition from the unattached posterior tip of the scale to a point where the scale was completely attached to the intersquamous skin on both sides. At the latter point, the minimum thickness of the intersquamous skin was measured between scale row five and each of the two adjacent rows. Those two measurements were averaged to yield a single measure of thickness for the sample. By using the minimum skin thickness of each sample to calculate cross-sectional area, the results provide a conservative estimate of area but may overestimate the stress required to stretch skin circumferentially.
Dorsal scale rows
Regional variation in the number of dorsal scale rows was quantified from
digital images of previously preserved skin samples using the method described
by Peters (1964). The skin
samples (N=108) were from 12 individual snakes: the 11 used for
mechanical tests and one additional specimen.
Determination of in vivo strain
Three additional specimens were euthanized as previously described and
regions ai were located and marked on the intact
specimen. Within the anterior half of each region (i.e. the half subjected to
mechanical testing in the previous specimens), the in situ body
circumference was measured to the nearest millimeter by wrapping cotton thread
(Bellevue 16/4; American & Efird Thd. Mills, Inc., Mt Holly, NC, USA)
around the body and marking both ends at a point where they overlapped. A
linear measurement of the straightened string was made with digital calipers.
The process was repeated three times for each region, yielding three
independent measurements. These values were then averaged to yield a single
value of in situ circumference for each region. Skin samples were
excised from each region, as previously described, and placed on a smooth,
moist glass surface. To prevent curling of the tissue, and to simulate the
storage of samples used for mechanical analysis (see next section), a thin
piece of glass was placed over the sample and a linear measurement of body
circumference was recorded with digital calipers. This method facilitated the
acquisition of accurate measurements and did not induce strain in the resting
samples. The process was repeated three times for each region and those
measurements were averaged to yield a single value of ex situ
circumference. These data were used to determine the degree to which skin was
strained in vivo and allowed for the normalization of any skewed
strain data.
Mechanical testing
All samples used for mechanical analysis were positioned between folded
strips of paper towel moistened with reptilian Ringer's solution
(Guillette, 1982) and placed
in a waterproof plastic container. The encased skin samples were saturated
with Ringer's solution by filling the container, which was then placed on ice
and transported to NASA Langley Research Center (Hampton, VA, USA) for
mechanical testing. All samples were tested within 8 h of being excised
(usually within 6 h). Skin samples were kept on ice until they were removed
for measurement, at which time samples were submerged in a vial of reptilian
Ringer's solution maintained at room temperature (2224°C). Upon
removal from the solution, the circumference, gage length
(l0) and width of each sample were measured to the nearest
0.01 mm using digital calipers (Mitutoyo America Corp., Aurora, IL, USA).
Width was recorded as the maximum distance parallel to the longitudinal body
axis. For measurements of circumference and gage length, moist skin samples
were spread flat on a smooth glass surface and allowed to retract prior to
recording data. Gage length was equal to the linear distance between the
ventral edges of the first dorsal scale row of both the left and right sides
(Fig. 2).
|
Data analysis
Recorded loadextension data were converted to text files (.txt) and
imported into SigmaPlot (version 6.0; SPSS, Inc.). Data were smoothed using a
polynomial regression, and weights calculated from the Gaussian density
function with a sampling proportion of 0.05. Using a custom macro, initial
loads were zeroed and subsequent values were adjusted accordingly. Stress
(=N mm2=MN m2=MPa) was computed by
dividing load values (N) by the cross-sectional area of the test sample (width
x thickness in mm2). Strains (
) were calculated using
extension data and the corresponding gage length. Because the distance preset
between the grips (5 mm) was less than the gage length of each of the test
samples, we scaled the strain data so that a strain of zero corresponded to
the point when the inter-grip distance was equal to the linear measurement of
gage length made prior to testing. Stressstrain curves were then
generated from these data, with the results from each skin sample being
translated into a single curve. Each individual snake had the potential to
generate nine curves, representing the nine sample regions of the body
(Fig. 3).
|
Mechanical data collected for each sample included the strains and instantaneous elastic moduli (E) at stresses of 1.0 and 2.0 MPa. Instantaneous elastic moduli were equal to the instantaneous slope of the curve at the points measured and were calculated using the 1st-derivative function macro of SigmaPlot (version 8.0). The macro computed the running average of 50 adjacent numerical derivatives.
All statistical analyses were performed using SPSS (version 10.0; SPSS, Inc.). In all two-way ANOVA and MANOVA analyses, regions were treated as fixed effects, and specimens (i.e. individuals) were treated as random effects. For data sets not meeting the assumptions of homogeneity of variances and normality, assumptions were satisfied by square-root transformation of the data. Variables showing significant regional effects were analyzed independently using a randomized-block ANOVA and Tukey multiple comparison test; the latter was used to identify homogeneous regional subsets. Unless stated otherwise, results are reported as means ± standard error of the mean (S.E.M.).
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Results |
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Skin thickness
Thickness varied among individual samples from 0.019 to 0.107 mm. Skin was
thinnest in anterior regions (0.038±0.003 mm for region a) and
increased in thickness posteriorly (0.081±0.005 mm for region
i; Fig. 4). Data were
analyzed using a two-way randomized-block ANOVA, and significant differences
among regions were found (F=20.111; d.f.=8,79; P<0.001).
Results of a Tukey test indicated that, although there was nonclinal variation
within the mid-body regions, the anterior-most (a), mid-body
(e) and posterior-most (i) regions were significantly
different from one another.
|
Dorsal scale rows
Scale-row reduction from 19 to 17 rows occurred in all specimens examined;
19 dorsal scale rows were present in regions ad, and
17 were present in regions fi. Region e
represents a transitional region where 17, 18 and 19 scale rows were observed
among the 12 specimens examined. Scale-row reduction involved the loss of
scale row four on both the left and right sides and occurred between regions
d and f (usually between regions e and f;
Fig. 5).
|
Mechanical tests
To detect significant differences among sample regions for all variables,
mechanical data (strains and elastic moduli) were square-root transformed and
analyzed using a two-way mixed-model MANOVA. Significant regional differences
were detected (F=3.082; d.f.=32; P<0.001). Each variable
was then analyzed independently using a randomized-block ANOVA. Significant
regional differences were detected for all four variables
(P<0.001; Table
1).
|
Mean strain values at both stresses (1.0 and 2.0 MPa) were highest in anterior regions (1.565±0.123 and 1.775±0.135 for region a, respectively) and decreased posteriorly (0.790±0.090 and 0.886±0.090 for region i, respectively; Fig. 6). These results indicate that the skin of anterior regions is more compliant than the skin of posterior regions. At both stresses, the anterior-most skin is capable of approximately twice the strain of the posterior-most skin. For both strain variables, mean values for each region were always less than the adjacent, more-anterior region. Results of separate regression analyses on both variables were significant. Mean strain at 2.0 MPa was slightly more strongly correlated with body region (r2=0.534; P<0.001; Fig. 6) than strain at 1.0 MPa (r2=0.487; P<0.001). For each strain variable, Tukey tests indicated that anterior regions ac did not differ significantly from each other and that posterior regions fi did not differ significantly. However, the anterior regions (ac) were significantly different from the posterior regions (fi). In addition, although there was considerable overlap among the homogeneous subsets identified by the Tukey tests, the anterior-most (a), mid-body (e) and posterior-most (i) regions were all significantly different from each other at both levels of stress (Fig. 6).
|
Mean values for the elastic modulus at both stresses (1.0 and 2.0 MPa) were lower for anterior regions than for posterior regions, indicating that skin is more compliant in anterior regions and stiffer in posterior regions (Fig. 7). Mean modulus values at 1.0 MPa were lowest in region a (3.421±0.456 MPa) and highest in region i (9.0±0.552 MPa). Mean modulus values at 2.0 MPa were lowest for region b (6.180±0.507 MPa) and highest for region g (12.338±0.912 MPa; Fig. 7). Linear regression analyses were conducted on elastic moduli at both stresses and indicated a significant (P<0.001) relationship between body region and skin stiffness. Coefficients of determination were nearly equal for elastic moduli at 1.0 and 2.0 MPa (r2=0.417 and 0.413, respectively). However, the coefficients were low in comparison to the strain data, in part because consecutive regions did not consistently increase posteriorly. Results from Tukey tests at both stresses indicate that mean moduli for regions ae comprise a homogeneous subset that differs significantly from a second homogeneous subset consisting of regions fi (Fig. 7). To determine the relationship of these two homogeneous groups to the location of the pylorus, which marks the posterior end of the stomach, two specimens were dissected and the pylorus was located. The pylorus lies between regions e and f, and therefore between the two regional groups defined by integumentary mechanics.
|
The circumference (c) of each skin sample at 2.0 MPa was
calculated using the formula:
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Discussion |
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Whereas Jayne (1988) found
only slight differences in skin mechanics among dorsoventral locations within
a specimen when subjected to longitudinal loading, this study found that
differences among anteroposterior regions were highly significant in response
to circumferential loading. Although the contrasting results may reflect
differences in skin morphology among the species examined (Thamnophis
sirtalis in this study vs six species in
Jayne, 1988
), we suspect that
the direction in which the load was applied (i.e. circumferential vs
longitudinal) had a much larger effect. Skin of another elongate vertebrate,
the American eel (Anguilla rostrata), has been shown to be
anisotropic (Hebrank, 1980
).
The mean terminal elastic modulus for the skin of eels tested in the
circumferential direction was an order of magnitude larger
(1.47x107 N m2) than the modulus for skin
tested in the longitudinal direction (3.54x106 N
m2). The existing data indicate that snakes differ from eels
in the direction in which the skin is stiffer.
Thamnophis sirtalis has considerably more extensible skin than do
geckos, the only other squamate group for which mechanical data on skin are
available. Bauer et al. (1989)
found that the skin of two species of geckos, Ailuronyx seychellensis
and Gecko gecko, had mean failure strains (
f) of
0.31 and 0.57, respectively, tested in the longitudinal direction.
Mechanics of snake skin
The skin of Thamnophis sirtalis exhibits substantial variation in
its mechanical properties among regions of the body. Mean strain was highest
in the anterior-most region of the body and decreased caudally. At both
stresses (1.0 and 2.0 MPa), strains for region i were approximately
50% (0.505 and 0.499, respectively) of the strains attained for region
a. Tukey tests demonstrated that regional differences in strain were
sufficient to identify significantly different anterior (a), mid-body
(e) and posterior (i) regions, despite considerable overlap
among immediately adjacent regions.
The elastic modulus (i.e. stiffness) of the skin increased two- to three-fold between regions a and i. A substantial increase in skin stiffness is observed posterior to the pylorus (i.e. behind region e). Tukey tests for the elastic moduli at both stress levels found significant differences between the prepyloric regions (ae) and the postpyloric regions (fi). This difference in mechanical properties is not surprising. Like most snakes, Thamnophis sirtalis consumes its prey intact, and the bolus is reduced in the stomach prior to passage through the pylorus into the intestine. Therefore, the posterior skin need not be capable of extension as great as that of the anterior skin. Because T. sirtalis is viviparous, it is possible that reproductive females experience different selective pressures in regard to the ability of the posterior skin to stretch, associated with an increase in embryonic size during gestation. While beyond the scope of this paper, subsequent studies could seek to determine whether mechanical differences exist between the skin of reproductively mature male and female snakes.
This study attempted to examine mechanical properties of the ophidian
integument in a biologically relevant context. Tensile tests were conducted at
temperatures within the range at which Thamnophis sirtalis is active
and known to feed in nature (Carpenter,
1956; Nelson and Gregory,
2000
). The use of rectangular strips of tissue produced a more
uniform stress on the sample during loading and allowed crosshead displacement
to be related directly to sample strain, particularly at the low stresses
reported here (Edsberg et al.,
1999
; Foutz et al.,
1992
). Furthermore, because properties of the skin may vary from
the ventrolateral to the middorsal regions, the use of complete
circumferential strips is more likely to reflect behavior of the skin in
vivo. Uniaxial tensile tests were conducted to the point of skin failure.
However, due to the nontapered shape of the mechanically tested skin samples,
severe necking occurred at high stresses and failure of samples occurred at or
near the grips in 61 of the 93 (65.6%) tensile tests. Shearing of the
grip-fastened skin occasionally occurred at high stresses; however, by
visually monitoring the extension of each skin sample, it was determined that
the mechanical data were not affected by shearing or slippage at the low
stresses reported. Nonetheless, because of these complications, failure
strains and maximum stresses were not considered accurate or biologically
informative. The measurement of skin thickness from histological sections was
necessitated by the complex, heterogeneous structure of ophidian skin. While
the use of ethanol in the preparation of the histological samples may have
induced shrinkage, any effects should be constant across all skin samples, and
thus do not impact our conclusions. In addition, the use of formalin-fixed
histological sections for determining skin thickness has been employed in
other studies of vertebrate integumentary mechanics
(Bauer et al., 1992
;
Bauer et al., 1993
) and
provides more accurate values of stress than the method of measuring minimum
skin thickness employed by Jayne
(1988
).
It is probable that data collected using biaxial tensile tests would more
accurately reflect in vivo strain and stiffness values. However, the
intention of this paper is not to describe the exact quantitative properties
of skin in vivo but rather to describe the relative pattern of skin
extensibility among longitudinal regions of the body. We believe that the
quantitative differences observed among regions within our data provide valid
comparisons. In addition, because the majority of studies examining the
mechanical properties of vertebrate integument have used only uniaxial tensile
tests (Jayne, 1988; Bauer et
al., 1989
,
1992
,
1993
;
Brainerd, 1994
;
Greven et al., 1995
;
Zanger et al., 1995
;
Swartz et al., 1996
;
Schwinger et al., 2001
), our
use of this method allows for comparisons across taxa.
Our comparison of in situ and ex situ circumference supports the use of linear measurements of circumference. Biological materials are often pre-strained in vivo, and when samples of such tissues are excised, contraction may result in the inflation of observed strains. However, we observed no significant differences between the two series of skin measurements. We therefore conclude that the skin of Thamnophis sirtalis is not substantially strained in vivo and that the lengths of the excised samples accurately reflected the resting circumference of each region. For an organism that requires substantial extension of the skin when it feeds, it seems reasonable that no appreciable a priori strain exists, since such a resting strain would reduce the possible circumferential distention when prey is consumed.
Integumentary morphology
Along the length of the body, the mean skin thickness of Thamnophis
sirtalis varies by a factor of more than two. Skin is thinnest in the
anterior-most region of the body (region a) and increases caudally,
concomitant with the gradient in decreasing compliance. Although the overall
data show a negative relationship between strain and skin thickness
(Fig. 9), weak positive
relationships exist within seven of the nine regions (ae,
r2=0.000.09; f, r2=0.41; g,
r2=0.19). This suggests that regional differences in the
integument other than variation in thickness along the body axis may influence
the mechanical function of the skin. Such differences may include the number
of dorsal scale rows, the quantity of intersquamous skin, and the angle formed
between adjacent scale rows (Savitzky et
al., 2004). In some macrostomate taxa, it has been argued that
higher numbers of dorsal scale rows are associated with a greater capacity for
stretching (Gans, 1974
;
Pough and Groves, 1983
;
Mullin, 1996
). Shine
(2002
) found that high numbers
of mid-body scale rows were significantly related to the proportion of the
diet consisting of mammals. However, when body size of the snake was accounted
for, the results were not significant. We suggest that a better integumentary
predictor of prey diameter is the pattern of scale-row reduction. Rather than
simply examining the number of dorsal scale rows at mid-body, a more
appropriate approach may be to examine the number of mid-body scale rows
relative to the number of anterior rows. Thamnophis sirtalis has 19
dorsal scale rows in regions ad and 17 rows in
regions fi. The location of this scale-row reduction
corresponds fairly closely to the location of the pylorus, where skin
stiffness noticeably increases. The relative change in strain and elastic
modulus that corresponds to the transition between regions e and
f represents the single largest change between two sequential regions
(Table 2). For values of the
modulus, the magnitude of this change was more than twice that seen between
any other adjacent regions.
|
|
Here, we propose a possible mechanism for the marked decrease in compliance
observed between regions e and f. We suggest that scale row
reduction impacts skin extensibility by decreasing the potential amount of
intersquamous skin that is available to be stretched. The skin, which is
present as folds in anterior regions, permits greater circumferential
extension of the skin as the folds are straightened. It is possible,
therefore, that initial strains are not the result of stressing a taut
material but rather are associated with unfolding. This would help explain why
the initial extension of the skin occurs with relatively little resistance
(Fig. 3). This mechanism for
allowing large extensions is different from that described by Brainerd
(1994) for comparable skin
extension in the puffer fish, Diodon holocanthus, for which no
macrofolds of skin were observed but rather where folded collagen fibers are
the structural innovation. Additionally, regional differences in dermal
ultrastructure, such as diameters and orientation of collagen fibers within
the intersquamous skin, may have a substantial impact on the ability of skin
to stretch once unfolded. While beyond the scope of this paper, future studies
are planned to examine regional variation in the structure of the ophidian
dermis.
The role of skin in feeding
If the maximum circumference attainable during feeding resulted only from
the extensibility of the skin, then large food items would meet gradually
increasing integumentary resistance as they moved through the esophagus and
stomach toward the pylorus. However, the maximum circumference attainable to
accommodate prey is the result of two factors, skin extensibility and body
circumference at rest. As skin extensibility decreases within regions
ae, resting body circumference correspondingly
increases. This increase in resting body circumference within regions
ae partially compensates for the concomitant decrease
in skin compliance, resulting in a higher, less variable maximum attainable
circumference during feeding; such a result was predicted by Cundall and
Greene (2000). Posterior to
region e, body circumference decreases caudally as skin compliance
continues to decrease. The combination of these two factors results in a rapid
decrease in the attainable circumference within postpyloric regions, where
food items have already been reduced in mass.
Phylogenetic trends
Although the skin of Thamnophis sirtalis shows a remarkable
capacity for stretching, it is likely that the skins of certain other species
of snakes have an even greater capacity. Viperid snakes show numerous
morphological adaptations for feeding on very large prey, including
modifications in cranial structure and body shape
(Pough and Groves, 1983).
Although gape obviously represents the first limiting factor in consuming
large prey (King, 2002
), the
extensibility of the skin and certain internal structures, such as the gut,
are also potential constraints. However, it is counterintuitive that the
external skin would evolve the capacity to accommodate large-diameter prey
without concomitant adaptations of internal structures. With respect to
macrophagy, a parallel examination of cranial and integumentary morphology in
basal and advanced alethinophidian snakes should be conducted to determine
whether a correlation exists between gape size and characters associated with
circumferential distention. Likewise, a phylogenetic analysis of the
biomechanical properties of skin may reveal patterns related to the transition
to macrostomy.
If the regional trends in integumentary structure observed in
Thamnophis sirtalis are typical of macrostomate snakes, an
examination of the integument of basal alethinophidian snakes, which are
obligate consumers of slender prey
(Greene, 1997), may reveal a
different pattern. For snakes that do not require highly extensible skin,
regional variation may be minimal. Furthermore, many basal taxa have a
relatively cylindrical body shape. These factors suggest that the skin of
these snakes may be more homogeneous along the length of the body.
This study is the first to provide quantitative evidence demonstrating that skin compliance varies regionally within snakes. We also provide the first mechanical evidence that variation in the properties of skin varies with the demands of macrophagy. Thickness of the skin co-varies with compliance and may be one of its major determinants. Within prepyloric regions, compliance shows an inverse relationship with resting body circumference. Additionally, postpyloric skin is significantly stiffer than prepyloric skin. Scale row reduction, which occurs near the level of the pylorus, coincides with a substantial increase in skin stiffness, perhaps resulting from a reduction in the amount of intersquamous skin due to the loss of one scale row from each side of the body. Further histological and mechanical investigations may shed additional light on the evolution of the ophidian dermis and the diversity that exists among both basal and macrostomate snakes.
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Acknowledgments |
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References |
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