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Can Geckos Increase Shedding Rate to Remove
Fouling?
Authors: Fushida, Ayano, Riedel, Jendrian, Nordberg, Eric J., Pillai,
Rishab, and Schwarzkopf, Lin
Source: Herpetologica, 76(1) : 22-26
Published By: The Herpetologists' League
URL: https://doi.org/10.1655/Herpetologica-D-19-00039
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Herpetologica, 76(1), 2020, 22–26
Ó2020 by The Herpetologists’ League, Inc.
Can Geckos Increase Shedding Rate to Remove Fouling?
AYANO FUSHIDA
1,2
,JENDRIAN RIEDEL,ERIC J. NORDBERG,RISHAB PILLAI,AND LIN SCHWARZKOPF
College of Science and Engineering, James Cook University, Townsville, Queensland 4811, Australia
ABSTRACT: All vertebrates shed the outer layer of their epidermis, usually continuously, but squamate reptiles shed periodically, losing large
pieces of this layer at once. While the cellular processes leading to loss of the outer epidermal layer, or shedding, in squamates have been studied
in detail, few studies have examined the factors associated with shedding frequency. Shedding is an obligate event, linked to somatic growth and
the regeneration of damaged or worn epidermal areas. Another proposed role for periodic shedding in squamates is the removal of ectoparasites
and fouling substances stuck on the epidermis. It is unclear whether the removal of ectoparasites and fouling substances is completely passive,
only mediated by a fully obligate shedding cycle, or if shedding can be mobilized directly in response to parasite attachment or fouling. To test
these hypotheses, we first assessed whether shedding reduced the adherence of parasites to the skin of six different species of geckos by counting
mites on the outer epidermis before and after shedding events. Next, we assessed whether shedding was triggered by fouling. Using four species
of geckos, we applied artificial substances (marker pen [Sharpie
TM
], and wood glue [polyvinyl acetate]) to the outer layer of the epidermis and
recorded the time between shedding events (shedding interval) compared to unmanipulated controls. There was a clear decrease in parasite loads
after shedding events, confirming that shedding reduces adherence of parasites. Our experiments with artificial substances applied to the outer
epidermis showed that most gecko species did not change their shedding intervals, regardless of skin-fouling treatment. Hemidactylus frenatus,
however, decreased their shedding interval in response to the application of wood glue. Thus, we found that parasites, if present, are removed by
shedding, and external fouling can trigger shedding at least in one species of gecko.
Key words: Australia; Ectoparasites; External stressor; Reptile; Skin; Sloughing
ACOMMON feature of all vertebrates is that the outermost
layer of the epidermis is removed and replaced by a new
layer in a process referred to as shedding (ecdysis). The
process and frequency of shedding differs among taxa.
Squamate reptiles have a particularly complex, multilayered
epidermis and a regular shedding cycle, shedding the entire
outer epidermal layers (including the stratum corneum)
either at once, or in large fragments (Landmann 1979;
Maderson 1985; Irish et al. 1988; Harkewicz 2002). Before
the old epidermal layer (exuviae) is sloughed, new keratino-
cytes fully differentiate underneath to form a new multilay-
ered epidermis, and shedding is triggered once these
keratinocytes mature (Alibardi 1995, 1998, 2014; Lillywhite
2006).
Shedding occurs for several reasons. First, it allows for
growth and regeneration (Maderson and Licht 1967; Irish et
al. 1988; Harkewicz 2002). As body size increases, the
epidermal layers must expand, or if the epidermis is
damaged, it must be replaced (Ling 1972; Irish et al.
1988). Shedding also restores epidermal functions that may
be reduced by fouling from substances sticking to, or
growing on, the epidermal surface (B ¨
ohme and Fisher 2000;
Cramp et al. 2014). For example, geckos have water-
repellent skin, allowing self-cleaning by water droplets
rolling over hydrophobic skin surfaces (Hiller 2009; Watson
et al. 2015), and both fouling and damage can reduce this
self-cleaning ability, so renewal by shedding is useful.
Finally, parasites may adhere to the epidermis, and shedding
may remove them and reduce their impact, although
demonstrations of this are rare (Zann et al. 1975; Chinnas-
amy and Bhupathy 2013; Lillywhite and Menon 2019), and
some studies have found that shedding does not reduce
ectoparasite numbers (Klukowski and Nelson 2001).
Although the histology and ultrastructure of the outer
epidermis and the cellular and biochemical processes
associated with shedding in squamates are relatively well
studied (Maderson 1966, 1967; Alibardi 1998; Maderson et
al. 1998), few studies examine the factors affecting shedding
rate. It is, therefore, unclear whether shedding occurs
exclusively as an obligate event, at regular intervals, or if
shedding frequency can be modified facultatively, for
example by increasing shedding rate in response to external
skin stressors such as parasites, damage, or fouling. A high
shedding frequency in association with fouling has been
reported in some reptiles; for example, some sea snakes,
which are often fouled by ectoprocts, shed frequently
(Kropach and Soule 1973). To our knowledge, however, no
studies have examined if shedding frequency can be
increased as a direct response to ectoparasites or fouling.
Some lizards shed more frequently at higher ambient
temperatures (Chiu and Maderson 1980), and humidity
can influence shedding interval (Maderson et al. 1998),
whereas hormones appear to have no effect on shedding
interval at a given temperature (Chiu et al. 1986). It remains
unclear, however, whether shedding can be triggered by
external stressors on the epidermis itself, such as when the
skin is damaged or fouled, or when parasitic attachment has
taken place.
We used geckos as a model system to determine (1)
whether shedding frequency was influenced by fouling, and
(2) if shedding was an important mechanism to remove
parasites. We quantified if shedding rate was increased by
the presence of (artificial) fouling substances on the skin. We
also determined if shedding was associated with removal of
ectoparasites in these lizard species, and if the shedding
interval was related to parasite load. To accomplish these
aims, we quantified the shedding interval of four species of
1
PRESENT ADDRESS: Monash University, Wellington Road, Clayton,
Victoria 3800, Australia
2
CORRESPONDENCE: e-mail, ayano.fushida@my.jcu.edu.au
22
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geckos before and after experimental skin fouling was
applied, and we counted ectoparasites before and after
shedding in six species of geckos while recording shedding
interval in relation to parasite load.
MATERIALS AND METHODS
Collection and Housing
Individuals of six species of gecko were collected and used
in this study: Common House Geckos (Hemidactylus
frenatus; SVL ¼49 60.75 mm, SE), Eastern Spiny-tailed
Geckos (Strophurus williamsi; SVL ¼52 61.58 mm, SE),
Box-patterned Geckos (Lucasium steindachneri; SVL ¼49
61.32 mm, SE), Northern Velvet Geckos (Oedura
castelnaui; SVL ¼74 63.80 mm, SE), Northern Spotted
Velvet Geckos (Oedura coggeri; SVL ¼71 62.63 mm, SE),
and Ocellated Velvet Geckos (Oedura monilis; SVL ¼83 6
1.70 mm, SE). A total of 73 H. frenatus,10S. williamsi,5L.
steindachneri,10O. castelnaui,11O. coggeri, and 10 O.
monilis, were captured. Hemidactylus frenatus,S. williamsi,
L. steindachneri, and O. castelnaui were all hand-captured
from the buildings and bushland surrounding the James
Cook University (JCU) campus, Townsville, Queensland,
Australia (19819034 00 S, 14684502600 E; in all cases datum ¼
WGS84), while O. coggeri and O. monilis were collected
near Hidden Valley, Queensland, Australia (1885803900 S,
146802014 00 E), between March and September in 2017. All
geckos used for experiments were sexually mature. Geckos
were transported to a controlled-temperature room at JCU
and were kept in a 12:12-h light:dark room at 288628C
during the day and 228628C at night, at a constant relative
humidity (67%). Geckos were held individually in translu-
cent plastic containers (28 mm 319 mm 310 mm), with
mesh lids to allow air exchange. Geckos were provided with a
heat strip running under one side of the enclosure to allow
for thermoregulation (maximum temperature ¼338C) and
supplied with a water dish, and several layers of paper towel
and a tile, which served as shelter. Geckos were fed
European Domestic Crickets (Acheta domestica) three times
per week.
Shedding Interval
We documented the shedding interval of H. frenatus over
a period of 5 mo and of three other species of geckos (S.
williamsi,L. steindachneri,andO. castelnaui) over a period
of 3 mo. To establish that shedding had occurred, enclosures
were visually examined daily for skin fragments in the
enclosure (except for H. frenatus, see below). Treatment
groups included (1) a control with no fouling agent, (2) a 1-
cm line (0.25-cm width) applied with a nontoxic permanent
marker (glyceride, pyrrolidone, and resin; Sharpie
TM
) to the
dorsal surface of the geckos, or (3) a 1-cm strip (0.25-cm
width) of transparent-drying white wood glue (polyvinyl
acetate; PARFIX
TM
) mixed with nontoxic food coloring
(Queen
TM
) or fluorescent powder for visual detection,
applied to the dorsal surface of the geckos. We chose two
types of fouling agents (marker and glue) because they were
inexpensive, easy to apply, and had different physical
properties. By using both glue and a marker, we covered
both viscous and fluid adherent types.
Because we had a large number of H. frenatus available,
we compared shedding interval among groups of this
species. Ten H. frenatus represented controls (no external
fouling applied), 30 were exposed to permanent marker, and
10 had wood glue applied to their epidermis. Some
individuals were tested more than once by reapplying the
treatment after shedding. Individuals of the other three
species of geckos (S. williamsi,n¼10; L. steindachneri,n¼
5; and O. castelnaui,n¼10), received each of the three
treatments sequentially in a random order, such that all
individuals (n¼25) were exposed to all treatments (control,
permanent marker, and wood glue). When an individual
shed, a new treatment was applied the same day. We were
not able to monitor the shedding frequency for O. coggeri
and O. monilis long enough to collect data as they were
added later in the project.
Detection of Shedding in Keratophagic Species
Hemidactylus frenatus was the only keratophagic species
in our experiment (they eat skin fragments as they shed;
Mitchell et al. 2006), so shedding could not be easily or
accurately detected for this species by looking for shed
epidermis in their enclosures. For H. frenatus, we recorded
the dates when fouling disappeared from the dorsum as our
measure of shedding interval. As this was not possible for the
control group, we measured shedding interval of control
animals by checking for epidermal remnants in the feces. We
estimated gut passage times to determine how long
epidermal fragments would remain in the gut by feeding
geckos small inert plastic beads and watching for their
reappearance in feces. Two to three beads were injected into
the body cavity of a cricket and fed to each gecko, after
which all fecal samples were collected in the days following
and searched for beads to calculate approximate gut passage
time. We calculated gut passage time as the interval between
consumption of the beads and the appearance of the first
bead in the feces. Small fragments of epidermis could also be
identified from fecal dissections under a microscope, and
therefore, given estimated gut passage times, we were able to
back-calculate the date of shedding. We applied both the
disappearance of the fouling and the appearance of
epidermal fragments in the feces to determine shedding
rate in the geckos that had been fouled with marker pen. In
this way, we could ensure that the shedding interval
calculated with these different methods (looking for shed
skin in feces and looking for the disappearance of marker
pen) matched the actual shedding interval.
Ectoparasite Load
A total of 69 geckos (H. frenatus,n¼23; S. williamsi,n¼
10; L. steindachneri,n¼5; O. castelnaui,n¼10; O. coggeri,
n¼11; O. monilis,n¼10) were used to test for differences
in external parasite loads before and after shedding. Initially
we did not include H. frenatus in our ectoparasite
experiment because they are keratophagic, and we could
not identify when they shed their skin. However, after
running the fouling experiment, we realized that marker pen
could be used to determine shedding interval. All observed
ectoparasites were pterygosomatid mites (Barnett et al.
2018). The total number of mites on the skin surface of each
gecko was counted using a hand lens, and all mites were
counted before (upon capture) and 1 to 2 d after shedding
for each gecko.
23
FUSHIDA ET AL.—SHEDDING RATES IN GECKOS
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Statistical Analyses
To detect differences in the abundance of mites before
and after shedding for those species that had mites upon
capture, we used a linear mixed-effect model (LME) in the
nlme package (Pinheiro et al. 2017). Our model included the
number of mites as the response variable, species and time
(before or after shedding) as fixed-effects, and the gecko
individual as a random factor. In addition, correlation
between shedding interval and number of mites in H.
frenatus was examined with Pearson’s correlation coefficient.
All analyses were conducted using the statistical software R
v3.4.1 (RStudio Inc., Boston, MA).
To determine the effects of the fouling treatments on
shedding interval, we used an LME model with shedding
interval as the response variable, species and treatments as
fixed factors, and the gecko individual as a random factor.
Using these models to identify significant effects, Wald’s v
2
test was used to find overall significance, and a Type II
analysis of variance table was produced using the car package
(Fox and Weisberg 2011). Where appropriate, multiple
comparisons using Tukey’s procedure were conducted with
the package lsmeans (Lenth 2016) to compare among
species, as well as among treatments.
RESULTS
Shedding Interval in Response to Fouling
There was a significant difference in natural shedding
periods (determined by comparing control animals) among
the four species of geckos (F
3,71
¼8.52, P,0.01; Fig. 1).
Strophurus williamsi had significantly longer shedding
intervals than H. frenatus and L. steindachneri (P,0.01
and P¼0.021, respectively; Fig. 1), whereas there was no
significant difference in shedding interval between S.
strophurus and O. castelnaui (P¼0.23).
In H. frenatus, there was no significant difference in the
shedding intervals determined by the presence of shed skin
fragments in feces versus the disappearance of marker pen
(mean shedding rate interval using the appearance of skin
fragments in the feces: 21 62.73 d, SE, n¼11; mean
shedding rate interval using the disappearance of marker
pen: 17.17 61.20 d, SE, n¼42; t¼1.92, df ¼1, P.0.05).
Thus, we used the data from both of these methods together
in the rest of these analyses. There was a significant
difference in shedding rate among fouling treatments in H.
frenatus, such that geckos fouled with wood glue had a
significantly shorter shedding interval than controls or those
fouled with marker pen (wood glue versus the control, P,
0.01; wood glue versus marker pen, P,0.01; Table 1).
There was no significant difference in the shedding intervals
of control unmarked lizards and lizards marked with marker
pen (P¼0.79; Table 1). Moreover, there was no significant
effect of the fouling treatments on shedding interval in the
other three species (S. williamsi,L. steindachneri, and O.
castelnaui; Fig.1).
The Influence of Shedding on Ectoparasite Loads
Of the six species we examined, 91.3% of Hemidactylus
frenatus (21 of 23 individuals, an average of 62.0 613.26
mites per individual), 72.7% of O. coggeri (8 of 11
individuals, 19.2 611.08 mites per individual), and 80% of
O. monilis (8 of 10 individuals, 5.6 61.86 mites per
individual) had mites upon capture (i.e., preshedding),
whereas L. steindachneri,O. castelnaui, and S. williamsi
had no mites present upon capture. After shedding, H.
frenatus carried an average of 38.19 69.36 mites per
individual, O. coggeri carried 0 mites per individual, and O.
monilis carried 0.13 60.13 mites per individual. The LME
showed significant differences among species (v
2
¼12.97, df
¼2, P,0.01; Fig. 2), and before and after shedding in the
number of mites (v
2
¼21.58, df ¼1, P,0.01; Fig. 2).
Hemidactylus frenatus had higher natural average parasite
loads than did O. monilis and O. coggeri (Fig. 2).
Importantly, H. frenatus (t
20
¼4.25, P,0.01; Fig. 2), O.
coggeri (t
7
¼3.41, P¼0.011), and O. monilis (t
7
¼2.57, P¼
0.037) all had significantly fewer mites after shedding. There
was a weak, marginally significant correlation between
parasite number and shedding interval in H. frenatus (R
2
¼0.35, P¼0.10, n¼23).
DISCUSSION
Geckos benefit from shedding their epidermis by
reducing the total abundance of ectoparasitic mites, as
parasites negatively impact host fitness in lizards (Pence and
Selcer 1988; Par´
e 2008; Caballero et al. 2015). Similarly,
shedding reduced the number of cutaneous microbes on
frogs (e.g., Cramp et al. 2014; Ohmer et al. 2015).
Hemidactylus frenatus, an introduced species, had the
highest parasite loads, and individuals lost about 50% of
FIG. 1.—The number of days between shedding events in four different
species of geckos, Common House Geckos (Hemidactylus frenatus,n¼73),
Box-patterned Geckos (Lucasium steindachneri,n¼5), Northern Velvet
Geckos (Oedura castelnaui,n¼10), and Eastern Spiny-tailed Geckos
(Strophurus williamsi,n¼10), unfouled or fouled with two different
treatments (ink, Sharpie
TM
marker pen; glue, polyvinyl acetate adhesive).
The bars show shedding intervals. Asterisks indicate a significant decrease in
shedding interval among treatments for Common House Geckos (H.
frenatus).*P0.05. ** P0.01.
TABLE 1.—Pairwise comparisons showing the differences in shedding
interval (days) among three different fouling treatments using Tukey’s post-
hoc tests for Common House Geckos (Hemidactylus frenatus).
Multiple comparison
Mean
difference (d) SE df Pvalue
Control: marker 0.94 1.43 95 0.788
Control: wood glue 7.50 1.47 95 ,0.0001
Marker: wood glue 6.56 1.50 95 0.0001
24 Herpetologica 76(1), 2020
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their parasites when they shed. In contrast, native species
had much lower parasite loads, and lost all their mites upon
shedding. We assessed mite numbers when geckos were
captured, and then counted mites after shedding, after
geckos had been in captivity for some time. It is possible that
mite load was somehow reduced by the time in captivity,
rather than by shedding. We think this unlikely, however, as
mites are notoriously difficult to eliminate in captivity, and
simply reinfest untreated reptiles (Harkewicz 2001). Instead,
we think it most likely that shedding was the factor that
eliminated the mites in this study. Another study also found
high mite loads in H. frenatus compared to Australian native
geckos (Torchin et al. 2003), and one study found two
species of ectoparasitic mites, restricted to H. frenatus, that
have apparently coevolved with them, suggesting that high
host specificity of mites may explain high infestation (Coates
et al. 2017). Also, there was a trend in our study for higher
mite loads in H. frenatus to be associated with slightly
shorter shedding intervals, suggesting this species may
mobilize shedding to eliminate parasites.
Consistent with a previous study (Weldon et al. 1993), we
found H. frenatus was keratophagous. In squamates,
keratophagy is widely documented, especially for geckos
(Bustard and Maderson 1965). In our study, S. williamsi,L.
steindachneri, and O. castelnaui did not consume their shed
epidermis, which was particularly interesting as keratophagy
is reported for some of their close relatives (e.g., Diplodac-
tylus elderi [now Strophurus elderi], Bustard and Maderson
1965; O. marmorata, and O. tyroni, Weldon et al. 1993).
Shed epidermis may be consumed to reduce parasite loads
(Mitchell et al. 2006). Possibly, H. frenatus is keratophagous
in an attempt to reduce the relatively high mite loads they
carry, compared to native geckos.
Another role suggested for keratophagy is to recover
nutrients (Noble 1954; Bustard and Maderson 1965; Weldon
et al. 1993; Mitchell et al. 2006). In our study, the
occurrence of keratophagy was associated with the ability
to mobilize shedding in response to fouling. Perhaps
mobilization of shedding, or a decrease in shedding interval,
was possible in H. frenatus because they can recover the lost
nutrients in the shed epidermis more easily than geckos that
do not consume their shed epidermis. Further study of the
causes and functions of keratophagy may reveal why it occurs
in some species but not others, and whether it is more
generally coincident with mobilization of shedding. Com-
parison of a wider range of gekkonids and diplodactylids may
help elucidate the variation in and causes of keratophagy.
We examined how shedding interval responded to
epidermal fouling in a range of geckos. Fouling, while
similar to ectoparasites in some ways, is a different epidermal
integrity problem faced by animals. We found that H.
frenatus individuals responded to the presence of glue on
their epidermis by decreasing their shedding interval,
perhaps indicating that they can increase their shedding
frequency as a reaction to fouling. As fouling, or attachment
of substances to the skin, is potentially harmful (B ¨
ohme and
Fisher 2000; Cramp et al. 2014), this suggests that at least
some squamate reptiles can increase their shedding rate to
remove these kinds of external stressors, as suggested for
some species of sea snakes (Zann et al. 1975; Lillywhite and
Menon 2019). Contrary to H. frenatus, we found no evidence
that fouling with polyvinyl acetate (glue) and ink altered
shedding rate in the other species, suggesting that shedding
interval is influenced by fouling only in some species. We
therefore suggest that, rather than altering shedding cycles
in response to fouling events, most species have evolved an
optimal shedding frequency which balances the resources
required to generate a new epidermis with the rate at which
their epidermis becomes sufficiently fouled, dirty, or
damaged, so its function is maintained.
There was a wide range in shedding intervals, from 18 d in
H. frenatus and L. steindachneri,to40dinS. williamsi.In
contrast, the shedding interval reported for Tokay Geckos
(Gecko gecko) was approximately 25 d (Chui and Masterson
1980). Some studies have shown that the level of hydration in
the epidermis plays an important role in shedding for
squamates (Maderson et al. 1998; Lillywhite 2006), but
factors causing variation in these periods still needs further
exploration. Possibly, food availability and environmental
conditions (e.g., humidity), as well as the amount of damage
or fouling typically encountered may be factors causing
differences in shedding intervals. In our study, it was not
clear what was driving such differences. Hemidactylus
frenatus had the fastest shedding cycle of the species we
examined, which may be associated with high levels of
fouling by ectoparasites. The effect of fouling on shedding
frequency may differ among species that occupy different
microhabitats; for example, ground-dwelling species may
accumulate more epidermal adherents than do tree-dwelling
species (Riedel et al. 2019). However, H. frenatus,O.
castelnaui,andS. williamsi are all arboreal, whereas L.
steindachneri is terrestrial, so the differences in shedding
interval we observed do not align well with microhabitat, and
we have too small a group of species from which to draw
conclusions.
In general, H. frenatus reacted differently from the other
species. Hemidactylus frenatus had the highest mite load,
lost the smallest proportion of that load when shedding, had
the ability to activate shedding in response to fouling, shed in
small pieces, and was keratophagous. All these differences
FIG. 2.—Differences in the number of mites before and after shedding for
Common House Geckos (Hemidactylus frenatus,n¼23), Northern Spotted
Velvet Geckos (Oedura coggeri,n¼11), and Ocellated Velvet Geckos (O.
monilis,n¼10). The bars indicate the mean number of mites and the error
bars show the standard error of the mean. Asterisks indicate a significant
reduction in mite loads after shedding for each species. *P0.05. ** P
0.01.
25
FUSHIDA ET AL.—SHEDDING RATES IN GECKOS
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could be related to phylogenetic affiliation, as H. frenatus
belongs to the family Gekkonidae, whereas the other species
we studied all belong to the Diplodactylidae. It is difficult,
therefore, to generate adaptive explanations for differences
between H. frenatus and the other species, as there may be
phylogenetic influences on their physiology that produce
differences that are characteristic of the group. Further
studies comparing larger groups of gekkonids and diplodac-
tylids are required to examine these questions.
Acknowledgments.—We thank J. Simme for assistance with checking
and caring for the geckos. The study was approved by the James Cook
University Animal Ethics Permit (A2409). Animals were collected under the
scientific purposes permit WISP 18552417 granted by the Department of
Environment and Heritage Protection. Fieldwork was supported by a grant
from the Skyrail Rainforest Foundation.
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Accepted on 30 November 2019
Associate Editor: Denis Ota
´vio Vieira Andrade
26 Herpetologica 76(1), 2020
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