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Ethology. 2021;127:465–474. wileyonlinelibrary.com/journal/eth
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465© 2021 Wiley- VCH GmbH
1 | INTRODUCTION
Predator- based natural selection has produced many examples of
convergence in antipredator traits and is a major driver of phenotypic
diversit y (Arbuckle & Speed, 2015; Barber et al., 2015; Langerhans
& DeWitt, 2004; Walsh & Reznick, 2009). Antipredator traits are
diverse and can include chemical (Arbuckle & Speed, 2015), me-
chanical (Stankowich & Campbell, 2016), and color defenses (Davis
Rabosk y et al., 2016). Relative to other antipredator trait s, color de-
fenses can function to startle (Umbers et al., 2017), decoy (Watson
et al., 2012), or warn of a defense (Kozak et al., 2015; Summers &
Clough, 2001; Wang & Shaf fer, 2008) (sometimes falsely in the case
Received: 18 Septemb er 2020
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Revised: 12 Ma rch 2021
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Accepted: 13 March 2021
DOI: 10.1111/eth.13152
RESEARCH ARTICLE
Tactile stimuli induce deimatic antipredator displays in ringneck
snakes
Christian L. Cox1,2 | Albert K. Chung2,3 | Christopher Blackwell4 | Maura M. Davis2 |
Miranda Gulsby2,5 | Hasib Islam2 | Nathan Miller2,6 | Carson Lambert2 | Olivia Lewis2 |
Ian V. Rector2 | Marleigh Walsh2 | Alannah D. Yamamoto2,7 | Alison R. Davis Rabosky8
1Department of Biological Sciences, Florida
International University, Miami, FL , USA
2Mounta in Lake Biological Statio n,
University of Vi rginia, Charlottesville, VA,
USA
3Department of Ecology and Evolutionary
Biolog y, Universi ty of California Los Angel es,
Los Angeles, CA , USA
4Tidewater Community College,
Chesapeake, VA, USA
5Department of Biology, Kennesaw State
University, Kennesaw, GA, USA
6James Madison Uni versit y, Harriso nburg,
VA, USA
7University of Marylan d, College Park, MD,
USA
8Department of Ecology and Evolutionary
Biolog y and Museum of Zoology, (UMMZ)
Correspondence
Christ ian L. Cox, Department of Biological
Sciences, Florida International University,
Miami, FL , 33199.
Email: ccox@fiu.edu
Editor: Jonathan Wright
Abstract
Adaptations for predator defense are often complex traits with integrated display
components spanning multiple signaling modalities. For antipredator coloration like
deimatic or startle coloration, behavioral variation controlling dynamic color dis-
plays is an important but poorly understood component of the predator defense in
most taxa. We studied antipredator behavior in North American ringneck snakes
(Diadophis punctatus), which possess a brightly colored (red to yellow) ventral surface
of the body and the tail compared to the mostly gray dorsal coloration. We sought
to (a) characterize intraspecific variation in antipredator behaviors in ringneck snakes
and (b) test which stimuli can induce antipredator displays. First, we assessed anti-
predator displays in the field and during routine handling during data collection by
comparing categorical classifications of all displayed behavior across 25 individuals.
Second, we performed experimental assays with tactile and visual stimuli to deter-
mine the cues that can elicit an antipredator display in ringneck snakes. We found
that antipredator displays include ventral displays and tail- coiling and that these com-
ponents were induced by tactile cues in the field and the lab, but not visual cues. Our
work is the first to show that a snake species with bright ventral coloration uses this
behavior in response to tactile cues from a potential predator, but only in response to
relatively strong stimuli (i.e., handling). This experimental evidence that tactile stimuli
can induce a behavior revealing bright ventral coloration highlights the importance of
correlated evolution of antipredator coloration and behavior.
KEY WORDS
antipredator behavior, antipredator color, aposematism, deimatism, flash coloration, startle
coloration
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COX et al.
of mimicry). While much attention has been paid to antipredator col-
oration in general, we know relatively little about certain types of
antipredator coloration (e.g., startle and decoy coloration) and the be-
haviors that are associated with these color patterns (Stevens, 2015;
Umbers et al., 2017). For antipredator coloration like startle color-
ation, behavior is an integrated component of the predator defense
that has not been well- studied in most taxa (Rowe & Halpin, 2013).
Deimatic or startle coloration is a type of antipredator col-
oration whereby brightly contrasting (Bordignon et al., 2018)
or threatening (Martins, 1989; Stevens, 2005; Stevens &
Ruxton, 2014) patterns or colors are concealed until a predatory
attack. During a predator y attack, the deimatic coloration is re-
vealed suddenly, which causes the predator to pause or startle,
granting the prey a brief period in which to escape (Umbers et al.,
2015, 2017). Deimatic coloration might also warn of chemical de-
fenses that would leave prey unpalatable or toxic to predators
(Lenzi- Mattos et al., 2005; Umbers & Mappes, 2015). Crucially,
deimatism requires that the antipredator color trait is coupled
to defensive behavior (Umbers et al., 2015, 2017). Deimatic col-
oration is phylogenetically widespread, with well- known ex-
amples including insects (Loeffler- Henry et al., 2019; Umbers &
Mappes, 2015), cephalopods (Langridge, 2009a), frogs (Bordignon
et al., 2018; Martins, 1989), lizards (Badiane et al., 2018), and
snakes (McCallum, 2006; Richards, 2017). However, for many tax-
onomic groups like snakes, deimatic coloration is diagnosed based
solely upon the presence of color traits not immediately evident on
the organism's most visible surface. Indeed, lit tle is known about
the antipredator behavior of snakes with deimatic coloration or
the cues that stimulate their expression.
Many defensive behaviors are deployed in response to a
stimulus, which can include signals from predators or other dan-
gerous situations (Blanchard et al., 1994). The predatory stimu-
lus can be of a t actile (Brodie et al., 1991; Davis Rabosky et al.,
2021; Mukherjee & Trimmer, 2020; Roth & Johnson, 2004), ol-
factor y (Peacock, 1998), auditory (Curlis et al., 2016), or visual
nature (Davis Rabosky et al., 2021; Herzog et al., 1989; Moore
et al., 2020). The behavioral response that is invoked in response
to the predatory stimuli is often potentiated by the intensity of the
stimulus (Herzog et al., 1989; Roth & Johnson, 2004) and body tem-
perature in ectotherms (Brodie et al., 1991). Antipredator displays
in some species with deimatic coloration are generally stimulated
by relatively intense stimuli, such as tactile stimuli (Lenzi- Mattos
et al., 2005; Martins, 1989; Umbers & Mappes, 2015). However,
the stimuli that can induce antipredator displays in other species
with deimatic coloration, including snake species, are not as well
understood.
Snakes ca n possess a bri ghtly colore d ventral sur face that is wid ely
interpreted as evidence of deimatic coloration (Gehlbach, 1970). This
brightly colored venter can be red, orange, yellow, and even brilliant
white (Deepak, 2015; Greene, 1997). Anecdotally, many species that
possess bright ventral coloration also display conspicuous inversion
behaviors that dynamically expose the ventral surface of the body
or tail (Davis, 1948; Fitch, 1975; Greene, 1973), and bright ventral
coloration can be associated with lower predation in some species
(Cyriac & Koda ndaramaiah, 2019). For this r eason, some aut hors have
suggested that bright ventral coloration might ser ve an antipreda-
tor role as deimatic coloration (Ernst & Ernst, 20 03; Greene, 1997;
Jensen, 2008). However, even for well- studied species, there is little
more than anecdotal evidence that species with bright ventral col-
oration have behavioral reper toires that are deployed in response to
potential predators.
We studied antipredator behavior in ringneck snakes (Diadophis
punctatus), which possess bright ventral coloration that is very differ-
ent from their cryptic dorsum (Davis, 1948; Richards, 2017). Ringneck
snakes are small- bodied and widely distributed across Nor th America
(Fontanella et al., 20 08). These snakes have wide habit at preferences
and are fou nd from deciduous f orest to desert w here they subsist u pon
invertebrates and small vertebrates (Ernst & Ernst, 2003). In some lo-
calities, they can be the most abundant vertebrate in an ecosystem
(Fitch, 1993). While these snakes are grey to brown dorsally with a
prominent yellow nuchal collar, their ventral sur face is brightly colored
in hues ranging from red to yellow (Figure 1). When confronted by a
predator, these snakes frequently (60%– 96% of encounters) perform
an antipredator display that involves writhing and coiling the tail to
expose the brightly colored venter (Fitch, 1975; Smith, 1975). Despite
being an abundant and relatively well- studied ver tebrate, little else is
known about variation in their antipredator behavior that might be as-
sociated with their bright ventral coloration.
We sought to 1) characterize antipredator behaviors in ringneck
snakes and 2) te st which stimuli c an induce antipredator displays that
are typically associated with deimatic coloration. To do this, we re-
corded antipredator displays in the field and during routine handling
during dat a collection. Second, we performed behavioral assays with
tactile and visual stimuli to test whether the antipredator display in
ringneck snakes is cue- dependent. We found that antipredator be-
haviors of ringneck snakes included ventral displays and tail- coiling,
and these behaviors were instigated by tactile (but not visual) cues
in the field and the lab.
2 | MATERIALS AND METHODS
2.1 | Field collection and morphology
We collected 25 ringneck snakes from a rocky area adjacent to a
road near Mountain Lake Biological Station in Virginia, USA in the
first t wo weeks of June 2018. Due to its location and high density of
snakes, this area is likely a hibernacula and oviposition site for gravid
females. Rocks were c arefully turned, and the snakes underneath
were captured by hand and placed into a container for transport .
All snakes that were encountered were retained for this study and
all snakes experienced each stimulus type. From initial capture until
release, we attempted to handle all snakes in as similar fashion as
possible to standardize the environment. We scored behavior dur-
ing this initial encounter (see section 2.4, below). At the end of each
sampling event, the snakes were transpor ted back to the laboratory
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COX et al.
in Mountain Lake Biological Station for processing on the evening
of capture. Body size was measured as snout- vent length (SVL) and
total length (TL) to the nearest mm using a ruler as well as body mass
to the nearest 0.1 g using an AWS- 100 Digital Scale. Sex was deter-
mined based upon observing the width of the base of the tail (wider
and less tapering in males than females) and occasionally ever ting
the hemipenes. Scars (binary variable), gravid status (binary variable
for females only, based upon palpating abdomen), and state of ecdy-
sis (binar y variable, based upon opaque eyes and shedding skin) were
also recorded. We also noted all behaviors exhibited during process-
ing, which was an encounter likely to instigate defensive behavior.
The same three individuals collected snakes and made behavioral
observations during capturing and processing.
2.2 | Visual stimuli experiments
All behavioral trials took place in the following two days after capture.
During this period of time, snakes were housed in 1- liter plastic con-
tainers with a moist substrate at a depth of ca. 3 cm to allow burrow-
ing. During the day (0900– 1600), the snakes were held in a research
laboratory for behavioral experiments but housed in a temperature-
controlled room (maint ained at a constant temperature of 25°C) on a
12L:12D light cycle for the rest of the time period. Snakes were not fed
during this time, and because we palpated the abdomen of the snakes
to check for stomach contents, all snakes were likely post- absorptive
during behavioral trials. Snakes were only handled during capture, pro-
cessing, and the transfer to behavioral arenas.
We tested the behavioral response of snakes to three different
visual stimuli: human hand, taxidermy prepared crow, and taxidermy
prepared raccoon. All snakes were exposed to all visual stimuli prior
to tactile stimuli experiments. We used only a single mounted pred-
ator and human to standardize the visual stimulus. Because we used
a single model for each stimulus, this limits our inference to the class
of visual stimuli, and we do not draw conclusions about generalized
antipredator responses to crows, raccoons, or humans (Kroodsma
et al., 2001). The same three individuals conducted all visual stimuli
experiments. We did not use a control group, because we were in-
terested specifically in stimuli that would lead to a ventral display,
and not a general exploration of antipredator behavior. Prior to
each trial, the snake was placed in a behavioral arena (82 × 45 cm)
with soil substrate (from nearby forest) to a depth of ca. 4 cm and
a refuge in the form of a flat cover object (a flat tile that measured
45 × 45 cm). We did not attempt to control for odor among visual or
tactile stimuli trials for practical reasons, but the presence of multi-
ple humans in the room would have likely standardized odors among
stimuli t ypes. The snake was allowed to acclimate in the behavioral
arena for 30 min prior to the trial. Because the snakes began each
trial under the cover object, the cover object was removed to reveal
the snake. Following cover object removal, the stimulus was pre-
sented after a 5 s lapse. Each stimulus was presented for 10 s at ap-
proximately 25 cm from the head of the snake. Each individual was
presented with visual stimuli across three trials, separated by 10 min
of rest. The order of the stimuli for each individual was randomized
to avoid bias created by any order effect.
2.3 | Tactile stimuli experiments
Following the visual stimuli experiments, we tested the behavioral re-
sponse of snakes to four dif ferent tactile stimuli: prodding gently with
a clear rod, brushing gently with a paintbrush (1 cm width), covering
with a gloved human hand, and picking up with a gloved human hand.
We included prodding with the clear rod to provide a tactile cue with
minimal visual stimuli. We chose the paintbrush stimuli as it is similar to
a classic approach to motivate antipredator behavior in snakes (Brodie
III, 1993) and is a low- intensity stimulus. We used hand covering and
picking up with a human hand to have stimuli of different intensity
FIGURE 1 The ringneck snake
(Diadophis punctatus) at rest (a- b) and
exhibiting tail- coiling (c) and ventral
display (d) [Colour figure can be viewed at
wileyonlinelibrary.com]
(a) (b)
(c) (d)
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COX et al.
involving a human hand, with hand covering a lower intensity stimulus
than picking up. The same four individuals conducted all tac tile stimuli
experiments. We did not use a control group, because we were inter-
ested specifically in stimuli that would lead to a ventral display, and not
a general exploration of antipredator behavior. Prior to each trial, the
snake was placed in a behavioral arena with soil substrate (from nearby
forest) and a refuge in the form of a flat cover object (a flat tile). The
snake was allowed to acclimate in the behavioral arena for 30 min prior
to the trial. Because the snakes began each trial under the tile, the tile
was removed to reveal the snake. Following tile removal, the stimulus
was presented after a 5 s lapse. Each individual was presented with
tactile stimuli across three trials, separated by 10 min of rest . The order
of the stimuli for each individual was randomized to avoid bias created
by any order ef fect.
2.4 | Behavioral classification
We took behavioral notes for all snakes during the initial capture in the
field, during morphological processing, and for both set s of visual and
tactile stimuli trials. Snakes can exhibit a complex suite of responses
to threats or potential predators, which can include fleeing, threat s
(striking, threat displays), death feigning, startling or misdirection
(deimatic behavior), odorous attack deterrents (musking and defeca-
tion), and aggressive defenses (biting and constric ting). We classified
behaviors as no response, fleeing, lip curling (observed during process-
ing and field collection only), tail- coiling, ventral display, musking and
defecation, and biting. Behavior was classified as fleeing whenever
the snake moved away from the stimulus. We note that this fleeing
behavior was not possible to obser ve in the field or during data pro-
cessing as most individuals were not given the opportunity to flee. Lip
curling was noted as the lateral or bilateral lifting of the labium. Tail-
coiling was noted when the snakes raised their t ails and exposed the
caudoventral surface (Ernst & Ernst, 2003). The ventral display was
noted as the writhing behavior that exposed the ventral surface of the
body (Ernst & Ernst, 2003). Musking and defecation were noted when
the snake released musk or defecated, as this species will musk and
writhe, smearing musk, and feces (Ernst & Ernst, 2003). Constriction
behavior was noted when the snake wrapped tightly around the stimu-
lus source. Finally, biting was noted when the snake gaped, struck at,
or bit the stimulus sources. The presence of each behavior was scored
during the trial, and multiple behaviors could be observed in each trial.
2.5 | Statistical analyses
Because collecting animals and subjecting them to data processing
has the potential to alter behavior in subsequent experimental trials,
we analyzed behaviors exhibited during the first contact of individu-
als with a potential predator (humans) during the initial capture. We
also documented behaviors expressed during processing, which en-
tailed prolonged handling that could potentially instigate a behavio-
ral response. We compared the presence or absence of all behaviors
exhibited during field collection and processing to sex (n = 3 males
and 22 females), gravid state (n = 16 gravid females and 6 non- gravid
females), and ecdysis state (n = 5 in ecdysis and 20 not in ecdysis)
using contingency analyses and determined statistical significance
with Fisher's exact test. We compared the presence or absence of
behaviors exhibited during field collection and processing to body
temperature at time of collection, body length (SVL), and body mass
using nominal logistic regression.
For the experimental trials, we examined both visual and tac tile
stimuli. Beyond an initial foray, visual stimuli data were not statisti-
cally analyzed because none of the snakes exhibited a focal behavior
(tail- coiling or ventral display). For the tactile stimuli trials, we ana-
lyzed all behaviors that were collected. We first used a mixed- model
analysis to compare the presence of each behavior in separate sta-
tistical models (i.e., each model had a single behavior as the response
variable) for each tactile stimulus to sex, gravid state, ecdysis state,
body temperature, body length, and body mass, with individual as a
random factor and all other factors fixed (12 total models).
We also analyzed whether the presence of a behavior differs
among types of stimuli and whether behaviors are associated using
three dif ferent approaches. First, we analyzed whether the snake
exhibited the behavior during the first trial, ignoring subsequent tri-
als. We chose this approach as this would represent behavior prior
to any capacity of acclimation to the stimulus. Second, we scored
the presence of the behavior across any of the three trials, where
the behavior was marked as present if it was exhibited in any of the
three trials. We chose this approach as the least sensitive to stochas-
tic error in low- frequency behaviors. For both the first and second
approaches, we then used non- parametric Wilcoxon signed- rank
test to compare frequencies of behaviors in response to different
stimuli, because of the repeated- measures nature of our behavioral
trials and non- normality of the data. We also used contingency anal-
yses and assessed significance with Fisher's exact test to test for
an association between behavior types. The Fisher's exact test was
used because it is most appropriate for contingency tables with low
sample sizes in some cells. Third, we summed the results across all
three trials by creating an ordinal variable that scored the number
of trials in which a snake exhibited a behavior (i.e., a value of three
if the snake exhibited the behavior in all three trials). We chose this
approach to estimate a propensity to display a particular behavior
across all three trials. We then used Spearman's rank correlation to
test for an association between the number of times that a trait was
exhibited across the three trials. All analyses were conducted in JMP
9.0 and significance assessed with an α = 0.05.
3 | RESULTS
3.1 | Field collection and processing
During field collection, only a single snake attempted to bite (4%),
while ever y snake deployed musking and defecation. Eighty percent
of snakes displayed tail- coiling, while approximately one quarter of all
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COX et al.
snakes (24%) initiated a ventral display. During processing, we found
that every snake released musk and defecated. Surprisingly, nearly
half (44%) of snakes attempted to bite, and all of these biting attempts
occurred while they were grasped behind the head and measured for
body length. This biting was often preceded (46% of the time) by a lip
curling display, and lip curling was significantly associated with biting
(Fisher's Exact Test, p =.0087). Tail- coiling (88%) and ventral displays
(28%) were also frequently used during processing. The ventral dis-
play was not significantly associated with tail- coiling in either the field
(Fisher's Exact Test, p =.2887) or the laboratory during processing
(Fisher's Exact Test, p =.5343). We found that none of the behavior
exhibited during field collection or processing was significantly asso-
ciated with sex, parturition status, ecdysis status, body temperature
at time of capture, or body size (SVL or body mass, Table 1).
3.2 | Visual Stimuli
The most common response of snakes to any visual stimuli (hand,
taxidermy raccoon, or taxidermy crow) was fleeing (40.1% of trials).
There were no snakes that deployed scent- based defenses (musk-
ing or defecation). Similarly, no snakes exhibited either tail- coiling or
ventral displays in response to visual stimuli. Because no focal be-
haviors were instigated by visual stimuli, we did not further analyze
the response to visual stimuli.
3.3 | Tactile stimuli
3.3.1 | Association between
behaviors and organismal traits
We found that there was no relationship between sex, par turition
status, ecdysis status, body temperature at time of capture, or body
size and behavior exhibited in any of the t actile stimuli trials, using
fully factorial mixed models with subject as a random factor (all
p's > .05), although these results should be interpreted with caution
given the low sample size for some comparisons (e.g., sex). While
sexes or other groups did not significantly differ in antipredator dis-
plays, it is worth noting that both sexes, including both gravid and
non- gravid females, and snakes both in shed and out of shed exhibit
the ventral display behavior.
3.3.2 | First trial
Snakes exhibited tail- coiling significantly more frequently
(Figure 2) in response to being picked up than the tactile stimuli
of the clear rod (Wilcoxon signed- rank test, p =.0 054), the brush
(Wilcoxon signed- rank test, p =.0111), or being covered by a hand
(Wilcoxon signed- rank test, p =.0026). Similarly, snakes exhibited
the ventral display significantly more frequently in response to
being picked up than the tactile stimuli of the clear rod (Wilcoxon
signed- rank test, p =.0084), the brush (Wilcoxon signed- rank test,
p =.0162), or being covered by a hand (Wilcoxon signed- rank test ,
p =.0012). Snakes most frequently responded to the tactile stimuli
of the clear rod by fleeing (88%), followed by the ventral display
and tail- coiling (4% each), with no snakes biting or deploying a
scent defense (musk and defecation). In response to the brush,
snakes most frequently fled (72%), followed by ventral displays
and tail- coiling (8% each), and no snakes attempted to bite or de-
ployed a scent defense (musk and defecation). In response to cov-
ering by a gloved hand, no snakes exhibited any focal behavior
(Figure 2). Finally, for the tactile trials where snakes were picked
up by a gloved hand, snakes frequently used tail- coiling (32%) and
ventral displays (36%) in response to being picked up but did not
deploy musking and defecation. Additionally, two snakes thrashed
and tried to escape vigorously.
TABLE 1 The statistical relationship between behaviors
exhibiting during collection and processing
Variable
Behavior
Biting
Tail-
coiling
Ventral
Display
Behavior during collection
Sex Test Statistic – – –
p1 1 .5539
Gravid Test Statistic – – –
p1.1348 .3341
Ecdysis Test Statistic – – –
p.2 1 1
Body Temp Test Statistic . 61 1.73 1.56
p.4 351 .1881 .2109
SVL Test Statistic .02 1.34 2.19
p.8753 . 2462 .1391
Body Mass Test Statistic .12 1.08 1.26
p.7315 .2981 . 2621
Behavior during processing
Sex Test Statistic – – –
p1.3304 1
Gravid Test Statistic – – –
p1 1 .3341
Ecdysis Test Statistic – – –
p.6232 .5043 1
Body Temp Test Statistic .22 .01 1.82
p.6394 .9043 .1767
SVL Test Statistic 0.14 0
p.9533 .7098 .9461
Body Mass Test Statistic .2 1.22 .07
p.6543 . 2702 .7917
Note: Where the tes t statistic is absent (indicated with – ), we used
contingency tables and assessed signific ance with Fisher's exact test.
Test statistic is the W s tatistic from the Wilcoxon sign- rank test.
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COX et al.
3.3.3 | Presence of behavior across all trials
Across all three trials, snakes exhibited tail- coiling in at least one trial
(Figure 2) significantly more frequently in response to being picked
up than the tactile stimuli of the clear rod (Wilcoxon signed- rank test,
p =.0049), the brush (Wilcoxon signed- rank test, p <.0001), or being
covered by a hand (Wilcoxon signed- rank test, p <.0 001). Snakes also
exhibited ventral displays in at least one trial significantly more fre-
quently in response to being picked up than the tactile stimuli of the
clear rod ( Wilcoxon signed- rank test, p =.0093), the brush (Wilcoxon
signed- rank test, p =.0009), or being covered by a hand (Wilcoxon
signed- rank test, p <.0001). Snakes most frequently responded
to the tac tile stimuli of the clear rod by fleeing in at least one trial
(100%), followed by the tail- coiling and ventral displays (24% and 32%,
respec tively), with no sna kes biting or deployi ng a scent defense (musk
and defecation). In response to the brush, snakes most frequently fled
in at least one trial (96%), followed by ventral displays and t ail- coiling
(12% and 28%, respectively), and no snakes attempted to bite or de-
ployed a scent defense (musk and defecation). In response to cover-
ing by a gloved hand, a single snake attempted to flee in at least one
trial (4%), and one snake coiled their tail in at least one trial (4%), but
no other behaviors were observed. Finally, for the tactile trials where
snakes were picked up by a gloved hand, 28% of snakes thrashed and
tried vigorously to escape. However, snakes frequently used tail-
coiling (64%) and ventral displays (72%) in response to being picked
up in at least one trial but did not deploy musking and defecation.
3.3.4 | Behavior and number of trials
Snakes fled from the clear rod (mean number of trials ± SEM,
2.68 ± 0.11) and the brush (2.60 ± 0.11) in most trials (Figure 2), but
rarely f led in response to t he cover stimuli (0. 04 ± 0.04). Sna kes rarely
exhibited tail- coiling or ventral displays during trials in response to
the clear rod (tail- coiling, 0.32 ± 0.11; ventral display, 0.36 ± 0.11),
brush (tail- coiling, 0.16 ± 0.10; ventral display, 0.32 ± 0.11), or cover
stimuli (tail- coiling, 0.04 ± 0.04; ventral display, 0.0 ± 0.0). However,
the pickup stimuli instigated tail- coiling (1.28 ± 0.23) and ventr al dis-
plays (1.48 ± 0.23) in significantly more trials than the other stimuli
(Wilcoxon signed- rank tests, all p's < .01).
3.4 | Behavioral correlations
Tail- coiling and ventral displays were not significantly correlated
during collection or processing (all p's > .07). However, it is worth
noting that all snakes that exhibited ventral displays during either
collection or processing also exhibited tail- coiling (Figure 2). During
the pickup stimuli (the only stimuli that substantially induced tail-
coiling or ventral displays), we did find that tail- coiling and ventral
displays were significantly correlated (p =.0053). No other behavio-
ral traits were significantly correlated during collection, processing,
or the pickup stimuli trials.
4 | DISCUSSION
Bright ventral coloration in snakes has frequently been proposed
to be startle coloration and has been associated with deimatic tail-
coiling and ventral displays (Ernst & Ernst, 2003; Greene, 1997). Our
work shows that a snake species with bright ventral coloration uses
this behavior in response to tac tile cues from a potential predator,
and only in response to relatively strong stimuli (i.e., handling). This
experimental evidence that bright ventral coloration could be linked
to antipredator behavior suggests that the correlated evolution of
color and behavior might be impor tant for understanding the dy-
namics of antipredator coloration.
FIGURE 2 Behavior exhibited in response to tactile stimuli
for the first trial (a), presence of behavior in any of the three
trials (b), or number of trials with the behavior. Symbols indicate
mean ± SEM. While snakes frequently fled in response to some
tactile stimuli (clear rod, brush), only the pickup stimuli could induce
ventral displays or tail- coiling
0
25
50
75
100
Behavior (%)
Flee
Tail-Coiling
Ventral Display
Clear RodBrush Pick up
First Trial
Cover
0
25
50
75
100
Behavior (%)
Clear RodBrush Pick upCover
All trials (presence)
0
1
2
3
Stimulus
Behavior (# trials)
Clear RodBrush Pick upCover
All trials (#)
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COX et al.
Deimatic coloration and behavior is widespread in the animal
kingdom (Umbers et al., 2015, 2017) as a response to predators and
even competitors (Langridge, 2009b; Umbers et al., 2015, 2017).
Our research experimentally demonstrates that tactile cues can
cause snakes to reveal concealed coloration. Similar to previous
work in other species, we found that tail- coiling and ventral displays
were only instigated by substantial physical contact (Lenzi- Mattos
et al., 2005; Williams et al., 2000), which would likely represent
later or final stages of predation (Badiane et al., 2018). Specifically,
we found that snakes only deployed tail- coiling or ventral displays
under the most intensive of tactile cues, which involved capturing
and handling snakes in the field and in the laboratory. Most tactile
cues did not initiate any ventral displays or tail- coiling, and no visual
stimuli elicited any behavior beyond fleeing. However, it is wor th
noting that the limited repertoire of visual stimuli and use of a single
model for visual stimuli constrains the generality of these findings
(Kroodsma et al., 20 01). Future research could incorporate more
visual stimuli and individual variation within stimuli to reach more
general conclusions about visual stimuli and antipredator behavior
in these snakes. Our interpretation is that capturing and handling
snakes simulates predation and is able to elicit a behavioral display
that would have been used during an actual predation event. Visual
stimuli might be less likely than intensive tactile stimuli to induce
a deimatic display because of limited visual acuity in this species,
or to avoid revealing bright coloration and drawing attention to an
otherwise cryptic animal. We also found that these displays were de-
ployed in bot h sexes and regardle ss of body size or parturition s tatus,
which implies that displays could have fitness benefits that are not
specific to a single sex or life stage. Many species that exhibit dei-
matic colors and displays are dangerous or unpalatable, suggesting
a role for aposematism in deimatic displays (Kang et al., 2016; Lenzi-
Mattos et al., 2005; Umbers et al., 2017; Umbers & Mappes, 2015).
While ringneck snakes are not unpalatable (i.e., consumed by multi-
ple predators; Ernst & Ernst, 2003), they possess rear fangs and are
venomous (Hill & Mackessy, 2000; O’Donnell et al., 2007), although
it remains unknown if this venom is deployed defensively. However,
while our research has demonstrated that ringneck snakes will use
a deimatic display in response to predation, the impact of ventral
displays on behavior of ac tual predators is unknown.
The traditional interpretation of the function of deimatic color-
ation and displays is that they either serve as concealable warnings
of toxicity or unpalatability, or that they startle or confuse the pred-
ator, allowing the prey to escape (Umbers et al., 2017). Both of these
interpretations rely on the potential prey modifying predator behav-
ior to facilitate survival. However, predator responses to deimatic
displays have only rarely been assessed (Holmes et al., 2018; Kang
et al., 2016; Kim et al., 2020; O’Hanlon et al., 2018), probably for a
variety of logistical reasons (e.g., selection of appropriate predator,
accurately assessing predator response and cognition). In general,
research on predator cognition has lagged behind research on prey
species that exhibit antipredator traits (e.g., mimicry, decoy color-
ation). Hence, future research should determine predator response
to ventral displays and tail- coiling in snakes.
While we have discussed bright ventral coloration and behavioral
displays in s nakes in the context of un defended deimat ism, it is worth
noting that concealed coloration and behavioral displays might serve
other functions. First, bright or contrasting ventral coloration could
be both an aposematic and deimatic signal (i.e., defended deimatism,
Umbers & Mappes, 2016), warning of a dangerous or unpalatable
prey. For example, coral snakes of the western hemisphere often
employ tail- coiling when disturbed, and these brightly banded t ails
may warn of their deadly venom (Greene, 1973, 1997). Defended
deimatism is probably most likely when the snake is highly venomous
(e.g., defensive gaping and venom in cottonmouths, Agkistrodon pi-
scivorous, Gibbons & Dorcas, 2002; Glaudas & Winne, 2007) or toxic
(e.g., toxic nuchal glands and bright nuchal coloration in Rhabdophis
tigrinus, Hutchinson et al., 2007; Mori & Burghardt, 2001), while
undefended deimatism would be common in snakes without robust
defenses. Second, some have suggested that tail- coiling could be a
decoy trait, whereby predatory attacks are focused on a less vital
region of the body (Greene, 1973; McCallum, 2006). Importantly, in
a complex, multicausal world, antipredator traits could vary in their
function (e.g., deimatic vs. aposematic) based upon the contex t of
the predatory attack (e.g., location, time, predator). Regardless, our
work strongly supports that ventral displays and tail- coiling are ini-
tiated in response to intensive predatory at tacks to expose bright
ventral body and tail coloration.
While the focus of our research was on deimatic behavior, we
also documented that ringneck snakes will also bite (although this
was rare), flee, and both musk and defecate in response to capture,
handling, and other stimuli. Fleeing in response to predators is the
most direct way to avoid predation. However, during the initial cap-
ture and handling, snakes also exhibited musking and defecation.
Musking and defecation is a widespread behavior in snakes, and
probably renders the snakes unpalatable to potential predators
(Delaney, 2019; Gangloff et al., 2014; Mar tins, 1996). We found that
snakes only used this antipredator behavior during the first contact
of capturing and handling during processing, but did not musk or def-
ecate during visual or tactile stimuli experiments. This finding might
suggest that individual snakes are limited in their ability to mount
this defense repeatedly in response to frequent predation attempts.
One unexpected outcome of this study was that the ringneck
snake, which is a species that is frequently noted for its docile de-
meanor (Ernst & Ernst , 20 03; Krysko et al., 2019), can be reliably
induced to bite. This behavior was only stimulated by grasping the
snake behind the head, as was done when measuring the body
length of the snake. This raises the intriguing possibility that this
is an antipredator trait for a very specific type of predator y attack.
Snakes are important predators of other snake species because
the shape of snakes and other elongate organisms provides max-
imal energy while minimizing costs to locomotion from a bulky
food item (Cundall & Greene, 2000). However, snakes are unlikely
to be the primary target of a deimatic display because of dimin-
ished visual acuity and nocturnal habits of most species (Sillman
et al., 1999; Walls, 1942). Ophiophagous snakes often initiate
feeding on snakes by grasping their ophidian prey behind the head,
472
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COX et al.
and ringneck snakes can thwart the predatory at tack by biting
their snake predator on the head or mouth (Rossi & Rossi, 1994).
Crucially, our study documents this biting behavior in response to
a specific tactile stimulus to a single body region that can be tar-
geted by predators.
Color is one of the primary axes of phenotypic diversity in
snakes because of their simplified body form. Previous research
has found that predator- based selection is impor tant for the evolu-
tionary diversity of color in snakes (Brodie III, 1992; Davis Rabosky
et al., 2016; Jackson et al., 1976). Our research highlights that dei-
matic coloration is yet another color trait whose evolution could
be driven by predator- based selection. In addition, we found that
a species with concealed coloration also possessed deimatic dis-
plays, and that two deimatic displays (tail- coiling and ventral dis-
plays) were correlated. These linkages between color and multiple
behavioral trait s suggest that all deimatic traits could be parts of
co- adapted character complexes (Brodie III, 1992; Cheverud, 1996;
Lande, 1984; Vidal- García et al., 2020). Future research should (a)
assess the determinants of deimatic behaviors in other snake spe-
cies with concealed coloration, (b) document behaviors correlated
with other types of antipredator coloration in poorly studied groups
(Creer, 2005; Davis Rabosky et al., 2021; Moore et al., 2020), and
(c) determine the comparative pattern of bright ventral coloration
across the snake tree of life. The goal of this research would be to
reveal the evolutionary forces underlying the evolution of color di-
versity in snakes.
ACKNOWLEDGEMENTS
We thank Edmund D. Brodie III, Eric Nag y, and Jaime B. Jones for
logistical help during the commission of this study. We also thank
Mountain Lake Biological Station for supporting this research
through their educational programs.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
AUTHOR CONTRIBUTIONS
All authors designed the study. H.I., M.D., M.W., C.L.C and A.K.C.
conducted the field collection and animal processing. I.V.R., N. M.,
O. L., and A. D. Y. conducted visual stimuli assays. M.G., C.L., and
C.B. conducted tactile stimuli assays. C .L.C ., A.K.C., and A.R.D.R .
processed and analyzed data. All authors contributed text to the
first draft of the manuscript, and C.L.C produced the first draft of
the manuscript. All authors contributed to revising and editing the
manuscript.
ETHICAL STATEMENT
This research was completed under IACUC protocol 3927– 0415 to
Edmund D Brodie III (Director of Mountain Lake Biological Station).
DATA AVAIL ABI LIT Y S TATEM ENT
Data are available via FigShare (10.6084/m9.figshare.14210972).
ORCID
Christian L. Cox https://orcid.org/0000-0002-9424-8482
Alison R. Davis Rabosky https://orcid.
org/0000-0002-4664-8246
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