Social Behavior of Rattlesnakes: A Shifting Paradigm
Gordon W. Schuett1, 2, 3, Rulon W. Clark4, Roger A. Repp3, 5, Melissa Amarello2, 6, Charles F. Smith 2,3,7, and Harry W. Greene8
1 Department of Biology and Neuroscience Institute
Georgia State University
Atlanta, Georgia 30303, USA.
2 e Copperhead Institute
Spartanburg, South Carolina 29304, USA.
3 Chiricahua Desert Museum
Rodeo, New Mexico 88056, USA.
4 Department of Biology
San Diego State University
San Diego, California 92182, USA.
5 National Optical Astronomy Observatory
Tucson, Arizona 85719, USA.
6 Advocates for Snake Preservation
Tucson, Arizona 85717, USA.
7 Department of Biology
Spartanburg, South Carolina 29303, USA.
8Department of Ecology and Evolutionary Biology
Ithaca, New York 14853, USA.
New eras don’t come about because of swords,
they’re created by the people who wield them.
Gordon W. Schuett
Breaking conceptual barriers that concern the complexity and importance of social behavior in snakes has been a lin-
gering and uneasy progression for ethologists, herpetologists, and other scientists who study their biology. Certainly,
in popular western culture, these biases remain largely unchanged (Burghardt et al., 2009; Doody et al., 2013), but
even broadly trained scientists are often ignorant of basic information about snakes, such as their social behavior
(Greene, 1997, 2013; Lillywhite, 2014). Activities related to sex, such as male combat, courtship, and mating, are
clearly social (Gillingham, 1987). But, snakes aggregate and interact with each other for reasons other than procre-
ation (Rivas and Burghardt, 2001, 2002).
Klauber (1956, 1972) was rst to describe and popularize the massive winter denning aggregations of Prairie Rat-
tlesnakes (Crotalus viridis) in South Dakota and elsewhere in the western United States. In parts of their respective
ranges, the Timber Rattlesnake (C. horridus) and Western Diamond-backed Rattlesnake (C. atrox) also aggregate in
dens during winter (Sexton et al., 1992; Repp, 1998; Clark et al., 2012). Yet, however intriguing, embarrassingly few
studies have been published concerning individual-based social interactions at these communal dens (Repp, 1998;
Amarello, 2012; Clark et al., 2012). Most of what we know of this phenomenon does not concern the snakes, but
rather the environmental conditions (temperatures) and geologic features (Sexton et al., 1992; Hamilton and Nowak,
2009; Gienger and Beck, 2011) of the dens themselves. ere are only sparse long-term data on ingress, egress, and
social activities of individual snakes at communal dens. In general, detailed, long-term studies of social interactions
of individual snakes in nature are rare (Sexton et al., 1992; Amarello, 2012; Clark et al., 2012, 2014).
Here, we discuss sociality in snakes, highlighting rattlesnakes from temperate regions and their proclivity to aggre-
gate at dens. We suggest that communal denning oers unique opportunities to study social behavior. Accordingly,
we propose new research programmes with the intent to shift unproductive perspectives and dogma so that we can
look at and investigate snakes dierently and creatively. As others have suggested, we will not move forward until
we put ourselves in the shoes of the subjects we are investigating (Rivas and Burghardt, 2001, 2002). Ultimately, we
must scientically challenge wide held beliefs, stereotypes, prejudices, and biases that snakes are little more than
mere automatons slithering in the wilderness. We begin with these basic yet important observations: all snakes com-
municate, are social, and have culture (Doody et al., 2013). Interactions, however, vary greatly with respect to context
and frequency. Furthermore, there are clear dierences among species and individuals. We accept a priori that snakes
have personalities. We will discuss how the social lives of rattlesnakes are often complex.
You know, I don’t think snakes are going to be doing this.
-Temple Grandin, quoted in the Nature® documentary,
Animal Odd Couples (2012)
Temple Grandin, in the above quote, casts doubt whether snakes
are social. Given that professor Grandin has made a profession-
al career by highlighting the behavioral complexity of animals,
and she openly speaks about our profound underestimation of
their mental experiences, we nd it peculiar and disheartening
that she questions whether snakes are social animals. As we will
discuss throughout this chapter, this perception and limitation
is not at all isolated. It is, unfortunately, the prevailing view of
snakes among laypersons and even professional biologists (Rivas
and Burghardt, 2001, 2002; Doody et al., 2013).
Here, our goal is to review and challenge prevailing dogma
regarding sociality in snakes. At the outset, we admit to biases be-
cause we do not doubt that snakes have complex communicative
systems and complex social lives (Greene et al., 2002; Amarello,
2012; Clark et al., 2012, 2014; Lillywhite, 2014). We will discuss
sociality with emphasis on rattlesnakes because all of us have had
personal experience with this group both in the laboratory and
in the wild.
To many, snakes are an alien
In the snake, all the organs are sheathed; no hands, no feet,
no ns, no wings. In bird and beast, the organs are released,
and begin to play.
-Ralph Waldo Emerson (1870)
Why have snakes been held in such low regard in most western
cultures? Beyond the strife created by the biblical myth of Adam
and Eve, we suggest that the answer is simple: snakes bear little
resemblance to us or the animals that we enjoy and with whom
we share relationships, such as dogs, horses, cats and birds (Mur-
ray and Foote, 1979; Shine, 1991; Greene, 1997; Burghardt et
al., 2009; Doody et al., 2013; Lillywhite, 2014). Most notably,
all extant snakes (> 3000 species) lack external limbs (or at least
of signicant size) and their associated structures (Shine, 1991;
Greene, 1997; Lillywhite, 2014). With no hands to wave or feet
to stomp – even the ns of shes are often used to put on beauti-
ful and elaborate displays (Dugatkin, 2009) – snakes appear un-
able at rst glance to be able to express social behaviors which
are common to humans and other vertebrates (Wittenberger,
1981; Alcock, 1998; Dugatkin, 2009). We will rst discuss the
morphological and behavioral attributes that appear to limit the
ability of snakes to be social, followed by what snakes do in com-
pensation, so to speak, to exhibit their own brand of sociality.
To understand them, we must step inside their shoes (Rivas and
Burghardt, 2001, 2002; Burghardt, 2005).
Despite how variable they are in appearance, snakes are es-
sentially a specialized tube with openings at both ends. With few
exceptions, such as in cobras (hoods), vipers (head ornaments,
tail ornaments), and rattlesnakes (rattle), snakes rarely possess
permanent body structures we would term ornaments or weap-
ons (Figure 1); to the best of our knowledge, none are used in
social displays. Interestingly, among extant snakes, these struc-
tures are prominent only among viperids, all which of course are
venomous. Sexually dimorphic ornaments seasonally regulated
by steroid hormones, such as antlers in male ungulates, are all but
absent in snakes (Emlen, 2014; Lillywhite, 2014).
Figure 1. Head and tail structures of Old- and New World viperid snakes. a) Eye horns of the Saharan Horned Viper (Cerastes cerastes). b) Snout horns of
the Rhinoceros Viper (Bitis nasicornis). c) Rattle of the Rock Rattlesnake (Crotalus lepidus). d) Head and tail ornaments of the Iranian Spider-tailed Viper
(Pseudocerastes urarachnoides). Photos (a-b) by William Love. Photo (c) by George Grall. Photo (d) by Frank Deschandol.
Figure 1. Head and tail structures of Old- and New World viperid snakes. a) Eye horns of the Saharan Horned Viper (
Figure 1. Head and tail structures of Old- and New World viperid snakes. a) Eye horns of the Saharan Horned Viper (
Without exception, all snakes lack moveable eyelids, giving
them the ill-deserved reputation of not being able to sleep, or that
they are capable of staring down (“hypnotizing”) their enemies
or prey to submission (Shine, 1991; Greene, 1997; Lillywhite,
2014). Perhaps just as obvious is that all snakes lack external
ears and ear openings. is has led to the long-held and erro-
neous belief that snakes cannot hear (Wever and Vernon, 1960;
Lillywhite, 2014). Quite to the contrary, snakes tested thus far,
including rattlesnakes, are quite capable of detecting (hearing)
air-borne sounds of certain frequencies (Young and Aguiar, 2002;
Friedel et al., 2008; Christensen et al., 2012).
Unlike most mammals, snakes and other reptiles are incapable
of, or have limited abilities to, exhibit facial expressions. To pri-
mates, which rely signicantly on facial expressions as a primary
source of social information, social “moods” or “emotions” seem
remarkably xed or unchanging in snakes. e expression of de-
fense (fear or anger) is mostly unlike that of other vertebrates,
especially when compared to mammals. Acts such as tail vibra-
tion and body attening are examples used by snakes. Use of the
“lips” and nostrils for expressing emotions is limited (but see de
Queiroz, 1997), but mouth displays are not uncommon. North
American relatives of rattlesnakes, the Cottonmouths (Agkistro-
don piscivorus, A. conanti), are perhaps best known for their am-
boyant open-mouth display (Figure 2) when startled or behaving
defensively (Greene, 1988, 1997; Glaudas and Winne, 2007). In
many species, including rattlesnakes, the mouth is held shut, but
the tongue is overtly protracted and displayed, waving slowly up
and down and sometimes even touching the anterior head scales
Complex vocalizations are absent in snakes, and the primary
sounds produced in the head region (oral and nasal cavities) are
hissing and related sounds (Lillywhite, 2014). Large-bodied rat-
tlesnakes, such as C. atrox, are capable of audible hissing, with the
mouth held slightly open (Kinney et al., 1998). Certain viperids,
such as saw-scaled vipers (Echis spp.), produce rasping and hiss-
ing-like sounds by rubbing their lateral body scales when alarmed
(Greene, 1988, 1997; Lillywhite, 2014). Multiple lineages of
snakes can vibrate their tails on the ground and against objects to
produce sound. Of course, rattlesnakes have a remarkable organ
Figure 2. A young adult Western Cottonmouth (Agkistrodon pi-
scivorus) in a full, open mouth defensive display. Cottonmouths are
North American viperids and close relatives of rattlesnakes. Photo by
Shannon K. Hoss.
that when shaken produces a highly distinctive sound (Klauber,
1956, 1972; Moon et al., 2003). e mouth and tongue, the neck
region (hooding, glandular secretions), tail, and cloaca (popping
sounds, musking, voiding wastes), are common anatomical struc-
tures used by snakes to convey anti-predator and social informa-
tion (Carpenter, 1977; Carpenter and Ferguson, 1977; Greene,
1988, 1997; Shine, 1991; Lillywhite, 2014).
Finally, because they are ectotherms, snakes exhibit slow move-
ments when exposed to chronic cold conditions, which tends to
exaggerate the alien-like characteristics we have already discussed
(Brattstrom, 1974; Doody et al., 2013). Many early experimen-
tal studies of snakes and other reptiles were awed, for example,
owing to inappropriate environmental conditions, primarily in-
correct (suboptimal) temperatures (Brattstrom, 1974). Today,
researchers are more knowledgeable and far better equipped to
simulate environmental variables, such as temperature, relative
humidity, substrate, hide-spots (refugia), diet, and social needs in
their studies (Murphy and Collins, 1980; Warwick et al., 1995).
A modern (and dierent)
view of snakes
Research by Stephen Secor and colleagues (Secor and Diamond,
1998; Costello et al., 2010), Todd Castoe’s laboratory (Castoe et
al., 2008; Castoe, 2014; Shield et al., this volume, Genomics),
Bud Lindstedt (Rome and Linstedt, 1998), Stephen Mackessy
(Mackessy, 2008), Johnnie Andersen and his team (Andersen et
al., 2005), and others drives home an important message: our
understanding of the behavior and physiology of snakes is still in
its infancy. In their studies, these authors demonstrate that snakes
(e.g., pythons and rattlesnakes) exhibit uniquely extreme capabil-
ities in digestion, which includes radical changes in anatomy and
physiology (Castoe, 2014; Lillywhite, 2014; see Shield et al., this
volume, Genomics). For instance, Secor and Diamond (1998)
showed in juvenile Burmese Pythons (Python bivittatus) that after
prey (rat) consumption the small intestine doubles in wet and
dry mass within 1 day, largely as a result of a six-fold increase in
Figure 3. A young adult Prairie Rattlesnake (Crotalus viridis) waving its
tongue with tongue tips (tines) touching its head. is behavior occurs
under multiple contexts including defensive ones. Male C. viridis most
likely have longer tines than females (Smith et al., 2008). Photo by
Martin J. Feldner.
microvillus length and a doubling of mucosal enterocyte volume.
Within 1–3 days, there are up to two-fold increases in the mass
of the stomach, liver, pancreas, heart, lungs, and kidneys. Once
a snake subjugates and consumes a large meal (e.g., rat, rabbit, or
pig), it must increase its oxygen consumption by many fold to meet
high metabolic demands. Such demands create stress on the heart
and other components of the cardiovascular system. Andersen et al.
(2005) showed that only 48 h after feeding, there is an extraordi-
narily rapid increase (40% gain) in ventricular muscle mass in the
Burmese Python. is increase is the result of gene expression of
muscle-contractile proteins. Because this ventricular hypertrophy
occurs naturally and is fully reversible, it could provide a useful
model for investigating the mechanisms that lead to cardiac growth
and development in humans and other animals (Andersen et al.,
Rattlesnakes have specialized tailshaker muscles capable of
sustained, high-frequency contractions, similar to cardiac muscle
(Savitzky and Moon, 2008). e Western Diamond-backed Rat-
tlesnake (C. atrox), for example, can rattle continuously for hours
at a time at frequencies that approach 90 Hz, which demonstrates
an aerobic capacity uncommon among the reptiles and rare among
all other vertebrates (Schaeer et al., 1996; Rome and Linstedt,
1998; Moon et al., 2003; Savitzky and Moon, 2008). As Schaef-
fer and colleagues (1996, p. 351) state, “Extremes of performance
often provide insights into physiological mechanisms unlikely to
surface in organisms of ‘average’ performance (Schmidt-Nielsen,
1967; Yates, 1979). Without question, the tailshaker muscles of
the rattlesnake exemplify an extreme of skeletal muscle function.”
Accordingly, because it is extreme, this muscle group is an ideal
model system to investigate specic properties common to all skel-
etal muscle of vertebrates (e.g., excitation–contraction coupling,
mechanisms which link ATP to its demand).
e skeletons of snakes lack forelimbs, shoulder girdles, and
sternal elements, thus vertebrae were assumed to have become less
regionalized when the limbs were lost. Recent work by Jason Head
and P. David Polly (2015) on Hox in snakes, lizards, and other
amniotes shows that snakes have many more vertebrae compared
to lizards, absence of key skeletal elements common to most tetra-
pods (shoulder girdles), and appear less regionalized, but they are
nevertheless highly regionalized. In fact, Hox gene expression per
region (e.g., cervical, thoracic, lumbar) is congruent in lizards and
snakes. e phylogenetic structure of primaxial (vertebrae, dorsal
ribs) morphology in reptiles does not support a loss of regionaliza-
tion in the evolution of snakes. e developmental origin of snakes
is perhaps best explained by decoupling of the primaxial and ab-
axial (limbs, sternum) domains and by increases in somite number,
not by changes in the function of primaxial Hox genes (Head and
Polly, 2015). ese authors conclude that “…the origin of snakes
was not associated with deregionalization of the primaxial domain,
but rather with loss of the abaxial skeleton and increases in verte-
bral numbers independent of primaxial Hox domain boundaries.”
Facultative parthenogenesis is the ability of sexually reproduc-
ing species to reproduce without a male (see Taylor and Booth,
this volume, Reproduction). Facultative parthenogenesis (FP) was
not known (conrmed) in snakes until 1997 (Dubach et al., 1997;
Schuett et al., 1997, 1998). Since these early publications, FP has
been identied in multiple lineages of snakes and in several spe-
cies of monitor lizards (genus Varanus), including the Komodo
Dragon (V. komodoensis). Recently, FP was documented in several
species of sharks (Chapman et al., 2007; Booth and Schuett, 2011;
see Taylor and Booth, this volume, Reproduction). Because FP in
snakes occurs in the wild (Booth et al., 2012), and because females
snakes (e.g., Boa constrictor) produced by way of FP have them-
selves successfully reproduced (Booth and Schuett, under review),
this extreme alternative reproductive tactic (Oliveira et al., 2008),
oers legitimate evolutionary problems (e.g., evo-devo, phenotypic
plasticity) for researchers to tackle; it can no longer be relegated to
being just a captive syndrome (Booth and Schuett, 2011, 2016;
Booth et al., 2014).
Advances that illustrate behavioral complexity of snakes also
have been slowly emerging. Until recently, for example, it was the
prevailing dogma that snakes were not territorial (Gillingham,
1987; Shine, 1991; Duvall et al., 1992). To be perfectly fair, ter-
ritoriality has been suspected to occur in certain snake species (e.g.,
fast-moving and aggressive taxa such as Mambas (Dendroaspis spp.)
and the Boomslang (Dispholidus typus), capable of defending a re-
source such as weaver bird nests, but it has not been documented.
Furthermore, the denition of territoriality has changed over the
years (reviewed in Wittenberger, 1981), and depending on the
denition one adopts, snakes either exhibit territoriality or they
do not. Coming from somewhat out of left eld, Wen-San Huang
and colleagues (2011) describe territorial behavior in the Taiwanese
Kukrisnake (Oligodon formosanus). Adult females of O. formosanus
defend sea turtle nests, often for weeks, and repel conspecics until
the eggs hatch or are consumed by the guarding snake. Members
of the genus Oligodon have massively enlarged teeth that are used
to slit turtle eggshells and in territorial defense of sea turtle eggs.
Again, many of us did not see this coming, but patient observation
in nature tends to pay o in science. Recently, Webb and colleagues
present sound evidence for territoriality in an Australian elapid, the
Small-eyed Snake, Cryptophis nigrescens (Webb et al., 2015). In the
wild, larger males of C. nigrescens were found under thermally im-
portant rocks with more or larger females. In staged contests, males
actively defended rocks from male competitors. Consequently,
larger males actively displaced their smaller rivals. From these re-
sults the authors suggested that the thermally driven concentration
of female C. nigrescens has rendered rock sites as economically de-
fensible, and thus has favored the evolution of territoriality in this
species of snake.
All of the abovementioned cases exemplify that research is both
changing and expanding our understanding of and appreciation
for the complexity of snakes. Moreover, many snakes clearly exhibit
behavioral, physiological, and developmental (evo-devo) peculiari-
ties that are extreme and thus suitable as general models to study
adaptation (Shield et al., this volume, Genomics). Even synthetic
approaches are possible (MacLennan and Burghardt, 1994). e
doors are opening wide to see snakes and other reptiles as dynamic
model organisms. Here, we will show that snakes, in particular
rattlesnakes, can have complex social lives (Greene, 1997, 2013;
Greene et al., 2002; Clark, 2004, 2007; Amarello, 2012; Clark
et al., 2012, 2014; Smith and Schuett, 2015). is acknowledg-
ment alone will have an impact on how we perceive these animals.
Importantly, we feel that a change of perception will help guide
us to develop new and exciting research programmes (Rivas and
Burghardt, 2001, 2002; Doody et al., 2013).
Why snakes are important
Obviously, reptiles are unlikely to teach us much about the
hormonal control of parental care.
-Moore and Lindzey (1992, p. 77)
Snakes, lizards, and amphisbaenians constitute the squamate
reptiles (Squamata), which number well over 7,000 extant species
(Reptile Database, http://reptiledatabase.org; accessed 5-24-2015).
Squamates are members of a larger and evolutionary important
group (clade) of tetrapods called amniotes, comprised of mammals
(Mammalia) and all reptiles (Reptilia), which includes birds (Aves).
e number of extant mammal species is over 4,200, and the num-
ber of bird species is possibly greater than 10,000 (Gill, 2006; Cle-
ments, 2007). If one of our goals in science is to develop a robust
synthesis of the evolution of social behavior in amniotes, neglect-
ing 7,000 species, or at least a large subset of those taxa, would
be reckless and unscientic (Brattstrom, 1974). Furthermore, we
must have in-depth knowledge of the groups we select to inves-
tigate. About 25-years-ago, in a review chapter, it was stated that
post-partum parental care of progeny in squamates is rare, and no
substantive studies were cited that concerned snakes (Shine, 1988;
Clutton-Brock, 1991). Just 14 years later, Greene and colleagues,
highlighting their long-term study on the Black-tailed Rattlesnake
(Crotalus molossus) in the Chiricahua Mountains of southeastern
Arizona, published their groundbreaking analysis on parental be-
havior in pitvipers (Greene et al., 2002). Subsequent research on
parental care in North American pitvipers illustrates it appears to
be ubiquitous and can be investigated from multiple perspectives
(Reiserer et al., 2008; Amarello et al., 2011; Hoss, 2013; see vol-
ume 1, Species Accounts). In contrast to the dim view about pa-
rental care and hormones in reptiles illustrated in the above quote,
Shannon Hoss and team have given us the rst study of maternal
care and steroid hormones in any snake, the Cottonmouth (Agkis-
trodon piscivorus), a viviparous pitviper of North America (Hoss,
2013; Hoss and Clark, 2014; Hoss et al., 2014, 2015) and close
relative to rattlesnakes. Unquestionably, parental care and many
other social behaviors in mammals and birds are often more com-
plex than in snakes (or so they seem), but that fact should not dis-
suade researchers from investigating simpler systems from which
complexity is presumed to be derived (Doody et al., 2013; Greene,
Communication and sociality
Somewhat remarkably, social behavior can start in the egg.
-Doody, Burghardt and Dinets (2013, p. 3)
Our introductory comments serve to illustrate that snakes ex-
hibit far more behavioral complexity and variation than is un-
derstood by the majority of laypersons and many professional
biologists. Nonetheless, most of the abovementioned examples
are anti-predator responses and, therefore, are not used in most
male-female, male-male, or female-female communication epi-
sodes (Carpenter, 1977; Carpenter and Ferguson, 1977; Greene,
1988, 1997; Shine, 1991; Lillywhite, 2014). With respect to sen-
sory modalities, most communication in snakes involves vision,
tactility (touch), vibration, and chemosensation, which includes
the vomeronasal senses (Halpern and Martinez-Marcos, 2003;
Filaramo and Schwenk, 2009; Lillywhite, 2014). Other sensory
modalities, such as hearing, appear to be of secondary importance
(Gillingham, 1987; Young and Aguiar, 2002; Young, 2003; Lil-
Carpenter (1977, p. 217) broadly dened communication as
the transfer of information from one individual to another. Lewis
and Gower (1980, p. 2) provide a similar denition of communi-
cation, and they emphasize that selection favors both the produc-
tion (sender) and reception of the signal by the receiver (Allaby,
2009). We emphasize receiver response or comprehension. A re-
sponse might occur immediately but also can be delayed (e.g.,
minutes, days, years). Accordingly, all animals communicate with
various sensory modalities and between members of their own
species and others (Lewis and Gower, 1980).
All sociality in snakes and other animals must involve com-
munication. Beyond what we can observe directly, snakes uti-
lize multiple sensory modalities in communication and social-
ity which include tactile, vibrational, and auditory information
(Young et al., 2002; Young, 2003; Friedel et al., 2008; Lillywhite,
2014, pp. 167–169), in addition to chemical information via
vomeronasal, olfactory, and taste (taste buds) systems (Halpern
and Martinez-Marcos, 2003; Mason and Parker, 2010; Lilly-
white, 2014, pp. 169–173). Finally, infrared (thermal) informa-
tion is processed in pitvipers and several other lineages of snakes
(Lillywhite, 2014, pp. 173–176). Sensory organs (free nerve end-
ings, mechanoreceptors) in the integument also can be involved
in communication and process social information (Lillywhite,
2014, pp. 177–179). Auditory (hearing) senses appear to be sec-
ondary (Gillingham, 1987; see Young and Aguiar, 2002; Friedel
et al., 2008; Christensen et al., 2012).
Mind games: breaking from
traditions and self-imposed
Language, mathematics, music, and art are powerful tools in
communication and conceptualization, and all are integral to the
condition of being human (Wilson, 1975, 2014; Grin, 1981).
Verbal and written languages are particularly important because
they are major conduits for our cultural evolution and heritage
(Boyd and Richerson, 1985).
Nonetheless, as the proverb goes, if we live by the sword, we
also shall die by it, and thus while verbal and written languages,
for instance, are hugely benecial, they also can be the very pit-
falls that interfere with scientic progress. We will use a graphic
and unpleasant example to illustrate this point. When the term
“rape” was rst introduced as a term in the study of non-human
animals (Brownmiller, 1975), perhaps as a shorthand for “forced
copulation” or “sexual coercion,” it drew heavy criticism from
academics as being unscientic (Palmer, 1989; Mitchell et al.,
1997; ornhill and Palmer, 2000). Many other terms were (and
continue to be) avoided in animal behavior owing to their con-
nections or connotations of being anthropomorphic (Grin,
1981, 2001; Rivas and Burghardt, 2001, 2002; Beko, 2007),
which is essentially saying they are not testable or scientic
(Burghardt, 1997; see Wynne, 2007). Early on, ethologists and
others studying behavior came to regard anthropomorphism as
a serious error that must be avoided at all costs in scientic dis-
cussion and research (Rivas and Burghardt, 2001, 2002). at
perception spread to all levels of the study of animal behavior and
became engrained in our psyche for decades. In fact, as a response
to anthropomorphism, and perhaps to our detriment, the study
of animal behavior became overly mechanistic (proximate), with
excessive emphasis on responses to stimuli and descriptions of
behavioral acts (e.g., xed action patterns; modal action patterns;
state-transition analysis). is perspective placed prominence on
an individual’s movements, but not motivation or intentions;
hindsight indicates we were transforming our reptilian subjects
James Gillingham provided the rst modern and comprehen-
sive review of social behavior of snakes, concentrating on various
aspects of mating behavior, male ghting, and aggregation, with
emphasis on describing of patterns of individual acts using ow
diagrams (Gillingham, 1987). Despite its scholarly appeal, one
can see that his work shows few of the terms we have presented
in the Glossary. Terms like personality, kin-association, family,
bystander, eavesdropping, cheating, public information, and sen-
tinel were absent. Post-partum maternal care by rattlesnakes was
briey mentioned, but knowledge and documentation on this
topic was in its infancy (Greene et al., 2002). As a result, the sub-
ject matter of his review was not controversial. Why? e plain
and simple answer must include the biases, prejudices, and ste-
reotypes of that time. Let us imagine that Gillingham produced
a chapter with the abovementioned terms and others in our glos-
sary. We believe he would have been laughed out of the park, as
the saying goes, along with his reputation as a sane biologist. It
was not the acceptable lexicon for describing behavior and social-
ity of snakes and other reptiles in the late 1980s. Unbelievably,
with few exceptions, many biologists today convey the social lives
of snakes in their own published research with the same wide held
beliefs, stereotypes, and personal biases.
Are we stuck? If we are, then why is that the case? Essentially,
snakes are still largely relegated as mere automatons slithering in
the wilderness. Select an article about snake behavior in a high-
ranking, peer-reviewed journal. Bets are on it will likely be a fairly
sti read. But talk to the authors of these papers at a conference
about their subjects and a truth or reality emerges that is quite
dierent from the printed pages. In most cases, colorful, inter-
esting, and striking stories are told about individual snakes and
groups. How “Winston” hunts dierently from “George” or CA-
55 (“Double-Nickel”) has a unique and large home range, or that
Aggregation: groups of two or more organisms that are conspe-
cics (e.g., herds, schools, and ocks).
Aggression: an overt interaction with one or more other indi-
viduals that often results in inicted damage.
Altruism: behavior by an individual (actor) that increases the
tness of a dierent individual (recipient) that may decrease the
evolutionary tness of the actor.
Anthropomorphism: attributing human properties to nonhu-
man (organic or inorganic) entities.
Audience eect: the impact that a passive audience has on an
Behavioral syndromes: suites of correlated behaviors across
situations. An example is an aggression syndrome where some
individuals are more aggressive, whereas others are less aggressive
across a range of situations and contexts.
Boldness: the tendency of an individual to take risks and to
explore novel contexts (shy-bold continuum).
Brood parasitism: a category of kleptoparasitism that involves
the manipulation and use of host individuals either of the same
or dierent species to raise the young of the brood-parasite.
Bystander: individual within range to detect interactions or sig-
naling of other conspecics.
Cheating: to receive a benet at the cost of other organisms. A
cheater is an individual who does not cooperate (or cooperates
less than their fair share) but can potentially gain the benet
from others cooperating (Dugatkin, 1999).
Clan: a group of conspecics united by actual (or perceived)
kinship and descent.
Cognitive ethology: a branch of ethology concerned with the
inuence of conscious awareness and intention on the behavior
of an animal.
Cooperative breeding: a social system characterized by selective
breeding with allomaternal behavior and where helpers provide
care for ospring produced by breeding group members.
Copying: mimicking behavior of local conspecics.
Crèche: animals taking care of young that are not their own.
Culture: a process that involves social transmittance of a shared
behavior among local conspecics through successive genera-
tions. Dawkins (1976) discussed the unit of cultural transmis-
sion termed “meme.”
Deceit: intentional misinformation provided by a sender to a
receiver. Also, dishonest signals.
Dominance: relative behavioral and or physical superiority.
Eavesdropping: acquiring information from conspecics and
heterospecics often without detection.
Epigenetic: heritability of traits by daughter cells not caused by
changes in DNA sequences.
Epigenome: record of the chemical changes to the DNA and
histone proteins of an organism that can be transmitted to o-
Ethology: the naturalistic study of behavior from an evolutionary
Family: a genetic unit comprised of adults and their progeny, in-
cluding cases where ospring continue to interact regularly with
their parents and siblings into adulthood (see Emlen, 1995).
Hamiltonian spite: behaviors occurring among conspecics that
have a cost for the actor and a negative impact upon the recipient.
Helpers at the nest: genetic relatives (brothers, sisters, aunts) as-
sisting in the care of eggs and or progeny.
Imprinting: any kind of phase-sensitive learning. e existence
of a sensitive period (e.g., neonatal stages) during which the in-
dividual is susceptible to the inuence of experience. Experiences
which occur after the sensitive period cannot reverse prior eects.
See Natal habitat preference induction (NHPI).
Kin: genetic relatives, such as parents or siblings, or more distant
such as aunts, uncles, and grandparents.
Kin-associations: the tendency of kin to a form groups.
Kin-recognition: the ability to detect and recognize close rela-
Natal habitat preference induction (NHPI): experience with a
natal habitat that shapes the habitat preferences of individuals
and is a source of individual variation in habitat selection.
Pair-bond: conspecic association of a particular individuals,
Parental care: care directed by mother or father to eggs and o-
Personal information: specic information about the environ-
ment (e.g., the location of a den) that an animal has acquired and
acted on previously. It may include social information.
Personality: specic behaviors of an individual that are consistent
(repeatable) in a particular context; similar to the terms tempera-
ment and behavioral syndromes (Stamps and Groothuis, 2010).
Play behavior: play is incompletely functional in the context in
which it appears. (a) It is spontaneous, pleasurable, rewarding, or
voluntary; (b) It diers from other more serious behaviors in form
(e.g., exaggerated) or timing (e.g., occurring early in life before the
more serious version is needed); (c) It is repeated, but not in abnor-
mal and unvarying stereotypic form (e.g., rocking or pacing); and
(d) It is initiated in the absence of severe stress (Burghardt, 2005).
Public information: information that is potentially available to a
wide audience (Clark, 2007).
Rape: the act of sexual intercourse (or other forms of sexual pen-
etration) carried out by physical force, coercion, abuse of authority
or against a person who is incapable of valid consent (i.e., uncon-
scious, incapacitated, or below the legal age of consent) (ornhill
and Palmer, 2000).
Reaction norm: degree of phenotypic plasticity (e.g., behavior) of
Reciprocity: the evolution of cooperative or altruistic behavior
may be favored by the probability of future mutual interactions.
Sentinel: the behavior of an individual to protect others, such as an
alpha male guarding a group of conspecics.
“Beatrice” alternates her den sites from year to year, and so on.
It is not uncommon to hear stories of nding dozens of female
rattlesnakes beneath one rock with their ospring. Why are
males sometimes found near birthing aggregations, rookeries,
or nurseries (Dunkle and Smith, 1937; Holycross and Fawcett,
2002; Amarello et al., 2011; O’Connor et al., 2015; see Figure
17 in Davis et al., volume 1, Crotalus cerberus)? What bridge do
we need to cross to write about these observations above and
beyond simple anecdotes? We strongly feel that anecdotes are
vital, but how do we develop research programmes to study and
test the social lives of snakes within a new lexicon? What are
the important questions that should be addressed? All of these
points are important, yet the rst steps must be to change our
biases and perceptions.
Gordon Burghardt and his collaborators have been strident
leaders in re-examining anthropomorphism, and they have
forced us to question and re-consider the ways in which we
study and interpret animal behavior. Burghardt’s areas of exper-
tise are learning, ontogeny, play, chemoreception, and social be-
havior of reptiles. Other giants in the eld who have made simi-
lar advancements to our understanding of anthropomorphism
in other vertebrates include Marc Beko (Allen and Beko,
1997; Beko and Allen, 1997; Beko, 2007), Frans de Waal
(de Waal, 2005), Jane Goodall (Whiten et al., 1999; Goodall,
2010), Temple Grandin (Grandin and Johnson, 2006), Donald
Grin (Grin, 1981, 2001), and Irene Pepperberg (Pepper-
One of the most important advancements from the
Burghardt laboratory was to expand upon the original four aims
of ethology laid out by Nobel Laureate, Nikolaas Tinbergen
see Tinbergen, 1963; reviewed by Stamps, 2003). To these four
categories, Burghardt amended a fth aim to illuminate the im-
portance of private experience (Nagel, 1974; Burghardt, 1997,
1998, 2005; Rivas and Burghardt, 2001, 2002).
Self-awareness: the ability to recognize oneself as an individual
and separate from the environment and other like individuals.
Self-organization: a spontaneous process where some form of co-
ordination (organization or order) emerges out of local interactions
between components (e.g., individuals) of a system that was origi-
nally disordered. Common examples include animal aggregations,
such as the formation of ocks (birds) and schools (sh).
Social: any activity between conspecics (cf. Wittenberger, 1981).
Social learning: learning that is inuenced by the observation of
or interaction with another individual.
Social network: a set of social individuals (or organizations) and a
set of the dyadic ties between these individuals (or organizations).
Territoriality: defense of a dened object or area against conspecif-
ics or individuals of another species.
Trans-generational inheritance: the transmittance of information
from one generation to the next that aects the traits of ospring
without alteration of the primary DNA sequence or from environ-
1. Control: the study of causation and proximate mecha-
nisms (e.g., physiology).
2. Adaptive function: the study of adaptation; survival and
3. Development: the study of ontogeny, including the in-
uence of maturation and experience.
4. Evolution: the study of populations; genetic, epigenetic,
5. Private Experience: the “mental experience” of individu-
als; personal world.
What does private experience mean? Why is private experi-
ence important to the discipline of ethology and evolution? As
Burghardt (2005) explains, Nikolaas Tinbergen was well aware of
this fth aim, but during his career the time was not appropriate
for its introduction as part of “science” to the community. With
a range of advances since Tinbergen’s time, we are now better
able to investigate taboo topics in ethology, sociality, and evolu-
tion (Box 1). Similar progression and change (= paradigm shifts)
have been made in all branches of the sciences. In particular, Carl
Sagan comes to mind as a recent victim (http://en.wikipedia.
Box 1. A taboo topic in animal behavior studies: anthropomorphism
Anthropomorphism: attributing human properties to nonhuman entities. Such entities can be supernatural (gods), animate, or inanimate.
One of the greatest challenges in studying social behavior in snakes is that they stray in likeness from familiar warm and fuzzy creatures featured on
television and other venues. is point cannot be overstated. Whenever a research endeavor begins with strong preconceptions of what will (or will
not) happen, the biggest hurdle is unintentional blindness. Or, put more bluntly, the inability and failure to see the elephant in the room (cf. Rivas and
Burghardt, 2001, 2002). If one accepts that snakes are “deaf” and thus do not have the sensory organs for hearing, for example, it is quite unlikely that
meaningful audiological measurements will be attempted. If one holds (or is not critically thinking) that kin recognition, family structure, or culture
does not exist in snakes, or that it is not even possible, it will not be measured. Once those kind of conceptual barriers are broken, however, we are
emancipated from the grips of narrow thinking; ideas once viewed as mere distractions or incorrect become research projects and programmes. Or, we
can put new wine in old bottles (Burghardt and Gittleman, 1990). e time is ripe for conceptual blockbusting.
Do other animals have feelings? Personalities? Even a sense of self? How do we measure these kinds of human attributes in nonhuman organisms,
from great apes and dogs to snakes and insects? Despite being noted for bold and out-of-the-box ideas and statements about animal behavior, Temple
Grandin herself cannot escape the very error she is trying to undue when she states in a recent lm that snakes probably do not have social lives. Un-
familiarity breeds contempt.
org/wiki/Carl_Sagan). Professor Sagan, who was a visionary, was
probably denied entry into the prestigious National Academy of
Sciences owing to his popularization of science and views about
the possibilities of life existing elsewhere than earth. Today, citizen
science (= crowd-sourced science and networked science) has an
enormous impact in helping to advance natural history and scien-
tic quests (http://www.citizensciencealliance.org/). Exobiology is
testable, hugely popular, and billions (and billions!) of dollars are
spent in the United States alone to probe Mars and asteroids for
traces of life (e.g., amino and nucleic acids) and, of course, life it-
Box 1. Continued
Anthropomorphism by omission: the failure to consider that other animals have a dierent world than ours.
Without realizing it, scientists can attribute human traits by failing to consider that many species perceive the world dierently from humans. To move
forward, we must accept as fact that animals have private worlds that are both similar and dierent from humans (reviewed by Rivas and Burghardt,
Critical anthropomorphism: a perspective in the study of animal behavior that encompasses using the sentience of the observer to generate hypotheses
in light of scientic knowledge of the species, its perceptual world, and its ecological and evolutionary history.
Gordon Burghardt (1985) defended anthropomorphism and argued its legitimacy in science if it is used to develop hypotheses that can be tested cre-
atively and rigorously. He also introduced critical anthropomorphism as means of using various sources of information to generate ideas that can be
used in experimental studies of animal behavior (Burghardt, 1991, 2007). Anthropomorphism is a natural tendency of human beings, including biolo-
gists. By using critical anthropomorphism and trying to “wear the animals’ shoes” (Rivas and Burghardt, 2001; Burghardt, 2005), we can overcome
part of our natural bias and accomplish a more legitimate understanding of the life of other species in their natural world. We agree with Burghardt and
Rivas that anthropomorphism is only harmful in science when it is unacknowledged, unrecognized, and used as the basis for accepting conclusions that
are not tested scientically. Not everyone agrees that critical anthropomorphism is appropriate in addressing scientic hypotheses (see Wynne, 2007).
However, despite criticisms, we feel moving forward with a critical eye is the rst important step in nding appropriate language and other tools to
understand and discuss the private lives of snakes and other animals (Beko, 2007).
Gordon W. Schuett
self (https://astrobiology.nasa.gov/exobiology/). Paradoxically, sci-
entic revolutions and paradigm shifts rarely occur due to strong
inertia; advances and progress emerge on the scene suddenly and
from seemingly from “nowhere” with saltatory leaps (Kuhn, 1996).
Presently, we are building towards a much broader apprecia-
tion of what social and “private experience” means for all animals,
including snakes and other reptiles. Our lexicon for animal social
behavior has expanded greatly, owing not only to technical ad-
vancements but by challenging our own perceptions and restric-
tive language (biases, taboos, and stereotypes) that have prohib-
ited advancement. Although many of the terms in the Glossary
and Box 1 are rarely used when discussing the social behaviors of
snakes (Shine et al., 2000), they have been described and used in
empirical research of a wide variety of other animals, from spiders
and ants to shes, birds, and mammals (ornhill and Alcock,
1983; Boyd and Richerson, 1985; Dugatkin, 1999, 2009; Earley
and Dugatkin, 2002; Earley et al., 2003, 2005; Bonnie and Earley,
2007; Earley, 2010; Doody et al., 2013).
Crotalomorphism by omission
is more than a metaphor
e following text (italicized) is directly from Rivas and
Burghardt (2002, pp. 11-12):
A researcher is studying the behavior of a very colorful lizard. When
this lizard sees a person it rapidly changes its color and matches the
background, just as octopuses are well known to do. e researcher con-
cludes that the change in color is a cryptic response to avoid predation.
Just at this time, however, a large female timber rattlesnake (Crotalus
horridus) quietly observing the researcher from some nearby brush is
suddenly spotted by the researcher, who is both startled and scared.
Rattlesnakes, being pitvipers, can detect patterns of infrared radiation
from mammals through the loreal pits situated between the eyes and
nostrils. erefore, when she perceives the researcher she detects it as a
very warm animal moving in a much cooler background (not unlike
the way the human sees the colorful lizard). Now when the startled
researcher saw the rattlesnake, adrenaline kicked in and the ow of
blood to the arms and legs was reduced along with all other peripheral
circulation; a normal response to stress. e researcher turned cooler
and was therefore duller to the infrared detecting ‘eyes’ of the snake.
Our clever rattlesnake concludes that the person is trying to escape by
matching the cooler background: the drop in peripheral temperature
was a cryptic response against predators with heat sensing organs.
To most biologists this scene may seem rather unremark-
able in most ways yet it is an insightful and powerful example
of crotalomorphism by omission, using a common experience
of a rattlesnake. Rivas and Burghardt (2002) note that stress
from a predator can cause its prey to exhibit a lower body tem-
perature. However, the rattlesnake’s “conclusion” would prob-
ably be dismissed as erroneous by the majority of behaviorists.
Is the rattlesnake’s “conclusion” dierent from the conclusion
of the researcher studying the lizard? Crotalomorphism high-
lights the problem of interpreting the world solely by one spe-
cies’ standard, perception, or bias (see Box 2 and Box 3).
Box 2. A history lesson, paying homage to Bayard Brattstrom
Historically, our perceptions about snakes and other reptiles have changed over the millennia, from early respect and reverence (eastern societies) to in-
dierence and absolute disgust (western societies). Fascinating to be sure, a reasonable account of this topic would require another analysis and space in
another book (see Reiserer, volume 1, Art and Rattlesnakes). But if we begin at the middle of the 19th century, when biology is about to change forever,
we start with Charles Darwin himself, who seems to have loathed certain reptiles and given them less than a standing ovation for their intelligence.
From his own pen, Darwin (1839) wrote in Voyage of the Beagle that he was not particularly fond of the large Galapagos Land Iguanas (Conolophus
subcristatus), which he mentioned existed in massive numbers on all of the islands he visited. Not only did he describe them as physically unsightly, but
he also saw them as having a rather unintelligent appearance. He also described the awkward and ungainly manner of Marine Iguanas (Amblyrhynchus
cristatus) on land, though did report their swimming proclivities. Although Darwin was not the only biologists who frowned upon reptiles, his negative
views about their “mental limitations” were widely read and popularized. It was not until the middle of the 20th century that we begin to turn some
Over four decades ago, Bayard Brattstrom (1974) reviewed the evolution of social behavior of reptiles. Many of the issues and pitfalls we discuss here
are resurrected from his insights and profound knowledge of this group of vertebrates. e way I see it, in an odd sort of way, Bayard was giving us a
mild scolding about the manner (context and relevance) we carried out laboratory research on reptiles; we treated them as if they were domesticated ro-
dents. He discussed proper temperatures, humidity, diet, shelter, health, and even social conditions. I have no doubt that Bayard was practicing critical
anthropomorphism (crotalomorphism) far ahead of its time. Put yourself in the shoes of the creature you want to understand. Aptly, Bayard mentioned
that there was nearly nothing known about sociality in snakes.
Two years after Brattstrom’s remarkable and insightful review, a symposium on social behavior of reptiles was organized in 1976, and the proceedings
were published the following year (Greenberg and Crews, 1977). Oddly, Bayard was not among the authors who participated.
Bayard challenged the status quo and opened doors. Progress on social behavior in snakes has been relatively slow ever since, but it is being made. I am
delighted that Bayard is alive and able to witness and participate in this revolution which he helped to ignite.
Gordon W. Schuett
Putting aside for a moment the meaning of “private experiences,” I should have seen this coming a long time ago. Several past encounters with lizards
and snakes relate to the question now at hand, so the broader concern is, why didn’t I ask it sooner? How can someone who’s loved scaly creatures since
his rst encounters with a Texas Horned Lizard and a Western Diamond-backed Rattlesnake, at age seven, presume for so long that they’re internally
simple and essentially hard-wired? is backstory query is important, however rhetorical, because it emphasizes a pervasive, misleading status quo in
the minds of many nature lovers—prejudice against venomous snakes entails far more that hateful attitudes of ignorant people. And it’s time for us
all to move forward, to embrace a dierent starting assumption, one that imagines the serpentine stars of this book are behaviorally, even mentally
I’d received Klauber’s two-volume Rattlesnakes as a seventeenth birthday present, and thus realized my observations on diet and reproduction in West-
ern Massasaugas (Sistrurus tergeminus) were worthy of publication. Moreover, thanks to a high school internship with reptile ecologist Henry Fitch,
I’d learned to carefully record that a litter of pups found with their mom on a Texas prairie had “cloudy eyes” and thus were “pre-shed”—but I failed
to recognize this meant those little Massasaugas were not quite “newborn” and she was attending them (Greene and Oliver, 1965, p. 227). Perhaps by
then I’d bought into Klauber’s (1956, p. 737) authoritative pronouncement, “ere is no nal evidence that young rattlers stay with their mothers for
more than a few days or so at most; if they are found together there is no proof the young are no more than a few days old or that their propinquity is
caused by other than use of a common refuge.” Evidently I shared his preconception of behavioral simplicity in snakes.
As for a second set of foreshadowing encounters, it was my good fortune to earn a Ph.D. with ethologist Gordon Burghardt. By the end of one se-
mester at University of Tennessee I was pursuing Nobel Laureate Niko Tinbergen’s four aims of ethology—to understand how behavior is shaped by
evolutionary history, genes and development, physiological mechanisms, and ecology. As it also happened, Gordon wanted to study neonate reptiles in
the wild and took me with him to watch Green Iguanas (Iguana iguana) on an islet o Barro Colorado Island, Panama. is we did during three eld
seasons, lming babies as they crawled from nests, swam between islands, and embarked on the dangerous business of eating and avoiding predators.
To our astonishment, little iguanas emerged from underground, moved about in the forest, ate vegetation, and even slept in clusters, often in contact
with conspecics (Burghardt, 1977a, b; Burghardt et al., 1977). eir cohesive, interactive behavior was thus like that inferred from trackways of ex-
tinct dinosaurs, who at the time were touted as bird-like rather than lizard-like. Back then I viewed Iguana sociality as highly unusual convergence with
dinosaurs (including birds), thus reecting the prevalent view of small-brained, non-archosaurian reptiles as internal simpletons.
Box 3. What are the private experiences of rattlesnakes?
Two other pivotal encounters took place more than a decade later in Arizona’s Chiricahua Mountains, during a study whose initial goal was to observe
free-living Black-tailed Rattlesnakes (Crotalus molossus), with emphasis on foraging tactics. Over the course of 15 years and some 4,000 observations
of 50 radio-telemetered animals, physician collaborator David Hardy Sr. and I documented many fascinating events, of which the most dramatic was
maternal care. Key to our “discovery” was daily checking on six gestating snakes, in particular “Super Female 21,” whom we monitored through four
pregnancies (see Greene, 2013). e big surprise came one July morning when Dave found that rather than having dispersed, six neonates were clus-
tered around their basking mom, with whom they remained for ten days before one by one shedding their skins in front of her. Meanwhile three col-
leagues from Stetson University ran clever experiments on mutual recognition by mothers and neonate Pygmy Rattlers (Sistrurus miliarius), so together
we demonstrated maternal attendance and perhaps family-like social systems characterizes almost all pitvipers (Greene et al., 2002) — a fact that had
lurked in the natural history literature for years (e.g., Greene and Oliver, 1965), but repeatedly had been treated as inconsequential.
e fourth and decisive blow to my own biases also began with a telemetered Black-tailed Rattlesnake, found one morning as he crawled into the
shaded edge of a dry streambed. After 13 minutes of tongue-icking along 2 m of a Cli Chipmunk’s (Tamias dorsalis) runway, Male 41 set up an
ambush coil aimed at the rodent’s trail. rough binoculars I could see a dried fern ~20 cm in front of his snout, such that it might impair a strike, and
two minutes later the rattler extended his foreparts like a shepherd’s crook—a posture otherwise used during male-male combat around nearby recep-
tive females—and depressed the frond, then retracted them into his ambush coil. Alberta naturalist Jonathan Wright later wrote me that he’d seen a
Prairie Rattlesnake (Crotalus viridis) likewise mash down grass around Deer Mouse (Peromyscus maniculatus) burrows before setting up its ambush, and
Putman and Clark (2015) conrmed by videography that Northern Pacic Rattlesnakes (C. oreganus) modify overhanging vegetation to create ambush
windows for hunting California Ground Squirrels (Otospermophilus beecheyi). Clearly rattlesnakes can solve barrier problems, and it stretches credulity
to not attribute intentionality to their responses.
ere have, of course, been other hints of sophisticated behavior along the way. As examples, Fitch (1935) opined from eld studies that alligator
lizards are among the most intelligent of squamates, a view bolstered by recent lab observations (Greene et al., 2006), whereas research on other non-
avian reptiles suggest we keep an open mind as to just which taxa can solve particular problems (Burghardt, 1977a; Leal and Powell, 2011). In 1984,
when I visited a Prairie Rattlesnake study site in Wyoming, the aggregations of females with young (see Duvall et al., 1985) left me grinning with a
dumbfounded sense of really not knowing much at all about rattler behavior. Our own eld observations of Blacktails began soon thereafter, about
the same time as Chiszar et al., (1991) demonstrated self-recognition in captive Timber (C. horridus) and Prairie Rattlesnakes, and before Shine et al.,
Box 3. Continued
(2002) described “accidental altruism” in Shedao Island Pitvipers (Gloydius shedaoensis)—small snakes kill birds too big to eat that are then taken as car-
rion by adults, and adults kill birds too big for them to eat that could have eaten juveniles. Now it turns out Komodo Monitors (Varanus komodoensis)
play (Burghardt et al., 2002), genetic analyses have revealed that aggregating female Timber Rattlers are close relatives (Clark et al., 2012), and remote
photography by Amarello et al. (this chapter) has documented allo-parenting in wild Arizona Black Rattlers (C. cerberus), all of which convinces me
that we indeed are only beginning to grasp what it might mean to be a serpent.
At this point let’s circle back to Tinbergen’s four aims of ethology, to which Burghardt (1997) added a fth—that we combine critical anthropomor-
phism, eld observations, and experiments to ask, what are the private experiences of animals? By “critical anthropomorphism,” Gordon meant that
we should steer clear of conceptualizing rattlesnakes as imperfect humans, thereby diminishing their essential rattlesnake-ness, yet use what we know
about our own internal states to pose testable questions about those of other species. By choosing the term “private experiences,” he deliberately avoided
“cognition,” itself deserving of consideration under a “ve aims of ethology” paradigm. How then might Gordon’s fth question, with its implication of
mentalities in other species, aect studies of Shedao Island Pitvipers or Arizona Black Rattlesnakes? Where does this all leave us? It’s time to study snakes
in the eld and the lab with the presumption that their inner worlds, however vastly dierent from our own, not only exist but are surely complex. It’s a
safe bet that as wild animals they grow up incorporating new information into exible, multifaceted behavioral repertoires, with much of that richness
internal and therefore not immediately accessible to study.
Answering Gordon’s fth question, about the private experiences of other animals, will always be challenging intellectually, but all the more rewarding
personally, so let’s give him the last words here (Burghardt 1977b, p. 188-189):
“…extant reptiles, behaviorally at least, are not the dullards that we have considered both them and dinosaurs to be. As eco-evolutionary studies show, dierences
in organisms relate not to abstract ideas of superiority and inferiority, but to chance and selective factors in a given environmental nexus…Attempts to uplift our
attitudes to dinosaurs are admirable…but to do so at the expense of extant reptile behavior is not only to cut o an important source of evidential support for
social complexity in dinosaurs, but also to obligingly demonstrate selective scholarship, the exaltation of ignorance, perhaps even bigotry. At best we have been too
hasty and uncritical in accepting the common wisdom. Although I can understand the shaping of discriminatory attitudes through generations of unconscious
cultural (and even genetic) bias, sympathy and patronizing patience do not seem appropriate in the presence of well-publicized propaganda. us we need to be
on guard against ‘science’ being uncritically accepted as supporting and encouraging our deeply held prejudices...For if their physiology limits reptiles’ quantity
Box 3. Continued
Dening social behavior
In 1976, a handful of researchers held the rst ever sympo-
sium on the social behavior in reptiles, at the 64th annual
meeting of the American Society of Zoologists ... Surpris-
ingly, after more than three decades, there remains no de-
tailed review of social behavior in reptiles or in vertebrates
- Doody, Burghardt, and Dinets (2013 p. 3)
Despite how simple, or even pedantic, it might seem, largely be-
cause we think we know it when we see it, identifying sociality
and dening the term “social behavior” has been fraught with
diculty and contention (Tinbergen, 1966; Wittenberger, 1981;
Doody et al., 2013). Here, we prefer to avoid jargon and thus
provide a broad denition of “social behavior” to avoid the in-
evitable diculties of exclusivity. Social behavior is any activity
between conspecic individuals. By applying the broadest ap-
proach, our denition can therefore include standard and obvi-
ous social interactions (e.g., ghting, courtship, play, grooming),
as well as cryptic behaviors such as those that that involve chemi-
cal communication by pheromones (Mason and Parker, 2010;
Shine and Mason, 2011; Doody et al., 2013).
Classically, species have often been categorized as either social
or non-social (social-nonsocial dichotomy). Not only is this view
unproductive but it can severely impede new scientic growth
(Doody et al., 2013). Clearly, in vertebrates, many species form
colonies (e.g., bats), while others form massive herds (e.g., wilde-
beest), large schools (e.g., herring, tuna), or complex, long-term
pods (e.g., Orca). As humans, we easily identify with these ex-
amples as constituting social behavior. Why? We are condent
that it is because we behave in roughly equivalent ways. But if we
expand the term social to other types of interactions outside of
our primary sensory domain (vision), such as chemical sociality
of behavior and prevents them from being hyper, nervous, and frenetic as are so many mammals and birds, I say thank God. ey, at least have time to think,
rest, and contemplate. e age of reptiles was long, glorious, and successful; its end is still a mystery. How many times do each of us wish the ‘world would slow
down.’ e problem, my friends, is not with the world, but with the over-riding of our reptilian heritage by the mammalian hot-blooded capacity for overwork
and overkill, as well as the dream that reason really plays an important role in the lives of so-called higher species, in which category humans, but not iguanas,
are always placed.”
Harry W. Greene
Box 3. Continued
(e.g., pheromones), the picture is less clear and much more dif-
cult to interpret. Nonetheless, it is still social behavior by our
Why be social?
e evolution of social behavior is far less bewildering today ow-
ing to the genius of the late William D. Hamilton (Hamilton,
1963, 1964, 1972). Hamilton brought us a staggering view on
genetic kinship theory and its consequences to understanding
aspects of sociality (e.g., altruism, cooperation, inclusive tness,
kin recognition, and kin selection). Other pioneers in the eld
of social behavior theory include the late George C. Williams
(Williams, 1966), Robert Trivers (Trivers, 1972), Richard Alex-
ander (Alexander, 1974), E. O. Wilson (Wilson, 1975), and the
late John Maynard Smith (Maynard Smith, 1982). Also, we pay
homage to three gentlemen: Konrad Lorenz, Nikolaas Tinbergen,
and Karl von Frisch, all deceased, who shared the 1973 Nobel
Prize in Physiology or Medicine for their groundbreaking work
in vertebrates and bees (http://www.nobelprize.org/nobel_prizes/
medicine/laureates/1973/). For in-depth information on social
behavior evolution, we highly recommend reading the works of
all of these authors. Also, there are many books that summarize
this information and are generally more accessible to individuals
with limited skills in mathematics (Brown, 1975; Wilson, 1975;
Wittenberger, 1981; ornhill and Alcock, 1986; Alcock, 1998;
Dugatkin, 2009). If we are to understand sociality, it becomes
clear from this body of work that we must have a solid founda-
tion of a species (individuals) spacing behavior, especially in cases
where the spatial organization is clumped.
We will partition “clumped spacing behavior” into three main
categories, but know they are not mutually exclusive; thus, both
coarse and ne gradations exist between them. e following
categorization of clumped spacing behavior is based on Witten-
berger (1981, pp. 303–305).
Aggregations: the simplest type of clumped spacing in ani-
mals is aggregation, which are temporary assemblages of like
(conspecic) or unlike (heterospecic) individuals brought to-
gether by physical forces in the environment or the attraction
of many individuals to external stimuli or resources (Witten-
berger, 1981) ese groups or assemblages are not the results
of mutual attraction or cooperation of conspecics. Further-
more, coordinated activities and integrated social relation-
ships are generally absent. Examples include assemblages of
organisms forced to group by marine or wind currents, river-
ine oods, and the like; groups utilizing limited shelter dur-
ing inclement weather (hurricanes), and the sudden erup-
tion of an unanticipated food source (e.g., insects, sh eggs).
Forced-imprinting to specic sites, such as in beach areas for
egg-laying in sea turtles, is an example of aggregative behavior.
Social Groups: unlike aggregations, social groups are hy-
pothesized to form and evolve through mutual attraction of
individuals for cooperative benets to survival and tness.
Both kin- and nonkin-based social groups often occur in a pre-
dictable manner and on a seasonal basis (Hatchwell, 2010).
Importantly, behavior may be coordinated by way of a social
communication network, which automatically partitions in-
dividuals into subgroups. Subgroups may form dominance
hierarchies or other types of assemblages. Classic examples are
whale pods, monkey troops, and ungulate herds (Wittenberg-
er, 1981; Dugatkin, 2009). As we discuss later, certain forms
of communal denning in snakes, especially in rattlesnakes, are
bona de examples of social groups or colonies (Shine et al.,
2000; Amarello, 2012; Clark et al., 2012; Schuett et al., 2014).
Colonies: Colonies are very similar to social groups, and vary
primarily in aspects of spatial organization (Evans et al., 2015).
e activities of colony members (kin- and non-kin based) are
centered on a xed location, such as extensive burrow systems
(prairie dogs), rocky den sites (snakes), specialized trees (egrets,
weavers), beaches (seals), and shallow, brackish water (amingos).
Benets and costs of social living
e benets of social groups and colonies (kin- and non-kin
based) include increased vigilance to predators and enemies, pro-
tection from the environment, increased opportunities for repro-
duction, expression of social behaviors including grooming and
parental duties (e.g., uniparental, biparental, and helpers). How-
ever, costs of social living can be severe and include the spread of
parasites and disease, limited numbers of mates, and competition
for food and space itself (Wittenberger, 1981; Alcock, 1998; Kok-
ko et al., 2002; Lehmann and Keller, 2006; Dugatkin, 2009; Ev-
ans et al., 2015). Living in kin-based groups (see an evolutionary
framework for families by Emlen, 1994, 1995) oers individuals,
among other benets, opportunities for increasing their inclusive
tness (Hamilton, 1964; see Dugatkin, 2009). Consequently, a
variety of cooperative and altruistic behaviors can evolve, such
as forsaking reproduction and caring for the progeny of relatives
(Hamilton, 1963, 1972; Dugatkin, 2009). Culture often evolves
more quickly in kin-based groups (Boyd and Richerson, 1985).
Are all snakes equally social?
No. ere is a great deal of variation in types of aggregations or
groups, even within a genus with a relatively small number of spe-
cies, such as in Crotalus (see below). Sociality in animals, like any
other trait, can range from being absent (or nearly so) in some
taxa (e.g., abalone) to being extreme in others, such as in humans
and other primates (Wilson, 1975; Alcock, 1998). Many of the
extant big cats, like most rattlesnakes, are members of a single
genus (Panthera), which oers to researchers a rich compara-
tive perspective: some species are highly solitary (Tigers) and at
least one species is highly social, such as African and Asian Lions
(http://en.wikipedia.org/wiki/panthera). We assume additional
eld work will advance this simple dichotomy or binary division
(Doody et al., 2013). Although our conclusions are subject to
modication as more data are collected, at least from overt be-
haviors of snakes, there appears to be large dierences in degrees
of sociality between rattlesnake species.
Why study sociality in rattlesnakes?
Rattlesnakes (genera Crotalus and Sistrurus) oer researchers
many “natural experiments” to study sociality owing to their in-
herent biological diversity and proclivity to aggregate (Klauber,
1972; Graves and Duvall, 1995). Despite our best eorts to nd
one, we conclude that there is no single study published that has
explored communal denning in rattlesnakes using comparative
phylogenetic methods, though a preliminary analysis shows this
phenomenon appears to be: a) largely conned to the genus Cro-
talus; b) mostly restricted temperate regions; c) more common
in younger lineages, and d) documented mostly in medium- to
large-bodied species (G. Schuett et al., unpubl. data).
Communal denning: a window
to the study of sociality
I hope to provide at least a partial answer to the question:
“why do snakes den communally?”
-Patrick. T. Gregory (1984, p. 57)
e topics in social behavior are far too numerous to cover in a
single chapter; thus, we converged on a decision – with little dif-
culty – to overview the topic of communal denning and social-
ity in rattlesnakes. e phenomenon of communal denning in
rattlesnakes is presented at length by Klauber (1956, 1972; see
Sexton et al., 1992; Graves and Duvall, 1995). His re-descrip-
tions and discussion of A. M. Jackley’s observation of denning in
Prairie Rattlesnakes (Crotalus viridis) from South Dakota are bril-
liant and thought-provoking. Like most, Klauber (1956, 1972)
focused primarily on environmental factors associated with com-
munal denning, such as protection from cold and inclement
weather. Nearly all reports on communal denning in rattlesnakes
since Klauber lack details of social behavior, especially at the level
of the individual (but see Clark, 2004; Amarello, 2012; Clark et
Gregory (1984) oered three mutually inclusive hypotheses
regarding the occurrence and formation of communal denning
in snakes, with no particular reference to or emphasis on rattle-
snakes. ese are:
1) Availability of suitable den sites low;
2) Enhancement of thermoregulation (reducing heat loss) ow-
ing to numbers; and
3) Increased opportunities for mating success owing to close
proximity of individuals.
An assumption or bias in most publications on communal
denning in rattlesnakes is that the use of dens by rattlesnakes is re-
stricted to the months of winter. Observations of several western
species (Crotalus cerberus, Crotalus concolor), for example, indicate
that communal dens, and physical structures (e.g., boulders) im-
mediately adjacent to them, are used as birthing rookeries (Graves
and Duvall, 1995; Amarello et al., 2011) or nurseries (Amarello
et al., 2011; Parker et al., 2013; see Davis et al., volume 1, Crota-
lus cerberus). Furthermore, owing to the availability of prey (e.g.,
lizards), young-of-the year and juveniles of these two species often
occupy dens (and nearby areas) for a period of up to several years
post-birth (M. Feldner, pers. comm.; G. Schuett and L. Porras,
unpubl. data). Adults, particularly females, may remain at dens
(or nearby areas) year-round when undergoing gestation (Graves
and Duvall, 1995; G. Schuett and L. Porras, unpubl. data).
Beyond reproductive behaviors, we envision many other types
of social interactions are possible at communal dens (see Glos-
sary and Box 1). Communal dens of snakes, similar to hives of
wild bees, are centers for social communication where individuals
acquire and process visual, tactile, infra-red (pitvipers), and che-
mosensory information (see Shine et al., 2000). How could they
not be unless snakes are mere automatons? From this point, we
will be stepping away from tradition — we will not discuss stan-
dard and conventional topics concerning communal denning in
snakes; rather, based on the introductory discussion, we will oer
new perspectives and fresh approaches to the study of communal
denning and social behavior. Neglected topics, collectively under
the umbrella of culture and cultural transmission, include eaves-
dropping, copying, audience and bystander eects. Furthermore,
new-generation approaches that provide linkages to the study of
behavior and evolution are trans-generational phenomena (epi-
genetics) involving stress, genomic imprinting on mate prefer-
ence, and sex determination (Ohlsson et al., 1995; Bossdorf et
al., 2008; Crews et al., 2007, 2012; Crews, 2008; Warner et al.,
Over the past quarter century, the study of social behavior in
dicult-to-study vertebrates (e.g., cryptic or secretive species such
as many snakes) has entered a period of remarkable growth and
development owing to technological advances in miniaturized
telemetry coupled with GPS technology (Dorcas and Willson,
2009; Beaupre, this volume, Monitoring Technologies), DNA-
based methods to ascertain the identity of individuals and recover
unique pedigrees (Clark et al., 2014), and the rising utility of ge-
nomic information and next-generation computational programs
capable of rapid analysis of complex sequence data (Shield et al.,
this volume, Genomics). To understand the whereabouts of in-
dividuals, miniaturized radio-transmitters coupled with satellite
technology provides highly accurate GPS information, which has
permitted the investigation of Earth’s most massive creatures on
land and seas, and among its smallest hiding in tree canopies and
the recesses of rock clis. Humans have become excellent voyeurs
Most studies of denning in snakes cover communal denning
(Gregory, 1984; Gregory et al., 1987; Shine et al., 2000; Repp
and Schuett, 2009). Indeed, in snakes, individuals of many spe-
cies of temperate zones overwinter alone at shelters. However,
we are fascinated by those species and populations where dozens
or even hundreds of individuals converge and form impressive
groups or aggregations (Klauber, 1972; Gregory, 1984; Sexton et
al., 1992). In many of these cases, however, forming these groups
is a function of necessity (survival) because den sites are often a
limited resource (for example, an aggregation; see above for an
explanation of the term).
Even more fascinating to us is when communal denning oc-
curs under conditions that do not appear to be dictated by envi-
ronmental constraints (e.g., cold, limited number of den sites).
e paper by Repp (1998) on communal denning in Western
Diamond-backed Rattlesnakes (Crotalus atrox) in southern Ari-
zona was an important springboard for subsequent research of C.
atrox at the Suizo Mountains (described herein; see Schuett et al.,
volume 1, Crotalus atrox). In central and southern Arizona, adult
individuals of C. atrox often aggregate in dens (2–15 individu-
als) made of granite or caliche formations. Why do they do this?
e climate in southern Arizona bears absolutely no resemblance
to winter in South Dakota. We thus can (mostly) rule out ex-
treme cold as a motivating environmental factor. Furthermore,
most individuals using these dens are not below the surface;
rather, they are mostly ush with the desert oor (sometimes
above it) and can be located, observed, and recorded (youtube.
com/watch?v=QUsFafhR6SA). Moreover, basking outside the
den during winter can be common (Repp, 1998; Schuett et al.,
2006; Repp and Schuett, 2008). In fact, some individuals, espe-
cially males, make both short (several meters) and long (several
hundred meters) movements during winter; sometimes, albeit
rarely, they play “musical den sites” for reasons we do not yet
fully understand (R. Repp and G. Schuett, unpubl. data). None-
theless, we persevere to t into their shoes to discover answers.
Despite the fact that communal dens are a rich resource to
study social behavior of rattlesnakes, few detailed studies are
available. Long-term studies monitoring specic individuals are
extremely scarce (Sexton et al., 1992; Repp, 1998; Amarello,
2012). Before discussing social behaviors and communal den-
ning in rattlesnakes, it is important to briey classify or catego-
rize rattlesnake dens into several dierent types based on social
Types of communal dens
While it is often assumed that pitvipers…breed after emer-
gence from hibernation or any time thereafter, there is in-
creasing evidence along two lines to the contrary. Observa-
tions based upon radio-tracking indicate that most mating
occurs during mid- to late summer away from the dens…
is conict suggests that the study of social systems of a
variety of species on either side of 38° latitude would be a
worthwhile subject of study.
-Sexton et al. (1992, p. 343)
Research on communal denning behavior in rattlesnakes from
temperate regions is usually centered on topics that concern lo-
cation, structure, and thermal environments of dens. Moreover,
emphasis is almost exclusively on how dens provide shelters or
safety during “winter” (November through March). Most often
communal dens are described as permanent structures and made
of rock, e.g., dens are often metamorphic rocks (Klauber, 1972;
Sexton et al., 1992; Repp, 1998; Hamilton and Nowak, 2009;
Gienger and Beck, 2011). However, they can also be ephemeral,
such as a rodent nests or middens (Repp, 1998; R. Babb, pers.
comm.). Sometimes, rattlesnakes use articial sites (e.g., aban-
doned mines, building and home materials, and other anthropo-
genic structures) as communal dens (see Nowak and Greene, this
volume, Conservation). Table 1 provides a preliminary glimpse at
the activities of rattlesnakes at communal dens which include: a)
reproduction (e.g., courtship and mating sites); b) birth sites; and
A preliminary inspection of seasonal activities of rattlesnakes (genus Crotalus) at communal dens. FMD = fall-mating at den. SMD =
spring-mating at den. BD = birth at dens. DDS = duration at den in spring: brief (B) or protracted (P).
c) shelters during the active seasons. Clearly, even in this simple
eort (Table 1), there are key dierences between species. And
as we will discuss, there are clear dierences between popula-
tions, especially those that occur below 38° latitude (Sexton et
al., 1992). e study of social behavior of rattlesnakes at com-
munal dens will vary greatly in types of behavior exhibited and
thus information generated by researchers.
Benchmark studies of social
behavior in rattlesnakes
We have selected three species of rattlesnakes to discuss the topic
of sociality and communal denning. Furthermore, with respect to
our selection of studies, emphasis was placed on the study of indi-
viduals and reporting individual dierences (Clutton-Brock and
Sheldon, 2010; Dall et al., 2012). ese studies are the exception
to the rule insofar as our knowledge base is concerned.
Timber Rattlesnake (Crotalus horridus)
We begin this section with the Timber Rattlesnake (C. horridus), a
wide-ranging species of Eastern North America whose geographic
distribution dips approaches and Ernst, 2012). No other species
of rattlesnake in the United States has received as much attention
in the past several decades with respect to eld research (Brown,
1993), and there are many outstanding peer-reviewed papers and
book chapters on its ecology throughout its extensive range in the
United States (reviewed in Brown, 1993; see chapters in Schuett et
Ditmars’ (1907, 1942, http://en.wikipedia.org/wiki/Ray-
mond_Ditmars) recollections of communal denning in the Tim-
ber Rattlesnake (C. horridus) are legendary among herpetologi-
cal circles. He mostly discussed populations occurring in New
York and nearby New England states. Accounts can be found
throughout early American literature (Klauber, 1956, 1972;
Brown, 1993; see Reiserer, volume 1, Art and Rattlesnakes).
Also, a body of work is available on conspecic trailing and den
location in newborn C. horridus (Brown and MacLean, 1983;
Reinert and Zappalorti, 1988; Cobb et al., 2005).
Do rattlesnakes show kin recognition?
Living in groups has both costs and benets (Hamilton, 1964;
Alexander, 1974; Wittenberger, 1981). Common benets in-
clude increased vigilance, predator defense, access to mates,
and control over other resources (Wittenberger, 1981; Alcock,
1998; Dugatkin, 2009). Costs include use of limited resources
and spreading disease or parasites (Wittenberger, 1981; Alcock,
1998; Dugatkin, 2009). Although group living in animals does
not necessarily involve close kin-associations or groups (Mato-
cq and Lacey, 2004; Lucas et al., 2005; Buston et al., 2007;
Dugatkin, 2009; Murrant et al., 2014), inclusive tness theory
predicts that the evolutionary benets of group defense will be
greater when they are composed of kin rather than unrelated
individuals (Hamilton, 1964).
Motivated by the fact that Timber Rattlesnakes of all age
and size classes commonly aggregate to communal dens during
winter, and females often form “birthing rookeries” (2 or more
individuals) at or near dens, one of us (RWC) designed a study
to investigate whether captive-reared Timber Rattlesnakes (Cro-
talus horridus) have the ability to recognize kin, i.e., siblings
(Clark, 2004). Although kin recognition occurs across a wide
range of vertebrates (Dugatkin, 2009), at the time I initiated
this study it had not been documented in any snake species.
Earlier studies were hinting at or demonstrating that snakes
could identify individuals (Schuett and Gillingham, 1989; Yea-
ger and Burghardt, 1991), but kin tests were not performed.
Even today, only several species of snakes, including the pitvi-
per Agkistrodon piscivorus, have been tested for kin recognition
(Pernetta et al., 2009; Hoss, 2013; Hoss et al., 2015). In these
taxa, kin recognition was demonstrated.
To approximate a natural birthing rookery, individually
marked mothers and neonates of three litters were housed to-
gether in a communal enclosure. Upon shedding their natal
skin, I placed neonates individually in 20 gallon terraria, where
they were maintained in isolation from each other for 2.5 years.
Because female Timber Rattlesnakes may be more gregarious
than males, I tested kin associations between male and female
subjects separately (Clark, 2004). Trials were conducted using
four treatments: pairs of female kin, pairs of female non-kin,
pairs of male kin, and pairs of male non-kin. ere were 10 fe-
males from three dierent litters available, leading to a possibil-
ity of 12 dierent unique pairings of female kin. Because these
pairings involved use of the same subjects in multiple trials, all
treatments were balanced after this fashion. e same individu-
als were used in the same number of trials when pairing female
non-kin, and 10 randomly selected males from the three fami-
lies were used in pairings of male kin and non-kin. us, each
treatment consisted of 12 unique pairings of individuals, with
some individuals being used in more than one pair in a bal-
anced design. Prior to the study, all individuals were coded with
small paint marks on their dorsum. e observer was blind as
to the familial identity of the snake subjects. At the beginning
of each trial, two subjects were introduced simultaneously into
an open-topped arena lined with clean construction paper. e
position of each individual was recorded during daylight hours
four times daily, at 3 h intervals for 3 days. Each individual
was recorded as being in either an active (uncoiled) or resting
(coiled) position, and the minimum distance between the indi-
viduals was estimated to the nearest 5 cm.
I found that pairs of female siblings associated more closely
with each other than unrelated females (males of either type
were not as gregarious), indicating that C. horridus females can
recognize kin, even after being maintained for more than 2
years in strict isolation (Clark, 2004).
Cryptic sociality and kin associations
Building on the laboratory-based kin recognition research,
one of us (RWC) recently identied kin-based aggregations
in natural populations of C. horridus (Clark et al., 2012). We
used microsatellite markers to characterize relatedness among
eld aggregations of Timber Rattlesnakes (Crotalus horridus),
a largely solitary reptile that relies heavily on chemical cues for
communication. Our results show that juveniles and pregnant
females preferentially aggregate with kin under certain condi-
tions (Figure 4). However, other types of aggregations showed
no kin preference (e.g., winter denning). Potential benets of
aggregating with kin include thermoregulatory, predator de-
fense, and possibly other cooperative behaviors (Evans et al.,
Research on social behavior has largely concentrated on birds
and mammals in visually active, cooperatively breeding groups
(although such systems are relatively rare) and focused much less
on species like Timber Rattlesnakes that are solitary for much of
their life, but occasionally exhibit social aggregations. e abil-
ity to recognize kin and enhance indirect tness thus might be
Figure 4. Rattlesnake aggregations of close kin. a) Pregnant Timber Rattlesnakes (Crotalus horridus) at a rookery in New York. Photo by Rulon W. Clark.
far more widespread than implied by studies of animals whose
behavior is primarily visually and or acoustically mediated, and
we predict that molecular markers will reveal many additional
examples of cryptic sociality in snakes and in other reptiles.
Integrating individual behavior
and landscape genetics
Previous studies have documented that Timber Rattlesnakes
which occupy the same dens have higher relatedness than con-
speci cs using neighboring winter dens (Bushar et al., 1998).
Figure 4. b) A female C. horridus and newborn from New York. Because DNA-based parentage analysis was not performed, we infer that the female is the
mother of this o spring. Photo by Harry W. Greene.
Rattlesnakes and other pitvipers exhibit other characteristics con-
sistent with advanced sociality, including group defense, conspe-
cic alarm signals, and maternal defense of young (Graves and
Duvall, 1987, 1988, 1995; Graves, 1989; Greene et al., 2002;
Repp and Schuett, unpubl. data). As in some lizards (Chapple,
2003), these ndings reinforce the view that, rather than being
solitary and non-social, some snake species are gregarious and so-
cial and may even form kin groups (e.g., families) or at least some
mixture of kin- and non-kin members (below; see Schuett et al.,
2014) at specic times of the year (Emlen, 1994, 1995; Greene
et al., 2002).
Timber Rattlesnakes in the northern part of their range not
only often assemble in large numbers at communal dens in the
fall and remain in them throughout winter (Ditmars, 1907,
1942; Sexton et al., 1992; Brown, 1993; Martin, 2002), but also
exhibit high levels of natal philopatry (term reviewed in Davis
and Stamps, 2004). Individuals born at or near a particular den
often return to that identical site the following season, and they
continue to do so as adults and presumably throughout their lives
(Brown, 1993). We (Clark et al., 2008) investigated the genetic
structure of Crotalus horridus at specic dens in the northeast-
ern United States using DNA-based (microsatellite loci) methods
(Gibbs and Weatherhead, 2001; Blouin, 2003).
Snakes that were sampled at specic dens exhibited only mod-
est levels of genetic dierentiation, indicating a signicant level
of gene ow between most dens. is result was unexpected given
previous evidence from demographic mark–recapture studies in-
dicating that less than 1% of individuals ever dispersed from their
natal den and nearby area. Also, there was no signicant correla-
tion between genetic dierentiation and geographical distance,
but a signicant positive correlation was detected between genet-
ic dierentiation and a cost-based distance metric adjusted to in-
clude the amount of potential basking habitat between den sites.
Genetic parentage analyses conrmed high levels of philopatry
of both sexes to their birth dens (= maternal dens); however, ap-
proximately 30% of paternity assignments involved individuals
between dens, conrming that gene ow largely occurs through
dispersal of adult males during the mating season from late sum-
mer to early fall (Brown, 1993).
e results of this study illustrate the importance of integrat-
ing individual-level behaviors and landscape features with stud-
ies of ne-scale population genetics in species. ese ndings
also underscore how species-typical requirements and habitat
specialization result in complex patterns of population connec-
tivity. Landscape genetic approaches to population connectivity
have been useful in elucidating how habitat structure (e.g., cor-
ridors) aects genetic structure in a variety of species (reviewed
in Manel et al., 2003; Manel and Holderegger, 2013). Finally,
the modest degree of genetic dierentiation among the dens and
male-mediated eective gene ow in C. horridus has important
conservation implications. For example, anthropogenic barriers
to movements, such as roads, can have a strong impact on gene
ow and population structure in this species (Bushar et al., 1998,
2014; Clark et al., 2008; Anderson, 2010; ; see Herrmann, this
volume, Molecular Conservation; Nowak and Greene, this vol-
ume, Conservation). Accordingly, conservation planning must
consider including all, or at least the most important aspects, of
a species’ landscape (e.g., dispersal corridors, summer hunting
grounds, winter dens).
Experimental studies on inadvertent social
information and public information
Social information obtained outside the context of direct com-
munication and signaling is termed Inadvertent Social Infor-
mation (ISI). Public Information (PI), on the other hand, is a
specic category of ISI where individuals use information from
conspecics to assess the quality of important resources, such as
food (Valone and Templeton, 2002; Danchin et al., 2004). Re-
search on the phenomenon of ISI, specically PI, has focused
almost exclusively on social foragers that live in groups and moni-
tor nearby individuals. PI is potentially available to individuals
that hunt or forage alone as well, in the form of cues (such as
chemical cues) that persist in the environment after conspecics
are no longer present.
To test for the potential for rattlesnakes to use public infor-
mation, I (Clark, 2007; see Glossary) experimentally investi-
gated the responses of C. horridus, a solitary sit-and-wait hunter,
to chemical cues from conspecics that had recently fed as op-
posed to those that had been deprived of food. Subjects were
run through a standard T-maze with or without chemical cues
of snakes that had recently fed. I also used an enclosure test
(Choice test) and found that individuals were more likely to
select ambush sites in areas with chemical cues from conspecif-
ics that had recently fed. e T-maze experiment indicated that
Timber Rattlesnakes always follow conspecic chemical trails
out of the maze, regardless of whether or not the individual leav-
ing the trail had recently fed. However, the enclosure choice test
found that individuals are more likely to select ambush sites in
areas with chemical cues from conspecics that had recently fed.
My ISI-PI study with C. horridus raises the possibility that ISI-
PI may be used by animals that are low-energy ambush predators
(Nowak et al., 2008; see Clark, this volume, Hunting and Feed-
ing Behavior). ese predators often exhibit a 2-stage foraging
strategy, with a short search stage while they move through the
environment looking for appropriate ambush sites, and a pro-
longed wait stage where they remain concealed and attempt to
ambush prey that come within strike range (Clark, 2006, this vol-
ume, Hunting and Feeding Behavior). ese ambush predators
may assess both the presence and success of conspecics during
the search stage, while attempting to locate good ambush sites.
Western Diamond-backed Rattlesnake (Crotalus atrox)
e Western Diamond-backed Rattlesnake (Crotalus atrox) is the
indisputable iconic snake of the American Southwest. Perhaps no
other species of rattlesnake has received as much attention, or is
better known, owing to movies and roadside curio shops (Rubio,
1998), rattlesnake round-ups (Fitzgerald and Painter, 2000), dis-
plays at zoological gardens, and snakebite victims (Klauber 1972;
Campbell and Lamar, 2004; Schuett et al., volume 1, Crotalus
atrox). Despite its abundance and undeserved infamous status,
long-term research on the behavior and ecology of this taxon is
lacking. Although eld studies on C. atrox in Arizona exist (e.g.,
Beck, 1995; Taylor et al., 2004; Nowak, 2005, 2009), the longest
continuous study is by two of us (GWS and RAR), which has been
coined e Suizo Mountain Project (SMP) after the mountain
range which bears the same name (see Schuett et al., volume 1,
Introduction to the Suizo Project
In March 2001, the SMP was initiated and long-term (5 years
or greater) research projects were planned involving the Western
Diamond-backed Rattlesnake (Crotalus atrox) and other venom-
ous reptiles inhabiting the area (Repp and Schuett, 2008, 2009;
Schuett et al., 2011, 2013a, b; Clark et al., 2014). e SMP re-
mains in operation at the time of this writing (January, 2016).
In studying C. atrox, our initial goal was to test three hypotheses
concerning den use and den occupants: 1) Do individuals exhibit
den delity? 2) Are individuals that occupy communal dens closely
related or kin? 3) Do individuals overwinter individually? Here, we
provide our preliminary ndings and discuss future research.
Use of and delity to solitary
and communal dens
e ubiquitous phenomenon of aggregation in all life forms – from
microbes and insects to elephants and whales – has promoted the
investigation of the formation, pattern, and persistence of this be-
havior, particularly in conspecics (Parrish and Edelstein-Keshet,
1999; Chowhury et al., 2004; Couzin, 2006). In vertebrates, ag-
gregations of single species can vary greatly in size from several
individuals in primates and cats to literally tens of thousands or
greater in shes and bats. Furthermore, these groups are both kin-
and non-kin based (Krause and Ruxton, 2002; Covas and Griess-
er, 2007; Clutton-Brock, 2009; Dugatkin, 2009; Godfrey et al.,
2014). erefore, are these aggregations or societies dynamically
changing members (e.g., ssion-fusion type; Croft et al., 2008) or
are they relatively unchanging and stable?
Communal denning during winter is an important compo-
nent of the spatial ecology and social structure of some popula-
tions of C. atrox in Arizona (Klauber, 1972; Sexton et al., 1992;
Repp, 1998; Repp and Schuett, 2008). Preliminary observations
made by Repp (1998) suggested that at least some individuals of
C. atrox in southern Arizona regularly return in fall and aggregate
at dens they used the previous year and sometimes earlier. Simi-
lar to other species of snakes, the spatial ecology and activities
of neonatal and juvenile C. atrox are largely unknown (Beaupre,
this volume, Monitoring Technologies). Preparation for the win-
ter period (mid-November to mid-March) in adult C. atrox at
the Suizos involves two primary stages: migration and den selec-
tion. In adult males, migration is initiated in fall (mid-October
to early November) from their home range area, and movements
are directed toward dens. Dens most often used by adult males
are composed of metamorphic rock (e.g., feldspar, gneiss, granite)
and are located at the edges of (or contained within) the Suizo
Mountains. Distance traveled from a home range to a den may be
up to 1.6 km and require several weeks. After a den has been lo-
cated and ingress occurs, usually by November, we classied them
as solitary- (only a single individual present) or communal-type.
To be classied as a communal den, two or more conspecics
must be present (Sexton et al., 1992). Furthermore, communal
dens have been further categorized into three sub-types (Repp,
1998; Schuett et al., volume 1, Crotalus atrox). Briey, these are
gash, crevice, and talus dens; depending on the location, one or
all types of communal dens may be present. At the Suizos, crev-
ice and gash dens are the most common of the three (R. Repp
and G. Schuett, unpubl. data). Also, we have found that adult
males show 100% delity to both solitary and communal dens
(Repp, 1998; R. Repp and G. Schuett, unpubl. data). In both
cases the dens are composed of metamorphic rock. Once the dens
are reached ingress occurs, but animals often shuttle in and out
of them over a period of days to weeks, mostly to bask. In some
locations, basking sometimes occurs during winter (Repp, 1998;
Schuett et al., 2006). Courtship and mating do not occur at dens
in the fall.
Adult females, in contrast to males, may or may not use the
same type of dens. ey are similar to males in that they migrate
from their home range to reach a den (solitary or communal),
but are dierent in that they may select mammal burrows (e.g.,
rodent, Ground Squirrel, Badger) or mammal nests (e.g., free-
standing Packrat middens located in bajada areas) as a winter den
actually within their summer home range. Burrows of mammals
are short-lived relative to most communal dens (metamorphic
rock). To the best of our knowledge, burrows are occupied only
by a single snake during winter (R. Repp and G. Schuett, unpubl.
data); hence, based on our classication schema, these are solitary
dens. Interestingly, we never observed adult males using mammal
burrows as den sites. Unlike males, adult females may or may not
show delity to dens. Sometimes they overwinter in a den soli-
tarily (burrows, nests, or rock shelters), yet other times they are
found in communal dens with or without males present (R. Repp
and G. Schuett, unpubl. data).
At Suizos, the number of adult C. atrox at communal dens
varies from 2 to 22 adults, and sex ratio tends to be male-biased
(e.g., 2.1 to 5.1). Neonates and juveniles are not present at com-
munal dens used by adults (Repp, 1998; Schuett et al., volume
1, Crotalus atrox; R. Repp and G. Schuett, unpubl. data). As best
as we can determine, young individuals overwinter in solitary
shelters, e.g., mammal burrows (R. Repp and G. Schuett, un-
publ. data). Unlike many rattlesnake species (Graves and Duvall,
1995), pregnant C. atrox at the Suizos do not use dens or nearby
shelters as birthing sites or long-term rookies during gestation (R.
Repp and G. Schuett, unpubl. data).
In the southern populations we have discussed, there is typi-
cally ample opportunity to observe social activity at communal
dens during winter and spring (November through March) or
longer, depending on weather conditions (Repp, 1998; Schuett
et al., 2006).
Genetic relationships at communal dens
Genotypic analyses of C. atrox at the Suizos (Clark et al., 2014)
involved the use of 28 microsatellite markers developed by Hans-
Werner Herrmann and colleagues (Pozarowski et al., 2012). With
these markers we assessed the genetic relationships of individuals
from 7 dierent communal dens that were sampled from March
2001 to December 2010. For this analysis, a grand total of 191
adult C. atrox were genotyped; of these, 46 (19 ♂, 27 ♀) were
being studied using radio-telemetry and 50 were known to oc-
cupy one of 7 dierent communal dens (Schuett et al., 2011,
2013a, b). In an initial analysis, a test for mean genetic related-
ness (R) across all dens was signicant (mean R = 0.0291720, P
< 0.001); however, of the 7 dens, 4 of them had several to many
relatives (half-sibs) and the remaining 3 had no detectable rela-
tives (Schuett et al., 2014; Table 2).
Based on the ubiquitous presence of suitable den sites in the
Suizo Mountains and our preliminary genetic results, selection of
dens appears to be by social choice, kin-based choice, or a com-
bination of the two. Accordingly, we propose that the function of
communal dens in C. atrox, and perhaps in other rattlesnakes of
southern latitudes, is fundamentally dierent from those of high-
er latitudes, where survival appears to be the primary and most
important function of aggregation. Potential studies to exploit
this fact have been described further along in this chapter. At this
point, however, it appears that communal dens of C. atrox at the
Suizos are a mix of kin-based (close relatives, families) groups and
non-kin groups described by low genetic relatedness, but indi-
viduals, nonetheless, are strongly connected and associate during
certain times of year (Mesterton-Gibbons and Dugatkin, 1992;
Emlen, 1994, 1995; Lucas et al., 2005; Clutton-Brock, 2009;
Godfrey et al., 2014). Whether or not rattlesnakes associate as
true families or other type of genetic associations similar to cases
involving lizards remains to be tested (Gardner et al., 2001, 2002,
2015; O’Connor and Shine, 2003, 2006; While et al., 2009).
Quantifying individual mating
and reproductive success
Long-term studies of individual animals in nature contribute dis-
proportionately to our understanding of the principles of ecology
and evolution (Clutton-Brock, 1988; Clutton-Brock and Shel-
don, 2010). Such eld studies can benet greatly from integrat-
ing the methods of molecular genetics with traditional approach-
es. Despite the fact that molecular genetic tools (microsatellite
sequence data) are particularly valuable for investigating species
that are dicult to observe directly, they have not been widely
adopted. We used genotypic methods in a radio-telemetric inves-
tigation of the Western Diamond-backed Rattlesnake (C. atrox)
at the Suizo mountains that spanned 10-years for an analysis of
its mating system and to measure sexual selection. Specically,
we used microsatellite markers to genotype 299 individuals, in-
cluding neonates from litters of focal females, to ascertain parent-
age using full-pedigree likelihood methods (Clark et al., 2014).
We detected high levels of multiple paternity in litters, yet found
little concordance between paternity and observations of court-
ship and mating behavior. Although larger males did not father
signicantly more ospring, we did nd evidence for size-specic
male-mating strategies, with larger males guarding females for
longer periods in the two mating seasons. Furthermore, the spa-
tial proximity of males to mothers was signicantly associated
with greater reproductive success. Overall, our eld observations
alone would have been entirely insucient to quantitatively mea-
sure the mating system of this population of C. atrox. We thus
urge more widespread adoption of molecular tools by eld re-
searchers studying mating systems and sexual selection in snakes.
Bateman gradients, sex dierences, and sexual
Angus J. Bateman (1948) pioneered laboratory studies that were
directed to quantify mating and reproductive metrics to infer the
strength of sexual selection acting on males and females (cf. Dar-
win, 1871). Using fruit ies (Drosophila melanogaster) as a model,
Bateman compared reproductive results for males and females
and concluded that (i) males have higher variance in the number
of mates (mating success), and (ii) males have higher individu-
al variation in the number of ospring produced (reproductive
success); and (iii) the slope of the relationship between mating
and reproductive success is steeper in males; this is the sexual
Genotype results of adult Western Diamond-backed Rattlesnakes (Crotalus atrox) from Den-1 (AD-1) at the Suizo Mountains. Site was sampled from
2001 to 2010. HS = half-sibs. See Clark et al. (2014) and Schuett et al. (2014).
selection or Bateman gradient (cf. Arnold and Duvall, 1994).
ese conclusions constitute Bateman’s Principles (Arnold and
Duvall, 1994; Shuster and Wade, 2003; Jones, 2015). Bateman
explained this variability in mating and reproductive success be-
tween the sexes owing to dierences in gametic investment (an-
isogamy). Most female organisms, relative to males, only have
a few (e.g., 1–100) large gametes (ova); males tend to have mil-
lions of much smaller gametes (spermatozoa). Consequently, in
most species, females are the limiting sex and males compete for
priority-of-access to them (Darwin, 1871; Trivers, 1972; Emlen
and Oring, 1977).
Modern investigators of sexual selection generate mating and
reproductive data to obtain data on sex-specic opportunities
for selection (I), sexual selection (Is), and Bateman gradients
(βss) (Shuster and Wade, 2003). ousands of empirical and
theoretical papers have emerged since Darwin, Bateman, and
Trivers invited us to investigate and measure sexual selection
in males and females (Duvall et al., 1992, 1993; Arnold and
Duvall, 1994; Shuster and Wade, 2003). However, measuring
and interpreting sexual selection is not without controversy and
disagreement. Here, we supply a few recent papers to provide
a cogent background to this lively discussion (Gerlach et al.,
2012; Collet et al., 2014; Apakupakul and Rubenstein, 2015;
Typical animal subjects in sexual selection studies conducted
in nature tend to be large, common, and or easy to measure
(e.g., elephant seals, red deer, shes, and many insects). Mea-
suring sexual selection in small and cryptic organisms can be
dicult, and hence there are few studies on pitvipers and oth-
er snakes (reviewed in Clark et al., 2014; Levine et al., 2015;
Smith et al., 2015). Nonetheless, parentage assignments using
genotypic markers, combined with behavioral observations, al-
low for robust estimation of sexual selection metrics (Levine et
al., 2015; Smith et al., 2015).
Following the protocol used in a recent paper by Levine
et al. (2015) on sexual selection in Copperheads (Agkistrodon
contortrix), including a method in the software package BATE-
MANATER to account for open population bias (Mobley and
Jones, 2012; Jones, 2015), we (G. Schuett, B. Levine, R. Clark,
and R. Repp, unpubl. data) estimated sexual selection in male
and female C. atrox using data generated in Clark et al. (2014).
First, both I and Is were calculated using standard methods (cf.
Arnold and Duvall, 1994) where adult females produced o-
spring (n = 18 litters), and males both did and did not produce
ospring (n = 78). Males: I = 2.95, Is = 2.79. Females: I = 0.32,
Is = 0.28. e F-ratio tests showed male and female estimates
for both parameters to be signicantly dierent from each other
(critical value = 2.00; P < 0.05).
Next, these data were run using BATEMANATER, which
not only corrects for open population bias, but is also sensitive
to sex ratio information, such as the operational sex ratio, OSR
(Emlen and Oring, 1977; Duvall et al., 1992, 1993). We ran
the program with an OSR of 2 males:1 female based on a de-
cade of reproductive research at the Suizo Mountains (Schuett
et al., 2011, 2013a, b; Schuett et al., volume 1, Crotalus atrox).
Our simulation using BATEMANATER was conducted with
a 2:1 sex ratio, only males and females with ospring, and
1000 bootstraps. We found signicant dierences among male
and female estimates for I and Is. Males: I = 1.16 (95% CI:
0.95–1.59), Is = 1.50 (95% CI: 1.27 –1.55). Females: I = 0.32
(95% CI: 0.15–0.52), Is = 0.28 (95% CI: 1.27–1.55). Bateman
gradients were generated and regression slopes were compared
with analysis of covariance (Figure 5). However, we found no
signicant dierence between male and female gradients (AN-
COVA: F-value = 2.95, P = 0.089). Accordingly, in contrast to
our prediction, sexual selection does not seem to be acting more
strongly on males than it is on females in this population of C.
atrox (for similar results in salamanders, see Gopurenko et al.,
2007; Williams and DeWoody, 2009; for birds, see Gerlach et
al., 2012, plus a critique of Bateman gradients and interpreting
sexual selection in females). We agree with Rivas and Burghardt
(2005) that most snake mating systems are best characterized as
being polygynandrous (Shuster and Wade, 2003).
Interestingly, we found that snout-vent length (standardized
SVL) in male C. atrox was not positively correlated with reproduc-
tive success (number of ospring; r2 = 0.001, P = 0.78). is was
similar to results in Clark et al. (2014), but unlike results found by
Levine et al. (2015) with male Copperheads, A. contortrix (Figure
6; see YouTube presentation by Brenna Levine, http://www.you-
tube.com/watch?v=kTdYKo4w9uQ). In our original hypothesis,
we predicted that male body size (> SVL) would be a target for
selection in C. atrox for reasons outlined in Duvall et al. (1992,
1993) and Clark et al. (2014). However, that outcome was
rejected, and we provide several possible explanations for this
result. First, in Amarello et al. (2010), sexual size dimorphism
(SSD) of the Suizo population is not pronounced when com-
pared to other regions in Arizona. Second, two mating sea-
sons, long-term sperm storage by females, and high levels of
multiple paternity, coupled with the likelihood of cryptic fe-
male choice and alternative male reproductive tactics (e.g., small
Figure 5. Sexual selection (Bateman gradients, βss) for adult male (solid
blue line) and adult female (dashed red line) Western Diamond-backed
Rattlesnakes (Crotalus atrox) from the Suizo Mountains (see Clark et
al., 2014; G. Schuett, B. Levine, R. Clark, and R. Repp, unpubl. data.)
is analysis was derived using 78 males and 13 females. Filled blue tri-
angles and open red circles denote males and females, respectively. Both
males and females had statistically signicant (positive) Bateman gradi-
ents (males βss = 1.949: r2= 0.66; P < 0.001; females: βss = 1.518; r2 =
0.34; P < 0.01). However, we found no signicant dierence between
male and female gradients (ANCOVA: F-Value 2.95,P= 0.089). See
text for details.
sneaky males) likely diminish the reproductive inuence of any
one size class of male (see results above). Last, Suizo females have
relatively small litters (µ = 4.3 ospring/litter); consequently, our
sample size may have been too small to produce a signicant re-
sult. Clearly, more work is necessary to gain a better understand-
ing of the relationship between male body size, reproductive suc-
cess, and sexual selection in C. atrox.
Arizona Black Rattlesnake (Crotalus cerberus)
e Arizona Black Rattlesnake (Crotalus cerberus) is a medium-
sized denizen of montane forests in Arizona, and a restricted re-
gion of western New Mexico that borders Arizona (see Davis et
al., volume 1, Crotalus cerberus). Observations made by John M.
Slone on the behavior of C. cerberus at multiple communal dens
and rookeries in central Arizona indicated that this species was a
prime candidate for research on social structure (https://commu-
tantly, Slone’s eld investigations provided a research site where
social interactions of C. cerberus could documented and the im-
petus for one of us (MA) and my colleague (Jerey J. Smith) to
initiate research on their social behavior (Amarello et al., 2011).
Specically, Je and I made frequent and repeated observations
on these snakes to study association patterns and describe the
social structure of several denning groups using association index
and social network analysis methods (Amarello, 2012; M. Ama-
rello and J. Smith, unpubl. data). See Box 4 and Glossary 2.
Background and methods
Similar to other species of rattlesnakes (Klauber, 1956, 1972;
Sexton et al., 1992), C. cerberus will often aggregate annually at
rock structures during fall to escape cold temperatures. Further-
more, these individuals will often remain in aggregations at these
communal dens for days (sometimes even weeks!) on the surface
near the den after emerging in spring (Figure 7). Reproductive
activity (courtship and mating) in C. cerberus occurs during late
summer and early fall; it does not occur in spring, which is a
common pattern in North American pitvipers (Schuett, 1992;
Figure 6. e standardized selection gradient (blue line) for snout-to-
vent length (SVL) of 10 male Copperheads (Agkistrodon contortrix)
was estimated by regressing relative tness data on standardized SVL
measurements. Relative tness was calculated by dividing individual
reproductive success by mean male reproductive success. e SVL mea-
surements were standardized to have a mean equal to zero and a stan-
dard deviation equal to one. Filled triangles denote males. A signicant
selection gradient on male SVL was detected (r2 = 0.50; P = 0.023).
Box 4. Social network analysis
Social structure can be dened as the pattern of relationships among individuals, which are dened by the quality and pattern of associations among
individuals (Wilson, 1975; Hinde, 1976; Whitehead, 2008; Sih et al., 2009). Social structure of organisms is important because it aects many aspects
of population biology, including mating systems, dispersal, and movements (Wilson, 1975; Couzin, 2006; Whitehead, 2008; Kelley et al., 2011). us,
detailed observations of individuals and associations among them are vital to understanding species social structure and many other aspects of their
ecology (Wilson, 1975; Croft et al., 2008; Whitehead, 2008; Clutton-Brock and Sheldon, 2010).
In squamate reptiles (lizards and snakes), detailed observations of associations among individuals have been primarily limited to several lineages of
lizards. ese studies have revealed a variety of social structures, including polygynous family group-living and monogamous pair-living (Chapple,
2003; Davis et al., 2011; McAlpin et al., 2011). With few exceptions (Clark, 2006), most studies of snake behavior and ecology in the wild have been
conducted using mark-recapture or radio-telemetry (Fitch, 1987; Clark, 2006; Brown et al., 2007; Dorcas and Willson, 2009; Schuett et al., 2011). In
mark-recapture, a large proportion of the population is sampled, but repeated observations of individuals are infrequent due to the diculty of locat-
ing individuals owing to their secretive nature (Dorcas and Willson, 2009). Alternatively, radio-telemetry provides the opportunity for more frequent,
repeated observations, but is generally feasible for only a small proportion of the population, because of the costly nature (both time and money) of
this technique (Dorcas and Willson, 2009).
A social network is a graphical representation of a group’s social structure. Social Network Analysis describes the population as a whole while account-
ing for the lack of independence among associating individuals within the population (Croft et al., 2008; Leu et al., 2010; Kelley et al., 2011; Krause
et al., 2015). Animal interaction network is a suitable alternative name (Krause et al., 2015). A desirable feature of the network paradigm is that it is a
single conceptual framework with which social organization of animals can be studied at all levels and for all types of interactions. For example, inter-
actions between individuals generate a social environment at the population level which in turn selects for behavioral strategies at the individual level
(Krause et al., 2015). Social network analysis has been used to describe social structure of primates (Ramos-Fernández et al., 2009), cetaceans (Gero et
al., 2005; Lusseau et al., 2006), bats (Vonhof et al., 2004; Kerth and van Schaik, 2012), birds (Oh and Badyaev, 2010), lizards (Leu et al., 2010), and
sh (Croft et al., 2004; Kelley et al., 2011). Amarello (2012) and M. Amarello and J. Smith (unpubl. data) used AI to construct a weighted, undirected
social network for two rattlesnake (C. cerberus) communities (MC and ATR, see below; Croft et al., 2008; Whitehead, 2008).
Aldridge and Duvall, 2002; Graham et al., 2008; Amarello,
2012; M. Amarello and J. Smith, unpubl. data). From early
April to mid-May, individuals of C. cerberus emerge each day
from communal shelters, adjacent to communal basking sites,
aggregate in relatively small areas, and return to their shelters at
night, probably to avoid cool temperatures and predators (Sex-
ton et al., 1992).
Acquaintances: a dyad that was observed together at least once,
but were not preferred associates (sensu Gero et al., 2005).
Associated: a dyad observed within a specied dimension, e.g.,
body length (≤ 1 m) of each other (Whitehead, 2008; Ramos-
Fernández et al., 2009).
Association index (AI): an estimate of the proportion of time
each dyad is together, which permits the comparison of rela-
tionship strength among dyads within a population (Cairns and
Schwager, 1987; Whitehead, 2008). ere are multiple methods
to calculate AIs which can help correct biases in the data or ex-
clude demographic eects (Whitehead, 2008).
Association strength: metric of individual - individual connec-
tions in a social network; it incorporates both the number and
strength of associations for each individual (Croft et al., 2008;
Attribute data: data that describe properties of individual nodes.
Binary network: a network in which the edges carry no weight.
Community: a group where most individuals associate with
each other and rarely with individuals from other communities
Degree: the number of edges joined to a node.
Dyad: a pair of individuals.
Edge: a line between two nodes and represents an association or
Gambit of the group: animals are assumed to be associating if
they are found in the same group.
Network: a collection of nodes connected by edges.
Node: each object in a network, such as an individual snake.
Preferred associates: a dyad whose association index is more
than twice the mean (excluding zero values) of randomized AI,
(Gero et al., 2005; Whitehead, 2008). is threshold value ap-
proximates twice the expected value if individuals were associat-
ing randomly (Whitehead, 2008).
Randomization test: a method of testing network structure sta-
tistically by randomizing node labels, edge labels, or some other
feature of the dataset.
Regular network: a network in which every node has the same
Spring embedding: a visualization algorithm of the network lay-
out (Krause et al., 2009)
Undirected network: a network in which the relations are all, or
are assumed to be, un-reciprocated.
Weighted social network: asocial network based on association
indices or interaction rates, rather than presence or absence of
associations or interactions (Croft et al., 2008; Whitehead 2008;
Krause et al., 2015).
We studied C. cerberus at a site with abundant isolated gran-
ite outcrops at the interface of Petran Montane Conifer Forest
and Interior Chaparral (Brown, 1994); elevation is 1850 m (asl).
Several basking sites were used by C. cerberus after they emerged
from their den in early April until mid-May. ese sites, with sur-
face areas of 15–48 m2, were adjacent to outcrops that presum-
ably contained their winter dens. Five basking sites (= MC) were
located within 20 m of each other on one side of a heavily used
dirt road and multipurpose trail; two additional basking sites (=
ATR) were located several meters apart across the road and trail
(~350 m from MC site). Although the area between these two
basking communities has additional rocky outcrops that appear
capable of supporting C. cerberus aggregations, extensive searches
(2009–2012) failed to locate additional basking sites.
At these communal basking sites, we used opportunistic
observations (point-sampling) and remote time-lapse cameras
(Timelapse PlantCam and TimelapseCam 8.0, Wingscapes, Inc.,
Alabaster, Alabama, USA) to record semi-continuous behavioral
observations of C. cerberus (see Amarello et al., 2011; Amarello,
2012; M. Amarello and J. Smith, unpubl. data). Additional de-
tails on the study site, snake identi cation, and data extraction
can be found in Amarello (2012). Two techniques novel to be-
havior research of snakes to analyze observations were used: as-
sociation index analysis (Whitehead, 2008, Ramos-Fernández
Figure 7. Arizona Black Rattlesnakes (Crotalus cerberus) at or near dens
communally basking, which includes adults with neonates and juve-
niles, Yavapai County, Arizona. Photos (a-b) by John M. Slone. Photo
(c) by Martin J. Feldner.
et al., 2009; Kelley et al., 2011; Krause et al., 2015) and social
network analysis (Croft et al., 2004, 2008; Ramos-Fernández et
al., 2009; Kelley et al., 2011; Krause et al., 2015).
Association index analysis
Association indices (AI) estimate the proportion of time each dyad
(two individuals) spends together, which permits comparison of re-
lationship strength among dyads within a population (Cairns and
Schwager, 1987; Whitehead, 2008, 2009). e simplest AI divides
the number of times a dyad was observed together by the total
number of times either individual was observed (0 = never associ-
ated; 1 = always associated). Amarello (2012; M. Amarello and J.
Smith, unpubl. data) used the half-weight AI, which is less biased
when some individuals within a group cannot be identied (Cairns
and Schwager, 1987; Whitehead, 2008). ese indices have been
used to distinguish between random associations (e.g., mutual at-
traction to a physical resource; see Gillingham, 1987; Graves and
Duvall, 1995) and non-random associations in lizards (Leu et al.,
2010), primates (Ramos-Fernández et al., 2009), cetaceans (Gero
et al., 2005; Lusseau et al., 2006), bats (Vonhof et al., 2004), and
sh (Kelley et al., 2011). Additionally, AI can be used to construct
weighted social networks (Croft et al., 2008; Whitehead, 2008;
Kelley et al., 2011; M. Amarello and J. Smith, unpubl. data).
When individuals are selective about whom they associate with
(i.e., there are individuals avoided and or individuals with whom
they select to be in association), then variation in AI (CV: coe-
cient of variation) will be greater for observed than random (White-
head, 2008). If individuals are not selective about their associates,
then variation in AI will not dier between observed and random
data (Whitehead, 2008, 2009). To test for nonrandom patterns of
association in C. cerberus, M. Amarello and J. Smith (unpubl. data)
used a permutation test which shues group membership within
sampling periods to generate a random distribution of data (Bejder
et al., 1998); this procedure accounts for demographic eects in-
cluding individuals entering and leaving sites throughout the study
(Gero et al., 2005; Whitehead, 2008). For these permutation tests,
P values indicate the proportion of permuted data that were less
variable than the observed data, thus at the 0.05 level, P < 0.025
and P > 0.975 are considered signicantly dierent than random
expectation. e dyads that were identied were classied as ac-
quaintances, preferred associates, or never observed together (AI
= 0). Association index analysis was conducted in SOCPROG 2.4
(Whitehead, 2009), weighted, undirected social networks based
on association indices for each rattlesnake community were cre-
ated with NetDraw 2.121 (Borgatti, 2002), and all other graph-
ics were created in the R statistical package (R Foundation for
Statistical Computing, 2011) with ggplot2 (Wickham, 2009).
Results of social network analysis
We found that individuals were selective concerning their asso-
ciations. Observed variation in AI was signicantly greater than
random data at site MC (n = 4005 possible dyads, observed CV
= 4.33, random CV = 2.85, P = 0.999) and site ATR (n = 136,
observed CV = 1.93, random CV = 1.32, P = 0.999). At both
sites, male-male (MC: n = 78, observed CV = 1.96, random CV =
1.70, P = 0.999; ATR: n = 21, observed CV = 1.14, random CV =
0.77, P = 0.999), female-juvenile (MC: n = 2926, observed CV =
4.51, random CV = 3.05, P > 0.999; ATR: n = 45, observed CV =
2.73, random CV = 1.53, P = 0.997), female-male (MC: n = 630,
observed CV = 2.97, random CV = 2.42, P = 0.999; ATR: n = 45,
observed CV = 2.39, random CV = 1.75, P > 0.999), juvenile-
male (MC: n = 2211, observed CV = 4.38, random CV = 3.52, P
= 0.999; ATR: n = 91, observed CV = 1.86, random CV = 1.52, P
= 0.999) dyads and at MC female-female (n = 253, observed CV
= 2.75, random CV = 1.63, P = 0.999), and juvenile-juvenile (n =
1431, observed CV = 5.58, random CV = 3.96, P = 0.999) dyads
were selective about their associates (Figure 8). Only female-female
(n = 3, observed CV = 1.55, random CV = 1.55, P = 0.46) and
juvenile-juvenile (n = 21, observed CV = 2.76, random CV = 2.68,
P = 0.776) dyads at ATR were not selective about their associates
Adult female C. cerberus were more likely to form preferred
associations with each other (2.3% of all possible female-female
dyads; Figure 9) than with juveniles (0.6% of possible female-ju-
venile dyads) or males (0.3% of possible female-male dyads; Fig-
ure 10, Table 3). Despite the fact that 30.3% of male-male dyads
were acquaintances, none formed preferred associations (Figure
11, Table 3). Juveniles were more likely to have never associated
with each other (95.8% of possible juvenile-juvenile dyads) than
with females (93.7% of possible female-juvenile dyads) or with
males (92.5% of possible male-juvenile dyads).
Figure 8. Visualization of social networks for Arizona Black Rattle-
snakes (Crotalus cerberus) using spring-embedding layout. Left image
is MC research site. Right image is ATR research site. Associations are
represented by lines between nodes (nodes = individuals), weighted so
that stronger associations are heavier lines. Node color and size depict
individual attributes. Color indicates demographic group (orange = fe-
male; blue = male; gray = juvenile; no sex provided). Size indicates as-
sociation strength. Disconnected nodes represent individuals that never
were observed to be in association with a conspecic.
Figure 9. Two adult female Arizona Black Rattlesnakes (Crotalus cer-
berus) that were scored as preferred associates (i.e., they were observed
in association more than twice as often as expected against a random
model; see Glossary 2). is particular pair had an association index
(AI) of 0.57, and the random expectation for this community (= MC)
was 0.22 (Cairns and Schwager, 1987; Whitehead 2008). Photo by
Social network analysis: using spatial
Social networks also can be constructed using temporal data
(Psorakis et al., 2015) and spatial data, such as home range es-
timates (Formica et al., 2010; Godfrey et al., 2013. Amarello
and colleagues (M. Amarello, G. Schuett, R. Clark, and R Repp,
unpubl. data) used a pairwise matrix of average home range
overlap (see Clark et al., 2014 for details on this spatial calcula-
tion) to construct a weighted, undirected social network of the
Arizona population (Suizo Mountains) of Western Diamond-
backed Rattlesnakes (Crotalus atrox) discussed above. Spatial data
Figure 10. Observed variation (orange) in association indices (AI) for Ari-
zona Black Rattlesnakes (Crotalus cerberus) was signicantly greater than
random data (gray) overall and for all dyad types at MC location (a) and
overall and for all dyad types except female-female and juvenile-juvenile
dyads at ATR location (b). See text for statistical results.
Figure 11. Distribution of proportion of dyads that were preferred as-
sociates (orange; observed in association more than twice as often as
expected if snakes associated randomly) and acquaintances (blue; ob-
served in association at least once, but not as often as preferred associ-
ates). Most (93%) dyads were never observed together.
on all individuals can be viewed at Google Earth (http://www.
copperheadinstitute.org/#!atrox-plos-one-data-set/c1j6c) at e
Copperhead Institute. A single community was identied with
a network density of 0.08, six subgroups (Q = 0.115), and no
disconnected individuals (Figure 12).
Dierences in association strength were not signicant (in
this case, total home range overlap) between 27 adult females
and 19 adult males (females: mean ± SD = 4.34 ± 2.52, range
= 0.54–10.08, n = 27; males: 2.97 ± 2.12, range = 0.39–7.14,
n = 19; 2-tailed P = 0.067). e probability that any male and
female associated was not signicant (probability of association
= 0.078). However, males were less likely to associate with each
other (probability of association = 0.048, P = 0.039) and females
were more likely to associate with each other (probability of as-
sociation = 0.110, P = 0.054).
In future work with our C. atrox dataset, we will investigate
whether genetic relatedness explains the strength of the relation-
ships in this network (see Clark et al., 2014, for genetic infor-
mation). For example, a social network of the Australian scincid
called the Sleepy Lizard (Tiliqua rugosa) is structured by strong-
ly connected individuals yet low genetic relatedness, which is
thought to avoid inbreeding and aggressive behavior toward rela-
tives (Godfrey et al., 2013, 2014).
Proportion of demographic dyads in Arizona Black Rattlesnakes
(Crotalus cerberus) that were identied as preferred associates (Pa),
acquaintances (Aq) or never associated (Na). FF = adult female-
female, FJ = female-juvenile, JJ = juvenile-juvenile, MJ = male-
juvenile, MM = adult male-male, and FM = adult female-male.
See text for details.
Figure 12. Visualization of the social network constructed for Western
Diamond-backed Rattlesnakes (Crotalus atrox) using spring-embed-
ding layout (Croft et al., 2008; Krause et al., 2009). Associations are
represented by lines between nodes (individuals) and weighted so that
stronger associations are denoted by heavier lines (Glossary 2). Node
color indicates the subgroup to which a particular individual belongs (6
groups; Q = 0.115). Node shape and size depicts individual attributes:
shape indicates sex (circles = males; squares = females) and size indicates
an individual’s association strength.
Social behavior of rattlesnakes:
conclusions and future directions
We have highlighted some of the problems and deciencies in the
study of social behavior of snakes, and several productive ways were
identied to ameliorate them. e rst step is to understand our own
shortfalls. We need to see the elephant in the room. Stasis in the study
of sociality of snakes is not simply the product of innocuous igno-
rance or unintentional (perceptual) blindness. We have real concep-
tual problems that almost require ushering in some form of “academic
therapy” on a large scale (see Koestler, 1978, for parallel problems in
other aspects of society). Most informed researchers likely agree that
we have just begun to scratch the surface concerning sociality in rattle-
snakes and other snake species. Perhaps, we have re-shaped perspec-
tives and dissolved some biases and prejudice. Unfortunately, there
are too few studies and researchers working on these problems. Only
a handful of brave souls and their studies have led us out of ignorance
and opened doors to a brave new world of the lives of snakes.
Various authors have addressed so-called grand challenges in or-
ganismal biology (reviewed by Schwenk et al., 2009; Padilla et al.,
2014). We do not disagree with their assessments or the identi-
cation of future challenges, such as synthesis. However, there has
been little emphasis (or discussion) on particular organisms (or lin-
eages) for which information is scarce. Furthermore, there has been
less emphasis on behavior of individuals. We thus propose that a
grand challenge in biology is gaining a greater understanding of
the sociobiology and culture of snakes (cf. Taborsky et al., 2015).
Where do we go from here?
With a slight congratulatory pat on our backs, we achieved what
was once thought to be unachievable in the days of Laurence Klau-
ber – learning the secret lives of snakes without major disturbance
or harm. Since Klauber, miniaturized radio-telemetry has provided
valuable data to understand spatial ecology (Dorcas and Willson,
2009; see Beaupre, this volume, Monitoring Technologies), we
regularly use passive integrated transponders (PIT-tags) to identify
individuals (Gibbons and Andrews, 2004), and powerful DNA-
based tools have been developed to robustly explore population
genetics, relationships, and produce reliable pedigrees (Gibbs and
Weatherhead, 2001; Clark et al., 2014; Levine et al., 2015, 2016;
Shield et al., this volume, Genomics).
Potential research topics to explore
As indicated throughout this chapter, we have a long road to hoe
before gaining a robust synthesis of sociality in snakes. Nonethe-
less, we have the beginnings of a rm foundation, and a rich body
of work by other researchers who study a wide range of other or-
ganisms to act as a source of inspiration and guidance. We do
not have to re-invent the entire wheel. Physical tools aside (i.e.,
radio-transmitters, DNA-based methods for improved genotyp-
ing, software), the most important changes will involve: (1) in-
terpreting observation-based studies of individuals with new per-
spectives within a critical anthropomorphic framework (Rivas and
Burghardt, 2001, 2002; Doody et al., 2013), and (2) designing
experiments that provide the appropriate context and relevance for
the subjects under study, such as rattlesnakes (Dugatkin, 2009).
In the ve examples below, we assume the researcher has access to
basic and key instrumentation (e.g., radio-telemetry, motion-sensor
cameras, remote time-lapse cameras, eld glasses, weather stations;
see Dorcas and Willson, 2009; Beaupre, this volume, Monitoring
Technologies), and a laboratory equipped for genotyping individu-
als and performing computational analyses of sequence data to de-
velop and understand populations genetics and both shallow- and
deep pedigrees (Clark et al., 2014; Levine et al., 2015, 2016).
Watching individuals at dens: documenting cultural transmission (local
enhancement, eavesdropping, copying, bystander eects, social networks,
and lek-like behavior)
Published studies involving long-term observations of individual
rattlesnakes at dens are rare; detailed information on the behavior
of individuals is limited to several studies (see Amarello, 2012).
Our own research on Crotalus atrox is long-term (> 10 years) and
detailed, including genotyping information, but the methods we
used, more-or-less, are reminiscent of point-sampling; continuous
(highly frequent) observations of individuals was limited (Schuett
et al., 2011, 2013a, b, 2014; Clark et al., 2014). As described above,
thus far we have been able to construct a social network of C. atrox
using only home range and home range overlap data, but not by di-
rect observation methods (M. Amarello, G. Schuett, R. Clark, and
R. Repp, unpubl. data).
Here, in the rst example, we discuss the utility of observing
rattlesnakes at dens to investigate culture and cultural transmis-
sion (e.g., local enhancement, public information, eavesdropping,
copying, and bystander eects). Cultural transmission is a power-
ful force in evolution; Dugatkin (2009, p. 162) dened it as “…a
system of information transfer that aects an individual’s pheno-
type by means of either teaching or some form of social learning”
(cf. Boyd and Richerson, 1985). Because we take the approach of
critical anthropomorphism (crotalomorphism), we make a priori
assumptions that cultural transmission occurs in rattlesnakes and
their cultures can sometimes be kin-based (Clark, 2004; Clark et
al., 2012, 2014; Schuett et al., 2014).
As we have discussed, social networks emerge and are useful
to address a variety of evolutionary questions, from mate choice
and social dominance to migration and disease transmission
(Dugatkin, 1999; Bull, 2000; Bull et al., 2001, 2012; Fenner et
al., 2011). Other social learning behaviors that might emerge,
based on studies of other vertebrates, include conditional co-
operation and cheating (Earley and Dugatkin, 2002, 2003;
Dugatkin, 2009; Earley, 2010). Finally, personalities of indi-
viduals (e.g., boldness, curiosity, and persistence) inuence cul-
tural transmission and how social networks develop. Ultimately,
understanding the adaptive features of dierent personalities is
key, albeit a dicult task (Nicolaus et al., 2012). e ecology
of individual dierences and animal personality is reviewed by
Gosling (2001), Réale (2007), Stamps and Groothuis (2010),
Dall et al., (2012), and Wolf and Weissing (2012). See Sih et
al. (2004a, b) for a review of behavioral syndromes, as well as
similarities and dierences between the concepts of behavioral
syndrome and personality.
Research on cultural transmission is a rich area for exploration
of the social systems of rattlesnakes that exhibit communal den-
ning, particularly in taxa that tend to linger at these specic sites
(or nearby areas) in spring to nd mates and copulate, or to use
dens as refugia beyond the period of winter (Table 1; see Schuett et
al., volume 1, Crotalus atrox). For example, in adult Crotalus atrox
that exhibit communal denning at the Suzio Mountains, emer-
gence is in spring (March–April), and egress occurs in step-wise
fashion, sometimes taking up to a month or more before all den
members initiate long-distance (1–1.5 km) spring migrations to
feeding areas (= home range). e number of adult C. atrox ranges
from 2 to 12, with a sex ratio that is typically male biased at least
4:1 (Repp and Schuett, unpubl. data). During the period of linger-
ing, basking, mate-guarding (several forms), male combat (dyadic
ghts), courtship, coitus and other behaviors, to various degrees,
occur on a daily basis weather permitting (Repp, 1998; Repp and
ese activities provide a robust “natural laboratory” to conduct
extensive observations (e.g., watching, video) of wild snakes (e.g.,
Amarello, 2012; M. Amarello and J. Smith, unpubl. data) and op-
portunities for experimentation (e.g., removal or addition of den
members, other manipulations). To a large extent, it is self-evident
that bystanders aect (and are aected by) social interactions (e.g.,
dyadic male ghts) that occur within their social environment
(Earley and Dugatkin, 2002). An audience eect is operating when
individuals engage in agonistic ghts and change their behavior in
the presence of a bystander (e.g., receptive female). However, eaves-
dropping is operating when a male watches a ght and his own be-
havior may be modied in subsequent social situations (Earley and
Dugatkin, 2002). Eavesdropping can provide useful information
on the ghting ability of a conspecic without the eavesdropper
himself engaging in direct combat (Earley and Dugatkin, 2002;
Dugatkin, 2009). It is also possible that a male rattlesnake can ex-
tract the ghting ability of conspecics by watching solitary indi-
viduals, and if a ghting disadvantage is perceived, the observing
male might make decisions that include not to engage in ghts
with that particular individual (Earley et al., 2003, 2005). Accord-
ingly, in cases which involve contestants (dyad) and a bystander,
these interactions carry the potential to lead to the formation of a
complicated social communication network that may involve nu-
merous individuals in large populations (McGregor, 2005). Last,
we will discuss in another publication that C. atrox has exhibited
lek-like behavior on multiple occasions at our Suizo site (R. Repp
and G. Schuett, unpubl. data). In these cases, adult females visited
dens in spring that were not used by them but known to have many
males (and none or few females). In this case, not only is there sex-
role reversal in who pursues who in courtship, but a new category
added to the mating system for snakes (Duvall et al., 1992, 1993;
Shuster and Wade, 2003). Lek systems appear to be rare in reptiles
(Partecke et al., 2002; Shuster and Wade, 2003; Dugatkin, 2009)
and relatively common in other vertebrates, including amphibians.
Watching individuals at dens: male mate-guarding and dominance
Previous work in Arizona during the 1990s (O’Leile et al., 1994)
and current work at the Suizo Mountains (Repp and Schuett,
2008; R. Repp and G. Schuett, unpubl. data) on the Western
Diamond-backed Rattlesnake (C. atrox) has shown that males use
alternative tactics to guard and defend mates. Repp (1998) de-
scribed male combat in C. atrox from southern Arizona in spring
(March–April), which occurs at or nearby communal dens (see
below). Laboratory research on C. atrox (Gillingham et al., 1983)
and other North American pitvipers (Schuett, 1997) has demon-
strated that in physical bouts, which last minutes to hours, win-
ners often gain priority-of-access to mates.
Alternatively, a male may act as a “sentinel” and guard mul-
tiple females at a communal den (Box 5), a behavior that may be
more common than previously known. Roger Repp and Gordon
Schuett (unpubl. data) have only witnessed this in large males. Fi-
nally, Jack O’Leile and colleagues (O’Leile et al., 1994) described
a novel form of mate-guarding behavior by male C. atrox that he
termed “stacking” (Schuett et al., volume 1, Crotalus atrox). is
behavior in C. atrox appears to only occur at or near communal
dens during the spring mating season (R. Repp and G. Schuett,
Watching individuals: parental care and ospring development
Our knowledge of parental care in snakes has grown substantially
over the past 20 years (reviewed by Gillingham, 1987; Shine,
1988; see Somma, 2003), especially with the landmark chap-
ter by Greene and colleagues (Greene et al., 2002). Once highly
doubted and scoed, especially concerning care of newborns, pa-
rental care in snakes is approached and studied today with vigor
and enthusiasm. Pitvipers (Greene et al., 2002; Reiserer et al.,
2008; Amarello et al., 2011; Hoss, 2013; Hoss and Clark, 2014;
Hoss et al., 2014, 2015), and pythons (Stahlschmidt et al., 2008;
Brashears and DeNardo, 2012) are the primary snake subjects
used in recent experimental studies. With a few exceptions (Ama-
rello et al., 2011; R. Repp and G. Schuett, unpubl. data), there
are no long-term studies of maternal care in wild rattlesnakes.
More details are required on parental behavior of wild indi-
viduals using continuous sampling, opportunistic observations
(point-sampling), and remote time-lapse cameras. In several spe-
cies of rattlesnakes, birth occurs close to winter dens (Graves and
Duvall, 1995; Greene et al., 2002; Amarello et al., 2011; Davis
et al., volume 1, Crotalus cerberus). In these cases, radio-teleme-
try may not have to be used. In C. atrox at the Suizos, however,
communal dens are never used as birth sites (nests), and birth-
ing mostly occurs in small mammal burrows or packrat middens
within summer home ranges (Schuett et al., volume 1, Crotalus
atrox; R. Repp and G. Schuett, unpubl. data); use of radio-telem-
etry is a necessity in this case.
We envision a series of observations and experimental ma-
nipulations that can be made studying pregnancy, birthing, and
parental care of rattlesnakes in situ. e work of Greene et al.
(2002) and Hoss and colleagues (Hoss, 2013; Hoss and Clark,
2014; Hoss et al., 2014, 2015) should be performed with wild
subjects using slightly dierent methods; for example, we would
manipulate sheds of ospring and the ospring themselves (e.g.,
During the winter of 1995–96, I was approached by Oxford Scientic Film Company with an inquiry about the possibility of lming combat and
mating behaviors of Crotalus atrox. While such behaviors are normally staged with captive animals, neither they nor I could nd anybody keeping
them at that time. ey were told that lming these behaviors in the wild was possible, provided that certain protocols were followed. Also, the crew
was suciently interested to at least explore several communal dens under our watch. Once they saw what we had—they were listening intently to a
plan I laid out.
e aggregate den that they wisely chose to lm carries the moniker “Ron’s Den” (Repp, 1998, p. 54), named in honor of a friend of mine, Ron Harris,
who is a hunter. Ron found this particular den during the Javelina hunt in February 1995. Rather than blasting bloody geysers through the mass of
diamondback rattlers basking that day, as many hunters might have done, Ron made a mental note to inform me of this den’s location. To his credit,
he left the den in peace, rather than pieces, and gave me some rough directions to its whereabouts.
Ron’s Den was not an easy place to nd, but on 19 March 1995, two close pals of mine and I eventually stumbled onto it. We were told to look for a
mighty Saguaro that stood alone in an area that has few of these majestic cactus, make a left turn, then immediately seek rocks that look like cement.
Once we located the “Lone Saguaro” we made that critical left turn, and the cement-like rocks (caliche) were discovered. At our approach, a large (~1.2
m total length) male Crotalus atrox reacted to our presence by slithering a distance of about 2 meters in front of a gash-like entrance at the base of these
cement boulders. Rather than retreat into the gash, he settled on top of a pile of several other smaller atrox that were just outside the west edge of the
gash. And then, all action froze as we quietly took some photographs and moved on. Without realizing it, we had our rst look at the supreme alpha
male (sentinel) male of this den, who would one day earn the name of “Tyson.” e name needs no explanation.
It thus came to pass that several of the cinematographers positioned themselves at Ron’s Den, assuming the appropriate angles to maximize lming
while minimizing their presence. ey remained patiently at their post for an entire week. I insisted that they choose several days to lm either side of
19 March, as experience had taught me this was the Holy Grail period where one cannot fail to witness courtship, mating, and sometimes male combat.
At the end of their stay, they edited the lm down to 30 minutes and invited me to watch their snake show.
e crew lmed mating activity in C. atrox that was so graphic the lm crew should have been arrested for showing it to me! eir combat segments
were rather lackluster, but enough to make the big screen for a National Geographic special titled, “Sonoran Desert, a Violent Eden.” Needless to say, I
Box 5. Tail signaling in Crotalus atrox
watched that half-hour screening of Ron’s Den with full enthusiasm. rough it all, the male atrox we named Tyson commanded center stage. He was
omnipresent, in nearly every frame, and always on the move. He was alert and aggressively took note of every nook, cranny, and snake on his turf. He
appeared to have complete command of his world (Figure 13).
To be sure, there was mating and ghting, but that
is not what got me out of my chair. What truly
piqued my attention was the intense tail waving
that transpired. In one sequence, Tyson was inves-
tigating (rapid tongue icking) a cluster of about
15 adult conspecics. As he crawls on top of the
pile, four tails immediately rose out and began
waving back-and-forth in sinusoidal fashion, not
unlike caudal luring. Similar behavior occurs in
male copperheads during dominant-subordinate
episodes or bouts (Schuett, 1997). Tyson zeroed
in on one of those tails and used his snout to push
and extract the snake that owned it. It turns out
this other snake was a male, but not quite as big
as Tyson. e excellent footage clearly showed that
his rattles were tapered and complete—a younger
snake, perhaps an “upstart” at Ron’s Den. Once
Upstart caught wind he was noticed by Tyson, he
rapidly ed the pile, heading downslope and jet-
ting toward a sandy wash positioned south of the cement-like rocks. Male dominance was clearly exhibited without sparring in outright combat with
neck-to-neck vertical postures (see Schuett et al., volume 1, Crotalus atrox).
Box 5. Continued
Figure 13. Large male Western Diamond-backed Rattlesnakes (Crotalus atrox) named “Tyson” on
top of a group of C. atrox in front of Ron’s Den (see Repp, 1998). Note that the head of an adult
female is poking out from beneath the lower body of another rattlesnake. Photo by Roger A. Repp.
Now, I’m out of my chair, exclaiming “Whoa, can we rewind that?” One of the three lm crew members asked me, “Is that tail-waving a sign of sub-
mission?” I had to admit that I had never seen that behavior before, but submission certainly seemed a likely explanation.
During the entire mini-production there were several other episodes of tail-waving, which we now call tail signaling. Unfortunately, this lm ended up
on the cutting room oor and discarded. e lm crew was paid to produce a special that was not concerned with anything but what the producers
wanted. ey wanted combat and mating, period. ey got both and the rest is history.
On 20 March 1998, I was once again viewing Tyson at Ron’s Den. He was coiled on top of a group of several other atrox at the eastern-most entrance
to the den. Only the front two-thirds of his body were visible. e rear third of his body was buried and groping into the cluster beneath him. While
he was doing this, a young, smaller adult male atrox emerged from the depths of the den and coiled beside him. Tyson showed great interest in this
new development and immediately began to chin rub on the coiled form. In almost nonchalant fashion, the new arrival pulled his tail from beneath
his coils, and methodically waved it back and forth. His tail was positioned in such a way that it was directly in front of Tyson’s face. Tyson’s reaction
was swift and erce. He ascended half his body length above the new arrival (~0.6 m) and came crashing back down on him. As Tyson crashed on that
snake the thud was audible—it was a rm smacking. Without further encouragement, the new arrival shot back down into the den, out of sight in one
at second. Tyson gave a limited chase for half a body length, and returned to the cluster of snakes beneath him as if nothing had happened.
What had transpired between these male snakes? e new male settled beside Tyson for unknown reasons. Tyson might have initially sensed this new
arrival was a female, and began to lavish his attention on “her.” By waving his tail at Tyson, the new arrival told Tyson “No, idiot, you got me all wrong.
You can’t mate with me—I’m a male!” Rather than respond with his tail, Tyson used “dominant” body language to let his intentions be known. “Oh,
really … you’re another male? en you better get out of here!” e new male got the message, and o he went. However simple or complex it was,
these two snakes communicated with each other. A message was delivered and received — loud and clear.
As I recollect these tail signaling events, Gordon (G. Schuett), Marty (M. Feldner), and I are positioned and ready to move forward as observers, pho-
tographers, and videographers to further document this behavior. We promise that unused “lm” will never end up on the cutting oor and discarded.
Roger A. Repp
Box 5. Continued
numbers, allo-parenting). Following mothers may require radio-
telemetry (see Beaupre, this volume, Monitoring Technologies).
In the spirit of Davis and Stamps (2004) and others, it would be
especially helpful if we knew the eects of natal experience on new-
born rattlesnakes. Do progeny inherit their mother’s home range,
microhabitat sites, or even winter dens? Are their sex dierences in
acquiring a home range? Do daughters inherit nest sites used by
their mother (Brown and Shine, 2007)?
As we have discussed so far, studies of parental care of snakes
has largely been restricted to maternal care of eggs and newborns
(Greene et al., 2002; Somma, 2003). Biparental care appears to
be absent, but anecdotes of males visiting female rattlesnakes with
litters raise the possibility that males (fathers?) might be involved
in care, however limited (Amarello et al., 2011; O’Connor et al.,
2015). e critical step is to genotype visiting males, moms, and
the newborn snakes they associate with to gain a clearer picture.
Watching individuals at dens: packrats and rattlesnakes
Symbiosis is a powerful driver in evolution (Darwin, 1859; Margulis
and Fester, 1991; Paracer and Ahmadjian, 2000; Futuyma, 2009).
e most common symbiotic relationships studied are mutualism,
commensalism, and parasitism. Other categories of symbiosis also
see Paracer and Ahmadjian, 2000), though are less known. ou-
sands of symbiotic relationships are known, but among our favor-
ite involves the amboyant and colorful Clownshes (Amphiprion
spp.) and their invertebrate hosts, the often equally beautiful Sea
Anemones (Fautin and Allen, 1997). At rst sight these species
appear to be odd bed fellows, but the simple story is they enjoy a
remarkable mutualistic relationship. Sea Anemones oer resident
Clownshes protection from predators via nematocyst-studded
tentacles that harbor venomous stings, and in return the Clown-
shes groom and feed their protector and dangerous host. In many
cases, Clownshes ontogenetically acquire chemical immunity
(development of specic glycoproteins in their epidermal mucus)
from the deadly stings of their host through a “touch ‘n’ go” pro-
cess termed acclimation (Balamurugan et al., 2015). In some cases,
things do not go well for the Clownsh; illness and incomplete ac-
climation make them vulnerable, i.e., stung and consumed by the
Anemone (data gathered from numerous web sites). Not a 100%
sure thing, sh*t happens, but close enough for it to be a good BFF
story in evolution. See Venkataraman et al. (2015) for a good wolf
in sheep’s clothing story.
Roger Repp’s groundbreaking publication (Repp, 1998) on
communal denning in C. atrox was the impetus for the Suizo Proj-
ect. at work has provided a wealth of information on communal
denning in C. atrox that we are still exploring and will keep us
(RR, GS) busy for many years to come. One particularly fascinat-
ing observation that gets almost everyone’s attention is that C. atrox
shares its communal den in winter not only with other reptiles (see
Schuett et al., volume 1, Crotalus atrox), but also a small mamma-
lian denizen of the Sonoran Desert, the White-throated Woodrat
(Neotoma albigularis), or just Packrat (http://animaldiversity.org/
accounts/neotoma_albigula/; also see Betancourt et al., 1990).
Early on in his exploration of communal dens of C. atrox,
Roger observed that the entrances would often be choked with
both fresh and old pads of Teddy Bear Cholla (Cylindropuntia
bigelovii) and other plant materials, but Teddy Bear Cholla
(TBC) was the dominant plant. ese decorations were obvi-
ously not the work of rattlesnakes or tortoises, but rather by
Packrats (Kohl et al., 2014). Roger inspected over 50 commu-
nal dens in southern Arizona used by C. atrox and noted that
they were similarly decorated. Intriguingly, despite the fact
that adult C. atrox in Arizona hunt and feed on a wide variety
rodents (and other vertebrates) from March through Octo-
ber (Repp and Schuett, unpubl. data), Packrats do not appear
to be a common prey item on the menu (see diet analysis in
Schuett et al., volume 1, Crotalus atrox). Roger observed that,
during winter, Packrats and rattlesnakes were sharing com-
munal dens, and the rats appeared none for the worse. Repp
made these almost surreal comments (Repp, 1998, p. 53):
“I have many observations of strange interactions between
Packrats and atrox during the colder months. For example, on
November 25, 1995, a group of six of us saw a Packrat resting
with one of its paws against the anks of a very large atrox. One
week later, on a solo jaunt, I saw what appeared to be the same
rat snuggled against the anks of the same snake. e rat was
sleeping when rst viewed, and only lazily opened one eye when
my light [ashlight] hit it in the face. It does not surprise me that
the snakes do not appear to eat the rats during the colder months.
What does surprise me is the fact that the rats seem to know they
Further on, Roger (p. 55) provides us with several testable hy-
potheses concerning the relationship between Packrats and rattle-
snakes; below is one concerning temperature regulation:
“…there appears to be a true symbiotic relationship between predator
and prey. e predator benets in many ways from this relationship.
e rst and foremost of these is the insulation to the den that the
debris gathered by the rat provides … [Also] body warmth of the rats
may increase the ambient temperature within the den.”
What about the fate of the Packrat? How does it benet from
spending time so close to this potentially deadly companion?
Roger (p. 55) indicated this point by way of example:
“… a large predator, such as a Bobcat or Badger, might think twice
about trying to dig a Packrat out of a [communal den] with atrox!”
To me (GS), Roger’s observations knock it out of the ballpark.
I never fail to mention them when delivering lectures about our
work on communal denning in C. atrox. But there is still so
much that remains unanswered and untested. Perhaps, like the
relationship between Clownshes and Sea Anemones, Packrats
and diamondbacks have made, at least partially, an agreement to
get along in winter to form a mutualistic relationship. Perhaps,
like the Clownsh, Packrats and rattlesnakes experience some
form of acclimation period. We just do not know. Roger and
I rarely call them just rattlesnake dens anymore since so much
more is happening with Packrats and other animals (see You-
Tube piece lmed at the Suizo site; Packrat discussion and a bit
of Packrat behavior is at end of this mini documentary (https://
www.youtube.com/watch?v=QUsFafhR6SA). It is complex and
compelling. e fortress of cholla pads and other sharps that
the Packrat gathers to choke the entrance of their rock crevices
used as communal dens might deter some predators (Kohl et
al., 2015), but clearly it does little to halt the ingress and egress
of large C. atrox. Large C. atrox are often found with numerous
cholla spines penetrating their body; we have not observed this
in neonates and juveniles, which supports our observations that
they do not use communal dens until they attain a certain size
(1 m or greater).
e story of diamondbacks and Packrat relations does not
end with communal denning. It continues to unfold…and
bae us. Repp and Schuett (unpubl. data) have collected un-
equivocal information to show that female C. atrox often use ac-
tive Packrat nests (middens) as birthing sites. ese are not the
rock middens used for communal denning described above, but
rather free-standing ones built of plant materials in the bajada
and desert ats (Figure 14).
Repp and Schuett have observed, on numerous occasions,
rats moving about the middens with mother rattlesnakes and
young tucked away inside. It does not appear that rattlesnakes
are eating or bothering the resident Packrat. In Schuett et al.
(volume 1, Crotalus atrox), Carol Spencer provides dietary data
for C. atrox based on 186 museum specimens from Arizona.
Interestingly, of all these records, nary a one shows that wild
C. atrox consumes Neotoma spp. is is very odd, given that
under captive circumstances C. atrox will eat pre-killed Packrats
(R. Repp, unpubl. data). Despite the fact that we have recently
obtained photographic evidence that young C. atrox in Arizona
consume Neotoma (R. Repp, unpubl. data), the possibility re-
mains that these two species interact in much more complicated
ways than we ever imagined. Oddly, in a fairly recent multi-
authored volume on Packrats (Betancourt et al., 1990), the re-
lationship of Packrat and rattlesnake is never discussed. Accord-
ingly, it is a ripe time to don our proverbial thinking caps and
begin inventing and testing hypotheses.
Figure 14. Packrat midden in area of bajada at the Suizo Mountains.
Photo by Roger A. Repp.
Watching individuals: long-term use of radio-telemetry
Our long-term (15 consecutive years) research on C. atrox at the
Suizos has provided us with a wealth of information about the socio-
spatial structure of this particular population. rough observation
and DNA-based analyses, we are just beginning to understand the
behavior and personalities of individual animals and their social net-
works. However, we make no claims about individuals of C. atrox in
other populations and whether they behave similarly. Much more
work is needed to determine the role of geographic variation.
To conclude this chapter, we provide an example (Box 6. e Sis-
ters) of the utility of watching individuals on a long-term basis with
radio-telemetry and incorporating DNA-based methods to gain in-
formation on social-genetic relationships and pedigrees. In this par-
ticular study of C. atrox, 28 microsatellite markers were used (Clark
et al., 2014) to identify and estimate relationships of 299 individuals
(adults, juveniles, neonates), including 19 adult males and 27 adult
females that were followed using radio-telemetry. is kind of in-
formation has provided our team with invaluable insights that have
helped to shape our view of the complex social lives of rattlesnakes.
is kind of longitudinal approach has worked well with certain
lizard systems. See papers by C. Michael Bull and colleagues (Bull,
2000; Bull et al., 1994, 1998, 2001, 2012) and Stephan T. Leu and
colleagues (Leu et al., 2010, 2011, 2015).
On 15 March 2001, Gordon Schuett and I initiated a multi-spe-
cies radio-telemetric study in the Suizo Mountains, a remote and
mostly pristine swath of Sonoran Desert Upland, roughly 80 km
north of Tucson, Arizona, named the Suizo Project (Schuett et al.,
volume 1, Crotalus atrox). Although we were studying several spe-
cies of venomous reptiles, our primary focus concerned questions
about winter denning in the Western Diamond-backed Rattle-
snake (Crotalus atrox). Our research was hypothesis-driven, but
we kept an open-minded approach to new or interesting behav-
iors unrelated to our original goals. Consequently, new hypoth-
eses were indeed formulated. Some of these could be described
as “hypothesis du jour,” for which later observations would nd
no support. Some hypotheses were solid, substantiated and pub-
lished, and some remain to be tested. After 15 years of observing
and radio-tracking animals at the Suizos, we seem to have the how,
what, and when under control, but often scratch our heads and
speculate over the biggest question – why?
By the end of March 2001, three female C. atrox (Ca) were cap-
tured and fully processed, which included blood samples collected
for subsequent DNA analyses, PIT-tags imbedded, and radio-
transmitters surgically implanted. All three “ladies” were released
at the site of capture. With such fanfare as that, our three subjects
(Ca-1, Ca-2, and Ca-3) entered what would become the longest
running radio-telemetric study involving multiple species of ven-
omous reptiles in the history of Arizona (15 years, ending January
2016). All three female subjects originated from the same denning
Box 6. e Sisters
aggregation (communal den), which was a location that one of us [RR] had been observing since February 1999. Because many dens used by C. atrox are
found at this study site, many of them communal dens, it was designated as Atrox Den Number-1, or “AD-1” for short.
During that important rst season (2001) under our microscope, the three girls revealed to us interesting information about their spatial ecology. For
instance, if they themselves had looked over a topographic map of the Suizos and had agreed to which patch of ground was going to be their own to oc-
cupy, they could not have done a better job of sanctifying discrete home ranges. During egress and migrations in late March 2001, Ca-1 (“Ruth”) jetted
on a straight course to the southeast, Ca-2 (“Dianna”) traveled due west, and Ca-3 (“Patricia”) ventured smack dab between them. Furthermore, when all
spatial data for 2001 were formally analyzed (Clark et al., 2014; to visualize our spatial analyses of these three girls and all other atrox subjects via Google
Earth, go to http://www.copperheadinstitute.org/#!publications/cee5/; go to Publications, see Clark et al., 2014) there was a clear line of demarcation
between home ranges. At times, their spring and summer home ranges (activity area) nearly touched, but overlap never occurred to our knowledge. At a
minimum, it is not reected in our analyses. With our puny N of three, our “hypothesis du jour” was “females that overwinter in a communal situation
are in close contact, but once the active season begins, never the ‘twain shall meet’.” As we will show, this view was supported during the spring and early
summer of 2002, when all three of these females set up for the active season by occupying their previous home ranges.
After a full season of radio-tracking the three girls in 2001, they settled into their overwintering sites by November. Ca-1 and Ca-3 returned to AD-1
(den delity), but Ca-2 found and settled in at another site, about 100 m west of AD-1, which was a midden of a White-throated Wood Rat (Neotoma
albigula) beneath a Palo Verde Tree (Parkinsonia spp.). On 18 May 2002, while tracking Ca-3, a bit of serendipitous foot work led us to a coiled and very
healthy new female C. atrox. She was captured for a radio-transmitter. During a thorough processing that followed, Gordon ascertained that there were
as many as 8 developing ova inside her distended anks. She was named Ca-8, and was back in the eld by early morning on 24 May. We were ecstatic
to add a pregnant female to our study. But Ca-8 was not the only pregnant C. atrox under our watch.
By early May of 2002, Ca-3 was also receiving good health reports. To be sure, we had not yet processed her to ascertain pregnancy, but her ever expand-
ing-anks were beginning to indicate her pregnancy to be a foregone conclusion. On 11 May, she was found buried in a rather unimpressive, at, and
very old stick and bark Packrat midden. Meanwhile, as I mentioned above, Ca-8 was released on the morning of 24 May. By the morning of 25 May,
she had moved roughly 10 m from her capture and subsequent release site. at small move took her directly into the same attened midden that Ca-3
occupied! Both snakes were not visible, but the signals from their radio-transmitters indicated they were close to each other in the center of the midden.
Hence, our hypothesis that female C. atrox avoided each other during the active season was shot down. But the fact that both snakes were pregnant was
Box 6. Continued
not lost on us. We were thrilled at the prospects of watching what would happen with these two girls. Unfortunately, our excitement was short-lived.
On the evening of 3 June, the radio-transmitter for Ca-8 was found on the ground roughly 20 m north of the midden that both snakes had occupied.
In a full panic, I headed for the midden, already knowing the bad news. Indeed, the midden had the tell-tale elliptical hole bored through its center. e
rattle and transmitter of Ca-3 were found in this hole. Both snakes had been killed and likely devoured by a Badger. Gordon and I have observed Badgers
carrying adult atrox.
roughout the remainder of 2002, and up to August 2003, the female C. atrox under our watch once again spent their active seasons in separate home
ranges. Meanwhile, even though we had lost Ca-3 and Ca-8, we had increased our N of females considerably. By August 2003, we were tracking 10 adult
females with radio-transmitters and ve were pregnant. Next, we will focus on the activities of one we named “Sister-1” (female Ca-30).
Before going into detail about Sister-1, it is important to understand the complexities of the landscape she and the other C. atrox occupy at the Suizo
Mountains and surrounding bajada. It is immediately noticeable that there are large numbers of White-throated Wood (Packrat) Rat (Neotoma albigula)
middens, which are commonly associated with clumps of Prickly Pear Cactus (Opuntia engelmannii). Also, there are small mammal burrows (“small
holes”) beneath most Creosotes (Larrea tridentata). Badger (Taxidea taxus) burrows, both old and new, auger their way through the soil beneath Palo
Verde (Parkinsonia spp.) and Ironwood (Olneya tesota) trees. e Suizos contains all the ingredients necessary to be a “Shangri-La” for rattlesnakes. We
always marvel at the seemingly innite number of suitable shelters.
Many species of rattlesnake from temperate climates aggregate to give birth (reviewed in Graves and Duvall, 1995). Moreover, they usually form these
rookeries close to overwintering sites (usually communal dens). e function of female birthing aggregations is complicated and largely untested in snakes
(Graves and Duvall, 1987; 1995), but there is a strong argument that lack of suitable sites for parturition might force them together. Social functions are
far more appealing yet dicult to test (see Schuett et al., volume 1, Crotalus atrox).
To date, everything that we see with C. atrox at the Suizos indicates that they do not form rookeries (aggregations of pregnant female) where they will
give birth (Graves and Duvall, 1995). Most females migrate far (sometimes > 1 km) from their overwintering sites before settling into a suitable site to
give birth (“nest site”). e climate of the Sonoran Desert does not force them to nd a specic place with favorable conditions. As far as we can tell,
one location seems just about as good as the next. With 10 years of radio-tracking 33 female C. atrox, we have never observed two females to give birth
together at the same site. We conclude that C. atrox rookeries do not occur on our turf.
Box 6. Continued
e behavior of pregnant C. atrox diers from most other rattlesnake species. Simply put, they do not just sit around until they give birth (cf. Graves
and Duvall, 1995; Greene et al., 2002). Pregnant C. atrox at our site are constantly on the prowl and actively hunting for their next meal (Schuett et al.,
2011, 2013a). We have robust, though limited evidence, that they will hunt and consume meals when the opportunity presents itself, right up to the day
they give birth.
On 3 August 2003, Sister-1 was highly suspected of being pregnant. Our method for determining pregnancy is simple but has proven highly eective
for us. We gently lift the snake with a hook and or tongs, keeping the head up and the body and tail dangling beneath. With a pregnant individual, the
neonates form a series of conspicuous bulges toward the posterior end of the body. is does not occur with a food bolus or feces. Our “primitive ultra-
sound” method was performed on Sister- 1 at her Site-13, and without “killing a rabbit” we had our ocial diagnosis – she was pregnant.
By 20 August, Sister-1 was at her Site-17, where our observations and subsequent photographs indicated her anks to be distended by a major food bolus.
On 24 August, she was not visible at her Site-18, which was at Creosote that was riddled with small mammal holes at its base. On 28 August, Sister-1’s
signal once again led us to Site-18. We noticed there was a slender adult female C. atrox coiled under the Creosote. She was facing a soil hole (small mam-
mal burrow) in what we now recognize and term “Nest-Watching.” A careful check of Sister-1’s radio signal indicated that this female was not her. is
new snake was captured (female Ca-46), and we moved on to track Sister-1, who on this day was in an old Badger burrow about 30 m from her Site-18.
With regard to the apparent “nest-watching episode” that involved female Ca-46, we revisited Site-1 for Ca-46 (= Site-18 for Sister-1) on 1 September,
and observed three shed skins from newborn C. atrox draped over the lower branches of the Creosote, just above the burrow Ca-46 had been watching
three days earlier. We observed two more neonates inside the burrow (nest) itself. Also, we have evidence that Sister-1 visited female Ca-46 shortly before
CA-46 gave birth. Yet, Sister-1 moved on and was still quite pregnant.
Sister-1 (female Ca-30) was observed at her nest site on 1 September 2003, the same day that we collected shed skins of neonates from the nest of Ca-46.
Next, Sister-1 was at her Site-20, which was an active Packrat midden, stued with the usual oerings of cholla, sticks, bark, a downed Palo Verde branch
in the mix, with towering Creosote to the west edge. Sister-1 was very close to giving birth when she rst visited her Site-20. Late in the evening of 4
September, a large Packrat was viewed prowling above the west edge of the midden at Site-20. (Packrats are often present when C. atrox give birth at the
middens.) Just to the west of the Packrat was a coiled, adult female C. atrox. is was another new snake for us, so she was captured and named Ca-47.
us, “Sister-2” was added to our study.
Box 6. Continued
On 7 September, 3 shed skins of neonates from Sister-1 were collected from deep parts of the midden at her Site-20. One more shed appeared and was
collected on 8 September. Sister-1 moved from Site-20 shortly thereafter. Sister-2 produced three neonates on 12 September, while held in a rather uncer-
emonious laboratory situation. Following her radio-transmitter surgery, she was released on 20 September with her brood at the nest site of Sister-1. Her
three progeny all shed shortly after being released. During the fall and winter of 2003, the two “Sisters” led separate lives. ey did not overwinter together.
Sister 1 remained close to her parturition site in bajada habitat. Sister-2 led us to a new communal den we named AD-7, which continues to thrive to the
time of this writing.
In 2004 and 2005, the Sisters had “o-years” with respect to reproduction. eir movements and activities were like other non-pregnant C. atrox under our
watch. Both females made livings out of very separate home ranges, and were never located by us to be within 100 m of each other. In 2006, they started
the year o in the same isolated fashion. By July of 2006, both snakes were deemed pregnant. On 29 July, Sister-2 began working her way toward the area
of Sister-1, and that day were less than 20 m apart from each other. Was history was about to repeat itself?
On 5 August, the signals from both Sisters indicated that the pair was likely coiled together, buried in a series of soil holes (burrows) beneath a Prickly Pear.
While there was not an obvious Packrat midden to be seen here, scat from Packrats was scattered everywhere—in the holes, and all around the base of the
Prickly Pear. Sister-1 was at her Site-77 and Sister 2 was at her Site-58. In order to keep what follows simple, we will call this Prickly Pear location “Nest
Site 1.” Our next visit to Nest Site 1 was 1 week later on 12 August. On this triumphant morning, we tracked the two sisters and immediately viewed 6
neonates clustered in a southeast facing elliptical soil hole (burrow) on the eastern edge of the Prickly Pear (see Schuett et al., volume 1, Crotalus atrox).
Up to this point, we had not been able to get any good images of newborn C. atrox in a nesting situation. With all previous attempts at photography, the
neonates at other nests quickly bolted out of sight, with no chance for anything but a “quick ‘n’ dirty” photo. On this day, we were able to actually get the
camera into the hole, inches away from them. I nally had to pull the camera out when one of the neonates, a female, unexpectedly charged the camera.
As we backed the lens out, the female neonate came all the way out of the hole, and laid there glowering at us! While all this was transpiring, the two sisters
remained out of sight, the signals indicated they were coiled together 1.5 meters to the south of the neonates. e big question was, “Who is the mother?”
at question was partially answered that evening. I visited Nest Site 1, and as I approached Sister-2 was viewed sprawled outside the nest entrance. She
had obviously lost some mass, but still looked pretty good given the circumstances. She bolted into the nest when I approached. e tell-tale sign was
that neonates began to disperse, two were viewed in the nest entrance and two others were less than 1 m out dangling in Bursage. Finally, two others were
Box 6. Continued
shedding in the center of the Prickly Pear. Sister-1 was not visible under the Prickly Pear, which was about 1 m south of the nest entrance. Whether
she was pregnant or not remained to be determined, but there was certainly no doubt that she had remained with Sister-2 for her parturition —from
birthing to nest egress. Radio-telemetry is a godsend in being a good voyeur.
About 24 hours later, Sister-2 left the nest site and was located about 30 m to the west. Gordon and I located her still moving away from the nest. All
the neonates had cleared, leaving four more shed skins to collect (a source of DNA we used for parentage analyses; see Clark et al., 2014). Sister-1 was
coiled in a hunting posture on open ground just outside the nest site. She was large and still pregnant! e following evening, on 14 August, she was
back at the Prickly Pear shelter of Nest Site 1. Here was the big question: “Will she give birth at Nest Site 1?” e big answer was “no.”
On 19 August, Sister-1 was viewed in an old Badger burrow beneath a Prickly Pear. Whether a coincidence or not, this same Badger hole had been the
nest site of another female atrox (Ca-59) in 2004. Finally, on 20 August, Sister-1 was located at her Site-78, which was a mini-gash soil hole under a
scraggly Prickly Pear. e site was littered with the detritus and scat of a Packrat, which was all beneath the south canopy of a Palo Verde. She could
not have selected a more convenient nest site for us to observe. It was less than 5 m from where we normally park our vehicles. Her kids were probably
born at Nest Site 2 the same day she entered it. By the evening of 26 August, she egressed, leaving behind a glob of seven shed skins of neonates to
add to our ever-burgeoning DNA hopper. During the 6-day period that elapsed between ingress and egress of Nest Site 2, Sister 2 was nowhere close
to the scene. After all, she was no longer pregnant, why would she visit?
Like the meaning of George Harrison’s song, “All ings Must Pass,” so did Sister-1. On 19 May 2007 we found her radio-transmitter buried under a
small, at rock in the bajada between the hill and wash that constitutes the center of her home range. Our impression was that she had been dead for
weeks, and the radio-transmitter had been buried under sandy soil in the center channel of the wash proper. Some “critter” likely found it and placed it
under the rock, roughly 30 m from the site where we found her carcass. Sister-2, on the other hand, was still chugging away; on 25 July 2007, she was
viewed with a food bolus and also deemed pregnant. On that day, she was just entering the northern extent of Sister-1’s former home range.
On 5 August 2007, Sister-2 was tracked to Nest Site 2, the area Sister 1 used as a nest site in 2006. It was here that Sister-2 also gave birth. On the eve-
ning of 14 August, she was observed just outside the exact small mammal burrow (hole in the ground) that Sister-1 had used as her nest the year earlier.
Two shed skins of neonates were collected from that burrow. Two dierent C. atrox using the same burrow for their broods was a new observation for
us; however, it has not been repeated with animals under our watch. at this was by chance or mere coincidence seems to us to be innitesimally small.
Box 6. Continued
We have called females Ca-30 and Ca-47 “sisters” because they were at least half-siblings, sharing the same mom or same father. By the close of 2010, un-
der the guidance of Drs. Rulon Clark, Hans-Werner Herrmann, and Gordon Schuett, all of our blood and shed samples (DNA sources) were analyzed to
answer multiple questions regarding identity, parentage, and pedigree. Using a large number of microsatellite markers (28), which was heavily backed by
10 years of rock-solid data, we have begun to answer those questions. It is more common for snakes that routinely overwinter together to not be closely-
related (e.g., non-kin) than we ever would have guessed (see above). And for those of you who think that seeing a pile of snakes together suggests that they
are close relatives, I would have agreed with you in earlier days before understanding the power of molecular analyses. e bottom line is that while close
relations and family units can be found throughout our C. atrox system, aggregations per se do not indicate close relations. Analysis of DNA sequence data
provided insight that Ca-30 and Ca-47 were at least half-sibs. Our tracking work shows at least 7 other dierent parings of pregnant female C. atrox. e
DNA results of the individuals participating in these “parturition pairings” will likely reveal similar close kinship.
Because I was on the ground for all of this, it is easy to humor myself into thinking that I am the person most qualied to guess at what I was seeing. My
“hypothesis du jour” for the incidents of the sisters is that these two snakes had the reasons, resources, and desire to make it a point to “stay in touch.” ey
might have been born together in the same nest — likely a Packrat midden. ey both beat the odds and survived to adulthood by learning survival tactics
that were repeated throughout their lives. ey came together two times over a three-year period of their life that we know about, and in both cases they
were pregnant when they did. ese visitations were likely part of a pattern in their lives that started with their rst litters. ey might have come together
again in 2007, but death removed Sister-1 from that possibility. Perhaps, Sister-2 chose the next best thing by giving birth at Sister-1’s last nest site. Further-
more, we suggest that, through pheromones and or whatever communicative channels may remain unseen between sibling rattlesnakes, Sister-2 deliberately
inspected the nest site of Sister-1 before giving birth. Perhaps enough of the “chemical ghost” of Sister-1 remained to empower Sister-2 to know this was
the place to give birth. Maybe just the familiarity or “comfort factor” of being in her sister’s chemical milieu made the birthing process easier (cf. Brown
and Shine, 2007). Perhaps, it was the next best thing to being with her for the experience.
Roger A. Repp
Box 6. Continued
is book would not have been possible without the support and
encouragement of Bob and Sheri Ashley, owners of the Chiricahua
Desert Museum (Rodeo, New Mexico) and Eco Publishing. We
owe a large debt of gratitude to many individuals along the way
of our respective careers for thinking boldly, broadly, profoundly,
and transformatively. Our own thinking has undergone meta-
morphosis. In particular, we acknowledge Bayard Brattstrom,
Gordon Burghardt, Jesus Rivas, Steve Arnold, Jim Gillingham,
Fred Kraus, John Porter, and David Duvall. Two of our close col-
leagues and friends, Chuck Carpenter and David Chiszar, passed
while this chapter was in its early stages. We sorely miss them. For
photos, eld assistance, and various other courtesies, we thank
Randall Babb, Mike Cardwell, Dale DeNardo, Frank Deschan-
dol, Marty Feldner, Bob Hansen, Dave Hardy, Sr., Hans-Wer-
ner Herrmann, Shannon Hoss, Bill Love, Erika Nowak, Charlie
Painter, Louis Porras, Diana Repp, Ryan Sawby, John Slone, Je
Smith, Emily Taylor, and Blake omason. We appreciate all the
friendship. Brenna Levine performed the Bateman analyses for
C. atrox. is research has been supported by our respective in-
stitutions, the National Science Foundation (GWS, RWC, MA,
HWG), and private sources. We thank two reviewers for help-
ful comments and suggestions; however, we bear the burden of
any blunders. Finally, a big thanks goes to our families who have
tolerated our insatiable need to be “in the eld” for long and
Alcock, J. 1998. Animal Behavior. An Evolutionary Approach. 6th edn. Sinau-
er Associates, Sunderland, Massachusetts.
Aldridge, R. D., and D. Duvall, D. 2002. Evolution of the mating season in
the pitvipers of North America. Herpetol. Monogr. 16: 1–25.
Alexander, R. D. 1974. e evolution of social behavior. Ann. Rev. Ecol. Syst.
Allaby, M. 2009. A Dictionary of Zoology, 3rd edn. Oxford University Press,
Oxford, United Kingdom.
Allen C., and M. Beko. 1997. Species of Mind: e Philosophy and Biology
of Cognitive Ethology. MIT Press, Cambridge, Massachusetts.
Amarello, M. 2012. Social Snakes? Non-random Association Patterns Detect-
ed in a Population of Arizona Black Rattlesnakes (Crotalus cerberus). Unpub-
lished thesis. Arizona State University, Tempe, Arizona.
Amarello, M., J. J. Smith, and J. Slone. 2011. Family values: maternal care
in rattlesnakes is more than mere attendance. Nature Precedings dx.doi.
Amarello, M., E. M. Nowak, E. N. Taylor, G. W. Schuett, R. A. Repp, P. C.
Rosen, and D. L. Hardy Sr. 2010. Potential environmental inuences on varia-
tion in body size and sexual size dimorphism among Arizona populations of
the Western Diamond-backed Rattlesnake (Crotalus atrox). J. Arid Environ.
Andersen, J. B., B. C. Rourke, V. J. Caiozzo, A. F. Bennett, and J. W. Hicks.
2005. Physiology: postprandial cardiac hypertrophy in pythons. Nature 434:
Anderson, C. D. 2010. Eects of movement and mating on gene ow among
overwintering hibernacula of the Timber Rattlesnake (Crotalus horridus). Co-
peia 2010: 54–61.
Apakupakul, K., and D. R. Rubenstein. 2015. Bateman’s principle is reversed
in a cooperatively breeding bird. Biol. Lett. 11: 20150034.
Arnold, S. J., and D. Duvall. 1994. Animal mating systems: a synthesis based
on selection theory. Am. Nat. 143: 317–348.
Balamurugan, J. T. T. Ajith Kumar, R. Kannan, and H. D. Pradeep. 2015.
Acclimation behaviour and bio-chemical changes during Anemonesh (Am-
phiprion sebae) and Sea Anemone (Stichodactyla haddoni) symbiosis. Symbiosis
Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity 2: 349–
Beck, D. D. 1995. Ecology and energetics of three sympatric rattlesnake spe-
cies in the Sonoran Desert. J. Herpetol. 29: 211–223.
Bejder, L., D. Fletcher, and S. Bräger 1998. A method for testing association
patterns of social animals. Anim. Behav. 56: 719–725.
Beko, M. 2007. e Emotional Lives of Animals. New World Library, No-
Beko, M., and C. Allen. 1997. Cognitive ethology: slayers, skeptics, and pro-
ponents. Pp. 313–334 In R. W. Mitchell, N. S. ompson, and H. L. Miles
(Eds.). Anthropomorphism, Anecdotes, and Animals. State University of New
York Press, New York, New York.
Betancourt, J. L., T. R. Van Devender, and P. S. Martin. 1990. Packrat Mid-
dens. e Last 40,000 Years of Biotic Change. e University of Arizona Press,
Blouin, M. S. 2003. DNA-based methods for pedigree reconstruction and
kinship analysis in natural populations. Trends Ecol. Evol. 18: 503–511.
Blundell, G. M., M. Ben-David, P. Groves, T. Bowyer, and E. Geend. 2004.
Kinship and sociality in coastal River Otters: are they related? Behav. Ecol. 15:
Booth, W., and G. W. Schuett. 2011. Molecular genetic evidence for alterna-
tive reproductive strategies in North American pitvipers (Serpentes: Viperi-
dae): long-term sperm storage and facultative parthenogenesis. Biol. J. Linn.
Soc. 104: 934–942.
Booth, W., and G. W. Schuett. 2016. e emerging phylogenetic pattern of
parthenogenesis in snakes. Biol. J. Linn. Soc. 118: 172–186.
Booth, W., G. W. Schuett, A. Ridgway, D. W. Buxton, T. A. Castoe, G. Bas-
tone, C. Bennett, and W. McMahan. 2014. New insights on facultative par-
thenogenesis in pythons. Biol. J. Linn. Soc. 112: 461–468.
Booth, W., C. F. Smith, P. H. Eskridge, S. K. Hoss, J. R. Mendelson III, and
G. W. Schuett. 2012. Facultative parthenogenesis discovered in wild verte-
brates. Biol. Lett. 8: 983–985.
Bonnie, K. E., and R. L. Earley. 2007. Expanding the scope for social informa-
tion use. Anim. Behav. 74: 171–181.
Borgatti, S. P. 2002. NetDraw: Graph Visualization Software. Available from:
Borgatti, S. P., M. G. Everett, and L. C. Freeman. 2002. Ucinet for Windows:
Software for Social Network Analysis. https://sites.google.com/site/ucinetsoft-
Bossdorf, O., C. L. Richards, and M. Pigliucci. 2008. Epigenetics for ecolo-
gists. Ecol. Lett. 11: 106–115.
Boyd, R., and P. J. Richerson. 1985. Culture and the Evolutionary Process.
e University of Chicago Press, Chicago, Illinois.
Brashears, J., and D. F. DeNardo. 2012. Do brooding pythons recognize their
clutches? Investigating external cues for ospring recognition in the Children’s
Python, Antaresia childreni. Ethology 118: 793–798.
Brattstrom, B. H. 1974. e evolution of reptilian social behavior. Amer.
Zool. 14: 35–49.
Brown, D. E. 1994. Biotic Communities of the Southwestern United States
and Northwestern Mexico. University of Utah Press, Salt Lake City, Utah.
Brown, G. P., and R. Shine. 2007. Like mother, like daughter: inheritance of
nest-site location in snakes. Biol. Lett. 3: 131–133.
Brown, J. L. 1975. e Evolution of Behavior. W.W. Norton & Company,
New York, New York.
Brown, W. S. 1993. Biology, Status, and Management of the Timber Rattle-
snake (Crotalus horridus). SSAR Herpetol Circ. 22: 1–78.
Brown, W. S., M. Kery, and J. E. Hines. 2007. Survival of Timber Rattle-
snakes (Crotalus horridus) estimated by capture-recapture models in relation
to age, sex, color time, and birthplace. Copeia 2007: 656–671.
Brown, W. S., and F. M. MacLean. 1983. Conspecic scent-trailing by new-
born Timber Rattlesnakes, Crotalus horridus. Herpetologica 39: 430–436.
Brownmiller, S. 1975. Against our Will: Men, Women, and Rape. Simon and
Shuster, New York, New York.
Bull, C. M. 2000. Monogamy in lizards. Behav. Process. 51: 7–20.
Bull, C. M., S. J .B. Cooper, and B. C. Baghurst. 1998. Social monogamy
and extra-pair fertilization in an Australian lizard, Tiliqua rugosa. Behav. Ecol.
Sociobiol. 44: 63–72.
Bull, C. M., S. S. Godfrey, and D. M. Gordon. 2012. Social networks and
the spread of Salmonella in a Sleepy Lizard population. Mol. Ecol. 21: 4,386–
Bull, C. M., M. Doherty, L. R. Schulze, and Y. Pamula. 1994. Recognition of
ospring by females of the Australian skink, Tiliqua rugosa. J. Herpetol. 28:
Bull, C. M., C. L. Grin, M. Bonnett, M. G. Gardner, and S. J. B. Copper.
2001. Discrimination between related and unrelated individuals in the Austra-
lian lizard, Egernia striolata. Behav. Ecol. Sociobiol. 50: 173–179.
Burghardt, G. M. 1977a. Learning processes in reptiles. Pp. 555–681 In C.
Gans and D. W. Tinkle (Eds.), Biology of the Reptilia, Vol. 7, Ecology and
Behavior. Academic Press, New York, New York.
Burghardt, G. M. 1977b. Of iguanas and dinosaurs: social behavior and com-
munication in neonate reptiles. Amer. Zool. 17: 177–190.
Burghardt, G. M. 1985. Animal awareness: current perceptions and historical
perspective. Amer. Psychol. 40: 905–919.
Burghardt, G. M. 1991. Cognitive ethology and critical anthropomorphism:
a snake with two heads and Hognose Snakes that play dead. Pp. 53–90 In C.
A. Ristau (Ed.), Cognitive Ethology. e Minds of Other Animals. Erlbaum,
San Francisco, California.
Burghardt, G. M. 1997. Amending Tinbergen: a fth aim for ethology. Pp.
254–295 In R. W. Mitchell, N. S. ompson, and H. L. Miles (Eds.). Anthro-
pomorphism, Anecdotes, and Animals. State University of New York Press,
Albany, New York.
Burghardt, G. M. 1998. Snake stories: from the additive model to ethology’s
fth aim. Pp. 77–95 In L. Hart (Ed.), Responsible Conduct of Research in
Animal Behavior. Oxford University Press, Oxford, United Kingdom.
Burghardt, G. M. 2005. e Genesis of Animal Play: Testing the Limits. MIT
Press, Cambridge, Massachusetts.
Burghardt, G. M. 2007. Critical anthropomorphism, uncritical anthropocen-
trism, and naïve nominalism. Comp. Cog. Behav. Rev. 2: 136–138.
Burghardt, G. M., and J. L. Gittleman. 1990. Comparative behavior and phy-
logenetic analysis: new wine, old bottles. Pp. 192–225 In M. Beko and D.
Jamieson (Eds.), Interpretation and Explanation in the Study of Animal Be-
havior, Vol. 2. Westview Press, Boulder, Colorado.
Burghardt, G. M., H. W. Greene, and A. S. Rand. 1977. Social behavior in
hatchling Green Iguanas: life at a reptile rookery. Science 195: 689–691.
Burghardt, G. M., J. B. Murphy, D. Chiszar, and M. Hutchins. 2009. Com-
bating ophiophobia: origins, treatment, education and conservation tools. Pp.
262–280 In S. J. Mullin and R. A. Seigel (Eds.), Snakes. Ecology and Conser-
vation. Cornell University Press, Ithaca, New York.
Burghardt, G. M., D. Chiszar, J. B. Murphy, J. Romano Jr., T. Walsh, and J.
Manrod. 2002. Behavioral complexity, behavioral development and play. Pp.
78–117 In J. B. Murphy, C. Cio, C. de La Panouse, and T. Walsh (Eds.),
Komodo Dragons. Biology and Conservation. Smithsonian Institution Press,
Washington, District of Columbia.
Bushar, L. M., H. K. Reinert, and L. Gelbert. 1998. Genetic variation and
gene ow within and between local populations of the Timber Rattlesnake,
Crotalus horridus. Copeia 1998: 411–422.
Bushar, L. M., C. C. B. Aborde, S. Gao, M. V. Gonzalez, J. A. Homan, I. K.
Massaro, A. H. Savitzky, and H. K. Reinert. 2014. Genetic structure of Tim-
ber Rattlesnake (Crotalus horridus) populations: physiographic inuences and
conservation implications. Copeia 2014: 694–706.
Buston, P. M., S. M. Bogdanowicz, A. Wong, and R. G. Harrison. 2007. Are
Clownsh groups composed of close relatives? An analysis of microsatellite
DNA variation in Amphiprion percula. Mol. Ecol. 16: 3,671–3,678.
Cairns, S. J., and S. J. Schwager. 1987. A comparison of association indices.
Anim. Behav. 35: 1,454–1,469.
Campbell, J. A., and W. W. Lamar. 2004. e Venomous Reptiles of the West-
ern Hemisphere, 2 vols. Cornell University Press, Ithaca, New York.
Carpenter, C. C. 1977. Communication and displays of snakes. Amer. Zool.
Carpenter, C. C., and G. W. Ferguson. 1977. Variation and evolution of
stereotyped behavior in reptiles. Pp. 335–554 In C. Gans and D. W. Tinkle
(Eds.), Biology of the Reptilia, Vol. 7. Academic Press, New York, New York.
Castoe, T. A. 2014. Snake genomes provide insight into the evolutionary ori-
gins of extreme phenotypes in vertebrates. Biology of the Pitvipers 2, Tulsa,
Castoe, T. A., Z. J. Jiang, W. Gu, Z. O. Wang, and D. D. Pollock. 2008. Adap-
tive evolution and functional redesign of core metabolic proteins in snakes.
PLoS ONE 3: e2201.
Chapman, D. D., M. S. Shivji, E. Louis, J. Sommer, H. Fletcher, and P. A.
Prodöhl. 2007. Virgin birth in a Hammerhead Shark. Biol. Lett. 3: 425–427.
Chapple, D. G. 2003. Ecology, life-history, and behavior in the Australian
scincid genus Egernia, with comments on the evolution of complex sociality in
lizards. Herpetol. Monogr. 17: 145–180.
Chiszar, D, H. M. Smith, C. M. Bogert, and J. Vidaurri. 1991. A chemi-
cal sense of self in Timber and Prairie Rattlesnakes. Bull. Psychon. Soc. 29:
Chiszar, D., H. M. Smith, and C. W. Radclie. 1993. Zoo and laboratory
experiments on the behavior of snakes: assessments of competence in captive-
raised animals. Amer. Zool. 33: 109–116.
Chowhury, D., K. Nishinari, and A. Schadschneider. 2004. Self-organizing
patterns and trac ow in colonies of organisms: from bacteria and social
insects to vertebrates. Phase Transitions 77: 601–624.
Christensen, C. B., J. Christensen-Dalsgaard, C. Brandt, and P. T. Madsen.
2012. Hearing with an atympanic ear: good vibration and poor sound-pres-
sure detection in the Royal Python, Python regius. J. Exp. Biol. 215: 331–342.
Clark, R. W. 2004. Kin recognition in rattlesnakes. Biol. Lett. 271: S243–
Clark, R. W. 2006. Fixed videography to study predation behavior of an am-
bush foraging snake, Crotalus horridus. Copeia 2006: 181–187.
Clark, R. W. 2007. Public information for solitary foragers: Timber Rattle-
snakes use conspecic chemical cues to select ambush sites. Behav. Ecol. 18:
Clark, R. W., W. S. Brown, R. Stechert, and K. R. Zamudio. 2008. Integrat-
ing individual behaviour and landscape genetics: the population structure of
Timber Rattlesnake hibernacula. Mol. Ecol. 17: 719–730.
Clark, R. W., W. S. Brown, R. Stechert, and H. W. Greene. 2012. Cryptic
sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis. Biol.
Lett. 8: 523–525.
Clark, R. W., G. W. Schuett, R. A. Repp, M. Amarello, C. F. Smith, and H.-W.
Herrmann. 2014. Mating systems, reproductive success, and sexual selection
in a secretive species: a case study of the Western Diamond-backed Rattle-
snake, Crotalus atrox. PLoS ONE 9: e90616.
Clements, J. F. 2007. e Clements Checklist of Birds of the World, 6th edn.
Cornell University Press, Ithaca, New York.
Clutton-Brock, T. H. (Ed.) 1988. Reproductive Success. Studies of Individual
Variation in Contrasting Breeding Systems. e University of Chicago Press,
Clutton-Brock, T. H. 1991. e Evolution of Parental Care. Princeton Uni-
versity Press, Princeton, New Jersey.
Clutton-Brock, T. H. 2009. Cooperation between non-kin in animal societies.
Nature 462: 51–57.
Clutton-Brock, T. H., and B. C. Sheldon. 2010. Individuals and populations:
the role of long-term, individual-based studies of animals in ecology and evo-
lutionary biology. Trends Ecol. Evol. 25: 562–573.
Cobb, V.A., J. J. Green, T. Worrall, J. Pruett, and B. Glorioso. 2005. Initial
den location behavior in a litter of neonate Crotalus horridus (Timber Rattle-
snakes). Southeast. Nat. 4: 723–730.
Collet, J. M., R. F. Dean, K. Worley, D. S. Richardson, and T. Pizzari. 2014:
e measure and signicance of Bateman’s principles. Proc. R. Soc. B 281:
Costello, E. K., J. I. Gordon, S. M. Secor, and R. Knight. 2010. Postprandial
remodeling of the gut microbiota in Burmese Pythons. e ISME Journal 4:
Couzin, I. D. 2006. Behavioral ecology: social organization in ssion–fusion
societies. Current Biol. 16: R169–R171.
Covas, R., and M. Griesser. 2007. Life history and the evolution of family liv-
ing in birds. Proc. R. Soc. Lond. B 274: 1,349–1,357.
Crews, D. 2008. Epigenetics and its implications for behavioral neuroendocri-
nology. Front. Neuroendocrinol. 29: 344–357.
Crews, D., A. C. Gore, T. S. Hsu, N. L. Dangleben, M. Spinetta, M. D. An-
way, and M. K. Skinner. 2007. Transgenerational epigenetic imprints on mate
preference. Proc. Natl. Acad. Sci. USA. 104: 5,942–5,946.
Crews, D., R. Gillettea, S. V. Scarpinoa, M. Manikkamb, M. I. Savenkovab,
and M. K. Skinner. 2012. Epigenetic transgenerational inheritance of altered
stress responses. Proc. Natl. Acad. Sci. USA. 109: 9,143–9,148.
Croft, D. P., R. James, and J. Krause. 2008. Exploring Animal Social Net-
works. Princeton University Press, Princeton, New Jersey.
Croft, D. P., J. Krause, and R. James. 2004. Social networks in the Guppy
(Poecilia reticulata). Proc. R. Soc. B 271: S516–S519.
Dall, S. R. X., A. M. Bell, D. I. Bolnick, and F. L. W. Ratnieks. 2012. An
evolutionary ecology of individual dierences. Ecol. Lett. 15: 1,189–1,198.
Danchin, E., L. A. Giraldeau, T. J. Valone, and R. H. Wagner. 2004. Public in-
formation: from nosy neighbors to cultural evolution. Science 305: 487–491.
Darwin, C. 1839. e Voyage of the Beagle. John Murray, London, United
Darwin, C. 1859. On the Origin of Species by Means of Natural Selection.
John Murray, London, United Kingdom.
Darwin, C. 1871. e Descent of Man, and Selection in Relation to Sex. John
Murray, London, United Kingdom.
Davis, A. R., A. Corl, Y. Surget-Groba, and B. Sinervo. 2011. Convergent
evolution of kin-based sociality in a lizard. Proc. R. Soc. B 278: 1,507–1,514.
Davis, J. M., and J. A. Stamps 2004. e eect of natal experience on habitat
preferences. Trends Ecol. Evol. 19: 411–416.
Dawkins, R. 1976. e Selsh Gene. Oxford University Press, New York, New
de Queiroz, A. 1997. Lip-aring in thamnophiine snakes and its possible as-
sociation with soft-bodied, sticky prey. Herpetol. Rev. 28: 28–29.
de Waal, F. 2005. Our Inner Ape. Riverhead Books, New York, New York.
Ditmars, R. L. 1907. e Reptile Book. Doubleday, New York, New York.
Ditmars, R. 1942. Snakes of the World. Macmillan, New York, New York.
Doody, J. S., G. M. Burghardt, and V. Dinets. 2013. Breaking the social–
non-social dichotomy: a role for reptiles in vertebrate social behavior research?
Ethology 199: 1–9.
Dorcas, M. E., and J. D. Willson. 2009. Innovative methods for studies of
snake ecology and conservation. Pp. 5–37 In S. J. Mullin and R. A. Seigel
(Eds.), Snakes. Ecology and Conservation. Cornell University Press, Ithaca,
Dubach, J., A. Sajewicz, and R. Pawley. 1997 Parthenogenesis in the Arafuran
File Snake, Acrochordus arafurae. Herpetol. Nat. Hist. 5: 11–18.
Dugatkin, L. 1999. Cheating Monkeys and Citizen Bees. e Nature of Co-
operation in Animals and Humans. Harvard University Press, Cambridge,
Dugatkin, L. A. 2009. Principles of Animal Behavior. 2nd edn. W. W. Norton
& Company, New York, New York.
Dunkle, D. H., and H. M. Smith. 1937. Notes on some Mexican ophidians.
Occ. Pap. Mus. Zool. Univ. Mich. 363: 1–15.
Duvall, D., M. B. King, and J. Gutwiller. 1985. Behavioral ecology and ethol-
ogy of the Prairie Rattlesnake. Nat. Geogr. Res. 1: 80–111.
Duvall, D., S. J. Arnold, and G. W. Schuett. 1992. Pitviper mating systems:
ecological potential, sexual selection, and microevolution. Pp. 321–336 In J.
A. Campbell and E. D. Brodie Jr. (Eds.), Biology of the Pitvipers. Selva, Tyler,
Duvall, D., G. W. Schuett, and S. J. Arnold. 1993. Ecology and evolution of
snake mating systems. Pp. 165–200 In R. A. Seigel and J. T. Collins (Eds.),
Snakes. Ecology and Behavior. McGraw-Hill, New York, New York.
Earley, R. L. 2010. Social eavesdropping and the evolution of conditional co-
operation and cheating strategies. Phil. Trans. R. Soc. Lond. B 365: 2,675–
Earley, R. L., and L. A. Dugatkin. 2002. Eavesdropping on visual cues in
Swordtail (Xiphophorus helleri) ghts – a case for networking. Proc. R. Soc.
Lond. B 269: 943–952.
Earley, R. L., M. Tinsley, and L. A. Dugatkin. 2003. To see or not to see: does
previewing a future opponent aect the contest behavior of Green Swordtail
males (Xiphophorus helleri)? Naturwissenschaften 90: 226–230.
Earley, R. L., M. Druen, and L. A. Dugatkin. 2005. Watching ghts does not
alter a bystander’s response toward naïve conspecics in male Green Swordtail
sh (Xiphophorus helleri). Anim. Behav. 69: 1,139–1,145.
Emerson, R. W. 1870. Society and Solitude. Fields Osgood, Boston, Mas-
Emlen, D. J. 2014. Animal Weapons. e Evolution of Battle. Henry Holt &
Company, New York, New York.
Emlen, S. T. 1994. Benets, constraints, and the evolution of the family.
Trends Ecol. Evol. 9: 282–285.
Emlen, S. T. 1995. An evolutionary theory of the family. Proc. Natl. Acad. Sci.
USA 98: 8,092–8,099.
Emlen, S. T., and L. W. Oring. 1977. Ecology, sexual selection, and the evolu-
tion of mating systems. Science 19: 215–223.
Ernst, C. H., and E. M. Ernst. 2012. Venomous Reptiles of the United States,
Canada, and Northern Mexico, 2 vols. Johns Hopkins University Press, Bal-
Evans, J. C., S. C. Votier, and S. R. X. Dall. 2015. Information use in colonial
living. Biol. Rev. 91: 658–672.
Fautin, D. G., and G. R. Allen. 1997. Anemone Fishes and their Host Sea
Anemones: A Guide for Aquarists and Divers. Western Australian Museum,
Fenner, A. L., S. S. Godfrey, and C. M. Bull. 2011. Using social networks to
deduce whether residents or dispersers spread parasites in a lizard population.
J. Anim. Ecol. 280: 835–843.
Filaramo, N. I., and K. Schwenk, 2009. e mechanism of chemical delivery
to the vomeronasal organs in squamate reptiles: a comparative morphological
approach. J. Exp. Zool. 311A: 20–34.
Fitch, H. S. 1935. Natural history of the Alligator Lizards. Transactions of the
Academy of Science of Saint Louis 29: 1–38.
Fitch, H. S. 1987. Collecting and life-history techniques. Pp. 143–164 In R.
A. Seigel, J. T. Collins, and S. S. Novak (Eds.), Snakes. Ecology and Evolution-
ary Biology. Macmillan Publishing, New York, New York.
Fitzgerald, L. A., and C. W. Painter. 2000. Rattlesnake commercialization:
long-term trends, issues, and implications for conservation. Wildl. Soc. Bull.
Fitzpatrick, C. L. 2015. Expanding sexual selection gradients: a synthetic re-
nement of sexual selection theory. Ethology 121: 207–215.
Formica, V. A., M. E. Augat, M. E. Barnard, R. E. Buttereld, C. W. Wood,
and E. D. Brodie III. 2010. Using home range estimates to construct social
networks for species with indirect behavioral observations. Behav. Ecol. Socio-
biol. 64: 1,199–1,208.
Friedel, P. L., B. A. Young, and J. L. van Hemmen. 2008. Auditory localization
of ground-borne vibrations in snakes. Phys. Rev. Lett. 100: 048701.
Futuyma, D. 2009. Evolution, 2nd edn. Sinauer Associates, Sunderland, Mas-
Gardner, M. G., C. M. Bull, S. J. B. Cooper, and G. A. Dueld. 2001. Genet-
ic evidence for a family structure in stable social aggregations of the Australian
lizard Egernia stokesii. Mol. Ecol. 10: 175–183.
Gardner, M. G., C. M. Bull, and S. J. B. Cooper. 2002. High levels of genetic
monogamy in the group-living Australian lizard Egernia stokesii. Mol. Ecol.
Gardner, M. G., S. K. Pearson, G. R. Johnson, and M. P. Schwarz. 2015.
Group living in squamate reptiles: a review of evidence for stable aggregations.
Biol. Rev. (early view). doi: 10.1111/brv.12201.
Gerlach, N. M., J. W. McGlothlin, P. G. Parker, and E. D. Ketterson. 2012.
Reinterpreting Bateman gradients: multiple mating and selection in both sexes
of a songbird species. Behav. Ecol. 23: 1,078–1,088.
Gero, S., L. Bejder, H. Whitehead, J. Mann, and R. C. Connor. 2005. Behav-
iourally specic preferred associations in Bottlenose Dolphins, Tursiops spp.
Can. J. Zool. 83: 1,566–1,573.
Gibbons, J. W., and K. M. Andrews. 2004. PIT tagging: simple technology at
its best. BioScience 54: 447–454.
Gibbs, H. L., and P. J. Weatherhead. 2001. Insights into population ecology
and sexual selection in snakes through the application of DNA-based genetic
markers. J. Heredity 92: 173–179.
Gienger, C. M., and D. D. Beck. 2011. Northern Pacic Rattlesnakes (Cro-
talus oreganus) use thermal and structural cues to choose overwintering hiber-
nacula. Can. J. Zool. 89: 1,084–1,090.
Gill, F. 2006. Birds of the World: Recommended English Names. Princeton
University Press, Princeton, New Jersey.
Gillingham, J. C. 1987. Social behavior. Pp. 184–209 In R. A. Seigel, J. T.
Collins, and S. S. Novak (Eds.), Snakes. Ecology and Evolutionary Biology.
MacMillan Publishing Company, New York, New York.
Gillingham, J. C., C. C. Carpenter, and J. B. Murphy. 1983. Courtship, male
combat and dominance in the Western Diamondback Rattlesnake, Crotalus
atrox. J. Herpetol. 17: 265–270.
Glaudas, X., and C. T. Winne. 2007. Do warning displays predict striking
behavior in a viperid snake, the Cottonmouth (Agkistrodon piscivorus)? Can. J.
Zool. 85: 574–578.
Godfrey, S. S., A. Sih, and C. M. Bull. 2013. e response of a Sleepy Lizard
social network to altered ecological conditions. Anim. Behav. 86: 763–772.
Godfrey, S.S., T. H. Ansari, M. G. Gardner, D. R. Farine, and C. M. Bull.
2014. A contact-based social network of lizards is dened by low genetic relat-
edness among strongly connected individuals. Anim. Behav. 97: 35–43.
Goodall, J. 2010. In the Shadow of Man. 50th Anniversary of Gombe Edition.
Mariner Books, Boston, Massachusetts.
Gopurenko, D., R. N. Williams, and J. A. DeWoody. 2007. Reproductive
and mating success in the Small-mouthed Salamander (Ambystoma texanum)
estimated via microsatellite parentage analysis. Evol. Biol. 34: 130–139.
Gosling, S. D. 2001. From mice to men: what can we learn about personality
from animal research? Psychol. Bull. 127: 45–86.
Graham, S. P., R. L. Earley, S. K. Hoss, G. W. Schuett, and M. S. Grob-
er. 2008. e reproductive biology of male Cottonmouths (Agkistrodon pi-
scivorus): do plasma steroid hormones predict the mating season? Gen. Comp.
Endocrinol. 159: 226–235.
Grandin, T., and C. Johnson. 2006. Animals in Translation: Using the Myster-
ies of Autism to Decode Animal Behavior. Harcourt, Boston, Massachusetts.
Graves, B. M. 1989. Defensive behavior of female Prairie Rattlesnakes (Crota-
lus viridis) changes after parturition. Copeia 1989: 791–794.
Graves, B. M., and D. Duvall. 1987. An experimental study of aggregation
and thermoregulation in Prairie Rattlesnakes (Crotalus viridis viridis). Herpe-
tologica 43: 259–264.
Graves, B. M., and D. Duvall. 1988. Evidence of an alarm pheromone from
the cloacal sacs of Prairie Rattlesnakes. Southwest. Nat. 33: 339–345.
Graves, B. M., and D. Duvall. 1995. Aggregation of squamate reptiles as-
sociated with gestation, oviposition, and parturition. Herpetol. Monogr. 9:
Greenberg, N., and D. Crews. 1977. Introduction to the symposium: social
behavior in reptiles. Amer. Zool. 17: 153–154.
Greene, H. W. 1988. Antipredator mechanisms in reptiles. Pp. 1–152 In C.
Gans and R. B. Huey (Eds.), Biology of the Reptilia, Vol. 16, Ecology B, De-
fense and Life History. Alan R. Liss, New York, New York.
Greene, H. W. 1997. Snakes. e Evolution of Mystery in Nature. University
of California Press, Berkeley, California.
Greene, H. W. 2003. Appreciating rattlesnakes. Wild Earth 13: 28–32.
Greene, H. W. 2013. Tracks and Shadows. Field Biology as Art. University of
California Press, Berkeley and Los Angeles, California.
Greene, H. W., and G. V. Oliver Jr. 1965. Notes on the natural history of the
Western Massasauga. Herpetologica 21: 225–228.
Greene, H. W., P. G. May, D. L. Hardy, Sr., J. M. Sciturro, and T. M. Farrell.
2002. Parental behavior by vipers. Pp. 179–206 In G. W. Schuett, M. Hög-
gren, M. E. Douglas, and H. W. Greene (Eds.), Biology of the Vipers. Eagle
Mountain Publishing, LC, Eagle Mountain, Utah.
Greene, H. W., J. J. S. Rodríguez, and B. J. Powell. 2006. Parental behavior in
anguids. South American J. of Herpetol. 1: 9–19.
Gregory, P. T. 1984. Communal denning in snakes. Pp. 57–76 In R. A. Seigel,
L. E. Hunt, J. L. Knight, L. Malaret, and N. L. Zuschlag (Eds.), Vertebrate
Ecology and Systematics: A Tribute to Henry S. Fitch. Univ. Kansas Mus. Nat.
Hist. Spec. Publ. 10.
Gregory, P. T., J. M. Macartney, and K. W. Larsen. 1987 Spatial patterns and
movements. Pp. 366–395 In R. A. Seigel, J. T. Collins, and S. S. Novak (Eds.),
Snakes. Ecology and Evolutionary Biology. Macmillan, New York, New York.
Grin, D. R. 1981. e Question of Animal Awareness. Evolutionary Con-
tinuity of Mental Experience. e Rockefeller University Press, New York,
Grin, D. R. 2001. Animal Minds: Beyond Cognition to Consciousness. e
University of Chicago Press, Chicago, Illinois.
Halpern, M., and A. Martinez-Marcos. 2003. Structure and function of the
vomeronasal system: an update. Progr. Neurobiol. 70: 245–318.
Hamilton, B. T., and E. M. Nowak. 2009. Relationships between insolation
and rattlesnake hibernacula. Western North American Naturalist 69: 319–328.
Hamilton, W. D. 1963. e evolution of altruistic behavior. Am. Nat. 97:
Hamilton, W. D. 1964. e genetical evolution of social behaviour I, II. J.
eor. Biol. 7: 1–52.
Hamilton, W. D. 1972. Altruism and related phenomena, mainly in social
insects. Annu. Rev. Ecol. Syst. 3: 193–232.
Hatchwell, B. J. 2010. Cryptic kin selection: kin structure in vertebrate pop-
ulations and opportunities for kin-directed cooperation. Ethology 116: 203
Head, J. J., and P. D. Polly. 2015. Evolution of the snake body form reveals
homoplasy in amniote Hox gene function. Nature 520: 86–89.
Hinde, R. A. 1976. Interactions, relationships and social structure. Man 11:
Holekamp, K. E., J. E. Smith, C. C. Strelio, R. R. van Horn, and H. E.
Watts. 2012. Society, demography and genetic structure in the Spotted Hyena.
Mol. Ecol. 21: 613–632.
Holycross, A. T., and J. D. Fawcett. 2002. Observations on neonatal aggrega-
tions and associated behaviors in the Prairie Rattlesnake, Crotalus viridis viri-
dis. Am. Midl. Nat. 148: 181–184.
Hoss, S. K. 2013. Maternal Attendance of Young in Cottonmouths (Agkis-
trodon piscivorus): Adaptive Value and Hormonal Mechanisms. Unpublished
dissertation, San Diego State University, San Diego, California.
Hoss, S. K., and R. W. Clark. 2014. Mother Cottonmouths (Agkistrodon pi-
scivorus) alter their anti-predator behavior in the presence of neonates. Ethol-
ogy 120: 933–941.
Hoss, S. K., M. J. Garcia, R. L. Earley, and R. W. Clark. 2014. Fine-scale hor-
monal patterns associated with birth and maternal care in the Cottonmouth
(Agkistrodon piscivorus), a North American pitviper. Gen. Comp. Endocrinol.
Hoss, S. K, D. H. Deutschman, W. Booth, and R. W. Clark. 2015. Post-birth
separation aects the aliative behavior of kin in a pitviper with maternal at-
tendance. Biol. J. Linn Soc. 116: 637–648.
Huang, W.-S., H. W. Greene, T.-J. Chang, and R. Shine 2011.Territorial be-
havior in Taiwanese Kukri Snakes (Oligodon formosanus). Proc. Natl. Acad. Sci.
USA 108: 7,455–7,459.
Jones, A. G. 2015. BATEMANATER: a computer program to estimate and
bootstrap mating system variables based on Bateman’s principles. Mol. Ecol.
Res. 15: 1,396–1,402.
Kelley, J. L., L. J. Morrell, C. Inskip, J. Krause, and D. P. Croft. 2011. Preda-
tion risk shapes social networks in ssion-fusion populations. PLoS ONE 6:
Kerth, G., and J. van Schaik. 2012. Causes and consequences of living in
closed societies: lessons from a long-term socio-genetic study on Bechstein’s
bats. Mol. Ecol. 21: 633–646.
Kinney, C., G. Abishahin, and B. A. Young. 1998. Hissing in rattlesnakes:
redundant signaling or inationary epiphenomenon? J. Exp. Zool. 280: 107–
Klauber, L. M. 1956. Rattlesnakes. eir Habits, Life Histories, and Inuence
on Mankind, 2 vols. University of California Press, Berkeley and Los Angeles,
Klauber, L. M. 1972. Rattlesnakes. eir Habits, Life Histories, and Inuence
on Mankind, 2 vols., 2nd edn. University of California Press, Berkeley and Los
Koestler, A. 1978. Janus: A Summing Up. Random House, New York, New
Kohl, K. D., A. W. Miller, and M. D. Dearing. 2014. Evolutionary irony:
evidence that defensive plant spines act as a proximate cue to attract a mam-
malian herbivore. Oikos 124: 835–841.
Kokko, H., E. Ranta, G. Ruxton, and P. Lundberg. 2002. Sexually transmit-
ted disease and the evolution of mating systems. Evolution 56: 1,091–1,100.
Krause, J., and G. D. Ruxton. 2002. Living in Groups. Oxford University
Press, Oxford, United Kingdom.
Krause, J., R. James, D. W. Franks, and D. P. Croft. 2015. Animal Social Net-
works. Oxford University Press, Oxford, United Kingdom.
Kuhn, T. S. 1996. e Structure of Scientic Revolutions. 3rd edn. University
of Chicago Press, Chicago, Illinois.
Leal, M, and B. J. Powell. 2011. Behavioural exibility and problem-solving in
a tropical lizard. Biol. Lett. 8: 28–30.
Lehmann, L., and L. Keller. 2006. e evolution of cooperation and altru-
ism – a general framework and a classication of models. J. Evol. Biol. 19:
Leu, S. T., J. Bashford, P. M. Kappeler, and C. M. Bull. 2010. Association
networks reveal social organization in the Sleepy Lizard. Anim. Behav. 79:
Leu, S. T., P. M. Kappeler, and C. M. Bull. 2011. Pair-living in the absence
of obligate biparental care in a lizard: trading o sex and food? Ethology 117:
Leu, S. T., D. Burzacott, M. J. Whiting, and C. M. Bull. 2015. Mate familiar-
ity aects pairing behaviour in a long-term monogamous lizard: evidence from
detailed bio-logging and a 31-year eld study. Ethology 121: 760–768.
Levine, B. A., C. F. Smith, G. W. Schuett, M. R. Douglas, M. A. Davis, and
M. E. Douglas. 2015. Bateman-Trivers in the 21st Century: sexual selection in
a North American pitviper. Biol. J. Linn. Soc. 114: 436–445.
Levine, B. A., C. F. Smith, M. R. Douglas, M. A. Davis, G. W. Schuett, S. J.
Beaupre, and M. E. Douglas. 2016. Population genetics of the Copperhead at
its most northeastern distribution. Copeia 2016: 448–457.
Lewis, D. B., and D. M. Gower. 1980. Biology of Communication. John
Wiley & Sons, New York, New York.
Lillywhite, H. B. 2014. How Snakes Work. Structure, Function and Behavior
of the World’s Snakes. Oxford University Press, New York, New York.
Lucas, D., V. Reynolds, C. Boesch, and L. Vigilant. 2005. To what extent does
living in a group mean living with kin? Mol. Ecol. 14: 2,181–2,196.
Lusseau, D., B. Wilson, P. S. Hammond, K. Grellier, J. W. Durban, K. M.
Parsons, T. R. Barton, and P. M. ompson. 2006. Quantifying the inuence
of sociality on population structure in Bottlenose Dolphins. J. Anim. Ecol.
Mackessy, S. P. (Ed.). 2009. Handbook of Venoms and Toxins of Reptiles.
CRC Press, Boca Raton, Florida.
MacLennan, B. J., and G. M. Burghardt. 1994. Synthetic ethology and the
evolution of cooperative communication. Adaptive Behavior 2: 161–188.
Manel, S., M. K. Schwartz, G. Luikart, and P. Taberlet. 2003. Landscape ge-
netics: combining landscape ecology and population genetics. Trends Ecol.
Evol. 18: 189–197.
Manel, S., and R. Holderegger. 2013. Ten years of landscape genetics. Trends
Ecol. Evol. 28: 614–621.
Margulis, L., and R. Fester. 1991. Symbiosis as a Source of Evolutionary In-
novation. MIT Press, Cambridge, Massachusetts.
Martin, W. H. 2002. Life history constraints on the Timber Rattlesnake (Cro-
talus horridus) at its climatic limits. Pp. 285–306 In G. W. Schuett, M. Hög-
gren, M. E, Douglas, and H. W. Greene (Eds.), Biology of the Vipers. Eagle
Mountain Publishing, LC, Eagle Mountain, Utah.
Mason, R. T., and M. R. Parker. 2010. Social behavior and pheromonal com-
munication in reptiles. J. Comp. Physiol. A 196: 729–749.
Matocq, M. D., and E. A. Lacey. 2004. Philopatry, kin clusters, and genetic
relatedness in a population of Woodrats (Neotoma macrotis). Behav. Ecol. 15:
Maynard-Smith, J. 1982. Evolution and the eory of Games. Cambridge
University Press, New York, New York.
McAlpin, S., P. Duckett, and A. Stow. 2011. Lizards cooperatively tunnel to
construct a long-term home for family members. PLoS ONE 6: e19041.
McGregor, P. K. 2005. Animal Communication Networks. Cambridge Uni-
versity Press, Cambridge, United Kingdom.
Mesterton-Gibbons, M., and L. A. Dugatkin. 1992. Cooperation among un-
related individuals: evolutionary factors. Q. Rev Biol. 67: 267–281.
Mitchell, R. W., N. S. ompson, and H. L. Miles (Eds.). 1997. Anthro-
pomorphism, Anecdotes, and Animals. State University of New York Press,
Albany, New York.
Mobley, K. B., and A. G. Jones. 2012. Overcoming statistical bias to estimate
genetic mating systems in open populations: a comparison of Bateman’s prin-
ciples between the sexes in a sex-role reversed Pipesh. Evolution 67: 646–660.
Moon, B. R., K. E. Conley, S. L. Lindstedt, and M. R. Urquhart. 2003. Mini-
mal shortening in a high-frequency muscle. J. Exp. Biol. 206: 1,291-1,297.
Moore, M. C., and J. Lindzey. 1992. e physiological basis of sexual behavior
in male reptiles. Pp. 70–113 In C. Gans and D. Crews (Eds.), Biology of the
Reptilia, Vol. 18. e University of Chicago Press, Chicago, Illinois.
Murrant, M. N., J. Bowman, and P. J. Gopurenko. 2014. A test of non-kin
social foraging in the Southern Flying Squirrel (Glaucomys volans). Biol. J.
Linn. Soc. 113: 1,126–1,135.
Murray, E. J., and F. Foote. 1979. e origins of fear of snakes. Behav. Res.
er. 17: 489–493.
Nagel, T. 1974. What is it like to be a bat? Phil. Rev. 83: 435–450.
Nicolaus, M., J. M. Tinbergen, K. M. Bouwman, S. P. M. Michler, R. Ubels,
C. Both, B. Kempenaers, and N. J. Dingemanse. 2012. Experimental evi-
dence for adaptive personalities in a wild passerine bird. Proc. R. Soc. B. 279:
Nowak, E. M. 2005. Movement patterns and life history of Western Dia-
mond-backed Rattlesnakes (Crotalus atrox) at Tuzigoot National Monument,
Arizona. Pp. 253–274 In C. van Riper and D. Mattson (Eds.), Proceedings of
the 7th Biennial Conference of Research on the Colorado Plateau. University
of Arizona Press, Tucson, Arizona.
Nowak, E. M., T. C. eimer, and G. W. Schuett. 2008. Functional and
numerical responses of predators: where do vipers t in the traditional para-
digms? Biol. Rev. 83: 601–620.
Nowak, E. M. 2009. Ecology and Management of Venomous Reptilian
Predators Unpublished dissertation, Northern Arizona University, Flagsta,
O’Connor, B. P., G. W. Schuett, and B. La Forrest. 2015. Natural History
Notes. Crotalus willardi (Ridge-nosed Rattlesnake). Pregnancy/Maternal Care/
Male Activity. Herpetol. Rev. 46: 446–447.
O’Connor, D., and R. Shine. 2003. Lizards in ‘nuclear families’: a novel rep-
tilian social system in Egernia saxatilis (Scincidae). Mol. Ecol. 12: 743–752.
O’Connor, D. E., and R. Shine. 2006. Kin discrimination in the social lizard
Egernia saxatilis (Scincidae). Behav. Ecol. 17: 206–211.
Oh, K. P., and A. V. Badyaev. 2010. Structure of social networks in a passerine
bird: consequences for sexual selection and the evolution of mating strategies.
Am. Nat. 176: E80–E89.
Ohlsson, R., K. Hall, and M. Ritzen. 1995. Genomic Imprinting. Causes and
Consequences. Cambridge University Press, Cambridge, Massachusetts.
O’Leile, J. K., S. J. Beaupre, and D. Duvall. 1994. A novel form of mate
guarding/female defense polygyny in Western Diamondback Rattlesnakes.
Amer. Zool. 34: 62A.
Oliveira, R. F., M. Taborsky, and H. Jane Brockman (Eds.). 2008. Alternative
Reproductive Tactics. Cambridge University Press, New York, New York.
Padilla, D. K., T. L. Daniel, P. S. Dickinson, D. Grunbaum, et al. 2014. Ad-
dressing grand challenges in organismal biology: the need for synthesis. Bio-
Science 64: 1,178–1,187.
Palmer, C. T. 1989. Rape in nonhuman animal species: denitions, evidence,
and implications. J. Sex Res. 26: 355–374.
Paracer, S., and V. Ahmadjian, 2000. Symbiosis. An Introduction to Biological
Associations. Oxford University Press, United Kingdom.
Parker, J. M., S. F. Spear, and S. Oyler-McCance. 2013. Natural History
Notes. Crotalus oreganus concolor (Midget Faded Rattlesnake). Nursery aggre-
gation. Herpetol. Rev. 43: 658–659.
Parrish, J. K., and L. Edelstein-Keshet. 1999. Complexity, pattern, and evolu-
tionary trade-os in animal aggregation. Science 284: 99–101.
Partecke, J., A. von Haeseler, and M. Wikelski. 2002. Territory establishment
in lekking Marine Iguanas, Amblyrhynchus cristatus: support for the hotshot
mechanism. Behav. Ecol. Sociobiol. 51: 579-587.
Pepperberg, I. M. 2002. e Alex Studies: Cognitive and Communicative
Abilities of Grey Parrots. Harvard University Press, Cambridge, Massachusetts.
Pernetta, A. P., C. J. Reading, and J. A. Allen. 2009. Chemoreception and kin
discrimination by neonate Smooth Snakes, Coronella austriaca. Anim Behav.
Pozarowski, K., D. S. Bryan, R. Bosse, E. Watson, and H.-W. Herrmann.
2012. Development of polymorphic microsatellite loci for the rattlesnake spe-
cies Crotalus atrox, C. cerastes, and C. scutulatus (Viperidae: Crotalinae) and
cross-species amplication of microsatellite markers in Crotalus and Sistrurus
species. Conserv. Genet. Res. 4: 955–961.
Psorakis, I., B. Voelkl, C. J. Garroway, R. Radersma, et al. 2015. Inferring
social structure from temporal data. Behav. Ecol. Sociobiol. 69: 857–866.
R Foundation for Statistical Computing. 2011. R: A language and environ-
ment for statistical computing. Available from: http://www.r-project.org.
Ramos-Fernández, G., D. Boyer, F. Aureli, and L. Vick. 2009. Association
networks in Spider Monkeys (Ateles georoyi). Behav. Ecol. Sociobiol. 63:
Réale, D., S. M. Reader, D. Sol, P. T. McDougall, and N. J. Dingemanse.
2007. Integrating animal temperament within ecology and evolution. Biol.
Rev. 82: 291–318.
Reinert, H. K., and R. T. Zappalorti. 1988. Field observation of the associa-
tion of adult and neonatal Timber Rattlesnakes, Crotalus horridus, with pos-
sible evidence for conspecic trailing. Copeia 1988: 1,057–1,059.
Reiserer, R. S., G. W. Schuett, and R. L. Earley. 2008. Dynamic aggregations
of newborn sibling rattlesnakes exhibit stable thermoregulatory properties. J.
Zool. 274: 277–283.
Repp, R. A. 1998. Wintertime observations on ve species of reptiles in the
Tucson area: shelter site selections/delity to shelter sites/notes on behavior.
Bull. Chicago Herpetol. Soc. 33: 49–56.
Repp, R. A., and G. W. Schuett. 2008. Adult Western Diamond-backed Rat-
tlesnakes (Crotalus atrox) gain water through harvesting and drinking rain,
sleet, and snow. Southwest. Nat. 53: 109–115.
Repp, R. A., and G. W. Schuett. 2009. Natural History Notes. Crotalus atrox
(Western Diamond-backed Rattlesnake). Adult predation on lizards. Herpe-
tol. Rev. 40: 353–354.
Rivas, J. A., and G. M. Burghardt. 2001. Understanding sexual size dimor-
phism in snakes: wearing the snake’s shoes. Anim. Behav. 62: F1–F6.
Rivas, J. A., and G. M. Burghardt. 2002. Crotalomorphism: a metaphor to
understand anthropomorphism by omission. Pp. 9–17 In M. Beko, A. Colin,
and G. M. Burghardt (Eds.), e Cognitive Animal: Empirical and eoreti-
cal Perspectives on Animal Cognition. MIT Press, Cambridge, Massachusetts.
Rivas, J. A., and G. M. Burghardt. 2005. Snake mating systems, behavior, and
evolution: the revisionary implications of recent ndings. J. Comp. Psychol.
Rome, L. C., and S. L. Linstedt. 1998. e quest for speed: muscles built for
high-frequency contractions. News Physiol. Sci. 13: 261–268.
Rubio, M. 1998. Rattlesnakes. Portrait of a Predator. Smithsonian Institution
Press, Washington, District of Columbia.
Savitzky, A. H., and B. R. Moon. 2008. Tail morphology in the Western Dia-
mond-backed Rattlesnake, Crotalus atrox. J. Morphol. 269: 935–944.
Schaeer, P. J., K. E. Conley, and S. L. Lindstedt. 1996. Structural correlates
of speed and endurance in skeletal muscle: the rattlesnake tailshaker muscle. J.
Exp. Biol. 199: 351–358.
Schmidt-Nielsen, K. 1967. e unusual animal, or to expect the unexpected.
Fedn. Proc. Fedn. Am. Socs. Exp. Biol. 26: 981–986.
Schuett, G.W. 1992. Is long-term sperm storage an important component of
the reproductive biology of temperate pitvipers? Pp. 169–184 In J. A. Camp-
bell and E.D. Brodie, Jr. (Eds.). Biology of the Pitvipers. Selva, Tyler, Texas.
Schuett, G. W. 1997. Body size and agonistic experience aect dominance and
mating success in male Copperheads, Agkistrodon contortrix. Anim. Behav. 54:
Schuett, G. W., and J. C. Gillingham. 1989. Male-male agonistic behaviour
of the Copperhead, Agkistrodon contortrix. Amphibia-Reptilia 10: 243–266.
Schuett, G. W., P. F. Fernandez, W. F. Gergits, N. J. Casna, D. Chizsar, H. M.
Smith, J. B. Mitton, S. P. Mackessy, R. A. Odum, and M. J. Demlong. 1997.
Production of ospring in the absence of males: evidence for facultative par-
thenogenesis in bisexual snakes. Herpetol. Nat. Hist. 5: 1–10.
Schuett, G. W., P. F. Fernandez, D. Chizsar, and H. M. Smith. 1998. Father-
less sons: a new type of parthenogenesis in snakes. Fauna 1: 20–25.
Schuett, G. W., M. Höggren, M. E. Douglas, and H. W. Greene (Eds.). 2002.
Biology of the Vipers, Eagle Mountain Publishing, LC, Eagle Mountain, Utah.
Schuett, G. W., R. A. Repp, E. N. Taylor, D. F. DeNardo, R. L. Earley, E. A.
Van Kirk, and W. J. Murdoch. 2006. Winter prole of plasma sex steroid lev-
els in free-living male Western Diamond-backed Rattlesnakes, Crotalus atrox
(Serpentes: Viperidae). Gen. Comp. Endocrinol. 149: 72–80.
Schuett, G. W., R. A. Repp, and S. K. Hoss. 2011. Frequency of reproduction
in female Western Diamond-backed Rattlesnakes from the Sonoran Desert of
Arizona is variable in individuals: potential role of rainfall and prey densities.
J. Zool. 284: 105–113.
Schuett, G. W., R. A. Repp, M. Amarello, and C. F. Smith. 2013a. Unlike
most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed
throughout pregnancy. J. Zool. 289: 101–110.
Schuett, G. W., R. A. Repp, S. K. Hoss, and H.-W. Herrmann. 2013b. En-
vironmentally cued parturition in a desert rattlesnake, Crotalus atrox. Biol. J.
Linn. Soc. 110: 866–877.
Schuett, G. W., R. W. Clark, R. A. Repp, M. Amarello, C. F. Smith, M. R.
Douglas, M. E. Douglas, and H-W Herrmann. 2014. Communal denning
in the Western Diamond-backed Rattlesnake (Crotalus atrox): molecular evi-
dence for kin-related social structure. Biology of the Pitvipers 2, Tulsa, Okla-
Schwenk, K., D. K. Padina, G. S. Bakken, and R. J. Full. 2009. Grand chal-
lenges in organismal biology. Integr. Comp. Biol. 49: 7–14.
Secor, S. M., and J. M. Diamond. 1998. A vertebrate model of extreme physi-
ological regulation. Nature 395: 659–662.
Sexton, O. J., P. Jacobson, and J. E. Bramble. 1992. Geographic variation in
some activities associated with hibernation in Nearctic pitvipers. Pp. 337–346
In J. A. Campbell and E. D. Brodie Jr. (Eds.), Biology of the Pitvipers. Selva,
Shine, R. 1988. Parental care in reptiles. Pp. 275–330 In C. Gans and R. B.
Huey (Eds.), Biology of the Reptilia, Vol. 16, Ecology B. Defense and Life
History. Alan R. Liss, New York, New York.
Shine, R. 1991. Australian Snakes. A Natural History. Cornell University
Press, Ithaca, New York.
Shine, R., and R. T. Mason. 2011. An airborne sex pheromone in snakes. Biol.
Lett. 8: 183–185.
Shine, R., D. O’Connor, and R. T. Mason. 2000. Sexual conict in the snake
den. Behav. Ecol. Sociobiol. 48: 392–401.
Shine, R., L.-X. Sun, M. Fitzgerald, and M. Kearney. 2002. Accidental al-
truism in insular pit-vipers (Gloydius shedaoensis, Viperidae). Evol. Ecol. 16:
Shuster, S. M., and M. J. Wade. 2003. Mating Systems and Strategies. Princ-
eton University Press, Princeton, New Jersey.
Sih, A., A. M. Bell, J. C. Johnson, and R. E. Ziemba. 2004a. Behavioral syn-
dromes: an integrative overview. Q. Rev. Biol. 79: 241–277.
Sih, A., A. Bell, and J. C. Johnson. 2004b. Behavioral syndromes: an ecologi-
cal and evolutionary overview. Trends Ecol. Evol. 19: 372–378.
Sih, A., S. F. Hanser, and K. A. McHugh. 2009. Social network theory: new
insights and issues for behavioral ecologists. Behav. Ecol. Sociobiol. 63: 975–
Smith, C. F., and G. W. Schuett. 2015. Putative pair-bonding in Agkistrodon
contortrix (Copperhead). Northeast. Nat. 22: N1–N5.
Smith, C. F., G. W. Schuett, and M. Amarello. 2015. Male mating success in
a North American pitviper: inuence of body size, testosterone, and spatial
metrics. Biol. J. Linn. Soc. 115: 185–194.
Somma, L. A. 2003. Parental Behavior in Lepidosaurian and Testudinian Rep-
tiles. A Literature Survey. Krieger Publishing, Malabar, Florida.
Stahlschmidt, Z. R., T. C. M. Homan, and D. F. DeNardo. 2008. Postural
shifts during egg-brooding and their impact on egg water balance in the Chil-
dren’s Python (Antaresia childreni). Ethology 114: 1,113–1,121.
Stamps, J. 2003. Behavioural processes aecting development: Tinbergen’s
fourth question comes of age. Anim. Behav. 66: 1–13.
Stamps, J., and T. G. G. Groothuis. 2010. e development of animal person-
ality: relevance, concepts and perspectives. Biol. Rev. 85: 301–325.
Taborsky, M., H. A. Homan, A. K. Beery, D. T. Blumstein, L. D. Hayes,
et al. 2015. Taxon matters: promoting integrative studies of social behavior.
NESCent working group on integrative models of vertebrate sociality: evolu-
tion, mechanisms, and emergent properties. Trends. Neurosci. 38: 189–191.
Taylor, E. N., D. F. DeNardo, and D. H. Jennings. 2004. Seasonal steroid
hormone levels and their relation to reproduction in the Western Diamond-
backed Rattlesnake, Crotalus atrox (Serpentes: Viperidae). Gen. Comp. Endo-
crinol. 136: 328–337.
ornhill, R. 1980. Rape in Panorpa scorpionies and a general rape hypoth-
esis. Anim. Behav. 28: 52–59.
ornhill, R., and J. Alcock. 1983. e Evolution of Insect Mating Systems.
Harvard University Press, Cambridge, Massachusetts.
ornhill, R., and C. T. Palmer. 2000. A Natural History of Rape: Biological
Bases of Sexual Coercion. e MIT Press, Cambridge, Massachusetts.
Tinbergen, N. 1963. On aims and methods of ethology. Zeitschrift für Tier-
psychologie 20: 410–433.
Tinbergen, N. 1966. Social Behavior in Animals with Special Reference to
Vertebrates. Methuen Publishers, London, United Kingdom.
Trivers, R. L. 1972. Parental investment and sexual selection. Pp. 136–179
In B. Campbell (Ed.), Sexual Selection and the Descent of Man, 1871-1971.
Aldine, Chicago, Illinois.
Valone, T. J., and J. J. Templeton. 2002. Public information for the assessment
of quality: a widespread social phenomenon. Phil. Trans. R. Soc. Lond. B Biol.
Sci. 357: 1,549–1,557.
Venkataraman, V. V., J. T. Kerby, N. Nguyen, Z. T. Ashena, and P. J. Fashing.
2015. Solitary Ethiopian wolves increase predation success on rodents when
among grazing Gelada Monkey herds. J. Mammalogy 96: 129–137.
Vonhof, M. J., H. Whitehead, and M. B. Fenton. 2004. Analysis of Spix’s
Disc-winged Bat association patterns and roosting home ranges reveal a novel
social structure among bats. Anim. Behav. 68: 507–521.
Warner, D. A., U. Tobias Uller, and R. Shine. 2013. Transgenerational sex
determination: the embryonic environment experienced by a male aects o-
spring sex ratio. Scientic Reports 3: 2709 doi: 10.1038/srep02709.
Warwick, C., F. L. Frye, and J. B. Murphy. 1995. Health and Welfare of Cap-
tive Reptiles. Chapman & Hall, New York, New York.
Webb, J. K., M. L. Scott, M. J. Whiting, and R. Shine. 2015. Territoriality in
a snake. Behav. Ecol. Sociobiol. 69: 1,657–1,661.
West, S. A., I. Pen, and A. S. Grin. 2002. Cooperation and competition
between relatives. Science 296: 72–75.
Wever, E., and J. Vernon. 1960. e problem of hearing in snakes. J. Aud.
Res. 1: 77–83.
While, G. M., T. Uller, and E. Wapstra. 2009. Family conict and the evolu-
tion of sociality in reptiles. Behav. Ecol. 20: 245–250.
Whitehead, H. 2008. Analyzing Animal Societies: Quantitative Methods for
Vertebrate Social Analysis. University of Chicago, Chicago, Illinois.
Whitehead, H. 2009. SOCPROG programs: analyzing animal social struc-
tures. Behav. Ecol. Sociobiol. 63: 765–778.
Whiten, A., J. Goodall, W. C. McGrew, T. Nishida, V. Reynolds, Y. Sugiyama,
C. E. G. Tutin, R. W. Wrangham, and C. Boesch. 1999. Cultures in Chim-
panzees. Nature 399: 682–685.
Wickham, H. 2009. ggplot2: elegant graphics for data analysis. Available
Williams, G. C. 1966. Adaptation and Natural Selection. Princeton Univer-
sity Press, Princeton, New Jersey.
Williams, R. N., and J. A. DeWoody. 2009. Reproductive success and sexual
selection in wild Eastern Tiger Salamanders (Ambystoma t. tigrinum). Evol.
Biol. 36: 201–213.
Wilson, E. O. 1975. Sociobiology. e New Synthesis. Harvard University
Press. Cambridge, Massachusetts.
Wilson, E. O. 2014. e Meaning of Human Existence. W. W. Norton &
Company, New York, New York.
Wittenberger, J. F. 1981. Animal Social Behavior. Duxbury Press, Boston,
Wolf, M., and F. J. Weissing. 2012. Animal personalities: consequences for
ecology and evolution. Trends Ecol. Evol. 27: 452–461.
Wynne, C. D. L. 2007. What are animals? Why anthropomorphism is still not
a scientic approach to behavior. Comp. Cog. Rev. 2: 125–135.
Yates, F. E. 1979. Comparative physiology: compared to what? Am. J. Physiol.
Yeager, C. P., and G. M. Burghardt. 1991. Eect of food competition on ag-
gregation: evidence for social recognition in the Plains Garter Snake (amno-
phis radix). J. Comp. Psychol. 105: 380–386.
Young, B. A. 2003. Snake bioacoustics: toward a richer understanding of the
behavioral ecology of snakes. Q. Rev. Biol. 78: 303–325.
Young, B. A., and A. Aguiar. 2002. Response of Western Diamondback Rat-
tlesnakes Crotalus atrox to airborne sounds. J. Exp. Biol. 205: 3,087–3,092.