Clinicalreptilebehavior: Lionel Schilliger,, Claire Vergneau-Grosset,, Marion R. Desmarchelier

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Clinical Reptile Behavior

Lionel Schilliger, DVM, DECZM (Herpetology), DABVP (Reptile and Amphibian Practice)a,
Claire Vergneau-Grosset, DVM, IPSAV, CES, DACZMb,*,
Marion R. Desmarchelier, DVM, DACZM, DECZM (ZHM), DACVBc

KEYWORDS
 Snake  Lizard  Chelonian  Tortoise  Turtle  Behavior
 Environmental enrichment

KEY POINTS
 Owners and veterinarians less familiar with reptiles may misinterpret reptile behaviors. Un-
derstanding the natural history of different species is key to interpreting their behavior in
captivity.
 Common reasons for behavioral consultations include hyperactivity, self-mutilation,
frequent biting, abnormal repetitive behaviors, and postural abnormalities.
 Abnormal behaviors identified by owners can be normal, but inappropriate, or abnormal
and secondary to environmental or medical causes.
 Aggression can be induced by various factors, such as fear, pain, resource guarding, or
sex hormones. Appropriate management begins by identifying the cause.
 Addressing behavioral issues involves understanding the root cause, implementing rele-
vant environmental modifications, developing a behavior modification plan, and choosing
medication when appropriate.

Video content accompanies this article at http://www.vetexotic.theclinics.com.

Reptile behavior is complex and varies widely among the approximately 11,000 spe-
cies included in the nonavian reptile class.1 It is estimated that more than 5 million rep-
tiles were kept as pets in 2007 in the United Stated alone.2 North America is the
biggest consumer market for companion reptiles worldwide, with a 22% increase in
the number of animals exchanged since 2002.3 Although pet reptiles are becoming
more common in households, their behavior could be misinterpreted by owners less
familiar with reptile physiology and natural history. Reptile behavior is increasingly be-
ing studied from complex cognition4 to adaptation to spaceflight conditions, where

a
Clinique Vétérinaire du Village d’Auteuil, 35 Rue Leconte de Lisle, Paris 75016, France;
b
Service de Médecine Zoologique, Department of Clinical Sciences, Université de Montréal,
3200 rue Sicotte, Saint-Hyacinthe, Québec J2S 2M2, Canada; c Department of Clinical Sciences,
Université de Montréal, 3200 rue Sicotte, Saint-Hyacinthe, Québec J2S 2M2, Canada
* Corresponding author.
E-mail address: claire.grosset@umontreal.ca

Vet Clin Exot Anim 24 (2021) 175–195


https://doi.org/10.1016/j.cvex.2020.09.008 vetexotic.theclinics.com
1094-9194/21/ª 2020 Elsevier Inc. All rights reserved.
176 Schilliger et al

thick-toed geckos were shown to be able to remain attached to surfaces during


weightlessness.5 Although the fascinating topic of reptile behavior cannot be summa-
rized in a single article, the objective of this article is to help practitioners differentiate
normal from abnormal behaviors in reptiles commonly encountered in veterinary
consultation. Thus, crocodilians, venomous reptiles, and tuataras will not be dis-
cussed in this article. Another goal is to assist practitioners in addressing common
owner complaints regarding reptile behaviors. These may include behaviors associ-
ated with inappropriate husbandry where veterinarians should be able to advise the
owner appropriately.

NORMAL REPTILE BEHAVIOR


In Captive Settings
Knowledge of what constitutes normal behavior is required to identify abnormal
behavior. Because reptiles are ectotherms, their physiology and behavior are influ-
enced by their environment, as evidenced by the dramatic changes in their locomotor,
reproductive, and feeding behavior under differing environmental conditions.
Reptile location in a terrarium is strongly influenced by available ultraviolet light (UV)
and environmental temperature. For instance, captive juvenile leopard geckos (Euble-
pharis macularius) favor behavioral thermoregulation rather than hiding from potential
predators.6 When exposed to excessive temperatures, bearded dragons and spiny
tailed lizards (Uromastyx spp.) keep their mouth open and breath with short, shallow
respirations (polypnea), which should be differentiated from true dyspnea. Tempera-
tures outside of the preferred optimal temperature zone can also induce brumation
or estivation, especially in tortoises of the genus Agrionemys spp. Brumation and esti-
vation are associated with decreased activity, which should not be interpreted as leth-
argy. Snakes spending an extensive amount of time in their water bowls might be kept
in conditions with excessive temperature, but should also be examined to detect
mites, as bathing is a common response to mite infestation. Chameleons rely heavily
on access to UVB light, and studies have shown that they exhibit light-seeking
behavior according to individual vitamin D requirements.7 When stressed, certain rep-
tiles also change body posture; bearded dragons flatten their body dorsoventrally,
while chameleons tend to flatten laterally, vibrate, and stay close to vertical elements.
Whenever juvenile bearded dragons (Pogona vitticeps) encounter conspecifics or are
approached by handlers, they may display circling motions of the forelimbs, which is a
common behavior in this species (Video 1).
Reptiles were once believed to have a low degree of sociality and parenteral care;
however, this hypothesis is increasingly questioned by recent findings. Chelonians
can learn visual cues by observing conspecifics,8 and skinks can participate in com-
plex social organization.9 Reptiles display a wide diversity in maternal care, such as
egg brooding in ball pythons (Python regius), protective maternal behavior toward
hatchlings among prehensile-tailed skinks (Corucia zebrata), and even sharing shel-
ters with conspecifics among certain lizards (Fig. 1). Conspecific interactions among
reptiles typically increase during breeding season, as evidenced by complex nuptial
parades in anoles (Anolis spp.).10 Madagascar boas (Acrantophis madagascariensis)
fight using their spurs, while male box turtles (Terrapene spp.) will sometimes place
their hind limbs between the carapace and plastron of the female during mating to pre-
vent the female from closing her shell.11
Reptiles communicate through visual and vocal signals, as well as through phero-
mones. Among visual signals, color changes and dewlap expansion (throat fan) in
anoles and frilled lizards (Chlamydosaurus kingii) (Fig. 2) can be impressive, and
Clinical Reptile Behavior 177

Fig. 1. Example of a gregarious behavior in which a male and a female leopard gecko (Eu-
blepharis macularius) share the same shelter despite being provided multiple hiding places
at the same temperature. (Courtesy of C. Vergneau-Grosset, DVM, Saint-Hyacinthe, Canada.)

they are typically displayed by males to attract females.10 Male anoles with heavy mite
burden display less frequently and progressively lose dewlap coloration.10 Many spe-
cies, including male green iguanas (Iguana iguana) and anoles display head bobbing
and flex/extend their arms (push-ups) as an intimidation signal or to indicate territori-
ality.12 The throat of bearded dragons darkens in situations of agonistic behavior to-
ward a conspecific. When occurring in individually housed animals, it is often
caused by their reflection on glass surfaces. Green iguanas and bearded dragons
can approach competitors with a slight head tilt, not to be mistaken for a vestibular
syndrome. Chameleons can change light reflections on their skin by rearranging me-
lanosomes within their skin chromatophores in order to change their color. Changes in
colors are sudden and indicate differing physiologic or behavioral changes. For
instance, female veiled chameleons (Chameleo calyptratus) show typical colors during
folliculogenesis characterized by blue and orange spots. Pregnant female chameleons
will also show a typical color pattern (Fig. 3). In male veiled chameleons, mathematical
models have shown a correlation between the brightness of the body stripes and head

Fig. 2. Frilled-necked lizard (Chlamydosaurus kingii) spreading out its frill and gaping its
mouth when frightened, displaying bright orange scales. (Courtesy of K. Daoues, Paris,
France.)
178 Schilliger et al

Fig. 3. Example of a pregnant female chameleons (Chamaeleo calyptratus) showing a


typical color pattern. (Courtesy of C. Grosset, DVM, Saint-Hyacinthe, Canada.)

color, and the likelihood of engaging in fights.13 Skin color in reptiles can also be
affected by nutritional factors and environmental temperature. For instance, lizards
on a diet high in carotenoids will display brighter red-orange colors.14
Certain visual signals that require UV vision are not detectable to the human eye.15
Many reptiles possess UV vision, including members of the Iguanidae, Gekkonidae,
and snakes.16 Hence, certain male lizards will copulate with females only when they
harbor a receptive pattern, which is only visible under UV light.16 Thus, lack of
breeding success should not be necessarily interpreted as a behavioral problem, as
visual deficits or inappropriate cues can interfere with mating.
Reptiles also communicate through vocal signals. For instance, tokay geckos
(Gekko gecko) are able to adjust their vocalization to the surrounding noise intensity,
indicating a sophisticated degree of communication ability.17 Repeated calls are
normal in this species and should not be misinterpreted for distress by owners
(Video 2). Reptiles also perceive pheromones via their vomeronasal organ and perform
repeated tongue flicks when exploring a new environment.
Normal feeding and drinking behaviors can sometimes raise questions from owners.
Chameleons are unable to drink from bowls as they lick water off of leaves in the wild;
therefore, a drip system or spraying water on plants is necessary in captivity. Unusual,
but normal, feeding behaviors include juvenile green pythons moving their tails as a
lure to catch prey. Geckos frequently eat their molt (Fig. 4). Whether this behavior is
related to protein recycling, a defense mechanism against predators, or both remains
unknown. Wood turtles (Glyptemys insculpta) stomp their feet to create vibrations to
mimic rain in an effort to lure earthworms to the surface.18 Lithophagy (ingestion of
soil and substrate) is considered normal in many tortoises and might be a way to ac-
quire mineral nutrients.

During Handling, Physical Examination, and Medical Procedures


During clinical examination, reptiles will behave in various fashions depending on the
taxa involved. Tortoises tend to lie motionless on the examination table and retract
completely into their shells as a means of self-defense. Large African tortoises (leop-
ard tortoises [Stygmochelys pardalis]) and African spurred tortoises (Centrochelys
sulcata) possess a powerful retraction reflex, and the clinician must be careful
Clinical Reptile Behavior 179

Fig. 4. A carrot-tail leopard gecko (Eublepharis macularius) after ingesting its molt. The re-
maining molt is visible on its head. (Courtesy of C.Grosset, DVM, Saint-Hyacinthe, Canada.)

when positioning his or her hands around the head, neck, and limbs, especially at the
level of the prefemoral pits and the axillofacial depressions. In a testament to their
strength, these species can sometimes only be properly examined under sedation.
Smaller species can also display a retracting reflex (Burmese star tortoises [Geoche-
lone platynota] and Indian star tortoises [Geochelone elegans]). Some species can
enclose themselves within their shell by use of a cranial hinged plastron (eg, Mada-
gascarian spider tortoises [Pyxis arachnoides]), dual cranial and caudal hinged plas-
trons (eg, box turtles [Terrapene sp., Cuora sp.]), or a hinged caudal carapace (eg,
Bell hinge-back tortoises [Kinixys belliana], forest hinge-back tortoise [Kinixys
homeana]).
In contrast, nonapathetic aquatic turtles tend to be active and move quickly on the
examination table. When handled, they usually thrash around and can inflict severe
scratches or bites wounds (Fig. 5). Like tortoises, they often urinate on the consulta-
tion table if stressed. Some species (eg, African helmeted turtle [Pelomedusa subrufa])
can expel malodorous cloacal glands secretions when stressed.

Fig. 5. Snapping turtle (Chelydra serpentina) trying to bite when handled. (Courtesy of L.
Schilliger, DVM, Paris, France.)
180 Schilliger et al

Large lizards (eg, green iguanas, monitor lizards [Varanus sp.], tegus [Tupinambis
sp.]) can bite, tail whip, or inflict serious scratches in self-defense. Inflation of the
body, opening the mouth, unfolding the gular dewlap (where present), standing in
an elevated position, and jerking head movements are displayed to intimidate preda-
tors or rivals, or impress a potential mate (Video 3). The green iguana often adopts a
U-shaped position on the examination table, presenting its head and tail in readiness
to attack. Iguanas tend to attempt escape; a firm restraint is therefore crucial by hold-
ing both forelimbs against the thorax and both hindlimbs against the tail. Bearded
dragons (P vitticeps, P henrylawsoni) are generally docile and can be handled easily,
without biting or trying to escape. They can become cataleptic and immobile when
held in a supine position, but will revert to a normal state once replaced into the prone
position. This behavior, associated or not with the oculocardiac reflex, can be
exploited to facilitate clinical examination. However, there are few data on the impacts
of this procedure (oculocardiac reflex) on the stress of the animals. It is unknown
whether the oculocardiac reflex eliciting vagal stimulation can be part of a fear-free ex-
amination, or whether applying ocular pressure is actually uncomfortable. Male cha-
meleons sometimes adopt a defensive posture and can inflict a painful bite (eg,
veiled chameleons). Some species (eg, leaf chameleons [Brookesia sp.], Oustalet cha-
meleons [Furcifer oustaleti]) vibrate when handled, similar to that of a phone vibrator,
which should not be a cause of concern.
When seized from behind the helmet, chameleons and some other species (eg,
geckos) tend to open the mouth, which facilitates examination of the oral cavity
(Fig. 6). Some lizards (eg, crested geckos [Correlophus ciliatus], day geckos [Phel-
suma sp.]) display an autotomy reflex by breaking off their tail at the level of predeter-
mined fractures on the coccygeal vertebrae (Fig. 7). Vibration of the tail precedes this
action, in which case the animal should be quickly released to prevent an amputated
tail and a disgruntled owner. The tail can also break off when a thrashing lizard is held
firmly by the tail. Day geckos can spin during handling and remove a part of their skin,
exposing underlying subcutaneous tissues. Geckos belonging to the genus Geckole-
pis spp. can shed their skin, which is a natural response against predation.

Fig. 6. When seized from behind the head, some lizards (such as chameleons and geckos)
tend to open the mouth, which facilitates examination of the oral cavity. (Courtesy of L.
Schilliger, DVM, Paris, France.)
Clinical Reptile Behavior 181

Fig. 7. Autotomized tail in a leopard gecko (Eublepharis macularius). (A) Individual with a
recently autotomized tail. (B) Autotomized distal tail (spontaneous movements may be pre-
sent on the separated tail for a few seconds). (Courtesy of C.Grosset, DVM, Saint-Hyacinthe,
Canada.)

Surprisingly, intraspecific aggression, and not predation, has been shown to be the
major cause of tail loss in 2 gecko species on Mediterranean islands.19 Some geckos
utter a loud barking cry when seized (eg, tokay gecko [G gecko]). Other species-
specific behaviors include that of the girdled lizard (Ouroborus cataphractus), which
seizes its own tail in its mouth to take the appearance of an armadillo (Fig. 8), or the
horned lizard (Phrynosoma sp.), which can eject blood from ocular and periocular
blood vessels up to 1 m in distance.
The behavior of snakes is family-specific. Colubrids are usually lively and seek to
escape as soon as their cage is opened. During handling, they will incessantly seek

Fig. 8. Girdled lizard (Ouroborus cataphractus), seizing its tail in its mouth to take the
appearance of an armadillo. (Courtesy of C. Paillusseau, DVM, Paris, France.)
182 Schilliger et al

to escape the person’s grasp. Some species (eg, aquatic colubrids) secrete
malodorous musk scents from their cloacal glands. Boids are more indolent when
the transport bag or box is opened and tend to remain within the container. The
constrictor boa (Boa constrictor), the Burmese python (Python molurus bivittatus),
the reticulated python (Malayopython reticulatus), the green tree python (Morelia viri-
dis), and the emerald tree boa (Corallus caninus) are among the many boids that
can bite in self-defense. On the other hand, the ball python is rarely aggressive and
adopts a rather peculiar behavior when stressed; it wraps itself into a ball, its head
buried into the rings formed by its body. Boids and colubrids can produce a loud noise
during handling because of quick ejection of the air from the lung through the small
tracheal opening. Most snakes handled shortly after a meal will regurgitate in response
to stress and the attempt to escape. Autotomy is also described in African colubrids
belonging to the genus Psammophis spp., Natriciteres spp., and Hapsidophrys spp.11
When handling venomous snakes, it goes without saying that particular care must
be taken to avoid being bitten. Rattlesnakes will shake their rattle at the end of their
tails to warn predators. Cobras flatten their necks in the shape of a cap and stand
up on their curved body before projecting themselves forward to bite. Some nonven-
omous snakes mimic this behavior, notably the North American colubrids (Lampropel-
tis sp. and Pantherophis sp.), which shake the end of their tail when cornered.
Hognose snakes (Heterodon sp.) flatten their neck by adopting a typical cobra position
to confuse predators and can also display astonishing thanatosis when threatened.
The thanatosis display consists of convulsions in the supine position and then mimicry
of a state of apparent death with the mouth open, extruded tongue, and expressing a
putrid odor from cloacal glands. This behavior is also well described in the grass snake
(Natrix helvetica). Tail display in also a prey-predator defensive mechanism that can be
observed in the South American hognose snake (Xenodon durbignyi) (Fig. 9).

Fig. 9. Tail display in a prey/predator defensive mechanism in a South American hognose


snake (Xenodon durbignyi). (Courtesy of C. Paillusseau, DVM, Paris, France.)
Clinical Reptile Behavior 183

When placed back into a cotton transport bag, most snakes will typically seek to exit
it immediately. It is, therefore, advisable to tighten the bag around the forearm of the
arm holding the snake before releasing the snake into the bag.

Behavioral Considerations During Hospitalization


Although reptile behavior is species-specific, the flight reflex is near universal across
species. Turtles and tortoises constantly attempt to escape their terrarium, especially
when kept in a cramped space. Some species of snakes (eg, colubridae) will exploit
every opportunity to escape, including the smallest opening in their terrarium, while
larger and more powerful snakes are able to slide open unlocked terrarium doors.
Some species of lizards (eg, Physignathus cocincinus) will rub their rostrum against
transparent terrarium panes during the entire period of their hospitalization, resulting
in self-administered rostral wounds (Fig. 10).20 In such species, terrariums with trans-
parent panes should be avoided.
To avoid behavioral abnormalities in hospitalized reptiles, it is important to have a
dedicated room heated to 28 C for most species. Nonreptile patients, such as
dogs, cats, ferrets, rats, or rabbits must be kept in a separate room as they are reptile
predators or preys, and their presence can cause psychological stress and trigger a
dramatic flight reflex. Similarly, reptile patients should not be in eyesight of other pred-
atory reptiles (eg, lizards and snakes). Each terrarium should be equipped with a sepa-
rate hotspot to create a warmer zone heated at the species’ maximal preferred
temperature (typically 32 C). Shade-dwelling species should be offered the appro-
priate amount of filtered light and UVBs. It has been shown that UVAs can trigger
agonistic behaviors in certain lizards (eg, green anole [Anolis carolinensis]).21 Dietary
supplements can also affect animal behavior; in 1 study, basking time (necessary in
the production of pre- and provitamin D3) decreased as vitamin D3 supplementation
was increased.7 Similarly, exposure to natural sunlight can increase aggression levels
in some species by increasing testosterone levels (eg, green anole [A carolinensis]).22
A hiding place should be present in every terrarium to allow the reptiles to hide from
visual stressors. In the case of gestating females, a laying box must always be

Fig. 10. Self-administered rostral wounds in a Chinese water dragon (Physignathus cocinci-
nus) after rubbing his rostrum against transparent terrarium panes. (Courtesy of L. Schilliger,
DVM, Paris, France.)
184 Schilliger et al

provided (eg, humid sand); this is especially crucial in the case of patients with egg
retention, where a suitable laying box can help trigger oviposition. Lizards and turtles
ingest terrarium substrate when alimentary fibers or minerals are deficient in the diet,
and reptiles should be monitored when offered nesting material. Snakes sometimes
ingest pads or paper towels if they can smell traces of prey animals.

MAIN PRESENTATIONS FOR BEHAVIORAL PROBLEMS IN PRACTICE


Restlessness and Hyperactivity
Restlessness and hyperactivity are commonly related to overheating, which increases
thermodependent metabolism and activity levels. Agitation, as evidenced by continu-
ously seeking to escape the terrarium, should first prompt verification of the terrar-
ium’s temperature setting. Overcrowding, cohabitation with a territorial or
aggressive specimen, sexual arousal, and severe hunger can also cause hyperactivity.
In female aquatic and terrestrial turtles, restlessness can also be suggestive of
imminent oviposition; a laying box should be immediately provided to avoid egg reten-
tion. Restlessness can also be observed in stressed or wild-caught snakes.

Self-Mutilation
Self-mutilation in reptiles can have various causes. Lizards indefatigably rubbing their
rostrum on transparent panes of a terrarium can become a compulsive repetitive
behavior (especially in water dragons), which can result in severe rostral trauma, even-
tually leading to maxillary and mandibular osteomyelitis (see Fig. 10). This behavior
can also be caused when lighting from inside the terrarium creates a reflective surface
on the glass, causing the lizard to confuse its reflection with a congener (especially
chameleons and green iguanas). In this instance, it is recommended to apply plasti-
cized films onto the glass or plastic panes to reduce reflections. Stressors within
the terrarium that triggers the animal’s flight reflex can also cause rubbing of the
rostrum against the terrarium.
Autotomy is a behavioral reflex that involves self-amputation of the tail to escape a
predator’s grasp or cause a diversion that allows for escape (see Figs 7 & 12). It is
seen in the Cordylidae, Dactyloidae, Dibamidae, Gerrhosauridae, Gymnophthalmidae,
Lacertidae, Leiocephalidae, Liolaemidae, Opluridae, Shinisaudidae, Sphenodontidae,
Xantusiidae families, as well as some species within the Agamidae, Iguanidae, and
Teiidae families.11 Geckos of the genus Correlophus sp. can also remove their stitches
after surgery, which is a form of self-induced trauma.
Thermal burns are a form of unintentional self-mutilation that arises when thermal
gradients are not respected (eg, excessive hot spot or excessive cold spot), leading
reptiles to remain stuck on a heat source from which they suffer severe burns.

Aggression
Interspecific and intraspecific aggressions are commonly seen in pet reptiles. Biting is
the most common manifestation of aggression toward people. Aggression is a natural
behavior with many different functions for reptiles. Predatory aggression is the silent
and rapid aggression leading to the death and ingestion of a prey. Territorial aggres-
sion is displayed toward conspecifics and other intruders when defending a certain
area, usually to defend limited resources, including females.23 Not all reptile species
are territorial in the wild. Intraspecific aggression also occurs during the breeding sea-
son between males fighting for females. Finally, fear-based aggression occurs when a
reptile feels threatened and chooses fight instead of flight.24
Clinical Reptile Behavior 185

All of these types of aggression can be seen in captivity in normal expected contexts
or as displaced inappropriate behaviors. Reptiles rely heavily on smell and pheromone
detection to hunt prey. Therefore, it is advisable not to handle rodent bedding or live
prey before accessing a carnivorous reptile enclosure, as this could result in an acci-
dental predatory aggression. To condition reptiles to feed only in certain areas and
improve owner’s safety, some individuals benefit from being fed exclusively outside
of their terrarium, in a different tank. Territorial aggression is often overdiagnosed
when a reptile bites the hand that is entering the terrarium. Although this is an appro-
priate differential diagnosis in this context, most reptiles actually bite because of fear
of the upcoming handling and potential previous negative experiences in a similar sit-
uation. To avoid this situation, owners should be educated to not handle snakes during
or prior to molt. Learning the reptile body language is also key to bite prevention, as
warning signs are often ignored by the owners. For instance, corn snakes usually
display vibrations of the distal part of the tail before biting. Many snakes will display
an S shape with their neck before striking. Bearded dragons may develop a black gular
region prior to biting. Green iguanas may display head bobbing or a tail flick before
swiping with their tail or biting. Chameleons may take a darker color and open the
mouth (Fig. 11). Reviewing videos of the behavior problems with the owners might
help target some individual fearful behaviors. Appropriate handling to improve reptile
comfort should also be taught to owners, such as handling the reptile with 2 hands,
never letting the caudal part of the body hang down, and refraining from holding the
snake forcefully behind its head. Pain-related aggression occurs in reptiles. One of
the authors (CVG) has seen this occur in a carpet python presented with a pancreatitis.
Therefore, potential causes of pain should be investigated when a reptile is presented
for an acute onset of repetitive biting. Intraspecific aggression is normal when testos-
terone increases during the breeding season in many species. It is important to
research the species natural history to avoid inappropriate social groupings. For
instance, intact adult male leopard geckos should never be kept in the same terrar-
ium.25 Intraspecific biting may also be misinterpreted by owners, especially during
mating behavior, which often involves female neck biting by the male.26 Aggression
behavior linked to sex hormones could be redirected toward people as is commonly
seen in mature male green iguanas. Only an accurate identification of the type of

Fig. 11. Color darkening in a veiled chameleon (Chamaeleo calyptratus). (Courtesy of L.


Schilliger, DVM, Paris, France.)
186 Schilliger et al

aggression allows for appropriate management of the situation. Treating fear aggres-
sion like territorial aggression could result in a vicious circle of increased fear and bite
intensity.

Repetitive Behaviors
Owners may consult for repetitive behaviors observed in their reptiles. Again, practi-
tioners should attempt to different normal from abnormal behavior. Reptiles trying
to escape an inadequate environment may move back and forth in front of a window
in an attempt to find an exit from the terrarium. Pregnant females trying to dig a nest
may also attempt to dig frenetically even if no substrate is present in the habitat. In
these cases, repetitive nonproductive behaviors are the result of a suboptimal captive
environment.
Alternatively, certain repetitive movements may reveal underlying medical prob-
lems. For instance, chelonians displaying rhythmic limb movements may in fact be
dyspneic. Abnormal repetitive movements can also be associated with stress. Similar
to what is described in mammals, it is documented that certain prenatal factors, such
as egg incubation temperature, can predispose individual lizards to developing ste-
reotypic behaviors.27

Postural Abnormalities
Reptiles may be presented for postural abnormalities. In this case, strictly behavioral
abnormalities should be differentiated from medical problems.
Turtles floating with 1 side tilted toward the surface may have asymmetrical lung le-
sions or dilations of the gastrointestinal tract by gas.28
Neurologic signs should be differentiated from musculoskeletal problems, behav-
ioral signs, and developmental abnormalities. Certain selected reptile morphs will
often display neurologic abnormalities affecting their locomotion and body posture.
This is the case of spider ball pythons and jaguar carpet pythons (Morelia spilota),
which develop a wobble syndrome of genetic origin characterized by head tremors,
incoordination, and lack of righting reflex.29
Head tilt may be of behavioral or neurologic origin in certain lizards. If the origin is
behavioral, this sign will be intermittent. Opisthotonus should be differentiated from
dyspnea in snakes; indeed, snakes in respiratory distress may keep their head and
cranial part of the body toward the ceiling and wave it back and forth laterally. This
behavior may be an attempt to clear the upper airways as mucus may fall toward
the lung with gravity. In case of compensatory behavior associated with dyspnea, res-
piratory sounds may be heard; open mouth breathing may be present, and gular
breathing may be visible. Differential diagnoses for this behavior include true opistho-
tonus, which may be caused by pathogens affecting the central nervous system, or
thiamine deficiency.
Lack of righting reflex should be differentiated from catalepsy, a state where reptiles
retain rigidity and may not return to sternal position. Catalepsy or thanatosis is a phys-
iologic mechanism described in certain ophidian species such as grass snakes (Natrix
natrix) or hog-nosed snakes (Heterodon spp.).30 This behavior is thought to be a de-
fense mechanism discouraging predators from attacking the snake.

Loss of Appetite Related to Improper Diet or Husbandry


Partial or complete anorexia in reptiles can be the result of a poor quality diet, inade-
quate environmental conditions, or pain.31 Failure to meet nutritional requirements,
such as feeding animal tissue to a herbivore or plant material to a carnivore, or
providing species-inappropriate prey can induce eating and drinking disorders. It
Clinical Reptile Behavior 187

should be noted that for many species, dietary preferences change with age, espe-
cially among omnivores, such as bearded dragons. Feeding behavior has been shown
to be a marker of postoperative pain in snakes.31
Similarly, abnormally low or high ambient temperature or hygrometry can affect
drinking behavior. Species-specific hydration behavior should be taken into account
for every species. For example, chameleons drink only water that is beading on sur-
faces (eg, rocks or leaves), and the absence of a dripper or misting system in a chame-
leon terrarium can cause dehydration.
Pain-Related Behavioral Issues
Recognizing and characterizing pain in animals are often difficult (Table 1). In compar-
ison to higher vertebrates commonly seen in veterinary practice, reptiles are even less
able to provide interpretable information on the intensity and character of nocicep-
tion.32 According to the International Association for the Study of Pain, pain is defined
as an unpleasant sensory and emotional experience associated with actual or poten-
tial tissue damage, or described in terms of such damage.33 This definition includes a
central modulation of pain that is not confirmed in reptiles devoid of neocortex. There-
fore, the term nociception is more rigorous in certain reptiles, while pain can be used in
chelonians who have a neocortex. Identifying nociception in reptiles thus requires
careful observation to discriminate normal behavior from behavior possibly indicative
of discomfort (Figs. 12 and 13).34 Feeding delay may be an interesting indicator of
nociception in snakes.31 However, certain changes can be subtle in reptiles. For
more information about nociceptive signs and antinociception in reptiles, readers
should refer to other reviews.35,36

ADDRESSING BEHAVIORAL ISSUES

Reptiles are rarely presented to veterinarians primarily for a behavioral issue, but
rather to address the observed consequences of an inappropriate behavior. This

Table 1
Behavioral signs of nociception and pain in reptiles

The Following Clinical Signs May Be Related to Pain in Reptiles:


Snakes Chelonians Lizards
Reduced appetite, delayed Reduced appetite Reduced appetite
striking
- Closed eyelids Closed eyelids
- Head and neck stretched Elevating and extending
in and out of the shell their head
Biting when handled Biting when handled Biting when handled
- Lameness Lameness
Abnormal posture Abnormal posture Abnormal posture
- - Color changes
Abnormal respiratory Abnormal respiratory Abnormal respiratory
movements movements movements
Restless, agitation during - -
handling
Body less coiled at the site - Arching the back
of pain Avoid ventral recumbency

Data from Refs.31,32,34–36


188 Schilliger et al

Fig. 12. Spayed female veiled cameleon (Chamaeleo calyptratus) displaying pain and
discomfort (trying to bite) when handled. (Courtesy of L. Schilliger, DVM, Paris, France.)

might be because some owners are not able to recognize behavioral abnormalities,
do not know veterinarians can provide them with solutions to these issues, or
because reptiles do not display abnormal behavior as much as domestic species
do. Pet reptiles have not been domesticated; therefore, selection of aberrant behav-
iors or neurotransmitter diseases is less likely to have occurred. In parallel, genetic
diversity is generally preserved, and inbreeding is less likely to affect the behavior
of captive reptiles. However, captive environment and life as pets can have some
significant effects on reptile mental health. Reasons for behavior consultations
include interspecific aggression (toward people or other species), intraspecific
aggression, and self-mutilation as already mentioned. Every patient with behavioral
issues will benefit from a systematic approach to reach an accurate diagnosis and
then choose the most appropriate management plan.37 This approach includes get-
ting a thorough history, a behavioral analysis, and a medical evaluation.37 When po-
tential causes are identified for the problem behavior, a combination of behavior
modification, environmental adjustments, and/or medication can be appropriately
implemented.

Fig. 13. Closed eyelids and lethargy can be signs related to pain in lizards (Pogona vitticeps).
(Courtesy of F. Gandar, DVM, Liège, Belgium.)
Clinical Reptile Behavior 189

Getting to a Diagnosis Through a Systematic Approach


Failure to appropriately diagnose behavioral issues is often because of the absence of
an organized approach that should be similar to that used for medical work-ups.37
Every case should be considered unique even if the presentation appears similar; a
water dragon can hurt its rostrum because the terrarium is too small, because of
loud noises in the environment, or because a cat is jumping on the sides of the enclo-
sure. Thus, the same behavior in the same species resulting in the same physical con-
sequences can have various causes that will require different approaches. In order to
establish a thorough list of differential diagnoses for the behavioral issue, the following
3 steps should be considered, in no particular order:
Taking a thorough history is an important part of every reptile consultation.
When addressing a behavioral issue, review of the diet and the environment is as
critical as for any medical presentation.
Rearing situation, breeding history, previous social environment, complete medical
history, and play, elimination, sleep, and exploratory patterns should be reviewed
if applicable.
Many environmental modifications may be identified at that stage to help decrease
the problem behavior and improve the overall animal health and welfare. And although
rearing history cannot be changed for the current case, recognizing predisposing fac-
tors might help prevent similar cases from occurring in the future. It is known, for
example, that incubation temperature can affect gecko behavior.38 Behavior analysis
will determine in which context the problem behavior occurs, what the triggers are,
what the behavior looks like, and what the consequences for the animals are. This
will allow one to adjust the environment to modify the problem situation, to remove
environmental triggers if present, and to work on consequences. If the animal repeats
the behavior, it is most likely reinforcing to the animal, in a way that can be obvious or
sometimes difficult for practitioners to comprehend. This analysis will lead to the
behavior modification plan, a key to the therapeutic success. Last, but not least, an
exhaustive physical examination with appropriate diagnostics is essential to establish
potential involvement of an underlying medical condition.

Behavior Modification in Pet Reptiles


Most behavior problems will be more effectively managed if a behavior modification
plan is implemented. It is especially important in cases of aggression toward people.
Identification of the context and the triggers of the aggression will allow for a better pre-
vention of the aggression. For example, if a snake bites every time the owner puts his or
her hand in the terrarium when the snake is hungry, the authors could recommend alter-
native ways to interact with the animal. The snake could be gently transferred with a
hook into a container so the owner could clean the terrarium. Ideally, the snake could
be trained to target and then to voluntarily transfer into another space where it could
be fed or exercised while the cage is accessible to the owner.39 Adjusting the diet
and feeding in a different area could also be a good option. Cases of fear-based aggres-
sion should focus on allowing the reptile to escape the threat, removing the fearful stim-
ulus as much as possible, and interacting in a positive way with the animal (ie, target
training). Predictable interactions are also reassuring for reptiles and will decrease
fear-induced behavior. Independent of the primary cause of the aggression, whether
it was fear, territorial, testosterone-related, or predatory, the animal has learned that
aggression functioned well to achieve its goal. Although one can often address the pri-
mary cause with drugs and environmental changes, only a behavior modification plan
190 Schilliger et al

will teach the reptile which alternative behavior is more appropriate to reach the same
reinforcing consequence. If one can provide it with an even more reinforcing conse-
quence to this alternate appropriate behavior, it will most likely make the right choice
for both parties. Target training is easily achieved in most chelonians and lizards, and
although slightly more challenging, can also be used in snakes (Videos 4 and 5). Results
can be reached within days with turtles and lizards and within a few weeks with most
snakes. Excellent education groups and resources are available on the Internet and
can provide training and support to an owner willing to start training his or her pets.
Behavior modification techniques can also be useful for patients with specific medical
conditions. With biomedical training, captive reptiles can be weighed, injected, trained
for voluntary blood draws, and stand still for nail filing or wound care.40 Food is the most
common reinforcer used with reptiles (eg, insects, fruit purees, baby food, and nectar),
but scratching under the neck for lizards or on the shell for chelonians can also be
preferred by some individuals (Video 6). The reader is referred to the article about
behavior modification in this issue for more information.41

Environmental Enrichment for Behavior Problems


Most reptiles presented in consultation benefit from environmental changes to
improve their health. Additional adjustments can easily be implemented to enhance
their behavior and welfare. Enrichment increases animal choice and control over their
environment, and promotes species-appropriate behaviors.42 Providing hiding places
will help resolve fear aggression cases. Promoting exercise with enrichment items
such as climbing walls, platforms, branches, and paper rolls is likely to reduce stress
and boredom and will encourage normal behavior.4 Offering appropriately sized ter-
rariums is important, but inciting reptiles to display natural behaviors, even in the
smallest quarantine containers, is critical (Video 7). Objects that are easily available
can be used to enrich small snake enclosures (Fig. 14). Animals do not perform behav-
iors that serve no purpose. Behavioral thermoregulation is a key activity in reptiles.
Reptiles need a thermal gradient and should not have to choose between a warm
place or a place to hide. Providing resources and enrichment throughout an appro-
priate thermal gradient can, therefore, reduce stress and inappropriate behaviors.11
Finding the right balance between safety, hygiene, and enrichment when choosing
the substrate for a pet reptile can be challenging. If natural substrates like sand or

Fig. 14. Objects that are easily available can be used to enrich small snake enclosures, as
shown with this Thai bamboo ratsnake (Oreocryptophis porphyraceus coxi). (Courtesy of
L. Petrella, Calgary, Canada.)
Clinical Reptile Behavior 191

Fig. 15. Black and white tegu (Salvator merianae) using a dog food toy as enrichment.
(Courtesy of J. Baldwin, Totton, UK.)

soil cannot be used on a regular basis in the terrarium, they could still be offered as
enrichment under supervision. For example, lizards could be allowed to hunt in a
sand box (Video 8). Feeding toys and food puzzles for dogs and cats can be used
by reptiles (Fig. 15). Most plastic toys float and can be given to aquatic species. Socks
provide great additional hiding places for snakes. Adapting the social environment is
essential, as aggression is common when keeping a nonsocial species at unnatural
high densities.43 Many reptiles are relatively solitary as adults, but can be social and
benefit from group housing when younger (eg, crocodilians and iguanas) or even for
life (eg, geckos) (see Fig. 1; Video 2). Some species even exhibit stable social grouping
and family systems (eg, Australian black rock skinks [Eugernia saxatilis] and great
desert skinks [E kintorei]).44

Behavior-Influencing Medications
True anxiety disorders are uncommon in pet reptiles. The use of psychotropic drugs in
an attempt to control normal behaviors displayed by reptiles placed in stressful situ-
ations, such as keeping multiple males without any possibility to escape, should not
be recommended. Environmental changes should always be implemented when
necessary. It is likely that aggression is in part regulated by monoamine neurotransmit-
ters in reptiles as it is in other species.45,46 However, the use of psychotropic drugs
should be reserved to cases where the animal’s welfare is affected by a condition
impairing normal neurotransmission (ie, anxiety disorders) or only temporarily before
environmental adjustments are made. These medications aim at restoring normal
neurochemical balance in some neurotransmitter pathways, but are unlikely to be effi-
cient to help animals with normal neurotransmitter function in an abnormal situation.
By asking if most reptiles would behave in a similar way if placed in the same context,
one can differentiate between an inappropriate, but normal behavior, and an aberrant
behavior that could benefit from psychotropic medication. There is no information in
the literature on the use of short-acting medication (ie, trazodone) that could be useful
to relieve fear, anxiety, and stress during hospitalization and transport in reptiles.
Further research is required in this area.
Normal elevation of blood testosterone appears associated with increased
aggressive behaviors in males of various species.47,48 Intraspecific aggression dur-
ing the reproductive season has been favored by natural selection and can be redir-
ected toward people in captivity. Although normal, these behaviors can be
192 Schilliger et al

problematic and even dangerous in some species. If the individual is not part of a
breeding program, its welfare can be affected by these seasonal increases in sex
hormones as they encourage natural behavior that cannot take place and might
create frustration, leading to redirected aggression toward owners. Chemical or sur-
gical castration could, therefore, be considered.49,50 Although more studies are
required, timing of intervention appears to be important. Reduction of testosterone
levels is best achieved if the treatment is applied before the initial increase.48 Celio-
scopic and celioscopy-assisted orchiectomy has been safely used in several spe-
cies, including chelonians and iguanas.50,51 Deslorelin implants have shown
promising results to reduce gonadotropin levels in some species in anecdotal re-
ports (ie, bearded dragon and green iguanas),52,53 but not in others (ie, yellow-
bellied sliders [Trachemys scripta]).54
Observing reptile behavior proves captivating, as one can continuously learn more
about species-specific behavior and individual preferences. A better understanding of
their body language is the first step to make the right diagnosis, medical or behavioral.
As knowledge improves on what is normal for them to do, clinicians are better equip-
ped to recognize abnormal findings earlier in the process. Although the science of
reptile welfare is still in its infancy, it has come a long way from keeping reptiles in
barred environments to enriched flexariums promoting natural behaviors. Training
reptiles with positive reinforcement is getting more and more popular in the owner
community and is a great way to start communicating with pet reptiles in a language
they can understand. All of these changes strengthen the reptile-owner bond and
result in a better welfare for the pet and in an increased level of veterinary care.

CLINICS CARE POINTS


 Hyperactivity and self-mutilation may be associated with inappropriate environ-
ments in reptiles. Thus, taking a thorough history is strongly recommended.
 Biting may be associated with improper handling technique and/or pain, which
should be investigated through a medical approach.
 Postural abnormalities are often a clinical sign of medical problem, and should be
investigated with advanced diagnostic tests as needed.

DISCLOSURE

No conflict of interest to disclose.

SUPPLEMENTARY DATA

Supplementary data related to this article can be found online at https://doi.org/10.


1016/j.cvex.2020.09.008.

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