Abstract

Reptiles have traditionally been considered unthinking and unfeeling animals. However, recent research has revealed complex intelligence, cognition, and behaviors in various reptile species. Many owners, keepers, and veterinarians are now considering and discussing the mental well-being of reptiles in captivity—including providing enrichment through diet, husbandry, and behavioral training. Enrichment benefits reptiles by encouraging natural behaviors, increasing choice, and enhancing welfare. Behavioral training can be utilized to provide enrichment, reduce stress, facilitate veterinary care, and improve human-animal interactions. This masterclass lecture will include reviews of reptile intelligence and cognition, unique reptile behaviors, enrichment opportunities in captivity, and behavioral training of reptiles.

Introduction

Reptiles have traditionally been considered unthinking and unfeeling animals.¹ However, recent research has revealed complex intelligence, cognition, and behaviors in various reptile species.¹ Coverage of this research in popular science, media, and herpetology magazines has increased public appreciation for reptile behavior. As the popularity of reptile pets grows, there is increased interest in improving their care.^1-3 Many owners, keepers, and veterinarians are now considering and discussing the mental well-being of reptiles in captivity—including providing enrichment through diet, husbandry, and behavioral training. Enrichment benefits reptiles by encouraging natural behaviors, increasing choice, improving health, and enhancing welfare.^1,4 Behavioral training can be utilized to provide enrichment, reduce stress, facilitate veterinary care, and improve human-animal interactions.⁴

Veterinarians play an integral role in improving the health and welfare of captive reptiles.⁵ Failure to provide for the physical needs of reptiles is a source of stress and is recognized as a significant cause of health problems.⁶ Physical and mental health are intricately interconnected; veterinarians must consider and address both in order to provide the best medical care for their patients and enhance the lives of captive reptiles.^5,6

Behavior

Each of the more than 10,000 known species of reptiles has a unique natural history, including varied diets, environments, and behaviors.⁷ It is important for those who keep and care for reptiles—including veterinarians—to become familiar with the natural histories of the species they manage.² Knowledge of a specific species’ natural history can inform choices for their captive care, including diet, husbandry, enrichment, and medical evaluation.^2,8

Ethology is the study of behavior from a naturalistic and evolutionary perspective.¹ It requires careful description of behaviors observed in natural and captive conditions, including the behavior itself as well as its stimulus or context.¹ Reports of behaviors are typically organized systematically, including locomotion, foraging and ingestion, body care and elimination, protection against predators, fighting and antagonism, territory formation and maintenance, dominance, courtship, nesting, and parental care.¹

Historically, behavioral research neglected reptiles relative to birds and mammals, especially with regard to cognition, emotions, social behaviors, and enrichment needs.¹ Much of what we know about reptile behavior is from sparse primary research and informal or anecdotal reports that lack thorough documentation.¹ However, reptiles share many traits with mammals and birds, including complex communication, problem-solving, parental care, play, and social behaviors.^1,9 Reptile behavior has historically been interpreted through a mammal-centric perspective. Burghardt explains, “We cannot use simplistic evaluations of behavior viewed through our human-centered lens, since poikilothermic vertebrates operate at different time scales, lack readily interpreted facial and vocal signals of internal states, and rely on sensory cues, often chemical, outside the range of those we can readily evaluate with our mammalian infrastructure.”¹

The diversity of behaviors among reptile species is comparable to mammals and birds.⁸ Within the reptile clade, there are large variations in sensory abilities, temperaments, reproductive strategies, neonatal strategies, anti-predator responses, foraging strategies, social organization, and habitat selections.¹

Reptile senses include visual, auditory, tactile, and chemosensory systems. Most reptiles have good vision, which is used in foraging and predator avoidance, as well as social behaviors including head bobbing, body coloration changes, courtship gestures, and submissive postures.^3,7 Hearing is relatively well developed in reptiles; many reptiles vocalize and/or respond to auditory stimulation.^3,7 Tactile sensation is evident in the detection of vibrations, as well as in behaviors such as stroking or rubbing in courtship, or ramming or biting in fighting.³ Chemosensation is also well developed and is used in communication, reproduction, foraging, and predator avoidance.^3,7 Consideration for these sensory systems is important in captive husbandry, including in identifying sources of stress as well as providing enrichment.

Most reptile species are not considered social, but there are numerous reports of social behavior in various species.^1,6,9 Some species have social dynamics that change with life stage or reproductive status.⁶ Examples of social behavior include courtship, territoriality, monogamy, social grouping, definite social orders, and parental care.^1,2,6,7,9

Intelligence and Cognition

Reptiles were historically considered to be unthinking and unfeeling—their behaviors were interpreted as mere responses to stimuli without higher cognition.¹ Indeed, colloquial references to the “lizard brain” belie their more complex neurologic anatomy; some reptiles have neural structures homologous to structures in mammals that govern emotion, decision-making, and consciousness.^1,10 There have been relatively few studies about reptile intelligence and cognition compared to mammals and birds.¹ Early studies also did not take differences between reptiles and mammals into account when establishing measures of intelligence.¹

Reptiles have been shown to have signs of intelligence and cognition, including spatial cognition, sensory discrimination, reversal learning, equivalence, individual recognition, gaze following, complex social dynamics, social learning, curiosity and play behaviors, and problem-solving.^1,9 Examples of behaviors supportive of cognition include counting-like skills in monitors, play behaviors in Komodo dragons and turtles, and predator gaze monitoring in hognose snakes feigning death.¹

Reptiles also have the abilities to learn and be trained when the training accommodates their sensory systems and behavioral repertoires.^1,3,4,6,9 Burghardt argues that lack of accommodation to human training does not necessarily reflect an animal’s lack of intelligence.¹ Turtles, crocodilians, and lizards are especially adept with traditional learning and training techniques.¹ Some turtles have demonstrated prolonged memories, remembering how to complete a training task years after reinforcement last occurred.¹ Snakes may rely more on chemosensory cues that are less familiar to their human trainers¹; however, indigo snakes were shown to respond to operant conditioning at a similar rate as pigeons or rats.³ More research into snakes’ receptivity to training is necessary.¹

Stress

Stress or stressors are any physical, chemical, or emotional force that disturbs or threatens homeostasis and the accompanying adaptive responses (the stress response) that attempts to restore homeostasis.^5,6 Stressors are categorized as physical (those necessitating physiologic coping mechanisms) or psychologic (those that may indicate imminent threat but are not directly harmful).^5,6 Physical stressors include inadequate or excessive environmental temperature, humidity, or photoperiod; thirst or dehydration; hunger or undernutrition; inappropriate diet or malnutrition; oxygen deprivation; disease; trauma; and reproduction.^5,6 Psychologic stressors include social interactions, overcrowding, confinement, novel stimuli or environments, human-reptile interactions, and lack of appropriate seclusion.^5,6

Stress responses can be categorized by their chronicity. Responses to short-term stressors are typically adaptive measures to increase energy for the animal to cope with or escape the stressor. Short-term stress responses include activation of the sympathetic nervous system, the hypothalamic-pituitary-adrenal axis, and other endocrine functions.^5,6 Responses to chronic stressors may become maladaptive through dysregulation, often due to the inability of the animal to cope with or escape the chronic stressor.^5,6 Chronic stress can lead to the inhibition of non-essential behaviors, reduction of physiologic functions, and immunosuppression.^2,5,6

A common cause of chronic stress is long-term husbandry deficiency.^5,6 Captivity is inherently stressful for non-domesticated species, because it cannot fully provide for all of an animal’s needs.^1,2,6,8 Reptile keepers’ attempts to mimic species’ natural environments are based on limited knowledge and abilities.^1,8 For example, enclosures are often a fraction of the size of normal territories, and artificial lighting is a poor alternative to the sun. Captivity also affects behavior. Behaviors exhibited in captivity, such as escape attempts or nose rubbing, can indicate distress.^6,7 More subtle signs of stress may be overlooked or misinterpreted by keepers, but can include abnormal behaviors, behavioral inhibition, hypervigilance, excessive hiding, startle, aggression, or immobilization.⁶ Reptiles may change their behavior in the presence of human observers in captivity, and they also often mask signs of disease.^1,5,6,8

Relevance to Veterinary Medicine

Evaluating a reptile’s behaviors is an important part of its clinical assessment.^5-8 Physical and mental health are interconnected; physical health will influence behaviors, and mental health will influence physiologic responses.^5,6 Behavioral change in reptiles is often an early indicator of distress, injury, or disease.⁸ Stressed reptiles may display false indications of physical illness, such as erratic behavior, feigning death, or increased respiration rates.³ Interpreting subtle behavioral changes necessitates familiarity with the species’ natural history and behaviors, as well as the patient’s individual history.⁵ An unfamiliar keeper or clinician may misinterpret normal behaviors as indicators of disease, or abnormal behaviors as normal.⁷

Maladaptive or abnormal behaviors may result in physical injury or disease, such as rostral abrasions, thermal burns, injuries due to conspecific aggression, or intestinal impactions due to pica.^2,8 Chronic stress is detrimental to health and welfare, including immune function, reproduction, and growth.^2,5,6 Medical management of reptiles must incorporate both treatment of the pathologic process as well as identifying and reducing stressors in the environment.⁶

There are also iatrogenic stressors inherent with medical care, including transportation, restraint, and diagnostic procedures.⁶ Clinicians must balance the potential benefit of a procedure against its potential for causing stress.⁶ Stress responses may also affect results of the physical examination and biochemical laboratory results.³ Stressing a compromised animal with restraint may result in severe harm or even death.³ Strategies for minimizing stress should be utilized during the examination, including appropriate environmental conditions, reduced stimuli, examining at a distance when possible, and behavioral training.³

Enrichment

Enrichment is a popular and effective strategy for enhancing captive animal welfare.^1,6 The Association of Zoos and Aquariums Behavior Scientific Advisory Group defines enrichment as “a dynamic process for enhancing animal environments within the context of the animal’s behavioral biology and natural history…with the goal of increasing the animal’s behavioral choices and drawing out their species-appropriate behaviors, thus enhancing animal welfare.”⁶ The purpose of enrichment is to create an environment that enables an animal to have opportunities to exhibit natural behaviors similar to a wild conspecific.^1,2,4,6 Enrichment can also be used to reduce or eliminate chronic stress.^2,5 Enrichment is sometimes considered a luxury that keepers may choose to provide, but it actually may be essential for proper captive management.¹ Good enrichment should be based on knowledge of the ethology and natural history of a species, and it should encompass all aspects of husbandry.^1,4

A survey of reptile zookeepers indicated the main goals of their enrichment programs included promotion of natural behaviors, behavioral conditioning, reducing stereotypies, providing public education, and the promotion of general well-being.¹¹ More broadly, the goals of an enrichment program should promote species-appropriate behaviors, provide behavioral opportunities, and provide animals with choices or control over their environment.⁴ The incorporation of choice and control can help modulate stress response in many species.⁵

When designing an enrichment program, one should have a specific and measurable goal in order to evaluate the success of the program.⁴ Examples of goals include utilization of the provided enrichment, increase in a desired behavior, reduction of an undesired behavior, improved biological growth measurements and stress indicators, or decreased corticosterone levels.¹¹ The “SPIDER” framework used by some zoos includes the following steps: Setting goals, Planning, Implementing, Documenting, Evaluating, and Readjusting.^4,12

“Opportunities to Thrive” is another framework for improvements in animal care and welfare created by San Diego Zoo Global.^5,6 The five opportunities are for a well-balanced diet (including varied presentation), to self-maintain (including shelter and comfort behaviors), for optimal health, to express species-specific behaviors, and for choice and control (the choice to perform a variety of behaviors or not).^5,6

When designing enriching enclosures, considerations must be made for the species’ natural history and ethology, although natural conditions are difficult to approximate in captivity.^1,2,6,8 Methods for providing enrichment include natural enrichment devices, manmade enrichment devices, social enrichment, and structure or habitat design.¹¹ Considerations for enclosures include temperature ranges, thermoregulation behaviors, activity levels, vertical and horizontal space, substrate type and depth, airflow, olfaction or chemosensory cues, lighting spectrum, photoperiod, humidity, drinking water provision, variety of diet, foraging or hunting behaviors, diet presentation, shelter types, anti-predator behaviors, visual barriers (including tolerance for “invisible” barriers such as glass), social behaviors, and crowding.^2,5,6 Choice is also an important consideration; many of the variables listed above should be provided on a gradient to allow the reptile to choose its microhabitat, including temperature, lighting spectrum, humidity, and shelter.² Temporal variation should also be considered for species whose natural history includes seasonal variation.² Naturalistic environments provide more enrichment and less stress than clinical environments.^2,6 However, naturalistic enclosures may be more difficult to maintain and clean than clinical enclosures.^2,6 Enriching enclosures may be designed without naturalistic aesthetics by utilizing artificial material to accomplish the same enrichment goals. Frequent changes to enclosures can provide novelty and enrichment; however, frequent changes to an animal’s environment may also be a source of stress.⁵ The tolerance of the individual animal should also be considered when designing enrichment.⁵

Relevance to Veterinary Medicine

Veterinarians should encourage keepers to improve their reptiles’ physical and mental health by providing species-appropriate enrichment, including choices and opportunities to express natural behaviors.⁵ Enrichment can enhance health and welfare, decrease stress (especially chronic stress), and improve an animal’s ability to cope with stressors.³ This author includes discussions of enrichment along with husbandry and diet requirements during routine and medical examinations of reptiles.

Training

Behavioral training is one method of enrichment. Training benefits the reptile by providing enrichment, physical activity and exercise, mental stimulation, improved welfare, and reduced stress associated with human interaction.^2,3 Training can also benefit the human trainer by providing increased interaction with the reptile, increased safety during interactions, ease of movement of large reptiles, reduced necessity of restraint for medical procedures, and potential information for research in animal intelligence.^3,4 Many reptile owners want to be able to interact more meaningfully with their pet reptile; training provides a method of communicating desired actions and promised rewards, and is enriching for human-reptile interaction.⁴

Operant conditioning is commonly studied in mammals and birds. While fewer published studies describe operant conditioning in reptiles, it is commonly used in zoological institutions and by private keepers.⁴ Many techniques for training in reptiles have been extrapolated from those used with mammals and birds.³ A survey of reptile zookeepers found that their sources for reptile enrichment and training ideas included word of mouth from other keepers, the internet, peer-reviewed published journal articles, zoo-accreditation-supplied networking, and herpetology magazines.¹¹ There are also social media groups dedicated to reptile training, which may provide ideas and networking for reptile keepers but are not peer-reviewed published techniques. Generally, operant conditioning should rely on positive reinforcement as much as possible to reduce fear response.³

When establishing a training program, the trainer must recognize differences between mammals or birds and reptiles, including sensory capabilities, social dynamics, and metabolic rates. Reptiles that lack external ears may not respond to auditory cues, but a variety of visual, auditory, tactile, and/or olfactory cues should be considered.³ Reinforcements are typically dietary, but these are not necessarily appropriate for species that feed infrequently (such as many snakes) or species that are prone to obesity in captivity.³ Determining the best reinforcement for an individual animal takes careful observation to recognize what the animal values.⁵ Trainer safety must also be considered, as some reptiles can become aggressive when anticipating food; the reinforcement can be delivered with tongs or similar equipment.³

A relatively simple form of training is desensitization, which is the process of acclimating an animal used to a stimulus through gradual exposure.³ Desensitization may be passive (habituation) or active (counterconditioning). Habituation involves introduction of the stimulus in a way that allows the animal to choose to interact with it, but does not force the interaction.³ Counterconditioning is an active pairing of the stimulus with a reinforcement to create a positive association; it is generally faster than habituation.³ Desensitization is a useful technique for getting a reptile used to human handling.^2,3,6 It is important to provide a cue before handling to reduce the startle response, since many reptiles are prey species.³

Target training can be accomplished in almost any animal species.^3,5 It is a very powerful training tool that can be used as a bridge to train other behaviors.¹ A target is an object that an animal is taught to touch, follow, or approach; common targets include ball on a stick, human hand, straw, spoon, or dish.³ A positive association with the target is formed through operant conditioning. Target training can also be used to teach stationing, which is to direct an animal to go to a specific item or location and remain there.³ Stationing is useful for shifting animals into and out of transport cages and reducing physical or chemical restraint necessary for medical procedures.^2,3 Target and station training may provide safe methods to position and manipulate even large or dangerous reptiles.³ Stations can be brought to novel environments such as veterinary offices to provide a consistent training framework and reduce stress.³

Relevance to Veterinary Medicine

Training techniques may facilitate veterinary care and reduce associated stress.^2-4 Decreased stress can increase the efficacy of a procedure and validity of diagnostic results.³

Target and station training can reduce stress associated with capture and transportation for both the reptile and the keeper.^2,4 Reptiles that are desensitized to human handling are less likely to experience stress when handled during medical procedures.^3,5 Desensitization training should incorporate the veterinarian, touch, equipment, and common medical procedures.³ Reptiles may be desensitized to diagnostic procedures such as weighing, ultrasounds, or venipuncture.³ Notably, Aldabra tortoises were trained to station for venipuncture.¹³ Target, station, and desensitization training can also improve safety for the handler and animal by reducing fear behaviors and resultant injuries.³

Additionally, keepers who have routine interaction with their reptiles may be more aware of their normal and abnormal behaviors.³ These keepers may notice earlier or more subtle signs of disease in the reptile, which would allow for veterinary care to be delivered earlier in the progression of the disease and potentially a better prognosis.³ People who have regular or meaningful interactions with their reptile may also become more invested in its care.³

Conclusion

Reptiles can have complex intelligence, cognition, and behaviors. Many are capable of learning and can respond to operant conditioning and other training. Enrichment through environmental, dietary, and behavioral training modalities is important for the health and welfare of reptiles in captivity. Behavioral training can be utilized to provide enrichment, reduce stress, facilitate veterinary care, and improve human-reptile interactions. Behavior, stress, enrichment, and training are important considerations for veterinarians who treat reptile species. Continued research into reptile behavior, intelligence, enrichment, and training is important due to the relative paucity of published information. This author encourages readers interested in reptile behavior, intelligence, and training to explore the resources and references provided for more information to develop their own enrichment, training, and/or research programs.

Acknowledgements

I would like to thank Arizona Exotic Animal Hospital; Jay Johnson, DVM; and Heather Bjornebo, DVM, DABVP (Reptile and Amphibian Practice), CertAqV, for their continued support.

References

1.  Burghardt GM. Environmental enrichment and cognitive complexity in reptiles and amphibians: concepts, review, and implications for captive populations. Applied Animal Behaviour Science. 2013;147:286–298.

2.  Wilkinson SL. Reptile wellness management. Vet Clin North Am Exot Anim Pract. 2015;18:281–304.

3.  Hellmuth H, Augustine L, Watkins B, Hope K. Using operant conditioning and desensitization to facilitate veterinary care with captive reptiles. Vet Clin North Am Exot Anim Pract. 2012;15:425–443.

4.  Skurski ML, Fleming GJ, Daneault A, Pye GW. Behavioral training and enrichment of reptiles. In: Divers SJ, Stahl SJ, eds. Mader’s Reptile and Amphibian Medicine and Surgery. 3rd ed. St. Louis, MO: Elsevier Saunders; 2019:100–104.

5.  Clayton LA, Tynes VV. Keeping the exotic pet mentally healthy. Vet Clin North Am Exot Anim Pract. 2015;18:187–195.

6.  Hunt CJG. Stress and welfare. In: Divers SJ, Stahl SJ, eds. Mader’s Reptile and Amphibian Medicine and Surgery. 3rd ed. St. Louis, MO: Elsevier Saunders; 2019:105–108.

7.  Durso AM, Maerz JC. Natural behavior. In: Divers SJ, Stahl SJ, eds. Mader’s Reptile and Amphibian Medicine and Surgery. 3rd ed. St. Louis, MO: Elsevier Saunders; 2019:90–99.

8.  Warwick C, Arena P, Lindley S, Jessop M, Steedman C. Assessing reptile welfare using behavioral criteria. In Practice. 2013;35:123–131.

9.  Wilkinson A, Huber L. Cold-blooded cognition: reptilian cognitive abilities. In: Shackelford TK, Vonk J, eds. Oxford Handbook of Comparative Evolutionary Psychology. Oxford: Oxford University Press; 2012:129–143.

10.  Norimoto H, Fenk LA, Li H, et al. A claustrum in reptiles and its role in slow-wave sleep. Nature. 2020;578:413–418.

11.  Eagan T. Evaluation of enrichment for reptiles in zoos. J Appl Anim Welf Sci. 2019;22:69–77.

12.  Animal Enrichment. Available at: www.animalenrichment.org. Accessed April 5, 2020.

13.  Weiss E, Wilson S. The use of classical and operant conditioning in training Aldabra tortoises (Geochelone gigantea) for venipuncture and other husbandry issues. J Appl Anim Welf Sci. 2003;6:33–38.