Article

Environmental enrichment impacts discrimination between familiar and unfamiliar human odours in snakes (Pantherophis guttata)

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Abstract

Environmental enrichment has been found to significantly influence the cognitive abilities of a variety of mammalian and avian species, with effects ranging from positive to negative, however, these effects have been little studied in reptiles. This is problematic given their increasing popularity as pets and the wide variation in their care. Therefore, the aim of this study was to examine how exposure to environmental enrichment affected discrimination between familiar and unfamiliar humans in a popular species of pet reptile, the corn snake. Snakes (n = 11) were individually housed for four weeks in either an enriched or standard environment before we tested their discrimination between familiar and unfamiliar odours of humans (familiar handler vs. unfamiliar stranger). The snakes were then swapped into the other housing treatment (either enriched to standard, or standard to enriched) for a further four weeks before being tested again. In the discrimination tests, the snakes were simultaneously presented with the odours of a familiar and unfamiliar human within a test arena, and the time spent in close proximity to either stimulus was recorded. We found that after being housed in the enriched enclosures the snakes spent significantly more time investigating the unfamiliar human odour, suggesting successful discrimination of the handlers, and an attraction to novelty. In contrast, snakes housed in the standard enclosures did not discriminate between the two odours despite exploring the stimuli for the same overall amount of time. Therefore, this study demonstrates that corn snakes can recognize the odour of familiar humans; however, this was only observed in the enriched group, suggesting that the absence of environmental enrichment may interfere with discrimination in this task. We recommended that enclosures incorporate enrichment in order to promote good welfare.

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... Unfortunately, the EE preferences of less popular species, such as snakes and other reptiles, are rarely studied [6][7][8]. This is problematic as the number of snakes under human care are increasing, particularly as pets [9]. The importance of expanding the literature on reptile enrichment is further emphasised by those few studies that have shown its benefits. ...
... The importance of expanding the literature on reptile enrichment is further emphasised by those few studies that have shown its benefits. EE produces cognitive benefits in turtles [10], lizards [7,11], and snakes [9,12]. For example, rat snakes (Pantherophis obsoleta) were housed under either standard or enriched conditions [12]. ...
... In another study, some corn snakes (Pantherophis guttatus) were provided with EE, including aspen bedding, branches and a board on which to climb, a large water dish, and various hides [9]. Snakes housed under standard conditions were given whole newspaper bedding with a single shelter and a small water dish. ...
Article
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The environmental enrichment needs of snakes are often disregarded. Using preference testing, we aimed to shed light on the enrichment preferences of a popular pet species, the western hognose snake (Heterodon nasicus). Snakes’ enclosures were divided into enriched and standard sides. The enriched half had substrate for burrowing, interactive stimuli, and a large water dish. The standard half had paper towel substrate and a small water dish. Each side also contained a single shelter. We provided belly heat to create a thermal gradient on one side of the cage. Snakes were observed for 6 days, four times daily. We predicted a preference for enriched conditions and, as snakes are ectothermic, a preference for the warmer side. Snakes were additionally given an exploration assay, to explore whether differences in preference for environmental enrichment interact with boldness levels. We found that hognose snakes preferred enrichment, and the strength of this preference increased over time. Preference for enrichment was stronger when the enriched side was cooler. This may be due to the burrowing tendencies of these snakes. We found no relationship between preference and boldness. These findings emphasise the importance of preference testing in establishing research-informed enrichment opportunities for reptiles.
... There are very few studies investigating snake welfare (e.g. Warwick et al., 2013;Van Waeyenberge et al., 2018) and even fewer papers considering the benefits of enrichment (Cardiff, 1996;Almli and Burghardt, 2006;Rose et al., 2014;Spain et al., 2020;Nagabaskaran et al., 2021). This makes it difficult to provide the necessary evidence-based guidance for how to house snakes in order to maximise their welfare. ...
... Crucially, none of the above studies looked beyond differences in within-enclosure behaviour to investigate enrichment effects on performance in preference tests, in which the animals could choose to spend time in the different environments, or behavioural/cognitive tests. Nagabaskaran et al. (2021) revealed that performance in a discrimination task differed with housing condition; when snakes were housed in Enriched enclosures they discriminated between familiar and unfamiliar human odours whereas when housed in Standard enclosures they did not. Almli and Burghardt (2006) also found that increasing cage complexity resulted in different behavioural profiles of ratsnakes (Elaphe obsoleta) as determined by a range of cognitive/behavioural tests. ...
... Rose et al. (2014) also found that the provision of enrichment and the opportunity to climb resulted in corn snakes being visible a significantly greater proportion of time, a finding that was mirrored in our study, despite the snakes having more places to hide in the Enriched enclosure. Further, our recent work (Nagabaskaran et al., 2021) found that when snakes were housed in Enriched enclosures they were able to discriminate between the odours of familiar and unfamiliar humans, whereas when housed in Standard enclosures they did not. Taken together, these findings suggest a benefit to owners as well as their snakes, with interactions likely to be improved as a result of pet snakes being able to discriminate between people, and owners likely to appreciate the increased opportunities to observe their pet; inclusion of enrichment will therefore likely contribute towards an improved pet-owner bond (e.g. ...
Article
There is a wealth of evidence demonstrating the benefits of environmental enrichment across a range of different animal species. However, there is comparatively little such research into the effect of enrichment provision on captive reptiles. The aim of this study was therefore to ascertain if an increase in environmental complexity was beneficial to the behaviour and welfare of corn snakes (Pantherophis guttatus). The study used a combination of behavioural observations in the home enclosure, behavioural tests of anxiety, and a preference test. The snakes used the enrichment when it was available to them and enriched snakes showed changes in general behaviour reflective of improved welfare. However, the anxiety tests revealed few effects of enrichment provision on performance. In contrast, the snakes exhibited a strong preference for the enriched enclosure when given a choice. These findings suggest that the provision of environmental complexity to the enclosure was beneficial to the behaviour and welfare of captive corn snakes. We therefore recommend enrichment should be used when keeping captive snakes.
... This taxonomic bias is grounded on the false belief that all that a reptile needs to be happy is food, a heat source, and a refuge. However, the limited evidence available shows that, when correctly implemented, enrichment improves reptile welfare and performance in cognitive tasks (Burghardt 2013;Londoño et al. 2018;Nagabaskaran et al. 2021). This area is one in which much fascinating and important progress is both possible and needed to enhance the lives of all captive animals. ...
Chapter
Despite abundant evidence to the contrary, non-avian reptiles are widely considered as behavioural and cognitive underachievers. The persistent myth of the sluggish, primitive, stupid reptile can be traced, at least in part, to long-standing misconceptions about reptilian brain size and organisation. Historically, reptile brains have been considered small and lacking the neural structures that support complex cognition in other vertebrates. In particular, the notion that reptiles lack a cerebral cortex has led to expectations that their behaviour and cognition should be simple and unsophisticated in comparison with birds and mammals. However, it was shown several decades ago that reptiles possess a large pallium comprising three–four distinct cortical areas and a dorsal ventricular ridge that may be functionally equivalent to parts of mammalian neocortex. In fact, forebrain organisation conforms to a common plan in birds and reptiles, which may seem surprising given the recent trend to put the cognitive achievements of birds above those of reptiles yet on a par with mammals. Moreover, the view that reptiles do not exhibit complex cognition faces a growing list of exceptions. Reptiles are capable of spatial, social, reversal, problem-solving, and many other types of learning and cognitively demanding behaviours provided that experimental designs account for some peculiarities of their biology involving their morphology, physiology, and ecology. Unlike frequent caricatures that depict reptiles as clumsy, inflexible, and instinct-driven, much reptile behaviour is precisely performed, delicate in appearance, readily modified, and contextually determined. Recent work has shown that reptiles can show elaborate communication and social systems, parental care, social learning, and play. Although such research is sparse compared to endothermic vertebrates, and the diversity among them immense, captive reptiles also benefit from enrichment, recognise their caretakers individually and form bonds with them, and are affected by early social isolation in ways similar to birds and mammals. Still, the gap between what we know and what we would like to know about reptilian behaviour and cognition is enormous.KeywordsBrainBrain sizeCerebral cortexCognitionLearningBehaviourComplex behaviourSocial behaviourParental carePlay
... Almli and Burghardt [31] found that rat snakes (Elaphe obsolete) housed in enriched conditions were less reactive and completed a problem-solving task faster than their counterparts housed in standard conditions. In another study, Nagabaskaran et al. [32] found that corn snakes (Pantherophis guttata) housed in enriched conditions could differentiate between familiar and unfamiliar human scents. Additionally, there is evidence that snakes will choose to spend more time in an enriched enclosure when given the choice to do so. ...
Article
Full-text available
All animals have the capacity to learn through operant conditioning and other types of learning, and as a result, zoos and other animal care facilities have shifted towards the use of positive reinforcement training to shape the behavior of animals under their care. Training offers animals the choice to participate in their own husbandry routines and veterinary procedures, while also providing mental stimulation. By adopting these practices, the welfare of animals in human care has improved, but it has not been applied equally across taxa. Snakes are frequently overlooked in the discussion of choice and control in a captive setting, likely due to the historical misinterpretation of their intelligence and behavioral needs. In this study, a shaping plan was developed for 28 juvenile false water cobras (Hydrodynastes gigas), a rear-fanged venomous species, from four clutches. Snakes were rewarded with food when completing behaviors related to the ultimate goal of following a target into a shift container. The purpose of this study is to incorporate the trained behaviors in routine husbandry practices, while preventing unnecessary stress in the snakes and risk to the keeper.
... There is a similar lack of studies on their environmental enrichment needs, although despite the paucity of literature, Eagan found that there is in fact a lot of practical work being undertaken by zoos, particularly in the area of habitat design [6]. Recently, Nagabaskaran et al. has shown that zoo-housed snakes (Fig.5 ) are better able to perform their natural behaviours when living in an enriched environment [17], while Bashaw et al. found an improvement in captive leopard gecko welfare with the provision of different types of enrichment. The geckos reportedly responded to enrichment in a manner similar to carnivorous mammals [1]. ...
Conference Paper
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This workshop is focused on the design of novel kinds of environmental enrichment for zoo-housed reptiles, using technology to support the development of interactive systems and devices for capturing data. Participants will work virtually in small groups to ideate, reflect on and develop concepts, using a ZooJam approach, which is similar to a game jam. Briefs for participants may include lizards, snakes, turtles and crocodilians.
... Geckos responded more frequently to the novel images (car) than to an image of a conspecific gecko, independently of colouration (Table 3). To our knowledge, this is the first study that has examined the effect of novel images on the behaviour of multiple species of geckos, but studies in mammals, fish, leopard geckos, and other reptiles have found similar results, where more time was spent interacting with novel objects (Antunes & Biala, 2012;Kundey & Phillips, 2021; -Xiccato & Dadda, 2016;Nagabaskaran et al., 2021). However, we need to be cautious in interpreting the different responses to the two images, as 2D images may not be perceived as 'real' objects and may lack characteristics (e.g., movement, pheromones, visual displays, three-dimensional orientation, UV reflectance) commonly used in object, individual, or species recognition (e.g., Bovet & Vauclair, 2000;d'Eath, 1998;Mason & Parker, 2010;Ord et al., 2002). ...
Article
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... This highlights the importance of providing suitable hiding places and environmental complexity alongside additional space, improving the quality as well as the quantity of space (e.g. Buchanan--Smith et al., 2004), because corn snakes require a suitable selection of hides and other resources to meet their behavioural and cognitive needs Nagabaskaran et al., 2021). ...
Article
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Eight garter snakes (Thamnophis radix) were observed during 10 daily 10-min sessions in an open field, and minute-by-minute records were kept of the frequency of tongue flicking and square traversing. The behavior of the snakes indicated that they were exploring the apparatus, and considerable individual differences were evidenced in both dependent variables. Correlational analyses compared the daily pattern of individual differences for each measure with the patterns on each other day; individual differences in each measure were found to be reliable. An interpretation of tongue flick rate is offered which suggests that this behavior may represent either an index of obligatory information gathering made necessary by a need for stimulus redundancy or an index of information processing capacity.
Article
In recent years red-footed tortoises have been shown to be proficient in a number of spatial cognition tasks that involve movement of the animal through space (e.g., the radial maze). The present study investigated the ability of the tortoise to learn a spatial task in which the response required was simply to touch a stimulus presented in a given position on a touchscreen. We also investigated the relation between this task and performance in a different spatial task (an arena, in which whole-body movement was required). Four red-footed tortoises learned to operate the touchscreen apparatus, and two learned the simple spatial discrimination. The side-preference trained with the touchscreen was maintained when behaviour was tested in a physical arena. When the contingencies in the arena were then reversed, the tortoises learned the reversal but in a subsequent test did not transfer it to the touchscreen. Rather they chose the side that had been rewarded originally on the touchscreen. The results show that red-footed tortoises are able to operate a touchscreen and can successfully solve a spatial two-choice task in this apparatus. There was some indication that the preference established with the touchscreen could transfer to an arena, but with subsequent training in the arena independent patterns of choice were established that could be evoked according to the test context.
Article
Environmental enrichment is a powerful way to stimulate brain and behavioral plasticity. However the required exposure duration to reach such changes has not been substantially analyzed. We aimed to assess the time-course of appearance of the beneficial effects of enriched environment. Thus, different behavioral tests and neurobiological parameters (such as neurogenesis, brain monoamines levels, and stress-related hormones) were concomitantly realized after different durations of enriched environment (24 h, 1, 3, or 5 weeks). While short enrichment exposure (24 h) was sufficient to improve object recognition memory performances, a 3-week exposure was required to improve aversive stimulus-based memory performances and to reduce anxiety-like behavior; effects that were not observed with longer duration. The onset of behavioral changes after a 3-week exposure might be supported by higher serotonin levels in the frontal cortex, but seems independent of neurogenesis phenomenon. Additionally, the benefit of 3-week exposure on memory was not observed 3 weeks after cessation of enrichment. Thus, the 3-week exposure appears as an optimal duration in order to induce the most significant behavioral effects and to assess the underlying mechanisms. Altogether, these results suggest that the duration of exposure is a keystone of the beneficial behavioral and neurobiological effects of environmental enrichment.
Article
The ability of hatchling pine snakes (Pituophis melanoleucus) to follow or avoid the chemical trails of conspecifics and a king snake (Lampropeltis getulus) on paper substrates was investigated inY-maze experiments. Hatchlings entered the arm with the adult conspecific trail and avoided the arm containing the king snake trail at a frequency much greater than that due to chance. The data support the hypotheses that pine snakes follow the chemical trails of adult conspecifics and avoid the chemical trails of a predator.
Article
A study was conducted to determine if different handling procedures would affect the behavior, growth and adrenal gland morphology of growing pigs. Sixty-four young gilts (8–10 weeks) in groups of 4 were exposed to one of 4 handling treatments (Positive, Negative, Minimal or Aversive) for 10 weeks. The experimenter entered the Minimal pens only when it was necessary to clean the area. For all other treatments, the experimenter entered the pens for 2 min/day, 5 days a week, in order to impose the treatments. Aversive-treatment pigs were electrically shocked if they failed to avoid the experimenter. To handle pigs in a Positive manner, the experimenter squatted, allowed the pigs to contact the experimenter, and would attempt to scratch the pigs only when they appeared receptive to scratching. A treatment consisting of signals which had previously been evaluated as Negative involved remaining upright, approaching the pigs and reaching toward the pigs' heads with gloved hands.When tested for approach behavior toward a human standing erect in a small arena at 3 weeks and at the end of the trial. Minimal-, Positive- and Negative-treatment pigs approached the human more quickly and interacted with the human more frequently than did the Aversive pigs. Minimal and Positive pigs did not differ in growth rate, but Negative and Aversive pigs gained less during the initial 6 weeks of the trial than did those on the other treatments. Only the Aversive treatment resulted in adrenal morphology (increased area of cortex) which was indicative of chronic stress. It is concluded that if frequent handling of animals is necessary, non-aversive methods should be employed to avoid deleterious growth responses.
Article
The effect of cage size as a factor causing the development of stereotypies was investigated. To separate the process of acquisition of stereotypies from the performance of already established stereotypies, the ontogeny of stereotyped digging in Mongolian gerbils (Meriones unguiculatus) in two different cage sizes was recorded. Thirteen, gerbils from three litters were reared in standard laboratory cages (34×56×19 cm), and 13 gerbils from three litters were reared in cages which were four times larger (68 × 112 × 19 cm). The development of normal digging and stereotyped digging between the ages of 17 and 37 days in the two cage types were compared. Normal digging and the ontogeny of stereotyped digging were not affected by cage size. Spatial confinement by itself seems not to be a factor causing the development of stereotypies in young gerbils. The development of stereotyped digging in standard laboratory cages may indicate a lack of adequate stimuli that would control digging in the burrowing context.
Article
Evaluations were made of >4000 reptiles maintained in captive situations to assess numerous abnormal behaviours and any related environmental and other influences. Certain behavioural restrictions warrant concern because they result in physical injuries while others are primarily related to inhibited ethological expression; this paper concentrates on the latter. Hyperactivity, hypoactivity, persecution from other occupants, disposition-related environmental temperature preference, interaction with transparent boundaries and aggression are a few examples of abnormal behaviours resulting from concept- and design-deficient artificial environments, and all may be related to poor adaptability and environmentally induced trauma. It is probable that the adaptability of reptiles to unnatural environments is substantially compromised by the fundamental biological principle of their innate education system which results in greatly reduced susceptibility to other educative influences.The importance of a sound knowledge of a species natural life style (wherever possible prior to their acquisition) is to be emphasised if preventative action regarding abnormal behaviour and evaluations of current problems are to be thoroughly addressed. Very little work has been done on this subject probably because natural behaviours of reptiles may present observational difficulties and because “lower” vertebrates are often perceived as being highly adaptable to captivity and thus warrant low priority.
Article
Domestic cats have had a 10,000-year history of cohabitation with humans and seem to have the ability to communicate with humans. However, this has not been widely examined. We studied 20 domestic cats to investigate whether they could recognize their owners by using voices that called out the subjects' names, with a habituation-dishabituation method. While the owner was out of the cat's sight, we played three different strangers' voices serially, followed by the owner's voice. We recorded the cat's reactions to the voices and categorized them into six behavioral categories. In addition, ten naive raters rated the cats' response magnitudes. The cats responded to human voices not by communicative behavior (vocalization and tail movement), but by orienting behavior (ear movement and head movement). This tendency did not change even when they were called by their owners. Of the 20 cats, 15 demonstrated a lower response magnitude to the third voice than to the first voice. These habituated cats showed a significant rebound in response to the subsequent presentation of their owners' voices. This result indicates that cats are able to use vocal cues alone to distinguish between humans.
Article
Institutional and federal ethics committees regulate research on live vertebrate animals. Current regulations require researchers to provide environmental enrichment for laboratory animals. The intention is that such enrichment reduces stress and prevents atypical behavior of captive animals, enhancing the ethical treatment of these individuals, as well as providing more robust scientific results. Enrichment can take various forms but most frequently mimics aspects of the animal's natural environment, such as the inclusion of plant life, shelters, conspecifics, or providing challenges to keep the animals occupied. These approaches have proven effective for mammals and birds; however, we know little about the effectiveness of environmental enrichment for other common research taxa, such as reptiles and amphibians. These taxa are more phylogenetically distant from humans, making intuition an unreliable guide upon which to base decisions about ethics best practice, including the benefits of environmental enrichment. The eastern fence lizard, Sceloporus undulatus, spends much of its time off the ground. Therefore, we provided climbing enrichment to captive fence lizards to allow them the opportunity to carry out this common natural behavior in captivity, and tested its effect on a range of ecologic- and scientifically relevant physiological and behavioral parameters. The provision of environmental enrichment, in the form of raised basking platforms, did not affect survival (P=. 0.25), baseline levels of plasma corticosterone (an indicator of physiological stress; P=. 0.81), activity (P=. 0.19), basking behavior (P=. 0.89), time spent hiding (P=. 0.59), growth (mass: P=. 0.44; snout-vent length: P=. 0.47), or overall body condition of these lizards (P=. 0.61). This lack of an effect highlights the need for researchers to objectively test the effectiveness of enrichment, rather than relying on subjectivity and anthropomorphism when making decisions about their use.
Article
A key question in the management of group-housed captive animals is how long can an individual be removed from a social group and still be reintroduced with minimal social upheaval. In order to answer this question we require a knowledge of how long cage-mates, following a specified period of group-housing, can remember one another after separation. This issue was investigated in laboratory rats (Rattus norvegicus). Rats were group-housed for 18 days before being housed individually. One hour, 48 hr, and 96 hr after separation, they were exposed simultaneously to odour cues originating from unfamiliar rats and from former cage-mates. The rats spent significantly more time investigating the unfamiliar odour 1 hr and 48 hr, but not 96 hr, after separation, suggesting that, after 18 days of group-housing, juvenile rats remember former cage-mates for between 48 and 96 hr. The implications of this result for animal welfare are discussed.
Article
Although its adaptive properties are recognized, fear can harm the welfare and performance of intensively housed poultry. Its alleviation in individually caged domestic chicks via the independent or integrated application of regular handling and environmental enrichment regimes was investigated. The test situations incorporated varying degrees of exposure to novel, inanimate stimuli and of human involvement. Enrichment reduced freezing and avoidance of a novel object introduced into the home cage, accelerated emergence from a sheltered area into an exposed, unfamiliar one and increased vocalization, ambulation and pecking in an open field or novel environment. It also reduced the chicks' avoidance of a nearby, visible experimenter and attenuated their tonic immobility reaction to manual restraint. Such wide-ranging effects suggest that environmental enrichment may have modified general, non-specific fearfulness. Regular handling also attenuated the chicks' tonic immobility responses and their avoidance of the experimenter but it exerted few other detectable effects and there was no demonstrable effect of handling in the presence of enrichment. These findings are consistent with the suggestion that repeated gentle handling may exert its strongest influence, by facilitating habituation to human beings rather than by reducing underlying fearfulness. The implications of reduced fearfulness and other potential benefits of handling and enrichment procedures are discussed.
Article
Aging-associated brain changes include functional alterations that are usually related with memory decline. Epidemiological reports show that a physically and intellectually active life provides a protective effect on this decline and delays the onset of several neurodegenerative diseases. The cellular mechanisms behind the behavioral-based therapies, such as environmental enrichment (EE) exposure, as a method for alleviating age-related memory impairments, are still unknown. Although some reports have shown the benefits of EE exposure in cognitive outcomes in old mice and in animals with experimental neurodegenerative conditions, the effects of lifelong animal exposure to EE have not been explored in detail. In the present work we tested in a rat model the effects of intermittent lifelong exposure since youth to EE on behavioral performance, object recognition memory and anxiety level, as well as on some morphological and biochemical markers of brain plasticity such as hippocampal neurogenesis, synaptophysin content and synaptic morphology. We found that environmental factors have a positive impact on short-memory preservation, as well as on the maintenance of synapses and in the increase in number of new generated neurons within the hippocampus during aging.
Article
Neonatal (early) handling (EH) and environmental enrichment (EE) of laboratory rodents have been the two most commonly used methods of providing supplementary environmental stimulation in order to study behavioral and neurobiological plasticity. A large body of research has been generated since the 1950s, unequivocally showing that both treatments induce profound and long-lasting behavioral and neural consequences while also inducing plastic brain effects and being "protective" against some age-related deficits. The present work is aimed at reviewing the main neurobehavioral effects of both manipulations, with the final purpose of comparing them and trying to find out to what extent the effects of both treatments may share (or not) possible neural mechanisms.
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Coldblooded care: understanding reptile care and implications for their welfare
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Environmental enrichment: the creation of opportunities for informal learning
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