Abstract
Reptiles are kept in diverse husbandry situations, including zoological collections, private pet or hobby keeping, scientific and laboratory studies, quarantine, and numerous commercial settings such as for livestock, skin, and meat production, and this chapter is relevant to all these areas. In recent years, a major paradigm shift has occurred favouring naturalistic conditions for the health and welfare of captive reptiles. Increasing data and opinion indicate that the physical, ethological, and psychological well-being of animals (including reptiles) is best served in naturalistic conditions. Despite the generally accepted and growing use of naturalistic environments, husbanders could make greater efforts to incorporate spacious, naturalistic environments across all captive reptile situations. Given now wide acceptance that naturalistic environments infer positive benefits over unnaturalistic conditions, husbanders across all captive situations should evaluate their responsibilities with a refreshed sense of obligation towards developing animal housing to reflect the natural environments in which reptiles evolved.
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15.1 Introduction
Reptiles are kept in diverse husbandry situations, including zoological collections, private pet or hobby keeping, scientific and laboratory studies, quarantine, and numerous other settings, such as for livestock, skin, and meat production (Schlaepfer et al. 2005; UNEP/WCMC 2009; Mason 2010). This chapter has relevance across all the aforementioned areas, in particular concerning concepts and principles relevant to biological needs and husbandry. Numerous early works must be recognised for their foundational influence in the evolution and principles of reptile welfare biology (including Cowan 1980; Greenberg et al. 1989; Morton et al. 1990; Lance 1990; Warwick 1990a, b, 1991; Bielitzki 1992; Ford 1992; Greenberg 1992; Lance 1992; Mason et al. 1992; Pough 1992; Chiszar et al. 1993; Kreger 1993; Burghardt 1996; Burghardt et al. 1996, as well as the first edition of this volume). Nevertheless, the past quarter-century has produced many important contributions to, and in many examples reinforcements of, our understanding of reptile biology and welfare, as well as its association with essential and advanced reptile husbandry (for further examples seeFootnote 1). Within this cited body of work and its extended reference resource, numerous directly consider the different husbandry approaches involving naturalistic (e.g. based on natural provisions) or unnaturalistic (e.g. based on minimalistic and clinical provisions) environments (including: Warwick 1990a, b, 1991; Pough 1991; Chiszar et al. 1995; Newberry 1995; Burghardt et al. 1996; Bernard et al. 1997; Mellen and Sevenich MacPhee 2001; Almli and Burghardt 2006; Ferguson et al. 2010; Phillips et al. 2011; Burghardt 2013; Whitham and Wielebnowski 2013; Alligood and Leighty 2015; Baines et al. 2016; Bashaw et al. 2016; Januszczak et al. 2016; Oonincx and van Leeuwen 2017; Mendyk 2018; Warwick et al. 2018; Warwick et al. 2019).
In the first edition of this chapter (Warwick and Steedman 1995), and largely with the intention of promoting debate, we deliberately adopted a more critical approach towards minimalistic and clinical environments. Since then, a major paradigm shift has, as predicted, occurred favouring naturalistic environments. Also, for the first edition a table was provided outlining suggested summary terminology concerning environments associated with captive reptiles (Table 15.1), and those definitions are retained herein. However, whereas originally the focus of this section compared naturalistic (typically elaborate zoological) with clinical (typically minimalistic or reductionist laboratory or quarantine) environments, the proliferation of pro-naturalistic conditions across various use sectors warrants a less narrow remit. Accordingly, this revision will look more holistically at naturalistic versus unnaturalistic environments because this approach offers a broader and thus more representative assessment.
15.2 Terminology for Types of Environment
Various terms and meanings exist that refer to relevant environments in the wild and in captivity. The situation is not particularly straightforward. Reptiles in the wild can be completely free of direct, and possibly indirect, human interference. They also can be effectively wild but conceptually captive where one or another form of artificial human-made boundary surrounds a natural area. In regular captive situations there exist, as outlined above, diverse categories wherein reptiles can be placed. Unsurprisingly, husbandry perspectives, as well as the conditions for reptiles, vary greatly between and within these categories. Table 15.1 provides descriptions for commonly used terms relating to wild and captive reptiles that might assist to clarify and standardise relevant terminology, although there is likely overlap in certain situations.
Terms such as ‘sterile’ and ‘semi-sterile’ have been intentionally avoided because where animal husbandry is concerned these descriptions are largely self-contradictory in that they suggest incomplete absolutes. Such terms offer little or no advantages over the suggested preferred terms in Table 15.1 and, unless specifically qualified when used, potentially add to existing confusion over meanings.
15.3 Naturalistic Versus Unnaturalistic
Animal enclosures and associated husbandry vary considerably both between and within different settings. Typically, the two major applied environmental concepts and types can be characterised as ‘naturalistic’ and ‘unnaturalistic’. This division is based according to whether the essential intention achieves conditions that strongly mimic nature or artificiality. It is inarguable that nature offers greater diversity, complexity, and ecological context than artificial conditions. However, clearly, there is a continuum between natural diverse and complex environments (highly stimulatory, organism-occupying, conditions) at one end of the scale, and artificial minimalist environments (deprived conditions) at the other, with positive, neutral, and negative implications for welfare varying along this continuum.
In some instances, for example, where zoological collections and private pet reptiles are concerned, it is widely accepted that, in principle, there are few or no constraints on why animals should not be provided with carefully organised environments that seek to simulate the natural one, and which are intended to fulfil, as much as possible, species-specific physical, ethological, and psychological needs (Warwick et al. 2013a; Benn et al. 2019; Warwick 2023). In other cases, for example, where scientific studies and veterinary scenarios are concerned, it is widely believed that, for various reasons outlined later, reptiles should be housed in very basic, ‘clean’, and ‘easily managed’ environments, even though these offer less potential to fulfil biological needs (Cooper and Williams 1995).
Reptiles that are physically, ethologically, and psychologically compromised due to inappropriate environments probably experience greater stress (Cowan 1980; Frye 1991; Warwick et al. 2013a, b; Benn et al. 2019; Warwick 2023). Depending on the nature, context, and extent of stress-inducing influences, as well as species, individual character, and condition of the animal, a reptile may either deal with its stressors utilising normal coping mechanisms or fail to cope, languish, and die (Warwick et al. 2013a, b; Phillips et al. 2015; Benn et al. 2019; Jessop et al. 2023; Warwick 2023). The loss of a single animal due to poor welfare management can be regarded as both a heavy moral and a miniature ecological disaster.
Where formal zoological collections, and especially pet animals, are involved, these usually are the major ethical aspects to consider. However, in the case of many scientific investigations, further specific considerations must be made. Whether the effects of stressors are mild, moderate, or severe, any serious adverse alteration of an animal’s holistic health probably alters the purity of the experimental subject and raises serious questions regarding the quality of research data in such cases (Warwick 1990b; Gangloff and Greenberg 2023). Those involved in research, therefore, arguably have even greater responsibilities than others to ensure the good health and welfare of the animals that they are studying (National Research Council 2011).
15.4 Naturalistic Environments
In captivity, it is probably impossible to create anything more than a partial simulation of a reptile’s natural habitat. Accordingly, a ‘naturalistic’ environment is necessarily one that aims towards providing an animal with as many features as possible that replicate nature including relevant: space, temperature gradients and thermoregulatory opportunities, lighting, circadian cycles, diet, water, substrate, furnishings, and conspecifics (see Arena and Warwick 2023; Doody 2023; Mendyk and Augustine 2023), as well as eliminating unnatural aversive stimuli such as noise and light disturbances (Arena et al. 2023; Mancera and Phillips 2023). Naturalistic environments accommodate and stimulate normal positive behaviours (consistent with quiescence and comfort; see Warwick 2023) and states that are also important to promoting good welfare. Understimulating and unnaturalistic environments may impose negative and possibly inescapable stressors, such as thermoregulatory deficiencies, lack of control of environmental interactions, ‘boredom’, as well as exposure to excessive light and disturbance. Complex, naturalistic, and appropriately stimulating environments cannot objectively be considered negative, and today their value is broadly and widely recognised (e.g. Webster 1994; Mellen and Sevenich MacPhee 2001; Burghardt 2013; Warwick et al. 2013a, b; Martinez-Silvestre 2014; Rose et al. 2014; Carter et al. 2015; Bashaw et al. 2016; Mellor 2016; Oonincx and van Leeuwen 2017; Brando and Buchanan-Smith 2018; Greggor et al. 2018; Mendyk 2018; Benn et al. 2019; Brando and Burghardt 2019; Burghardt 2019; Gangloff and Greenberg 2023; Jessop et al. 2023; Warwick 2023).
15.4.1 General Captive Conditions
An assessment of 62 environmental enrichment studies published between 1985 and 2004 found that only 0.57% concerned reptiles, whereas 92.2% involved mammals (de Azevedo et al. 2007). Years on, despite the raft of significant advancements in understanding captive reptile management, along with recognising the value and application of naturalistic principles, there remains much to do in order to align reptile-based academic study with that of mammals. Although Eagan (2019) found that 95% of zoos practise some environmental enrichment for reptiles (e.g. thermal, humidity and light range diversity, choice of seclusion sites, and habitat variation), Burghardt (2019) points out that increased enrichment in zoo exhibits and general welfare concerns are far greater for mammals than for reptiles, and stresses the need to ‘alter biases’ against reptiles, especially snakes.
Spacious, naturalistic enclosures typically incorporate more examples of normal behaviour, although abnormal and problematic behaviour can also be observed (see e.g. Benn et al. 2019; Loughman 2020; Spain et al. 2020). However, unnaturalistic or clinical conditions always include abnormal and problematic behaviour (see Warwick 2023), and frequently little normal behaviour.
It is important to consider that whilst the absence of normal behaviour and the presence of abnormal behaviour are often associated with captivity stress (see Warwick 2023), the presence of some normal behaviour may not conclusively indicate that an animal is in harmony with its environment (Warwick 1990a; Kreger 1993; Warwick 1995; Warwick 2023). There is clearly a need for careful comparative monitoring of both normal and abnormal and problematic states in reptiles, and at present behavioural assessments appear favourable over physiological measures (see Martinez-Silvestre 2014; Gangloff and Greenberg 2023). Obviously, demands made on an animal’s evolved coping mechanisms are greater in those conditions where the individual must try to adjust. Similarly, animals cared for in the least natural environments may require the greatest input from humans to promote optimal health and well-being.
More specific research has highlighted a number of issues where naturalistic environments are superior to unnaturalistic environments. Naturalistic conditions are synonymous with environmental enrichment, which can provide a positive outlet for frustration and other problem behaviours or a means of allowing an individual to adequately address, escape, or retreat from stressors (Kuppert 2013; Sneddon et al. 2016). Indeed, environmental enrichment, or naturalistic environments, may be both an essential component of good management (Burghardt 2013) and a problem-solver in terms of a remedy for under-stimulation (‘boredom’) (Mason and Burn 2018).
The most naturalistic environments are generally associated with formal zoological collections. There is a significant collection of studies illustrating the benefits of naturalistic environments and environmental enrichment in zoo animals (Alligood and Leighty 2015). Boissy et al. (2007) pointed to the wide acceptance that good animal welfare involves not merely absence of negative experiences, but primarily the presence of positive experiences for animals. Keepers with good understanding of an animal’s biological and behavioural needs are more likely to have zoo enclosures that promote positive experiences.
Research by Therrien et al. (2007) using behavioural assessment in enriched conditions found that environmental enrichment (such as novel play items and slow food release devices) was as effective for marine reptiles as for other animals and encouraged its use for all captive sea turtles. Relatedly, Arena et al. (2014) found that marine turtles in a naturalistic lagoon showed no signs of captivity stress (effects of stressors in captive conditions), such as hyperactivity, rapid body movement, boundary exploration, surface congregation, and apprehension, aggression, and cannibalism, aside from occasional boundary exploration. Case et al. (2005) used preference tests to study box turtle physiology and behaviour and found that turtles preferred naturalistic conditions and made less attempts to escape, and both physiological and behavioural assessments positively correlated with enriched rather than barren enclosures. Mehrkam and Dorey (2015) found that naturalist environmental enrichment (such as scented coconut shells for primates) was often preferred by the animals in their study and discuss the importance of appropriate enrichment in increasing species typical behaviours and reducing abnormal behaviours.
Although frequently under-considered, spatial factors are important and integral to reptile welfare (Warwick 1990a; Warwick et al. 2018, 2019; Arena and Warwick 2023). Appropriate environmental diversity undoubtedly provides greater opportunities for animal-environment interaction. Some empirical evidence indicates that reptiles recover more successfully from disease under natural or naturalistic conditions (Warwick 1991; Arena et al. 2023), which could result from fewer or no negative influences or the impact of positive influences on immune competence (see Gangloff and Greenberg 2023).
However, a naturalistic enclosure that is space-restrictive applies a highly significant constraint whereby it is, in effect, at least partially devolved into a reductionist environment. Phillips et al. (2011) found that where food was spread about the environment lizards became more active and spent less time hiding. Also, when space was increased the lizards walked longer and further on their first day, thus stimulating exploratory behaviour, and then longer and further for the rest of the experiment, thus increasing general activity.
Reduced space also infers a lack of naturalistic conditions such as appropriate lighting, temperature, and humidity gradients (Arena and Warwick 2023). Perhaps the view should be more widely fostered that generally reduced naturalistic conditions are simply a move in the wrong direction for animal welfare, as are spacious environments with few or no furnishings. Therefore, whilst small naturalistic environments might be thought of as reasonable natural microcosms, the true inference of a naturalistic environment requires an increasing, not decreasing, relationship with the natural world, that is, spaciousness and diversity. Broadly, in terms of improved welfare, reptiles probably benefit from environmental enrichment as much as any other captive animal (e.g. Burghardt et al. 1996; Almli and Burghardt 2006; Therrien et al. 2007; Arena et al. 2014; Wilkinson 2015; Bashaw et al. 2016; Brando and Burghardt 2019).
15.4.2 Research Conditions
In nature, a myriad of interconnected genetic (e.g. innate drives), internal (e.g. physiological dynamics), and external (e.g. thermal) factors affect physiological, behavioural, and psychological states. These states change from moment to moment; thus, life in nature is highly dynamic. Dynamic implies variability, and variables are resistant to control. Classically, scientific experiments are designed to limit or control variables. Because naturalistic conditions are favoured for studying normal behavioural expression, the type of ethological research contemplated here refers to work under the reductionist approach.
Reduction of environments to simplify systems and expose targeted behaviours is commonly practised. This distinctly non-holistic concept presents complications of its own in that, for example, deliberate isolation of behaviours from human-perceived undesirable influences also unavoidably reduces the diverse gross and subtle behavioural interactions found under more naturalistic situations. Studying biological features (e.g. physiological, behavioural, or psychological) in captivity arguably significantly limits their relevance within situations of captivity. Yet, the rationales and protocols associated with a reductionist policy are widely accepted as valid. Moreover, is a reductionist environment ethically acceptable in a purely animal welfare context?
Garner (2005) noted that enrichment may improve research validity, reliability, and replicability by reducing the number of abnormal animals in experiments. Warwick (1990b) and Snowdon and Burghardt (2017) highlighted the need for researchers to be mindful that highly clinical environments, where animals lack the facilities needed to express normal behaviour, may impact the validity of behavioural studies. Moreover, without an in-depth understanding of normal behaviour in the wild, or in highly naturalistic settings, there is no control baseline on which to test hypotheses in behavioural studies.
Thus, captive-based studies instil incongruency at the interface of natural and artificial conditions, not least because the experimenter must select or deselect biological and environmental factors precisely to assess and analyse them in the controlled environment. Accordingly, information based on free-living reptiles can and should inform our approaches to the captive situation whether for research or general husbandry.
15.4.3 Summary Conclusion
In general husbandry, there appears to be no justification for failing to provide environments that are as naturalistic as possible for the species concerned. In some situations where the express purpose is targeting specific biological or research factors, reductionist or minimalistic environments can be rationalised, but in the majority of study conditions, there also appears to be no restrictive reasons why naturalistic conditions should not be maintained.
15.5 Unnaturalistic Environments
Some authors continue to comment on the welfare suitability of unnaturalistic environments for reptiles. For example, Divers and Stahl (2018) suggested there was an absence of scientific evidence that snakes require more intellectual stimulation beyond the clinical conditions of, for example, minimalistic rack housing. However, apart from the wider acceptance of naturalistic environments by the scientific community, absence of evidence does not infer evidence of absence. Furthermore, small typically minimalistic conditions, such as snake racks, are countered by research and strong criticism regarding increased risk of self-injury, under-stimulation, and stress-related disease, and other work that shows snakes prefer larger more diverse environments (Warwick 1990a, b, 1995; Mendyk 2018; Warwick et al. 2018; Lambert et al. 2019; Warwick et al. 2019; Spain et al. 2020; Arena and Warwick 2023; Font et al. 2023). Diminutive enclosures such as snake racks involve major behavioural restrictions due to enforced inability for snakes to fully stretch (Warwick 1990a, b, 1995; Astley and Jayne 2007; Hu et al. 2009; Cannon and Johnson 2012; Warwick et al. 2013a, b; BVZS 2014; Hedley 2014; Jepson 2015; Wilkinson 2015; Scott 2016; Arena et al. 2018; RSPCA 2018; RVC 2018a, b; Warwick et al. 2018; Warwick et al. 2019; Arena and Warwick 2023; Mendyk and Warwick 2023).
A study by Rosier and Langkilde (2011) employed raised basking platforms as a form of climbing enrichment to assess habitat use among lizards and found no difference in hiding or active behaviours between the control group and the ‘enriched’ habitat group; thus, the authors concluded that researchers need to objectively evaluate the effectiveness of any environmental enrichment. Others have emphasised the importance of using species-specific and appropriate environmental enrichment in research for such studies to be meaningful (e.g. Mellen and Sevenich MacPhee 2001; Case et al. 2005; Borgmans et al. 2018; Loughman 2020; Spain et al. 2020).
It is also possible that studies into the effectiveness of environmental enrichment that appear to show no positive effect on the animals’ physiological or behavioural parameters may be compromised by many variables, such as length of the study, possible unaccounted for negative stimuli, and plasma corticosterone as an indicator of stress taken out of context (Moore and Jessop 2003; Warwick et al. 2013a; Martinez-Silvestre 2014). Oonincx and van Leeuwen (2017) concluded that studies into enrichment should take account of several welfare indicators (e.g. neural, behavioural, endocrine, reproductive, metabolic, psychological), and risk factors (e.g. phylogenetic, ecological), and cautioned that no single measure corresponds directly to an animal’s holistic welfare state.
Razal and Miller (2019) found that observers consistently rated naturalistic enclosures as their preferred environment for ‘livability’ of zoo animals. However, conditions that may look naturalistic to a human onlooker may not be at all appropriate for the species concerned (Fàbregas et al. 2012). Hare et al. (2007) wrote that even though harm and fatal consequences have resulted from well-furnished diverse environments, keepers are ethically obliged to provide enriched environments for the animals’ physical and psychological well-being; such environments also allow for greater choice or ‘individual agency’ by animals over control of interactions with their environments.
15.5.1 Veterinary Management
Veterinary management presents special considerations where naturalistic and clinical environments are concerned (Cooper and Williams 1995). It can be appreciated that microorganisms and megaparasites that may be innocuous to healthy animals might become opportunistic secondary pathogens in diseased or otherwise immunocompromised individuals. Relatedly, injured animals might be at greater risk of local (possibly leading to systemic) infection or other forms of wound contamination if there are open lesions. Also, as outlined previously, it is worth considering the potential compromising effects of greater captivity stress in clinical environments, and possible associated increases in susceptibility to secondary opportunistic and primary diseases (Martinez-Silvestre 2014). Similarly, the rate of an animal’s recovery might be slowed or hindered in high-stress conditions; for example, wound healing has been shown to be slower in restraint-stressed lizards (Gouin and Kiecolt-Glaser 2011a, b). This perspective, does, of course, apply to all aspects of clinical (including veterinary) situations.
Collection of samples, such as faeces, is occasionally necessary for a variety of purposes, and these obviously should be as free as possible from environmental (including co-occupant) contamination. Sometimes, such management may be simpler in clinical environments, but it should not be presumed that it is possible only in such facilities. Samples collected even from the most clinical environments may not mean zero contamination. Prompt and effective removal of droppings from a cage (regardless of whether it is a naturalistic or clinical one) may be the most important procedure in minimising contamination of samples. Of course, faecal and other relatively ‘solid’ samples are easier to collect than highly fluid ones, such as urine, which are quickly absorbed into a deep substrate in a naturalistic environment. However, a paper floor covering in a clinical environment also might absorb fluids to the point where useful collection is also very difficult.
Clinical environments, at least during veterinary treatment, are clearly suitable much of the time. Temporary clinical environments do not have to imply bare conditions, and some elements for retreat can still be provided, such as species- and individual-specific seclusion zones (e.g. disposable cardboard boxes). In some cases, naturalistic environments may lead to greater chances of recovery, because captivity- and disease-related stresses may contribute to poor prognoses (Warwick 1991). That said, carefully managed clinical environments for numerous aspects of short-term veterinary treatment and related research may offer a justifiable solution to a potentially complicated dilemma. A highly significant justification for clinical conditions in all veterinary aspects (treatment, investigation of disease, and quarantine) may reside in the fact that most treatment involves short-term hospitalisation, thus avoiding chronic captivity stress. Although some stress is probably experienced in the clinical setting, and such stresses can have long-term consequences, its impact may be moderated and balanced with the benefits of remedial and regular expert supervision. However, it must be noted that should chronic captivity-stress situations develop, then conceivably this could tip the balance away even from any clinical setting.
15.5.2 Quarantine
Quarantine facilities are often associated with the housing of animals short term or at short notice. In these circumstances, healthy animals may be included for straightforward observation, or diseased and injured animals for segregation and treatment. As far as healthy animals are concerned, naturalistic facilities seem to be the best candidates because of the greater comfort afforded animals by these conditions, as indicated by their preference behaviours, greater behavioural normality, and probable greater perceived security (e.g. Case et al. 2005; Rose et al. 2014; Benn et al. 2019; Spain et al. 2020). There is obvious merit in a simple, standardised, housing system for short-term accommodation of animals. Nevertheless, in principle, naturalistic conditions cannot be precluded even from such management situations.
15.5.3 Summary Conclusion
In some, but not all, examples of veterinary treatment, research, and quarantine, a number of reasonable arguments appear to exist for providing clinical environments. It also seems reasonable that the use of naturalistic conditions even in the most stringent clinical situations is feasible and at least open to debate. Overall, the advantages of clinical environments over naturalistic environments may be more perceived than real, and in a purely welfare context, such approaches require precise and careful justification.
15.6 Practical Considerations
In addition to environmental suitability in fulfilling an animal’s biological needs, preference for either naturalistic or unnaturalistic environments may be influenced by other practical considerations, such as access to animals, efficacy of maintenance, and hygiene. Managing preferences may vary according to situation; for example, zoological collections, private pet or hobby keeping, scientific and laboratory studies, quarantine, and numerous commercial settings. Nevertheless, certain considerations may also be generally applied.
15.6.1 Access to Animals
Access to animals for inspection or capture is obviously necessary on occasion. The ease or difficulty with which inspection or capture is achieved can be, but is not necessarily always, affected by whether or not the environment is naturalistic or unnaturalistic. For example, a human presence can elicit specific responses from reptiles - both wild and captive. Observations of free-living lizards awoken at a regular rest site by a distant human presence (and which showed no overt response on that occasion) were nevertheless sufficiently affected by the experience to avoid the same resting place the following night (Sugerman and Hacker 1980; Bowers and Burghardt 1992). Human handling may also disrupt important periods of thermoregulation (Arena et al. 2023; Arena and Warwick 2023; Mancera and Phillips 2023; Warwick 2023). Stockley et al. (2020) showed that even gentle handling of a normally ‘placid’ species (bearded dragons (Pogona sp.)) appeared to increase anxiety-related behaviour (tongue flick rate), which may suggest that direct contact with these animals should be minimal.
These two very different examples illustrate potentially profound effects of subtle disturbances. It is important to consider that consequences of some disturbances may themselves be subtle or profound, and act earlier, later, or continuously (see also Bowers and Burghardt 1992; Gillingham and Clark 2023; Lillywhite 2023). Intentional or incidental human contact with reptiles is, therefore, something that has to be evaluated very carefully - perhaps especially where the researcher-reptile relationship is involved. Further, disturbance of animals during their rest cycle (which may differ from human activities) should be avoided wherever possible (Arena et al. 2023; Arena and Warwick 2023; Warwick 2023). Accordingly, careful training is now used by numerous professional facilities to condition reptiles to certain handling requirements and procedures (see Font et al. 2023).
15.6.2 Maintenance Efficiency and Hygiene
Certain concerns regarding threats to hygiene in well-maintained naturalistic environments relate to potential contamination risks associated with water, substrata, and plant life. In naturalistic environments, substrata or bedding contaminated by faeces or sloughed skin is practically removed as dry solid matter, often along with a small quantity of substratum, during ‘spot-cleaning’ – which helps prevent contaminant accumulation. Fluid waste deposits are absorbed into substrate until a ‘bowl’ of moist material forms, which can then be easily removed as a single ‘unit’. Small amounts of waste products inevitably remain in the environment, but build-up is slow and often easily managed. Drinking and bathing water that is heavily contaminated presents the potential threat of disease, but water quality management of both small and large bodies of water is similar across all captive settings.
In unnaturalistic or clinical situations, artificial substrate (e.g. paper) has comparatively low absorption potential, and requires frequent removal; floor surfaces also require cleansing on a very regular basis - which infers more handling. Zoological collection managers anecdotally report that well-managed substrata can remain viable furnishings for several years, although clearly this is not a specific recommendation. Proponents of unnaturalistic or clinical environments routinely recognise that naturalistic substrata are required for certain species. Such reasoning could be far more broadly applied. Cautionary hygiene is widely accepted as important both for non-human and human animal health. Clearly, excessive build-up of waste and decaying organic matter is to be avoided. However, the extent and not the mere presence of contamination (as well as the animal’s existing state of health) imply relative risk. Nevertheless, caution must be exercised not to introduce potentially harmful contaminants (e.g. pesticides) via introduced natural furnishings (Murphy 2015).
During a survey by Warwick et al. (1992) researchers expressed far greater difficulty in experimentally infecting reptiles in naturalistic conditions than reptiles in unnaturalistic or clinical conditions. Indeed, this apparently was so evident that reptiles to be infected were deliberately rehoused in clinical environments to increase the chances of them acquiring a forced disease. A. Lambiris (pers. comm.) reports on experiences that suggest that free-living reptiles presented with normal biological (including immunological) stresses are at an advantage over captive animals facing problems in the artificial environment. In captive reptiles maintained in scrupulously hygienic conditions, and where keepers had perceived them to be free of stress, disease occurred with far greater virulence than in wild populations. The aetiology, at least in part, was attributed to captivity-related chronic stress and compromised immune competence arising from environments that were too clean and/or resulted in related stress. One could argue that there exists the possibility that over-cleaning reduces or eliminates conceivably important subtle stimulation of an animal’s immune system. Exercise of the immune response due to background microbiology may be integral to overall maintenance of immune competence.
As indicated above, threats to animals from normally innocuous factors may only be realised as a result of compromised immune competence. This negative effect may be reduced by naturalistic, and thus biologically more comfortable, environments. At what level of microorganism infestation in an environment should one start to become concerned for animal health? If the mere presence of potentially pathogenic organisms is always to cause alarm, then alarm will be caused constantly; the point here being that truly dirty water, decaying sloughed skin, and other bacteria-laden organic debris, as well as chemically noxious substances, present unreasonable, greater-than-natural threats to animal health than naturalistic biotic conditions. A well-maintained naturalistic environment ought to present minimal hygiene risk.
Extreme cleaning of an environment may have other adverse implications. For example, cage-cleaning can delete familiar chemical cues that are known to have a calming effect on reptiles (see Chiszar et al. 1993, 1995). What level of stress might regularly repeated hygiene protocols have on individual animals? In addition, might frequent disinfection lead to the emergence of mutant, antimicrobial resistant, and possibly more serious pathogens?
Arguably, when one accepts the highly limited value of striving for substantial cleanliness, then one has to consider carefully the negative implications of captivity stress in a clinical environment. General clinical protocols should perhaps be considered as ways of keeping over-contamination out, rather than ways of keeping ‘sterility’ in.
In nature, animals are exposed to a myriad of microbial organisms and particles, as well as many contaminants throughout all living conditions, and indeed such factors continue to operate after death. Whilst all such environmental characteristics may present potential challenges to good health, they are also frequently integral to it. What constitutes good versus bad hygiene is significantly a matter of balance between the nature of a potential threat and individual immune competence. Therefore, good hygiene management is a target of responsible husbandry, which implies appropriate cleanliness, and does not infer sterility. Access to animals may be an important occasional requirement. However, the proliferation of naturalistic environments in use globally offers testimony to their reasonable practicality. Accordingly, naturalistic conditions should not be interpreted to suggest impractical or problematic hygiene or access to animals.
15.7 Animal Welfare Conclusions
Historical and some current preferences for unnaturalistic environments appear primarily founded on long-established habits rather than scientific approaches. Increasing data and opinion indicate that the physical, ethological, and psychological well-being of animals (including reptiles) is best served in naturalistic conditions.
Providing environments that allow animals to fulfil natural behaviours is probably essential to promote welfare, and thus optimise health. Innate (inborn) drives or needs are importantly met in order to aid welfare in both human and non-human species (Ross and Mason 2017). Innateness is a fundamental characteristic of reptilian biology where psychological and behavioural attributes and needs are hard-wired or pre-set to the natural conditions of life in the wild (Warwick 1990a, b, 1995; Warwick et al. 2013a; Warwick 2023). In humans, environmental enrichment has been shown to improve cognitive performance (e.g. Singhal et al. 2019). Assuming such considerations may be applicable to reptiles, then greater environmental complexity may also be related to the cognitive capacities of these animals.
Despite the generally accepted and growing use of naturalistic environments, husbanders could make greater efforts to incorporate spacious, naturalistic environments across all captive reptile situations. Early attention should be given to factor in spatial, environmental complexity, and cost issues to provide naturalistic accommodation for animals when captivity-based facilities or projects are considered. This approach offers the potential to contemplate more fully animal requirements over the conveniences of an establishment’s extant architecture, rather than vice versa.
Also, general managers and researchers who are reluctant to employ naturalistic conditions could make greater efforts to record and balance perceived advantages and disadvantages, both practical and conceptual, of naturalistic and unnaturalistic conditions, with an overview bias towards reptile welfare. Placing or producing a reptile in captivity may constitute the most challenging environment in which it might be expected to survive (Warwick 1995).
Just as ‘environmental enrichment’ ought to be thought of as a baseline norm of nature, naturalistic environments should be considered as fundamental to enclosure concept and design (see Greenberg 2023); they are not, and should be, viewed as ‘additional’ or ‘extra’ provisions or facilities. Given now wide acceptance that naturalistic environments infer positive benefits over unnaturalistic conditions, husbanders across all captive situations should evaluate their responsibilities with a refreshed sense of obligation towards developing animal housing to reflect the natural environments in which reptiles evolved.
Notes
- 1.
Examples of recent relevant publications: (Mason and Mendl 1993; Bernard et al. 1997; Blake et al. 1998; Hayes et al. 1998; de Vosjoli 1999; Mellen and Sevenich MacPhee 2001; Scott and Warwick 2002; Moore and Jessop 2003; Burghardt 2005, 2013, 2015; Case et al. 2005; Almli and Burghardt 2006; Morgan and Tromberg 2007; Therrien et al. 2007; Manrod et al. 2008; Ferguson et al. 2010; Phillips et al. 2011; Rosier and Langkilde 2011; Leal and Powell 2012; Wilkinson and Huber 2012; Arbuckle 2013; Doody et al. 2013; Kuppert 2013; Warwick et al. 2013a, 2018, 2019; Whitham and Wielebnowski 2013; Mancera et al. 2014, 2017; Martinez-Silvestre 2014; Rose et al. 2014; Mellor and Webster 2014; Wilkinson 2015; Baines et al. 2016; Bashaw et al. 2016; Mellor 2016; Howell and Bennett 2017; Moszuti et al. 2017; Waters et al. 2017; Oonincx and van Leeuwen 2017; Siviter et al. 2017; Mason and Burn 2018; Mendyk 2018; Benn et al. 2019; Lambert et al. 2019; Whitehead 2018; Tetzlaff et al. 2019).
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Warwick, C., Steedman, C. (2023). Naturalistic Versus Unnaturalistic Environments. In: Warwick, C., Arena, P.C., Burghardt, G.M. (eds) Health and Welfare of Captive Reptiles. Springer, Cham. https://doi.org/10.1007/978-3-030-86012-7_15
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