Introduction
Most definitions of environmental enrichment centre on the idea of implementing changes in a captive animal’s environment to improve its welfare. As such, environmental enrichment has the potential to be an effective welfare tool, widely and increasingly used in the management of captive animals in a variety of contexts, from private ownership/collections to zoos. For zoos and aquaria especially, increased public demand, and stricter legal and industry regulations are ensuring standards are sought to be improved (Whitham & Wielebnowski Reference Whitham and Wielebnowski2013; Kagan et al. Reference Kagan, Carter and Allard2015). This has occurred in conjunction with an intensification of zoo-based welfare research and an increased use of evidence-based welfare methods (Mellor et al. Reference Mellor, Hunt and Gusset2015; Ward et al. Reference Ward, Sherwen and Clark2018; Rose et al. Reference Rose, Brereton, Rowden, de Figueiredo and Riley2019; Whittaker et al. Reference Whittaker, Golder-Dewar, Triggs, Sherwen and McLelland2021). Furthermore, since its popularisation in the 1990s (Shepherdson Reference Shepherdson2003), the theoretical framework for environmental enrichment has developed considerably (Newberry Reference Newberry1995; Mellen & MacPhee Reference Mellen and MacPhee2001; Shepherdson Reference Shepherdson2003; Tarou & Bashaw Reference Tarou and Bashaw2007; Watters Reference Watters2009; Alligood & Leighty Reference Alligood and Leighty2015), leading to a steady increase in research studies (Hoy et al. Reference Hoy, Murray and Tribe2010). However, in spite of these advances, the use of enrichment as a welfare tool has been impeded by various persistent gaps in knowledge, particularly regarding zoo animal welfare (Melfi Reference Melfi2009).
First, animal welfare science has traditionally focused on avoiding poor welfare (e.g. pain, fear), hence the prevalence of negative indicators and the relative lack of knowledge regarding positive measurements (Yeates & Main Reference Yeates and Main2008; Melfi Reference Melfi2009; Maple & Perdue Reference Maple and Perdue2013). In addition, animal welfare in zoos has mostly been assessed using resource-based measurements, namely what resources are provided to the animals (e.g. enclosure dimensions, shelter, nutrition), instead of directly measuring the animals’ physical, physiological, psychological, and behavioural state (i.e. animal-based; European Food Safety Authority [EFSA] 2012). Nevertheless, a shift in perspective is taking place on both fronts (Butterworth et al. Reference Butterworth, Mench, Wielebnowski, Olsson, Appleby, Olsson and Galindo2011; Whitham & Wielebnowski Reference Whitham and Wielebnowski2013). There is increased awareness of the need to use more positive measures of welfare (e.g. Boissy et al. Reference Boissy, Manteuffel, Jensen, Moe, Spruijt, Keeling, Winckler, Forkman, Dimitrov, Langbein, Bakken, Veissier and Aubert2007; Mellor Reference Mellor2016; Yeates Reference Yeates2016; Williams et al. Reference Williams, Chadwick, Yon and Asher2018; Yon et al. Reference Yon, Williams, Harvey and Asher2019), and to move progressively towards the use of animal-based welfare measures to complement and validate resource-based measurements (e.g. Hewitt & Small Reference Hewitt and Small2021; Whittaker et al. Reference Whittaker, Golder-Dewar, Triggs, Sherwen and McLelland2021; Augustine et al. Reference Augustine, Baskir, Kozlowski, Hammack, Elden, Wanner, Franklin and Powell2022; Howard & Freeman Reference Howard and Freeman2022).
A second, long-standing issue is the use of tradition, myths, or anecdotal evidence as a staple source of information for husbandry practices (Melfi et al. Reference Melfi, Bowkett, Plowman, Pullen, Plowman and Tonge2005; Melfi Reference Melfi2009; Mendyk Reference Mendyk, Berger and Corbett2018; Riley & Rose Reference Riley and Rose2020; Mendyk & Warwick Reference Mendyk, Warwick, Warwick, Arena and Burghardt2023), rather than systematic empirical studies that evaluate the effectiveness of specific welfare tools. Arbuckle (Reference Arbuckle2010, Reference Arbuckle2013) introduced the term ‘folklore husbandry’ in the context of exotic animal husbandry (particularly herpetofauna) to refer to established methods in husbandry that lack empirical evaluation. Many such methods are shared through dubious or non-peer reviewed literature, such as reports, internet articles, care-sheets and other grey literature (Melfi Reference Melfi2009; Riley & Rose Reference Riley and Rose2020; Tuite et al. Reference Tuite, Moss, Phillips and Ward2022; Mendyk & Warwick Reference Mendyk, Warwick, Warwick, Arena and Burghardt2023).
Third, environmental enrichment pursues the improvement of an animal’s well-being, so its effectiveness needs to be evaluated empirically. This necessary step is frequently overlooked due to a lack of welfare assessment tools and/or resources and information (Therrien et al. Reference Therrien, Gaster, Cunningham‐Smith and Manire2007; Rosier & Langkilde Reference Rosier and Langkilde2011; Warwick et al. Reference Warwick, Arena, Lindley, Jessop and Steedman2013; Alligood & Leighty Reference Alligood and Leighty2015; Alligood et al. Reference Alligood, Dorey, Mehrkam and Leighty2017; Benn et al. Reference Benn, McLelland and Whittaker2019). In addition, enrichment strategies involve environmental modification, the design of which needs to be carefully tailored to each species’ normal behavioural repertoire and life history (Newberry Reference Newberry1995; Mellen & MacPhee Reference Mellen and MacPhee2001; Shepherdson Reference Shepherdson2003; Kuppert Reference Kuppert2013; Greenberg Reference Greenberg, Warwick, Arena and Burghardt2023), which is lacking or limited for many captive species (Mellor et al. Reference Mellor, Hunt and Gusset2015).
Finally, zoo animal welfare research has traditionally shown a marked taxonomic bias towards mammals, with studies involving other taxa (e.g. reptiles) lagging behind (Burghardt et al. Reference Burghardt, Ward and Rosscoe1996; Burghardt Reference Burghardt2013, Reference Burghardt, Melfi, Dorey and Ward2020; Kuppert Reference Kuppert2013; Mehrkam & Dorey Reference Mehrkam and Dorey2014; Rose et al. Reference Rose, Brereton, Rowden, de Figueiredo and Riley2019). For instance, Rose et al. (Reference Rose, Brereton, Rowden, de Figueiredo and Riley2019) conducted a systematic review of zoo and aquarium welfare research from 2009 to 2018 and found that 69% of research papers focused on mammals, similar to that reported in other studies (Melfi Reference Melfi2009; Binding et al. Reference Binding, Farmer, Krusin and Cronin2020). In the case of environmental enrichment, de Azevedo et al. (Reference De Azevedo, Cipreste and Young2007) analysed 744 peer-reviewed enrichment papers (from 1985 to 2004) and reported that 90.2% (n = 635) focused on mammals, with reptiles representing a mere 0.57% (n = 4). Similarly, Alligood and Leighty (Reference Alligood and Leighty2015) found that only 7% (n = 7) of articles pertained to reptiles and amphibians in the period from 2002 to 2014 compared to 90% (n = 86) devoted to mammals; as a case-in-point, primate studies quintupled those with reptiles and amphibians. This taxonomic bias persists, despite ample evidence that reptiles can benefit from properly designed enrichment protocols (e.g. Case et al. Reference Case, Lewbart and Doerr2005; Burghardt Reference Burghardt2013; Londoño et al. Reference Londoño, Bartolomé, Carazo and Font2018; Hoehfurtner et al. Reference Hoehfurtner, Wilkinson, Nagabaskaran and Burman2021).
Unfortunately, many gaps in our knowledge exist regarding successful enrichment practices for reptiles, and the current status for reptiles in zoos is relatively unknown (e.g. Eagan Reference Eagan2019; Riley & Rose Reference Riley and Rose2020; Tuite et al. Reference Tuite, Moss, Phillips and Ward2022). In this study, we evaluated reptile enrichment practices in European zoos. Specifically, we used two surveys to address the following questions: (1) To what extent is enrichment being used for reptiles in European zoos? (2) What are the sources of information, assessment methods, and goals of enrichment for reptiles? (3) Which enrichment types are being used more frequently and for which taxa in particular?
Materials and methods
Data collection
We used the survey platform Typeform© to create and distribute two surveys to collect information on the use of enrichment for reptiles in European zoos. The surveys were available in English, French, Spanish, Czech, Italian, and German. We made a contact list of 384 zoos, cross-referencing a list of zoos accredited by the European Association of Zoos and Aquaria (EAZA), the list of zoos and aquariums of the world (Fisken Reference Fisken2020), and internet searches for zoos in all European countries. Zoos that stated clearly on their webpage that they had no reptiles were not included in the contact list. We used public contact information (email and website contact forms) to reach the participants and of the 384 zoos we contacted for the first survey (hereafter referred to as main survey), 60% were EAZA-accredited while the remainder had either a different accreditation status or none at all. We created a second survey (hereafter referred to as follow-up survey) to gather information on specific enrichment measures implemented by zoos that had previously responded to the main survey.
Both surveys were prefaced with short introductions stating the rationale of the study and requesting that the survey be completed by a staff member directly involved in the caring for reptiles, as well as a confidentiality and anonymity statement. The survey platform automatically assigned a random code to each participant for use in data analysis. We also provided a definition of environmental enrichment, as well as examples of the different enrichment types established for this study (Table 1). To enable our results to be compared with a previous study of USA zoos (Eagan Reference Eagan2019), we used the same categories for both reptile groups and enrichment types, except for the merging of ‘natural enrichment devices’ and ‘man-made enrichment devices’ into a single category of ‘enrichment objects and devices.’ We included olfactory enrichment in a broader category entitled ‘sensory enrichment’ (Table 1). The following reptile categories were used: (a) non-venomous snakes; (b) venomous snakes; (c) turtles; (d) tortoises; (e) crocodilians; (f) monitor lizards (genus Varanus); and (g) non-monitor lizards.
Categories and specific examples of environmental enrichment for captive reptiles in zoos (adapted from Eagan 2009)
The main survey was endorsed by the Council of the Societas Europaea Herpetologica (SEH), which provided a support letter to be included with the initial contact email. We sent this first email in October 2020. Two reminders were sent to zoos that did not respond initially in December and January 2021. Data collection for the main survey ended in late February 2021, when we started sending out the follow-up survey to the zoos that had answered the main one. Data collection for the follow-up survey lasted two months.
Statistical methods
We performed G-tests to determine whether our sample was biased by accreditation status (EAZA vs non-EAZA) relative to the population of zoos that were contacted. We also performed G-tests to determine if significant differences existed between (a) reptile groups for each type of enrichment, and (b) enrichment type use within each reptile group. All P-values were adjusted following the Holm-Bonferroni correction for multiple testing (Holm Reference Holm1979). To control for the effect of zoo, we performed a binomial generalised linear mixed model (GLMM) with ‘Provided to taxa’ as the response variable, ‘Enrichment’, ‘Taxon’ and the interaction between the two as fixed factors, and ‘Zoo’ as a random factor. We coded the binary response variable ‘Provided to taxa’ (1, 0) for each enrichment type if the zoo applied it to the taxa included in their collection (1) or not (0). To explore the use of each enrichment type within each taxon we fitted an additional binomial GLMM with the same predictors for each reptile group. We used ANOVA type III to compute P-values.
Most questions in the follow-up survey were open-ended, and the answers were analysed using thematic analysis (Braun & Clarke Reference Braun and Clarke2006, Reference Braun, Clarke, Cooper, Camic, Long, Panter, Rindskopf and Sher2012). After familiarisation with the data, we started coding the responses using a deductive approach in a descriptive way, generating initial codes for all the enrichment techniques described by the respondents. Once these initial codes were identified, we categorised them into different themes, looking for patterns that matched the general categorisation of enrichment types. Finally, we reviewed the themes and codes, searching for redundancy and eliminating or merging codes and/or elevating them to theme category when necessary. All remaining data were analysed using descriptive statistics.
Results
Participants
The main survey had a 32% response rate (n = 121). Among the zoos we contacted initially (n = 384), 229 were accredited by EAZA while 155 were not. Of those zoos that responded to the survey, 73% were accredited by EAZA, 12% had a different accreditation status (e.g. BIAZA, AIZA, SAZA, EPP), and 15% had none. The response rate was higher from EAZA-accredited zoos, with 88 participants (40% of the 229 initially contacted) being accredited by EAZA. In contrast, the response rate for non-EAZA-accredited zoos was 20% (33 out of 155 initially contacted). We found a significant difference in response rates based on accreditation status (G-test: G = 8.58, df = 1; P = 0.0034).
Almost all respondents (98%; 118) reported using some form of enrichment for at least some of their animals; out of these 118 zoos, 14% (16) did not use any enrichment for their reptiles. Of the zoos that reported not using enrichment with their reptiles, 14 were EAZA-accredited, one had another accreditation status, and one had no accreditation.
Regarding the person completing the survey on behalf of the zoo, 36% (44) were zookeepers, 31% (37) listed ‘management’ as their occupation, 12% (15) were veterinarians, and 21% (25) listed ‘other’ as their job. Twenty of the participants that chose the latter option (17% of the total) listed ‘curator’ as their occupation using the space provided. The remaining five participants that chose ‘other’ (4% of the total) did not specify their occupation. As ‘curator’ was not listed in the available options, we note that responses under the option ‘management’ may include curatorial roles. Almost half of respondents (45%; 55) had received formal training in environmental enrichment, while 54% (65) had not.
The most common taxa in the respondents’ institutions were tortoises (88%), non-monitor lizards (84%), and non-venomous snakes (83%), followed by turtles (75%) and crocodilians (60%). Monitor lizards were kept in 40% of participants’ zoos and only 22% had venomous snakes.
The remaining demographic information regarding institution type, number of species and number of reptile specimens in the institution, and country where the institution is located can be found in the Supplementary material (Tables S2–S5).
The follow-up survey was sent to the 102 zoos that answered the main survey and provided their reptiles with enrichment. This had a 42% response rate (n = 43).
Main survey results
We found significant differences in the type of enrichment across and within reptile groups (Table 2). Additionally, we found a significant interaction between enrichment type and taxon (GLMM [binomial]: χ 2 = 169.19, df = 30; P < 0.001), evidencing that the use of different enrichment types varied depending on the taxa. Overall, monitor lizards and tortoises were the most enriched, followed by non-monitor lizards and turtles. Crocodilians, non-venomous snakes and venomous snakes were the least enriched groups (Figure 1). ‘Structural/habitat design’ and ‘dietary’ enrichment stood out as the most commonly used enrichment types (Figure 1). When broken down by reptile group, these two enrichment types remained the most frequently used except for snakes, for whom ‘dietary’ enrichment was provided in a relative lower proportion than for other taxa (Figure 2). ‘Training/behavioural conditioning’ was used the least except for crocodilians and monitor lizards, for whom it was the third most frequent enrichment type (Figure 2). Frequency for all enrichment types was very similar for both groups of snakes but, overall, non-venomous snakes were more likely to be provided with enrichment than venomous ones (Figure 2). Turtles and particularly tortoises stood out in the use of ‘social’ enrichment in comparison with other taxa (Figure 2). Use of enrichment for these taxa in USA zoos (Eagan Reference Eagan2019) follows a similar trend as in Europe (Figure 3).
Provision of different types of environmental enrichment for reptiles in study zoos (%) and G-test results 1
1 Numbers in parentheses next to each reptile group represent the total number of zoos that are providing reptiles with enrichment and have that particular reptile group in their installations. The total number of zoos that provided reptiles with enrichment was n = 102. Numbers in parentheses under each form of enrichment are the raw number of respondents. P-values reported remained significant after applying Holm’s (Reference Holm1979) sequential Bonferroni correction for experiment-wise error rate due to multiple testing. Percentages >50 are in bold.
Frequency of general enrichment use for (a) each reptile taxon and (b) each enrichment category utilisation. Letters represent a compact letter display (cld) of every post hoc pair-wise comparison. Means not sharing any letter are significantly different by the Tukey-test at the 5% level of significance.
Frequency of each type of enrichment for each reptile taxon. Letters represent a compact letter display (cld) of every post hoc pair-wise comparison. Means not sharing any letter are significantly different by the Tukey-test at the 5% level of significance.
Percentage usage of each type of enrichment for all reptile taxa in European zoos (pink) and USA zoos (blue; Eagan Reference Eagan2019). Numbers in parentheses below each reptile group name represent the total number of zoos providing reptiles with any type of enrichment and having that particular group in their installations. The numbers on top of each bar indicate the total number of zoos providing that specific type of enrichment for the corresponding reptile group. In our study, we used the category of ‘enrichment objects and devices’ as the sole category, unlike the two categories used in the USA study to refer to object enrichment. To enable comparison between both locations, we calculated the mean percentage and number of respondents for the categories ‘natural enrichment devices’ and ‘man-made enrichment devices’ in the USA. As each zoo hosting any reptile group may use different types of enrichment simultaneously, the percentages for a single taxon may exceed 100.
Participants were questioned about whether they kept track of enrichment provision frequency and type of enrichment used, with 79% declaring that they did not follow any kind of schedule, compared to 21% who did. Of those using a schedule, 90% kept track of how often enrichment was provided and 88% kept track of the type of enrichment provided.
Most respondents (92%) considered that promoting natural/species-specific behaviours was the main reason for enrichment, followed by the facilitation of husbandry/veterinary procedures (50%). Almost half of the participants also chose the reduction of abnormal/stereotyped behaviour as a reason, but it was only considered a primary reason in 1% of cases (Table 3). Responses for ‘other reasons’ included increase of activity levels of reptiles for public viewing, and mental stimulation.
Reasons given by study zoos for providing reptiles with enrichment 1
1 Percentages calculated out of total of zoos that provide enrichment to reptiles (n = 102). The question for ‘reasons’ was multiple choice but for ‘primary reason’ participants could select only one answer.
Zoos that reported not using enrichment were directed to a set of questions asking the reasons why (Table 4). The main reason was ‘not knowing what to use’ (37%) followed by lack of time (26%) and staff (16%). Lack of money was also a primary reason (11%). Of the 19 zoos that did not provide enrichment to any of their animals, ten had not considered it, according to the respondents.
Reasons given by study zoos to explain a lack of provision of enrichment 1
1 Percentages calculated out of total of zoos that did not provide enrichment to reptiles or to any of their animals (n = 19)
Regarding how enrichment for reptiles was assessed for effectiveness, most participants reported using behavioural measures (i.e. 70% measured whether there was an increase in normal behaviour, while 54% measured use of enrichment by the animals) followed by biological measurements such as growth, weight and shedding (42%). Nineteen percent of respondents did not use any assessment (Table 5).
Assessment methods utilised by study zoos to ascertain effectiveness of reptile enrichment 1
1 Percentages calculated out of total of zoos that provide enrichment to reptiles (n = 102)
Most participants relied on word-of-mouth information from other zookeepers for enrichment ideas for reptiles; along with the internet, this made up for 57% of primary enrichment sources. Other primary sources such as peer-reviewed journal articles and books on environmental enrichment, although reported to be commonly used, were not part of the most used primary sources (Table 6).
Sources of information for study zoos as regards ideas for reptile enrichment 1
1 Percentages calculated out of total of zoos that provide enrichment to reptiles (n = 102)
Follow-up survey results
Most of the follow-up survey questions were open-ended, allowing participants to answer freely what they considered to be enrichment in each of the previously established categories and for each reptile group. All answers are presented in Table 7, resulting in 42 codes and 15 themes. Frequencies were calculated using the codified answers within each taxon (see Table S1 in Supplementary material). Due to the large amount of data, Table S1 only reflects the most frequent themes/codes, amounting to ≥ 65% of the total frequency of enrichment techniques for each reptile group.
General codes (themes) and specific codes for the thematic analysis of the follow-up study’s open-ended questions regarding specific enrichment techniques
Two of the most common enrichment techniques for all taxa were ‘structural/thermal complexity’ and ‘enrichment objects’, followed by ‘cohabitation’ and ‘varying feeding presentations/patterns’ (the latter were present in all taxa but monitor lizards and crocodilians, respectively). ‘Varying feeding presentations/patterns’ included hiding and hanging food around the enclosure, among other techniques of which ‘food chase’ stood out for non-venomous snakes. Another nutritional enrichment used by most zoos is ‘different food items’, present in all taxa except snakes. ‘Varying furniture’ was an enrichment technique only used for turtles and non-venomous snakes, while ‘olfactory enrichment’ made up an important percentage of enrichment for both groups of snakes and non-monitor lizards. Finally, ‘associative learning’ was only prevalent for crocodilians and monitor lizards, and it encompassed ‘target training’, ‘behavioural conditioning for medical procedures’ and ‘behavioural conditioning for eating/cleaning’ (Table S1).
When asked whether enrichment for reptiles was considered an essential practice or something tackled as a luxury, more than half (60%; 26) reported it to be essential. A smaller percentage (14%; 6) expressed the opinion that for them enrichment was a luxury for reptiles while the rest (26%; 11) considered it to be dependent upon the taxon. Those who chose the latter option were asked for which of their reptiles was enrichment considered essential. All participants that checked this option and had monitor lizards in their collection (9) considered it essential for them. The opposite was seen with venomous snakes: no zoos with venomous snakes (2) considered enrichment essential for them. Regarding the rest of the groups, 56% of zoos deemed enrichment essential for crocodiles (9), 38% for tortoises (8), 33% for turtles (9), 25% for non-monitor lizards (8), and 11% for non-venomous snakes (9).
Open-ended questions were formulated to explore why enrichment was considered essential, a luxury, or group dependent. For those who considered it essential, the reasons were as follows: general well-being (38%), promotion of natural behaviour (31%), mental health (27%), physical health (15%), basic husbandry measure (12%), better management (8%), promotion of reproduction (4%), ethical reasons (4%), avoidance of boredom (4%), decreased stress (4%), and improved quality of life (4%). When asked why enrichment was considered a luxury for reptiles in their installations, the reasons listed, in equal proportion, were: lack of time (33.3%), lack of staff (33.3%), and enrichment considered less important for reptiles than for other groups (33.3%). Responses from participants that answered that the need for enrichment varied according to taxon included: difficulty in implementing, financial restrictions, lack of validation for enrichment in some groups, and insufficient resources to enable enrichment for all species or individuals. To this question, several respondents added information, particularly referring to monitor lizards and crocodilians: “Large, charismatic species and enrichment form part of public engagement” (referring to Komodo dragons [Varanus komodoensis]); “I think that monitor lizards and crocodilians are more intelligent than other reptiles”; “There are more studies being made on this group” (referring to monitor lizards); “They have different necessities than the rest” (referring to monitor lizards). We also questioned participants whether enrichment for reptiles was used routinely, or reactive to arising issues (e.g. behavioural, medical problems). More than half of respondents answered that enrichment in their facility was used routinely (56%; 24), while 12% (5) used it to deal with problems (reactive). Thirty-three percent (14) used it routinely for some reptiles but reactively for others. Regarding this last option, 100% of zoos with monitor lizards in their collection used it routinely for them (8), followed by 89% for crocodilians (10), 50% for non-monitor lizards (13), 29% for tortoises (14), 21% for non-venomous snakes (14), 20% for turtles (10) and 0% for venomous snakes.
Finally, we asked participants to rate, on a scale from 1 to 10, how important they considered enrichment for several groups of animals. Mean scores calculated out of the total of respondents (n = 41) were: 9.3 (± 1.4) for mammals, 8.6 (± 1.4) for birds, 7.2 (± 1.9) for reptiles, 5.1 (± 2.8) for fishes, and 4.4 (± 2.6) for invertebrates.
Discussion
Using a survey approach, we have examined the current status of environmental enrichment for reptiles in European zoos. Our results allow us to gain a picture of the current practices for reptiles in Europe and to compare the situation to that in the USA. Use of environmental enrichment seems widespread in European zoos, particularly dietary and structural enrichment. Our surveys provided data on enrichment type, and specific enrichment techniques used within each category of enrichment. These data are relevant to help in understanding how reptile enrichment is perceived by practitioners. Additionally, in both surveys, we asked an array of complementary questions that provide valuable insight into the limitations affecting enrichment implementation. Despite being generally considered as important, enrichment implementation presents greater challenges in reptiles in terms of understanding and application compared to various other animal groups, possibly as a result of scarcity of information and a number of other limitations. Foremost among these is the taxonomic bias (‘taxonomic chauvinism’; e.g. Bonnet et al. Reference Bonnet, Shine and Lourdais2002; Pawar Reference Pawar2003) that affects reptiles and other neglected groups.
Importance of environmental enrichment for reptiles and general use
Our results would suggest that the use of environmental enrichment for reptiles in zoos and aquaria is widespread in Europe, however only 121 zoos out of the 384 originally contacted (32% response rate) responded. Also, a greater representation of EAZA-accredited zoos among survey respondents was noted, with a response rate double that of non-accredited zoos or zoos with different accreditation status. It is possible therefore that sampling bias has overestimated the proportion of zoos conducting environmental enrichment with reptiles. Almost all our respondents (118; 98%) used environmental enrichment in their facilities but 14% (16) used it for other animals but not for reptiles. Similarly, all zoos (76) in the USA study (Eagan Reference Eagan2019) reported using enrichment for their animals, but only 5% (4) provided enrichment to some of their animals but not to reptiles. The latter may only provide enrichment for certain token species or to most animals in their care except reptiles (and all the possibilities in-between). When asked about the rationale for allocation of environmental enrichment, zoos that did not enrich their animals reported time, staff and budget constraints, echoing the limitations already detected in other studies (Hoy et al. Reference Hoy, Murray and Tribe2010; Riley & Rose Reference Riley and Rose2020; Tuite et al. Reference Tuite, Moss, Phillips and Ward2022). However, the main reason for the absence of enrichment reported in our study was a lack of knowledge regarding what is appropriate to use.
The taxonomic bias affecting research on environmental enrichment plays a major role in this lack of information (de Azevedo et al. Reference De Azevedo, Cipreste and Young2007; Melfi Reference Melfi2009; Rose et al. Reference Rose, Brereton, Rowden, de Figueiredo and Riley2019; Riley & Rose Reference Riley and Rose2020). The EAZA issues Best Practice Guidelines for species or groups of closely related species kept in zoos (EAZA 2022). Only six of the Guidelines available (as per January 2023) concern reptile species, while mammals garner 32 documents (the rest include one report for fish, four for invertebrates, seven for amphibians, and ten for birds). This example illustrates how taxonomic bias affects the amount of information readily available for zoos. Also, most enrichment practices in non-mammalian species are modelled on enrichment practices designed for mammals, which can be problematic when applied without proper modification and/or evaluation (Mendyk & Augustine Reference Mendyk, Augustine, Warwick, Arena and Burghardt2023). At its inception, environmental enrichment was designed as a means of promoting activity and countering behavioural or welfare problems (a reactive, rather than proactive, approach) in mammals, mainly primates (Young Reference Young2003). Later, its study progressed to a behavioural engineering approach in which the primary stimulus utilised was food (Young Reference Young2003; Fernandez & Martin Reference Fernandez and Martin2021). Exercise and increased activity levels also became important focal points of research (mostly in primates and felines), which shaped the subsequent development of environmental enrichment science and its application. When translated to ectotherms, this inertia is inadequate given that they do not need such frequent feeding, have lower metabolic rates, and their activity is more dependent on ambient temperature.
Zoo professionals also report other barriers to enrichment. For instance, there is a perceived lack of institutional support (i.e. limited interest from zoo management, scarcity of resources, money, or staff) and lack of interest from the wider community in the use of enrichment (Riley & Rose Reference Riley and Rose2020), and a prioritisation of health and physical well-being over psychological or mental well-being (Tuite et al. Reference Tuite, Moss, Phillips and Ward2022). These barriers hamper the widespread use of enrichment; therefore, it is worth considering how enrichment is prioritised for different taxa.
In our follow-up survey we asked participants to rate, on a scale from one to ten, the importance of enrichment for different taxa: reptiles scored third after mammals and birds, which again reflects the taxonomic bias affecting animal welfare and enrichment science. Many reasons contribute to reptiles lagging behind in any prioritisation enrichment plan. Underlying those reasons is the perception that reptiles are perceptually/cognitively limited animals whose requirements in captivity are modest compared to other groups, and are capable of tolerating even the most impoverished captive conditions (Burghardt Reference Burghardt2013; Maple & Perdue Reference Maple and Perdue2013). These misconceptions, which often stem from inadequate or misleading information, have been sternly criticised (e.g. Burghardt Reference Burghardt, Gans and Tinkle1977; Warwick et al. Reference Warwick, Frye and Murphy1994; Burghardt Reference Burghardt, Mitchell, Thompson and Miles1997; Young Reference Young2003; Font et al. Reference Font, Burghardt, Leal, Warwick, Arena and Burghardt2023; Mendyk & Warwick Reference Mendyk, Warwick, Warwick, Arena and Burghardt2023), but these have had limited success in correcting such widespread misconceptions about reptile biology and behaviour. Recently, public interest in animal welfare has prompted a perspective shift in how reptiles are perceived and treated. Studies on reptile sentience (e.g. for reviews, see Lambert et al. Reference Lambert, Carder and D’Cruze2019; Learmonth Reference Learmonth2020), cognition (e.g. Cooper et al. Reference Cooper, Liew, Andrle, Cafritz, Dallas, Niesen, Slater, Stockert, Vold, Young and Mendelson2019; Font Reference Font2019, Reference Font, Vonk and Shackelford2020; Burghardt Reference Burghardt, Melfi, Dorey and Ward2020; LaDage et al. Reference LaDage, Roth, Cerjanic, Sinervo and Pravosudov2012; Szabo et al. Reference Szabo, Noble and Whiting2021), play (e.g. Burghardt Reference Burghardt2005, Reference Burghardt2013, Reference Burghardt2015; Dinets Reference Dinets2015; Kane et al. Reference Kane, Davis and Michaels2019), and complex sociality (e.g. Doody et al. Reference Doody, Burghardt and Dinets2013, Reference Doody, Dinets and Burghardt2021; Gardner et al. Reference Gardner, Pearson, Johnston and Schwarz2016; Dinets Reference Dinets2017; Skinner & Miller Reference Skinner and Miller2020; Baker et al. Reference Baker, Frère, Franklin, Campbell, Irwin and Dwyer2023) have accumulated in recent years. Although this shift in perception is positive, the lack of scientific validation for reptile husbandry practices is a persistent problem, particularly important given the large number and diversity of reptiles being traded into captivity (e.g. Warwick Reference Warwick2014; Draper & Jones Reference Draper and Jones2017; Warwick et al. Reference Warwick, Steedman, Jessop, Arena, Pilny and Nicholas2018; Altherr & Lameter Reference Altherr and Lameter2020).
Foundations of enrichment for reptiles in European zoos
The use of reliable, validated welfare tools is of utmost importance in the pursuit of successful husbandry practices (Alligood & Leighty Reference Alligood and Leighty2015; Benn et al. Reference Benn, McLelland and Whittaker2019). This process requires a solid basis, from the conception of any husbandry idea to the evaluation of its effectiveness; therefore, participants were questioned on the foundations of current zoo enrichment practices for reptiles. In both Eagan’s (Reference Eagan2019) and the present study, the primary source of enrichment ideas was word-of-mouth, i.e. information from other zookeepers and professionals. Peer-reviewed articles are used as a primary source behind internet articles and information provided by zoos’ accreditation institutions. Riley and Rose (Reference Riley and Rose2020) reported low use of journal articles by zoo practitioners, and their perception was that literature availability was limited when making decisions on enrichment. It is possible that the scientific advances on reptile welfare and enrichment go unnoticed either because they are published outside the direct scope of zoological publishing (Mendyk Reference Mendyk2022), or because accessibility to peer-reviewed literature is limited (Riley & Rose Reference Riley and Rose2020), so zoo professionals rely on more proximate or familiar sources. Some of those alternative sources fall into the realm of grey literature, and this can be problematic due to a lack of validation. Although easily disseminated and more accessible, information distributed through non-reviewed sources, such as internet articles or word-of-mouth, has a higher probability of containing misinformation (Warwick et al. Reference Warwick, Arena, Lindley, Jessop and Steedman2013; Warwick Reference Warwick2014; Draper & Jones Reference Draper and Jones2017; D’Cruze et al. Reference D’Cruze, Paterson, Green, Megson, Warwick, Coulthard, Norrey, Auliya and Carder2020; Mendyk & Warwick Reference Mendyk, Warwick, Warwick, Arena and Burghardt2023). Thus, these types of sources are not only unreliable (Loughman Reference Loughman2020), but can become fertile ground for the perpetuation of folklore husbandry. To move towards evidence-based husbandry, a key distinction has to be made between husbandry practices that are backed by empirical evidence vs ones that are accepted only because of tradition (Arbuckle Reference Arbuckle2013). Otherwise, there is a risk of perpetuating collective knowledge that is at best ineffective and at worse harmful for reptiles in captivity. For instance, one of the most patent examples of folklore husbandry relates to snakes and the size of their enclosures. The use of racks for snake-keeping is commonplace (Loughman Reference Loughman2020), and typically feature small boxes that prevent snakes fully stretching (Warwick et al. Reference Warwick, Arena and Steedman2019). Some of the reasons why snake enclosures are often small and simple derive from folklore (e.g. snakes are sedentary animals that dislike open or large spaces; see Warwick et al. Reference Warwick, Arena and Steedman2019), and sources that recommend their use are based on outdated practices no longer supported by scientific evidence (Warwick et al. Reference Warwick, Grant, Steedman, Howell, Arena, Lambiris, Nash, Jessop, Pilny, Amarello, Gorzula, Spain, Walton, Nicholas, Mancera, Whitehead, Martínez-Silvestre, Cadenas, Whittaker and Wilson2021).
In the present study, the most frequently used assessment methods for effectiveness were an increase in normal behaviour and use of the enrichment provided, similar to Eagan’s study (2019). In both studies, a similar percentage of zoos reported a lack of formal assessment of their enrichment techniques (14 and 19% in USA and Europe, respectively). Animal-based measurements, although of increasing importance in reptile welfare, lag behind resource-welfare measurements (Benn et al. Reference Benn, McLelland and Whittaker2019). For example, physiological welfare indicators (e.g. corticosterone levels) have barely been studied in reptiles and need to be validated in a wider range of species (Benn et al. Reference Benn, McLelland and Whittaker2019; Gangloff & Greenberg Reference Gangloff, Greenberg, Warwick, Arena and Burghardt2023). In our study, we only asked about the use of animal-based measurements, so we cannot know whether there is a preference for animal-based measurements in European zoos, or if the use of resource-based measurements is still dominant for reptile species, as has traditionally been the case (Benn et al. Reference Benn, McLelland and Whittaker2019; Jones et al. Reference Jones, Sherwen, Robbins, McLelland and Whittaker2022). Regardless, behavioural methods seem to be of importance for zoos, probably because they are easier to implement than invasive or resource-intensive methods (Whittaker et al. Reference Whittaker, Golder-Dewar, Triggs, Sherwen and McLelland2021; Jones et al. Reference Jones, Sherwen, Robbins, McLelland and Whittaker2022).
When using behavioural indicators of welfare, it is essential they are applied within a species-specific context that will allow proper interpretation (Bacon Reference Bacon2018; Benn et al. Reference Benn, McLelland and Whittaker2019; Spain et al. Reference Spain, Fuller and Allard2020). For reptiles especially, this comes into direct conflict with the relative scarcity of behavioural observations in the wild (Warwick et al. Reference Warwick, Arena, Lindley, Jessop and Steedman2013), making it difficult to establish what qualifies as abnormal behaviour in captivity. A key but frequently overlooked issue is that reptiles are a highly diverse group, with close to 12,000 currently recognised species. This adds to the challenge of identifying and validating behavioural welfare indicators (Burghardt & Layne-Colon Reference Burghardt, Layne-Colon, Warwick, Arena and Burghardt2023). Finally, interpreting reptile behaviour poses a special challenge due to its characteristics and to our own anthropomorphic tendencies (e.g. Burghardt Reference Burghardt and Ristau1991; Rivas & Burghardt Reference Rivas, Burghardt, Bekoff, Allen and Burghardt2002; Batt Reference Batt2009; Wilkins et al. Reference Wilkins, McCrae and McBride2015; Mather Reference Mather2019). For example, reptilian ectothermic physiology and lack of facial expressions have been proposed as two main factors that may inhibit or complicate assessment of aversive states such as fear or pain (Warwick et al. Reference Warwick, Jessop, Arena, Pliny, Nicholas and Lambiris2017; Whitehead Reference Whitehead2018; Williams & Beck Reference Williams and Beck2021), which in many cases can go unnoticed (Malik Reference Malik2018). Also, there is ample evidence that a species’ likeability decreases with phylogenetic distance and dissimilarity to our species (e.g. Batt Reference Batt2009; Miralles et al. Reference Miralles, Raymond and Lecointre2019). In general, reptiles tend to be disliked by humans and, particularly in the case of snakes, are target of a myriad of negative cultural beliefs (Ceríaco Reference Ceríaco2012; Whitehead Reference Whitehead2018; Janovcová et al., Reference Janovcová, Rádlová, Polák, Sedláčková, Peléšková, Žampachová, Frynta and Landová2019; Da Silva et al. Reference Da Silva, Braga-Pereira, Da Silva, de Oliveira, de Faria Lopes and Alves2021). Yet, not every reptile group is perceived in the same manner.
Differences in enrichment use for each reptile group and specific enrichment techniques
Several studies indicate that some reptiles, such as turtles and tortoises, are perceived in a positive light in contrast to, for instance, snakes (Czech et al. Reference Czech, Krausman and Borkhataria1998; Janovcová et al. Reference Janovcová, Rádlová, Polák, Sedláčková, Peléšková, Žampachová, Frynta and Landová2019; Da Silva et al. Reference Da Silva, Braga-Pereira, Da Silva, de Oliveira, de Faria Lopes and Alves2021). This taxonomic bias is also reflected in our results. Tortoises and monitor lizards received the most enrichment amongst all reptile groups, and all respondents that had monitor lizards in their installations considered it essential for them. The number of respondents for these questions was small, but the narrative in open-ended questions provides insight into why enrichment is perceived differently across taxonomic groups. Some specified that the animals that most likely benefit from enrichment are those that are more active and show more appetite, which mirrors the aforementioned historical inertia for mammal environmental enrichment. One of the respondents wrote that “[Enrichment] may benefit other groups just as much, but it is difficult to tell, when no behaviours are displayed as a reaction to the enrichment.” Particularly with monitor lizards, participants invoked their ‘high intelligence’ and ‘high interaction with environment.’ Size and longevity also seem to be important factors when prioritising the use of enrichment within reptiles, particularly in favour of large, long-lived species such as giant tortoises or crocodiles. It should be noted, however, that the use of enrichment for different reptiles may be affected by how easily its application is perceived (i.e. certain types of enrichment may be thought to be more difficult to implement in reptiles that are potentially dangerous for their caretakers, such as crocodiles or venomous snakes). In any case, as noted by previous studies, research and husbandry efforts focus on large, charismatic species that appeal to the public (e.g. Melfi Reference Melfi2009; Carr Reference Carr2016; Albert et al. Reference Albert, Luque and Courchamp2018; Hosey et al. Reference Hosey, Melfi, Ward, Angelici and Rossi2020) and for which more studies are available. Moreover, scientists and zoo professionals may devote greater efforts to studying more familiar species as there is more information available for them (Rose et al. Reference Rose, Brereton, Rowden, de Figueiredo and Riley2019). Lack of understanding as to what constitutes environmental enrichment was an issue for some of our respondents. For instance, one participant commented that “the problem is that enrichment is not anything definite in reptile-keeping”, while another pointed out that “[…] we are just beginning to understand the importance of reptile enrichment in husbandry.”
Enrichment refers to a change in the environment that fulfils some welfare goals and results in an improvement for the animal. It does not refer to any change or modification for which the outcome is unknown, even though that is how the term is sometimes used (Newberry Reference Newberry1995). In this sense, the present study collected a lot of information on what zoo professionals consider enriching for reptiles. In our follow-up survey we focused on retrieving information on specific enrichment techniques. This resulted in a wide diversity of responses and raises the question as to whether some of these reported enriching techniques should indeed be considered enrichment (Mendyk & Augustine Reference Mendyk, Augustine, Warwick, Arena and Burghardt2023). For example, one of the most commonly reported enrichment techniques in five out of seven reptile groups in our study was the use of different food items: can feeding reptiles with multiple types of food/different prey be considered enrichment or is it simply a matter of basic husbandry? Discrepancies in what qualifies as enrichment for reptiles may be another contributing factor to the taxonomic bias (Riley & Rose Reference Riley and Rose2020), particularly when approaching enrichment from a mammalian perspective (Mendyk & Augustine Reference Mendyk, Augustine, Warwick, Arena and Burghardt2023). Perhaps, what some consider enrichment is just controlled deprivation (Burghardt Reference Burghardt, Burghardt, Bielitzki, Boyce and and Schaeffer1996, Reference Burghardt2013).
Animal welfare implications and conclusion
The need for enrichment has long been recognised as an integral part of husbandry; its use seems widespread in European zoos, but there are also many limitations that prevent its full and consistent implementation. All the gaps affecting animal welfare mentioned above (see Introduction) likely have a greater impact on taxa that have traditionally been neglected. Although reptile welfare is subject to increasing attention, further research is needed on their ecology, behaviour, husbandry, validation of welfare methods, etc. Our study highlights some of the main barriers limiting the use of environmental enrichment for reptiles (such as a scarcity of validated assessment methods, limited access to literature, or lack of well-grounded ideas), underscoring the urgent need for a shift in perspective in reptile environmental enrichment. For instance, zookeepers acknowledge the absence of a clear understanding of enrichment, which can result in mistaking fundamental basic husbandry for enrichment protocols. Hence, reptile enrichment research would benefit from adopting a broader perspective, such as considering a wider array of enrichment types, increasing the number of species studied, and validating different welfare assessment methods. Consider, for example, the use of chemosensory enrichment, which seems to lag behind other types of enrichment despite the critical importance of chemoreception for reptiles (e.g. Chiszar et al. Reference Chiszar, Tomlinson, Smith, Murphy, Radcliffe, Warwick, Frye and Murphy1995; Bashaw et al. Reference Bashaw, Gibson, Schowe and Kucher2016; Londoño et al. Reference Londoño, Bartolomé, Carazo and Font2018).
Furthermore, our study adds to the growing body of literature that evaluates the relationship between captive reptiles and their human carers with regards to different aspects of reptile welfare. This type of approach allows scientists and professionals from other areas to weave different paths of communication that should contribute to mitigate the disconnect between practice and science (Loughman Reference Loughman2020; Riley & Rose Reference Riley and Rose2020; Mendyk Reference Mendyk2022). Our results also reveal a wide set of specific enrichment techniques that are currently being used for reptiles in zoos. In order to clarify the boundary between basic husbandry and enrichment, further research should inquire about what is considered enriching for each species according to zoo professionals.
To conclude, our study highlights the importance of basing species-specific environmental enrichment protocols on currently available information, and to empirically assess them for effectiveness. Zoos are appropriate venues to focus on traditionally disregarded groups such as reptiles, which are also likely to benefit the most from this research.
Supplementary material
The supplementary material for this article can be found at http://doi.org/10.1017/awf.2023.43.
Acknowledgements
We thank all of the zoos that participated in this study. We are grateful to Dr Clifford Warwick for encouragement and advice during the early stages of this project, and to Jindřich Brejcha, Nathalie Feiner, Arnaud Badiane, and Javier Ábalos for kindly translating the survey to Czech, German, French and Italian, respectively. We also thank Taylor Eagan for providing the full questionnaire of her study and for kindly answering our questions. Finally, we would like to thank Antigoni Kaliontzopoulou and the Societas Europaea Herpetologica for endorsing this study and providing a letter of support. This project was funded in part by a grant from the Spanish Ministerio de Ciencia e Innovación (PID2019-104721GB-IOO). AB was supported by a FPU predoctoral fellowship from the Spanish Ministerio de Universidades (FPU18/04021).
Competing interest
None.
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