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The physiological and behavioural impacts of and preference for an enriched environment in the eastern box turtle (Terrapene carolina carolina)

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Abstract

The physiological and behavioural impact of, as well as preference for, enriched versus barren environments was determined for captive eastern box turtles (Terrapene carolina carolina). Thirty-eight box turtles were randomized to either barren (flat newspaper substrate) or enriched (cypress mulch substrate, shredded paper and a hide box) enclosures for a 1-month period. Complete blood counts, fecal corticosterone, and body weights were measured at the beginning and end of the test period. Activities performed within the two environments were also compared.Turtles in enriched enclosures had a significantly lower heterophil to lymphocyte ratio (H/L) at the end of the treatment period (p=0.01). Enriched-housed turtles also spent significantly less time engaged in escape behaviour (p

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... Those studies that have been carried out have generally found that enrichment is beneficial (e.g. Chelonia, Therrien et al., 2007;Case et al., 2005;Mehrkam andDorey, 2014 andlizards Phillips et al., 2011;Hennig and Dunlap, 1978;Londoño et al., 2018;Bashaw et al., 2016). There are very few studies investigating snake welfare (e.g. ...
... Furthermore, the lack of a choice of hiding places in the Standard condition resulted in the snakes using suboptimal hiding places (i.e. under the newspaper), as seen in Eastern box turtles who took shelter under the paper substrate or water dish when no hiding places were provided (Case et al., 2005). ...
... e. Enriched > Standard) rather than being the 'best' possible resource; and so, in this instance, the Enriched enclosure that we provided was preferred to the Standard enclosure, rather than being the optimal environment for housing corn snakes. There have been few preference tests applied in reptiles, but Case et al. (2005) identified a distinct preference for an enriched, rather than a barren, enclosure in eastern box turtles (Terrapene carolina carolina), regardless of their previous housing experience. Further applications of this approach are therefore strongly recommended given its importance and apparent effectiveness in reptile welfare assessment. ...
Article
There is a wealth of evidence demonstrating the benefits of environmental enrichment across a range of different animal species. However, there is comparatively little such research into the effect of enrichment provision on captive reptiles. The aim of this study was therefore to ascertain if an increase in environmental complexity was beneficial to the behaviour and welfare of corn snakes (Pantherophis guttatus). The study used a combination of behavioural observations in the home enclosure, behavioural tests of anxiety, and a preference test. The snakes used the enrichment when it was available to them and enriched snakes showed changes in general behaviour reflective of improved welfare. However, the anxiety tests revealed few effects of enrichment provision on performance. In contrast, the snakes exhibited a strong preference for the enriched enclosure when given a choice. These findings suggest that the provision of environmental complexity to the enclosure was beneficial to the behaviour and welfare of captive corn snakes. We therefore recommend enrichment should be used when keeping captive snakes.
... This result also supports the idea that reptiles respond to enrichment like carnivorous mammals: that they benefit from increased behavioral opportunities. Case et al. (2005) found that eastern box turtles (Terrapene carolina carolina) in barren enclosures spent more of their time trying to escape and less time resting, compared to those in enriched housing [26]. However, there have been studies that have not demonstrated benefit from enrichment in reptiles, such as Rosier & Langkilde's (2011) study on the arboreal eastern fence lizard (Sceloporus undulates) [27]. ...
... This result also supports the idea that reptiles respond to enrichment like carnivorous mammals: that they benefit from increased behavioral opportunities. Case et al. (2005) found that eastern box turtles (Terrapene carolina carolina) in barren enclosures spent more of their time trying to escape and less time resting, compared to those in enriched housing [26]. However, there have been studies that have not demonstrated benefit from enrichment in reptiles, such as Rosier & Langkilde's (2011) study on the arboreal eastern fence lizard (Sceloporus undulates) [27]. ...
... An increase in the ratio of heterophils to lymphocytes in whole blood is often seen in response to stress [46]. However, in Case et al.'s (2005) study on the eastern box turtle, whilst the enriched group displayed a significantly lower heterophil to lymphocyte ratio, there was no change in corticosterone concentration between the two groups [26]. Terrapins under hyperosmotic stress also tended to have increased hematocrit, heterophil count, sodium, chloride and potassium [47]. ...
Article
Full-text available
Reptiles are held at wildlife parks and zoos for display and conservation breeding programs and are increasingly being kept as pets. Reliable indicators of welfare for reptiles need to be identified. Current guidelines for the captive management of reptiles utilize resource-based, rather than animal-based indicators; the latter being a more direct reflection of affective state. In this paper we review the literature on welfare assessment methods in reptiles with a focus on animal-based measures. We conclude that, whilst a number of physiological and behavioral indicators of welfare have been applied in reptiles, there is need for further validation of these methods across the diversity of species within the Class. Methods of positive welfare state assessment are comparatively understudied and need elucidation. Finally, we examine some widely-used welfare assessment tools in mammals and explore the application of the Welfare Quality® Protocol to the endangered pygmy blue-tongue skink, Tiliqua adelaidensis. We propose that this framework can form the basis for the development of taxon-specific tools with consideration of species-specific biology.
... Different reasons have been suggested for this. The repertoire of abnormal behaviours is still relatively unknown for most reptile species (Warwick, 1990), which has probably contributed to promote the misconception that reptiles are highly adaptable and tolerant to impoverished captivity conditions, so that enrichment is not needed or is less important than in other taxa (Case, Lewbart, & Doerr, 2005). In addition, reptiles are not as common companion and/or production animals as other vertebrates, and hence there has been less economic and social incentive to study their husbandry, health and captive management (Phillips et al., 2011). ...
... is an abnormal behaviour exhibited by lizards in captivity, including P. liolepis (e.g., Gómez et al., 1993), and has been previously used as an indicator of poor welfare in reptiles (Bashaw, Gibson, Schowe, & Kucher, 2016;Case et al., 2005;Manrod & Hartdegen, 2008;Warwick, 1990). Every day, after lights went on (8:00 hr), one observer (C.L.) recorded the occurrence of the afore-mentioned behaviours using scan sampling (every 15 min between 8:00 and 11:00 hr) and an instantaneous recording rule. ...
... We also detected a marked decrease in escape attempts in enriched versus control lizards. "Escape attempt" is an abnormal behaviour frequently associated with poor welfare in reptiles (e.g., Case et al., 2005;Warwick, 1990 Drazilova, 2006). We suggest that, in our experiment, changing the identity of odour donors may have contributed to these long-lasting effects by preventing habituation (e.g., Carazo et al., 2008). ...
... Experimental manipulation of captive-reared animals should help elucidate such trends and inform management. Previous work demonstrated adult eastern box turtles prefer an enriched environment over an unenriched one (Case et al., 2005), but how prior captive conditions affect preference has not been considered. ...
... For instance, captive-raised juvenile coal tits (Periparus ater) and blue tits (Cyanistes caeruleus) with no experience of vegetation demonstrated innate preference for the vegetation type each respective species commonly selects in nature (Partridge, 1974). In an experiment similar to ours, adult eastern box turtles spent over 90% of their time in an enriched environment when given the choice between enriched and unenriched sides of an enclosure, regardless of previous short-term housing condition (Case et al., 2005). However, the prior experiences of turtles used in that study were not entirely known like they were for our captiveborn turtles. ...
... However, the returns for others may be rather limited if animals have innate preference for particular habitats that cannot be shaped by captive-rearing conditions. Regardless, addressing basic animal welfare concerns during captive-rearing can be easily accomplished by conducting such experimental assessments of captive habitat preference (Case et al., 2005). ...
Article
Habitat choice has broad repercussions for animals, but mechanisms influencing such choices are generally not understood. When conducting conservation translocations using captive-reared animals, elucidating mechanisms influencing habitat preference pre-release could inform rearing methods and post-release behavior. We raised 32 captive-born eastern box turtles (Terrapene carolina ) for eight months—16 in naturalistic enriched enclosures and 16 in unenriched enclosures. We then let each turtle choose between environments simulating both rearing conditions in a novel enclosure to evaluate the hypothesis that rearing environment influences habitat selection. Preference for the enriched environment was exhibited by enriched (selection probability = 0.81, 95% CI: 0.54–0.96) and unenriched (selection probability = 0.88, 95% CI: 0.62–0.98) turtles. Those that chose the enriched habitat (n = 27) did so in less than half the time (x = 504.8 sec, 95% CI: 266.49–743.04) than those that selected the unenriched one (n = 5, x = 1339.0 sec, 95% CI: 783.84–1894.07, P = 0.009). Selection latency did not differ between rearing treatments (P = 0.871). We conducted a second experiment to clarify if preferences were based on familiarity or novelty by using the same enclosure, but we gave individuals a choice between the habitat representing their rearing condition and a novel object (empty tissue box). Preference for respective rearing environment was exhibited by enriched (selection probability = 0.87, 95% CI: 0.59–0.98) and unenriched (selection probability = 0.81, 95% CI: 0.54–0.96) individuals. Selection latency did not differ based on side chosen (P = 0.439) or rearing treatment (P = 0.764). Selection latency was repeatable by individuals (R = 0.47, 90% CI = 0.24–0.71, P = 0.003), and this personality trait may be heritable since it was also repeatable by clutch mates (R = 0.36, 90% CI = 0.03–0.62, P = 0.001). Preference for a naturalistic environment by captive-born eastern box turtles appears to be driven by an innate mechanism rather than based on prior experience. Housing this species in enriched enclosures should increase welfare. Moreover, our collective findings highlight the importance of evaluating how intrinsic effects could affect translocation outcomes.
... Remarkably, and in contrast to previously mentioned research on mammals and birds, there does not appear to be a general consensus about the effect of EP on stress levels in reptiles. While the majority of research does demonstrate a positive effect of EP on the animals' well-being, the studies by Case et al (2005) andTherrien et al (2007) give mixed results whereby certain variables do not indicate a positive effect of EP. Research that should be discussed separately, given the fact that it is a good example of a study with negative findings ...
... Heterophils (neutrophils in mammals and amphibians) are part of the innate immune system, while lymphocytes are part of the acquired immune system. High ratios of heterophils to lymphocytes in blood samples are considered an indication of high glucocorticoid and stress values in all vertebrate taxa (for a review, see Davis & Maerz 2008), including reptiles ( Saad & Elridi 1988;Morici et al 1997;Lance & Elsey 1999;Case et al 2005;Chen et al 2007). Blood (max 60 µl) was obtained from the post-orbital sinus via insertion of a capillary tube (75 mm; 60 µl) between the eye and the eyelid ( Maclean et al 1973). ...
... This small sample size could have resulted in inaccurate results for the FCM measurements. Another possible explanation is discussed in the study by Case et al (2005). They state that, although acute stress is often associated with an increase of plasma corticosterone, chronic stress could actually lead to a suppression of corticosterone production. ...
Article
Full-text available
In response to an increased awareness concerning the welfare of captive animals, several studies have investigated the effect of provisions on stress levels in model species, such as small mammals, birds and fish. In contrast, reptiles have received less attention. Although many reptilian species are becoming increasingly popular in the pet trade and are frequently used as model species in various branches of biology and a number of studies have explored how they react to stress in different contexts (eg social, predatory), little is known about how they react to stress induced by housing conditions or experimental treatments. In this study, we quantified the effect of provision of perches and leaves as refuges (provisioned) on the behaviour, morphology and physiology of the green anole (Anolis carolinensis). Our results showed that increased or decreased structural complexity of the cage had no effect on body mass, tail-base width, heterophil to lymphocyte ratios (H/L ratios), brightness, body colour, behaviour and faecal corticosterone metabolite (FCM) levels for both males and females in the experimental treatments (provisioned or deprived situation). Our study animals did score very highly for several stress-indicating variables in the three weeks preceding the experiments — suggesting that they had experienced considerable stress during capture, transport and temporary housing in the pet store.
... Recently, there has been increased research focus on identifying behaviours that may be indicative of welfare state in reptiles [21][22][23][24][25][26][27][28][29][30]. However, there remains a dearth of primary studies exploring reptile behaviours, their relation to affective state, and how husbandry practices may modify expression of these behaviours. ...
... To date, the most common method of assessing the behavioural impacts of enrichment items or enclosure changes in reptiles has been ethogram use, to assist in recording changes in behaviour and to create an activity budget [21][22][23]26,33]. Additionally, there are no studies assessing the welfare implications of reduced space for tortoises and, conversely, the welfare improvements to be gained by increasing space for tortoises. ...
Article
Full-text available
Reptile behaviour and welfare are understudied in comparison with mammals. In this study, behavioural data on three species (Astrochelys radiata, Stigmochelys pardalis, Aldabrachelys gigantea) of tortoises were recorded before and after an environmental change which was anticipated to be positive in nature. The environmental changes differed for each population, but included a substantial increase in enclosure size, the addition of substrate material, and a change in handling procedure. A tortoise-specific ethogram was created to standardise data collection. Focal behaviour sampling was used to collect behavioural data. Changes in the duration of performance of co-occupant interaction and object interaction in the leopard (Stigmochelys pardalis) and Aldabra (Aldabrachelys gigantea) tortoises were observed following the environmental changes. The Shannon–Weiner diversity index did not yield a significant increase after the changes but had a numerical increase which was relatively greater for the leopard tortoise group, which had experienced the greatest environmental change. The leopard tortoises also demonstrated changes in a greater number of behaviours compared to the other species, and this was sustained over the study period. However, this included a behaviour indicative of negative affect: aggression. Whilst we are unable to conclude that welfare was improved by the management changes, there are suggestions that behavioural diversity increased, and some promotion of positive social behaviours occurred.
... Recently there has been increased research focus on identifying behaviours that may be indicative of welfare state in reptiles [21][22][23][24][25][26][27][28][29][30]. However, there remains a dearth of primary studies exploring reptile behaviours, their relation to affective state, and how husbandry practices may modify expression of these behaviours. ...
... To date the most common method of assessing the behavioural impacts of enrichment items or enclosure changes in reptiles has been ethogram use, to assist in recording changes in behaviour and to create an activity budget [21][22][23]26,33]. Additionally, there are no studies assessing the welfare implications of reduced space for tortoises, and conversely the welfare improvements to be gained by increasing space for tortoises. ...
Preprint
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Reptile behaviour and welfare are understudied in comparison with mammals. In this study, behavioural data on three species of tortoises were recorded before and after an environmental change which was anticipated to be positive in nature. The environmental changes differed for each population, but included a substantial increase in enclosure size, the addition of substrate material , and a change in handling procedure. A tortoise-specific ethogram was created to standardise data collection. Focal behaviour sampling was used to collect behavioural data. Changes in the duration of performance of co-occupant interaction and object interaction in the leopard (Stigmo-chelys pardalis) and Aldabra (Aldabrachelys gigantea) tortoises were observed following the environmental changes. The Shannon-Weiner's diversity index did not yield a significant increase after the changes but had a numerical increase which was relatively greater for the leopard tortoise group, which had experienced the greatest environmental change. The leopard tortoises also demonstrated changes in a greater number of behaviours compared to the other species, and this was sustained over the study period. However, this included a behaviour indicative of negative affect; aggression. Whilst we are unable to conclude that welfare was improved by the management changes, there are suggestions that behavioural diversity increased, and some promotion of positive social behaviours occurred.
... Within the scientific literature, a strong mammal-centric bias is prominent, with a scarcity of studies regarding reptile enrichment [12,14,[18][19][20]. This may be in part due to the long-held misconception that reptiles are stoic, highly adaptable, and tolerant to suboptimal conditions [21], as well as too neurologically simple to suffer [22,23] and thus not requiring enrichment. Where enrichment is utilized, structural or habitat design-based enrichment was the most employed provision for reptiles within U.S. collections, with an average of 86% of holders reporting this provision across all the reptile taxa [17]. ...
... Despite the attention bias, this is a developing field (Figure 1), and the studies that have been published in peer-reviewed journals support the notion that reptiles benefit from enrichment [21,[26][27][28][29][30][31] and that it is in fact essential [32]. Evidence for enrichment as a beneficial practice with reptiles is documented through an increase in natural behaviors and relaxed postures under structural enriched environments [33,34]. ...
Article
Full-text available
Enrichment has become a key aspect of captive husbandry practices as a means of improving animal welfare by increasing environmental stimuli. However, the enrichment methods that are most effective varies both between and within species, and thus evaluation underpins successful enrichment programs. Enrichment methods are typically based upon previously reported successes and those primarily with mammals, with one of the main goals of enrichment research being to facilitate predictions about which methods may be most effective for a particular species. Yet, despite growing evidence that enrichment is beneficial for reptiles, there is limited research on enrichment for Varanidae, a group of lizards known as monitor lizards. As a result, it can be difficult for keepers to implement effective enrichment programs as time is a large limiting factor. In order for appropriate and novel enrichment methods to be created, it is necessary to understand a species’ natural ecology, abilities, and how they perceive the world around them. This is more difficult for non-mammalian species as the human-centered lens can be a hinderance, and thus reptile enrichment research is slow and lagging behind that of higher vertebrates. This review discusses the physiological, cognitive, and behavioral abilities of Varanidae to suggest enrichment methods that may be most effective.
... Stressed organisms can experience a rise in corticosterone plasma levels that reduces the responsiveness of the immune system (Davis et al. 2008). However, while increased plasma corticosterone represents a quick response to stress, H/L ratio in ectotherms may take several hours to rise, hence it is not affected by capture stress (Case et al. 2005). The influence of impoverished environments as a factor contributing to increased H/L ratio in reptiles was demonstrated experimentally by Case et al. (2005) with eastern box turtles (Terrapene carolina), but its applicability to wild populations has hardly been accomplished. ...
... However, while increased plasma corticosterone represents a quick response to stress, H/L ratio in ectotherms may take several hours to rise, hence it is not affected by capture stress (Case et al. 2005). The influence of impoverished environments as a factor contributing to increased H/L ratio in reptiles was demonstrated experimentally by Case et al. (2005) with eastern box turtles (Terrapene carolina), but its applicability to wild populations has hardly been accomplished. Smyth et al. (2014) found no difference in H/L ratios of sleepy lizard (Tiliqua rugosa) populations from two agricultural sites with different levels of habitat fragmentation, whereas French et al. (2008) measured a decreased H/L ratio in the tree lizards (Urosaurus ornatus) from urban sites compared to those from non-urban sites. ...
Article
Full-text available
Despite the importance of reptiles in agroecosystems, little is known about the effects of agricultural intensification and pesticide use on these animals. We compared antioxidant and haematological biomarkers in the wild Italian wall lizards Podarcis siculus from three olive groves representing a gradient of management intensity. Lizards from the conventional grove showed induced antioxidant defences relative to those from the organic field. However, this induction did not avoid the occurrence of oxidative stress in males from intensively managed olive groves, who showed TBARS levels 58%–133% higher than males from the other sites. Haematological responses also suggested increased stress in females from the intensively managed olive groves, with a heterophil-to-lymphocyte ratio 5.3 to 14.8-fold higher than in the other sites. The observed stress responses of lizards along the studied gradient of agricultural management suggest their potential usefulness as non-destructive biomarkers to environmental stressors associated with agricultural intensification.
... Gross and Siegel (1983) established this measure for use in birds, demonstrating that administered exogenous corticosterone (the primary stress hormone in birds) led to correlative increases in plasma corticosterone and H:L ratio. Since then, the H:L ratio has been used in studies of acute and chronic stress in a variety of animals such as birds (e.g., Al-Murrani et al., 2002;Huff et al., 2005;Campo et al., 2005Campo et al., , 2007, reptiles (e.g., Case et al., 2005), and mammals (e.g., Hansen and Damgaard, 1993;Fisher et al., 1997), including people (e.g., Duffy et al., 2006). Among these studies, increased H:L ratios were associated with measures of primary, secondary, and tertiary stress indices, including increased plasma cortisol/corticosterone concentrations (Gross and Siegel, 1983;Hansen and Damgaard, 1993;Fisher et al., 1997), increased susceptibility to infectious disease (Al-Murrani et al., 2002;Huff et al., 2005), increased occurrence or duration of distress behaviors (Hansen and Damgaard, 1993;Case et al., 2005;Campo et al., 2005Campo et al., , 2007, reduced weight, and mortality (Huff et al., 2005;Duffy et al., 2006). ...
... Since then, the H:L ratio has been used in studies of acute and chronic stress in a variety of animals such as birds (e.g., Al-Murrani et al., 2002;Huff et al., 2005;Campo et al., 2005Campo et al., , 2007, reptiles (e.g., Case et al., 2005), and mammals (e.g., Hansen and Damgaard, 1993;Fisher et al., 1997), including people (e.g., Duffy et al., 2006). Among these studies, increased H:L ratios were associated with measures of primary, secondary, and tertiary stress indices, including increased plasma cortisol/corticosterone concentrations (Gross and Siegel, 1983;Hansen and Damgaard, 1993;Fisher et al., 1997), increased susceptibility to infectious disease (Al-Murrani et al., 2002;Huff et al., 2005), increased occurrence or duration of distress behaviors (Hansen and Damgaard, 1993;Case et al., 2005;Campo et al., 2005Campo et al., , 2007, reduced weight, and mortality (Huff et al., 2005;Duffy et al., 2006). This study demonstrates an association between increased H:L ratios and weight loss, reduced body condition, and increased variability in the occurrence of distress behaviors among animals in the loud tank group. ...
Thesis
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Loud noise in aquaria represents a cacophonous environment for captive fishes. I tested the effects of loud noise on acoustic communication, feeding behavior, courtship behavior, and the stress response of the lined seahorse, Hippocampus erectus. Total Root Mean Square (RMS) power of ambient noise to which seahorses are exposed in captivity varies widely but averages 126.1 +/- 0.8 deciBels with reference to one micropascal (dB re: 1 μPa) at the middle of the water column and 133.7 +/- 1.1 dB at the tank bottom, whereas ambient noise in the wild averages 119.6 +/- 3.5 dB. Hearing sensitivity of H. erectus, measured from auditory evoked potentials, demonstrated maximum spectrum-level sensitivities of 105.0 +/- 1.5 dB and 3.5 X 10-3 + 7.6 X 10-4 m/s2 at 200 Hz; which is characteristic of hearing generalists. H. erectus produces acoustic clicks with mean peak spectrum-level amplitudes of 94.3 +/- 0.9 dB at 232 +/- 16 Hz and 1.5 X 10-3 +/- 1.9 X 10-4 m/s2 at 265 +/- 22 Hz. Frequency matching of clicks to best hearing sensitivity, and estimates of audition of broadband signals suggest that seahorses may hear conspecific clicks, especially in terms of particle motion. Behavioral investigations revealed that clicking did not improve prey capture proficiency. However, animals clicked more often as time progressed in a courtship sequence, and mates performed more courtship behaviors with control animals than with muted animals, lending additional evidence to the role of clicking as an acoustic signal during courtship. Despite loud noise and the role of clicking in communication, masking of the acoustic signal was not demonstrated. Seahorses exposed to loud noise in aquaria for one month demonstrated physiological, chronic stress responses: reduced weight and body condition, and increased heterophil to lymphocyte ratio. Behavioral alterations were characterized by greater mean and variance of activity among animals housed in loud tanks in the first week, followed by habituation. By week four, animals in loud tanks demonstrated variable performance of clicking and piping, putative distress behaviors. Despite the physiological stress response, animals in loud tanks did not reduce feeding response or courtship behavior, suggesting allostasis.
... In captivity, turtles actively selected enclosures enriched with vegetation, water and hiding areas (Tetzlaff, Sperry & DeGregorio, 2018). Enrichment stimulated exploratory and play behaviors (Burghardt, Ward & Rosscoe, 1996) and decreased escape behavior (Case, Lewbart & Doerr, 2005). The effectiveness of new enrichments is usually assessed based on frequency of use and behavioral changes, with decreases expected in stress indicators (Bishop, Hosey & Plowman, 2013). ...
... Frequent escape behavior is associated with stress or low welfare caused by the unavoidable limitations in space and structural complexity (Burghardt, 2013) and may cause abrasions or wounds to the head and neck, seen in captive but not in wild reptiles (Rose, Nash & Riley, 2017). Studies on other species of freshwater turtles showed that object and structural enrichment reduced undesirable behaviors and stimulated behaviors associated with good welfare by providing behavioral choices (Burghardt et al., 1996, Case et al., 2005. ...
Article
The effect of environmental enrichment on the behavior and welfare in captivity of reptiles and of freshwater turtles in particular, which are popular aquarium and pet species, is very little studied compared to other taxa. We carried out a small scale case‐study on the effect of colored object enrichment, with and without fish scent, on the behavior of a group of 15 cooters (Pseudemys sp.) and sliders (Trachemys scripta ssp.) on display at a public aquarium. The new enrichment aimed to reduce the escape behavior (interaction with transparent boundaries) and increase exploration and random swimming. We used simultaneous recording of behavior at whole group level and for focal individually‐marked turtles. The escape behavior decreased on days with new enrichment before feeding at whole group level and for the focal turtles overall, in spite of the relatively low interest in the colored objects. Fish‐scented objects attracted significantly more interest. Random swimming, enrichment focus, aggression and submission increased significantly, and basking decreased significantly at whole group level before feeding, with smaller differences after feeding. There were large differences between individual turtles with respect to activity budgets and changes in behavior on days with new enrichment, with both increases and decreases seen in escape behavior, aggression, and levels of activity. Our outcomes suggested that introducing new colored objects with food scent may be beneficial for reducing escape behavior in captive freshwater turtles. However, careful monitoring of effects at individual level and much larger scale investigations, including postenrichment periods, are needed. Research Highlights • The presence of colored objects reduced the escape behavior of freshwater turtles, mainly before feeding. • There was more interest when the new objects were fish‐scented. • There were differences in behavior and response to enrichment at individual level.
... 25 As more attention is directed toward the nutritional requirements of these reptilian wildlife species, increasing differences are being observed between what these species eat in their wild habitats and what they are fed when they are housed in managed care facilities (MC) such as aquariums, rehabilitation facilities, and zoos. 6,9,23 Previous literature has indicated inherent trends between wild animals and those kept in MC across many taxa, including reptiles. [10][11][12]14,21,22 In particular, MC species previously examined tend to have lower polyunsaturated fatty acids. ...
... 17,23 Similarly, the diets of EBT in MC are quite varied but are often reported as a mixture of different fruits and vegetables, supplemented with canned cat or dog food, and prey items (e.g., mealworms, night crawlers, shrimp, earthworms). 6,9,18 It is important that MC facilities carefully consider what is accessible and appropriate when formulating diets for individual chelonian species. To create a balanced diet, it is helpful to first determine the circulating nutrient concentrations for the species of interest. ...
Article
The housing of wild animals in managed care facilities requires attention to all aspects of husbandry. Diets of wild animals often differ in composition, consistency, and quantity when compared with those in managed care settings including zoos, rehabilitation facilities, and aquaria. It was hypothesized that dietary differences from wild versus managed care would be reflected in data of circulating fatty acids based on previous studies. The current study examined the effect of species and environment on fatty acid concentrations in two omnivorous species of chelonians: Eastern box turtles, Terrapene carolina carolina, and common snapping turtles, Chelydra serpentina, located in the wild and managed care. Whole blood was collected and placed on spot cards for analysis of 26 fatty acids in a total lipid fatty acid profile. The present research indicated that Eastern box turtles have significantly (P < 0.05) higher percentages of linoleic acid (18:2n6), eicosadienoic acid (20:2n6), and mead acid (20:3n9). Common snapping turtles have significantly (P < 0.05) higher percentages of myristic acid (14:0), dihomo-γ-linolenic acid (20:3n6), erucic acid (22:1n9), and n-6 docosapentaenoic acid (22:5n6). Environmental effects also were noted; wild turtles had higher percentages of α-linolenic acid (18:3n3), arachidic acid (20:0), eicosadienoic acid (20:2n6), and eicosatrienoic acid (20:3n3) (P < 0.05), whereas n-6 docosapentaenoic acid (22:5n6) was higher for the managed care group. Eicosadienoic acid (20:2n6), behenic acid; 22:0), adrenic acid (22:4n6), n-6 docosapentaenoic acid (22:5n6), and nervonic acid (24:1) were significantly different (P < 0.05) in species-environment interactions without any noted species or environment patterns. Fatty acids are useful for many important biological functions including proper immune system regulation, and therefore, the present research provides medically relevant data for reptile diagnostics. This research may help further improve diets of all chelonians kept in managed care, regardless of species.
... One could also argue husbandry attributes associated with herpetocultural practice should then be driven by observations and investigations in nature, where the species in question occurs naturally and evolved. Approaches similar to Case [15] and Tetzlaff [16], who used an evidence based approach comparing minimalistic with naturalistic care, and documented increased stress in Terrapene carolina (Eastern Box turtles) maintained in simple versus complex conditions, help support one approach over another. Regarding behavioral enrichment, reptiles time and time again have been shown in scientific studies to respond to complex captive environments [11,[15][16][17], complex thermal repetoires [11,18,19], and complex diets [11,18] in ways that decrease stress and demonstrate choice. ...
... Approaches similar to Case [15] and Tetzlaff [16], who used an evidence based approach comparing minimalistic with naturalistic care, and documented increased stress in Terrapene carolina (Eastern Box turtles) maintained in simple versus complex conditions, help support one approach over another. Regarding behavioral enrichment, reptiles time and time again have been shown in scientific studies to respond to complex captive environments [11,[15][16][17], complex thermal repetoires [11,18,19], and complex diets [11,18] in ways that decrease stress and demonstrate choice. Evidence based husbandry has become a favorable herpetocultural approach [11,12,14], specifically to those who hope to avoid folklore husbandry practices [11,14]. ...
Article
Full-text available
Herpetocultural practices are based on norms driven by economy of space and time for keepers, with little scientific inference backing their practice. In recent years, a subset of herpetoculturalists have promoted evidence-based husbandry that relies on science and experimental design to generate husbandry practice. A theoretical framework and protocol are proposed herein that enables any individual who has access to the internet the ability to use various outlets of natural history information (scientific literature databases, social media sources, and weather websites) and previously published husbandry reports as evidence to drive the creation of novel herpetocultural practice. A case study is provided which compares readily available information on the care of Hydrodynastes gigas (false water cobra), such as online care sheets for the species, with the proposed evidence based herpetocultural protocol founded on natural history information and published care and captive breeding reports. Results were assessed for protocol efficacy and determined that the natural history informed evidence-based approach increased animal welfare and generated new information specific to the natural history of H. gigas.
... Heterophils (neutrophils in mammals and amphibians) are part of the innate immune system, while lymphocytes are part of the acquired immune system. High ratios of heterophils to lymphocytes in blood samples are considered an indication of high glucocorticoid and stress values in all vertebrate taxa (review in Davis and Maerz, 2008), including reptiles (Saad and El Ridi, 1988;Morici et al., 1997;Lance and Elsey, 1999;Case et al., 2005;Chen et al., 2007;Borgmans et al., 2018Borgmans et al., , 2019. ...
... Only our H/L ratio results pointed towards a potential higher cost of dominance for dominant males compared to subordinate males as we found that dominant males had a significantly higher H/L ratio at the end of the trial period. H/L ratio has been shown to be positively correlated to levels of glucocorticoids (Saad and El Ridi, 1988;Morici et al., 1997;Lance and Elsey, 1999;Chen et al., 2007;Case et al., 2005;Davis et Maerz, 2008;Borgmans et al., 2018Borgmans et al., , 2019 and thus the higher H/L ratio for the dominant males could indicate a higher level of stress. We also found that the H/L ratios for both dominant and subordinate males were lowest at one week after group formation. ...
Article
Male Anolis carolinensis lizards will fight and form social dominance hierarchies when placed in habitats with limited resources. Dominance may procure benefits such as priority access to food, shelter or partners, but may also come with costs, such as a higher risk of injuries due to aggressive interaction, a higher risk of predation or a higher energetic cost, all of which may lead to an increase in stress. While most research looks at dominance by using dyadic interactions, in our study we investigated the effect of dominance in a multiple male group of A. carolinensis lizards. Our results showed that dominant males in a multiple male group had priority access to prey and potential sexual partners but may run a higher risk of predation. We could not confirm that dominant males in a multiple male group had a higher risk of injuries from aggressive interactions or a higher energetic cost by being dominant. Overall our results seem to indicate that dominant male A. carolinensis lizards in a multiple male group obtain clear benefits and that they outweigh the disadvantages.
... A few studies have shown initial research into reptile welfare (e.g. Kreger and Mench 1993 (ball python -Python regius, Blue-tongued skink -Tiliqua scincoides), Schuett et al., 2004 (rattlesnakes -Crotalus atrox) Case et al., 2005 (box turtles -Terrapene carolina carolina), Kalliokoski et al., 2012 (green iguanas -Iguana iguana)) and there is literature that highlights the importance of this subject area (Burghardt, 2013;Hernandez-Divers, 2001;Stanford, 2013;Warwick et al., 2013). Experimental studies have revealed an effect of housing environment on behaviour and immune response, as well as environmental prefer-ences (Case et al., 2005) and impact of handling on behavioural and physiological measures (e.g. ...
... Kreger and Mench 1993 (ball python -Python regius, Blue-tongued skink -Tiliqua scincoides), Schuett et al., 2004 (rattlesnakes -Crotalus atrox) Case et al., 2005 (box turtles -Terrapene carolina carolina), Kalliokoski et al., 2012 (green iguanas -Iguana iguana)) and there is literature that highlights the importance of this subject area (Burghardt, 2013;Hernandez-Divers, 2001;Stanford, 2013;Warwick et al., 2013). Experimental studies have revealed an effect of housing environment on behaviour and immune response, as well as environmental prefer-ences (Case et al., 2005) and impact of handling on behavioural and physiological measures (e.g. Schuett et al., 2004;Langkilde and Shine, 2006;Kalliokoski et al., 2012; although see Kreger and Mench 1993). ...
Article
Whilst a great deal of research has been focused on identifying ways to assess the welfare of captive mammals and birds, there is comparatively little knowledge on how reptilian species are affected by captivity, and the ways in which their welfare can be accurately assessed. The present study investigated response to novelty − a commonly used approach to assess anxiety-like behaviour and hence welfare in non-human animals − in two species of reptile with the aim of determining whether this approach could be successfully translated from use in mammalian and avian species for use in reptiles, and whether we could also identify reptile-specific and/or species-specific behaviours. Eight red-footed tortoises (Chelonoidis carbonaria) and seventeen bearded dragons (Pogona vitticeps) were observed individually in both familiar and novel environments for 10 minute time periods, and their behaviour recorded. Tortoises were found to begin locomotion sooner when placed in a familiar environment than when placed in a novel environment, they extended their necks further in a familiar environment and their neck length increased over time in both familiar and novel environments, suggesting an overall anxiety-like response to novelty as seen in non-reptilian species. In contrast, whilst bearded dragons exhibited significantly more tongue-touches in a novel, compared to a familiar, environment, they showed no difference between familiar and novel environments in their latency to move. This result suggests that, whilst the dragons appeared to discriminate between the two environments, this discrimination was not necessarily accompanied by an anxiety-like response. This study has confirmed the translatability of response to novelty as an approach to assess anxiety-like behaviour in one species of reptile, as well as identifying species-specific behaviours that have the potential to be used in future studies when assessing the welfare of reptiles in response to captive environments, but our results also highlight the need to be aware of species differences within a class as diverse as reptilia.
... A study more focused on overall living arrangements involved preference of box turtles for a barren or 'enriched' environment containing mulch substrate, shredded paper, and a hide box (Case et al., 2005). Turtles were 38 adults, either wild-caught or long-term captives. ...
... While overall weight change did not differ based on housing treatment, the wild-caught animals gained more weight than the long-term captives. In terms of behavior, filmed half way through the 1-month period on both feeding and non feeding days for 6 h each, barren housed animals spent more time trying to escape and less time resting and engaging in non-escape movements (Case et al., 2005). ...
Article
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Reptiles and amphibians have been neglected in research on cognition, emotions, sociality, need for enriched and stimulating environments, and other topics that have been greatly emphasized in work on mammals and birds. This is also evident in the historic lack of enriching captive environments to reduce boredom and encourage natural behavior and psychological well-being. This paper provides those responsible for the care of reptiles and amphibians a brief overview of concepts, methods, and sample findings on behavioral complexity and the role of controlled deprivation in captive herpetological collections. Most work has been done on reptiles, however, and so they are emphasized. Amphibians and reptiles, though not admitting of easy anthropomorphism, do show many traits common in birds and mammals including sophisticated communication, problem solving, parental care, play, and complex sociality. Zoos and aquariums are important resources to study many aspects of these often exotic, rare, and fascinating animals, and rich research opportunities await those willing to study them and apply the wide range of methods and technology now available. (c) 2013 Elsevier B.V. All rights reserved.
... Captive conditions alter and reverse wild patterns of antipredator behavior of reptiles (Hennig and Dunlap 1978;Hennig 1979, both in Anolis carolinensis) and strike-induced chemosensory searching ("scent-trailing;" Marmie et al. 1990 in Crotalus enyo). The provision of a complex environment in captivity improves cognitive behavior (Almli and Burghardt 2006 in Elaphe obsoleta) and reduces stress hormone levels and stress-related escape behavior (Case et al. 2005 in Terrapene carolina). Blue-tongue skinks (Tiliqua scincoides) show alterations to activity patterns and exhibit reduced weight gain and obesity when provided with larger enclosures and the opportunity to hunt for insect prey (Phillips et al. 2011). ...
... Blue-tongue skinks (Tiliqua scincoides) show alterations to activity patterns and exhibit reduced weight gain and obesity when provided with larger enclosures and the opportunity to hunt for insect prey (Phillips et al. 2011). Complex environments are also actively sought out by reptiles (Case et al. 2005 in T. carolina), while individuals of cryptic species may also seek out and prefer appropriately colored refugia (Garrett and Smith 1994 in Morelia viridis), as do wild amphibians (Pacific treefrogs, Pseudacris regilla; Morey 1990). Furthermore, although sometimes controversial (Burghardt 2005), some reptiles have been reported to engage in divertive, play behavior when provided with novel objects (Burghardt et al. 1966 andBurghardt 2005 in Trionyx triunguis ;Hill 1946, Murphy 2002and Burghardt 2005 in Varanus komodoensis; Lazell and Spitzer 1977 in Alligator mississippiensis). ...
Article
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Enrichment, broadly the provision of stimuli to improve the welfare of captive animals, is known to be important in husbandry practice and in the success of ex situ conservation and reintroduction programs. Practical evidence of the importance of enrichment exists for a number of taxa, yet amphibians are poorly represented. There is no reason to assume a priori that amphibians would not benefit from enrichment and, given their increasing prominence in captive programs, their requirements in captivity beyond basic husbandry should be the focus of more intense study. We review the existing body of research on enrichment for amphibians, as well as that for fish and reptiles, which may be regarded as behaviorally and neurologically broadly similar to amphibians. We also briefly discuss mechanisms by which enrichment might affect amphibian fitness and, therefore, reintroduction success. Our review supports the contention that there may be important consequences of enrichment for both captive welfare and ex situ conservation success in amphibians and that amphibian enrichment effects may be highly variable taxonomically. In the face of increasing numbers of captive amphibian species and the importance of ex situ populations in ensuring their species level persistence, enrichment for amphibians may be an increasingly important research area.
... In a recent study of box turtles ( Terrapene c. carolina ), H : L ratios were used to determine how individuals responded to captivity in low-vs. highquality housing conditions (Case, Lewbart & Doerr 2005). In this case, individuals housed in high-quality conditions (i.e. with mulched floors, shredded paper and a hide box) had lower H : L ratios than those housed in low-quality conditions (i.e. ...
... Therefore they should be treated more as a starting place for future work than a set of absolutes. Furthermore, reference values can vary among investigators because of differences in handling procedures before sampling, or captive housing conditions (see Case et al. 2005), leading to cases where two or more groups of investigators report vastly different 'reference' haematological parameters for the same species. In one such case, Cathers et al. (1997) reported leukocyte profiles of American bullfrogs (Rana catesbeiana) with lymphocyte and neutrophil proportions of 63% and 22%, respectively. ...
Article
© 2008 The Authors. Journal compilation © 2008 British Ecological Society ... The use of leukocyte profiles to measure stress ... AK Davis1*, DL Maney2 and JC Maerz1 ... 1D.B. Warnell School of Forestry and Natural Resources, The University of Georgia, Athens, GA 30602, USA; ...
... Assessment of leukocyte ratios has also been considered a promising method for the assessment of physiological stress due to advantages such as a slower response time than that of glucocorticoids, the need for only a very small amount of blood to make a blood smear, and little monetary expense (Davis, 2005). However, recent studies have suggested that the relationship between CORT and leukocyte ratios is not always straightforward, and may vary across taxa (Vleck et al., 2000;Case et al., 2005;Müller et al., 2011;Seddon and Klukowski, 2012). In general, little is yet known regarding (1) natural variation in the relationship between CORT and leukocyte ratios, particularly in non-avian species, (2) repeatability of both CORT and leukocyte ratios within individuals, (3) how quickly leukocyte ratios change in response to capture stress, (4) how leukocyte ratios covary with ecological and demographic factors in the wild and (5) how long-term captivity affects both CORT and leukocyte ratios. ...
... We found that CORT and H:L ratios were not correlated within individual garter snakes, either in the wild or in captivity (Fig. 1, Table 1). This finding is consistent with recent studies in birds and other reptiles that suggest that a correlation between CORT and H:L ratios may be absent or weak, and these indices represent at least partially independent responses to stress or other factors (Vleck et al, 2000;Case et al., 2005;Müller et al., 2011;Seddon and Klukowski, 2012). Interestingly, however, we also found that CORT and H:L ratios do exhibit some of the same general trends with regard to both ecotype and temporal changes in captivity. ...
... Gross and Siegel (1983) established this measure for use in birds, demonstrating that administered exogenous corticosterone (the primary stress hormone in birds) led to correlative increases in plasma corticosterone and H:L ratio. Since then, the H:L ratio has been used in studies of acute and chronic stress in a variety of animals such as birds (e.g., Al-Murrani et al., 2002;Huff et al., 2005;Campo et al., 2005Campo et al., , 2007, reptiles (e.g., Case et al., 2005), and mammals (e.g., Hansen and Damgaard, 1993;Fisher et al., 1997), including people (e.g., Duffy et al., 2006). Among these studies, increased H:L ratios were associated with measures of primary, secondary, and tertiary stress indices, including increased plasma cortisol/corticosterone concentrations (Gross and Siegel, 1983;Hansen and Damgaard, 1993;Fisher et al., 1997), increased susceptibility to infectious disease (Al-Murrani et al., 2002;Huff et al., 2005), increased occurrence or duration of distress behaviors (Hansen and Damgaard, 1993;Case et al., 2005;Campo et al., 2005Campo et al., , 2007, reduced weight, and mortality (Huff et al., 2005;Duffy et al., 2006). ...
... Since then, the H:L ratio has been used in studies of acute and chronic stress in a variety of animals such as birds (e.g., Al-Murrani et al., 2002;Huff et al., 2005;Campo et al., 2005Campo et al., , 2007, reptiles (e.g., Case et al., 2005), and mammals (e.g., Hansen and Damgaard, 1993;Fisher et al., 1997), including people (e.g., Duffy et al., 2006). Among these studies, increased H:L ratios were associated with measures of primary, secondary, and tertiary stress indices, including increased plasma cortisol/corticosterone concentrations (Gross and Siegel, 1983;Hansen and Damgaard, 1993;Fisher et al., 1997), increased susceptibility to infectious disease (Al-Murrani et al., 2002;Huff et al., 2005), increased occurrence or duration of distress behaviors (Hansen and Damgaard, 1993;Case et al., 2005;Campo et al., 2005Campo et al., , 2007, reduced weight, and mortality (Huff et al., 2005;Duffy et al., 2006). This study demonstrates an association between increased H:L ratios and weight loss, reduced body condition, and increased variability in the occurrence of distress behaviors among animals in the loud tank group. ...
Article
Loud noise in aquaria represents a cacophonous environment for captive fishes. I tested the effects of loud noise on acoustic communication, feeding behavior, courtship behavior, and the stress response of the lined seahorse, Hippocampus erectus. Total Root Mean Square (RMS) power of ambient noise to which seahorses are exposed in captivity varies widely but averages 126.1 +/- 0.8 deciBels with reference to one micropascal (dB re: 1 muPa) at the middle of the water column and 133.7 +/- 1.1 dB at the tank bottom, whereas ambient noise in the wild averages 119.6 +/- 3.5 dB. Hearing sensitivity of H. erectus, measured from auditory evoked potentials, demonstrated maximum spectrum-level sensitivities of 105.0 +/- 1.5 dB and 3.5 x 10-3 + 7.6 x 10-4 m/s2 at 200 Hz; which is characteristic of hearing generalists. H. erectus produces acoustic clicks with mean peak spectrum-level amplitudes of 94.3 +/- 0.9 dB at 232 +/- 16 Hz and 1.5 x 10 -3 +/- 1.9 x 10-4 m/s2 at 265 +/- 22 Hz. Frequency matching of clicks to best hearing sensitivity, and estimates of audition of broadband signals suggest that seahorses may hear conspecific clicks, especially in terms of particle motion. Behavioral investigations revealed that clicking did not improve prey capture proficiency. However, animals clicked more often as time progressed in a courtship sequence, and mates performed more courtship behaviors with control animals than with muted animals, lending additional evidence to the role of clicking as an acoustic signal during courtship. Despite loud noise and the role of clicking in communication, masking of the acoustic signal was not demonstrated. Seahorses exposed to loud noise in aquaria for one month demonstrated physiological, chronic stress responses: reduced weight and body condition, and increased heterophil to lymphocyte ratio. Behavioral alterations were characterized by greater mean and variance of activity among animals housed in loud tanks in the first week, followed by habituation. By week four, animals in loud tanks demonstrated variable performance of clicking and piping, putative distress behaviors. Despite the physiological stress response, animals in loud tanks did not reduce feeding response or courtship behavior, suggesting allostasis.
... The ratio of these cells has been increasingly used among ornithologists to document the effects of various stressful conditions including transport stress (Groombridge et al., 2004) and reproductive output (Moreno et al., 2002a). Research with Eastern Box Turtles (Terrapene carolina carolina) also used this approach to document stress (Case et al., 2005). Furthermore, a series of lab experiments beginning in the 1960s showed that amphibians appear to have the same response, in multiple stress-inducing conditions such as limb amputation (Bennett, 1986), temperature extremes (Bennett and Daigle, 1983), osmotic stress (Bennett and Johnson, 1973), photoperiod stress (Bennett and Reap, 1978), and direct administration of hydrocortisone (Bennett and Alspaugh, 1964;Bennett and Newell, 1965;Bennett and Harbottle, 1968;Bennett et al., 1972). ...
... Also in birds, individuals with high ratios have been shown to be more susceptible to diseases than those with low ratios (Al-Murrani et al., 2002). Finally, and perhaps more related to captive husbandry, the quality of the housing environment has been shown to be an important predictor of hematological stress parameters in Box Turtles (Terrapene carolina) in captivity (Case et al., 2005). These studies, as well as the present one, all highlight the importance of knowing the conditions under which animals become stressed in research projects, and more generally, the influence of stress on immune systems and life history patterns of all vertebrates, including herpetofauna. ...
Article
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Measuring stress in animals is an important component of many research studies, and it has traditionally been performed via sampling levels of corticosterone in plasma. A secondary, ''hematological'' approach used most commonly by researchers of birds, mammals, and other taxa involves evaluating leukocyte profiles from blood smears. Such research has shown that leukocytes have a characteristic response to stress, although in amphibians this phenomenon is not as well studied. In general, stress can induce a rise in the ratio of neutrophils to lymphocytes. We evaluated the hematological response of paedomorphic Mole Salamanders (Ambystoma talpoideum) to captivity stress, specifically focusing on this parameter, but also examining other white blood cell types. Individuals captured in the wild and held in captivity for ten days before sampling had significantly more neutrophils, fewer lymphocytes, and higher ratios of neutrophils to lymphocytes than those captured from the same locations and sampled within one hour. Captive individuals also had significantly higher numbers of eosinophils. These results are consistent with hematological research in birds and other taxa and highlight the utility of this approach for measuring stress in amphibians.
... Novel object enrichment (Burghardt et al. 1996;Therrien et al. 2007;Mehrkham and Dorey, 2014;Bashaw et al. 2016) and structural enrichment (Case et al. 2005;Rose et al. 2014;Tetzlaff et al. 2018) reduced repetitive behaviours and increased levels of activity in turtles. Coloured object enrichment reduced the escape behaviour and increased the level of activity of a group of captive river cooters Pseudemys sp. and pond sliders Trachemys scripta before feeding, but there were differences in the direction of change in escape behaviour at individual level (Bannister et al. 2021), indicating that it is important to study the impact of any new enrichment not only at group level, but also on each individual concerned. ...
Article
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Recent studies showed that freshwater turtles display inter-individual differences in various behavioural traits, which may influence their health and welfare in captivity due to differences in response to husbandry and enrichment strategies and in ability to cope with the limitations of the captive environment. This study investigated a possible correlation between individual level of escape behaviour under standard enrichment conditions and level of interest in coloured objects in a group of cooters Pseudemys sp. and sliders Trachemys scripta ssp. on display at a public aquarium. Interest in different colours, colour preference and individual differences in behavioural changes in the presence of the new enrichment were also studied. Turtles categorised as 'high' and 'moderate escape behaviour' (17-34% of behavioural budget) showed more interest in coloured objects and tended to display less escape behaviour in their presence, while turtles categorised as 'low escape behaviour' (<10% of behavioural budget) were less interested in coloured objects and tended to display more escape behaviour in their presence. Overall, there was more interest in yellow than in red, white or green objects, with more contacts with coloured objects before feeding and at the start of each observation period and a preference for yellow against red objects. The individual differences in behavioural changes in the presence of the new enrichment suggested that more studies into colour preference and response to novelty in turtles would be beneficial to ensure that no individuals are unduly stressed by new enrichments.
... It has been suggested that the most reliable means of visualising stress includes behavioural assays in order to supplement lab-based hormonal measurements (Otovic & Hutchinson 2015). The major glucocorticoid or stress hormone in turtles (like all herpetofauna) is corticosterone (Case et al. 2005). Non-invasive methods of measuring the stress hormone corticosterone, including the use of faecal corticosterone metabolites (FCM), are becoming more prominent in the assessment of stress (Dehnhard et al. 2001;Weingrill et al. 2004;Franceschini et al. 2008;Narayan et al. 2012;Shepherdson et al. 2013;Watson et al. 2013;Narayan et al. 2018). ...
... Nile soft-shelled turtles (Trionyx triunguis) provided with environmental enrichment show a large decrease in self-mutilation behaviour, high levels of interaction with the enrichment devices, and increased overall activity (Burghardt et al. 1996). Physiological indicators, including blood counts, faecal corticosterone and body weights, have been used to show that box turtles (Terrapene carolina carolina) prefer enriched housing environments over unenriched ones (Case et al. 2005). Even captive-reared box turtles innately preferred naturalistic habitat, and such innate behaviour would hopefully aid successful reintroduction of captive-reared box turtles to the wild (Tetzlaff et al. 2018). ...
Article
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Wild sea turtles that are admitted to turtle hospitals and rehabilitation centers suffering from illnesses and injuries may be held for extended periods of months to years, until they are recovered and ready for release back to the wild. During this time, natural behaviors may be limited, potentially adversely affecting the long-term rehabilitation success, however, little research has been carried out on the behavior of hospitalized sea turtles. Here we report that environmental enrichment can be an effective means of encouraging natural behaviors in turtles in hospital/rehabilitation and aquarium settings, but find that enrichment should be monitored and tailored to individual turtles to achieve positive results.
... These ornaments also convey information about immunological condition. In two species (Case et al., 2005;Chen et al., 2007;Davis et al., 2008;Murray et al., 2015). A plausible explanation for these observed negative associations between heterophils or H:L ratio and size, saturation, and conspicuousness of particular color components is that mounting an innate immune response by means of abundant heterophils entails physiological costs that negatively affect the production of color (Ibáñez et al., 2014;Mészáros et al., 2019). ...
Article
Colorful ornaments are important visual signals for animal communication that can provide critical information about the quality of the signaler. In this study, we focused on different color characteristics of the abdominal patches of males of six lizard species from the genus Sceloporus. We addressed three main objectives. First, we examined if size, brightness, saturation, and conspicuousness of these ornaments are indicative of body size, condition, immune function, or levels of testosterone and corticosterone. Second, we evaluated if the distinct components of these abdominal patches (blue or green patches and black stripes) transmit similar information about the signaler, which would support the redundant signal hypothesis, or if these components are related to different phenotypic traits, which would support the multiple message hypothesis. Third, we compared the phenotypic correlates of these ornaments among our six species to understand the degree of conservatism in the signaling patterns or to find species-specific signals. Using data collected from males in natural conditions and a multi-model inference framework, we found that in most species the area of the patches and the brightness of the blue component are positively related to body size. Thus, these color characteristics are presumably indicative of the physical strength and competitive ability of males and these shared signals were likely inherited from a common ancestor. In half of the species, males in good body condition also exhibit relatively larger blue and black areas, suggesting that the expression of these ornaments is condition-dependent. Abdominal patches also provide information about immunocompetence of the males as indicated by different correlations between certain color characteristics and ectoparasite load, counts of heterophils, and the heterophil:lymphocyte ratio. Our findings reveal that area and brightness of the abdominal patches signal the size and body condition of males, whereas blue saturation and conspicuousness with respect to the surrounding substrate are indicative of immune condition, thus supporting the multiple message hypothesis. However, some of these correlations were not shared by all species and, hence, point to intriguing species-specific signals.
... Preference tests of habitat complexity indicated eastern box turtles preferred an enriched environment with cypress mulch substrate, shredded paper, and a box for hiding over only a flat newspaper substrate (Case et al., 2005). Zebrafish and checker barbs preferred a structured over a simple compartment, and the latter used particular areas of the structured compartment more (Kistler et al., 2011). ...
Article
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Can the main methods of social welfare analysis be extended to cover multiple species? Following a non-anthropocentric approach, we examine the pros and cons of various objective and subjective methods of well-being comparisons across species. We argue against normalizing by specific capacities but in favor of taking account of individual preferences and specializations. While many conceptual and practical difficulties remain, it appears possible to develop methods for the assessment of collective well-being of multi-species communities and ecosystems.
... Furthermore, there is no evidence suggesting that snakes benefit from smaller, less enriched enclosures or that they are unharmed by such conditions. Although further work is welcome, recent studies (e.g., [8,26,31,35,37,38,41,143]) strongly cross-corroborate other works to confirm that snakes naturally occupy large home ranges, utilize available space, prefer more spacious and diverse habitats, and commonly adopt stretch-out postures, and that such postures are important for the avoidance of harm and achievement of quiescence and comfort. ...
Article
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Snakes are sentient animals and should be subject to the accepted general welfare principles of other species. However, they are also the only vertebrates commonly housed in conditions that prevent them from adopting rectilinear behavior (ability to fully stretch out). To assess the evidence bases for historical and current guidance on snake spatial considerations, we conducted a literature search and review regarding recommendations consistent with or specifying ≥1 × and <1 × snake length enclosure size. We identified 65 publications referring to snake enclosure sizes, which were separated into three categories:
... Furthermore, there is no evidence suggesting that snakes benefit from smaller, less enriched enclosures or that they are unharmed by such conditions. Although further work is welcome, recent studies (e.g., [8,26,31,35,37,38,41,143]) strongly cross-corroborate other works to confirm that snakes naturally occupy large home ranges, utilize available space, prefer more spacious and diverse habitats, and commonly adopt stretch-out postures, and that such postures are important for the avoidance of harm and achievement of quiescence and comfort. ...
Article
Full-text available
Snakes are sentient animals and should be subject to the accepted general welfare principles of other species. However, they are also the only vertebrates commonly housed in conditions that prevent them from adopting rectilinear behavior (ability to fully stretch out). To assess the evidence bases for historical and current guidance on snake spatial considerations, we conducted a literature search and review regarding recommendations consistent with or specifying ≥1 × and <1 × snake length enclosure size. We identified 65 publications referring to snake enclosure sizes, which were separated into three categories: peer-reviewed literature (article or chapter appearing in a peer-reviewed journal or book, n = 31), grey literature (government or other report or scientific letter, n = 18), and opaque literature (non-scientifically indexed reports, care sheets, articles, husbandry books, website or other information for which originating source is not based on scientific evidence or where scientific evidence was not provided, n = 16). We found that recommendations suggesting enclosure sizes shorter than the snakes were based entirely on decades-old ‘rule of thumb’ practices that were unsupported by scientific evidence. In contrast, recommendations suggesting enclosure sizes that allowed snakes to fully stretch utilized scientific evidence and considerations of animal welfare. Providing snakes with enclosures that enable them to fully stretch does not suggest that so doing allows adequate space for all necessary normal and important considerations. However, such enclosures are vital to allow for a limited number of essential welfare-associated behaviors, of which rectilinear posturing is one, making them absolute minimum facilities even for short-term housing.
... Single hatchlings in a tank devoid of any environmental enrichment may be too exposed to feel safe. Future studies including environmental enrichment on isolated hatchlings could be conducted to gain an improved understanding of the physiological and behavioral responses to isolation on loggerhead hatchlings, as suggested by Case et al. (2005). ...
Article
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Frequently, stranded sea turtles require rehabilitation under controlled conditions. Currently, few publications have described the conditions under which rehabilitation is to take place, particularly with respect to the hatchling life stage. To address this paucity of data, we conducted some experiments to assist rehabilitating facilities assess their handling of hatchlings. While in captivity, hatchlings are routinely handled, for example, for data collection and cleaning. Standardization of handling and housing protocols is necessary to define the most adequate rearing conditions to maintain hatchling welfare. Accordingly, the aim of this study was to assess plasma circulating corticosterone (Cort) concentration and growth, as a biomarker for the stress of hatchling loggerhead sea turtles (Caretta caretta) under controlled conditions. We performed two experiments to analyze handling frequency and stocking density. In both, Cort was measured and correlated with variations in animal weight and length. In handling experiments, Cort exhibited no significant increase when hatchlings were handled once a week, whereas Cort was significantly elevated when hatchlings were handled once every 2 weeks, suggesting that hatchlings have the ability to acclimate to frequent handling. However, hatchlings exhibited similar growth and mortality, regardless of handling regime. In stocking density experiments, hatchling isolation induced a significant elevation of Cort, in comparison with hatchlings placed with conspecifics at increasing densities. Growth increased in singly housed hatchlings, while mortality increased in tanks with three or more hatchlings. The results obtained suggest that Cort, growth, and mortality should be measured to assess hatchling welfare when kept under controlled conditions.
... Heterophils (neutrophils in mammals and amphibians) are part of the innate immune system, while lymphocytes are part of the acquired immune system. High ratios of heterophils to lymphocytes in blood samples are considered an indication of high glucocorticoid and stress values in all vertebrate taxa (review in Davis & Maerz 2008), including reptiles (Borgmans, Palme, Sannen, Vervaecke, & Van Damme, 2018;Case, Lewbart, & Doerr, 2005;Chen, Niu, & Pu, 2007;Lance & Elsey, 1999;Morici, Elsey, & Lance, 1997;Saad & Elridi, 1988). ...
Article
The effect of long term captivity is a factor that is important for all research utilizing wild caught animals. Despite the fact that it can be considered to be one of the most fundamental potential sources of stress in captivity, it has received a low amount of interest in recent research on lizards. Given the wide variety in ecology and life history among lizards species, it would make sense to investigate the effect of long term captivity on wild caught lizards on a broader scale. In this study we investigated the effect of long term captivity (four months) on the physiology and behavior of male and female Anolis carolinensis lizards. Our results showed no negative effects of four months of captivity on physiological and behavioral measurements in male A carolinensis lizards. Similar results for females were found for all measurements except body mass and tail width. Here our results indicated a potential negative effect of four months of captivity on body mass and tail width in females.
... 19 An increase in hematocrits, an elevation of circulating corticosterone, and changes in enzymes and heterophil/lymphocyte (H/L) ratios have been used to assess stress levels in reptiles. 14,18,24 Increased glucocorticoid levels can be associated with heterophilia, lymphopenia, and degranulation of the granulocytes (heterophils and eosinophils) in some species. 25 Further obscuring hematologic interpretation is the lack of RIs for many reptilian species, along with the notion that stress and infection are often interrelated. ...
Article
A healthy adult, intact female keeled box turtle (Cuora mouhotii) was found to have a marked heterophilic leukocytosis using normal hematologic parameters established for the eastern box turtle (Terrapene carolina carolina), a related chelonian species. This animal was monitored with serial complete blood counts (CBCs) over the next 15 years despite remaining asymptomatic for an infectious condition. Retrospective CBC data were compiled from 38 presumably healthy keeled box turtles to establish hematologic values for comparison in this species. Using this species‐specific data, over the 15‐year period, the female keeled box turtle had two times where the white blood cell (WBC) count was greater than 2 standard deviations (SD) above the mean, six times where the WBC count was greater than 1 SD above the mean, six times where the PCV was greater than 2 SD above the mean, and eight times where the PCV was greater than 1 SD above the mean. Infection and inflammation are the most common causes of leukocytosis in reptiles; however, given the clinical presentation of this patient, it was postulated that these clinicopathologic changes could be secondary to a stress response. Establishing reference intervals and understanding how stress impacts CBC parameters are important for evaluating the health status of keeled box turtles kept in captivity and for assessing the effects of environmental changes on the health status of wild populations of this endangered chelonian species.
... Providing western chuckwallas (Sauromalus obesus obesus) with a rock feature that created additional choices for concealment led to decreased stereotypic behavior and increased use of retreats (Rose et al., 2014). Additionally, studies with both juvenile (Tetzlaff et al., 2018) and adult (Case et al., 2005) box turtles (Terrapene carolina) have shown that, given the choice, turtles preferred living in enriched, naturalistic environments, even when they were raised in simplistic and non-natural conditions. Habitat modifications including increased spatial complexity and the addition of climbing structures have also yielded positive behavioral results for corn snakes (Rose et al., 2014). ...
... Such an effect conforms to previous quantification of plasma glucocorticoid responses to acute social encounters in this species and vertebrates of most classes (Summers et al., 2003;Creel et al., 2013). Analyses of FGM variation in other reptile species have also yielded similar responses to different types of stressors (e.g., Kalliokoski et al., 2012), although some applications may not be ecologically relevant (e.g., Case et al., 2005;Rittenhouse et al., 2005;Ganswindt et al., 2014). For territorial reptiles such as A. carolinensis, social stress is an inherent component of the environment during the breeding season as males often interact to secure territory possession and social rank (Stamps and Krishnan, 1994;Jenssen and Nunez, 1998). ...
Article
Agonistic encounters necessary for territory establishment and maintenance can be stressful for those involved. Stress responsiveness associated with territorial behavior can occur on both acute and chronic temporal scales contingent upon social status. Social interactions that recur for territory maintenance pose periodic stressors that incur variable physiological costs across social ranks. Adult males of the Green Anole, Anolis carolinensis, experience stressful social encounters during territorial disputes as individuals contest status within a dominance hierarchy. Dominant males in stable territories are known to exhibit greener body coloration and lower levels of stress hormone, corticosterone, relative to their subordinate counterparts. Periodic interactions with novel competitors, however, may induce comparable levels of cumulative glucocorticoid secretion regardless of social status. Glucocorticoid metabolites excreted in feces can be quantified to assess the chronic hypothalamic–pituitary–adrenal (HPA) axis response to periodic social stressors. Fecal glucocorticoid metabolite (FGM) levels in male A. carolinensis were hypothesized to increase in response to novel social encounters that simulated territory establishment and maintenance. Adrenocortical response to recurring episodes of territoriality was predicted to generate similar longitudinal FGM levels across social ranks. FGM analysis was combined with behavioral assessment of body coloration to further contextualize measured stress levels of dominant and subordinate anoles. Prolonged social interaction led to similarly increased levels of fecal glucocorticoid metabolites in both dominant and subordinate anoles relative to those that were solitary. This study provides an alternative perspective on the activity of the HPA axis in dominant-subordinate relationships of A. carolinensis over prolonged periods of territoriality.
... H:L was affected by both age class and sex, being highest in adult, female turtles. As increased H:L is recognized as a measure of stress in reptiles [37,[48][49], metabolic stress due to vitellogenesis may induce changes in heterophil and lymphocyte populations. Higher Ca, P, and Ca:P in females compared to males can also be explained by reproductive physiology, while higher CK in males compared to females is better explained by behavior. ...
Article
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Chelonians are one of the most imperiled vertebrate taxa on the planet due to changes in the environment, anthropogenic influences, and disease. Over the last two decades, conservation strategies including nest protection, head-starting and meso-predator control have been successfully adopted by the Lake County Forest Preserve District for a population of state-endangered Blanding’s turtles (Emydoidea blandingii) in Illinois. Only recently have efforts expanded to assess the effects of management action on turtle health. The objectives of this study were to 1) establish reference intervals for 16 hematologic and plasma biochemical analytes in free-ranging Blanding’s turtles, 2) characterize demographic and temporal drivers of clinical pathology values including age class, sex, month, and year, and 3) describe bloodwork differences between a managed (SBCP) and unmanaged (IBSP) study site. Hematology and plasma biochemistries were performed for 393 turtles from 2017–18 at two sites in the Lake Plain region. Subject or population-based reference intervals were established based on the index of individuality per American Society for Veterinary Clinical Pathology guidelines. Analytes differed by age class [packed cell volume (PCV), total solids (TS), total white blood cell counts (WBC), heterophils, lymphocytes, heterophil:lymphocyte ratio (H:L), total calcium (Ca), calcium:phosphorous (Ca:P), bile acids (BA), aspartate aminotransferase (AST)], sex [H:L, Ca, phosphorus (P), Ca:P, creatine kinase (CK)], month [eosinophils, H:L, Ca, P, uric acid (UA), AST], and year [PCV, WBC, lymphocytes, basophils, H:L, Ca, P, UA]. Several analytes also varied by site [PCV, TS, monocytes, eosinophils, P, UA, AST], suggesting that health status may be affected by habitat management or lack thereof. The results of this study provide a baseline for ongoing health assessments in this region as well as across the Blanding’s turtle range.
... These are open-ended questions that might be addressed in a separate paper, drawing from current knowledge of animal neurobiology and cognition, and their needs and wants for a "life worth living" [4,42]. There is some evidence that some species do indeed display an innate preference for naturalistic "enriched" enclosures as opposed to basic artificial environments without many features (barren environments) (Box Turtles [43,44]; Coal tits and blue tits [45]), suggesting that some animals may indeed have a capacity to identify natural environments. Alternatively, perhaps they just innately prefer non-barren, enriched environments-perhaps these animals would be just as likely to select enriched artificial environments over any basic or barren environments. ...
Article
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This ethical discourse specifically deals with dilemmas encountered within zoological institutions, namely for the concept of natural living, and a new term—wilding. It is agreed by some that zoos are not ethically wrong in principle, but there are currently some contradictions and ethical concerns for zoos in practice. Natural living is a complicated concept, facing multiple criticisms. Not all natural behaviours, nor natural environments, are to the benefit of animals in a captive setting, and practical application of the natural living concept has flaws. Expression of natural behaviours does not necessarily indicate positive well-being of an animal. Herein it is suggested that highly-motivated behaviours may be a better term to properly explain behaviours of more significance to captive animals. Wilding refers to extrapolation of the natural living concept to treating an animal as wild, residing in a wild habitat. This definition is intrinsically problematic, as quite literally by definition, captivity is not a wild nor natural environment. Treating a captive animal exactly the same as a wild counterpart is practically impossible for many species in a few ways. This article discusses complexities of natural living versus natural aesthetics as judged by humans, as well as the possibility of innate preference for naturalness within animals. Zoos nobly strive to keep wild animals as natural and undomesticated as possible. Here it is argued that unintended and unavoidable genetic and epigenetic drift favouring adaptations for life in a captive environment may still occur, despite our best efforts to prevent this from occurring. This article further discusses the blurred lines between natural and unnatural behaviours, and the overlaps with more important highly-motivated behaviours, which may be better predictors of positive affective states in captive animals, and thus, better predictors of positive well-being and welfare. Finally, as we are now in the Anthropocene era, it is suggested that human-animal interactions could actually be considered natural in a way, and notwithstanding, be very important to animals that initiate these interactions, especially for “a life worth living”.
... In avian species, the H:L has also been used to predict susceptibility to disease (Al- Murrani et al. 2002Murrani et al. , 2006), growth rates ( Moreno et al. 2002) and survival to the next breeding season ( Kilgas et al. 2006;Lobato et al. 2005). In box turtles, lower ratios were observed in individuals living under more enriched conditions (e.g., mulched floors, shredded paper and a box for shelter as opposed to newspaper flooring alone: Case et al. 2005); whereas in pigs, differences in humoral immune responses were reported for individuals raised in barren compared to environments enriched with straw bedding ( Bolhuis et al. 2003). In sheep, outdoor access had beneficial effects on lymphocyte proliferation, while reduced space had a negative impact on humoral responses (Caroprese et al. 2009). ...
Chapter
To reverse the trend of declining wildlife populations globally, individuals must be provided with conditions that allow them to not just survive, but to thrive. It is no longer only the remit of captive breeding programs to ensure animal well-being; in situ conservation efforts also must consider how environmental and anthropogenic pressures impact wild populations, and how to mitigate them—especially with regards to reproduction and survival. Stress and welfare are complex concepts that necessitate an understanding of how stressors affect animals on both individual and population levels. There are species differences in how factors impact well-being, related in part to natural history, which also are shaped by individual perceptions and coping abilities. A multitude of stress-related responses then have the potential to disrupt fertility on many levels, and ultimately fitness. A major limitation to advancing welfare science is the lack of definitive tests to verify welfare status; i.e., is the animal happy or not? While analyses of circulating or excreted glucocorticoids have for decades been the primary method of assessing stress, today we recognize the need for more objective indicators that incorporate multiple physiological systems, including behavior, to assess both negative and positive welfare states. In this chapter, we discuss the potential for stress to disrupt, and sometimes facilitate reproduction, including the key role that glucocorticoids play. We then discuss a number of physiological biomarkers, which in addition to glucocorticoids, have the potential to assess well-being and the role of stress on reproduction. Finally, we discuss allostatic load, a method by which multiple physiological markers are used to inform on morbidity and mortality risk in humans, which if applied to wildlife, could be a powerful tool for conservation.
... The behavioural benefits of environmental enrichment have been demonstrated for mammals, reptiles, fish and birds (Poole 1990;McPhee 2003;Almli and Burghardt 2006). Enriched animals often have lower stress levels and are healthier (Case et al. 2005;Burghardt 2013). Although enriched experiences have long been acknowledged as important for the growth of speciesspecific brain characteristics of captive animals (Fox 1968), the applicability of the technique to translocation science is more recent (Reading et al. 2013) and rests on the assumption that the behaviours stimulated in captivity better prepare animals for post-release survival and integration into resident populations. ...
Article
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Context Wildlife translocation is a conservation tool with mixed success. Evidence suggests that longer time in captivity may negatively affect an animal's post-release behaviour and survival. However, environmental enrichment may reduce the deleterious effects of captivity for animals that are going to be released into the wild. Aims The aim of the present study was to compare first-year post-release survival and behaviour of translocated ratsnakes (Pantherophis obsoletus) held captive for varying durations (1-7 years) either with or without enrichment, with that of resident and wild-to-wild (W-W)-translocated ratsnakes. Key results Being in captivity before release negatively affected survival; 11 of 19 (57.9%) captive snakes died or were removed from the study within 12 months, compared with 3 of 11 (27.3%) resident snakes and none of five (0%) W-W snakes. Furthermore, survival probability declined the longer a snake had been in captivity. Six of the seven snakes (86%) that we released that had been in captivity for four or more years before release died during this study, regardless of whether they were enriched or not. Although W-W-translocated ratsnakes moved more often and further than did snakes in other groups, this difference was apparent only in the first month post-release. We found no evidence that abnormal movement patterns or winter behaviour was the cause of reduced survival for captive snakes. Instead, our data suggested that spending time in captivity reduced concealment behaviour of snakes, which likely increased the vulnerability of snakes to predators. Captivity also compromised the foraging ability of some of the snakes. Although there were no overall differences in percentage weight change among the four groups, two snakes (one enriched, one unenriched) were removed from the study because of extreme weight loss (>30%). Conclusions Our results suggested that environmental enrichment did not offset the negative effects of captivity on ratsnakes and that the likely mechanism responsible for low survival was vulnerability to predators. Implications Whether extended periods in captivity render other species unsuitable for translocation, how long it takes for captivity to have deleterious effects, and whether environmental enrichment is also ineffective at offsetting captivity effects in other species remain to be determined.
... 56 Box turtles offered mulch, paper shredding, and a hide box have lower stress levels, based on lower heterophil to lymphocyte ratios. 57 They also spent less time trying to escape than turtles with only a paper substrate. Tree runners become more active when provided with scattered insects in a complex environment, than by insects slowly released from a device. ...
Chapter
The provision of a good light source is important for reptiles. For instance, ultraviolet light is used in social interactions and used for vitamin D synthesis. With respect to housing, most reptilians are best kept pairwise or individually. Environmental enrichment can be effective but depends on the form and the species to which it is applied. Temperature gradients around preferred body temperatures allow accurate thermoregulation, which is essential for reptiles. Natural distributions indicate suitable ambient temperatures, but microclimatic conditions are at least as important. Because the nutrient requirements of reptiles are largely unknown, facilitating self-selection from various dietary items is preferable.
... This deficiency in empirical data means that the husbandry of captive reptiles is either frequently based on anecdotal reports or human intuition, which can be particularly unreliable when applied to animals that are so phylogenetically different from ourselves (Langkilde and Shine, 2006). There is, however, a limited literature on the benefits of enrichment for a small number of reptile species: box turtles (Terrapene) were found to have a preference for an enriched environment over a 'barren' one (Case et al., 2005) and sea turtles displayed fewer stereotypic behaviours when they were provided with novel objects (Therrien et al., 2007). Among lizards, the Varanidae (Monitor lizard family) is known to show various behavioural characteristics that are usually attributed to 'higher' vertebrates, such as counting (Pianka and Vitt, 2003) and problem solving (Manrod et al., 2008) and respond well to both environmental and behavioural enrichment as a part of their husbandry (Manrod et al., 2008;Doody and Burghardt, 2013;Michaels et al., 2014). ...
Article
Staggering food availability through a delivery device is a common way of providing behavioural enrichment as it is usually thought to increase the amount of natural behaviour due to the unpredictability of the food source. Tree-runner lizards (Plica plica) are a Neotropical, scansorial, insectivorous species. We provided these lizards with an enrichment device that slowly released insect prey and tested its effect on the activity and frequency of a number of behaviours in comparison with a scatter control (where prey items were broadcast in the enclosure; standard food presentation for captive insectivorous lizards) and a non-feeding control. Both types of food increased activity and counts of several behaviours in comparison with the non-feeding control. However, we found the provision of the behavioural enrichment device led to a significantly lower frequency of almost all analysed behaviours in comparison with scatter control trials, mainly in behaviours associated with activity (unsuccessful strikes (= unsuccessful capture of prey) (p = 0.004), locomotion (p = 0.004), alertness (p = 0.004) and the number of times a boundary in the enclosure was crossed ie. activity (p = < 0.001)). The frequencies significantly increased in the enrichment trials (relative to the scatter control) were the number of successful strikes (= successful capture of prey; p = <0.001) and targeting prey (p = <0.001). There was no significant difference in latency to first strike (p = 0.24), duration of hunting activity (p = 0.83) or enclosure use (p>0.05) between scatter and enriched trials. The relative success of the scatter feed in promoting activity and increasing hunting difficulty was likely partly due to the enclosure design, where the complex physical environment contributed to the difficultly in catching the prey. However, when the feeding duration and enclosure use was analysed there was no significant difference between the scatter control and enrichment trails. The results from this study highlight the importance of evaluating enrichment strategies, and the role of complex enclosure design in creating effective enrichment for insectivores, which can contribute to their welfare in captivity.
... In fact, studies demonstrate these stress-induced patterns of change in leucocyte profiles of fish, i.e. lymphocytopenia (Ghazaly 1992;Barcellos et al. 2004a,b) accompanied or not by neutrophilia (Ellsaesser & Clem 1986;Khangarot, Rathore & Tripathi 1999;Valenzuela, Silva & Klempau 2008;Rijn & Reina 2010). In accordance with the dichotomous response observed in leucocyte profiles after stress, the N:L ratio can be used as an index of a secondary stress response (Davis et al. 2008), but just a few studies use this parameter to assess stress in fish (Rijn & Reina 2010;Anderson et al., 2011) despite the extensive body of evidence that sustain the N:L ratio (or Hetephils:Lymphocytes) as a measure of stress for other vertebrate groups (Gross & Siegel 1983;Hansen & Damgaard 1993;Fisher, Crowe, O Nuall ain, Monaghan, Prendiville, O'Kiely & Enright 1997;Davis, Anderson & Carroll 2000;Parga, Pendl & Forbes 2001;Moreno, Merino, Martinez, Sanz & Arriero 2002;Case, Lewbart & Doerr 2005;Obernier & Baldwin 2006;Chen, Niu & Pu 2007;L opez-Olvera, Marco, Montan e, Casas-D ıaz & Lav ın 2007;Noda, Akiyoshi, Aoki, Shimada & Ohashi 2007). ...
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Crowding is one of the most common stressors found in intensive aquaculture, compromising growth rates and immune function. Plasmatic cortisol is a classic stress biomarker for fish, but its quantification is expensive and demands blood volumes that small individuals do not provide, constraining the usage of this technique to assess stress in fingerlings. The leucocyte profile is an alternative methodology to quantify stress with reduced costs and volumes of blood. Stress conditions promote neutrophilia and lymphocytopenia as response to elevated glucocorticoids levels. Considering the difficulties to assess stress imposed by intensive fish farming using measurement of glucocorticoid hormones, this study aimed to evaluate the stress-induced changes in leucocyte profiles and growth rates imposed by crowding in fingerlings of Odontesthes bonariensis, a promising South-American candidate for freshwater aquaculture. To meet these objectives, fingerlings (initial weight 0.05 ± 0.06 g and length 1.68 ± 0.13 cm) were reared for 45 days under three rearing densities (1, 5 and 10 fingerlings L−1). At the end of this period, fish were anaesthetized and euthanized to obtain the leucocyte profile, neutrophil:lymphocyte ratio (N:L) and growth rate. Increasing density promoted: significant reduction in growth (final length, weight and specific growth rate); neutrophilia and lymphocytopenia; and increased N:L ratio. Concluding, the tested rearing densities imposed distinct levels of stress characterized by different N:L ratio, demonstrating that the leucocyte profile is a reliable alternative to measure stress levels in O. bonariensis fingerlings and probably in other fish species.
... Currently, to our knowledge, no field studies exist that examine physiological aspects of disturbance in turtles using H:L ratios, but some captive studies do exist that examine H:L ratios (reviewed by Davis et al. 2008). For instance, Case et al. (2005) found that eastern box turtles (Terrapene carolina carolina) held in higher-quality housing conditions (i.e., cages with cover and mulch) had significantly lower H:L ratios than turtles kept in lower-quality housing conditions. Chen et al. (2007) found increased H:L ratio levels in ponds with greater densities of Chinese softshell turtles (Pelodiscus sinensis). ...
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The effect of human disturbance on wildlife is of increasing interest because of the growing use of wildlands by humans for recreation. Few studies have documented the effect of human disturbance on behavior and physiology simultaneously, with no studies existing for any turtle species. Turtles are one of the most endangered taxonomic groups and many are of conservation concern, including the yellow-blotched sawback (Graptemys flavimaculata), a freshwater turtle of the Pascagoula River system, Mississippi, USA. We studied G. flavimaculata individual-and population-level basking behavior, while also documenting the effects of human disturbance on basking behavior at recreationally disturbed and control sites. We also assessed the physiological response of turtles to human disturbance by measuring heterophil/lymphocyte levels (H:L; higher levels indicate increased stress) and shell condition of captured turtles at the 2 sites. At the individual level, disturbed turtles at the recreationally disturbed site basked for significantly shorter durations than undisturbed turtles at the same site and undisturbed turtles at the control site; disturbed turtles at the control site basked longer than all groups possibly because the few instances of disturbances all occurred during a time of year when basking durations were longest. At the population level, we detected significantly lesser basking percentages at the recreationally disturbed site relative to the control site, possibly because of natural differences among the sites (i.e., a more stable thermal environment) or because of the higher level of human disturbance. At the recreationally disturbed site, more disturbances occurred on weekend and weekend bordering days relative to weekdays, and larger and slower boats disturbed significantly greater percentages of basking turtles compared to smaller and faster watercraft. Further, turtles from the disturbed site had significantly higher H:L levels relative to the undisturbed site, and an index of shell condition was significantly poorer at the disturbed site. Boating records indicate that the impact of recreational boating at the disturbed site likely has grown over the last 22 years because of an increase in the number and size of boats using the river; this trend will likely continue unless restrictions are enacted by managers and/or state entities to limit the number and size of boats that access the river. ß 2013 The Wildlife Society.
Article
Providing enrichment that expands the range of behavioral opportunities associated with food acquisition and environmental exploration is an important contributing factor to the well-being of zoo animals. These behaviors can be difficult to promote in carnivores, given their foraging strategies and the logistical, ethical, and financial challenges of providing live prey. In this study, we introduced a novel feeding enrichment to Jacksonville Zoo and Gardens' five adult American alligators (Alligator mississippiensis) in an attempt to simulate a live prey organism within the exhibit and promote natural hunting behaviors like chasing and lunging, as well as increase daily activity levels. The enrichment promoted some behavioral goals for two of the alligators, but it did not promote behavioral goals for the other three alligators. This could have been due to a variety of factors including an existing dominance hierarchy amongst the group's females and the resulting spatial distribution of individuals across a habitat with only one water feature. Our results suggest that female alligators may carve out territories and avoid overlapping space usage with other females during the warmest months of the year. Given the outcomes and limitations of this enrichment strategy, we provide recommendations for this group specifically as well as future enrichment efforts in the general captive crocodilian population.
Article
Environmental enrichment supports the well-being and welfare of captive animals. In the current study, the most suitable form of enrichment device for captive green turtles (Chelonia mydas) was investigated, to support head-start programs rearing turtles for release into their natural habitat. Fifteen-day-old turtles (113-114 g initial weight, n = 75) were randomly distributed into 15 experimental plastic tanks, comprising 5 treatments across three pools of each condition. The turtles in the experimental groups were exposed to four forms of enrichment devices (RS, ring shape; HSQS, hollow square shape; SS, sphere shape; CS, cylinder shape), and their outcomes related to growth, feed utilization, behavior, reduction of injury from conspecifics, and several health parameters were compared to those of a control group. At the end of the 10-week trial, the growth and feed utilization parameters did not differ across the five groups (p > .05). Of the turtles in the experimental treatments, those in the RS treatment spent more time interacting with the enrichment device, followed by the HSQS group. The percentage of wounds suffered through biting was significantly reduced in the groups exposed to enrichment devices, notably in the turtles exposed to the SS device, followed by the RS device. Significant differences between experimental groups in the specific activities of the major intestinal protein-digesting enzymes (trypsin and chymotrypsin) were observed. There were no effects noted in the hematological parameters and the main carapace elemental profile as compared to the control treatment. These findings suggest that the RS device is most appropriate in enriching the environment of juvenile green turtles in captivity programs, as well as in zoos or aquaria.
Chapter
Reptiles include more than 10000 species, including turtles, tortoises, snakes, lizards, and crocodilians. Most snakes and crocodilian reptiles are carnivorous, whereas many tortoises and turtles are herbivorous or omnivorous. Pet reptiles may be housed in an indoor, enclosed, climate‐controlled area, or 'vivarium', although some might be kept in more open outdoor environments. Reptiles are generally not sociable and many reptiles may suffer when housed in groups. Human company is not a need for reptiles, and there is no convincing evidence that reptiles enjoy human presence or contact. Some diseases are common to many reptile species, including those caused by viruses, bacteria, fungi, protozoa, worms, and mites. The best method of euthanasia is often sedation if necessary, followed by an injection of an overdose of pentobarbitone into a vein or head trauma in some reptiles. Behavioural stereotypies have been recorded in reptiles, although there is limited understanding of their causes and significance.
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Performance of Abnormal Repetitive Behavior (ARB) is noted in many captive wild species. ARB can be categorized into two basic forms; those whose aim appears to be to compulsively reach an inappropriate goal, and those whose performance is linked to an inappropriate motor function. While the negative welfare connotations of ARBs are well-known, the precise reason for their performance remains the subject of debate. As zoos move forward in collection planning and to gather more evidence on the biological needs of the species being kept, the idea that ARBs may be part of a “coping function” adds more weight to arguments that some species may not be suitable for the zoo at all. Modern-day definitions of animal welfare tell us to measure the wellbeing of the individual based on its attempts at coping with its immediate environment. A failure to cope, and hence performance of ARB, is an objective and measureable welfare metric that may highlight which species are appropriate for captivity. As conservation pressures on zoos mount, and the need to take in more “captive naïve” species increases, past research on why captive wild animals develop ARB can be used to inform practice. In this paper we aim to review the welfare issues across three basic categories of zoo animal (mammals, birds, ectothermic vertebrates), and critique how research into ARBs can be used by zoos to promote wild-type behavior patterns by providing biologically-relevant management and husbandry regimes, which allow animals the key components of control and choice over what they do and how they do it.
Chapter
Since their emergence 310-320 million years ago, reptiles have evolved to be one of the most adaptive and remarkable groups of vertebrate animals on earth. Comprising over 9500 species, they can be found in diverse niches ranging from the arid Sahara desert to the tropical wetlands of the Amazon. Diverse reproductive physiologies and behaviors, along with adaptive characteristics such as parthenogenesis and development of venom glands for prey immobilization, make them attractive models for biomedical and basic biological research. This chapter provides information regarding biology, husbandry, and the diseases commonly affecting captive reptiles most frequently used in research.
Article
Animal welfare is a high priority for pet owners and accredited zoos and aquariums. Current approaches to measuring welfare focus on identifying consensus among behavioral and physiological indicators of positive and negative emotions. Environmental enrichment is a common strategy used to improve the welfare of captive animals. In enrichment programs, knowledge of an animal’s ecology and individual history are applied to modify the animal’s current environment and management to increase environmental complexity, make the environment more functional or natural, and increase behavioral opportunities. While enrichment techniques for primates and large mammals are well-studied, reptile enrichment has received little attention to date despite a few promising studies. In this study, we monitored the responses of 16 leopard geckos to five types of enrichment (Thermal, Feeding, Olfactory, Object, and Visual) using a repeated-measures design. We measured both specific behaviors we expected to change in response to each enrichment type and four behavioral indicators of welfare: exploratory behavior, species-specific behaviors (behavioral thermoregulation and hunting), behavioral diversity, and abnormal repetitive behaviors. We found geckos interacted with all five types of enrichment at above-chance levels (i.e., no 95% CIs for engagement time overlapped with 0 sec). Geckos spent more time interacting with Thermal and Feeding enrichment than the other types (F(4,60) = 49.84, p < 0.001). Thermal, Feeding, Olfactory, and Object enrichments (but not Visual enrichment) changed specific relevant behaviors (e.g., Thermal enrichment altered thermoregulatory behaviors, Wilk’s lambda = 0.25, F(3,13) = 13.39, p < 0.001) and improved behavioral indicators of welfare (e.g., behavioral diversity, Wilks’ lambda = 0.30, F(12,178) = 12.31, p < 0.001). These results suggest that geckos respond to environmental enrichment, that their responses are predictable based on their ecology, and that environmental enrichment improves gecko welfare. As in mammals and birds, enrichments that address behavioral needs (here: thermoregulation and feeding) appear more effective than enrichments that simply provide novel stimuli to increase exploration. The extent to which our results can be generalized to other reptile species awaits further study, but we suggest that enrichment should be more widely used to improve reptile welfare.
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The North Carolina State University College of Veterinary Medicine Turtle Rescue Team has been treating and releasing wild turtles since 1996 and has compiled a collection of almost 4,000 medical records, now available for consultation by researchers via the North Carolina State University Libraries Special Collections Research Center. Data available for each case include county where turtle was discovered, patient identification number, admission date, species, sex and reproductive status, physical examination findings, clinical diagnosis, last case-entry date, length of stay, and final disposition. Additional data in the records include a day-by-day description of treatment and husbandry performed for each turtle. This report summarizes 2,613 turtle cases examined between 1996 and 2012 by the Turtle Rescue Team, including 12 native species of turtle from 63 North Carolina counties. The sex distribution of those of known sex were evenly distributed. The most common presenting condition was vehicular trauma while garden equipment and fishequipment- related trauma, pet surrender, and other human-induced injury represented an additional 154 cases. Animal attacks and trauma due to unknown causes were also represented. Other conditions diagnosed on presentation included infection, aural abscessation, nutritional disorder, neurologic disorder, buoyancy disorder, prolapse, and other. A small number of turtles were not diagnosed or were healthy. Ultimate disposition data were available for 2,318 turtles, of which 1,227 were released to the wild. The epidemiological data presented here are similar to information collected in Illinois, Tennessee, and Virginia. Medical records from wildlife hospitals and primary care facilities represent an important opportunity to gain valuable insight into the epidemiology of human interaction with native wildlife species.
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Health data for free-living eastern box turtles (Terrapene carolina carolina) at the Maryland Zoo in Baltimore were analyzed. One hundred and eighteen turtles were captured on or near zoo grounds over the course of 15 yr (1996-2011), with recapture of many individuals leading to 208 total evaluations. Of the 118 individuals, 61 were male, 50 were female, and 7 were of undetermined sex. Of the 208 captures, 188 were healthy, and 20 were sick or injured. Complete health evaluations were performed on 30 turtles with physical examination records, complete blood counts (CBCs), and plasma biochemistry profiles. Eight animals were sampled more than once, yielding 40 total samples for complete health evaluations of these 30 individuals. The 40 samples were divided into healthy (N=29) and sick (N=11) groups based on clinical findings on physical examination. Samples from healthy animals were further divided into male (N=17) and female (N= 12) groups. CBC and biochemistry profile parameters were compared between sick and healthy groups and between healthy males and females. Sick turtles had lower albumin, globulin, total protein (TP), calcium, phosphorous, sodium, and potassium than healthy animals. Sick turtles also had higher heterophil to lymphocyte ratios. Healthy female turtles had higher leukocyte count, eosinophil count, total solids, TP, globulin, cholesterol, calcium, and phosphorous than healthy males. Banked plasma from all 40 samples was tested for antibodies to Mycoplasma agassizii and Mycoplasma testudineum via enzyme-linked immunosorbent assay. One sample from a clinically healthy female was antibody positive for M. agassizii; none were positive for M. testudineum. This study provides descriptive health data for eastern box turtles and CBC and biochemistry profile information for T. carolina carolina at and near the Maryland Zoo in Baltimore. It also reports low serologic evidence of exposure to mycoplasmosis.
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This study reports baseline adrenocortical, hematological, and plasma biochemical values for clinically healthy juvenile green turtles from a discrete population at Kaneohe Bay, island of Oahu, Hawaii. Using a general linear modeling program, we compared mean values for these parameters with mean values of a group afflicted with green turtle fibropapillomas (GTFP). Turtles of similar size classes from both groups were collected under the same conditions in the same study area and season at the same time of the day. Corticosterone, hematological, and enzymatic responses to acute and chronic stress were characterized for each group at four different sampling periods: 0 h (within 2 min of capture), 1 h, 3-4 h, and 24 h postcapture. On the basis of the differences identified between groups and times within a group, we conclude that turtles with GTFP are chronically stressed and immunosuppressed.
Chapter
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During the past decade, increased concern for the psychological as well as the physical well-being of animals has allowed environmental enrichment to mature as a focal concept in their captive management (Shepherdson 1989, 1991a,b, 1992). As the concept has developed, its scope has expanged to include almost any variable linked to the perceptual universe, or umwelt (von UcxkiillI909), of the captive animal (Shepherdson 1992). Despite this rapid conceptual growth, environmental enrichment remains an approach applied largely to mammals (Warwick 1990a; Shepherdson 1992; King 1993); other groups, such as amphibians and reptiles, are rarely addressed. For example, a recent extensive catalogue of enrichment ideas (Copenhagen Zoo 1990) devoted only a single page to these taxa. In other reviews, amphibians and reptiles either are not mentioned (duBois 1991; Griede 1992; Shepherdson 1991a; Tudge 1991) or appear only briefly in passing discussion (Markowitz 1982). Nascent efforts have been made to address the psychophysiological problems of reptiles in captivity (Bels 1989; Warwick 1990a,b; Burghardt and Layne 1995), but these are the salient exceptions. The purpose here is to provide a foundation for designing environmental enrichment programs for amphibians and reptiles. Because amphibians and reptiles are species-rich groups (more than 4,000 species of amphibians and 6,000 species of reptiles are currently recognized; Zug 1993) and the literature on their behavior is vast, this review is not intended to be comprehensive. Rather, we address selected topics that provide a basis for exploring enrichment opportunities. In particular, we review the requirements of captive amphibians and reptiles in three areas: (1) contact with conspecifics, (2) interaction with other species, and (3) physical characteristics of the captive environment. Further, we interpret experimental and observational data that address these areas in an enriclunent context and identify opportunities to improve the well-being of captive amphibians and reptiles. Finally, because the maturation and socialization of captive-reared amphibians and reptiles may require some form of emichrnent (see Miller et aI., Chapter 7, this volume), we emphasize the pivotal role of enrichment in captive-breeding programs that have repatriation as a goal (i.e., repopulation of extirpated wild populations as per Reinert 1991; see also Nielsen 1988).
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This study evaluated space use and activity of individually housed Phelsuma guentheri to formulate recommendations for environmental enrichment. Gecko location within small (0.03 m3) and large (0.22 m3) vivaria and substrate use data were collected over five 24 h periods. Thermogradients within each enclosure type were determined by measuring temperature at various heights. From these data, geckos' space use, activity cycle, and substrate preference were calculated in relation to temperature changes and photoperiod. Geckos did not utilize their environment uniformly. Heavily utilized locations contained cage furnishings or hides. Geckos avoided the use of vertical glass walls. Thermogradients were not actively utilized; however, when given the opportunity, geckos would orient towards natural sunlight. Enclosure size did not affect activity cycle, which was nocturnal with crepuscular peaks. Recommendations for enclosure improvement include provision of more furnishings and hides at different thermal levels. An alternate focal heat source other than UV light is recommended to provide warmth without light. Larger enclosures may encourage more uniform use of available space. Transparent glass may not be an appropriate substrate for these geckos. Once recommendations have been implemented, a similar study must be conducted to assess benefit.
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Giving captive animals the opportunity to interact with objects in a “playful” manner is often considered a method of environmental enrichment. However, the occurrence of play in nonavian reptiles is controversial and poorly documented. Similarly, the role of environmental enrichment in fostering psychological well-being in reptiles has been little studied. For several years, an adult, long-term captive, Nile soft-shelled turtle, Trionyx triunguis, at the National Zoo (Washington, D.C.), was provided objects such as balls, sticks, and hoses in an attempt to reduce self-mutilation behavior. The turtle spent considerable time with the objects, and the level of self-mutilation behavior decreased greatly over many months. Video recordings made in various contexts were analyzed in detail, and an ethogram of this turtle's behavior was developed. The turtle interacted with the objects (e.g., basketball, hose, stick) for 20.7% of the time it was observed and was active for 67.7% of the time. Both figures are unusually high for any animal, especially a turtle. The relative lack of play in ectothermic reptiles is supported by the surplus resource theory of play, which considers the joint effects of parental care, metabolism, endothermy, and arousal in providing the context in which playfulness could be manifested and promoted in vertebrate evolution. The existence of vigorous playlike behavior in a member of an ancient reptilian lineage indicates that, in the right circumstances, object play can be performed by reptiles and that having the opportunity to do so may be beneficial in captivity. © 1996 Wiley-Liss, Inc.
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Physical aspects of the laboratory environment, such as type of cage or bedding, are often ignored by investigators but may be quite important for the animals. We examined whether golden hamsters preferred living in wire mesh floored, stainless steel cages or solid floored, plastic cages with corn-cob litter. Forty hamsters of 2 ages were housed in wire or solid floored cages for 3 weeks. Caging preference was then tested using a choice apparatus in which hamsters could move freely between the 2 cages for 6 days. Scan data were collected on cage occupation and behaviour. Results showed that most hamsters preferred the solid floored cage with litter, but prolonged experience on wire led to a wire floored cage preference in 40% of these animals. Also, wire-housed hamsters showed higher levels of hoarding and lower levels of gnawing behaviour during testing, and spent significantly different amounts of time from litter-housed hamsters performing sleeping, exploring, grooming, gnawing, eating, and hoarding behaviours while on solid floored cages with litter. This study shows that previous housing condition can affect cage preferences and behaviour and supports the assertion that husbandry practices can be better evaluated by asking laboratory animals, rather than only humans, how their living conditions are perceived.
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We have studied the effects of long-term social isolation of male Wistar rats, after early weaning (16 days), on the activity of the hypothalamo-pituitary-adrenal (HPA) axis. In addition to studying basal HPA activity, the response of the HPA axis to 15 min of immobilization stress was examined. Plasma corticosterone concentrations were measured, and the relative weights of adrenal glands, thymus, and testes were obtained, the latter to check whether gonadal function was affected by the isolation paradigm. Moreover, we carried out a quantitative immunohistochemical study of pituitary ACTH and its hypothalamic secretagogues: CRF, arginine vasopressin (AVP), and oxytocin (OT), both at the level of the synthesizing cell bodies in the hypothalamic paraventricular nucleus and of the releasing fibers in the median eminence (ME). Body weight and daily consumption of food and water were not altered, but social isolation caused a reduction in plasma corticosterone levels, both under basal and stress-stimulated conditions; this was correlated with an increased thymus weight, without affecting adrenal or testicular weights. The immunohistochemical study revealed that isolation caused a smaller increase in the number of ACTH-immunoreactive cells in the pars distalis of the anterior pituitary after exposure to restraint stress, as compared with control animals. This result indicates that fewer corticotrophs were activated by restraint stress in isolated animals, such cells being smaller and exhibiting a smaller ACTH-immunoreactive area than in control animals. Isolated animals also showed an increase in the content of CRF-ir fibers in the ME and a smaller decrease in the neuropeptide immunoreactivity after stress than that observed in control animals. This result could indicate a reduced release of CRF into the portal vasculature in response to acute stress and may partially explain the reduced activation of corticotrophs observed in the pituitary of isolated animals. However, no changes were found in the content of CRF, AVP, or OT within the paraventricular nucleus, nor of the AVP or OT content in the ME. The results of this study show that long-term social isolation after early weaning caused a hypofunction of the HPA axis in the adult rat. This hypofunction was particularly evident after exposure to an acute stressor, suggesting a desensitization of this axis to stressful stimuli.
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Three turtles, Clemmys insculpta, were kept together in a terrarium in a climatic chamber at 18 degrees C, with lights on at 07:00 h and off at 19:00 h. In one corner of the terrarium an infrared lamp produced an operative temperature of 42.5 degrees C, thereby allowing behavioral temperature regulation during the light period. When the turtles were handled only once a day for the purpose of taking cloacal temperature, their body temperature held stable at about 22-23 degrees C. Immediately after being handled the turtles sought the radiant heat and regulated their body temperature at about 4 degrees C higher than before the handling. When repeatedly handled every 15 min for 2 h the turtles maintained a high body temperature by their behavior. When not repeatedly handled the turtles returned to their initial preferred body temperature ca 22-23 degrees C within 2 h. It is hypothesized that handling causes in turtles a fever similar to that observed in stressed mammals. The turtles were equipped with an electrocardiogram radio transmitter and their heart rate was recorded at a distance. Heart rate in undisturbed turtles was 28.3+/-0.6 bt/min. During a 1-min handling, their heart rate rose to 40.2+/-0.8 bt/min. This tachycardia persisted several minutes, then their heart rate returned to the baseline value in ca. 10 min. Stress fever and tachycardia are taken as signs of emotion in turtles.
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Exposure to concentrations of glucocorticoids analogous to those produced during stress, trauma and malnutrition had rapid but varying effects on the major classes of cells within the marrow. Corticosterone (CS) was given as a subdermal implant in young mice and generated 60-95 microg CS/dl of blood compared to 5-15 microg CS/dl for sham controls over a period of 36 hr. Within 24 hr CS had caused losses of 30-70% among the early pro-B, pre-B and immature B cells. The pre-B cells were virtually eliminated by 36 hr and the capacity of surviving pro- and pre-B cells to cycle was reduced by 70-80%. Interestingly, the earliest of B cells, the prepro-B cells, showed considerable resistance to CS, being reduced by only 20% at 36 hr. Thus, the pattern of survival within the B-cell compartment paralleled the expression of Bcl-2. At the 36-hr time-point there were no changes in the proportion of progenitor cells, erythroid or monocytic cells, or number of nucleated cells in the marrow. By contrast, 36 hr after exposure to CS there was an increase of 30% in the proportion and absolute number of cells in the granulocytic compartment. Chronic production of CS appears to reprogramme lymphopoiesis and myelopoiesis, perhaps to preserve the first line of immune defence at the expense of the lymphoid branch. Resistance to apoptosis and modifications in the activity of the glucocorticoid receptor and cytokines produced by stromal cells are postulated as targets for CS-driven changes.
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A reciprocal regulation exists between the central nervous and immune systems through which the CNS signals the immune system via hormonal and neuronal pathways and the immune system signals the CNS through cytokines. The primary hormonal pathway by which the CNS regulates the immune system is the hypothalamic-pituitary-adrenal axis, through the hormones of the neuroendocrine stress response. The sympathetic nervous system regulates the function of the immune system primarily via adrenergic neurotransmitters released through neuronal routes. Neuroendocrine regulation of immune function is essential for survival during stress or infection and to modulate immune responses in inflammatory disease. Glucocorticoids are the main effector end point of this neuroendocrine system and, through the glucocorticoid receptor, have multiple effects on immune cells and molecules. This review focuses on the regulation of the immune response via the neuroendocrine system. Particular details are presented on the effects of interruptions of this regulatory loop at multiple levels in predisposition and expression of immune diseases and on mechanisms of glucocorticoid effects on immune cells and molecules.
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Psychological stress is associated with immunosuppression in both humans and animals. Although it was well established that psychological stressors stimulate the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system, resulting in the release of various hormones and neurotransmitters, the mechanisms underlying these phenomena are poorly understood. In this study, mu-opioid receptor knockout (MORKO) mice were used to investigate whether the mu-opioid receptor mediates the immunosuppression induced by restraint stress. Our results showed that wild-type (WT) mice subjected to chronic 12-h daily restraint stress for 2 days exhibited a significant decrease in splenocyte number with a substantial increase in apoptosis and CD95 (Fas/APO-1) expression of splenocytes. The effects are essentially abolished in MORKO mice. Furthermore, inhibition of splenic lymphocyte proliferation, IL-2, and IFN-gamma production induced by restraint stress in WT mice was also significantly abolished in MORKO mice. Interestingly, both stressed WT and MORKO mice showed a significant elevation in plasma corticosterone and pituitary proopiomelanocortin mRNA expression, although the increase was significantly lower in MORKO mice. Adrenalectomy did not reverse restraint stress-induced immunosuppression in WT mice. These data clearly established that the mu-opioid receptor is involved in restraint stress-induced immune alterations via a mechanism of apoptotic cell death, and that the effect is not mediated exclusively through the glucocorticoid pathway.
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Research on physical or psychological stress, in order to monitor objective parameters for animal welfare, is usually performed during experimental stress induction. To avoid treatment of animals with physical or physiological stress, addition of the stress-related hormone corticosterone to the drinking water, may serve as a practical alternative to reproducibly investigate hormone-related stress in broiler chickens. Rapid uptake of the hormone and distribution in the bloodstream were affirmed by elevated plasma corticosterone concentrations immediately after start of the treatment. The effect of hormone administration was evaluated by examination of corticosterone-sensitive organs. Comparable to the observations during physiological stress, we found in our model that uptake of endogenous corticosterone reduced body and spleen growth, increased heterophil counts, and decreased formation of antibodies against sheep red blood cells. Furthermore, corticosterone decreased adrenal gland responsiveness, measured by corticosterone production, after a challenge with adrenocorticotropic hormone. The simple performance, and the close relation between circulating corticosterone levels and heterophil counts, makes this an easy and quick method that is sensitive to increased levels of circulating corticosterone from base levels. The changed responsiveness of the adrenal glands to adrenocorticotropic hormone after increased circulating corticosterone levels may be an indication of the coping strategies during stress. Therefore, this test may be a promising tool in the research of adaptation to stress by broiler chickens.
Book
This most important book fully examines the welfare of captive reptiles and discusses the positive and negative implications of general husbandry and research programmes. The editors, acknowledged experts in their own right, have drawn together an extremely impressive international group of contributors providing clearly written and comprehensive accounts of aspects such as physiology, physical stress, diet, veterinary and environmental issues, normal behaviour, psychological stress and informed design in research.
Article
The increasing destruction of box turtle habitat, as well as heightened interest in box turtles as pets, has placed this animal in high profile to the public as well as possible danger of extinction. As a result, wildlife rehabilitators are encountering this animal more frequently than ever before. Few wildlife rehabilitators have more than a passing acquaintance with reptiles. Reptiles have distinct needs during rehabilitation that require knowledge not commonly found in either the rehab community or even among most general practice veterinarians. The author provides a brief introduction to the natural history and a basic introduction to triage practices based on experience as well as some of the more recent findings on these species of turtles.
Article
Reptile species are rarely the subjects of environmental enrichment programs, and there is little data available in the literature from enrichment studies involving these species. The authors share their studies of enriching the environments of Nile soft-shelled turtles.
Article
Research to be described in this chapter was initiated by Conant (1971) when he called attention to the fact that cage-cleaning had arousing effects on numerous species of vertebrates at Philadelphia Zoo. His 1971 article focused exclusively on amphibians and reptiles, but his earliest experience along these lines was with mammals, as related in the following personal communication (1990) reproduced here by permission.
Article
Behavior and heart rate response of seven ornate box turtles (Terepene ornata) to visual threat, touch, forced diving, and voluntary diving were investigated. Visual stimulus resulted in two different behavioral and two different heart rate responses. Three of seven turtles turned and walked away from the stimulus with no change in heart rate. Four turtles stopped walking and withdrew their feet and head. Heart rate was reduced 37%. Atropine had no effect on behavior but abolished bradycardia. Tactile stimulus resulted in withdrawal of feet and head and reduction of heart rate by each of the turtles. Heart rate was reduced 68%. Atropine abolished bradycardia but did not alter behavior. Reduction in heart rate was instantaneous and occurred during the first R-R interval following stimulus. Forced diving reduced the heart rate 56%. Bradycardia was abolished with atropine. Bradycardia onset was gradual, suggesting chemoreceptor involvement. Voluntary diving was not accompanied by bradycardia.
Chapter
During the past few decades, there have been numerous improvements in practical methods of reptile care. However, these gains in enhanced management and animal well-being have been accompanied by revelations emphasizing the intricacies of reptilian biology and, further, the needs of the individual. In effect, the more that is learnt about reptiles, the more apparent become the potential deficiencies associated with their lives in captivity. Improvements to the lifestyles of captive reptiles, in at least some professional centres, seem set to continue. It is, however, essential that any optimism is tempered by the clear prospect that it may never be possible to hold these animals, or other wildlife, under artificial conditions where they do not, either consciously or otherwise, notice that they are not where they ‘should’ be or where they are not adversely affected by their captivity.
Article
Factors affecting use of daytime resting forms by box turtles do not appear to be specific to sex or size cohort of the adult population. -P.J.Jarvis
Chapter
The purpose of this chapter is to present various considerations, not necessarily related, that may directly or indirectly have a significant bearing on reptile health and welfare. It is hoped that at the very least their inclusion may create or stimulate an awareness of these and other issues which affect the well-being of captive reptiles.
Article
Evaluations were made of >4000 reptiles maintained in captive situations to assess numerous abnormal behaviours and any related environmental and other influences. Certain behavioural restrictions warrant concern because they result in physical injuries while others are primarily related to inhibited ethological expression; this paper concentrates on the latter. Hyperactivity, hypoactivity, persecution from other occupants, disposition-related environmental temperature preference, interaction with transparent boundaries and aggression are a few examples of abnormal behaviours resulting from concept- and design-deficient artificial environments, and all may be related to poor adaptability and environmentally induced trauma. It is probable that the adaptability of reptiles to unnatural environments is substantially compromised by the fundamental biological principle of their innate education system which results in greatly reduced susceptibility to other educative influences.The importance of a sound knowledge of a species natural life style (wherever possible prior to their acquisition) is to be emphasised if preventative action regarding abnormal behaviour and evaluations of current problems are to be thoroughly addressed. Very little work has been done on this subject probably because natural behaviours of reptiles may present observational difficulties and because “lower” vertebrates are often perceived as being highly adaptable to captivity and thus warrant low priority.
Article
A simple method for extracting ovarian steroids from feces is presented, together with enzyme immunoassay systems for measuring estrogen and progesterone metabolites. Small amounts of feces were combined in a 1:10 proportion with a modified phosphate buffer, shaken for 24 h, centrifuged, and decanted; the supernatant was directly measured for estrogen and progesterone metabolites by enzyme immunoassays. Serum estradiol and progesterone profiles were compared to urinary and fecal profiles in the same animals to determine the degree to which each reflected the ovarian events detectable in serum. The correlation coefficients for the relationship between serum, urinary, and fecal hormones for individual animal cycles were found to be statistically significant in every case but one, where the relationship between serum estradiol and urinary estrone conjugates was not significant. Urinary and fecal measurements were used to determine whether estrogen and progesterone metabolism and excretion varied within and between animals. Variation in unconjugated estrogen and progesterone metabolites was observed in the follicular phase, the luteal phase, and early pregnancy.
Article
Sympatric box turtles Terrapene carolina and wood turtles Clemmys insculpta in south-central Pennsylvania possess the following contrasting constellations of characteristics. Clemmys have large home ranges and long daily foraging paths, include green leaves among their major diet categories, remain active during summer dry periods, and are restricted to lowland areas. Terrapene have small home ranges and short daily foraging paths, do not eat green leaves, generally are inactive during dry spells, and occur in both the lowlands and the dry summits of the folded Appalachians. These differences appear to be associated with the turtles' different ways of combatting desiccation, and with spatial and temporal food distribution patterns.-Author
Article
The question ‘Do hens suffer in battery cages?’ is difficult to answer because of the problem of objectively assessing suffering in animals. It is argued that preference tests may be one way of throwing light on this difficult problem. This paper describes some experiments on habitat preference in domestic hens. No preference was observed between a commercial battery cage and a large pen when hens were given continuous access to the two. A simultaneous choice between a battery cage and an outside hen-run showed a clear preference for the run, but choice was strongly influenced by prior experience. The strength of the run preference was investigated by ‘pitting’ the run against food and access to companions.
Article
Previously we showed that pigs reared in an enriched environment had higher baseline salivary cortisol concentrations during the light period than pigs reared under barren conditions. In the present experiment, it was investigated whether these higher baseline salivary cortisol concentrations were a real difference in cortisol concentration or merely represented a phase difference in circadian rhythm. The effects of different cortisol concentrations on the behavioral responses to novelty and learning and long-term memory in a maze test were also studied in enriched and barren housed pigs. At 9 weeks of age enriched and barren housed pigs did not differ in baseline salivary cortisol concentrations nor in circadian rhythm, but at 22 weeks of age barren housed pigs had a blunted circadian rhythm in salivary cortisol as compared to enriched housed pigs. The differences in baseline salivary cortisol concentrations between enriched- and barren-housed pigs are age-dependent, and become visible after 15 weeks of age. Enriched- and barren-housed piglets did not differ in time spent on exploration in the novel environment test. Barren-housed pigs had an impaired long-term memory in the maze test compared to enriched-housed pigs; however, no differences in learning abilities between enriched- and barren-housed pigs were found. Because blunted circadian cortisol rhythms are often recorded during states of chronic stress in pigs and rats or during depression in humans, it is suggested that the blunted circadian rhythm in cortisol in barren-housed pigs similarily may reflect decreased welfare.
Article
Microfilm. Thesis--University of Michigan. Abstracted in Microfilm Abstracts 9:2.
Article
The number of lymphocytes in chicken blood samples decreased and the number of heterophils increased in response to stressors and to increasing levels of corticosterone in the chicken feed. The ratio of heterophils to lymphocytes was less variable than the number of heterophil or lymphocyte cells, and the range of values for this ratio was greater than the range of values for heterophils and lymphocytes among control and experimental groups. The heterophil/lymphocyte ratio appears to be a more reliable indicator of levels of corticosterone in the feed and to social stress than were the plasma corticosteroid levels.
Article
A simple method for extracting ovarian steroids from feces is presented, together with enzyme immunoassay systems for measuring estrogen and progesterone metabolites. Small amounts of feces were combined in a 1:10 proportion with a modified phosphate buffer, shaken for 24 h, centrifuged, and decanted; the supernatant was directly measured for estrogen and progesterone metabolites by enzyme immunoassays. Serum estradiol and progesterone profiles were compared to urinary and fecal profiles in the same animals to determine the degree to which each reflected the ovarian events detectable in serum. The correlation coefficients for the relationship between serum, urinary, and fecal hormones for individual animal cycles were found to be statistically significant in every case but one, where the relationship between serum estradiol and urinary estrone conjugates was not significant. Urinary and fecal measurements were used to determine whether estrogen and progesterone metabolism and excretion varied within and between animals. Variation in unconjugated estrogen and progesterone metabolites was observed in the follicular phase, the luteal phase, and early pregnancy.
Article
The current study supported the hypothesis that individuals with a propensity to join groups score more psychologically healthy than individuals less so inclined.
Article
Sixty juvenile alligators were implanted subcutaneously with slow release pellets of corticosterone or placebo. Alligators were divided into five different groups such that each group received a different dose. A blood sample was taken prior to and 4 days after the implants were in place to measure hormone levels. Additional blood samples were collected at 1 month and 3 months. At 4 days corticosterone levels ranged from 3,400 ng/ml in the group treated with the high dose to 40 ng/ml in the group implanted with the low dose. The extremely high dose caused 40% mortality within 4 weeks. It was evident that the pellets did not release the hormone for the expected 90 days. Circulating levels of corticosterone were back to baseline levels by 3 months. Hormone levels achieved at 4 days were a reliable predictor of subsequent growth. Rate of growth was negatively correlated with plasma corticosterone at 4 days (r2 = 0.711) and at 1 month (r2 = 0.544) posttreatment. Differential white blood cell counts performed after 1 month of treatment showed a clear effect of the implant. Alligators treated with corticosterone had decreased percentages of lymphocytes, eosinophils, and basophils and had a higher heterophil/lymphocyte (H/L) ratio than the placebo group. Furthermore, histological examination of the spleen revealed a significant depletion of lymphoid cells in alligators treated with the highest dose of hormone. The results from this study demonstrate that exogenous corticosterone can mimic the effects of prolonged stress in juvenile alligators.