Captive Settings Research Articles

Effects of prey-based and non-prey-based scent enrichment on two zoo-housed monitor lizards

Environmental enrichment is a powerful tool in maintaining positive welfare for captive animals but investigation of this in reptiles has been limited. Monitor lizards are active, intelligent animals that represent high priority targets for enrichment in a captive setting, but more data are required to develop evidence-based recommendations and to understand variation in the responses to enrichment of both individuals and species. We exposed two monitor lizards, Varanus cumingi and Varanaus macraei, both adult females, to olfactory enrichment comprising prey-based and non-prey-based scent trails and then measured changes in activity and tongue-flicking versus a control. Randomisation analysis, employed to deal with small sample size, showed that the V. cumingi significantly increased both behaviours in response to both enrichment types, versus control, while the V. macraei responded significantly only to the prey-based scent for both behaviours. These findings provide an evidence-based case study demonstrating the potential effectiveness of enrichment for captive monitors, but also the need for context-specific evaluation of enrichment strategies to ensure maximal benefit for a given individual animal.

Pharmacokinetics and safety of topical fluralaner in koalas (Phascolarctos cinereus)

Sarcoptic mange (etiological agent Sarcoptes scabiei) is among the most important parasitic diseases of some marsupial species and has been an emerging disease of koalas, causing welfare and conservation implications. Fluralaner (Bravecto® MSD Animal Health), an ectoparasiticide of the isoxazoline class, has been demonstrated as a long-lasting and efficacious chemotherapeutic agent against sarcoptic mange in multiple mammal species and may also be beneficial for impacted koalas. Here, we evaluated the pharmacokinetics and clinical safety of fluralaner in koalas. Healthy captive individuals were treated topically with 85 mg/kg fluralaner administered to the interscapular epidermis. Following treatment, fluralaner was detected in plasma using ultra-performance liquid chromatography and tandem mass-spectrometry over a 12-week period. The mean maximum plasma concentration (Cmax) was 66.4 ng/mL; mean time was Cmax of 2.71 days; plasma elimination half-life (T1/2) was 30.91 days; and mean residence time (MRT) was 27.38 days. Haematological, blood biochemical, animal husbandry and clinical observations, over the same time period, demonstrated fluralaner was well tolerated. Overall, this research suggests fluralaner is a safe and long-lasting chemotherapeutic agent that may be efficacious against S. scabiei in koalas. Further research focussed on quantifying efficacy in captive and field settings, and across a range of disease severities would be valuable.

Considering management context when investigating behavioral profiles in a group of captive Javan gibbons (Hylobates moloch)

ABSTRACT Effective animal husbandry aims to produce behavioral profiles consistent with those observed in wild counterparts. However, few studies have examined the impacts of management history on sociality. We investigate social dynamics in a group of Javan gibbons (Hylobates moloch) at Perth Zoo using behavioral and proximity data. The group consists of an aging adult female and her two offspring – a maturing sub-adult female and a juvenile male. This composition diverges from commonly observed groupings in the wild. The study group’s social relationships generally align with species-typical behaviors, with the exception of the patterning of play behavior and resting-in-contact. These results indicate an uncharacteristically close bond between the mother and her maturing same sex-offspring, as well as an unexpectedly distant mother-juvenile bond. These relationships are best explained by the group’s management history and resulting atypical group composition including: the absence of an adult male, the mother’s advanced age, and the hand-rearing of the juvenile male. This study gives insight into the effects of a captive setting on social development and provides further evidence of social flexibility in gibbons.

Effects of Social Group Housing on the Behavioral and Physiological Responses of Captive Sub-Adult Giant Pandas.

Wild giant pandas are inherently solitary creatures, however, the ex-situ conservation efforts significantly alter the living circumstances of their captive counterparts. Following the breeding period, giant pandas in captivity may be maintained in social groups. Currently, there is a lack of research on the effects of group housing on the physiology, behavior, and gut microbiota of captive giant pandas. This study divided six captive giant pandas into two groups following the breeding period. By comparing the behavior, physiology, and microorganisms of the two groups, we aim to investigate the behavioral responses and physiological adaptation mechanisms exhibited by captive giant pandas in a "group living" state. Our findings indicate that sub-adult giant pandas housed in group settings exhibit a significantly longer duration of playing behavior (including interactive and non-interactive play) compared to their counterparts housed separately (p < 0.001) while also demonstrating a significantly lower duration of stereotyped behavior than their separately housed counterparts. Additionally, an analysis of urine cortisol and heart rate variability between the two groups revealed no significant differences. Simultaneously, the group housing strategy markedly elevated the β diversity of gut microbiota in sub-adult giant pandas. In conclusion, the group-rearing model during the sub-adult stage has been shown to significantly alter the behavioral patterns of captive giant pandas. In conclusion, within the present captive setting, the group-rearing approach during the sub-adult stage proved to be less distressing for adult captive giant pandas.

Adaptations and Preferences of Wild Hummingbirds Introduced into a Captive Setting

Adaptations and Preferences of Wild Hummingbirds Introduced into a Captive Setting

Chironomid farming in consideration of various physicochemical parameters and reuse of condensate water

AbstractLarvae of chironomids are benthic organisms, having the extreme capability to adapt to the changing physicochemical parameters of the aquatic body and the potentiality to accommodate that adverse situation. In spite of the demand for chironomid larvae as fish food, no proper technique of chironomid farming has been reported till today. This instance encourages the research on farming these larvae, in both open and captive settings. The present research shows a good result all over the year, with seasonal variance along with changing physicochemical parameters. This farming is based on minimal space requirements, reuse of condensate water, and the application of a low‐cost diet, resulting in enormous production of this insect. Thus, it can be placed as a small‐scale industry to uplift the economic status of rural people. A nutritious diet for both carnivorous and omnivorous fish and low‐cost farming with a huge production of these larvae is good for the fish industry as well.

Variable effects of captivity on microbiomes in populations of IUCN-endangered Blanding's turtles (Emydoidea blandingii).

Microbiome composition is increasingly considered in species reintroduction efforts and may influence survival and reproductive success. Many turtle species are threatened by anthropogenic pressures and are frequently raised in captivity for reintroduction efforts, yet little is known about turtle microbiome composition in either wild or captive settings. Here, we investigated trends in microbiome composition of captive and wild IUCN-endangered Blanding's turtles (Emydoidea blandingii). We amplified and sequenced the V4 region of the 16S rDNA locus from plastron, cloaca, and water samples of wild E. blandingii adults and two populations of captive E. blandingii juveniles being raised for headstarting. Plastron, cloaca, and water-associated microbiomes differed strongly from each other and were highly variable among captive sites and between captive and wild sites. Across plastron, cloaca, and water-associated microbial communities, microbial diversity changed over time, but not in a predictable direction between captive sites. Plastron beta diversity correlated with growth rate in captive samples, indicating that external microbiomes may correlate with individual fitness. Our results indicate that external and internal microbiomes vary between captive and wild turtles and may reflect differences in fitness of captive-raised individuals.

Male juvenile golden snub-nosed monkeys acting as the mountee to receive grooming in their same-sex mounts

Abstract Same-sex mounts provide male juvenile golden snub-nosed monkeys (Rhinopithecus roxellana) with opportunities to practice heterosexual copulatory skills and are often followed by grooming (post-mounting grooming, PMG). We hypothesized that juveniles acted as the mountee and provided mounting opportunities to receive grooming from their peer mounter. Here, we observed same-sex mounts among male juveniles (N = 5) in a captive group of R. roxellana in Shanghai Wild Animal Park, China, from November 2014 to June 2015. Among 1,044 mounts recorded, 45.40% were accompanied by PMG initiated by the mounter and only 3.74% were followed by PMG initiated by the mountee. Mountees were more likely to receive PMG when they performed a mounting solicitation than when they did not, or when they were mounted for a longer time (even if they did not solicit). Over a long timeframe (1 month), mountee’s tended to choose partners who groomed them more often than others after mounting, regardless of how long the grooming lasted. However, whether the mounter groomed the mountee did not predict the mounting direction in their subsequent mount. Our results suggest that, in the context of same-sex mounts, juveniles provide mounting opportunities to receive grooming from peers on a long-term, rather than on a short-term basis. This study provides the first evidence that juveniles’ same-sex mounting strategy may be associated with the grooming market in nonhuman primates, which necessitates further investigation with large free-ranging groups due to the limited sample size of individuals and the captive setting of the current study.

Hybridization in an isolated population of blesbok and red hartebeest.

Hybridization in antelope species has been widely reported in South African national parks and provincial reserves as well as on private land due to anthropogenic effects. In a closed management setting, hybridization may occur due to the crossbreeding of closely related species with unequal sex ratios, resulting in either sterile or fertile offspring. In this study, we used molecular techniques to evaluate the risk of anthropogenic hybridization between blesbok (Damaliscus pygargus phillipsi) and red hartebeest (Alcelaphus buselaphus caama) in an isolated group that purposely included the two species with unequal sex ratios (one red hartebeest male and 19 male and female blesbok). Genetic analysis based on microsatellites confirmed the presence of seven hybrid individuals. Mitochondrial analysis verified that hybridization occurred between blesbok females and the red hartebeest male. STRUCTURE and NEWHYBRIDS classified the hybrids as F1. It is suspected that the hybrid individuals were sterile as the males had undeveloped testes and only F1 hybrids were detected. Thus, the risk of hybridization between these two species may be limited in the wild. In captive settings, genetic monitoring should be included in management plans for blesbok and red hartebeest to ensure that the long-term consequences of wasted reproductive effort are limited.

Genomic insights into anthropozoonotic tuberculosis in captive sun bears (Helarctos malayanus) and an Asiatic black bear (Ursus thibetanus) in Cambodia

Contact between humans and wildlife presents a risk for both zoonotic and anthropozoonotic disease transmission. In this study we report the detection of human strains of Mycobacterium tuberculosis in sun bears and an Asiatic black bear in a wildlife rescue centre in Cambodia, confirming for the first time the susceptibility of these bear species to tuberculosis when in close contact with humans. After genotyping revealed two different strains of M. tuberculosis from cases occurring between 2009 and 2019, 100 isolates from 30 sun bear cases, a single Asiatic black bear case, and a human case were subjected to whole genome sequencing. We combined single nucleotide polymorphism analysis and exploration of mixed base calls with epidemiological data to indicate the evolution of each outbreak. Our results confirmed two concurrent yet separate tuberculosis outbreaks and established a likely transmission route in one outbreak where the human case acted as an intermediatory between bear cases. In both outbreaks, we observed high rates of transmission and progression to active disease, suggesting that sun bears are highly susceptible to tuberculosis if exposed under these conditions. Overall, our findings highlight the risk of bi-directional transmission of tuberculosis between humans and captive bears in high human tuberculosis burden regions, with implied considerations for veterinary and public health. We also demonstrate the use of standard genomic approaches to better understand disease outbreaks in captive wildlife settings and to inform control and prevention measures.

Comparison of animal welfare assessment tools and methodologies: need for an effective approach for captive elephants in Asia.

Welfare is a fundamental aspect of animal management and conservation. In light of growing public awareness and welfare concerns about captive elephants, there is an urgent need for comprehensive, globally coordinated efforts for Asian elephants (Elephas maximus) that participate in religious, logging, or tourist activities in range countries where the majority reside, and where welfare issues have been identified but not addressed. This review provides a comparative analysis of available animal assessment tools. Each offers distinct features for assessment that allow institutions to select criteria for specific needs and available resources. Most are applied to general animal welfare assessments, although some are tailored to particular species, including elephants. The tools span diverse formats, from digital to primarily paper-based assessments. Assessments operate at individual and institutional levels and across multiple welfare domains. Methodologies rely on keeper ratings or expert evaluations, incorporate numerical scoring and Likert scales for welfare grading, and encompass inputs including behaviors, health, and physiological indicators. For tourist camp elephants, one challenge is that the tools were developed in zoos, which may or may not have application to non-zoological settings. Digital tools and assessment methodologies such as keeper ratings face logistical challenges when applied across tourist venues. As with any tool, reliability, validity, and repeatability are essential and must address the unique welfare challenges of diverse captive settings. We propose that a holistic, context-specific, evidence-based, and practical tool be developed to ensure high elephant welfare standards in non-zoological facilities throughout Asia.

Comparative analysis of mother–infant interactions between free-ranging and captive rhesus macaques in Kathmandu, Nepal

Rhesus macaques (Macaca mulatta) are gregarious, social primates whose infants depend on maternal support for survival. This study aimed to compare mother–infant interactions between free-ranging rhesus macaques (Swayambhunath Temple) and those in a captive setting (Central Zoo, Lalitpur) in Kathmandu, Nepal. Interactions such as duration of proximity and duration of contact between the dyads and symmetry, duration of out-of-proximity, duration of carrying or leaving by the mother while moving, and duration of nipple contact were compared. Five-minute focal animal sampling of maternal macaques was used to record the duration of mother–infant interactions. The behavioral state of the mother was also recorded via instantaneous scan sampling at one-minute intervals during focal samples. Our results revealed that the durations of proximity and contact were greater in the free-ranging macaques than in the zoo macaques. Similarly, the duration of carrying or leaving by the mother while moving was also greater in the free-ranging condition. The free-ranging mother–infant dyads spent significantly more time in nipple contact than did those in the captive setting. The infants were found to be primarily responsible for initiating both contact and proximity in the captivity. The symmetry for contact was balanced in free-ranging macaques; however, the infants were more responsible than the mothers for proximity behavior.

Comparing the gut microbiota of Sichuan golden monkeys across multiple captive and wild settings: roles of anthropogenic activities and host factors

BackgroundCaptivity and artificial food provision are common conservation strategies for the endangered golden snub-nosed monkey (Rhinopithecus roxellana). Anthropogenic activities have been reported to impact the fitness of R. roxellana by altering their gut microbiota, a crucial indicator of animal health. Nevertheless, the degree of divergence in gut microbiota between different anthropogenically-disturbed (AD) R. roxellana and their counterparts in the wild has yet to be elucidated. Here, we conducted a comparative analysis of the gut microbiota across nine populations of R. roxellana spanning China, which included seven captive populations, one wild population, and another wild population subject to artificial food provision.ResultsBoth captivity and food provision significantly altered the gut microbiota. AD populations exhibited common variations, such as increased Bacteroidetes and decreased Firmicutes (e.g., Ruminococcus), Actinobacteria (e.g., Parvibacter), Verrucomicrobia (e.g., Akkermansia), and Tenericutes. Additionally, a reduced Firmicutes/Bacteroidetes ratiosuggested diminished capacity for complex carbohydrate degradation in captive individuals. The results of microbial functional prediction suggested that AD populations displayed heightened microbial genes linked to vitamin and amino acid metabolism, alongside decreased genes associated antibiotics biosynthesis (e.g., penicillin, cephalosporin, macrolides, and clavulanic acid) and secondary metabolite degradation (e.g., naphthalene and atrazine). These microbial alterations implied potential disparities in the health status between AD and wild individuals. AD populations exhibited varying degrees of microbial changes compared to the wild group, implying that the extent of these variations might serve as a metric for assessing the health status of AD populations. Furthermore, utilizing the individual information of captive individuals, we identified associations between variations in the gut microbiota of R. roxellana and host age, as well as pedigree. Older individuals exhibited higher microbial diversity, while a closer genetic relatedness reflected a more similar gut microbiota.ConclusionsOur aim was to assess how anthropogenic activities and host factors influence the gut microbiota of R. roxellana. Anthropogenic activities led to consistent changes in gut microbial diversity and function, while host age and genetic relatedness contributed to interindividual variations in the gut microbiota. These findings may contribute to the establishment of health assessment standards and the optimization of breeding conditions for captive R. roxellana populations.

Correlates of Bird Collection Compositions in Thai Zoos: Implications for Conservation and Management

Zoo collection management is increasingly driven by meeting global conservation needs. Many avian species have experienced population declines throughout Southeast Asia, underscoring the importance of ex situ conservation in these countries. We focus on Thailand, a bird diversity hotspot with a long tradition of keeping birds in captive settings. We aimed to understand what drives species acquisition and maintenance in Thai zoos. To that end, we surveyed 55 zoos, making a complete inventory of reptiles, birds, and mammals on display. We recorded 249 bird species, of which 149 are not native to Thailand. Bird species diversity was positively correlated with mammal species diversity but not with the entry ticket price, the Gross Domestic Product of the province in which the zoo was based, or the size of the zoo. Diversity did differ significantly between zoo types (accredited, government and private zoos). There was a clear difference in the proportion of native and non-native species between zoos, with private zoos containing the highest number of non-native species, which may be related to the licensing status of these zoos. The composition of bird species in Thai zoos appears to be largely driven by their availability, the legal status for keeping them and serendipity. The conservation status seems to be of minor importance, contradicting the typical role of a zoo. To be considered global conservation players, zoos in countries of high species diversity, such as Thailand, have the unique opportunity to provide breeding programmes for some of the rarest species, yet they must improve their collection management plans to focus on such aims.

Analytical and biological validation of a noninvasive measurement of glucocorticoid metabolites in feces of Geoffroy's spider monkeys (Ateles geoffroyi).

We report on an analytical and biological validation of a commercial cortisol enzyme immunoassay (EIA)to measure glucocorticoids (GC)in feces of Geoffroy's spider monkeys (Ateles geoffroyi). Validation of endocrinological methods for each sample matrix and study species is crucial to establish that the methods produce reliable results. For the analytical validation of the EIA, we assessed parallelism, accuracy, and precision. We carried out a biological validation based on three well-studied GC patterns with the following predictions: (1) increased fecal GC metabolite (fGCM)concentrations after veterinary intervention; (2) increased fGCM concentrations during early morning hours; and (3) higher fGCM concentrations during gestation than in other female reproductive states. For the first prediction, we sampled feces of two zoo-housed females 2 days before, the day of, and 2 days after a veterinary intervention. For the second prediction, we analyzed 284 fecal samples collected from 12 wild males using a linear mixed model (LMM).For the third prediction, we analyzed 269 fecal samples of eight wild females using an LMM. Analytical validation revealed that the EIA showed parallelism, was accurate, and precise within each assay. However, there was elevated variation in between-assay precision. The biological validation supported all predictions: (1) the two zoo-housed females showed a substantial increase in fGCM concentrations 2.5and 11 h after veterinary intervention; (2) there was a negative effect of sample collection time on fGCM concentrations (i.e., higher concentrations during early morning); (3) gestating females had significantly higher fGCM concentrations than lactating females. Thus, we analytically validated the commercial EIA and, despite between-assay variation, we were able to find three biologically relevant GC signals in captive and wild settings, and in males and females. We are therefore confident that the method can be used to noninvasively address behavioral endocrinology questions in Geoffroy's spider monkeys.

Advances in biologging can identify nuanced energetic costs and gains in predators.

Foraging is a key driver of animal movement patterns, with specific challenges for predators which must search for mobile prey. These patterns are increasingly impacted by global changes, principally in land use and climate. Understanding the degree of flexibility in predator foraging and social strategies is pertinent to wildlife conservation under global change, including potential top-down effects on wider ecosystems. Here we propose key future research directions to better understand foraging strategies and social flexibility in predators. In particular, rapid continued advances in biologging technology are helping to record and understand dynamic behavioural and movement responses of animals to environmental changes, and their energetic consequences. Data collection can be optimised by calibrating behavioural interpretation methods in captive settings and strategic tagging decisions within and between social groups. Importantly, many species' social systems are increasingly being found to be more flexible than originally described in the literature, which may be more readily detectable through biologging approaches than behavioural observation. Integrating the effects of the physical landscape and biotic interactions will be key to explaining and predicting animal movements and energetic balance in a changing world.

Unexpected appetitive events promote positive affective state in juvenile European sea bass

Some animal species exhibit considerable physiological and behavioural alterations in response to captivity. It has been hypothesized, but rarely tested, that such changes reflect a negative affective state that is associated to this specific context. In the last years, judgement bias measures have emerged as reliable indicators of animal affective state, under the assumption that individuals in a negative affective state are more likely to evaluate ambiguous stimuli as negative and display therefore pessimistic behaviours. Here, we have developed a judgement bias task for juvenile European sea bass (Dicentrarchus labrax) aiming to measure optimism/pessimism in this marine species, which have previously been reported to show important dysregulations in captive settings. Our results show that juvenile sea bass exhibit a considerable bias towards pessimistic behaviours in laboratory settings. Furthermore, juveniles that received an unexpected positive event during the judgement bias test displayed more optimistic responses toward ambiguous stimuli as compared to control fish, indicating a positive change in their affective state induced by the appetitive experience. These results reveal a direct interaction of the internal affective state with decision-making processing under ambiguity in juvenile European sea bass, highlighting therefore the potential of judgement bias tests as a tool for the advancement and improvement of our understanding of welfare in finfish aquaculture.

Diet-related factors strongly shaped the gut microbiota of Japanese macaques.

Although knowledge of the functions of the gut microbiome has increased greatly over the past few decades, our understanding of the mechanisms governing its ecology and evolution remains obscure. While host genetic distance is a strong predictor of the gut microbiome in large-scale studies and captive settings, its influence has not always been evident at finer taxonomic scales, especially when considering among the recently diverged animals in natural settings. Comparing the gut microbiome of 19 populations of Japanese macaques Macaca fuscata across the Japanese archipelago, we assessed the relative roles of host genetic distance, geographic distance and dietary factors in influencing the macaque gut microbiome. Our results suggested that the macaques may maintain a core gut microbiome, while each population may have acquired some microbes from its specific habitat/diet. Diet-related factors such as season, forest, and reliance on anthropogenic foods played a stronger role in shaping the macaque gut microbiome. Among closely related mammalian hosts, host genetics may have limited effects on the gut microbiome since the hosts generally have smaller physiological differences. This study contributes to our understanding of the relative roles of host phylogeography and dietary factors in shaping the gut microbiome of closely related mammalian hosts.

Environmental DNA‐based detection of pathogens in trade and captive settings: Best practices and validation for Batrachochytrium salamandrivorans

Abstract Detecting pathogens in the live animal trade is critical for tracking and preventing their movement, introduction and spillover into susceptible fauna. However, the scale of the live animal trade makes individually testing animals infeasible for all but the most economically important taxa. For instance, while the fungal pathogen, Batrachochytrium salamandrivorans (Bsal), threatens amphibian, particularly caudate diversity, in Europe and the Americas, screening even a fraction of the millions of live amphibians imported into the United States, alone, is impractically laborious and expensive. A promising alternative to individual‐level sampling (e.g. swabbing the skin of salamanders) is to instead collect DNA from the animals' environment (e.g. housing container or water) which allows us to screen a whole group of animals at a time. We used a series of experiments with Bsal‐spiked water and substrates and experimentally infected rough‐skinned newts (Taricha granulosa) to determine which methods yield the most Bsal environmental DNA (eDNA) and evaluate the capacity of these methods to detect Bsal‐infected animals in conditions found in captive settings and trade. We found that filtering water housing infected animals for even an hour can consistently recover detectable levels of Bsal eDNA, that there is little evidence of Bsal eDNA being clumped in housing containers or swamped or inhibited by dirty housing containers, and that eDNA‐based methods achieves an equivalent or higher chance of detecting Bsal infections in a (virtual) population of co‐housed newts with fewer samples than individual swabs. By sampling the genetic materials accumulated from a whole group of animals, eDNA‐based methods are a powerful means of detecting pathogens, such as Bsal, in shipments and captive populations. These methods bring routine pathogen surveillance into reach in many more contexts and can thus be an important tool in conservation and disease control.

Measurement of Salivary Cortisol in Two New World Primate Species.

Glucocorticoids (GCs) are mammalian steroid hormones involved in a variety of physiological processes, including metabolism, the immune response, and cardiovascular functions. Due to their link to the physiological stress response, GC measurement is a valuable tool for conservation and welfare assessment in animal populations. GC levels can be measured from different matrices, such as urine and feces. Moreover, especially in captive settings, measuring GCs from saliva samples proved particularly useful as those samples can be collected non-invasively and easily from trained animals. Salivary GC levels can be measured using a variety of analytical methods, such as enzyme immunoassays. However, it is crucial to validate the analytical method for each specific application and species when using a new matrix. Using high-pressure liquid chromatography and a cortisol enzyme immunoassay, we show that the main glucocorticoids secreted in the saliva of squirrel monkeys and brown capuchin monkeys are cortisol and cortisone. Our biological validation found the expected salivary cortisol level to decline throughout the day. Our findings support the reliability of salivary cortisol measurements and their potential to be used as a valid tool in research and welfare assessment for these non-human primates.