Captive Settings Research Articles

Captivity Is Associated With Gut Mycobiome Composition in Tibetan Macaques (Macaca thibetana).

Although recent studies have revealed that gut fungi may play an important functional role in animal biology and health, little is known concerning the effects of anthropogenic pressures on the gut mycobiome. Here, we examined differences of the gut mycobiome in wild and captive populations of Tibetan macaques (Macaca thibetana) targeting the fungal internal transcribed spacer (ITS) and using next generation sequencing. Our findings demonstrate that the diversity, composition, and functional guild of the Tibetan macaque gut mycobiome differ across populations living in different habitats. We found that Tibetan macaques translocated from the wild into a captive setting for a period of 1 year, were characterized by a reduction in fungal diversity and an increase in the abundance of potential gut fungal pathogens compared to wild individuals. Furthermore, we found that the relative abundance of two main fungal guilds of plant pathogens and ectomycorrhizal fungi was significantly lower in captive individuals compared to those living in the wild. Our results highlight that, in addition to bacteria, gut fungi vary significantly among individuals living in captive and wild settings. However, given limited data on the functional role that fungi play in the host’s gut, as well as the degree to which a host’s mycobiome is seeded from fungi in the soil or ingested during the consumption of plant and animal foods, controlled studies are needed to better understand the role of the local environment in seeding the mycobiome.

Target Training Juvenile False Water Cobras (Hydrodynastes gigas)

Because all animals have the capacity to learn through operant conditioning and other types of learning, zoos and other animal care facilities have shifted towards the utilization of positive reinforcement training to shape the behavior of animals in captivity. Training provides animals the choice to participate in their own husbandry routines and veterinary procedures. While the adoption of these practices has improved the welfare of animals in human care, it has not been applied equally across taxa. Snakes are often overlooked in the discussion of choice and control in a captive setting, likely due to the historical misinterpretation of their intelligence and needs. In general, there is an overall lack of documentation of reptile training. In this study, a shaping plan was developed for juvenile false water cobras (Hydrodynastes gigas), a rear-fanged venomous species. Using behavioral approximations, snakes were rewarded with food when completing behaviors related to the ultimate goal of willingly entering a shift container. At this point in the training process, all snakes have made significant progress towards reliably performing this behavior. The purpose of this project is to use the trained behaviors to allow for routine husbandry practices, such as enclosure cleaning and weighing, while preventing unnecessary stress in the snakes, as well as risk to the keeper.

Leveraging Social Learning to Enhance Captive Animal Care and Welfare

From ants to zebras, animals are influenced by the behavior of others. At the simplest level, social support can reduce neophobia, increasing animals’ exploration of novel spaces, foods, and other environmental stimuli. Animals can also learn new skills more quickly and more readily after observing others perform them. How then can we apply animals’ proclivity to socially learn to enhance their care and welfare in captive settings? Here, I review the ways in which animals (selectively) use social information, and propose tactics for leveraging that to refine the behavioral management of captive animals: to enhance socialization techniques, enrichment strategies, and training outcomes. It is also important to consider, however, that social learning does not always promote the uniform expression of new behaviors. There are differences in animals’ likelihood to seek out or use socially provided information, driven by characteristics such as species, rank, age, and personality. Additionally, social learning can result in inexact transmission or the transmission of undesirable behaviors. Thus, understanding when, how, and why animals use social information is key to developing effective strategies to improve how we care for animals across settings and, ultimately, enhance captive animal welfare.

Assessing evolutionary processes over time in a conservation breeding program: a combined approach using molecular data, simulations and pedigree analysis

Captive breeding for conservation is widely used to prevent extinction, however these programs face many challenges due to small population size, founder effects, lack of migration and potential adaptation to captivity. Together these influence how selection, genetic drift and gene flow shape the genetic makeup of small populations, so examining these in a captive setting is valuable for appropriate biodiversity management. We have quantified the effects of selection, drift and gene flow in 503 individuals across five generations from the Tasmanian devil insurance population. To determine whether different processes were acting in different settings, we separately analysed animals housed under individual-based management, versus those that were released to an island site. We found that a greater proportion of alleles were lost over time in the smaller island population than in captivity and propose that genetic drift is the most likely process influencing this result. We found that the captive population became more heterozygous over time, while the island population stayed constant. Our molecular measure of inbreeding found a decrease over generations in captivity that is not captured by pedigree-based analysis. As management of breeding interactions only takes place in the captive population, our results are consistent with gene flow through managed breeding in captivity minimising inbreeding over time. Gene flow was also evident through changes to population structure in the captive population. Our findings serve as an example of how conservation managers can assess the impact of evolutionary processes on managed populations and adapt management practices if required.

Chimpanzees' (Pan troglodytes) problem-solving skills are influenced by housing facility and captive care duration.

Although a large body of primate cognition research is done in captive institutions, little is known about how much individuals from different facilities vary in their experiences and cognitive skills. Here we present the results of an experimental study investigating how physical cognitive skills vary between chimpanzees in relation to captive settings and their time in captivity. We tested 59 chimpanzees housed at two different captive facilities (a rehabilitation center (sanctuary) and a zoo) in three problem-solving tasks. Our results showed that chimpanzees at the two housing facilities significantly differed in overall task performance. On average, the sanctuary chimpanzees outperformed the chimpanzees housed at the zoo in the detour reaching task and the honey trap task. However, the zoo chimpanzees performed slightly better on average in the learning task. We propose that, for this particular sample, the documented differences result from a combination of factors, such as prior experience with cognitive testing, motivation levels and varying degrees of human exposure. Within the sanctuary sample, we found that chimpanzees who arrived at an earlier age at the sanctuary and had therefore spent a larger percentage of their lives in a captive environment, were better problem-solvers than those that arrived at a later age to the sanctuary. Thus, rehabilitation and time in captivity contributed to improved physical cognitive skills in sanctuary chimpanzees. Our results highlight the importance of studying intraspecific variation and the effect that previous experience and living conditions might have on physical cognitive skills in non-human apes. Accordingly, we should be cautious when extrapolating findings of cognitive studies from one population to the species as a whole.

Effects of physiological changes and social life events on adrenal glucocorticoid activity in female zoo-housed Asian elephants (Elephas maximus).

Ensuring good health and welfare is an increasingly important consideration for conservation of endangered species and includes breeding of individuals managed under human care. Understanding how factors in the captive environment affect individual animal wellbeing can be aided by long-term monitoring of biological functioning. This study involved longitudinal assessments (4 to 28 years) of reproductive and adrenal hormones in zoo-housed female Asian elephants (Elephas maximus) (age range 4 to ~71 years) to elucidate patterns in adrenal glucocorticoid (GC) activity in association with reproductive and demographic factors, and examine individual response to major social changes. Concentrations of serum and urinary cortisol covaried more consistently with physiological changes (ovarian cycle phase, puberty, pregnancy, lactational anestrus, and age) than with social life events (births, deaths, and facility transfers). Cortisol fluctuated across the ovarian cycle with mean concentrations being higher in the follicular than in the luteal phase, and concentrations were highest in lactational anestrous compared to all other reproductive states. The elephants in this study exhibited substantial individuality in adrenal GC response to major social change, reinforcing the need to assess welfare on an individual basis and to consider factors influencing the impact of perceived stressors, such as social relationships, social support, temperament, and life history. Outcomes from this study deepen our understanding of Asian elephant physiology and highlight the importance of taking intrinsic patterns of hormone secretion into account when evaluating the impact of external factors. Finally, a better understanding of the impact of social change and resiliency in response to real and perceived stressors allows us to improve social management to enhance welfare in both captive settings and free-ranging environments.

Use of Introduction Enclosures to Integrate Multimale Cohorts into Groups of Female Rhesus Macaques (Macaca mulatta).

Integrating animals into a new group is a challenge for both free-ranging and captive adult male rhesus monkeys (Macaca mulatta), and for females in groups receiving new males. To ensure the genetic viability of the population, however, male transfers must occur in both natural and captive settings. To facilitate the introduction of groups of adult males to adult females, we designed a new enclosure that is attached to the outdoor compound where females are housed. Here we describe the construction of 3 introduction enclosures, their use during 4 introductions of groups of adult males to adult females, a brief comparison of introduction success rates associated with the new introduction enclosures with those of our traditional male introduction method, and a critique by the various groups of staff members working with the new enclosures. Overall, the introduction enclosures benefitted both the macaques and the facility personnel and appear to be a useful enhancement to our process of integrating breeding groups.

Behavioral mimicry predicts social favor in adolescent rhesus macaques (Macaca mulatta).

Non-conscious mimicry is a highly conserved component of animal behavior with multifaceted connections to sociality across taxa. One intriguing consequence of this mimicry in primates is that it promotes positive social feedback from the recipient toward the mimicker. This suggests that mimicry in primates may be an important aspect of positive social interaction, but few studies have tracked the consequences of mimicry in naturally occurring complex social conditions. Here, we designed a novel ethogram to characterize mimicry between conspecifics, to better understand whether mimicry is associated with affiliation between primates in a semi-naturalistic captive setting. In this study, 15 juvenile (aged 2-4years) rhesus macaques (Macaca mulatta) were observed at the California National Primate Research Center. Frequencies of mimicry defined a priori (e.g. following, postural mimicry) were observed over a course of 12weeks. In separate observations during the same period, focal social behavior (e.g. aggression, play, affiliation) with group members was also observed. Subjects that exhibited higher degrees of mimicry were not more prosocial, but they received significantly more play overtures from social partners (p < 0.01). Additionally, rates of mimicry were higher in 2- and 3-year-olds than 4-year-olds. These results provide proof of principle in a small sample of monkeys that mimicry is associated with social advantages in a complex, semi-naturalistic setting in primates.

Training fails to elicit behavioral change in a marsupial suffering evolutionary loss of antipredator behaviors

Abstract Attempts to reintroduce threatened species from ex situ populations (zoos or predator-free sanctuaries) regularly fail because of predation. When removed from their natural predators, animals may lose their ability to recognize predators and thus fail to adopt appropriate antipredator behaviors. Recently, northern quolls (Dasyurus hallucatus; Dasyuromorpha: Dasyuridae) conserved on a predator-free “island ark” for 13 generations were found to have no recognition of dingoes, a natural predator with which they had coevolved on mainland Australia for about 8,000 years. A subsequent reintroduction attempt using quolls acquired from this island ark failed due to predation by dingoes. In this study, we tested whether instrumental conditioning could be used to improve predator recognition in captive quolls sourced from a predator-free “island ark.” We used a previously successful scent-recognition assay (a giving-up density experiment) to compare predator-scent recognition of captive-born island animals before and after antipredator training. Our training was delivered by pairing live predators (dingo and domestic dog) with an electrified cage floor in repeat trials such that, when the predators were present, foraging animals would receive a shock. Our training methodology did not result in any discernible change in the ability of quolls to recognize and avoid dingo scent after training. We conclude either that our particular training method was ineffective (though ethically permissible); or that because these quolls appear unable to recognize natural predators, predator recognition may be extremely difficult to impart in a captive setting given ethical constraints. Our results point to the difficulty of reinstating lost behaviors, and to the value of maintaining antipredator behaviors in conservation populations before they are lost.

Evaluation of the Impacts of Radio-Marking Devices on Feral Horses and Burros in a Captive Setting

Evaluation of the Impacts of Radio-Marking Devices on Feral Horses and Burros in a Captive Setting

Deciphering genetic mate choice: Not so simple in group-housed conservation breeding programs.

Incorporating mate choice into conservation breeding programs can improve reproduction and the retention of natural behaviors. However, different types of genetic‐based mate choice can have varied consequences for genetic diversity management. As a result, it is important to examine mechanisms of mate choice in captivity to assess its costs and benefits. Most research in this area has focused on experimental pairing trials; however, this resource‐intensive approach is not always feasible in captive settings and can interfere with other management constraints. We used generalized linear mixed models and permutation approaches to investigate overall breeding success in group‐housed Tasmanian devils at three nonmutually exclusive mate choice hypotheses: (a) advantage of heterozygous individuals, (b) advantage of dissimilar mates, and (c) optimum genetic distance, using both 1,948 genome‐wide SNPs and 12 MHC‐linked microsatellites. The managed devil insurance population is the largest such breeding program in Australia and is known to have high variance in reproductive success. We found that nongenetic factors such as age were the best predictors of breeding success in a competitive breeding scenario, with younger females and older males being more successful. We found no evidence of mate choice under the hypotheses tested. Mate choice varies among species and across environments, so we advocate for more studies in realistic captive management contexts as experimental or wild studies may not apply. Conservation managers must weigh up the need to wait for adequate sample sizes to detect mate choice with the risk that genetic changes may occur during this time in captivity. Our study shows that examining and integrating mate choice into the captive management of species housed in realistic, semi‐natural group‐based contexts may be more difficult than previously considered.

The case for extended lifespan in cooperatively breeding mammals: a re-appraisal.

Recent comparative studies have suggested that cooperative breeding is associated with increases in maximum lifespan among mammals, replicating a pattern also seen in birds and insects. In this study, we re-examine the case for increased lifespan in mammalian cooperative breeders by analysing a large dataset of maximum longevity records. We did not find any consistent, strong evidence that cooperative breeders have longer lifespans than other mammals after having controlled for variation in body mass, mode of life and data quality. The only possible exception to this general trend is found in the African mole-rats (the Bathyergid family), where all members are relatively long-lived, but where the social, cooperatively breeding species appear to be much longer-lived than the solitary species. However, solitary mole-rat species have rarely been kept in captivity or followed longitudinally in the wild and so it seems likely that their maximum lifespan has been underestimated when compared to the highly researched social species. Although few subterranean mammals have received much attention in a captive or wild setting, current data instead supports a causal role of subterranean living on lifespan extension in mammals.

Encounters with Wild, Ecotour, and Captive Marine Mammals: What Do They Tell Us About Human Well-Being and Environmental Behavior?

Nature recreation can be beneficial for human health and well-being, and this article invites discussion about whether environmental behavior nature contact can influence nature contact. As human life becomes more urbanized, people interact less closely with nature, and nature connections are weakened. Tourism provides an opportunity to enhance nature contact, and hence nature connection, and may motivate proenvironmental behavior. This study uses the R statistical package to analyze questionnaire data from 679 participants who have encountered marine mammals in the wild, as part of an ecotour, and in captive settings. It considers the questions: Does a connection to nature mediate the role between nature contact and well-being? Do marine mammal experiences specifically contribute to human well-being and environmental behavior? The role of nature connection as a mediator between nature contact and well-being is described in a structural equation model. Marine mammal experiences are shown to be significantly and positively related to human well-being (three-way ANOVA) and environmental behavior (Kruskal–Wallis H test). We conclude that nature connectedness mediates the effect of nature contact on well-being, and marine mammal experiences have an effect on well-being and environmental behavior. This study adds to research on cetacean experiences by including all marine mammals across different experience types. The results assist identify paths through which recreation time may achieve a two-way benefit of well-being and environmental behavior.

Machine learning goes wild: Using data from captive individuals to infer wildlife behaviours.

1. Remotely tracking distinct behaviours of animals using acceleration data and machine learning has been carried out successfully in several species in captive settings. In order to study the ecology of animals in natural habitats, such behaviour classification models need to be transferred to wild individuals. However, at present, the development of those models usually requires direct observation of the target animals. 2. The goal of this study was to infer the behaviour of wild, free-roaming animals from acceleration data by training behaviour classification models on captive individuals, without the necessity to observe their wild conspecifics. We further sought to develop methods to validate the credibility of the resulting behaviour extrapolations. 3. We trained two machine learning algorithms proposed by the literature, Random Forest (RF) and Support Vector Machine (SVM), on data from captive red foxes (Vulpes vulpes) and later applied them to data from wild foxes. We also tested a new advance for behaviour classification, by applying a moving window to an Artificial Neural Network (ANN). Finally, we investigated four strategies to validate our classification output. 4. While all three machine learning algorithms performed well under training conditions (Kappa values: RF (0.82), SVM (0.78), ANN (0.85)), the established methods, RF and SVM, failed in classifying distinct behaviours when transferred from captive to wild foxes. Behaviour classification with the ANN and a moving window, in contrast, inferred distinct behaviours and showed consistent results for most individuals. 5. Our approach is a substantial improvement over the methods previously proposed in the literature as it generated plausible results for wild fox behaviour. We were able to infer the behaviour of wild animals that have never been observed in the wild and to further illustrate the credibility of the output. This framework is not restricted to foxes but can be applied to infer the behaviour of many other species and thus empowers new advances in behavioural ecology.

A novel method for captive rearing and translocation of juvenile common loons.

Common loons (Gavia immer) are diving waterbirds that are particularly challenging to keep in captivity due to their specific behavioral and physiologic needs, special housing requirements, and susceptibility to stress-related disease. We report a novel method for housing and captive rearing common loon chicks that was developed as part of the first-ever loon translocation effort in southeast Massachusetts,from 2015 to 2017. Thirteen loon chicks were reared in aquatic pens in a natural lake environment, utilizing noninvasive feeding and monitoring techniques that avoided human habituation. Chicks were reared in aquatic pens for 16-28 days before being released onto the lake. All chicks remained clinically normal and were monitored on the lake for up to 4 months following release. At least four of the chicks were subsequently confirmed to have survived to adulthood when they returned to the area in breeding plumage two to 3 years following release. Two of these confirmed adults displayed prolonged territorial pair behavior together, and this is an encouraging early sign that captive-reared individuals may form successful breeding pairs in the future. Because most immature loons remain on the ocean until at least 3 years of age, we expect additional captive-reared loons to return to the release area in subsequent years. These husbandry techniques could be applied to other loon and diving bird species that are notoriously difficult to house in captivity. The novel feeding techniques described here could also be adapted for loon chicks being reared in pools or other traditional captive settings.

For Better, For Worse: Manatee-Associated Tursiocola (Bacillariophyta) Remain Faithful to Their Host.

With the advent of more comprehensive research into the microbiome and interactions between animals and their microbiota, new solutions can be applied to address conservation challenges such as husbandry and medical care of captive animals. Although studies on epizoic algae are relatively rare, and the function and role of those mainly photosynthetic organisms in the animal microbiome is not well understood, recent surveys on epizoic diatoms show that some of them exhibit traits of obligate epibionts. This study explores diatom communities on captive-born manatees from the Africarium in Wroclaw, Poland. Light and scanning electron microscopy analyses revealed that skin of all animals sampled was dominated by apochlorotic Tursiocola cf. ziemanii, an epizoic species described recently from Florida manatees, that reached 99,9% of the total diatom abundance. Despite using media with a wide range of salinity (0-34), the isolated Tursiocola cells did not grow, whereas the normally pigmented Planothidium sp., that was only occasionally found on the animal substratum, survived in all culture media tested. Our observations provide direct evidence that manatee-associated Tursiocola endure the dramatic salinity changes that occur regularly during their host life cycle, and can thrive in an artificial captive setting, if the manatee substratum is available. The impact of practices and routines used by the Africarium on manatee-associated diatoms, as well as ultrastructure of areolae in Tursiocola, are briefly discussed.

Fitness costs associated with ancestry to isolated populations of an endangered species

Habitat fragmentation from urban development leaves species vulnerable to inbreeding depression and genomic erosion. Restoring gene flow can reduce inbreeding and preserve genetic diversity, but a common concern is that genomic incompatibilities may lead to outbreeding depression. The introduction of deleterious genetic load is less commonly considered. The endangered Pacific pocket mouse (Perognathus longimembris pacificus) persists in three isolated populations in southern California. Mitochondrial and microsatellite data indicated that effective population sizes were extremely small (Ne< 50), and continued declines prompted a conservation breeding program founded by individuals from each population. We tracked genetic diversity and individual fitness (measured by reproductive success) in a captive setting over six generations of admixture. Although we observed an increase in fitness in the F1 and F2 generations relative to the founding populations, inbreeding depression alone did not explain the fitness patterns, and outbreeding depression was difficult to rule out as reproductive success waned after F2. However, reproductive success was consistently higher in admixed individuals than founders from Dana Point, the smallest population with the lowest heterozygosity. Across generations, we saw a strong negative correlation between individual reproductive success and ancestry to Dana Point, leading to a rapid decrease of Dana Point alleles. Although the genomic underpinnings remain to be determined, reduced fitness associated with Dana Point ancestry is consistent with high deleterious genetic load in this population, and thus any facilitated migration should be unidirectional. Our findings highlight that, even in the absence of outbreeding depression, there may be a cost to restoration of gene flow if populations harbor high genetic load.

A review of research in primate sanctuaries.

While non-human primate studies have long been conducted in laboratories, and more recently at zoological parks, sanctuaries are increasingly considered a viable setting for research. Accredited sanctuaries in non-range countries house thousands of primates formerly used as subjects of medical research, trained performers or personal pets. In range countries, however, sanctuaries typically house orphaned primates confiscated from illegal poaching and the bushmeat and pet trafficking trades. Although the primary mission of these sanctuaries is to rescue and rehabilitate residents, many of these organizations are increasingly willing to participate in non-invasive research. Notably, from a scientific standpoint, most sanctuaries provide potential advantages over traditional settings, such as large, naturalistic physical and social environments which may result in more relevant models of primates' free-ranging wild counterparts than other captive settings. As a result, an impressive scope of research in the fields of primate behaviour, cognition, veterinary science, genetics and physiology have been studied in sanctuaries. In this review, we examine the range and form of research that has been conducted at accredited sanctuaries around the world. We also describe the potential challenges of sanctuary-based work and the considerations that external researchers may face when deciding to collaborate with primate sanctuaries on their research projects.

Underwater video cameras allow for detection of North American giant salamanders (Cryptobranchus alleganiensis alleganiensis) in both captive and wild streams

Captive propagation and translocation are becoming vital components of conservation and management strategies for Eastern hellbender (Cryptobranchus a. alleganiensis) populations. Zoos, aquaria, universities, and state and federal agencies are concomitantly collaborating on the protection, education, and maintenance of captive populations of this unusual, cryptic salamander. Conservation strategies include the use of artificial nesting structures, collection of eggs from the wild, and head-starting individuals in zoos or hatcheries. The effects of these strategies need to be monitored, however, traditional survey and monitoring methods for the species in the wild involves rock-lifting, which has the potential to both harm habitat and alter reproductive behavior. Therefore, there is a need to develop effective, non-invasive and non-destructive methods of monitoring both wild and captive populations of Eastern hellbenders. Herein, we compare two simple, affordable, underwater video and camera systems (borescope and Aqua-Vu cameras) in their ability to 1) facilitate detection of adults under potential cover items and 2) facilitate nest detection and monitoring in both wild and captive environments. Both cameras were successful in detecting individual hellbender presence, albeit with different resolutions and detection times. The borescope was better at accessing deep cavities given its large flexible attachment which allowed for greater flexibility of scanning crevices of adult shelters. However, search time increased and even low levels of suspended sediment reduced visibility with the borescope. The Aqua-Vu camera provided greater overall visibility and faster detection of individuals under both natural and artificial shelters. There was a significant difference in the amount of time required to detect hellbenders with each camera design when searching under natural rocks (borescope: median = 67.8 s, Aqua-Vu: median = 39.1 s; Kruskal Wallis Test H = 15.62, p < 0.001) and artificial shelters (borescope: median = 30.9 s, Aqua-Vu: median = 13 s; Kruskal Wallis Test H = 25.23, p < 0.0001). We detected 8 natural nests with actively guarding males and only one individual using a wild artificial shelter. We recommend hellbender researchers utilize a combination of underwater video cameras to suit their specific survey goals in both captive and field settings. Moreover, we recommend zoo staff incorporate these methods to not only monitor captive populations but also to potentially record breeding behavior in zoos and aquariums.

Must all signals be evolved? A proposal for a new classification of communicative acts.

While signals in evolutionary biology are usually defined as "acts or traits that have evolved because of their effect on others", work on gestures and vocalizations in various animal taxa have revealed population- or even individual-specific meanings of social signals. These results strongly suggest that communicative acts that are like signals with regard to both form and function (meaning) can also be acquired ontogenetically, and we discuss direct evidence for such plasticity in captive settings with rich opportunities for repeated social interactions with the same individuals. Therefore, in addition to evolved signals, we can recognize invented signals that are acquired during ontogeny (either through ontogenetic ritualization or social transmission). Thus, both gestures and vocalizations can be inventions or innate adaptations. We therefore propose to introduce innate versus invented signals as major distinct categories, with invented signals subdivided into dyad-specific and cultural signals. We suggest that elements of some signals may have mixed origins, and propose criteria to recognize acquired features of signals. We also suggest that invented signals may be most common in species with intentional communication, consistent with their ubiquity in humans, and that the ability to produce them was a necessary condition for the evolution of language. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Linguistics > Evolution of Language Psychology > Comparative Psychology.