Species differences in responses to captivity: stress, welfare and the comparative method

Approximately 26 billion animals, spanning over 10 000 species, are kept on farms and in zoos, conservation breeding centers, research laboratories and households. Captive animals are often healthier, longer-lived and more fecund than free-living conspecifics, but for some species the opposite is true. Captivity is a very long way from the ideal 'common garden' often assumed by evolutionary and ecological researchers using data for captive animals. The use of comparative methods to investigate the fundamental biological causes of these species differences would help to improve husbandry and enclosure design, and might even reveal relationships between susceptibilities to poor captive welfare and susceptibilities to anthropogenic threat in the wild. Studies of these species differences could also inspire and facilitate 'evo-mecho' research into the functions of behavioral control mechanisms.     

Captive Breeding Does Not Alter Brain Volume in a Marsupial Over a Few Generations

Captive breeding followed by reintroduction to the wild is a common component of conservation management plans for various taxa. Although it is commonly used, captive breeding can result in morphological changes, including brain size decrease. Brain size reduction has been associated with behavioral changes in domestic animals, and such changes may negatively influence reintroduction success of captive‐bred animals. Many marsupials are currently bred in captivity for reintroduction, yet the impacts of captive breeding on brain size have never been studied in this taxa. We investigated the impacts of a few generations (2–7) of captive breeding on brain volume in the stripe‐faced dunnart (Sminthopsis macroura), and found that captive breeding in a relatively enriched environment did not cause any changes in brain volume. Nonetheless, we advocate that great care be taken to provide suitable husbandry conditions and to minimize the number of captive generations if marsupial reintroduction programs are to be successful. Zoo Biol 31:82;–86, 2012. © 2011 Wiley Periodicals, Inc.     

Environmental enrichment to address behavioral differences between wild and captive black-and-white ruffed lemurs (Varecia variegata)

I compared the behaviors of wild Varecia variegata living in a Malagasy rain forest with those of caged groups living in zoos in the United Kingdom in order to design environmental enrichment to encourage more natural behaviors. Comparisons were made between wild and captive animals in terms of activity budgets (instantaneously sampled at 1-min intervals) and social and solitary behaviors, which were continuously recorded for focal individuals. I followed the same sampling protocol during behavioral enrichment experiments, with additional monitoring of the amount and type of food consumed, and with more detailed observations of feeding behavior. No significant differences were found in resting or moving between wild and captive V. variegata. However, captive V. variegata spent more time on self-grooming and social behaviors, and less time feeding than wild V. variegata. There was also a lack of manual manipulation of food items. Behavioral enrichment experiments were carried out in which whole rather than chopped fruit was provided and presented in a more naturalistic manner. With this method of dietary presentation, manual manipulation of dietary items increased. Time spent feeding also increased significantly. Captive conservation breeding programs should not be wholly concerned with maintaining a diverse gene pool-they should also be concerned with conserving species-typical behaviors, especially if they are to produce behaviorally intact captive animals that can be reintroduced to the wild with minimal training, financial resources, and loss of individuals.     

Captive breeding of pangolins: current status,problems and future prospects

Pangolins are unique placental mammals with eight species existing in the world, which have adapted to a highly specialized diet of ants and termites, and are of significance in the control of forest termite disaster. Besides their ecological value, pangolins are extremely important economic animals with the value as medicine and food. At present, illegal hunting and habitat destruction have drastically decreased the wild population of pangolins, pushing them to the edge of extinction. Captive breeding is an important way to protect these species, but because of pangolin’s specialized behaviors and high dependence on natural ecosystem, there still exist many technical barriers to successful captive breeding programs. In this paper, based on the literatures and our practical experience, we reviewed the status and existing problems in captive breeding of pangolins, including four aspects, the naturalistic habitat, dietary husbandry, reproduction and disease control. Some recommendations are presented for effective captive breeding and protection of pangolins.     

Conservation and behavioral neuroendocrinology

The total number of threatened species of vertebrates is likely to be more than 10,000, with approximately one quarter of the world's mammal species, one eighth of the birds and one third of the amphibians threatened with extinction. The rate of loss of animal species and hence of biodiversity is increasing and may become even greater as ecosystems become affected by climate change due to global warming. Behavioral neuroendocrinology, which considers interactions between behavior and neuroendocrine function in animals from all vertebrate taxa, can contribute to animal conservation. Research with laboratory animals can address questions in basic biology relevant to conservation and develop methods for use with threatened animals. Field work with free-living animals considers the basic biology of new species and the use of endocrine tools to assess the susceptibility of species to threats. Non-invasive measurements of hormone concentrations, especially fecal steroids, are extensively used to assess reproductive function and the stress status of animals in captive breeding programs and in the wild. Biodiversity and natural selection both depend on individual variation, and conservation programs often work with animals on an individual basis. The consideration of data from individuals is essential in conservation endocrinology. Direct contributions to conservation programs are challenging as study situations are determined by practical conservation concerns. Indirect contributions such as the provision of scientific input to conservation plans and participation in public education programs offer significant benefits for conservation programs. Directly and indirectly, there are many opportunities for behavioral neuroendocrinologists to contribute to conservation.     

Effects of odors on behaviors of captive Amur leopards Panthera pardus orientalis

Captive environments often fail to resemble the wild environment in respects of limited space,unchanging habitat,lack of stimulus and contingency. Common animal welfare problems which occur in captive animals include low behavioral diversity,abnormal behavior and excessive inactivity. Environmental enrichment,as an effective strategy to tackle these problems and promote mental health of captive animals,has been recognized as an important principal for captive animal management. Among all the enrichment techniques,olfactory enrichment is a simple and effective method for improving the well-being of the olfactory sensitive felids. Behavioral problems were observed in six Amur leopards Panthera pardus orientalis at Beijing Zoological Garden.These were held in the older type exhibits which have now been rebuilt. These behaviors include stereotypic behavior and excessive inactivity caused by the spatially limited enclosures with low levels of stimuli. To determine the effects of predator,prey,and herb odors as potential enrichment materials for captive leopards,we conducted olfactory enrichment experiments for the leopards and tested the effects of nutmeg Myristica fragrans,feces of roe deer Capreolus capreolus and urine of Amur tiger Panthera tigrisaltaica to test for an increase in behavioral repertoire and activity. Odors provided in this study were also believed to improve the psychological and physiological health of individuals. To standardize the method of presentation the odors were introduced to the enclosures by rubbing or spraying onto a clean towel. Our results show that the selected three odors effectively increased the behavioral diversity. Ten new behavior types were observed in the nutmeg experiment,eight in the feces of roe deer experiment and six in the tiger urine experiment. Among the three odors,cats responded to nutmeg for the longest duration,followed by tiger urine and feces of roe deer. Leopards showed more play behavior in presence of nutmeg while more investigatory behavior in presences of feces of roe deer and tiger urine. Providing novel odors increased the spatial use of the exhibit and the animal' s increased use of the logs,sleeping platforms and bars in the cages. Novel odors also significantly increased the overall activity of the leopards,but the effects were diminished in about three hours.     

Long-term captive breeding does not necessarily prevent reestablishment: lessons learned from Eagle Lake rainbow trout

Captive breeding of animals is often cited as an important tool in conservation, especially for fishes, but there are few reports of long-term (<50 years) success of captive breeding programs, even in salmonid fishes. Here we describe the captive breeding program for Eagle Lake rainbow trout, Oncorhynchus mykiss aquilarum, which is endemic to the Eagle Lake watershed of northeastern California. The population in Eagle Lake has been dependent on captive breeding for more than 60 years and supports a trophy fishery in the lake. Nevertheless, the basic life history, ecological, and genetic traits of the subspecies still seem to be mostly intact. Although management has apparently minimized negative effects of hatchery rearing, reestablishing a wild population would ensure maintenance of its distinctive life history and its value for future use as a hatchery fish. An important factor that makes reestablishment possible is that the habitat in Eagle Lake is still intact and that Pine Creek, its major spawning stream, is recovering as habitat. With the exception of an abundant alien brook trout (Salvelinus fontinalis) population in Pine Creek, the habitat factors that led to the presumed near-extinction of Eagle Lake rainbow trout in the early twentieth century have been ameliorated, although the final stages of reestablishment (eradication of brook trout, unequivocal demonstration of successful spawning migration) have still not been completed. The Eagle Lake rainbow trout story shows that long-term captive breeding of migratory salmonid fishes does not necessarily prevent reestablishment of wild populations, provided effort is made to counter the effects of hatchery selection and that natural habitats are restored for reintroduction. Long-term success, however, ultimately depends upon eliminating hatchery influences on wild-spawning populations. Extinction of Eagle Lake rainbow trout as a wild species becomes increasingly likely if we fail to act boldly to protect it and the Eagle Lake watershed.     

Effects of captivity,diet, and relocation on the gut bacterial communities of white‐footed mice

Microbes can have important impacts on their host's survival. Captive breeding programs for endangered species include periods of captivity that can ultimately have an impact on reintroduction success. No study to date has investigated the impacts of captive diet on the gut microbiota during the relocation process of generalist species. This study simulated a captive breeding program with white‐footed mice (Peromyscus leucopus) to describe the variability in gut microbial community structure and composition during captivity and relocation in their natural habitat, and compared it to wild individuals. Mice born in captivity were fed two different diets, a control with dry standardized pellets and a treatment with nonprocessed components that reflect a version of their wild diet that could be provided in captivity. The mice from the two groups were then relocated to their natural habitat. Relocated mice that had the treatment diet had more phylotypes in common with the wild‐host microbiota than mice under the control diet or mice kept in captivity. These results have broad implications for our understanding of microbial community dynamics and the effects of captivity on reintroduced animals, including the potential impact on the survival of endangered species. This study demonstrates that ex situ conservation actions should consider a more holistic perspective of an animal's biology including its microbes.     

Behavioral responses of maned wolves (Chrysocyon brachyurus, Canidae) to different categories of environmental enrichment stimuli and their implications for successful reintroduction

The maned wolf (Chrysocyon brachyurus, Illiger, 1815, Canidae) is a threatened species that inhabits the cerrados of Brazil, Argentina, Peru, Bolivia, Paraguay, and Uruguay. Captive maned wolves could be potentially used in reintroduction programs for species conservation; however, it is necessary that their behavior and cognitive abilities are conserved. Environmental enrichment is a tool used to stimulate captive animals and maintain a natural behavioral repertoire. To compare the variation of captive maned wolves' behavioral responses to environmental enrichment, we studied three maned wolves held by Belo Horizonte Zoo, Brazil. Foraging, interspecific, and intraspecific stimuli were offered to the animals and their responses were compared with a baseline and postenrichment treatments. The test was used to help in choosing which one of the three individuals would participate in a reintroduction project. The results showed that stimuli type did influence the animal's responses, and that individually wolves responded differently to foraging, interspecific, and intraspecific enrichment items (P80.05 for some behaviors in each enrichment category). The individual's personality seemed to influence their behavioral responses, with animals showing bold and shy responses, and this trait should be considered during decision makings for reintroduction.     

Stereotypies and other abnormal repetitive behaviors: potential impact on validity, reliability, and replicability of scientific outcomes

Normal behavior plays a key role in facilitating homeostasis, especially by allowing the animal to control and modify its environment. Captive environments may interfere with these behavioral responses, and the resulting stress may alter many physiological parameters. Abnormal behaviors indicate that an animal is unable to adjust behaviorally to the captive environment and, hence, may be expressing abnormal physiology. Therefore, captive environments may affect the following aspects of an experiment: validity, by introducing abnormal animals into experiments; reliability, by increasing interindividual variation through the introduction of such individuals; and replicability, by altering the number and type of such individuals between laboratories. Thus, far from increasing variability, enrichment may actually improve validity, reliability, and replicability by reducing the number of abnormal animals introduced into experiments. In this article, the specific example of abnormal repetitive behaviors (ARBs) is explored. ARBs in captive animals appear to involve the same mechanisms as ARBs in human psychiatry, which reflect underlying abnormalities of brain function. ARBs are also correlated with a wide range of behavioral changes that affect experimental outcomes. Thus, ARBs in laboratory animals may compromise validity, reliability, and replicability, especially in behavioral experiments; and enrichments that prevent ARB may enhance validity, reliability, and replicability. Although many links in this argument have been tested experimentally, key issues still remain in the interpretation of these data. In particular, it is currently unclear (1) whether or not the differences in brain function seen in animals performing ARB are abnormal, (2) which common behavioral paradigms are affected by ARB, and (3) whether enrichment does indeed improve the quality of behavioral data. Ongoing and future work addressing these issues is outlined.     

育幼经历对圈养成年雌性大熊猫尿液皮质醇含量的影响

为研究育幼期不同的育幼方式对圈养成年雌性大熊猫Ailuropoda melanoleuca福利状况的影响情况,了解圈养育幼模式可能引发成年雌性大熊猫的应激问题,完善育幼期大熊猫的饲养管理和兽舍参数设计,提高育幼过程中圈养大熊猫福利状况,选择成都大熊猫繁育研究基地育幼期采取不同育幼方式管理的成年雌性大熊猫为研究对象,利用...     

Captive care and welfare considerations for beavers

Beavers (Castor spp.) tend not to be a commonly held species and little published material exists relating to their captive care. We review published material and discuss husbandry issues taking into account the requirements of wild beavers. As social mammals with complex chemical communication systems and with such an ability to modify their environments, studies of wild counterparts suggest the captive requirements of beavers may actually be more sophisticated than generally perceived. Common field techniques may have practical application in the captive setting. Their widespread utilisation in conservation, including reintroductions, translocations and habitat management, also requires components of captive care. As welfare science advances there is increasing pressure on captive collections to improve standards and justify the keeping of animals. Conservation science is increasingly challenged to address individual welfare standards. Further research focusing on the captive care of beavers is required. Zoo Biol. 34:101–109, 2015. © 2015 The Authors. Zoo Biology published by Wiley Periodicals, Inc.     

Encouraging natural feeding behavior in captive-bred black and white ruffed lemurs (Varecia variegata variegata)

Captive breeding of endangered species is commonly proposed as a means of conserving biodiversity. The suggestion is that captive populations can be built up to provide individuals to reinforce or re-establish wild populations. However, there is evidence to suggest that captive-bred animals lack the skills necessary for survival in their natural habitat. This research was designed to assess whether a group of captive-bred Varecia variegata variegata exhibit such behavioral deficiencies in relation to feeding behavior compared to two wild groups. A further aim was to determine which of four methods of food presentation and two captive environments were most effective in encouraging the exhibition of natural feeding behavior. An identical focal animal, instantaneous time-sampling technique was used to collect data from the wild groups in the Betampona Reserve, Madagascar, and the captive group at Chester, UK. Results from Betampona confirm the highly frugivorous and arboreal nature of V. v. variegata. Under all captive conditions, except the rooftop feed in the cage environment, the captive V. v. variegata spent significantly less time feeding than their wild conspecifics. Suspensory feeding postures are an important adaptation enabling wild V. v. variegata to harvest fruit in the small-branch setting. Similar frequencies of use of such postures to those observed at Betampona were most effectively encouraged among captive V. v. variegata in the cage environment by the rooftop food presentation method and on a naturalistic island exhibit by the suspended method of food presentation. Differences in feeding behavior between the wild and captive V. v.variegata can be explained in terms of structural differences between their environments. As naturalistic captive environments allow lemurs to experience the challenges associated with feeding in the wild, it is strongly recommended that zoos endeavor to provide them with such conditions. Zoo Biol 17:379–392, 1998. © 1998 Wiley-Liss, Inc.     

Effect of new founders on retention of gene diversity in captive populations: A formalization of the nucleus population concept

A nucleus population is a small captive population genetically supported by periodic importation of wild caught animals. Periodic importation will allow nucleus populations to maintain the same amount of gene diversity as larger captive populations that do not import wild caught animals. The function of nucleus populations as envisioned by the IUCN/SSC Captive Breeding Specialist Group (CBSG) is to make additional captive space available for endangered taxa not currently maintained in captivity. In this article, mathematical models are developed to assess the effectiveness of the nucleus population concept in reducing the population sizes necessary to maintain appreciable amounts of gene diversity in captive populations. It is shown that the Nucleus I population concept, as defined and promoted by the CBSG, requires an importation rate 10–20 times greater than they have indicated. Whereas nucleus populations are not appropriate for maintenance of significant amounts of gene diversity in long-term breeding programs, small populations can be valuable for research, education, and reintroduction projects with short-term goals. Decisions have to be made on which of the many endangered taxa will be maintained and for what purposes, if captive breeding is to be an effective component of species conservation. © 1993 Wiley-Liss, Inc.     

Killing of experimental rabbits with captive bolt guns according to animal welfare regulations]

Captive bolt guns for small animals could be used for killing rabbits quickly with little alterations of tissue caused by agony. The application is acceptable for animal welfare if the captive bolt gun is placed on the head between the base of the ears and the rabbit is bled dry by cutting a large artery immediately after the shooting.     

Conservation breeding programmes: an important ingredient for species survival

Captive populations for the primary purpose of securing the survival of species through stable self-sustaining populations need to be founded and managed according to sound scientific principles. Given the current rate of habitat fragmentation and its effect on animal populations, species conservation over the long term increasingly will require management to reduce risk of extinction. This may include ex situ populations which can support and interact demographically and genetically with wild populations. This paper presents a review of what can be achieved through a multidisciplinary approach, involving science, interactive management, politics, environmental education, habitat preservation and habitat restoration. Examples of what conservation-oriented breeding programmes have contributed to date, what represents a viable population and what is meant by effective conservation are provided, and various scenarios for the future are discussed.     

Propagation of endangered birds in US institutions: How much space is there?

Captive breeding is often touted as a way to preserve species disappearing in the wild. Zoos and related institutions have limited space for animals, however, and use of what space exists may be restricted by conflicting demands of entertainment, education, and propagation. Curators of US bird collections sponsored an analysis of space available for long-term captive management. Seventy-three collections responded to a survey, providing data on 3,174 exhibits and holding areas under their control. The most optimistic analysis indicates room for fewer than 141 long-term management programs. To use space resources optimally for conservation, there is a strong need to develop priorities within management groups. New models and strategies for using captive propagation as a short-term tool to bolster wild populations should be created. Immediate attention should be paid to the most effective and efficient ways of improving husbandry and management techniques for birds. © 1995 Wiley-Liss, Inc.     

Thirty years after Brambell: whither animal welfare science?

It has been just over 30 years since the Brambell Committee issued its clarion call for research on the welfare of animals used in agriculture. What progress has farm animal welfare science made in those 30 years, and what challenges will it face in the next 30? In this article, I discuss the ways in which the Brambell report, with its emphasis on behavioral needs and suffering, both propelled and constrained the development of animal welfare science. The role that economic factors play and the ways in which they have imposed other kinds of constraints on scientists working with farm animals are also mentioned. Despite these constraints, animal welfare science has contributed to a number of significant improvements in the welfare of farm animals. There is, however, a growing sense that animal welfare science has reached an impasse and that ethical and scientific questions about animal welfare have become hopelessly entangled. In this context, I address what I view to be the principal challenge facing farm animal welfare science, namely to move the issue of beyond suffering to an evaluation of broader quality-of-life questions and their application to improvements in welfare.     

Improving the Welfare of a Zoo-Housed Male Drill (Mandrillus leucophaeus poensis) Aggressive Toward Visitors

Improving the welfare of nonhuman animals in captivity and maintaining behavioral competence for future conservation purposes is of the highest priority for zoos. The behavior of an aggressive male drill (Mandrillus leucophaeus poensis) was assessed in Barcelona Zoo. The 2-year study presented in this article examined the effects of introducing changes in the exhibit of the drill to improve his welfare by analyzing scan behaviors. First, a partial visual barrier was applied and proved to be insufficient to decrease the long-term stress indicators assessed. Next, a feeding enrichment program was implemented. The results supported the hypothesis that feeding and explorative activities would increase, whereas apathetic and stereotypic behaviors would decrease. However, visitor-directed aggression did not vary, indicating that more profound structural modifications were needed to reduce the negative impact of the agonistic interactions between the drill and the public. The study emphasized the usefulness of environmental enrichment evaluations in assessing captive animal welfare.     

Unique multiple paternity in the endangered big‐headed turtle (Platysternon megacephalum) in an ex situ population in South China

Understanding the mating system and reproductive strategies of an endangered species is critical to the success of captive breeding. The big‐headed turtle (Platysternon megacephalum) is one of the most threatened turtle species in the world. Captive breeding and reintroduction are necessary to re‐establish wild populations of P. megacephalum in some of its historical ranges in China, where the original populations have been extirpated. However, the captive breeding of P. megacephalum is very difficult and this may be due to its mysterious reproductive strategies and special behavior (e.g., aggressive temperament and territoriality). In this study, we achieved successful captive breeding of P. megacephalum by creating a habitat that mimics natural conditions and then investigated its mating system using microsatellite makers. A total of 16 clutches containing 79 eggs of P. megacephalum were collected, and 52 were hatched successfully over two breeding seasons. Of the 15 effective clutches, 6 clutches (40%) exhibited multiple paternity. There was no significant correlation between clutch size and multiple paternity, and no significant difference in hatching success between multiple‐sired and single‐sired clutches. However, there was significant correlation between male body size and the number of offspring, with higher‐ranked males contributing to more clutches. Our results provide the first evidence of multiple paternity and male hierarchy in P. megacephalum. These findings suggest that multiple paternity and male hierarchy should be considered in captive breeding programs for P. megacephalum, and creating a habitat that mimics natural conditions is an effctive way to achieve successful captive breeding and investigate the mating systems of this species.