The utility of captive animals in actualistic research: A geometric morphometric exploration of the tooth row of Alligator mississippiensis suggesting ecophenotypic influences and functional constraints

Captive broad snouted crocodylians are generally thought to have wider, shorter rostra than their wild counterparts. Interpreted to reflect morphological change in response to the conditions of captivity, this qualitative pattern could affect the utility of these animals in a variety of fields of research. However, due to relative ease of access and availability of life history data, captive animals are often utilized in actualistic research. Thus, this issue should be addressed in more detail. Here we explore snout shape variation between captive and wild members of Alligator mississippiensis using two‐dimensional (2D) morphometric techniques. Several landmark schemesare used to assess the utility of different aspects of morphology in distinguishing the groups. While statistical analyses consistently differentiated between the groups, the area of morphospace occupied by wild members of A. mississippiensis generally overlapped with the larger area encompassing the captive specimens. This indicates that the captive condition is not as uniform as previously thought and instead encompasses a large spectrum of morphologies, ranging from the stereotypical broad, shortened snouts to outlines that are indistinguishable from the wild morphotype. These results align well with the interpretation that this change reflects an extreme example of ecophenotypy, since ranched, farmed, or zoo organisms are held in an array of enclosures, ranging from indoor, climate controlled pens to outdoor, more natural areas. This variation in environments should be reflected in different reactions to the animals' surroundings, resulting in a broad spectrum of morphotypes. While wild specimens are still preferred, especially for fine scale analyses, these results indicate that not all captive members of A. mississippiensis exhibit the extreme morphological alterations often cited in the literature. Weighing the conditions in which the animals are held and exploring the possibility of morphological differences against the benefits of using captive specimens should be part of any actualistic study. J. Morphol. 277:866–878, 2016. © 2016 Wiley Periodicals, Inc.     

Managerial strategies in the captive propagation of endangered species

A captive propagation manager, committed to the welfare of captive populations of exotic animals, must often make decisions that are risky to individual animals. Innovative decisions that place animals at risk are essential to the progress of captive propagation. Such decisions must be grounded thoroughly on peer consultation, the scientific and zoo literature, and where possible on original applied research targeted specifically to the procedure in question. The management of two closely spaced births in a gorilla group is provided as an example.     

Body weights of wild and captive lemurs

The mean body weight of a species is often used as a summary measure of size in evolutionary and functional studies. Additionally, body weight is often used to assess the health of captive animals. Contrasts of the captive and wild body weights of a species can be used to examine the effects of captivity on the species. We provide an analysis of adult body weight in nine taxa of Malagasy lemurs. We compare weights of wild and captive lemurs and provide analyses of relationships between captive weight variation and management actions. Body weights are derived from a number of sources, the majority from the Duke University Primate Center (DUPC) capture and husbandry records. Captive animals are, on average, heavier than wild conspecifics. However, the difference is significant in only three taxa (Hapalemur griseus griseus, Eulemur coronatus, E. macaco flavifrons). Based on a retrospective analysis of DUPC records, we assess patterns of adult weight relative to caging conditions and evaluate changes in mean weight over a period of approximately 20 years. Cage type appears to have no effect on body weight. Mean weight has decreased for some taxa housed at the DUPC over time. We calculate a weight-based criterion for identifying obese animals and demonstrate that obesity is not currently a prevalent condition in DUPC lemurs. Examinations of the physiological correlates of excessive weight, and especially relationships between weight and reproductive success, await further analysis. These analyses need to be based, in part, on reliable measures of body weight. We suggest that systematic weighing of wild and captive animals is important for further examinations of the overall health of captive animals as well as for studies ranging in scope from evolutionary to clinical. Zoo Biol 16:17–30, 1997. © 1997 Wiley-Liss, Inc.     

The phenotypic costs of captivity

The breeding of threatened species in captivity for release is a central tool in conservation biology. Given gloomy predictions for biodiversity trends in the Anthropocene, captive breeding will play an increasingly important role in preventing future extinctions. Relative to the wild, captive environments drastically alter selection pressures on animals. Phenotypic change in captive animals in response to these altered selection pressures can incur fitness costs post-release, jeopardising their potential contribution to population recovery. We explore the ways in which captive environments can hinder the expression of wild phenotypes. We also stress that the phenotypes of captive-bred animals differ from their wild counterparts in multiple ways that remain poorly understood. We propose five new research questions relating to the impact of captive phenotypes on reintroduction biology. With better use of monitoring and experimental reintroductions, a more robust evidence base should help inform adaptive management and minimise the phenotypic costs of captivity, improving the success of animal reintroductions.     

Gut microbial ecology of the Critically Endangered Fijian crested iguana (Brachylophus vitiensis): Effects of captivity status and host reintroduction on endogenous microbiomes

Animals often exhibit distinct microbial communities when maintained in captivity as compared to when in the wild. Such differentiation may be significant in headstart and reintroduction programs where individuals spend some time in captivity before release into native habitats. Using 16S rRNA gene sequencing, we (i) assessed differences in gut microbial communities between captive and wild Fijian crested iguanas (Brachylophus vitiensis) and (ii) resampled gut microbiota in captive iguanas released onto a native island to monitor microbiome restructuring in the wild. We used both cloacal swabs and fecal samples to further increase our understanding of gut microbial ecology in this IUCN Critically Endangered species. We found significant differentiation in gut microbial community composition and structure between captive and wild iguanas in both sampling schemes. Approximately two months postrelease, microbial communities in cloacal samples from formerly captive iguanas closely resembled wild counterparts. Interestingly, microbial communities in fecal samples from these individuals remained significantly distinct from wild conspecifics. Our results indicate that captive upbringings can lead to differences in microbial assemblages in headstart iguanas as compared to wild individuals even after host reintroduction into native conditions. This investigation highlights the necessity of continuous monitoring of reintroduced animals in the wild to ensure successful acclimatization and release.     

Primates got personality,too: Toward an integrative primatology of consistent individual differences in behavior

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free‐ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.     

Individual differences in temperament and behavioral management practices for nonhuman primates

Effective behavioral management plans are tailored to unique behavioral patterns of each individual species. However, even within a species behavioral needs of individuals can vary. Factors such as age, sex, and temperament can affect behavioral needs of individuals. While some of these factors, such as age and sex, are taken into account, other factors, such as an individual's temperament, are rarely specifically provided for in behavioral management plans. However, temperament may affect how animals respond to socialization, positive reinforcement training and other forms of enrichment. This review will examine how individual differences in temperament might affect, or be affected by, behavioral management practices for captive primates. Measuring temperament may help us predict outcome of social introductions. It can also predict which animals may be difficult to train using traditional methods. Further, knowledge of temperament may be able to help identify individuals at risk for development of behavioral problems. Taken together, understanding individual differences in temperament of captive primates can help guide behavioral management decisions.     

Impact of naturally spawning captive-bred Atlantic salmon on wild populations: depressed recruitment and increased risk of climate-mediated extinction

The assessment report of the 4th International Panel on Climate Change confirms that global warming is strongly affecting biological systems and that 20–30% of species risk extinction from projected future increases in temperature. It is essential that any measures taken to conserve individual species and their constituent populations against climate-mediated declines are appropriate. The release of captive bred animals to augment wild populations is a widespread management strategy for many species but has proven controversial. Using a regression model based on a 37-year study of wild and sea ranched Atlantic salmon (Salmo salar) spawning together in the wild, we show that the escape of captive bred animals into the wild can substantially depress recruitment and more specifically disrupt the capacity of natural populations to adapt to higher winter water temperatures associated with climate variability. We speculate the mechanisms underlying this seasonal response and suggest that an explanation based on bio-energetic processes with physiological responses synchronized by photoperiod is plausible. Furthermore, we predict, by running the model forward using projected future climate scenarios, that these cultured fish substantially increase the risk of extinction for the studied population within 20 generations. In contrast, we show that positive outcomes to climate change are possible if captive bred animals are prevented from breeding in the wild. Rather than imposing an additional genetic load on wild populations by releasing maladapted captive bred animals, we propose that conservation efforts should focus on optimizing conditions for adaptation to occur by reducing exploitation and protecting critical habitats. Our findings are likely to hold true for most poikilothermic species where captive breeding programmes are used in population management.     

Fertility assessment: new methods and implications for endangered species

Practical and reliable methods for assessing reproductive status are essential for any work designed to enhance fertility in captive endangered species. This paper described recent advances in the development and application of such methods and their implications for the management of captive breeding. Since non-invasive procedures are necessary when working with animals that are easily stressed, urinary hormone analysis provides the most feasible approach to long term studies on most endangered species. Simplified hormone assay methods have been developed and applied to the detection of ovulation and pregnancy in a variety of animals, including primates, the Giant Panda and ungulates. The possibility now exists for extending the application of these methods to studies in the field. Finally, the ability to monitor reproductive status in endangered animals provides the basis for future attempts to accelerate captive breeding by artificial means.     

Socialization strategies and disease transmission in captive colonies of nonhuman primates

In captive research environments for nonhuman primates (NHP), social housing strategies are often in conflict with protocols designed to minimize disease transmission. This is particularly true in breeding colonies, and is especially relevant when attempting to eliminate specific pathogens from a population of primates. Numerous strategies have been used to establish such specific pathogen free (SPF) breeding colonies (primarily of macaques), ranging from nursery rearing of neonates to single housing of socially reared yearlings to the rearing of infants in large social groups. All these strategies attempt to balance the effects of the chosen socialization strategy on parameters related to disease transmission, including the ultimate elimination of the target pathogens. Such strategies may affect the overall disease states of NHP breeding colonies through selective breeding processes. This can occur either by creating subpopulations of animals that do not have target diseases (SPF colonies), but may have other issues; or by creating situations in which the "best" animals are sold and the breeding colony is stocked with animals that may be more disease susceptible than those that were sold. The disease states of NHP research colonies also may be affected by selective utilization programs, in which animals removed from the breeding colony for health/behavior reasons, are preferentially chosen for use in scientific investigations. Such utilization criteria raise the question of whether ideal subjects are being chosen for use in research. Finally, captive primate colonies, where both socialization and disease states are intensely managed, may provide opportunities for those testing predictions from models of the interactions of socialization and disease transmission in the evolution of wild populations of NHP. This would be especially true for some extreme conditions of these disease ecology models, given the exceedingly high social densities and levels of pathogen control that exist in many captive nonhuman primate colonies.     

Modelling Ex Situ Animal Behaviour and Communication

Communication and behaviour of animals living ex situ has been one of the major sources of knowledge about wild animals. Nevertheless, it is also acknowledged that depending on the environment that the animals inhabit (or are kept in), there are differences in their communication and behaviour. With some species (especially large mammals) it is difficult to reproduce their natural environment to an extent that excludes deviations from the behaviour and communication exhibited by animals living in situ. In zoological gardens, welfare measures are introduced in order to counteract the effects of the captive environment and to grant an individual’s good physical and psychological well-being. The relation between good welfare and species-specific communication and behaviour is discussed, and as a result, a general model of ex situ animal communication and behaviour is proposed. The suggested model is inclusive of differences between captive animals and free-ranging animals and serves to explain the welfare-related reasons underlying individual animal’s deviations from species-specific behaviour and communication.     

Do experiments with captive non-domesticated animals make sense without population field studies? A case study with blue tits' breeding time

A complete understanding of the spatio-temporal variation in phenotypic traits in natural populations requires a combination long-term field studies with experiments using captive animals. Field studies allow the formulation of realistic hypotheses, but have the disadvantage that they do not allow the complete control of many potential confounding variables. Studies with captive animals allow tests of hypotheses that cannot be examined in the field, but have the disadvantage that artificial environments may provoke abnormal behaviour. Long-term studies that follow simultaneously captive and wild bird populations are rare. In a study lasting several years, we show here the unexpected patterns that two populations with a similar breeding time in the wild have non-overlapping breeding times in outdoor aviaries, and that two wild populations separated by a short geographical distance show differences in the expression of natural behaviour in captivity. The experimental design used is exceptional in the sense that the captive populations were held at similar latitudes and altitudes as the wild populations. Our case study shows that studies with captive animals can lead to wrong conclusions if they are carried out without population field studies, and without knowledge of the natural habits and habitats of the species involved. To examine the reliability of experiments with captive animals, comparisons with findings from population field studies are essential.     

Serum concentrations of vitamin D metabolites, vitamins A and E, and carotenoids in six canid and four ursid species at four zoos

Nutritional status for six captive canid species (n=34) and four captive ursid species (n=18) were analyzed. The species analyzed included: African wild dog (Lycaon pictus), arctic fox (Alopex lagopus), gray wolf (Canis lupus), maned wolf (Chrysocyon brachyurus), Mexican wolf (Canis lupus baleiyi), red wolf (Canis rufus), brown bear (Ursus arctos), polar bear (Ursus maritimus), spectacled bear (Tremarctos ornatus), and sun bear (Ursus malayanus). Diet information was collected for these animals from each participating zoo (Brookfield Zoo, Fort Worth Zoo, Lincoln Park Zoological Gardens, and North Carolina Zoological Park). The nutritional composition of the diet for each species at each institution met probable dietary requirements. Blood samples were collected from each animal and analyzed for vitamin D metabolites 25(OH)D and 1,25(OH)(2)D, vitamin A (retinol, retinyl stearate, retinyl palmitate), vitamin E (alpha-tocopherol and gamma-tocopherol) and selected carotenoids. Family differences were found for 25(OH)D, retinol, retinyl stearate, retinyl palmitate and gamma-tocopherol. Species differences were found for all detectable measurements. Carotenoids were not detected in any species. The large number of animals contributing to these data, provides a substantial base for comparing the nutritional status of healthy animals and the differences among them.     

Homosexual behaviour and female-male mounting in mammals—a first survey

Information from the literature is given on the presence or absence of homosexual behaviour and female-male mounting in 125 species of mammals, both captive and wild. Such behaviour occurs in the male and often female young of many species soon after their birth. It is more common in young, often in play, than in adults. Adult homosexual behaviour is widespread in male and female mammals (recorded in 63 and 71 species respectively), but common in few species. In males it is most likely to be correlated with dominance and thus to occur in species with hierarchies such as terrestrial monkeys and members of the sheep and goat tribe. In females it is often correlated with sexual condition; a female in heat most often mounted another female, and one in heat was next most likely to be mounted by another female. Anoestral females rarely mounted other anoestral females. Females of 43 species mounted males, which often excited them sexually. Captive mammals tended to mount animals of the same sex more often than did wild ones when comparative data were available. Domestic animals also mounted more man did wild ones, with several exceptions. Some phylogenetic groups of animals displayed similar degrees of homosexual mounting, but there was often considerable variation between closely related species. Nor could homosexual mounting be always correlated with the social structure of a group. The four reasons for, or contexts of, homosexual and female-male mountings were social play (in 34 species), aggression (19 species), sexual excitement (36 species), and physical contact—non-play (30 species). This last category included a state of tension, getting attention, greeting, grooming, caressing, reassurance and appeasement. There was some overlap between categories. Homosexual pair-bonds occur in captive mammals and have been observed throughout the year in non-captive female Japanese monkeys.     

The Three-Dimensional Morphological Effects of Captivity

Many captive animals are fed diets that are drastically different in mechanical properties than their wild diet. Most captive pantherines are fed a nutritionally supplemented diet consisting almost entirely of ground meat. While many zoos supplement this diet with bones, the fact remains that large captive felids are fed diets that require substantially less masticatory effort than those of their wild counterparts. The osteological effects of this dietary difference have not been fully evaluated. To this end, we compared linear measurements and 3D geometric morphometric landmarks of captive and wild lions and tigers. Using Principal Component (PC) analysis of the linear measurements, not only were the sexes and species statistically distinct, but so too was the population clearly divisible in terms of captivity status. The 3D analysis supported these findings: although the most influential variable in the sample (PC1, 21.5% of the variation) separates the two species, the second most influential contributor (PC2) to the overall skull shape is driven not by the sex differences in these highly dimorphic species, but rather by their captivity status. In fact, captivity status drives nearly twice as much of the 3D variation as sexual dimorphism (14.8% vs. 8.0% for PC2 vs. PC3). Thus the shape is influenced nearly twice as much by whether the animal was captive or wild than by whether it was male or female. If a causal relationship can be demonstrated between dietary mechanical properties and morphology, people who oversee the diets of captive carnivores should consider modifying these diets to account for not only nutritional but also the mechanical properties of a carcass-based diet as well. In addition to the husbandry implications, our analyses show the ways in which captive specimens are different than their wild counterparts – findings that have implications for morphologists when considering anatomical samples.     

Amphibians: suitable candidates for breeding-release programmes

Zoological parks are playing an increasingly important role in the management of threatened species through education, the maintenance of captive gene banks and the reintroduction of captive-bred animals into the wild. This paper discusses the suitability of amphibian species for reintroduction. The important features of amphibians for these programmes are highlighted, i.e., their high fecundity to allow rapid build-up of captive populations coupled with few behavioural problems with captive-bred animals, as well as the low cost of maintenance. The potential problems of inbreeding, poor retention of innate behavioural repertoires after multiple generation captive breeding, and the introduction of alien pathogens into wild populations are considered. Release programmes for two species, the Mallorcan midwife toad Alytes muletensis and the Puerto Rican crested toad Peltophryne lemur, are reviewed.     

The behavior of a group of captive pygmy chimpanzees (Pan paniscus)

A group of captive pygmy chimpanzees (Pan paniscus) was studied in the San Diego Zoological Gardens. The behavior patterns that these animals exhibit are described. Each of these behavior patterns is compared to those described for wild and captive common chimpanzees (P. troglodytes). Differences in behavior between these two species are attributed to specialization of the pygmy chimpanzee to a rain forest habitat and to a monogamous social system.     

Contrasting fecal corticosterone metabolite levels in captive and free-living colonial tuco-tucos (Ctenomys sociabilis)

The environment in which an animal lives can profoundly influence its biology, including physiological responses to external stressors. To examine the effects of environmental conditions on physiological stress reactions in colonial tuco-tucos (Ctenomys sociabilis), we measured glucocorticoid (GC) levels in captive and free-living members of this species of social, subterranean rodent. Analyses of plasma and fecal samples revealed immunoreactive corticosterone (metabolites) to be the most prevalent GC in this species. An adrenocorticotropic hormone challenge confirmed that fecal corticosterone metabolites are responsive to exogenous stressors and provided validation of the commercial enzyme immunoassay kit used to detect these metabolites. Comparisons of adult female C. sociabilis from natural and captive environments revealed significantly higher baseline concentrations of corticosterone metabolites and significantly greater individual variation in metabolite concentrations among free-living animals. These findings suggest that the natural environment in which these animals occur is more challenging and more variable than the captive housing conditions employed. In addition to providing the first evaluation of GC levels in captive and wild colonial tuco-tucos, our findings indicate that the influence of environmental conditions on stress physiology may have important implications for understanding the social behavior of this species in the laboratory and the field.     

Assortative mating among animals of captive and wild origin following experimental conservation releases

Captive breeding is a high profile management tool used for conserving threatened species. However, the inevitable consequence of generations in captivity is broad scale and often-rapid phenotypic divergence between captive and wild individuals, through environmental differences and genetic processes. Although poorly understood, mate choice preference is one of the changes that may occur in captivity that could have important implications for the reintroduction success of captive-bred animals. We bred wild-caught house mice for three generations to examine mating patterns and reproductive outcomes when these animals were simultaneously released into multiple outdoor enclosures with wild conspecifics. At release, there were significant differences in phenotypic (e.g. body mass) and genetic measures (e.g. G_st and F) between captive-bred and wild adult mice. Furthermore, 83% of offspring produced post-release were of same source parentage, inferring pronounced assortative mating. Our findings suggest that captive breeding may affect mating preferences, with potentially adverse implications for the success of threatened species reintroduction programmes.     

How Rearing History Affects Alarm-call Responses of Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Juvenile, but not adult, Belding’s ground squirrels (Spermophilus beldingi) exhibit markedly different responses to alarm calls as a function of their environment. Compared with same-aged, free-living juveniles, captive juveniles (housed in large outdoor enclosures) are more likely to respond to playbacks, to exhibit more exaggerated initial responses (e.g. enter a burrow vs. freeze) and to remain alert longer following playbacks of alarm and non-alarm calls. Two studies were conducted to identify the factors contributing to these response differences. Postemergent rearing environments (such as the opaque enclosure walls that limited visual and auditory stimulation in captivity, or the increased number of conspecifics and natural alarm calls that free-living juveniles experienced) could not account for the majority of response differences between captive and free-living juveniles (Study 1). To determine if the attenuated responses of free-living juveniles were due to foraging pressures, we compared the behaviours of food-provisioned captive juveniles with those of non-provisioned captive juveniles. Although sample sizes were small, no differences were evident in the development or expression of responses as a function of foraging pressure. Next, the development of captive juveniles was compared with that of juveniles reared in the field but housed in captivity after emergence (Study 2). Differences in the response patterns of field-reared and captive-reared animals matched the differences reported previously, as the responses of field-reared animals observed in captivity mirrored those of free-living juveniles that remained in the field. Thus, the differences in alarm-call responses originally observed between captive and free-living juveniles are attributed to their pre-emergent, but not post-emergent, rearing histories. Captive pups experienced levels of auditory, visual, tactile, and olfactory stimulation that were greater than those typically experienced by free-living pups. The increased exposure to conspecific alarm calls may have primed captive pups to respond more often and more intensely to the auditory stimuli they heard as juveniles. Sensitivity to early rearing environments may be adaptive for young ground squirrels if it facilitates the development of antipredator behaviour patterns that are appropriate for the local predator environment (e.g. openness of habitat, frequency of predators, availability of refuges).