Space use selectivity by chimpanzees and gorillas in an indoor-outdoor enclosure

Understanding the relationship between physical environments and nonhuman primate behavior is a key element for effective care and management in a range of settings. The physical features of the captive environment, including not only gross useable space but also environmental complexity, can have a significant influence on primate behavior and ultimately, animal welfare. But despite this connection, there remains relatively little conclusive data on how captive primates, especially great apes, use the spaces provided to them, especially in modern, indoor-outdoor enclosures that have become more prevalent in recent years. In this study, we used four years of detailed data on where 23 great apes (chimpanzees and gorillas) positioned themselves within a modern, indoor-outdoor zoo enclosure to determine not only how the apes utilized their space but also how access to outdoor areas affected their spatial selectivity. We found that both species used relatively little of their available space: chimpanzees and gorillas spent half their time in only 3.2 and 1.5% of their useable three-dimensional space, respectively. Chimpanzees utilized the outdoor space more than gorillas, but access to the outdoors did not affect space selectivity in the indoor area for either species. Although both species of ape were highly selective in their space use, consideration should be given to the importance of providing the choice to locate in a variety of spaces, including outdoor areas. These data represent an extremely detailed account of space selectivity by great apes in an indoor-outdoor environment and have substantial implications for future facility design and captive primate management.     

Water bathing alters threat perception in starlings

The majority of bird taxa perform water bathing, but little is known about the adaptive value of this behaviour. If bathing is important for feather maintenance then birds that have not bathed should have poorer feather condition, compromised escape ability and therefore increased responsiveness to cues of predation. We conducted two experiments examining the behaviour of captive starlings responding to conspecific alarm calls. Birds that had no access to bathing water showed a decreased willingness to feed and increased their vigilance behaviour following an alarm call. We argue that birds denied access to bathing water interpreted an ambiguous cue of threat as requiring more caution than birds that had access, consistent with higher levels of anxiety. Our results support the provision of bathing water for captive birds as an important welfare measure.     

Anti‐predatory behaviour of wild‐caught vs captive‐bred freshwater angelfish,Pterophyllum scalare

Environments and experiences encountered in early life stages of animals shape their adult behaviour. When environments are maintained for several generations, differential selection forces act upon individuals to select those most fit to the particular conditions. As such, differences in the behaviour of captive bred and wild caught individuals have been observed recurrently. In fish, hatchery raised individuals tend to seek refuge less, making them more vulnerable to predators. We tested the hypothesis that captive breeding induces non‐adaptive changes in behaviour of freshwater angelfish, Pterophyllum scalare. Wild‐caught and captive‐bred fish were exposed to a natural predator and measured for their anti‐predator behaviours; no differences were found in behaviour under control conditions. When exposed to a natural predator, wild‐caught fish exhibited significantly shorter freezing durations than captive‐bred fish, and took significantly shorter time to resume normal behaviour. No differences in the time taken to initiate investigations of the predator were detected. The results demonstrate that captive‐bred fish respond differently than their wild counterparts when exposed to a natural predator, and that this domestication has implications for captive rearing programmes.     

Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore

Energy maximization, time minimization, and linear programming models subject to various constraints have dominated foraging ecology ideas and methods for decades. However, animals must use very complex physiological processes and foraging decisions to ensure fitness that in many cases may not be adequately described by these approaches. An example of this problem occurs when brown bears, Ursus arctos, have access to both abundant salmon and fruit. Salmon are one of the most energy and nutrient dense foods available to bears. Fruits are often high in soluble carbohydrates, low to deficient in many required nutrients, and more difficult to efficiently exploit. Therefore, wild brown bears that fatten primarily on fruits without access to salmon are 50% smaller than salmon-feeding bears. Thus, we predicted based on a linear, energy-maximizing model without dietary interaction effects that wild brown bears with access to both abundant salmon and fruit would feed almost exclusively on salmon. However, wild adult females with or without accompanying offspring foraged three times longer per day on fruit than on salmon. Similarly, the relative dry matter intake of ad libitum apples and salmon by captive, adult brown bears averaged 76±5% fruit and 24±5% salmon. Captive brown bears consuming mixed diets with intermediate dietary protein levels had 60% lower maintenance energy costs, 37% to 139% higher efficiencies of mass gain, and 72% to 520% higher maximum rates of gain than when they consumed either salmon or fruit alone. These relationships were nonlinear functions of dietary protein content in which salmon and fruit provided complementary nutritional resources. Both wild and captive bears attempted to regulate total protein, energy, and carbohydrate intake within a multidimensional intake target that both maximized energy intake and mass gain.     

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.     

Spontaneous tool-use: an observation of a dingo (Canis dingo) using a table to access an out-of-reach food reward

Opportunities to observe non-human animals exhibiting naturalistic 'high-order' behaviour are rare. Examples featuring canids, although often anecdotal and involving captive animals are potentially valuable, as they may provide an opportunity to examine complex problem-solving behaviour not easily observed in free-ranging settings. This paper describes observations of two captive male dingoes (Canis dingo), representing possible examples of high-order behaviour. The first set of observations involved a sub-adult male that spontaneously (i.e., without training) learned to move objects around his enclosure, apparently to multiple ends, such as in an effort to gain the additional height required to attain objects otherwise out of reach, or to attain a better view of his surroundings. The second set of observations involved an adult male that learned to open a gate, possibly in an effort to gain access to a female. These observations add to the small number of anecdotal accounts offering a window into the cognitive abilities of canids, and the observations involving the sub-adult male appear to be the first documented cases of tool-use in a canid.     

Contrafreeloading in grizzly bears: implications for captive foraging enrichment

Although traditional feeding regimens for captive animals were focused on meeting physiological needs to assure good health, more recently emphasis has also been placed on non‐nutritive aspects of feeding. The provision of foraging materials to diversify feeding behavior is a common practice in zoos but selective consumption of foraging enrichment items over more balanced “chow” diets could lead to nutrient imbalance. One alternative is to provide balanced diets in a contrafreeloading paradigm. Contrafreeloading occurs when animals choose resources that require effort to exploit when identical resources are freely available. To investigate contrafreeloading and its potential as a theoretical foundation for foraging enrichment, we conducted two experiments with captive grizzly bears (Ursus arctos horribilis). In Experiment 1, bears were presented with five foraging choices simultaneously: apples, apples in ice, salmon, salmon in ice, and plain ice under two levels of food restriction. Two measures of contrafreeloading were considered: weight of earned food consumed and time spent working for earned food. More free than earned food was eaten, with only two bears consuming food extracted from ice, but all bears spent more time manipulating ice containing salmon or apples than plain ice regardless of level of food restriction. In Experiment 2, food‐restricted bears were presented with three foraging choices simultaneously: apples, apples inside a box, and an empty box. Although they ate more free than earned food, five bears consumed food from boxes and all spent more time manipulating boxes containing apples than empty boxes. Our findings support the provision of contrafreeloading opportunities as a foraging enrichment strategy for captive wildlife. Zoo Biol 29:484–502, 2010. © 2009 Wiley‐Liss, Inc.     

Constraints on herbivory by grizzly bears

Although well known as carnivores and not capable of digesting plant fiber, grizzly bears (Ursus arctos horribilis) consume over 200 species of plants and are entirely vegetarian in some ecosystems. Even in ecosystems with abundant meat resources, green vegetation can be an important seasonal food resource. Therefore, we examined the morphological, physiological, and environmental constraints that determine the nutritional value of herbaceous vegetation to grizzly bears. Short-term, board foraging trials were used with captive grizzly bears to determine constraints on intake rate including bite size, bite rate, bear size, plant species, plant height, and plant distribution. Feeding trials were conducted to determine the effect of protein level (12-35%) and digestible dry matter intake on weight gain. Finally, maximum daily intake, daily foraging time, and weight change were measured for captive bears foraging on highly abundant and nutritious forbs and grasses during 12-day trials. Intake during short-term board trials overestimated the intake of freely foraging bears from two- to seven-fold depending on bear size. Because of their relatively larger bite sizes, smaller absolute energy requirements, and relatively larger intake capacity, smaller bears (<120 kg) made greater weight gains than very large bears on herbaceous vegetation. Smaller bears with ad libitum access to palatable, nutritious forbs gained weight at rates equal to wild bears. However, depending upon plant characteristics, bite sizes and available daily foraging time increasingly prevented large bears (>120 kg) from gaining weight on herbaceous vegetation. Both captive and wild bears select forbs over grasses at similar growth stages because forbs are generally higher in protein and more digestible than grasses. Therefore, the nutritional well-being of wild grizzly bears could be improved in areas where bears are largely herbivorous and, thus, relatively small by purposefully managing for nutritious forbs.     

Do captive waterfowl alter their behaviour patterns during their flightless period of moult?

Many different behavioural changes have been observed in wild waterfowl during the flightless stage of wing moult with birds frequently becoming inactive and reducing time spent foraging. Increased predation risk, elevated energetic demands of feather re-growth and restriction of foraging opportunities are thought to underlie these changes. By studying captive populations of both a dabbling and a diving duck species at the same site, we determined whether captive birds would reflect the behavioural responses of wild waterfowl to moult. The time-budgets of 42 Common Eiders, Somateria mollissima, (a diving duck) and 18 Garganeys, Anas querquedula, (a dabbling duck) were recorded during wing moult (July–August) and non-moult (January) with behaviour recorded under six categories. Despite captivity providing a low predation risk and constant access to food, birds altered their behaviour during the flightless period of wing moult. Time allocated to foraging and locomotion decreased significantly during moult compared to non-moult periods, while resting time increased significantly. Moulting Eiders underwent a greater reduction in time spent foraging and in locomotion compared with Garganeys, which is likely to be in response to a higher energetic cost of foraging in Eiders. It is possible that increased resting in both diving and dabbling ducks reduces their likelihood of detection by predators, while allowing them to remain vigilant. We demonstrate that there is much potential for using captive animals in studies that can augment our knowledge of behaviours of free-living conspecifics, the former being a hitherto under-exploited resource.     

非人灵长类饲养与管理过程中的福利保障

实验动物饲养管理和福利保障的问题已越来越被国际社会所关注.与发达国家相比,中国对实验动物福利的研究及大众化意识则相对滞后.中国作为世界上最大的实验灵长类动物的饲养与出口国,每年遭受的国际贸易损失始终位居全球首位.为此,本文引入了实验灵长类福利的"5个自由"理论:1)动物有避免干渴、饥饿和营养不良等不利因素影响的自由;2)动物有获得舒适生活条件的自由;3)动物有脱离痛苦、受伤和疾病骚扰的自由;4)动物有表达自然行为的自由;5)动物有脱离恐惧和心理压力的自由.在上述理论的基础上,提高实验动物福利应具体从饲养的物理环境、营养供给、饲养管理、繁殖管理及饲养环境的多样性等几方面着手.通过总结国际与此相关的研究进展,旨为中国相关研究提供素材和为完善国内现行的法规及标准提出一些思路.     

Habituation to environmental enrichment in captive sloth bears—effect on stereotypies

The benefits to captive animals of environmental enrichment (EE) are widely recognized. Few studies have, however, studied how to maximise the effect of EE. One issue with EE programs seems to be habituation to the enrichment device. To study the effect of habituation to EE, 14 captive sloth bears (Melursus ursinus) were subjected to two different EE treatments. Treatment one presented EE (logs with honey containing holes) for five consecutive days, whereas treatment two presented EE on intermittent days for five days. Intermittent presentations tended to reduce habituation toward the EE. Both consecutive and intermittent presentations significantly reduced stereotypies; however, the consecutive presentations had a longer‐lasting effect. Explorative behaviors increased in both treatments, consistent with earlier findings that EE increase levels of natural behaviors. Other behaviors were unaffected by the EE presentations. The results show that intermittent presentation of EE objects may secure the interest of the animals, but continuous access to enrichment may be more efficient in reducing stereotypies in the long run. Zoo Biol 29:705–714, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

Controllability in environmental enrichment for captive chimpanzees (Pan troglodytes)

This study considers the use of nonsocial environmental enrichment by captive chimpanzees at the Primate Foundation of Arizona. The goal was to determine whether a relationship existed between controllability of enrichment items by captive chimpanzees and frequency of use. The study measured controllability, the ability of nonhuman animals to alter aspects of their environment by the potential destructibility of the enrichment item. This study examined additional factors that may affect enrichment use: individual age, sex, rearing history, social group composition, and availability of outdoor access. The chimpanzees in the study used destructible items—the enrichment category with the highest level of controllability—more than indestructible items across all age, sex, and rearing classes. Thus, controllability seems to be an important factor in chimpanzee enrichment. Younger individuals and groups with outdoor access used enrichment more than did older individuals and groups with indoor-only access. Individual sex, rearing history, and social group composition had minimal effects on enrichment use. These results support the importance of control to captive chimpanzees and further enable captive management to customize enrichment programs to the needs of particular animals.     

‘Captivity bias’ in animal tool use and its implications for the evolution of hominin technology

Animals in captive or laboratory settings may outperform wild animals of the same species in both frequency and diversity of tool use, a phenomenon here termed ‘captivity bias’. Although speculative at this stage, a logical conclusion from this concept is that animals whose tool-use behaviour is observed solely under natural conditions may be judged cognitively or physically inferior than if they had also been tested or observed under controlled captive conditions. In turn, this situation creates a potential problem for studies of the behaviour of extinct members of the human family tree—the hominins—as hominin cognitive abilities are often judged on material evidence of tool-use behaviour left in the archaeological record. In this review, potential factors contributing to captivity bias in primates (including increased contact between individuals engaged in tool use, guidance or shaping of tool-use behaviour by other tool-users and increased free time and energy) are identified and assessed for their possible effects on the behaviour of the Late Pleistocene hominin Homo floresiensis. The captivity bias concept provides one way to uncouple hominin tool use from cognition, by considering hominins as subject to the same adaptive influences as other tool-using animals.     

The Welfare of Bears in Zoos: A Case Study of Poland

The welfare of captive bears became a big issue of concern in Poland when a case of a bear being ill-treated became a high-profile case in the media. This case created a challenge to verify, study, and understand the main problems associated with bear keeping so that zoos could significantly improve the conditions in which they keep bears or ensure they keep bears at the minimum required standards. The results presented here are from 1 of the few countrywide studies of captive bear conditions conducted in all the captive institutions in Poland that keep bears. Thirteen institutions kept bears at the time of the study (2007–2009), including 54 individuals of 5 species. Major welfare problems were identified, and the results have been used to challenge zoos to address the changes required and focus the government's attention on areas that require legislative improvement.     

Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears

Ancient DNA studies have revolutionized the study of extinct species and populations, providing insights on phylogeny, phylogeography, admixture and demographic history. However, inferences on behaviour and sociality have been far less frequent. Here, we investigate the complete mitochondrial genomes of extinct Late Pleistocene cave bears and middle Holocene brown bears that each inhabited multiple geographically proximate caves in northern Spain. In cave bears, we find that, although most caves were occupied simultaneously, each cave almost exclusively contains a unique lineage of closely related haplotypes. This remarkable pattern suggests extreme fidelity to their birth site in cave bears, best described as homing behaviour, and that cave bears formed stable maternal social groups at least for hibernation. In contrast, brown bears do not show any strong association of mitochondrial lineage and cave, suggesting that these two closely related species differed in aspects of their behaviour and sociality. This difference is likely to have contributed to cave bear extinction, which occurred at a time in which competition for caves between bears and humans was likely intense and the ability to rapidly colonize new hibernation sites would have been crucial for the survival of a species so dependent on caves for hibernation as cave bears. Our study demonstrates the potential of ancient DNA to uncover patterns of behaviour and sociality in ancient species and populations, even those that went extinct many tens of thousands of years ago.     

Diet and environment shape fecal bacterial microbiota composition and enteric pathogen load of grizzly bears

Background

Diet and environment impact the composition of mammalian intestinal microbiota; dietary or health disturbances trigger alterations in intestinal microbiota composition and render the host susceptible to enteric pathogens. To date no long term monitoring data exist on the fecal microbiota and pathogen load of carnivores either in natural environments or in captivity. This study investigates fecal microbiota composition and the presence of pathogenic Escherichia coli and toxigenic clostridia in wild and captive grizzly bears (Ursus arctos) and relates these to food resources consumed by bears.

Methodology/Principal Findings

Feces were obtained from animals of two wild populations and from two captive animals during an active bear season. Wild animals consumed a diverse diet composed of plant material, animal prey and insects. Captive animals were fed a regular granulated diet with a supplement of fruits and vegetables. Bacterial populations were analyzed using quantitative PCR. Fecal microbiota composition fluctuated in wild and in captive animals. The abundance of Clostridium clusters I and XI, and of C. perfringens correlated to regular diet protein intake. Enteroaggregative E. coli were consistently present in all populations. The C. sordellii phospholipase C was identified in three samples of wild animals and for the first time in Ursids.

Conclusion

This is the first longitudinal study monitoring the fecal microbiota of wild carnivores and comparing it to that of captive individuals of the same species. Location and diet affected fecal bacterial populations as well as the presence of enteric pathogens.     

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.     

Blood‐feeding ecology of mosquitoes in zoos

To determine if the unique host assemblages in zoos influence blood‐feeding by mosquitoes (Diptera: Culicidae), a sampling programme was conducted in Greenville and Riverbanks Zoos, South Carolina, U.S.A., from April 2009 to October 2010. A total of 4355 female mosquitoes of 14 species were collected, of which 106 individuals of nine species were blood‐fed. The most common taxa were Aedes albopictus (Skuse), Aedes triseriatus (Say), Anopheles punctipennis (Say), Culex erraticus (Dyar & Knab), Culex pipiens complex (L.) and Culex restuans (Theobald). Molecular analyses (cytochrome b) of bloodmeals revealed that mosquitoes fed on captive animals, humans and wildlife, and took mixed bloodmeals. Host species included one amphibian, 16 birds, 10 mammals (including humans) and two reptiles. Minimum dispersal distances after feeding on captive hosts ranged from 15.5 m to 327.0 m. Mosquito–host associations generally conformed to previous accounts, indicating that mosquito behaviour inside zoos reflects that outside zoos. However, novel variation in host use, including new, exotic host records, warrants further investigation. Zoos, thus, can be used as experiment environments in which to study mosquito behaviour, and the findings extrapolated to non‐zoo areas, while providing medical and veterinary benefits to zoo animals, employees and patrons.