Empty Nest: A Case Study of Maternal Response to Separation From a Juvenile Offspring in a Captive Sumatran Orangutan (Pongo pygmaeus abelii)

Improving the welfare of captive nonhuman primates requires evaluating the stressors created by the captive environment and reducing their negative effects. Social separation, although sometimes necessary for managing the genetic diversity of captive populations of animals, causes both psychological and physiological stress in human and primate monkey infants. Few studies have examined the maternal response of great ape mothers to separation from their offspring. This article describes the behavioral changes of a mother orangutan (Pongo pygmaeus abelii) after separation from her juvenile daughter. We collected data on measures of proximity and social behavior before the separation of the mother-infant dyad and of locomotion, arboreality, abnormal behavior, solitary behavior, and vocalization both before and after separation. We observed no behavioral indications of protest but observed some indications of despair after separation: decreased locomotion, increased inactivity, and increased self-directed behavior. In addition, we observed increases in arboreality and object-oriented behavior during morning sessions. These findings suggest that mother-juvenile separation in orangutans might be less stressful for mothers than might be expected. Such research has implications for the welfare and management of captive animals.     

Behavioral and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment

The behavioral and adrenocortical responses of rhesus macaque mothers to a series of four consecutive 4-day separations from their 5-month old infants in an unfamiliar environment were examined. A biphasic behavioral response to separation was observed, with passive behavior, locomotion, and vocalization highest on Day 1 of separation, and self-directed behaviors and environmental exploration peaking during Days 2–4. Stereotyped locomotion increased, and passive behavior decreased, across successive weeks of separation. The rhesus mothers exhibited substantial cortisol elevations one and two hours postseparation, with cortisol decreasing on the fourth day of separation. The cortisol response was strongest during the first week of separation, but robust elevations occurred in response to repeated separations. No signs of behavioral depression were observed. The results indicate that infant separation combined with removal to a novel environment can be a potent stressor for rhesus macaque mothers.     

Social attachment in giraffe: Response to social separation

Attachment relationships between animals are often studied by separating a pair of individuals and recording their subsequent behavior. Studies of non‐human primates have shown that separation results in changes that are indicative of both psychological and physiological stress. Similar results have been found in several non‐primate species with differing social structures. This study examined the behavior of two female giraffe at Zoo Atlanta after the removal of the resident male. Data were collected on the giraffe before and after separation, using an instantaneous scan sampling technique to record levels of activity, social behaviors, solitary behaviors, proximity, and habitat utilization. After the removal of the resident male, both giraffe exhibited increased levels of activity, stereotypical behavior, contact behavior (particularly neck‐rubbing), and decreased habitat utilization. These results are similar to those found in earlier primate separation studies, supporting the hypothesis that complex social structure is not necessary for the formation of social attachments. Because social separation is often accompanied by behavioral and physiological indications of stress, an understanding of the variables involved in a species' response to separation is vital to the promotion of the psychological and physical well‐being of captive animals. Zoo Biol 19:41–51, 2000. © 2000 Wiley‐Liss, Inc.     

Calibration of remotely collected acceleration data with behavioral observations of roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis> L.)

Long-term, remote monitoring of animals under natural conditions is essential for obtaining information on animal activity. Advances in biotelemetry have led to the construction of low-power accelerometers placed on Global Positioning System (GPS) collars. Such acceleration data from roe deer have not yet been classified to the various behavioral categories. Here, we determined the threshold values of such data for different behavioral categories. We equipped captive roe deer with Global Positioning System–Global System for Mobile Communications/dual-axis acceleration sensor neck collars and simultaneously measured their movement and observed their behavior. The difference between feeding and slow locomotion was significant on the x- but not the y-axis, and both of these two behavioral categories differed significantly from resting and fast locomotion. Specific thresholds for the behavioral categories—resting, feeding, and slow and fast locomotion—were established by recursive partitioning. We compared the behavior determined by these threshold values with observed behavior and found that 92% of the behavioral categories were correctly assigned. A comparison of our results with those of earlier studies showed that thresholds derived for one species cannot be directly applied to another species. We provide recommendations for the further development of acceleration sensors based on the results obtained in this study.     

Activity budget and spatial distribution of Bennett's wallabies (Macropus rufogriseus) in open versus closed exhibit designs

Although many studies investigating the impacts of zoo exhibit designs on captive animals exist, none have been performed on how they influence the behavior and welfare of captive Bennett's wallabies (Macropus rufogriseus). Here, we assess the impact of exhibit design on the activity budget and spatial distribution of Bennett's wallabies. We compared animal behavior in two open exhibits (i.e. physical interaction between animals and visitors permitted) to two closed exhibits (i.e. physical interaction between animals and visitors prohibited). Behavioral data were collected using focal sampling, and spatial distribution was recorded on exhibit maps at regular time intervals. We found a significant increase in feeding and interactive behaviors in closed exhibits in comparison to open exhibits. However, other behaviors such as resting, locomotion, and vigilance did not vary with design. Functional use of space was similar between both designs; however, the effect of habituation may be relevant to consider in future studies. Although some support for visitor effects were present, our study provided no evidence for strong impacts of exhibit design on Bennett's wallaby welfare. Our study emphasizes the need for additional research into the impacts of how zoo environments affect Bennett's wallaby behavior and welfare.     

Current status and future directions of applied behavioral research for animal welfare and conservation

The papers that follow in this special issue reflect the state of knowledge and theory in the fields of animal welfare and conservation behavior. A particular focus is placed on how enrichment can be used judiciously to improve welfare and to prepare captive animals for release back to the wild. However, my purpose here is not simply to reiterate what the contributors of this special issue have said, but to provide an overview of the major themes, problems, and opportunities in applied animal behavior related to conservation and welfare. I review major issues in three interrelated areas: captive welfare, captive breeding, and conservation behavior research for wild populations. Despite many advancements in welfare science, one of the most significant impediments to a predictive science of welfare is the need to further refine theories advanced to explain environment–welfare relationships. I provide a brief overview of ten theories that have been proposed to explain good or poor welfare and suggest that they need to be made more conceptually distinct so that clear hypotheses can be articulated, and predictions made and tested. Captive breeding programs for ex situ conservation have borrowed and applied many of the concepts involved in welfare science to great advantage. Other keys to successful breeding programs include applying knowledge of social organization and processes to enhance reproduction; for example, finding the right combination of individuals to get animals breeding. However, behaviorists are only recently learning how to manipulate behavioral mechanisms, such as signaling behavior and mate choice, to optimize captive breeding for conservation. The emerging field of conservation behavior has played a role in captive breeding, but also is poised to play a major role in in situ conservation. Applied behavioral research can illuminate a number of issues important to conservation, including behavioral responses to habitat fragmentation and human disturbance (e.g., pollutants, noise, and light), and human–animal conflict (e.g., crop-raiding). Behavioral decisions made when animals are dispersing and selecting habitat for settlement determine the distribution of animals on the landscape and are important to understand for improving reserve and habitat corridor design. Captive–release and translocation programs require detailed behavioral knowledge to predict responses to novel environments and ensure that animals are adequately prepared for environmental change. This review underscores that many of the behavioral processes of interest to welfare science are also important for conservation behavior: perception, stress, assessment and decision-making rules, and other behavioral and physiological mechanisms. If properly understood, these mechanisms can be manipulated in the service of conservation goals, moving the field of conservation behavior from implication to application. A better integration of the disciplines of animal welfare and conservation behavior – together tackling problems at multiple levels of analysis – will further these goals.     

A case study employing operant conditioning to reduce stress of capture for red-bellied tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

Structural aspects of arboreality in titi monkeys (Callicebus moloch)

In nature titi monkeys spend virtually all of their time in trees. Preferences for certain heights above the ground or for trees per se are probably not, however, the immediate causes of this behavior, for animals housed in a large field cage containing many trees spend most of their time on a low-altitude artificial runway system. Further, the animals are not necessarily reluctant to touch the ground. To investigate the importance of perceived substrate structure as a determinant of arboreality, individuals were given opportunities to descend from their home runway and travel to food placed nearby on the ground. The animals travelled along a schematic model of a tree branch rather than across open ground when given a choice of these substrates, but they readily crossed the open ground when it was their only travel option. When the schematic model increased substantially in length and no longer provided a short route to food, it was still the preferred substrate. The results suggest that an abstract representation of a tree branch attracts and guides locomotion in titis, and that responsiveness to substrate characteristics contributes to arboreality in this species.     

Improved behavioral indices of welfare in continuous compared to intermittent pair-housing in adult female rhesus macaques (Macaca mulatta)

Limiting opportunities for captive nonhuman primates (NHPs) to express species-specific social behaviors may disrupt the adaptive drive for social companionship and may lead to increases in coping behaviors and inactivity. While captive NHPs show improved welfare when moving to pair-housing from single-housing, the impact of daily separation of pair-mates, as is implemented in intermittent pair-housing, is not fully understood. We compared behavioral indices of welfare exhibited by adult female rhesus macaques (Macaca mulatta) in two conditions: (1) intermittent pair-housing, involving daily overnight separation of pair-mates, and (2) continuous pair-housing, involving little separation of pair-mates. A within-subjects study design tested two groups of females experiencing both pairing conditions in an alternate order, switching either from continuous to intermittent pair-housing, or from intermittent to continuous pair-housing. Behavioral observations, recording activity state, self-directed, abnormal, and social behaviors, were conducted at midday when all females were paired, and in the afternoon when intermittent pairs were separated. Females exhibited higher levels of inactivity and self-directed behavior when separated due to intermittent pair-housing in comparison to continuous pair-housing. In addition, intermittently paired females showed higher levels of grooming and other types of affiliation when paired, than during the same time frame when they were continuously paired. These results suggest that females in the continuous presence of a social partner experience improved levels of activity and do not need to elevate levels of behavioral coping mechanisms (e.g., self-scratching, increased affiliation) as they receive the benefits associated with social companionship consistently throughout the day. Overall, this study provides the first evidence that continuous pair-housing affords better welfare than intermittent pair-housing in adult female rhesus macaques. Pair-housing options, such as continuous pairing, that reduce reliance on behavioral coping mechanisms and promote adaptive social behavior throughout the entirety of the day should be prioritized over husbandry care scheduled for convenience.     

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.     

Influence of zoo visitor presence on the behavior of captive Indian gaur (Bos gaurus gaurus) in a zoological park

Visitors to zoos can be a source of potential disturbance and stress to some captive, nonhuman animals in the wild. To determine the influence of visitor presence on captive bison (Bos gaurus gaurus), the study analyzed the behavior of 4 individuals at the Arignar Anna Zoological Park, India. The study often observed the behavior of the animals on visitor-present days and on days when visitors were absent. In the presence of zoo visitors, the bison showed a higher level of intragroup aggression and moving behavior. In contrast, the bison rested more when no visitors were present. The results revealed that the presence of zoo visitors significantly influenced the behavior of captive bison and thereby may have affected their welfare.     

Influence of Zoo Visitor Presence on the Behavior of Captive Indian Gaur (Bos gaurus gaurus) in a Zoological Park

Visitors to zoos can be a source of potential disturbance and stress to some captive, nonhuman animals in the wild. To determine the influence of visitor presence on captive bison (Bos gaurus gaurus), the study analyzed the behavior of 4 individuals at the Arignar Anna Zoological Park, India. The study often observed the behavior of the animals on visitor-present days and on days when visitors were absent. In the presence of zoo visitors, the bison showed a higher level of intragroup aggression and moving behavior. In contrast, the bison rested more when no visitors were present. The results revealed that the presence of zoo visitors significantly influenced the behavior of captive bison and thereby may have affected their welfare.     

A Case Study Employing Operant Conditioning to Reduce Stress of Capture for Red-Bellied Tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

Effect of Enclosure Quality on Reactivity and Welfare of Captive Soemmerring's Gazelle (Gazella soemmerringii)

The welfare of nonhuman animals in zoos is a great challenge to the zookeeper. Changes in the behavioral response of captive animals to their immediate environment can be used as a method for evaluating their welfare status. This study evaluates reactive responses of 3 groups of captive Soemmerring's gazelle (Gazella soemmerringii) kept in enclosures of different quality at Giza Zoo, Egypt. The study ascribes variations in observed behaviors to the differences in the living standards of the 3 groups. The group most concealed from visitors' disturbance (Group 3) was the least reactive. With the morning onset of human-nonhuman animal interaction, reactivity reached significantly higher levels. The study noted no difference in reactivity between male and female animals. The main sign of the animals' alertness was their attention to sources of disturbances; vocalization was minimal. Animals in Groups 1 and 2, those most accessible to visitors, had higher agonistic reactions than animals in Group 3.     

Effect of Enclosure Quality on Reactivity and Welfare of Captive Soemmerring's Gazelle (Gazella soemmerringii)

The welfare of nonhuman animals in zoos is a great challenge to the zookeeper. Changes in the behavioral response of captive animals to their immediate environment can be used as a method for evaluating their welfare status. This study evaluates reactive responses of 3 groups of captive Soemmerring's gazelle (Gazella soemmerringii) kept in enclosures of different quality at Giza Zoo, Egypt. The study ascribes variations in observed behaviors to the differences in the living standards of the 3 groups. The group most concealed from visitors' disturbance (Group 3) was the least reactive. With the morning onset of human-nonhuman animal interaction, reactivity reached significantly higher levels. The study noted no difference in reactivity between male and female animals. The main sign of the animals' alertness was their attention to sources of disturbances; vocalization was minimal. Animals in Groups 1 and 2, those most accessible to visitors, had higher agonistic reactions than animals in Group 3.     

Effects of early rearing conditions on problem‐solving skill in captive male chimpanzees (Pan troglodytes)

Early rearing conditions of captive chimpanzees characterize behavioral differences in tool use, response to novelty, and sexual and maternal competence later in life. Restricted rearing conditions during early life hinder the acquisition and execution of such behaviors, which characterize the daily life of animals. This study examined whether rearing conditions affect adult male chimpanzees' behavior skills used for solving a problem with acquired locomotion behavior. Subjects were 13 male residents of the Chimpanzee Sanctuary Uto: 5 wild‐born and 8 captive‐born. A pretest assessed bed building and tool use abilities to verify behavioral differences between wild‐ and captive‐born subjects, as earlier reports have described. Second, a banana‐access test was conducted to investigate the problem‐solving ability of climbing a bamboo pillar for accessing a banana, which might be the most efficient food access strategy for this setting. The test was repeated in a social setting. Results show that wild‐born subjects were better able than captive‐born subjects to use the provided materials for bed building and tool use. Results of the banana‐access test show that wild‐born subjects more frequently used a bamboo pillar for obtaining a banana with an efficient strategy than captive‐born subjects did. Of the eight captive‐born subjects, six avoided the bamboo pillars to get a banana and instead used, sometimes in a roundabout way, an iron pillar or fence. Results consistently underscored the adaptive and sophisticated skills of wild‐born male chimpanzees in problem‐solving tasks. The rearing conditions affected both the behavior acquisition and the execution of behaviors that had already been acquired. Am. J. Primatol. 72:626–633, 2010. © 2010 Wiley‐Liss, Inc.     

Brief communication: Swimming and diving behavior in apes (Pan troglodytes and Pongo pygmaeus): First documented report

Extant hominoids, including humans, are well known for their inability to swim instinctively. We report swimming and diving in two captive apes using visual observation and video recording. One common chimpanzee and one orangutan swam repeatedly at the water surface over a distance of 2–6 m; both individuals submerged repeatedly. We show that apes are able to overcome their negative buoyancy by deliberate swimming, using movements which deviate from the doggy‐paddle pattern observed in other primates. We suggest that apes' poor swimming ability is due to behavioral, anatomical, and neuromotor changes related to an adaptation to arboreal life in their early phylogeny. This strong adaptive focus on arboreal life led to decreased opportunities to interact with water bodies and consequently to a reduction of selective pressure to maintain innate swimming behavior. As the doggy paddle is associated with quadrupedal walking, a deviation from terrestrial locomotion might have interfered with the fixed rhythmic action patterns responsible for innate swimming. Am J Phys Anthropol 152:156–162, 2013. © 2013 Wiley Periodicals, Inc.     

Assessing the Welfare of Dairy Cattle

This article attempts to determine the effects of environment (captive or wild) and a simple form of environmental enrichment on the behavior and physiology of a nonhuman animal. Specifically, analyses first compared behavioral budgets and stereotypic behavior of captive coyotes (Canis latrans) in kennels and pens to their counterparts in the wild. Second, experiments examined the effect of a simple form of environmental enrichment for captive coyotes (food-filled bones) on behavioral budgets, stereotypies, and corticosteroid levels. Overall, behavioral budgets of captive coyotes in both kennels and pens were similar to those observed in the wild, but coyotes in captivity exhibited significantly more stereotypic behavior. Intermittently providing a bone generally lowered resting and increased foraging behaviors but did not significantly reduce stereotypic behavior or alter corticosteroid levels. Thus, coyote behavior in captivity can be similar to that exhibited in the wild; in addition, although enrichment can affect proportions of elicited behaviors, abnormal behaviors and corticosteroid levels may require more than a simple form of environmental enrichment for their reduction.     

Chemosensory enrichment as a simple and effective way to improve the welfare of captive lizards

Environmental enrichment has proven to be a useful and effective welfare tool in order to evaluate and enhance the well‐being of captive animals, but only when it is based on detailed knowledge of each species' natural behaviour. Chemoreception is fundamental to many aspects of reptilian biology; however, sensory enrichment with chemical stimuli has rarely been applied to reptiles. In this study, we evaluate the use of chemosensory enrichment as a method to enhance the welfare of Podarcis liolepis. For seven weeks, we exposed field‐caught males to scents from donor conspecific males collected on pieces of filter paper (i.e., “enriched” group, n = 18), and compared their behaviour to that of control males provided with unscented pieces of filter paper (n = 18). We measured the occurrence of normal (e.g., locomotion) and abnormal (escape attempts) behaviours each day for three weeks. In addition, we conducted two exploration tests and a visual barrier test. Compared to controls, enriched lizards showed a consistent long‐term decrease (29%–38%) in the occurrence of escape attempts. During exploration tests, enriched lizards spent less time performing escape attempts and devoted more time to perching than controls. As expected, both control and enriched lizards showed a reduction of time in locomotion and an increase in the time spent perching between the first and second exploration test, but these changes were significantly more pronounced for enriched animals. Taken together, our results suggest improved welfare of enriched animals, as they spent less time engaging in abnormal behaviours, more time in normal behaviours, and showed signs of faster habituation to a novel environment. Chemosensory enrichment is a relatively simple enrichment strategy that could potentially be applied to improve the welfare of a wide range of captive lizards, and reptiles at large.     

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta)

Ring‐tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring‐tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species‐typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring‐tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring‐tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring‐tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.