Applying Behavioral Conditioning to Identify Anticipatory Behaviors

The ability to predict regular events can be adaptive for nonhuman animals living in an otherwise unpredictable environment. Animals may exhibit behavioral changes preceding a predictable event; such changes reflect anticipatory behavior. Anticipatory behavior is broadly defined as a goal-directed increase in activity preceding a predictable event and can be useful for assessing well being in animals in captivity. Anticipation may look different in different animals, however, necessitating methods to generate and study anticipatory behaviors across species. This article includes a proposed method for generating and describing anticipatory behavior in zoos using behavioral conditioning. The article also includes discussion of case studies of the proposed method with 2 animals at the San Francisco Zoo: a silverback gorilla (Gorilla gorilla gorilla) and a red panda (Ailurus fulgens). The study evidence supports anticipation in both animals. As behavioral conditioning can be used with many animals, the proposed method provides a practical approach for using anticipatory behavior to assess animal well being in zoos.     

Visitors' Effects on the Welfare of Animals in the Zoo: A Review

Since the 1970s, research about zoo visitors' effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and—to alesser extent physiological—changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors' effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor-animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the “visitor effect” concept.     

Visitors' effects on the welfare of animals in the zoo: a review

Since the 1970s, research about zoo visitors' effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and—to alesser extent physiological—changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors' effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor-animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the “visitor effect” concept.     

Advances in Applied Zoo Animal Welfare Science

ABSTRACT

Nonhuman animal welfare science is the scientific study of the welfare state of animals that attempts to make inferences about how animals feel from their behavior, endocrine function, and/or signs of physical health. These welfare measurements are applicable within zoos yet inherently more complex than in farms and laboratories. This complexity is due to the vast number of species housed, lack of fundamental biological information, and relatively lower sample sizes and levels of experimental control. This article summarizes the invited presentations on the topic of “Advances in Applied Animal Welfare Science,” given at the Fourth Global Animal Welfare Congress held jointly by the Detroit Zoological Society and the World Association of Zoos and Aquariums in 2017. The article focuses on current trends in research on zoo animal welfare under the following themes: (a) human–animal interactions and relationships, (b) anticipatory behavior, (c) cognitive enrichment, (d) behavioral biology, and (e) reproductive and population management. It highlights areas in which further advancements in zoo animal welfare science are needed and the challenges that may be faced in doing so.     

Evaluating changes in salivary oxytocin and cortisol following positive reinforcement training in two adult male western lowland gorillas (Gorilla gorilla gorilla)

Positive reinforcement training (PRT) is associated with increases in species-typical behavior and decreases in stereotypic and abnormal behavior in participating animals. Physiological changes following PRT, for example, increases in oxytocin (OXT) and/or decreases in cortisol (CORT), may facilitate these behavioral changes. This study evaluated salivary OXT and salivary CORT concentrations in two adult male western lowland gorillas (Gorilla gorilla gorilla) following PRT with their primary animal care staff. Following PRT, no change in OXT was observed. CORT decreased in one subject following PRT. Changes in endogenous OXT are related to affiliative interactions and interact with strongly bonded conspecifics. PRT may not activate the oxytocinergic system because PRT is not a species-specific affiliative interaction and/or animal care staff are not viewed as conspecifics. Regardless, PRT may still be viewed as a positive interaction resulting in stress reduction via a decrease in CORT. Relationships are unique, thus these results only apply to these two gorillas and one animal caregiver. Larger population-level studies are needed to understand overall trends in human–animal interactions, and ultimately human–animal relationships. Further evaluation of physiological changes following human–animal interactions should be informative for understanding the human–animal relationship in zoos.     

Post-occupancy evaluation in the zoo

Post-occupancy evaluations (POE) of the built environment provide systematic information about the success or failure of environmental designs. Research instruments developed for application in human settings can also be adapted for use in zoos. The zoo environment must be evaluated for its impact on animal residents, zoo visitors and staff. Evaluations conducted by our Atlanta research team included studies of the Atlanta Zoo and zoos in nearby cities. The range of available methodologies are reviewed, and the unique constraints of zoo settings are discussed. Our studies indicate that naturalistic environments facilitate the expression of normal and complex animal behavior patterns and tend to enhance the visitor experience. POE represents an exciting new dimension in zoo research and promises to contribute to the success of future generations of zoo design.     

Psychological and social well-being of bony fishes in zoos and aquariums

Research on the behavior of animals in zoos has been conducted for decades and observations have provided information that has improved the psychological and social well-being of animals. However, research on fishes in zoos and aquariums seems to be lacking. Here we assess the current state of research on fishes in zoos and aquariums by surveying peer-reviewed literature. Our assessment differs from previous surveys in that we examine the taxonomic classes Chondrichthyes (sharks and rays) and Osteichthyes (bony fishes) separately. Our survey finds that bony fishes have been drastically underrepresented in zoo journals, more so than chondrichthyans, revealing an urgent need for zoos and aquariums to conduct research on the behavior of the bony fishes in their care, to ensure a positive state of psychological and social well-being. To plot a course for the future, we discuss the few studies that have been conducted on the behavior of bony fishes in zoos and aquariums, and we discuss research conducted on bony fishes in food-fish aquaculture and biomedicine to identify the types of studies that could be conducted in zoos and aquariums. We conclude that data-driven analyses of fish behavior could aid in development of evidence-based practices that enhance the well-being of bony fishes in zoos and aquariums, just as they already do for terrestrial animals.     

Dither: A unifying model of the effects of visitor numbers on zoo animal behavior

Interest in the impact of human presence on the behavior and well-being of zoo and aquarium animals is increasing. Previous work has conceptualized the presence of zoo visitors as having one of three impacts on the behavior of animals in zoos: positive, negative, or neutral. Research suggests the same species may exhibit all three responses under different conditions, calling into question whether the positive/negative/neutral framework is the most useful way of considering visitor impact on animal behavior. Here we present a model of visitor effects that unifies these three predictions. Our model suggests that zoo-goers may provide a “dither effect” for some animals living in zoos. We posit animals may show nonlinear behavioral responses over a range of visitor densities, effectively exhibiting changes in both comfortable and anxiety-like behaviors under different levels of human presence. We tested this model during two COVID-19 related closures at the San Francisco Zoo, studying seven species for evidence of nonlinear relationships between visitor numbers and animal behavior. Our results support the dither effect acting in several species observed.     

The influence of feeding,enrichment, and seasonal context on the behavior of Pacific Walruses (Odobenus rosmarus divergens)

Though some research exists concerning general behavior and activity patterns of Walruses in zoos or aquariums, less is known about how these patterns change in response to various environmental and temporal contexts. This study presents two studies assessing behavioral changes in relation to feeding period, object enrichment (OE), and season in a social group of four Pacific Walruses at the New York Aquarium. Study 1 examined behavior in relation to feeding context (nonfeed, prefeed, postfeed); data were collected over a three‐week period, resulting in 47 observation sessions for each feeding context. Study 2 examined behavior in relation to OE and season; data were collected in two phases resulting in 12 enrichment and 9 no‐enrichment (NE) observation sessions (Phase 1), and 21 enrichment and 18 NE observation sessions (Phase 2). Study 1 showed that after feeding, oral behavior increased while social behavior and total swim frequency decreased. In Study 2, both swim frequency and social behavior were found to interact with OE and phase, while oral behavior remained constant across all conditions. As in the wild, both studies found all animals to be swimming the majority of the time. Though every animal spent much of its swim time engaged in an Individual Swimming Pattern (ISP), both studies showed that the proportion of ISP (in relation to total time swimming) remained stable across all contexts, suggesting a potential functional role of the ISPs. These results are discussed in light of the ongoing debate over the role of stereotypies in welfare assessment. Zoo Biol 29:397–404, 2010. © 2009 Wiley‐Liss, Inc.     

Visitor Circulation and Nonhuman Animal Welfare: An Overlooked Variable?

This article investigates visitor circulation and behaviors within a gallery of primate exhibits in relation to their possible implications for nonhuman animal welfare. When entering a primate house, the majority of visitors (84%) turned right, a pattern upheld throughout all times of the day. These findings demonstrate the existence of the "right-turn" principle, a concept previously identified and investigated in the museum setting. The existence of this circulation pattern in zoos has important implications for the practical management of animal welfare issues because unbalanced or large numbers of visitors at specific enclosures could present a stressful influence. The "direction bias" could not be attributed to demographic or behavioral traits, therefore suggesting that the principle, like similar findings from museum research, generalizes across visitor populations and, therefore, zoos. A visitor sample at another exhibit (located outside the exhibit gallery) did not display a direction bias, suggesting that the marked circulation pattern may be specific to exhibit galleries. The article discusses the significance and consequences of visitor circulation with respect to visitor management and animal welfare.     

Toward a Science of Welfare for Animals in the Zoo

Although the accredited institutions of the Association of Zoos and Aquariums have all committed to enhancing the welfare of nonhuman animals, acceptable standards and best practices are still under debate. Currently, experts from zoos and the field hold widely divergent opinions about exhibition and management standards for elephants. Standards and practices for managing nonhuman primates provide a model for other nonhuman creatures exhibited in zoos and aquariums. Examining the key issues for primates demonstrates the value of applying scientific data before promulgating standards. The field of applied behavior analysis provides a wealth of information to frame the debate. Animal behaviorists have contributed to an emerging science of animal welfare, which may provide a foundation for empirical zoo management, standards, and practices.     

Toward a science of welfare for animals in the zoo

Although the accredited institutions of the Association of Zoos and Aquariums have all committed to enhancing the welfare of nonhuman animals, acceptable standards and best practices are still under debate. Currently, experts from zoos and the field hold widely divergent opinions about exhibition and management standards for elephants. Standards and practices for managing nonhuman primates provide a model for other nonhuman creatures exhibited in zoos and aquariums. Examining the key issues for primates demonstrates the value of applying scientific data before promulgating standards. The field of applied behavior analysis provides a wealth of information to frame the debate. Animal behaviorists have contributed to an emerging science of animal welfare, which may provide a foundation for empirical zoo management, standards, and practices.     

Zoo behaviour science in the Research Centre for Vertebrate Studies of the Academy of Sciences of the German Democratic Republic (in the Animal Park of Berlin)

This is a report of the results of behaviour science studies in the Animal Park of Berlin and the Academy of Sciences in the German Democratic Republic (G.D.R.). The major goal of this research is to investigate the behaviour of rare animals as a basis for zoological research, systematics and comparative studies in evolution. In addition, further research provided information directly applicable to behavioural management in zoos, farms and wild animal collections. Three main comparative studies dealt with urination and defecation in mammals, allelomimetic behaviour in vertebrates, and audio-visual orientation responses in several species of birds and mammals. Ethograms were created for the Red Woolly Opossum, Maned Wolf, Takin and Giant Eland Antelope. Social and reproductive behaviour studies were conducted on the Wolf, Golden Lion Marmoset, Père David's Deer, Mouflon and Wild Boar. Reports are included on the circadian activity of Pigmy Armadillo and Wild Boar. New information was revealed regarding communication in Mouflon and Père David's Deer, in addition to the new finding that some social behaviour patterns in Wild Boar are dependent on circadian rhythms. Three wolf packs studied consecutively in the same enclosure revealed that each pack differed in its social behaviour and that the dominant female (alpha female) determined the social structure. The problem of animal-human interactions is discussed. Zoos are seen as a medial stage between wilderness and farm management. It is suggested that an important task of zoo behaviour science is to study the ability of wild animals to adapt to purposes such as animal farms, animal husbandry institutes and domestic animal productivity, and to study the behaviour of the original forms of domestic animals in order to better understand and manage them.     

An investigation of browsing enrichment,especially non-leaf foraging,on giraffes (Giraffa camelopardalis reticulata) at Kyoto City Zoo in Japan

Browsing enrichment may aid in developing species-specific behaviors for giraffes managed in zoos as a means of improving animal welfare. By nature, giraffes are tree-feeding animals, including tree bark, but the extent of food other than leaves as a form of browsing enrichment has not been well investigated. Therefore, to investigate the effectiveness of non-leaf foraging, three giraffes at the Kyoto City Zoo in Japan were observed for 228 h from May 2019 to February 2020. In conjunction with behavioral instantaneous sampling, tree use (landscape tree or enrichment branch) and plant part (leaves, twigs, or barks) were recorded by the 1-0 sampling method. There was no significant change in the foraging behavior on the leaves of enriched branches, nor was there any significant change in the foraging behavior of the giraffes, except for one animal in the deciduous phase. No significant changes were observed in rumination or other behaviors between the two phases. Although vegetation foraging behavior significantly decreased, except for one animal, dry hay foraging behavior significantly increased in all the animals during the deciduous phase. Some individuals also showed a significant increase in the foraging behavior for non-leafy parts of the enrichment branches (twigs and bark) during the deciduous phase. This suggests that in some tree species, giraffes forage on the bark and twigs to compensate for the loss of leaves during the deciduous phase, similar to feeding on hay or hay cubes as a substitute for tree leaves.     

Increasing browse and social complexity can improve zoo elephant welfare

While recent work has assessed how environmental and managerial changes influence elephant welfare across multiple zoos, few studies have addressed the effects of management changes within a single institution. In this paper, we examine how management changes related to social structure and diet affect the behavior of a group of zoo elephants over a 23‐month period while also considering underlying factors, such as time of day, hormonal cycle, and individual differences. We recorded individual behaviors using 2‐min scan samples during 60‐min sessions. We analyzed behavioral changes across several study variables using generalized linear mixed models. We found that increasing browse can improve opportunities for foraging throughout the day but may not be sufficient to reduce repetitive behaviors. We observed that increasing group size and integration of bulls with cows can lead to increased social interaction in African elephants. Our results highlight the importance of using multiple management alterations to address elephant welfare, and considering environmental factors, when making management decisions.     

Preliminary evaluation of porcine zona pellucida (PZP) immunocontraception for behavioral effects in feral horses (Equus caballus)

Successful management of captive populations of wild animals requires effective control of reproduction. Contraception is one tool for controlling reproduction of animals in zoos; however, the options available to the animal manager are limited. Contraceptives vary in efficacy, reversibility, and side effects, and thus may not be suitable for widespread use. One consideration when selecting a contraceptive is its potential for side effects on behavior, especially given the fact that reproduction plays such a prominent role in the biology of any species. To date, there have been few evaluations of contraceptives for behavioral effects, and those that have been conducted have focused on hormone-based contraceptives. This study sought to evaluate a novel method of population control, immunocontraception, for behavioral effects in a population of feral horses. Porcine zona pellucida (PZP) immunocontraception prevents fertilization of ova and does not alter normal hormone secretion patterns. It therefore should leave the animal behaviorally intact in terms of reproductive behavior. The study examined the behavior of 43 sexually mature mares on Assateague Island during the 1997 breeding season and, with help from Earthwatch volunteers, collected observations over a 3-month period. The study found no significant differences between treated and untreated mares in general activity budget, aggression given or received, and spatial relationships relative to the stallion. These preliminary findings indicate that PZP contraception seems to have no acute behavioral effects on the behavior of individuals. The study findings also suggest that PZP could be a desirable and effective management tool for captive species in which social behavior plays an integral role in group dynamics. Analyses of group level effects and population level effects are continuing.     

Visitor circulation and nonhuman animal welfare: an overlooked variable?

This article investigates visitor circulation and behaviors within a gallery of primate exhibits in relation to their possible implications for nonhuman animal welfare. When entering a primate house, the majority of visitors (84%) turned right, a pattern upheld throughout all times of the day. These findings demonstrate the existence of the “right-turn ”principle, a concept previously identified and investigated in the museum setting. The existence of this circulation pattern in zoos has important implications for the practical management of animal welfare issues because unbalanced or large numbers of visitors at specific enclosures could present a stressful influence. The “direction bias ”could not be attributed to demographic or behavioral traits, therefore suggesting that the principle, like similar findings from museum research, generalizes across visitor populations and, therefore, zoos. A visitor sample at another exhibit (located outside the exhibit gallery) did not display a direction bias, suggesting that the marked circulation pattern may be specific to exhibit galleries. The article discusses the significance and consequences of visitor circulation with respect to visitor management and animal welfare.     

Can zoo records help answer behavioral research questions? The case of the left‐handed lemurs (Lemur catta)

Most zoos keep comprehensive records, which potentially form a database for use in answering some research questions, such as in veterinary and population management research. They have not, however, been widely used to answer questions about animal behavior and welfare. Here we try to assess the usefulness to behavioral research of two sorts of zoo records (ARKS, the Animal Records Keeping System, and student dissertations held on file) to test the hypothesis that ring-tailed lemurs with a left limb preference experience more negative social lives. We found that, as predicted, lemurs with a left limb preference (LH) received more aggression and were involved in less grooming than nonleft-preferent lemurs (NLH), though the differences were not statistically significant. Contrary to prediction, LH lemurs had fewer reported woundings than NLH lemurs, but again the difference was not statistically significant. We found that the ARKS reports did not contain sufficient quantified and systematic behavioral data for our purposes, although otherwise they provided an excellent context for interpreting results. The student dissertations were also of limited use, primarily because of the small time frame in which they were carried out. Because of these shortcomings we were unable to distinguish whether our inability to find significant effects was due to biological (perhaps hand preference had no consequences for the lemurs) or data reasons. We suggest that closer liaison between zoo research staff, zoo record keepers and academic supervisors could help to improve the usefulness of zoo records for behavioral research.