An Empirical Case Study Examining Effectiveness of Environmental Enrichment in Two Captive Australian Sea Lions (Neophoca cinerea)

This case study examined the effect of environmental enrichment on the activity budgets of a male and female Australian Sea Lion (Neophoca cinerea) housed together at Adelaide Zoo. Using non-food-related (intrinsic) and food-related (extrinsic) enrichment objects, the study conducted an ABABA (withdrawal) experimental design over a 30-day period (180 hr). The study expected extrinsically reinforcing objects to be more effective than intrinsically reinforcing objects in reducing pattern swimming. The male sea lion spent more than 45% of scans engaged in pattern swimming during the initial baseline, which was reduced by at least 25% when enrichment items were present. However, there was no evidence of stereotypic behavior in the female sea lion, indicating that individual differences may exist. When enrichment was present, the study observed more active behaviors in both nonhuman animals. They spent more time interacting with the non-food-related objects overall. Therefore, introducing simple enrichment devices offers a cheap, practical, and effective method of adding complexity to the environment, which is likely to benefit the animals' welfare and enhance the zoo-visitor experience.     

Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and research

Environmental conditions such as housing and husbandry have a major impact on the laboratory animal throughout its life and will thereby influence the outcome of animal experiments. However, housing systems for laboratory animals have often been designed on the basis of economic and ergonomic aspects. One possible way to improve the living conditions of laboratory animals is to provide opportunities for the animals to perform a species-specific behavioral repertoire. Environmental enrichment should be regarded both as an essential component of the overall animal care program and equally important as nutrition and veterinary care. The key component of an enrichment program is the animal staff, whose members must be motivated and educated. It is critically important to evaluate environmental enrichment in terms of the benefit to the animal by assessing the use of and preference for a certain enrichment, the effect on behavior and the performance of species-typical behavior, and the effect on physiological parameters. At the same time, it is necessary to evaluate the impact on scientific outcome, how the enrichment influences the scientific study, and whether and how the statistical power is affected. The result will depend on the parameter measured, the type of enrichment used, and the animal strain. In this article, goals of enrichment are defined and discussed. Animal behaviors and needs are described, along with the translation of those needs into environmental enrichment programs. Specific types of environmental enrichment are outlined with examples from the literature, and an evaluation of environmental enrichment is provided.     

Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques

Operant conditioning using positive reinforcement techniques has been used extensively in the management of nonhuman primates in both zoological and laboratory settings. This research project was intended to test the usefulness of counter-conditioning techniques in reducing the fear-responses of singly housed male rhesus macaques living in the laboratory environment. A total of 18 male rhesus macaques (Macaca mulatta) were selected for this project and randomly assigned to one of three groups: a desensitization training group, a husbandry training group, or a control group. Behavioral data were collected before and after a 6 weeks training and/or habituation period during which the first two groups received a total of 125 min of positive reinforcement training (and also were assumed to undergo habituation to the environment) and the control group experienced only simple habituation to the environment. Based on a Wilcoxon Matched-Pairs Sign Test, we found that a significant proportion of animals exposed to desensitization training showed a reduction in the rate at which they engaged in cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), cringing in general (exact significance=0.016, one-tailed, N-ties=6), and in stress-related behaviors (exact significance=0.016, one-tailed, N-ties=6). This was not the case for animals exposed to basic husbandry training or animals in the control group. A significant proportion of desensitization-exposed animals also showed a reduction in the duration of time spent cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), but not in cringing behaviors in general or in stress-related behaviors. There were not a significant proportion of animals in either the husbandry training group or the control group that showed a decrease in duration of these behaviors. Results of this study could enhance both laboratory animal welfare and laboratory animal research, and could be a first step in developing techniques for reducing fearful behavior in rhesus monkeys in the laboratory environment.     

Assessing the effectiveness of environmental enrichment in bottlenose dolphins (Tursiops truncatus)

Environmental enrichment is often used to improve well-being and reduce stereotyped behaviors in animals under human care. However, the use of objects to enrich animal environments should not be considered to be effective until its success has been scientifically demonstrated. This study was conducted at Asterix Park in France in April 2009. The study investigated the use of 21 familiar objects with a group of six bottlenose dolphins (Tursiops truncatus). The dolphin trainers introduced four different objects into the dolphin pool every day on a rotating basis. Using a focal-object sampling method, we collected and analyzed data from twenty-one 15 min sessions. The results revealed a positive correlation between interest behaviors and interactive behaviors. Some dolphins had "favorite toys". However, only 50% of objects elicited manipulative behaviors. These findings demonstrate that dolphins do not treat all objects provided to them as "toys". Behavioral changes in the animals subsequent to the introduction of objects do not necessarily indicate an enrichment effect of the objects; rather, the motivation for the dolphins' behaviors toward the objects must be investigated. The animals' behavior must be considered in light of the social context and of the animals' individual behavioral profiles. The relevance of a constructivist approach to evaluating the effectiveness of enrichment programs is discussed.     

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.     

Human–Ape Interactions in a Zoo Setting: Gorillas and Orangutans Modify Their Behavior Depending upon Human Familiarity

Understanding how human presence influences animal behavior, specifically the behavior of nonhuman primates, has important implications for methodology in cognitive and behavioral studies, for our understanding of human–animal relationships and for animal welfare in captive settings. Conducted in the San Diego Zoo, this study partially replicates an existing study on human–animal relationships, which focused on familiarity effects on the human-directed behavior of great apes residing in the Toronto Zoo. Such a replication in a new location and with different individuals is necessary to expand sample size and to better understand how ontogeny and living environment influence human-directed ape behavior. All-occurrence sampling of human-directed behavior was used to gather data on two gorilla groups and one orangutan group, all housed at the San Diego Zoo. The aim was to compare ape-initiated behaviors toward zoo staff with apeinitiated visitor-directed behavior, in accordance with predictions of the Human–Animal Relationship (HAR) model. Overall, human-directed behaviors were more frequent toward visitors than toward staff, mainly caused by increased visitor-directed visual behavior, specifically brief glances. Given that visual monitoring has been seen as fearful behavior, potentially related to predator monitoring, this would confirm the expectation that lack of familiarity will lead to increased visual vigilance. However, the visitor-directed visual behaviors may not be antagonistic or fearful. Considering the specific behaviors and exhibit designs, curiosity may be an equally likely explanation in this context. Aiming to also understand whether these groups exhibited species differences in human-directed behavior, it was found that orangutans engaged in more affiliative behavior overall than gorillas. Comparing our results with the previous study, we conclude that while effects of familiarity are present, those effects are modulated by both individual ontogeny and exhibit design. While the HAR model is partially supported, additional factors may need to be included to fully interpret the observed behavior. Additional research is needed to further understand the effects of species, sex, and ontogeny on the predictions of the HAR model.     

Habituation and the reinforcing effectiveness of visual stimuli

The term "sensory reinforcer" has been used to refer to sensory stimuli (e.g. light onset) that are primary reinforcers in order to differentiate them from other more biologically important primary reinforcers (e.g. food and water). Acquisition of snout poke responding for a visual stimulus (5s light onset) with fixed ratio 1 (FR 1), variable-interval 1min (VI 1min), or variable-interval 6min (VI 6min) schedules of reinforcement was tested in three groups of rats (n=8/group). The VI 6min schedule of reinforcement produced a higher response rate than the FR 1 or VI 1min schedules of visual stimulus reinforcement. One explanation for greater responding on the VI 6min schedule relative to the FR 1 and VI 1min schedules is that the reinforcing effectiveness of light onset habituated more rapidly in the FR 1 and VI 1min groups as compared to the VI 6min group. The inverse relationship between response rate and the rate of visual stimulus reinforcement is opposite to results from studies with biologically important reinforcers which indicate a positive relationship between response and reinforcement rate. Rapid habituation of reinforcing effectiveness may be a fundamental characteristic of sensory reinforcers that differentiates them from biologically important reinforcers, which are required to maintain homeostatic balance.     

Activity‐based exhibition of five mammalian species: Evaluation of behavioral changes

Activity‐based management of captive animals involves the training and movement of animals among several exhibits and holding areas. We studied the effectiveness of this system in producing variation in behavior, controlling stereotypies, and eliciting natural behaviors. Twelve animals representing five species of mammals (orangutans, siamangs, tapirs, babirusa, and Sumatran and Siberian tigers) were the subjects of focal observations measuring activity levels, stereotypies, natural behaviors, and space utilization. Statistical analysis was used to assess the association between variation in behavior and the movement among the four exhibits. For several animals, the persistence of behavioral changes was studied over a period of 3 years. We also examined the influence of the previous animal in the exhibit on the focal animal. Moving animals among the exhibits affected activity levels and/or space utilization in all animals in the activity‐based management system. In cases for which 3‐year data were available, there was evidence of habituation to the novelty of changing exhibits. Stereotypies, usually in the form of pacing, were affected by exhibits, providing the opportunity to manipulate these behavior patterns by exhibit placement. Natural behaviors in the form of urine‐spraying by the female tapir and the Sumatran tiger were affected by which animal had previously been in the exhibit. The results support the conclusion that exposure to varying exhibits produces variation in the behavior of the animals and elicits natural behaviors that would be unlikely to occur in a traditional single‐species exhibit. Activity‐based management provides unique opportunities for the behavioral enrichment of captive animals. Zoo Biol 22:269–285, 2003. © 2003 Wiley‐Liss, Inc.     

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.     

Effects of environmental enrichment on reproduction

Although there have been few demonstrations of a direct empirical relationship between environmental enrichment and reproductive success in captive animals, indirect and anecdotal evidence indicates the importance of physical and temporal complexity for reproduction. We discuss three major mechanisms through which environmental enrichment that specifically increases the complexity of an animal's surroundings may influence reproductive physiology and behavior: developmental processes, modulation of stress and arousal, and modification of social interactions. In complex environments developing animals learn that performing active behavior produces appropriate functional outcomes. Learning to control their environment influences their ability to adapt to novel situations, which may profoundly influence their reproductive behavior as adults in breeding situations. Chronic stress may compromise reproductive physiology and behavior; enrichment reduces stress by providing increased opportunity for behavioral coping responses. However, some degree of acute stress may be beneficial for reproduction by maintaining an animal's level of responsiveness to socio-sexual stimuli necessary for sexual arousal and reproductive activation. Finally, environmental enrichment may influence reproductive success by stabilizing social groups, reducing aggression and increasing affiliative and play behaviors. It is concluded that multi-variate multi-institutional behavioral research in zoos will play an increasingly important role in the successful captive propagation of many species by closely examining relationships between environmental variables and reproductive potential of individual animals. © 1994 Wiley-Liss, Inc.     

Housing, husbandry and handling of rodents for behavioral experiments

Most animals used in research are rodents, mainly mice because of their predominance in genetics and molecular biology. This article attempts to provide an introduction to mice and rats: health considerations (of the experimenter); choice of species, age, strain and sex; housing and environmental enrichment; and animal identification, handling and dosing. These considerations apply to animal work in general; the rest of the article focuses on the preliminary aspects of behavioral testing, including a protocol for an open field test. This procedure is traditionally associated with activity measurements, and although automated versions are readily available these days, the latter are expensive and may be unavailable in many non-behavioral departments. Moreover, particularly when testing novel genetically modified animals or pharmacological agents, there is no substitute for direct visual observation to detect abnormal signs in the animals: for example, ptosis, piloerection, tremor, ataxia or exophthalmos. The open field test can be adapted in several ways: to assess general behavior and activity (similar to a primary screen in the pharmaceutical industry) or to measure memory (habituation) or anxiety.     

Behavioral effects of environmental enrichment on harbor seals (Phoca vitulina concolor) and gray seals (Halichoerus grypus)

Zoos and aquariums have been incorporating environmental enrichment into their animal care programs for the past 30 years to increase mental stimulation and promote natural behaviors. However, most attempts to document the effects of enrichment on animal behavior have focused on terrestrial mammals. Staff at the National Aquarium in Baltimore conducted an investigation of the behavioral effects of enrichment on the seven harbor seals and two gray seals housed in the aquarium's outdoor seal exhibit. We expected that enrichment would change the amount of time the animals spent engaged in specific behaviors. The behaviors recorded were: resting in water, resting hauled out, maintenance, breeding display, breeding behavior, aggression, pattern swimming, random swimming, exploration, and out of sight. Activity levels (random swimming and exploration) were expected to increase, while stereotypic behaviors (pattern swimming) were expected to decrease. The frequency and duration of behaviors were documented for 90 hr in both the control phase (without enrichment) and the experimental phase (with enrichment). Statistically significant differences (P<0.05) in the time spent in pattern swimming, random swimming, exploration, and out of sight were observed between the two phases. With enrichment, pattern swimming and out of sight decreased, while random swimming and exploration behavior increased. These findings demonstrate that enrichment can promote behaviors (random swimming and exploration) that are likely to be normal for phocids in the wild, and that may contribute to the behavioral complexity of these seals in captivity. Zoo Biol 21:375–387, 2002. © 2002 Wiley‐Liss, Inc.     

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.     

Operant behavior in dwarf hamsters (Phodopus campbelli): Effects of rate of reinforcement and reinforcer flavor variety

We investigated operant behavior in a novel species, the dwarf hamster (Phodopus campbelli). In two experiments, hamsters were trained to lever-press for food reinforcement. In Experiment 1, rate of reinforcement was manipulated across conditions using four variable-interval schedules of reinforcement (delivering one to eight reinforcers per min). As predicted, within-session decreases in responding were steepest on the richest schedule. In Experiment 2, lever-pressing was reinforced by either a constant or a variety of flavored food pellets. Within-session decreases in responding were steeper when the reinforcer flavor remained constant than when it was varied within the session. In both experiments, subjects hoarded most reinforcers in their cheek pouches rather than consuming them in the operant chambers. These results are incompatible with post-ingestive satiety variables as explanations for within-session decreases in operant responding and suggest that habituation to repeatedly presented reinforcers best accounts for subjects’ response patterns. Additionally, a mathematical model that describes behavior undergoing habituation also described the present results, thus strengthening the conclusion that habituation mediates the reinforcing efficacy of food.     

Survey of stereotypic behavior in prosimians

Captive animals have been observed to perform a variety of stereotypic behaviors. However, little is known about stereotypic behavior in prosimians. We sent surveys to 96 AZA-accredited institutions to examine stereotypic behavior in these primates. Forty-eight surveys were returned, providing information on 440 individuals of 10 genera. According to the responses, 13.2% of the prosimians surveyed exhibited some form of stereotypic behavior. Pacing was the most common behavior. A logistic regression was used to examine intrinsic characteristics that might influence the performance of stereotypic behavior. The genus of the prosimian was a significant predictor of stereotypic behavior. Individuals of the genus Varecia and Microcebuswere more likely to engage in stereotypic behavior than members of the other genera. Rearing history, age, and sex were not significant predictors of stereotypic behavior. To examine the influence of extrinsic variables on stereotypic behavior, we transformed the data into the percentage of individuals within the enclosure that were reported to exhibit stereotypic behavior, and analyzed them at the enclosure level using a general linear model (GLM) analysis of variance (ANOVA). The only environmental variable that significantly predicted stereotypic behavior was the frequency with which enrichment was provided. Frequent enrichment was provided to those exhibits with a higher percentage of prosimians that engaged in stereotypic behavior. The results of this survey suggest that stereotypic behavior in prosimians may be associated with intrinsic factors (i.e., individual or genus differences) in addition to extrinsic factors related to housing. This knowledge may be helpful in identifying the causes of and effective treatments for stereotypic behavior in prosimians.     

Genetic engineering and other factors that might affect human-animal interactions in the research setting

Evidence exists, particularly in the welfare literature of nonhuman animals on the farm, that the interaction between nonhuman animals and the personnel who care for them can have a strong effect on the animals' behavior, productivity, and welfare. Among species commonly used for biomedical research, mice appear to be the least-preferred species in animal care facilities. A review of the literature and observations of animal care staff interacting with mice indicated that the following factors may influence this: their small size, their particular behavioral characteristics, and husbandry constraints (such as housing in ventilated racks). In addition, this study questioned whether animal care personnel have a different perception of genetically engineered animals and whether this, in turn, has an effect on their interactions with these animals. The ability to carefully observe an animal's behavior is key in carrying out an animal-wellness assessment and in minimizing pain and distress. Attention to human-animal interactions in the research setting represents an opportunity for refinement for large numbers of animals and potentially for reduction of animal use.     

Genetic Engineering and Other Factors That Might Affect Human-Animal Interactions in the Research Setting

Evidence exists, particularly in the welfare literature of nonhuman animals on the farm, that the interaction between nonhuman animals and the personnel who care for them can have a strong effect on the animals' behavior, productivity, and welfare. Among species commonly used for biomedical research, mice appear to be the least-preferred species in animal care facilities. A review of the literature and observations of animal care staff interacting with mice indicated that the following factors may influence this: their small size, their particular behavioral characteristics, and husbandry constraints (such as housing in ventilated racks). In addition, this study questioned whether animal care personnel have a different perception of genetically engineered animals and whether this, in turn, has an effect on their interactions with these animals. The ability to carefully observe an animal's behavior is key in carrying out an animal-wellness assessment and in minimizing pain and distress. Attention to human-animal interactions in the research setting represents an opportunity for refinement for large numbers of animals and potentially for reduction of animal use.     

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.     

Response to novel objects and foraging tasks by common marmoset (Callithrix jacchus) female pairs

The authors analyze the effects of enrichment devices on the behavior of common marmoset female pairs, and determine which aspects of these devices are more likely to elicit explorative behaviors, and how their presence affects aggressive and stress-related behaviors. The results support the use of enrichment devices for captive primates and show that in marmosets, their effectiveness strongly depends on location within the enclosure and the presence of hidden food.