Philosophy of environmental enrichment: Past,present, and future

The brief tenure of environmental enrichment has been influenced both directly and indirectly by the field of psychology, from the work of B.F. Skinner to that of Hal Markowitz. Research on enrichment supports the supposition that an enriched environment does indeed contribute to a captive animal’s well‐being. Critical elements of effective environmental enrichment are 1) assessing the animal’s natural history, individual history, and exhibit constraints and 2) providing species‐appropriate opportunities, i.e., the animal should have some choices within its environment. This paper presents a historic perspective of environmental enrichment, proposes a broader, more holistic approach to the enrichment of animals in captive environments, and describes a framework or process that will ensure a consistent and self‐sustaining enrichment program. Zoo Biol 20:211–226, 2001. © 2001 Wiley‐Liss, Inc.     

Behaviour as a tool in the assessment of animal welfare

A central issue in animal welfare research is how to assess the welfare state of animals objectively and scientifically. I argue that this issue can be approached by asking two key questions: 1) is the animal physically healthy and 2) does the animal have what it wants? Behaviour is used to answer both of these questions. In the assessment of physical health, it can be used for clinical and pre-clinical diagnosis. In the assessment of what animals want, it has a major role through choice and preference testing. It is particularly important that applied ethologists develop methods for assessing welfare in situ--in the places where concern for animal welfare is greatest such as on farms and in zoos.     

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.     

Mirrors as environmental enrichment for African green monkeys

Stainless steel circular mirrors were employed in an enrichment plan for 105 singly housed male African green monkeys. We observed 25 randomly selected males to measure mirror use and to assess the mirrors' effectiveness as an enrichment item. We conducted additional mirror-use surveys on all 105 males using fingerprint accumulation as an indicator (rated on a scale of 0 to 4). Use was defined as either being in contact with the mirror (contact use (CU)) or looking directly into the mirror without contact (non-contact use (NC)). Mirror-use data were collected 10 months after the initial introduction of the mirrors and again at 16 months. The two time points were compared by paired t-tests. No significant difference in use was found between the two data collection points. On average, the monkeys used the mirrors 5.2% of the total time intervals recorded (approximately 3 min/hr). Results from the five fingerprint-accumulation surveys showed that 102 of 105 males (97%) had CU with their mirrors over the survey points. Based on the sustained use of the mirrors over a 6-month period, we concluded that the mirrors were an effective enrichment tool that the vast majority of our monkeys routinely used. Habituation did not appear to occur even a year after the mirrors were introduced.     

Environmental enrichment improves behaviors rather than the growth and physiology of rock bream Oplegnathus fasciatus

Environmental enrichment has the potential to improve the welfare and post-release survival of hatchery fish stocked for conservation purposes. However, the effectiveness of environmental enrichment is partly dependent on the fish species, life stage, and specific enrichment structure used. To enhance the effectiveness of environmental enrichment, it is crucial to focus on characteristic differences in enrichment structures, such as type and level. This study investigated how differences in enrichment type and level affected physiological and behavioral aspects of the welfare of pre-release juvenile rock bream Oplegnathus fasciatus by evaluating growth performance, basal and stressed cortisol levels, antioxidant enzyme activities, and exploratory behaviors regarding anxiety and flexibility. Fish were reared for 4 weeks in different enrichment treatments: barren, low-level cover structure, high-level cover structure, low-level interference structure (LI), and high-level interference structure (HI). The results revealed that fish reared with the LI treatment showed less anxiety and greater flexibility with respect to exploratory behaviors, without oxidative damage being detected. Despite exhibiting less anxiety as well, fish reared in the HI treatment had oxidative damage, indicated by lower superoxide dismutase activity, compared to those in the barren treatment. In addition, none of these enrichment structures enhanced growth performance or mitigate chronic and acute stress responses. Overall, the low-level interference structure may be more favorable in promoting the behavioral welfare of the fish. Application of this type and level of enrichment may increase the survival of the hatchery fish after release, which is critical to stocking success.     

Environmental enrichment for captive stumptail macaques (Macaca arctoides)

Background  The behavior of animals is modified by captivity. Environmental enrichment (EE) is a program designed to enhance the welfare of confined animals by providing them with a more stimulating background. This is carried out by the implementation of a series of activities that encourages them to present behaviors typical of their species, as well as keeps them active. The aim of this study was the evaluation of the influence of the EE in the behavioral variables in a colony of 24 stumptail macaques ( Macaca arctoides ). Our hypothesis is that the application of this program will reduce aggression, stereotypes and coprophilia behaviors and, at the same time, will increase exploration and solitary play.
Methods  The behavioral frequency previous to EE was compared with that during EE implementation.
Results  Our results showed that aggression, coprophilia stereotypic behaviors and social play were significantly reduced during EE, whereas exploration was significantly enhanced. The response of the individuals according to gender was similar for both sexes.
Conclusions  Environmental enrichment programs are indispensable for captive animals' wellbeing as they reduce aggression and stress while providing animals both physical and cognitive entertainment.     

Effects of environmental enrichment on activity and lameness in commercial broiler production

The aim of this pilot study was to investigate the effects of commercially applied environmental enrichments on behavior and lameness in broilers. Two consecutive flocks of broilers were observed at 16 days and 30 days of age to investigate differences between enriched (peat, bales of lucerne hay, and elevated platforms) and control birds with regards to behavioral activities and lameness. More running (p < .001), worm running (p = .006), play fighting (p = .015), dust bathing (p = .009), and ground pecking while standing (p < .001) were observed at 16 days than at 30 days. Across both ages, enriched birds showed more wing flapping (p = .016), wing stretching (p = .002), body shaking (p = .002), ground scratching (p < .001), and ground pecking while standing (p < .001) and lying (p = .003) compared with control birds. Even when no enrichments were close, enriched birds showed more body shaking (p = .008) and ground pecking while standing (p < 0.001) and lying (p = .010) than birds in comparable locations in control pens. There was a tendency for a lower gait score (i.e., reduced lameness) with the enriched treatment (p = .077). In conclusion, enriched birds showed higher levels of several activities compared with control birds, and demonstrated higher levels in areas where no enrichments were present.     

Gnawing bones as enrichment for farmed blue foxes ( Vulpes lagopus)

According to present acts and regulations, farmed foxes shall have a gnawing or other enrichment object in their cages. However, research on the welfare effects of gnawing objects has been scarce. We assessed physiology and health, that is weight development, urinary cortisol-creatinine ratio, serum cortisol level after adrenocorticotropic hormone administration, internal organ masses and incidence of gastric ulcerations as well as dental and overall oral health, in pair-housed juvenile blue foxes that were housed either with or without a possibility to interact with bones (cattle femur) during their growing season (July to December). The results show that the physiological effects of the possibility to interact with bones were either non-significant or suggested that competition for bones may jeopardize the welfare of subordinate individuals. However, the results clearly show that gnawing bones are beneficial for the dental health of farmed foxes.     

Coated nuts as an enrichment device to elicit tool use in tufted capuchins (Cebus apella)

The present paper describes a simple technique that hardens the shell of nuts and makes the use of a tool to crack them open more compelling. Walnuts were coated with a dough of sawdust and nontoxic white glue in different combinations; they were tested for hardness by using machines normally used to test different kinds of wood. Data on relative hardness for uncoated walnuts and walnuts coated with dough of two different combinations are presented. The coated walnuts were significantly harder to break than the uncoated ones, whereas no significant difference was found when comparing the hardness of two types of coated walnuts. Furthermore, observations on a captive group of tufted capuchins (Cebus apella) are described. The monkeys needed significantly more time to break open the coated walnuts. Early results show that coated walnuts may favor acquistion of tool use skills in a juvenile capuchin.     

Stereotypic behavior and fecal cortisol level in captive giant pandas in relation to environmental enrichment

Stereotypic behavior is exhibited by a wide range of captive animals. Its association with hormones, especially elevated cortisol level and lack of naturalistic stimuli in the environment, has been little studied. This study hypothesizes that stereotypic behavior is caused by stress due to lack of appropriate, naturalistic stimuli in the environment. Using four adult pandas (Ailuropoda melanoleuca) in the Beijing Zoo from March–July in 2003, we tested the following predictions: 1) stereotypic behavior and fecal cortisol level will not change associated with the progress of reproductive state; 2) there is a positive correlation between the occurrence of stereotypic behavior and fecal cortisol level; and 3) environmental enrichment by adding a naturalistic stimulus will reduce both stereotypic behavior and fecal cortisol level. We did not find any significant differences in the occurrence of stereotypic behavior and fecal cortisol level but did find a significant difference in the total time engaged in displaying the stereotypic behavior among the three estrous periods. The level of stereotypic behavior was correlated with elevated fecal cortisol level. Enrichment simply by adding a naturalistic stimulus did not show significant effects on stereotypic behavior, or on fecal cortisol level. Our results supported the second prediction, but did not completely support the first and the third ones perhaps because of the small sample size. Additionally, our results showed that stereotypic behavior might be a response to a heightened level of cortisol. Zoo Biol 0:1–15, 2006. © 2006 Wiley‐Liss, Inc.     

Examining deep litter as environmental enrichment for a family group of wolf's guenons,Cercopithecus wolfi

Manipulable substrates promote species‐typical behavior and decrease abnormal behavior in a variety of primate species. However, the effects of providing litter to arboreal primates are not as well studied, and there is little information specifically concerning enrichment for guenons. To inform the captive management of an under‐studied species, we evaluated deep litter substrate as environmental enrichment for a family group of Wolf's guenons, Cercopithecus wolfi. We expected it to promote species‐typical behavior and to act as an intervention by reducing aggressive behaviors targeted toward a juvenile group member by his parents. We compared the guenons' behavior during baseline periods in which normal husbandry routines were followed to periods when the entire floor of their enclosure was covered with 30 cm of straw or wood wool. We then evaluated the group's preference between litters by comparing their relative use. The guenons spent more time feeding and were more active during both litter conditions, but relative to their respective baselines, they spent more time examining straw and less time examining wood wool. Straw, but not wood wool, promoted some affiliative behavior as well as greater tolerance of the juvenile's social proximity to others. However, the addition of deep litter did not ameliorate patterns of agonistic behavior among our subjects. Our results suggest that straw conferred greater behavioral benefits than wood wool as a deep litter substrate for this guenon group and may constitute a form of environmental enrichment for this species. Zoo Biol 29:626–632, 2010. © 2009 Wiley‐Liss, Inc.     

Training penguins to interact with enrichment devices for lasting effects

The modern zoo has brought about two major advances in the behavioral welfare of their exhibited animals: (a) The use of environmental enrichment to promote naturalistic behaviors and (b) the use of training to improve voluntary husbandry care. Whereas training itself has been talked about as an effective enrichment strategy, little has been done to combine training procedures with enrichment. Typically, enrichment is treated as a trial and error process, where potential enrichment items or procedures are cycled through until successful enrichment is found. The use of shaping or other training techniques has seldom been documented to increase engagement with possible enrichment items or procedures. The following study examined the possibility of combining training and enrichment to produce continued interactions with enrichment devices. Two species of penguin, Magellanic and southern rockhopper penguins, were studied. Two measures were taken: Time spent swimming and contact with enrichment devices. The enrichment devices could be manipulated by placing fish within and hanging out of each device. During baseline sessions, no hits to either device were observed. During training sessions, several hits were recorded when fish were in the devices and overall swimming time increased during these conditions. When baseline was reintroduced without fish in the devices, contact with the enrichment devices rapidly declined and swimming time for the rockhopper penguins decreased. When the devices were reintroduced with fish but without training, the greatest number of enrichment device contacts and the highest percentage of time spent swimming were observed for the rockhopper penguins.     

Physical enrichment research for captive fish: Time to focus on the DETAILS

Growing research effort has shown that physical enrichment (PE) can improve fish welfare and research validity. However, the inclusion of PE does not always result in positive effects and conflicting findings have highlighted the many nuances involved. Effects are known to depend on species and life stage tested, but effects may also vary with differences in the specific items used as enrichment between and within studies. Reporting fine-scale characteristics of items used as enrichment in studies may help to reveal these factors. We conducted a survey of PE-focused studies published in the last 5 years to examine the current state of methodological reporting. The survey results suggest that some aspects of enrichment are not adequately detailed. For example, the amount and dimensions of objects used as enrichment were frequently omitted. Similarly, the ecological relevance, or other justification, for enrichment items was frequently not made explicit. Focusing on ecologically relevant aspects of PE and increasing the level of detail reported in studies may benefit future work and we propose a framework with the acronym DETAILS ( D imensions, E cological rationale, T iming of enrichment, A mount, I nputs, L ighting and S ocial environment). We outline the potential importance of each of the elements of this framework with the hope it may aid in the level of reporting and standardization across studies, ultimately aiding the search for more beneficial types of PE and the development of our understanding and ability to improve the welfare of captive fish and promote more biologically relevant behaviour.     

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.     

Evaluation of a chimpanzee enrichment enclosure

A large, three-part playground for captive chimpanzees was constructed and evaluated in terms of area use and behavior changes. Comparative behavioral samples were obtained on 38 subjects in the existing indoor-outdoor run and in the enclosure. The chimpanzees used the inside run, connective chute, concrete slab, and grass areas most. Activity and environmental manipulation increased in the enclosure while abnormal and self-directed behaviors decreased.     

Assessment of environmental enrichment for different primate species under low budget: A case study

The 2011 European Union Zoo Inquiry presented evidence that most zoos fail to achieve adequate levels of nonhuman animal welfare. Appropriate environmental enrichment (EE) can play a role in the promotion of welfare. However, financial and staff constraints frequently make it challenging to implement EE on a daily basis. The aim of this study was to test how individuals of three different nonhuman primate species at the Maia Zoo in Portugal (white-handed gibbons, Hylobates lar; Mona monkeys, Cercopithecus mona; and brown lemurs, Eulemur fulvus) reacted to EE devices. Another aim was to investigate whether simple, inexpensive devices can have positive outcomes for animal welfare. The results showed that all individuals reacted to the EE intervention, but individual responses to the EE devices differed. EE devices had consistently positive effects for all three species as demonstrated by an increase in the expression of natural behaviors and a general decrease in abnormal behaviors (46% compared with baseline). This study demonstrates that it is important to simultaneously test multiple individuals from different species in different situations to evaluate the effectiveness of EE.