Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Primate puzzleboard: A simple environmental enrichment device for captive chimpanzees

An environmental enrichment device was designed and evaluated for captive chimpanzees. The puzzleboard consisted of a 61-cm, square piece of clear plastic with holes of various sizes drilled into the center. The puzzleboard was bolted to the roof of a chimpanzee enclosure. Flavored primate treats were arranged on top of the board, and the chimpanzee used a finger to manipulate the food across the board to be retrieved through the larger holes. The behavior and puzzle use of 29 chimpanzees housed in eight groups were evaluated while the device was empty and while filled with food. For each group, four 1-hr scan samples were recorded for each condition. Data showed that an average of 40 min elapsed from the time the puzzleboard was filled to the last recorded contact by a subject. Mean individual use ranged from 4.8 to 23.8 min/hr. Female chimpanzees used the puzzle significantly more often than did males. Aggressive, affiliative, inactive, and self-directed behaviors were significantly reduced when the puzzle was filled. In addition, the puzzleboard was inexpensive, sturdy, and easily constructed, mounted, and operated.     

Behavioral responses of unrelated rhesus monkey females paired for the purpose of environmental enrichment

An attempt was made to socialize unrelated and unfamiliar adult rhesus monkey females that had lived in single cages for more than one year. Partners first were given the opportunity for noncontact familiarization in partitioned double cages. They were then transferred into an ordinary double cage. Clear-cut rank relationships were evident within the first 90 minutes of pair formation in 94% (17/18) of dyads tested. Only 28% (5/18) of pairs resorted to fighting (in no case with infliction of serious injury), while 50% (9/18) engaged in social grooming or hugging during this initial phase of pair formation. Eighty-three percent (15/18) of pairs were compatible, with none of the partners showing signs of depression and none inflicting serious injury on the other. Seventeen percent (3/18) of pairs were incompatible (two cases of depression, one serious tail injury) and were separated. It was concluded that the barren environment of singly caged rhesus monkey females can be enriched with little risk by carefully making them compatible companions.     

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.     

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.     

Preference assessments as a tool to evaluate environmental enrichment

Environmental enrichment is an important tool utilized to improve animal welfare in zoological institutions through opportunity for mental and physical stimulation. Many past studies have focused on the impact enrichment has on animal behavior; however, none have conducted preference assessments on enrichment items to examine the relationship between animals' preferences and interaction with enrichment over a 24-hr period. Ten-minute free operant, paired-choice preference assessments were implemented in Study 1 to determine the enrichment preferences of African lions (N = 3). Following Study 1, Study 2 was conducted, which examined the behavior of African lions with enrichment items over the course of 30, 24-hr trials to evaluate the relationship between preferences established in Study 1 and long-term interaction with the enrichment. Generalized estimating equations revealed a statistically significant relationship between the percentage of time the enrichment was approached first and the average duration of interaction in Study 1 to the total duration of interaction and the percent of hours interacted with the item in Study 2. Additionally, the first 2 min of the preference data resulted in comparable statistically significant findings, demonstrating shorter preference assessments can produce similar results. The results support our prediction that preference assessments can be used to estimate the amount of interaction with enrichment over the course of time, with preferred items being interacted with more frequently and in longer duration. Information gained from this study suggests preference assessments can be a time and cost-effective tool to evaluate enrichment preference and predicted efficacy.     

Causation and influence of environmental enrichment on feather picking of the crimson-bellied conure (Pyrrhura perlata perlata)

This study examined the effect of environmental enrichment on feather picking in the crimson-bellied conure Pyrrhura perlata perlata. A total of 10 conures was observed, 8 of which showed minor to severe plumage problems. In a pre-enrichment period the conures were observed without changes in the environment to assess their social behavior and activity patterns, in particular, feather picking behavior. Feather picking was self-inflicted; furthermore, conures with plumage problems spent more time on all comfort activities, including preening, and less time on flying and vocalization. In three successive periods, several enrichment materials were tested to examine whether, and how environmental enrichment altered their behavior. The conures preferred natural and edible enrichment materials over less natural ones. Observed changes in activity patterns were an increase in locomotion and a decrease in preening behavior. However, no improvement of the plumage was visible during the weeks of observation. The results suggest that environmental enrichment was successful in altering the behavior of conures, but had only a stabilizing effect on existing plumage problems. Zoo Biol 16:161–172, 1997. © 1997 Wiley-Liss, Inc.     

Variation in visitor perceptions of a polar bear enclosure based on the presence of natural vs. un-natural enrichment items

A debate exists among modern zoo staff as to whether or not the addition of un-naturalistic enrichment takes away from, or even defeats, the educational messages designers are trying to incorporate in naturalistic exhibits. A visitor study was conducted at the Central Park Zoo's polar bear exhibit in order to determine whether or not the type of enrichment in an enclosure actually alters guest perceptions. Visitors were exposed to one of two enrichment treatments in the bear enclosure: Naturalistic or Un-naturalistic. The results of this study suggest that enrichment type did not alter the perceptions of visitors. However, it did identify some of the different ways adults and youths perceive animals and zoos. Additionally, the study highlighted the varying perceptions individuals have of the concept of polar bears vs. their perceptions of the captive individuals at the Central Park Zoo. Implications for enrichment usage and exhibit design are discussed. Zoo Biol 28:292–306, 2009. © 2008 Wiley-Liss, Inc.     

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.     

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.     

The role of novelty and fat and sugar concentration in food selection by captive tufted capuchins (Sapajus apella)

Capuchins, like other primates, use feedback from sensory cues and digestion to make decisions about which foods to consume and which to avoid. However, little is known about how capuchins make consumption decisions when simultaneously presented with novel and familiar foods, or how food familiarity and macronutrient concentration together influence food choice, topics with potential implications for developmental and health research. In this study, we evaluated the role of familiarity, as well as fat and sugar concentration, in the food selections of captive tufted capuchins (Sapajus apella). In the first experiment, over 10 sessions, subjects were assigned to either a group that chose between one familiar and one novel food item both high in fat or sugar (high condition), or to a group that chose between one familiar and one novel food item both low in fat or sugar (low condition). In the second experiment, subjects were divided into three groups, familiarized with food over five feeding sessions, and then offered the familiarized food and a novel food that varied in fat or sugar for 10 sessions. When offered foods high in fat, capuchins showed no clear signs of neophobia, forming an initial preference for the novel food, rejecting foods less frequently, and selecting foods faster than when offered foods low in fat. These trends were generally not observed in response to foods with sugar. When presented with options that varied in macronutrient concentration, subjects showed an initial interest in the novel food irrespective of whether it was high in fat or sugar, yet formed a final preference for the higher-concentration item. Findings suggest that the concentration of fat or sugar in novel foods may be an important mediator of exploratory behavior and that capuchins rely on immediate feedback from taste and other sensory cues to make consumption decisions.     

Exposure to environmental enrichment elicits differential hippocampal cell proliferation: role of individual responsiveness to anxiety

Environmental enrichment (EE) is a largely employed behavioral procedure in which animals are exposed to high stimulation compared with conventional housing conditions. Animal exposure to an EE exerts beneficial effects on the performance of different learning tasks and induces a number of behavioral, neurochemical, and neuroanatomical changes including hippocampal cell proliferation. However, the importance of voluntary interaction with the environment in these changes has not been clearly resolved yet. Moreover, the effects of a complex environment on animal emotionality still remains questionable and has not been explored in detail under conditions that allow unmasking individual responses among subjects in a group. The present study was aimed at exposing groups of rats to an EE, and analyzing individual differences in activity levels during EE sessions. We observed differences with respect to the activity level displayed by rats during the enriched sessions, which correlated with differences in the rate of hippocampal cell proliferation. It is suggested that exposure to EE may reduce anxiety-like behaviors and may elicit individual differences on emotional reactions positively linked with hippocampal neurogenesis and testosterone levels.     

Effects of environmental enrichment and regrouping on natural autoantibodies-binding danger and neural antigens in healthy pigs with different individual characteristics

Pigs living in commercial husbandry systems may experience both acute stress due to standard management procedures and chronic stress through limitations in their barren housing environment. This might influence their immune status, including antibody responses to neural and danger autoantigens. Levels of natural autoantibody (NAAb)-binding phosphorylcholine-conjugated bovine serum albumin (PC-BSA) and myelin basic protein (MBP) were measured over time in pigs that were kept in environmental enriched v. barren housing, and that underwent a regrouping test. In total, 480 pigs were housed in 80 pens in either barren or straw-enriched pens from 4 through 23 weeks of age. Blood samples were taken from pigs before (week 8), and 3 days after a 24 h regrouping test (week 9), and at 22 weeks of age. Phosphorylcholine-conjugated bovine serum albumin (PC-BSA) and MBP antibody titres in serum were measured using ELISA. Enriched-housed pigs had higher levels of IgM-binding MBP, and tended to have higher levels of IgG-binding MBP and IgA-binding PC-BSA than barren-housed pigs. Each NAAb measured in this study was affected by gender and litter. These results suggest that enriched housing conditions, as well as acute regrouping stress, have an influence on levels of serum NAAb-binding danger and neural antigens in pigs.     

Maternal effects provide phenotypic adaptation to local environmental conditions

In outcrossing plants, seed dispersal distance is often less than pollen movement. If the scale of environmental heterogeneity within a population is greater than typical seed dispersal distances but less than pollen movement, an individual's environment will be similar to that of its mother but not necessarily its father. Under these conditions, environmental maternal effects may evolve as a source of adaptive plasticity between generations, enhancing offspring fitness in the environment that they are likely to experience. This idea is illustrated using Campanula americana, an herb that grows in understory and light-gap habitats. Estimates of seed dispersal suggest that offspring typically experience the same light environment as their mother. In a field experiment testing the effect of open vs understory maternal light environments, maternal light directly influenced offspring germination rate and season, and indirectly affected germination season by altering maternal flowering time. Results to date indicate that these maternal effects are adaptive; further experimental tests are ongoing. Evaluating maternal environmental effects in an ecological context demonstrates that they may provide phenotypic adaptation to local environmental conditions.     

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.     

Change of enclosure in langur monkeys: implications for the evaluation of environmental enrichment

A group of Hanuman langurs (Presbytis entellus) was studied before and after it was moved from an old cage‐style enclosure to a novel naturalistic environment at the London Zoo. Eating and locomotion occupied more of the langurs' time in their new enclosure, whereas dozing, allogrooming, and aggression decreased, along with an increase in inter‐individual distances. These changes are attributed to the larger area, the stimulating new environment, and the langurs' increased distance from visitors. Nevertheless, the study raises questions about how to define standards of desirable environmental enrichment, as the activity patterns recorded in both the old and new enclosures are within the variation observed in the wild. Zoo Biol 21:549–559, 2002. © 2002 Wiley‐Liss, Inc.