A turtle cognition research demonstration enhances visitor engagement and keeper-animal relationships.

Environmental enrichment techniques present animals with cognitive challenges while providing them opportunities to make choices and exert control over their environment. In this way, cognitive research and training is enriching to animals and can be used as a form of enrichment in zoos and aquariums. Cognitive research demonstrations also provide an opportunity to enhance visitor experience, as well as foster interactions between animals and keepers. We investigated how cognitive research sessions involving eastern box turtles (Terrapene carolina carolina) at Disney's Animal Kingdom® impacted both the rate of visitors coming to the exhibit and the amount of time they spent engaged. Further, we used a questionnaire to assess the impact of keeper participation in these sessions on their relationships with and perceptions of the turtles. While visitation rate to the exhibit was not impacted, cognitive research sessions held visitor attention for longer than keeper interpretation or at times during which no keepers or researchers were present. We also found that keepers that had worked with the turtles for longer and keepers that regularly participated in cognitive research sessions reported stronger bonds with the turtles. Our research suggests that use of cognitive research and training demonstrations for guest viewing in zoos and aquariums may enhance visitor learning opportunities by increasing the amount of time they spend at the exhibit. Our study also provides evidence that participation in such demonstrations by zoo and aquarium professionals can be related to improved keeper-animal bonds, potentially resulting in better husbandry and enhanced animal welfare.

Plumage variation and social partner choice in the greater flamingo (Phoenicopterus roseus).

There is evidence that plumage coloration is related to mate choice in several different bird species. However, the relationship between plumage coloration to mate or other social partner choice has rarely been investigated in flamingos. This is important to study because we know plumage coloration can be an indicator of welfare. We assessed plumage color score in relation to sex, age, and social partner choice over a 9-month period in a flock of 34 adult greater flamingos (Phoenicopterus roseus) living at Disney's Animal Kingdom® . When looking at primary social partners, redder males were more likely to have primary social partners compared to less red males. In addition, primary social partners tended to have similar color scores to each other. These findings provide insight into one factor that might influence social partner choice in greater flamingos living in ex situ situations. Future studies should investigate how these results relate to reproductive success as part of ex situ management. Zoo Biol. 35:409-414, 2016. © 2016 Wiley Periodicals, Inc.

Impact of visual context on public perceptions of non-human primate performers.

Prior research has shown that the use of apes, specifically chimpanzees, as performers in the media negatively impacts public attitudes of their conservation status and desirability as a pet, yet it is unclear whether these findings generalize to other non-human primates (specifically non-ape species). We evaluated the impact of viewing an image of a monkey or prosimian in an anthropomorphic or naturalistic setting, either in contact with or in the absence of a human. Viewing the primate in an anthropomorphic setting while in contact with a person significantly increased their desirability as a pet, which also correlated with increased likelihood of believing the animal was not endangered. The majority of viewers felt that the primates in all tested images were "nervous." When shown in contact with a human, viewers felt they were "sad" and "scared", while also being less "funny." Our findings highlight the potential broader implications of the use of non-human primate performers by the entertainment industry.

Early adverse experience increases emotional reactivity in juvenile rhesus macaques: relation to amygdala volume.

This study investigated the impact of infant maltreatment on juvenile rhesus monkeys' behavioral reactivity to novel stimuli and its associations with amygdala volume. Behavioral reactivity to novel stimuli of varying threat intensity was measured using Approach/Avoidance (AA) and Human Intruder (HI) tasks. In vivo magnetic resonance imaging (MRI) was used to measure amygdala volume. Interestingly, group behavioral differences were context-dependent. When exposed to a human intruder, maltreated subjects displayed more anxious behaviors than controls; however, when presented with fear-evoking objects, maltreated animals exhibited increased aggression and a shorter latency to inspect the objects. Finally, under testing conditions with the lowest levels of threat (neutral novel objects) maltreated animals also showed shorter latencies to inspect objects, and reduced avoidance and increased exploration compared to controls. This suggests alterations in threat assessment and less behavioral inhibition in animals with early adverse experience compared to controls. Some of these behavioral responses were associated with amygdala volume, which was positively correlated with abuse rates received during infancy, particularly reflecting a relationship with exploration, consistent with previous studies.

The effect of changes in group composition on social dynamics in marabou storks (Leptoptilos crumeniferus).

The reduction of aggressive behaviors can be a concern whenever animals are socially housed, but for some species, such as marabou storks, zoos are still unsure of the best management strategies. To learn more about marabou behavior and how dynamics change as group composition changes, we monitored a total of 3.5 marabous as individuals were added and removed over 2 years. We found that, in mixed-sex groups, males were more likely to be the initiators of displacements and females were more likely to be the recipients. Most contact aggression was intra-sexual, and females engaged in contact aggression more often than males. The highest levels of aggression were seen in our all-female groups, which was unexpected given the high number of male attacks on females reported in zoos. Because females were being added and removed but our males remained the same throughout the study, we are unsure whether this was due to a higher level of instability among females or a true sex difference; regardless, these data highlight the need to monitor aggression even within all female stork groups. Overall, we observed low levels of inter-sexual aggression, suggesting that some fatal attacks may be due, in part, to non-social factors, such as enclosure design. Social birds like marabous may benefit from the same type of group management approach that is commonly utilized with other social taxa. A two-pronged approach of observation and management of marabou social dynamics and some modification of their enclosure structure may limit injurious aggression in the future.

Brain white matter microstructure alterations in adolescent rhesus monkeys exposed to early life stress: associations with high cortisol during infancy.

BACKGROUND: Early adverse experiences, especially those involving disruption of the mother-infant relationship, are detrimental for proper socioemotional development in primates. Humans with histories of childhood maltreatment are at high risk for developing psychopathologies including depression, anxiety, substance abuse, and behavioral disorders. However, the underlying neurodevelopmental alterations are not well understood. Here we used a nonhuman primate animal model of infant maltreatment to study the long-term effects of this early life stress on brain white matter integrity during adolescence, its behavioral correlates, and the relationship with early levels of stress hormones. METHODS: Diffusion tensor imaging and tract based spatial statistics were used to investigate white matter integrity in 9 maltreated and 10 control animals during adolescence. Basal plasma cortisol levels collected at one month of age (when abuse rates were highest) were correlated with white matter integrity in regions with group differences. Total aggression was also measured and correlated with white matter integrity. RESULTS: We found significant reductions in white matter structural integrity (measured as fractional anisotropy) in the corpus callosum, occipital white matter, external medullary lamina, as well as in the brainstem of adolescent rhesus monkeys that experienced maternal infant maltreatment. In most regions showing fractional anisotropy reductions, opposite effects were detected in radial diffusivity, without changes in axial diffusivity, suggesting that the alterations in tract integrity likely involve reduced myelin. Moreover, in most regions showing reduced white matter integrity, this was associated with elevated plasma cortisol levels early in life, which was significantly higher in maltreated than in control infants. Reduced fractional anisotropy in occipital white matter was also associated with increased social aggression. CONCLUSIONS: These findings highlight the long-term impact of infant maltreatment on brain white matter structural integrity, particularly in tracts involved in visual processing, emotional regulation, and somatosensory and motor integration. They also suggest a relationship between elevations in stress hormones detected in maltreated animals during infancy and long-term brain white matter structural effects.

An evaluation of nest-building behavior by sanctuary chimpanzees with access to forested habitats.

All of the great apes build nests, but captive chimpanzees rarely have vegetation from which to build nests. The forested environment at Chimp Haven does allow captive chimpanzees to build nests of natural vegetation. Between February 2007 and December 2010, 238 nests were found in 2 forested habitats. Nests were made of naturally available vegetation, and more nests were made on the ground than in the trees (Z = 7.27, p < 0.001); nests were also built in the interior forest rather than on the periphery (Z = 7.06, p < 0.001). There was no correlation between the number of months in the habitat and the nests built per chimpanzee (rs = -0.07, p = 0.52). More nests were observed when more wild-born females were in the group (rs = 0.27, p = 0.01), and during warmer temperatures (rs = 0.45, p < 0.001). These findings support the goal of naturalistic environments in suitable climates for captive chimpanzees.

Relational responding by eastern box turtles (Terrapene carolina) in a series of color discrimination tasks.

Prior work with chelonians has demonstrated their capacity for successful performance in cognitive tasks, including those requiring color discrimination. Here, we sought to expand on historical research and determine whether eastern box turtles (Terrapene carolina) are capable of not only making simple color discriminations but also whether they can demonstrate abstract concept formation evidenced by using a relational response rule in their discrimination performance. Two eastern box turtles were rapidly and successfully trained on a black-and-white two-choice discrimination task using painted paddles and food reinforcement. After mastery, a medium gray paddle was added as a choice stimulus and turtle "Flippy" was reinforced for selecting the darker of the 2 stimuli presented in each trial, and turtle "Mario" was reinforced for selecting the lighter of the paddles presented. Nonreinforced probe trials incorporating light and dark gray stimuli paired with all other color options were then added to each session to test the turtles' ability to use the relationship between choice stimuli to guide responding. The turtles successfully selected the paddles corresponding to their assigned relational response rule of "darker" or "lighter" at a level significantly above that predicted by chance. The turtles then demonstrated immediate generalization of their relational rule in testing with a novel array of blue paddles. Finally, the turtles continued to use their relational rule when presented with a novel array of green paddles in a traditional transposition task. Together, these findings support the capacity for higher order cognitive functioning in chelonians beyond that previously described.

Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotropin-releasing hormone challenge during the first 3 years of life in group-living rhesus monkeys.

In this study we investigated the development of the hypothalamic-pituitary-adrenal (HPA) axis in 21 group-living rhesus monkeys infants that were physically abused by their mothers in the first few months of life and in 21 nonabused controls. Cortisol and adrenocorticotropin hormone (ACTH) responses to a corticotropin-releasing hormone (CRH) challenge were assessed at 6-month intervals during the subjects' first 3 years of life. Abused infants exhibited greater cortisol responses to CRH than controls across the 3 years. Abused infants also exhibited blunted ACTH secretion in response to CRH, especially at 6 months of age. Although there were no significant sex differences in abuse experienced early in life, females showed a greater cortisol response to CRH than males at all ages. There were no significant sex differences in the ACTH response to CRH, or significant interactions between sex and abuse in the ACTH or cortisol response. Our findings suggest that early parental maltreatment results in greater adrenocortical, and possibly also pituitary, responsiveness to challenges later in life. These long-term alterations in neuroendocrine function may be one the mechanisms through which infant abuse results in later psychopathologies. Our study also suggests that there are developmental sex differences in adrenal function that occur irrespective of early stressful experience. The results of this study can enhance our understanding of the long-term effects of child maltreatment as well as our knowledge of the development of the HPA axis in human and nonhuman primates.