Group structure and individual relationships of sanctuary-living Grauer's gorillas (Gorilla beringei graueri).

The study of individual social relationships and group structure provides insights into a species' natural history and can inform management decisions for animals living in human care. The Gorilla Rehabilitation and Conservation Education (GRACE) center provides permanent sanctuary for a group of 14 Grauer's gorillas (Gorilla beringei graueri), a critically endangered and poorly studied subspecies of the genus gorilla, in the Democratic Republic of the Congo. We monitored the association patterns of the gorillas at GRACE over eight months and here describe their individual relationships and group structure via multiple social network statistics. The group was highly connected but associations between individuals were weak on average. Social network metrics describe that an adult female was the most gregarious and socially central individual within the group. In fact, adult females were the most gregarious and socially central on average. Group level association patterns were significantly correlated over the study period and across observation types, suggesting the group was socially stable during the eight month study period. The data collected in this study were done so by GRACE caregivers as part of their daily husbandry routine and provided important insights into this group's behavior, ultimately informing on their care, welfare and future release considerations. The methodological approaches implemented here are easily scalable to any primate sanctuary or care facility seeking to use data to inform husbandry and management procedures. Lastly, our study is the first social network analysis to be conducted on Grauer's gorillas and provides tentative insights into the behavior of this poorly studied subspecies. Though more research is needed to evaluate if the findings here are reflective of this subspecies' natural history or the idiosyncrasies of the group.

Home is where the home range is: Identifying territoriality and exhibit preferences in an ex-situ group of all-male Nile crocodiles (Crocodylus niloticus).

Here, the presence or absence of territoriality was evaluated in an all-male Nile crocodile (Crocodylus niloticus) group living in an ex-situ environment. Location data for each crocodile within the exhibit were collected three times per day over a two-year period, including two warm seasons and two cold seasons. A geographic information system (GIS) was used to create seasonal home ranges and core areas for each crocodile, to quantify the overlap of these home ranges and core areas to assess potential territoriality, and to calculate exhibit preferences of the group. Core area overlap was significantly lower than home range overlap, suggesting the crocodiles established territories within their exhibit. This pattern of behavior was similar across seasons, though it moderately intensified during the cold season. The crocodiles appeared to be more territorial in water, as overlap was most concentrated on the central beach, the only feature utilized more than expected based in its availability in the exhibit. These findings highlight the behavioral complexity of Nile crocodiles in human care, specifically the ability of Nile crocodiles to adapt to ex-situ environments similar to their wild counterparts by forming territories despite spatial constraints. Identifying the presence of territorial behavior is important for the care and welfare of ex-situ animals, as territorial animals have specific requirements that may result in increased agonism when unmet. It can also provide valuable context to aid in mitigation strategies, for example, when undesirable levels of agonism do occur. The findings here provide an example of how methodology from the wildlife ecology field can be adapted to ex-situ settings using a GIS and contributes to the current understanding of crocodilian behavior in human care.

Urinary oxytocin and cortisol concentrations vary by group type in male western lowland gorillas (Gorilla gorilla gorilla) in North American zoos.

Evaluating how primates in human care function within their social environment is important for understanding and optimizing their management and welfare. The neuroendocrine hormone oxytocin is associated with affiliation and bonding, suggesting it can be used to evaluate the affiliative nature of social groupings. When paired with cortisol concentrations, social stressors can simultaneously be assessed, providing a more complete picture of primate social environments than if measuring either hormone independently. Here, we measured both oxytocin and cortisol in urine within a large subset of male western lowland gorillas (Gorilla gorilla gorilla; n = 71) living in North American zoos. Both endocrine measures were compared between social group types, with an emphasis on comparing bachelor and mixed-sex groupings to understand how these broad management practices affect male gorillas in zoos. Oxytocin concentrations were greater in bachelor group males than mixed-sex group males and singly housed males, providing physiological evidence that males in bachelor groups form comparatively stronger affiliative relationships than males in other group types. Cortisol concentrations did not differ between bachelor and mixed-sex group males and males in both group types had lower cortisol concentrations than singly housed males. These results indicate that males are similarly capable of coping with group-specific social stressors, and single management may expose males to additional stressors for which further study is needed. These data contribute to a larger body of research highlighting the value of bachelor groups from both a population management and individual welfare perspective.

Treatment and Outcomes of Tusk Fractures in Managed African Savanna and Asian Elephants (Loxodonta africana and Elephas maximus) across Five Continents.

Elephant tusk fractures are a clinical challenge that can impact the overall health of the animal, particularly when they result in pulp exposure. An international survey was sent to veterinarians to understand individual fracture characteristics and management strategies as they relate to outcomes, with the goal of better informing treatment procedures. The data set consisted of 79 fractures from 64 elephants (including Asian and African males and females), 44.3% of which were Class III fractures with pulpal involvement. Of this subset, pulp canal exposures of >0.5 cm were 23.8-fold more likely to develop pulpitis than fractures with <0.5 cm exposed, though canal size did not impact healing versus extraction outcome. Odds ratios showed that treatments including endodontics were 12.0-fold more likely to heal than tusks treated exclusively with medical management, though no association was observed in reducing the risk of pulpitis. Further, pulpitis was 7.58-fold more likely to develop when tap water was used to rinse exposed pulpal tissue; a finding that merits further investigation. The use of endodontic treatment versus medical management alone was significantly associated with improved recovery outcomes (i.e., reduced risk of extraction) in tusk fractures with pulpal involvement.

Out of Sight, Out of Mind or Just Something in the Way? Visual Barriers Do Not Reduce Intraspecific Agonism in an All-Male Group of Nile Crocodiles (Crocodylus niloticus).

Here, we evaluated if visual barriers could reduce intraspecific agonism in an all-male group of Nile crocodiles (Crocodylus niloticus) living in a zoo. Crocodiles were monitored for nearly 100 h, and four "hotspots" of aggression within their exhibit were identified. Within these four locations, visual barriers were placed at the surface of the water with the goal of reducing agonism by targeting sight lines associated with their species-typical minimum exposure posture, where crocodiles submerge their body but maintain facial sensory organs above the water line. Crocodile behavior was then monitored for 226 h, evaluating both short- and long-term effects of the visual barriers. In both observation periods, intraspecific agonism was unaffected by visual barriers. However, crocodiles were more likely to be on land and closer together, after the barriers were installed, showing the barriers affected nonagonistic behaviors. Monitoring of such unintended effects is significant to ensure no welfare concerns are created in any exhibit or husbandry modification attempt. Additionally, time of day and temperature were significant predictors of behavior, highlighting the importance of such factors in the analysis of reptilian behavior. While ineffective at reducing agonism, this is the first published study evaluating exhibit design and behavior of crocodilians in zoos and aquariums. The methodologies and findings here should provide useful information for future behavioral and welfare studies of this understudied taxa.

Distinguishing mobility and immobility when establishing species-specific activity budgets: A case study with gorillas (Gorilla berengei berengei and Gorilla gorilla gorilla).

Activity budgets characterize the distribution of behavior over a specified time period. In some cases, having comparable data from free-ranging populations can help inform the management of wildlife in zoos and sanctuaries. For example, although variations exist across subspecies, seasons, and study sites, diurnal activity budgets for free-ranging gorillas largely consist of feeding and resting. Unfortunately, most studies do not consistently differentiate between the type of activities gorillas exhibit while locomoting versus stationary. Therefore, it can be difficult to characterize optimal levels of aerobic activity that might enhance body condition or promote gorilla health in zoos and sanctuaries. In this study, we concurrently measured the mobility state and activity of mountain gorillas (Gorilla beringei beringei) in Volcanoes National Park, Rwanda. From June to August 2015, behavioral data were collected using group scan sampling with 15-min intervals in two groups (N = 29 gorillas) monitored by the Dian Fossey Gorilla Fund International. Overall, gorillas spent significantly more time immobile (85.2% of observations) than mobile (14.8%), revealing energy expenditure levels comparable to western lowland gorillas living in zoos. There was no difference in behavioral diversity when gorillas were mobile versus immobile but adult females exhibited substantially less behavioral diversity while immobile than other age-sex classes. There was more diversity in behaviors following the transition from immobile to mobile than vice versa, particularly for adult females. Future studies should concurrently measure mobility state and behavior to improve the precision of activity budget data and serve as a more useful tool for evaluating optimal activity levels for wildlife in human care.

About pace: How variations in method and definition affect quantification of pacing in bears.

Repetitive pacing behavior is exhibited by many species in zoos and is particularly prevalent in carnivores with large home ranges, such as bears. Pacing can be a behavioral indicator of poor welfare, however, understanding this behavior can be challenging. As many bears that pace are singly housed, efforts to systematically examine and ameliorate pacing may be strengthened by multi-institutional studies. However, there is currently no standardized method to quantify pacing, which makes cross-institutional analyses of causal factors and intervening measures challenging. The purpose of this study was to compare multiple sampling methods and definitions for quantifying pacing in bears to understand how they affect outcome measures. We analyzed video recordings of two grizzly and two black bears pacing, using three sampling methods (continuous, instantaneous 30-s interval, instantaneous 1-min interval), and three definitions of pacing (AB-two repetitions of the path, ABA-three repetitions, ABAB-four repetitions). A generalized linear mixed model revealed that continuous and instantaneous 30-s interval methods captured more pacing than instantaneous 1-min methods, and definitions captured a decreasing amount of pacing from AB to ABA to ABAB. AB also captured the highest number of pacing bouts. The importance of comparability across institutions is growing, and a standard methodology and definition for recording pacing would be useful. We suggest that the combination of instantaneous sampling and the ABA definition presents a good balance between capturing the right data and being flexible enough for a variety of institutions to implement.

Teacher training as a means to sustained and multiplicative behavior change: An example using fuel-efficient stoves.

Chimpanzee conservation is dependent on addressing key threats such as habitat degradation, which is fueled by collection of firewood in Uganda's Kibale National Park. To address this threat, sustained behavior change that reduces dependence on fuelwood is needed. One of the greatest challenges for conservation education programs and behavior change campaigns is to have long-term and consistent effects on communities. Teacher trainings have potential to influence a large number of students over an extended period of time. In this study, we tested if teacher training on an activity designed to reduce community impact on the environment and thus reduce habitat encroachment in a critical chimpanzee habitat-construction of fuel-efficient stoves (FES)-could lead to retained knowledge and attitude improvements for students as well as sustained behavioral change in communities around Kibale National Park up to 2 years after initial training on the topic. We consistently found improvements in student knowledge and attitude change between the beginning and end of the year for third- and sixth-grade students in 11 program schools, but not in four control schools. In addition, the number of FES built by 120 teachers engaged in the program and their students continued to average over 150 stoves per year across 4 years. Our study suggests that teacher training can lead to sustained and multiplicative behavior change, which may mitigate threats to chimpanzees and other wildlife threatened by habitat encroachment in the park over time.

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.

Monitoring the social behavior of a bachelor mandrill (Mandrillus sphinx) dyad participating in touchscreen-mediated cognitive testing.

Cognitive testing of primates in zoos is becoming increasingly common. Cognition experiments are generally thought to be beneficial as they provide participants with an opportunity to engage in species-specific cognitive functioning, perhaps more so than with traditional forms of environmental enrichment. However, testing may increase competition and aggression between conspecifics if it has monopolizable features or creates social tension within groups. The purpose of this study was to monitor the social behavior of a bachelor mandrill (Mandrillus sphinx) dyad participating in a touchscreen-mediated cognition study. The mandrills' behavior was monitored before and after testing sessions for 8 months. Positive changes in the mandrills' affiliative behavior were observed. Rates of play, presentations, and silent bared-teeth face increased posttesting. No change in rates of agonism were observed between pre- and posttesting conditions. The observed positive changes in affiliative behavior suggest cognitive testing was enriching for the mandrills and participating in testing improved their welfare. Zoos beginning cognitive studies should monitor participant behavior to ensure their welfare is not compromised and is, ideally, enhanced.

Validating the use of a commercial enzyme immunoassay to measure oxytocin in unextracted urine and saliva of the western lowland gorilla (Gorilla gorilla gorilla).

The neuroendocrine hormone oxytocin, which is an important physiological driver of social behavior and bonding, is increasingly being measured in conjunction with behavior to better understand primate sociality. To date no data are available on oxytocin concentrations within the genus Gorilla; however, as a result of their close genetic relatedness to humans, and tolerance-based social system, Gorilla represents an important group of study. The purpose of this study was to validate the measurement of urinary and salivary oxytocin in western lowland gorillas (Gorilla gorilla gorilla) to help facilitate future study of the interaction between oxytocin and behavior within the subspecies. The primary validation procedure was an intranasal challenge. Elevated oxytocin concentrations were observed in saliva samples taken 15-120 min post challenge. Urine levels remained within baseline range approximately 30 and 90 min following the challenge; however, elevated levels were observed 24 h post challenge. No diurnal variation was found in salivary samples taken at regular intervals throughout the day; however, morning urine samples had higher concentrations than afternoon samples. In addition, samples were collected opportunistically following three social events: play, breeding, and the death of a conspecific. Following the play bouts, salivary oxytocin was almost three times greater than baseline. Salivary oxytocin was also significantly higher 15 min post breeding compared to match-control samples. Following the death of a conspecific, the group mate's urinary oxytocin concentrations decreased by half compared to a baseline period when the group was intact. This study provides a biological validation of the measurement of urinary and salivary oxytocin in western lowland gorillas. These results suggest that urinary oxytocin measurements are suitable for establishing baseline levels, as they represent the build up of the previous day's concentrations, and salivary oxytocin measurements are suitable for assessing changes following specific events.

Patterns of wounding in hamadryas baboons (Papio hamadryas) in North American zoos.

In North American zoos, hamadryas baboons (Papio hamadryas) have traditionally been housed as single one-male units (single male groups). In recent years, efforts have been made to house hamadryas in groups composed of multiple one-male units (multi-male groups) to more closely mirror their natural social structure, in addition to all-male or bachelor groups to manage surplus males. Given that the majority of social conflict in hamadryas occurs between males during the acquisition and defense of females, it was thought that managing hamadryas in these multi-male groups would result in increased rates of wounding. To assess this, incidences of wounding were recorded over one year across seven zoos (10 social groups, 59 individuals). Overall, we found no difference in wounding rates between group types, or by sex, and group type. These data provide evidence that managing hamadryas in multi-male and bachelor groups is an effective husbandry practice that does not negatively impact the welfare of the individuals, in addition to providing a more species-appropriate social setting for hamadryas in zoos. As the management of hamadryas in multi-male and bachelor groups continues and expands, additional research will be needed to understand what factors contribute to optimal cohesion, and welfare of groups and if wounding rates change as group size continues to increase.

Evaluating the effect of a year-long film focused environmental education program on Ugandan student knowledge of and attitudes toward great apes.

Films, as part of a larger environmental education program, have the potential to influence the knowledge and attitudes of viewers. However, to date, no evaluations have been published reporting the effectiveness of films, when used within primate range countries as part of a conservation themed program. The Great Ape Education Project was a year-long environmental education program implemented in Uganda for primary school students living adjacent to Kibale National Park (KNP) and Bwindi Impenetrable National Park (BINP). Students viewed a trilogy of conservation films about great apes, produced specifically for this audience, and participated in complementary extra-curricular activities. The knowledge and attitudes of students participating in the program from KNP, but not BINP were assessed using questionnaires prior to (N = 1271) and following (N = 872) the completion of the program. Following the program, students demonstrated a significant increase in their knowledge of threats to great apes and an increase in their knowledge of ways that villagers and students can help conserve great apes. Additionally, student attitudes toward great apes improved following the program. For example, students showed an increase in agreement with liking great apes and viewing them as important to the environment. These data provide evidence that conservation films made specifically to address regional threats and using local actors and settings can positively influence knowledge of and attitudes toward great apes among students living in a primate range country.

The effects of group type and young silverbacks on wounding rates in western lowland gorilla (Gorilla gorilla gorilla) groups in North American zoos.

In North American zoos, male gorillas are often housed in all-male (bachelor) groups to provide socialization for males not managed in breeding groups. These groups exhibit long-term cohesion and stability and males in bachelor groups are no more aggressive than males in mixed-sex groups. Previous studies have shown that aggression in male gorillas is more directly related to age rather than group type, with young silverbacks (YSB; males 14-20 years of age) having higher rates of aggressive behavior than males of other age classes. Despite this, anecdotal reports have persisted that bachelor groups have higher wounding rates than mixed-sex groups. To assess wounding in zoo-housed gorillas, all instances of wounding across 28 zoos (180 gorillas, 45 social groups) were recorded over a 26 months period via a standardized data sheet. Similar to previous reports, we found age to be an important determinant in wounding. Bachelor groups that contained YSB's had significantly more wounds than bachelor groups without YSB's (U = 14.0, z = -2.193, P = 0.029). There was no difference in wounding rates between mixed-sex and bachelor groups without YSB's (U = 69.5, z = -0.411, P = 0.689). These data further demonstrate the importance of behavioral management of YSB's in zoos and the viability of bachelor groups as a long-term housing solution for male gorillas.