Lack of reinforcement is hard to "bear": Assessing judgment bias in grizzly bears (Ursus arctos horribilis).

Cognitive biases reveal underlying affective state by indicating optimism and pessimism. This methodology may permit assessment of positive welfare in animals that have few validated positive welfare indicators, such as bears. Our goal was to validate a judgment bias test for assessing optimism in brown bears, using a touchscreen. After training the bears on a conditional discrimination, we compared responses to an ambiguous stimulus in a 2 × 2 nested design involving four experimental conditions representing presence or absence of a behind-the-scenes tour and presence or absence of a keeper training session with food reinforcement. We recorded bears' behavior during the conditions as a measure of convergent validity. Testing revealed the possibility of pessimism in the absence of reinforcement in one bear. More frustration behaviors were also observed during the no food reinforcement conditions. This is the first experimental demonstration of brown bears using a touchscreen and one of only three reports in which bears have been reported to perform a conditional discrimination. This method of assessing underlying affective state shows promise for the future.

The Effects of Choice-Based Design and Management on the Behavior and Space Use of Zoo-Housed Amur Tigers (Panthera tigris altaica).

Choice-based design allows animals in human care opportunities to move at will between multiple interconnected spaces. Some evidence suggests providing environmental choice confers benefits to animals, but there is a dearth of research in this area with large carnivores. To understand the effects of this design strategy on large felids, behavioral and space use data were collected on three Amur tigers housed in a new habitat at Cleveland Metroparks Zoo. Data were collected in two conditions: 1) restricted to a single habitat, and 2) access to two habitats. With choice, tigers were less frequently inactive (p = 0.003), and locomoted more frequently (p = 0.009). They also showed different preferences in space use with choice, and a strong preference for overhead runways between habitats (E* = 0.83, E* = 0.78). These results add to what is known about environmental impacts on zoo animal behavior and suggest this design and management strategy may be effective in conferring positive welfare benefits to tigers and other large carnivores.

Do zoo animals use off-exhibit areas to avoid noise? A case study exploring the influence of sound on the behavior, physiology, and space use of two pied tamarins (Saguinus bicolor).

Noise can be a known stressor but our understanding of its effects on animals living in zoo environments remains limited. Although exposure to loud, chronic noise may be expected to negatively impact welfare, providing access to quiet areas to escape loud noise may buffer these negative effects. In this study, we explored the benefits of access to quiet, off-exhibit areas for animals living in a chronically loud sound environment. Two pied tamarins (Saguinus bicolor) living near a large waterfall feature that emitted loud, chronic noise were experimentally exposed to varying sound levels during 2-week treatment conditions. Baseline conditions (waterfall feature on and access to quiet, off-exhibit areas), were followed by a Quiet sound condition (waterfall off), a Loud sound condition (waterfall on and a speaker in the off-exhibit area playing volume-matched white noise), and a final Baseline condition. During Baseline conditions, sound levels were greater than 10 dBA higher in the exhibit than in the off-exhibit area (i.e., roughly twice as loud). The number of visitor groups present during behavior observations were consistent throughout the study. Both tamarins modified their space use during treatment conditions. Under Baseline conditions, both individuals showed frequent usage of quiet, off-exhibit areas. During the Quiet and Loud conditions, where sound levels were generally consistent across spaces, both individuals used off-exhibit areas less and their use of exhibit and off-exhibit areas was not significantly different than would be expected by chance, given the size of the areas. Additional behavioral changes were minimal. No significant differences in fecal glucocorticoid metabolites were observed. Although the monkeys in this study appeared to avoid noise, the overall impact on welfare appeared to be minimal considering the limited behavioral and hormonal changes observed. This study highlights the potential benefits of off-exhibit spaces as a quiet refuge from noise in the zoo environment.

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.

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.

Prevalence of regurgitation and reingestion and occurrence of coprophagy in the North American AZA Gorilla (Gorilla gorilla gorilla) population.

The aims of this study were to determine the current prevalence of regurgitation and reingestion (R/R) and gain an insight on the occurrence of coprophagy in the Association of Zoos & Aquariums (AZA) gorilla (Gorilla gorilla gorilla) population. To do this, an online survey was sent to all AZA accredited gorilla institutions in 2018. This survey collected information on the severity of R/R at the individual level and the occurrence of coprophagy at the zoo level. Previous research suggests more than half of zoo-housed gorillas in the North American population engaged in R/R and coprophagy to some extent. The current study had a 100% response and completion rate; data were collected on all 296 noninfant gorillas in the population. Responses indicated that 60% of the AZA gorilla population engages in R/R to some degree and 24% of the population are observed exhibiting coprophagy on a weekly basis. With this preliminary information on coprophagy, and the realization that the Zoo community has been unsuccessful at eliminating R/R over the past 30 years, the next steps should be aimed at empirically assessing the potential drivers of these behaviors. Continuing efforts to further understand and eliminate R/R and coprophagy in zoo-housed primates is important not only because these behaviors are unsightly to visitors, but more importantly, R/R and coprophagy may signal deficiencies in current practices surrounding animal care.

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.

The effects of increased hay-to-grain ratio on behavior, metabolic health measures, and fecal bacterial communities in four Masai giraffe (Giraffa camelopardalis tippelskirchi) at Cleveland Metroparks Zoo.

We evaluated whether increasing the hay-to-grain ratio offered to Masai giraffe (Giraffa camelopardalis tippelskirchi) at Cleveland Metroparks Zoo would reduce oral stereotypies and alter feeding behaviors, maintain or increase serum calcium-to-phosphorus ratio, decrease serum insulin-to-glucose ratio and salivary insulin, and alter fecal bacterial community structure. Giraffe transitioned to a ∼90:10 hay-to-grain ratio in even increments over 8 weeks. A ration balancer was added during the seventh week of transition to ensure proper mineral and nutrient balance. We collected (1) behavioral data collected approximately daily using instantaneous focal sampling; (2) serum collections every other week for insulin-to-glucose and calcium-to-phosphorus ratio analysis and saliva weekly for insulin analysis; and (3) weekly fecal sample collections to examine changes in bacterial community structure during the 8 weeks preceding and following the diet change. After the diet change, giraffe spent significantly more time feeding and less time performing tongue and mouth stereotypies, people-directed and alert behaviors. Salivary and serum insulin and serum insulin-to-glucose ratio decreased, and fecal bacterial community structure changed significantly. However, serum calcium-to-phosphorus ratio remained >1:1 throughout the study. While further studies are needed to elucidate the nature and implications of the change in fecal bacterial community structure and metabolic hormones, the results of this study show promise for incremental improvements in health and welfare from feeding a higher proportion of forage in the diet.

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.

Sources of morbidity in lorises and pottos in North American zoos: A retrospective review, 1980-2010.

Delineating patterns of morbidity can reveal management practices in need of reassessment to improve individual welfare, as well as population health and sustainability. We reviewed medical records from 38 North American zoological institutions for 276 slender lorises, slow lorises, and pottos born between January 1, 1980 and December 31, 2010. This sample included animals identified as 116 Nycticebus pygmaeus, 84 N. coucang, 48 Loris tardigradus tardigradus, 6 L.t. nordicus (now classified as L. lydekkerianus nordicus), and 22 Perodicticus potto. Taxonomy for lorises and pottos is developing, and two of these populations (N. coucang and P. potto) likely included hybrids and/or multiple species. Our focus was to examine trends based on species and age. Across all species, whole body disease events, abnormalities of bloodwork, and dental diseases were the most common sources of morbidity. Other major sources of morbidity varied by species and included trauma, respiratory disease, and ocular disease. A recent upsurge in research has informed feeding practices for slow lorises living in human care, and a similar, evidence-based approach is needed to improve diets for other species. Given the prevalence of trauma in this sample, social needs and reproductive management practices are also important areas for further investigation. Species-level health trends reveal risk factors for individual welfare that can guide husbandry practices in zoos, as well as in sanctuaries caring for the influx of lorises and pottos rescued from the growing wildlife trade.

A work-for-food enrichment program increases exploration and decreases stereotypies in four species of bears.

Zoo-housed bears are prone to exhibiting stereotypic behaviors, generally considered indicators of negative welfare. We explored the effects of a variable-time feeding enrichment schedule on behavioral indicators of welfare in four bear species at Cleveland Metroparks Zoo. We distributed the diets of eight bears in one of five enrichment items, for two consecutive days each, and monitored behavior throughout the day. In Experiment 1, we compared variable-time to fixed-time presentation of enrichment over two, 10-day periods. Overall, bears performed more exploratory behavior when enriched (p < 0.0001). Furthermore, variable-time enrichment was associated with a greater increase in exploratory behavior than fixed-time enrichment when compared to baseline (p < 0.001). Both fixed-time (punadjusted <0.05, padjusted = 0.07) and variable-schedule (punadjusted <0.05, padjusted = 0.09) enrichment were also associated with similar decreases in abnormal behavior compared to baseline. For Experiment 2, we tested habituation to enrichment over 30 days using multiple items and a semi-variable presentation schedule. Again during the enrichment period, bears exhibited increased exploratory behavior (p < 0.0001) and decreased abnormal behaviors compared to baseline (punadjusted = 0.05, padjusted = 0.09). We observed no habituation during the 30-day sustained enrichment period for these behaviors. Collectively, these results suggest that daily, variable-schedule feeding enrichment, with intermittent presentation of unique enrichment items, increases behavioral indicators of positive welfare and decreases behavioral indicators of negative welfare.

Variables affecting the manifestation of and intensity of pacing behavior: A preliminary case study in zoo-housed polar bears.

High-speed video analysis was used to quantify two aspects of gait in 10 zoo-housed polar bears. These two variables were then examined as to how they differed in the conditions of pacing versus locomoting for each bear. Percent difference calculations measured the difference between pacing and locomoting data for each bear. We inferred that the higher the percent difference between pacing and locomoting in a given subject, the more intense the pacing may be. The percent difference values were analyzed alongside caregiver survey data defining the locations, frequency, and anticipatory nature of pacing in each bear, as well as each bear's age and sex, to determine whether any variables were correlated. The frequency and intensity of pacing behavior were not correlated. However, location of pacing was significantly correlated both with the subjects' age and whether or not the subject was classified as an anticipatory pacer. Bears appeared to select specific spots within their exhibits to pace, and the location therefore seemed tied to underlying motivation for the behavior. Additionally, bears that were classified in the survey as pacing anticipatorily displayed significantly more intense pacing behavior as quantified by gait analysis.

Using video and theater to increase knowledge and change attitudes-Why are gorillas important to the world and to Congo?

Applying environmental education in primate range countries is an important long-term activity to stimulate pro-conservation behavior. Within captive settings, mega-charismatic species, such as great apes are often used to increase knowledge and positively influence attitudes of visitors. Here, we evaluate the effectiveness of a short-term video and theater program developed for a Western audience and adapted to rural people living in two villages around Nouabalé-Ndoki National Park, Republic of Congo. We assessed the knowledge gain and attitude change using oral evaluation in the local language (N = 111). Overall pre-program knowledge about Western gorillas (Gorilla gorilla) was high. Detailed multivariate analysis of pre-program knowledge revealed differences in knowledge between two villages and people with different jobs while attitudes largely were similar between groups. The short-term education program was successful in raising knowledge, particularly of those people with less pre-program knowledge. We also noted an overall significant attitude improvement. Our data indicate short-term education programs are useful in quickly raising knowledge as well improving attitudes. Furthermore, education messages need to be clearly adapted to the daily livelihood realities of the audience, and multi-variate analysis can help to identify potential target groups for education programs.

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.

Fecal glucocorticoid metabolite responses to management stressors and social change in four species of callitrichine monkeys.

The use of enzyme immunoassays (EIA) for the non-invasive measurement of glucocorticoids provides a valuable tool for monitoring health and welfare in sensitive species. We validated methods for measuring fecal glucocorticoid metabolites (FGM) using the response to veterinary exams for four species of callitrichine monkeys: golden lion tamarin (Leontopithecus rosalia, n = 7), callimico (Callimico goeldii, n = 2), pied tamarin (Saguinus bicolor, n = 2), and white-fronted marmoset (Callithrix geoffroyi, n = 2). Routine veterinary exams were performed for the golden lion tamarins and callimicos, but exams for the pied tamarins and white-fronted marmosets were prompted by the death of a social partner. Prior to veterinary exams, fecal markers were evaluated to allow collection of individual samples and estimate approximate gut transit times. Based on this assessment, individual markers were fed in the afternoon, and fresh morning fecal samples were collected throughout this study. Following a veterinary exam, FGM increased roughly 3- to 28-fold above baseline in all species. Although FGM for most species returned to baseline concentrations within 24-48 h, the marmosets exhibited a progressive increase in FGM after an exam in response to the death of a breeding female and subsequent hand-rearing of a neonate. Individual differences were noted in the callimicos and tamarins, with higher baseline FGM levels in females vs. males, although small sample size precluded a clear determination of sex differences. To our knowledge, this is the first study to measure FGM in callimicos and white-fronted marmosets and the first to compare FGM across callitrichine species. These findings highlight the broad applicability of this EIA to measure the stress response of callitrichine monkeys. The progressive increase in FGM in the marmosets during hand-rearing of a neonate suggests that care should be taken to minimize this disturbance as much as possible.

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.