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.

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.

Foraging in a social setting: a comparative analysis of captive gorillas and chimpanzees.

This study was designed to investigate the foraging behavior of zoo-housed western lowland gorillas (Gorilla gorilla gorilla) and compare it with that of zoo-housed chimpanzees (Pan trogloydytes) tested previously in a similar paradigm. Specifically, we aimed to document how a group of zoo-housed gorillas foraged within a familiar environment to discover novel food sources and whether they sought out more preferred foods, even if they had to travel further to reach them, as they do in the wild. Gorillas were provided plastic tokens to exchange with researchers at two locations-at the same location as the tokens (close) for carrot pieces and another 6.5 m away (far) for grapes. Over the course of 30 sessions, a single individual-the silverback male-accounted for 96% of the 1546 tokens exchanged, all of which took place at the far location. Inter-individual distance measures collected during each session, as well as during matched control sessions, showed that while both gorillas and chimpanzees express similar patterns of social association across the two conditions, the average dyadic association for chimpanzees was stronger than that for gorillas. Together, these findings provide an example of the value of employing identical methodologies to compare cognition and behavior across species as well highlight the importance of the social context in which studies take place.

Western lowland gorilla (Gorilla gorilla gorilla) birth patterns and human presence in zoological settings.

There is some evidence to suggest that zoo visitors may have a disruptive impact on zoo-housed animals, especially primates. While some consider western lowland gorillas (Gorilla gorilla gorilla) to be particularly reactive to large crowds, the evidence of these effects is mixed, and is likely highly influenced by exhibit design, and group composition. While the majority of studies have focused on behavioral responses to human presence, there is the potential for physiological effects as well, including the possibility of affecting the timing of parturition. Such effects have been demonstrated in laboratory-housed callitrichids and chimpanzees, but unlike laboratory settings where human presence is lowest during the weekends, human presence might peak during weekends in public zoo settings. However, in a study of zoo-housed chimpanzees, there were no significant differences between the number of chimpanzee births that occurred on weekdays compared to weekends [Wagner and Ross, 2008], and we sought to test these questions with gorillas. We analyzed the timing of 336 live gorilla births and 48 stillbirths at 53 accredited North American zoos from 1985-2014, and similarly to chimpanzees, found no weekend or weekday effect on number of births (live births: G = 0.000, p = 1; stillbirths: G = 0.166, p < 0.684). These data add to our understanding of the potential influence of human presence on primate behavior and physiology, and add to evidence suggesting that the effects of zoo visitors on exhibited species may be less profound than previously assumed.

Captive chimpanzee foraging in a social setting: a test of problem solving, flexibility, and spatial discounting.

In the wild, primates are selective over the routes that they take when foraging and seek out preferred or ephemeral food. Given this, we tested how a group of captive chimpanzees weighed the relative benefits and costs of foraging for food in their environment when a less-preferred food could be obtained with less effort than a more-preferred food. In this study, a social group of six zoo-housed chimpanzees (Pan troglodytes) could collect PVC tokens and exchange them with researchers for food rewards at one of two locations. Food preference tests had revealed that, for these chimpanzees, grapes were a highly-preferred food while carrot pieces were a less-preferred food. The chimpanzees were tested in three phases, each comprised of 30 thirty-minute sessions. In phases 1 and 3, if the chimpanzees exchanged a token at the location they collected them they received a carrot piece (no travel) or they could travel ≥10 m to exchange tokens for grapes at a second location. In phase 2, the chimpanzees had to travel for both rewards (≥10 m for carrot pieces, ≥15 m for grapes). The chimpanzees learned how to exchange tokens for food rewards, but there was individual variation in the time it took for them to make their first exchange and to discover the different exchange locations. Once all the chimpanzees were proficient at exchanging tokens, they exchanged more tokens for grapes (phase 3). However, when travel was required for both rewards (phase 2), the chimpanzees were less likely to work for either reward. Aside from the alpha male, all chimpanzees exchanged tokens for both reward types, demonstrating their ability to explore the available options. Contrary to our predictions, low-ranked individuals made more exchanges than high-ranked individuals, most likely because, in this protocol, chimpanzees could not monopolize the tokens or access to exchange locations. Although the chimpanzees showed a preference for exchanging tokens for their more-preferred food, they appeared to develop strategies to reduce the cost associated with obtaining the grapes, including scrounging rewards and tokens from group mates and carrying more than one token when travelling to the farther exchange location. By testing the chimpanzees in their social group we were able to tease apart the social and individual influences on their decision making and the interplay with the physical demands of the task, which revealed that the chimpanzees were willing to travel farther for better.

The birth of an infant decreases group spacing in a zoo-housed lowland gorilla group (Gorilla gorilla gorilla).

Changes in group composition can alter the behavior of social animals such as gorillas. Although gorilla births are presumed to affect group spacing patterns, there is relatively little data about how these events affect gorilla group cohesion. We investigated how members of a western lowland gorilla group (n = 6) at Lincoln Park Zoo (Chicago, IL, USA) spaced themselves prior to and after the birth of an infant, to investigate changes in group cohesion. Gorillas were housed in an indoor-outdoor enclosure in which access to the outdoors was permitted when temperatures exceeded 5°C. We recorded spatial locations of each group member using 30-min group scans on tablet computers with an electronic map interface, as well as noting their access to outdoor areas. Data from the 4 months following the birth was compared to a control period corresponding to early pregnancy. We measured distances between all possible group dyads for each scan and subsequently calculated a mean distance between all group members. An ANOVA revealed that access to the outdoors had no effect on group spacing (F(1,56) = 0.066, P = 0.799). However, the presence of an infant resulted in a significant reduction in inter-individual distance (F(1,56) = 23.988, P = 0.000), decreasing inter-individual spacing by 12.5%. This information helps characterize the behavioral impact of a new birth on captive gorilla social structure and could potentially inform future management of breeding gorilla groups.

The choice to access outdoor areas affects the behavior of great apes.

Outdoor access is often cited as a critical component of appropriate housing for great apes in captivity, and although studies have shown that offering primates choices can improve welfare, choice to access specific areas has been empirically neglected. Behavioral data were collected on chimpanzees and gorillas housed in naturalistic enclosures while (a) restricted to an indoor enclosure and (b) permitted free access to an adjacent outdoor area. To isolate the factor of choice, only the sessions in which apes remained indoors were compared. With choice, chimpanzees showed more frequent social, F(1, 5) = 20.526, p = .006, and self-directed behaviors, F(1, 5) = 13.507, p = .014, and lower inactivity levels, F(1, 5) = 9.239, p = .029. Gorillas were more frequently inactive, F(1, 8) = 22.259, p = .002, and produced lower levels of object manipulation, F(1, 8) = 8.243, p = .021, and feeding, F(1, 8) = 5.407, p = .049. Results are consistent with an association between choice and the expression of species-typical and arousal behaviors in chimpanzees. The effects are less evident in gorillas, but this outcome may be buffered by the species' lower motivation to utilize the outdoor spaces. Findings highlight species-specific reactions to access to choice that may offer insight for enclosure design, management, and nonhuman animal welfare.