Effects of captions on viewers' perceptions of images depicting human-primate interaction.

Promoting human contact with wildlife can be harmful to animal conservation and welfare by exposing animals to unsafe situations and driving demand for wildlife tourism and exotic pets. Conservationists and researchers justifiably use social media to raise awareness, but professionals posting pictures of themselves with animals can have unintended negative consequences for conservation. Though the International Union for Conservation of Nature Best Practice Guidelines for Responsible Images of Non-Human Primates suggests researchers and animal professionals provide context in captions of images of humans interacting with primates, there is little research investigating whether this approach is effective. We investigated whether informative captions affect viewers' desires to have primates as pets and attitudes toward wildlife conservation. Using 4 mock Instagram posts depicting human-gorilla and human-slender loris interactions, we surveyed 2977 respondents to assess the effect of captions on viewers' perceptions of the images and primate conservation. Likert scale response data were analyzed with ordered probit regression models. Captions clearly contextualizing an image as research resulted in a significantly higher agreement that posts depicted wildlife research (gorilla ß = 0.28 [SE 0.06], p < 0.001; loris ß = 0.18 [0.06], p = 0.002), but such captions resulted in no significant difference in responses regarding viewers' desires to own primates as pets or questions regarding the primates' conservation statuses. Although most participants agreed the primates were endangered, more than 56% and 59%, respectively, stated they would have a gorilla or loris as a pet, that they would make good pets, or both, further supporting the conclusion that captions do not minimize harmful impacts of images of human-primate interactions.

Efectos de los pies de foto sobre la percepción del público de imágenes de la interacción humano-primate Resumen La promoción del contacto humano con la fauna puede ser dañina para la conservación y el bienestar animal al exponer a la fauna a situaciones poco seguras e incrementar la demanda por el turismo de fauna y las mascotas exóticas. Los conservacionistas y los investigadores usan con justificación las redes sociales para generar conciencia, pero los profesionales que publican imágenes de sí mismos con los animales pueden generar sin intención consecuencias negativas para la conservación. Aunque la Guía de Buenas Prácticas de la Unión Internacional para la Conservación de la Naturaleza para la Obtención Responsable de Imágenes de Primates No Humanos sugiere que los investigadores y profesionales de fauna proporcionen contexto en los pies de foto de las imágenes de humanos interactuando con primates, hay muy poca investigación sobre si esta estrategia es efectiva. Investigamos si los pies de foto informativos afectan el deseo del público de tener primates como mascotas y la actitud hacia la conservación de la fauna. Usamos cuatro publicaciones simuladas de Instagram representando interacciones humano-gorila y humano-loris para encuestar a 2,977 respondientes y estudiar el efecto de los pies de foto sobre la percepción del público de las imágenes y la conservación de primates. Analizamos los datos de respuesta de escala Likert con modelos de regresión probit ordenada. Los pies de foto que contextualizaban con claridad una imagen como trabajo de investigación resultaron en mayor aceptación de que las publicaciones representaban investigación sobre la fauna (gorila ß = 0.28 [SE 0.06], p < 0.001; loris ß = 0.18 [0.06], p = 0.002), pero dichos textos resultaron en una diferencia no significativa en las respuestas con respecto al deseo del público de tener primates como mascota o preguntas sobre el estado de conservación de los primates. Mientras que la mayoría de los participantes estuvo de acuerdo en que los primates están en peligro de extinción, más del 56% y 59%, respectivamente, afirmaron que tendrían un gorila o un loris como mascota, que serían buenas mascotas, o ambas. Esto suma a la conclusión de que los pies de foto no minimizan el impacto dañino de las imágenes de interacciones humano-primate.

Choice, control, and animal welfare: definitions and essential inquiries to advance animal welfare science.

The ways in which humans can support good welfare for animals in their care is an ongoing subject of debate: some place emphasis on the animals' physical health; others, on animals' ability to live "natural lives"; and others on animals' affective states or psychological wellbeing. Recently, there has been an increase in interest in how an animal's ability to exercise control over its environment could impact their welfare. In this article, we take the stance that the relevant aspects of the first two concepts of animal welfare (physical health, natural lives) are largely addressed when an animal's psychological wellbeing is prioritized. Through that lens, we review the current state of the literature regarding the psychology of control, and the intersection between choice, control, and welfare. We clarify terms to support future work, and propose future directions that could lead to a better understanding of the psychological benefits of choice and control and ultimately inform animal care decisions.

Chimpanzees organize their social relationships like humans.

Human relationships are structured in a set of layers, ordered from higher (intimate relationships) to lower (acquaintances) emotional and cognitive intensity. This structure arises from the limits of our cognitive capacity and the different amounts of resources required by different relationships. However, it is unknown whether nonhuman primate species organize their affiliative relationships following the same pattern. We here show that the time chimpanzees devote to grooming other individuals is well described by the same model used for human relationships, supporting the existence of similar social signatures for both humans and chimpanzees. Furthermore, the relationship structure depends on group size as predicted by the model, the proportion of high-intensity connections being larger for smaller groups.

Do zoo-housed primates retreat from crowds? A simple study of five primate species.

An animal's welfare state is directly influenced by the mental state, which is shaped by experiences within the environment throughout the animal's life. For zoo-housed animals, visitors to the zoo are a large part of that environment and a fluctuating influence within it. This study examines the impact of zoo visitors on the space use of five species of zoo-housed primates (Eastern black-and-white colobus monkeys, Colobus guereza, n = 5, Allen's swamp monkeys, Allenopithecus nigroviridis, n = 2, DeBrazza's monkeys, Cercopithecus neglectus, n = 3, Bolivian gray titi monkeys, Callicebus donacophilus, n = 3, and crowned lemurs, Eulemur coronatus, n = 3). Specifically, we considered whether primates' distance from visitor areas changed as crowd sizes increased. Data were collected using the ZooMonitor app. Observers recorded spatial coordinates for each animal over periods ranging from 12 to 32 months. Data were analyzed using two types of regression models (linear and logistic) to examine the influence of visitors on the location of the primates. Both analyses revealed a statistically significant but small decrease in primate distance from visitor viewing glass as the number of visitors increased. Behavioral indicators of welfare were also unaffected by the presence of visitors. These results suggest that, with additional validation, distance from visitors may be one promising, simple way to evaluate the influence of visitors on primate welfare.

Younger generations are more interested than older generations in having non-domesticated animals as pets.

The trade and private ownership of non-domesticated animals has detrimental effects on individual animals and their wild populations. Therefore, there is a need to understand the conditions that motivate and dissuade interest in non-domesticated pet ownership. Past research has demonstrated that the way in which non-domesticated animals are portrayed in images influences the public's perception that they are suitable as pets. We conducted an online survey of people residing in the United States to investigate how viewing images that could be realistically captured in the zoo and broader tourism industries impact the degree to which people report interest in having that animal as a pet. We focused on two species, reticulated pythons (Malayopython reticulatus) and two-toed sloths (Choloepus hoffmanni), and presented each species in six different visual contexts. After viewing an image, respondents reported interest in pet ownership on a four-point Likert scale. Each species was studied separately in a between-subjects design and results were analyzed using ordinal logistic regression models. Thirty-nine percent of respondents reported interest in sloth pet ownership, and 21% reported interest in python pet ownership. However, contrary to our hypotheses, we found that viewing these species in different visual contexts did not significantly affect survey respondents' reported interest in having either species as a pet. Generation was a significant predictor of interest in both sloth and python pet ownership, with younger generations reporting more interest in having these species as pets. Male respondents reported more interest in python pet ownership, whereas there were no significant differences between genders regarding interest in sloth ownership. We consider how modern media exposure to animals in unnatural contexts may relate to the generational effect and discuss priorities for future research to better understand the development of individual interests in non-domesticated pet ownership.

The relationship between personality, season, and wounding receipt in zoo-housed Japanese macaques (Macaca fuscata): A multi-institutional study.

It is important to those managing Japanese macaques (Macaca fuscata) in captive settings to understand predictors of wounding. While studies have demonstrated that season (breeding or nonbreeding) and sex predict rates of wounding received by zoo-housed Japanese macaques, we investigated whether individual differences in personality ratings also might explain some of the observed interindividual variance in wounding. Such patterns were previously observed in rhesus macaques (M. mulatta), such that individuals rated higher on Anxiety and Confidence received greater wounding. Here, we collected wounding data over 24 months on 48 Japanese macaques from eight AZA-accredited zoos. Each macaque was also rated by keepers using a 26-item personality questionnaire. Principle components analysis of these ratings revealed four personality components: Openness, Friendliness, Dominance, and Anxiety/Reactivity. The model with the best fit revealed an interaction effect between season (breeding vs. nonbreeding) and the personality component Friendliness, such that individuals rated higher on Friendliness incurred fewer wounds in the nonbreeding season. The second-best model revealed both a main effect of the season as well as an interaction effect between season and Openness, such that macaques rated higher in Openness received more wounds in the nonbreeding season than those rated lower in Openness. Thus, as with rhesus macaques, personality mediated wounding receipt rate in Japanese macaques, although different personality components explained interindividual variance in wounding for these two species. These differences likely reflect species differences in behavior and personality structure, as well as the influence of differing management practices, highlighting the importance of species-specific approaches for captive primate care and welfare. This study provides further support for understanding primate personality to create individualized strategies for their care.

Erratum: Cofeeding tolerance in chimpanzees depends on group composition: A longitudinal study across four communities.

[This corrects the article DOI: 10.1016/j.isci.2021.102175.].

Cofeeding tolerance in chimpanzees depends on group composition: a longitudinal study across four communities.

Social tolerance is generally treated as a stable, species-specific characteristic. Recent research, however, has questioned this position and emphasized the importance of intraspecific variation. We investigate the temporal stability of social tolerance in four groups of sanctuary-housed chimpanzees over eight years using a commonly employed measure: experimental cofeeding tolerance. We then draw on longitudinal data on the demographic composition of each group to identify the factors associated with cofeeding tolerance. We find appreciable levels of variation in cofeeding tolerance across both groups and years that correspond closely to changes in group-level demographic composition. For example, cofeeding tolerance is lower when there are many females with young infants. These results suggest that social tolerance may be a "responding trait" of chimpanzee sociality, reflecting individual-level behavioral responses to social changes. Additional, experimental research is needed to better model the causal drivers of social tolerance within and among species.

Mapping Shade Availability and Use in Zoo Environments: A Tool for Evaluating Thermal Comfort.

For many species in zoos, particularly megafauna vulnerable to heat stress, shade is a key environmental resource. However, shade availability has received comparatively less attention than other aspects of the zoo environment. In this study, we share a simple low-cost approach that we applied to document shade availability across 33 zoo enclosures. We then combined these assessments with behavioral observations of enclosure use and shade-seeking behavior during summer months in a case study focused on Sichuan takin (Budorcas taxicolor tibetana) (n = 3), a large cold-adapted bovid. Behavioral observations were conducted before and after installation of a shade sail for the takin. Results indicated that shade availability varied widely across zoo enclosures, with the percent of shaded space ranging from 85 % to 22 % across enclosures during summer months. Shade was a dynamic resource and increased throughout the year and fluctuated across the day, with the least shade available midday. Takin showed general preferences for shaded areas near the walls of their enclosure but were observed using newly available shade from the shade sail after its installation. These accessible methods can be easily applied to assess shade within existing enclosures, evaluate enclosure modifications, and provide guidance for the design of new enclosures.

Food Cleaning by Japanese Macaques: Innate, Innovative or Cultural?

Japanese macaques (Macaca fuscata) display a number of cultural behaviours including food washing, stone handling and certain grooming techniques. These are deemed cultural behaviours because it is presumed that they are socially learned and, importantly, that social learning is essential for their emergence. Recently, however, research has revealed that culturally naïve primates can re-innovate presumed cultural behaviours. These behaviours are said to fall within that species' "zone of latent solutions" (ZLS). A notable cultural behaviour of Japanese macaques is food washing, first reported by Japanese researchers studying wild Japanese macaques in the 1950s. To test whether culturally naïve Japanese macaques would spontaneously wash food and also, therefore, whether food-washing behaviour is within their ZLS, we presented 12 zoo-housed macaques with sweet potato covered in sand near a pool in their exhibit. Over 11 days we recorded the macaques' behaviour. While 11 of the 12 macaques ate the potato pieces, none washed them. However, 4 macaques cleaned their food, brushing off the sand using their hand or rubbing the potato against their body or another food item, using three distinct techniques. We found no change over time in the rate at which monkeys cleaned or consumed potato, but there was a significant positive correlation between the number of potato pieces a monkey ate and the number of cleaning behaviours performed. We conclude that, minimally, food-cleaning behaviour is within macaques' ZLS.

Sex and season predict wounds in zoo-housed Japanese macaques (Macaca fuscata): A multi-institutional study.

Japanese macaque societies are characterized by frequent intragroup conflict both in free-ranging and zoo-housed conditions. In zoos, understanding the factors that contribute to wounding is of interest because this knowledge can aid in proactive husbandry and management planning that can minimize the negative impacts wounding can have on individual welfare. This study sought to determine whether the variables sex, season and age predicted wounding rates. Data were collected for 24 months on 119 Japanese macaques living in 10 zoos, and we analyzed the contribution of variables using generalized linear mixed models. A total of 1,007 wounds were reported, and the best model included the interaction between sex and season. Follow-up analyses revealed that females incurred more wounds than males, and this sex difference was more pronounced during the breeding compared to the nonbreeding season. On average, individuals received 4.67 (±SEM: 0.55) wounds per year and 77.31% of the population incurred at least one wound in the study period. The majority of wounds were superficial and did not require veterinary intervention. Wound locations were not randomly distributed across body regions and were most often reported on the face. Finally, macaques living in larger social groups experienced more wounds, on average. This study represents the first quantification of wounding in this species and may provide insight to help inform husbandry and management strategies in zoos.

Evaluating the Behavior and Temperament of African Penguins in a Non-Contact Animal Encounter Program.

Animal ambassador programs are increasingly prevalent in zoos, yet few studies have investigated their impact on animal welfare. We assessed the effects of an ambassador program on the behavior of a colony (N = 15) of zoo-housed African penguins (Spheniscus demersus) and evaluated whether individual characteristics were predictive of participation. Behavioral data were collected for 16 weeks and included 43 "penguin encounters", during which zoo visitors entered a designated portion of the penguins' enclosure. When comparing colony behavior following encounters to behavior during a matched control period lacking an encounter, we found no significant difference between affiliative or aggressive behaviors, suggesting that the encounters did not disrupt interactions in the colony. The same was true when comparing behavior preceding the encounter to a matched control period, indicating that any anticipatory period was similarly non-disruptive. Space use during encounters suggested comfort near visitors. We also measured penguin temperament on the shy-bold continuum by recording the birds' response to novel objects and found that penguins' temperament, sex, and age were predictive of participation. We concluded that this program had a neutral or positive impact on penguin welfare and considered the findings in relation to aspects of the ambassador program that provided penguins with control over their involvement.

The Social Rank of Zoo-Housed Japanese Macaques is a Predictor of Visitor-Directed Aggression.

The effect that visitors have on the behavior and welfare of animals is a widely-studied topic in zoo animal welfare. Typically, these studies focus on how the presence or activity levels of visitors affect animals. However, for many species, and particularly primates, social factors, such as social rank, can also have a large impact on behavior. Here, we considered the influence of both the role of visitors (crowd size and activity levels) and rank on the occurrence of visitor-directed aggression by zoo-housed Japanese macaques (Macaca fuscata, N = 12). We conducted 52 weeks of observation (443.8 hours) of macaques living in a large outdoor habitat and recorded 1574 events of visitor-directed behavior, 94.2% of which was characterized as aggressive. We calculated rank using the Elo-rating method. GLMM comparisons indicate that rank was a significant predictor of visitor-directed aggression, with lower-ranked individuals displaying more frequent aggression towards visitors. Additionally, visitor-directed aggression differed by crowd activity levels, but not crowd size. These results support our prediction that rank is associated with differences in visitor-directed aggression, and we interpret this pattern as lower-ranking macaques redirecting aggression toward zoo visitors as safe targets. This work emphasizes how factors emanating from the zoo environment can combine with social dynamics to influence primate response to human presence in the zoo setting.

Population-specific social dynamics in chimpanzees.

Understanding intraspecific variation in sociality is essential for characterizing the flexibility and evolution of social systems, yet its study in nonhuman animals is rare. Here, we investigated whether chimpanzees exhibit population-level differences in sociality that cannot be easily explained by differences in genetics or ecology. We compared social proximity and grooming tendencies across four semiwild populations of chimpanzees living in the same ecological environment over three consecutive years, using both linear mixed models and social network analysis. Results indicated temporally stable, population-level differences in dyadic-level sociality. Moreover, group cohesion measures capturing network characteristics beyond dyadic interactions (clustering, modularity, and social differentiation) showed population-level differences consistent with the dyadic indices. Subsequently, we explored whether the observed intraspecific variation in sociality could be attributed to cultural processes by ruling out alternative sources of variation including the influences of ecology, genetics, and differences in population demographics. We conclude that substantial variation in social behavior exists across neighboring populations of chimpanzees and that this variation is in part shaped by cultural processes.

A multi-institutional assessment of a short-form personality questionnaire for use with macaques.

There are two commonly-used methods for calculating primates' personality dimensions, behavioral assessments and surveys, which can be used separately or in conjunction. However, these methods have limitations. Behavioral assessments, such as the novel object test or human intruder test, often require subjects to be separated and demand highly-controlled conditions. This is likely not feasible in many zoological institutions. Furthermore, it may be difficult to replicate methods across institutions. While surveys are easier to implement, the most commonly used one - the Hominoid Personality Questionnaire (HPQ) - is long and can be time consuming to complete, especially if multiple individuals need assessing. Therefore, we developed a short-form personality questionnaire for use with macaques. We aimed to retain elements of published scales while creating a tool that would be less time consuming to complete. After creating a novel 26-item scale (28 fewer items than the HPQ), we gathered ratings for 63 Japanese macaques (Macaca fuscata) living in eight zoos accredited by the Association of Zoos and Aquariums. Using principal components analysis, we identified four components to describe the Japanese macaque personality: Openneness, Friendliness, Dominance, and Anxiety/Reactivity. While further testing is required to fully validate this scale, we tested for the convergent validity of our questionnaire by correlating the responses of a subset of the monkeys to a novel object and assessed the face validity of our scale in comparison to previously-published scales.

Collaborative hierarchy maintains cooperation in asymmetric games.

The interplay of social structure and cooperative behavior is under much scrutiny lately as behavior in social contexts becomes increasingly relevant for everyday life. Earlier experimental work showed that the existence of a social hierarchy, earned through competition, was detrimental for the evolution of cooperative behaviors. Here, we study the case in which individuals are ranked in a hierarchical structure based on their performance in a collective effort by having them play a Public Goods Game. In the first treatment, participants are ranked according to group earnings while, in the second treatment, their rankings are based on individual earnings. Subsequently, participants play asymmetric Prisoner's Dilemma games where higher-ranked players gain more than lower ones. Our experiments show that there are no detrimental effects of the hierarchy formed based on group performance, yet when ranking is assigned individually we observe a decrease in cooperation. Our results show that different levels of cooperation arise from the fact that subjects are interpreting rankings as a reputation which carries information about which subjects were cooperators in the previous phase. Our results demonstrate that noting the manner in which a hierarchy is established is essential for understanding its effects on cooperation.

Studying primate cognition in a social setting to improve validity and welfare: a literature review highlighting successful approaches.

BACKGROUND: Studying animal cognition in a social setting is associated with practical and statistical challenges. However, conducting cognitive research without disturbing species-typical social groups can increase ecological validity, minimize distress, and improve animal welfare. Here, we review the existing literature on cognitive research run with primates in a social setting in order to determine how widespread such testing is and highlight approaches that may guide future research planning. SURVEY METHODOLOGY: Using Google Scholar to search the terms "primate" "cognition" "experiment" and "social group," we conducted a systematic literature search covering 16 years (2000-2015 inclusive). We then conducted two supplemental searches within each journal that contained a publication meeting our criteria in the original search, using the terms "primate" and "playback" in one search and the terms "primate" "cognition" and "social group" in the second. The results were used to assess how frequently nonhuman primate cognition has been studied in a social setting (>3 individuals), to gain perspective on the species and topics that have been studied, and to extract successful approaches for social testing. RESULTS: Our search revealed 248 unique publications in 43 journals encompassing 71 species. The absolute number of publications has increased over years, suggesting viable strategies for studying cognition in social settings. While a wide range of species were studied they were not equally represented, with 19% of the publications reporting data for chimpanzees. Field sites were the most common environment for experiments run in social groups of primates, accounting for more than half of the results. Approaches to mitigating the practical and statistical challenges were identified. DISCUSSION: This analysis has revealed that the study of primate cognition in a social setting is increasing and taking place across a range of environments. This literature review calls attention to examples that may provide valuable models for researchers wishing to overcome potential practical and statistical challenges to studying cognition in a social setting, ultimately increasing validity and improving the welfare of the primates we study.

Chimpanzee culture extends beyond matrilineal family units.

The 'grooming handclasp' is one of the most well-established cultural traditions in chimpanzees. A recent study by Wrangham et al.[1] reduced the cultural scope of grooming-handclasp behavior by showing that grooming-handclasp style convergence is "explained by matrilineal relationship rather than conformity" [1]. Given that we previously reported cultural differences in grooming-handclasp style preferences in captive chimpanzees [2], we tested the alternative view posed by Wrangham et al.[1] in the chimpanzee populations that our original results were based on. Using the same outcome variable as Wrangham et al.[1] - the proportion of high-arm grooming featuring palm-to-palm clasping - we found that matrilineal relationships explained neither within-group homogeneity nor between-group heterogeneity, thereby corroborating our original conclusion that grooming-handclasp behavior can represent a group-level cultural tradition in chimpanzees.

Tool use for corpse cleaning in chimpanzees.

For the first time, chimpanzees have been observed using tools to clean the corpse of a deceased group member. A female chimpanzee sat down at the dead body of a young male, selected a firm stem of grass, and started to intently remove debris from his teeth. This report contributes novel behaviour to the chimpanzee's ethogram, and highlights how crucial information for reconstructing the evolutionary origins of human mortuary practices may be missed by refraining from developing adequate observation techniques to capture non-human animals' death responses.