Effects of food-based enrichment on enclosure use and behavioral patterns in captive mammalian predators: a case study from an Austrian wildlife park.

Background: Combining naturalistic enclosure design and animal welfare with visitor interests and education can be challenging for zoos and wildlife parks. To accomplish both purposes, different types of enrichment (food-based or non-food-based items, such as environmental, sensory, cognitive, social) can be used. The aim of the present study is to investigate the effect of food-based and olfactory enrichments on enclosure use, behavior, and visibility of captive brown bears (Ursus arctos), pine martens (Martes martes), domestic ferrets (Mustela putorius furo), and golden jackals (Canis aureus). Methods: We used observational approaches to measure enclosure use, behavior, and visibility during three different experimental phases: (1) pre-enrichment (baseline, no experience with the enrichment yet), (2) during enrichment (enrichment was provided at low frequented locations in the enclosures that are easily visible to visitors), and (3) post-enrichment (enrichment was removed from the enclosures). Results: We found that enrichment led to a uniform use of the enclosure and enhanced visibility in brown bears, increased activity budgets in pine martens, and observed high object interaction in both species. No effects of enrichment were detected in domestic ferrets. Golden jackals did not leave their burrows during daytime during the entire observation period; thus, observations were not possible at all. Our results suggest different effects of food-based enrichment, e.g., enclosure use, temporal activity patterns, and animal visibility. However, further studies should control for the specific role of the factors involved. Our study represents one of the first explorations of food-based enrichment in rather understudied species.

Sudden death caused by Aeromonas hydrophila in a Crab-eating Macaque (Macaca fascicularis) associated with captivity stress.

Aeromonas hydrophila is a facultative anaerobic gram-negative bacterium regarded as an opportunistic pathogen in animals. A 17-year-old female crab-eating macaque (Macaca fascicularis) died after experiencing anorexia and depression for several days. The carcass was severely emaciated, and the sternum was exposed under subcutaneous lesions in the thorax. Many abnormal pathological lesions were found, including tracheal inflammation, pulmonary inflammatory emphysema, yellowish discoloration of the liver, enlargement of the gall bladder, necrosis of the heart, congested bilateral kidneys, and enlargement of the adrenal glands. The stomach was empty, mucosal ulcerations were found, and the duodenum was congested. Giemsa staining revealed rod-shaped organisms in the whole blood smear and major organs, which were identified as A. hydrophila. The animal had experienced stress, and decreased immune system function possibly contributed to the infection.

Don't use it? Don't lose it! Why active use is not required for stimuli, resources or "enrichments" to have welfare value.

Current frameworks for designing and evaluating good enclosures and "enrichments" typically focus on animals' active interactions with these features. This has undoubtedly improved the welfare of zoo-housed animals over the last 30 years or more. However, literature reviews from this same period identify persistent gaps in how such frameworks are applied: experiences and behaviors that do not rely on active interaction with stimuli or resources are largely ignored, when evaluating the welfare value of enclosures and enrichments within them. Here, we review research evidence demonstrating that active interaction is not always a reliable measure of welfare value, showing that items that elicit little or no interaction can nevertheless still reduce stress and improve well-being. This evidence largely comes from research on humans, lab animals and farm animals, but also from some zoo studies too. We then investigate why. We review psychology and ethology literatures to show that such welfare benefits can arise from five, non-mutually exclusive, processes or mechanisms that are well-understood in humans and domestic animals: (1) some motivations are sated quickly by interaction with resources, yet still have large welfare benefits; (2) active interaction may just be a way to achieve a goal or solve a problem, without being beneficial for welfare in itself; (3) having opportunities for choice and control may be inherently beneficial, even when not acted on; (4) some enclosure features meet social needs for structure, landmarks, and blocked sightlines; and (5) some stimuli may be preferred because they signaled good environments to an animal's ancestors. We use this information to identify  improved ways of enhancing and assessing zoo animal welfare. Incorporating these concepts should expand the scope of behaviors and subjective experiences that are targeted, to now include those that involve little active interaction and yet still are important for good welfare.

Learning outcomes measured in zoo and aquarium conservation education.

Communicating the topic of conservation to the public and encouraging proenvironmental behaviors can mitigate loss of biodiversity. Thus, the evaluation of educational efforts is important to ascertain the educational effects and provide high-quality conservation education. The learning outcomes of conservation education are diverse (e.g., attitudes, knowledge, and behavior). Considering the specific characteristics of these different outcomes and the factors that influence them is crucial to delivering successful conservation education. We reviewed 29 peer-reviewed articles published in English from January 2011 to April 2020 on empirical studies of learning outcomes of on-site conservation education in zoos and aquaria, institutions that seek to educate the public about conservation. We examined the range of learning outcomes, their definitions, and factors that influenced them. Cognitive outcomes were most frequently investigated (37%) in comparison with other outcomes (e.g., affective outcomes, 31%). The articles did not use explicit definitions for learning outcomes, and implicit or explorative definitions provided were inconsistent. Outcomes were influenced by various factors (e.g., prior experiences, staff interaction, animal behavior). Our results suggest the agenda of conservation education research should be broadened by examining all learning outcomes relevant to behavior change. Educational and behavior change theories should be used as a background for conservation education research to ensure clear and consistent definitions, derive appropriate instruments to measure learning outcomes, and relate learning outcomes to influencing factors. We recommend conservation education researchers and practitioners to treat conservation education holistically and acknowledge its learning outcomes' full complexity.

Resultados del Aprendizaje Medidos en la Educación para la Conservación en Zoológicos y Acuarios Resumen La comunicación del tema de conservación y el fomento de las conductas proambientales entre el público puede mitigar la pérdida de la biodiversidad. Así, la evaluación de los esfuerzos educativos es importante para determinar sus efectos y proporcionar una educación para la conservación de gran calidad. Los resultados del aprendizaje de la educación para la conservación son diversos (p.ej.: actitudes, conocimiento y comportamiento). Es importante considerar las características específicas de estos diferentes resultados y los factores que les influyen para proporcionar una educación para la conservación exitosa. Analizamos 29 artículos, revisados por pares y publicados en inglés entre enero de 2011 y abril de 2020, sobre los estudios empíricos de los resultados del aprendizaje de la educación para la conservación in situ en zoológicos y acuarios, instituciones que educan al público sobre la conservación. Analizamos la variedad de resultados del aprendizaje, sus definiciones y los factores que les influyen. Los resultados cognitivos fueron los que se investigaron con mayor frecuencia (37%) en comparación con otros resultados (p.ej.: resultados afectivos, 31%). Los artículos no usaron definiciones explícitas para los resultados del aprendizaje, y las definiciones implícitas o exploratorias que se proporcionaron fueron incoherentes. Los resultados estuvieron influenciados por diversos factores (p.ej.: experiencias previas, interacción con el personal, comportamiento animal). Nuestros resultados sugieren que la agenda de la investigación sobre la educación para la conservación debería extenderse mediante la examinación de los resultados del aprendizaje relevantes para el cambio en el comportamiento. Las teorías del cambio educativo y conductual deberían usarse como trasfondo para la investigación sobre la educación para la conservación para garantizar definiciones claras y concisas, derivar instrumentos adecuados para medir los resultados del aprendizaje y relacionar los resultados del aprendizaje con los factores influyentes. Recomendamos que los investigadores y los practicantes de la educación para la conservación la manejen de forma holística y reconozcan toda la complejidad de sus resultados de aprendizaje.

Conservation psychology and the legacy of Carol Saunders for zoo and aquarium programs, networks, practices, and exhibits.

Conservation Psychology created a dialog between environmental conservation and behavioral sciences. With an outsized influence by Dr. Carol Saunders, it started at Brookfield Zoo in Chicago exploring questions about the impacts of a zoo visit, and particularly how human behavior influences environmental outcomes for our planet. Here we explore how Conservation Psychology influenced the development of programs, exhibits and communities of practice at Brookfield Zoo and elsewhere in the zoo and aquarium world, and how eventually these applications changed the way modern zoos and aquariums operate. We present testimonials and review a handful of examples in which Conservation Psychology led to tangible programs, practices and wide professional networks at zoos and aquariums. These include an exploration of the future of zoos with George Rabb, followed by the legacy of nature play and the groundbreaking Hamill Family Play Zoo. Furthermore, we discuss how visitor studies at zoos and aquariums were influenced by Conservation Psychology, including the development of the Association of Zoos and Aquariums Social Science Research and Evaluation Scientific Advisory Group and two climate change education networks. We end with the development of tools, practices, and professional networks to explore empathy for animals. Most of these programs were envisioned or facilitated by Dr. Saunders, who was always a role model with an impact and a legacy that lives on.

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.

Effects of browsing enrichment associated with the temperature-humidity index and landscaping trees in giraffes (Giraffa camelopardalisreticulata).

Enclosure environments for captive giraffes can be improved by promoting species-specific behaviors and extending foraging behavior. To date, however, the effects of climatic (temperature-humidity index, THI) and environmental factors (landscaping trees) on the enrichment of captive settings have not been studied. Therefore, the present study explored the effects of browsing enrichment on the licking behavior of captive giraffes. From May 2019 to February 2020, three giraffes in the Kyoto City Zoo, Japan, were observed for 270 h over two consecutive seasons (pre- and post-deciduous). Overall, branch foraging behavior and licking behavior were weakly and negatively correlated. In the pre-deciduous period, THI was significantly and negatively correlated with giraffe activity, and some individuals exhibited significantly reduced foraging behavior. Therefore, browsing enrichment under extreme heat may not improve giraffe rearing environments. Moreover, in the post-deciduous period, with decreased availability of leaves on landscaping trees, the non-branch foraging behavior of giraffes was significantly increased, with a corresponding significant increase in licking behavior. Therefore, landscaping trees affect the foraging behavior of captive giraffes.

Variation in personality can substitute for social feedback in coordinated animal movements.

Collective movements are essential for the effective function of animal societies, but are complicated by the need for consensus among group members. Consensus is typically assumed to arise via feedback mechanisms, but this ignores inter-individual variation in behavioural tendency ('personality'), which is known to underpin the successful function of many complex societies. In this study, we use a theoretical approach to examine the relative importance of personality and feedback in the emergence of collective movement decisions in animal groups. Our results show that variation in personality dramatically influences collective decisions and can partially or completely replace feedback depending on the directionality of relationships among individuals. The influence of personality increases with the exaggeration of differences among individuals. While it is likely that both feedback and personality interact in nature, our findings highlight the potential importance of personality in driving collective processes.

Zoo-housed mammals do not avoid giving birth on weekends.

There is evidence that zoo visitor presence can influence the behaviour and, in some cases, adrenal response of zoo animals, and can sometimes compromise animal welfare. In some laboratory studies, significantly more primate births have been reported on weekends, when fewer people are working there, compared with weekdays when staffing levels are at their highest. Here, we investigate whether there is evidence of a "weekend effect" on births in zoo animals as a result of visitor numbers. Unlike laboratories, zoos are typically busier with visitors on weekends than on weekdays, although staffing levels remain fairly consistent across days of the week. If zoo animal parturition is sensitive to human presence, then fewer births would be expected on weekends compared with weekdays. We tested this using birth data and visitor numbers on the entrance gate from zoo records across 16 species representing artiodactyls, perissodactyls, carnivores and primates at four British zoos, to see whether there is an association between mean daily birth rates and average visitor numbers. We predict that, if there is a visitor effect, daily births should be lower on weekends than weekdays and should correlate with mean daily visitor numbers. Results showed that births for all 16 species were randomly distributed through the week, and there was no significant decline in births on weekends. We conclude that the "weekend effect", if such a thing exists, does not appear to be a feature of zoo births, suggesting that elevated weekend visitor numbers are not sufficiently stressful to trigger delayed parturition.

Development of bed-building behaviors in captive chimpanzees (Pan troglodytes): Implication for critical period hypothesis and captive management.

Wild great apes build beds for sleeping by combining tree branches or other vegetation, but the development of this behavior is poorly understood. We investigated the development of bed-building behaviors by conducting complementary cross-sectional and longitudinal studies of captive chimpanzees. In the cross-sectional study, we created an ethogram of behaviors related to bed-building by observing 59 chimpanzees living at the Kumamoto Sanctuary, Kyoto University, and the Kyoto City Zoo. In the longitudinal study, we installed bed-building platforms, provided branches on the platforms on a regular basis, and recorded behaviors of five chimpanzees (including an infant born in 2013) over a 3-year period from February 2015 to February 2018 at the Kyoto City Zoo (total 490.7 h). We found that all the chimpanzees performed some form of bed-building behavior but wild-born chimpanzees possessed more sophisticated techniques than captive-born chimpanzees. We also found that although the offspring of a wild-born female only showed simple techniques at the beginning of the longitudinal study, his repertoire of bed-building behaviors became as complex as that of his mother by the age of five. Our results suggest that improved bed-building behaviors can be supported in captive-born great apes by providing learning opportunities during appropriate stages of development.

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus).

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.

Food preference and nutrient composition in captive bonobos (Pan paniscus).

Food preference has been studied in a range of Hominoidea in the wild and in captivity, allowing for interspecific comparisons. Chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla gorilla) prefer low-fibre, high-sugar foods, suggesting that frugivory and their dietary overlap are a result of their shared preference for the same nutrients. Comparable tests of the nutritional preference of bonobos do not exist. In this study we examined food preferences of five captive bonobos for 23 familiar and ten novel food items. We performed paired-choice food tests, resulting in a clear rank order in food preference, with minor individual differences. Fruits were more preferred than vegetables. We correlated nutritional composition of the food items with the bonobos' preference. We found that preferences for familiar food items were positively correlated with total energy and carbohydrate content and negatively correlated with water and micronutrient (sodium, calcium, phosphorus, iron, zinc, manganese, selenium) content. Food preference for the novel food items also showed a significant positive correlation with total energy and carbohydrate content. Our study supports the idea that food preference among bonobos follows the pattern of the other great apes and that the shared frugivorous diets may be the result of a common preference for the same nutrients. In the wild, these preferences may be less clear due to the interference of preferred nutrients with secondary compounds. Combining food preference data and nutritional information can help in providing a healthy diet with a balanced nutrient composition in captivity. Individual food preferences can help in optimizing food choice for positive reinforcement training and food-related tasks in future research.

Monitoring of group mates in relation to their behavior in mandrills.

Primates are known to have considerable knowledge about the social relationships that link their group mates and are likely to derive this information from observing the social interactions that occur in their social group. They may, therefore, be hypothesized to pay particular attention to the social interactions involving group mates. In this study, we evaluated how the attention captive mandrills (Mandrillus sphinx) devote to their group mates was modulated by the behavior of the latter. Mandrills looked most frequently at foraging individuals and least frequently at sleeping individuals. Mandrills also looked at grooming individuals more than at individuals that were simply sitting in contact. Grooming dyads were looked at regardless of the social rank and kinship of the individuals involved. These results contribute to our understanding of how primates obtain their social knowledge.

Investigating the Function of Mutual Grooming in Captive Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes).

Social grooming is often exchanged between individuals in many primate species. Rates of bidirectional (or simultaneous mutual) grooming vary across primate species, and its function is not yet fully understood. For example, mutual grooming is frequent in chimpanzees but rare in most primate species including wild bonobos. There are, however, no quantitative data available in captive bonobos. Therefore, through the direct comparison between captive bonobos and chimpanzees, this study aimed to (i) compare the frequency of mutual grooming between Pan species, (ii) explore and compare the function of mutual grooming, and (iii) discuss the rarity of this behavior in wild bonobo populations. We tested three hypotheses following the previous literature in wild chimpanzees. The social bonding hypothesis states that mutual grooming facilitates the maintenance of strong dyadic bonds. The immediate investment hypothesis states that it serves to signal willingness to invest in the interaction. The switching hypothesis states that mutual grooming serves no function but only occurs as an overlap to change the direction of unidirectional grooming. Our findings strongly supported the immediate investment hypothesis, but not the others. Grooming bouts that included mutual grooming were longer and more equitable than bouts without, illustrating that captive Pan species use mutual grooming to maximize their short-term benefits and increase the social value of their interaction. Captive bonobos performed mutual grooming in similar proportions and for similar functions as captive and wild chimpanzees do. This contrasts with wild bonobos who engage in this behavior only rarely. We suggest that the differences in patterns of mutual grooming between captive and wild bonobos might be explained by different degrees of kinship or by a potential intraspecies variation.

Testing use of a potential cognitive enrichment device by an Indo-Pacific bottlenose dolphin (Tursiops aduncus).

Cognitive enrichment aims to provide animals with opportunities to use their cognitive skills and to promote behaviors associated with positive wellbeing. Cooperation in mammals has been recorded during various behavioral contexts such as hunting, mating, playing, and parental care. Coordinated activity, often with some level of problem-solving action included, is required during cooperation. To investigate dolphins' ability for collaborative problem-solving, an enrichment device was introduced to two adult male Indo-Pacific bottlenose dolphins (Tursiops aduncus). The device contained fish and ice and was designed to be opened by simultaneously pulling on both ends. After repeated presentation, it became apparent that only one dolphin had active interest in the device. To facilitate opportunities for problem-solving by this individual, an alternative collaborator, a human partner, was provided. Still, both dolphins had access to the device throughout the entire experiment. After the first opening, the same dolphin was highly successful in collaborating with the human in both joined (93%) and delayed (100%) partner conditions. The device provided a novel opportunity for the dolphin to use his cognitive skills. Even though only one dolphin participated actively, both dolphins showed varying degrees of interest to the device throughout the study. Both dolphins spent an average of 48% and 16% of their time, respectively, with the device, which resulted in a significant decrease in their other two most frequently observed behaviors: swimming and poolside observation. As a novel cognitive challenge, the device may be considered as a type of cognitive enrichment.

Gorillas' (Gorilla g. gorilla) knowledge of conspecifics' affordances: intraspecific social tool use for food acquisition.

The use of tools, long thought to be uniquely human, has now been observed in other animal taxa including several species of birds, non-primate mammals as well as some non-human primate species. Chimpanzees, one of humankind's closest living relatives, exceed all other non-human animal species as they have been reported to use an exceptionally large toolkit. However, relatively little is known about the tool-use skills of the other great ape species. While the majority of tools described are inanimate objects, the use of social tools has received relatively little attention. Here we provide the first evidence of naturally occurring spontaneous exploitative behaviour of a conspecific as a social tool for food acquisition in non-human animals. We observed gorillas in captivity utilising a conspecific as a ladder to gain access to unreachable food. We discuss our findings in the light of other studies on social tool use and suggest the need for more nuanced interpretations of gorillas' cognitive skills.

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.

Responses to a dead companion in a captive group of tufted capuchins (Sapajus apella).

The observation of specific reactions by animals to dead conspecifics raises questions about their capacity to understand death. We describe the behavior of a captive group of tufted capuchins in the hours following the death of an adult female. The behavior of 12 subjects was recorded over a 5-h period. Most group members displayed exploratory behaviors toward the corpse, peering at it, smelling, touching, lifting or pulling it at least once. Interactions with the corpse were particularly frequent in the first hour, then decreased in the following hours. The relatives of the deceased female were the most involved individuals, and her daughter spent more time near her body than the other members of the group. Rates of interaction with the body were especially high in subadult individuals. Most of the behaviors directed to the body of the deceased individual appeared to be investigative.

Prolonged care and cannibalism of infant corpse by relatives in semi-free-ranging capuchin monkeys.

Cannibalism is a quite common behaviour in animals that can have survival value when food is scarce or in the case of overpopulation. Conversely, cannibalism can also increase pathogen transmission and reduce fitness. In primates, some cases of cannibalism are associated with infanticide or are performed by mothers after their newborn has died (filial cannibalism). We report here the first observation of cannibalism, specifically infant cannibalism, in a semi-free-ranging group of brown capuchin monkeys (Sapajus apella). The baby was likely stillborn, as parts of the cranial bones were missing and no fresh injuries were visible. After half a day of taking care of the dead infant, the mother ate part of the corpse's skin and the highly nutritional viscera, possibly thereby compensating for the physiological costs of pregnancy. After attentively watching his mother's behaviour, the older brother of the dead newborn similarly ate parts of the corpse. Although we cannot rule out idiosyncrasy and vertical social transmission, it is possible that cannibalism is a normal-albeit rare-part of the behavioural repertoire of capuchin monkeys.

How Target Animacy Affects Manual Laterality in Hylobatidae: The First Evidence in Northern White-Cheeked Gibbons (Nomascus leucogenys).

Our study presents the first evidence on how target animacy impacts on manual laterality in the Hylobatidae and contributes to filling the knowledge gap between monkeys and great apes in primate evolution of emotional lateralization. Eleven captive individuals of northern white-cheeked gibbons (Nomascus leucogenys) were chosen as focal subjects. There were significantly more ambipreferent individuals than left/right-handed individuals for both inanimate (χ2(1, n = 11) = 7.364, p = 0.007) and animate (χ2(1, n = 11) = 4.455, p = 0.035) targets, meaning no significant group-level hand preference. The right hand was more frequently used than the left hand for inanimate targets whereas the left hand was more frequently used than the right hand for animate targets, although the interaction between target animacy and hand use was not significant (proportion: F1, 10 = 0.283, p = 0.607; rate: F1, 10 = 0.228, p = 0.643). Our findings in N. leucogenys could not fully support either the tool use theory or the right hemisphere hypothesis.