Lateralization in seven lemur species when presented with a novel cognitive task.

OBJECTIVES: Asymmetrical behavior patterns are observed in many animal species, but the potential adaptive significance of lateralization and the evolutionary forces driving it remain unclear. Most laterality studies have focused on a single species, which makes interspecies comparisons difficult. The aim of this study was to examine differences in the strength and direction of lateralization in multiple lemur species when engaged in a standardized, novel cognitive task. MATERIALS AND METHODS: We assessed laterality in seven lemur species at the Duke Lemur Center when using a novel puzzle-box. We recorded which hand opened the apparatus door and which hand picked up the food reward. We also recorded whether the mouth was used for either action instead of the hands. We then calculated handedness indices (HI), z-scores, and mouth-use rates. RESULTS: Overall, 62% of individuals were more lateralized than chance. However, within-genera, there were relatively equal numbers of individuals with a left- or right-hand bias, which resulted in ambipreference at the genus level. The hand a lemur used on its first success in the task predicted its overall HI value, and the strength of lateralization increased as the number of successes increased. Varecia had significantly higher mouth-use rates than all other genera. DISCUSSION: We found evidence of an individual learning trajectory in which the hand used on a lemur's first success was canalized as the preferred (and lateralized) hand, in support of the "cognitive simplicity" hypothesis. Individual variability in hand preference was high, which is consistent with previous research. Between-genera differences in mouth use appear to reflect species-specific feeding postures and differences in manual dexterity.

Gorillas with white sclera: A naturally occurring variation in a morphological trait linked to social cognitive functions.

Human eye morphology is considered unique among the primates in that humans possess larger width/height ratios (WHR), expose a greater amount of visible sclera (SSI; width of exposed eyeball/width of visible iris), and critically, have a white sclera due to a lack of pigmentation. White sclera in humans amplifies gaze direction, whereas the all-dark eyes of apes are hypothesized to conceal gaze from others. This study examines WHR and SSI in humans (N = 13) and gorillas (N = 85) engaged in direct and averted gazes and introduces a qualitative assessment of sclera color to evaluate variations in sclera pigmentation. The results confirm previous findings that humans possess a larger WHR than gorillas but indicate that humans and gorillas display similar amounts of visible sclera. Additionally, 72% (N = 124) of gorilla eyes in this sample deviated from the assumed all-dark eye condition. This questions whether gaze camouflage is the primary function of darkened sclera in non-human primates or whether other functional roles can be ascribed to the sclera, light or dark. We argue that white sclera evolved to amplify direct gazes in humans, which would have played a significant role in the development of ostensive communication, which is communication that both shows something and shows the intention to show something. We conclude that the horizontal elongation of the human eye, rather than sclera color, more reliably distinguishes human from great ape eyes, represented here by gorillas.

Human caregivers are integrated social partners for captive chimpanzees.

In a captive environment, it is challenging to ensure the highest level of social and psychological well-being for species with naturally complex social organizations and structures. There is a growing need to meet the social requirements for individuals of these species, especially chimpanzees, housed in zoos, sanctuaries, rehabilitation centers, and laboratories. Complex social interactions and broader social structures can be aptly described via social network analysis. We expand on the literature regarding captive chimpanzee social networks, but uniquely consider their human caregivers as potential social partners. We observed the social interactions between one group of seven chimpanzees (Pan troglodytes) and their caregivers in six behavioral contexts (nearest neighbor, play, aggression, grooming, grooming solicitation, and social vigilance) at Chimpanzee Sanctuary Northwest (USA). By constructing multiple chimpanzee and chimpanzee-caregiver social networks, our results indicate that caregivers are integrated partners in this group's social structure. Additionally, we observed that the type and strength of chimpanzee-caregiver relationships varied between the chimpanzees. These results support the notion that caregivers offer additional opportunities (i.e., beyond those with conspecifics) for captive chimpanzees to construct and maintain meaningful social relationships. Our results show that considerations of captive primate social dynamics should include caregivers as potentially important social partners. Our results also highlight the importance of evaluating individual chimpanzee characteristics when developing philosophies of care and adopting husbandry practices that offer fulfilling social niches. Our findings bear influence on contemporary discussions of interspecies social relationships, captive welfare, health, translocation, and husbandry protocols for captive chimpanzees and other nonhuman primates.

A new identification of the monkeys depicted in a Bronze Age wall painting from Akrotiri, Thera.

Bronze Age Aegean (ca. 3500-1100 B.C.) wall paintings from the islands of Crete and Thera depict monkeys in a variety of roles such as running wild in nature, possibly following (trained) commands, and participating in sacred activities. These images, while stylistically Aegean, are traditionally considered closely related to-and descendant from-Egyptian, Near Eastern, and Mesopotamian monkey imagery. While monkey depictions in the latter regions may provide species-specific characteristics, Aegean wall paintings typically lack this level of detail. In an attempt to better understand the relationships between the monkeys depicted in Aegean wall paintings and the species that were encountered by the Aegean, Mesopotamian, and Egyptian peoples, a collaborative team of primatologists, a taxonomic illustrator, and an art historian/archaeologist identified species-indicative visual characteristics. This collaborative approach led us to identify a new region that serves as a source for monkey iconography: the Indus River Valley. With an emphasis on the primatological aspect and the growing corpus of possible Indus goods and possible species found in the Aegean, a broader iconographic and socioreligious sphere of interaction emerges. In this expanded system, Mesopotamia functions as an intermediary that enables the movement of goods, raw materials, people, and iconography between the east and west. Mesopotamia may have even afforded an opportunity for Aegean peoples to encounter the creatures themselves, first-hand. Of primary importance to the methodology employed for this project is the cooperation of scholars from disparate disciplines-the stitching together of various projects and experiences in attempt to answer both new and previously unanswerable questions. This type of interdisciplinary approach can be applied to other species, sites, paintings, and objects to hone our understanding of period, place, animal, movement, and trade.

Social network and dominance hierarchy analyses at Chimpanzee Sanctuary Northwest.

Different aspects of sociality bear considerable weight on the individual- and group-level welfare of captive nonhuman primates. Social Network Analysis (SNA) is a useful tool for gaining a holistic understanding of the dynamic social relationships of captive primate groups. Gaining a greater understanding of captive chimpanzees through investigations of centrality, preferred and avoided relationships, dominance hierarchy, and social network diagrams can be useful in advising current management practices in sanctuaries and other captive settings. In this study, we investigated the dyadic social relationships, group-level social networks, and dominance hierarchy of seven chimpanzees (Pan troglodytes) at Chimpanzee Sanctuary Northwest. We used focal-animal and instantaneous scan sampling to collect 106.75 total hours of associative, affiliative, and agonistic data from June to September 2016. We analyzed our data using SOCPROG to derive dominance hierarchies and network statistics, and we diagrammed the group's social networks in NetDraw. Three individuals were most central in the grooming network, while two others had little connection. Through agonistic networks, we found that group members reciprocally exhibited agonism, and the group's dominance hierarchy was statistically non-linear. One chimpanzee emerged as the most dominant through agonism but was least connected to other group members across affiliative networks. Our results indicate that the conventional methods used to calculate individuals' dominance rank may be inadequate to wholly depict a group's social relationships in captive sanctuary populations. Our results have an applied component that can aid sanctuary staff in a variety of ways to best ensure the improvement of group welfare.

Comparative Investigations of Social Context-Dependent Dominance in Captive Chimpanzees (Pan troglodytes) and Wild Tibetan Macaques (Macaca thibetana).

Theoretical definitions of dominance, how dominance is structured and organized in nature, and how dominance is measured have varied as investigators seek to classify and organize social systems in gregarious species. Given the variability in behavioral measures and statistical methods used to derive dominance rankings, we conducted a comparative analysis of dominance using existing statistical techniques to analyze dominance ranks, social context-dependent dominance structures, the reliability of statistical analyses, and rank predictability of dominance structures on other social behaviors. We investigated these topics using behavioral data from captive chimpanzees (Pan troglodytes) and wild Tibetan macaques (Macaca thibetana). We used a combination of all-occurrence, focal-animal, and instantaneous scan sampling to collect social, agonistic, and associative data from both species. We analyzed our data to derive dominance ranks, test rank reliability, and assess cross-context predictability using various statistical analyses. Our results indicate context-dependent dominance and individual social roles in the captive chimpanzee group, one broadly defined dominance structure in the Tibetan macaque group, and high within-context analysis reliability but little cross-context predictability. Overall, we suggest this approach is preferable over investigations of dominance where only a few behavioral metrics and statistical analyses are utilized with little consideration of rank reliability or cross-context predictability.

Playing it cool: Characterizing social play, bout termination, and candidate play signals of juvenile and infant Tibetan macaques (Macaca thibetana).

Play behaviors and signals during playful interactions with juvenile conspecifics are important for both the social and cognitive development of young animals. The social organization of a species can also influence juvenile social play. We examined the relationships among play behaviors, candidate play signals, and play bout termination in Tibetan macaques (Macaca thibetana) during juvenile and infant social play to characterize the species play style. As Tibetan macaques are despotic and live in groups with strict linear dominance hierarchies and infrequent reconciliation, we predicted that play would be at risk of misinterpretation by both the individuals engaged in the play bout and by those watching, possibly leading to injury of the players. Animals living in such societies might need to frequently and clearly signal playful intent to play partners and other group members to avoid aggressive outcomes. We gathered video data on 21 individually-identified juvenile and infant macaques (one month to five years of age) from the Valley of the Wild Monkeys, Mt. Huangshan, China. We used all-occurrence sampling to record play behaviors and candidate play signals based on an ethogram. We predicted that play groups would use multiple candidate play signals in a variety of contexts and in association with the number of audience members in proximity to the players and play bout length. In the 283 playful interactions we scored, juvenile and infant macaques used multiple body and facial candidate play signals. Our data showed that juvenile and infant Tibetan macaques use a versatile repertoire of play behaviors and signals to sustain play.