Macaques preferentially attend to visual patterns with higher fractal dimension contours.

Animals' sensory systems evolved to efficiently process information from their environmental niches. Niches often include irregular shapes and rough textures (e.g., jagged terrain, canopy outlines) that must be navigated to find food, escape predators, and master other fitness-related challenges. For most primates, vision is the dominant sensory modality and thus, primates have evolved systems for processing complicated visual stimuli. One way to quantify information present in visual stimuli in natural scenes is evaluating their fractal dimension. We hypothesized that sensitivity to complicated geometric forms, indexed by fractal dimension, is an evolutionarily conserved capacity, and tested this capacity in rhesus macaques (Macaca mulatta). Monkeys viewed paired black and white images of simulated self-similar contours that systematically varied in fractal dimension while their attention to the stimuli was measured using noninvasive infrared eye tracking. They fixated more frequently on, dwelled for longer durations on, and had attentional biases towards images that contain boundary contours with higher fractal dimensions. This indicates that, like humans, they discriminate between visual stimuli on the basis of fractal dimension and may prefer viewing informationally rich visual stimuli. Our findings suggest that sensitivity to fractal dimension may be a wider ability of the vertebrate vision system

Macaque cardiac physiology is sensitive to the valence of passively viewed sensory stimuli.

Autonomic nervous system activity is an important component of affective experience. We demonstrate in the rhesus monkey that both the sympathetic and parasympathetic branches of the autonomic nervous system respond differentially to the affective valence of passively viewed video stimuli. We recorded cardiac impedance and an electrocardiogram while adult macaques watched a series of 300 30-second videos that varied in their affective content. We found that sympathetic activity (as measured by cardiac pre-ejection period) increased and parasympathetic activity (as measured by respiratory sinus arrhythmia) decreased as video content changes from positive to negative. These findings parallel the relationship between autonomic nervous system responsivity and valence of stimuli in humans. Given the relationship between human cardiac physiology and affective processing, these findings suggest that macaque cardiac physiology may be an index of affect in nonverbal animals

Rhesus monkeys have an interoceptive sense of their beating hearts

The sensation of internal bodily signals, such as when your stomach is contracting or your heart is beating, plays a critical role in broad biological and psychological functions ranging from homeostasis to emotional experience and self-awareness. The evolutionary origins of this capacity and, thus, the extent to which it is present in nonhuman animals remain unclear. Here, we show that rhesus monkeys (Macaca mulatta) spend significantly more time viewing stimuli presented asynchronously, as compared to synchronously, with their heartbeats. This is consistent with evidence previously shown in human infants using a nearly identical experimental paradigm, suggesting that rhesus monkeys have a human-like capacity to integrate interoceptive signals from the heart with exteroceptive audiovisual information. As no prior work has demonstrated behavioral evidence of innate cardiac interoceptive ability in nonhuman animals, these results have important implications for our understanding of the evolution of this ability and for establishing rhesus monkeys as an animal model for human interoceptive function and dysfunction. We anticipate that this work may also provide an important model for future psychiatric research, as disordered interoceptive processing is implicated in a wide variety of psychiatric conditions

Social and Nonsocial Content Differentially Modulates Visual Attention and Autonomic Arousal in Rhesus Macaques

The sophisticated analysis of gestures and vocalizations, including assessment of their emotional valence, helps group-living primates efficiently navigate their social environment. Deficits in social information processing and emotion regulation are important components of many human psychiatric illnesses, such as autism, schizophrenia and social anxiety disorder. Analyzing the neurobiology of social information processing and emotion regulation requires a multidisciplinary approach that benefits from comparative studies of humans and animal models. However, many questions remain regarding the relationship between visual attention and arousal while processing social stimuli. Using noninvasive infrared eye-tracking methods, we measured the visual social attention and physiological arousal (pupil diameter) of adult male rhesus monkeys (Macaca mulatta) as they watched social and nonsocial videos. We found that social videos, as compared to nonsocial videos, captured more visual attention, especially if the social signals depicted in the videos were directed towards the subject. Subject-directed social cues and nonsocial nature documentary footage, compared to videos showing conspecifics engaging in naturalistic social interactions, generated larger pupil diameters (indicating heightened sympathetic arousal). These findings indicate that rhesus monkeys will actively engage in watching videos of various kinds. Moreover, infrared eye tracking technology provides a mechanism for sensitively gauging the social interest of presented stimuli. Adult male rhesus monkeys' visual attention and physiological arousal do not always trend in the same direction, and are likely influenced by the content and novelty of a particular visual stimulus. This experiment creates a strong foundation for future experiments that will examine the neural network responsible for social information processing in nonhuman primates. Such studies may provide valuable information relevant to interpreting the neural deficits underlying human psychiatric illnesses such as autism, schizophrenia and social anxiety disorder

Addressing the challenges of research on human-wildlife interactions using the concept of coupled natural & human systems

© 2021 The Authors. Published by Elsevier. This is an open access article available under a Creative Commons licence. The published version can be accessed at the following link on the publisher’s website: https://doi.org/10.1016/j.biocon.2021.109095With the global expansion of human populations, research on human-wildlife interactions (HWIs) has become increasingly important in conservation science. Despite its growing importance, such research faces challenges that include a bias towards evaluating wildlife- compared to human-related aspects of interactions, limited focus on the complexity of HWIs and their effects, assessments of more observable compared to hidden/subtle effects, and the lack of comparative studies. Here we review how the Coupled Natural and Human Systems (CNHS) approach has been useful to address these challenges. We demonstrate the relative dearth in studies that have implemented CNHS approaches in the context of HWIs, compared to human interactions with biophysical, abiotic, and other biotic natural systems. We next review conceptual CNHS frameworks implemented to model HWIs, their structural and functional similarities and differences, and reveal how they help to address some, but not all, of the afore-mentioned challenges. We then construct a general, integrated conceptual framework for human-wildlife CNHS borrowing elements from pre-existing frameworks, which includes a standardized designation/nomenclature of CNHS components and their relationships and builds on pre-existing frameworks by placing a greater emphasis on less visible outcomes of HWIs that remain under-represented in the CNHS literature. We discuss the potential and scope of this integrated framework in terms of its usefulness to address the above challenges, and the importance of moving human-wildlife CNHS frameworks from merely providing conceptual platforms towards their analytical utility as single ‘whole’ systems

Infant survival among free-living bonnet macaques (Macaca radiata) in South India

© 2021 The Authors. Published by Springer. This is an open access article available under a Creative Commons licence. The published version can be accessed at the following link on the publisher’s website: https://doi.org/10.1007/s10764-021-00198-3Female reproductive success depends to a large extent on infants’ ability to survive to maturity. While most studies of female reproductive success have focused on the effects of individuals’ sociodemographic factors (e.g. age/parity, dominance rank) on offspring survival among wild primates living in less disturbed habitats, little research has focused on offspring survival in urban or peri-urban animals. Here we investigated sociodemographic and anthropogenic determinants of infant survival (up to 1-yr of age) in free-ranging bonnet macaques (Macaca radiata) living in a peri-urban environment in Southern India. We conducted the study from November 2016 to May 2018, on two groups of bonnet macaques at the Thenmala tourist site in the state of Kerala. Fifty infants were born across two birth seasons. 29.2% of infants died or disappeared in 2017 and 26.9% died or disappeared in 2018. We found that infant survival was strongly influenced by the mother’s parity: infants of experienced mothers had a better chance of survival than those of first-time mothers. We also found that male infants were more likely to die than female infants. However, we found no effects of mothers’ dominance rank, or of frequency of mothers’ interactions with humans and time spent foraging on anthropogenic food, on infant survival. Our results, consistent with findings from other wild primate species, show that even in challenging human-impacted environments, experienced bonnet macaque mothers have greater success than inexperienced ones

Interactions with humans impose time constraints on urban-dwelling rhesus macaques (Macaca mulatta)

Time is a valuable but limited resource, and animals’ survival depends on their ability to carefully manage the amount of time they allocate to each daily activity. While existing research has examined the ecological factors affecting animals’ activity budgets, the impact of anthropogenic factors on urban dwelling animals’ time budgets remains understudied. Here we collected data through focal animal sampling from three groups of rhesus macaques in Northern India to examine whether interactions with humans decrease macaques’ resting and social time (time constraints hypothesis), or whether, by contrast, foraging on anthropogenic food, that is potentially high in calories, leads macaques to spend more time resting and in social interactions (free time hypothesis). We found that macaques who interacted more frequently with people spent significantly less time resting and grooming, supporting the time constraints hypothesis. We argue that these time constraints are likely caused by the unpredictability of human behavior.National Science Foundatio

Implementing social network analysis to understand the socioecology of wildlife co-occurrence and joint interactions with humans in anthropogenic environments

This is an accepted manuscript of an article published by Wiley in Journal of Animal Ecology on 28/08/2021, available online: https://doi.org/10.1111/1365-2656.13584 The accepted version of the publication may differ from the final published version.Human population expansion into wildlife habitats has increased interest in the behavioural ecology of human-wildlife interactions. To date, however, the socio-ecological factors that determine whether, when or where wild animals take risks by interacting with humans and anthropogenic factors still remains unclear. 2.We adopt a comparative approach to address this gap, using social network analysis (SNA). SNA, increasingly implemented to determine human impact on wildlife ecology, can be a powerful tool to understand how animal socioecology influences the spatiotemporal distribution of human-wildlife interactions. 3.For 10 groups of rhesus, long-tailed, and bonnet macaques (Macaca spp.) living in anthropogenically-impacted environments in Asia, we collected data on human-macaque interactions, animal demographics, and macaque-macaque agonistic and affiliative social interactions. We constructed ‘human co-interaction networks’ based on associations between macaques that interacted with humans within the same time and spatial locations, and social networks based on macaque-macaque allogrooming behaviour, affiliative behaviours of short duration (agonistic support, lip-smacking, silent bare-teeth displays, and non-sexual mounting), and proximity. 4.Pre-network permutation tests revealed that, within all macaque groups, specific individuals jointly took risks by repeatedly, consistently co-interacting with humans64within and across time and space. GLMMs revealed that macaques’ tendencies to co-interact with humans was positively predicted by their tendencies to engage in short-duration affiliative interactions and tolerance of conspecifics, although the latter varied across species (bonnets>rhesus>long-tailed). Male macaques were more likely to co-interact with humans than females. Neither macaques’ grooming relationships nor their dominance ranks predicted their tendencies to co-interact with humans. 5.Our findings suggest that, in challenging anthropogenic environments, less (compared to more) time-consuming forms of affiliation, and additionally greater social tolerance in less ecologically flexible species with a shorter history of exposure to humans, may be key to animals’ joint propensities to take risks to gain access to resources. For males, greater exploratory tendencies and less energetically demanding long-term life-history strategies (compared to females), may also influence such joint risk-taking. From conservation and public health perspectives, wildlife connectedness within such co-interaction networks may inform interventions to mitigate zoonosis, and move human-wildlife interactions from conflict towards co-existence.The authors were supported by the U.S. National Science Foundation (Grant no. 1518555) awarded to PI McCowan

Miscarriage and stillbirth following maternal Zika virus infection in nonhuman primates.

Zika virus (ZIKV) infection is associated with congenital defects and pregnancy loss. Here, we found that 26% of nonhuman primates infected with Asian/American ZIKV in early gestation experienced fetal demise later in pregnancy despite showing few clinical signs of infection. Pregnancy loss due to asymptomatic ZIKV infection may therefore be a common but under-recognized adverse outcome related to maternal ZIKV infection

Individuals in urban dwelling primate species face unequal benefits associated with living in an anthropogenic environment

In primates, living in an anthropogenic environment can significantly improve an individual’s fitness, which is likely attributed to access to anthropogenic food resources. However, in non-professionally provisioned groups, few studies have examined whether individual attributes, such as dominance rank and sex, affect primates’ ability to access anthropogenic food. Here, we investigated whether rank and sex explain individual differences in the proportion of anthropogenic food consumed by macaques. We observed 319 individuals living in nine urban groups across three macaque species. We used proportion of anthropogenic food in the diet as a proxy of access to those food resources. Males and high-ranking individuals in both sexes had significantly higher proportions of anthropogenic food in their diets than other individuals. We speculate that unequal access to anthropogenic food resources further increases within-group competition, and may limit fitness benefits in an anthropogenic environment to certain individuals.This work was supported by the U.S. National Science Foundation (Grant no. 1518555)