First noncontact millimeter-wave radar measurement of heart rate in great apes: Validation in chimpanzees (Pan troglodytes).

Heart rate is a crucial vital sign and a valuable indicator for assessing the physical and psychological condition of a target animal. Heart rate contributes to (1) fundamental information for cognitive research, (2) an indicator of psychological and physical stress, and (3) improving the animal welfare of captive animals, especially in nonhuman primate studies. Heart rate has been measured using a contact-type device; however, the device burdens the target animals and that there are risks associated with anesthesia during installation. This study explores the application of heartbeat measurement techniques using millimeter-wave radar, primarily developed for humans, as a remote and noninvasive method for measuring the heart rate of nonhuman primates. Through a measurement test conducted on two chimpanzees, we observed a remarkable correspondence between the peak frequency spectrum of heart rate estimated using millimeter-wave radar and the mean value obtained from electrocardiograph data, thereby validating the accuracy of the method. To the best of our knowledge, this is the first demonstration of the precise measurement of great apes' heart rate using millimeter-wave radar technology. Compared to heart rate measurement using video analysis, the method using millimeter-wave radar has the advantage that it is less susceptible to weather and lighting conditions and that measurement techniques for multiple individuals have been developed for human subjects, while its disadvantage is that validation of measurement from long distances has not been completed. Another disadvantage common to both methods is that measurement becomes difficult when the movement of the target individual is large. The possibility of noncontact measurement of heart rate in wild and captive primates will undoubtedly open up a new research area while taking animal welfare into consideration.

Measuring heart rate in captive chimpanzees without anesthesia.

Heart rate measurements can be useful for the monitoring of both physical and mental condition in humans and nonhuman animals. Yet, information about heart rates in chimpanzees, who are phylogenetically the closest species to humans, is scarce. Existing data on chimpanzee heart rates have mainly been collected from chimpanzees under anesthesia. To address this issue, we conducted electrocardiogram recordings in captive chimpanzees under normal conditions without anesthesia based on positive reinforcement training. We obtained a total of 771 recordings from 35 individuals (22 males and 13 females, 14-53 years old) with no cardiac problems. The females had a higher heart rate than the male chimpanzees, and heart rate decreased as a function of age. In addition, heart rate was lower in the morning and increased during the day. Overall, the mean heart rate of adult males was 86.5 beats/min, and that of female chimpanzees 106.4 beats/min. Our data could serve as a reference point for future research and health-based monitoring of chimpanzee heart rates.

State-transition-free reinforcement learning in chimpanzees (Pan troglodytes).

The outcome of an action often occurs after a delay. One solution for learning appropriate actions from delayed outcomes is to rely on a chain of state transitions. Another solution, which does not rest on state transitions, is to use an eligibility trace (ET) that directly bridges a current outcome and multiple past actions via transient memories. Previous studies revealed that humans (Homo sapiens) learned appropriate actions in a behavioral task in which solutions based on the ET were effective but transition-based solutions were ineffective. This suggests that ET may be used in human learning systems. However, no studies have examined nonhuman animals with an equivalent behavioral task. We designed a task for nonhuman animals following a previous human study. In each trial, participants chose one of two stimuli that were randomly selected from three stimulus types: a stimulus associated with a food reward delivered immediately, a stimulus associated with a reward delivered after a few trials, and a stimulus associated with no reward. The presented stimuli did not vary according to the participants' choices. To maximize the total reward, participants had to learn the value of the stimulus associated with a delayed reward. Five chimpanzees (Pan troglodytes) performed the task using a touchscreen. Two chimpanzees were able to learn successfully, indicating that learning mechanisms that do not depend on state transitions were involved in the learning processes. The current study extends previous ET research by proposing a behavioral task and providing empirical data from chimpanzees.

Show me your best side: Lateralization of social and resting behaviors in feral horses.

Growing evidence shows a variety of sensorial and motor asymmetries in social and non-social interactions in various species, indicating a lateralized processing of information by the brain. Using digital video cameras on tripods and drones, this study investigated lateralization in frequency and duration of social behavior patterns, in affiliative, agonistic, and resting contexts, in a feral population of horses (Equus ferus caballus) in Northern Portugal, consisting of 37 individuals organized in eight harem groups. Affiliative interactions (including grooming) were more often performed, and lasted longer, when recipients were positioned to the right side. In recumbent resting (animals lying down) episodes on the left side lasted longer. Our results of an affiliative behavior having a right side tendency, provide partial support to the valence-specific hypothesis of Ahern and Schwartz (1979) - left hemisphere dominance for positive affect, affiliative behaviors. Longer recumbent resting episodes on the left side may be due to synchronization. However, in both instances it is discussed how lateralization may be context dependent. Investigating the position asymmetries of social behaviors in feral equids will contribute to a better understanding of differential lateralization and hemispheric specialization from the ecological and evolutionary perspectives.

Non-contact respiratory measurement in a horse in standing position using millimeter-wave array radar.

This study aimed to apply radar technology to a large quadruped animal. We first developed a non-contact respiration measurement system using millimeter-wave array radar for a horse in standing position. Specifically, we measured the respiration of a stationary domestic horse in stables. Simultaneously, we measured the respiration rate using infrared thermography and developed a method for analyzing the radar information while verifying the rate of agreement. Our results suggested that the radar technology detected breathing and accurately measured the respiration of a horse, despite variation in the breathing frequency. To the best of our knowledge, this is the first study to apply a non-contact respiration measurement system using millimeter-wave array radar has been applied to large animals in an upright position, thereby demonstrating its potential application in animal husbandry and welfare.

Hepatitis C virus infection reduces the lifespan of chimpanzees used in biomedical research.

Chimpanzees were used in hepatitis research for over three decades with the aim to identify and develop treatments for the virus, a leading cause of chronic liver disease in humans. We used a dataset of 120 chimpanzees housed at a single institution in Japan, 22 of whom became chronically infected with hepatitis C virus (HCV), to examine whether HCV infection results in a reduced lifespan as reported in humans. Survival analysis showed that HCV carriers experienced a higher mortality risk compared with non-carriers. Although no chimpanzee died from hepatic disease, carriers showed higher gamma-glutamyl transpeptidase (γGTP) levels compared with non-carriers suggesting that HCV infection negatively affected their liver condition. These results provide evidence that special attention is necessary to monitor the long-term condition of ex-biomedical primates.

Cerebral cortical processing time is elongated in human brain evolution.

An increase in number of neurons is presumed to underlie the enhancement of cognitive abilities in brain evolution. The evolution of human cognition is then expected to have accompanied a prolongation of net neural-processing time due to the accumulation of processing time of individual neurons over an expanded number of neurons. Here, we confirmed this prediction and quantified the amount of prolongation in vivo, using noninvasive measurements of brain responses to sounds in unanesthetized human and nonhuman primates. Latencies of the N1 component of auditory-evoked potentials recorded from the scalp were approximately 40, 50, 60, and 100 ms for the common marmoset, rhesus monkey, chimpanzee, and human, respectively. Importantly, the prominent increase in human N1 latency could not be explained by the physical lengthening of the auditory pathway, and therefore reflected an extended dwell time for auditory cortical processing. A longer time window for auditory cortical processing is advantageous for analyzing time-varying acoustic stimuli, such as those important for speech perception. A novel hypothesis concerning human brain evolution then emerges: the increase in cortical neuronal number widened the timescale of sensory cortical processing, the benefits of which outweighed the disadvantage of slow cognition and reaction.

Chimpanzees (Pan troglodytes) exhibit gaze bias for snakes upon hearing alarm calls.

Calls of several species of nonhuman animals are considered to be functionally referential. However, the cognitive mechanisms underlying audience behaviors remain unclear. This study used an audiovisual cross-modal preferential-looking paradigm to examine whether captive chimpanzees spontaneously associated a conspecific call with images of a corresponding item. Chimpanzees were presented with videos of snakes and fruit side-by-side while hearing playbacks of alarm calls, food-associated calls, or no sound (as a baseline condition). Chimpanzees looked at videos of snakes for longer when hearing alarm calls compared with food calls or baseline. However, chimpanzees did not look at videos of fruit for longer when hearing food calls compared with baseline. An additional experiment tested whether chimpanzees' gaze bias to the snake videos was driven by negative affective states in general via affect-driven attention biases. When chimpanzees were presented with the same snake and fruit videos while hearing playbacks of conspecific screams or no sound, they exhibited no gaze bias for snake videos. These results suggest that chimpanzees spontaneously associated alarm calls with images of a potential threat in a preferential-looking experiment and that this response was not simply driven by an affective state matching process. These findings should be interpreted in consideration of a procedural limitation related to pseudoreplication in the experimental stimuli. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

The Eyes Are More Eloquent Than Words: Anticipatory Looking as an Index of Event Memory in Alzheimer's Disease.

Alzheimer's disease (AD) is a disorder in which individuals experience a difficulty in maintaining event memory for when, where, who, and what. However, verbal deficiency, one of the other symptoms of AD, may prevent a precise diagnosis of event memory because existing tests are based on verbal instructions by the tester and verbal response from patient. Therefore, non-verbal methods are essential to evaluate event memory in AD. The present study, using eye tracking, investigated whether AD patients deployed anticipatory looking to target acts related to future events based on previous experience when an identical video was presented to them twice. The results revealed the presence of anticipatory looking, although AD patients were unable to verbally report the content of the video. Our results illustrate that AD patients have a one-time event memory better than previously thought.

Putrescine--a chemical cue of death-is aversive to chimpanzees.

As in many other species of nonhuman primates, chimpanzee mothers with a dead infant may continue to care for and transport the infant for days, weeks, or even longer. The bereaved females do this despite what humans perceive as the foul odour from the putrefying corpse. Putrescine is a major contributor to the "smell of death," and it elicits behaviours aimed at getting rid of the source of the smell, or escape responses in mammals including humans. However, it has never been shown that the odour of putrescine is aversive to chimpanzees. To address this question, we visually presented six adult chimpanzees with the corpse of a small bird, or a stuffed glove, in association with putrescine, ammonia, or water, and recorded the chimpanzees' reactions. The apes spent significantly less time near the object when it was paired with putrescine than the other substances, although they showed no signs of increased arousal or anxiety. We interpret the findings as evidence of an aversion to the smell of death in chimpanzees, discuss the implications for understanding the continued maternal-like behaviour of bereaved female chimpanzees, and suggest future research directions for the field of comparative evolutionary thanatology.

Behavioural synchronization in a multilevel society of feral horses.

Behavioural synchrony among individuals is essential for group-living organisms. The functioning of synchronization in a multilevel society, which is a nested assemblage of multiple social levels between many individuals, remains largely unknown. The aim of the present study was to build a model that explained the synchronization of activity in a multilevel society of feral horses. Multi-agent-based models were used based on four hypotheses: A) horses do not synchronize, B) horses synchronize with any individual in any unit, C) horses synchronize only within units, and D) horses synchronize across and within units, but internal synchronization is stronger. The empirical data obtained from drone observations best supported hypothesis D. This result suggests that animals in a multilevel society coordinate with other conspecifics not only within a unit but also at an inter-unit level. In this case, inter-individual distances are much longer than those in most previous models which only considered local interaction within a few body lengths.

Plant-eating carnivores: Multispecies analysis on factors influencing the frequency of plant occurrence in obligate carnivores.

Plant-eating behavior is one of the greatest mysteries in obligate carnivores. Despite unsuitable morphological and physiological traits for plant consumption, the presence of plants in scat or stomach contents has been reported in various carnivorous species. However, researchers' interpretations of this subject are varied, and knowledge about it is scarce, without any multispecies studies. This study assessed the extent of variation in the frequency of plant occurrence in scat and stomach contents, as well as its relationship with various factors in 24 felid species using data from 213 published articles. Since the frequency of plant occurrence has not always been reported, we created two-part models and estimated parameters in a Bayesian framework. We found a significant negative relationship between the frequency of plant occurrence and body mass. This may be because plant-eating behavior reduces the energy loss caused by parasites and increases the efficiency of energy intake, which has a greater importance in smaller animals that have relatively high metabolic rates. This exploratory study highlights the importance of considering plant consumption in dietary studies on carnivorous species to understand the adaptive significance of this behavior and the relationship between obligate carnivores and plants.

Comparative survival analyses among captive chimpanzees (Pan troglodytes) in America and Japan.

Detailed, long-term datasets on the life histories of long-lived species such as great apes are necessary to understand their survival patterns but are relatively rare. Such information requires prolonged and consistent record-keeping over many generations, so for chimpanzees (Pan troglodytes), this equates to many decades of input. As life history variables can be altered by differences in environmental influences (whether natural or artificial), there is substantial value to being able to compare across populations. Here, we present the first comparative analysis of life history data for two ex situ chimpanzee populations residing in North America (1975-2020; n = 730) and Japan (1980-2020; n = 660). Overall, survival patterns were similar between regions, and the median life expectancy from birth is estimated at 35.7 (95% CI = [32.4-40.0]) years for females and 30.1 (27.3-34.3) years for males across both populations. Females who survive to their first birthday are estimated to survive 42.4 (40.0-46.3) years and males 35.5 (32.6-38.0) years. We found that birth type (wild-born or captive-born) did not influence survival patterns in either population, but there were differential effects of sex on longevity. In the America population, males had higher mortality rates than females, whereas in the Japan population we found no differences between the sexes. First year mortality did not differ between populations for males (18-20%), but for females it was lower in America (15%) compared to Japan (25%). Survival patterns of chimpanzees in the present study will be useful for future investigation into potential causes of regional differences and cross-species comparisons.

Great apes' understanding of biomechanics: eye-tracking experiments using three-dimensional computer-generated animations.

Visual processing of the body movements of other animals is important for adaptive animal behaviors. It is widely known that animals can distinguish articulated animal movements even when they are just represented by points of light such that only information about biological motion is retained. However, the extent to which nonhuman great apes comprehend the underlying structural and physiological constraints affecting each moving body part, i.e., biomechanics, is still unclear. To address this, we examined the understanding of biomechanics in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), following a previous study on humans (Homo sapiens). Apes underwent eye tracking while viewing three-dimensional computer-generated (CG) animations of biomechanically possible or impossible elbow movements performed by a human, robot, or nonhuman ape. Overall, apes did not differentiate their gaze between possible and impossible movements of elbows. However, some apes looked at elbows for longer when viewing impossible vs. possible robot movements, which indicates that they may have had knowledge of biomechanics and that this knowledge could be extended to a novel agent. These mixed results make it difficult to draw a firm conclusion regarding the extent to which apes understand biomechanics. We discuss some methodological features that may be responsible for the results, as well as implications for future nonhuman animal studies involving the presentation of CG animations or measurement of gaze behaviors.

New indices to characterize drawing behavior in humans (Homo sapiens) and chimpanzees (Pan troglodytes).

Techniques used in cave art suggest that drawing skills emerged long before the oldest known representative human productions (44,000 years BC). This study seeks to improve our knowledge of the evolutionary origins and the ontogenetic development of drawing behavior by studying drawings of humans (N = 178, 3- to 10-year-old children and adults) and chimpanzees (N = 5). Drawings were characterized with an innovative index based on spatial measures which provides the degree of efficiency for the lines that are drawn. Results showed that this index was lowest in chimpanzees, increased and reached its maximum between 5-year-old and 10-year-old children and decreased in adults, whose drawing efficiency was reduced by the addition of details. Drawings of chimpanzees are not random suggesting that their movements are constrained by cognitive or locomotor aspect and we cannot conclude to the absence of representativeness. We also used indices based on colors and time and asked children about what they drew. These indices can be considered relevant tools to improve our understanding of drawing development and evolution in hominids.

Comparative analysis of sperm motility in liquid and seminal coagulum portions between Bornean orangutan (Pongo pygmaeus) and chimpanzee (Pan troglodytes).

Coagulum in the semen of some primates plays different roles, depending on the species. In the present study, we examined sperm motility in the coagulum and liquid portions of semen collected from captive individuals from two great ape species: two adult Bornean orangutans (Pongo pygmaeus) (n = 27) and three adult chimpanzees (Pan troglodytes) (n = 14). The results revealed that orangutan sperm remained motile for significantly longer in the coagulum than in the liquid portion (> 18 h). By contrast, chimpanzee sperm motility did not differ significantly over time between the two portions of the semen, although motility was slightly higher in the liquid portion than in the coagulum. The evolution of the seminal coagulum is thought to be related to postcopulatory sperm competition; however, functions of seminal coagulum have not been completely elucidated. Our data from the orangutan semen suggest that in this species, seminal coagulum may strengthen own-sperm survival. This report is the first to provide evidence for this distinctive function of the seminal coagulum. This unique property of orangutan seminal coagulum might be attributable to their reproductive traits, e.g., difficulty in predicting ovulation due to a lack of genital swelling during estrus. The orangutan is a Critically Endangered species, and captive breeding, including artificial insemination (AI), is expected. However, worldwide, only one case of orangutan AI has been successful. Our findings may contribute to an understanding of their basic semen characteristics and help improve the AI method.

Aerial drone observations identified a multilevel society in feral horses.

The study of non-human multilevel societies can give us insights into how group-level relationships function and are maintained in a social system, but their mechanisms are still poorly understood. The aim of this study was to apply spatial association data obtained from drones to verify the presence of a multilevel structure in a feral horse society. We took aerial photos of individuals that appeared in pre-fixed areas and collected positional data. The threshold distance of the association was defined based on the distribution pattern of the inter-individual distance. The association rates of individuals showed bimodality, suggesting the presence of small social organizations or "units". Inter-unit distances were significantly smaller than those in randomly replaced data, which showed that units associate to form a higher-level social organization or "herd". Moreover, this herd had a structure where large mixed-sex units were more likely to occupy the center than small mixed-sex units and all-male-units, which were instead on the periphery. These three pieces of evidence regarding the existence of units, unit association, and stable positioning among units strongly indicated a multilevel structure in horse society. The present study contributes to understanding the functions and mechanisms of multilevel societies through comparisons with other social indices and models as well as cross-species comparisons in future studies.