How to treat mixed behavior segments in supervised machine learning of behavioural modes from inertial measurement data.

The application of supervised machine learning methods to identify behavioural modes from inertial measurements of bio-loggers has become a standard tool in behavioural ecology. Several design choices can affect the accuracy of identifying the behavioural modes. One such choice is the inclusion or exclusion of segments consisting of more than a single behaviour (mixed segments) in the machine learning model training data. Currently, the common practice is to ignore such segments during model training. In this paper we tested the hypothesis that including mixed segments in model training will improve accuracy, as the model would perform better in identifying them in the test data. We test this hypothesis using a series of data simulations on four datasets of accelerometer data coupled with behaviour observations, obtained from four study species (Damaraland mole-rats, meerkats, olive baboons, polar bears). Results show that when a substantial proportion of the test data are mixed behaviour segments (above ~ 10%), including mixed segments in machine learning model training improves the accuracy of classification. These results were consistent across the four study species, and robust to changes in segment length, sample size, and degree of mixture within the mixed segments. However, we also find that in some cases (particularly in baboons) models trained with mixed segments show reduced accuracy in classifying test data containing only single behaviour (pure) segments, compared to models trained without mixed segments. Based on these results, we recommend that when the classification model is expected to deal with a substantial proportion of mixed behaviour segments (> 10%), it is beneficial to include them in model training, otherwise, it is unnecessary but also not harmful. The exception is when there is a basis to assume that the training data contains a higher rate of mixed segments than the actual (unobserved) data to be classified-such a situation may occur particularly when training data are collected in captivity and used to classify data from the wild. In this case, excess inclusion of mixed segments in training data should probably be avoided.

Reduction of bitter taste receptor gene family in folivorous colobine primates relative to omnivorous cercopithecine primates.

Bitter taste perception is important in preventing animals from ingesting potentially toxic compounds. Whole-genome assembly (WGA) data have revealed that bitter taste receptor genes (TAS2Rs) comprise a multigene family with dozens of intact and disrupted genes in primates. However, publicly available WGA data are often incomplete, especially for multigene families. In this study, we employed a targeted capture (TC) approach specifically probing TAS2Rs for ten species of cercopithecid primates with diverse diets, including eight omnivorous cercopithecine species and two folivorous colobine species. We designed RNA probes for all TAS2Rs that we modeled to be intact in the common ancestor of cercopithecids ("ancestral-cercopithecid TAS2R gene set"). The TC was followed by short-read and high-depth massive-parallel sequencing. TC retrieved more intact TAS2R genes than found in WGA databases. We confirmed a large number of gene "births" at the common ancestor of cercopithecids and found that the colobine common ancestor and the cercopithecine common ancestor had contrasting trajectories: four gene "deaths" and three gene births, respectively. The number of intact TAS2R genes was markedly reduced in colobines (25-28 detected via TC and 20-26 detected via WGA analysis) as compared with cercopithecines (27-36 via TC and 19-30 via WGA). Birth or death events occurred at almost every phylogenetic-tree branch, making the composition of intact genes variable among species. These results show that evolutionary change in intact TAS2R genes is a complex process, refute a simple general prediction that herbivory favors more TAS2R genes, and have implications for understanding dietary adaptations and the evolution of detoxification abilities.

Estimating individual exposure to predation risk in group-living baboons, Papio anubis.

In environments with multiple predators, vulnerabilities associated with the spatial positions of group-living prey are non-uniform and depend on the hunting styles of the predators. Theoretically, coursing predators follow their prey over long distances and attack open areas, exposing individuals at the edge of the group to predation risk more than those at the center (marginal predation). In contrast, ambush predators lurk unnoticed by their prey and appear randomly anywhere in the group; therefore, isolated individuals in the group would be more vulnerable to predators. These positions of vulnerability to predation are expected to be taken by larger-bodied males. Moreover, dominant males presumably occupy the center of the safe group. However, identifying individuals at higher predation risk requires both simultaneous recording of predator location and direct observation of predation events; empirical observations leave ambiguity as to who is at risk. Instead, several theoretical methods (predation risk proxies) have been proposed to assess predation risk: (1) the size of the individual 'unlimited domain of danger' based on Voronoi tessellation, (2) the size of the 'limited domain of danger' based on predator detection distance, (3) peripheral/center position in the group (minimum convex polygon), (4) the number and direction of others in the vicinity (surroundedness), and (5) dyadic distances. We explored the age-sex distribution of individuals in at-risk positions within a wild baboon group facing predation risk from leopards, lions, and hyenas, using Global Positioning System collars. Our analysis of the location data from 26 baboons revealed that adult males were consistently isolated at the edge of the group in all predation risk proxies. Empirical evidence from previous studies indicates that adult male baboons are the most frequently preyed upon, and our results highlights the importance of spatial positioning in this.

Influence of rainfall on sleeping site choice by a group of anubis baboons (Papio anubis).

For diurnal nonhuman primates, shifting among different sleeping sites may provide multiple benefits such as better protection from predators, reduced risk of parasitic infection, and closer proximity to spatially and temporally heterogeneous food and water. This last benefit may be particularly important in sleeping site selection by primates living in savanna-woodlands where rainfall is more limited and more seasonally pronounced than in rainforests. Here, we examined the influence of rainfall, a factor that affects food and water availability, on the use of sleeping sites by anubis baboons (Papio anubis) over two 13-month study periods that differed in rainfall patterns. We predicted that during wet periods, when food and water availability should be higher, the study group would limit the number of sleeping sites and would stay at each one for more consecutive nights than during dry periods. Conversely, we predicted that during dry periods the group would increase the number of sleeping sites and stay at each one for fewer consecutive nights as they searched more widely for food and water. We also predicted that the group would more often choose sleeping sites closer to the center of the area used during daytime (between 07:00 and 19:00) during wet months than during dry months. Using Global Positioning System data from collared individuals, we found that our first prediction was not supported on either monthly or yearly timescales, although past monthly rainfall predicted the use of the main sleeping site in the second study period. Our second prediction was supported only on a yearly timescale. This study suggests that baboons' choice of sleeping sites is fluid over time while being sensitive to local environmental conditions, one of which may be rainfall.

Capture, immobilization, and Global Positioning System collaring of olive baboons (Papio anubis) and vervets (Chlorocebus pygerythrus): Lessons learned and suggested best practices.

As the value of Global Positioning System (GPS) technology in addressing primatological questions becomes more obvious, more studies will include capturing and collaring primates, with concomitant increased risk of adverse consequences to primate subjects. Here we detail our experiences in capturing, immobilizing, and placing GPS collars on six olive baboons (Papio anubis) in four groups and 12 vervet monkeys (Chlorocebus pygerythrus) in five groups in Kenya. We captured baboons with cage traps and vervets with box traps, immobilized them, and attached GPS collars that were to be worn for 1 year. Adverse consequences from the trapping effort included incidental death of two nonsubjects (an adult female and her dependent infant), temporary rectal prolapse in one baboon, superficial wounds on the crown of the head in two vervets, and failure to recapture/remove collars from two baboons and two vervets. Obvious negative effects from wearing collars were limited to abrasions around the neck of one vervet. A possible, and if so, serious, adverse effect was greater mortality for collared adult female vervets compared with known uncollared adult female vervets, largely due to leopard (Panthera pardus) predation. Collared animals could be more vulnerable to predation because trapping favors bolder individuals, who may also be more vulnerable to predation, or because collars could slow them down or make them more noticeable to predators. Along with recommendations made by others, we suggest that future studies diversify trapping bait to minimize the risk of rectal prolapse, avoid capturing the first individuals to enter traps, test the movement speeds of collared versus noncollared animals, include a release system on the collars to avoid retrapping failure, and publish both positive and negative effects of capturing, immobilizing, and collaring.

Complete rectal prolapse in wild anubis baboons (Papio anubis).

This report describes two cases of rectal prolapse in wild anubis baboons (Papio anubis), with one spontaneous resolution. Both occurred after individuals consumed low-water, high-fibre dried maize during provisioning prior to capture, while one also experienced distress during capture.

Expression Changes of Structural Protein Genes May Be Related to Adaptive Skin Characteristics Specific to Humans.

Human skin is morphologically and physiologically different from the skin of other primates. However, the genetic causes underlying human-specific skin characteristics remain unclear. Here, we quantitatively demonstrate that the epidermis and dermis of human skin are significantly thicker than those of three Old World monkey species. In addition, we indicate that the topography of the epidermal basement membrane zone shows a rete ridge in humans but is flat in the Old World monkey species examined. Subsequently, we comprehensively compared gene expression levels between human and nonhuman great ape skin using next-generation cDNA sequencing (RNA-Seq). We identified four structural protein genes associated with the epidermal basement membrane zone or elastic fibers in the dermis (COL18A1, LAMB2, CD151, and BGN) that were expressed significantly greater in humans than in nonhuman great apes, suggesting that these differences may be related to the rete ridge and rich elastic fibers present in human skin. The rete ridge may enhance the strength of adhesion between the epidermis and dermis in skin. This ridge, along with a thick epidermis and rich elastic fibers might contribute to the physical strength of human skin with a low amount of hair. To estimate transcriptional regulatory regions for COL18A1, LAMB2, CD151, and BGN, we examined conserved noncoding regions with histone modifications that can activate transcription in skin cells. Human-specific substitutions in these regions, especially those located in binding sites of transcription factors which function in skin, may alter the gene expression patterns and give rise to the human-specific adaptive skin characteristics.

The role of sleeping sites in the predator-prey dynamics of leopards and olive baboons.

Predation is widely recognized as an important selective pressure on prey animals such as baboons (Papio spp.), which face high leopard (Panthera pardus) predation risk, particularly at night. Baboons regularly sleep on cliff faces and in trees at night, ostensibly to avoid such predators. Despite retreating to such "refuges," baboons are most often killed by leopards at or near their sleeping sites. Because of the challenges of studying nocturnal behavior and human-averse predators, few systematic data exist to reveal how leopard ranging near baboon sleeping sites influences baboons' selection of sites and behavior at those sites. To investigate leopard-baboon dynamics at sleeping sites we deployed GPS/VHF radio collars on six representatives of four baboon groups and four leopards during a 14-month field study in Kenya. We used locations recorded every 15 min to identify baboons' cliffside and riverine sleeping sites, the frequency and duration of leopard visits to these sites, and baboons' adjustments in site use after leopard visits. Collared leopards visited riverine sites more frequently than cliffside sites, whereas most baboon groups strongly preferred cliffside sites, suggesting that leopard visits were often due to factors other than baboon presence, and that baboons used cliffside sites to reduce their risk of leopard predation. Regardless of type, collared leopards remained near baboon-occupied sleeping sites longer than vacant ones, indicating interest in hunting baboons then. Baboons at riverine sites departed later on mornings after leopard visits. Baboon groups occasionally shared sleeping sites simultaneously, possibly reducing risk through dilution. However, they did not reduce risk by frequently changing sleeping sites, minimizing detection at sleeping sites, or after leopard visits, arriving earlier the next evening or moving to a different site. Future research should explore if baboons readily detect nocturnal leopard presence and if predation-related changes in sleeping site use have cascading ecological effects.

Wound healing in wild male baboons: Estimating healing time from wound size.

Wound healing in animals is important to minimize the fitness costs of infection. Logically, a longer healing time is associated with higher risk of infection and higher energy loss. In wild mammals, wounds caused by aggressive intraspecific interactions can potentially have lethal repercussions. Clarifying wounding rate and healing time is therefore important for measuring the severity of the attacks. In addition, impact of secondary damage of wounds (e.g., accidental peeling off of scabs) on heeling time is unknown despite the risk of infection in wild mammals. In baboons, most male injuries have been reported to result from male to male fights. Here, we investigated the relationship between wound size and healing time in wild anubis baboons to clarify the healing cost of physical attacks including secondary damage of wounds. Observations were conducted daily between August 2016 and July 2017 in Kenya for seven adult male anubis baboons. The individual wound rate was one per month on average. In 16 cases, we were able to assess the number of days required for wound healing, and the median healing time was 13 d. Wound healing time was longer for larger wounds. When the scab was peeled off accidentally because of external factors, healing time became longer. One of the causes of scabs' peeling off was baboons' scab-picking behavior, and the behaviour was considered self-injurious behavior. However, its predicted healing cost might not be high. We concluded that wounds less than 800 mm2 (the largest observed in this study) in baboon males have little effect on survival. Our results suggest that lethal wounds by physical attacks rarely occur in male baboons, and that healing time and delay caused by secondary damages can be estimated by measuring wound area.

Group size effects on inter-blink interval as an indicator of antipredator vigilance in wild baboons.

Vigilance in animals is an important means for predator detection. Animals living in groups reduce their predation risk as more individuals are present. In contrast to most other animals studied, many studies on primates do not support the prediction that individual vigilance will decline as group size increases. For animals to obtain visual information during vigilance behaviour, their eyes must be open. Therefore, if animals are able to perceive differential risk of predation, the inter-blink interval (eye-opening) should increase, and the blink duration (eye-closure) should decrease under higher predation risk. We tested this prediction by measuring inter-blink interval in wild anubis baboons (Papio anubis) in peripheral and centre individuals within a group, and between larger and smaller groups. We found that the inter-blink interval for young males, often located at the front edge of the group, was longer than that of adult males, adult females, and young females, often located in the center of the group, and that the inter-blink interval for adult males was longer when the group was smaller. These results suggest that inter-blink interval can be used as an indicator of primate vigilance toward predators.

GPS-identified vulnerabilities of savannah-woodland primates to leopard predation and their implications for early hominins.

Predation is thought to have been a key selection pressure in primate evolution, especially in the savannah-woodland habitats where several early hominin species lived. However, predator-primate prey relationships are still poorly understood because human presence often deters predators, limiting our ability to quantify the impact of predation. Synchronized high-resolution tracking of leopards (Panthera pardus), vervets (Chlorocebus pygerythrus), and olive baboons (Papio anubis) during a 14-month study in Kenya revealed that increased vulnerability to leopard predation was not associated with higher encounter rates, smaller body size, smaller group size, or greater distance from refuges, contrary to long-standing inferences. Instead, the initiation, rate, timing, and duration of encounters, outcome of approaches, and predation events showed only a diel pattern of differential vulnerability. In the absence of human observers, vervets were more vulnerable during the day, whereas baboons were more vulnerable at night, but overall neither species was more vulnerable than the other. As our results show that leopards avoided baboons during the day and hunted them at night, we suggest that the same pattern would have applied to hominins-because they were even larger than baboons and bipedal, resulting in similarly offensive capability on the ground during the day but poorer agility in the trees at night, especially as they became committed bipeds. Drawing from hominid behavior and archaeopaleontological and ethnographic evidence, we hypothesize that ground-sleeping hominins initially dealt with this formidable threat by using stone tools to modify Acacia branches into 'bomas', thorny enclosures that provided nighttime shelter. The ability of hominins to create their own nightly refuges on the ground wherever Acacia spp. were available would have allowed them to range more widely, a crucial step in furthering the spread of hominins across Africa and beyond.

GPS-identified, low-level nocturnal activity of vervets (Chlorocebus pygerythrus) and olive baboons (Papio anubis) in Laikipia, Kenya.

OBJECTIVES: Except for owl monkeys (Aotus spp.), all anthropoid primates are considered strictly diurnal. Recent studies leveraging new technologies have shown, however, that some diurnal anthropoids also engage in nocturnal activity. Here we examine the extent to which vervets (Chlorocebus pygerythrus) and olive baboons (Papio anubis) are active at night. MATERIALS AND METHODS: We deployed GPS collars with tri-axial accelerometer data loggers on 18 free-ranging adult females: 12 vervets spread among 5 social groups, and 6 olive baboons spread among 4 groups. Their locations were recorded every 15 min, and their activity levels, for 3 s/min over 7.5 months. We also used camera traps that were triggered by heat and movement at seven sleeping sites. RESULTS: Travel was detected on 0.4% of 2,029 vervet-nights involving 3 vervets and 1.1% of 1,109 baboon-nights involving 5 baboons. Travel was mainly arboreal for vervets but mainly terrestrial for baboons. During the night, vervets and baboons were active 13% and 15% of the time, respectively. Activity varied little throughout the night and appeared unaffected by moon phase. DISCUSSION: Our results confirm the low nocturnality of vervets and olive baboons, which we suggest is related to living near the equator with consistent 12-hr days, in contrast to other anthropoids that are more active at night. Since anthropoid primates are thought to have evolved in northern latitudes, with later dispersal to tropical latitudes, our results may have implications for understanding the evolution of anthropoid diurnality.

Sexually dimorphic preference for altruism in the opposite sex according to recipient.

Sexual selection may affect human altruistic behaviour. Evolutionary psychology predicts that human mate preference reflects sexual selection. We investigated sex differences in preference for opposite-sex altruism according to recipient because the reasons for altruistic behaviour differ according to the relationship between actor and recipient. We employed the Self-Report Altruism Scale Distinguished by the Recipient, which was newly developed to evaluate altruism among Japanese undergraduates. We asked participants to evaluate preferences for each item based on the recipient of the altruistic behaviour (family members, friends or acquaintances, and strangers). Preference for opposite-sex altruism differed according to recipient, gender of the participant, and relationship type, and several significant interactions were observed among these factors. We suggest that whereas women use a potential partner's altruism towards strangers as a costly signal of their resource-holding potential when choosing a mate, they consider altruism towards family when they are in a long-term relationship to ensure that resources are not allocated to non-relatives.

Ranging behavior of Mahale chimpanzees: a 16 year study.

We have analyzed the ranging patterns of the Mimikire group (M group) of chimpanzees in the Mahale Mountains National Park, Tanzania. During 16 years, the chimpanzees moved over a total area of 25.2 or 27.4 km(2), as estimated by the grid-cell or minimum convex polygon (MCP) methods, respectively. Annually, the M group used an average of 18.4 km(2), or approximately 70 %, of the total home-range area. The chimpanzees had used 80 % of their total home range after 5 years and 95 % after 11 years. M group chimpanzees were observed more than half of the time in areas that composed only 15 % of their total home range. Thus, they typically moved over limited areas, visiting other parts of their range only occasionally. On average, the chimpanzees used 7.6 km(2) (in MCP) per month. Mean monthly range size was smallest at the end of the rainy season and largest at the end of the dry season, but there was much variability from year to year. The chimpanzees used many of the same areas every year when Saba comorensis fruits were abundant between August and January. In contrast, the chimpanzees used several different areas of their range in June. Here range overlap between years was relatively small. Over the 16 years of the study we found that the M group reduced their use of the northern part of their range and increased their frequency of visits to the eastern mountainous side of their home range. Changes in home-range size correlated positively with the number of adult females but not with the number of adult males. This finding does not support a prediction of the male-defended territory model proposed for some East African chimpanzee unit-groups.

Estrous asynchrony causes low birth rates in wild female chimpanzees.

Estrous cycle asynchrony likely functions to elevate individual females' sexual attractiveness during female mate choice. Female chimpanzees show physiological estrus as anogenital swelling. Copulations are concentrated during the period of maximal tumescence, which is called the estrous period. A group of female chimpanzees in Mahale Mountains National Park, Tanzania, was shown to display asynchrony in both maximal tumescence and periovulatory periods. We tested the hypothesis that females establish asynchronous maximal tumescence or periovulatory periods with respect to other females to increase copulation frequency and birth opportunities (Hypothesis 1). We analyzed differences in birth rates between four asynchronous years and five nonasynchronous years. Counter to Hypothesis 1, females in periovulatory periods during asynchronous years showed significantly lower birth rates than those in nonasynchronous years. In addition, periovulatory females copulated more frequently on days on which no other female in a periovulatory period was present. These results suggest that birth rates tend to decrease when females experience nonoverlapping ovulation cycles, although copulation frequency is high. Such a decrease in the birth rate may have resulted from the cost associated with multiple copulations. We tested two other hypotheses: paternity confusion (Hypothesis 2) and sperm competition (Hypothesis 3). Both of these hypotheses were partially supported. The highest-ranking male most effectively monopolized access to receptive females when relatively few other males and receptive females from the party (or subgroup) were present. The viability of Hypotheses 2 and 3 requires that dominant males are able to hinder a female from mating with other males. Given that the male-biased operational sex ratio created by female asynchrony is likely to reduce the efficiency of mate guarding by dominant males, an asynchronous female may gain a fitness benefit by increasing the probability of mating with at least one male who produces superior sperm.

Cross-cultural perceptions of facial resemblance between kin.

Humans use facial comparisons to identify their relatives and adjust their behavior accordingly. However, the mechanisms underlying the assessment of facial similarities are poorly known. Here, we investigate the role of exposure to particular faces for the detection of facial similarities by asking judges to detect parent-child pairs using faces from different origins. In a first phase, French and Senegalese judges assessed facial resemblance in French and Senegalese families. In a second phase, Senegalese judges who had immigrated to France, as well as French and Senegalese stationary judges, were asked to rate a second set of Senegalese and French families. The judges showed no differences in their ability to detect parent-child pairs in French and Senegalese families in both the first and second phases. For judges who changed their country of residence, the answer time and duration of stay in the new country were not associated with correct assignment rates. Our results suggest that exposure has a limited role in the ability to process facial resemblance in others, which contrasts with facial recognition processing. We also discuss whether processing facial similarities is a by-product of the facial recognition system or an evolved ability to assess kinship relationships.

Altruists are trusted based on non-verbal cues.

The identification of altruists based on non-verbal cues might offer a solution to the problem of subtle cheating. Previous studies have indicated that the ability to discriminate altruists from non-altruists emerges during evolution. However, behavioural differences with regard to social exchanges involving altruists and non-altruists have not been studied. We investigated differences in responses to videotaped altruists and non-altruists with the Faith Game. Participants tended to entrust real money to altruists more than to non-altruists, providing strong evidence that cognitive adaptations evolve as counter-strategies to subtle cheating.

Sniffing behaviors in Mahale chimpanzees.

Although it is difficult for observers to determine how non-human primates use olfaction in a natural environment, sniffing is one clue. In this study, the sniffing behaviors of wild chimpanzees were divided into six categories, and sex differences were found in most categories. Males sniffed more frequently than females in sexual and social situations, while females sniffed more often during feeding and self-checking. Chimpanzees sniffed more frequently during the dry season than during the wet season, presumably due to the low humidity. This suggests that the environment affects olfactory use by chimpanzees and that chimpanzees easily gather new information from the ground via sniffing.

Proximity and estrous synchrony in Mahale chimpanzees.

Since McClintock [Nature 229:244-255, 1971] first reported menstrual synchrony in women, a number of studies have reported similar phenomena. Many researchers have suggested that one of the proximate factors leading to synchrony is spatial proximity among females (e.g., close friends or roommates). However, most studies on menstrual synchrony have been conducted in limited spaces, and it remains to be determined whether controlled environments, such as those used in experiments, actually exist in the wild. In this study, we analyzed the relationship between proximity and estrous synchrony using data from wild female chimpanzees at Mahale, Tanzania. In the cycling females, we observed two pairs that spent a large amount of time together. We compared the estrous synchrony indices (ESIs) between these two pairs and the other females. Our results showed that the ESIs of the high-proximity pairs did not differ from those of other pairs. .