Genetic differentiation and diversity of the Bolivian endemic titi monkeys, Plecturocebus modestus and Plecturocebus olallae Abstract The genetic variability of New World primates is still poorly documented. We present the first genetic study on two threatened endemic titi monkey species in northern Bolivia (Plecturocebus modestus and Plecturocebus olallae) using six microsatellite markers to investigate genetic structure and variability of 54 individuals from two wild populations. A low level of genetic diversity was found (34 alleles in the total sampled population). Locus 1118 presented the greatest number of alleles. The mean number of alleles per locus in the total population was 5.6 and the average heterozygosity was 0.38 (range 0.12–0.88). The FIS value for the total population using all microsatellite loci shows a statistically significant heterozygote deficit. The inbreeding coefficients (FIS) were positive and significantly different from zero (0.064 for P. olallae and 0.213 for P. modestus). The genetic differentiation between populations (FST) was moderate with a pair-wise FST estimate of 0.14. Population structure analyses assigned the two populations to two differentiated clusters (K = 2). These results suggest that these two species with very close distributional ranges arose from a single population, and that they remain in a process of genetic differentiation and speciation. This study further underlines the urgent need for conservation actions for both endemic primate species.

Do chimpanzees ( Pan troglodytes ) console a bereaved mother? Abstract Comparative thanatology encompasses the study of death-related responses in non-human animals and aspires to elucidate the evolutionary origins of human behavior in the context of death. Many reports have revealed that humans are not the only species affected by the death of group members. Non-human primates in particular show behaviors such as congregating around the deceased, carrying the corpse for prolonged periods of time (predominantly mothers carrying dead infants), and inspecting the corpse for signs of life. Here, we extend the focus on death-related responses in non-human animals by exploring whether chimpanzees are inclined to console the bereaved: the individual(s) most closely associated with the deceased. We report a case in which a chimpanzee (Pan troglodytes) mother experienced the loss of her fully developed infant (presumed stillborn). Using observational data to compare the group members’ behavior before and after the death, we found that a substantial number of group members selectively increased their affiliative expressions toward the bereaved mother. Moreover, on the day of the death, we observed heightened expressions of species-typical reassurance behaviors toward the bereaved mother. After ruling out several alternative explanations, we propose that many of the chimpanzees consoled the bereaved mother by means of affiliative and selective empathetic expressions.

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

Horses and nomads in Mongolia

Population abundance and distribution of the endangered golden langur ( Trachypithecus geei , Khajuria 1956) in Bhutan Abstract Reliable population estimates are lacking for many South Asian primate species, including the golden langur (Trachypithecus geei), which is endangered and restricted to Bhutan and northeast India. Although well studied in India, few studies exist on this species in Bhutan. In November 2017, we undertook a nationwide survey of golden langurs in Bhutan using double observers along trail-based transects in 17 blocks within its habitat, and modeled its distribution using MaxEnt. A total of 2439 golden langurs in 222 groups were collectively encountered by 17 teams of double observers, from which, an overall population of 2516 ± SE 363 individuals and 236 ± SE 9 groups were estimated. Group sizes varied from 2 to 35 individuals with a mean of 11 ± SD 0.38 individuals. A total of 468 adult males (19%), 924 adult females (38%), 649 juveniles (27%), and 398 infants (16%) were counted. Adult male-to-female sex ratio was 1:1.97 and adult female-to-infant ratio was 1:0.43. We determined 2848 km2 of suitable area for golden langurs in Bhutan and estimated a density of 0.88 individuals/km2. Our population estimate of golden langurs in Bhutan is much lower than the current IUCN estimate of 4000 individuals for Bhutan, necessitating a reassessment of its current conservation status due to threats from road kills, electrocution, and development activities like road construction, hydropower, and electrical transmission lines. We further recommend our refined double-observer survey method to reliably estimate primate populations in rugged terrain.

Eulerian videography technology improves classification of sleep architecture in primates Abstract Sleep is a critically important dimension of primate behavior, ecology, and evolution, yet primate sleep is under-studied because current methods of analyzing sleep are expensive, invasive, and time-consuming. In contrast to electroencephalography (EEG) and actigraphy, videography is a cost-effective and non-invasive method to study sleep architecture in animals. With video data, however, it is challenging to score subtle changes that occur in different sleep states, and technology has lagged behind innovations in EEG and actigraphy. Here, we applied Eulerian videography to magnify pixels relevant to scoring sleep from video, and then compared these results to analyses based on actigraphy and standard infrared videography. We studied four species of lemurs (Eulemur coronatus, Lemur catta, Propithecus coquereli, Varecia rubra) for 12-h periods per night, resulting in 6480 1-min epochs for analysis. Cramer’s V correlation between actigraphy-classified sleep and infrared videography-classified sleep revealed consistent results in eight of the nine 12-h videos scored. A sample of the infrared videography was then processed by Eulerian videography for movement magnification and re-coded. A second Cramer’s V correlation analysis, between two independent scorers coding the same Eulerian-processed video, found that interobserver agreement among Eulerian videography increased sleep vs. awake, NREM, and REM classifications by 7.1%, 46.7%, and 34.3%, respectively. Furthermore, Eulerian videography was more strongly correlated with actigraphy data when compared to results from standard infrared videography. The increase in agreement between the two scorers indicates that Eulerian videography has the potential to improve the identification of sleep states in lemurs and other primates, and thus to expand our understanding of sleep architecture without the need for EEG.

High but not low tolerance populations of Japanese macaques solve a novel cooperative task Abstract Currently, it has been revealed that high levels of tolerance facilitate the occurrence of cooperative behavior in animals. This predicts that Japanese macaques (Macaca fuscata) would fail to solve cooperative food-retrieval tasks because of their low level of social tolerance. However, Japanese macaques exhibit regional differences in their levels of tolerance. In this study, we showed how inter-group difference in social tolerance could affect cooperation, by presenting a well-established cooperative rope-pulling task with two free-ranging groups of Japanese macaques that exhibit different levels of social tolerance. We used the task that required two macaques to pull both ends of a single rope simultaneously to obtain food rewards. We found that some macaques from the more tolerant group successfully solved the task, and one of them learned to wait for a partner when a partner was absent. In contrast, however, those of the less tolerant group almost never succeeded in the task. These results indicate that Japanese macaques possess the abilities to cooperate with conspecifics, but such abilities may be constrained in their typically despotic society.

Shape variation in the facial part of the cranium in macaques and African papionins using geometric morphometrics Abstract Macaques are one of the most successful nonhuman primates, and morphological distinctions from their close relatives, African papionins, are easily detected by the naked eye. Nevertheless, evolutionary allometry often accounts for a large amount of the total variation and potentially hides and precludes the detection of morphological distinctions that exist between macaques and African papionins, thus distorting their phyletic comparison. Geometric morpgometric analyses were performed using landmark coordinates in cranial samples from macaques (N =  135) and African papionins (N =  152) to examine the variation in their facial shape. A common allometric trend was confirmed to represent a moderately long face in macaques as being small-to-moderate-bodied papionins. Macaques possessed many features that were distinct from those of African papionins, while they simultaneously showed a large intrageneric variation in every feature, which precluded the separation of some groups of macaques from African papionins. This study confirmed that a moderately smooth sagittal profile is present in non-Sulawesi macaques. It also confirmed that a well-developed anteorbital drop is distinct in Mandrillus and Theropithecus, but it showed that Papio resembles macaques regarding this feature. This finding showed that apparently equivalent features which can be detected by the naked eye were probably formed by different combinations of the principal patterns. It should be noted that the differences detected here between macaques and African papionins are revealed after appropriate adjustments are made to eliminate the allometric effects over the shape features. While landmark data sets still need to be customized for specific studies, the information provided by this article is expected to help such customization and to improve future phyletic evaluation of the fossil papionins.

A green racer snake ( Philodryas nattereri , Colubridae) killed but not eaten by a blonde capuchin monkey ( Sapajus flavius , Cebidae) Abstract We report the killing of a snake (Philodryas nattereri, Colubridae) by a blonde capuchin monkey (Sapajus flavius, Cebidae). This endemic primate species from the northeast of Brazil includes vertebrates such as lizards and marsupials in its diet, but we can find no previously published record of an attack upon or consumption of snakes by this species of platyrhine monkey. During the attack, the group mobbed the snake, with individuals uttering agonistic vocalizations and displaying behaviors such as raising their tails, moving tree branches, piloerecting, and baring their teeth. An adult male monkey seized the snake, bit and twisted its body, thereby killing it; he then dropped the carcass onto tree branches, but did not consume it. This single event suggests that this Cebidae species may be able to distinguish dangerous from harmless snakes, and it also may be an example of a lethally violent reaction to a potential predator or competitor, exemplifying the plasticity and cognitive skills exhibited by genus Sapajus.

Seed dispersal by proboscis monkeys: the case of Nauclea spp. Abstract Frugivorous vertebrates such as primates are important dispersal agents in tropical forests, although the role of folivorous colobines is generally not considered. However, recent studies reported seed dispersal by endo- and epizoochory in colobine primates, including the proboscis monkey (Nasalis larvatus), suggesting that the role colobines play in seed dispersal might have been underestimated. In the Lower Kinabatangan Floodplain in Sabah, Malaysian Borneo, we investigated whether seeds were still able to germinate after being ingested by proboscis monkeys. Faecal samples (n = 201) from proboscis monkeys were collected between 2015 and 2017. Intact seeds belonging to eight plant species were found in 77% of the faecal samples. Nauclea spp. were the most abundant plant species, accounting for 98% of all intact seeds. This study is the first to conduct germination trials on seeds defecated by proboscis monkeys. Higher germination success was recorded in ingested Nauclea spp. seeds than in control seeds, from both ripe and unripe Nauclea orientalis fruits (P < 0.001). Therefore, we suggest that proboscis monkeys play a role in seed dispersal by enhancing the germination success of defecated seeds for at least some plant species. Similar to other colobines, although proboscis monkeys may provide a lower contribution to seed dispersal (low seed diversity over short distances) than other sympatric frugivores, this study emphasises that proboscis monkeys do contribute to the dispersal of intact seeds, such as Nauclea spp., in potentially suitable riverine habitats.