Wild chimpanzees deprived a leopard of its kill: Implications for the origin of hominin confrontational scavenging.

This study reports the first observed case of wild chimpanzees (Pan troglodytes) obtaining animal prey freshly killed by a sympatric leopard (Panthera pardus) and scavenging it with the leopard still nearby. This observation has important implications for the emergence of confrontational scavenging, which may have played a significant role in human evolution. Many scholars agree that eating meat became important during human evolution, and hominins first obtained meat by scavenging. However, it is debatable whether scavenging behavior was "passive" or "confrontational (power)." The latter is more dangerous, as it requires facing the original predator, and it is thus considered to have been important for the evolution of several human traits, including cooperation and language. Chimpanzees do scavenge meat, although rarely, but no previous evidence of confrontational scavenging has hitherto emerged. Thus, it was assumed that they are averse to confrontation with even leopard-sized predators. However, in the observed case the chimpanzees frequently emitted waa barks, which indicated that they were aware of the leopard's presence but they nevertheless continued to eat the scavenged meat. In addition, we compiled and reviewed 49 cases of chimpanzee encounters with animal carcasses in the Mahale Mountains of Tanzania in 1980-2017. Chimpanzees scavenged meat in 36.7% of these cases, and tended to eat the meat when it was fresh or if the animal species was usually hunted by chimpanzees. However, no evidence indicated that carcasses were avoided when leopard involvement was likely. These results suggest that chimpanzee-sized hominins could potentially confront and deprive leopard-size carnivores of meat.

What volume of seeds can a chimpanzee carry in its body?

Great apes are important seed dispersers with large bodies, able to swallow large seeds and travel long distances. Although there have been several studies investigating seed dispersal quality [sensu Schupp (Vegetatio 107/108:15-29, 1993)] by chimpanzees, there is little information on the volume of seeds they can carry in their bodies. When a relatively fresh corpse of a mature female chimpanzee was found at Mahale, Tanzania, we took advantage of the rare opportunity to investigate the total weight and cubic volume of seeds recovered from the corpse. The seeds contained in the corpse weighed 258.8 g (dry weight) and measured 489.4 cm3. The volume of seeds was 14.7 % of the previously reported capacity of the digestive tract of a chimpanzee in captivity. We also indirectly estimated the volume of seeds from the values of observed seed volume in feces, the reported number of defecations per day, and the seed passage time. The estimated volume was significantly lower than the observed seed volume, suggesting that the number of defecations per day is underestimated because it may not include nighttime defecation.

What makes wild chimpanzees wake up at night?

I examined the possible cause of night awakening among wild chimpanzees (Pan troglodytes) in Mahale Mountains National Park, Tanzania. Chimpanzee vocalizations and activity-related sounds (CVSs) were used to indicate awakening because I was unable to visually observe them. Over a 5-night observation period, CVSs (n = 128) were heard every night, and most (n = 91) were observed within 5 min of previous CVSs. Chimpanzees use CVSs as social communication to maintain spatial contact with other chimpanzees who occasionally travel at night. The first sound in a sequence of CVSs (CVS bout) was heard immediately following the vocalization or sound of another animal (n = 11), defecation or urination by a chimpanzee (n = 7), or unknown (n = 19). CVS bouts were longer when preceded by defecation or urination than when preceded by the vocalization or sound of other animals or an unknown factor. This suggests that the degree of wakefulness varies according to the possible cause of the disturbance. CVSs at night may be provoked by various factors, and awakening during the night is probably common among diurnal primates.

Brief communication: Orphaned Male Chimpanzees die young even after weaning.

If a social-living animal has a long life span, permitting different generations to co-exist within a social group, as is the case in many primate species, it can be beneficial for a parent to continue to support its weaned offspring to increase the latter's survival and/or reproductive success. Chimpanzees have an even longer period of dependence on their mothers' milk than do humans, and consequently, offspring younger than 4.5-5 years old cannot survive if the mother dies. Most direct maternal investments, such as maternal transportation of infants and sharing of night shelters (beds or nests), end with nutritional weaning. Thus, it had been assumed that a mother's death was no longer critical to the survival of weaned offspring, in contrast to human children, who continue to depend on parental care long after weaning. However, in theory at least, maternal investment in a chimpanzee son after weaning could be beneficial because in chimpanzees' male-philopatric society, mother and son co-exist for a long time after the offspring's weaning. Using long-term demographic data for a wild chimpanzee population in the Mahale Mountains, Tanzania, we show the first empirical evidence that orphaned chimpanzee sons die younger than expected even if they lose their mothers after weaning. This suggests that long-lasting, but indirect, maternal investment in sons continues several years after weaning and is vital to the survival of the sons. The maternal influence on males in the male-philopatric societies of hominids may be greater than previously believed.

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.

Frequency of removal movements during social versus self-grooming among wild chimpanzees.

Grooming was observed in 11 wild chimpanzees (Pan troglodytes schweinfurthii) in Mahale, Tanzania, and the number of removal and stroke movements and grooming duration were recorded. Removal movements were more frequent during social grooming than during self-grooming. Chimpanzees used one or both hands for grooming, and grooming using both hands was more efficient for removing small objects. Due to physical constraints, self-grooming of the arms was almost always done using only one hand. The removal movement frequency during arm grooming was lower when self-grooming than when grooming another. They were more likely to use both hands during grooming another than during self-grooming, and fewer physical constraints during social grooming enabled a higher level of hygienic grooming.

Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae).

In order to obtain basic data on parasitic infections of Bornean orangutans, Pongo pygmaeus morio (Owen, 1837), in Danum Valley, Sabah, Malaysia, fecal examinations were conducted. Based on a total of 73 fecal samples from 25 individuals, cysts of Entamoeba coli, Entamoeba spp., and Chilomastix mesnili, cysts and trophozoites of Balantidium coli, and eggs of Trichuris sp. or spp., unknown strongylid(s), Strongyloides fuelleborni, and an unknown oxyurid, plus a rhabditoid larva of Strongyloides sp., were found. Mature and immature worms of Pongobius hugoti Barus et al., 2007 and Pongobius foitovae n. sp. (Oxyuridae: Enterobiinae) were recovered from fecal debris and described. Pongobius foitovae is readily distinguished from P. hugoti by having a much longer esophageal corpus, a longer and distally hooked spicule in males, and a more posteriorly positioned vulva in female. Presence of plural species of non- Enterobius pinworms is a remarkable feature of the orangutan-pinworm relationship, which may reflect speciation process of the orangutans, host switching, and coevolution by pinworms.

Prevalence of muzzle-rubbing and hand-rubbing behavior in wild chimpanzees in Mahale Mountains National Park, Tanzania.

In 1998, four chimpanzees in the Mahale Mountains National Park, Tanzania, were observed wiping their mouths with non-detached leaves or stalks of grass, or rubbing their mouths with a tree trunk or branch, especially while eating lemons. The number of mouth-wiping/rubbing individuals increased to 18 in 1999. By 2005, 29 chimpanzees were documented wiping/rubbing their muzzles in this way. Although it is difficult to determine whether the chimpanzees acquired this behavior as a result of trial and error or social learning, the fact that chimpanzees at other sites perform this behavior with detached leaves or leafy twigs much more often than with intact items suggests the possibility that cleaning with intact plant parts at Mahale spread via social learning.

Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees.

Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.

Food conditions, competitive regime, and female social relationships in Japanese macaques: within-population variation on Yakushima.

Feeding conditions, competitive regime, and female social relationships of Japanese macaques (Macaca fuscata) on Yakushima were compared between the two habitats at two different altitudes (coniferous forest, 1,000-1,200 m and coastal forest, 0-200 m). Fruit availability was higher in the coastal forest. There was no consistent difference in the frequency of agonistic interactions within a group during feeding between the two habitats. The coastal forest evoked stronger inter-group contest competition compared to the coniferous forest as evidenced by a higher inter-group encounter rate and a higher proportion of aggressive encounters to non-aggressive ones. Birth rate was higher in larger groups compared to smaller ones in the coastal forest, but did not differ in the coniferous forest. In spite of these differences in competitive regime, no variation in female social relationships was observed, such as direction and concentration on particular individuals in grooming, linearity in dominance rank, counter-attack, and support of juvenile kin during agonistic interactions. The present results indicate that the female social relationships of Japanese macaques are robust and do not change according to changes in the current environment.

Tool-use for drinking water by immature chimpanzees of Mahale: prevalence of an unessential behavior.

Use of leaves or sticks for drinking water has only rarely been observed during long-term study of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Recently, however, we observed 42 episodes of tool-use for drinking water (73 tools and two cases of using "tool-sets") between 1999 and 2004. Interestingly, all of the performers were immature chimpanzees aged from 2 to 10 years. Immature chimpanzees sometimes observed the tool-using performance of others and subsequently reproduced the behavior, while adults usually paid no attention to the performance. This tool-use did not seem to occur out of necessity: (1) chimpanzees often used tools along streams where they could drink water without tools, (2) they used tools for drinking water from tree holes during the wet season when they could easily obtain water from many streams, and (3) the tool-using performance sometimes contained playful aspects. Between-site comparisons revealed that chimpanzees at drier habitats used tools for drinking water more frequently and in a more "conventional" manner. However, some variations could not be explained by ecological conditions. Such variations and the increase in this tool-use in recent years at Mahale strongly suggest that social learning plays an important role in the process of acquiring the behavior. We should note here that such behaviors that lack obvious benefits or necessity can be prevalent in a group.

Comparisons of food availability and group density of Japanese macaques in primary, naturally regenerated, and plantation forests.

We compared food availability and group density of Japanese macaques in Yakushima, southern Japan, among primary forest and two habitats that had been disturbed by logging and had different regeneration histories. The study was conducted in an undisturbed national park, forest that was logged 7-18 years ago and later naturally regenerated, and forest that was logged 19-27 years ago and later planted with Japanese cedar (Cryptomeria japonica) trees. The plantation forest was primarily composed of large Cryptomeria japonica trees at low stand density, while the naturally regenerated forest was composed of many small trees. The total basal area and number of trees in the primary forest were comparable to those in the plantation forest. Annual fruit production was greatest in the naturally regenerated forest, intermediate in the primary forest, and negligible in the plantation forest. Herb availability was high in the naturally regenerated forest, but low in the primary and plantation forests. The group density of Japanese macaques was high in the naturally regenerated forest, intermediate in the primary forest, and low in the plantation forest. Since group size in the naturally regenerated forest was small, individual density was almost the same as in the primary forest. These results suggest that the effects of regeneration on macaques vary between the two habitats. The plantation forest consisted mostly of Cryptomeria japonica, which supplies only flowers as food in a limited season, and had a lower density of macaques. On the other hand, in the naturally regenerated forest, fruit production and herb availability were high (probably because of the enhanced light conditions after logging), and the density of macaques was as high as in the primary forest.

New method to census primate groups: estimating group density of Japanese macaques by point census.

We devised a new method to estimate the density of primate groups in habitats that preclude the use of a line-transect census because the ground is too steep. We combined point census and group follows. From the number of groups counted at a fixed point for an hour, n, group density D was calculated: D = lambda n / pi. Lambda, the detectability constant, was a constant when distance-dependent detectability g(y) was regressed on a half-normal model: g(y) = e (-lambda y(2)) and can be estimated by combining the information of group follow and point census. Using this method, we estimated the group density of Japanese macaques in Yakushima. A census area of 7 km(2) was divided into 28 grid squares (500 m x 500 m). One observer was positioned at a point in each grid square, and those points were censused simultaneously for 4-6 days from 0600-0700 to 1500-1600 hr. Four troops were followed for 144 hr during the point census. Distance-dependent detectability closely correlated with the half-normal model. The detectability constant varied with the time of day, but it was not influenced by troop identity or topography. Group density was calculated to be 1.48 +/- 0.61 and 0.701 +/- 0.432 groups/km(2) in the disturbed and undisturbed areas, respectively (95% confidence limit). "True" group density estimated by home range data was within the confidence limit calculated by a point census in the home range of the troops for two troops, suggesting that this method was valid. This method is applicable to other species as long as at least one group can be followed, because it satisfies the fundamental assumptions of point census, and the detectability does not seem to be biased by troop or topography.

Demography, female life history, and reproductive profiles among the chimpanzees of Mahale.

Demography provides critical data to increase our understanding of the evolution, ecology, and conservation of primate populations. The chimpanzees of the Mahale Mountains National Park, Tanzania, have been studied for more than 34 yr on the basis of individual identification and standardized attendance records. From this long-term study, we derived the following demographic data: The major cause of death was disease (48%), followed by senescence (24%) and within-species aggression (16%). Fifty percent of Mahale chimpanzees died before weaning. The median ages of female life history variables were: first maximal swelling, 10.0 yr (n = 5); emigration, 11.0 yr (n = 11); and first birth, 13.1 yr (n = 5). The median period of adolescent infertility was 2.8 yr (n = 4) when calculated from the age at immigration to that at first birth. Female fecundity was highest between 20 and 35 yr of age, with an annual birth rate of 0.2. Twenty-six females that were observed from a young age (10-13 yr) to death at various ages (15-40 yr) gave birth to an average of 3.9 and weaned an average of 1.4 offspring. Twenty-five females that were observed from middle age (18-33 yr) to death in older age (31-48) gave birth to an average of 2.7 and weaned an average of 2.0 offspring. The post-reproductive lifespan for female chimpanzees was defined as the number of years that passed from the year when the last offspring was born to the year when the female died, minus 5. Twenty-five percent of old females had a post-reproductive lifespan. The interbirth interval after the birth of a son (x = 72 mo) tended to be longer than that after the birth of a daughter (x = 66 mo). The extent of female transfer, which is a rule in chimpanzees, is influenced by the size and composition of the unit group and size of the overall local community.

Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama.

I investigated the effect of the density of louse eggs (Pedicinus obtusus and P. eurygaster) on grooming site preferences in Japanese macaques (Macaca fuscata). Louse eggs were more often found on the outer side of the body (upper back, lower back, outer arms, and outer legs) than on the inner side of the body (chest, belly, inner arms, and inner legs). Japanese macaques were more likely to be groomed on the outer side than the inner side of the body by allogrooming and autogrooming. Such grooming site preferences correlated with the distribution of louse eggs but not with the areas of body parts. Thus, the ecology of lice might affect grooming behavior of Japanese macaques. Five hundred and fifty louse eggs were estimated to parasitize an adult female Japanese macaque. Considering the intrinsic rate of natural increase of lice, monkeys need to be groomed almost every day. This suggests that Japanese macaques need grooming partners and form social bonds with others for everyday grooming.

Leaf-grooming by a wild chimpanzee in Mahale.

During the course of systematic observations of the leaf-grooming behavior by the chimpanzees (Pan troglodytes) of the Mahale Mountains National Park, Tanzania, I recovered a louse from a leaf "groomed" by an adult male chimpanzee after a typical leaf-grooming session. During the leaf-grooming session I observed a small object on his lower lip. He picked up a leaf, transferred the small object from his lip to the leaf, folded the leaf and crushed the folded side of the leaf with his thumb. I present this observation as further evidence of the "squashing ectoparasites" hypothesis for leaf-grooming.