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The ability to determine hormonal profiles of primate populations using non-invasive techniques can help to monitor physical fitness, stress, and physiological responses to environmental changes. We investigated fecal glucocorticoids (fGC) and DHEAS concentrations in captive Japanese macaques (Macaca fuscata) in relation to environmental, biological, and social factors. The subjects were female Japanese monkeys from 4 months to 31 years old housed in captivity (27 in social groups and 12 in single cages). Fecal samples were collected from all females, and behavioral data from the social groups during the mating season and the following birth season. Hormonal concentrations were analyzed by enzyme immunoassay. Our results revealed that both fGC and fecal DHEAS concentrations are higher in females housed indoors in single cages than in those living outdoors in social groups. We also found that fGC concentrations were higher in the cycling females during the mating (winter) season than the lactating females in the birth (spring) season. Age was negatively associated to both fGC and fecal DHEAS levels, but the relationship between age and fecal DHEAS was more evident in females housed indoors in single cages than in females housed in outdoor social groups. We did not observe any association of dominance rank with either fecal DHEAS or fGC. This study showed that measurement of fecal DHEAS and fGC can be a good method to assess stress in Japanese macaques. These findings provide insights about the physiology of these two adrenal hormones in female Japanese macaques, which can be applied to wild populations and is fundamental for captive management and conservation biology. Am. J. Primatol. 76:1084–1093, 2014. © 2014 Wiley Periodicals, Inc.

Leaf swallowing behavior, known as a form of self-medication for the control of nematode and tapeworm infection, occurs widely in all the African great apes (Pan troglodytes schweinfurthii, P. t. troglodytes, P. t. verus, P. t. vellerosus, Pan paniscus, Gorilla gorilla graueri), except mountain gorillas. It is also reported to occur in a similar context across a wide array of other animal taxa including, domestic dogs, wolves, brown bears, and civets. Despite long-term research on Asian great and small apes, this is the first report of leaf swallowing in an Asian species, the white-handed gibbon (Hylobates lar) in Khao Yai National Park, central Thailand. We present the first evidence of leaf swallowing (Gironniera nervosa Planch CANNABACEA) behavior (N = 5 cases) and parasite (Streptopharagus pigmentatus) expulsion (N = 4 cases), recorded during 4,300 hr of direct animal observations during two distinct research projects. We recovered 4-18 rough, hairy, and hispid surfaced leaves from each sample, undigested and folded, from the freshly evacuated feces of five different individuals (2 males, 3 females, 5 to 34+ years old) living in three different social groups, between the hours of 06:00 to 10:30. Based on close inspection of the leaves, as observed in chimpanzees, it was clear that they were taken into the mouth, one at a time, folded and detached from the stem with the teeth before swallowing them whole. All instances occurred during the rainy season, the time when nematode worms were also found in the feces, although they were not found together with leaves in the same feces. These striking similarities in the details of leaf swallowing between white-handed gibbons and African great apes, and other animal species, suggest a similar self-medicative function.

Numerous behavioral and ecological factors are associated with parasite transmission. One factor explored in human research, but absent from nonhuman primate research, is parasite transmission from soil ingestion. Human studies suggest geophagy, the regular and deliberate consumption of soil, increases risk of soil-transmitted helminth (STH) infection. Geophagy, which is prevalent in nonhuman primates, has several positive associations: gastrointestinal distress alleviation, possible mineral supplementation, and bacterial infection prevention. Our objective was to determine whether STH transmission was possible from deliberate or accidental soil ingestion, in a troop of chacma baboons (Papio hamadryas ursinus) that engaged in geophagy, foraged on the terrestrial substrata, and had a Trichuris sp. sample prevalence of 100%. We collected and analyzed 80 soil samples from geophagy and ground foraging sites on and around Wildcliff Nature Reserve, South Africa. Forty soil samples were collected from sites where soil was consumed, and 40 were collected from sites where soil was not consumed. At geophagy sites, the number of Trichuris sp. eggs recovered varied significantly between areas used and unused by the baboons, suggesting behavior is an important factor. In contrast, at foraging sites, there was only a tendency to recover more eggs at used than unused areas, and we propose egg recovery was influenced by fecal contamination that occurred throughout foraging stands. The difference in egg recovery between used areas at geophagy sites and used areas at foraging sites was not significant. These preliminary findings suggest both geophagy and foraging sites are a potential source of STH infection for this troop. Whether geophagy benefits outweigh the potential cost of parasite reinfection for this baboon troop is unknown, so we encourage future research on the influence that host foraging behavior may have on parasite reinfection. Am. J. Primatol. 74:940-947, 2012. © 2012 Wiley Periodicals, Inc.

Self-medication by great apes to control intestinal parasite infections has been documented at sites across Africa. Chimpanzees (Pan troglodytes) swallow the leaves of certain plant species whole, without chewing. Previous studies demonstrated a relationship between chimpanzee leaf swallowing and expulsion of nematode worms (Oesophagostomum sp.) and tapeworms (Bertiella sp.) in dung. We investigated the relationship between leaf swallowing and parasite expulsion in chimpanzees inhabiting a fragmented forest-farm mosaic at Bulindi, Uganda. During 13 months whole undigested leaves occurred in chimpanzee dung at a considerably higher frequency (10.4% of dungs) than at other sites (0.4-4.0%). Leaf swallowing occurred year-round and showed no pronounced seasonality. Chimpanzees egested adults of multiple species of Oesophagostomum (including O. stephanostomum) and proglottids of two tapeworms-Bertiella sp. and probably Raillietina sp. The latter may not be a true infection, but the byproduct of predation on domestic fowl. Compared to previous studies, the co-occurrence of whole leaves and parasites in chimpanzee dung was low. Whereas the presence of leaves in dung increased the probability of adult nematode expulsion, no association between leaf swallowing and the shedding of tapeworm proglottids was apparent. Anthropogenic habitat changes have been linked to alterations in host-parasite interactions. At Bulindi, deforestation for agriculture has increased contact between apes and people. Elevated levels of leaf swallowing could indicate these chimpanzees are especially vulnerable to parasite infections, possibly due to environmental changes and/or increased stress levels arising from a high frequency of contact with humans. Frequent self-medication by chimpanzees in a high-risk environment could be a generalized adaptation to multiple parasite infections that respond differently to the behavior. Future parasitological surveys of apes and humans at Bulindi are needed for chimpanzee health monitoring and management, and to investigate the potential for disease transmission among apes, people, and domestic animals.

Despite baboons' widespread distribution across Africa, geophagy among all subspecies has been poorly documented. We used video camera traps and soil analyses to investigate geophagy in chacma baboons (Papio cynocephalus ursinus) inhabiting the Western Cape of South Africa. During an 18-month study, from August 2009 to January 2011, we continually monitored the largest and most frequently visited geophagy sites with camera traps for 545 days and captured soil consumption at one or more sites on 266 of those days (49%). In 3,500 baboon visits to geophagy sites, video camera traps captured 58.6 hr of geophagy. From these data, we evaluated site preference based on time spent consuming soil among these four geophagy sites. One hundred and seventy days of soil consumption data from the most frequently visited geophagy site allowed us to look for demographic trends in geophagy. Selected consumed soils from geophagy sites were analyzed for mineral, physical, and chemical properties. The baboons spent more time consuming white alkaline soils with high percentages of clay and fine silt, which contained higher concentrations of sodium than non-white acidic soils that contained higher concentrations of iron. Our data indicate that pregnant chacma baboons spent more time consuming soil at monitored geophagy sites than baboons of any other age class, sex, or reproductive state. Based on analytical results, the soils consumed would be effective at alleviating gastrointestinal distress and possibly supplementing minerals for all age/sex classes, but potentially for different age/sex requirements. Am. J. Primatol. 74:48–57, 2012. © 2011 Wiley-Liss, Inc.

Individuals adapt to changes in their environment, such as food availability and temperature, by adjusting the amount of time spent in different behavioral activities. These adjustments in behavior should vary across age-sex class according to specific physiological and social needs. We studied the activity budgets of three social Japanese macaque groups inhabiting either vegetated or nonvegetated enclosures in order to compare the effects of access with vegetation, as both food and substrate on resting, feeding, grooming and moving activities over a 12-month period. Daily access to natural foods for monkeys in the vegetated enclosure seems to be largely responsible for the differences in daily time budgets of these three groups. Resting time in all three groups was longer than the time devoted to other activities. Resting and moving time in the two nonvegetated enclosures was significantly longer than in the vegetated enclosure. In contrast, feeding and grooming time was significantly longer in the vegetated enclosure. Seasonal variation in time spent feeding, resting and grooming was significantly effected by enclosure type. In all three enclosures, immatures, particularly females, spent more time feeding and moving, whereas adults spent more time resting. Significant monthly variation in time spent by age-sex class was noted only for feeding and resting. Interestingly, in the vegetated enclosure, time spent feeding on natural vegetation was equal to the amount of time spent feeding on provisioned food. This suggests that factors other than energetic and nutritional needs may be important determinants of the activity budget of the species. These results have important implications for the enrichment of captive primates and our understanding of the maintenance of activity patterns by primates in the wild.

This study describes the stone handling (SH) behavior of captive rhesus macaques and compares it with that of a captive troop of Japanese macaques with reference to the relative contributions of phylogeny-driven behavioral propensities, environmental differences and socially facilitated learning to the formation of culture. These systematically collected data demonstrate for the first time that two closely related macaque species might share a common cultural behavior, SH. The rhesus troop displayed SH behavioral patterns that was already described in Japanese macaque troops. The one exception was a new pattern not yet seen in any Japanese macaque troop. Differences in the physical environment of the two study enclosures may be responsible for some of the variation in observed SH behavioral patterns in these two troops. These data support the idea that environmental factors can be important for the formation of cultural variation, when the key materials needed to perform the behavior are present in both habitats (stones). Our results are consistent with the prediction made by Huffman and Hirata [The biology of tradition: Models and evidence. Cambridge: Cambridge University Press. p 267–296] that an interactive triad of phylogenetic, environmental and social factors can be responsible for the formation of cultural variation in primates. Am. J. Primatol. 70:1124–1132, 2008. © 2008 Wiley-Liss, Inc.

By addressing the influence of food provisioning on stone handling (SH), a behavioral tradition in Japanese macaques, this study contributes to the ongoing debate in cultural primatology by asking whether human intervention influences the emergence or propagation of behavioral traditions. SH is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. We tested the hypothesis that the frequency of food provisioning affects the daily performance, form, and context of occurrence of SH by influencing a troop's feeding-related activity budget. We used a standardized observation procedure to investigate SH in ten troops of Japanese macaques. In troops provisioned several times a day, SH was more frequent, longer, and more prevalent during provisioning than nonprovisioning periods. These effects of provisioning were not significant in troops provisioned less frequently. SH was more frequently integrated with food-related activities in troops supplied with food several times a day than in the other troops. Food provisioning may be a key factor in the innovation and transformation phases of the SH tradition in Japanese macaques. Am. J. Primatol. 70:803–813, 2008. © 2008 Wiley-Liss, Inc.

We examined seasonal patterns of fruit availability, dietary quality, and group size in the descendants of an introduced chimpanzee population on Rubondo Island, Tanzania. The site has supported a free-ranging population without provisioning for 40 years. Our goals were to determine whether Rubondo chimpanzees experience periods of fruit shortage, and whether they respond to changes in fruit availability similarly to chimpanzees at endemic sites. We indexed the fruit availability of tree and liana species on transects stratified across three chimpanzee ranging areas. We used fecal analyses to evaluate seasonal changes in diet, and used data on party size and nesting group size to examine seasonal patterns of grouping. Tree fruit availability was positively correlated with rainfall, with a period of relative tree fruit scarcity corresponding with the long dry season. Liana fruit availability was not related to rainfall, and lianas exhibited less variable fruiting patterns across seasons. Fruits made up the majority of the chimpanzee diet, with lianas accounting for 35% of dietary fruit species. Fruits of the liana Saba comorensis were available during all months of phenological monitoring, but they were consumed more when tree fruit was scarce, suggesting that Saba comorensis fruits may be a fallback food for Rubondo chimpanzees. There were no increases in consumption of lower-quality plant parts between seasons, and there were no changes in group size between seasons. These results contrast with evidence from several endemic chimpanzee study sites, and indicate that Rubondo chimpanzees may have access to abundant and high-quality foods year round. Am. J. Primatol. 69:487–502, 2007. © 2007 Wiley-Liss, Inc.

The ability to determine hormonal profiles of primate populations using non-invasive techniques can help to monitor physical fitness, stress, and physiological responses to environmental changes. We investigated fecal glucocorticoids (fGC) and DHEAS concentrations in captive Japanese macaques (Macaca fuscata) in relation to environmental, biological, and social factors. The subjects were female Japanese monkeys from 4 months to 31 years old housed in captivity (27 in social groups and 12 in single cages). Fecal samples were collected from all females, and behavioral data from the social groups during the mating season and the following birth season. Hormonal concentrations were analyzed by enzyme immunoassay. Our results revealed that both fGC and fecal DHEAS concentrations are higher in females housed indoors in single cages than in those living outdoors in social groups. We also found that fGC concentrations were higher in the cycling females during the mating (winter) season than the lactating females in the birth (spring) season. Age was negatively associated to both fGC and fecal DHEAS levels, but the relationship between age and fecal DHEAS was more evident in females housed indoors in single cages than in females housed in outdoor social groups. We did not observe any association of dominance rank with either fecal DHEAS or fGC. This study showed that measurement of fecal DHEAS and fGC can be a good method to assess stress in Japanese macaques. These findings provide insights about the physiology of these two adrenal hormones in female Japanese macaques, which can be applied to wild populations and is fundamental for captive management and conservation biology.

Self-medication by great apes to control intestinal parasite infections has been documented at sites across Africa. Chimpanzees (Pan troglodytes) swallow the leaves of certain plant species whole, without chewing. Previous studies demonstrated a relationship between chimpanzee leaf swallowing and expulsion of nematode worms (Oesophagostomum sp.) and tapeworms (Bertiella sp.) in dung. We investigated the relationship between leaf swallowing and parasite expulsion in chimpanzees inhabiting a fragmented forest-farm mosaic at Bulindi, Uganda. During 13 months whole undigested leaves occurred in chimpanzee dung at a considerably higher frequency (10.4% of dungs) than at other sites (0.4-4.0%). Leaf swallowing occurred year-round and showed no pronounced seasonality. Chimpanzees egested adults of multiple species of Oesophagostomum (including O. stephanostomum) and proglottids of two tapeworms-Bertiella sp. and probably Raillietina sp. The latter may not be a true infection, but the byproduct of predation on domestic fowl. Compared to previous studies, the co-occurrence of whole leaves and parasites in chimpanzee dung was low. Whereas the presence of leaves in dung increased the probability of adult nematode expulsion, no association between leaf swallowing and the shedding of tapeworm proglottids was apparent. Anthropogenic habitat changes have been linked to alterations in host-parasite interactions. At Bulindi, deforestation for agriculture has increased contact between apes and people. Elevated levels of leaf swallowing could indicate these chimpanzees are especially vulnerable to parasite infections, possibly due to environmental changes and/or increased stress levels arising from a high frequency of contact with humans. Frequent self-medication by chimpanzees in a high-risk environment could be a generalized adaptation to multiple parasite infections that respond differently to the behavior. Future parasitological surveys of apes and humans at Bulindi are needed for chimpanzee health monitoring and management, and to investigate the potential for disease transmission among apes, people, and domestic animals.

Numerous behavioral and ecological factors are associated with parasite transmission. One factor explored in human research, but absent from nonhuman primate research, is parasite transmission from soil ingestion. Human studies suggest geophagy, the regular and deliberate consumption of soil, increases risk of soil-transmitted helminth (STH) infection. Geophagy, which is prevalent in nonhuman primates, has several positive associations: gastrointestinal distress alleviation, possible mineral supplementation, and bacterial infection prevention. Our objective was to determine whether STH transmission was possible from deliberate or accidental soil ingestion, in a troop of chacma baboons (Papio hamadryas ursinus) that engaged in geophagy, foraged on the terrestrial substrata, and had a Trichuris sp. sample prevalence of 100%. We collected and analyzed 80 soil samples from geophagy and ground foraging sites on and around Wildcliff Nature Reserve, South Africa. Forty soil samples were collected from sites where soil was consumed, and 40 were collected from sites where soil was not consumed. At geophagy sites, the number of Trichuris sp. eggs recovered varied significantly between areas used and unused by the baboons, suggesting behavior is an important factor. In contrast, at foraging sites, there was only a tendency to recover more eggs at used than unused areas, and we propose egg recovery was influenced by fecal contamination that occurred throughout foraging stands. The difference in egg recovery between used areas at geophagy sites and used areas at foraging sites was not significant. These preliminary findings suggest both geophagy and foraging sites are a potential source of STH infection for this troop. Whether geophagy benefits outweigh the potential cost of parasite reinfection for this baboon troop is unknown, so we encourage future research on the influence that host foraging behavior may have on parasite reinfection.

The geographic distribution of Japanese macaques includes populations with the most northern range of any primate species. Not surprisingly, females of this species are characterized by physiological adaptations and unique fat deposition mechanisms that facilitate their survival through the sometimes-harsh seasonal conditions of temperate climates, as well as sustaining the metabolic costs of mating, pregnancy, and lactation. Here, we explore the relationship between nutritional status, seasonality, and reproductive status using anthropometric and leptin measures from 14 captive female Japanese macaques. No seasonal patterns were found in the levels of leptin, but there were differences between seasons in anthropometric measures, specifically between the beginning and the end of the mating season. Females gained weight and accumulated energy reserves in fall to prepare for mating activity, and to survive the severe conditions of winter, which is also the period of gestation if pregnancy occurs. Lactating females had larger total skinfolds relative to nonlactating individuals, and females with older babies at the beginning of the mating season had larger abdominal skinfolds than did those with younger babies. There was a relationship between the likelihood of conception and nutritional status, with females that conceived during one mating season being in better condition at the end of their previous mating season. Together, these results suggest that, even in captive settings, seasonal breeding has a cost on the energetic demands of mating, and that higher condition (i.e. fatter) females could afford the demands of lactation and reproduced more rapidly.

The release of any species into a novel environment can evoke transmission of parasites that do not normally parasitize the host as well as potentially introducing new parasites into the environment. Species introductions potentially incur such risks, yet little is currently known about the parasite fauna of introduced primate species over the long term. We describe the results of long-term monitoring of the intestinal parasite fauna of an unprovisioned, reproducing population of chimpanzees introduced 40 years earlier (1966–1969) onto Rubondo Island in Lake Victoria, Tanzania, a non-native habitat for chimpanzees. Two parasitological surveys (March 1997–October 1998 and October 2002–December 2005) identified Entamoeba spp. including E. coli, Iodamoeba buetschlii, Troglodytella abrassarti, Chilomastix mesnili, Trichuris sp., Anatrichosoma sp., Strongyloides spp., Strongylida fam. gen. sp., Enterobius anthropopitheci, Subulura sp., Ascarididae gen. sp., and Protospirura muricola. The parasite fauna of the Rubondo chimpanzees is similar to wild chimpanzees living in their natural habitats, but Rubondo chimpanzees have a lower prevalence of strongylids (9%, 3.8%) and a higher prevalence of E. anthropopitheci (8.6%, 17.9%) than reported elsewhere. Species prevalence was similar between our two surveys, with the exception of Strongyloides spp. being higher in the first survey. None of these species are considered to pose a serious health risk to chimpanzees, but continued monitoring of the population and surveys of the parasitic fauna of the two coinhabitant primate species and other animals, natural reservoir hosts of some of the same parasites, is important to better understand the dynamics of host–parasite ecology and potential long-term implications for chimpanzees introduced into a new habitat. Am. J. Primatol. 72:307–316, 2010. © 2009 Wiley-Liss, Inc.

Japanese macaques live in multi-male/multi-female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The alpha male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid alpha male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen-related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation.

This is the first detailed report of social factors affecting fish-eating in Japanese macaques under natural circumstances. We video-recorded a complete event of fish eating, involving a new fish food species for the monkeys on Koshima island. Following the discovery of a large beached sea bass by a peripheral male, we observed a total of 16 individuals feeding on the fish in turns, and interacting around it. The rank order of access to the fish was mainly explained by the spatial position of group members, whereas dominance determined how long the fish was monopolized. Although limited, the tolerated presence of close-bystanders while feeding was affected by kinship and affiliation. Genealogic data suggested that fish-eating behavior was well maintained in terms of maternal lineages. This report should contribute to a better understanding of how social features may constrain the long-term diffusion of feeding innovations in free-ranging primate groups.

Stone handling (SH) in Japanese macaques, a form of solitary-object play, is newly acquired only by young individuals, and is the first example of a directly nonadaptive behavior that is maintained as a behavioral tradition within free-ranging provisioned social troops. We report here the first systematic investigation of this behavior in a stable captive social troop, the Takahama troop, which is housed in an outdoor enclosure of the Primate Research Institute (PRI), Kyoto University, Japan. This study was conducted to evaluate relevant competing hypotheses regarding the function of object play (e.g., misdirected foraging behavior and motor training) to explain the proximal causes and ultimate function(s) of SH. The "misdirected foraging behavior" hypothesis can be ruled out because of the lack of a clear temporal relationship between feeding and the occurrence of SH in any age class. Age-related differences in SH performance and behavioral patterns were observed, suggesting possible differences in the immediate cause and ultimate function between young and adults. Young individuals engaged in frequent bouts of short duration, involving locomotion and vigorous body actions throughout the day, which is typical for play by young in general. This pattern of behavior is consistent with the motor training hypothesis, which states that play occurs during the development of motor and perceptual skills and is thus potentially critical for neural and cognitive development. This practice is continued by those who acquire it at an early age, with adults engaging in significantly fewer but longer bouts that involve more stationary, complex manipulative patterns, almost exclusively in the late afternoon. We propose that for adults, at the proximate level SH is psychologically relaxing, but ultimately functions to maintain and regenerate neural pathways, and potentially helps to slow down the deterioration of cognitive function associated with advanced age in long-lived provisioned and captive macaques.