Search

Stone handling (SH) is a form of solitary object play widely documented in four species of macaques and most recently also in geladas (Theropithecus gelada). Here, we describe the SH activity of two mother-reared captive gelada males, who combined different behavioral patterns in a sequence that occasionally led to the production of colored marks on a hard surface. Two playful techniques of different complexity emerged spontaneously in the two subjects. In the etching and releasing technique, the stone or pieces of it were repeatedly scraped across either a vertical or horizontal hard surface. In the grindandfinger technique, additional patterns were recruited such as scratching the stone to produce small debris that the subjects manipulated through a thumb–index finger precision grip. Animals selected preferentially hard surfaces when their SH sessions involved patterns that potentially released color and engaged in such patterns for longer and in a repeated way. This evidence suggests the high motivation of the two males to engage in drawing-like behavior that, as it occurs for other forms of play, can be characterized by its autotelic self-rewarding nature. Digital video images related to the article are available at http://www.momo-p.com/showdetail-e.php?movieid=momo220922tg01a and http://www.momo-p.com/showdetail-e.php?movieid=momo220923tg01a

Non-invasive measures of stress are crucial for captive and conservation management programs. The adrenal hormone dehydroepiandrosterone-sulfate (DHEAS) has recently been adopted as a stress marker, but there is little investigation of its relationship to glucocorticoids (GC), well-known indicators of stress. This study examined the influence of age, reproductive state and environment on GC and DHEAS levels in orangutans, to test whether the GC/DHEAS ratio can provide an index of stress response in primates. We measured fecal GC (fGC) and fecal DHEAS (fDHEAS) concentrations in 7 captive orangutans from zoological parks in Japan and 22 wild orangutans from Danum Valley Conservation Area, Malaysia. We found that in a stressful condition (transportation), fDHEAS levels increased 2 days after the fGC response, which occurred 1 day after the stressor. One pregnant female had elevated levels of both hormones, and a higher fGC/fDHEAS ratio than baseline. Females in the first year of lactation had fGC levels and the fGC/fDHEAS ratio significantly higher than both baseline and females in the second and subsequent years of lactation. There was no effect of age on fGC levels, but the fGC/fDHEAS ratio was higher in infants than adults and adolescents. fDHEAS concentrations were lower in infants than juveniles, adolescents and adults, a phenomenon known as adrenarche, shared with humans and other great apes. We suggest that changes in DHEAS during orangutan life history are associated with changes in the dynamics of maintaining homeostasis that vary with age and reproductive state. The GC/DHEAS ratio index is useful to evaluate age-related abilities of responding to stressful challenges.

Salivary alpha-amylase (sAA) enzyme functions as a digestive enzyme in many species that consume starch in their diet. Human studies have also revealed that sAA enzyme activity levels are positively correlated with the release of the stress hormone norepinephrine, allowing sAA to act as a biomarker for sympathetic nervous system activity. Recent non-human primate studies have incorporated sAA as a physiological stress marker. However, no published reports have investigated the time course of sAA from a stressful event to return to baseline levels in non-human primates. Furthermore, no validation of sAA as a stress biomarker has been reported for Japanese macaques (Macaca fuscata). This study had two primary aims: (1) to develop a systematic method for non-invasive saliva collection and, (2) to investigate sAA as a biomarker of acute stress in M. fuscata in order to better understand its acute stress-related characteristics. We developed a non-invasive method for cooperative saliva collection using positive reinforcement training (PRT) and tracked individual progress over 595 trials in ten individually housed Japanese macaques. We detected sAA enzyme in M. fuscata via kinetic reaction assay, then performed 22 acute stress tests. Four tests met conditions for interpreting sAA in response to an acute stressor and these results show that on average sAA activity rapidly increased post-stressor (mean ± SD = 4.2 ± 0.9 min) and returned to baseline shortly thereafter (10.4 ± 0.6 min). Our report reveals for the first time the temporal dynamics of sAA when applying acute stress to Japanese macaques and could be a useful tool for assessing animal welfare.

Maternal care towards dead infants has been observed in many wild and captive mammals, but the consequences of this behavior for social interactions and the physiological status of the mother remain elusive. Here, we report changes in rates of aggression and grooming time, and fecal glucocorticoid (fGC) levels in a free-ranging female Japanese macaque (Macaca fuscata) that carried her dead infant for 20 days. Our observations revealed that when carrying the dead infant, the mother showed increased rates of grimace, avoidance, and human-directed behaviors, along with reduced allogrooming time and fleeing from other individuals. Postpartum fGC levels were comparable to those of non-pregnant and non-lactating females, suggesting that the energetic costs and stress of carrying a dead infant are low. Our findings indicate that carrying a dead neonate can have three profound consequences on the mother: increased fearful behavior, decreased allogrooming, and a rapid return to baseline fGC levels. We hypothesize that dead infant-carrying may have evolved as a strategy to mitigate stress from infant loss. These findings have implications for our understanding of grief in nonhuman primates and can impact management protocols surrounding deaths in captive social groups.

Functions of play, which may be performed solo or in a social context, include motor training and behavioral flexibility. Play is often more common in infancy and the juvenile period, although it also occurs in adults of many species. In contrast to social play, few studies have investigated solitary play. Here, we present new empirical data on solitary water play in a subadult and two adult mountain gorillas in Bwindi Impenetrable National Park, Uganda, observed on three different days between January and February 2018. Focal sampling was used to record the behavior of the individuals interacting with water. Movements included vigorous rotation of the arms, splashing the water, tilting the head, making a play face, and sweeping with the hands to create waves on the water surface. One of the episodes represents the first vigorous display of splashing water ever reported for Bwindi gorillas. Our observations highlight three significant components of mountain gorilla development and behavior: play, behavioral flexibility, and exploration.

Demographic studies on translocated primate groups provide a unique opportunity to study population dynamics, social strategies, and reproductive parameters of a species adapting to new environments. In 1996, 38 Japanese macaques (Macaca fuscata) of the Minoo-H group (Osaka Prefecture, Japan) were translocated to Affenberg Landskron, a four-hectare naturally forested park in southern Austria. By January 2020, the population had increased to 160 individuals, and a total of 223 births were recorded. Births peaked in late April to late May, and the timing was influenced by neither offspring sex nor parity status of the mother. Infant mortality was low (8.97%), mostly involving primiparous females, and the average interbirth intervals were shorter following the death of an infant (1.10 years) than a surviving infant (1.77 years). Females rarely had offspring with the same males repeatedly, and the reproductive success among males declined with increasing years of presence in the group. The main aspects of reproduction, mortality, and mate choice are consistent with published data on natural and provisioned populations in Japan and those translocated to other countries. The life expectancy for females, however, was relatively high (11.72% chance of reaching the age of 20), whereas birth control prevented them from using their lifetime reproductive potential. By January 2020, the number of old individuals (> 18 years; 17.5%) was close to that of juveniles (

The ecosystem response to wildfire is often linked to fire severity, with potentially large consequences for belowground biogeochemistry and microbial processes. While the impacts of wildfire on belowground processes are generally well documented, it remains unclear how fire affects the fine-scale composition of microbial communities. Here, we investigate the composition of soil bacterial and fungal communities in burned and unburned forests in an attempt to better understand how these diverse communities respond to wildfire. We explored the belowground responses to three wildfires in Linville Gorge, NC, USA. Wildfires generally increased soil carbon content while simultaneously reducing soil respiration. We employed amplicon sequencing to describe soil microbial communities and found that fires decreased both bacterial and fungal diversity. In addition, wildfires resulted in significant shifts in both bacterial and fungal community composition. Bacterial phylum-level distributions in response to fire were mixed without clear patterns, with members of Acidobacteria being representative of both burned and unburned sites. Fungal communities showed consistent increases in Ascomycota dominance and concurrent decreases in Basidiomycota and Zygomycota dominance in response to burning. Indicator species analysis confirmed shift to Ascomycota in burned sites. These shifts in microbial communities may reflect differences in the quality and quantity of soil organic matter following wildfires.

Measuring hormonal profiles is important in monitoring stress, physical fitness, and reproductive status in primates. Noninvasive methods have been used to measure several steroid hormones in primates without causing them stress. However, few studies have used feces or urine to measure dehydroepiandrosterone sulfate (DHEAS), an important precursor of sex steroids that has been studied as a biomarker of aging, pregnancy, and stress in humans and nonhuman primates. We developed an enzyme immunoassay to detect DHEAS in the feces of Japanese macaques (Macaca fuscata). Our subjects included eight singly housed Japanese macaques. To validate the assay, we administrated oral DHEA to one male and one female macaque, collected their feces, and measured DHEAS levels over time. Given that DHEAS is related to gonadal steroids and the stress response, we also measured DHEAS concentrations in response to adrenal (adrenocorticotropic hormone [ACTH]) and gonadal (human chorionic gonadotropin [hCG]) stimulation. Our assay successfully detected DHEAS in Japanese macaque feces, and levels of DHEAS were associated with the amount of DHEA ingested. Parallelism and accuracy tests revealed that fecal extracts were reliable measures of DHEAS. Neither ACTH nor hCG challenge appeared to affect DHEAS levels. The method we describe is less expensive than that using the commercially available kits and is applicable to investigations involving aging, stress, and reproduction in Japanese macaques.

Infectious diseases including those acquired through direct or indirect contact with people and livestock threaten the survival of wild great apes. Few studies have reported enterobacterial pathogens in chimpanzees. We used multiplex PCR to screen faeces of chimpanzees sharing a landscape with villagers and livestock in Bulindi, Uganda for Salmonella spp., enterohemorrhagic Escherichia coli (E. coli) and Shigella spp./enteroinvasive E. coli. All three potentially zoonotic pathogens were detected. Individual prevalence ranged between 7 and 20%, with most infections observed in mature male chimpanzees. These preliminary findings suggest detailed investigation of enterobacterial infections in people, primates and livestock in this ecosystem is warranted.

Cultural primatology (i.e., the study of behavioral traditions in nonhuman primates as a window into the evolution of human cultural capacities) was founded in Japan by Kinji Imanishi in the early 1950s. This relatively new research area straddles different disciplines and now benefits from collaborations between Japanese and Western primatologists. In this paper, we return to the cradle of cultural primatology by revisiting our original articles on behavioral innovations and traditions in Japanese macaques. For the past 35 years, our international team of biologists, psychologists and anthropologists from Japan, France, Sri Lanka, the USA and Canada, has been taking an integrative approach to addressing the influence of environmental, sociodemographic, developmental, cognitive and behavioral constraints on the appearance, diffusion, and maintenance of behavioral traditions in Macaca fuscata across various domains; namely, feeding innovation, tool use, object play, and non-conceptive sex.

The introduction and eradication of alien invasive plant species potentially alters feeding and spatial ecology of wild primates. We investigated whether the removal of an important dietary resource for wild chacma baboons (Papio hamadryas ursinus), black wattle (Acacia mearnsii), from a nature reserve would result in longer daily path lengths (DPLs) and greater movement toward other resources, specifically alternative black wattle stands outside the reserve, agricultural plots, and sleeping and geophagy sites. We fitted a juvenile male baboon with a self-releasing GPS collar to track the focal troop’s movements on Wildcliff Nature Reserve and adjacent properties, located in the Western Cape, South Africa, from January 25, 2010 to January 18, 2011. During this time, Working for Water, an environmental conservation initiative of the South African Department of Water Affairs, removed black wattle from the baboons’ home range. We estimated monthly home range (5.30–20.58 km2) and DPL (1.7–11.7 km) and quantified the baboons’ use of five dominant vegetation types. Our vegetation use-availability analysis indicated that the troop preferred black wattle, Afromontane forests, and, to a lesser extent, pasture, but used agricultural plots and fynbos less than expected by availability. With increasing black wattle removal in the core area, the troop traveled further toward distant sources of black wattle, using sleeping sites out of their core area to accommodate such long day journeys. A general linear model indicated that movement to black wattle stands, as well as changing sleeping sites, day length, and both spring and winter seasons all significantly increased DPL. We suggest the influence that alien invasive species and their eradication has on ranging behavior should be a consideration in primate conservation and management policies.

Dung beetles serve as the intermediate host for Streptopharagus pigmentatus, a nematode parasite that infects an old world primate, the Japanese Macaque (Macaca fuscata). This study compares the behaviors of infected and uninfected beetles in both transmission dynamics and the ecological role of the parasite. The results suggest that parasitism does not alter the beetle’s use of shelter or choice of substrate on Yakushima Island, Japan. However, infected beetles consume significantly less feces. Dung beetles remove the majority of fecal material in this forest ecosystem, eliminating breeding grounds for many insect pests and burying nutrients that are essential for plant health. Thus, the nematode parasite S. pigmentatus, by altering its host’s behavior, changes the availability of fecal resources to both plant and animal communities and should therefore be classified as an ecosystem engineer.

Stone handling (SH) behavior was systematically studied in a captive troop of rhesus macaques housed at the Primate Research Institute of Kyoto University, and compared with the results of long-term studies of this behavior in Japanese macaques, to evaluate the similarities of SH behavior in these two closely related species. Similar to Japanese macaques, rhesus macaques showed age-related differences in SH. Young animals were more active and displayed more SH patterns and bouts than did adults. Furthermore, the young displayed SH at a higher frequency and their bouts were of a shorter duration, compared to adults. Young adults were more active and displayed more patterns than did older adults. On the other hand, older adults were more conservative and displayed fewer patterns, and engaged in them for longer durations. All individuals displayed SH more frequently in relaxed environmental and social conditions. While lacking an apparent immediate adaptive value, practice of the behavior has been proposed to have long-term functional value for neural and cognitive development in the young and for the maintenance or repair of neuro-pathways in aging macaques that habitually perform the behavior. The results presented here are consistent with what we know about Japanese macaque SH. Given the uniformity of SH behavioral parameters and these two macaque species' close phylogenetic relatedness, we propose that a similar functional and adaptive value for SH can be inferred for rhesus macaques.

Translocation programs releasing animals into the wild need to assess the potential risks associated with the exchange of parasites and other pathogens between native and translocated species. We assessed the composition of the parasite communities in sympatric native and introduced primates. Over a 3-yr period we monitored the gastrointestinal parasites of 3 primate species living in the isolated ecosystem of Rubondo Island National Park, Tanzania: translocated chimpanzees (Pan troglodytes) and guerezas (Colobus guereza) and the indigenous vervets (Chlorocebus aethiops pygerythrus). We detected Troglodytella abrassarti and Enterobius cf. anthropopitheci only in chimpanzees and Chilomastix mesnili in chimpanzees and guerezas. In vervets, we recorded Anatrichosoma sp. and Subulura sp., previously reported in Rubondo chimpanzees. We found Blastocystis sp., Giardia sp., Iodamoeba buetschlii, Entamoeba coli, Entamoeba spp., Trichuris sp., Strongyloides spp., spirurids (cf. Protospirura muricola), and undetermined strongylids in all 3 primate species. Considering the absence of Protospirura muricola in other wild populations of chimpanzees and guerezas, it has probably been acquired from the native vervets, as have Anatrichosoma sp. and Subulura sp. Lower parasite load in Rubondo chimpanzees, in comparison with wild populations at other study sites of this species, might be due to their stay in captivity in Europe before being released on the island. Despite a lack of any apparent health problems from infections in introduced Rubondo primates, parasite monitoring during reintroduction/introduction projects is necessary to decrease potential risks resulting from the exchange of parasites between translocated and native species.

Demonstrating the ability to 'copy' the behavior of others is an important aspect in determining whether social learning occurs and whether group level differences in a given behavior represent cultural differences or not. Understanding the occurrence of this process in its natural context is essential, but can be a daunting task in the wild. In order to test the social learning hypothesis for the acquisition of leaf swallowing (LS), a self-medicative behavior associated with the expulsion of parasites, we conducted semi-naturalistic experiments on two captive groups of parasite-free, naïve chimpanzees (Pan troglodytes). Individuals in the group were systematically provided appropriate stimuli (rough hispid leaves) identical to those used by chimpanzees in the wild. Individuals initially responded in a variety of ways, ranging from total aversion to normal chewing and swallowing. Over time, however, the two groups adopted different variants for inserting and folding the leaves in the mouth prior to swallowing them (complete and partial LS), following the specific method spontaneously displayed by the first and primary LS models in their respective groups. These variants were similar to LS displayed by chimpanzees in the wild. Using the option-bias method, we found evidence for social learning leading to group-level biased transmission and group-level stabilization of these two variants. This is the first report on two distinct cultural variants innovated in response to the introduction of natural stimuli that emerged and spread spontaneously and concurrently within two adjacent groups of socially housed primates. These observations support the assertion that LS may reflect a generalized propensity for ingesting rough hispid leaves, which can be socially induced and transmitted within a group. Ingesting an adequate number of these leaves induces increased gut motility, which is responsible for the subsequent expulsion of particular parasite species in the wild. Cultural transmission and maintenance of LS within a group and associative learning by the individual of the positive consequences of this otherwise non-nutritive mode of ingestion is proposed to be the pivotal link between this feeding propensity and its maintenance as a self-medicative behavior by great apes in the wild.

We identified 3 nematodes not previously reported in chimpanzees (Pan troglodytes) introduced on Rubondo Island, Tanzania: Protospirura muricola, Subulura sp., and Anatrichosoma sp. Vervet monkeys (Cercopithecus aethiops pygerythrus), rodents, and intermediate insect hosts might maintain Protospirura muricola and Subulura sp., and indigenous monkeys on the island might also maintain Anatrichosoma sp. Low prevalence of Subulura sp. and Anatrichosoma sp. suggests that chimpanzees acquired them from ingestion of contaminated food.

We examined bone mineral density (BMD) of the femoral neck and lumbar vertebrae of four chimpanzee skeletons from Mahale Mountains National Park, Tanzania, and four captive ones, with a dual energy X-ray absorptiometer. The BMD of Wansombo, an old female chimpanzee from Mahale, was remarkably lower than the mean of the other six younger adult female chimpanzees and categorized as osteoporosis. Posture, locomotion, and trunk-sacral anatomy of chimpanzees may have prevented fractures in Wansombo, whose BMD was below human osteoporosis criteria.

We collected data on parasitic prevalence and leaf-swallowing behavior of bonobos (Pan paniscus) between August 1998 and April 1999 at the Iyema research site, Lomako Forest, Democratic Republic of Congo. We report the first detailed observations of leaf-swallowing among bonobos and the first record of the behavior at Iyema-Lomako. Bonobo leaf-swallowing closely fits the description of the behavior among chimpanzees. Bonobos ingested leaves of Manniophyton fulvum, as occurs in two chimpanzee populations in Central and Western Africa and among bonobos at Wamba, about 200 km from Iyema-Lomako. All leaf-swallowing occured in the rainy season. In conformity with patterns among Mahale chimpanzees, the prevalence of Oesophagostomum sp. infection in bonobos increased after the onset of the rainy season.

In a long-term study of sexual behavior in Japanese macaques, we found that matrilineal inbreeding accounted for 2.9% of the copulations recorded for the Arashiyama B troop during 7 mating seasons between 1968 and 1984. Of the 906 copulatory dyads, 46 (5.1%) occurred among kin. Close matrilineal kin dyads (r = 1/2−1/8, 1.1% of the total of copulatory dyads) strongly avoided matrilineal inbreeding, but for remote kin dyads (r > 1/8, 4.0% of the total) the tendency was weaker in some years. Among the possible determinants of matrilineal inbreeding, we found that it tended to occur among younger and lower-ranking males as an effect of troop demographic changes. There is no significant association between female rank and matrilineal inbreeding. Our results are consistent with the hypothesis that different degrees of kin relatedness are discriminated by individuals with respect to mate choice.

Results: Urinary PkDNA was detected on day 2, but was not amplified using DNA templates extracted from the samples on day 4, day 5 and day 6. Subsequently, urinary PkDNA was detected from day 7 until day 11, and from day 20 until day 30. PkDNA in faeces was detected from day 7 until day 11, and from day 20 until day 37. Moreover, real-time quantitative PCR showed a remarkable increase in the amount of urinary PkDNA following anti-malarial treatment. This might have been due to the release of a large amount of PkDNA from the degraded parasites as a result of the anti-malarial treatment, leading to excretion of PkDNA in the urine. Methods. Urine and faeces were obtained from a Plasmodium knowlesi infected-Japanese macaque (Macaca fuscata) over the course of an experimentally induced infection. P. knowlesi DNA (PkDNA) extracted from urine and faeces were monitored by nested PCR targeting the P. knowlesi specific cytochrome b (cytb) gene. Background: Diagnostic techniques based on PCR for the detection of Plasmodium DNA can be highly sensitive and specific. The vast majority of these techniques rely, however, on the invasive sampling of blood from infected hosts. There is, currently, considerable interest in the possibility of using body fluids other than blood as sources of parasite DNA for PCR diagnosis. Conclusions: The cytb-PCR system using urine and faecal samples is of potential use in molecular epidemiological surveys of malaria. In particular, monkey faecal samples could be useful for the detection of zoonotic primate malaria in its natural hosts., Malaria Journal, 13(1), 373; 2014

When physiological adaptation is insufficient, hosts have developed behavioral responses to avoid or limit contact with parasites. One such behavior, leaf-swallowing, occurs widely among the African great apes. This behavior involves the slow and deliberate swallowing without chewing of whole bristly leaves. Folded one at a time between tongue and palate, the leaves pass through the gastro-intestinal (GI) tract visibly unchanged. Independent studies in two populations of chimpanzees (Pan troglodytes schweinfurthii) showed significant correlations between the swallowing of whole leaves and the expulsion of the nodule worm Oesophagostomum stephanostomum and a species of tapeworm (Bertiella studeri). We integrate behavioral, parasitological and physiological observations pertaining to leaf-swallowing to elucidate the behavioral mechanism responsible for the expulsion and control of nodule worm infections by the ape host. Physical irritation produced by bristly leaves swallowed on an empty stomach, increases motility and secretion resulting in diarrhea which rapidly moves leaves through the GI tract. In the proximal hindgut, the site of third-stage larvae (L3) cyst formation and adult worm attachment, motility, secretion and the scouring effect of rough leaves is enhanced by haustral contractions and peristalsis-antiperistalsis. Frequently, at the peak of reinfection, a proportion of nonencysted L3 is also predictably vulnerable. These factors should result in the disruption of the life cycle of Oesophagostomum spp. Repeated flushing during peak periods of reinfection is probably responsible for long-run reduction of worm burdens at certain times of the year. Accordingly, leaf-swallowing can be viewed as a deliberate adaptive behavioral strategy with physiological consequences for the host. The expulsion of worms based on the activation of basic physiological responses in the host is a novel hitherto undescribed form of parasitic control.

Previous studies on nonhuman primate maternal styles showed that variation in infant-directed behavior falls along two dimensions, traditionally labeled as protectiveness and rejection. We investigated maternal styles in rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques living in analogous captive social groups, and correlated them with the levels of estrogen metabolites excreted in female feces during the perinatal period. We focally observed mother-infant pairs 3 hours per week during the first 12 weeks of infant life. We collected fecal samples twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Three significant components were extracted by principal component analysis from 15 different infant directed behaviors, each reflecting a different aspect of mothering style: rejection is correlated with behavioral measures of maternal opposition to contact; protectiveness is correlated with maternal solicitude; and independence is correlated with time in contact, grooming and cradling. Levels of estrogen metabolites are significantly correlated to rejection but not to protectiveness or independence, indicating that, in nonhuman primates, individual endocrine changes related to maternal behavior might specifically affect the timing of contact interruption.

We gathered data on the amount, composition, and rate of ingestion of foods and soils by the provisioned Japanese macaques (Macaca fuscata fuscata) at Arashiyama, Japan. Behavioral observations spanned one year on 8 adult females, using focal animal sampling. We analyzed a subsample of their foods for nutritional and toxic secondary compound content. We also analyzed soils eaten by the macaques for several physical-chemical properties and tested their adsorption affinity to tannins and alkaloids. Geophagy occurred at a high rate of 2.97 g/indiv./day with an elevated frequency in the afternoon. About two-thirds of their foods (by fresh weight) were provisioned items, which are extremely rich in proteins and soluble carbohydrates. The soils that they ingested were generally poor in mineral elements, the bio-availability of which was low. The soils had a high adsorption capacity for plant alkaloids but were poorly absorptive for tannins. They were rich in clay minerals of proven buffering capacity. Geophagy at Arashiyama may improve the health of macaques via buffering gastric upset. We discuss the results from the viewpoint of several hypotheses on geophagy.

Termite mound soils eaten by chimpanzees of the Mahale Mountains and Gombe National Parks, Tanzania, have mineralogical and geochemical compositions similar to many soils eaten by higher primates, but release very low levels of either toxic or nutritional inorganic elements to solution at acid pH. Comparison with control (uneaten) soils from the same areas showed lower levels of carbon and nitrogen in the eaten soils, a relationship confirmed by surface analysis. Surface analysis also revealed lower levels of iron on particle surfaces versus interiors, and higher levels of iron on ingested versus control soil particle surfaces. The soils can adsorb dietary toxins, present in the plant diet or those produced by microorganisms. Taking the toxic alkaloids quinine, atropine, sparteine, and lupanine as examples, it is evident that soils from Mahale have a very good adsorptive capacity. A new adaptive advantage of geophagy is proposed, based on the prevention of iron uptake. The behavior of the soils in vitro is consistent with the theory that geophagy has a therapeutic value for these chimpanzees.

There is wide interest in the effects of reproductive biology, mating partner preference, and rank on mating success (MS) and reproductive success (RS) in primates. In particular, theory stresses importance on the mechanisms for attaining RS. Most theory hedges on competitive ability and priority of access to resources, whether they be food or estrous females. However, the majority of data used in favor of such hypotheses come from relatively short-term studies. We review these hypotheses based on long-term data from provisioned and unprovisioned populations of Japanese macaques. Neither MS nor RS were consistently attained by high-ranking males and females. For males, female choice and mating partner preference is seen to over-ride most male-male competitive behaviors likely to affect MS and RS through priority of access to estrous females. Long-term mating patterns driven largely by female partner preferences, results in decreasing MS and RS for older higher-ranking males. The long-term trend for females to prefer less familiar or novel partners results in higher MS and RS for younger, middle-ranking males. The effects of this vary according to troop size and the duration of male tenure. For females, no consistent trend was recognized for rank related RS in either provisioned or unprovisioned troops. Non-reproductive mating may provide differential benefit to high-ranking females for access to limited food resources in some habitats but overall the relationship was inconclusive. Distribution and defendability of food resource, rather than provisioning per se may be more important.

We studied factors affecting party size and composition of wild chimpanzees at Mahale (M group) over an 11-month period. Parties with 1–5 individuals were most frequent (37.8%; 153/405 parties); they included 94.7% of all male parties (n = 76) and 81.3% of all female parties (n = 75). The median of monthly values was the standard for analysis. We divided the year into four periods based on the median size of monthly bisexual parties (30.9 individuals; includes both males and females): monthly bisexual party sizes were larger in May–June (period II) and October–January (period IV) and smaller in February–April (period I) and July–September (period III). Only bisexual parties changed in size with period. The number of fruit items (=species) eaten was fewer in periods II and IV when abundance per item appeared to be great. The sizes of bisexual parties, which included cycling females with maximal anogenital swelling, were larger, and their representation (%) in all bisexual parties was greater in periods III and IV. The numbers of both cycling females and cycling females with maximal anogenital swelling were also larger in periods III and IV. The percentage of cycling females with maximal anogenital swelling was greater in periods II and III. The results of this study and those of Nishida (1979) suggest that seasonal variation in party size of Mahale chimpanzees maintains a relatively consistent annual cycle. The factors assumed to affect party sizes are fruit availability and the presence of cycling females with maximal anogenital swelling.

Thiarubrine A, an antimicrobial and nematocidal 1,2-dithiin polyyne has been reported to be a constituent of Aspilia leaves swallowed whole by chimpanzees. Aspilia samples were analyzed for the presence of thiarubrine A and other sulfur-containing polyynes using high-performance liquid chromatography (HPLC) and an antifungal bioassay. Thiarubrines A, B, D, and E and their corresponding thiophenes were not present in the leaves of three Aspilia species including A. mossambicensis and A. rudis, which are swallowed by chimpanzees at Mahale Mountains National Park and Gombe National Park, Tanzania. Antifungal activity, indicative of the presence of thiarubrines, was not detected in Aspilia leaf samples. Small amounts of thiarubrines A and B, and thiophenes A and B were found in A. mossambicensis roots. Analysis of three North American taxa found high concentrations of thiarubrines and thiophenes in the roots of Eriophyllum lanatum and Chaenactis douglasii, and the roots and leaves of Ambrosia chamissonis.

A longitudinal study of nematode infection in chimpanzees was conducted between 1989 and 1994 on the M group chimpanzees of the Mahale Mountains National Park, Tanzania during two annual dry and rainy season periods and a third rainy season. Chemical and physical antiparasite properties of medicinal plant use against the strongyle nematodeOesophagostomum stephanostomum have recently been reported at Mahale. Here, the incidence of nematode infections were analyzed for seasonal trends to elucidate the possible influence of parasite infection on previously reported seasonality of medicinal plant use and to test the hypothesis that the use of these plants is stimulated byO. stephanostomum. The number of chimpanzees infected byO. stephanostomum was significantly higher in the rainy season than in the dry season of both 1989–1990 and 1991–1992. However, the incidence ofTrichuris trichura andStrongyloides fuelleborni showed no seasonality. Reinfection of individuals byO. stephanostomum occurred in synchrony with annual variation in rainfall: there was a sharp rise in the occurrence of new infections per individual within one to two months after the beginning of the first heavy rains of the season. This pattern coincides with the reproductive cycle of this nematode species.O. stephanostomum (95%) infections were associated significantly more frequently with medicinal plant use than eitherT. trichiura (50%) orS. fuelleborni (40%) infections. These observations are consistent with previous reports for the increased use of these plants during the rainy season and are consistent the hypothesis that medicinal plant use is stimulated byO. stephanostomum infection.

Background Ingestion of plant parts purportedly for their non-nutritive and/or bioactive properties has been widely reported across the animal kingdom. Many of these examples are viewed as behavioral strategies to maintain health by controlling the level of parasite infections. One such behavior is leaf swallowing, the folding and swallowing of whole leaves without chewing. Void of any nutritional benefit, defecation of the whole leaves is associated with the physical expulsion of intestinal parasites. Fecal samples of the Chinese lesser civet Viverricula indica were collected along a fixed transect line monthly for 17 months in the Fushan Experimental Forest, northeastern Taiwan. We inspected samples for the occurrence of undigested leaves and parasite worms to test the possible antiparasitic function of the behavior in this species. Results Of the collected feces, 14.3% contained whole, folded, undigested leaves of grass. The co-occurrence of undigested grass and Toxocara paradoxura worms in the feces was statistically significant. Adult worms of T. paradoxura were trapped inside the fecal-grass mass or on the surface of leaves in these samples. Increases in the T. paradoxura prevalence and infection intensity were associated with a higher presence of whole leaves in the feces. Conclusions Reported for the first time in the context of self-medication for civet species, we propose that swallowing grass may facilitate expulsion of adult worms of T. paradoxura, which resembles behaviors widely reported in African great apes, bears, and geese.

Swallowing whole leaves by chimpanzees and other African apes has been hypothesized to have an antiparasitic or medicinal function, but detailed studies demonstrating this were lacking. We correlate for the first time quantifiable measures of the health of chimpanzees with observations of leaf-swallowing in Mahale Mountains National Park, Tanzania. We obtained a total of 27 cases involving the use ofAspilia mossambicensis (63%),Lippia plicata (7%),Hibiscus sp. (15%),Trema orientalis (4%), andAneilema aequinoctiale (11%), 15 cases by direct observation of 12 individuals of the Mahale M group. At the time of use, we noted behavioral symptoms of illness in the 8 closely observed cases, and detected single or multiple parasitic infections (Strongyloides fulleborni, Trichuris trichiura, Oesophagostomum stephanostomum) in 10 of the 12 individuals. There is a significant relationship between the presence of whole leaves (range, 1–51) and worms of adultO. stephanostomum (range, 2–21) in the dung. HPLC analysis of leaf samples collected after use showed that thiarubrine A, a compound proposed to act as a potent nematocide in swallowingAspilia spp., was not present in leaves ofA. mossambicensis or the three other species analyzed. Alternative nematocidal or egg-laying inhibition activity was not evident. Worms ofO. stephanostomum were recovered live and motile from chimpanzee dung, trapped within the folded leaves and attached to leaf surfaces by trichomes, though some were moving freely within the fecal matter, suggesting that the physical properties of leaves may contribute to the expulsion of parasites. We review previous hypotheses concerning leaf-swallowing and propose an alternative hypothesis based on physical action.

Earth from a termite mound in the Mahale Mountains National Park, Tanzania, eaten by chimpanzees, was analyzed to determine the possible stimulus, or stimuli, for geophagy. The termite mound sample contains relatively high aluminum (10.0%), iron (3.0%), and sodium (0.5%). This correlates well with the mineralogy of the clay (

Based on a sample of 237 live births recorded over a period of 30 years, a tendency for longer interbirth intervals following the birth of daughters than sons was recognized, in the provisioned Arashiyama troop of Japanese macaques. This may indicate that female infants were more costly to produce than male infants. This tendency seemed to be independent of a mother’s rank.

The bitter and related constituents have been isolated fromVernonia amygdalina (Compositae), a plant ingested by wild chimpanzees possibly suffering from parasite-related diseases in the Mahale Mountains National Park, Tanzania. Isolated from the plant were four known sesquiterpene lactones, seven new steroid glucosides, and two aglycones of the glucosides. The sesquiterpene lactones showed significant in vitro antischistosomal, plasmodicidal, and leishmanicidal activities. Antischistosomal activity was also found for the major steroid glucoside, vernonioside B1. A trend in the glucosides to show significant antischistosomal, plasmodicidal, and amebicidal activities when the sugar moiety was removed, was observed. Vernodalin, judged as the most significant constituent for antiparasitic activities in vitro, was tested for in vivo antischistosomal effect. It was, however, highly toxic to the cercaria-infected mouse. Chimpanzees have been only rarely observed to ingest anything but the pith of the young stem. The occurrence of vernonioside B1 and its aglycone vernoniol B1, the major constituents among the steroid-related constituents, were detected at significant levels in the pith. However, vernodalin was abundant only in the leaves and bark. Thus, chimpanzees at Mahale were hypothesized to control parasite-related diseases by ingesting the young pith of this tree containing steroid-related constituents.

Potential medicinal plants for wild chimpanzees have been studied in order to discover their physiologically active compounds. Tests of the physiological activity of 3 plant species—Vernonia amygdalina, Aspilia mossambicensis, andFicus exasperata—indicate that they contain a variety of active compounds. From one species,V. amygdalina, an antitumor agent and 2 possible antitumor promoters are identified. Furthermore, steroid glucosides were isolated as the bitter substances. These structurally new compounds are expected to exhibit a number of significant physiological activities. The chemical investigation of possible medicinal plants used by chimpanzees should be helpful in recovering naturally occurring compounds of medicinal significance for human use.

A 12-year-old female chimpanzee (Pan troglodytes schweinfurthii) of M-Group in the Mahale Mountains National Park, Tanzania was seen to rouse, capture, and eat a squirrel hiding in the narrow hole of a tree. The kill was aided by the use of a sturdy tool modified from a branch of the same tree. This appears to be the first reported case for chimpanzees, or any other nonhuman primate, of tool-use that directly led to the capture of a mammalian prey species. This behavior is discussed in relation to possible factors contributing to the occurrence of tool-use in small mammal predation especially by females to exploit a low competition meat source.

Over a 30-year period from 1954 to 1983, 975 live births were recorded for Japanese macaque females at the Iwatayama Monkey Park, Arashiyama, Japan. Excluding unknown birth dates, primiparous mothers gave birth to 185 infants (182 cases with age of mother known) and multiparous mothers gave birth to 723 infants (603 cases with age of mother known). The peak month of birth was May with 52.3% of the total births occurring during the period. Multiparous females who had not given birth the previous year did so earlier than multiparous females who had given birth the previous year and also earlier than primiparous females. Among the females who had given birth the previous year, females whose infant had died gave birth earlier than females who had reared an infant the previous year. The offspring sex ratio (1:0.97) was not significantly different from 1:1, and revealed no consistent association with mother's age. Age-fecundity exhibited a humped curve. The annual birth rate was low at the age of 4 years but increased thereafter, ranging between 46.7% and 69.0%, at between 5 and 19 years of age, but again decreased for females between 20 and 25 years of age. Some old females displayed clear reproductive senescence. The infant mortality within the first year of age was quite low (10.3%) and the neonatal (less than 1 month old) mortality rate accounted for 49.0% of all infant deaths. There was no significant difference between the mortality rates of male and female infants. A female's rank-class had no apparent effect on the annual birth rate, infant mortality, and offspring sex ratio. These long-term data are compared with those from other primate populations.

Dominance relationships among male chimpanzees in the Mahale Mountains National Park, Tanzania, were analyzed. Although all adolescent males were unequivocally subordinate to all adult males, dominance relationships within the age classes were much less clear. Especially among adolescent males, few pant-grunts or agonistic interactions occurred. While adolescent males frequently pant-grunted at adult males, these latter males, except the alpha and the youngest, rarely pant-grunted to one another. This suggests that a difference of social status exists between adolescent and adult males. Adult males rarely display overt dominance to one another probably because the presence of other males affects their interactions. Moreover, they seem to try to keep their dominance relationship ambiguous when making it overt is not advantageous to them. This may be a political way for males to coexist with one another in a unit-group.

Stone-play, a newly innovated cultural behavior, has been observed among the free-ranging Arashiyama B troop Japanese macaques near Kyoto, Japan since 1979. Conditions in which the non-purposeful handling of stones might possibly give rise to tool behavior are discussed. The progression of this behavior is traced through three phases: transmission, tradition, and transformation. During the first two phases, through social learning, the behavior was established within the group as a regular item of their behavioral repertoire and was most frequently observed after eating provisioned grain. In the third phase, observations suggest a “faddish” shift in the practice of certain behavioral sub-types between 1984 and 1985. During this period young individuals increasingly began to carry stones away from the feeding station, mixing stone manipulation with forage-feeding activities in the forest. Observations suggest under such conditions, stone handling is likely to lead to the occasional use of stone as a tool. This conclusion probably can be applied to species other thanMacaca fuscata. Consideration of the eco-setting and social learning correlates of stone handling suggests how the instrumental use of stone might emerge from a tradition of non-instrumental manipulation.

Detailed observations on the consumption ofVernonia amygdalina (Del.), a naturally occurring plant of known ethnomedicinal value, by an adult female chimpanzee (Pan troglodytes schweinfurthii) of M-group in the Mahale Mountains, Tanzania were made. Chewing the pith of several shoots, she sucked out and swallowed the astringent, bitter tasting juice; spitting out the fibrous remains. The female was followed during this period for 11 hr, over two consecutive days, and was recognized to be in irregular health at the time of consumption, exhibiting signs of lethargy, lack of appetite, and irregularity of bodily excretions. The low frequency and lack of seasonality in the usage of this plant suggest that it is sought after for reasons other than as a food source. These factors suggest that for chimpanzees, the consumption of this plant is primarily medicinal. The symptoms displayed by the female are the same as those experienced by people throughout tropical Africa who utilize this plant as a medicinal treatment for them. Interactions between the female and others suggest that they too were aware of her condition and coordinated their activities with the female and her infant.