Koichiro Zamma

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.

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

I investigated the effect of the density of louse eggs (Pedicinus obtusus andP. 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.

Environmental determinants of the altitudinal variations in relative group densities of Japanese macaques on Yakushima

Altitudinal variations in relative group densities of the Japanese macaques on Yakushima were studied. This is an ideal place for studying resource limitations because it avoids various complicating factors that are difficult to quantify but might affect animal densities, such as predation, interspecific competition, and past catastrophes. The relative group density was high in the coastal forest (0–400 m), while it did not differ among the higher zones (400–800, 800–1200 and 1200–1886 m). To examine this variation, three habitat variables were analyzed: total basal area of food trees per unit area, seasonal variations in fruit abundance, and total annual fleshy fruit production. All of these variables indicate that fruit and seeds are most available in the coastal forest. Thus, altitudinal variations in the density of Japanese macaques on Yakushima are determined by the total annual food abundance.

Vertical Distribution of Wild Yakushima Macaques (Macaca fuscata yakui) in the Western Area of Yakushima Island, Japan : Preliminary Report

A census of wild Yakushima macaques (Macaca fuscata yakui) was carried out in a 23-km2 area of the western coast of Yakushima Island, Japan. We analyzed the census data to investigate changes in monkey distribution associated with the vertical distribution of vegetation. In the lowland coastal zone of 0–300 m above sea level (a.s.l.), 4.8 troops and 62.4–99.8 monkeys are estimated to have existed per km2. In the mountainside zones of 300–900 m a.s.l., the troop density decreased to 1.3–1.6 troops/km2. Since there was no difference in size between the coastal and mountainside troops, population density should decrease with altitude to about 30–36 monkeys per km2. On the other hand, 2.4 troops and about 36 monkeys were estimated to have inhabited per km2 in the mountain summit zone of 900–1,323 m a.s.l.

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.

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.

A New Code of Observation Employed at Mahale: Prevention against a Flu-like Disease

Associate Editors: Christophe Boesch, Max-Planck Institute, Germany Jane Goodall, Jane Goodall Institute, USA Takayoshi Kano, Kyoto University, Japan Tetsuro Matsuzawa, Kyoto University, Japan William C. McGrew, University of Cambridge, UK John C. Mitani, University of Michigan, USA Vernon Reynolds, Budongo Forest Project, UK Yukimaru Sugiyama, Kyoto University, Japan Richard W. Wrangham, Harvard University, USA

Density of Japanese Macaque (Macaca fuscata yakui) Males Ranging Alone: Seasonal and Regional Variation in Male Cohesiveness with the Group

Abstract. We conducted point censuses in Yakushima island to estimate the density of Japanese macaque (Macaca fuscata yakui) males ranging alone, focusing on its vegetational, seasonal, and regional variation. In highland areas, the detection frequency of males ranging alone did not differ among different types of vegetation, despite the latters effect on overall population density. The detection frequency of males ranging alone in the mating season was a third of that in the non-mating season. In the mating season, males exhibit strong cohesiveness with a group, probably in search of resident estrous females. Outside of the mating season, we detected 25% fewer males ranging alone in lowland areas, which have high population densities and strong inter-group competition, than in highland areas. The absolute density of males ranging alone was estimated to be 1.2–5.7 individuals/km2. Meanwhile, the group and population densities were 1.25/km2 and 19.3/km2, respectively. A considerable number of males therefore remained outside of groups, and male cohesiveness with groups is flexible in relation to ecological and social circumstances.

Study Sites of Chimpanzees and Bonobos

Local names of the major study-sites referred in the Glossary are listed below with main reference sources. Shorter-term study sites such as Bai Hokou, Beni, Campo, Filabanga, Kabogo, Kanka-Sili, Kasakati, Moukalaba, Ndoki, Odzala, Petit Loango, and Tongo are described in the glossary.

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.