No abstract

In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual’s position within the group’s social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female’s position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.

ABSTRACT. 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 nematode Oesophagostomum 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 by O. stephanostomum. The number of chimpanzees infected by O. stephanostornum was significantly higher in the rainy season than in the dry season of both 1989-1990 and 1991-1992. However, the incidence of Trichuris trichiura and Strongyloides fuelleborni showed no seasonality. Reinfection of individuals by O. 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 either T. trichiura (50~ or S. 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 by O. stephanostomum infection.

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.

Variation in the availability and distribution of food resources is a strong selective pressure on wild primates. We explored variation in Tibetan macaque gut microbiota composition during winter and spring seasons. Our results showed that gut microbial composition and diversity varied by season. In winter, the genus Succinivibrio, which promotes the digestion of cellulose and hemicellulose, was significantly increased. In spring, the abundance of the genus Prevotella, which is associated with digestion of carbohydrates and simple sugars, was significantly increased. PICRUSt analysis revealed that the predicted metagenomes related to the glycan biosynthesis and metabolic pathway was significantly increased in winter samples, which would aid in the digestion of glycan extracted from cellulose and hemicellulose. The predicted metagenomes related to carbohydrate and energy metabolic pathways were significantly increased in spring samples, which could facilitate a monkey’s recovery from acute energy loss experienced during winter. We propose that shifts in the composition and function of the gut microbiota provide a buffer against seasonal fluctuations in energy and nutrient intake, thus enabling these primates to adapt to variations in food supply and quality.