Ria R. Ghai

Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda.

Background Whipworms (Trichuris sp.) are a globally distributed genus of parasitic helminths that infect a diversity of mammalian hosts. Molecular methods have successfully resolved porcine whipworm, Trichuris suis, from primate whipworm, T. trichiura. However, it remains unclear whether T. trichiura is a multi-host parasite capable of infecting a wide taxonomic breadth of primate hosts or a complex of host specific parasites that infect one or two closely related hosts. Methods and Findings We examined the phylogenetic structure of whipworms in a multi-species community of non-human primates and humans in Western Uganda, using both traditional microscopy and molecular methods. A newly developed nested polymerase chain reaction (PCR) method applied to non-invasively collected fecal samples detected Trichuris with 100% sensitivity and 97% specificity relative to microscopy. Infection rates varied significantly among host species, from 13.3% in chimpanzees (Pan troglodytes) to 88.9% in olive baboons (Papio anubis). Phylogenetic analyses based on nucleotide sequences of the Trichuris internal transcribed spacer regions 1 and 2 of ribosomal DNA revealed three co-circulating Trichuris groups. Notably, one group was detected only in humans, while another infected all screened host species, indicating that whipworms from this group are transmitted among wild primates and humans. Conclusions and Significance Our results suggest that the host range of Trichuris varies by taxonomic group, with some groups showing host specificity, and others showing host generality. In particular, one Trichuris taxon should be considered a multi-host pathogen that is capable of infecting wild primates and humans. This challenges past assumptions about the host specificity of this and similar helminth parasites and raises concerns about animal and human health.

Going, Going, Gone: A 15-Year History of the Decline of Primates in Forest Fragments near Kibale National Park, Uganda

Given accelerating trends of deforestation and human population growth, immediate and innovative solutions to conserve biodiversity are sorely needed. Between 1995 and 2010, we regularly monitored the population size and structure of colobus monkey populations in the forest fragments outside of Kibale National Park, Uganda. Through this monitoring we assessed the monkeys’ gastrointestinal parasites and fecal cortisol levels. Over 15 years, we documented a rapid decline in the number of fragments that supported primates, largely as a result of tree removal. Fecal cortisol levels of primates found in the fragments were consistently higher than in populations found in the continuous forest of the national park. The fragment populations also harbored gastrointestinal parasites rarely found in the main forest and exchanged bacteria with nearby people and livestock at high rates, suggesting that fragmentation facilitates disease transmission. Fragments supported the fuelwood needs of an average of 32 people living immediately adjacent to the fragment, and partially supported families up to three farms away (~400 m, representing 576 people). Intensive fuelwood harvesting occurred when neighboring households engaged in brewing beer (an average of 9.6 % of the households), distilling gin (8.8 %), or producing charcoal (14.5 %). Our data suggest that the future of small and unprotected forest fragments is bleak; a scenario that is unfortunately typical outside protected areas in many tropical regions.

Sickness behaviour associated with non-lethal infections in wild primates

Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.

Group living and pathogen infection revisited

Group living enhances the costs of pathogen infection by increasing the exposure of social individuals to infectious organisms. This hypothesis is well-supported, particularly for pathogens transmitted by close contact. However, recent and compelling research suggests that it is time to revisit this idea. Here, we focus on new findings which suggest that group living can: (i) enhance host resistance to pathogen infection, and (ii) reduce the fitness impacts of infection. This research raises the exciting possibility that there may be common anti-parasite benefits of group living, in addition to well-known pathogen costs.

Primates in Fragments 10 Years Later: Once and Future Goals

In 2010, the Food and Agriculture Organization of the United Nations (FAO) estimated that 16 million hectares of forest per year were lost globally in the 1990s (FAO 2010), and approximately 12.5 million hectares/year were lost in countries with primate populations, an area just smaller than Greece or the US State of Mississippi (Chapman and Peres 2001; Chapman and Gogarten 2012). In contrast, in the last decade (2000–2010), the rate of deforestation has decreased globally by approximately 5.2 million hectares/year, and reforestation and natural expansion of forests in some countries significantly reduced the net loss of forest (FAO 2010). This may be in part due to the lack of resonance in satellite imagery between secondary and primary forest regions, particularly in the tropics. Unfortunately, the increase in forested lands has principally affected temperate regions of Europe and eastern Asia (e.g., China, Japan), but deforestation of most tropical forests has continued steadily (e.g., annual loss: 0.5 % in Africa, 1.2 % in Mesoamerica, 0.5 % in South America, 0.4 % in southeastern Asia; FAO 2011).

Protozoan parasites in group‐living primates: testing the biological island hypothesis

A series of articles by W.J. Freeland published in the 1970s proposed that social organization and behavioral processes were heavily influenced by parasitic infections, which led to a number of intriguing hypotheses concerning how natural selection might act on social factors because of the benefits of avoiding parasite infections. For example, Freeland [1979] showed that all individuals within a given group harbored identical gastrointestinal protozoan faunas, which led him to postulate that social groups were akin to “biological islands” and suggest how this isolation could select specific types of ranging and dispersal patterns. Here, we reexamine the biological island hypothesis by quantifying the protozoan faunas of the same primate species examined by Freeland in the same location; our results do not support this hypothesis. In contrast, we quantified two general changes in protozoan parasite community of primates in the study area of Kibale National Park, Uganda, over the nearly 35 years between sample collections: (1) the colobines found free of parasites in the early 1970s are now infected with numerous intestinal protozoan parasites and (2) groups are no longer biological islands in terms of their protozoan parasites. Whatever the ultimate explanation for these changes, our findings have implications for studies proposing selective forces shaping primate behavior and social organization. Am. J. Primatol. 74:510–517, 2012.

Arteriviruses, pegiviruses, and lentiviruses are common among wild African monkeys

ABSTRACT Nonhuman primates (NHPs) are a historically important source of zoonotic viruses and are a gold-standard model for research on many human pathogens. However, with the exception of simian immunodeficiency virus (SIV) (family Retroviridae), the blood-borne viruses harbored by these animals in the wild remain incompletely characterized. Here, we report the discovery and characterization of two novel simian pegiviruses (family Flaviviridae) and two novel simian arteriviruses (family Arteriviridae) in wild African green monkeys from Zambia (malbroucks [Chlorocebus cynosuros]) and South Africa (vervet monkeys [Chlorocebus pygerythrus]). We examine several aspects of infection, including viral load, genetic diversity, evolution, and geographic distribution, as well as host factors such as age, sex, and plasma cytokines. In combination with previous efforts to characterize blood-borne RNA viruses in wild primates across sub-Saharan Africa, these discoveries demonstrate that in addition to SIV, simian pegiviruses and simian arteriviruses are widespread and prevalent among many African cercopithecoid (i.e., Old World) monkeys. IMPORTANCE Primates are an important source of viruses that infect humans and serve as an important laboratory model of human virus infection. Here, we discover two new viruses in African green monkeys from Zambia and South Africa. In combination with previous virus discovery efforts, this finding suggests that these virus types are widespread among African monkeys. Our analysis suggests that one of these virus types, the simian arteriviruses, may have the potential to jump between different primate species and cause disease. In contrast, the other virus type, the pegiviruses, are thought to reduce the disease caused by human immunodeficiency virus (HIV) in humans. However, we did not observe a similar protective effect in SIV-infected African monkeys coinfected with pegiviruses, possibly because SIV causes little to no disease in these hosts.

Providing health care to improve community perceptions of protected areas

Impoverished communities often turn to illegal extraction of resources from protected areas to alleviate economic pressures or to make monetary gains. Such practices can cause ecological damage and threaten animal populations. These communities also often face a high disease burden and typically do not have access to affordable health care. Here we argue that these two seemingly separate challenges may have a common solution. In particular, providing health care to communities adjacent to protected areas may be an efficient and effective way to reduce the disease burden while also improving local perceptions about protected areas, potentially reducing illegal extraction. We present a case study of a health centre on the edge of Kibale National Park, Uganda. The centre has provided care to c. 7,200 people since 2008 and its outreach programme extends to c. 4,500 schoolchildren each year. Contrasting the provision of health care to other means of improving community perceptions of protected areas suggests that health clinics have potential as a conservation tool in some situations and should be considered in future efforts to manage protected areas.

Limited sharing of tick-borne hemoparasites between sympatric wild and domestic ungulates.

Tick-borne hemoparasites (TBHs) are a group of pathogens of concern in animal management because they are associated with a diversity of hosts, including both wild and domestic species. However, little is known about how frequently TBHs are shared across the wildlife-livestock interface in natural settings. Here, we compared the TBHs of wild Grants gazelle (Nanger granti) and domestic sheep (Ovis aries) in a region of Kenya where these species extensively overlap. Blood samples collected from each species were screened for piroplasm and rickettsial TBHs by PCR-based amplification of 18S/16S ribosomal DNA, respectively. Overall, 99% of gazelle and 66% of sheep were positive for Babesia/Theileria, and 32% of gazelle and 47% sheep were positive for Anaplasma/Ehrlichia. Sequencing a subset of positive samples revealed infections of Theileria and Anaplasma. Sequences sorted into seven phylogenetically distinct genotypes-two Theileria, and five Anaplasma. With the exception of a putatively novel Anaplasma lineage from Grants gazelle, these genotypes appeared to be divergent forms of previously described species, including T. ovis, A. ovis, A. bovis, and A. platys. Only one genotype, which clustered within the A. platys clade, contained sequences from both gazelle and sheep. This suggests that despite niche, habitat, and phylogenetic overlap, the majority of circulating tick-borne diseases may not be shared between these two focal species.

Human–Wildlife Interactions Predict Febrile Illness in Park Landscapes of Western Uganda

AbstractFevers of unknown origin complicate treatment and prevention of infectious diseases and are a global health burden. We examined risk factors of self-reported fever—categorized as “malarial” and “nonmalarial”—in households adjacent to national parks across the Ugandan Albertine Rift, a biodiversity and emerging infectious disease hotspot. Statistical models fitted to these data suggest that perceived nonmalarial fevers of unknown origin were associated with more frequent direct contact with wildlife and with increased distance from parks where wildlife habitat is limited to small forest fragments. Perceived malarial fevers were associated with close proximity to parks but were not associated with direct wildlife contact. Self-reported fevers of any kind were not associated with livestock ownership. These results suggest a hypothesis that nonmalarial fevers in this area are associated with wildlife contact, and further investigation of zoonoses from wildlife is warranted. More generally, our findings of land use–disease relationships aid in hypothesis development for future research in this social-ecological system where emerging infectious diseases specifically, and rural public health provisioning generally, are important issues.