Urinary neopterin reflects immunological variation associated with age, helminth parasitism, and the microbiome in a wild primate.

Neopterin, a product of activated white blood cells, is a marker of nonspecific inflammation that can capture variation in immune investment or disease-related immune activity and can be collected noninvasively in urine. Mounting studies in wildlife point to lifetime patterns in neopterin related to immune development, aging, and certain diseases, but rarely are studies able to assess whether neopterin can capture multiple concurrent dimensions of health and disease in a single system. We assessed the relationship between urinary neopterin stored on filter paper and multiple metrics of health and disease in wild geladas (Theropithecus gelada), primates endemic to the Ethiopian highlands. We tested whether neopterin captures age-related variation in inflammation arising from developing immunity in infancy and chronic inflammation in old age, inflammation related to intramuscular tapeworm infection, helminth-induced anti-inflammatory immunomodulation, and perturbations in the gastrointestinal microbiome. We found that neopterin had a U-shaped relationship with age, no association with larval tapeworm infection, a negative relationship with metrics related to gastrointestinal helminth infection, and a negative relationship with microbial diversity. Together with growing research on neopterin and specific diseases, our results demonstrate that urinary neopterin can be a powerful tool for assessing multiple dimensions of health and disease in wildlife.

Ecology eclipses phylogeny as a major driver of nematode parasite community structure in a graminivorous primate.

Understanding the relative strength of ecology and phylogeny in shaping parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.We characterized the gastrointestinal (GI) parasite community of wild geladas (Theropithecus gelada), primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.Geladas exhibited very constrained GI parasite communities: only two genera (Oesophagostomum and Trichostrongylus) were identified across 303 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g., Bos taurus, Ovis aries) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to Oesophagostomum sp., seven to Trichostrongylus sp., and one to T. vitrinus.Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited ~4x higher ASV richness than geladas at a less disturbed location within the park.In this system, ecology was a stronger predictor of parasite community structure than phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.

High mortality associated with tapeworm parasitism in geladas (Theropithecus gelada) in the Simien Mountains National Park, Ethiopia.

Despite increasing appreciation for parasitism as an important component of primate ecology and evolution, surprisingly few studies have demonstrated the costs of helminth parasitism in primates. Detecting parasite-related costs in primates is particularly difficult because it requires detailed, long-term data on individual host reproductive success, survival, and parasitism. The identification of the larval tapeworm Taenia serialis in geladas under intensive long-term study in the Ethiopian Highlands (Nguyen et al. [2015] American Journal of Primatology, 77:579-594; Schneider-Crease et al. [2013] Veterinary Parasitology 198:240-243) provides an opportunity to examine how an endemic parasite impacts host reproductive success and survival. We used survival analyses to assess the mortality risk associated with protuberant larval cysts characteristic of T. serialis using a decade of data from a gelada population in the Simien Mountains National Park (SMNP), Ethiopia. We demonstrated strikingly high mortality associated with T. serialis cysts in adult females, particularly for younger adults. The estimated effect of cysts on male mortality was similar, although the effect was not statistically significant, likely owing to the smaller sample size. Additionally, the offspring of mothers with cysts experienced increased mortality, which was driven almost entirely by maternal death. Mothers with cysts had such high mortality that they rarely completed an interbirth interval. Comparison with a study of this parasite in another gelada population on the Guassa Plateau (Nguyen et al. [2015] American Journal of Primatology, 77:579-594) revealed lower cyst prevalence in the SMNP and similar cyst-associated mortality. However, many more females with cysts completed interbirth intervals at Guassa than in the SMNP, suggesting that T. serialis cysts may kill hosts more rapidly in the SMNP. Our results point toward the underlying causes of individual and population-level heterogeneity in T. serialis-associated mortality as important areas for future research.

Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population.

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.