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“‘Mild’ diseases in wild primates: acquiring baseline data about causes and effects of Plasmodium spp. infection in African great apes (Pan troglodytes verus)”

Increasing anthropogenic alterations propelled by a growing human population paired with ecological perturbations and climate change has amplified rates of disease transmission at the human-wildlife interface. While attention has focused primarily on diseases that cause high rates of morbidity and mortality, there is a dearth of research on more common, non-lethal “mild” infections. However, despite less obvious and immediate consequences, these infections still have long-term effects on both public health and the conservation of wildlife. Currently, disease research is primarily cross-sectional, with a lack of longitudinal studies, leading to an undervaluation of the dynamic nature of disease systems. In addition to pathogen monitoring, concurrently being able to measure immune system activation will help to clarify the effects of non-lethal diseases on host health and to provide further insights into life-history trade-offs. Here, I investigated malaria parasite (Plasmodium spp.) infections, a “mild” disease, in wild habituated chimpanzees (Pan troglodytes verus) residing in Taï National Park (TNP), Côte d'Ivoire. I used historical biological samples collected from non-human primates (including chimpanzees) and humans, as well as collected mosquitoes within their habitat. First, I identified longitudinal patterns of malaria parasite prevalence detected in chimpanzee faeces; next, I validated a biomarker of immune system activation, urinary neopterin, in wild chimpanzees; and lastly, within a larger ecological framework, I examined the interface of malaria parasite transmission between humans and non-human primates sharing a habitat.
With a longitudinal study design, I found substantial intra- and inter-annual fluctuations in the faecal detection of malaria parasites across four non-consecutive sampling periods between 2004 and 2015. Peaks were observed during wet seasons—suggesting that environmental factors relating to vector abundance determine infection patterns. A higher prevalence was also detected in younger individuals, suggesting that the availability of susceptible hosts plays a role. With variations in parasite detection, similar trends should also be observed in health status. Urinary neopterin, an early inflammation marker of the non-specific immune response, increases during malaria parasite infections in humans and has been
validated as a marker of immune system activation in laboratory and captive non-human primates. However, it was unclear whether it would be sensitive enough to provide a clear signal in mild diseases against the back-drop of co-infections commonly seen in wildlife. Therefore, we first needed to validate urinary neopterin as a biomarker of immune system activation during severe disease in wild animals. I measured urinary neopterin before, during, and after a severe respiratory outbreak and showed that levels corresponded to respiratory symptoms and predicted mortality. While urinary neopterin is sensitive enough to detect changes in immune system activation during severe disease, future research should still aim to validate its use in mild diseases, such as malaria. Finally, human-to-animal disease transmission is known to occur in TNP, with direct declines in chimpanzee populations observed that resulted from several outbreaks caused by human respiratory diseases. Given the zoonotic origin of malaria parasites in humans, I examined the genetic diversity of malaria parasites infecting humans and non-human primates sharing a habitat. Mosquitoes were also captured to identify potential vectors that may bridge transmission between host species. Only P. malariae was found in both humans and chimpanzees—however, the directionality of cross-species transmission would require a larger sample size to correctly assess. Additionally, no anopheline mosquitoes, the only known vector of mammalian malaria parasites, or mosquitoes positive for human- or great ape-specific malaria parasites were captured—suggesting that transmission events may be rare due to the sparsity of vectors in this region.
This thesis shows that malaria epidemiology is a temporally and spatially diverse system that requires the use of longitudinal datasets and diverse sampling schemes. This thesis provides a baseline of data on which future malaria parasite research can build. Additionally, the validation of urinary neopterin will allow researchers to pursue questions on how mild diseases affect host health and to investigate questions relating to strategies and variations in life history trade-offs. This thesis is relevant for research on wildlife disease ecology, eco-immunology, and in the creation of pathogen and health surveillance programs.

Identiferoai:union.ndltd.org:DRESDEN/oai:qucosa:de:qucosa:36152
Date15 November 2019
CreatorsWu, Doris
ContributorsUniversität Leipzig
Source SetsHochschulschriftenserver (HSSS) der SLUB Dresden
LanguageEnglish
Detected LanguageEnglish
Typeinfo:eu-repo/semantics/acceptedVersion, doc-type:doctoralThesis, info:eu-repo/semantics/doctoralThesis, doc-type:Text
Rightsinfo:eu-repo/semantics/openAccess

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