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      Hemoparasites in a wild primate: Infection patterns suggest interaction of Plasmodium and Babesia in a lemur species

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          Abstract

          Hemoparasites can cause serious morbidity in humans and animals and often involve wildlife reservoirs. Understanding patterns of hemoparasite infections in natural populations can therefore inform about emerging disease risks, especially in the light of climate change and human disruption of natural ecosystems. We investigated the effects of host age, sex, host group size and season on infection patterns of Plasmodium sp., Babesia sp. and filarial nematodes in a population of wild Malagasy primates, Verreaux's sifakas ( Propithecus verreauxi), as well as the effects of these infections on hematological variables. We tested 45 blood samples from 36 individuals and identified two species of Plasmodium, one species of Babesia and two species of filarial nematodes. Plasmodium spp. and Babesia sp. infections showed opposite patterns of age-dependency, with babesiosis being prevalent among young animals, while older animals were infected with Plasmodium sp. In addition, Babesia sp. infection was a statistically significant negative predictor of Plasmodium sp. infection. These results suggest that Plasmodium and Babesia parasites may interact within the host, either through cross-immunity or via resource competition, so that Plasmodium infections can only establish after babesiosis has resolved. We found no effects of host sex, host group size and season on hemoparasite infections. Infections showed high prevalences and did not influence hematological variables. This preliminary evidence supports the impression that the hosts and parasites considered in this study appear to be well-adapted to each other, resulting in persistent infections with low pathogenic and probably low zoonotic potential. Our results illustrate the crucial role of biodiversity in host-parasite relationships, specifically how within-host pathogen diversity may regulate the abundance of parasites.

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          Highlights

          • Wild primates, Verreaux's sifakas, are naturally infected with 5 hemoparasite species.

          • Plasmodium sp. and Babesia sp. infections show opposite patterns of age-dependency.

          • This suggests within-host parasite interaction via cross-immunity or competition.

          • Infection status did not influence hematology values, indicating low pathogenicity.

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          Most cited references108

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          PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference

          PHYML Online is a web interface to PHYML, a software that implements a fast and accurate heuristic for estimating maximum likelihood phylogenies from DNA and protein sequences. This tool provides the user with a number of options, e.g. nonparametric bootstrap and estimation of various evolutionary parameters, in order to perform comprehensive phylogenetic analyses on large datasets in reasonable computing time. The server and its documentation are available at .
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            Species interactions in a parasite community drive infection risk in a wildlife population.

            Most hosts, including humans, are simultaneously or sequentially infected with several parasites. A key question is whether patterns of coinfection arise because infection by one parasite species affects susceptibility to others or because of inherent differences between hosts. We used time-series data from individual hosts in natural populations to analyze patterns of infection risk for a microparasite community, detecting large positive and negative effects of other infections. Patterns remain once variations in host susceptibility and exposure are accounted for. Indeed, effects are typically of greater magnitude, and explain more variation in infection risk, than the effects associated with host and environmental factors more commonly considered in disease studies. We highlight the danger of mistaken inference when considering parasite species in isolation rather than parasite communities.
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              Emphasizing the ecology in parasite community ecology.

              In natural systems, individuals are often co-infected by many species of parasites. However, the significance of interactions between species and the processes that shape within-host parasite communities remain unclear. Studies of parasite community ecology are often descriptive, focusing on patterns of parasite abundance across host populations rather than on the mechanisms that underlie interactions within a host. These within-host interactions are crucial for determining the fitness and transmissibility of co-infecting parasite species. Here, we highlight how techniques from community ecology can be used to restructure the approaches used to study parasite communities. We discuss insights offered by this mechanistic approach that will be crucial for predicting the impact on wildlife and human health of disease control measures, climate change or novel parasite species introductions.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology: Parasites and Wildlife
                Elsevier
                2213-2244
                20 October 2015
                December 2015
                20 October 2015
                : 4
                : 3
                : 385-395
                Affiliations
                [a ]Behavioral Ecology and Sociobiology Unit, German Primate Center, Kellnerweg 4, 37077 Göttingen, Germany
                [b ]Project Group “Epidemiology of Highly Pathogenic Microorganisms”, Robert-Koch-Institut, Seestraße 10, 13353 Berlin, Germany
                [c ]Department of Sociobiology and Anthropology, University of Göttingen, Kellnerweg 6, 30077 Göttingen, Germany
                Author notes
                []Corresponding author. aspringer@ 123456dpz.eu
                Article
                S2213-2244(15)30020-1
                10.1016/j.ijppaw.2015.10.006
                4683568
                49d5387a-ca3e-4e95-a786-2cd5c0447852
                © 2015 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 22 June 2015
                : 21 August 2015
                : 16 October 2015
                Categories
                Article

                verreaux's sifakas,propithecus verreauxi,plasmodium sp.,babesia sp.,hemoparasites,cross-immunity,parasite community

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