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      Co-Infection and Wild Animal Health: Effects of Trypanosomatids and Gastrointestinal Parasites on Coatis of the Brazilian Pantanal

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          Abstract

          Wild animals are infected by diverse parasites, but how they influence host health is poorly understood. We examined the relationship of trypanosomatids and gastrointestinal parasites with health of wild brown-nosed coatis ( Nasua nasua) from the Brazilian Pantanal. We used coati body condition and hematological parameters as response variables in linear models that were compared using an information theoretic approach. Predictors were high/low parasitemias by Trypanosoma cruzi and T. evansi, and indices representing the abundance of distinct groups of gastrointestinal parasites. We also analyzed how host health changed with host sex and reproductive seasonality. Hemoparasites was best related to coati body condition and hematological indices, whereas abundance of gastrointestinal parasites was relatively less associated with coati health. Additionally, some associations were best predicted by models that incorporated reproductive seasonality and host sex. Overall, we observed a lower health condition during the breeding season, when coatis are under reproductive stress and may be less able to handle infection. In addition, females seem to handle infection better than males. Body condition was lower in coatis with high parasitemias of T. evansi, especially during the reproductive season. Total red blood cell counts, packed cell volume, platelets and eosinophils were also lower in animals with high T. evansi parasitemias. Total white blood cell counts and mature neutrophils were lower in animals with high parasitemias for both Trypanosoma species, with neutrophils decreasing mainly during the reproductive season. Overall, decreases in hematological parameters of females with T. evansi high parasitemias were less evident. For T. cruzi, monocytes decreased in individuals with high parasitemias. High abundances of microfilariae in the bloodstream, and cestode eggs and coccidian oocysts in feces were also associated with coati blood parameters. This study shows the potential value of examining hematological parameters as an approach to better understand the ecological relevance of parasite-host interactions.

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          Eosinophils: changing perspectives in health and disease

          Key Points Eosinophils have been traditionally perceived as terminally differentiated cytotoxic effector cells. Recent studies have provided a more sophisticated understanding of eosinophil effector functions and a more nuanced view of their contributions to the pathogenesis of various diseases, including asthma and respiratory allergies, eosinophilic gastrointestinal diseases, hypereosinophilic syndromes and parasitic infection. Eosinophils are granulocytes that develop in the bone marrow from pluripotent progenitors in response to cytokines, such as interleukin-5 (IL-5), IL-3 and granulocyte–macrophage colony-stimulating factor (GM-CSF). Mature eosinophils are released into the peripheral blood and enter tissues in response to cooperative signalling between IL-5 and eotaxin family chemokines. Eosinophils in peripheral blood and tissues are uniquely identified by their bilobed nuclei, their large specific granules that store cytokines, cationic proteins and enzymes, and their expression of the IL-5 receptor and CC-chemokine receptor 3 (CCR3). In addition, the receptors sialic acid-binding immunoglobulin-like lectin 8 (SIGLEC-8) and SIGLEC-F are expressed by human and mouse eosinophils, respectively. IL-5 has a central and profound role in all aspects of eosinophil development, activation and survival. IL-5 is produced by T helper 2 (TH2) cells, and more recently the contributions of the epithelium-derived innate cytokines thymic stromal lymphopoietin (TSLP), IL-25 and IL-33 in promoting eosinophilia via the induction of IL-5 have also been recognized. Although eosinophil responses are influenced by cytokines produced by T cells, eosinophils in turn modulate the functions of B and T cells. Eosinophils also communicate with a range of innate immune cells (such as mast cells, dendritic cells, macrophages and neutrophils). Eosinophils serve to bridge innate and adaptive immunity by regulating the production of chemoattractants and cytokines (including CC-chemokine ligand 17 (CCL17), CCL22, a proliferation-inducing ligand (APRIL) and IL-6) and via antigen presentation. Both successful and unsuccessful attempts to target eosinophils have yielded remarkable insights into their contribution to disease pathogenesis. Many eosinophil-associated inflammatory conditions have been shown to be heterogeneous in nature. As such, successful therapeutic strategies will depend on the correlation of disease activity with dysregulated eosinophil function as well as the identification of the crucial molecules that regulate eosinophil accumulation in the affected tissues. Supplementary information The online version of this article (doi:10.1038/nri3341) contains supplementary material, which is available to authorized users.
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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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              Sex differences in parasite infections: patterns and processes.

              M Zuk (1996)
              Sex differences in parasite infection rates, intensities, or population patterns are common in a wide range of taxa. These differences are usually attributed to 1 of 2 causes: (1) ecological (sociological in humans); and (2) physiological, usually hormonal in origin. Examples of the first cause include differential exposure to pathogens because of sex-specific behavior or morphology. The second cause may stem from the well-documented association between testosterone and the immune system; sexually mature male vertebrates are often more susceptible to infection and carry higher parasite burdens in the field. Although many researchers favor one explanation over the other, the requisite controlled experiments to rule out confounding variables are often neglected. We suggest that sex differences in disease have evolved just as sex differences in morphology and behavior, and are the result of selection acting differently on males and females. Research has often focused on proximate mechanistic explanations for the sex difference in infection rates, but it is equally important to understand the generality of the patterns in an evolutionary context. Because males potentially gain more than females by taking risks and engaging in competition, sexual selection pressure has shaped male behavior and appearance to maximize competitive ability and attractiveness. Many of the classic male attributes such as antlers on deer are testosterone-dependent, putting males in what appears to be a cruel bind: become vulnerable to disease by developing an attractive secondary sexual ornament, or risk lowered mating success by reducing it. A variety of hypotheses have been put forward to explain why males have not circumvented this dilemma. The mating system of the host species will influence the likelihood of sex differences in parasite infection, because males in monogamous species are subject to weaker sexual selection than males in polygynous species. Whether these evolutionary generalizations apply to invertebrates, which lack testosterone, remains to be seen.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                14 December 2015
                2015
                : 10
                : 12
                : e0143997
                Affiliations
                [1 ]Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Rio de Janeiro, Brazil
                [2 ]Laboratório de Biologia de Tripanosomatídeos, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Janeiro, Rio de Janeiro, Brazil
                [3 ]Laboratório de Parasitologia Animal, Universidade Católica Dom Bosco, Campo Grande, Mato Grosso do Sul, Brazil
                [4 ]Departamento de Biologia Aplicada à Agropecuária, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Jaboticabal, São Paulo, Brazil
                [5 ]Laboratório de Vida Selvagem, Centro de Pesquisa Agropecuária do Pantanal, Empresa Brasileira de Pesquisa Agropecuária, Mato Grosso do Sul, Corumbá, Brazil
                [6 ]Department of Fisheries and Wildlife Sciences, University of Missouri, Columbia, Missouri, Unites States of America
                Universidad Nacional Autonoma de Mexico, MEXICO
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NO AMJ HMH RCB PSD GMM MEG. Performed the experiments: NO RCB. Analyzed the data: NO RCB MEG. Contributed reagents/materials/analysis tools: AMJ HMH PSD GMM MEG. Wrote the paper: NO AMJ HMH RCB PSD MEG.

                Article
                PONE-D-14-52924
                10.1371/journal.pone.0143997
                4678147
                26657699
                071d60cd-af8e-4a42-8ef9-1ebc5c8bd7b0
                © 2015 Olifiers et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 8 January 2015
                : 12 November 2015
                Page count
                Figures: 2, Tables: 3, Pages: 19
                Funding
                Funds were provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (process number 484501/2006-2) to GMM, NO, AMJ, HMH, RCB, PSD; Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (process number 6654.235.476.06032007) to GMM, NO, AMJ, HMH, RCB, PSD; Empresa Brasileira de Estudos Agropecuários (Macroprograma 3) to GMM, NO, AMJ, HMH, RCB, PSD; Fundação Oswaldo Cruz to AMJ e PSD; University of Missouri to MEG; and Earthwatch Institute to NO, AMJ, HMH and PSD. Doctoral grants were provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to RCB and by the University of Missouri to NO. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article
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                All relevant data are available via Figshare ( http://dx.doi.org/10.6084/m9.figshare.1613286).

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