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      Host Life History Strategy, Species Diversity, and Habitat Influence Trypanosoma cruzi Vector Infection in Changing Landscapes

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          Abstract

          Background

          Anthropogenic land use may influence transmission of multi-host vector-borne pathogens by changing diversity, relative abundance, and community composition of reservoir hosts. These reservoir hosts may have varying competence for vector-borne pathogens depending on species-specific characteristics, such as life history strategy. The objective of this study is to evaluate how anthropogenic land use change influences blood meal species composition and the effects of changing blood meal species composition on the parasite infection rate of the Chagas disease vector Rhodnius pallescens in Panama.

          Methodology/Principal Findings

          R. pallescens vectors (N = 643) were collected in different habitat types across a gradient of anthropogenic disturbance. Blood meal species in DNA extracted from these vectors was identified in 243 (40.3%) vectors by amplification and sequencing of a vertebrate-specific fragment of the 12SrRNA gene, and T. cruzi vector infection was determined by pcr. Vector infection rate was significantly greater in deforested habitats as compared to contiguous forests. Forty-two different species of blood meal were identified in R. pallescens, and species composition of blood meals varied across habitat types. Mammals (88.3%) dominated R. pallescens blood meals. Xenarthrans (sloths and tamanduas) were the most frequently identified species in blood meals across all habitat types. A regression tree analysis indicated that blood meal species diversity, host life history strategy (measured as r max , the maximum intrinsic rate of population increase), and habitat type (forest fragments and peridomiciliary sites) were important determinants of vector infection with T. cruzi. The mean intrinsic rate of increase and the skewness and variability of r max were positively associated with higher vector infection rate at a site.

          Conclusions/Significance

          In this study, anthropogenic landscape disturbance increased vector infection with T. cruzi, potentially by changing host community structure to favor hosts that are short-lived with high reproductive rates. Study results apply to potential environmental management strategies for Chagas disease.

          Author Summary

          Understanding how host species influence vector-borne pathogen transmission in anthropogenically disturbed landscapes is important to predicting and preventing disease transmission. This study evaluates how host diversity, anthropogenic land use change, and host life history influence vector- borne multihost pathogen transmission in Panama, where the triatomine bug Rhodnius pallescens is the principal vector of Trypanosoma cruzi, agent of Chagas disease. We hypothesize that blood meal species composition and vector infection differ as a function of habitat disturbance, and that the host species intrinsic rate of increase is positively associated with T. cruzi vector infection. We collected R. pallescens across a gradient of anthropogenic disturbance. Blood meal species composition and T. cruzi vector infection were determined by molecular methods. Vector infection rates were higher in deforested habitats and forest fragments as compared to contiguous forests. Vectors fed primarily on mammals, likely accounting for a relatively high vector infection prevalence, and that host blood meal species composition varied across habitat types. Regression tree analysis demonstrates that higher T. cruzi vector infection indices we associated with sites that had blood meal species with higher, more variable, and more skewed r max (intrinsic rates of increase) values, lower blood meal species diversity, and disturbed habitats, namely fragmented forests and peridomiciliary sites.

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          Most cited references52

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          The population consequences of life history phenomena.

          L. Cole (1954)
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            Machine learning methods without tears: a primer for ecologists.

            Machine learning methods, a family of statistical techniques with origins in the field of artificial intelligence, are recognized as holding great promise for the advancement of understanding and prediction about ecological phenomena. These modeling techniques are flexible enough to handle complex problems with multiple interacting elements and typically outcompete traditional approaches (e.g., generalized linear models), making them ideal for modeling ecological systems. Despite their inherent advantages, a review of the literature reveals only a modest use of these approaches in ecology as compared to other disciplines. One potential explanation for this lack of interest is that machine learning techniques do not fall neatly into the class of statistical modeling approaches with which most ecologists are familiar. In this paper, we provide an introduction to three machine learning approaches that can be broadly used by ecologists: classification and regression trees, artificial neural networks, and evolutionary computation. For each approach, we provide a brief background to the methodology, give examples of its application in ecology, describe model development and implementation, discuss strengths and weaknesses, explore the availability of statistical software, and provide an illustrative example. Although the ecological application of machine learning approaches has increased, there remains considerable skepticism with respect to the role of these techniques in ecology. Our review encourages a greater understanding of machin learning approaches and promotes their future application and utilization, while also providing a basis from which ecologists can make informed decisions about whether to select or avoid these approaches in their future modeling endeavors.
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              Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk.

              Parasite infections often lead to dramatically different outcomes among host species. Although an emerging body of ecoimmunological research proposes that hosts experience a fundamental trade-off between pathogen defences and life-history activities, this line of inquiry has rarely been extended to the most essential outcomes of host-pathogen interactions: namely, infection and disease pathology. Using a comparative experimental approach involving 13 amphibian host species and a virulent parasite, we test the hypothesis that 'pace-of-life' predicts parasite infection and host pathology. Trematode exposure increased mortality and malformations in nine host species. After accounting for evolutionary history, species that developed quickly and metamorphosed smaller ('fast-species') were particularly prone to infection and pathology. This pattern likely resulted from both weaker host defences and greater adaptation by parasites to infect common hosts. Broader integration between life history theory and disease ecology can aid in identifying both reservoir hosts and species at risk of disease-driven declines. © 2012 Blackwell Publishing Ltd/CNRS.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                November 2012
                15 November 2012
                : 6
                : 11
                : e1884
                Affiliations
                [1 ]Department of Veterinary Pathology, University of Georgia College of Veterinary Medicine, Athens, Georgia, United States of America
                [2 ]Graduate School of Environmental Sciences and Global Center of Excellence Program on Integrated Field Environmental Science, Hokkaido University, Sapporo, Japan
                [3 ]Programa de Investigación en Enfermedades Tropicales, Escuela de Medicina Veterinaria, Universidad Nacional, Heredia, Costa Rica
                [4 ]Departamento de Parasitología, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panama City, Panama
                [5 ]Odum School of Ecology, The University of Georgia, Athens, Georgia, United States of America
                Universidad de Buenos Aires, Argentina
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NLG CRC JEC AS. Performed the experiments: NLG JEC AS. Analyzed the data: NLG LFC. Contributed reagents/materials/analysis tools: NLG JEC AS LFC. Wrote the paper: NLG LFC.

                Article
                PNTD-D-12-00485
                10.1371/journal.pntd.0001884
                3499412
                23166846
                d629a6d6-cef3-49a7-b954-bf9a4e778632
                Copyright @ 2012

                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
                : 20 April 2012
                : 14 September 2012
                Page count
                Pages: 11
                Funding
                This study was supported by Environmental Protection Agency Science to Achieve Results (STAR) Fellowship FP-91669001, Sigma Xi Scientific Research Grant G200803150739, a University of Georgia Graduate School Dissertation Completion Award, a Dean A. Lindholm Memorial Travel Award, and a University of Georgia Center for Latin American Studies Scholarship. Scholarship support was also provided by the Wildlife Disease Association. Funding was provided to LFC by the Japan Society for the Promotion of Science. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Evolutionary Ecology
                Terrestrial Ecology
                Microbiology
                Vector Biology
                Medicine
                Infectious Diseases
                Neglected Tropical Diseases
                Chagas Disease
                Parasitic Diseases
                Chagas Disease
                Vectors and Hosts
                Veterinary Science
                Veterinary Diseases
                Zoonotic Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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