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      Biodiversity Can Help Prevent Malaria Outbreaks in Tropical Forests

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          Abstract

          Background

          Plasmodium vivax is a widely distributed, neglected parasite that can cause malaria and death in tropical areas. It is associated with an estimated 80–300 million cases of malaria worldwide. Brazilian tropical rain forests encompass host- and vector-rich communities, in which two hypothetical mechanisms could play a role in the dynamics of malaria transmission. The first mechanism is the dilution effect caused by presence of wild warm-blooded animals, which can act as dead-end hosts to Plasmodium parasites. The second is diffuse mosquito vector competition, in which vector and non-vector mosquito species compete for blood feeding upon a defensive host. Considering that the World Health Organization Malaria Eradication Research Agenda calls for novel strategies to eliminate malaria transmission locally, we used mathematical modeling to assess those two mechanisms in a pristine tropical rain forest, where the primary vector is present but malaria is absent.

          Methodology/Principal Findings

          The Ross–Macdonald model and a biodiversity-oriented model were parameterized using newly collected data and data from the literature. The basic reproduction number ( ) estimated employing Ross–Macdonald model indicated that malaria cases occur in the study location. However, no malaria cases have been reported since 1980. In contrast, the biodiversity-oriented model corroborated the absence of malaria transmission. In addition, the diffuse competition mechanism was negatively correlated with the risk of malaria transmission, which suggests a protective effect provided by the forest ecosystem. There is a non-linear, unimodal correlation between the mechanism of dead-end transmission of parasites and the risk of malaria transmission, suggesting a protective effect only under certain circumstances (e.g., a high abundance of wild warm-blooded animals).

          Conclusions/Significance

          To achieve biological conservation and to eliminate Plasmodium parasites in human populations, the World Health Organization Malaria Eradication Research Agenda should take biodiversity issues into consideration.

          Author Summary

          Plasmodium vivax malaria is a neglected infectious disease that can cause severe symptoms and death in tropical regions. It is associated with an estimated 80–300 million cases of malaria worldwide. Brazilian tropical rain forests are home to a rich community of animals that can participate in the dynamics of malaria transmission. In this study, we used real data and computer simulation to study two aspects of biodiversity (an increase in the abundance of wild warm-blooded animals; and an increase in the abundance of non-malarial mosquitoes) and the effects they have on malaria outbreaks. We found that both aspects can help prevent malaria outbreaks in tropical forests. We also found that a decrease in the abundance of wild warm-blooded animals can increase the population of malarial mosquitoes and thus increase the chances of malaria outbreaks. Forest conservation and malaria control are not incompatible and thus biodiversity issues should be included in the World Health Organization Malaria Eradication Research Agenda in order to achieve the desirable goals of biological conservation and maintenance of low malaria transmission.

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          Most cited references41

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          The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis

          Background This is the second in a series of three articles documenting the geographical distribution of 41 dominant vector species (DVS) of human malaria. The first paper addressed the DVS of the Americas and the third will consider those of the Asian Pacific Region. Here, the DVS of Africa, Europe and the Middle East are discussed. The continent of Africa experiences the bulk of the global malaria burden due in part to the presence of the An. gambiae complex. Anopheles gambiae is one of four DVS within the An. gambiae complex, the others being An. arabiensis and the coastal An. merus and An. melas. There are a further three, highly anthropophilic DVS in Africa, An. funestus, An. moucheti and An. nili. Conversely, across Europe and the Middle East, malaria transmission is low and frequently absent, despite the presence of six DVS. To help control malaria in Africa and the Middle East, or to identify the risk of its re-emergence in Europe, the contemporary distribution and bionomics of the relevant DVS are needed. Results A contemporary database of occurrence data, compiled from the formal literature and other relevant resources, resulted in the collation of information for seven DVS from 44 countries in Africa containing 4234 geo-referenced, independent sites. In Europe and the Middle East, six DVS were identified from 2784 geo-referenced sites across 49 countries. These occurrence data were combined with expert opinion ranges and a suite of environmental and climatic variables of relevance to anopheline ecology to produce predictive distribution maps using the Boosted Regression Tree (BRT) method. Conclusions The predicted geographic extent for the following DVS (or species/suspected species complex*) is provided for Africa: Anopheles (Cellia) arabiensis, An. (Cel.) funestus*, An. (Cel.) gambiae, An. (Cel.) melas, An. (Cel.) merus, An. (Cel.) moucheti and An. (Cel.) nili*, and in the European and Middle Eastern Region: An. (Anopheles) atroparvus, An. (Ano.) labranchiae, An. (Ano.) messeae, An. (Ano.) sacharovi, An. (Cel.) sergentii and An. (Cel.) superpictus*. These maps are presented alongside a bionomics summary for each species relevant to its control.
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            Impacts of biodiversity on the emergence and transmission of infectious diseases

            Biodiversity is good for you Changes in biodiversity have the potential to either increase or reduce the incidence of infectious disease in plants and animals — including humans — because they involve interactions among species. At a minimum, this requires a host and a pathogen; often many more species are involved, including additional hosts, vectors and other organisms with which these species interact. Felicia Keesing and colleagues review the evidence that reduced biodiversity affects the transmission of infectious diseases of humans, other animals and plants. Despite important questions still to be answered, they conclude that the evidence that biodiversity exerts a protective effect on infectious diseases is sufficiently strong to include biodiversity protection as a strategy to improve health. Supplementary information The online version of this article (doi:10.1038/nature09575) contains supplementary material, which is available to authorized users.
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              The diversity-stability debate.

              There exists little doubt that the Earth's biodiversity is declining. The Nature Conservancy, for example, has documented that one-third of the plant and animal species in the United States are now at risk of extinction. The problem is a monumental one, and forces us to consider in depth how we expect ecosystems, which ultimately are our life-support systems, to respond to reductions in diversity. This issue--commonly referred to as the diversity-stability debate--is the subject of this review, which synthesizes historical ideas with recent advances. Both theory and empirical evidence agree that we should expect declines in diversity to accelerate the simplification of ecological communities.
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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
                March 2013
                21 March 2013
                : 7
                : 3
                : e2139
                Affiliations
                [1 ]Departamento de Epidemiologia, Faculdade de Saúde Pública, Universidade de São Paulo, São Paulo, São Paulo, Brazil
                [2 ]Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, São Paulo, Brazil
                [3 ]Instituto de Física Teórica, Universidade Estadual Paulista Júlio de Mesquita Filho, São Paulo, São Paulo, Brazil
                University of Notre Dame, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GZL PIKLdP RAK RMC MAMS. Performed the experiments: GZL. Analyzed the data: GZL RMC. Contributed reagents/materials/analysis tools: GZL MAMS. Wrote the paper: GZL PIKLdP RAK RMC MAMS.

                Article
                PNTD-D-12-00523
                10.1371/journal.pntd.0002139
                3605282
                23556023
                d81cb4e5-de72-451b-908a-f5f13b1cc37f
                Copyright @ 2013

                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
                : 4 May 2012
                : 12 February 2013
                Page count
                Pages: 12
                Funding
                MAMS received financial support from Fundação de Amparo à Pesquisa no Estado de São Paulo (process n. 05/53973-0). GZL is a recipient of a FAPESP postdoctoral fellowship n. 2012/09939-5. RMC is a recipient of a FAPESP doctorate fellowship n. 2010/09464-1. 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
                Medicine
                Epidemiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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