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      Global change, parasite transmission and disease control: lessons from ecology

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          Abstract

          Parasitic infections are ubiquitous in wildlife, livestock and human populations, and healthy ecosystems are often parasite rich. Yet, their negative impacts can be extreme. Understanding how both anticipated and cryptic changes in a system might affect parasite transmission at an individual, local and global level is critical for sustainable control in humans and livestock. Here we highlight and synthesize evidence regarding potential effects of ‘system changes’ (both climatic and anthropogenic) on parasite transmission from wild host–parasite systems. Such information could inform more efficient and sustainable parasite control programmes in domestic animals or humans. Many examples from diverse terrestrial and aquatic natural systems show how abiotic and biotic factors affected by system changes can interact additively, multiplicatively or antagonistically to influence parasite transmission, including through altered habitat structure, biodiversity, host demographics and evolution. Despite this, few studies of managed systems explicitly consider these higher-order interactions, or the subsequent effects of parasite evolution, which can conceal or exaggerate measured impacts of control actions. We call for a more integrated approach to investigating transmission dynamics, which recognizes these complexities and makes use of new technologies for data capture and monitoring, and to support robust predictions of altered parasite dynamics in a rapidly changing world.

          This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

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          Most cited references212

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          Ecological and Evolutionary Responses to Recent Climate Change

          Ecological changes in the phenology and distribution of plants and animals are occurring in all well-studied marine, freshwater, and terrestrial groups. These observed changes are heavily biased in the directions predicted from global warming and have been linked to local or regional climate change through correlations between climate and biological variation, field and laboratory experiments, and physiological research. Range-restricted species, particularly polar and mountaintop species, show severe range contractions and have been the first groups in which entire species have gone extinct due to recent climate change. Tropical coral reefs and amphibians have been most negatively affected. Predator-prey and plant-insect interactions have been disrupted when interacting species have responded differently to warming. Evolutionary adaptations to warmer conditions have occurred in the interiors of species' ranges, and resource use and dispersal have evolved rapidly at expanding range margins. Observed genetic shifts modulate local effects of climate change, but there is little evidence that they will mitigate negative effects at the species level.
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            Tropical deforestation and habitat fragmentation in the Amazon: satellite data from 1978 to 1988.

            Landsat satellite imagery covering the entire forested portion of the Brazilian Amazon Basin was used to measure, for 1978 and 1988, deforestation, fragmented forest, defined as areas less than 100 square kilometers surrounded by deforestation, and edge effects of 1 kilometer into forest from adjacent areas of deforestation. Tropical deforestation increased from 78,000 square kilometers in 1978 to 230,000 square kilometers in 1988 while tropical forest habitat, severely affected with respect to biological diversity, increased from 208,000 to 588,000 square kilometers. Although this rate of deforestation is lower than previous estimates, the effect on biological diversity is greater.
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              The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk.

              The extent to which the biodiversity and community composition of ecosystems affect their functions is an issue that grows ever more compelling as human impacts on ecosystems increase. We present evidence that supports a novel function of vertebrate biodiversity, the buffering of human risk of exposure to Lyme-disease-bearing ticks. We tested the Dilution Effect model, which predicts that high species diversity in the community of tick hosts reduces vector infection prevalence by diluting the effects of the most competent disease reservoir, the ubiquitous white-footed mouse (Peromyscus leucopus). As habitats are degraded by fragmentation or other anthropogenic forces, some members of the host community disappear. Thus, species-poor communities tend to have mice, but few other hosts, whereas species-rich communities have mice, plus many other potential hosts. We demonstrate that the most common nonmouse hosts are relatively poor reservoirs for the Lyme spirochete and should reduce the prevalence of the disease by feeding, but rarely infecting, ticks. By accounting for nearly every host species' contribution to the number of larval ticks fed and infected, we show that as new host species are added to a depauperate community, the nymphal infection prevalence, a key risk factor, declines. We identify important "dilution hosts" (e.g., squirrels), characterized by high tick burdens, low reservoir competence, and high population density, as well as "rescue hosts" (e.g., shrews), which are capable of maintaining high disease risk when mouse density is low. Our study suggests that the preservation of vertebrate biodiversity and community composition can reduce the incidence of Lyme disease.
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                Author and article information

                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos. Trans. R. Soc. Lond., B, Biol. Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                5 May 2017
                13 March 2017
                13 March 2017
                : 372
                : 1719 , Theme issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’ compiled and edited by Joanne Lello and Andy Fenton
                : 20160088
                Affiliations
                [1 ]School of Biosciences, Cardiff University , Cardiff CF10 3AX, UK
                [2 ]Department of Neuroscience, Psychology and Behaviour, University of Leicester , Leicester LE1 7RH, UK
                [3 ]The James Hutton Institute , Invergowrie, Dundee DD2 5DA, UK
                [4 ]School of Veterinary Sciences, University of Bristol , Bristol BS40 5DU, UK
                [5 ]Grantham Institute – Climate Change and the Environment, Faculty of Natural Sciences, Imperial College London , Exhibition Road, London SW7 2AZ, UK
                [6 ]Department of Biodiversity and Molecular Ecology, Centre for Research and Innovation , Fondazione Edmund Mach, Via E. Mach 1, 38010 S. Michele all'Adige, Trentino, Italy
                [7 ]School of Biology, University of Leeds , Leeds LS2 9JT, UK
                [8 ]Vector-borne Viral Diseases Programme, The Pirbright Institute , Ash Road, Pirbright, Woking GU24 0NF, UK
                [9 ]School of Medicine, Pharmacy and Health, Durham University , Durham TS17 6BH, UK
                Author notes
                Author information
                http://orcid.org/0000-0002-8510-7055
                http://orcid.org/0000-0003-3955-6674
                http://orcid.org/0000-0002-2000-2914
                Article
                rstb20160088
                10.1098/rstb.2016.0088
                5352815
                28289256
                5d564743-1969-4530-b8c1-7dfe0359ffd7
                © 2017 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 25 August 2016
                Funding
                Funded by: Welsh Government and Higher Education Funding Council for Wales through the Sêr Cymru National Research Network for Low Carbon, Energy and Environment;
                Award ID: Aquawales
                Categories
                1001
                87
                Articles
                Review Article
                Custom metadata
                May 5, 2017

                Philosophy of science
                infectious disease,climate change,sustainable control,stressors
                Philosophy of science
                infectious disease, climate change, sustainable control, stressors

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