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      Land use-induced spillover: a call to action to safeguard environmental, animal, and human health

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          Abstract

          The rapid global spread and human health impacts of SARS-CoV-2, the virus that causes COVID-19, show humanity's vulnerability to zoonotic disease pandemics. Although anthropogenic land use change is known to be the major driver of zoonotic pathogen spillover from wildlife to human populations, the scientific underpinnings of land use-induced zoonotic spillover have rarely been investigated from the landscape perspective. We call for interdisciplinary collaborations to advance knowledge on land use implications for zoonotic disease emergence with a view toward informing the decisions needed to protect human health. In particular, we urge a mechanistic focus on the zoonotic pathogen infect–shed–spill–spread cascade to enable protection of landscape immunity—the ecological conditions that reduce the risk of pathogen spillover from reservoir hosts—as a conservation and biosecurity priority. Results are urgently needed to formulate an integrated, holistic set of science-based policy and management measures that effectively and cost-efficiently minimise zoonotic disease risk. We consider opportunities to better institute the necessary scientific collaboration, address primary technical challenges, and advance policy and management issues that warrant particular attention to effectively address health security from local to global scales.

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          Most cited references73

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          Pathways to zoonotic spillover

          Zoonotic diseases present a substantial global health burden. In this Opinion article, Plowrightet al. present an integrative conceptual and quantitative model that reveals that all zoonotic pathogens must overcome a hierarchical series of barriers to cause spillover infections in humans. Supplementary information The online version of this article (doi:10.1038/nrmicro.2017.45) contains supplementary material, which is available to authorized users.
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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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              Zoonotic host diversity increases in human-dominated ecosystems

              Land use change-for example, the conversion of natural habitats to agricultural or urban ecosystems-is widely recognized to influence the risk and emergence of zoonotic disease in humans1,2. However, whether such changes in risk are underpinned by predictable ecological changes remains unclear. It has been suggested that habitat disturbance might cause predictable changes in the local diversity and taxonomic composition of potential reservoir hosts, owing to systematic, trait-mediated differences in species resilience to human pressures3,4. Here we analyse 6,801 ecological assemblages and 376 host species worldwide, controlling for research effort, and show that land use has global and systematic effects on local zoonotic host communities. Known wildlife hosts of human-shared pathogens and parasites overall comprise a greater proportion of local species richness (18-72% higher) and total abundance (21-144% higher) in sites under substantial human use (secondary, agricultural and urban ecosystems) compared with nearby undisturbed habitats. The magnitude of this effect varies taxonomically and is strongest for rodent, bat and passerine bird zoonotic host species, which may be one factor that underpins the global importance of these taxa as zoonotic reservoirs. We further show that mammal species that harbour more pathogens overall (either human-shared or non-human-shared) are more likely to occur in human-managed ecosystems, suggesting that these trends may be mediated by ecological or life-history traits that influence both host status and tolerance to human disturbance5,6. Our results suggest that global changes in the mode and the intensity of land use are creating expanding hazardous interfaces between people, livestock and wildlife reservoirs of zoonotic disease.
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                Author and article information

                Journal
                Lancet Planet Health
                Lancet Planet Health
                The Lancet. Planetary Health
                The Author(s). Published by Elsevier Ltd.
                2542-5196
                6 March 2021
                6 March 2021
                Affiliations
                [a ]Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA
                [b ]Center for Large Landscape Conservation, Bozeman, MT, USA
                [c ]Department of Environmental Science and Policy, George Mason University, Fairfax, VA, USA
                [d ]University of Rhode Island, Providence, RI, USA
                [e ]Yellowstone to Yukon Conservation Initiative, Canmore, AB, Canada
                [f ]IUCN, Chelsea, QC, Canada
                [g ]Department of Population Health Sciences, Global Health Institute, University of Wisconsin–Madison, Madison, WI, USA
                [h ]Department of Biology, University of Oklahoma, Norman, OK, USA
                [i ]Huck Institutes of the Life Sciences, Pennsylvania State University, State College, PA, USA
                Author notes
                [* ]Correspondence to: Dr Raina K Plowright, Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
                [†]

                Contributed equally

                Article
                S2542-5196(21)00031-0
                10.1016/S2542-5196(21)00031-0
                7935684
                33684341
                94a4d9be-7434-40f9-b193-9454871ecc16
                © 2021 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY-NC-ND 4.0 license

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

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