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      Fungicides: An Overlooked Pesticide Class?

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          Abstract

          Fungicides are indispensable to global food security and their use is forecasted to intensify. Fungicides can reach aquatic ecosystems and occur in surface water bodies in agricultural catchments throughout the entire growing season due to their frequent, prophylactic application. However, in comparison to herbicides and insecticides, the exposure to and effects of fungicides have received less attention. We provide an overview of the risk of fungicides to aquatic ecosystems covering fungicide exposure (i.e., environmental fate, exposure modeling, and mitigation measures) as well as direct and indirect effects of fungicides on microorganisms, macrophytes, invertebrates, and vertebrates. We show that fungicides occur widely in aquatic systems, that the accuracy of predicted environmental concentrations is debatable, and that fungicide exposure can be effectively mitigated. We additionally demonstrate that fungicides can be highly toxic to a broad range of organisms and can pose a risk to aquatic biota. Finally, we outline central research gaps that currently challenge our ability to predict fungicide exposure and effects, promising research avenues, and shortcomings of the current environmental risk assessment for fungicides.

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          Most cited references189

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          Plant disease: a threat to global food security.

          A vast number of plant pathogens from viroids of a few hundred nucleotides to higher plants cause diseases in our crops. Their effects range from mild symptoms to catastrophes in which large areas planted to food crops are destroyed. Catastrophic plant disease exacerbates the current deficit of food supply in which at least 800 million people are inadequately fed. Plant pathogens are difficult to control because their populations are variable in time, space, and genotype. Most insidiously, they evolve, often overcoming the resistance that may have been the hard-won achievement of the plant breeder. In order to combat the losses they cause, it is necessary to define the problem and seek remedies. At the biological level, the requirements are for the speedy and accurate identification of the causal organism, accurate estimates of the severity of disease and its effect on yield, and identification of its virulence mechanisms. Disease may then be minimized by the reduction of the pathogen's inoculum, inhibition of its virulence mechanisms, and promotion of genetic diversity in the crop. Conventional plant breeding for resistance has an important role to play that can now be facilitated by marker-assisted selection. There is also a role for transgenic modification with genes that confer resistance. At the political level, there is a need to acknowledge that plant diseases threaten our food supplies and to devote adequate resources to their control.
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            Environmental fate and exposure; neonicotinoids and fipronil

            Systemic insecticides are applied to plants using a wide variety of methods, ranging from foliar sprays to seed treatments and soil drenches. Neonicotinoids and fipronil are among the most widely used pesticides in the world. Their popularity is largely due to their high toxicity to invertebrates, the ease and flexibility with which they can be applied, their long persistence, and their systemic nature, which ensures that they spread to all parts of the target crop. However, these properties also increase the probability of environmental contamination and exposure of nontarget organisms. Environmental contamination occurs via a number of routes including dust generated during drilling of dressed seeds, contamination and accumulation in arable soils and soil water, runoff into waterways, and uptake of pesticides by nontarget plants via their roots or dust deposition on leaves. Persistence in soils, waterways, and nontarget plants is variable but can be prolonged; for example, the half-lives of neonicotinoids in soils can exceed 1,000 days, so they can accumulate when used repeatedly. Similarly, they can persist in woody plants for periods exceeding 1 year. Breakdown results in toxic metabolites, though concentrations of these in the environment are rarely measured. Overall, there is strong evidence that soils, waterways, and plants in agricultural environments and neighboring areas are contaminated with variable levels of neonicotinoids or fipronil mixtures and their metabolites (soil, parts per billion (ppb)-parts per million (ppm) range; water, parts per trillion (ppt)-ppb range; and plants, ppb-ppm range). This provides multiple routes for chronic (and acute in some cases) exposure of nontarget animals. For example, pollinators are exposed through direct contact with dust during drilling; consumption of pollen, nectar, or guttation drops from seed-treated crops, water, and consumption of contaminated pollen and nectar from wild flowers and trees growing near-treated crops. Studies of food stores in honeybee colonies from across the globe demonstrate that colonies are routinely and chronically exposed to neonicotinoids, fipronil, and their metabolites (generally in the 1–100 ppb range), mixed with other pesticides some of which are known to act synergistically with neonicotinoids. Other nontarget organisms, particularly those inhabiting soils, aquatic habitats, or herbivorous insects feeding on noncrop plants in farmland, will also inevitably receive exposure, although data are generally lacking for these groups. We summarize the current state of knowledge regarding the environmental fate of these compounds by outlining what is known about the chemical properties of these compounds, and placing these properties in the context of modern agricultural practices.
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              Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond?

              During the past 50 years, the human population has more than doubled and global agricultural production has similarly risen. However, the productive arable area has increased by just 10%; thus the increased use of pesticides has been a consequence of the demands of human population growth, and its impact has reached global significance. Although we often know a pesticide's mode of action in the target species, we still largely do not understand the full impact of unintended side effects on wildlife, particularly at higher levels of biological organization: populations, communities, and ecosystems. In these times of regional and global species declines, we are challenged with the task of causally linking knowledge about the molecular actions of pesticides to their possible interference with biological processes, in order to develop reliable predictions about the consequences of pesticide use, and misuse, in a rapidly changing world.
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                Author and article information

                Journal
                Environ Sci Technol
                Environ. Sci. Technol
                es
                esthag
                Environmental Science & Technology
                American Chemical Society
                0013-936X
                1520-5851
                05 March 2019
                02 April 2019
                05 March 2020
                : 53
                : 7
                : 3347-3365
                Affiliations
                []Institute for Environmental Sciences, University of Koblenz-Landau , Fortstraße 7, D-76829 Landau, Germany
                []Eußerthal Ecosystem Research Station, University of Koblenz-Landau , Birkenthalstraße 13, D-76857 Eußerthal, Germany
                [§ ]Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences , Lennart Hjelms väg 9, SWE-75007 Uppsala, Sweden
                []Wageningen Environmental Research, Wageningen University and Research , Wageningen, The Netherlands
                []Laboratoire d’Hydrologie et de Géochimie de Strasbourg (LHyGeS) , Université de Strasbourg/ENGEES, CNRS, 1 rue Blessig, 67084 Strasbourg Cedex, France
                [# ]Aarhus University , Dept. of Bioscience, Vejlsoevej 25, 8600 Silkeborg, Denmark
                []University of South Florida , Department of Integrative Biology, Tampa, Florida, United States
                [Δ ]Department of Biological Sciences, Environmental Change Initiative, and Eck Institute for Global Health, University of Notre Dame , Notre Dame, Indiana, United States
                []U.S. Geological Survey , New Jersey Water Science Center, Lawrenceville, New Jersey, United States
                Author notes
                [* ]Phone: (+49) 6341 280 31361; fax: (+49) 6341 280 31326; e-mail: zubrod@ 123456uni-landau.de .
                Article
                10.1021/acs.est.8b04392
                6536136
                30835448
                d1deb50d-22a3-4cf8-b288-663a69422784
                Copyright © 2019 American Chemical Society

                This is an open access article published under an ACS AuthorChoice License, which permits copying and redistribution of the article or any adaptations for non-commercial purposes.

                History
                : 07 August 2018
                : 05 March 2019
                : 14 December 2018
                Categories
                Critical Review
                Custom metadata
                es8b04392
                es-2018-04392f

                General environmental science
                General environmental science

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