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      Bottom‐up effects of fungicides on tadpoles of the European common frog ( Rana temporaria)

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          Abstract

          Biodiversity is under pressure worldwide, with amphibians being particularly threatened. Stressors related to human activity, such as chemicals, are contributing to this decline. It remains, however, unclear whether chemicals exhibiting a fungicidal activity could indirectly affect tadpoles that depend on microbially conditioned leaf litter as food source. The indirect effect of fungicides (sum concentration of a fungicide mixture composed of azoxystrobin, carbendazim, cyprodinil, quinoxyfen, and tebuconazole: 100 µg/L) on tadpoles was assessed relative to leaf litter colonized by microbes in absence of fungicides (control) and a worst‐case scenario, that is leached leaf litter without microbial colonization. The quality of leaf litter as food for tadpoles of the European common frog ( Rana temporaria) was characterized through neutral lipid fatty acid profiles and microbial sum parameters and verified by sublethal responses in tadpoles (i.e., feeding rate, feces production, growth, and fatty acid composition). Fungicides changed the nutritious quality of leaf litter likely through alterations in leaves’ neutral lipid fatty acid profiles (i.e., changes in some physiologically important highly unsaturated fatty acids reached more than 200%) in combination with a potential adsorption onto leaves during conditioning. These changes were reflected by differences in the development of tadpoles ultimately resulting in an earlier start of metamorphosis. Our data provide a first indication that fungicides potentially affect tadpole development indirectly through bottom‐up effects. This pathway is so far not addressed in fungicide environmental risk assessment and merits further attention.

          Abstract

          Tadpoles consuming leaf litter of different quality show changes in their energy reserves, more specifically the composition of fatty acids, and growth dynamics. Low‐quality food ultimately leads to a higher number of individuals entering metamorphosis.

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          Global biodiversity: indicators of recent declines.

          In 2002, world leaders committed, through the Convention on Biological Diversity, to achieve a significant reduction in the rate of biodiversity loss by 2010. We compiled 31 indicators to report on progress toward this target. Most indicators of the state of biodiversity (covering species' population trends, extinction risk, habitat extent and condition, and community composition) showed declines, with no significant recent reductions in rate, whereas indicators of pressures on biodiversity (including resource consumption, invasive alien species, nitrogen pollution, overexploitation, and climate change impacts) showed increases. Despite some local successes and increasing responses (including extent and biodiversity coverage of protected areas, sustainable forest management, policy responses to invasive alien species, and biodiversity-related aid), the rate of biodiversity loss does not appear to be slowing.
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            Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity

            Anthropogenic trade and development have broken down dispersal barriers, facilitating the spread of diseases that threaten Earth’s biodiversity. We present a global, quantitative assessment of the amphibian chytridiomycosis panzootic, one of the most impactful examples of disease spread, and demonstrate its role in the decline of at least 501 amphibian species over the past half-century, including 90 presumed extinctions. The effects of chytridiomycosis have been greatest in large-bodied, range-restricted anurans in wet climates in the Americas and Australia. Declines peaked in the 1980s, and only 12% of declined species show signs of recovery, whereas 39% are experiencing ongoing decline. There is risk of further chytridiomycosis outbreaks in new areas. The chytridiomycosis panzootic represents the greatest recorded loss of biodiversity attributable to a disease.
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                Author and article information

                Contributors
                bundschuh@uni-landau.de
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                21 March 2021
                May 2021
                : 11
                : 9 ( doiID: 10.1002/ece3.v11.9 )
                : 4353-4365
                Affiliations
                [ 1 ] iES Landau Institute for Environmental Sciences University of Koblenz‐Landau Landau Germany
                [ 2 ] Department of Aquatic Sciences and Assessment Swedish University of Agricultural Sciences Uppsala Sweden
                [ 3 ] Eusserthal Ecosystem Research Station University of Koblenz‐Landau Landau Germany
                [ 4 ]Present address: UFZ Department of Ecological Chemistry Helmholtz Centre for Environmental Research Leipzig Germany
                Author notes
                [*] [* ] Correspondence

                Mirco Bundschuh, iES Landau, Institute for Environmental Sciences, University of Koblenz‐Landau, Fortstraße 7, D‐76829 Landau, Germany.

                Email: bundschuh@ 123456uni-landau.de

                Author information
                https://orcid.org/0000-0003-4876-220X
                Article
                ECE37332
                10.1002/ece3.7332
                8093721
                c731e2fc-036c-49bf-b3cb-19346a535194
                © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 January 2021
                : 21 August 2020
                : 03 February 2021
                Page count
                Figures: 7, Tables: 2, Pages: 13, Words: 9074
                Funding
                Funded by: DFG , open-funder-registry 10.13039/501100001659;
                Award ID: 326210499/GRK2360
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                May 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.2 mode:remove_FC converted:04.05.2021

                Evolutionary Biology
                fatty acid composition,food quality,fungicides,metamorphosis,tadpoles
                Evolutionary Biology
                fatty acid composition, food quality, fungicides, metamorphosis, tadpoles

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