Antibiotic and pesticide susceptibility and the Anthropocene operating space

Rising levels of antimicrobial and pesticide resistance increasingly undermine human health and systems for biomass production, and emphasize the sustainability challenge of preserving organisms susceptible to these biocides. In this Review, we introduce key concepts and examine dynamics of biocide susceptibility that must be governed to address this challenge. We focus on the impact of biocides on the capacity of susceptible organisms to prevent spread of resistance, and we then review how biocide use affects a broader suite of ecosystem services. Finally, we introduce and assess the state of what we term the Anthropocene operating space of biocide susceptibility, a framework for assessing the potential of antibiotic and pesticide resistance to undermine key functions of human society. Based on current trends in antibiotic, insecticide and herbicide resistance, we conclude that the states of all six assessed variables are beyond safe zones, with three variables surpassed regionally or globally.

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Fig. 1: Niche construction of the Anthropocene operating space of biocide susceptibility.
Fig. 2: Resilience of biocide-susceptible organisms.
Fig. 3: Intercontinental spread of non-native plants, agricultural insect pests and antibiotic resistance genes.
Fig. 4: The ecosystem consequences of biocide use.
Fig. 5: State of the Anthropocene operating space of biocide susceptibility.

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Acknowledgements

This is a product of the Living with Resistance project supported by the National Socio-Environmental Synthesis Center (SESYNC) under funding received from the National Science Foundation DBI-1639145 and led by P.S.J. and S.P.C. We thank everyone who contributed to the four project meetings in 2016 and 2017. P.S.J. acknowledges funding from the Carlsberg foundation CF14-1050 and CF15-0988, FORMAS 2016-00451 and the Erling-Persson Family programme.

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P.S.J. conceived the manuscript on the basis of four workshops where all authors contributed in person or virtually. P.S.J. wrote the first draft of the manuscript with primary contributions from Y.C., S.D., R.R.D., G.E., G.L., H.M.S. and D.W. P.S.J., Y.C., E.Y.K., D.W. and D.J. performed the assessment of the Anthropocene operating space. P.S.J. and F.K. designed the figures. M.S. and P.S.J. conceived the feedback loops of Fig. 4. All authors commented on and contributed to the writing of the manuscript.

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DowDuPont and Monsanto did not provide funding to support this work, but may be affected by the publication of this paper and have funded other work by Y.C. All other authors have no competing interests.

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Jørgensen, P.S., Aktipis, A., Brown, Z. et al. Antibiotic and pesticide susceptibility and the Anthropocene operating space. Nat Sustain 1, 632–641 (2018). https://doi.org/10.1038/s41893-018-0164-3

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