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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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References

  1. Ellis, E. C. Ecology in an anthropogenic biosphere. Ecol. Monogr. 85, 287–331 (2015).

    Google Scholar 

  2. Carroll, S. P. et al. Applying evolutionary biology to address global challenges. Science 346, 1245993 (2014).

    Google Scholar 

  3. Palumbi, S. R. Humans as the world’s greatest evolutionary force. Science 293, 1786–1790 (2001).

    CAS  Google Scholar 

  4. Millennium Ecosystem Assessment. Ecosystems and Human Well-being: Synthesis (Island, Washington DC, 2005).

    Google Scholar 

  5. Jørgensen, P. S., Wernli, D., Folke, C. & Carroll, S. P. Changing antibiotic resistance: sustainability transformation to a pro-microbial planet. Curr. Opin. Environ. Sustain 25, 66–76 (2017).

    Google Scholar 

  6. Wernli, D. et al. Mapping global policy discourse on antimicrobial resistance. BMJ Glob. Health 2, e000378 (2017).

    Google Scholar 

  7. Polasky, S., Carpenter, S. R., Folke, C. & Keeler, B. Decision-making under great uncertainty: environmental management in an era of global change. Trends Ecol. Evol. 26, 398–404 (2011).

    Google Scholar 

  8. IPBES/5/Inf/24: Update on the Classification of Nature’s Contributions to People by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES, 2017).

  9. Zhang, W., Ricketts, T. H., Kremen, C., Carney, K. & Swinton, S. M. Ecosystem services and dis-services to agriculture. Ecol. Econ. 64, 253–260 (2007).

    Google Scholar 

  10. Fisher, B., Costanza, R., Kerry, T. & Morling, P. Defining and Classifying Ecosystem Services for Decision Making CSERGE Working Paper EDM 07-04 (CSERGE, 2007).

  11. Saunders, M. E. Ecosystem services in agriculture: understanding the multifunctional role of invertebrates. Agric. For. Entomol. 20, 298–300 (2018).

    Google Scholar 

  12. Saunders, M. E., Peisley, R. K., Rader, R. & Luck, G. W. Pollinators, pests, and predators: recognizing ecological trade-offs in agroecosystems. Ambio 45, 4–14 (2016).

    Google Scholar 

  13. Saunders, M. E. & Luck, G. W. Limitations of the ecosystem services versus disservices dichotomy. Conserv. Biol. 30, 1363–1365 (2016).

    Google Scholar 

  14. Lynch, S. V. & Pedersen, O. The human intestinal microbiome in health and disease. N. Engl. J. Med. 375, 2369–2379 (2016).

    CAS  Google Scholar 

  15. Díaz, S. et al. The IPBES Conceptual Framework—connecting nature and people. Curr. Opin. Environ. Sustain 14, 1–16 (2015).

    Google Scholar 

  16. Daulaire, N., Bang, A., Tomson, G., Kalyango, J. N. & Cars, O. Universal access to effective antibiotics is essential for tackling antibiotic resistance. J. Law Med. Ethics 43, 17–21 (2015).

    Google Scholar 

  17. Creanza, N., Kolodny, O. & Feldman, M. W. Cultural evolutionary theory: how culture evolves and why it matters. Proc. Natl Acad. Sci. USA 114, 7782–7789 (2017).

    CAS  Google Scholar 

  18. Faith, D. P., Magallón, S., Hendry, A. P. & Donoghue, M. J. Future benefits from contemporary evosystem services: a response to Rudman et al. Trends Ecol. Evol. 32, 717–719 (2017).

    Google Scholar 

  19. Faith, D. P. et al. Evosystem services: an evolutionary perspective on the links between biodiversity and human well-being. Curr. Opin. Environ. Sustain 2, 66–74 (2010).

    Google Scholar 

  20. Rudman, S. M., Kreitzman, M., Chan, K. M. A. & Schluter, D. Evosystem services: rapid evolution and the provision of ecosystem services. Trends Ecol. Evol. 32, 403–415 (2017).

    Google Scholar 

  21. Rudman, S. M., Kreitzman, M., Chan, K. M. A. & Schluter, D. Contemporary evosystem services: a reply to Faith et al. Trends Ecol. Evol. 32, 719–720 (2017).

    Google Scholar 

  22. Baquero, F. et al. Public health evolutionary biology of antimicrobial resistance: priorities for intervention. Evol. Appl 8, 223–239 (2015).

    CAS  Google Scholar 

  23. Powles, S. B. & Yu, Q. Evolution in action: plants resistant to herbicides. Annu. Rev. Plant Biol. 61, 317–347 (2010).

    CAS  Google Scholar 

  24. Davies, J. & Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417–33 (2010).

    CAS  Google Scholar 

  25. Cousens, R. D. & Fournier-Level, A. Herbicide resistance costs: what are we actually measuring and why? Pest Manag. Sci. 74, 1539–1546 (2018).

    CAS  Google Scholar 

  26. Carpenter, S., Walker, B., Anderies, J. M. & Abel, N. From metaphor to measurement: resilience of what to what? Ecosystems 4, 765–781 (2001).

    Google Scholar 

  27. Sommer, F., Anderson, J. M., Bharti, R., Raes, J. & Rosenstiel, P. The resilience of the intestinal microbiota influences health and disease. Nat. Rev. Microbiol. 15, 630–638 (2017).

    CAS  Google Scholar 

  28. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).

    CAS  Google Scholar 

  29. Chen, Q.-L. et al. Do manure-borne or indigenous soil microorganisms influence the spread of antibiotic resistance genes in manured soil? Soil Biol. Biochem. 114, 229–237 (2017).

    CAS  Google Scholar 

  30. Griffiths, B. S. & Philippot, L. Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 37, 112–129 (2013).

    CAS  Google Scholar 

  31. Mullineaux-Sanders, C., Suez, J., Elinav, E. & Frankel, G. Sieving through gut models of colonization resistance. Nat. Microbiol 3, 132–140 (2018).

    CAS  Google Scholar 

  32. Francino, M. P. Antibiotics and the human gut microbiome: dysbioses and accumulation of resistances. Front. Microbiol 6, 1543 (2016).

    Google Scholar 

  33. Andersson, D. I. & Hughes, D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat. Rev. Microbiol. 8, 260–271 (2010).

    CAS  Google Scholar 

  34. Waglechner, N. & Wright, G. D. Antibiotic resistance: it’s bad, but why isn’t it worse? BMC Biol. 15, 84 (2017).

    Google Scholar 

  35. Seekatz, A. M. et al. Recovery of the gut microbiome following fecal microbiota transplantation. MBio 5, e00893–14 (2014).

    Google Scholar 

  36. Caballero, S. et al. Cooperating commensals restore colonization resistance to vancomycin-resistant Enterococcus faecium. Cell Host Microbe 21, 592–602 (2017).

    CAS  Google Scholar 

  37. Baquero, F., Coque, T. M. & Cantón, R. Counteracting antibiotic resistance: breaking barriers among antibacterial strategies. Expert Opin. Ther. Targets 18, 851–861 (2014).

    CAS  Google Scholar 

  38. REX Consortium. Heterogeneity of selection and the evolution of resistance. Trends Ecol. Evol. 28, 110–118 (2013).

    Google Scholar 

  39. Wales, A. & Davies, R. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics 4, 567–604 (2015).

    CAS  Google Scholar 

  40. Pal, C., Bengtsson-Palme, J., Kristiansson, E. & Larsson, D. G. J. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16, 964 (2015).

    Google Scholar 

  41. Baker-Austin, C., Wright, M. S., Stepanauskas, R. & McArthur, J. V. Co-selection of antibiotic and metal resistance. Trends Microbiol. 14, 176–182 (2006).

    CAS  Google Scholar 

  42. Chang, Q., Wang, W., Regev‐Yochay, G., Lipsitch, M. & Hanage, W. P. Antibiotics in agriculture and the risk to human health: how worried should we be? Evol. Appl 8, 240–247 (2015).

    Google Scholar 

  43. Neve, P., Busi, R., Renton, M. & Vila‐Aiub, M. M. Expanding the eco‐evolutionary context of herbicide resistance research. Pest Manag. Sci. 70, 1385–1393 (2014).

    CAS  Google Scholar 

  44. Zhu, Y.-G. et al. Microbial mass movements. Science 357, 1098–1099 (2017).

    Google Scholar 

  45. Zhu, Y. G. et al. Human dissemination of genes and microorganisms in Earth’s critical zone. Glob. Chang. Biol 24, 1488–1499 (2018).

    Google Scholar 

  46. Elmqvist, T. et al. Response diversity, ecosystem change, and resilience. Front. Ecol. Environ. 1, 488–494 (2003).

    Google Scholar 

  47. Folke, C. et al. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Evol. Syst. 35, 557–581 (2004).

    Google Scholar 

  48. Nyström, M., Folke, C. & Moberg, F. Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 (2000).

    Google Scholar 

  49. Spasojevic, M. J. et al. Scaling up the diversity–resilience relationship with trait databases and remote sensing data: the recovery of productivity after wildfire. Glob. Chang. Biol 22, 1421–1432 (2016).

    Google Scholar 

  50. Biggs, R. et al. Toward principles for enhancing the resilience of ecosystem services. Annu. Rev. Environ. Resour. 37, 421–448 (2012).

    Google Scholar 

  51. Ives, A. R. & Carpenter, S. R. Stability and diversity of ecosystems. Science 317, 58–62 (2007).

    CAS  Google Scholar 

  52. Rivera-Chávez, F. et al. Depletion of butyrate-producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host Microbe 19, 443–454 (2016).

    Google Scholar 

  53. Manichanh, C. et al. Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res. 20, 1411–1419 (2010).

    CAS  Google Scholar 

  54. Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018).

    CAS  Google Scholar 

  55. Wright, G. D. Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol. 13, 589–594 (2010).

    CAS  Google Scholar 

  56. Surette, M. & Wright, G. D. Lessons from the environmental antibiotic resistome. Annu. Rev. Microbiol. 71, 309–329 (2017).

    CAS  Google Scholar 

  57. Wybouw, N., Pauchet, Y., Heckel, D. G. & Van Leeuwen, T. Horizontal gene transfer contributes to the evolution of arthropod herbivory. Genome Biol. Evol 8, 1785–1801 (2016).

    CAS  Google Scholar 

  58. Ambrose, K. V., Koppenhöfer, A. M. & Belanger, F. C. Horizontal gene transfer of a bacterial insect toxin gene into the Epichloë fungal symbionts of grasses. Sci. Rep 4, 5562 (2014).

    CAS  Google Scholar 

  59. Van Kleunen, M. et al. Global exchange and accumulation of non-native plants. Nature 525, 100–103 (2015).

    Google Scholar 

  60. Stokstad, E. New crop pest takes Africa at lightning speed. Science 356, 473–474 (2017).

    CAS  Google Scholar 

  61. Multi-pronged Approach Key for Effectively Defeating Fall Armyworm in Africa (CIMMYT, 2017); https://www.cimmyt.org/press_release/multi-pronged-approach-key-for-effectively-defeating-fall-armyworm-in-africa/

  62. Tay, W. T. et al. Mitochondrial DNA and trade data support multiple origins of Helicoverpa armigera (Lepidoptera, Noctuidae) in Brazil. Sci. Rep 7, 45302 (2017).

    CAS  Google Scholar 

  63. Nagoshi, R. N. et al. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS One 12, e0181982 (2017).

    Google Scholar 

  64. Watt, S. Biotype of Australias Russian Wheat Aphid Populations Now Known (GRDC, 2017); https://grdc.com.au/news-and-media/news-and-media-releases/south/2017/11/biotype-of-australias-russian-wheat-aphid-populations-now-known

  65. Berrazeg, M. et al. New Dehli metallo-beta-lactamase around the world: an eReview using Google Maps. Euro Surveill 19, 20809 (2014).

    Google Scholar 

  66. Campos, J., Cristino, L., Peixe, L. & Antunes, P. MCR-1 in multidrug-resistant and copper-tolerant clinically relevant Salmonella 1,4,[5],12:i:- and S. Rissen clones in Portugal, 2011 to 2015. Euro Surveill. 21, 30270 (2016).

    Google Scholar 

  67. Munoz-Price, L. S. et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect. Dis. 13, 785–796 (2013).

    Google Scholar 

  68. Porse, A., Schou, T. S., Munck, C., Ellabaan, M. M. H. & Sommer, M. O. A. Biochemical mechanisms determine the functional compatibility of heterologous genes. Nat. Commun. 9, 522 (2018).

    Google Scholar 

  69. Dutil, L. et al. Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg. Infect. Dis. 16, 48–54 (2010).

    Google Scholar 

  70. Surveillance Bulletin: Reductions in Antimicrobial Use and Resistance: Preliminary Evidence of the Effect of the Canadian Chicken Industry’s Elimination of Use of Antimicrobials of Very High Importance to Human Medicine (CIPARS, 2016).

  71. Overdevest, I. et al. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg. Infect. Dis. 17, 1216–1222 (2011).

    Google Scholar 

  72. Tamang, M. D. et al. Prevalence and molecular characterization of CTX-M β-lactamase-producing Escherichia coli isolated from healthy swine and cattle. Foodborne Pathog. Dis. 10, 13–20 (2013).

    CAS  Google Scholar 

  73. Davis, M. A. et al. Recent emergence of Escherichia coli with cephalosporin resistance conferred by bla CTX-M on Washington State dairy farms. Appl. Environ. Microbiol. 81, 4403–4410 (2015).

    CAS  Google Scholar 

  74. Cormier, A. C. et al. Extended-spectrum-cephalosporin resistance genes in Escherichia coli from beef cattle. Antimicrob. Agents Chemother. 60, 1162–1163 (2016).

    CAS  Google Scholar 

  75. 2015 NARMS Integrated Report (NARMS, 2017).

  76. Bennett, E. M., Peterson, G. D. & Gordon, L. J. Understanding relationships among multiple ecosystem services. Ecol. Lett 12, 1394–1404 (2009).

    Google Scholar 

  77. Raudsepp-Hearne, C., Peterson, G. D. & Bennett, E. M. Ecosystem service bundles for analyzing tradeoffs in diverse landscapes. Proc. Natl Acad. Sci. USA 107, 5242–5247 (2010).

    CAS  Google Scholar 

  78. Renard, D., Rhemtulla, J. M. & Bennett, E. M. Historical dynamics in ecosystem service bundles. Proc. Natl Acad. Sci. USA 112, 13411–13416 (2015).

    CAS  Google Scholar 

  79. Spake, R. et al. Unpacking ecosystem service bundles: towards predictive mapping of synergies and trade-offs between ecosystem services. Glob. Environ. Chang 47, 37–50 (2017).

    Google Scholar 

  80. Mie, A. et al. Human health implications of organic food and organic agriculture. Environ. Health 16, 88 (2017).

    Google Scholar 

  81. Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).

    CAS  Google Scholar 

  82. Lessa, F. C. et al. Burden of Clostridium difficile infection in the United States. N. Engl. J. Med. 372, 825–834 (2015).

    CAS  Google Scholar 

  83. Bohnhoff, M., Drake, B. L. & Miller, C. P. Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc. Soc. Exp. Biol. Med. 86, 132–137 (1954).

    CAS  Google Scholar 

  84. Wadolkowski, E. A., Burris, J. A. & O’Brien, A. D. Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157: H7. Infect. Immun. 58, 2438–2445 (1990).

    CAS  Google Scholar 

  85. Wadolkowski, E. A., Laux, D. C. & Cohen, P. S. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of growth in mucus. Infect. Immun. 56, 1030–1035 (1988).

    CAS  Google Scholar 

  86. Desneux, N., Decourtye, A. & Delpuech, J.-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106 (2007).

    CAS  Google Scholar 

  87. Wilson, L. J., Bauer, L. R. & Lally, D. A. Effect of early season insecticide use on predators and outbreaks of spider mites (Acari: Tetranychidae) in cotton. Bull. Entomol. Res. 88, 477–488 (1998).

    CAS  Google Scholar 

  88. Romeis, J., Meissle, M. & Bigler, F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat. Biotechnol. 24, 63–71 (2006).

    CAS  Google Scholar 

  89. Naranjo, S. E. Impacts of Bt transgenic cotton on integrated pest management. J. Agric. Food Chem. 59, 5842–5851 (2010).

    Google Scholar 

  90. Ellsworth, P. C. & Martinez-Carrillo, J. L. IPM for Bemisia tabaci: a case study from North America. Crop Prot. 20, 853–869 (2001).

    Google Scholar 

  91. Gould, F., Kennedy, G. G. & Johnson, M. T. Effects of natural enemies on the rate of herbivore adaptation to resistant host plants. Entomol. Exp. Appl 58, 1–14 (1991).

    Google Scholar 

  92. Carrière, Y. et al. Large-scale, spatially-explicit test of the refuge strategy for delaying insecticide resistance. Proc. Natl Acad. Sci. USA 109, 775–780 (2012).

    Google Scholar 

  93. Liu, X. et al. Natural enemies delay insect resistance to Bt crops. PLoS One 9, e90366 (2014).

    Google Scholar 

  94. Klein, A.-M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. Lond. B 274, 303–313 (2007).

    Google Scholar 

  95. Olotu, M. I. & Gujar, G. T. Many-fold less than the field recommended concentrations of neonicotinoids and malathion affect foraging of honeybee in three important crops in India. ENTOMON 41, 47–60 (2016).

    Google Scholar 

  96. Assessment Report on Pollinators, Pollination and Food Production (IPBES, 2016); https://www.ipbes.net/assessment-reports/pollinators

  97. Hokkanen, H. M. T., Menzler-Hokkanen, I. & Keva, M. Long-term yield trends of insect-pollinated crops vary regionally and are linked to neonicotinoid use, landscape complexity, and availability of pollinators. Arthropod. Plant. Interact 11, 449–461 (2017).

    Google Scholar 

  98. Feld, L. et al. Pesticide side effects in an agricultural soil ecosystem as measured by amoA expression quantification and bacterial diversity changes. PLoS One 10, e0126080 (2015).

    Google Scholar 

  99. National Research Council. The Impact of Genetically Engineered Crops on Farm Sustainability in the United States (National Academies Press, Washington DC, 2010).

    Google Scholar 

  100. Schlatter, D. C., Yin, C., Hulbert, S., Burke, I. & Paulitz, T. Impacts of repeated glyphosate use on wheat-associated bacteria are small and depend on glyphosate use history. Appl. Environ. Microbiol. 83, e01354–17 (2017).

    CAS  Google Scholar 

  101. Langdon, A., Crook, N. & Dantas, G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med 8, 39 (2016).

    Google Scholar 

  102. Barzegari, A., Saeedi, N. & Saei, A. A. Shrinkage of the human core microbiome and a proposal for launching microbiome biobanks. Future Microbiol. 9, 639–656 (2014).

    CAS  Google Scholar 

  103. Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).

    CAS  Google Scholar 

  104. Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258–1270 (2012).

    CAS  Google Scholar 

  105. Riiser, A. The human microbiome, asthma, and allergy. Allergy, Asthma Clin. Immunol. 11, 35 (2015).

    Google Scholar 

  106. Von Hertzen, L. et al. Helsinki alert of biodiversity and health. Ann. Med. 47, 218–225 (2015).

    Google Scholar 

  107. Martinez, J. L. & Olivares, J. in Antimicrobial Resistance in the Environment (eds Keen, P. L. & Montforts, M. H. M. M.) 151–172 (Wiley, Hoboken, 2012).

  108. Berendonk, T. U. et al. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13, 310–317 (2015).

    CAS  Google Scholar 

  109. Lerner, A., Jeremias, P. & Matthias, T. The world incidence and prevalence of autoimmune diseases is increasing. Int. J. Celiac Dis 3, 151–155 (2015).

    Google Scholar 

  110. Stefka, A. T. et al. Commensal bacteria protect against food allergen sensitization. Proc. Natl Acad. Sci. USA 111, 13145–13150 (2014).

    CAS  Google Scholar 

  111. Tito, R. Y. et al. Insights from characterizing extinct human gut microbiomes. PLoS One 7, e51146 (2012).

    CAS  Google Scholar 

  112. Zaneveld, J. R., McMinds, R. & Vega Thurber, R. Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat. Microbiol 2, 17121 (2017).

    CAS  Google Scholar 

  113. Steffen, W., Broadgate, W., Deutsch, L., Gaffney, O. & Ludwig, C. The trajectory of the Anthropocene: the Great Acceleration. Anthr. Rev 2, 81–98 (2015).

    Google Scholar 

  114. Rockström, J. et al. Planetary boundaries: exploring the safe operating space for humanity. Ecol. Soc. 14, 32 (2009).

    Google Scholar 

  115. Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).

    Google Scholar 

  116. Shen, Z., Wang, Y., Shen, Y., Shen, J. & Wu, C. Early emergence of mcr-1 in Escherichia coli from food-producing animals. Lancet Infect. Dis. 16, 293 (2016).

    Google Scholar 

  117. Ventola, C. L. The antibiotic resistance crisis: part 1: causes and threats. P T 40, 277–83 (2015).

    Google Scholar 

  118. Hersh, A. L., Newland, J. G., Beekmann, S. E., Polgreen, P. M. & Gilbert, D. N. Unmet medical need in infectious diseases. Clin. Infect. Dis. 54, 1677–1678 (2012).

    Google Scholar 

  119. Eades, C., Hughes, S., Heard, K. & Moore, L. S. Antimicrobial therapies for Gram-positive infections. Pharm. J. 9, 20203363 (2017).

    Google Scholar 

  120. Aksoy, D. Y. & Unal, S. New antimicrobial agents for the treatment of Gram-positive bacterial infections. Clin. Microbiol. Infect. 14, 411–420 (2008).

    CAS  Google Scholar 

  121. Johnson, A. P. et al. Mandatory surveillance of methicillin-resistant Staphylococcus aureus (MRSA) bacteraemia in England: the first 10 years. J. Antimicrob. Chemother 67, 802–809 (2012).

    CAS  Google Scholar 

  122. Edgeworth, J. D. Has decolonization played a central role in the decline in UK methicillin-resistant Staphylococcus aureus transmission? A focus on evidence from intensive care. J. Antimicrob. Chemother. 66, 41–47 (2011).

    Google Scholar 

  123. Sparks, T. C. & Nauen, R. IRAC: mode of action classification and insecticide resistance management. Pestic. Biochem. Physiol. 121, 122–128 (2015).

    CAS  Google Scholar 

  124. Heap, I. & Duke, S. O. Overview of glyphosate‐resistant weeds worldwide. Pest Manag. Sci. 74, 1040–1049 (2017).

    Google Scholar 

  125. Tabashnik, B. E. & Carrière, Y. Surge in insect resistance to transgenic crops and prospects for sustainability. Nat. Biotechnol. 35, 926–935 (2017).

    CAS  Google Scholar 

  126. Gual, M. A. & Norgaard, R. B. Bridging ecological and social systems coevolution: a review and proposal. Ecol. Econ. 69, 707–717 (2010).

    Google Scholar 

  127. Rockwood, L. L. et al. (eds) Foundations of Environmental Sustainability: The Coevolution of Science and Policy (Oxford Univ. Press, Oxford, 2009).

  128. Bernhardt, E. S., Rosi, E. J. & Gessner, M. O. Synthetic chemicals as agents of global change. Front. Ecol. Environ. 15, 84–90 (2017).

    Google Scholar 

  129. Pesticides Use Database (FAO, accessed 4 October 2017); http://www.fao.org/faostat/en/#data/RP

  130. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, 2016) .

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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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Living with Resistance project. 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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  • DOI: https://doi.org/10.1038/s41893-018-0164-3

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