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Organic farming promotes biotic resistance to foodborne human pathogens

Jones, Matthew S., Fu, Zhen, Reganold, John P., Karp, Daniel S., Besser, Thomas E., Tylianakis, Jason M., Snyder, William E.
Journal of applied ecology 2019 v.56 no.5 pp. 1117-1127
Coleoptera, Escherichia coli O157, Sus scrofa, animal pathogens, biodiversity, biological control, coasts, conventional farming, dung beetles, ecosystem services, farm management, farms, feces, feral animals, food pathogens, food safety, habitats, laboratory experimentation, landscapes, livestock, organic production, pastures, pollination, risk, soil bacteria, vegetables, vertebrates, wildlife, United States
Farmland biodiversity benefits pollination, biological control and other key ecosystem services. Food safety has been seen as an exception to this broader pattern, as diverse farmlands attract wildlife that vector foodborne human pathogens. Resulting mitigation efforts thus often seek to deter wildlife by removing natural habitats, while also excluding vertebrate livestock. However, surprising recent evidence suggests that farm simplification actually increases the likelihood that produce will be contaminated with human pathogens. Here, we consider the possibility that intensified agriculture harms faeces‐feeding (coprophagous) beetles and bacteria, which could contribute to heightened food‐safety risk. In 70 commercial vegetable fields spanning the US west coast, using either organic or conventional farming methods, we surveyed coprophages both above‐ and below‐ground. We also measured removal rates of the faeces of Sus scrofa, which vectors foodborne pathogens both as livestock and as feral wildlife. Above‐ground, organic farms fostered dung beetle species that removed S. scrofa faeces more rapidly than was seen on conventional farms, although this benefit was weakened in simplified landscapes dominated by pasture and an introduced dung beetle. Below‐ground, organic farming encouraged significantly higher biodiversity among soil bacteria. Organic farming similarly benefitted dung beetles and bacteria on farms that produced livestock alongside vegetables, or vegetables alone. Complementary laboratory experiments revealed that the dung beetle species and biodiverse bacterial assemblages typical of organic farms were significantly more effective at suppressing human‐pathogenic Escherichia coli O157:H7, compared to coprophage communities associated with conventional farms. This suggests that farm management practices, coprophage conservation, and human–pathogen suppression might be linked. Synthesis and applications. Altogether, our results indicate that insects and microbes can rapidly remove faeces, with the potential to also decrease the persistence of human pathogens. In turn, this suggests that improved food safety may be an important, and perhaps underappreciated, ecosystem service that is enhanced by on‐farm biodiversity. We recommend that farm managers and regulators consider the risks and benefits to coprophages when making management decisions regarding food safety.