One Health Farming: Noninvasive monitoring reveals links between farm vertebrate richness and pathogen markers in outdoor hoofstock

Abstract

Outdoor farming contributes to biodiversity conservation and enhances animal welfare, but also raises biosafety concerns due to livestock contact with potentially infected wildlife. Thus, there is a need to assess the balance between vertebrate species richness on farms, visits by wildlife species posing a biosafety risk, and pathogen circulation in open-air farming systems. We explored these links in a pilot study involving 15 open-air hoofstock farms (6 cattle, 5 small ruminant, and 4 pig farms), where we conducted interviews and risk point inspections and used two noninvasive tools: short-term camera trap (CT) deployment and environmental nucleic acid detection (ENAD). CTs were deployed to assess the richness of birds and mammals, as well as to determine the percentage of CTs detecting defined risk species. We also collected livestock feces and used sponges to sample surfaces for environmental DNA (eDNA), testing for nine pathogen markers. Total vertebrate richness ranged from 18 to 42 species, with waterholes significantly contributing to farm vertebrate richness, since 48.2 % of all wild vertebrates were detected at waterbodies, and 28.6 % were exclusively detected at waterholes. Pathogen markers detected at risk points correlated with those detected in livestock samples. Notably, the frequency of uidA marker detection correlated with the total number of pathogen markers detected per farm. Overall marker richness, an indicator of pathogen diversity, varied between farms, being higher in small ruminant farms compared to cattle or pig farms. At the farm level, wild vertebrate richness was negatively correlated with the richness of pathogen markers detected at risk points. Additionally, risk points with a higher probability of detecting more pathogen markers had lower vertebrate richness. Although CT-based assessments of vertebrate richness and ENAD-based pathogen marker detection are only indicators of actual biodiversity and farm health, respectively, our findings suggest that farmland vertebrate communities provide important ecosystem services and may help limit the circulation of multi-host pathogens.