Biotic interactions in soil and dung shape parasite transmission in temperate ruminant systems: An integrative framework

Gastrointestinal helminth parasites undergo part of their life cycle outside their host, such that developmental stages interact with the soil and dung fauna. These interactions are capable of affecting parasite transmission on pastures yet are generally ignored in current models, empirical studies and practical management. Dominant methods of parasite control, which rely on anthelmintic medications for livestock, are becoming increasingly ineffective due to the emergence of drug-resistant parasite populations. Furthermore, consumer and regulatory pressure on decreased chemical use in agriculture and the consequential disruption of biological processes in the dung through nontarget effects exacerbates issues with anthelmintic reliance. This presents a need for the application and enhancement of nature-based solutions and biocontrol methods. However, successfully harnessing these options relies on advanced understanding of the ecological system and interacting effects among biotic factors and with immature parasite stages. Here, we develop a framework linking three key groups of dung and soil fauna-fungi, earthworms, and dung beetles-with each other and developmental stages of helminths parasitic in farmed cattle, sheep, and goats in temperate grazing systems. We populate this framework from existing published studies and highlight the interplay between faunal groups and documented ecological outcomes. Of 1756 papers addressing abiotic drivers of populations of these organisms and helminth parasites, only 112 considered interactions between taxa and 36 presented data on interactions between more than two taxonomic groups. Results suggest that fungi reduce parasite abundance and earthworms may enhance fungal communities, while competition between dung taxa may reduce their individual effect on parasite transmission. Dung beetles were found to impact fungal populations and parasite transmission variably, possibly tied to the prevailing climate within a specific ecological context. By exploring combinations of biotic factors, we consider how interactions between species may be fundamental to the ecological consequences of biocontrol strategies and nontarget impacts of anthelmintics on dung and soil fauna and how pasture management alterations to promote invertebrates might help limit parasite transmission. With further development and parameterization the framework could be applied quantitatively to guide, prioritize, and interpret hypothesis-driven experiments and integrate biotic factors into established models of parasite transmission dynamics.