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

Abstract

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.

Keywords: agroecology; agroecosystems; biocontrol; parasite control; sustainable agriculture.

FIGURE 1

Schematic diagram depicting influence of key soil fauna on parasite transmission. Compartments are detailed with relevant life cycle stages of the parasite. Black arrows indicate the progression through the environmental stages of the gastrointestinal nematode life cycle. Three key soil fauna groups are considered in the schematic: earthworms, dung beetles, and fungi. White arrows indicate movements between environmental compartments with associated organisms detailed within white box. Curved white arrows describe movement within compartment, with corresponding organisms contained within. Red arrows indicate a negative impact on the vital rates of that stage of the parasite life cycle, with the soil fauna that causes this impact labeled. Some active unassisted movement of gastrointestinal nematode (GIN) L3 between the dung, soil subsurface, and herbage does occur (Rose et al., 2015), but this figure considers the deeper soil layers. L1 and L2 refer to GIN specifically; eggs include GIN and other helminths.

FIGURE 2

Schematic diagram displaying selection of eligible papers from systematic review. Number of total papers investigating the general terms and two‐species combinations (a). The table considers the number of papers investigating each combination, with the total number of accepted papers that explore the interaction on the top line, followed by the number initially returned in the bracket below (b). The driver column shows the number of papers initially returned for each soil fauna group with the abiotic driver terms included (Box 1).

FIGURE 3

Schematic diagram detailing number of papers that investigate combinations of three or more taxonomic groups using general terms (Box 1). The diagram displays the total number of papers returned for each three or four species combination searches, alongside the general terms, in parentheses. The number of papers that investigate those interactions are above, that is, the figure not in parentheses.

FIGURE 4

Schematic diagram detailing number of papers that investigate combinations of at least two species with general and driver terms. The diagram displays the number of papers returned for each two, three, or four species combination searches, alongside the general terms and driver terms. The number of papers returned in the search is given in parentheses, and the number that specifically investigate the interactions is above, that is, not in parentheses.