Mammalian engineers drive soil microbial communities and ecosystem functions across a disturbance gradient

Abstract

The effects of mammalian ecosystem engineers on soil microbial communities and ecosystem functions in terrestrial ecosystems are poorly known. Disturbance from livestock has been widely reported to reduce soil function, but disturbance by animals that forage in the soil may partially offset these negative effects of livestock, directly and/or indirectly by shifting the composition and diversity of soil microbial communities. Understanding the role of disturbance from livestock and ecosystem engineers in driving soil microbes and functions is essential for formulating sustainable ecosystem management and conservation policies. We compared soil bacterial community composition and enzyme concentrations within four microsites: foraging pits of two vertebrates, the indigenous short-beaked echidna (Tachyglossus aculeatus) and the exotic European rabbit (Oryctolagus cuniculus), and surface and subsurface soils along a gradient in grazing-induced disturbance in an arid woodland. Microbial community composition varied little across the disturbance gradient, but there were substantial differences among the four microsites. Echidna pits supported a lower relative abundance of Acidobacteria and Cyanobacteria, but a higher relative abundance of Proteobacteria than rabbit pits and surface microsites. Moreover, these microsite differences varied with disturbance. Rabbit pits had a similar profile to the subsoil or the surface soils under moderate and high, but not low disturbance. Overall, echidna foraging pits had the greatest positive effect on function, assessed as mean enzyme concentrations, but rabbits had the least. The positive effects of echidna foraging on function were indirectly driven via microbial community composition. In particular, increasing activity was positively associated with increasing relative abundance of Proteobacteria, but decreasing Acidobacteria. Our study suggests that soil disturbance by animals may offset, to some degree, the oft-reported negative effects of grazing-induced disturbance on soil function. Further, our results suggest that most of this effect will be derived from echidnas, with little positive effects due to rabbits. Activities that enhance the habitat for echidnas or reduce rabbit populations are likely to have a positive effect on soil function in these systems.

A global database and “state of the field” review of research into ecosystem engineering by land animals

“…Fungi and microbial communities were least reported in studies (4%). The research on these taxa focussed on species richness and composition, particularly as a response to soil disturbance by burrowing engineers (Eldridge, Delgado‐Baquerizo, Woodhouse, & Neilan, ), and following reintroduction of regionally extinct engineer species (Clarke, Weyrich, & Cooper, ).…”

“…Three of the eight species studied were reintroduced. Because these engineers were reintroduced after long periods of regional extinction, it was possible to observe how the presence of burrowing species not only facilitated the survival and establishment of other threatened species (Hayward et al., ), but was also strongly associated with changes in ground‐dwelling arthropod, fungal and microbial communities (Clarke et al., ; Eldridge et al., ; Silvey et al., ), and changes in abundance and behaviour that affected the function of other engineers (Coggan, Hayward, & Gibb, ). The role of all burrowing species (particularly vertebrates) in supporting diversity by providing shelter is reflected in observations globally (see reviews by Davidson et al., ; Root‐Bernstein & Ebensperger, ).…”

Bioturbation by bandicoots facilitates seedling growth by altering soil properties

“…Decomposition rates are influenced by climate, litter chemistry (Aerts, ), soil microbial and fungal communities (Beare et al., ) as well as litter position (above‐ vs. below‐ground) and microhabitat characteristics (Austin et al., ). Buried litter decomposes faster than surface litter (Austin et al., ), potentially due to the increased exposure to microbial and fungal communities (Beare et al., ), with microbial communities varying in association with animal foraging activities (Eldridge et al., ).…”

Heavy livestock grazing negatively impacts a marsupial ecosystem engineer

“…Digging and burrowing animals not only enhance habitat heterogeneity (Parsons et al ., ), thus creating habitat for other small mammals, reptiles and invertebrates (Davidson, Lightfoot & McIntyre, ; Ewacha et al ., ), but can influence ecosystems through non‐engineering pathways such as predation and competition (Prugh & Brashares, ). Therefore, maintaining or enhancing ecosystem engineer populations may be a cost‐effective tool to lessen the negative impacts of grazing on soil health, restore degraded habitats and assist in the recovery of other species of conservation concern (Eldridge & James, ; Eldridge et al ., ; McCullough Hennessy et al ., ).…”