Belowground interactions with aboveground consequences: Invasive earthworms and arbuscular mycorrhizal fungi

Abstract

A mounting body of research suggests that invasive nonnative earthworms substantially alter microbial communities, including arbuscular mycorrhizal fungi (AMF). These changes to AMF can cascade to affect plant communities and vertebrate populations. Despite these research advances, relatively little is known about (1) the mechanisms behind earthworms' effects on AMF and (2) the factors that determine the outcomes of earthworm-AMF interactions (i.e., whether AMF abundance is increased or decreased and subsequent effects on plants). We predict that AMF-mediated effects of nonnative earthworms on ecosystems are nearly universal because (1) AMF are important components of most terrestrial ecosystems, (2) nonnative earthworms have become established in nearly every type of terrestrial ecosystem, and (3) nonnative earthworms, due to their burrowing and feeding behavior, greatly affect AMF with potentially profound concomitant effects on plant communities. We highlight the multiple direct and indirect effects of nonnative earthworms on plants and review what is currently known about the interaction between earthworms and AMF. We also illustrate how the effects of nonnative earthworms on plant-AMF mutualisms can alter the structure and stability of aboveground plant communities, as well as the vertebrate communities relying on these habitats. Integrative studies that assess the interactive effects of earthworms and AMF can provide new insights into the role that belowground ecosystem engineers play in altering aboveground ecological processes. Understanding these processes may improve our ability to predict the structure of plant and animal communities in earthworm-invaded regions and to develop management strategies that limit the numerous undesired impacts of earthworms.

Invasive earthworms erode soil biodiversity: A meta‐analysis

“…Mycorrhizal fungi were among the most negatively affected microbial groups due to earthworm invasion, however, these results are based on relatively lower number of studies (Figure a). Invasive earthworms’ burrowing activities and potentially direct feeding on fungal hyphae have been argued to detrimentally affect mycorrhizal fungi in the soil (Paudel et al., ). Such earthworm‐induced reduction in mycorrhizal fungi are detrimental to plant communities (Paudel et al., ), such as for the performance of native plant species (Gundale, ) as confirmed by a recent meta‐analysis (Craven et al., ).…”

“…Invasive earthworms’ burrowing activities and potentially direct feeding on fungal hyphae have been argued to detrimentally affect mycorrhizal fungi in the soil (Paudel et al., ). Such earthworm‐induced reduction in mycorrhizal fungi are detrimental to plant communities (Paudel et al., ), such as for the performance of native plant species (Gundale, ) as confirmed by a recent meta‐analysis (Craven et al., ). Due to a low number of studies, we were unable to assess how microbial groups may differentially respond to earthworm invasion effects in different layers of the soil.…”

“…Specifically, invasive earthworms detrimentally affect fungal communities by disrupting their hyphal networks, whereas earthworm effects on bacterial communities are less conspicuous (Dempsey, Fisk, & Fahey, ; Eisenhauer, Schlaghamerský, Reich, & Frelich, ). Earthworms additionally disrupt mycorrhizal networks in the soil, with important implications for nutrient mineralization and plant nutrient uptake (Frelich et al., ; Paudel et al., ).…”

Soil chemistry turned upside down: a meta‐analysis of invasive earthworm effects on soil chemical properties

“…While burrowing, earthworms secrete labile carbon (C) compounds in the form of mucus and form nutrient‐rich casts (Brown , Eisenhauer ). Burrowing activities were also found to disrupt fungal hyphae influencing the nutrient supply of plants associating with mycorrhizal fungi (Lawrence et al , Paudel et al ). Moreover, soil layers are mixed and, thus, organic matter is transported to lower soil layers, resulting in a vertical redistribution of nutrients (Knollenberg et al , Eisenhauer et al ).…”

Impacts of invasive biota in forest ecosystems in an aboveground–belowground context

“…Belowground effects include homogenization of soil physical structure, stimulation of soil microbial activity and greater mineralization of nutrients, and loss of organic matter (Bohlen et al 2004). Aboveground, effects can include short term enhancement of plant nutrition and growth (Scheu and Parkinson 1994), but adverse longer term biogeochemical effects and impaired recruitment of forest tree species resulting from the loss of organic matter (Frelich et al 2006;Eisenhauer et al 2009;Paudel et al 2016). However, earthworm invasion of natural forests is comparatively recent, and we still have limited knowledge of how this will impact on forest dynamics and ecosystem functioning over the longer term.…”