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

Abstract

Recent studies have shown that invasive earthworms can dramatically reduce native biodiversity, both above and below the ground. However, we still lack a synthetic understanding of the underlying mechanisms behind these changes, such as whether earthworm effects on soil chemical properties drive such relationships. Here, we investigated the effects of invasive earthworms on soil chemical properties (pH, water content, and the stocks and fluxes of carbon, nitrogen, and phosphorus) by conducting a meta‐analysis. Invasive earthworms generally increased soil pH, indicating that the removal of organic layers and the upward transport of more base‐rich mineral soil caused a shift in soil pH. Moreover, earthworms significantly decreased soil water content, suggesting that the burrowing activities of earthworms may have increased water infiltration of and/or increased evapotranspiration from soil. Notably, invasive earthworms had opposing effects on organic and mineral soil for carbon and nitrogen stocks, with decreases in organic, and increases in mineral soil. Nitrogen fluxes were higher in mineral soil, whereas fluxes in organic soil were not significantly affected by the presence of invasive earthworms, indicating that earthworms mobilize and redistribute nutrients among soil layers and increase overall nitrogen loss from the soil. Invasive earthworm effects on element stocks increased with ecological group richness only in organic soil. Earthworms further decreased ammonium stocks with negligible effects on nitrate stocks in organic soil, whereas they increased nitrate stocks but not ammonium stocks in mineral soil. Notably, all of these results were consistent across forest and grassland ecosystems underlining the generality of our findings. However, we found some significant differences between studies that were conducted in the field (observational and experimental settings) and in the lab, such as that the effects on soil pH decreased from field to lab settings, calling for a careful interpretation of lab findings. Our meta‐analysis provides strong empirical evidence that earthworm invasion may lead to substantial changes in soil chemical properties and element cycling in soil. Furthermore, our results can help explain the dramatic effects of invasive earthworms on native biodiversity, for example, shifts towards the dominance of grass species over herbaceous ones, as shown by recent meta‐analyses.

Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees

“…Nevertheless, we also cannot rule out the contribution of other forms of N to increase in mineral soil layers with higher earthworm densities, as shown by a recent meta-analysis (Ferlian et al, 2020).…”

“…Insect herbivory is widespread in both P. balsamifera and P. tremuloides despite differences in their growth and defense strategies (Peterson & Peterson, 1992;Philippe & Bohlmann, 2007). Invasive earthworms increase soil nutrient availability in mineral soil layers (Ferlian et al, 2020), at least in the initial years after invasion (Eisenhauer et al, 2019). In general, particular forms of soil N, such as soil nitrate, increase in earthworm-invaded mineral soil layers (Ferlian et al, 2020).…”

“…Several meta‐analyses and synthesis work have pointed out that invasive earthworms are detrimental to native biodiversity and can alter the functions of an ecosystem with no recent history of earthworms (Craven et al., 2017; Ferlian et al., 2018, 2020; Frelich et al., 2019; Hendrix et al., 2008). Our results indicate that saplings of two common deciduous trees ( P. balsamifera and P. tremuloides ) in North American boreal forests may become susceptible to insect herbivory at sites where the density of invasive earthworms is higher (Figure 2).…”

“…The spatial distribution and cycling of nutrients in soils are often altered by invasive earthworms (Ferlian et al., 2020), which can impact the growth of plants including trees (Donaldson et al., 2006; Jiang et al., 2018). For instance, soil nutrient availability can relax the trade‐off between investments in growth and defense in tree species, which mainly relates to fitness costs for trees associated with defense against herbivores at the cost of their growth (Donaldson et al., 2006; Hahn & Maron, 2016).…”

“…For instance, soil nutrient availability can relax the trade‐off between investments in growth and defense in tree species, which mainly relates to fitness costs for trees associated with defense against herbivores at the cost of their growth (Donaldson et al., 2006; Hahn & Maron, 2016). In general, N‐availability in the mineral soil layer increases in earthworm‐invaded sites (Ferlian et al., 2020). This mineral layer may represent the main layer of soil, where young trees extract nutrients from.…”