Invasive earthworm and soil litter response to the experimental removal of white‐tailed deer and an invasive shrub

Abstract

Recent studies have shown that complex species interactions can regulate above‐ and belowground processes in terrestrial systems. Ungulate herbivory and invasive species are known to have strong effects on plant communities in some systems, but their impacts on soil biota and belowground processes are lesser known. Growing evidence suggests white‐tailed deer (Odocoileus virginianus) and invasive plants facilitate increased abundance of exotic earthworms in temperate forests of the eastern United States. We conducted an experimental study that manipulated deer access and the presence of an invasive understory shrub in an eastern deciduous forest of southwestern Ohio, USA, from 2013 to 2017. Earthworm density and biomass, and standing litter biomass were measured in five paired deer access and exclosure plots, each with a split‐plot removal of Amur honeysuckle (Lonicera maackii). Earthworm density declined in response to the experimental exclusion of deer, with earthworm density decreasing over time in the deer exclosure plots relative to deer access plots. Deer exclusion produced greater variation in earthworm species composition relative to access plots. Multivariate analyses indicated that larger earthworms in the genus Lumbricus were associated with deer exclosure plots, while smaller endogeic species were ubiquitous in both treatments. Standing litter biomass decreased over time in the deer‐access plots. In contrast, honeysuckle removal had little effect on earthworm density and standing litter biomass. There was an interaction between deer and honeysuckle treatments on earthworm biomass, with honeysuckle removal reducing earthworm biomass when deer were excluded. Our results demonstrate strong effects of herbivores on invasive earthworms and ecosystem processes, but indicate a weaker influence of invasive shrubs. Further, our findings suggest that the effects of deer overabundance in forest ecosystems are potentially reversible with long‐term intervention.

Invasive dominance and resident diversity: unpacking the impact of plant invasion on biodiversity and ecosystem function

“…Note that in differentiating the two models (inclusion vs. subtraction), we use the term subtraction as opposed to exclusion to avoid confusing the approach with methods that involve the physical removal of invasive plants from field plots (Tekiela and Barney 2017) and/or the experimental exclusion of invasive animals and plants (Stokeld et al 2018, Mahon and Crist 2019). Further, for brevity, we also use the phrase “the two assemblage models” when discussing the inclusion and subtraction models in unison.…”

Multiple stressors prevent gains in native plant diversity following invasive species removal

“…Unfortunately, our understanding of how to control invasive earthworms within natural areas remains limited (Chang et al, 2021; Frelich et al, 2019). However, strong correlational evidence suggests that earthworms decline following fencing to exclude deer in northeastern forests (Dávalos, Simpson, et al, 2015; Mahon & Crist, 2019). Fencing to exclude deer may therefore be beneficial, especially as we also found that fencing decreased V. rossicum as well as A. petiolata , another common plant invader.…”

“…In North America, greater earthworm abundance and diversity are also associated with lower plant diversity and more graminoids (Craven et al, 2017). Additionally, earthworms alter competitive outcomes of interactions between native and invasive species (Nuzzo et al, 2009; Whitfeld et al, 2014) and may become more abundant in the presence of deer (Dávalos, Simpson, et al, 2015; Mahon & Crist, 2019). Invasive plants, earthworms, and white‐tailed deer may therefore interact with each other (Dávalos et al, 2014; Fisichelli & Miller, 2018) to drive plant community change in forests in the northeastern United States.…”

Large herbivores facilitate a dominant grassland forb via multiple indirect effects

“…We have focused on a few pathways, but acknowledge that other direct and indirect effects of large herbivores on the target forb species may be operating in our study system. These may include direct negative effects such as trampling (Schrama et al, 2013;van der Wal & Brooker, 2004), and indirect effects such as the deposition of animal excreta (Augustine & McNaughton, 2006;Day & Detling, 1990;Frank et al, 2018;Wang et al, 2018), the influences on insect herbivores (Huntzinger et al, 2008;Rambo & Faeth, 1999;van Klink et al, 2015;Zhong et al, 2017), pollinators (Guy et al, 2021;V azquez & Simberloff, 2004), seed and seedling predators (Foster et al, 2014;Goheen et al, 2010;Maclean et al, 2011), and decomposers (Eldridge et al, 2017;Mahon & Crist, 2019;Sankaran & Augustine, 2004). Further investigations are needed to assess the relative importance of these lessstudied indirect factors in mediating plant population and communities (see Figure 6).…”