Exotic Ecosystem Engineers Change the Emergence of Plants from the Seed Bank of a Deciduous Forest

Abstract

The anthropogenic spread of exotic ecosystem engineers profoundly impacts native ecosystems. Exotic earthworms were shown to alter plant community composition of the understory of deciduous forests previously devoid of earthworms. We investigated the effect of two exotic earthworm species (Lumbricus terrestris L. and Octolasion tyrtaeum Savigny) belonging to different ecological groups (anecic and endogeic) on the emergence of plants from the seed bank of a northern North American deciduous forest using the seedling emergence method. We hypothesized that (1) exotic earthworms change the seedling emergence from the plant seed bank, (2) L. terrestris increases the emergence of plant seedlings of the deeper soil layer but decreases that of the upper soil layer due to plant seed burial, and (3) O. tyrtaeum decreases plant seedling emergence due the damage of plant seeds. Indeed, exotic earthworms altered the emergence of plant seedlings from the seed bank and the functional composition of the established plant seedlings. Surprisingly, although L. terrestris only marginally affected seedling emergence, O. tyrtaeum changed the emergence of native plant species from the seed bank considerably. In particular, the number of emerging grass and herb seedlings were increased in the presence of O. tyrtaeum in both soil layers. Moreover, the impacts of earthworms depended on the identity of plant functional groups; herb species benefited, whereas legumes suffered from the presence of exotic earthworms. The results highlight the strong effect of invasive belowground ecosystem engineers on aboveground ecosystem characteristics and suggest fundamental changes of ecosystems by humanspread earthworm species.

Trophic cascades, invasive species and body-size hierarchies interactively modulate climate change responses of ecotonal temperate–boreal forest

“…Earthworms may be important seed and seedling predators with potentially strong effects on plant community composition [41]. Although interactions between earthworms and tree seeds have, to our knowledge, not been investigated, studies on herbaceous species stress strong selective pressure by earthworms on the fate of seeds, which is likely to change plant community composition of North American forest ecosystems [42]. Plant species not adapted to the presence of earthworms may suffer from their invasion, resulting in simplified herbaceous communities [39], which also play an important role in forest ecosystem function [43].…”

Ecological benefits and risks arising from liming sugar maple dominated forests in northeastern North America

“…In Minnesota, Larson et al (2010) found that sugar maple trees growing in invaded conditions were more sensitive to drought than trees growing in earthworm-free conditions. Other studies suggest that worm selectivity in seedling ingestion and their alteration of seedbed conditions can profoundly change plant community composition in deciduous forests (Hale et al 2005Frelich et al 2006;Holdsworth et al 2007;Eisenhauer et al 2009). The effects of liming on earthworms will be discussed further in section 4.3.…”

Non-native earthworms promote plant invasion by ingesting seeds and modifying soil properties

“…One of the most documented ecosystem alterations by non-native earthworms is the modification of the northern American hardwood forests following the colonization by European earthworms (Frelich et al, 2006;Hale et al, 2005). Indirect impacts of earthworms on plant community via soil modifications have also often been reported (Eisenhauer et al, 2009b(Eisenhauer et al, , 2007Holdsworth et al, 2007;Nuzzo et al, 2009), but only two studies have focused on the direct impact of non-native, invasive earthworms on plant communities through seed ingestion (Drouin et al, 2014;Eisenhauer et al, 2009b). In the first study, the effects of invasive earthworms, Lumbricus terrestris and Octoaedra tyrtaeum on seedling emergence in American northern hardwood forests were examined (Eisenhauer et al, 2009b).…”

“…Indirect impacts of earthworms on plant community via soil modifications have also often been reported (Eisenhauer et al, 2009b(Eisenhauer et al, , 2007Holdsworth et al, 2007;Nuzzo et al, 2009), but only two studies have focused on the direct impact of non-native, invasive earthworms on plant communities through seed ingestion (Drouin et al, 2014;Eisenhauer et al, 2009b). In the first study, the effects of invasive earthworms, Lumbricus terrestris and Octoaedra tyrtaeum on seedling emergence in American northern hardwood forests were examined (Eisenhauer et al, 2009b). The presence of the endogeic O. tyrtaeum significantly increased the emergence of all seedlings while the presence of the anecic L. terrestris increased the emergence of herb seedlings only.…”

“…The interactions between non-native species, and with their physico-chemical environment can lead to positive feedback loops, leading to drastic and irreversible changes in ecosystem functioning and the composition of communities that characterize an 'invasional meltdown' (Simberloff and Holle, 1999). Similarly, interactions of invasive earthworms with invaded plant communities favors a decline in native plant species and appears to facilitate plant invasions, at least in American northern hardwood forests (Eisenhauer et al, 2009b;Frelich et al, 2006;Hale et al, 2005). Nuzzo et al (2009) also suggested that earthworm invasion, rather than non-native plant invasion, was the driving force behind changes in forest plant communities in Northeastern North America.…”