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Invasive earthworms unlock arctic plant nitrogen limitation.

ABSTRACT: Arctic plant growth is predominantly nitrogen (N) limited. This limitation is generally attributed to slow soil microbial processes due to low temperatures. Here, we show that arctic plant-soil N cycling is also substantially constrained by the lack of larger detritivores (earthworms) able to mineralize and physically translocate litter and soil organic matter. These new functions provided by earthworms increased shrub and grass N concentration in our common garden experiment. Earthworm activity also increased either the height or number of floral shoots, while enhancing fine root production and vegetation greenness in heath and meadow communities to a level that exceeded the inherent differences between these two common arctic plant communities. Moreover, these worming effects on plant N and greening exceeded reported effects of warming, herbivory and nutrient addition, suggesting that human spreading of earthworms may lead to substantial changes in the structure and function of arctic ecosystems.

SUBMITTER: Blume-Werry G

PROVIDER: S-EPMC7156384 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Invasive earthworms unlock arctic plant nitrogen limitation.

Blume-Werry Gesche G Krab Eveline J EJ Olofsson Johan J Sundqvist Maja K MK Väisänen Maria M Klaminder Jonatan J

Nature communications 20200414 1

Arctic plant growth is predominantly nitrogen (N) limited. This limitation is generally attributed to slow soil microbial processes due to low temperatures. Here, we show that arctic plant-soil N cycling is also substantially constrained by the lack of larger detritivores (earthworms) able to mineralize and physically translocate litter and soil organic matter. These new functions provided by earthworms increased shrub and grass N concentration in our common garden experiment. Earthworm activity ...[more]

PMID: 32286301

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Project description:Asian pheretimoid earthworms (e.g. Amynthas and Metaphire spp.) are invading North American forests and consuming the vital detrital layer that forest floor biota [including the keystone species Plethodon cinereus (Eastern Red-backed Salamander)], rely on for protection, food, and habitat. Plethodon cinereus population declines have been associated with leaf litter loss following the invasion of several exotic earthworm species, but there have been few studies on the specific interactions between pheretimoid earthworms and P. cinereus. Since some species of large and active pheretimoids spatially overlap with salamanders beneath natural cover objects and in detritus, they may distinctively compound the negative consequences of earthworm-mediated resource degradation by physically disturbing important salamander activities (foraging, mating, and egg brooding). We predicted that earthworms would exclude salamanders from high quality microhabitat, reduce foraging efficiency, and negatively affect salamander fitness. In laboratory trials, salamanders used lower quality microhabitat and consumed fewer flies in the presence of earthworms. In a natural field experiment, conducted on salamander populations from "non-invaded" and "pheretimoid invaded" sites in Ohio, salamanders and earthworms shared cover objects ~60% less than expected. Earthworm abundance was negatively associated with juvenile and male salamander abundance, but had no relationship with female salamander abundance. There was no effect of pheretimoid invasion on salamander body condition. Juvenile and non-resident male salamanders do not hold stable territories centered beneath cover objects such as rocks or logs, which results in reduced access to prey, greater risk of desiccation, and dispersal pressure. Habitat degradation and physical exclusion of salamanders from cover objects may hinder juvenile and male salamander performance, ultimately reducing recruitment and salamander abundance following Asian earthworm invasion.

Project description:We test whether the invasive earthworm Lumbricus terrestris and leaf litter of the invasive herbaceous plant Alliaria petiolata interact to influence the native plant, Podophyllum peltatum, using both observational field data and a multi-year experiment. We hypothesized invader interactive effects on the native plant might result from either changes in allelochemical distribution in the soil or nutrient availability mediated by the invasive earthworm pulling leaf litter down into the soil. Within the field data we found that Alliaria petiolata presence and higher soil nitrogen correlated with reduced Podophyllum peltatum cover, and no evidence for an invader-invader interaction. Within the factorial experiment, we found a super-additive effect of the two invaders on plant biomass only when activated carbon was present. In the absence of activated carbon, there were no differences in Podophyllum peltatum biomass across treatments. In the presence of activated carbon, Podophyllum peltatum biomass was significantly reduced by the presence of both Lumbricus terrestris and Alliaria petiolata leaf litter. The absence of an effect of Alliaria petiolata leaves without activated carbon, combined with a failure to detect arbuscular mycorrhizal colonization, suggests that indirect effects of allelochemicals on arbuscular mycorrhizal fungi were not the primary driver of treatment responses. Rather direct nutrient availability might influence a potential interaction between these invaders. Leaf nitrogen content was higher and leaf CO2 concentration was lower in the presence of Lumbricus terrestris, but treatment did not influence maximum photosynthetic rate. While the field data do not suggest a negative interaction between these invaders, the experiment suggests that such an interaction is possible with greater environmental stress, such as increasing nitrogen deposition. Further, even plants with rapid physiological responses to increased nitrogen availability may have other physiological limits on growth that prevent them from compensating from the harm caused by multiple invaders.

Dataset Information

Invasive earthworms unlock arctic plant nitrogen limitation.

Publications

Invasive earthworms unlock arctic plant nitrogen limitation.

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