The uptake and storage of carbon in North American temperate forests is an important ecosystem service, locking up a portion of the carbon that would otherwise accumulate in the atmosphere as carbon dioxide, a potent greenhouse gas. Forests in the northern hemisphere take up many million tons of carbon annually and store about half of it in soils. Various factors can affect rates of forest carbon storage, including invasive species, which can dramatically change above and below-ground processes. One such invader that has tremendous potential to affect carbon storage in forest soils is the exotic earthworm, whose burrowing and feeding are central to soil function and soil carbon distribution. Human activities of the past century have led to introductions of several earthworm species into North American temperate forests. Although there has been a lot of recent research on earthworm invasions, no single study has examined changes in all pools of soil carbon that may be impacted. Further, no other study has examined how interactions among different earthworm species will affect carbon storage. This project will answer unresolved questions regarding changes in forest carbon storage in response to invasions involving multiple earthworm species.

This research will have important implications for assessments of exotic earthworm invasion impacts on forest carbon balances in temperate regions. Further, results will improve our understanding of biological invasions on temperate forests and their impacts on forest environmental, economic, and cultural values. The project also has an important international collaboration component that involves researchers in France, where these worms invaded forests long ago. Outcomes will have implications for science policy. For example, there are no current restrictions on the importation of exotic earthworm species to the U.S., nor is there current legislation designed to limit their further spread.

Project Report

This project contributes to our understanding of forest ecosystem service shifts in response to exotic earthworm invasions across North American temperate forests. Specifically, dissertation research supported by this award has (1) characterized spatial and temporal variability of exotic earthworm communities in a north temperate forest; (2) established fundamental baseline data to compare earthworm community impacts on soil carbon (C) budgets; and (3) described patterns of litter carbon (C) and nitrogent (N) redistribution by earthworm community composition and soil texture. (1) Earthworm community spatial and temporal patterns. We conducted field surveys over two years in a forest representative of the upper Great Lakes region, and where exotic earthworm species were first documented in the1950s. Communities included five species with varying densities: Lumbricus rubellus ≥ L. terrestris >> Dendrobaena octaedra ≥ Aporrectodea spp. (A. trapezoides + A. caliginosa). We observed unique associations between species distributions, environmental conditions, and potential introduction sites. L. terrestris and L. rubellus densities were positively associated with soil C and N content, Acer rubrum (red maple) litter inputs, and soil moisture; and negatively associated with Pinus strobus (white pine) litter inputs. D. octaedra and Aporrectodea spp. densities were negatively associated with plot-to-road distance. Total earthworm density and biomass positively associated with soil moisture and leaf litter inputs. Increased leaf litter decomposition was associated with L. terrestris and Aporrectodea spp. densities, and total earthworm biomass. These results characterize exotic earthworm distributions at scales relevant to forest ecosystem processes (100m – 1000m), allowing for future extrapolation of laboratory and controlled field studies across northern temperate forests. (2) Earthworm community impacts on soil C storage. We used a laboratory experiment to examine the impacts of earthworm species belonging to three ecological groups (L. terrestris [Anecic = litter feeding, vertical burrowing], A. trapezoides [Endogeic = mineral soil feeding and burrowing], and E. fetida [Epigeic = litter feeding, surface–dwelling]) on the structure and C budgets of forest soils. Over one year, we measured CO2 and dissolved organic carbon (DOC) losses, leaf litter decomposition, and soil C storage. Earthworm burrow system structure differed across earthworm treatments, but did not affect CO2 or DOC losses. Soil CO2 loss was 30% greater from the Endogeic×Epigeic treatment than from controls (no earthworms) over the first 45 days; though cumulative CO2 and DOC losses were similar across all treatments. Anecic species additions accelerated litter decomposition by 31 – 39%, with the greater red maple and aspen litter decomposition indicative of feeding preferences. Burrow system structure controlled vertical C distribution by mediating leaf litter contributions to A-horizon C and N pools, as indicated by (a) strong correlations between sub-surface vertical burrows and accelerated leaf litter decomposition; and (b) dense burrow networks in the A-horizon and the C and N properties of these pools. Final soil C storage was slightly lower in earthworm treatments, indicating that increased leaf litter C inputs into soil were more than offset by CO2 and DOC losses across earthworm community treatments. (3) Mediation of litter C and N redistribution by earthworm community composition and soil texture. In a second laboratory experiment, we tested (1) the potential for A. trapezoides [Endogeic = mineral soil feeding and burrowing] to modify the earthworm community impacts on forest soil carbon redistribution, and (2) how soil texture, a key environmental driver of earthworm distributions, constrains earthworm community impacts. Using isotopically enriched (13C and 15N) red maple (A. rubrum) litter additions and two soil textures (sandy/spodosol and clay-rich/alfisol) prevalent across the Great Lakes region, we quantified the co-transport of leaf litter C and N into forest soils by earthworm communities. The A-horizon was the dominant sink for leaf litter C and N, with 13C and 15N recovery significantly higher in clay-rich soils (50 – 85%) and in sandy soils containing both endogeic and anecic earthworm species (30 – 40%). Earthworm communities containing endogeic species also increased burrow soil 13C and 15N recovery relative to epigeic populations of equal biomass by 10 - 15%. Soil texture constrained litter C and N retention in the B-horizon with higher 13C recovery observed in clay-rich soils, and higher 15N recovery observed in sandy soils with mixed earthworm community treatments. These results highlight the importance of earthworm species interactions and environmental conditions in mediating nutrient cycling in north temperate forest soils. Through working at the interface of community ecology, earthworm ecology, and ecosystem ecology, this research has important implications for assessments of exotic earthworm invasion impacts on forests in temperate regions. Research findings have been disseminated to the broader scientific community through oral presentations at national conferences and scientific publications. Over the past five years, this work has also supported undergraduate student research and fostered interdisciplinary collaborations with researchers at the French National Institute of Agricultural Research, the University of Michigan Biological Station, and the University of Michigan School of Radiology.

Agency
National Science Foundation (NSF)
Institute
Division of Environmental Biology (DEB)
Type
Standard Grant (Standard)
Application #
1110494
Program Officer
Henry L. Gholz
Project Start
Project End
Budget Start
2011-06-01
Budget End
2013-05-31
Support Year
Fiscal Year
2011
Total Cost
$15,000
Indirect Cost
Name
University of Michigan Ann Arbor
Department
Type
DUNS #
City
Ann Arbor
State
MI
Country
United States
Zip Code
48109