Ecological effects if exotic earthworm invasion in hardwood forests

Lee E. Frelich
Director, The University of Minnesota Center for Hardwood Ecology Chair, MNDNR Commissioners Advisory Committee on Natural Areas and Nongame Wildlife Vice President, The Eastern Native Tree Society Vice Chair, Great River Greening Board

It may be doubted whether there are many other animals which have played so important a part in the history of the world, as have these lowly organized creatures.
-Charles Darwin, 1881

Global warming or Global worming?

Earthworms are ecosystem engineers that can alter the structure of soil, and change the H2O, N and P cycles, C dynamics and seedbed characteristics on a regional scale

Earthworm Invasion

Temperate Deciduous Forests

No earthworms before European settlement

(Modified from Hendrix and Bohlen 2002)

Multiple Ecological Groups

Endogeic -Mineral soil dweller -Rich soil feeder -Small-med. size Midden Epigeic -Litter dweller -Litter feeder -Small size

Anecic -Soil dweller -Litter and soil feeder -Vertical burrows -Large size (Modified from Brown 1995)

Common Earthworm Species and Ecological groups

Epigeic: Dendrobaena octaedra

Anecic: Lumbricus terrestris (nightcrawler)

~ 1 in.

Epi-endogeic: Lumbricus rubellus

Endogeic: Aporrectodea caliginosa

Dave Hansen

Liquid mustard extraction of earthworms

Photo: Dave Hansen, University of MN

Bellwort (Uvularia grandiflora)

Photos: Dave Hansen, University of MN

Nodding trillium (Trillium cernuum)

Twisted stalk (Streptopus roseus)

Yellow violet (Viola pubescens)

Photos: Dave Hansen, University of MN

Sweet cicely (Osmorhiza claytonii)

Blue cohosh (Caulophyllum thalictriodes)

Photo: Dave Hansen, University of MN

Photo: Dave Hansen, University of MN

Forest floor with heavy earthworm infestation

Photo: Dave Hansen, University of MN

Before earthworm invasion

Photo: Dave Hansen, University of MN

and after earthworm invasion

Examples of negatively and positively impacted plant species Negative

Bellwort Spikenard Yellow violet Trillium Solomons seal Sweet cicely

Positive
Penn sedge Jack-in-the-pulpit

Photo: Dave Hansen, University of MN

Soil profile, no earthworms

Photo: Dave Hansen, University of MN

Soil profile with earthworms

L. terrestris litter preferences

Effects of earthworm invasion on soils

Duff disappears N and P availability goes down Compaction-density goes up

Decrease in tree-ring width caused by earthworm invasion in maple forest

1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 -5 0 5 10 15 20 25 30 Invasion timing (years)

Ring width index

Worm free worm invaded

Photos: Cindy Hale

Greenhouse experiment by Cindy Hale

Consumption of duff by earthworms

Cindy Hale

Cindy Hale

Exposed fine root system of a spikenard plant

Cindy Hale

Sugar maple seedling tipped over

Regional Survey of earthworm abundance in the northern hardwoods: Andy Holdsworth

Forests in: Chippewa National Forest Chequamegon National Forest Natural areas near the Twin Cities
Twin Cities*

Modeled Occurrence of Heavily-Invaded Areas

Probability of Heavy Earthworm Invasion Low (0-0.1) Roadless Areas Moderate (0.1-0.5) High (0.5-0.9) Very High (0.9-1) Roads Lakes 1 km

David Augustine

Deer density measurement with cameras

Experiments show that deer grazing can cause two alternate states for the plant communitylush and sparse that depend on deer to plant ratio

Photos: David Augustine

Sylvania Wilderness maple and hemlock forest in 1988

Sylvania in 2006

Forest decline caused by European earthworms in Minnesota hardwood forests

Recent literature shows that Earthworms also facilitate germination and establishment of European buckthorn and garlic mustard by changing the seed bed

Photos: The Nature Conservancy

Kathleen Knight

A Lurking Invader Dusky slug (Arion subfuscus)

- Non-native slug of European origin - First recorded in N. America 1802 1 cm
Photo: P. Myers

- Likely introduced via soil on nursery plants - Mostly mesic deciduous and conifer forests but not dry oak woods - Generalist herbivore and fungivore - Major predator of juvenile seedlings

(Chichester and Getz 1973; Nystrand and Granstrom 2000, Christel et al. 2002; Gardescu 2003)

Slug-Related Aboveground Mortality Varies by Plant Species

Wild Columbine
1.2 1.0
Mortality (Arcsin SqRt prop.)
1.2

Solomons Plume
1.0

R2=0.23 p=0.02
Mortality (Arcsin SqRt prop.)

0.8 0.6 0.4 0.2 0.0 1 2 3 4 5 6 7

0.8 0.6 0.4 0.2 0.0 1 2 3 4 5 6 7

A. subfuscus Density (SqRt #/m2)

A. subfuscus Density (SqRt #/m2)

Forest decline: Changes in forest floor, soils, and nutrients cause loss of the standing crop of plants, and with lack of seed source, slug predation on small seedlings, high deer populations to prey on larger plants,and facilitation of garlic mustard and buckthorn, some (many??) plant species are unable to recover

Andy Holdsworth

Carex pensylvanica carpets are resistant to deer and earthworms These sedge carpets present a challenge for tree regeneration and restoration of other plant species

Photos: Dave Hansen, University of MN

Forest decline syndrome at Wood-Rill (lower) as compared to Taylors woods (upper)

Future work on earthworm invasion

Earthworm introduction

Higher leaching rates; lower N and P availability, lower NPP Warmer, drier soils

Loss of duff; plant and tree seedling death

Higher deer:plant ratio; more plant death

Forest dieback and regeneration failure Increase in Pennsylvania sedge

Future work part IIEarthworms, facilitation of invasive Plants and invasional meltdown
European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America George E. Heimpel Lee E. Frelich Douglas A. Landis Keith R. Hopper Kim Hoelmer Zeynep Sezen Mark K. Asplen Kongming Wu In press Biological Invasions

Recent literature shows that Earthworms also facilitate germination and establishment of European buckthorn and garlic mustard by changing the seed bed

Kathleen Knight

Asian ladybeetle

Soybean aphid

?
European Starling

Oat crown rust

Common buckthorn

oats

soybean Asian flatworm European Earthworm

Future work part III--impacts of earthworms on groundnesting songbirds

Scott Loss, Ph.D. student, NRSM, Rob Blair adviser

Does earthworm invasion change Ovenbird habitat quality?

Relationship between earthworm mass (grams) and the density (birds/hectare) of Ovenbirds (OVEN) and Hermit Thrushes (HETH) on study sites in the Chequamegon-National Forest, Wisconsin, summer 2008 & 2009.

Future work part IVearthworm impacts on water quality

Watershed Implications of Earthworm Invasion at the headwaters of the MississippiItasca State Park Hal Halvorson, James Cotner, and Meghan Jacobson

Regression of earthworm abundance and lake water bacterial respiration rates from 6 lakes in Itasca State Park. These very preliminary results indicate earthworms are contributing to eutrophication.

Synthesis of warming climate effects on water I Warmer climate + hardwoods, less conifers Warmer water

+earthworms +P in water Eutrophication

Acknowledgements:
Chippewa NF, Dave Shadis and John Casson Chequamegon NF, Linda Parker Leech Lake Department of Resource Management, Steve and Carol Mortensen MNDNR Natural Areas, Bob Djupstrom Three Rivers Park District Funding National Science Foundation Wood-Rill Foundation, Ruth and Bruce Dayton MNDNR Nongame Species Research Grant University of MN Center for Hardwood Ecology University of MN Lydia P. Anderson Fellowship University of MN Doctoral Dissertation Fellowship University of MN Charles J. Brand Fellowship University of MN Carolyn Crosby Fellowship Applied Ecological Services Graduate Research Grant