Ecological effects if exotic earthworm invasion in hardwood forests

Lee E. Frelich

Director, The University of Minnesota Center for Hardwood Ecology

Chair, MNDNR Commissioner’s 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

No earthworms Temperate before Deciduous European Forests settlement

(Modified from Hendrix and Bohlen 2002) Multiple Ecological Groups

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

Midden

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 Positive Bellwort Penn sedge Spikenard Jack-in-the-pulpit Yellow violet

Trillium

Solomon’s seal

Sweet cicely 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 Worm free 0.8 worm invaded 0.6 0.4 Ring width index 0.2 0 -5 0 5 10 15 20 25 30 Invasion timing (years) Photos: Cindy Hale

Greenhouse experiment by Cindy Hale Cindy Hale Consumption of duff by earthworms 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) Moderate (0.1-0.5) Roadless Areas 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 community—lush 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

- Likely introduced via soil on nursery 1 cm plants Photo: P. Myers - 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 Solomon’s Plume 1.2 1.2 R2=0.23 p=0.02 1.0 1.0

0.8 0.8

0.6 0.6 Mortality Mortality 0.4 0.4 (ArcsinSqRt prop.) (ArcsinSqRt prop.) 0.2 0.2

0.0 0.0

1 2 3 4 5 6 7 1 2 3 4 5 6 7 A. subfuscus Density A. subfuscus Density (SqRt #/m2) (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 Taylor’s woods (upper) Future work on earthworm invasion

Earthworm introduction

Higher leaching rates; Loss of duff; plant lower N and P avail- and tree seedling ability, lower NPP death

Warmer, drier soils Higher deer:plant ratio; more plant death

Forest dieback and regeneration failure Increase in Penn- sylvania sedge Future work part II—Earthworms, 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 ? Oat crown European rust Starling

oats Common buckthorn

soybean

Asian flatworm European Earthworm Future work part III--impacts of earthworms on ground- nesting 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 IV—earthworm impacts on water quality

Watershed Implications of Earthworm Invasion at the headwaters of the Mississippi—Itasca 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 Warmer climate water

+ hardwoods, less conifers

+earthworms +P in Eutrophication water 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