1. Effects of non-native earthworms on mycorrhizal fungi and tree seedling growth
Melissa McCormick
Katalin Szlavecz
Brenda Nieto
Lijun Xia
Dennis Whigham

2. "On a global basis...the two great destroyers of biodiversity are, first habitat destruction and, second, invasion by exotic species” - E.O. Wilson
ethanzuckerman.com
Image from The Nature Conservancy’s Wildland Invasive Species Task Force
appomattoxnews.com

3. Invasive Species
An invasive species is “an alien species whose introduction does, or is likely to cause, economic or environmental harm or harm human health”
In the U.S. there are nearly 6,600 non-native species
Invasive species have influenced all U.S. ecosystems
The current annual environmental, economic, and health-related costs of invasive species exceed those of all other natural disasters combined (estimated at $122 Billion in 2000).
Ehrenfeld 1997, Cox 1999, Rossman 2001, USGS 2010, Pimentel et al

4. Invaders under our feet
Below-ground biological invasions have gone largely unnoticed until recently:
Apart from a few familiar cases of Argentine fire ants (Solenopsis invicta) in Oceania and North America,
the Formosan termite (Coptotermes formosanus) in South Africa and the southeastern United States,
and the New Zealand flatworm (Arthurdendyus triangulatus) in the British Isles.
Photos courtesy Chi-han Chang

5. Exotic earthworms around the world
Hendrix et al Pandora’s box contained bait

6. Exotic Earthworms in North America
After last Ice Age many unutilized opportunities
Native
Introduced
James, 1995
Reynolds,1995

7. Earthworm invaders
Introduced earthworms now occur in every biogeographic region in all but the driest or coldest habitat types on Earth.
Hendrix et al. 2008

8. Earthworms
GOOD?
BAD?

9. Earthworm species differ
Amynthas hilgendorfi- Asian
Lumbricus rubellus - European
Eisenoides loennbergi - Native
Bouche 1977
Lumbricus friendi - European
Octolasion lacteum - European

10. PLANT FUNGUS Mycorrhizas Definition Mycorrhizal Function
INTRODUCTION
Definition
A mycorrhiza is a symbiotic association between a fungus and a plant root.
Mycorrhizas
Source: Smith & Read 1997
Mycorrhizal Function
A bi-directional exchange of nutrients
PLANT
FUNGUS
Carbon
Soil Nutrients

11. Conifers, Oaks, Hickories, Beeches, Birches, Chestnut ECM
Mycorrhizae have been identified in fossils of plants as early as 400mya and are considered crucial to plants adapting to life on land (Taylor et al. 1995, Taylor & Krings 2005, Krings et al. 2007).
Nearly all forest plants are mycorrhizal...except for some invasive species.
Conifers,
Oaks, Hickories,
Beeches,
Birches,
Chestnut
ECM
Tulip poplar,
Sweetgum, Maples,
Ashes,
Elms,
Sycamore AM

12. How do we look at fungi in the soil?
Extract DNA from soil
There are LOTS of fungi in the soil!
Up to 150 species in 0.5g of soil.
2 samples 15cm apart may share only 25% of their species.
We use specific PCR primers to look only at the DNA from the fungi we are interested in.
Soil core
Fungal DNA

13. Quantifying fungi in the soil:

14. A field experiment
Smithsonian Environmental Research Center (SERC), Edgewater, MD
48 plots (1mx1m) were trenched to 50 cm depth, lined with mesh screen and backfilled.

15. Manipulating earthworms
Earthworms were removed from half of the plots by repeated electroshocking.

16. Tree seedlings and leaf litter
Leaf litter was added (beech on one side and tulip poplar on the other) and seedlings planted in the plots.

17. Measured variables / expectations
Soil Processes:
Decomposition ↑
Respiration ↑
Abundance of microbial taxa (qPCR):
Mycorrhizal fungi
ECM (Tomentella, Russula) ↓
AM ↓
Tree seedling performance
Growth (biomass) ?
Plant mycorrhizal colonization ↓

18. Decomposition:
Decomposition was greater in forests with earthworms if mesh size allowed earthworms to access leaf litter. * *
Szlavecz et al. In press

19. Respiration:
Respiration was higher in plots with earthworms, especially on the side with tulip poplar leaf litter.
Mature Forest
Successional Forest

20. Mycorrhizal fungi were less abundant in plots with earthworms
Site p<0.001
EW p=0.08
Site x EW p=0.06
Site p<0.001
Site x EW p=0.08
Site p<0.001
EW p=0.05
0.14
AM fungi
Tomentella
Russula
0.12
0.10
0.08
(ng DNA/g dry soil/total quantified DNA)
0.06
Proportional Abundance
0.04
0.02
0.00
Old forest
Young forest
Old forest
Old forest
Young forest
Young forest
Site
No Earthworms
Earthworms

21. Log above-ground biomass
Tree seedling growth
Alex Binck
Oaks and beeches grew less in plots with earthworms. Maples grew more.
no EW EW
Oak ↓
Beech ↓
Maple ↑
old
young
-4.0
-3.5
-3.0
-2.5
-2.0
P=0.07
Tulip ↑
old
young
-2.00
-1.25
-0.50
0.25
1.00
old
young
-2.00
-1.50
-1.00
-0.50
0.00
-1.5
P=0.07
P=0.09
old
young
Log above-ground biomass
(mean g + se)
-2.0
-2.5
-3.0
-3.5
Few Tulip poplar seedlings survived in old forests and none in old forest plots without earthworms.
Forest Age

22. Key Conclusions
Earthworm activities affected mycorrhizal fungi and tree seedlings:
Mycorrhizal fungi were less abundant in plots with earthworms.
Earthworms affected growth of red oak and beech but not maple or tulip poplar.
Earthworm effects on tree seedlings differed with species:
Changes to nutrients affected early successional trees (+).
Changes to mycorrhizal fungi affected late successional trees (-).

23. What does this mean for our forests?
Forest composition may change:
Early successional trees may be better able to use nutrients made available by earthworms and may dominate longer.
Invasive plants may increase.
Forest floor habitat for ground-nesting birds may decrease.
Keep non-native earthworms out of forests where they haven’t already invaded:
Increase awareness of bait release, moving plants, compost (especially vermicomposting), and mulch.

24. Acknowledgements Funding: Field Help: USDA-CSREES 2007-35320-18375
NSF (EAR )
Smithsonian Women’s Committee
Field Help:
Jay O’Neill
Alex Binck
Matt Sievers
Scott Pitz
Helen Huang
Natalie Bray
Chi-Han Chang
Mike Bernard