Snakeworms-Pheretimoids Invasive in horticulture and forests

Josef Gorres Maryam Nouri-Aiin Earthworms in the USA

Pheretimoids are a group of Asian earthworms that used to be in a now defunct genus called , including the snake worms

How many species…in USA? 172 species (about 1/3 are exotic, ~1/10 are pheretimoids) 42 Genera 11 Families How Many Species in Vermont?

• 20 total species • 19 exotic species • 1 North American species (Sparganophilus Eiseni) • 4 Pheretimoid species • 3 of which are of concern • agrestis • • hilgendorfi. Seen this?

First diagnostic for earthworm invasions: Low understory cover and diversity History of Earthworm invasions in N. America No native earthworms Extent of last glaciation (Wisconsian)

Native earthworms

https://collections.slsa.sa.gov.au/resource/PRG+1373/19/50 First wave of invasions: European worms Lumbricidae: e.g. night crawler, Red worm

Second wave: : Great Lakes Worm Watch Snake worms… Japan gave 3,020 cherry blossom trees as a gift to the United States in 1912 to celebrate the nations' then-growing friendship, replacing an earlier gift of 2,000 trees which had to be destroyed due to disease in 1910. These trees were planted in Sakura Park in Manhattan and line the shore of the Tidal Basin and the roadway in East Potomac Park in Washington, D.C. The first two original trees were planted by first lady Helen Taft and Viscountess Chinda on the bank of the Tidal Basin. The gift was renewed with another 3,800 trees in 1965.[63][64] In Washington, D.C. the cherry blossom trees continue to be a popular tourist attraction (and the subject of the annual National Cherry Blossom Festival) when they reach full bloom in early spring.[65] Just outside of Washington, D.C., the suburb of Kenwood in Bethesda, Maryland has roughly 1,200 trees that are popular with locals and tourists.[66] From Wikipedia…

Image: National Park Service Biogeography of Pheretimoids

Original Range Canada • Japan • 1 single report of 2 species in southern-most Ontario • Korea (Reynolds, 2018) • Taiwan US • China • Reported from 37 States (Reynolds, 2018) mimizu • Sixteen pheretimoid species (Chang et al., 2016)

Red - main sources of the three species we are most concerned with at this point in time When were they first reported in some states? • California - 4 species 1860s to 1950s

• Connecticut – 5 species 1950s California earliest records in USA • Delaware – 3 species 2014 Amynthas diffringens 4 epi-endogeic 1862 Gates (1972c) Amynthas hawayanus 5 epi-endogeic 1953 Gates (1967a) • DC – 1 species 1937 Amynthas hilgendorfi 6 epi-endogeic 1958 Reynolds (1978a) • Florida – 13 species 1950 – 2010s Metaphire californica epi-endogeic 1866 Kinberg (1867) • Georgia -12 species 1936 – 1969 4. Renamed A. cortices • Illinois – 5 species 1914 – 2014 5. Renamed A. gracilis • Maine – 7 species 1954 6. Reclassified and renamed Metaphire hilgendorfi • New York – 6 species 1940 - 1999 • Vermont – 4 species 2011 - 2012

Reynolds, 2018 In Northeast, co-invasion of three species

Pheretimoid communities at some selected survey sites, color means Pheretimoids that travel together, presence of species, 30 sites … succeed together? • Amynthas tokioensis, T • 2 – 8 cm length • Usually, most abundant in community • , A • 7 – 14 cm length • Next most abundant • Metaphire hilgendorfi, H • 12 – 25 cm length • Least abundant

Chang et al., 2017 Where in the Northeast? Georeferenced Sites

Moore et al., 2017 How do they get around: The three most common vectors

Horticulture, Waste Recycling/Reuse, Bait Waste Recycling/Reuse

The Waste Pyramid The Problem • Recycling products of yard waste • Compost • Leaf mulch (uncomposted) • Reuse and recycling at home is best for stopping the spread

https://www.epa.gov/smm/sustainable-materials- management-non-hazardous-materials-and-waste- management-hierarchy Google maps

Raised beds Many Gardens Forest edge…

https://www.fs.usda.gov/detailfull/r4/fire- aviation/?cid=fseprd526615&width=full Vermicomposting

Internet sales of composting worms • Vendors used to be unaware of problems

• Now, their sales are a bit more nuanced • http://www.wormfarmfacts.com/ Alabama-Jumper.html • Some factual mistakes in this sales pitch. Horticulture Commercial Sales Plant Club/Neighbors/Friends/Family • Plant exchanges/Fund raising Plant sales • Be responsible… • Exchange with bare roots.. • Don’t exchange when you have these worms in your garden Characteristics and Life History Ecophysiological Group of Pheretimoids: Epi-endogeic

Makes them good mixers of mineral and organic horizons The looks and the moves

Some facts • Pheretimoids • A group of species in several genera that were formerly in the obsolete genus of Pheretima • 16 species in North America • Invasive pheretimoids in Vermont are from Japan and Korea • Species of concern in northern New England are • Amynthas agrestis • Amynthas tokioensis • Metaphire hilgendorfi • Thought of as parthenogens, but a small number may be able to have sex.

Diagnostics of pheretimoid worms: movement and clitellum goes all around body; they also thrash in your hand 250

] 2011 2 Life History Details - 200 2013 [m A 2014 Most interesting points 150 2015 100 Annual life cycle for the three snake worm 50 species we are most concerned with Abundance 0 10-Apr 19-Jul 27-Oct

Adults first appear between beginning of July A – Total Abundance 250 Date

] 2 and late August. B – Juvenile Abundance - 200 B 150 Cocoons produced from July to November. C – Adult Abundance 100

Steep increase in abundance in spring/early 50 Unpublished data [m Abundance summer varies also 0 10-Apr 19-Jul 27-Oct 150

] Date 2

There is a decrease in late early/mid July - Richardson et al 2009: 100 There appear to be some hatchlings in Die below 40 F and above 90 F C October 50

Abundance [m Abundance Unpublished data In nurseries they are ~3 weeks ahead of 0 forest populations. Sometimes 2 generations 10-Apr 19-Jul 27-Oct in nurseries. Date Cryptic part of the populations

Drought and cold dehydration Rehydrated cocoons

Cold hardy to at least -24oC. Other species to at least -400C Hatchlings emerge between 40 and 50 F, but …. Cocoon Bank? –always some cocoons ready to hatch

Figure 6: Embryo development in A. tokioensis cocoons Ecological Effects of the Invasion Effect of European Earthworms on Forest Soil Structure

Before Invasion After Invasion

Mor-type (duff) forest floor: Seed bank and Mull-type forest floor germination medium Dense A -horizon

Photo credits: Great Lakes WormWatch whose web page is a great resource Forest Soil Modifications by A. agrestis

Diagnostic of pheretimoid 5 cm castings Invasions Loose casting layer }

A Horizon B- Horizon B Horizon Earthworm invasions kick off a cascade of events

• Starting with the modification of soil structure

• May end with or include • modifications of decomposer community (e.g. Snyder et al., 2011; Zhang et al., 2010) • reduction in the abundance of larger fauna (birds, salamanders) (e.g. Ziemba et al., 2017; Loss et al., 2011) • reduction in forest plant biodiversity (e.g. Hale et al., 2006) • more invasive plants (e.g. Nuzzo et al., 2009) • remobilization of toxic trace metals (e.g. Richardson et al., 2015) • Altered nutrient and carbon cycles (e.g. Burtelow et al., 1998; Bohlen et al. 2004) Effect on Plant Biodiversity

Forests: Reduced biodiversity, reduced Horticulture: plant damage? tree regeneration.

Diagnostic of pheretimoid Invasions Loose casting layer: In this image the snakeworm has exposed the roots of a showy Ladyslipper which caused the demise of the Ladyslipper The Challenge of Controlling Pheretimoids

The earthworms themselves The very hardy cocoons (egg casings)

A. agrestis on woody mulch, up to 200 juveniles per 1000 to 2000 per square meter Square meter If there were a magic pixie dust, when would you sprinkle it? Multi-year cocoon bank? Total pheretimoids in a forest, First Adults intervene before first adults develop Adults in a forest

250 150 First 2011 C

200 Adults 2013

]

]

2

- 2 2014 - 100 150 2015

100

50

Abundance [m Abundance Abundance [m Abundance 50

0 0 10-Apr 30-May 19-Jul 7-Sep 27-Oct 10-Apr 30-May 19-Jul 7-Sep 27-Oct Date Date In gardens and nurseries the worms tend to become adults earlier Possible Interventions

Chemical – Physical measures However • No legal vermicides • Efficacy on pheretimoids not • Irritants drive the worms to the surface and some kill them been tested at large scale! • Mustard solution • Non-target effects (molluscicides • Early Bird ® contains molluscicide may act on fish)? • Maybe use them as a pot drench. • Admix sharp edged (angular) • Effective on worms but what of biochar/sands the cocoons? • Solarization on impervious ground • Prescribed burns don’t directly kill these worms in forests!!!! Don’t let them escape! http://westernipm.org/index.cfm/ipm-in-the- west/agriculture/soil-solarization-in-the-pacific-northwest/ Unpublished data More interventions

Naturally occurring microbial pathogens Flat worms, geckos and others • Maryam Nouri-Aiin has isolated some agents from dead cocoons • Flat worms (planeria) are worm and worms. predators • Need to replicate last years bio- • But exotic species themselves assays • Now found in northeastern USA • Were effective on juveniles regularly • Not so much on adults • May not work on pheretimoids • Need to better characterize the • Some lizards are vermivores pathogens Arun T.P., Bugwood.org, • Birds eat them (American www.invasive.org/browse/detail.c fm?&imgnum=5379895 Woodcock – obligate vermivore) Take home message

Spread Control • These worms are currently • But no effective best making the leap into the wild horticultural practices, yet

• There are common vectors • No effective method of • Horticulture controlling them in gardens or • Waste use, transport of earth materials forests • Maybe bait and other leisure activities • Some promise from biocontrol Acknowledgments

Collaborators Funders • Eppley Foundation for Research • Joseph Schall, UVM • College of Agriculture and Life Science, UVM • Erin Keller, UVM • Hardy Plant Club of Northern • Bradley Herrick, UW Vermont • Margaret Skinner, UVM • North American Maple Syrup • Bruce Parker, UVM Council • Chittenden County Maple Sugermakers Association Questions