Potential Edaphic and Aquatic Predators of a
Nonindigenous Asian Earthworm (Amynthas agrestis) in the
Eastern United States
John P. Gorsuch and Patrick C. Owen
Northeastern Naturalist, Volume 21, Issue 4 (2014): 652–661
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22001144 NORTHEASTERN NATURALIST 2V1(o4l). :2615,2 N–6o6. 14
Potential Edaphic and Aquatic Predators of a
Nonindigenous Asian Earthworm (Amynthas agrestis) in the
Eastern United States
John P. Gorsuch1, * and Patrick C. Owen1
Abstract - We examined the suitability of an invasive Asian earthworm, Amynthas agrestis
(Asian Crazy Worm or Alabama Jumper), as a prey item for a variety of native and naturalized
North American predators. We conducted no-choice feeding trials with three edaphic
predators—the nonindigenous Bipalium adventitium (Wandering Broadhead Planarian),
Scolopocryptops sexspinosus (Eastern Red Centipede), and Desmognathus monticola (Seal
Salamander)—and two aquatic predators, Nephelopsis obscura (Ribbon Leech) and Oronectes
rusticus (Rusty Crayfish). During feeding trials, Am. agrestis exhibited a variety of
novel defensive strategies, including apparent distastefulness, autotomization of posterior
body segments, secretion of a yellow fluid, and thrashing. Planarians, leeches, and salamanders
were more likely to capture lumbricid earthworm prey than Am. agrestis prey. Rusty
Crayfish showed limited differences in capture rates among the earthworm species, while
Eastern Red Centipedes were equally adept at capturing all earthworm species tested. Our
results suggest that endemic arthropods may provide a measure of biological resistance
against incipient Am. agrestis invasions.
Introduction
The megascoelecid earthworm Amynthas agrestis (Goto and Hatai) (Asian
Crazy Worm or Alabama Jumper) is an epigeic Asian earthworm that feeds on leaf
litter at the soil surface (Callaham et al. 2003). Subsequent to its introduction to
the United States, Am. agrestis has actively expanded into new habitats, including
undisturbed, remote, and high-elevation localities (Callaham et al. 2003, Gates
1982). Leaf litter constitutes an important physical and trophic resource in many
North American woodland ecosystems, and an invasion of epigeic earthworms can
lead to a reduction in leaf-litter volume (Maerz et al. 2009). The consequences of
leaf-litter reduction include an increase in the occurrence of nonindigenous plant
species (Maerz et al. 2009), a decline in woodland salamander abundance (Maerz et
al. 2009), and reductions in populations of native arthropods (Snyder et al. 2011).
Thus, the continued spread and persistence of Am. agrestis populations in North
America is cause for concern.
The success of Am. agrestis populations in North America (and, therefore, the
magnitude of their ecological impact) will partly depend upon their palatability and
vulnerability to local predators. Amynthas agrestis have been found to move about
actively on the soil surface (Callaham et al. 2003), and thus may be a convenient
1Biology Department, University of Cincinnati Blue Ash College, Cincinnati, Ohio 45236.
*Corresponding author - jgorsuch@biowishtech.com.
Manuscript Editor: Howard Ginsberg
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prey item for native, edaphic (soil-dwelling) predators that hunt at the soil surface.
The vulnerability of Am. agrestis to edaphic predators may partially determine the
earthworm’s long-term ability to occupy a given habitat.
Amynthas agrestis are also used as fishing bait in the eastern US under the
vernacular name “Alabama Jumper”, and they are common along stream banks in
central Kentucky, where fishermen refer to them as “Wood Eels” (J. MacGregor, KY
Department of Fish and Wildlife Resources, Frankfort, KY, pers. comm.). Therefore,
Am. agrestis may be a convenient prey item (albeit a transient one) for native
aquatic predators in streams used for recreational fishing.
Earthworms of the genus Amynthas are known to slither and thrash when disturbed,
traits which helped earned them notoriety among fishermen (J. MacGregor,
pers. comm.). Such unique defensive behaviors may impact Am. agrestis’ vulnerability
to native predators. We conducted a series of no-choice laboratory feeding trials
in which we examined the vulnerability of Am. agrestis to a variety of representative
predators that occupy forest floor and stream habitats in the eastern United States. We
tested Am. agrestis as a prey item for three predators that hunt at the soil surface—the
nonindigenous Bipalium adventitium (Hyman) (Wandering Broadhead Planarian),
Scolopocryptops sexspinosus (Say) (Eastern Red Centipede), and Desmognathus
monticola (Dunn) (Seal Salamander)—as well as two aquatic predators, Nephelopsis
obscura (Verrill) (Ribbon Leech), and Oronectes rusticus (Girard) (Rusty Crayfish).
No-choice feeding trials using the same predators also were conducted with the
nonindigenous lumbricid earthworms Lumbricus rubellus (Hoffmeister) (Red
Earthworm) and Aporrectodea longa (Ude) (Black-headed Worm), to test the baseline
effectiveness of these predators as consumers of earthworms.
Methods
Collection and maintenance of specimens
All earthworms used during the feeding trials were captured in the field and
maintained in the laboratory. We identified earthworms using Olson (1928, 1933)
and Reynolds (1978, 1995). We collected Amynthas agrestis from leaf-litter beds
along the banks of Swift Camp Creek, in the Red River Gorge area of the Daniel
Boone National Forest, KY, between 18 June 2011 and 6 August 2011. We selected
the lumbricid earthworms Lumbricus rubellus and Aporrectodea longa as controls
based upon their presence at the soil surface beneath flat stones and other cover
objects along stream banks and on the forest floor. We collected specimens from
University of Cincinnati Blue Ash campus grounds and housed all earthworms at
20 °C in plastic containers containing soil from the campus grounds as substrate.
Containers housing Am. agrestis were supplied with leaf litter for food (Zhang et al.
2010), and containers housing the lumbricid earthworm species were supplied with
coffee grounds and vegetable scraps for food (Zaborski 2002). We maintained all
predators individually in 10 cm x 10 cm plastic sandwich boxes with holes punched
for ventilation. Demographic and husbandry details for each predator species are
presented in Table 1. We maintained all predators in the laboratory at 20 °C.
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Table 1. Composition of predator groups in no-choice feeding trials. Taxonomy, colony size, mean and range of mass of individuals, source, and feeding
and watering details for all predator colonies utilized during the present study. Mass data for the size-matched earthworm prey which were paired with
each predator group during feeding trials are presented in the last three columns.
Ap. longa L. rubellus Am. agrestis
Mean mass mean mass mean mass mean mass
Predator n (range) Source Feeding Water (range) (range) (range)
Wandering Broadhead 12 47.5 mg Field Collected (OH) Redworms, Misted 0.34 g 0.40 g, 0.32 g
Planarian (20–75) 14-d intervals every 2 d (0.16–0.57) (0.11–0.81) (0.08g – 0.67)
n = 12 n = 12 n = 12
Eastern Red Centipede 15 0.48 g Field Collected (OH) Waxworm, Misted 0.22 g 0.45 g 0.41 g
(0.30–0.74) Moth Larva 2 x weekly (0.09–0.60) (0.24–0.57) (0.22–0.61)
7-d intervals n = 13 n = 15 n = 15
Seal Salamander 20 3.53 g Field Collected (KY) Crickets, Misted 0.25 g 0.37 g 0.39 g
(0.76–8.45) 7-d intervals every 2 d (0.12–0.43) (0.10–0.56) (0.15–0.60)
n = 20 n = 20 n = 20
Ribbon Leech 13 0.77 g Carolina Biological Redworms, Aquatic 0.34 g 0.53 g 0.49 g
(0.55–1.21) Supply 7-d intervals (0.12–0.89) (0.26–0.99) (0.24–1.02)
n = 13 n = 13 n = 13
Rusty Crayfish 13 6.34 g Field Collected (KY) Redworms, Aquatic 0.39 g 0.87 g 0.83 g
(4.25–8.97) 7-d intervals (0.19–0.85) (0.56–1.33) (0.62–0.99)
n = 13 n = 13 n = 13
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Feeding trials
For all feeding trials, we defined “capture” as any trial that resulted in the
complete consumption or death of the earthworm, as these outcomes achieve both
the removal of the earthworm from the ecosystem and the elimination of future
reproduction by that individual. We defined “escape” as any trial after which the
earthworm survived for 48 h and produced castings, as this outcome results in both
potential future fitness for the earthworm and continuing ecological impacts. Any
earthworm that appeared to survive an attack was placed into a separate container
lined with soil collected from campus grounds and observed for 48 hours to determine
survival. We defined a third potential outcome, “no contact”, as an event in
which the predator showed no interest in attacking the prey item.
Unless otherwise noted, all feeding trials were conducted under indirect, artificial
lighting at 20° C with the observer seated approximately 0.5 m away. Trials
were conducted in 10 cm x 10 cm plastic containers, with the exception of those for
Wandering Broadhead Planarians, which were conducted in petri dishes lined with
moistened paper towels. Because Amynthas are notoriously active and are apt to escape
from an open container, the containers were partially covered. We left the lids
ajar 2 cm to allow for observation while keeping both predator and prey contained
within the chamber. For aquatic predators, we filled containers with water sufficient
to cover the predator. For terrestrial species, we lined containers with moist paper
towels. Predators were introduced into the containers and allowed to acclimate for
1 minute, at which time we added an earthworm of the appropriate species to the
enclosure approximately 2 cm from the predator’s head. For all predators except
Eastern Red Centipede (which would not feed unless isolated in complete darkness,
see below), we recorded observations for ten minutes, at which point we scored the
trial either as capture, escape, or no contact, as defined above. To increase the likelihood
that all predators would be equally interested in feeding during trials, we fed
them on a schedule such that feeding trials fell on normal feeding days. Predators
that captured their earthworms were allowed to feed to satiation, and those that did
not were offered a different prey item of the type specified in Table 1. All predators
were used in three feeding trials, one with each earthworm species, while each
earthworm was used only once. Earthworm species were presented to predators in
random order.
Predator–prey pairs were size matched to minimize the impacts of size discrepancy
upon the outcome of feeding trials (Table 1). Although Wandering Broadhead
Planarians have been documented to attack earthworms from 55 times (Zaborski
2002) to 100 times (Ducey et al. 1999) their own mass, all feeding trials were conducted
with earthworms that were no more than 12 times the mass of their flatworm
opponents. We observed centipedes to be proficient at subduing large prey, and
earthworms of up to 1.5 times the mass of the centipede were used during feeding
trials. Earthworms used in Seal Salamander trials did not exceed 50% of the mass of
the salamander. For Ribbon Leeches, the earthworms used did not exceed the mass
of the leech. During trials with Rusty Crayfish, the earthworm prey did not exceed
the size of the crayfish.
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Eastern Red Centipedes did not feed under the same observation protocol as
described above. Instead, before each feeding trial, the mass of each centipede and
earthworm were recorded. Feeding trials were conducted by introducing an earthworm
of the appropriate species into each centipede’s enclosure and leaving it there
overnight. The following morning, earthworms were examined for bite marks and
evidence of envenomation, such as discoloration or liquefaction, and at this point
trials were scored as capture or escape.
Statistical analysis
G tests of independence were used to test the null hypothesis that earthworm
capture rates were independent of earthworm prey type (Quinn and Keough 2002).
If the null hypothesis of independence was rejected, then 95% confidence intervals
were calculated for odds ratios of predators capturing one earthworm prey species
over another to determine statistically significant comparisons between prey types.
If the confidence interval for an odds ratio did not include 1, this indicated a lack of
independence.
Results
Predators differed in their capture success for different earthworm species, except
for Red Centipedes, which successfully captured all three earthworm species
(Fig. 1, Table 2). Statistical analysis is presented in Table 2. In response to predator
attacks, Ap. longa and L. rubellus were observed writhing and secreting clear mucus.
In contrast, Am. agrestis were observed thrashing, autotamizing posterior body segments
and secreting a yellow fluid in response to predator attacks. Contact with this
yellow fluid was observed to cause a cessation of predatory activity during feeding
trials with the Wandering Broadhead Planarian. Such cessation was not observed in
Figure 1. Percentage of successful captures by each predator type for each of the three
earthworm species.
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Table 2 . Results of G tests of independence of the number of successful captures among prey types for each predator type. For each significant G, odds
ratios and confidence intervals were calculated to determine the likelihood of a predator successfully capturing one earthworm species over another. An
odds ratio indicated a lack of independence (α = 0.05) if its 95% confidence interval did not include 1 (indicated by *).
95% CI
Predator G df P Prey pair Odds ratio Lower Upper
Wandering Broadhead Planarian 11.00 2 0.0041 Ap. longa vs. L. rubellus 2.00 0.27 7.52
Ap. longa vs. Am. agrestis 1.40 2.05 235.93 *
L. rubellus vs. Am. agrestis 0.09 1.47 160.89 *
Eastern Red Centipede 0.56 2 0.7600 Ap. longa vs. L. rubellus 1.33 0.30 5.91
Ap. longa vs. Am. agrestis 1.75 0.40 7.66
L. rubellus vs. Am. agrestis 1.31 0.31 5.58
Seal Salamander 24.19 2 less than 0.0001 Ap. longa vs. L. rubellus 2.15 0.52 9.00
Ap. longa vs. Am. agrestis 36.00 5.80 223.40 *
L. rubellus vs. Am. agrestis 16.71 2.98 93.84 *
Ribbon Leech 17.67 2 0.0002 Ap. longa vs. L. rubellus 12.79 0.61 266.52
Ap. longa vs. Am. agrestis 81.00 3.76 1745.30 *
L. rubellus vs. Am. agrestis 6.33 1.22 32.96 *
Rusty Crayfish 7.84 2 0.0200 Ap. longa vs. L. rubellus 9.00 0.42 193.97
Ap. longa vs. Am. agrestis 23.40 1.51 475.28 *
L. rubellus vs. Am. agrestis 2.60 0.52 12.90
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response to contact with the mucous secretions of lumbricid earthworms. Seal salamanders
that struck at Am. agrestis often released the earthworm immediately and
were observed nose-rubbing the substrate afterwards. Salamanders that consumed
lumbricid earthworms were not observed to nose-rub after consuming their prey.
For both lumbricid earthworm species, if the worm escaped the salamander’s first
attack, the salamander pursued the earthworm and struck again. Salamanders were
not observed to pursue escaping Am. agrestis and make additional strikes.
Capture rates were not independent of earthworm prey type for Wandering
Broadhead Planarians, Ribbon Leeches, and Seal Salamanders (Table 2). The odds
of these predators capturing both Ap. longa and L. rubellus were both significantly
greater than for capturing Am. agrestis. Capture rates were also not independent of
prey type for the Rusty Crayfish; however, only the odds of capturing Ap. longa
were greater than for capturing Am. agrestis in this species (Table 2). For the Eastern
Red Centipede, there was no evidence to reject the null hypothesis that capture
rates were independent of worm prey type. Direct observation of centipede feeding
behaviors and earthworm responses to these behaviors was not possible (see Methods
above).
Discussion
Amynthas agrestis is a surface-dwelling consumer of leaf litter that is invading
the eastern United States both actively (Callaham et al. 2003) and through passive,
anthropogenic dispersion (Gates 1982), and it is often the dominant earthworm
species along invasion fronts in the Eastern United States (Snyder et al. 2011,
Zhang et al. 2010). The ecological impact of Am. agrestis and the susceptibility of
new habitats to invasion will partially depend upon the interactions between this
earthworm and native, edaphic predators. All of the predators we examined treated
Am. agrestis as potential prey and attacked them in the same manner as lumbricid
earthworms during feeding trials. However, few feeding trials involving the nonarthropod
Wandering Broadhead Planarian (8%), Seal Salamander (10%), and
Ribbon Leech (23%) resulted in successful capture of an Am. agrestis. Captures
were much more likely to occur during trials with lumbricid earthworms than with
Am. agrestis for these predators. Our observations suggest that the non-arthropod
predators may have been repelled by the primary (thrashing) and secondary (yellow
fluid) antipredator defenses exhibited by Am. agrestis that were not employed by
lumbricid earthworms.
In contrast, the arthropod predators (Eastern Red Centipede and Rusty Crayfish)
appeared equally adept at capturing different types of earthworm prey.
Eastern Red Centipedes successfully captured Am. agrestis in 53% of feeding trials,
and Rusty Crayfish managed to successfully capture Am. agrestis in 54% of
feeding trials. Lumbricid earthworm captures (specifically Ap. longa) were more
likely than Am. agrestis captures only for the Rusty Crayfish. Direct observation
of attacks was not possible for Eastern Red Centipedes, but we did not observe
Rusty Crayfish reacting negatively to the yellow liquid secreted by Am. agrestis
in response to attacks.
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Species with distasteful skin secretions have been found to be more vulnerable
to arthropod predators than to non-arthropods (Relyea and Werner 1999).
Although Rusty Crayfish and Eastern Red Centipedes are known to use chemoreception
in their feeding responses (Shelley 2002, Weisbord et al. 2012), they
demonstrated no observable aversion to contact with the putatively distasteful
secretions of Am. agrestis and were only occasionally repelled by its thrashing
behavior. Our observations suggest that, to the extent that such predators view
Am. agrestis as a potential food source, edaphic arthropod predators may provide
a measure of biological resistance against the advance of Am. agrestis along
invasion fronts. In order to better understand the role of Am. agrestis in North
American forest food webs, further studies should be conducted to determine
whether other arthropod predators endemic to the eastern United States are likely
predators of Am. agrestis in both a terrestrial or aquatic setting, and whether the
Seal Salamanders’ apparent distaste for Am. agrestis extends to other vertebrate
predators. Another area for further study is the potential for passive dispersion of
Am. agrestis through waterways (hydrochory). Costello et al. (2011) found that
earthworms of the family Megascoelecidae, to which Am. agrestis belongs, can
travel passively through waterways. All Am. agrestis that survived feeding trials
with aquatic predators also recovered from the ten minutes of submersion, raising
the possibility that Am. agrestis might be transferred passively to new habitats
through hydrochory, especially if other potential predators share the same apparent
distaste for their secretions as did the model predator species in our study.
It is worth noting that, because their putative food sources in the wild are different,
earthworms were maintained on different diets in the laboratory according
to published accounts of earthworm-colony maintenance (Zaborski 2002, Zhang
et al. 2010). Amynthas agrestis was fed a diet of leaf litter collected from campus
grounds, and both L. rubellus and Ap. longa were fed vegetable scraps and coffee
grounds. Although Zaborski (2002) did not note an impact of differing earthworm
diets upon feeding trials with the Wandering Broadhead Planarian, it is possible that
dietary differences impacted earthworm palatability. Additionally, we observed all of
our predators (with the exception of the Eastern Red Centipede, see above) to make
contact with their prey at least once, and thus categorized any subsequent earthworm
survival as an “escape” as opposed to “no contact”. However, in some cases (especially
for Wandering Broadhead Planarians and Ribbon Leeches, whose methods
of attack and simple locomotion are quite similar) it is possible that what appeared
to the observer to be a strike may have in fact been a non-aggressive contact. Such a
situation may have skewed the number of “escape” results, and artificially eliminated
the “no contact” outcomes. For these reasons, care should be taken when interpreting
these results and when applying them to conditions in the field.
The magnitude of the ecological disruption caused by nonindigenous, surfacedwelling
earthworms such as Am. agrestis will depend in part upon their success
in invading and occupying new habitats. A better understanding of the role of these
organisms in forest food webs, including their interactions with native predators, is
necessary to guide informed management strategies and policy decisions.
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Acknowledgments
Thanks to Steven Matter of the Arts and Sciences Biology Department of the University
of Cincinnati for assisting with the design of no-choice feeding trials, and to M.A. Callaham,
P.K. Ducey, and J.C. Maerz for generously offering advice regarding their individual areas
of expertise. Further thanks to Jim Anno of the Greater Cincinnati Herpetological Society
and to John MacGregor of the Kentucky Department of Fish and Wildlife Resources for
their assistance with specimen collection under less than optimal field conditions. Thanks
also to the Biology Department at UC Blue Ash for providing facilities and materials for
this study. Funding for this study was provided by a Summer Research Fellowship from the
University of Cincinnati Undergraduate Research Council to J. Gorsuch. Use of Seal Salamanders
in this study was approved by UC IACUC protocol 11-02-25-01. Collections made
in Kentucky were approved through a Kentucky Department of Fish and Wildlife Resources
(KDFWR) Scientific Collection Permit.
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