nena masthead
NENA Home Staff & Editors For Readers For Authors

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

Full-text pdf (Accessible only to subscribers. To subscribe click here.)

 

Access Journal Content

Open access browsing of table of contents and abstract pages. Full text pdfs available for download for subscribers.



Current Issue: Vol. 30 (3)
NENA 30(3)

Check out NENA's latest Monograph:

Monograph 22
NENA monograph 22

All Regular Issues

Monographs

Special Issues

 

submit

 

subscribe

 

JSTOR logoClarivate logoWeb of science logoBioOne logo EbscoHOST logoProQuest logo

Northeastern Naturalist 652 J.P. Gorsuch and P.C. Owen 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 Northeastern Naturalist Vol. 21, No. 4 J.P. Gorsuch and P.C. Owen 2014 653 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. Northeastern Naturalist 654 J.P. Gorsuch and P.C. Owen 2014 Vol. 21, No. 4 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 Northeastern Naturalist Vol. 21, No. 4 J.P. Gorsuch and P.C. Owen 2014 655 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. Northeastern Naturalist 656 J.P. Gorsuch and P.C. Owen 2014 Vol. 21, No. 4 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. Northeastern Naturalist Vol. 21, No. 4 J.P. Gorsuch and P.C. Owen 2014 657 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 Northeastern Naturalist 658 J.P. Gorsuch and P.C. Owen 2014 Vol. 21, No. 4 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. Northeastern Naturalist Vol. 21, No. 4 J.P. Gorsuch and P.C. Owen 2014 659 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. Northeastern Naturalist 660 J.P. Gorsuch and P.C. Owen 2014 Vol. 21, No. 4 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. Literature Cited Callaham, M.A., P.F. Hendrix, and R.J. Philips. 2003. Occurrence of an exotic earthworm (Amynthas agrestis) in undisturbed soils of the southern Appalacian Mountains, USA. Pedobiologia 47:466–470. Costello, D.M., S.D. Tiegs, and G.A. Lamberti. 2011. Do non-native earthworms in southeast Alaska use streams as invasional corridors in watersheds harvested for timber? Biololgical Invasions 13:177–187. Ducey, P.K., M. Messere, K. Lapoint, and S. Noce. 1999. Lumbricid prey and potential herpetofaunal predators of the invading terrestrial flatworm Bipalium adventitium (Turbellaria: Tricladida: Terricola). American Midland Naturalist 141:305–314. Gates, G.E. 1982. Farewell to North American megadriles. Megadrilogica 4:12–77. Maerz, J.C., V.A. Nuzzo, and B. Blossey. 2009. Declines in woodland salamander abundance associated with non-native earthworm and plant invasions. Conservation Biology 23:975–981. Olson, H.W. 1928. The Earthworms of Ohio, with a Study of their Distribution in R elation to Hydrogen-ion Concentration. Ohio State University Press, Columbus, OH. Olson, H.W. 1933. Two New Earthworms for Ohio. Ohio State University Press, Columbus, OH. Quinn, G.P., and M.J. Keough. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK. Relyea, R.A., and E.E. Werner. 1999. Quantifying the relation between predator-induced behavior responses and growth performance in larval anurans. Ecology 80:2117–2124. Reynolds, J.W. 1978. The earthworms of Tennessee (Oligochaeta) IV. Megascolecidae, with notes on the distribution, biology, and a key to the species in the state. Megadrilogica 3:117–129. Reynolds, J.W. 1995. Status of Exotic Earthworm Systematics and Biogeography in North America. CRC Press, Inc., Boca Raton, FL. Shelley, R.M. 2002. A synopsis of the North American centipedes of the order Scolopendromorpha (Chilopoda). Virginia Museum of Natural History Memoirs 5:1–108. Snyder, B.A., M.A. Callaham, and P. Hendrix. 2011. Spatial variabilityof an invasive earthworm (Amynthas agrestis) population and potential impacts on soil characteristics and millipedes in the Great Smoky MountainsNational Park, USA. Biological Invasions 13:349–358. Northeastern Naturalist Vol. 21, No. 4 J.P. Gorsuch and P.C. Owen 2014 661 Weisbord, C., D. Callaghan, and G. Pyle. 2012. Associative learning in male Rusty Crayfish (Oronectes rusticus): Conditioned behavioral response to an egg cue from Walleye (Sander vitreus). Canadian Journal of Zoology 90:85–92. Zaborski, E.R. 2002. Observations on feeding behavior by the terrestrial flatworm Bipalium adventitium (Turbellaria: Tricladida: Terricola) from Illinois. American Midland Naturalist 148:401–408. Zhang, W., P.F. Hendrix, B.A. Snyder, M. Molina, J. Li, X. Rao, E. Siemann, and S. Fu. 2010. Dietary flexibility aids Asian earthworm invasion in North American forests. Ecology 91:2070–2079.