Competition between invasive earthworms (Amynthas corticis, Megascolecidae) and native North American millipedes (Pseudopolydesmus erasus, Polydesmidae): Effects on carbon cycling and soil structure

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Abstract

Invasive earthworms can have significant impacts on C dynamics through their feeding, burrowing, and casting activities, including the protection of C in microaggregates and alteration of soil respiration. European earthworm invasion is known to affect soil micro- and mesofauna, but little is known about impacts of invasive earthworms on other soil macrofauna. Asian earthworms (Amynthas spp.) are increasingly being reported in the southern Appalachian Mountains in southeastern North America. This region is home to a diverse assemblage of native millipedes, many of which share niches with earthworm species. This situation indicates potential for earthworm–millipede competition in areas subject to Amynthas invasion.

In a laboratory microcosm experiment, we used two 13C enriched food sources (red oak, Quercus rubra, and eastern hemlock, Tsuga canadensis) to assess food preferences of millipedes (Pseudopolydesmus erasus), to determine the effects of millipedes and earthworms (Amynthas corticis) on soil structure, and to ascertain the nature and extent of the interactions between earthworms and millipedes. Millipedes consumed both litter species and preferred red oak litter over eastern hemlock litter. Mortality and growth of millipedes were not affected by earthworm presence during the course of the experiment, but millipedes assimilated much less litter-derived C when earthworms were present.

Fauna and litter treatments had significant effects on soil respiration. Millipedes alone reduced CO2 efflux from microcosms relative to no fauna controls, whereas earthworms alone and together with millipedes increased respiration, relative to the no fauna treatment. CO2 derived from fresh litter was repressed by the presence of macrofauna. The presence of red oak litter increased CO2 efflux considerably, compared to hemlock litter treatments.

Millipedes, earthworms, and both together reduced particulate organic matter. Additionally, earthworms created significant shifts in soil aggregates from the 2000–250 and 250–53 μm fractions to the >2000 μm size class. Earthworm-induced soil aggregation was lessened in the 0–2 cm layer in the presence of millipedes. Earthworms translocated litter-derived C to soil throughout the microcosm.

Our results suggest that invasion of ecosystems by A. corticis in the southern Appalachian Mountains is unlikely to be limited by litter species and these earthworms are likely to compete directly for food resources with native millipedes. Widespread invasion could cause a net loss of C due to increased respiration rates, but this may be offset by C protected in water-stable soil aggregates.

Introduction

Earthworm invasions in North America have been observed for over a hundred years (e.g. Eisen, 1900, Smith, 1928). The presence of non-native earthworms in disturbed sites has been documented throughout much of North America (e.g. Reynolds et al., 1974, Reynolds, 1978), but earthworm invasion of relatively undisturbed habitats has also been recorded. Callaham et al. (2003) recently observed the presence of Asian earthworms (Amynthas spp.) in the southern Appalachian Mountains. While the extent and impacts of these invasions are only now becoming clear, many of the ecological impacts of other earthworm invasions are well documented (Bohlen et al., 2004a, Hale et al., 2005, Frelich et al., 2006, Hendrix, 2006).

It is well known that earthworms can have significant impacts on many aspects of ecosystem functioning, including the carbon cycle. For instance, Aporrectodea caliginosa casting activity has been shown to increase C sequestration in soil micro- and macroaggregates of southern Appalachian Piedmont soils (e.g. Bossuyt et al., 2005). Incorporation of organic matter into the soil by earthworms can play a major role in C-cycling, but it is clear that these effects may vary with time, earthworm species, soil type, and C availability (Bohlen et al., 2004a, McLean et al., 2006).

Where earthworms are absent, millipedes are often the dominant detritivores (Hopkin and Read, 1992), however, very little is known about their ecosystem-scale effects. Millipedes function as fragmenters of organic material and are important to the primary decomposition of all forms of detritus (Ausmus, 1977, Hopkin and Read, 1992, Rawlins et al., 2006). Millipede fecal pellets can account for a significant percentage of organic soil layers (up to 39% of standing litter, Dangerfield and Milner, 1996) and because of their chemical and physical nature can serve as hotspots for microbial activity (Anderson and Bignell, 1980).

Millipedes, with few exceptions, primarily consume organic detritus and the microbial biomass living on this material, and tend to prefer more labile material and that with fewer defensive compounds (Hopkin and Read, 1992). Litter consumption by millipedes is a significant pathway for C movement (Rawlins et al., 2006). Millipedes assimilate little of the C they consume (Anderson and Bignell, 1982, Bonkowski et al., 1998, Toyota et al., 2006) although considerable variation is reported in the literature (<10–83%), possibly due to variability of food quality. Undigested C is deposited in fecal pellets where it is subject to increased microbial activity and C loss through respiration (Anderson and Bignell, 1980, Maraun and Scheu, 1996), but C remaining is subsequently protected in fecal pellet-derived aggregates (Toyota et al., 2006).

Millipedes share some niche space with earthworms, as they both live in and feed on leaf litter and soil. Millipede species are known to differentiate niches by utilizing different microhabitats (O'Neill, 1967, Enghoff, 1983) and different positions within a particular soil horizon (Geoffroy, 1981). Spatial niche partitioning occurs between millipedes and other detritivores (Davis and Sutton, 1977), but interactions between earthworms and millipedes have been little studied and are dependent on the ecological strategies of the species involved. In European Beech forests, endogeic earthworms (Octolasion lacteum) benefited from the presence of millipedes, and preferentially fed on their fecal pellets (Bonkowski et al., 1998). Although epigeic and anecic earthworm interactions with millipedes have not been demonstrated, these species all consume leaf litter and are likely to compete for this resource.

Given the increasing documentation of Amynthas spp. in the southern Appalachian Mountains, a region with high millipede biodiversity, high endemism, and many undescribed species (Snyder, 2008), we hypothesized that millipedes in this region are likely to face competition from these invading earthworms. To our knowledge earthworm–millipede competitive interactions have not been examined. Such competitive interactions could have consequences not only for millipede populations, but also for C dynamics at the ecosystem level. The aim of this study was to document the effects of an invasive earthworm species (Amynthas corticis) on the feeding behavior of millipedes (Pseudopolydesmus erasus) and the impacts of these species on C flow in laboratory microcosms, in order to determine potential consequences of widespread Amynthas introduction in the southern Appalachian Mountains.

Section snippets

Microcosm setup

Soil, FH-layer material, and naturally senesced non-13C enriched leaf litter were collected from Coweeta Hydrologic Laboratory (North Carolina, USA, 35°2′20″N, 83°27′10″W) from a high-elevation (ca. 1000 m) site. Soils are generally classified as Typic Haplubrepts at high elevation (Knoepp and Swank, 1998). Soil (initial δ13C, −26.4 ‰; C:N ratio, 16.6) and FH (initial δ13C, −28.0 ‰; C:N ratio, 24.9) material were both air dried and sieved (soil 2 mm, FH 4 mm) to remove large aggregates, roots, and

Millipede mortality and growth

Millipede mortality was slightly, but not significantly, higher in treatments with earthworms than without (39.6% relative to 33.3%). Dead millipedes were removed from microcosms before they decomposed appreciably, therefore contributing little to overall nutrient cycling. Litter treatments did not significantly affect millipede survival. Surviving millipedes gained mass in almost all replicates and treatments; however, growth was not affected by litter treatments or by earthworm presence.

Litter-derived C

GLM

Food preference and competition

Millipedes consumed and assimilated C from both red oak and eastern hemlock litter, even when both litter species were mixed. Oak was clearly the preferred species, as evidenced by greater assimilation of litter-derived C, as determined by a mixing model, when both litter species were present (Fig. 1b). The mass of each litter species may have played a role in millipede 13C assimilation, since a greater mass of oak litter than hemlock litter was provided. However, since the mass of each litter

Conclusions

Soil macroinvertebrate detritivores have been shown to significantly affect soil C. Amynthas corticis and P. erasus differed greatly in their impacts on C dynamics and soil structure in microcosms, yet preferred and competed for similar food resources. Impacts of A. corticis on soil structure were more extensive: macroaggregates were formed throughout the soil profile, whereas P. erasus only had such impacts within the surface layer. Earthworm impacts on soil aggregation were also more

Acknowledgements

We gratefully acknowledge the assistance of B. Ball, R. Potter, C.-Y. Huang, T. Maddox, and the staff of the Odum School of Ecology's Analytical Chemistry Lab. M.A. Callaham and two anonymous reviewers provided insightful comments on the manuscript. This research was supported by National Science Foundation grant number 0236276 to the University of Georgia Research Foundation, Inc.

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