Patterns Of Litter Disappearance In A Northern Hardwood Forest Invaded By Exotic Earthworms

154

Ecological Applications, 16(1), 2006, pp. 154–165q 2006 by the Ecological Society of America

PATTERNS OF LITTER DISAPPEARANCE IN A NORTHERN HARDWOODFOREST INVADED BY EXOTIC EARTHWORMS

ESTEBAN R. SUAREZ,1,4 TIMOTHY J. FAHEY,1 JOSEPH B. YAVITT,1 PETER M. GROFFMAN,2

AND PATRICK J. BOHLEN3

1Department of Natural Resources, Cornell University, Ithaca, New York 14853 USA2Institute of Ecosystem Studies, Box AB, Millbrook, New York 12545 USA

3Archbold Biological Station, Lake Placid, Florida 33852 USA

Abstract. A field study was conducted to evaluate the effects of exotic earthworminvasions on the rates of leaf litter disappearance in a northern hardwood forest in south-central New York, USA. Specifically, we assessed whether differences in litter quality andthe species composition of exotic earthworm communities affected leaf litter disappearancerates. Two forest sites with contrasting communities of exotic earthworms were selected,and disappearance rates of sugar maple and red oak litter were estimated in litter boxes inadjacent earthworm-free, transition, and earthworm-invaded plots within each site. After540 days in the field, 1.7–3 times more litter remained in the reference plots than in theearthworm-invaded plots. In the earthworm-invaded plots, rates of disappearance of sugarmaple litter were higher than for oak litter during the first year, but by the end of theexperiment, the amount of sugar maple and oak litter remaining in the earthworm-invadedplots was identical within each site. The composition of the earthworm communities sig-nificantly affected the patterns of litter disappearance. In the site dominated by the anecicearthworm Lumbricus terrestris and the endogeic Aporrectodea tuberculata, the percentageof litter remaining after 540 days (;17%) was significantly less than at the site dominatedby L. rubellus and Octolasion tyrtaeum (;27%). This difference may be attributed to thedifferences in feeding behavior of the two litter-feeding species: L. terrestris buries entireleaves in vertical burrows, whereas L. rubellus usually feeds on litter at the soil surface,leaving behind leaf petioles and veins. Our results showed that earthworms not only ac-celerate litter disappearance rates, but also may reduce the differences in decompositionrates that result from different litter qualities at later stages of decay. Similarly, our resultsindicate that earthworm effects on decomposition vary with earthworm community com-position. Furthermore, because earthworm invasion can involve a predictable shift in com-munity structure along invasion fronts or through time, the community dynamics of invasionare important in predicting the spatial and temporal effects of earthworm invasion on litterdecomposition, especially at later stages of decay.

Key words: Aporrectodea tuberculata; earthworm functional groups; exotic earthworm invasion;litter disappearance; litter quality; Lumbricus rubellus; Lumbricus terrestris; northern hardwood for-ests; Octolasion tyrtaeum; red oak; south-central New York, USA; sugar maple.

INTRODUCTION

Exotic earthworm species are invading many forestsin North America, producing profound ecosystemchanges, especially in Canada and northeastern andnorth-central United States where large native detriti-vores are absent (Alban and Berry 1994, Scheu andParkinson 1994, Hendrix and Bohlen 2002, Bohlen etal. 2004a). Among these changes, elimination of forestfloor organic horizons and reductions in soil organicmatter content are of particular concern due to the im-portance of soil organic matter to nutrient supply andcarbon sequestration. In spite of these effects, current

Manuscript received 10 May 2004; revised 9 June 2005; ac-cepted 10 June 2005. Corresponding Editor: J. Gulledge.

4 Present address: Wildlife Conservation Society–Ecuador,San Francisco 441 y Mariano Echeverrıa, Apartado Postal17-21-168, Quito, Ecuador. E-mail: [email protected]

carbon budgets and ecosystem models for these forestsassume that litter decay can be plainly characterized asa microbial process driven by litter quality and sitecharacteristics, an incorrect assumption in areas invad-ed by exotic earthworms (Andren et al. 2001, Bohlenet al. 2004b). In particular, only limited information isavailable about how different species of earthwormsaffect litter disappearance, or about how earthwormspecies effects interact with litter quality. In this paper,we analyze the effects of different invasive earthwormson northern red oak (Quercus rubra L. Michx.) andsugar maple (Acer saccharum Marsh.) litter disap-pearance rates in a northern hardwood forest in south-central New York, USA. These species were chosenbecause of presumed differences in litter quality, sugarmaple being more easily decayed than red oak(McClaugherty et al. 1985, Trofymow et al. 1995).

February 2006 155EXOTIC EARTHWORMS AND LITTER DISAPPEARANCE

Exotic earthworm activity has been shown to in-crease leaf litter disappearance in many agroecosys-tems and in natural tropical and temperate ecosystems(Bohlen et al. 1997, Liu and Zou 2002, Pouyat andCarreiro 2003). For example, an 85% reduction in thedensity of the exotic earthworm Amynthas rodericencisin a Puerto Rican tropical forest reduced litter decayrates by 20–50% (Liu and Zou 2002), and red oak litterdisappeared significantly faster in urban forest standsthat were heavily invaded by exotic earthworms thanin rural stands with little or no earthworm activity(Pouyat and Carreiro 2003). However, the effects ofearthworms on litter decay may depend upon the char-acteristics of the litter: litter quality and palatability(i.e., lignin, nitrogen, and tannin contents) may influ-ence earthworm feeding behavior, altering the rates oflitter disappearance (Edwards and Heath 1963, Satchelland Low 1967, Staaf 1987, Hendriksen 1990, Cote andFyles 1994, Gonzalez and Zou 1999). The implicationsof these interactions for soil and vegetation patternsand dynamics have been demonstrated (Boettcher andKalisz 1991, Wardle and Lavelle 1997).

The species composition of earthworm communitiesmay also influence their effect on litter disappearance.Although the large species diversity of the decomposercommunity has led to the conclusion that belowgroundcommunities are largely functionally redundant (An-dren et al. 1995), differences in the feeding ecology ofdifferent earthworm species suggest that their effectson decomposition could differ substantially. For ex-ample, different earthworm species are known to con-sume litter at different rates (Shipitalo et al. 1988), andsome species bury litter in the soil whereas others feedon litter at the soil surface, or specialize on more highlydecomposed organic matter (Edwards and Bohlen1996). To our knowledge, however, no studies of theinteractive effects of litter quality and earthworm spe-cies composition have been conducted in temperatefield settings. Furthermore, invasion can involve rapidshifts in earthworm community structure along inva-sion fronts, or successive introduction of different spe-cies through time as different species respond to chang-ing soil conditions (Bohlen et al. 2004c, Hale et al.2005). Understanding how these shifts in communitystructure will affect soil processes is key to understand-ing the effects of this invasion.

Many areas in the Allegheny Plateau in south-centralNew York have been invaded by mixed communitiesof exotic earthworms, as similarly observed in othernorthern forest regions (Gundale 2002, Hale 2004). Aprevious study at the Arnot Forest in Schuyler County(New York) showed that ;30% of this 1650-ha foresthas been invaded by heterogeneous communities ofexotic earthworms, including at least seven species(Bohlen et al. 2004a). Heavily invaded areas of thisforest are separated from earthworm-free areas by tran-sition zones with intermediate levels of earthworm den-sity and activity (Suarez et al. 2006), providing an ideal

setting to analyze the effects of the density and com-position of the exotic earthworm communities on therates of litter disappearance in areas with similar forestcomposition and soils. The objective of this study wasto evaluate the effects of different exotic earthwormcommunities on the disappearance of leaf litter of twospecies with different litter quality. We employed anarray of litter boxes positioned in plots with contrastingearthworm density and composition to address the fol-lowing questions. (1) How much does litter disap-pearance increase as a result of the activity of exoticearthworms in comparison to earthworm-free areas? (2)Does litter quality modify the effects of earthwormson litter disappearance? (3) Does earthworm speciescomposition affect rates of litter disappearance? Ourmain goal was to provide a better understanding of thecontrols of litter disappearance rates in earthworm-in-vaded forest soils.

METHODS

Study sites

The Arnot Teaching and Research Forest (428169 N,768289 W) is a 1650-ha property located in SchuylerCounty, in south-central New York State, USA. Thisforest was heavily logged at the end of the 19th century,but recovered to its present state with little anthropo-genic disturbance. The Arnot Forest is dominated bytypical species of Allegheny northern hardwood forestsuch as sugar maple (Acer saccharum Marsh.), northernred oak (Quercus rubra L. Michx.), American beech(Fagus grandifolia, Ehrh.), red maple (Acer rubrumL.), white ash (Fraxinus americana L.), and Americanbasswood (Tilia americana L.) (Fain et al. 1994, Fahey1998). Average annual rainfall at the site is 1000 mmand temperatures average 228C in June and 248C inJanuary. The soils are developed from locally derivedglacial till, and have been classified as acidic Dystro-chrepts with pH values ranging from 4.5 to 5.0.

In 2001, an extensive survey of the Arnot Forestrevealed that ;30% of the property has been invadedby exotic earthworms, creating a mosaic landscape inwhich heavily earthworm-invaded areas are usuallyseparated from noninvaded areas by patches of landwith intermediate levels of earthworm abundance andactivity, henceforth called transition zones (Bohlen etal. 2004a). Earthworm-free areas exhibit thick forestfloor organic horizons averaging 4 cm in thickness,whereas heavily invaded areas have no forest floor andshow abundant signs of earthworm activity (e.g., casts,middens, burrows). Transition zones are defined as ar-eas that retain some forest floor but also show clearevidence of earthworm activity. Three sites encom-passing adjacent earthworm-invaded, transition, andreference (earthworm-free) areas were selected for alarger study on the ecosystem-level effects of exoticearthworm invasion on northern hardwood forests(Bohlen et al. 2004b, Fisk et al. 2004, Groffman et al.

156 ESTEBAN R. SUAREZ ET AL. Ecological ApplicationsVol. 16, No. 1

2004, Suarez et al. 2004). For the present study, twoof those sites (site 2 and site 3) were selected becauseof their contrasting earthworm community composition(Bohlen et al. 2004a); at site 2 the earthworm-invadedplot was dominated by Lumbricus rubellus and Octo-lasion tyrtaeum, whereas Aporrectodea tuberculata andL. terrestris were dominant at site 3. Within each site,the sequence of earthworm-invaded, transition, and ref-erence plots was located on moderate slopes with ho-mogeneous soils and forest composition.

Litter disappearance method

Immediately after leaf abscission in October 2001,freshly fallen oak and sugar maple litter was collectedin monospecific plantations located in Ithaca, NewYork, 30 km southeast of the Arnot Forest field sites.The litter was transported to the laboratory and driedat room temperature for two weeks. Subsamples of eachlitter type were analyzed for initial nitrogen and lignincontent. Total nitrogen was determined with the Kjel-dahl procedure, whereas lignin was determined afteracid detergent treatment in an ANKOM Fiber Analyzer(John Morris Scientific, Sydney, Australia). After dry-ing, moisture content of the litter was measured on 10subsamples of each litter type by drying to constantmass at 658C. Samples of each litter type were storedin individual plastic bags and transported to the fieldsite for placement in the litter boxes.

Litter decay was measured using unconfined samplesbecause mesh bags can affect differentially the activityof detritivores that vary in size over a wide range (Bo-cock and Gilbert 1957, Anderson 1973). We installed30 litter boxes, 15 of each type of litter, at haphazardlocations in each reference, transition, and earthworm-invaded plot at each of the two study sites, for a totalof 180 boxes. Areas where microtopography was severewere avoided. The Oi horizon was cleared from a 503 50 cm area, and 25 cm long nails were placed in thecorners. A 2–3 cm deep trench was cut in the groundalong the sides of the square, and a single 2-m pieceof plastic garden edging was inserted in the trench,completing the sides of each box. The garden edgingwas 15 cm wide, so that the height of the sides of thelitter box was between 12 and 13 cm. Nylon mesh (holesize 1 cm) covered the bottom of each box, the meshsize being selected to enable the free movement ofearthworms, while facilitating the complete recoveryof the litter during sampling. During the last week ofNovember 2001, pre-weighed (60.01 g) samples of air-dried leaf litter (;79 g) were placed in each box; thisamount of litter is equivalent to the average 316 g/m2

of annual litterfall that had been previously measuredin these study plots (Fisk et al. 2004). Half of the litterboxes in each plot (15 boxes) received sugar maplelitter, while the other half received red oak litter. Toexclude new litter and avoid advective movement ofsample litter, we covered the top of each box with fi-berglass screen (1-mm mesh size) that was stapled to

the upper rim of the plastic garden edging. Three ad-ditional boxes of each litter type were built as describedand their litter was recovered immediately after to al-low a handling correction.

On each sampling date (May 2002, October 2002,and May 2003), all of the litter remaining was collectedfrom five randomly selected boxes of each litter typein each plot. The litter was stored in plastic bags andtransported to the laboratory where miscellaneous de-bris was carefully removed (e.g., fine roots, earthwormcasts, and plant seedlings). The litter was oven-driedto constant mass at 658C. Ash content for each samplewas determined by loss-on-ignition (8 h at 4508C) andthe percentage of litter remaining was calculated fromthe ash-free final mass of each sample, corrected forlitter handling. At the transition and earthworm-invad-ed plots, the process of decay was accompanied by thecomminution and burial of leaves by the earthworms.In this study, we could not separate the relative im-portance of the two processes, and ‘‘litter disappear-ance’’ refers to the mixed effects of earthworm feeding,microbial activity, and the physical modification andtransport of litter by earthworms.

Earthworm sampling method

After collecting the litter remaining in each litterbox, we used a formalin extraction method (Raw 1959)to collect the earthworms from each litter box. Usinga watering can, we slowly poured 8 L of 0.4% formalinsolution in the litter box area and waited for 10 minutes,collecting all of the earthworms that appeared at thesurface as well as those that were found in the littercollected in the box. The earthworms were preservedin 4% formalin solution and were then counted,weighed, and identified in the laboratory. Earthwormbiomass is presented as fresh biomass.

Analysis

We described litter disappearance using exponentialmodels of the form y 5 e2kt, where y is the percentageof litter remaining, t is the time in years, and k is thelitter disappearance constant (Olson 1963). The relativecontribution of earthworms to litter disappearance wasestimated with a calculation similar to that proposedby Heneghan et al. (1999); for each site, we used themean values of litter loss in the earthworm-invaded ortransition plots and compared them to the mean litterloss from the reference plots to calculate the litter dis-appearance due to earthworms (LDE) as: LDE 5 [(LW

2 LNW)/LW]100, where LW is the mean percentage oflitter disappearance from a plot with earthworms(earthworm-invaded or transition plots; subscript Wdenotes ‘‘worms’’), and LNW is the mean percentage oflitter disappearance from the corresponding reference(noninvaded; NW denotes ‘‘no worms’’) plot. To il-lustrate the variability of these estimates, we calculated95% confidence intervals using the sum of the vari-


TABLE 1. Repeated-measures ANOVA on the amount of ash-free litter remaining in litterboxes placed in earthworm-invaded, transition, and earthworm-free (reference) sites at theArnot Forest, south-central New York, USA.

Source df MS F P

Between-subjects effectsTreatment 2 6038.25 173.94 ,0.0001Litter type 1 400.21 11.53 0.0014Site 1 45.40 1.31 0.2582Treatment 3 Litter 2 60.64 1.75 0.1848Treatment 3 Site 2 255.95 7.37 0.0016Litter 3 Site 1 167.81 4.83 0.0326Error 20 34.71

Within-subject effectsDate 2 23 649.52 736.07 ,0.0001Date 3 Treatment 4 883.03 27.48 ,0.0001Date 3 Litter 2 108.82 3.39 0.0377Date 3 Site 2 178.48 5.56 0.0052Error 100 32.12

Notes: Treatments are earthworm-invaded, transition, and reference; sites are 2 and 3; littertypes are sugar maple and red oak; dates are May 2002, October 2002, and May 2003; n 5 5replicates for all treatment 3 litter type 3 site 3 date combinations.

FIG. 1. Sugar maple and red oak litter disappearancetrends measured in litter boxes in two earthworm-invaded(WRM), two transition (TRANS), and two earthworm-free(NW) plots in a northern hardwood forest. Decay trends wereestimated as the percentage of ash-free litter (mean 1 SE; n5 5 replicates) remaining in the litter boxes at each samplingdate. For statistical results, see Table 1.

ances for litter decomposition in the control and cor-responding transition or earthworm plot.

The differences in litter disappearance were analyzedthrough repeated-measures ANOVA with three levelsof the factor ‘‘treatment’’ (earthworm-invaded, tran-sition, and reference), two levels of ‘‘litter type’’ (oakand sugar maple), two levels of the factor ‘‘site,’’ andthree repeated measures of the factor ‘‘sampling date’’.Litter consumption rates and earthworm abundance andbiomass were analyzed through three-way and two-wayANOVA, respectively. Logarithmic transformationswere used when needed to meet the assumptions ofnormality and stability of variance of the models. Allof the analyses were performed with the GLM proce-dure of the SAS statistical package (SAS Institute1987).

RESULTS

Litter disappearance

The rates of litter disappearance varied as a functionof treatment (earthworm-invaded, transition, or refer-ence), litter type, and date of sampling, and most ofthe two-order interactions included in the ANOVAmodel were also significant (Table 1). In particular, allof the two-way interactions involving the repeatedmeasure (date) were statistically significant (Table 1).The main effect site was not statistically significant,but all of the two-way interactions involving it were.The more distinctive patterns associated with these ef-fects and interactions will be described.

Earthworms significantly increased litter disappear-ance (F2,50 5 173.94, P , 0.0001); after 540 days inthe field, the mean percentage of litter remaining in theearthworm-invaded plots was 1.7–3.0 times smallerthan the percentage of litter remaining in the referenceplots (Fig. 1). Although the litter boxes in the reference


TABLE 2. Density of exotic earthworms (earthworms/m2; mean 6 SE, n 5 15 samples per species) collected in litter boxeswith red oak or sugar maple litter in two earthworm-invaded and two transition plots in a northern hardwood forest insouth-central New York.

Plot and littertypes, by site

Lumbricusterrestris

Lumbricusrubellus

Octolasiontyrtaeum

Dendrobaenarubida

Aporrectodeatuberculata

Lumbricusimmature

Otherimmature

Totaldensity

Site 2Earthworm-invaded sites

Sugar maple 10.1 (2.2) 3.8 (1.6) 59.4 (9.0) 6.3 (2.4) 79.6 (10.2)Oak 7.2 (1.2) 4.8 (2.7) 59.7 (13.1) 19.5 (6.0) 81.6 (14.4)

Transition sitesSugar maple 2.5 (1.0) 0.3 (0.3) 0.3 (0.3) 22.1 (4.6) 1.4 (0.9) 26.5 (5.1)Oak 1.7 (0.8) 0.3 (0.3) 0.6 (0.4) 24.9 (5.4) 1.7 (1.2) 26.4 (6.3)


Sugar maple 3.4 (0.7) 2.7 (1.2) 2.8 (1.3) 29.1 (6.1) 32.7 (4.1) 28.7 (6.1) 99.4 (11.4)Oak 5.8 (1.0) 0.9 (0.5) 2.0 (0.7) 30.7 (6.1) 16.5 (2.9) 36.7 (9.5) 92.6 (15.6)

Transition sitesSugar maple 1.5 (1.0) 1.1 (0.8) 0.9 (0.6) 10.0 (2.3) 12.8 (4.4) 26.1 (6.8)Oak 1.9 (0.7) 0.3 (0.3) 1.4 (0.8) 1.1 (0.6) 6.3 (2.0) 10.5 (5.5) 21.5 (7.0)

Note: Transition plots were located in areas separating heavily invaded areas from earthworm-free areas in the forest.Blank cells indicate that no individuals of that earthworm species were found in samples of that treatment 3 site com-bination.

and transition plots had an average of 42–53% of litterremaining after 540 days, the earthworm-invaded plotshad only 17–27% of litter remaining (Fig. 1). The litterremaining in the reference and transition plots wasmostly composed of easily recognizable leaves and leafblade fragments, whereas litter remaining in the earth-worm-invaded plots was composed almost exclusivelyof leaf petioles and veins.

Initial lignin and nitrogen contents of the two littertypes were different. Sugar maple litter was 0.85% Nand 18.5% lignin, whereas red oak litter was 0.72% Nand 23.0% lignin. Nevertheless, on the final collectiondate, the two litter types had disappeared to about thesame extent within each treatment. At the referenceand transition plots at site 2, the amount of sugar mapleand oak litter remaining ranged between 46% and 50%,whereas at the earthworm-invaded plot, the litter ofboth types remaining in the boxes amounted to 27%.Similarly, at site 3 these percentages were 43–53% inthe reference and transition plots and 18–20% in theearthworm-invaded plot (Fig. 1). However, differenceson the earlier collection dates indicated that the tem-poral pattern of disappearance was affected by littertype; after 340 days at the earthworm-invaded plot ofsite 2, the percentage of oak litter remaining (39.4%)was 1.7 times higher than that of sugar maple litter(22.6%).

Two clear differences were observed between earth-worm-invaded plots at the two sites. First, after 340days, the disappearance of sugar maple litter was muchhigher at site 2 (22.6% remaining) than at site 3 (40.2%;Fig. 1). Secondly, at the end of the experiment, thepercentage of both litter types remaining in the earth-worm-invaded plot of site 3 (17.8% for sugar maple

and 19.7% for oak) was lower than at site 2 (27% forboth sugar maple and oak litter).

The values of the exponential decay constant (k, yr21)for the reference and transition plots (20.43 to 20.63)were roughly similar for sugar maple and oak litterwithin each site (see Appendix A for a complete tableof the decay constants). In contrast, litter disappearancerates at the earthworm-invaded plots were much fasterthan in reference and transition plots, as evidenced bydecay constants (20.96, 21.27) that were two to threetimes higher than in the reference plots at site 2 andsite 3, respectively.

Earthworm communities

The mean density of earthworms in the litter boxesin the earthworm-invaded plots ranged between 80 and100 earthworms/m2 (Table 2) and was similar betweensites (F1,56 5 1.39, P 5 0.244) and between litter types(F1,56 5 0.04, P 5 0.851). In contrast, earthworm bio-mass (fresh mass) was significantly greater (F1,56 535.6, P , 0.001) at site 3 (47–53 g/m2) than at site 2(15–17 g/m2; Table 3; see Appendix B for the full AN-OVA table). Within each site, the boxes with sugarmaple and oak litter had similar earthworm biomass(F1,56 5 0.14, P 5 0.705). At the transition plot at site2, earthworm density was 2.7–3.3 times lower than atthe earthworm-invaded plot, whereas the transition plotat site 3 had four times fewer worms than its corre-sponding earthworm-invaded plot. In the referenceplots, only four of the 20 sampled boxes had any earth-worms at site 2 and only three had earthworms at site3. None of these samples had more than two earth-worms and all of them were immature individuals.


TABLE 3. Biomass of exotic earthworms (g fresh mass/m2; mean 6 SE, n 5 15 samples per species) collected in litter boxeswith red oak or sugar maple litter in two earthworm-invaded and two transition plots in a northern hardwood forest insouth-central New York.

Plot and littertypes, by site

Lumbricusterrestris

Lumbricusrubellus

Octolasiontyrtaeum

Dendrobaenarubida

Aporrectodeatuberculata

Lumbricusimmature

Otherimmature

Totalbiomass


Sugar maple 8.60 (2.00) 1.56 (0.65) 6.88 (1.30) 0.34 (0.15) 17.38 (2.96)Oak 6.79 (1.51) 2.14 (1.13) 5.43 (1.16) 1.42 (0.52) 15.79 (2.64)

Transition sitesSugar maple 2.20 (0.97) 0.10 (0.10) 0.03 (0.03) 3.86 (0.98) 0.24 (0.13) 6.44 (1.60)Oak 1.71 (0.75) 0.11 (0.11) 0.05 (0.03) 9.67 (3.37) 0.22 (0.13) 11.76 (3.76)


Sugar maple 10.34 (2.41) 2.68 (1.24) 1.19 (0.58) 21.60 (4.75) 6.17 (1.03) 5.98 (1.46) 47.96 (5.61)Oak 18.97 (3.31) 0.74 (0.43) 0.73 (0.25) 22.48 (4.90) 3.49 (1.27) 7.48 (2.27) 53.90 (9.23)

Transition sitesSugar maple 5.16 (3.71) 0.96 (0.70) 0.55 (0.39) 2.67 (0.58) 2.69 (1.14) 12.03 (5.13)Oak 7.27 (2.77) 0.75 (0.75) 0.84 (0.45) 0.87 (0.49) 1.25 (0.43) 1.05 (0.60) 12.03 (3.32)

Note: Transition plots were located in areas separating heavily invaded areas from earthworm-free areas in the forest.Blank cells indicate that no individuals of that earthworm species were found in samples of that treatment 3 site com-bination.

FIG. 2. Linear relationships between leaf litter disap-pearance after 540 days in the field and exotic earthwormdensity. No significant differences were found between sugarmaple and red oak litter at the end of the experiment; thusthe models were built combining the two litter types. Per-centage of ash-free litter remaining and earthworm densitydata were collected in earthworm-invaded, transition, andearthworm-free (reference) plots in two northern hardwoodforest sites (site 2, solid line and open circles; site 3, dashedline and solid circles).

The five observed species of exotic earthworms werenot equally important in the two sites (Tables 2 and 3).Site 2 was dominated by the epi-anecic species Lum-bricus rubellus, which accounted for 60–70% of thedensity and biomass of adult earthworms. The onlyother common species at site 2 was the endogeic spe-cies Octolasion tyrtaeum. In contrast, at site 3, theearthworm community was dominated by the endogeicspecies Aporrectodea tuberculata (76–78% of adultdensity and 42–60% of biomass) and the anecic L. ter-restris (10–15% of adult density and 29–44% of bio-

mass). Although L. rubellus and O. tyrtaeum were pres-ent at site 3, they were minor components of the earth-worm community there (Tables 2 and 3). At both sites,transition plots were clearly dominated by immatureearthworms (Tables 2 and 3).

Litter consumption rates and earthworm contributionto litter disappearance

To assess the relationship between earthworm den-sity and litter disappearance, we combined the two littertypes because we did not find significant differencesbetween them at the end of the experiment. Mean litterremaining at the last sampling date regressed againstearthworm density (Fig. 2) showed that earthworm den-sity accounted for 73% (site 2) and 81% (site 3) of thetotal variability in litter disappearance (for site 2, y 550.47 2 0.20(X), F1,28 5 75.69, P , 0.0001; for site3, y 5 49.86 2 0.278(X), F1,27 5 115.42, P , 0.0001).The slope of the model for site 3, however, was sig-nificantly steeper than for site 2 (T 5 3.01, P , 0.05).

The rates of litter consumption (normalized as mil-ligrams per gram of worm biomass per week) weresignificantly different between litter types and sam-pling dates (Fig. 3; see Appendix C for the full ANOVAtable). For site 2, the consumption rate range was 40–88 mg·g21·wk21 and reached highest values betweenthe first and second sampling date (193–339 days), co-inciding with the 2002 growing season. At this site,the rates of sugar maple consumption were initiallygreater than those of oak litter consumption, but thisdifference disappeared by the end of the experiment.The consumption rate at site 3 (12–18 mg·g21·wk21)was much lower than at site 2, and little difference wasobserved among dates and litter types, with the excep-tion of a significantly higher consumption rate of sugar


FIG. 3. Temporal trends of red oak and sugar maple ash-free litter disappearance rates (mean 1 SE; n 5 5 replicates) intwo plots invaded by exotic earthworms in a northern hardwood forest in south-central New York. For statistical results, seeAppendix C.

maple litter between the start of the experiment and thefirst sampling date (Fig. 3). Litter consumption patternsin the transition plot at site 2 were almost identical tothose in the earthworm invaded site, both in terms ofthe temporal dynamics and the differences among litterspecies. In contrast, litter consumption rates at the tran-sition plot at site 3 were three to four times greaterthan the rates at the earthworm invaded site (Fig. 3).

The patterns of litter disappearance due to earth-worms (LDE; Fig. 4) differed markedly between sites,dates, and plots (invaded vs. transition). As expected,LDE values were often much higher in earthworm thantransition plots. In general, LDE values were lowest inthe first decay interval (0–190 days); during this in-terval, LDE was higher at site 3 than site 2. The tran-sition plots at site 2 exhibited particularly low LDEthroughout the duration of the study. Although LDEfor sugar maple tended to be higher than for oak, over-lap in the confidence intervals suggested that these dif-ferences may not be significant, except perhaps earlyin the decay process (Fig. 4).

DISCUSSION

The aim of the present study was to examine theinteracting effects of invasive earthworm abundance,earthworm species composition, and leaf litter qualityon litter disappearance in an Allegheny northern hard-wood forest. As reported in other studies (Staaf 1987,Cortez and Bouche 1998, Liu and Zou 2002, Pouyatand Carreiro 2003), we showed that litter disappearance

was greatly stimulated by earthworm activity (Fig. 1)and that a linear increase in the rate of litter loss wasobserved with increasing earthworm density (Fig. 2).Our study also suggests that earthworm effects on litterdisappearance differ substantially as a function of thecomposition of the earthworm community. These dif-ferences support previous observations (Haimi andHuhta 1990, Zhang and Hendrix 1995) that earthwormspecies differ in litter consumption activity.

The large differences in the patterns of litter dis-appearance between the two sites probably are ex-plained by the fact that earthworms of different func-tional groups distribute litter carbon in very differentpatterns and at very different rates according to theirfeeding, burrowing, and casting habits (Shipitalo et al.1988, Jegou et al. 1998). Our results illustrate thesedivergences in at least two instances. First, the slopefor the relationship between earthworm density andlitter disappearance was significantly steeper for site 3than for site 2 (Fig. 2), a difference that we attributeto the feeding behavior of Lumbricus terrestris (at site3); this anecic species buries entire leaves, removingsurface litter to a greater degree than the species thatdominate the earthworm community at site 2. Second,litter disappearance per unit earthworm biomass wasmuch higher at site 2 (dominated by L. rubellus) thanat site 3 (co-dominated by L. terrestris) (Fig. 3). In thissense, our results coincide with those of Shipitalo etal. (1988), who showed in a laboratory study that L.rubellus consumes more litter per body mass than the


FIG. 4. Temporal trends of the percentage of sugar mapleand oak ash-free litter mass loss contributed by exotic earth-worms (LDE, litter disappearance due to earthworms) in twoearthworm-invaded and two transition plots in a northernhardwood forest in south-central New York. For details onLDE calculation, see Methods. Error bars represent 95% con-fidence intervals.

much larger L. terrestris. Hence, the present study sup-ports the conclusion that the ecosystem-level effects ofexotic earthworms depend not only on their abundance,but also on the functional role of the species involvedin the invasion. These effects of earthworm functionalgroups on litter disappearance parallel previously ob-served effects on soil phosphorus dynamics in thesesites (Suarez et al. 2004).

Comparisons between the consumption rates in tran-sition and earthworm-invaded plots at the two sites(Fig. 3) suggest that age structure of the earthwormpopulations (and not only their functional role) couldchange the magnitude of their impact on litter disap-pearance. At both sites, the transition plots were clearlydominated by immature earthworms (Tables 2 and 3).At site 3, the rate of litter disappearance per unit earth-worm biomass was 3–4 times higher for the immatureearthworms at the transition plot than for the maturecommunity at the earthworm-invaded plot (Fig. 3).These faster consumption rates could be related to rapidgrowth of immature earthworms, which would increase

their chances of survival and reproduction before thedry period of midsummer or the cold winter months.

The calculated earthworm contribution to litter dis-appearance (LDE) also revealed important differencesbetween the two earthworm communities. In particular,the LDE values for the first sampling interval wereconsiderably higher in site 3 than in site 2 (Fig. 4). Theinitially lower values of LDE at both sites probablyresult primarily from low palatability of the fresh litter,while the much higher LDE in site 3 suggests thatearthworms at this site were less sensitive to initial lowlitter palatability. This unique ability of anecic earth-worms such as L. terrestris to accelerate decompositionof unpalatable litter material was posited by Cooke andLuxton (1980) to result from microbial colonization oflitter drawn into their burrows; hence, rapid litter dis-appearance can occur even when only poor-quality lit-ter is available (Muys et al. 1992). The effect of earth-worm community structure on decomposition has im-portant implications for predicting the dynamics of in-vasion and its effect on soil processes. Interestingly, ithas been suggested that earthworm invasion can in-volve a predictable shift in earthworm communities,with invasion by epigeic and epi-endogeic speciessometimes preceding invasion by anecic and endogeicspecies (Hale et al. 2005). This pattern was also ob-served at our plots, where the edge of earthworm dis-tribution was dominated by L. rubellus followed bycommunities dominated by L. terrestris (Suarez et al.2006). Understanding how the community structure ofinvading earthworms changes through time, and howthat structure affects ecosystem processes will be animportant part of predicting the spatial and temporaldynamics and effects of earthworm invasions. Morefield studies over a broader range of conditions will benecessary to test the generalities of these predictions.

As expected, the two litter types differed in chemicalquality, oak litter having more lignin and less nitrogenthat sugar maple litter. These different qualities sig-nificantly affected the rates of litter disappearance inthe earthworm-invaded plots (Table 1; Appendix C).Sugar maple litter was consumed at faster rates thanoak litter, especially at site 2 on the first two samplingdates (Fig. 3), and LDE values tended to be higher forsugar maple than oak litter early in the decay process(Fig. 4). These patterns suggest that the palatability ofthe two species differed enough to affect the foragingpatterns of the earthworms, especially at the beginningof the experiment. It has been shown that several litter-consuming earthworms forage selectively on weatheredleaves that have been on the ground for some time,ignoring fresh or recently fallen leaves (Satchell andLow 1967, Hendriksen 1990, Doube et al. 1997, Ber-nier 1998). It is likely that this weathering processcould be slower for oak leaves, which are thicker andcontain higher concentrations of phenolic substancesthan sugar maple leaves (McClaugherty et al. 1985,Trofymow et al. 1995). This conclusion also is sup-


ported by the fact that differences between litter typesin the earthworm-invaded plots were absent by the endof the experiment. Thus, after the first year, the twolitter types were consumed at similar rates. From theperspective of the long-term effects of introduced ex-otic earthworms, this interpretation suggests that, byingesting and mixing the litter into the mineral soil,earthworms could counteract differences in decay ratesowing to litter quality differences. Hence, forest soilswith exotic earthworms may be converted from a de-composer system controlled by litter quality, site char-acteristics, and microbial decomposition into a systemcontrolled more by the activity of detritivores (Hene-ghan et al. 1999, Gonzalez and Seastedt 2001). Thischange was clearly shown by the LDE (Fig. 4), whichincreased from 10% to 15% in the transition plots, toas high as 50% for some of the sampling dates in theearthworm-invaded plots.

Surprisingly, even after two full growing seasons,no differences in earthworm density, biomass, or spe-cies composition were observed between boxes con-taining litter of different tree species in each site (Ta-bles 2 and 3). Although these data do not provide aconclusive test of the effects of litter type on the com-position of earthworm communities, they do suggestthat in hardwood-dominated forests with a diverse mix-ture of tree species with litter of differing quality, forestcomposition may not exert a profound influence overlandscape-level patterns of earthworm distribution. Itis clear that plant species can have strong effects onlocal patterns of earthworm activity and communitycomposition (Hendricksen 1990, Boettcher and Kalisz1991, Muys et al. 1992, Zou 1993, Gonzalez and Zou1999), but these effects may be restricted to the ex-tremes of litter palatability (e.g., conifer, Rhododen-dron spp.). For example, earthworm surveys conductedin nearby monospecific tree plantations have shownstrong species effects of Norway spruce and red pine,which support negligible earthworm populations, butno difference in earthworm density among several ad-jacent plantations with different broadleaf deciduousspecies (Suarez 2004).

The rates of litter decomposition in our referenceplots were somewhat higher than for hardwood forestsin comparable climates. For example, in temperate ar-eas with little or no earthworm activity, the litter re-maining after one year of decay usually averages 65–70% (Anderson 1973, Kaneko and Salamanca 1999,Pouyat and Carreiro 2003), whereas after 340 days inour reference plots, these values were 57–64%. Thiswas also true for the decomposition coefficient con-stants (k), which in our reference plots were slightly,but consistently, greater (0.43–0.55) than the averagevalues of 0.33–0.42 reported in the literature for othernorth- temperate hardwood species (Melillo et al. 1982,Staaf 1987, Magill and Aber 1998). These differencesmay be explained in part by our use of litter boxesinstead of litterbags; previous studies have shown that

litterbags may reduce rates of litter decomposition rel-ative to unconfined litter by 10–15% (Bocock and Gil-bert 1957, Anderson 1973). Also, in contrast to otherlitterbag studies, we did not find any difference be-tween the decay rates of the two litter types in thereference plots, despite the differences in litter quality.Many studies have shown that decomposition rates dif-fer among leaf litters, usually as a result of their dif-ferent lignin and nitrogen contents (Anderson 1973,Howard and Howard 1980, Melillo et al. 1982, Kanekoand Salamanca 1999, Berg 2000). The lack of a litter-type effect may have resulted from the use of uncon-fined litter in this study, compared with litterbags inother studies. It is possible that the use of litterbagscould enhance differences in decomposition rates bydifferentially affecting the microclimate inside the lit-terbags, as well as the capacity of different litter typesto retain moisture during decomposition and access tothe litter by macroinvertebrates (Bocock and Gilbert1957, Anderson 1973).

The finding that exotic earthworm activity dramat-ically increased litter disappearance at our study sitewas not unexpected; many studies have shown thatearthworms accelerate the rates of litter disappearanceand organic matter dynamics (James 1991, Fragoso etal. 1993, McLean and Parkinson 1997, Burtelow et al.1998, Lavelle et al. 1998, Bohlen et al. 2004b), but thelarger implications are not always clear. The elimina-tion of the forest floor and the processing and incor-poration of virtually all of the annual litter fall by earth-worms means that a very large amount of carbon ismoved each year from the surface to deeper layers ofthe soil. At Arnot Forest, this change has increased theamount of organic matter in the mineral soil horizons,but the net result has been a 30% decrease in total soilorganic matter storage in the surface soil (Bohlen etal. 2004b). Because earthworms are known to havevery low assimilation efficiencies (Hendrix 1995, Ed-wards and Bohlen 1996), we assume that the increasedrates of organic matter decomposition must be drivennot by earthworm consumption directly, but by in-creased microbial activity in our earthworm-invadedplots (Li et al. 2002, Groffman et al. 2004). Presum-ably, the increased microbial-driven litter decay in ourearthworm-invaded plots is due to three factors: thecomminution of the litter by the earthworms ; its trans-location to deeper layers of the soil with more stablesoil moisture levels ; and the addition of labile formsof carbon during passage through the earthworm gut,which has been shown to fuel increased microbial ac-tivity (Scheu and Parkinson 1994, McLean and Par-kinson 1997, Haynes et al. 1999, Scheu et al. 2002,Groffman et al. 2004).

The large increase in litter disappearance that wemeasured (Fig. 1) and the reduction of soil organicmatter reported for our site and other earthworm-in-vaded sites (Alban and Berry 1994, Zhang and Hendrix1995, Bohlen et al. 2004b), strongly suggest that ac-


curate predictions of carbon budget changes in forestmust account for invasion by exotic earthworms. Fur-thermore, we have shown that the density and speciescomposition of the communities of invading earth-worms can control the magnitude and direction of theecosystem changes produced by these animals. Futurecarbon storage in northern forest soils is likely to de-pend on climatic patterns and land use histories andchange, but the presence of invasive earthworms, theirpotential spread, and the species composition of theircommunities should also be considered.

ACKNOWLEDGMENTS

We thank Will Kessler, Becky Fahey, Bob Fahey, Yon-Hua,and Suzanne Wapner for their help with field and laboratorywork, and for continuous logistical support. We also thankthe members of the Fahey, Yavitt, and Bedford lab groups atCornell University, who provided valuable suggestions forthe preparation of this manuscript, and Galo Zapata and twoanonymous reviewers for their helpful suggestions on thismanuscript. This research was funded by the National ScienceFoundation grant DEB-9726869, and E. Suarez was alsofunded by the Ecuadorian Foundation for Science and Tech-nology (FUNDACYT).

LITERATURE CITED

Alban, D. H., and E. C. Berry. 1994. Effects of earthworminvasion on morphology, carbon, and nitrogen of a forestsoil. Applied Soil Ecology 1:243–249.

Anderson, J. M. 1973. The breakdown and decomposition ofsweet chestnut (Castanea sativa Mill.) and beech (Fagussylvatica L.) leaf litter in two deciduous woodland soils. I.Breakdown, leaching and decomposition. Oecologia 12:251–274.

Andren, O., J. Bengtsson, and M. Clarholm. 1995. Biodi-versity and species redundancy among litter decomposers.Pages 141–151 in H. P. Collins, G. P. Robertson, and M.J. Klug, editors. The significance and regulation of soilbiodiversity. Kluwer Academic, Dordrecht, The Nether-lands.

Andren, O., T. Katterer, and R. Hyvonen. 2001. Projectingsoil fauna influence on long-term soil carbon balances fromfaunal exclusion experiments. Applied Soil Ecology 18:177–186.

Berg, B. 2000. Litter decomposition and organic matter turn-over in northern forest soils. Forest Ecology and Manage-ment 133:13–22.

Bernier, N. 1998. Earthworm feeding activity and develop-ment of the humus profile. Biology and Fertility of Soils26:215–223.

Bocock, K. L., and O. J. W. Gilbert. 1957. The disappearanceof leaf litter under different woodland conditions. Plant andSoil 9:179–185.

Boettcher, S. E., and P. J. Kalisz. 1991. Single-tree influenceof earthworms in forest soils in eastern Kentucky. SoilScience Society of America Journal 55:862–865.

Bohlen, P. J., P. M. Groffman, T. J. Fahey, M. C. Fisk, E.Suarez, D. M. Pelletier, and R. T. Fahey. 2004a. Ecosystemconsequences of exotic earthworm invasion of north tem-perate forests. Ecosystems 7:1–12.

Bohlen, P. J., R. W. Parmelee, D. A. McCartney, and C. A.Edwards. 1997. Earthworm effects on the carbon and ni-trogen dynamics of surface litter in corn agroecosystems.Ecological Applications 7:1341–1349.

Bohlen, P. J., D. M. Pelletier, P. M. Groffman, T. J. Fahey,and M. C. Fisk. 2004b. Influence of earthworm invasionon redistribution and retention of soil carbon and nitrogenin northern temperate forests. Ecosystems 7:13–28.

Bohlen, P. J., S. Scheu, C. M. Hale, M. McLean, S. Migge,P. M. Groffman, and D. Parkinson. 2004c. Non-native in-vasive earthworms as agents of change in northern tem-perate forests. Frontiers in Ecology and the Environment2:427–435.

Burtelow, A. E., P. J. Bohlen, and P. M. Groffman. 1998.Influence of exotic earthworm invasion on soil organic mat-ter, microbial biomass and denitrification potential in forestsoils of the northeastern United States. Applied Soil Ecol-ogy 9:197–202.

Cooke, A., and M. Luxton. 1980. Effect of microbes on foodselection by Lumbricus terrestris. Revue d’Ecologie etBiologie du Sol 17:365–370.

Cortez, J., and M. B. Bouche. 1998. Field decomposition ofleaf litters: earthworm–microorganism interactions: theploughing-in effect. Soil Biology and Biochemistry 30:795–804.

Cote, B., and J. W. Fyles. 1994. Leaf litter disappearance ofhardwood species of southern Quebec: interaction betweenlitter quality and stand type. Ecoscience 1:322–328.

Doube, B. M., O. Schmidt, K. Killham, and R. Correll. 1997.Influence of mineral soil on the palatability of organic mat-ter for lumbricid earthworms: a simple food preferencestudy. Soil Biology and Biochemistry 29:569–575.

Edwards, C. A., and P. J. Bohlen. 1996. Biology and ecologyof earthworms. Third edition. Chapman and Hall, London,UK.

Edwards, C. A., and G. W. Heath. 1963. The role of soilanimals in the breakdown of leaf materials. Pages 76–80in J. Doeksen and J. van der Dirft, editors. Soil organisms.North Holland, Amsterdam, The Netherlands.

Fahey, T. J. 1998. Recent changes in an upland forest insouth-central New York. Journal of the Torrey BotanicalSociety 125:51–59.

Fain, J. J., T. A. Volk, and T. J. Fahey. 1994. Fifty years ofchange in an upland forest in south-central New York: gen-eral patterns. Bulletin of the Torrey Botanical Club 121:130–139.

Fisk, M. C., T. J. Fahey, P. M. Groffman, and P. J. Bohlen.2004. Earthworm invasion, fine root distributions and soilrespiration in north temperate forests. Ecosystems 7:55–62.

Fragoso, C., I. Barois, C. Gonzalez, C. Arteaga, and J. C.Patron. 1993. Relationship between earthworms and soilorganic matter levels in natural and managed ecosystemsin the Mexican tropics. Pages 231–241 in K. Mulongoyand R. Merckx, editors. Soil organic dynamics and sus-tainability of tropical agriculture. Catholic University, Wi-ley-Sayce, Leuven, Belgium.

Gonzalez, G., and T. R. Seastedt. 2001. Soil fauna and plantlitter decomposition in tropical and subalpine forests. Ecol-ogy 82:955–964.

Gonzalez, G., and X. Zou. 1999. Plant and litter influenceson earthworm abundance and community structure in atropical wet forest. Biotropica 31:486–493.

Groffman, P. M., P. J. Bohlen, M. C. Fisk, and T. J. Fahey.2004. Exotic earthworm invasion and microbial biomassin temperate forest soils. Ecosystems 7:45–54.

Gundale, M. J. 2002. Influence of exotic earthworms on thesoil organic horizon and the rare fern Botrychium mormo.Conservation Biology 16:1555–1561.

Haimi, J., and V. Huhta. 1990. Effects of earthworms ondecomposition processes in raw humus forest soil: a mi-crocosm study. Biology and Fertility of Soils 10:178–183.

Hale, C. M. 2004. Ecological consequences of exotic invad-ers: interactions involving European earthworms and nativeplant communities in hardwood forests. Dissertation. Uni-versity of Minnesota, Minneapolis, Minnesota, USA.

Hale, C. M., L. E. Frelich, and P. Reich. 2000. Impacts ofinvading European earthworms on understory plant com-


munities in previously worm-free hardwood forest of Min-nesota. Abstracts of the Ecological Society of America 85:112.

Hale, C. M., L. E. Frelich, and P. B. Reich. 2005. ExoticEuropean earthworm invasion dynamics in northern hard-wood forests of Minnesota, USA. Ecological Applications15:848–860.

Haynes, R. J., P. M. Fraser, R. J. Tregurtha, and J. E. Piercy.1999. Size and activity of the microbial biomass and N, Sand P availability in earthworm casts derived from arableand pastoral soil and arable soil amended with plat residues.Pedobiologia 43:568–573.

Hendriksen, N. B. 1990. Leaf litter selection by detritivoreand geophagous earthworms. Biology and Fertility of Soils10:17–21.

Hendrix, P. 1995. Earthworm ecology and biogeography inNorth America. Lewis Publishers, Boca Raton, Florida,USA.

Hendrix, P., and P. J. Bohlen. 2002. Exotic earthworm in-vasions in North America: ecological and Policy implica-tions. BioScience 52:801–811.

Heneghan, L., D. C. Coleman, X. Zou, D. A. Crossley, andB. L. Haines. 1999. Soil microarthropod contributions todecomposition dynamics: tropical–temperate comparisonsof a single substrate. Ecology 80:1873–1882.

Howard, D. M., and P. J. A. Howard. 1980. Effect of species,source of litter, type of soil, and climate on litter decom-position. Microbial decomposition of tree and shrub leaflitter 3. Oikos 34:115–124.

James, S. W. 1991. Soil, nitrogen, phosphorus and organicmatter processing by earthworms in tallgrass prairie. Ecol-ogy 72:2101–2109.

Jegou, D., D. Cluzeau, J. Balesdent, and P. Trehen. 1998.Effects of four ecological categories of earthworms on car-bon transfer in soil. Applied Soil Ecology 9:249–255.

Kaneko, N., and F. Salamanca. 1999. Mixed leaf litter effectson decomposition rates and soil microarthropod commu-nities in an oak–pine stand in Japan. Ecological Research14:131–138.

Lavelle, P., B. Pashanasi, F. Charpentier, C. Gilot, J. Rossi,J. A. Derouard, J. Ponge, and N. Bernier. 1998. Large scaleeffects of earthworms on soil organic matter and nutrientdynamics. Pages 103–122 in C. A. Edwards, editor. Earth-worm ecology. St. Lucie Press, Boca Raton, Florida, USA.

Li, X., M. C. Fisk, T. J. Fahey, and P. J. Bohlen. 2002. In-fluence of earthworm invasion on soil microbial biomassand activity in a northern hardwood forest. Soil Biologyand Biochemistry 34:1929–1937.

Liu, Z. G., and X. Zou. 2002. Exotic earthworms accelerateplant litter decomposition in a Puerto Rican pasture and awet forest. Ecological Applications 12:1406–1417.

Magill, A. H., and J. D. Aber. 1998. Long-term effects ofexperimental nitrogen additions on foliar litter decay andhumus formation in forest ecosystems. Plant and Soil 203:301–311.

McClaugherty, C. A., J. Pastor, J. Aber, and J. M. Melillo.1985. Forest litter decomposition in relation to soil nitro-gen dynamics and litter quality. Ecology 66:266–275.

McLean, M. A., and D. Parkinson. 1997. Soil impacts of theepigeic earthworm Dendrobaena octaedra on organic mat-ter and microbial activity in lodgepole pine forest. Cana-dian Journal of Forest Research 27:1907–1913.

Melillo, J. M., J. D. Aber, and J. F. Muratore. 1982. Nitrogenand lignin control of hardwood leaf litter decompositiondynamics. Ecology 63:621–626.

Muys, B., N. Lust, and P. Granval. 1992. Effects of grasslandafforestation with different tree species on earthworm com-munities: litter decomposition and nutrient status. Soil Bi-ology and Biochemistry 24:1459–1466.

Olson, J. S. 1963. Energy storage and the balance of pro-ducers and decomposers in ecological systems. Ecology 44:322–331.

Pouyat, R. V., and M. M. Carreiro. 2003. Controls on massloss and nitrogen dynamics of oak leaf litter along an ur-ban–rural land-use gradient. Oecologia 135:288–298.

Raw, F. 1959. Estimating earthworm populations by usingformalin. Nature 184:1661–1662.

SAS Institute. 1987. SAS statistics user’s guide. Version 8.2.SAS Institute, Cary, North Carolina, USA.

Satchell, J. E., and D. G. Low. 1967. Selection of leaf litterby Lumbricus terrestris. Pages 102–119 in O. Graff and J.E. Satchell, editors. Soil organisms. North Holland, Am-sterdam, The Netherlands.

Scheu, S., and D. Parkinson. 1994. Effects of invasion of anaspen forest (Canada) by Dendrobaena octaedra (Lum-bricidae) on plant growth. Ecology 75:2348–2361.

Scheu, S., N. Schlitt, A. V. Tiunov, J. E. Newington, and T.H. Jones. 2002. Effects of the presence and communitycomposition of earthworms on microbial community func-tioning. Oecologia 133:254–260.

Shipitalo, M. J., R. Protz, and A. D. Tomlin. 1988. Effect ofdiet on the feeding and casting activity of Lumbricus ter-restris and L. rubellus in laboratory culture. Soil Biologyand Biochemistry 20:233–237.

Staaf, H. 1987. Foliage litter turnover and earthworm pop-ulations in three beech forests of contrasting soil and veg-etation types. Oecologia 72:58–64.

Suarez, E. 2004. Invasion of northern hardwood forests byexotic earthworm communities in south-central New York.Dissertation. Cornell University, Ithaca, New York, USA.

Suarez, E., T. J. Fahey, P. M. Groffman, J. B. Yavitt, and P.J. Bohlen. 2006. Spatial and temporal dynamics of exoticearthworm communities along invasion fronts in a tem-perate hardwood forest in south-central New York. Bio-logical Invasions 8, in press.

Suarez, E., D. M. Pelletier, T. J. Fahey, P. M. Groffman, P. J.Bohlen, and M. C. Fisk. 2004. Effects of exotic earthwormson soil phosphorus cycling in two broadleaf temperate for-ests. Ecosystems 7:28–44.

Trofymow, J. A., C. M. Preston, and C. E. Prescott. 1995.Litter quality and its potential effect on decay-rates of ma-terials from Canadian forests. Water Air and Soil Pollution82:215–226.

Wardle, D. A., and P. Lavelle. 1997. Linkages between soilbiota, plant litter quality and decomposition. Pages 107–124 in G. Cadisch and K. E. Giller, editors. Driven bynature: plant litter quality and decomposition. CAB Inter-national, Wallingford, UK.

Zhang, Q. L., and P. Hendrix. 1995. Earthworm (Lumbricusrubellus and Aporrectodea caliginosa) effects on carbonflux in soil. Soil Science Society of America Journal 59:816–823.

Zou, X. 1993. Species effects on earthworm density in trop-ical tree plantations in Hawaii. Biology and Fertility ofSoils 15:35–38.

APPENDIX A

A table showing litter disappearance exponential rate constants for sugar maple and red oak litter samples in two exoticearthworm invasion fronts at Arnot Forest (central New York) (Ecological Archives A016-010-A1).


APPENDIX B

An ANOVA table comparing the total density and biomass of exotic earthworms samples beneath litter boxes with sugarmaple or oak litter in two earthworm-invaded plots in a hardwood forest in central New York (Ecological Archives A016-010-A2).

APPENDIX C

An ANOVA table evaluating the effects of litter type, site, and sampling date on litter consumption rates (EcologicalArchives A016-010-A3).

Patterns Of Litter Disappearance In A Northern Hardwood Forest Invaded By Exotic Earthworms

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