E A R T H W O R M I N V A S I O N O F F O R E S T E C O S Y S T E M S

Ecosystem Consequences of ExoticEarthworm Invasion of North

Temperate Forests

Patrick J. Bohlen,1* Peter M. Groffman,2 Timothy J. Fahey,3

Melany C. Fisk,3,4 Esteban Suarez,3 Derek M. Pelletier,3 andRobert T. Fahey3

1Archbold Biological Station, Lake Placid, Florida 33852, USA; 2Institute of Ecosystem Studies, Box AB, Millbrook, New York12545, USA; 3Department of Natural Resources, Cornell University, Ithaca, New York 14853, USA; 4Department of Biology,

Appalachian State University, Boone, North Carolina 28608-2027, USA

ABSTRACTThe invasion of north temperate forests by exoticspecies of earthworms is an important issue that hasbeen overlooked in the study and management ofthese forests. We initiated research to address thehypothesis that earthworm invasion will have largeconsequences for nutrient retention and uptake inthese ecosystems. In this special feature of Ecosys-tems, we present five papers describing results fromour experiment. In this paper, we (a) introduce ourexperimental approach and conceptual model ofhow earthworms influence forest ecosystem pro-cesses, (b) describe the characteristics of the studyareas and earthworm communities at our two studylocations, and (c) provide a brief overview and syn-thesis of the main findings. The most dramatic ef-fect of earthworm invasion was the loss of the forestfloor at an undisturbed forest site, which altered thelocation and nature of nutrient cycling activity in

the soil profile. Invasion changed soil total carbon(C) and phosphorus (P) pools, carbon–nitrogen(C:N) ratios, the loss and distribution of differentsoil P fractions, and the distribution and function ofroots and microbes. Response to invasion variedwith site characteristics and earthworm species.Our results suggest that exotic earthworm invasionis a significant factor that will influence the struc-ture and function of northern temperate forest eco-systems over the next few decades. Regional eval-uations of these forests will need to consider thepresence or absence of earthworms along withother important ecosystem drivers, such as pollu-tion, climate, and underlying soil characteristics.

Key words: exotic species; invasions; carbon; ni-trogen; phosphorus; roots; nutrient cycling; forests.

INTRODUCTION

The effect of invasions by exotic species hasemerged as a major topic in ecology over the past 20years (Drake and Mooney 1989; Mack and others2000). However, most invasion studies have been

concerned with changes in aboveground plant andanimal communities, with a focus on losses inbiodiversity. Much less work has been devoted toinvasions of the soil community (Brussaard andothers 1997) or evaluation of the effect of invasionon ecosystem processes related to nutrient cyclingand loss (Hooper and others 2000; Ehrenfeld andothers 2001).

In forests in the northeastern United States, andin many other areas of the world, exotic species

Received 13 February 2002; accepted 27 January 2003; published online12 January 2004.*Corresponding author; e-mail: pbohlen@archbold-station.org

Ecosystems (2004) 7: 1–12DOI: 10.1007/s10021-003-0126-z ECOSYSTEMS

© 2004 Springer-Verlag

1

invasions are only one of a number of human andnatural stressors that threaten the integrity of theseecosystems. In addition to species changes, air pol-lution (for example, acid rain, ozone, nitrogen [N]deposition), insect outbreaks, increases in verte-brate herbivores (for example, deer, moose), cli-mate change, and other factors affect the structureand function of forest ecosystems in diverse andcomplex ways (Aber and others 1989, 2001, Pastorand others 1993). Our ability to predict and managethe structure and function of forest ecosystems willdepend on how well we can meet the difficult chal-lenge of evaluating the relative importance of dif-ferent stresses and understanding their interactionwith one another (Vitousek 1994).

The invasion of northern forests by exotic speciesof earthworms is an important issue that has beenoverlooked in the study and management of theseforests. Such invasion has the potential to lead tomajor changes in patterns of nutrient cycling andloss, especially in areas with no history of earth-worm activity. Earthworms can eliminate the forestfloor (see for example, Langmaid 1964; Alban andBerry 1994), which is considered to be a key com-ponent of the inherent stability of many forest eco-systems (Bormann and Likens 1979). Thus, theirintroduction to forest sites previously devoid ofearthworm populations may lead to state change inthose systems. There is evidence that such invasionsare occurring over a wide geographic area.

Biogeographic studies and analyses of earthwormdistribution suggest that native earthworm speciesare rare in the northern forests of North America,presumably because they were eliminated from theregion during the last glacial period and were slowto recolonize the area after the glaciers receded(Reynolds 1994; James 1995). Most earthwormsthat occur in northern forests in North America areexotic species, and their recent invasion into newareas has caused marked changes in forest floorcharacteristics and nutrient dynamics (Scheu andParkinson 1994a, 1994b; Alban and Berry 1994;Groffman and Bohlen 1999). Although earthwormsare a natural component of many forest ecosystems,it is not known how their invasion of new sites willaffect nutrient cycling in the short and long term.Nor is it known how widespread the earthworminvasion of northern forests is, or what areas aresusceptible to invasion, or how these circumstancesmight change over time with changing climate,land use, and other factors within these systems.

In 1998, we initiated a research project to addressthe global hypothesis that earthworm invasion ofnorth temperate forests will have large conse-quences for nutrient retention and uptake in these

ecosystems. Our study addressed the followingquestions: (a) How will earthworms influence thedistribution, storage, and transport of soil carbon(C), N, and phosphorus (P)? (b) Will earthworminvasion increase hydrologic losses of N and P andgaseous losses of C and N from forest soil? (c) Howwill earthworm invasion influence soil microbialbiomass and N cycling activities? (d) How willchanges in the forest floor induced by earthworminvasion influence the distribution of fine roots inthe soil profile? (e) Will the effect of earthworms onforest soil nutrient cycling have consequences forplant nutrient uptake and foliar nutrient ratios?

To address these questions, we set up study plotsin areas with and without earthworms in two forestsites with contrasting land-use histories dominatedby sugar maple (Acer saccharum) in New York State,USA. One of these forest sites was logged in the late19th century but has been undisturbed since thenand has never been cultivated. The other site waspreviously cultivated but abandoned to regrowth60–80 years ago. Our research characterized theeffects of earthworm invasion on forest floor depth,soil C and N storage and cycling, soil P forms, hy-drologic losses of N and P, soil microbial biomassand N cycling activities and fine-root distributionand soil respiration. The individual reports contrib-uted by Bohlen, Fisk, Groffman, Suarez and theircolleagues and collected in this special feature willaddress each of these issues in turn.

In this introductory paper, we (a) provide a gen-eral overview of our experimental approach andconceptual model of how earthworms influenceforest ecosystem processes; (b) describe the charac-teristics of the study areas, including earthwormcommunities and distribution patterns at one of ourstudy locations; and (c) provide a brief overview ofthe main findings from our research, which will bedescribed in detail in the four other papers thatcomprise this special feature.

CONCEPTUAL MODEL

Our conceptual model of the effects of earthwormson temperate forest ecosystem biogeochemistry at-tempts to encompass physical, geochemical, andbiological effects (Figure 1). The physical effects ofearthworms on soil porosity and water flow havebeen well studied in agricultural soils, but they havereceived less attention in forest soils (Tomlin andothers 1995; Edwards and Bohlen 1996; Jordan andothers 2000). The burrowing activity of certainearthworm species creates macropores that cantransport a significant proportion of soil water anddissolved nutrients from surface to subsurface soil

2 P. J. Bohlen and others

horizons. Although these macropores have beenshown to alter the distribution of water inputs be-tween surface runoff and infiltration to groundwa-ter in agricultural systems (Shipitalo and others1994; Subler and others 1997; Dominguez and othersforthcomming), their role in forest soils, which tendto have inherently high infiltration rates relative tocultivated soils, is less well understood. It is alsonoteworthy that different species of earthwormsform burrows and macropores with different orien-tation, continuity, size, and permanence; therefore,different species are likely to have different effectson the physical characteristics of forest soils.

A particularly striking physical effect of earth-worm invasion of forest soils is the alteration of soilhorizons. Often it leads to elimination of the surfaceorganic horizon or forest floor (Langmaid 1964;Alban and Berry 1994). The forest floor is consid-ered to be an important structural feature of manytemperate forest ecosystems, providing protectionagainst soil erosion and facilitating forest regenera-tion after disturbance (Covington 1981; Bormannand Likens 1979; Carlyle 1986). By eliminating ordecreasing the thickness or continuity of the forestfloor, invading earthworms can attenuate the mod-ulating effects of this important soil layer.

Earthworm activity creates a series of geochemi-cal effects that are especially important for the cy-cling and availability of P in forest soils. This isbecause the availability of P, unlike that of N, isstrongly influenced by the physical adsorption orfixation of P in mineral soil (Lopez-Hernandez andBurnham 1974; Pare and Bernier 1989b). Essen-

tially all of the P in the forest floor is in organic form(Harrison and others 1996). Much of the P uptakein forests with an intact floor takes place in theforest floor, where accumulated organic P is slowlymineralized and released for uptake by fine roots(Wood and others 1984; Yanai 1992). As earth-worms mix mineral material into the forest floor,they increase the likelihood that mineral oxides willfix P (Walbridge and others 1991), depending onsoil pH and the abundance of aluminum (Al) oriron (Fe) oxides (Pare and Bernier 1989b). A com-parison of mull (worm-worked) and mor (noworms) soils in sugar maple stands in the Appala-chian mountains of southern Quebec showed that Pavailability was significantly lower in mull than inmor soils (Pare and Bernier 1989a, 1989b, 1989c).However, at the initial stages of invasion, earth-worms may increase P availability in the mineralsoil by increasing soil pH and the mineralization oforganic matter in the forest floor, although thiseffect has not been well studied (Scheu and Parkin-son 1994a).

The biological effects of earthworm invasion oftemperate forest soils are complex and likely varyby site and invading species. The ability of earth-worms to accelerate the decomposition of fresh or-ganic material is well established (Satchell 1967;Neilson and Hole 1964; Edwards and Bohlen 1996).In combination with their ability to consume theforest floor, earthworm populations have the po-tential to reduce the levels of organic matter inforest soil. However, earthworm effects on decom-position can be balanced by increases in the amount

Figure 1. Conceptual modelillustrating mechanisms ofeffects of earthworm inva-sion on forest biogeochemis-try. The diagram is simplifiedto illustrate main effects; ac-tual mechanisms are moreinterrelated. For example,stimulation of microbial ac-tivity may not only increasecarbon (C) mineralizationbut also enhance denitrifica-tion and thus affect nitrogen(N) loss. Physical protectionof C in stable aggregatesformed from earthwormcasts may protect soil C fromfurther mineralization andenhance C storage.

Earthworm Invasion of Northern Forests 3

of C protected in stabilized earthworm casts (Martin1991) and by the formation of stable organo-min-eral complexes (Scheu and Wolters 1991).

The ability of earthworms to stimulate N cycleprocesses in forest soils is well established (Haimiand Huhta 1990; Haimi and Boucelham 1991; Rob-inson and others 1992; Scheu and Parkinson 1994a;Steinberg and others 1996; Burtelow and others1997). This condition arises from the creation ofnutrient-rich casts, which often have relatively highconcentrations of N and provide ideal conditions formicrobial activity compared to surrounding soils(Lunt and Jacobson 1944; Parle 1963; Lavelle andMartin 1992). Nitrification, which can foster themobilization and leaching of N and other nutrientsfrom the forest floor, is particularly susceptible tostimulation by earthworms (Day 1950; Parle 1963;Steinberg and others 1996).

Earthworm effects on biological processes mightalso lead to increases in gaseous losses of N fromforest ecosystems. Fresh earthworm casts generallyhave greater denitrification rates than surroundingsoil (Svensson and others 1986; Elliot and others1990). In pastures in England, surface-depositedearthworm casts accounted for an estimated 12% oftotal denitrification losses from an unfertilized pas-ture and 26% of losses from a fertilized pasture(Knight and others 1992). The effect of earthwormson denitrification in forest soils is unknown.

The elimination of forest floor horizons by earth-worms undoubtedly causes significant shifts in thedistribution of fine roots, as well as their physiologyand demographics, although no studies have explic-itly examined earthworm influences on fine-rootproduction and function in forests. Forest floorroots have been shown to differ significantly frommineral soil roots in structure, function, and de-mography (Hendrick and Pregitzer 1992; Fahey andHughes 1994). Fine roots in forest floor and mineralsoils may also have contrasting effects on soil Nturnover (Bradley and Fyles 1996). Lawrence andothers (2003) observed reduced mycorrhizal colo-nization rates and lower colonized root length inorganic surface soil horizons in areas with activeearthworm populations, suggesting that earth-worms may alter mycorrhizal interactions impor-tant to nutrient uptake by tree roots.

It is not known whether the changes in soil nu-trient cycling related to earthworm invasion influ-ence plant nutrient uptake or retranslocation pro-cesses in canopy trees. Much of the annualrequirement for N and P in temperate deciduousforests is met by retranslocation from foliage priorto leaf fall (Ryan and Bormann 1982). The sensitiv-ity of foliar nutrition to changes in soil nutrient

availability has been demonstrated in numerousfield fertilization trials (Binkley 1986), as well as innutrient depletion experiments (Waring and Pit-man 1985). Shifts in the relative availability of dif-ferent plant nutrients usually are translated rapidlyinto element ratio changes in foliage, which can belinked to nutrient deficiency or imbalances (Inges-tad and Agren 1992).

The sensitivity of nutrient retranslocation tochanges in soil nutrient status varies across forestecosystems. Less efficient P retranslocation hasbeen observed in fertilized forests as compared tounfertilized forests (Wienand and Stock 1995; Mu-gasha and others 1996; Fahey and others 1997).Hence it is uncertain whether the changes in P andN availability that occur after earthworm invasionwill alter the retranslocation of these nutrients. Pareand Bernier (1989c) found a negative correlationbetween foliar P nutrition of sugar maple and thepresence of earthworms across 10 sugar maplestands in southern Canada; they hypothesized thatreduced P supply in mull soils had led to impaired Pnutrition of trees.

Due to the ability of earthworms to alter physical,geochemical, and biological processes in soil, it islikely that earthworm invasion will have importanteffects on nutrient retention and loss in temperateforest ecosystems. These effects are likely to varystrongly with site and the species of earthworminvolved in the invasion. Sites with different inher-ent fertility, organic matter levels, and vegetationare likely to respond differently to invasion. Fur-thermore, different earthworm species have differ-ent effects on soil. The effects of deep-burrowingspecies (for example, the European species Lumbri-cus terrestris) likely differ dramatically from those oflitter-dwelling species (for example, the Asian spe-cies Amynthas hawayanus).

In light of these complex interactions, there is aneed for greater understanding of the role of earth-worm invasions in northern forests. We expect thatexotic earthworms will invade many forest sites inthe north temperate region of the United States andCanada in the coming decades due to their inadver-tent introduction by humans or natural invasion.Moreover, global warming could contribute to thenorthward expansion of the range of certain earth-worm species, such as Amynthas spp., that currentlyhave a more southerly distribution. Forests withearthworms may function in a fundamentally dif-ferent way from forests that lack earthworms. Inregional evaluations of forests as transformers ofmatter and energy, we may need to consider thepresence or absence of earthworms in conjunctionwith other important drivers of these transforma-

4 P. J. Bohlen and others

tions, such as pollution, climate, plant communitycomposition, or edaphic factors.

SITE DESCRIPTION AND EXPERIMENTALDESIGN

We used two experimental approaches to evaluatethe effect of earthworm invasion on the biogeo-chemistry of temperate forest ecosystems. The firstapproach involved comparing forest stands alreadyinvaded by earthworms with adjacent stands thatlacked earthworms, viewing these stands as end-points along a gradient of earthworm invasion. Re-sults from this comparison are contained in thisgroup of papers. The second approach involvedcontrolled introductions of earthworms into exper-imental forest plots. These plots will provide insightinto the transition that occurs immediately afterearthworm invasion, but we do not yet haveenough data from these plots to report on the ef-fects of the recent introductions.

We established research plots at two differentfield sites in New York State, USA. One set of plotswas located at Cornell University’s Arnot Forest, amaple-dominated second-growth forest with nohistory of agricultural activity, in central New York(42°16'N, 76°28'W). Another set of plots was lo-cated at the Institute of Ecosystem Studies’ Tomp-kins Farm, a maple-dominated secondary-growthforest on an abandoned farm site in eastern NewYork (41°50'N, 73°45'W). At each site, three sets ofpaired plots (20 � 20 m) were selected where areasof forest without any apparent earthworm activitywere adjacent to areas with established earthwormpopulations. Introduction plots (5 � 5 m) wereestablished near the no-worm reference areas ateach location.

The plots comparing invaded and noninvaded(reference) areas were carefully chosen to avoiddifferences in soils, vegetation, and topographyamong the plots in each pair. In most cases, plotswere located at different distances from obviousworm refugia—for example, wet areas orstreams—in similar slope positions and with similarvegetation. Ongoing research at the Arnot Forestsite is examining patterns and mechanisms of earth-worm colonization in more detail.

Arnot Forest is situated on the northern Allegh-eny Plateau physiographic province. Annual rain-fall is 100 cm; average summer and winter temper-atures are 22.0°C and �4.0°C, respectively. Soilsare derived from bedrock and glacial till, consistingmostly of shales of the Upper Devonian Period. Soilsare acidic Dystrochrepts with a well-developed for-est floor (Oi, Oe, Oa) averaging about 4 cm thick

and overlying an acidic (pH 4.5–5.0) mineral hori-zon. Forest composition and dynamics at Arnot For-est have been described in detail elsewhere (Fainand others 1994; Volk and Fahey 1994; Fahey1998). The current forest, which was logged in thelate 19th century and has developed with minimaldisturbance since then, is dominated by six speciescharacteristic of Allegheny northern hardwood for-ests (sugar maple, red maple, beech, white ash,basswood, hemlock).

Tompkins Farm is situated on the northern ex-tension of the Great Appalachian Valley of theRidge and Valley physiographic province. The sitereceives annual rainfall of around 98 cm, evenlydistributed throughout the year; it has a mean sum-mer temperature of 21.8°C and a winter tempera-ture of �2.4°C. Late Cambrian–early Ordovicianshales and slates underlie the upland forests at thesite. Soils are principally acidic (pH 4.2–5.0) Dystro-chrepts and are silt loams derived from glacial tilland outwash. Most of the 31-ha site was abandonedto regrowth within the past 60–80 years; prior tothat time, it had been in pasture and row cropagriculture.

EARTHWORM POPULATIONS ANDDISTRIBUTION PATTERNS

Earthworm populations were assessed in April 1999(the peak period of earthworm activity) at bothstudy sites using a standard formalin extractiontechnique (Raw 1959). After 8 L of 0.25% formalinwas applied to four 0.25-m2 areas within each plot,earthworms emerging from the soil were collectedinto vials containing 4% formalin and returned tothe lab for identification. Sampling was conductedin both earthworm-colonized and worm-free refer-ence plots. Collected worms were preserved in 4%formalin and identified to species. In June 2000 atArnot Forest, earthworm populations were sampledas in 1999, but additional samples were collected intransition zones between areas with worms and thosewithout worms to characterize the transition inearthworm communities between these two areas.

The distribution of earthworms in the Arnot For-est was surveyed using the line intercept technique(Canfield 1941). The surveys were conducted attwo different spatial scales; the entire 2,000-ha Ar-not Forest was surveyed in 2000, whereas the vi-cinity of the research plots was surveyed in 1998(Figure 2). The 1998 survey consisted of 10transects (total transect length, 3.41 km) that en-compassed the area of the three pairs of intensivestudy plots. In 2000, an extensive survey was con-ducted to encompass the entire 2,000-ha Arnot

Earthworm Invasion of Northern Forests 5

Forest; a grid of transects (total length, 60.92 km)that comprised the surveyed lot lines in the forestwas sampled. For both surveys, we recorded thelength of transect line intersecting three visualclasses that corresponded to different amounts ofearthworm mixing of the forest floor: (a) com-pletely mixed—mineral soil mostly exposed at thesurface; (b) transition—some visual evidence ofearthworm activity in the form of casts and middenpiles; and (c) no evidence of worm activity. Thisprocedure was not done at the Tompkins Farm sitebecause the relative lack of forest floor at that sitemade such assessments impractical.

Earthworm communities at the two sites differedfunctionally in that the communities at TompkinsFarm were dominated by the deep-burrowing, lit-ter-feeding species Lumbricus terrestris, whereas thecommunities at Arnot Forest were dominated bythe epi-endogeic species Lumbricus rubellus (exceptfor plot 3 at Arnot, where L. terrestris was dominant)(Table 1). In general, the earthworm communitywas more species-rich at Arnot, where there was atotal of six species, than at Tompkins, where therewere only four species. Furthermore, total earth-worm biomass was distributed more evenly amongspecies at Arnot forest than at Tompkins Farm,where L. terrestris comprised an average of 70% oftotal earthworm biomass. Octolasion tyrteaum wasthe main endogeic species at both sites, except atplot 3 at Tompkins Farm, where Aporrectodea tuber-culata was the only endogeic earthworm species.Population density did not differ between Arnot

Forest and Tompkins Farm, but earthworm biomasswas significantly greater at Tompkins Farm, be-cause large individuals of L. terrestris dominated thecommunity there (P � 0.049). The differences inearthworm communities between study sites andwithin plots at Arnot Forest may explain some ofthe observed functional effects of earthworms on,for example, soil P dynamics and nutrient leachingpatterns (Surez and others 2004).

Some earthworms were recovered from plotsdesignated as “no-worm” plots at both study sites in1999. At Arnot Forest, no earthworms were recov-ered from no-worm plots 2 and 3, but there werethree earthworms per meter totaling 0.15 g m–2, inno-worm plot 1, which could not be identified tospecies due to lack of mature individuals. The pres-ence of these worms was considered to be negligiblebecause they were all very small individuals andcomprised only 0.4% of the average earthwormbiomass in the adjacent worm plot at Arnot. AtTompkins Farm, no earthworms were recovered inno-worm plot 2, but there were 0.2 g m–2 of earth-worms in no-worm plot 1 and 2.5 g m–2 in no-worm plot 3 (L. castaneus and L. terrestris in bothcases), which amounted to 0.3% and 2.2%, respec-tively, of earthworm biomass in the adjacent pairedworm plots. The biomass of earthworms in two ofthe three no-worm plots at Tompkins is not ex-pected to have had significant influence on soilproperties because they comprised a very small pro-portion of the numbers and biomass of worms inadjacent “worm” plots.

Figure 2. Map of earthwormdistribution patterns at ArnotForest. The large map showsdistribution patterns over theentire area of Arnot Forest. Theinset map shows finer-resolu-tion distribution patterns at thethree paired study plots; theplots without earthworms aredesignated “NW” and thosewith earthworms are desig-nated “W.” Dark shading showsareas where the surface soilwas obviously thoroughlymixed by earthworms. Interme-diate shading indicates transi-tion between areas with andwithout worms. Unshaded ar-eas are those where there wereno visible signs of earthwormactivity.

6 P. J. Bohlen and others

The estimated area of Arnot Forest showing signs ofearthworm activity was 29.7%, with 56.6% of theforest showing no signs of earthworm activity and13.7% categorized as transitional between areas withand without worms (Figure 2). For the intensivelystudied areas, the proportions were 47.7%, 46.5%,and 5.8% for worm, no-worm, and transitional areas,respectively. In general, the more interior portions ofArnot Forest had fewer signs of earthworm activitythan the border areas of the forest. Some of thesteeply sloped well-drained areas with drier soils alsolacked earthworms, suggesting that certain locationswere not suitable for earthworm invasion due to un-derlying edaphic or hydrologic factors. Most of thehigh plateau in the border areas of the forest had beenin agriculture in the late 19th and early 20th centuryand now supports postagricultural forest with abun-dant exotic earthworm populations. These distribu-tion patterns support the view that exotic earthwormsinvaded the relatively undisturbed parts of the forestfrom adjacent lands that were formerly in agriculturalland use. The interior of the forest is farthest fromthese purported invasion routes and thus exhibits the

fewest signs of earthworm activity. It is likely thatsome of this area is susceptible to invasion and will beinvaded by earthworms over the next several de-cades.

OVERVIEW OF RESULTS

Our global hypothesis was that earthworm invasionof north temperate forests would have large conse-quences for nutrient retention and uptake in theseecosystems. In this special feature of Ecosystems, wepresent a series of papers describing results fromour comparison of previously invaded and refer-ence forest stands. Our predictions were that earth-worm invasion would:

1. Increase hydrologic losses of C, N, and P andgaseous losses of C and N, resulting in a reduc-tion in soil pools of these elements

2. Change the vertical distribution, production, andfunctioning of fine roots

3. Alter the size and activity of the soil microbialbiomass, resulting in a smaller, more active mi-

Table 1. Population Density of Earthworm Species at Three Study Plots in Arnot Forest and TompkinsFarm in Spring 1999

Species

Arnot Forest Tompkins Farm

Plot 1 Plot 2 Plot 3 Plot 1 Plot 2 Plot 3

Population density number/m2

Aporrectodea tuberculata 1.0 (2.0) — 12.0 (14.2) 5.0 (3.8) — 63.0 (32.6)Dendrobaena rubida — 1.0 (2.0) — — — —Eisenia rosea 7.0 (9.4) — — — — —Lumbricus castaneus — — — — 10.0 (1.46) 16.0 (18.8)Lumbricus rubellus 77.0 (34.5) 106.0 (25.8) 17.0 (21.8) — — —Lumbricus terrestris — — 29.1 (34.8) 51.0 (17.4) 78.0 (44.4) 70.0 (40.3)Octolasion tyrtaeum 95.0 (78.4) 39.0 (21.3) 21.0 (25.6) 120.0 (70.9) 14.0 (16.1) —O. tyrtaeum or E. rosea1 22.0 (44.0) — — — — —L. terrestris or L. rubellus1 — — 22.0 (25.6) — — —All species 202.0 (35.5) 146.0 (43.3) 101.1 (16.5) 196.0 (69.4) 102.0 (35.2) 149.0 (55.5)Biomass g/m2

Aporrectodea tuberculata 0.3 (0.6) — 5.9 (7.2) 2.7 (1.9) — 27.2 (12.0)Dendrobaena rubida — 0.05 (0.1) — — — —Eisenia rosea 1.3 (1.5) — — — — —Lumbricus castaneus — — — — 1.6 (1.5) 1.4 (1.6)Lumbricus rubellus 18.3 (11.9) 35.7 (16.8) 10.6 (12.3) — — —Lumbricus terrestris — — 26.6 (14.7) 38.00 (30.1) 95.30 (44.5) 82.70 (30.7)Octolasion tyrtaeum 17.1 (18.9) 8.1 (4.3) 2.3 (2.8) 16.90 (10.1) 1.8 (2.6) —O. tyrtaeum or E. rosea1 1.0 (2.0) — — — — —L. terrestris or L. rubellus1 — — 1.3 (1.5) — — —All species 38 (28.6) 43.9 (20.9) 46.7 (26.3) 57.6 (38.9) 98.7 (66.8) 111.3 (34.7)

Values are means (SD) for four sampling areas per plot in plots with earthworms. Very few earthworms were encountered in plots designated as “nonworm plots”.1These represent juvenile worms that could not be separated by species.

Earthworm Invasion of Northern Forests 7

crobial community with increased rates of Nmineralization and nitrification

4. Alter the forms and availability of P stored insoils by eliminating forest floor horizons

The most dramatic effect of earthworm invasionwas the loss of the forest floor (Figure 3), whichdramatically altered the location and nature of nu-trient cycling activity in the soil profile. Alterationof the forest floor changed total C and P pools, C:Nratios, the loss and distribution of different soil Pfractions, and the distribution and function of rootsand microbes. Variation in the response to invasionwas related to site characteristics and differences inearthworm species present. The effects of earth-worms on the forest floor were much less marked atthe Tompkins Farm site, which has a history ofcultivation and inherently thin forest floors, than atthe Arnot Forest site, which has no history of cul-tivation and inherently thick forest floors. Differ-ences in the burrowing activities of the dominantearthworm species in different plots were anothersource of variation, especially for the distributionand loss of different fractions of soil P.

The paper by Bohlen and others (2004) describeschanges in the amount and distribution of C and Nin the soil profile of earthworm-invaded and refer-ence stands. At Arnot Forest, the site with inher-ently thick forest floors, earthworms mixed most ofthe forest floor material into the mineral soil. Thenet effect of invasion at the Arnot site was a loss ofapproximately 25% of soil profile C to a depth of 12cm, mostly due to mineralization of forest floor C.At Tompkins Farm, the site with very thin forestfloors due to its agricultural history, the loss of the

forest floor was less marked. There was no enrich-ment of the mineral soil with organic matter and nonet loss of C from the soil profile in areas withearthworms.

Whereas invasion resulted in a significant loss ofC from the soil profile at the Arnot site, it did notresult in a loss of total soil N (Bohlen and others2004). Stable isotope analysis indicated that a sig-nificant percentage of forest floor N was conservedin the mineral soil, resulting in no net change in soilN to a depth of 12 cm at either site. Leaching losses,measured with zero-tension and tension lysimeters,were not strongly affected by invasion at either site.As a result, soil C:N ratios were greatly reduced byearthworms at the Arnot site. Earthworms had noeffect on total soil N or soil C:N ratio at TompkinsFarm.

Earthworm effects on soil P pools appeared tovary with earthworm species distribution amongthe sites and plots (Surez and others 2004). Worm-invaded plots dominated by the deep-burrowingearthworm Lumbricus terrestris had more total P be-tween 0 and 12 cm than their corresponding refer-ence plots. The two worm plots dominated by theepigeic (surface-dwelling) earthworm L. rubellushad significantly less total P than their referenceplots. The worm plots with L. terrestris that hadhigher amounts of total P also had a proportionallyhigher amount of unavailable P fixed in Al or Fehydroxides and of P contained in primary minerals.The increased amount of unavailable P forms sug-gests that the activity of the deep-burrowing L.terrestris mobilized unweathered soil particles fromdeeper layers of the soil and brought them to thesurface, increasing the stocks of total P in the sur-face soil. Conversely, the decrease in total P that weobserved in the plots dominated by the surface-feeding L. rubellus could be due to stimulation ofrates of P cycling in the soil by earthworm activity.This stimulation likely contributed to the signifi-cantly higher concentrations of P in zero-tensionlysimeters that we observed in autumn in earth-worm plots at the Arnot site. Over time, these losseshave likely reduced the total amount of P in theupper soil profile of plots dominated by L. rubellus.Although foliar P was not affected by earthworms ateither site, there was higher P in litterfall in plotswith worms, indicating higher root uptake andmore rapid external cycling of P.

The earthworm-induced redistribution of organicmatter in the soil profile led to correspondingchanges in the amount and distribution of microbialbiomass, with potential consequences for soil mi-crobial functioning in invaded plots (Groffman andothers 2004). Similar to pools of total C and N,

Figure 3. Forest floor mass in paired earthworm-invadedand reference plots at three locations at sites in western(Arnot) and eastern (Tompkins) New York State, USA.Data from Bohlen and others (2004).

8 P. J. Bohlen and others

earthworm invasion greatly reduced pools of micro-bial biomass in the forest floor and increased poolsin the mineral soil. Enrichment of the mineral soilwas much more marked at the Arnot site, whichhad inherently thick forest floors. The increase inmicrobial biomass C and N in the mineral soil at thissite was greater than the decrease in the forest floor,resulting in a net increase in total soil profile mi-crobial biomass in the invaded plots. There was anincrease in respiration in the mineral soil at bothsites, which was consistent with the movement oforganic matter and microbial biomass into the min-eral soil. However, N cycle processes (mineraliza-tion and nitrification) did not increase along withrespiration (Groffman and others 2004). It is likelythat the earthworm-induced input of C into themineral soil created a microbial sink for N, prevent-ing an increase in net mineralization and nitrifica-tion and conserving N in the soil profile. Pools ofmicrobial biomass C and respiration rates werehigher, and rates of N cycle processes were lower, atthe Arnot site than the Tompkins site, consistentwith the higher pools of total C and lower pools oftotal N at Arnot.

Whereas earthworm invasion increased micro-bial respiration, total soil respiration (roots plus mi-crobes) was not increased by invasion, suggestingthat root respiration was reduced by invasion (Fiskand others 2004). This suggestion is supported by asignificant reduction in fine-root biomass in in-vaded plots at the Arnot site. This reduction sug-gests that nutrient uptake efficiency is increased inthe invaded plots, but the mechanism for this in-crease is not clear. Total soil respiration was higherat Arnot Forest than at Tompkins Farm, which isconsistent with the higher levels of total soil C atthe Arnot site.

Our results suggest that exotic earthworm inva-sion is a significant factor that will influence thestructure and function of temperate forest ecosys-tems over the next few decades. There is little doubtthat earthworms are invading new habitats innorthern forest ecosystems and that such invasionconstitutes a potentially important change in thesesystems over wide geographic areas. If earthworminvasion is an important factor influencing patternsof nutrient cycling and loss in northern forests inthe coming decades, then regional evaluations offorests will need to consider the presence or ab-sence of earthworms along with other importantdrivers of those processes, such as pollution, cli-mate, or underlying soil characteristics.

Our focus on exotic, rather than native, earth-worm species stems from the fact that exotic specieshave been implicated in most, if not all, observa-

tions of earthworm invasions of north temperateforests. It is important to note that our observationsof earthworm invasions are not isolated, but aresupported by the observations of other ecologists,who have noted such invasions in different foresttypes in the Northeast, and by reports in the liter-ature of recent earthworm invasions of deciduousforests in other regions of the United States andCanada (Alban and Berry 1994; Scheu and Parkin-son 1994b). Moreover, all of the reported observa-tions implicate exotic species, suggesting that ex-otic, not native, species are most likely to invadenew habitats. Given that our results show that in-vasion effects differ according to earthworm spe-cies, we conclude that there is a clear need forevaluation of the factors that regulate the natureand extent of earthworm invasions and species dis-tributions throughout the north temperate region.

Although our work has focused on forests dom-inated by sugar maple, invasions have been ob-served in a variety of forest types (for example, oak,northern hardwood, hemlock) (Alban and Berry1994; Scheu and Parkinson 1994b; Steinberg andothers 1996). Given that our results show thatearthworm-induced redistribution of organic mat-ter influences microbial and root processes, wewould expect invasion effects to vary with differ-ences in canopy tree species, which can have astrong influence on organic matter quality and nu-trient cycling dynamics in forests (Pastor and others1984; Zak and others 1989; Finzi and others 1998;Lovett and Rueth 1999; Lawrence and others2000).

In addition to canopy species, our results showthat the effects of earthworm invasion vary dramat-ically with site land-use history and initial condi-tions. At sites with inherently thick forest floors (forexample, our Arnot Forest site), invasion results inboth positive and negative effects on soil C and Ndynamics. At sites with more intensive land-usehistory and inherently thin forest floors (for exam-ple, our Tompkins Farm site), invasion effects, bothpositive and negative, are much less marked. Webelieve that it is imperative to consider land-usehistory as a controller of invasion effects and toevaluate the other effects of invasion, such as soilerosion and changes in soil invertebrate communi-ties or spring ephemeral communities, which maybe sensitive to loss of the forest floor.

EXOTIC EARTHWORMS AS COMPONENTS OFCHANGING FORESTS

Shifts in land use and the introduction of exoticspecies both are important components of human-

Earthworm Invasion of Northern Forests 9

induced global change (Houghton 1991; Vitousekand others 1997), and these two factors are oftennot independent of one another. In the northeast-ern United States, much of the landscape has beentransformed from agricultural land to forest withinthe past 150 years (Williams 1990; Foster and oth-ers 1998; Compton and Boone 2000). Past agricul-tural land use, particularly cultivation, can havelasting effects on soil nutrient content, the distribu-tion of nutrients in the soil profile, and nutrienttransformation rates. Cultivation and other agricul-tural activities lead to substantial reductions in totalsoil C, and it may take more than 200 years forrecovery to levels comparable to primary forest(Hamburg 1984; Davidson and Ackerman 1993).

As forested land is logged and cleared for agricul-ture, the introduction and spread of exotic plantand animal species, including earthworms, is likelyto accelerate, making it difficult to separate out themultiple effects of land-use change and introduc-tion of exotic species. Even at the Arnot Forestplots, which have never been cultivated but wereselectively logged in the past, earthworms verylikely spread from adjacent areas on ridge tops thatwere cultivated or pastured and subsequently aban-doned over the past 100 years (Bohlen and others2004). At Tompkins Farm, earthworms were likelyintroduced when the land was cleared for cultiva-tion. The current patchy distribution patterns maybe less a reflection of recent invasion than of theincreasingly limited distribution of earthworms dueto changes in soil conditions after agricultural aban-donment and forest regrowth. Further clarificationof such dynamics will require broader-scale inves-tigations that include multiple sites with knownland-use histories.

Northern forest ecosystems are being subjected tomultiple environmental stresses, including contin-ued atmospheric deposition and potentially rapidenvironmental change. Our results indicate that theeffect of these changes on forest nutrient cyclesneeds to be interpreted in light of potential changesin soil biota—in particular, the invasion of theseforests by exotic earthworms. Recent evidence sug-gests that climatic changes may be contributing tolonger growing seasons and increases in productiv-ity and vegetation indices at northern latitudes(Keyser and others 2000; Papadopol 2000; Zhouand others 2001). Significant shifts in the distribu-tion of species and communities in the forest eco-systems of North America are likely to occur inresponse to changing climate and land-use patterns(Hansen and Dale 2001; Hansen and others 2001;Iverson and Prasad 2001). Such changes in thebiodiversity of these forest ecosystems, including

the continued spread and introduction of exoticspecies, are likely to result in strong biotic feedbacksto nutrient dynamics and ecological processes. It isstill uncertain how climate warming will affect soilC and N storage and dynamics, but this issue iscentral to understanding the biotic feedbacks ofterrestrial ecosystems to global climate (Davidson1995; Schlesinger 1995). Changing climatic condi-tions may facilitate the northward spread of differ-ent earthworm species by increasing their rates ofsurvival, fecundity, or dispersal. Such an acceler-ated expansion of earthworm populations, due tochanging climate, altered land use, or other humanactivities, could increase the potential for soil C loss,significantly change the distribution and quality ofsoil organic matter, and alter soil C, N, and P cyclesin some forest ecosystems.

ACKNOWLEDGEMENTS

This research was supported by a grant from theNational Science Foundation (DEB-9726869). Wethank Isabella Fiorentino, Emilie Stander, AbrahamParker, Ann Gorham, and Alan Lorefice for helpwith fieldwork and laboratory and data analysis.

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