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Non-Native Invasive Earthworms as Agents of Change in Northern Temperate Forests Author(s): Patrick J. Bohlen, Stefan Scheu, Cindy M. Hale, Mary Ann McLean, Sonja Migge, Peter M. Groffman, Dennis Parkinson Source: Frontiers in Ecology and the Environment, Vol. 2, No. 8 (Oct., 2004), pp. 427-435 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/3868431 Accessed: 11/11/2008 10:53 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. 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Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Frontiers in Ecology and the Environment. http://www.jstor.org REVIEWS REVIEWS REVIEWS Non-native of change invasive in earthworms northern temperate as agents forests Patrick J Bohlen1, Stefan Scheu2, Cindy M Hale3, Mary Ann McLean4, Sonja Migge5, Peter M Groffman6, and Dennis Parkinson7 I Exotic earthworms from Europe and Asia are invading many northern forests in North America that currently lack native earthworms, providing an opportunity to assess the role of this important group of invertebrates in forest ecosystems. Research on earthworm invasions has focused on changes in soil structure and carbon (C) and nitrogen (N) cycling that occur following invasion. These changes include the mixing of organic and mineral soil horizons, decreases in soil C storage, and equivocal effects on N cycling. Less well studied are changes in the soil foodwebs that accompany earthworm invasion. Soils of north temperate forests harbor a tremendous diversity of microorganisms and invertebrates, whose distribution and abundance can be substantially altered by earthworm invasion. Furthermore, invasive earthworms can affect understory plant communities, raising concerns over the loss of rare native herbs in some areas. The ecological consequences of earthworm invasion are mediated through physical, geochemical, and biological effects. These effects vary with different earthworm species, as well as with the characteristics of the site being invaded. Earthworm invasions may have important interactions with other rapid changes predicted for northern forests in the coming decades, including climate and land-use change, increased nutrient deposition, and other biological invasions. Front Ecol Environ 2004; 2(8): 427-435 forests are experiencing multiple stressesand Northern changes, including nutrient deposition and acidificadisease and pest outbreaks,changing climate, and biotion, invasions (Aber et al. 2001). Biological invasions in logical northern forests threaten to alter ecosystem structureand function, especially when they change the habitat of other species, alter the availability or transformationrates of key resources, or compete with or replace native species In a nutshell: * Many northerntemperateforestsin the US have had no naturalearthwormpopulationssince the last glacialperiod,due to slow northwardexpansionof native species * Exotic earthwormspecies from Europeand Asia are invading manyof these forests,substantiallyalteringforestsoils * These invasionscan alternutrientstorageand availability,and greatlyaffect populationsand communitiesof other flora and faunathat inhabitforestsoils * Invasions by earthwormsare likely to increase in northern forests with increasedhuman activity and changing climate; the consequences should be considered along with other importantchangestakingplace in these ecosystems 'Archbold Biological Station, Lake Placid, FL (pbohlen@ Universitdt archbold-station.org); 2Department of Biology,Technische 3The Natural Resources Research Darmstadt, Darmstadt, Germany; 4Indiana State Institute,Universityof Minnesota,Duluth,MN; Terre Haute,IN; 5Department University, of Biology,University of Gottingen,Gottingen,Germany;6Insttuteof EcosystemStudies, MillbrookNY; 7Department of Biology,Universityof Calgary, Calgary,Canada. ? The Ecological EcologicalSociety Society of America C (Vitousek 1990). Understandably,much of the focus on exotic species invasions in forestsand other ecosystemshas been on abovegroundinvaders,which are the most apparent. However, belowgroundinvasions may be equally widespread and may become better known as more ecologists begin to recognize the importanceof links between aboveground and belowground communities (Scheu 2001; Wardle 2002). Invasion of northern forestsby exotic earthworms,for example, is receiving increasingattention. Earthwormsare the best known of the large soil fauna, but many northern forests in North America lacked earthworm populations prior to European settlement, probably because of slow northward expansion of native earthworm populations following the last glacial period (James 1995). Foreign earthworm species, mainly of European and Asian origin, are currently invading these forests over a wide geographic area (eg Alban and Berry 1994; Scheu and Parkinson 1994; Bohlen et al. 2004a). The earthworm species involved belong to a group that have been termed the "peregrine"species, representing a small portion of overall earthworm diversity, and are characterized by their ability to colonize new habitats, spread rapidly, and tolerate a wide range of ecosystems and environmental conditions (James and Hendrix 2004). The introduction of these species into new habitats is facilitated by human activity, such as the construction of logging roads, direct releases of unused fishing bait by anglers, and the relocation of fill or horticultural materials (Hendrix and Bohlen 2002). Earthworm invasions of northern forests can lead to www.frontiersinecology.org www.frontiersinecology.org I Invasive earthwormsin temperateforests I rapid and dramatic changes in the soil environment (Langmaid 1964; Alban and Berry 1994) due to the important role of earthworms in modifying soil structure, redistributing organic matter, and altering the habitat of other organisms living in or on the soil (Neilson and Hole 1964). This key role of earthworms in forest humus formation has long been recognized and is captured in the historical mull, moder, and mor terminology used to describe forest soils (Parkinson et al. 2004). Several excellent recent reviews are available on the ecology of earthworms, their critical role in soil genesis, their effects on nutrient cycling and organic matter breakdown, and their interactions with soil microbial communities (Lavelle et al. 1999; Edwards 2004). The goal of this paper is not to review this extensive literature, but rather to point out that earthworm invasions in northern forests provide an opportunity to examine the generality of current concepts in earthworm ecology and to compare and contrast the importance of different functional groups of organisms in invasion biology. Because earthworms modify the surface soil, which is where the primary interactions between aboveground and belowground communities are mediated, these invasions have important consequences for the soil foodweb, nutrient cycling, and plant communities. The accompanying disturbances may be an important aspect of the current and future environmental change in these forests. * Earthworminvasions and nutrientcycling Much of the research on earthworm invasions has focused on the consequences for nutrient cycling and soil microbial processes (eg Scheu and Parkinson 1994; Bohlen et al. 2004b; Groffman et al. 2004). Earthwormsshift the soil system from a slower cycling, fungal-dominated system to a faster cycling, bacterial-dominated system, or at least one that is less fungus dominated (Wardle 2002). This is Bohlen et al. PJBohien accomplished through the redistribution and transformation of soil organic matter as earthworms consume organic-rich forest floor material and incorporate it into underlying mineral soil (Figure 1). The degree of mixing of soil layers depends upon the life history traits of particular earthworm species, which are often broadly categorized as belonging to one of three main ecological groups: epigeic, endogeic, and anecic (Edwardsand Bohlen 1996). Epigeic species reside mainly in the upper organic layer and may cause limited mixing of mineral and organic soil layers.Endogeic species reside in the mineral or mixed soil layers and often enhance mixing of organic and mineral soil layers. Anecic species (including Lumbricusterrestris, the common nightcrawler) form nearly vertical permanent burrowsup to 1-2 m deep. These species incorporate litter into the soil and bring mineral soil from different depths to the surface, resulting in soil mixing that is very different from the mixing caused by epigeic or endogeic species (Figures 1 and 2). Not all species fall neatly into these standard categories, but classification is useful for differentiating major ecological groups and their effects. The physical transformationof the soil is the most obvious sign of earthworminvasion in northern forests. How these physical changes and the associated redistribution of organic matter influence ecosystem level processes such as total C storage, N transformationrates, and loss of nutrients via hydrologic and gaseous pathways, and how these change over time, is not well understood. A shift towards a faster cycling system implies that earthworm invasion could result in a net loss of C from the soil. Northern forests are important global C sinks, but environmental changes may turn them into C sources (McKane et al. 1997; Hobbie et al. 2002). Earthworm invasion could enhance increased C flux from northern forests due to global warming, especially as the ranges of different ecological groups of earthworms expand into more of these forests. In fact, most studies have docu- Figure 1. Effectsof invasiveearthwormson forestsoilsin northernMinnesota.(a) Understoryvegetationand herblayerin areas soil layerwithcoverof leaflitter.(b) withoutearthworms.Note theabundanceof treeseedlingsandnativeherbsand theundisturbed Understoryvegetationand soil surfaceat a site invadedby earthworms.Note thelackof herblayer,exposedsoil surfacewithreduced litterlayerandabundantearthworm casts,andexposedrootsof canopytreesdue to disappearance of forestfloor. www.frontiersinecology.org www.frontiersinecology.org EcologicalSociety of America ?? The The EcologicalSociety of America P1 PJBohlen et al. mented an increase in soil C loss following earthworm invasion. Carbon loss of around 600 kg per hectare per year for a period of 14 years was reported for mixed hardwood forests in Minnesota (Alban and Berry1994), and of 28% of total surface soil C for sugar maple (Acer saccharum) forests in the northeastern US (Bohlen et al. 2004b). Such losses occur because recalcitrant C pools that accumulate at the soil surfacein the absence of earthwormsare exposed to greater mineralization rates after earthworms invade. The increased mineralization is partly a result of earthworm respiration, but is mostly due to the stimulation of microbial activity in earthworm guts and casts. Mineralization is also increased by the secretion of labile C compounds in mucus and subsequent alteration of soil structure (Edwardsand Bohlen 1996). In the long term, however, earthworm activity may contribute to stabilization of soil C in earthworm casts and other stable aggregates formed by earthworm activity (Scheu and Wolters 1991; Tiunov and Scheu 2000). The effects of earthworm invasion on N cycling and retention are more complex and less conclusive than the effects on C transformations.Nitrogen is both a limiting nutrient and an atmospheric pollutant, so the effects of earthworms on N cycling potentially influence nutrient uptake and the fate of atmospheric N deposited in forest ecosystems. Earthwormshave been shown to increase the N mineralization and leaching of N from forest soils in both lab and microcosm studies (Haimi and Huhta 1990; Scheu and Parkinson 1994; Burtelow et al. 1998), indicating that earthworm invasions have the potential to accelerate rates of N transformation. Earthworm activity has been shown to increase denitrification rates in some instances, though not in others, and the question of whether earthworm invasion influences overall gaseous N flux from forest soils remains unanswered (Burtelow et al. 1998; Bohlen et al. 2004b). It is also unclear whether earthworm invasion substantially alters N retention in those systems. They did not lead to large increases in N leaching from surface soil in undisturbed forest plots in New York(Bohlen et al. 2004b). Analysis of soil C and N content and stable isotope signatures of invaded forest sites in New Yorksuggested that total soil N remained unchanged following invasion, despite the fact that soil C storage decreased substantially (Bohlen et al. 2004b). An increase in total microbial biomass, which may act as a strong immobilization sink for available N in C-rich soils (Groffman et al. 2004), is one possible mechanism for N retention following earthworm invasion. This is an interesting finding because some studies have reported a decrease in microbial biomass in response to earthworm activity (Blair et al. 1997; Hendrix et al. 1998; Wolters and Joergensen 1992). However, most previous studies that reported a decrease in microbial biomass with earthworms involved agricultural or mixed soils, not organic-rich forest soils where earthworms can stimulate microbial biomass by mixing soil layers together (Scheu and Parkinson 1994; Saetre 1998). In the New ?C The The Ecological America of America EcologicalSociety Societyof Invasiveearthwormsin temperateforests Figure 2. Earthwormsrepresentativeof differentecological groups. (a) Epigeicspecies, such as Dendrodrilus rubidus, inhabitorganic-richsurfacelayersand feed mainlyon surface organic matter. (b) Endogeic species, such as Octolasion tyrtaeum, consumemoremineralsoil thanepigeicspecies,and mix mineraland organicsoil layerstogether.(c) Anecicspecies, suchas Lumbricusterrestris,livein deepverticalburrows,feed litterinto thesoilas well mainlyon surfacelitter,andincorporate as transporting mineralsoil to thesurfacefromdeepersoillayers. (Note that only the anteriorend of L terrestrisis shownhere; theposteriorendremainsin its burrow). www.frontiersinecology.org www.frontiersinecology.org PJBohien Bohlen et al. Invasive earthwormsin temperate temperateforests I Yorkstudy,the increasein microbialbiomasswas attributed to a more favorableenvironment that increasedthe "carrying capacity" of the mixed surface soil relative to undisturbed forest floor. Understanding or predicting the effects of earthworminvasion on N cycling in forest soils depends on the quantity and quality of soil organic matter, because of the tight coupling of soil C and N cycling. Earthworms may increaseN flux more in systemsfertilizedwith N, such as agricultural or pasture systems (Knight et al. 1992; Dominguezet al. in press);earthworminvasion might therefore be expected to increase N flux more in forests with high levels of N deposition than in more N-limited systems, though this remainsto be investigated. Earthworm invasion also affects phosphorus (P) cycling in soil, which is strongly influenced by physical and chemical modifications. Trees in areas with an intact forest floor concentrate a large proportion of their fine roots in this layer, where up to 80% of their annual P requirement is met by the tight linking of organic P mineralization and uptake (Wood et al. 1984; Yanai 1992). By eliminating the forest floor and mixing it with the underlying soil, earthworms can greatly alter P cycling by increasing P fixation by soil minerals and by altering the mineralization of organic P. For example, a study of sugar maple stands in Quebec showed that all stands that had forest floors mixed with mineral soil had lower concentrations of available P than did stands with intact forest floors, undisturbed by earthworm activity (Pare and Bemier 1989 a, b). A comparison of plots with and without earthworms in New York suggested that invasive earthworms influenced soil P cycling, but that the effects depended on the species composition of the earthworm community, possibly because various earthworm species differentially affect the degree of mixing of soil layers and the redistribution of organic and mineral components within the soil profile (Suarez et al. 2004). The effect of earthworms on P cycling is largely dependent on regional soil mineralogy, the degree of mixing of soil layers, and the timeframe of the invasion. An initial increase in organic P mineralization in the early stages of invasion may be followed by a decrease in available P as soil minerals fix more P. Dendrobaenaoctaedrainto pine forest soil in Alberta suggest that in the long term, fungal community diversity and richness decreased and dominance among fungi increased, apparently due to the disruption of fungal hyphae, decreased resource availability, and reduced spatial heterogeneity as the organic layers became homogenized (McLean and Parkinson 2000a). Competition among fungi was reduced soon after invasion, possibly through the addition of nutrients or as a result of disturbances due to burrowing and deposition of casts into the organic layers (McLean and Parkinson 1998b). Given the differences between epigeic, endogeic, and anecic earthwormsin terms of feeding behavior and effects on the soil profile, one might expect the response of soil fungi to earthworm invasion to vary in accordance with the ecological groupof the invading species. In fact, results from a laboratorymesocosm experiment suggest that some species, including fast-growingspecies of Trichoderma,are favored by the presence of the epigeic D octaedra,but are inhibited by the presence of anecic and/or endogeic earthworms, indicating that epigeic earthworms favor fungal species that tolerate moderate disturbances. Other fungi, including Mortierella sp (Zygomycetes), uniformly decreased in the presence of epigeic, anecic, or endogeic earthworms, reflecting their inability to tolerate hyphal disruption;this is due to the lack of septa to prevent cell content leakage. With so little data available, conclusions about the effects of earthwormson microfungalcommunities must remain preliminary. It is probable that earthworm invasions not only affect saprophytic but also mycorrhizal fungi, but this has not been well studied. Results from a laboratorystudy on the impacts of earthworms on mycorrhizal fungi are congruent with observations on saprophytic microfungi. The presence of earthworms of different ecological groups decreased colonization rates and abundance of arbuscular mycorrhizae of sugar maple, most likely due to physical disruption of fungal mycelia (Lawrence et al. 2003). Changes in the abundance and functioning of arbuscular mycorrhizal fungi probably contributed to alterations in forest herb communities. Soil invertebratecommunity responses * Alterationof the soil foodweb Soil microbial community responses Organic layers in the soil provide microhabitats and resources that support an abundant and diverse soil community. The profound changes in the soil organic layers resulting from earthworm invasion greatly alter microhabitats and resources for microorganisms and invertebrates (Figure 3). However, with the exception of studies in forests in Alberta, Canada, and in a maple forest in New York, data on the effects of earthworm invasions on soil microbial communities in forests are limited. Studies on the response of soil fungi to the invasion of www.frontiersinecology.org www.frontiersinecology.org Earthworm invasions can rapidly alter soil structure, humus forms, and plant communities, and some of these changes can occur in as short a period as 2 to 5 years (Langmaid 1964). However, the influence of these ecosystem engineers on other soil biota, eg microarthropods (mites, collembolans), enchytraeids (potworms), or nematodes is poorly understood, especially with repect to changes that occur following earthworm invasions in forest ecosystems. Soil-inhabiting vertebrates and their responses to invading earthworms as new food resources have only recently been examined in more detail (Maerz et al. in press), although the importance of earthwormsas a food source for a wide variety of vertebrates is well of America The EcologicalSociety of ?? The EcologicalSociety America PJ Bohlen et al. at. Invasiveearthwormsin temperateforests I Figure 3. The diversityof soil mixingeffectsof differentecologicalgroupsof earthwormsin boxes containingreconstructed soil layersfrom an aspenforestin southwestAlberta,Canada. (a) Boxeswithno earthworms;(b) boxescontainingindividuals of theepigeicearthwormspecies,D octaedra, whichhavemixed the organiclayerinto the mineralsoil; and (c) boxescontaining individualsof the endogeicspecies, 0 tyrtaeum, which have thoroughlymixed the mineraland organiclayerstogether.For moredetailssee Scheu& Parkinson(1994). established (Edwardsand Bohlen 1996). The rapidly spreading earthworm D octaedra mainly inhabits the forest floor, which is also the major habitat for soil-inhabiting microarthropods.Studies in a pine forest in Alberta confirmed the expected, positive influence of earthwormactivity on soil invertebrates (Wickenbrock and Heisler 1997; Lorangeret al. 1998), but only either in the short term or in unfavorable habitats. A high biomass of D octaedraresulted in increased oribatid mite diversity; in a laboratory experiment, intermediate levels of earthworm activity tended to increase microarthropod abundance after 3 months, probably due to an increase in microhabitats and microbial food resources (McLean and Parkinson 1998a). Similarly, the dry and unfavourable pine litter (L-layer) was modified by earthworm activity in a way that resulted in increased oribatid mite species richness and diversity (McLean and Parkinson 2000b). However, high earthworm biomass and activity in the longer term and in the lower organic layers, the main habitats of microarthropods in climates with hot and dry summers and cold winters, resulted in strong decreases in diversity and abundance. These declines can be attributed to the restructuringof the organic layer into earthworm casts and associated mechanical disturbance, as well as the competition for microbial food resources. More dramatic decreases in microarthropod diversity and abundance were observed in aspen forest soil in Alberta when L terrestris, an anecic species, and 0 tyrtaeum and Aporrectodeacaliginosa, both endogeic species, invaded soils previously devoid of earthworms. These large earthworm species mix organic material and ? The Ecological EcologicalSociety Society of America mineralsoil in much greaterquantitiesthan D octaedra,and therefore compete vigorously with microarthropods for microbial and organic food. They alter habitat and food resourcesmore stronglyand create mechanical disturbances which, as demonstratedin a 1-year laboratoryexperiment, may result in lower microarthropodabundances than are found in agricultural soils under conventional tillage (Migge 2001). The same processesoccur in the field; these will be slower in dry continental climates such as in the forestsof southern Alberta, but are likely to be much faster in the milder climates of the eastern forests.To date, there are no comparabledata available from other regions, and data on enchytreaids,nematodes, and macroarthropodsare lacking. Soil inhabiting vertebrates Recent studies on the foraging behavior of salamanders (Plethodonsp) suggest that introduced earthworms may play an important role in salamander diets, especially in lowland forests and during rainy seasons (Maerz et al. in press). Earthworms apparently increase the fecundity of adult salamanders by providing a high protein food source, but decrease the survival rates of young salamanders, presumably by reducing populations of smaller www.frontiersinecology.org www.frontiersinecology.org Invasive earthwormsin temperate temperateforests I PJBohien Bohlen et al. diverse community of herbs was present even in some areas that supported a high biomass of earthworm species other than L rubellus.However, where the L rubellusbiomass reached its maximum, the herbaceous plant community was dominated by Carex pennsylvanicaand Arisaema triphyllum,with rare occurrences of other native plant species. The disappearance of established populations of the rare goblin fern (Botrychiummormo) were also associated with the invasion of this earthworm (Gundale 2002). Earthworminvasion of hardwood forests can have both direct and indirect effects on the understory plant com* Plant community responses to earthworm munity. Direct mortality of herbaceous plants and small invasions tree seedlings rooted in the forest floor occurs when The abundance and diversity of native plant species and earthworms eat the forest floor out from under them tree seedlings can decline steeply following earthworm (James and Cunningham 1989; Hale 2004). Earthworms invasion (Figure 1). Some hardwood forest stands in may reduce plant regeneration by ingesting and burying northern Minnesota that had lush and diverse understory seeds and by reducing the shelter offered by the forest plant communities only 40 years ago now have only one floor layer, thus exposing seeds and seedlings to desiccaspecies of native herb and virtually no tree seedlings tion and predation by insects, small mammals, and other remaining after earthworm invasion, although other fac- organisms (Leck 1989; Kostel-Hughes 1995). After initial tors may also have contributed to these changes (Hale earthworm invasion, smaller understory plant popula2004). Concerns have therefore been raised about the tions become more vulnerable to the impacts of deer grazpotential for widespread loss of native forest plant species ing, which can lead to local extirpation (Augustine et al. and the stability of their communities in hardwood forest 1998). Changes in soil nutrient dynamics, including increases in N and P loss due to leaching and decreased ecosystems following earthworm invasion. Earthworm invasions in sugar maple-dominated forests availability, may also affect the growth and composition in northern Minnesota were first noted 15 to 20 years ago of herbaceous plant communities following earthworm invasion (Bohlen et al. 2004b; Hale 2004). (Mortensen and Mortensen 1998). Many stands contained discrete, visible leading edges of invasion where Individual responses of plant species to earthworm forest floor thickness decreased from 10 cm to zero in dis- invasion will be important in determining the trajectory tances as short as 75 meters. Associated with the loss of of compositional changes in hardwood forests following the forest floor across the leading edges were rapid earthworm invasion (Scheu 2003; Hale 2004). In a increases in earthworm biomass, the successive appear- greenhouse experiment, the addition of earthworms ance of up to eight earthworm species, and substantial increased plant mortality and altered root-to-shoot ratios, changes in soil physical and chemical properties (Hale et but the magnitude and direction of those changes al. in press). When not associated with some underlying depended on both the plant species and the particular gradient in initial soil conditions, this leading edge of species of introduced earthworm. In field studies, earthworm invasion provides an opportunity to assess the Arisaematriphyllum(Jack in the pulpit) and Allium tricocrelationships of earthworm biomass and species assem- cum (wild leeks) were both positively associated with blages to changes in the understory plant community, increasing earthworm biomass (Hale 2004). Changes in while controlling for site-specific factors that often the soil fungal community following earthworm invasion thwart field-based comparative studies. (Johnson et al. 1992; McLean and Parkinson 2000a; In study plots in northern Minnesota, the abundance Lawrence et al. 2003), may have consequences for native and diversity of the herbaceous plant species and tree understoryplants, the vast majority of which are strongly seedlings across leading edges of earthworm invasion mycorrhizal in northern forests (Brundrett and Kendrick decreased with increasing total earthworm biomass, but 1988; Baskin and Baskin 1998). The dominance of earththe magnitude of change depended on the species assem- worm-invaded sites by non-mycorrhizal herbs such as C pennsylvanicain Minnesota and Allia petioloata(garlic blage of the earthworm community (Hale 2004). Herbaceous plant communities were more strongly mustard) throughout the eastern US suggests that earthaffected when the epi-endogeic species Lumbricusrubellus worms may enhance the competitive success of non-mycwas present. A diverse community of herbaceous plants, orrhizal herb species at the expense of mycorrhizal ones including species that are often used as indicators of rich (Francis and Read 1994; Brussaard1999; Hale 2004). In addition to effects on understory herbs, earthworm sugar maple-dominated hardwood forests in the Great Lakes region (such as Caulophyllumthalictroides,Uvularia invasion may influence overstory trees by influencing grandiflora, Trillium spp, Osmorhiza claytonii, Asarum root distribution and function (Fisk et al. 2004). Invading canadensis,and Polygonatumpubescens;Kotar 2002), could earthworms can lower the soil surface by removing the be found in areas where L rubelluswas not present. This forest floor, thus leaving tree roots exposed and changing invertebrate food sources, or by altering the habitat in other ways. Further investigations are needed to understand how this influences salamanderpopulation dynamics and what impacts the invading earthworms will have on other predators, such as birds or small mammals. The changes observed in decomposer and plant communities, as well as vertebrate foraging strategies, imply that belowground invasions can also dramatically alter the aboveground food web. www.frontiersinecology.org www.frontiersinecology.org EcologicalSociety of America ?? The The EcologicalSociety of America P1Bohlen et al. PJ their distribution in the soil (Figure lb). Forest sites in New York overrun by earthworms had fewer fine roots than sites without earthworms, while the higher N concentration in roots in invaded sites indicated that earthworms altered allocation and possibly also functioning of fine roots and the efficiency of N uptake. The long-term consequences of such changes for tree nutrition, seedling establishment, and seed survival are unknown. Invasive earthwormsin temperate temperateforests Dispersal * source population * naturalexpansion * humanactivity * streams,rivers Resource quantity * plantprcoductivity * soil orgaanicmatter `11 a Physicaleffects burrowingand casting ? litterremoval ? soil aggregates porosity hydrology ? erosion Resource quality * vegetationtype * litterC:Nratio * tannins,polyphenotics Soil factors * moisturehydrology * texture,sand/silt/clay * acidity,base cations b` b Geochemicaleffects * mixingsoil layers * adsorption/desorption< * mineralweathering * change in minerology - Biologicaleffects ? change in soil habitat * faster nutrientcycling less fungally-dominated ? fewermycorrhizae ? change in rootingzone ? alteredseedbed * Conclusions communities Ecosystem properties Ecological Earthworm invasion of northern *C loss (shortterm) * plantinvasions * C stabilization (long term) < * loss of native herbs forests is influenced by many fac* N retention? ? soil invertebratecommunityshifts tors and has multiple ecological * P availability? * microbialcommunityshifts *Treenutrition? effects mediated through the physical, geochemical, and biological changes that occur follow- Figure 4. This conceptualmodel illustrateshow the influenceof earthwormson the ing invasion (Figure 4). The eco- biological,chemical,and physicalcharacteristics of the soil ecosysteminteractto determine of these the net earthworm invasion on logical consequences influenceof ecosystemprocessesand ecologicalcommunities invasions depend upon which (C = carbon,N = nitrogen,and P = phosphorus).See textfor explanation.(Modifiedfrom species or species complexes Bohlenet al. 2004a). invade and the characteristics of the site being invaded. Enough evidence exists to gener- sent an inadequate food source for earthwormswith rapid alize about some of these consequences, such as carbon growth rates. The quality of soil organic matter or plant loss and gross changes in microbial communities. Yet, litter, including such properties as the C:N ratio, or tandespite the vast literature on earthworm ecology, too lit- nin (polyphenol) content, is known to influence earthtle evidence is available to make general predictions worm feeding, growth, and fecundity. Forests with large about their effects on nutrient availability or loss, soil amounts of soil organic matter but poor food quality may erosion, and native microbial, plant, or invertebrate com- prevent establishment or limit growth and expansion of munities. Examining the response of the soil ecosystem to earthworm populations (Edwards and Bohlen 1996). earthworm invasion may help clarify current concepts in Finally, soil factors, such as texture, acidity, richness of earthworm ecology. It may even lead to new concepts base cations, and moisture, influence the establishment that will supplant long-held views about the role of earth- and size of earthworm populations. These various factors worms in forest ecosystems. may affect different species in dissimilar ways, so that Most research on earthworm invasions has focused on conditions that prevent colonization by one species may the consequences of invasion at particular forest sites, not prevent the establishment of another. with much less emphasis on the mechanisms of invasion The potential widespread loss of native understory and the broaderlandscape- and regional-scale factors that plant species that could result from expanding earthworm contribute to, or limit, invasion. These factors include invasion of northern hardwood forests raises the question agents of dispersal, the quantity and quality of resources of whether strategies could be developed to prevent furat invaded sites, the nature of the overstory vegetation, ther invasions or provide for restoration following invaand soil characteristics (Figure 4). Human activity has sion (Proulx 2003). Although local control of invasions been implicated as an important cause of earthworm dis- may be possible in some situations, the magnitude and persal, including anglers dumping unused fishing bait, regional scale of invasion by non-native earthworms suglogging trucks carrying mud that contains earthworms or gest that in the next few decades many northern tempercocoons into newly logged areas, and the spreading of ate forests that currently lack earthwormswill be invaded horticultural materials such as mulch or compost in gar- to some degree, rendering regional control strategies dens or along trails. Factors that affect either the quantity impractical. Reducing agents of dispersal by, for example, or quality of soil organic matter are important because educating fishermen about the effects of earthworm organic matter is the primary resource base for invading introductions, limiting the spreadof horticultural materiearthworms. Low quantities of organic matter may repre- als containing earthworms, or limiting new road con. ? The Ecological EcologicalSociety Society of America www.froneiersinecology.org www.frontiersinecology.org I Invasive earthworms in temperate Invasive earthworms forests temperateforests I PJ Bohlen et al. al. PJBohien pools in response to earthwormpopulation manipulations in agroecosystemswith differentN sources.Soil Biol Biochem29: 361-67. Bohlen PJ,GroffmanPM, FaheyTJ, et al. 2004a. Ecosystemconsequences of exotic earthworm invasion of north temperate forests.Ecosystems7: 1-12. Bohlen PJ, Groffman PM, Fahey TJ, et al. 2004b. Influence of earthworminvasion on redistributionand retention of soil carbon and nitrogen in northern temperateforests. Ecosystems7: 13-27. BrundrettMC and KendrickB. 1988. The mycorrhizalstatus, root anatomyand phenology of plants in a sugarmaple forest.CanJ Botany66: 1153-73. BrussaardL. 1999. On the mechanisms of interactions between earthwormsand plants. Pedobiologia 43: 880-85. Burtelow AE, Bohlen PJ, and Groffman PM. 1998. Influence of exotic earthworm invasion on soil organic matter, microbial biomass and denitrification potential in forest soils of the northeasternUnited States. ApplSoilEcol9: 197-202. DominguezJ, Bohlen PJ, and ParmeleeRW.Effectsof earthworms on movement of nitrogen into groundwaterin agroecosystems. Ecosystems.In press. EdwardsCA (Ed). 2004. Earthwormecology, 2nd edn. Boca Raton: CRC Press. EdwardsCA and Bohlen PJ. 1996. Biology and ecology of earthworms,3rd ed. London, UK: Chapmanand Hall. FiskMC, FaheyTJ, GroffmanPM, et al. 2004. Earthworminvasion, fine root distributionand soil respirationin hardwoodforests. Ecosystems7: 55-62. Francis R and Read DJ. 1994. The contributions of mycorrhizal fungi to the determinationof plant communitystructure.Plant Soil 159: 11-25. GroffmanPM, Bohlen PJ, Fisk MC, et al. 2004. Exotic earthworm invasion and microbial biomass in temperate forest soils. Ecosystems7: 45-54. Gundale MJ. 2002. The influence of exotic earthwormson soil organic horizon and the rare fern Botrychiummormo.Conserv Biol 16: 1555-73. Haimi J and Huhta V. 1990. Effectsof earthwormson decomposition processesin rawhumusforest soil: a microcosmstudy.Biol * Acknowledgements FertSoils 10: 178-183. Some of the research reported here was supported by Hale CM. 2004. Ecologicalconsequencesof exotic invaders:interactions involving Europeanearthwormsand native plant comgrants from the National Science Foundation (DEBmunities in hardwoodforests (PhD dissertation).St Paul, MN: 9726869 and DEB-0075236). The ideas presented in this University of Minnesota. paper benefited from discussions at a workshop on earth- Hale CM, Frelich LE, and Reich PB. Exotic Europeanearthworm invasion dynamicsin northernhardwoodforestsof Minnesota, worm invasions sponsored by the National Science USA. EcolAppl.In press. Foundation and the Institute of Ecology at the University Hansen AJ, Neilson RP, Dale VH, et al. 2001. Global change in of Georgia and organizedby Paul Hendrix. We thank Tim forests: responses of species, communities, and biomes. Fahey, Melany Fisk, Lee Frelich, Derek Pelletier, Peter Bioscience51: 765-79. Reich, and Esteban Suarez for their contributions to the Hendrix PF and Bohlen PJ. 2002. Exotic earthworminvasions in North America: ecological and policy implications. Bioscience work presented here. 52: 801-11. Hendrix PF, Peterson AC, Beare MH, and Coleman DC. 1998. * References Long-termeffectsof earthwormson microbialbiomassnitrogen AberJD,NeilsonRP,McNultyS, et al. 2001.Forestprocessesand in coarseand fine texturedsoils. ApplSoilEcol 9: 375-80. globalenvironmental change;predictingthe effectsof individ- Hobbie SE, NadelhofferKJ,and HogbergP. 2002. A synthesis:the ualandmultiplestressors. 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Invasion of exotic earthworms struction into forest tracts, may help slow dispersal of exotic earthworm species. The decline in some understory plant species following invasion is due to the cooccurrence of other factors, such as high deer densities (Augustine et al. 1998). In this situation, control of earthworms, even if it were possible, may not be sufficient to enhance recolonization of understory herbs without efforts to control deer densities. Northern temperate forests are facing rapid environmental transformations that include climate change, species invasion, changes in land-use patterns, and continued atmospheric deposition. Earthworminvasion is an additional factor that may interact with, and contribute to, these changes. Positive or negative interactions may occur, such as an acceleration of C loss (climate warming and earthworm invasion), increased gaseous or hydrologic flux of N (atmospheric deposition and earthworm invasion), or nutrient stress (drought or pollution and earthworm invasion). The increasing length of growing seasons and enhanced productivity currently occurring at northern latitudes (Papadopol 2000; Zhou et al. 2001) are likely to contribute to a more rapid northward expansion of earthworm populations and introductions of exotic species formerly limited by colder temperatures. Earthworminvasions are likely to interact with other biological invasions occurring concurrently or predicted to occur in forest ecosystems (Hansen et al. 2001). 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