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Non-native invasive earthworms as agents
of change in northern temperate forests
Patrick J Bohlen1, Stefan Scheu2, Cindy M Hale3, Mary Ann McLean4, Sonja Migge5, Peter M Groffman6, and
Dennis Parkinson7
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
N
orthern forests are experiencing multiple stresses and
changes, including nutrient deposition and acidification, disease and pest outbreaks, changing climate, and biological invasions (Aber et al. 2001). Biological invasions in
northern forests threaten to alter ecosystem structure and
function, especially when they change the habitat of other
species, alter the availability or transformation rates of key
resources, or compete with or replace native species
In a nutshell:
• Many northern temperate forests in the US have had no natural earthworm populations since the last glacial period, due to
slow northward expansion of native species
• Exotic earthworm species from Europe and Asia are invading
many of these forests, substantially altering forest soils
• These invasions can alter nutrient storage and availability, and
greatly affect populations and communities of other flora and
fauna that inhabit forest soils
• Invasions by earthworms are likely to increase in northern
forests with increased human activity and changing climate;
the consequences should be considered along with other
important changes taking place in these ecosystems
1
Archbold Biological Station, Lake Placid, FL (pbohlen@
archbold-station.org); 2Department of Biology, Technische Universität
Darmstadt, Darmstadt, Germany; 3The Natural Resources Research
Institute, University of Minnesota, Duluth, MN; 4Indiana State
University, Terre Haute, IN; 5Department of Biology, University of
Göttingen, Göttingen, Germany; 6Institute of Ecosystem Studies,
Millbrook NY; 7Department of Biology, University of Calgary,
Calgary, Canada.
© The Ecological Society of America
(Vitousek 1990). Understandably, much of the focus on
exotic species invasions in forests and other ecosystems has
been on aboveground invaders, which are the most apparent. However, belowground invasions may be equally widespread and may become better known as more ecologists
begin to recognize the importance of links between aboveground and belowground communities (Scheu 2001;
Wardle 2002). Invasion of northern forests by exotic earthworms, for example, is receiving increasing attention.
Earthworms are 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
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Invasive earthworms in temperate forests
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.
428
Earthworm invasions and nutrient cycling
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). Earthworms shift 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
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 (Edwards and 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 Lumbricus terrestris,
the common nightcrawler) form nearly vertical permanent burrows up 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 transformation of the soil is the most obvious
sign of earthworm invasion in northern forests. How these
physical changes and the associated redistribution of
organic matter influence ecosystem level processes such as
total C storage, N transformation rates, 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(b)
Courtesy of University of Minnesota Experiment Station
(a)
PJ Bohlen et al.
Figure 1. Effects of invasive earthworms on forest soils in northern Minnesota. (a) Understory vegetation and herb layer in areas
without earthworms. Note the abundance of tree seedlings and native herbs and the undisturbed soil layer with cover of leaf litter. (b)
Understory vegetation and soil surface at a site invaded by earthworms. Note the lack of herb layer, exposed soil surface with reduced
litter layer and abundant earthworm casts, and exposed roots of canopy trees due to disappearance of forest floor.
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© The Ecological Society of America
PJ Bohlen 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 Berry 1994), 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 surface in the absence of earthworms are
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 (Edwards and 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. Earthworms have 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 York suggested 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
© The Ecological Society of America
Invasive earthworms in temperate forests
(a)
(b)
(c)
Figure 2. Earthworms representative of different ecological
groups. (a) Epigeic species, such as Dendrodrilus rubidus,
inhabit organic-rich surface layers and feed mainly on surface
organic matter. (b) Endogeic species, such as Octolasion
tyrtaeum, consume more mineral soil than epigeic species, and
mix mineral and organic soil layers together. (c) Anecic species,
such as Lumbricus terrestris, live in deep vertical burrows, feed
mainly on surface litter, and incorporate litter into the soil as well
as transporting mineral soil to the surface from deeper soil layers.
(Note that only the anterior end of L terrestris is shown here;
the posterior end remains in its burrow).
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Invasive earthworms in temperate forests
430
York study, the increase in microbial biomass was attributed
to a more favorable environment that increased the “carrying capacity” of the mixed surface soil relative to undisturbed forest floor. Understanding or predicting the effects
of earthworm invasion 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 increase N flux more in systems fertilized with N, such
as agricultural or pasture systems (Knight et al. 1992;
Dominguez et al. in press); earthworm invasion 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 remains to 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 (Paré and
Bernier 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 (Suárez 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.
Alteration of 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
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PJ Bohlen et al.
Dendrobaena octaedra into 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 earthworms in 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 group of the invading species. In fact, results
from a laboratory mesocosm experiment suggest that some
species, including fast-growing species 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 earthworms on microfungal communities 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 laboratory study 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 invertebrate community responses
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 earthworms as
a food source for a wide variety of vertebrates is well
© The Ecological Society of America
PJ Bohlen et al.
(a)
Invasive earthworms in temperate forests
431
(b)
Figure 3. The diversity of soil mixing effects of different ecological groups of earthworms in boxes containing reconstructed
soil layers from an aspen forest in southwest Alberta, Canada.
(a) Boxes with no earthworms; (b) boxes containing individuals
of the epigeic earthworm species, D octaedra, which have mixed
the organic layer into the mineral soil; and (c) boxes containing
individuals of the endogeic species, O tyrtaeum, which have
thoroughly mixed the mineral and organic layers together. For
more details see Scheu & Parkinson (1994).
established (Edwards and 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 earthworm activity on soil invertebrates (Wickenbrock
and Heisler 1997; Loranger et al. 1998), but only either in
the short term or in unfavorable habitats. A high biomass
of D octaedra resulted 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 restructuring of 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
O tyrtaeum and Aporrectodea caliginosa, both endogeic
species, invaded soils previously devoid of earthworms.
These large earthworm species mix organic material and
© The Ecological Society of America
(c)
mineral soil in much greater quantities than D octaedra, and
therefore compete vigorously with microarthropods for
microbial and organic food. They alter habitat and food
resources more strongly and create mechanical disturbances
which, as demonstrated in a 1-year laboratory experiment,
may result in lower microarthropod abundances than are
found in agricultural soils under conventional tillage
(Migge 2001). The same processes occur in the field; these
will be slower in dry continental climates such as in the
forests of southern Alberta, but are likely to be much faster
in the milder climates of the eastern forests. To date, there
are no comparable data available from other regions, and
data on enchytreaids, nematodes, and macroarthropods are
lacking.
Soil inhabiting vertebrates
Recent studies on the foraging behavior of salamanders
(Plethodon sp) 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
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Invasive earthworms in temperate forests
432
invertebrate food sources, or by altering the habitat in
other ways. Further investigations are needed to understand how this influences salamander population 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.
Plant community responses to earthworm
invasions
The abundance and diversity of native plant species and
tree seedlings can decline steeply following earthworm
invasion (Figure 1). Some hardwood forest stands in
northern Minnesota that had lush and diverse understory
plant communities only 40 years ago now have only one
species of native herb and virtually no tree seedlings
remaining after earthworm invasion, although other factors may also have contributed to these changes (Hale
2004). Concerns have therefore been raised about the
potential for widespread loss of native forest plant species
and the stability of their communities in hardwood forest
ecosystems following earthworm invasion.
Earthworm invasions in sugar maple-dominated forests
in northern Minnesota were first noted 15 to 20 years ago
(Mortensen and Mortensen 1998). Many stands contained discrete, visible leading edges of invasion where
forest floor thickness decreased from 10 cm to zero in distances as short as 75 meters. Associated with the loss of
the forest floor across the leading edges were rapid
increases in earthworm biomass, the successive appearance of up to eight earthworm species, and substantial
changes in soil physical and chemical properties (Hale et
al. in press). When not associated with some underlying
gradient in initial soil conditions, this leading edge of
earthworm invasion provides an opportunity to assess the
relationships of earthworm biomass and species assemblages to changes in the understory plant community,
while controlling for site-specific factors that often
thwart field-based comparative studies.
In study plots in northern Minnesota, the abundance
and diversity of the herbaceous plant species and tree
seedlings across leading edges of earthworm invasion
decreased with increasing total earthworm biomass, but
the magnitude of change depended on the species assemblage of the earthworm community (Hale 2004).
Herbaceous plant communities were more strongly
affected when the epi-endogeic species Lumbricus rubellus
was present. A diverse community of herbaceous plants,
including species that are often used as indicators of rich
sugar maple-dominated hardwood forests in the Great
Lakes region (such as Caulophyllum thalictroides, Uvularia
grandiflora, Trillium spp, Osmorhiza claytonii, Asarum
canadensis, and Polygonatum pubescens; Kotar 2002), could
be found in areas where L rubellus was not present. This
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PJ 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 rubellus biomass reached its maximum, the herbaceous plant community was dominated by Carex pennsylvanica and Arisaema
triphyllum, with rare occurrences of other native plant
species. The disappearance of established populations of
the rare goblin fern (Botrychium mormo) were also associated with the invasion of this earthworm (Gundale 2002).
Earthworm invasion of hardwood forests can have both
direct and indirect effects on the understory plant community. Direct mortality of herbaceous plants and small
tree seedlings rooted in the forest floor occurs when
earthworms eat the forest floor out from under them
(James and Cunningham 1989; Hale 2004). Earthworms
may reduce plant regeneration by ingesting and burying
seeds and by reducing the shelter offered by the forest
floor layer, thus exposing seeds and seedlings to desiccation and predation by insects, small mammals, and other
organisms (Leck 1989; Kostel-Hughes 1995). After initial
earthworm invasion, smaller understory plant populations become more vulnerable to the impacts of deer grazing, which can lead to local extirpation (Augustine et al.
1998). Changes in soil nutrient dynamics, including
increases in N and P loss due to leaching and decreased
availability, may also affect the growth and composition
of herbaceous plant communities following earthworm
invasion (Bohlen et al. 2004b; Hale 2004).
Individual responses of plant species to earthworm
invasion will be important in determining the trajectory
of compositional changes in hardwood forests following
earthworm invasion (Scheu 2003; Hale 2004). In a
greenhouse experiment, the addition of earthworms
increased plant mortality and altered root-to-shoot ratios,
but the magnitude and direction of those changes
depended on both the plant species and the particular
species of introduced earthworm. In field studies,
Arisaema triphyllum (Jack in the pulpit) and Allium tricoccum (wild leeks) were both positively associated with
increasing earthworm biomass (Hale 2004). Changes in
the soil fungal community following earthworm invasion
(Johnson et al. 1992; McLean and Parkinson 2000a;
Lawrence et al. 2003), may have consequences for native
understory plants, the vast majority of which are strongly
mycorrhizal in northern forests (Brundrett and Kendrick
1988; Baskin and Baskin 1998). The dominance of earthworm-invaded sites by non-mycorrhizal herbs such as
C pennsylvanica in Minnesota and Allia petioloata (garlic
mustard) throughout the eastern US suggests that earthworms may enhance the competitive success of non-mycorrhizal herb species at the expense of mycorrhizal ones
(Francis and Read 1994; Brussaard 1999; Hale 2004).
In addition to effects on understory herbs, earthworm
invasion may influence overstory trees by influencing
root distribution and function (Fisk et al. 2004). Invading
earthworms can lower the soil surface by removing the
forest floor, thus leaving tree roots exposed and changing
© The Ecological Society of America
PJ Bohlen et al.
their distribution in the soil
(Figure 1b). 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 earthworms in temperate forests
Dispersal
• source population
• natural expansion
• human activity
• streams, rivers
Resource quantity
• plant productivity
• soil organic matter
Resource quality
• vegetation type
• litter C:N ratio
• tannins, polyphenotics
Soil factors
• moisture hydrology
• texture, sand/silt/clay
• acidity, base cations
Earthworm
invasion
Physical effects
• burrowing and casting
• litter removal
• soil aggregates
• porosity
• hydrology
• erosion
Conclusions
Biological effects
• change in soil habitat
• faster nutrient cycling
• less fungally-dominated
• fewer mycorrhizae
• change in rooting zone
• altered seedbed
Geochemical effects
• mixing soil layers
• adsorption/desorption
• mineral weathering
• change in minerology
Ecological consequences
Ecosystem properties
Ecological communities
Earthworm invasion of northern
• C loss (short term)
• plant invasions
• C stabilization (long term)
• loss of native herbs
forests is influenced by many fac• N retention?
• soil invertebrate community shifts
tors and has multiple ecological
• P availability?
• microbial community shifts
• Tree nutrition?
effects mediated through the
physical, geochemical, and biological changes that occur follow- Figure 4. This conceptual model illustrates how the influence of earthworms on the
ing invasion (Figure 4). The eco- biological, chemical, and physical characteristics of the soil ecosystem interact to determine
logical consequences of these the net influence of earthworm invasion on ecosystem processes and ecological communities
invasions depend upon which (C = carbon, N = nitrogen, and P = phosphorus). See text for explanation. (Modified from
species or species complexes Bohlen et al. 2004a).
invade and the characteristics of
the site being invaded. Enough evidence exists to gener- sent an inadequate food source for earthworms with 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
may affect different species in dissimilar ways, so that
worms in forest ecosystems.
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.
The potential widespread loss of native understory
with much less emphasis on the mechanisms of invasion
and the broader landscape- 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 earthworms will 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 spread of horticultural materiearthworms. Low quantities of organic matter may repre- als containing earthworms, or limiting new road con© The Ecological Society of America
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Invasive earthworms in temperate forests
434
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. Earthworm invasion 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.
Earthworm invasions are likely to interact with other biological invasions occurring concurrently or predicted to
occur in forest ecosystems (Hansen et al. 2001). These
invasions will have important consequences, not only for
biodiversity and conservation, but also for nutrient
cycling and ecosystem processes in northern forest ecosystems.
Acknowledgements
Some of the research reported here was supported by
grants from the National Science Foundation (DEB9726869 and DEB-0075236). The ideas presented in this
paper benefited from discussions at a workshop on earthworm invasions sponsored by the National Science
Foundation and the Institute of Ecology at the University
of Georgia and organized by Paul Hendrix. We thank Tim
Fahey, Melany Fisk, Lee Frelich, Derek Pelletier, Peter
Reich, and Esteban Suarez for their contributions to the
work presented here.
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