Download Non-Native Invasive Earthworms as Agents of Change in Northern

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
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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
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(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
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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.
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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
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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).
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Invasive earthwormsin temperate
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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
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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
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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
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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
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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.
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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
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PJ
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University of Minnesota.
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