Pandora's Box Contained Bait: The Global Problem of Introduced Earthworms

Author(s): Paul F. Hendrix, Mac A. Callaham Jr., John M. Drake, Ching-Yu Huang, Sam W.
James, Bruce A. Snyder and Weixin Zhang
Source: Annual Review of Ecology, Evolution, and Systematics, Vol. 39 (2008), pp. 593-613
Published by: Annual Reviews
Stable URL: https://www.jstor.org/stable/30245178
Accessed: 27-02-2020 19:26 UTC

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 Pandora's Box Contained Bait:
The Global Problem of
Introduced Earthworms*

Paul E Hendrix,1,2 Mac A. Callaham, Jr.,3

John M. Drake,1 Ching-Yu Huang,1 Sam W. James,4
Bruce A. Snyder,1 and Weixin Zhang5'6
1Odum School of Ecology, and 2Department of Crop & Soil Sciences, University of Georgia,
Athens, Georgia 30602; email: hendrixp@uga.edu
3 Center for Forest Disturbance Science, Southern Research Station, USDA Forest Service,
Athens, Georgia 30602

4Natural History Museum and Biodiversity Institute, University of Kansas, Lawrence, Kansas,
66045

s South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650

6Graduate University of Chinese Academy of Sciences, Beijing 100039, China

Annu. Rev. Ecol. Evol. Syst. 2008. 39:593-613 Key Words

The Annual Review ofEcology, Evolution, and
biological invasions, exotic species, oligochaete biogeography, soil fauna
Systematics is online at ecolsys.annualreviews.org

This article's doi: Abstract

10.1 146/annurev.ecolsys.39.110707.173426
Introduced exotic earthworms now occur in every biogeographic region in
Copyright @ 2008 by Annual Reviews. all but the driest or coldest habitat types on Earth. The global distribution
All rights reserved
of a few species (e.g., Pontoscolex corethrurus) was noted by early natural-
1543-592X/08/1201-0593$20.00
ists, but now approximately 120 such peregrine species are recognized to
*The U.S. Government has the right to retain a be widespread from regional to global scales, mainly via human activities.
nonexclusive, royalty-free license in and to any
Species adapted to human transport and to colonization of disturbed habi-
copyright covering this paper.
tats are most widespread and are the principal invasive species. We identify
a number of endogenous and exogenous factors that may contribute to the
successful establishment and spread of peregrine species. Quantification of
these factors may help to determine why certain species become invasive
while others do not. Recent advances in theory and modeling of biological
invasions and in molecular techniques should prove fruitful in improving our
understanding of invasive earthworms, as well as in predicting their impacts
on ecosystems.

593

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 INTRODUCTION

Apart from the familiar cases of Argentine fire ants (Soleopsis invicta) in Oceani
Invasive: refers to a the Formosan termite (Coptotermesformosanus) in South Africa and the southea
nonnative or exotic
and the New Zealand flatworm (Arthurdendyus triangulatus) in the British Is
species that causes
ological invasions have gone largely unnoticed until recently (Ehrenfeld &
disturbance to the
earthworms in particular escaped the attention of all but a few biologists intere
ecosystem that it
invades tion and ecology of soil invertebrates. The earliest surveys of terrestrial oligo
several earthworm species had achieved distributions well beyond their expec
Exotic: not naturally
occuring in the possibly displacing indigenous fauna (Beddard 1912, Eisen 1900). Througho
location in which it is tury there has been a steady accumulation of evidence of earthworm introducti
found (also referred to Gates 1972, Ljungstrom 1972, Stebbings 1962). Gates (1982), Jamieson (198
as alien)
later Omodeo (2000) presented modern syntheses of earthworm biogeograph
Introduced: brought ing phylogenetic uncertainties (Jamieson et al. 2002), these works represent
to a location by
the distributions of the major earthworm taxa, both indigenous and exotic, th
intentional and/or
accidental human However, it was probably the observations of dramatic changes in forest soi
action exotic European lumbricid earthworms (e.g., Alban & Berry 1994, Nielsen &
Parkinson 1994) that stimulated recent efforts to understand earthworm invasio
Peregrine: widely
ranging, often owing decade has seen a surge in research on earthworm invasion ecology and severa
to human action detailed effects of introduced earthworms on soils, biota, and ecosystem pr
and tropical regions (Bohlen et al. 2004a, Groffman & Bohlen 1999, Hendr
Bohlen 2002, Lavelle et al. 1999, Parkinson et al. 2004). It is clear that introdu
significantly alter soil structural properties, organic matter and nutrient dyn
animal communities above and belowground (see Table 1 for a summary of d
of five widespread introduced earthworm taxa). In spite of increasing knowled
there is still considerable uncertainly about the earthworms themselves, thei
mechanisms by which they come to be introduced and invasive in new areas. Ou
is to address these uncertainties by attempting to answer the following quest

" How widespread are exotic earthworms and what factors affect their dis
" Can we recognize characteristics of earthworms that contribute to their
" How can we predict which species will be invasive, which geographic a
and what the consequences of earthworm invasions will be?

BIOGEOGRAPHY AND GLOBAL EXTENT

OF EARTHWORM INVASIONS

Historical Perspective
Exotic earthworms now occur on every continent (except Antarctica), on oceanic
biogeographic region, and in nearly every type of ecosystem (including desert oases
Early records identified a dozen or more species that were termed peregrine by M
i.e., "those species which possess some powers of migration over the sea, denied t
worms, and probably due to the direct interference of man" (Beddard 1912). Th
apparently ubiquitous Pontoscolex corethrurus and Eudrilus eugeniae in the tropic
ingly, being the only peregrine representative from the families Glossoscolecida
respectively); several species from the genera Amynthas, Microscolex, Dichogaster, a
Megascolecidae); and at least 10 species of Lumbricidae, which include "by far the
of peregrine forms" (Beddard 1912). Beddard also drew several conclusions from

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Table 1 Distributions and known impacts for select well-known invasive earthworm taxa

Biogeographic realm(s)
(see Figure 1)
Taxa Indigenous Introduced Impacts and selected references
Lumbricidae

Aporrectodea spp. Western ALLa,b Native earthworms (Winsome et al. 2006)

Palearctic

Plant growth (Doube et al. 1997, Welke & Parkinson 2003)

Nutrient cycling (Bohlen et al. 2004)
Dendrobaena octaedra Western ALL except Microarthropods (McLean & Parkinson 2000)
Palearctic Ethiopiana'b
Forest floor (Parkinson et al. 2004)
Soil structure and function (Hale et al. 2005)
Lumbricus rubellus and Western ALLa,b Microarthropods (Eisenhauer et al. 2007)
L. terrestris Palearctic

Plant community composition (Freli

Holdsworth et al. 2007)
Nutrient cycling (Bohlen et al. 2004
Soil structure and function (Hale et

Megascolecidae
Amynthas spp. Eastern Palearctic ALLab Macroarthro
Plant growth (Brown et al. 2006)
Nutrient cycling (Burtelow et al. 19
Steinberg et al. 1997)
Soil structure (B.A. Snyder, unpublis
Glossoscolecidae

Pontoscolex corethrurus Neotropical ALLa Plant community (Gonzalez et al. 2006)

Litter decomposition (Liu and Zou 2002)
Nutrient cycling (Lavelle et al. 1999)
Soil structure (Lavelle et al. 1999)

aGates 1972.
bDoes not include biogeographic realm of origin, as there is debate on the size of the region of origin for most earthworm taxa. P corethrurus is a notable
exception (Lavelle & Lapied 2003).

of peregrine earthworms: (a) The capacity of "extending their range beyond the limits assigned by
nature is not confined to any one family." He further suggested that the disproportionate numbers
of peregrine Lumbricidae, relative to other families, is a consequence of the "newness" of the
family coupled with the "vigour seen in new races." (b) "Some species are more capable of extend-
ing themselves than others." In the tropics, for example, E. eugeniae and P corethrurus are already
circummundane, whereas Dichogaster bolaui, Nematogenia panamaensis, and Pheretima taprobanae
occur in increasingly more restricted areas outside their indigenous home. (c) There appear to be
no "peculiarities of structure" common to all peregrine forms that might account for their success,
other than the fact that all are small to moderate in size. Whereas intolerance to low temperature
appears to limit success of tropical peregrines in temperate climates, the opposite does not seem to
be true, as a number of lumbricid species have become established in the tropics (e.g., Gates 1972).
Although temperate earthworms introduced into the tropics appear best adapted to montane
temperate areas, this latter conclusion by Beddard is of great modern interest as we attempt to

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 understand mechanisms of invasiveness and develop models to predict where and how extensively
earthworm invasions might occur.

Megadrile: large
terrestrial and
Systematics and Evolutionary History
semiaquatic segmented
worms, commonly Earthworms are classified within the phylum Annelida, class Clitellata, subclass Oligochaeta (in-
referred to as creasingly, Crassiclitellata). Seventeen families are usually recognized worldwide, making up the
earthworms, cf. semiaquatic and terrestrial forms commonly known as earthworms (Jamieson et al. 2002). Ap-
microdrile
proximately 3700 species of these megadrile oligochaetes have been described, and it is estimated
Microdrile: small, that total global species richness may exceed 7000 (Fragoso et al. 1999, Lavelle & Lapied 2003,
mostly aquatic
Reynolds 1994). Current distributions of the major families are shown in Figure 1.
oligochaete worms,
The broad outlines of earthworm distributions were set by geological and biological evolution:
but also including the
terrestiral diversification, dispersion, and extinction on slowly shifting land masses (James 2004). On smaller
Enchytraeidae spatiotemporal scales, changing climate and ecological processes affect earthworm distributions.
We present a brief overview of these subjects to clarify two points. First is how it is possible to
know that a particular species is exotic to a location. Second, it is important to know why some
locations were or are naturally devoid of earthworms, because such locations may respond very
differently to earthworm invasions than places where an indigenous earthworm community exists
(or once existed).
Earthworms have left no known pre-Neogene fossils of any kind, save possibly ichnofossils
of form consistent with modern earthworm-created structures (S. Hasiotis & S. James, personal

9 12 1 1

00
Ethiopian

1 Ailoscolecidae ae
3 Almidae 11 Lumbricidae
4 Biwadrilidae 12 Lutodrilidae # Indigenoustaxa only
5 Criodrilidae 13 Megascolecidae 0 Indigenous and introduced taxa
Eudrilidae 14 Microchaetidae
7 Glossoscolecidae 15 Moniligastridae Introduced taxa only
8 Hormogastridae 17 nerodriliae
9 Komarekionidae Sparganophilidae

Figure 1
Global distribution of indigenous and introduced species within earthworm families in each biogeographic realm (modified from
Reynolds 1994, with data from Gates 1982, Jamieson 1981, Omodeo 2000, Sims 1980).

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observation). Thus the origins of earthworms are uncertain in time and space, but their position
on the phylogenetic tree of Annelida: Clitellata is probably as a sister group to the Enchytraeidae
(Erseus 2005). In this view, the basal clitellates were aquatic, and ancestors of earthworms and Native: a taxon that
Enchytraeidae were most likely aquatic clitellates because the sister clade is the largely aquatic occurs naturally in the
Lumbriculidae leeches. location where it is
found
Apart from some uncertainties about the phylogenetic positions of the Syngenodrilidae, Al-
luroididae, and Moniligastridae, the distributions of the family-level taxa are mainly consistent
with post-Pangaean land area relationships (James 2004, Jamieson 1981, Sims 1980) insofar as
the phylogeny is known. This is important in the discussion of invasive earthworms because to
know if something is outside its natural range, one must have some basis for determining what
the natural range is. Until considerable knowledge of earthworm distributions accumulated, spe-
cialists were not surprised to find what we now know to be Asian and European species in various
other locations, and to name them for those locations as if the species were indigenous to the
places. Some examples are Amynthas hawayanus (junior synonym ofA. gracilis, material for which
was also first found well outside of Asia), and Allolobopohora iowana (syn. Aporrectodea caliginosa).
Amynthas loveridgei is not yet known from inside the natural genus range, only from the Western
Hemisphere, but no one would consider it native to any of the places it has been found.
In the pre-plate tectonics era, biologists often invoked long-distance dispersal and land bridges
to explain observed distributions (Stephenson 1930). However, some earthworm specialists sug-
gested that human activity was responsible for certain common introduced species' presence, noted
the associated disappearance of indigenous species, and correctly identified the continents of ori-
gin of the exotics (Eisen 1900, Ljungstrom 1972). Eventually, plate tectonics models of Earth's
crust removed the hypothetical imperative for land bridges and other esoteric dispersal scenarios.
Thus, support dwindled for considering multicontinental distributions of some exotic species as
natural (e.g., Omodeo 1963), and it became more straightforward to speak of native and exotic
species of earthworms.
To know if a species is not native to a site, we first refer to the primary concentration of
the relevant supraspecific taxon, such as Amynthas in mainland Asia, Pontoscolex in the Guyanan
Shield, or the Lumbricidae in Europe. Then we note that of the particular taxon, a subset is
widely distributed outside its presumed natural range, and the species in question belongs to
that subset. The evidence is circumstantial but is credible in light of the facts that there were no
remarkable land bridges and long-distance prehistoric dispersal is not a necessary condition to
achieve present-day natural and artificial distributions. Indeed, it is highly improbable that in the
absence of human transport, a single species would exist in numerous widely scattered locations
across the globe, such as the artificially pan-tropical P corethrurus.
Pleistocene glaciations are thought to have eliminated the earthworm fauna from most of the
northern temperate regions of Earth (Gates 1982, Tiunov et al. 2006). Natural refaunation by
dispersal from glacial refugia in North America, Europe, and Asia has been slow [-10 m year-'
(Terhivuo & Saura 2006)], leaving large areas of northern temperate forest, boreal forest, and
tundra devoid of native earthworms. In these areas, invasions take place in soils unoccupied by
earthworms (e.g., Alban & Berry 1994, Frelich et al. 2006, Tiunov et al. 2006). This is an important
distinction from regions inhabited by native earthworms because, compared with the latter sites,
naturally earthworm-free ecosystems have different soil process characteristics, different organic
matter breakdown regimes, and will show greater change when invaded by an ecosystem engineer
class that previously was absent (Bohlen et al. 2004). Where invasions take place into occupied soils
(or heavily disturbed soils where natives have been negatively impacted), soil structure may not be
so drastically altered, although it is still possible to have major structural changes (Hendrix et al.
2006). Other soil biota and vegetation are likely to be adapted to the influence of earthworms and

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 may be less affected by a change in earthworm community composition than biota unaccustomed
to earthworm presence.

Distributional Patterns of Introduced Earthworms

Among the approximately 3700 described species, about 3% (-120) have been identified as pere-
grine (Fragoso et al. 1999, Lee 1985), but the current state of knowledge allows few generalizatio
about distributional patterns of introduced earthworms. At global scales, Beddard's (1912) obse
vations still hold: Temperate regions tend to be invaded by temperate species, and tropical regio
by tropical species (with some temperate species also invading montane temperate elevations in
the tropics). Given that there are many more tropical than temperate earthworm species (Frago
et al. 1999, Lavelle & Lapied 2003), it is interesting that the proportion of peregrines is muc
higher among temperate species (tropical: 51 of an estimated several thousand species; temperate
45 of an estimated 500-600). This suggests that there are many more tropical peregrines that ha
not yet been discovered; that many more tropical species have yet to become peregrine, but cou
under appropriate conditions; that temperate species are inherently more prone to invasivenes
possibly through more euryoecious adaptations; or that current distributions of introduced eart
worms are mostly a function of global commerce that has favored transport of temperate mo
than tropical species over the past centuries. The last two hypotheses seem the most likely, but the
emergence of new tropical invasive species is an intriguing possibility, that is, that regional per
grines have the potential to become global peregrines, including several species of the pheretimo
genus Amynthas in Thailand (e.g., A. alexandri) and subtropical China.
At regional to local scales, it has long been held that exotic earthworms tend to coloniz
and become established in disturbed habitats (Eisen 1900, Lee 1985, Sims 1980, Smith 1928,
Stebbings 1962). Whether or not they become invasive appears to depend on local climatic,
edaphic, and land-use factors. For example, several studies found that introduced earthworm
failed to disperse into surrounding undisturbed areas even decades after introduction (Abbo
1985, Kalisz & Dotson 1989, Lavelle & Pashanasi 1989). However, other studies have shown th
introductions of exotic species may create hotspots that then become hubs for further invasion int
surrounding areas (e.g., Holdsworth et al. 2007). It is commonly believed that exotic earthworm
displace native species through competitive interactions, or that they occupy niches vacated by
extirpated native species. Kalisz & Wood (1995) summarized the prevailing idea that physic
disturbance or habitat fragmentation is prerequisite to establishment of and domination by exot
earthworms in soils occupied by native species. The proposed sequence is (a) habitat disturbance
(b) decline or extirpation of native species, (c) introduction of exotic species, and (d) colonizatio
of empty habitat by exotic species. Undisturbed soils occupied by native earthworms may exclu
exotic species (e.g., Wood et al. 1997), but coexistence of native and exotic species, however
transient it may be, has been reported in a number of locations (e.g., Callaham et al. 2003, Gros
et al. 2006, Hendrix et al. 2006). The extent to which native species persist in the presence
exotics may be attributable to the degree of habitat disturbance (Figure 2).

Regions of Origin and Introduction of Exotic Earthworms

As noted above, some representatives from most earthworm families have become established
exotic species in other biogeographic realms (Figure 1). The ~120 known peregrines include -50
Megascolecidae, -3 0 Lumbricidae, and -~40 species from 10 other families, at least one of whic
can be traced to an origin in each realm (Gates 1982, Jamieson 1981, Lee 1985, Omodeo 2000
Reynolds 1994, Sims 1980).

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 oE
0 Exotics
dominant

0 Mix of native
X and exotic
X species

. dominant

W Frequency
0" M

CC M

Indirect [Diffuse ) Concentrated

Direct Infrequent - Frequent
Superficial Profile disrupting
Figure 2
Hypothesized relationships between types of disturbance and expected proportions of native and exotic
species. Direct disturbances are categorized by frequency of occurrence and by intensity or degree of
physical perturbation of the soil profile. Frequency and intensity are related, but we envision a scenario
where extreme disruption of the soil profile need not be frequent to effect change in earthworm
communities (inset). Indirect disturbances include road density, human population density, degree of
fragmentation, and diversity of land-use types, among others.

The most widespread exotic earthworms come from the Palearctic European Lumbricidae,
including 20-30 species from the genera Lumbricus, Aporrectodea, Allolobophora, Octolasion, Den-
drobaena, Eisenia, and Eiseniella that can now be found in temperate habitats throughout the world
(Lee 1985, Reynolds 1995, Sims 1980). The highest diversity of the approximately 385 species
of Lumbricidae occurs in the unglaciated regions of southern Europe, only approximately 5% of
those species having spread into northern areas either by natural dispersion or through human
transport (Sims & Gerard 1999, Tiunov et al. 2006). The families Criodrilidae, Hormogastridae,
and Ailoscolecidae also occur in Europe but are not known to have become established widely
outside of the western Palearctic region. Interestingly, the now Holarctic genus Sparganophilus
(Sparganophilidae) may have been introduced into Great Britain and France from southeast-
ern North America, where it presumably originated. Introduced earthworms in Europe include
Amynthas spp., Dichogaster spp., Pontodrilus spp., Microscolex spp. (Megascolecidae), Ocnerodrilus
occidentalis (Ocnerodrilidae), and E. eugeniae (Eudrilidae), among others (Omodeo 2000, Sims &
Gerard 1999).
The Palearctic and Oriental biogeographic regions of East Asia contain a large diversity of
earthworms in the Megascolecidae, Lumbricidae, Biwadrilidae, Almidae, and Ocnerodrilidae.
These regions are also the origins of several important groups of invasive earthworms, including
the pheretimoid group of Megascolecidae and Lampito mauritii. Among the pheretimoids, Amyn-
thas and Metaphire are the dominant genera in southern China (Chen 1956, Zeng et al. 1982),
represented by 86 and 34 endemic species, respectively, mostly distributed in southern China
except for eight species also found in northern China. Of the 244 reported species in China,
approximately 32 are introduced, belonging to 7 families and 18 genera (Huang et al. 2006, Xu

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 1996). Collectively, 68% of nonnative earthworms in China belong to the Lumbricidae and are
distributed mainly in northern China; 57% of known species in northern China belong to the
Lumbricidae and their proportion of the total earthworm fauna decreases from north to south
across the country (Huang et al. 2006).
The Indian subcontinent has a large and diverse native fauna and is home to the pantropical
Perionyx excavatus, which is widespread in India owing to its importance in vermicomposting. Addi-
tional Perionyx species may be locally invasive, and there is enough morphological diversity within
compost operations to suggest that more than one species may be involved. Other exotic species
are Bimastosparvus and European Lumbricidae (in higher elevations of the Western Ghats and in
the Himalayas), R corethrurus, various pheretimoids (Amynthas, Metaphire), a few Ocnerodrilidae
and Dichogaster species, and some regional peregrines such as Lampito mauritii (Stephenson 1923;
S.W. James, personal observation).
European Lumbricidae, Asian pheretimoids, and South American Glossoscolecidae (P corethru-
rus) are the main invasive earthworms in Australia, New Zealand, Papua New Guinea, and the
South Pacific islands. In Australia, there are at least 66 introduced earthworm species and -350
described native species (Jamieson 1981). Two lumbricids, Aporrectodea trapezoides and A. calig-
inosa, are especially common in agricultural lands and pastures of Australia (Baker 2004, Mele
& Carter 1999). Similarly, a nationwide survey in New Zealand found that 64% of 216 farms
assessed were inhabited by at least 3-4 European lumbricid species, A. caliginosa being the most
widely distributed (Springett 1992). Lumbricid earthworms were introduced with early European
settlements in Australia and New Zealand for agricultural purposes. Peregrine earthworms in the
southwestern Pacific islands belong to the families Lumbricidae, Moniligastridae, Glossoscoleci-
dae, and Megascolecidae, the latter including Dichogaster spp, which collectively constitutes 14 of
26 recorded species in this area. Pontoscolex corethrurus is particularly widespread in the islands of
Fiji, Samoa, Tonga, and Niue (Easton 1984).
A sparse but growing literature deals with introduced earthworms in the Neotropics. For ex-
ample, it is estimated that 17% of the known species in Brazil are invasive (Brown et al. 2006),
but in the heavily populated state of Sio Paulo nearly 40% of all species collected were intro-
duced (Brown & James 2006). These introduced species included the ubiquitous R corethrurus and
E. eugeniae, but also many other species representing the families Megascolecidae (11 species),
Lumbricidae (2 species), Acanthodrilidae (6 species), Ocnerodrilidae (5 species), and Glossoscole-
cidae (1 species other than P corethrurus). Other parts of South America where information is
available include Argentina [25 species, 6 megascolecids, and 19 lumbricids (Mischis & Herrera
2006)], Uruguay [11 Megascolecidae and Lumbricidae that dominate Uruguayan soils, particu-
larly in more disturbed sites (Grosso et al. 2006)], and Andean Colombia [5 introduced species
of 18 collected from forested and pasture soils (Feijoo-Martinez et al. 2006)]. Regional sampling
in Mexico showed relatively few introduced species, but that these (particularly P corethrurus,
R elongata, and Ocnerodrilus occidentalis) were widespread (Fragoso et al. 1995). In Puerto Rico,
R corethrurus and Amynthas spp. make up the majority of invasive species, and these are known
to dominate soils where primary forest has been cleared (Gonzalez et al. 2006) Likewise, on the
islands of the Caribbean basin, there are relatively few invasive earthworms species, but these
are ubiquitous. Pontoscolex corethrurus occurs across the basin, and various Amynthas spp. are also
common (Fragoso et al. 1995).
African records of introduced earthworms, as is the case for many sparsely studied regions,
are mainly found scattered in the taxonomic literature where the specimens were found in col-
lections examined by specialists (Pickford 1937). Ljungstrom (1972) commented on the large
extent of invasions in urbanized and cultivated parts of South Africa. Recently, some ecological
and agricultural studies have provided indications of the extent of invasions in Africa. S.W. James

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(unpublished data) has found several Amynthas species and Octolasion tyrtaeum in KwaZulu Natal,
South Africa. Pontoscolex corethrurus is known from Kenya and probably inhabits almost all other
nondesert regions. North Africa is home to many European species in the wetter areas (Omodeo
2000), and the Canary Islands are entirely populated with exotic species (Talavera 2007).
In addition to the approximately 102 described native earthworm species in North America
north of Mexico (Fender 1995, James 1995; the former suggesting another 80+ undescribed
species), at least 45 exotic species have been introduced. As of the early 1990s, known exotics
included European Lumbricidae (25 species), African Acanthodrilidae (two species), Asian Megas-
colecidae (14 species of the pheretimoid group), South American Acanthodrilidae (two species),
African Eudrilidae (E. eugenia), South American Glossoscolecidae (P corethrurus), Asian Monili-
gastridae (1 species), and Ocnerodrilidae (2 species) (Gates 1982, Reynolds 1995). It is likely that
other species have been introduced but have not yet been reported in the literature. Interestingly,
only one Nearctic earthworm, Bimastos parvus, is known to have become established as an exotic
species outside of North America [e.g., in Europe, Nepal, East Asia, and Brazil (Brown et al. 2006,
Gates 1982)].
From our current knowledge of the distributions of introduced earthworms, an important
question arises: What accounts for the biogeographic asymmetry in exotic species distributions;
that is, why are some areas more highly invaded than others? This could be partly due to lack of
information from areas that have not been adequately surveyed (e.g., Africa), such that earthworm
introductions may be even more extensive than we currently know. But in regions of known
introductions, factors contributing to high species richness of exotic earthworms probably include
the history of introductions in the wake of human colonization and commerce and environmental
tolerances of introduced earthworms relative to conditions in their new habitats (Gonzalez et al.
2006, James & Hendrix 2004). Our ability to predict future invasions will require a much better
understanding of the biological and ecological mechanisms involved.

MECHANISMS OF EARTHWORM INVASIVENESS

What biological traits predispose species to be invasive is a fundamental question of invasion

biology (Simberloff 1989). A number of indicators of invasiveness have been postulated, including
high fecundity, single-parent reproduction, high genetic variability, phenotypic plasticity, high
abundance and wide range in native habitat, taxonomic isolation, and occupancy of vacant niche
in new habitat. Beddard (1912) lamented that there appear to be no "peculiarities of structure"
common to all peregrine earthworms. Nearly a century later, Lodge (1993) remarked with respect
to invasive species in general "[that] because all patterns are characterized by large variance and
exceptions, we cannot with any confidence predict the outcome of any particular introduction."
However, recent advances in data mining and statistical learning have reversed this conclusion.
Taxonomically grouped reliable predictors of invasiveness have now been identified for birds
(Jeschke & Strayer 2006, Sol et al. 2005), fishes (Jeschke & Strayer 2006, Kolar & Lodge 2002,
Marchetti et al. 2004), mammals (Jeschke & Strayer 2006), mollusks (Keller et al. 2007), pine
trees (Rejmainek & Richardson 1996), and woody plants (Reichard & Hamilton 1997).
Such findings have not been reported for invasive earthworms. Rather, where studies have
been performed, counterexamples have been identified. Thus, a number of morphological and
behavioral traits found in invasive species are also common to noninvasives (Hendrix & Bohlen
2002). Further, it appears that invasion success of one species is a poor indicator of invasion success
of closely related species. As examples, there are hundreds of Amynthas species, but only approxi-
mately 10 are widely invasive. Until recently, Pithemera was only known from approximately eight
invasive species (mostly in Pacific islands and Southeast Asia), but recent surveys in the Philippines

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 have discovered at least 50 noninvasive species (Hong et al. 2008). Thus, taxonomic sampling bias
must be considered because several years ago we might have believed that all Pithemera are invasive.
Other generalizations, however, might be useful in identifying potentially invasive earthworms.
Anthropochorous:
primarily associating
For example, species that exhibit a wide range of environmental plasticity in their native habitats are
with human habitation likely to become more widespread than species with more restrictive environmental requirements
(Fragoso et al. 1999, Williamson 1996). Although not satisfying from a mechanistic standpoint,
prior invasion success may be one of the clearest indicators of a species' potential to invade
new habitats, at least for the well-known, anthropochorous earthworms (Table 1). A systematic
comparative study of the characteristics of invasive versus noninvasive earthworms would be timely.

Invasiveness Characteristics and Vectors of Earthworm Transport

It has been suggested that biological invasions by cryptozoans are more similar to plant than
to animal invasions (di Castri 1991). This may be particularly true for earthworms because of
certain reproductive (e.g., cocoon production), behavioral (e.g., diapause), and economic (e.g., use
in vermiculture) features of these organisms. A number of factors, both inherent to earthworms
(endogenous) and to agents of their environment (exogenous), may contribute to the invasiveness
of at least some species (Fragoso et al. 1999, James & Hendrix 2004).
Endogenous factors include characteristics such as wide environmental tolerance (e.g., edaphic
plasticity), which, for example, allows anthropochores to establish in disturbed habitats; ability
to survive travel in dormancy or as cocoons; dispersal ability (e.g., mass migrations on rainy
nights); and reproductive strategies of high fecundity, continuous breeding (especially in tropical
species), short incubation time, high hatching success, and, important for colonizing species,
parthenogenesis, through which a single organism can establish a population (Fragoso et al. 1999,
Terhivuo & Saura 2006). Cocoon production may be particularly important. For example, in
Southeast Asia it is common at the end of the rainy season to see mass migrations and mass death
of earthworms (Gates 1972), possibly following mass reproduction and production of cocoons
that will endure the dry season. This adaptation may also allow such species to survive winter in
northern climates where they have been introduced, if timing of tropical dry seasons is similar
to that of northern winters [e.g., Amynthas spp. in the northern United States (Burtelow et al.
1998, Steinberg et al. 1997)]. Feeding behavior or ecological strategy may also be important for
habitat matching at fine spatial scales, such that epigeic earthworms are less likely than endogeic
ones to colonize open or grassland habitats without substantial surface litter layers (Hendrix &
Bohlen 2002). Sims (1980) noted that the most successful invasive lumbricid species are generalist,
edaphophagous feeders that inhabit temporary burrows and are able to withstand soil disturbances.
Several exogenous factors are important in facilitating movements of earthworms across areas
they are not likely to traverse on their own. As noted previously, over geologic time, drifting land
masses distributed ancestral stock from which contemporary earthworm taxa have evolved. On
shorter timescales, natural vectors of transport may include phoresy [e.g., transport of cocoons
on birds' feet (see Sims 1980)]; gravity, whereby earthworms and their cocoons roll downslope or
wash downstream in watersheds; winds, such as in convective storms that transport earthworm-
containing soil and forest floor material; and ocean currents that, for example, raft euryhaline
Pontodrilus litoralis or their cocoons in tropical seas, where these earthworms tend to live on pro-
tected shorelines (Sims 1980, Terhivuo & Saura 2006). Anthropogenic vectors now dominate
movements of earthworms and their propagules on a global scale. Historically, early agriculture,
commerce, and exploration by Chinese, Polynesian, and European mariners probably first in-
troduced many of the common peregrine earthworms that Eisen (1900), Beddard (1912), and
their predecessors reported (James & Hendrix 2004). Over the following century, expanding

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international trade has undoubtedly accelerated transport of the same peregrines as well as many
other earthworm species. In fact, Gates (1982) monitored oligochaetes intercepted with imported
plants and soils quarantined by the U.S. Department of Agriculture over a 32-year period (1950-
1982) and found that earthworms from all over the world were continually being imported into the
United States. At regional to local scales, modern commerce in horticulture, forestry, and vermi-
culture introduces earthworms widely in urban and managed ecosystems, whereas back-country
fishing and off-road recreation (pack animals and motorized vehicles) may be significant vectors
of transport into remote areas (e.g., Callaham et al. 2006, Holdsworth et al. 2007).
Recognition of these endogenous and exogenous factors involved in earthworm introductions
raises some interesting questions. Are all exotic/peregrine species invasive and do they display de-
grees of invasiveness? After all, to become invasive, that is, a self-sustaining, spreading, dominant
species, a species must transit several phases of invasion: entrainment in a pathway for redistribu-
tion, transport, establishment, and spread (Kolar & Lodge 2001, box 1). Or is invasiveness more
a matter of opportunism or stochasticity? Does one invasive species facilitate establishment of
others as in the relay effect described by Frelich et al. (2006), and could earthworm invasions
manifest as an invasional meltdown (Simberloff & von Holle 1999)?
Ultimately, it would be useful to identify characteristics that might aid in predicting invasiveness
of introduced earthworms. Measurable features or predictors might include feeding behavior or
life history strategy (i.e., epigeic, endogeic, anecic), environmental tolerances (e.g., soil pH, tem-
perature, water, and organic matter), reproductive characteristics (uni- versus biparental, cocoon
production rate and incubation time, parental investment in cocoons/embryos), morphological
features (e.g., length, width, mass; pigmentation; gut length; typhlosole development), locomo-
tion (activity, dispersability), travelability (ability to survive transport, response to vibration, mode
and length of dormancy), and tolerance to disturbance (maybe even commensalism with humans,
e.g., anthropochory). Habitat legacy effects might also be important predictors. For example, of
grassland, forest, or riparian species, what fraction is known or is likely to be invasive? Interest-
ingly, Octolasion tyrtaeum, a wetland species in its Palearctic home range, is now widespread in a
variety of habitats, including agricultural soil, in eastern North America (Terhivuo & Saura 2006),
suggesting the possibility of rapid phenotypic or genetic adaptations in at least some species.

MODELING EARTHWORM INVASIONS

Models and Prediction of Earthworm Invasion

Formal approaches to modeling invasions have rarely been applied to earthworms (e.g.,
Holdsworth et al. 2007), although models could be used to better understand many aspects of
earthworm invasions. A first step is modeling suitable habitat, a necessary condition for inva-
sion. Recent decades have seen rapid advances in computational methods for habitat modeling,
including the Genetic Algorithm for Rule Set Production [GARP (e.g., Drake & Bossenbroek
2004)], maximum entropy methods (Phillips et al. 2006), and a wide range of statistical and ma-
chine learning methods (e.g., Leathwick et al. 2006). With care, each of these can be used to
identify habitable environments from information on native range, museum records, and/or ini-
tial records from within the invaded range (but see Meynard & Quinn 2007, Stockman et al.
2006). A second condition for invasion success is introduction in numbers adequate to ensure
persistence. For species associated with human activity, (i.e., virtually all invasive earthworms) the
dominant mode of long-distance dispersal is attendance on mechanisms of human transportation,
for example, association with horticulture. Such human activities may be modeled using spatial
interaction or gravity models in which zones of attractiveness to traveling people are represented

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 as discrete sites (e.g., Leung et al. 2006). The final condition for invasion to occur is local spread
and dominance. Reaction-diffusion and integrodifference equations are models that integrate
population growth and spread for species that reproduce continuously or in discrete time steps,
respectively (Neubert & Parker 2004, Shigesada & Kawasaki 1997). Both families of models have
been widely used to understand and predict the spread of invasive species from many taxonomic
groups (e.g., Buckley et al. 2005, Krkosek et al. 2007). These models have rarely been applied to
earthworms or other soil invertebrates, probably because key data have not been collected. We
submit that if future studies make an effort to integrate theory and data, our understanding of
earthworm invasions will better inform invasion theory overall and our general understanding
of population growth and spread will aid the control and management of spreading earthworm
species.

Models of Earthworm Effects on Ecosystem Processes

Recently, simulation models have been applied in soil ecology for evaluation and prediction of po-
tential impacts of soil organisms on ecosystem functions, such as soil organic matter decomposition
and carbon cycling (Chertov & Komarov 1997, Fu et al. 2000, Hairiah et al. 2006, Lavelle et al.
2004). The potential impacts of earthworms on ecosystem function can also be evaluated by their
regulation of soil nutrient dynamics, especially in the case of earthworm invasions (Bohlen et al.
2004). Barot et al. (2007) ran a model of limiting nutrient cycles following three pathways: without
earthworms, with earthworm trophic (direct) effects, and with earthworm nontrophic (indirect)
effects. Their simulation results indicated that the presence of earthworms could increase primary
production through trophic and nontrophic effects because of the conservation of nutrients in
ecosystems. For earthworm invasions, simulation models might also apply to the estimation of
invasion history and to the prediction of the magnitude of their impacts on soil nutrient cycles.
Simulation models can give a rough calculation of time that has elapsed since the introduction of
earthworms and an assessment of potential influences on soil nutrients based on the knowledge
of impacts of invasive earthworms on decomposition and mineralization processes (C.-Y. Huang,
unpublished data). However, more work is needed for the development of a theoretical model that
is also supported by field experiments or observations of earthworm invasions.

Earthworms as Model Systems in Invasion Biology

Earthworms are underexploited as a model for invasion biology. Many recent studies have adopted
a comparative approach, taking advantage of uncontrolled invasions of plants, birds, fishes, mam-
mals, and invertebrates to answer a range of ecological questions. Thus, researchers have identified
traits correlated with invasion success (Hamilton et al. 2005, Kolar & Lodge 2001, Marchetti et al.
2004), tested hypotheses about the integration of introduced species into resident communities
(Menke & Holway 2006), and characterized transient biological phenomena such as population
growth at small population sizes (Davis et al. 2004) and species spread (Johnson et al. 2006).
Invasion biology would benefit by comparable studies on earthworms.
A first question is whether earthworms exhibit the same patterns as other invasive species. Do
earthworm invaders act like other invasive species, or are there unexplored mechanisms at work in
earthworm invasions? Are there different classes of earthworm invaders, or are all invasive earth-
worms alike? Do the same traits that predispose other species groups to establish new populations
or dominate resident communities also facilitate earthworm invasions? At what spatial scales are
native and introduced species richness positively versus negatively correlated (Stohlgren et al.
2003)?

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 Several characteristics lend earthworms to experimental research. At least some species are
easily cultured. Collection and relocation by researchers is rarely regulated. Natural source pop-
ulations are abundant in many places in the world. Individuals are large enough to be located in
experimental media, but small enough to be studied at the mesocosm scale. As a model for pop-
ulation ecology they are nearly ideal: Short generation times, small individual home ranges, and
representatives of both selfing and nonselfing forms are available. Growth and fitness are easily
observed. We think the following questions could be answered using experimental earthworm
systems as models:

1. What are the relative roles of propagule pressure (Williamson 1996) and habitat suitability
(Menke & Holway 2006) in population establishment? What role do biotic interactions play
in establishment (Mitchell et al. 2006)? What role does disturbance play in establishment
(Buckley et al. 2007)? How does the timing of introduction affect establishment (Drake et al.
2006)?
2. Do particular biological traits predispose species to traverse successfully the different tran-
sitions of a biological invasion, that is, transport, establishment, population growth, com-
munity dominance (Kolar & Lodge 2001)?
3. Are sequences of species introductions facilitative, resulting in invasional meltdown, or are
they saturating or idiosyncratic (Frelich et al. 2006, Ricciardi 2001, Simberloff & von Holle
1999)?
4. What role do coevolved versus novel natural enemies play in population establishment,
growth, and dominance (Colautti et al. 2004, Torchin et al. 2003)?
5. Under what conditions do invasive species displace resident species? How do invasive species
displace residents, that is, evolution of increased competitive ability (EICA) (Blossey &
Notzold 1995, Joshi & Vrieling 2005), novel weapons hypothesis (Callaway & Ridenour
2004)? When do invasive species increase versus reduce species richness (Gurevitch & Padilla
2004, Sax & Gaines 2003; cf. Clavero & Garcia-Berthou 2005, Ricciardi 2004)?
6. How do species spread in naturally heterogeneous environments (Hastings et al. 2005,
Melbourne et al. 2007)? When do long-distance and diffusive spread occur (Muirhead et al.
2006, Shigesada et al. 1995)? What biological characteristics cause species to spread rapidly
(Kinlan & Hastings 2005)?
7. Do genetic characteristics (e.g., outcrossing, heterosis) predispose species to invasiveness
(Drake 2006, Lee 2002)? How much adaptation occurs between introduction and growth
of invasive populations [e.g., via clone pool variability in parthenogenetic earthworms
(Terhivuo & Saura 2006)]? Does genetic adaptation explain observed lags between intro-
duction and detection (Shigesada & Kawasaki 1997)?

FUTURE PERSPECTIVES

Implications of Climate Change for Earthworm Distributions

Possible interactions between global change and earthworm invasions are of considerable in-
terest (Bohlen et al. 2004, Frelich et al. 2006). First, the distributions of invasive earthworms
worldwide could be altered with changes in land use and climate. Land transformation provides
more opportunities for invasion, and, conversely, invasions enhance and drive land transforma-
tion (Hobbs 2000). For example, deforestation and other human disturbances could create more
habitats suitable for occupation by introduced species. Climate change has the potential to modify
impacts of invasive species by affecting their sources, pathways, and destinations (Sutherst 2000).
Furthermore, with a warming climate, the demarcation lines of earthworm distributions might

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 advance poleward and to higher elevations, where few or no earthworms occur owing to conti-
nental and alpine glaciations. Some European lumbricid species (e.g., Dendrobaena octaedra and
Eisenia nordenskioldi) already occur near the Arctic Circle in Russia (Tiunov et al. 2006) and could
be expected to advance more rapidly northward into thawing permafrost. Even at lower latitudes
altered temperature and precipitation patterns could have more localized effects such as restriction
of temperate-adapted lumbricids in tropical areas or expansion of the ranges of regional peregrines
such as pheretimoid species in East Asia. Warming at high elevations might be a particular prob-
lem for biodiversity conservation; high endemism in mountainous areas could be threatened by
invading earthworms (e.g., Pop & Pop 2006). Second, the impacts of earthworms on global change
are likely to be complex. In the short term, especially in areas previously devoid of earthworms,
invasive earthworms may increase the decomposition of soil organic matter and release more CO2
into the atmosphere (Potthoff et al. 2001, Speratti & Whalen 2008), and in some cases also more
N20 (Rizhiya et al. 2007). In the longer term, earthworm activities may increase sequestration of
organic carbon in soil via protection from decomposition within water-stable aggregates resulting
from earthworm castings (Bossuyt et al. 2005, Martin 1991). Finally, it is interesting to speculate
on possible changes in the pool of candidate invasive earthworm species that could result from
changing climate, altered land use patterns, and expanding global commerce. In addition to the
possible expansion of regional peregrines noted above, rapid adaptations (phenotypic and genetic)
among known invasive species should be considered as possible mechanisms that could acceler-
ate their spread into new habitats (Terhivuo & Saura 2006). Conversely, introduced species with
narrower temperature or moisture tolerances may become more restricted in distribution under
warmer or dryer conditions induced by climate change.

Molecular Approaches to Invasion Analysis

Molecular data applications to invasive earthworms have yet to take root. It is now possible to
use genetic markers to identify earthworm prey from the guts of predators (Admassu et al. 2006,
Harper et al. 2006a,Juen & Traugott 2006), and therefore to look at dietary shifts in predators after
the arrival of invasive prey. However, Harper et al. (2006a) mention that intraspecific earthworm
haplotype diversity was an impediment to prey identification.
Perhaps more important at this early stage is to improve identification of the earthworms
because there are many problems with the taxonomy of invasive species. Some invasive species
are known or suspected to be two or more genetically isolated lineages with little morphological
distinction, and there are cases of molecularly definable subspecific taxa within what we identify as
a single species. Eiseniafetida and E. andrei are nearly identical except for pigmentation pattern but
are isolated (Dominguez et al. 2005), and the former appears to contain a truly cryptic subspecies
or species (Perez-Losada et al. 2005). Lumbricus terrestris cytochrome oxidase I (COI) barcode
region sequences (Hebert et al. 2003) show the presence of two distinct groupings (T. Decaens,
B. Richard, and R. Rougerie, unpublished data). Allolobophora chlorotica has two color forms (pink
and green), each composed of two reproductively isolated, sympatric lineages with > 10% COI
barcode divergence (King et al. 2006).
Some invasive species contain many parthenogenetic lineages, and some have been named as
separate species (Gates 1972). In two cases so far lacking molecular data, the body size, tail setal
dimensions, and setal shape vary independently and widely in P corethrurus, and body size and
pigmentation vary widely in Octolasion tyrtaeum. In the latter, this variation seems to be related to
habitat. The common invasive Aporrectodea caliginosa is diploid (Omodeo 1955), and the similar,
but only quantitatively distinguishable, A. trapezoides is a parthenogenetic triploid (Mezhzherin
et al. 2007, Garbar et al. 2007) or tetraploid (Omodeo 1955). Often, certain sexual characteristics

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used in taxonomy are deleted or strongly modified in parthenogenetic lineages and are different
in what appear to be lineages of the same species. Where different clonal populations vary in their
properties as invasive agents, molecular data such as microsatellite DNA (Harper et al. 2006b,
Velavan et al. 2007) or the ITS region may be the best way to reliably distinguish among them.
To date, little has been done with earthworms in DNA barcoding, but this is changing rapidly.
The COI barcode region apparently works well to recover morphologically distinguished pre-
sumptive species as monophyletic groups (H. Chang, S. James, Y. Hong, H.-P. Shen, and J.-H.
Chen, unpublished data), although the interspecific divergences were higher than the norm among
metazoans and have shown cryptic species in Lumbricus terrestris and E. fetida. The preparation
of DNA extracts, COI PCR, and sequencing are completely routine for earthworms, so there
are no barriers to further progress in this area. For large numbers of specimens, costs are nearly
competitive with specialist time.

Policy and Economic Implications of Earthworm Introductions

The continuing introduction and spread of invasive earthworms seem inevitable, as public policy
has hardly dealt with the issue, despite the significant impacts on natural resources (Callaham
et al. 2006, Hendrix 2006, Hendrix & Bohlen 2002). However, a public education campaign
has proven somewhat effective in reducing introductions to not-yet-invaded areas [Great Lakes
Worm Watch Program (see http://www.nrri.umn.edu/worms/; also Callaham et al. 2006)].
Therefore, broad-scale public education about earthworms and the invasive earthworm issue may
have a considerable impact on new earthworm introductions. In addition to policy and educational
solutions, land management can influence the spread of invasive earthworms into soils with a native
earthworm fauna present. Strategies to optimize the biotic resistance capacity (sensu Hendrix &
Bohlen 2002, Hendrix et al. 2006) of native earthworms and their habitats should be identified
and developed. These may range in scope from intensive practices designed to mimic historical
disturbance regimes such as annual fire (e.g., Callaham et al. 2003) to simply allowing native
vegetation to recover following disturbance (e.g., Sanchez-de Leon et al. 2003).

CONCLUSIONS

Earthworms function as consumers, decomposers, modulators, and food resources for othe
mals (Edwards 2004, Lee 1985, Zhang et al. 2007). These functions operate at a range of s
scales from microhabitat to ecosystem and even to regional or global scales (Lavelle et al. 20
Introduction and invasion of exotic earthworm species into new habitats may extend these f
tions or alter existing processes. There is urgent need for more detailed field surveys world
to reveal the full extent of earthworm introductions and ultimately their impacts; collabor
international studies across continents and biogeographic regions will be needed to achieve
In addition to surveys, future research should focus on comparisons of characteristics of inv
and noninvasive species to elucidate mechanisms that might contribute to the invasiveness o
troduced earthworms. Modeling and molecular techniques will provide insights into many as
of earthworm invasion biology, from impacts on predator communities to the genetic unde
nings of the traits that determine invasiveness. Because of these future research directions, the
tremendous potential for earthworm invasions to function as a model system for invasion biolo

DISCLOSURE STATEMENT

The authors are not aware of any biases that might be perceived as affecting the objectivity of this
review.

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 ACKNOWLEDGMENTS

Development of this paper was supported in part by National Science Foun

0236276 to the University of Georgia Research Foundation, Inc., and DEB
0516439 to the University of Kansas; National Natural Science Foundation
No. 30630015 and No. 30771704; and International Foundation for Science gr
acknowledge helpful discussions with J. Blackmon, L. Dame, K. Mordecai, and
editorial assistance from A. Silletti.

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