Exotic Earthworm Invasions in North America: Ecological and Policy Implications

Earthworms are the best known and, in many situations, the most important animals that live in soil. Over 3500 earthworm species have been described worldwide, and it is estimated that further surveys will reveal this number to be much larger (Reynolds 1994, Fragoso et al. 1999). Distinct taxonomic groups of earthworms have arisen on every continent except Antarctica, and, through human transport, some groups have been distributed worldwide (Jamieson 1988, Reynolds 1994). The earthworm fauna of North America, including Canada, the continental United States, Mexico, and the islands of the Caribbean, consists of both native (Nearctic and Neotropical) and exotic species imported from many other regions of the world (Fender 1995, Fragoso et al. 1995, James 1995, Reynolds 1995). Any given locality may be inhabited by all native species, all exotic species, a combination of native and exotic species, or by no earthworms at all. Relative abundance and species composition of local fauna depend greatly on soil, climate, vegetation, topography, land use history, and especially on past invasions by exotic species. Much of our knowledge of the earthworm fauna of North America is based on the work of Gordon E. Gates who, over a 60-year career, collected, described, and cataloged many of the currently recognized taxa, both native and exotic. Beginning in 1949, Gates collaborated with the US Department of Agriculture (USDA), Bureau of Plant Quarantine (now Animal and Plant Health Inspection Service, or APHIS) to intercept oligochaetes found in “plant-associated materials” (mostly soil) being imported into the United States. Over a 32-year period (1950–1982), Gates (1976, 1982) acquired thousands of specimens and was able to determine that earthworms from all over the world were continually being imported. There is no reason to expect that this situation has changed since 1982. Indeed, as with exotic plants, fungi, and insects (Ruesink et al. 1995, Campbell 2001, Mack and Lonsdale 2001), growing global commerce may be increasing the likelihood that exotic earthworms will be introduced, both inadvertently with the importation of soil-containing materials (e.g., agricultural and horticultural products; Gates 1976, 1982, Boag and Yeates 2001, Ehrenfeld and Scott 2001) and intentionally for use in commercial applications (e.g., waste management and land bioremediation; Lee 1995, Edwards 1998). Because previous invasions by exotic earthworms have had significant impacts on soil processes and plant communities in native ecosystems (e.g., Alban and Berry 1994, Groffman and Bohlen 1999, Hale et al. 2000), there may be reason for concern over continued unrestricted importation of earthworms. Regulatory activities have not been effective in reducing earthworm introductions in most areas of the world (Boag and Yeates 2001), probably because legal restrictions traditionally have not targeted earthworms or their propagules. There presently are no specific regulations concerning earthworm imports into the United States. Earthworm importations are regulated by APHIS under the Federal Plant Pest Act because of the potential for introduction of exotic plant pathogens in their guts and in soil that might accompany them (Tracy A. Horner, USDA APHIS, personal communication, 3 January 2002). The recent outbreak of foot-and-mouth disease in Europe has heightened concern about earthworm imports, because some species may be vectors for that viral pathogen and others (Edwards and Bohlen 1996, Jamieson 2000). APHIS is now considering guidelines specifically for the importation of earthworms into the United States. In this article, which is derived from a report prepared recently for APHIS, we review the status of earthworms in North America, address problems associated with exotic earthworm invasions, and discuss criteria for assessing potential risks of earthworm importation. Native earthworms in North America Earthworms are classified within the phylum Annelida, class Clitellata, subclass Oligochaeta, order Opisthophora. According to Jamieson (1988), there are 16 families worldwide (table 1). Six of these families (cohort Aquamegadrili plus suborder Alluroidina) comprise aquatic or semiaquatic worms, whereas the other 10 (cohort Terrimegadrili) consist of the terrestrial forms commonly known as earthworms. Two families (Lutodrilidae and Komarekionidae, both monospecific) and genera from three or four others (Sparganophilidae, Lumbricidae, Megascolecidae, and possibly Ocnerodrilidae) are Nearctic (Jamieson 1988, James 1995). No native earthworms have been reported from Canada east of the Pacific Northwest or from Alaska or Hawaii, although exotic species now occur in all of these regions. Native earthworms in the families Ocnerodrilidae, Glossoscolecidae, and Megascolecidae occur in Mexico and the Caribbean islands. Fragoso and colleagues (1995, 1999) discuss native and exotic earthworms in the south Nearctic and north Neotropical regions. In this article, we focus on the Nearctic region north of Mexico. Pleistocene glaciations are thought to have eliminated the earthworm fauna from most of Canada and the northern portion of the continental United States (Gates 1970). The southern limits of defaunation at the peak of the Wisconsinan glaciation may have extended to the edge of permafrost, a significant distance beyond the ice terminus (Gates 1970, Pielou 1991). Glacial refugia apparently remained along the Pacific Coast, where a number of native genera in the families Mega scolecidae and Sparganophilidae now occur (Fender and McKey-Fender 1990, Fender 1995), and in the eastern United States, where all of the other Nearctic groups occur (figure 1; Gates 1982, James 1995). Colonization of previously glaciated areas was apparently slow, and few native earthworms inhabited northern regions of North America at the time of European settlement (Gates 1967). Approximately 70 species of native earthworms have been described from the eastern United States and another 28 species from the Pacific region (table 2). An isolated group of megascolecids has recently been described in southern California, possibly as a relict of previously more widespread groups (Wood et al. 1997). With further surveys, more species will very likely be described in all of these regions (James 1995). North America thus has a rich and diverse indigenous earthworm fauna, which probably reaches its highest species diversity and exerts its greatest influence on soil processes in forest and grassland ecosystems (Fender 1995, Fragoso et al. 1995, James 1995, Kalisz and Wood 1995, Hendrix 1996). Remnants of native ecosystems in unglaciated areas have shown the most pristine communities of native earthworms, but the relative importance of these species in disturbed and intensively managed ecosystems has received little study. Habitat alteration and introduction of exotic earthworms may have reduced the abundance and ecological importance of native species. Exotic earthworms in North America In addition to the 100 or more native earthworm species in North America north of Mexico, at least 45 exotic species have been introduced (Gates 1976, 1982, Reynolds 1995). Exotics include European Lumbricidae (25 species); African (2 species), Asian (14 species of the “pheretimoid” group), and South American (2 species) Megascolecidae; African Eudrilidae (1 species); and South American Glossoscolecidae (at least 1 species) and Ocnerodrilidae (2 species). It is possible that other species, including some from other families, have been introduced but not yet reported in the literature. As with insect introductions into North America (Simberloff 1989), the preponderance of European species of earthworms is probably due to habitat similarities in these generally temperate regions and to historically high levels of commerce between them. European Lumbricidae are the most common exotic earthworms north of the glacial margins, and several species have become notorious for their effects on forest floors in northern forests formerly devoid of earthworms (Alban and Berry 1994, Scheu and Parkinson 1994, McLean and Parkinson 1997, Hale et al. 2000). The Asian megascolecid (Amynthas sp.) also is invading forests in the northeastern United States (Steinberg et al. 1997, Burtelow et al. 1998, Groffman and Bohlen 1999). Most of the nonlumbricid exotic species in North America occur in the southeastern and Pacific regions of the United States. In general, exotic earthworm distributions are patchy across the continent and appear to overlap with distributions of native species. There is debate as to whether exotic earthworms displace native earthworms in undisturbed habitats (Kalisz and Wood 1995). Ecological considerations Earthworms occur in a wide range of habitats where soil water and temperature are favorable for at least part of the year; across this range, they display a variety of adaptations to environmental conditions. Even in unsuitable regions, earthworms may inhabit local microsites where conditions are favorable (e.g., urban gardens, desert oases), especially if well-adapted species have been introduced. Within habitats, earthworms often show clumped spatial distributions that correspond to such factors as vegetation, soil texture, or soil organic matter content. Feeding behavior, in particular, dictates horizontal and vertical distributions of earthworm species within a soil volume and determines their effects on soil Ecological of earthworms. earthworm species a or may at a given by in the soil. from a variety of or adaptations et al. and species inhabit and on and of and and species inhabit soil within the and and species on but in in the soil (table these activities influence earthworm species soil species the and of species into the soil and and water through their vertical Edwards and Bohlen 1996). the ecological of species is to their potential effects on soil processes and on other effects of earthworms. over effects of exotic earthworms to the of earthworms being to was the to show that earthworms influence soil processes important to the of terrestrial in agricultural and has shown that earthworms often have favorable effects on in under management (e.g., no Earthworm has been reported to of plant and plant soil and and water and Lee Hendrix 1995, Edwards and Bohlen 1996, Edwards 1998, et al. 1999). earthworms are of through their be for to of have been reported to over in earthworm in managed grassland have shown that earthworm in in and in in the et al. and in in 1997). effects of earthworms on plant may about through and water of that plant or possibly through of that plant (Edwards and Bohlen 1996, et al. 1999). Earthworms and their activities have been to a number of including of organic through which has become a in North America (Edwards 1998, et al. of earthworms as of Lee 1995, Edwards and Bohlen and or of earthworms for which has a in the United States and Canada (Edwards and Bohlen 1996). are for much of the commercial of earthworms and a few species to and often introduced into in the families Lumbricidae, Glossoscolecidae, and of these species are now in North America, in or as in the commercial also appear to be the of for importation of exotic earthworm species (Tracy A. Horner, USDA APHIS, personal communication, 3 January 2002). effects of earthworms. the many and effects of earthworms on soil and plant some of earthworm activities are (Edwards and Bohlen 1996, et al. 1998, et al. 1998). activities include and of which soil from that and increasing of on the of and where they are a in and agricultural plant or them able to increasing of soil through and and increasing of soil through It is the of and effects of earthworms that determines whether they have impacts on ecosystems et al. 1998). such as of organic and soil may be in (e.g., urban and in another (e.g., native The impacts of exotic species are to assessing the risks associated with their introduction and of exotic earthworms The about exotic earthworms have been the potential for species to habitats and, the effects they may have on other and soil processes within habitats (Alban and Berry 1994, et al. 1998, Hale et al. 2000). Exotic earthworm As for many other exotic species (e.g., 1996, Mack and Lonsdale 2001), the for the introduction of exotic earthworms into areas has been through human and commerce over the past several (Gates Lee introductions were probably earthworms may have been in soil from or in imported plant more earthworms have also been imported and distributed there is a potential for exotic earthworms to become and they are or to into the or not they become on such as the of they and their effects on soil processes or other species. In North America, the most effects of exotic earthworm invasions on soil processes have been in areas previously devoid of earthworms (e.g., north of Pleistocene glacial Gates of exotic earthworm effects on soil In introduced soil to a of 1 over a in South in the soil in a forest in Canada, were by introduced and a significant effects of exotic earthworms on soil on and organic matter on other soil or on plant communities have been reported in in southern and Wood in (James et al. temperate forests in (Alban and Berry 1994, Hale et al. 2000), (Steinberg et al. 1997, Burtelow et al. 1998, Groffman and Bohlen et al. and Canada and Parkinson 1994, McLean and Parkinson 1997). effects of exotic earthworms in terrestrial ecosystems have also been reported in other of the world 1982, et al. Lee Edwards and Bohlen 1996, Edwards 1998, et al. 1999). In most of these exotic earthworms apparently were introduced inadvertently at some time in the past and effects over a period of to In several species of European across the forest by by and by species apparently into the forests from over several they were as et al. 2000). effects on soil processes have been reported for a of European in with exotic plant species introduced into in et al. 1999). of these situations, in which exotic species by are of described by and or the time of there has been debate over by which exotic earthworms become in ecosystems In many of the exotic species ecosystems previously devoid of earthworms. In areas inhabited by native earthworms, exotic invasions often are by of or (e.g., Kalisz and Fragoso et al. 1995, 1999, and 1999). of native earthworms by exotic has been little of this be Kalisz and Wood four in the of exotic earthworm in inhabited by native habitat or of native introduction of exotic species, and of by exotic species. Even in the of habitat some habitat may be to native earthworm and potential vectors for by exotic species into may to of native (Kalisz and Wood 1995). as with other exotic species the for of native earthworm is to be habitat alteration although the relative of these factors to be the most effects of exotic earthworms on soil processes have not been reported from areas inhabited by native earthworms, where and are In some where invasions have native species have remained over exotic species et al. 1995, 1999, and 1999, et al. 2000). In forests in native earthworms occur in undisturbed or disturbed whereas exotic species occur in disturbed (Kalisz and that the European forest inhabited by native megascolecid earthworms in South et al. 1998). of of European into a in of native by exotic in disturbed areas but continued of the native species under conditions. It has been that native earthworms are invading European to local soil and conditions and of and effects on in (James and 1999, et al. that earthworm fauna or of their native habitats or both may be to by some exotic earthworm species and, may the of exotic species on soil The of (Simberloff in the of earthworm invasions further Exotic earthworms as disease There have been of earthworms as or as Edwards and Bohlen 1996, Jamieson 2000), which the concern that exotic earthworm introduction be a for the introduction of pathogens into The most given the recent outbreak of foot-and-mouth disease in is a report of a of that disease by Edwards and Bohlen 1996). was in a where the remained for 3 to by the that as a and for the disease under conditions. some of human of and by apparently derived from earthworms not have been and pathogens by earthworms include and of and and and of and Edwards and Bohlen 1996). Earthworms also have been reported to and plant including of and and of plant (e.g., The most earthworm species have been European A. but megascolecid also the of a pathogen Edwards and Bohlen 1996). there are that earthworms the of and the of of of as as in the through soil of disease or in (Edwards and Bohlen 1996, and and also that might be earthworm there are no reported between exotic earthworms and the introduction of significant the potential for pathogens to be by earthworms of to such risks of exotic earthworm invasions the of earthworm invasions is because there is no of impacts and because the between ecological processes and are Much of the on invasions by terrestrial has on that have become important Because of their high and a number of insect have shown and have become the of and (Simberloff of soil has not been as and Scott 2001), with the of some and species of by more and soil fauna appear to be and from of other and may be more to plant invasions to of other animals 1991). by terrestrial (Boag and Yeates 2001) may be the best for and earthworm invasions because of similarities between these groups with to history, and of earthworm species importation. It is to which species in taxonomic group of animals or will be or to common to that have been (Simberloff 1996, Mack et al. 2000). In the of earthworms, most of the and in 3 be found in at least some species. of species of species. and are in and temperate whereas their and appear to be much possibly because they have not been as introduced or they are not as to a wide range of environmental conditions. of have been (e.g., high of and high abundance and wide range in native taxonomic or of in but many of these are to determine or not in some about species, concerning habitat and previous at may be in criteria for earthworm importation (Simberloff et al. 1995, 1996, Mack et al. 2000). is a of of introduced of of a species in a with increasing of the introduced with increasing of or In addition to a high introduction may the likelihood of into a ecological of earthworms may their including (e.g., and and of both of which to conditions. a number of earthworm species display or a that may the of Fragoso et al. 1999). high or introductions of species with high may a high of if the habitat is Habitat to conditions in the habitat of relative to of or areas of As a species that a wide range of environmental in their native habitats are likely to be more as species with more environmental 1996). Earthworm species from northern (e.g., European and some Asian are in or in temperate and continued and widespread introduction the United States, the commonly in is not often found in habitats in the southern United States. and both now distributed the apparently have not become in habitats in the continental United States where they have been introduced, with the of in south (Gates 1970, 1982, Fragoso et al. 1999). of with specific may be based on about or of introduced species (table these may not be of they be in the of effects exotic earthworm may have if it is into in Canada, the exotic the and of soil in a forest and Parkinson whereas a combination of and species the forest to a of to in forests in (Alban and Berry 1994, Hale et al. 2000). at may be of the of a potential to habitats, at least for the earthworms. There are of earthworm invasions the and a number of species are known to have wide distributions beyond their of in and temperate regions, because of their to and become in a wide variety of Lee that there are about 100 such all families and by of the earthworm species and some of their ecological are in criteria for assessing earthworms. Any of these habitat or previous at is not to the potential of earthworm species. these are to and ecological of invasions and not to the that earthworms may be vectors of of are in 1 as criteria for assessing and potential of exotic earthworms. criteria a of by and colleagues of for earthworm species which species may high potential if introduced into but it is that all of the will be for all introduced species. In the of might be to the of as much as possible (Ruesink et al. 1995), which be and by or others with earthworm invasions to the a of which is in the but in and or and of a with on habitat previous disease and on be a of such for some of the known species. a also Exotic earthworms have been introduced into most regions of the world through human commerce over the past few species were probably introduced and there was of potential possibly knowledge that importation was As a importations of earthworms were not as the impacts of importations have become have regulations been No As regulations to earthworm importation into the United States are based on the Federal Plant Pest under which APHIS imports soil that might In the of it that earthworm species may be that there is no specific of earthworms as is which has been as introductions of species risks have not yet been (Ruesink et al. 1995, Mack et al. 2000). With no in this it likely that invasions by as as species will considering 1982) that exotic earthworms are being introduced continually into the United States from many areas of the introductions also the of introduction of pathogens by earthworms imported from regions. importation of earthworms. importation of earthworm species the of possibly to that for of terrestrial invasions in and et al. 1998). In Canada, earthworms be imported from the and the United States species that are known to occur in a or and 1997, Mack et al. be on a with by to that species are imported. It be under this to have of both and species of earthworms. most likely ecological risks of by species known to be but on other species, it not that for importation not become this may not the risks of pathogen which occur through earthworms. restrictions on imported earthworms. importation of earthworms and earthworm materials as as such as of all materials importation in is in and and in the might include of and of with no soil in their be to in use for importation and of and (Ruesink et al. 1995). a probably the risks of disease importation earthworms may be and 1999) and the risks of exotic earthworm on imported earthworms. be to greatly the risks of introduction of and of invasions by exotic species. Earthworm have to on species in North Because many exotic species are this may not be on earthworms for and it might of native and and of possible of native earthworm species. a importation might also on earthworms or oligochaetes in and of earthworms (e.g., waste this might include for earthworms for or a be to with to introductions of earthworms or in horticultural or agricultural range of for earthworm importation is combination of of importation and might a of continued commerce in and of a may be on to importation of earthworms from with pathogens known or to be by earthworms (e.g., foot-and-mouth probably is for exotic species with the highest as with many other groups of (Simberloff Mack et al. 2000), more knowledge is of the and of earthworms in their native habitats and in ecosystems where they have and had significant factors their under native of the and of the habitats have to invasions and to important is which may occur in ecosystems inhabited by native native species with exotic species under native habitat a to and are to these and other there is a for and taxonomic work to the diversity and of native earthworm species, some of which may be to exotic invasions (James 1995). of local invasions and of have received little As activities of earthworms are often in agricultural and there probably be little to exotic species or them with native species in The focus be on invasions from such areas into ecosystems where exotic species are to have of exotic earthworms from soil is not likely to be on a but possible to further such as of unsuitable habitat which might be In addition to on importation at regulations at and or levels may be to of exotic earthworms into or by and groups (e.g., are in of problems associated with earthworm invasions in such and the of this are to Hale and Lee Department of of for and about exotic earthworm invasions in northern and to for about regulations in work was by from the Animal and Plant Health Inspection Service, under the of Horner, and from the families of and their regions of and estimated of species of native earthworms in North America, north of Mexico. Ecological and of earthworms. of some earthworm species now distributed beyond their regions of Most are with high and distributions of Nearctic earthworms in eastern and Pacific regions of North America in to Wisconsinan glacial areas of 100 species, some and some with very Fender Fragoso and colleagues James and Reynolds for

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