Biol Invasions DOI 10.1007/s10530-006-9016-6

ORIGINAL PAPER

Policy and management responses to invasions in

Mac A. Callaham Jr. Æ Grizelle Gonza´lez Æ Cynthia M. Hale Æ Liam Heneghan Æ Sharon L. Lachnicht Æ Xiaoming Zou

Ó Springer Science+Business Media B.V. 2006

Abstract The introduction, establishment and and functions associated with above- and spread of non-native earthworm species in North belowground foodwebs. However, many areas of America have been ongoing for centuries. These North America have either never been colonized introductions have occurred across the continent by introduced , or have soils that are and in some ecosystems have resulted in con- still inhabited exclusively by native earthworm siderable modifications to ecosystem processes fauna. Although several modes of transport and subsequent proliferation of non-native earth- worms have been identified, little effort has been made to interrupt the flow of new species into new areas. Examples of major avenues for introduction of earthworms are the fish-bait, M. A. Callaham Jr. (&) horticulture, and vermicomposting industries. In USDA Forest Service, Southern Research Station, this paper we examine land management prac- 320 Green Street, Athens, GA 30602, USA e-mail: [email protected] tices that influence the establishment of intro- duced species in several ecosystem types, and G. Gonza´lez identify situations where land management may USDA Forest Service, International Institute of be useful in limiting the spread of introduced Tropical Forestry, 1201 Ceiba Street, Rı´o Piedras, PR, USA earthworm species. Finally, we discuss methods to regulate the importation of earthworms and C. M. Hale earthworm-containing media so that introduction The Natural Resources Research Institute, University of new exotic species can be minimized or of Minnesota, Duluth, MN, USA avoided. Although our focus in this paper is L. Heneghan necessarily North American, many of the man- DePaul University, Environmental Science Program, agement and policy options presented here could Chicago, IL, USA be applicable to the problem of earthworm S. L. Lachnicht invasions in other parts of the world. USDA Agricultural Research Service, Morris, MN, USA Keywords Biological invasion Æ Quarantine Æ Biogeography Æ Earthworms Æ Lumbricidae Æ X. Zou Institute for Tropical Ecosystem Studies, University Megascolecidae Æ Glossoscolecidae Æ Introduced of Puerto Rico, 23341 San Juan, PR, USA species Æ Exotics

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Patterns of earthworm invasion slow, and the southern boundary of the glacial ice in North America sheets still provides an approximation of the northern extent of native earthworm distributions The present-day biogeographical distributions of (Fig. 1). earthworms in North America are the product of More recent, but no less profound than the two dramatic events in relatively recent geologic effects of glaciation, have been the effects of hu- time. The first of these events was the Wiscons- man colonization on the biogeographical distri- inan Glaciation ending about 12,000 years BP, butions of earthworms in North America. The and the second was the rapid colonization of the human mediated changes in earthworm biogeog- continent by humans of European origin begin- raphy are the focus of this paper. There have been ning about 400 years BP. three general manifestations of these effects. The principal effect of the Wisconsinan glaci- First, and perhaps the most important factor ation was to influence the distribution of the affecting current distributions of exotic earth- native North American earthworm fauna, with worm species, is the historic transport of exotic total extirpation of earthworms from soils directly earthworms via human activities associated with affected by ice sheets and permafrost. Since the European settlement and the continued spread of recession of the glacial ice sheets, climatic factors introduced species by the use of earthworms as a have been the primary drivers in the distribution commodity, as in the fish-bait and vermicompo- of native earthworm fauna, with major refugia for sting industries (Edwards and Bohlen 1996; Ed- native earthworms developing in wet and humid wards and Arancon 2004). Second, international regions of the continent such as the Pacific commerce involving horticultural materials has northwest, the southeastern US, and parts of been identified as a source of propagules for new southern California and Mexico (Gates 1966; earthworm species (Gates 1982; Hendrix and James 1990, 1995; Fender and McKey-Fender Bohlen 2002). Finally, soil disturbances associated 1990; Fragoso et al. 1995). Recolonization of with agricultural development, logging or other formerly glaciated soils by native species has been perturbations appear to be associated with

Fig. 1 The southern extent of the Wisconsinan Glaciation (bold line), and approximate present day distributions of native earthworm species in North America (hatched area). Redrawn from Hendrix and Bohlen 2002

123 Biol Invasions successful establishment of introduced earth- predictive variables). One important geographical worms in some areas (e.g. Kalisz and Dotson distinction in the patterns of earthworm invasion 1989; Gonza´lez et al. 1996; Zou and Gonza´lez and establishment involves the presence or 2001; Callaham et al. 2003) due to changes in soil absence of a native earthworm community (see physical and chemical properties, net primary Fig. 1). Whereas establishment of exotic earth- productivity, and plant litter chemistry (Fig. 2). worm species often appears to be less successful Taken together, these three factors provide cri- in soils where native earthworm populations and/ teria by which we can make informed predictions or native vegetation is intact (Kalisz and Dotson about the likelihood that a site will become 1989; Callaham et al. 2003; Zou and Gonza´lez inhabited by non-native species (i.e., distance 1997; Sanchez et al. 2003; Hendrix et al., this from roads, agricultural fields, waters frequented issue), it is clear that soils without a native by fishermen, or human habitations are good earthworm fauna are susceptible to invasion and

Fig. 2 Conceptual model depicting hypothesized linkages mixture of native species and exotic species with uncertain between land use, vegetation change, earthworm commu- biogeochemical properties. Evidence suggests that intro- nity change, and changes to soil properties (based on duced earthworms contribute to the movement of soil Gonza´lez et al. 1996). These interactions are seen to have ecosystems toward altered states that are not likely to revert two eventual outcomes in the event of land abandonment to the native condition. Indeed, introduced earthworms can and restoration through natural succession or other means. be the primary drivers of such changes even in the absence The first is a return to the native state with a full of large disturbances, as has been observed in soils complement of native species of plants and (in this previously devoid of native earthworms (see text for case soil invertebrates, including earthworms), and the examples) second is transition to an altered state consisting of a

123 Biol Invasions introduced earthworms are able to establish even soil horizonation (Scheu and Parkinson 1994; in pristine, undisturbed areas (Dymond et al. McLean and Parkinson 2000a, b). Further, intro- 1997; Bohlen et al. 2004; Hale et al. 2005; Frelich duced European earthworms play an important et al., this issue). role in litter decomposition in aspen forests in the Rocky Mountains of Colorado, USA (Gonza´lez et al. 2003). Similarly, in undisturbed sugar maple Ecological effects of introduced earthworms forest soils of New York, recent work has shown that introduced European earthworms of several The question of whether policy and procedures species had effects on forest floor structure, dis- are needed to manage the introduction of new tribution of microbial biomass, soil C storage, species of earthworms may be best answered by phosphorus cycling and fine root distributions an analysis of the ecological and economic risks (Bohlen et al. 2004; Groffman et al. 2004; Sua´rez associated with such introductions. Earthworms et al. 2004; Fisk et al. 2004). are widely considered to be ‘‘good’’ for soil by the In the north temperate forests of Minnesota, general public, and are usually suggested to be invasions of European earthworms resulted in beneficial for soil fertility and other soil charac- dramatic changes to soil structure; these changes teristics. Indeed, earthworms have frequently were associated with declines in soil nutrient been purposely introduced to soils with the availability, as well as declines in diversity and objective of soil improvement in agricultural set- abundance of tree seedlings and herbaceous tings (Baker 2004), and in soil reclamation pro- plants (Hale et al. 2005). Also in Minnesota, one jects (e.g., Butt et al. 1999; Curry and Boyle 1995; study linked the local extirpation of populations of Baker et al., this issue). Nevertheless, in spite of a rare fern, Bostrychium mormo, with the pres- the beneficial effects usually associated with ence of the introduced earthworms Lumbricus earthworms, it has also long been proposed that rubellus and Dendrobaena octaedra (Gundale earthworms are undesirable in certain situations. 2002). In this study, the dramatic changes in forest For example, Walton (1928) tested several floor structure associated with the mixing activity chemical treatments for control of unwanted of the epigeic and epi-endogeic earthworms was earthworms on golf courses where the castings of implicated in the destruction of appropriate earthworms interfered with smooth play on the habitat for the fern. putting greens. Later, Stebbings (1962) suggested The effects of earthworm introductions into that interactions between native and introduced ecosystems where a native earthworm assemblage species could be leading to the competitive is already present are less well known, but some exclusion of native earthworm assemblages. work detailing differences between the ecological However, only recently have there been thorough roles of native and introduced earthworms has assessments of the effects that introduced earth- been reported. In tropical forests of Puerto Rico, worms can have on ecological properties and the introduced species Pontoscolex corethrurus processes in natural systems (Fig. 2). The most increased rates of litter decomposition and CO2 dramatic of these effects was observed in areas efflux from the forest floor relative to rates that had previously been devoid of any earth- observed in the presence of native species alone worm fauna (i.e. areas north of Pleistocene glacial (Liu and Zou 2002). Also in Puerto Rican soils, margins; Frelich et al., and Tiunov et al., this native and introduced earthworm species had issue). differential effects on soil processes such as In the aspen and pine forests of Alberta, nitrogen mineralization and microbial respiration Canada, where the European earthworm Dend- (Gonza´lez et al. 1999; Lachnicht et al. 2002). In robaena octaedra was accidentally introduced, the the North American tallgrass prairies of Kansas, influence of this earthworm on the forest floor non-native earthworms were dormant during the was dramatic in terms of microbial characteristics, summer growing season, whereas native species changes in the community of other invertebrates, remained active, suggesting that the influences on changes in nutrient cycling, and even effects on soil processes of the different species are different

123 Biol Invasions depending on season, and may have important not broadly agreed upon. Although there is a implications for nutrient cycling in the system virtual consensus among ecologists on the risks (Callaham et al. 2001). Other examples of eco- associated with unchecked proliferation of logical impacts of introduced earthworms on invaders, public awareness of these problems is native assemblages are discussed by Hendrix more limited (Colton and Alpert 1998) and this et al., this issue. severely limits the political will to act. This problem is exacerbated when considering earth- worms as potential pests since the general Control of earthworm invasions perception is that earthworms are ‘good’. Fur- thermore, policies limiting the sale or distribution Policy context of non-native earthworms (or earthworm- containing materials) have the potential to result Increasingly, environmental policy has been in negative economic impacts for people involved developed in a context of formal risk analysis. in these trades, and as such, should be expected to Development of ‘‘rational policy’’ is possible meet with strong opposition. Crafting and when a problem is well defined, complete infor- implementing effective policy in this circumstance mation regarding risk is available, a range of depends upon promoting a more balanced and policy alternatives has been assessed, and the scientifically informed view of the effects of non- goals of the policy are agreed upon (Fiorino native earthworms on ecosystems. 1995). That is, in such circumstances, a theoretical Cost-benefit analysis has been promoted as a benign autocrat could weigh the pros and cons of useful economic tool to serve as the analytical a given situation and create uncontroversial and basis for policy (Patton and Sawicki 1993). Con- effective policy. Situations where the ‘‘rational ceptually, assessing both the negative and positive policy’’ model is applicable are rare. impacts associated with decisions is straightfor- In the case of developing strategies to mitigate ward. However, cost-benefit evaluation is analyt- problems associated with invasive earthworms, ically complex. Commonly, the approach is based none of the aforementioned conditions for a upon incremental costs, that is, the cost associated simple rational policy approach are adequately with moving to a new (usually more stringent) met. First, the problem is multifaceted and eludes level of control. In the case of policy regarding simple definition—that is, the problem can be earthworm invasions, there are currently no spe- stated as one concerning biodiversity decline, cific controls, so an assessment of marginal cost of harm to critical ecological services, loss of aes- going from no regulation to regulation is difficult thetic value (e.g., loss of native species), and to assess. Moreover, as is the case in most policy impairment of recreational opportunity (e.g., development associated with ecological risks, a earthworms damaging putting greens, or limiting subset of the objectives has a moral basis. That is, the use of non-native earthworms for fishing bait). although there are clear economic benefits asso- Secondly, although research on this topic has ciated with conserving species threatened by become more intensive in recent years, the con- invasive earthworms, not all of the motivation for clusions are not definitive and the risks associated limiting invasive earthworm damage is based with earthworm invasion are not thoroughly upon utility. Conservation is also based upon a understood or quantified for all species and all sense of responsible stewardship. Addressing potentially impacted ecosystems. Thirdly, policy policy alternatives to halt biodiversity decline alternatives have yet to be fully developed and may therefore not be a tractable problem for their efficacy is untested. Development of policy economic cost-benefit analysis to arbitrate alternatives awaits the outcome of a number of (Roughgarden 1995). Nevertheless, a quantitative different research programs which should evalu- and explicitly monetary assessment of policy ate the effectiveness of eradication, control, and decisions regarding earthworm invasion may still management of invasions. Finally, the goals of prove to be useful. Additionally, when perform- policy formulation for invasive earthworms are ing such an assessment, it is critical to consider

123 Biol Invasions that benefits of conservation accrue over the long however, knowing which introduced and natu- term, whereas costs associated with regulation ralizing species to target for eradication is made and management are both immediate and ongo- problematic by our limited ability to predict ing. Depending upon the discount rate used in which subset of introduced species will launch evaluating cost and benefit accruals stemming major ecosystem-modifying invasions (Williamson from conservation policy, investing in conserva- 1996). In the case of earthworms a systematic tion can seem unattractive to decision-makers evaluation of which earthworm species may have (Krautkraemer 1995). Therefore, creative incen- the greatest impact, and which ecosystems are tive schemes may be needed to make the benefits likely to be most impacted, will allow informed arising from seemingly esoteric policy (such as development of effective eradication and control regulation and management for invasive earth- strategies. worms) appear more attractive. Incentives are Finally, when an invader is expanding rapidly also crucial to make the benefits credible to those or has reached a saturation point in the invaded organizations and individuals who bear the costs systems, eradication is usually not the most fea- of implementing the policy. sible alternative. In this case, control of the spe- cies through land management practices or other Control by stages of invasion large-scale remediation of the damage caused by the species is most likely to be effective. In developing effective approaches to minimizing Below, we evaluate regulation and control the risks associated with invasions it is useful to strategies for earthworm invaders. This includes recognize a variety of stages associated with the discussion on regulating the importation or phenomenon of invasion. These include intro- movement of soils containing earthworm propa- duction, establishment, expansion, and saturation gules and discussion on the role of the manage- by an invader (Shigesada and Kawasaki 1997). ment of site disturbances in influencing the Each of these stages will require a different policy impact and spread of introduced earthworms. approach to be most effective. Arguably, the lowest cost associated with con- taining a major invasion is prevention, that is, Regulation of earthworm-containing materials regulation of materials deemed to harbor a potential invader. However, since not all intro- Regulation of other soil dwelling organisms duced species will mount a large-scale invasion (Williamson 1996) it would clearly be onerous and Regulation of soil-borne organisms has been prohibitively expensive to quarantine or restrict standard practice in the USA and Canada for all such importations. Therefore, a mechanism for many years, in an attempt to limit introductions or assessing risk associated with particular introduc- to control spread of agricultural or other plant tions has considerable value. Most of these pests. Examples within the USA include the root predictive tools are qualitative and based upon knot nematode (Meloidogyne spp.), soybean cyst expert assessment (Reichard and Hamilton 1997), nematode (Heterodera glycines), and the imported though some are quantitative (Kolar and Lodge fire ants (Solenopsis invicta and Solenopsis rich- 2002). Below we recommend an assessment teri). There is a full list of regulated organisms for approach suitable for peregrine earthworms. Canada as well (see http://www.inspection.gc.ca/ Approaches that attempt eradication or con- english/plaveg/protect/dir/d-00-04e.shtml). All of trol at the stage of establishment can be poten- these organisms are subject to some form of tially cost-effective. For instance, if one considers quarantine when propagules of the organism are the probable costs associated with containing the detected in materials flowing into an uninfected gypsy moth in Medford, Massachusetts in the region. For example, in the case of fire ants in the 1860s, relative to the current and ongoing costs of southern USA, soil may be transported from areas controlling this insect invader, the cost-benefits of that have been infested into areas not infested early intervention seem obvious. Once again, only when the destination is a laboratory that has

123 Biol Invasions been issued a special permit to receive such soils. certain behavioral, physiological, or reproductive In all other cases, soil or equipment originating characteristics that cause certain earthworm spe- from infested areas must be certified to be free of cies to be of particular concern in terms of eco- fire ants, farming implements or earthmoving logical risk associated with introduction. equipment must be cleaned of all soil capable of Likewise, the locality into which species are transporting fire ant propagules (USDA 2004), introduced may have much to do with the success and horticultural materials must be certified to be or failure of new species introductions. One ant-free before shipment to non-infested regions example of the influence of habitat matching is can be made. Measures of this type could easily be the case of the African earthworm species adapted for use in the regulation or limitation of Eudrilus eugeniae which is adapted to tropical transport of earthworm propagules from place to lowlands. Although this species has been suc- place within North America. cessfully cultured for sale in the fish-bait industry across the USA and Canada, there have been no Regulation of earthworms through policy published records of this earthworm existing anywhere in temperate North America outside Given the long time-frame and wide geographical the controlled environments found in gardens and extent of earthworm introductions across North culture beds (Gates 1970; Reynolds 1994a, b). America and the globe, it may be tempting to However, this species has been reported from subscribe to the opinion that it is too late for any natural systems in the American tropics (Puerto regulatory action to have meaningful results. Rico) where it may present serious ecological However, the most recent work to address this risks to native earthworm communities or eco- issue quantitatively (Gates 1982) indicates that system properties (Borges and Moreno 1994; G. the rate at which new species are introduced has Gonza´lez, personal observation). Thus, it is clear increased with the increase in international trade that regulation of material containing earthworms in materials that may contain earthworms or could be unnecessary and counterproductive in earthworm cocoons. These observations were certain cases, but it is equally clear that each case based on collections made at USDA agricultural should be examined carefully before the intro- inspection stations where materials from around duction of a new species is allowed; i.e., the pos- the world were examined for presence or absence sibility of widespread colonization should not be of earthworms. Furthermore, there still exist large left to chance. areas of the North American continent that have Here, we propose one potential decision-making yet to be invaded by exotic earthworms, and the tool with regard to handling of earthworm- potential ecological effects of invasion of these containing media at inspection stations where the areas are not well known (Hendrix and Bohlen destination may be sensitive to the importation of 2002). new earthworm taxa (Fig. 3). Formalized decision- For nations where no importation guidelines making processes such as the one proposed could exist, regulatory actions for dealing with the po- be a helpful alternative to the ad hoc requests for tential introduction of new species of earthworms guidance regarding earthworm importations range from ‘‘do nothing at all’’ to ‘‘do everything sometimes sought by regulating agencies. This possible’’. In practice, a resolution to ‘‘do some- decision-making process allows for the quarantine thing effective and efficient’’ is likely the most of materials containing propagules of earthworms desirable outcome. Decisions about whether and that have not been identified or widely introduced how to regulate the introduction of earthworms previously. These quarantines would provide time must be based upon the best information avail- to determine the ecological risk posed by the able about the ecological characteristics of the introduction of a given earthworm species into earthworm species in question and the suscepti- particular systems. Suggested types of information bility of invasion for the ecosystem where the needed to determine ecological risk associated exotic earthworm will be introduced (Hendrix with a quarantined earthworm species are listed in and Bohlen 2002). For example, there may be Table 1.

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Fig. 3 A prototype decision tree for regulation of earthworms or earthworm-containing media. The initial box represents a source of earthworms or earthworm cocoons, with the ideal scenario being that potential sources (horticultural materials or other soil cargos) could be certified as ‘‘worm-free’’, resulting in no regulatory action

Whereas areas supporting both native vegeta- impact of human activity is related to the proba- tion and native earthworm communities may bility that such activities may transport invasive possess a certain level of resistance to exotic earthworm species. Given these general obser- earthworm invasions (Hendrix et al., this issue), vations, when decisions are made about impor- areas without a native earthworm fauna may be tation of earthworm-containing materials special particularly susceptible to invasions whether the attention should be directed toward areas where native vegetation is intact or not (Hale et al. 2005; no earthworms (native or exotic) are currently Frelich et al., this issue). In these areas, the present, where human activities with a high

Table 1 Suggested Characteristic Reason for test Preferable result biological and ecological data to collect for Mode of reproduction Determine if Amphimictic complete risk assessment parthenogenic or of new earthworm species amphimictic potentially entering a new Number of embryos per Numerous embryos One or few embryos geographic area cocoon per cocoon increases per cocoon propagule pressure Ecological ‘‘strategy’’ Determines type of Depends on locality food resource and where introduced. If food soil stratum likely to resource or habitat of species be exploited by species is scarce, invasion less likely a problem Temperature/moisture/ Determines habitats Narrow tolerances limit areas pH tolerances and ecosystems where where invasion could occur. invasion could occur. Mismatch of temperature and moisture requirements to these conditions is desirable

123 Biol Invasions probability of transporting earthworms occur, or disturbance is an important determinant of the where human disturbances have been limited earthworm community composition. The tallgrass (and native earthworms are present). prairie system is one that has been subject to chronic disturbance since its beginnings, and in- deed the system appears to rely on disturbances Influence of management practices such as grazing, fire, and drought to maintain its on introduced earthworms characteristic vegetation (Knapp and Seastedt 1986). In this case, disturbances vital to the Once introduced, the success or failure of exotic maintenance of tallgrass vegetation were also earthworms to establish large populations ap- associated with maintenance of native earthworm pears to be influenced at least in part by the past communities (James 1988). Further work in this management of the site. In areas where native system showed that relatively short-term depar- earthworm populations are present this effect is tures from the natural disturbance regime (i.e., generally related to the degree of disturbance the the absence of regular fire) resulted in a shift in site has experienced: the less disturbed the site, dominance of the earthworm community to the lower the likelihood of exotic earthworm introduced species (Callaham and Blair 1999; establishment. This type of disturbance relation- Callaham et al. 2003). ship has been documented in forested systems of Land management may be influential even in temperate and tropical North America. Kalisz systems where no native earthworm species are and Dotson (1989) and Dotson and Kalisz (1989) present. Heneghan (2003) documented a syner- found differences in the frequency of exotic gistic relationship between an invasive shrub, and earthworms in soils of Kentucky to be dependent non-native earthworms in oak woodlands of the upon the continuity of forest vegetation and upper Midwest of the USA. Invasion of buck- proximity to roads or other severe anthropogenic thorn shrub into oak woodlands in the Chicago disturbance. In these studies the principal finding area had strong effects on several ecosystem was that the fragmented forestlands of the Blue- properties, including negative effects on under- grass physiographic region were largely domi- story vegetation (Heneghan et al. 2002). If the nated by exotic earthworm species, whereas the shrub was removed from an area soon after extensive non-fragmented forests of the Cum- invasion, then these negative effects on native berland Plateau were dominated by native species vegetation were short-lived. However, the pres- except where severe disturbances had occurred. ence of buckthorn was also associated with high In tropical systems of Puerto Rico, Zou and biomass of invasive European earthworms and Gonza´lez (1997) and Gonza´lez et al. (1999) found the additional effects of these earthworms on soil that conversion of native forest to pasture systems processes and soil structure caused negative resulted in dramatic differences in the earthworm effects on the understory plant community to assemblages with nearly total dominance of the persist for longer periods of time (Heneghan pasture systems by the pan-tropical exotic species 2003). Thus, early control measures to limit the Pontoscolex corethrurus. Although P. corethrurus encroachment of the invasive shrub in these was also present in forested systems, the earth- systems may also indirectly limit the size of worm species native to Puerto Rico were still non-native earthworm populations, and benefit dominant in the forest earthworm assemblages. restoration efforts in impacted areas. However, the regeneration of secondary forest Where non-native earthworms are not well through natural succession in abandoned pastures established or are found in discrete populations, was shown to promote the recovery of native the use of chemical treatments to eradicate earthworms, and the reduction of P. corethrurus undesirable worms may be a successful strategy. density (Sanchez et al. 2003). This approach has long been used in the man- In another system where introduced earth- agement of golf courses (e.g., Walton 1928; worms coexist with native earthworms, the tall- Schread 1952), and has also been successfully grass prairie ecosystems of North America, used in experimental manipulations of earthworm

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Fig. 4 Reproduction of a poster placed in bait shops and other public locations in Minnesota directed at educating consumers about the problem of earthworm introductions. Reproduced courtesy of Minnesota Department of Natural Resources

communities (e.g., Parmelee et al. 1990). Al- exotic earthworms. One example of this type of though these treatments are known to be highly effort is the Minnesota Worm Watch Program effective for earthworm control, it is clear that initiated by scientists at the University of non-target effects of chemicals on the system Minnesota. In a cooperative effort between the should be carefully examined before large-scale Minnesota Department of Natural Resources, use of such chemicals is recommended. Minnesota Worm Watch, and the Minnesota Given the diffuse nature of the spread of Native Plant Society, the program focuses on earthworms via a range of seemingly benign hu- halting the spread of non-native earthworms into man activities (such as recreational fishing or remote areas of Minnesota by educating the planting of ornamental vegetation), public edu- public about the ecological consequences of cational efforts will be a critical component of any introducing earthworms. A variety of educational comprehensive effort to control the spread of materials regarding earthworms is available on

123 Biol Invasions the internet (http://www.nrri.umn.edu/worms/ Long-Term Ecological Research Program in the Luquillo default.htm). A poster and exotic earthworm fact Experimental Forest. sheet were distributed to more than 1500 bait shops, as well as hundreds of nature centers, park References visitor centers, and other venues across the state (Fig. 4). Public response to these efforts has been Baker GH (2004) Managing earthworms as a resource in generally favorable, and the basic message to Australian pastures. In: Edwards CA (ed) Earthworm avoid dumping unused bait in remote areas has ecology, 2nd edn. St. Lucie Press, Boca Raton FL, been well received. pp 263–286 Bohlen PJ, Pelletier DM, Groffman PM, Fahey TJ, Fisk MC (2004) Influence of earthworms on redistribu- tion and retention of soil carbon and nitrogen in Conclusions northern temperate forests. Ecosystems 7:13–27 Borges S, Moreno AG (1994) Dos citas nuevas de oligo- quetos para Puerto Rico, y nuevas localidades para Although earthworm introductions have a long otras tres especies. Carib J Sci 30:150–151 history in North America, there are still many Butt KR, Fredrickson J, Lowe CN (1999) Colonisation, areas on the continent where no exotic species survival and spread of earthworms on a partially occur. Efforts to prevent the introduction of restored landfill site. Pedobiologia 43:684–690 Callaham MA Jr, Blair JM, Todd TC, Kitchen DJ, exotic earthworms into these areas are most likely Whiles MR (2003) Macroinvertebrates in North to be successful through some combination of American tallgrass prairie soils: Effects of fire, regulatory policy, public education, and imple- mowing, and fertilization on density and biomass. mentation of appropriate land management Soil Biol Biochem 35:1079–1093 Callaham MA Jr, Blair JM, Hendrix PF (2001) Different practices. We have suggested a decision-making behavioral patterns of the earthworms Octolasion strategy for regulation of earthworm-containing tyrtaeum and spp. in tallgrass prairie soils: materials flowing into North America as well as potential influences on plant growth. Biol Fert Soil movement of such materials from place to place 34:49–56 Callaham MA Jr, Blair JM (1999) Influence of differing within North America, but the data needed to land management on the invasion of North American efficiently implement this strategy are scarce. tallgrass prairie soils by European earthworms. More research into the characteristics of earth- Pedobiologia 43:507–512 worm species likely to become successful invaders Colton TF, Alpert P (1998) Lack of public awareness of biological invasions by plants. Nat Area J 18:262–266 of North American ecosystems is needed. Like- Curry JP, Boyle KE (1995) The role of organisms in soil wise, more research on land management effects restoration, with particular reference to earthworms on earthworm communities should result in better in reclaimed peat in Ireland. Acta Zoologica Fennica strategies for containment of non-native species 196:371–375 Dotson DB, Kalisz PJ (1989) Characteristics and ecologi- and conservation of native species. cal relationships of earthworm assemblages in undis- turbed forest soils in the southern Appalachians of Acknowledgements The authors wish to thank Wayne Kentucky, USA. Pedobiologia 33:211–220 Arendt, Ariel E. Lugo, Joseph O’Brien, John Stanturf, and Dymond P, Scheu S, Parkinson D (1997) Density and two anonymous reviewers for helpful comments on the distribution of Dendrobaena octaedra (Lumbricidae) manuscript. M. Callaham was partially supported through in aspen and pine forests in the Canadian Rocky funding from the Enriched Background Isotope Study Mountains (Alberta). Soil Biol Biochem 29:265–273 (EBIS) at Oak Ridge National Laboratory (ORNL), pro- Edwards CA, Arancon NQ (2004) The use of earthworms vided by the U.S. Department of Energy (DOE), Office of in the breakdown of organic wastes to produce ver- Science, Biological and Environmental Research, as a part micomposts and feed protein. In: Edwards CA of the Terrestrial Carbon Processes Program. ORNL is (ed) Earthworm ecology, 2nd edn. St. Lucie Press, managed by UT-Battelle, LLC, for the DOE under con- Boca Raton, FL, pp 345–380 tract DE-AC05-00OR22725. L. Heneghan was partially Edwards CA, Bohlen PJ (1996) Biology and ecology supported through the USDA Forest Service and the of earthworms, 3rd edn. Chapman and Hall, London, Gutgsell Foundation. G. Gonza´lez was partially supported p 426 through grant # DEB-0218039 from the National Science Fender WM, McKey-Fender D (1990) : Foundation to the Institute of Tropical Ecosystem Studies, Megascolecidae and other earthworms from western University of Puerto Rico, and the USDA Forest Service, North America. In: Dindal DL (ed) Soil biology International Institute of Tropical Forestry as part of the guide. John Wiley & Sons, New York, pp 357–378

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