Biol Invasions DOI 10.1007/s10530-006-9016-6 ORIGINAL PAPER Policy and management responses to earthworm invasions in North America 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 earthworms, 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 123 Biol Invasions 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 animals (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