Invasion of Exotic Earthworms Into Ecosystems Inhabited by Native Earthworms

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Invasion of Exotic Earthworms Into Ecosystems Inhabited by Native Earthworms Biol Invasions DOI 10.1007/s10530-006-9022-8 ORIGINAL PAPER Invasion of exotic earthworms into ecosystems inhabited by native earthworms P. F. Hendrix Æ G. H. Baker Æ M. A. Callaham Jr Æ G. A. Damoff Æ C. Fragoso Æ G. Gonza´lez Æ S. W. James Æ S. L. Lachnicht Æ T. Winsome Æ X. Zou Ó Springer Science+Business Media B.V. 2006 Abstract The most conspicuous biological inva- dynamics, other soil organisms or plant commu- sions in terrestrial ecosystems have been by exotic nities. Most of these cases are in areas that have plants, insects and vertebrates. Invasions by exo- been disturbed (e.g., agricultural systems) or were tic earthworms, although not as well studied, may previously devoid of earthworms (e.g., north of be increasing with global commerce in agricul- Pleistocene glacial margins). It is not clear that ture, waste management and bioremediation. A such effects are common in ecosystems inhabited number of cases has documented where invasive by native earthworms, especially where soils are earthworms have caused significant changes undisturbed. We explore the idea that indigenous in soil profiles, nutrient and organic matter earthworm fauna and/or characteristics of their P. F. Hendrix (&) Æ T. Winsome G. Gonza´lez Institute of Ecology and Department of Crop & Soil USDA Forest Service, International Institute of Sciences, University of Georgia, Athens, Tropical Forestry, 1201 Ceiba Street, Rı´o Piedras, GA 30602, USA PR 00926, USA e-mail: [email protected] S. W. James G. H. Baker Natural History Museum and Biodiversity Research CSIRO Entomology, GPO Box 1700, Canberra, Center, The University of Kansas, 1345 Jayhawk Blvd, ACT 2601, Australia Lawrence, KS 66045-7163, USA M. A. Callaham Jr S. L. Lachnicht USDA Forest Service, University of Georgia, Athens, USDA ARS NCSCRL, 803 Iowa Ave., Morris, GA 30602, USA MN 56267, USA G. A. Damoff X. Zou Arthur Temple College of Forestry, Stephen F. Institute for Tropical Ecosystem Studies, University Austin State University, Nacogdoches, TX 75962, of Puerto Rico, PO Box 23341, San Juan, PR 00931, USA USA C. Fragoso Departamento Biologı´a de Suelos, Instituto de Ecologı´a A.C., Km. 2.4 Carr. Antigua a Coatepec, No. 351, Col. Congregacio´ n el Haya. AP 63, Xalapa 91070 Veracruz, Mexico 123 Biol Invasions native habitats may resist invasion by exotic influence soil processes and are integral to the earthworms and thereby reduce the impact of functioning of terrestrial ecosystems. Docu- exotic species on soil processes. We review data mented effects of earthworms include accelerated and case studies from temperate and tropical plant litter decomposition, nutrient transforma- regions to test this idea. Specifically, we address tions and plant nutrient uptake; increased soil the following questions: Is disturbance a pre- aggregation and porosity; and enhanced water requisite to invasion by exotic earthworms? What infiltration and solute transport (see Satchell 1983; are the mechanisms by which exotic earthworms Lee 1985; Hendrix 1995; Edwards and Bohlen may succeed or fail to invade habitats occupied by 1996; Lavelle et al. 1999; Edwards 2004). While native earthworms? Potential mechanisms could these effects are usually considered desirable in include (1) intensity of propagule pressure (how agricultural soils, recent interest has focused on frequently and at what densities have exotic spe- detrimental impacts of invasive, exotic earth- cies been introduced and has there been adequate worms on soil processes in wildland ecosystems time for proliferation?); (2) degree of habitat (Hendrix and Bohlen 2002; Bohlen et al. 2004a,b; matching (once introduced, are exotic species James and Hendrix 2004). Exotic earthworms are faced with unsuitable habitat conditions, capable of significantly affecting soil profiles, unavailable resources, or unsuited feeding strat- nutrient and organic matter dynamics, other soil egies?); and (3) degree of biotic resistance (after organisms, and plant communities. Impacts have introduction into an otherwise suitable habitat, been reported in tropical forests (Zou and Gon- are exotic species exposed to biological barriers za´lez 1997; Zou and Bashkin 1998; Gonza´lez and such as predation or parasitism, ‘‘unfamiliar’’ Zou 1999; Fragoso et al. 1999; Liu and Zou 2002; microflora, or competition by resident native Decae¨ns et al. 2004); chaparral shrublands (Gra- species?). Once established, do exotic species co- ham and Wood 1991; Graham et al. 1995); grass- exist with native species, or are the natives lands (Stockdill 1982; James 1991; Callaham et al. eventually excluded? Do exotic species impact 2001); and particularly in temperate forests soil processes differently in the presence or (Langmaid 1964; Alban and Berry 1994; Scheu absence of native species? We conclude that (1) and Parkinson 1994; Steinberg et al. 1997; Burte- exotic earthworms do invade ecosystems inhab- low et al. 1998; McLean and Parkinson 2000; ited by indigenous earthworms, even in the Gonza´lez et al. 2003; Bohlen et al. 2004b; Hale absence of obvious disturbance; (2) competitive et al. 2005; also see Frelich et al. this issue). exclusion of native earthworms by exotic earth- Most of the work on earthworm invasions has worms is not easily demonstrated and, in fact, focused on a relatively few species (e.g., European co-existence of native and exotic species appears lumbricids, Amynthas spp., Pontoscolex corethru- to be common, even if transient; and (3) resis- rus) that have achieved wide distributions and are tance to exotic earthworm invasions, if it occurs, now abundant in many ecosystems. Moreover, the may be more a function of physical and chemical most dramatic effects of exotic species on soil characteristics of a habitat than of biological organic matter dynamics have been observed in interactions between native and exotic areas previously uninhabited by earthworms (e.g., earthworms. north of Pleistocene glacial margins; see Frelich et al., McLean et al., Migge-Kleian et al. and Keywords Native earthworms Æ Exotic Tiunov et al., this issue) or where native popula- earthworms Æ Biological invasions Æ Disturbance Æ tions have been reduced by disturbance (e.g., Competition pastures in Australia and Puerto Rico; see Baker et al. and Gonza´lez et al. in this issue). Effects of exotic earthworms have not been as frequently Introduction reported from invasions of ecosystems inhabited by native earthworm assemblages where soils and Research over the past century has shown that vegetation are undisturbed (e.g., Abbott 1985; where earthworms are abundant, they significantly Kalisz and Dotson 1989; Lavelle and Pashanasi 123 Biol Invasions 1989; Callaham and Blair 1999; Fragoso et al. native species? Kalisz and Wood (1995) summa- 1995, 1999). These observations suggest that some rized the prevailing idea that physical disturbance characteristics of indigenous earthworm fauna or habitat fragmentation are prerequisite to and/or their native habitats may be resistant to establishment of and domination by exotic invasion by exotic earthworm species and thus earthworms in soils occupied by native species. may reduce the impact of exotic species on soil The proposed sequence is (a) habitat disturbance, processes. In this paper, we explore the interac- (b) decline or extirpation of native species, (c) tions between native and exotic earthworms and introduction of exotic species, and (d) coloniza- factors that may facilitate or inhibit invasions by tion of empty habitat by exotic species. By con- exotic species into areas inhabited by native sidering the currently observed state of any earthworm species. particular earthworm assemblage, we can trace several possible series of events that may have led to that state from a presumed indigenous com- Interactions between native and exotic munity in a pristine ecosystem (Fig. 1). earthworms Pathway A represents the extreme case de- scribed by Kalisz and Wood (1995), through Habitat disturbance or competitive exclusion which disturbance leads to exclusively exotic assemblages, as often observed with ‘‘anthrop- Exotic earthworms have been spread throughout ochorous’’ earthworms in agricultural soils (e.g., the world, aided by human colonization and Parmelee et al. 1990; Baker et al. 2002). We can commerce for at least the past few centuries; speculate that the same outcome may occur under several peregrine species are now prevalent in less severe disturbance but perhaps with more many soils impacted by human activity (Ljung- aggressive exotic invaders, as in pathway B-1. strom 1972; Lee 1985; Kalisz 1993; Fragoso 1995, Pathways B-2 and C-1 lead to the often observed 1999; Reynolds 1995; Bhadauria et al. 2000). co-occurrence of native and exotic species Where these introductions have occurred in areas (Stebbings 1962; Abbott 1985; James 1991; inhabited by indigenous earthworms, exotic Fragoso et al. 1999) through varying levels of earthworms may not persist, they may occur habitat disturbance and invasion intensity. The exclusively, or they may co-occur with the native B-2 case again assumes at least moderate levels of earthworm species. Reasons for success or failure disturbance, which reduce native population of establishment, or for varying densities of exotic density and alter habitat conditions prior to species at any particular site may not be known invasion. The C-1 pathway suggests that com- with certainty, but probably include site charac- petitive displacement of native species by exotic teristics (e.g., soil and climatic conditions), inva- species may occur
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