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Date : 2006-06-03
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Date ebook Published : 2006-06-03 Abstract The effects and implications of inva- sive species in belowground terrestrial ecosystems are not well known in comparison with above- ground terrestrial and marine environments. The study of earthworm invasions in the tropics is limited by a lack of taxonomic knowledge and the potential for

Abstract The effects and implications of inva- sive species in belowground terrestrial ecosystems are not well known in comparison with above- ground terrestrial and marine environments. The study of earthworm invasions in the tropics is limited by a lack of taxonomic knowledge and the potential for loss of species in native habitats due to anthropogenic land use change. Alteration of land use plays a major role in determining the abundance and community structure of earth- worms and the establishment of exotic earth- worms in areas previously inhabited by worms. Once an exotic species has become established into a new place, site and species characteristics seem to be key factors determining their spread. We reviewed the literature on the distribution and effects of exotic earthworms to understand the interactions of earthworm invasion and land use history in the tropics. Patterns in the abun- dance, effects and mechanisms of earthworm invasions on ecosystem processes in the tropics are elucidated using Pontoscolex corethrurus as a case study. Keywords Tropics Æ Earthworms Æ Exotic Æ Native Æ Caribbean Æ Invasion Introduction Invasive species have become a major research issue in ecology, particularly due to the deleteri- ous or unknown effects that non-indigenous spe- cies can have on ecosystem health and functioning. Ecologists continue to pursue fun- damental questions related to biological invasions (i.e., why some communities are more invaded than others, or why some invading species are widespread and abundant; Colautti et al. 2004) yet have not unraveled the effects and implica- tions of invasive species in belowground terres- trial ecosystems. Invasive species include those organisms whose distribution and abundance are changing within historical times to include geographic regions in which they have not been present, and whose G. Gonza ́ lez ( & ) USDA Forest Service, International Institute of Tropical Forestry, 1201 Ceiba Street, Rı ́ o Piedras, PR 00926-1119, USA e-mail: [email protected] C. Y. Huang Institute of Ecology, University of Georgia, Athens, GA, USA X. Zou Institute for Tropical Ecosystem Studies, University of Puerto Rico, San Juan, PR, USA C. Rodrı ́ guez Facultad de Biologı ́ a, Universidad de La Habana, Ciudad de La Habana, Cuba Biol Invasions DOI 10.1007/s10530-006-9023-7 123 ORIGINAL PAPER Earthworm invasions in the tropics Grizelle Gonza ́ lez Æ Ching Yu Huang Æ Xiaoming Zou Æ Carlos Rodrı ́ guez migration is not always directly related to range shifts associated with changing climate or habitat. Invasion follows a predictable set of stages including arrival, establishment, and spread (Hager and Treple 2003). Ecological conse- quences and management options differ at all stages, and individual species will exhibit variation in success at each stage. Invasive species successful at establishment and spread typically lack natural checks on population growth and can have important ecological consequences in a system. Earthworms are the best known and often the most important animals influencing the function- ing of soil ecosystems (Hendrix and Bohlen 2002). Earthworms significantly influence soil structure, nutrient cycling and crop productivity. In terms of biomass, they often dominate the fauna of soil food webs (Lavelle et al. 1999; Lee 1985) and their casting and burrowing activities increase soil porosity, stimulate microbial activities, and accelerate litter decay and the release of nutrients into the soil (Lee 1985; Lavelle et al. 1999; Gon- za ́ lez and Seastedt 2001; Gonza ́ lez 2002; Liu and Zou 2002). The mechanisms by which land use history and exotic species invasions affect the relative abundance and species composition of local earthworm fauna are different than those caused by soil, climate, vegetation, and topogra- phy (Hendrix and Bohlen 2002). Invasions of exotic earthworms in areas inhabited by indigenous earthworms can lead to the exclusion of either species group or to their co-occurrence. The potential mechanisms explaining the relative abundance of native and exotic species and the success or failure of the establishment of an exotic earthworm after an invasion include the intensity of propagule pres- sure, and the degree of habitat matching and biotic resistance (for details see Hendrix et al. this issue). Earthworms have also invaded areas pre- viously devoid of earthworms (e.g., north of the Pleistocene glacial margin) (Hendrix 1995). In those areas, exotic European lumbricids have been shown to alter forest floor, change nutrient cycling rates and the distribution and function of microbes and roots, and negatively impact the native vegetation (e.g., Alban and Barry 1994; Gundale 2002; Bohlen et al. 2004; also see Frelich et al. McLean et al. and Tiunov et al. this issue). Land use history plays a major role in deter- mining the abundance and community structure of earthworms and the establishment of exotic earthworms in areas previously inhabited by na- tive worms. For example, in the tropics, conver- sion of forest to pastures has been associated with significant decreases in soil macro-invertebrate diversity (Lavelle and Pashanasi 1989) and with the dominance of a few exotic earthworm species that can persist along gradients of plant succes- sion after disturbance (Zou and Gonza ́ lez 1997; Sa ́ nchez-de Leo ́ n et al. 2003). Land use alteration in the tropics has historically been dominated by a shift from forest to agriculture, but there are also land use trends towards increasing urbanization and reforestation. The role of exotic earthworms includes influence on current pasture ecosystems, their potential invasion into surrounding forests and consequent ecosystem effects, their influence on regenerating secondary forests in abandoned pasture, and their overall effects on tropical bio- diversity. Many of these potential effects are unstudied and remain unknown. We have reviewed the literature on the distri- bution and effects of exotic earthworms to understand the interacting effects of earthworm invasion and land use history in the tropics. In the following sections, we evaluate the history of earthworm invasions in the tropics and the status of native and exotic earthworm species in this region. We elucidate patterns in earthworm abundance, effects of earthworm invasions on ecosystem processes and mechanisms of those effects in the tropics, using Pontoscolex core- thrurus great difficulty of earthworms crossing salt water (Stephenson 1930). Also, earthworms have failed to colonize the Lesser Antilles by over-water dispersal from nearby land masses inhabited by indigenous earthworms; there is no evidence of spread from South America into the Lesser Antilles or from the Greater Antilles to the east and south (James 1998). When considering the history of invasions of exotic earthworms in the tropics we need to consider their transport by humans. The invasions of exotic earthworms in the tropics can be ex- plained to a great extent by the historical dis- persal of humans and commerce (e.g., trade routes). For example, Gordiodrilus peguanus and Eudrilus eugenia (African species) are present mainly in former European colonies such as the Greater Antilles (Gates 1972) that were inhabited by African slave populations. These species are not present in countries such as Peru ́ and Me ́ xico where African slaves were practically non-exis- tent (Fragoso et al. 1999). Similarly, the dispersal to the Caribbean Islands of three native genera of South America ( Pontoscolex , Onychochaeta and Eukerria ) can be explained by human migration prior to European colonization (Righi 1984; Lavelle and Lapied 2003). Humans arrived in the Greater Antilles from South America some 2200 years ago by island hopping (Domı ́ nguez- Cristo ́ bal 2000). At least three successive groups or cultures of indigenous people from South America had arrived in Puerto Rico before 1493 (Go ́ mez-Acevedo and Ballesteros-Gaibrois 1980). Some of those indigenous groups mastered agriculture (Go ́ mez-Acevedo and Ballesteros- Gaibrois 1980) and their activities modified the flora and fauna by introducing new species to Puerto Rico (Francis and Liogier 1991). Also in Puerto Rico, exotic earthworms such as Dichog- aster sp., P. corethrurus and Amynthas roderic- ensis have been reported in caves (Peck 1974) which were commonly used by indigenous people and African emancipated slaves (Ayes-Sua ́ rez and Otero-Lo ́ pez 1986). Rightly so, Fragoso et al. (1999) stated that the absence from a given tropical country of native earthworms with wide range distributions can be explained by human activities rather than ecological factors. Merging rigorous scientific methodologies between ecology and human history could provide insights (James 1998) in the study of tropical earthworm invasions. In recent times, commercial transport of earthworms or earthworm-containing media has advanced the proliferation and establishment of non-indigenous earthworms into new areas (see Baker et al., and Callaham et al. this issue). The major sources of non-indigenous earthworm introductions are the fishing-bait, horticulture and waste management industries. Advances in com- munication technology (e.g., internet access) have facilitated the promotion of lucrative businesses that sell and export exotic earthworms interna- tionally. Most of the exotic earthworms used for waste management require high organic inputs earthworm richness could be at least twice the present count (Fragoso et al. 1999; Reynolds 1994). Fragoso et al. (1999) suggested that nearly 500 new native species could be expected to be discovered in Central America and the Caribbean islands once the surveys are completed. However, it has also been found that several peregrine earthworm species have invaded these tropical areas due to human activities (Fragoso et al. 1999), and the distribution of these exotic earth- worms overlaps the range of native earthworms. In fact, results from Lavelle and Lapied (2003) indicate that many native earthworm species are in danger of extinction or have already disap- peared in Amazonia due to the colonization by exotic species. Fragoso et al. (1999) listed 51 exotic earth- worms commonly distributed across the tropics. About 28 of them are present in the Caribbean Islands (Table 1). Over 50% of these exotic earthworms were originally from Europe and Asia (29 and 23%, respectively), 18% were from South America and 16% were from West Africa. They mainly belong to the Families Megascolec- idae (35%) and Lumbricidae (33%) (calculated from data by Fragoso et al. 1999) and are widely distributed in different land-use systems, includ- ing natural ecosystems, croplands, pastures, tree plantations, fallows and are also present in or- ganic wastes. There are about 400 native species of earthworms described in the tropics, with 67 % restricted to a single locality (Fragoso et al. 1999); approximately one third of those single localities are due to endemic species in the Caribbean Islands (Rodrı ́ guez et al. 2006). Native species in the Caribbean Islands mostly belong to the fam- ilies Octochaetidae (65%) and Glossoscolecidae (17%) (Rodrı ́ guez et al. 2006). Jamaica and His- paniola have the greatest percentage of native earthworm species (Rodrı ́ guez et al. in press), despite the scarcity of intensive surveys in both islands (Fragoso et al. 1999) and the extensive land use changes in Hispaniola. Therefore, the native earthworm fauna of the Caribbean Islands, like those of Amazonia, could be in danger of not being described or of extinction. Mechanisms of earthworm invasions in the tropics – Pontoscolex corethrurus as a case study Pontoscolex corethrurus , which was originally derived from South America, is now a dominantly invasive species around the world. Because of its superior capacities of adaptation, P. corethrurus has established populations throughout the moist tropical regions of over 56 tropical countries across the world (Fragoso et al. 1999). In Puerto Rico, P. corethrurus invaded primary cloud for- ests at the top of the Luquillo Mountains (Hen- drix et al. 1999). An invasion of P. corethrurus has also been noticed in the Najenshan Nature’s Reserve in southern Taiwan, a primary tropical rain forest (Zou et al. unpublished data). How- ever, the invasion of tropical exotic earthworms occurs most frequently in disturbed habitats. Establishment of exotic earthworms in a new area can occur (1) when they can compete suc- cessfully with native species in the new site, or (2) Table 1 The exotic earthworms of the Caribbean Islands (from Rodrı ́ guez et al. 2006) Family Species Acanthodrilidae Pontodrilus litoralis (Grube 1855) (= P. bermudensis ) Almidae Drilocrius hummalineki (Michaelsen 1933) Eudrilidae Eudrilus eugenieae (Kinberg 1867) Glossoscolecidae after they colonize disturbed habitats where hu- man activities have reduced or eliminated native earthworms (Fig. 1). Kalisz (1993) suggested that whether native earthworms will coexist with or be replaced by exotic earthworms depends on the disturbance history of the areas and the state of naturalness of the landscape. As shown in Fig. 1, in native ecosystems native earthworms may completely impede the invasion of exotic earth- worms because of their better adaptability to the original environments. But, disturbance (due to human activities or natural events) could result in extirpation or reduction of native species popu- lations due to sharp changes in soil physical structure, nutrient cycling (litter input), and microclimate (e.g., logging and deforestation), conditions that may reduce native earthworm populations prior to the invasion of exotic earth- worms. Opportunity for invasion in disturbed ecosystems occurs when native earthworms leave vacant niche spaces that are available for the introduction and colonization of exotic species (Kalisz and Wood 1995). It is then when the competitive relationship between native and exotic earthworms will become important for the coexistence of native and exotic earthworms or the presence of either population in a disturbed area (also see Hendrix et al. this issue). Disturbance due to anthropogenic practices seems to be the major cause of spread of exotic earthworms in the tropics. Exotic earthworms can establish their populations in sites modified after deforestation (e.g. forest–pasture conversion), in tree plantations and in cultivated areas, as well as in areas inhabited by humans (Gonza ́ lez et al. 1996; Zou and Gonza ́ lez 2001; Lapied and Lavelle 2003; Fig. 2). Some studies have argued that the increase in densities of P. corethrurus might directly cause the disappearance of native species populations (Fragoso et al. 1995; Lapied and Lavelle 2003). However, disturbed sites with a combination of both native and exotic species have been found (Gonza ́ lez et al. 1996; Kalisz 1993; Lapied and Lavelle 2003). This suggests that some native species might compete with exotic species and then exclude or co-exist with the exotics (Fig. 1). Certainly, more studies related to the relation- ships and consequences of native vs. exotic earthworm species are needed. The reasons for failure or success of establish- ment of exotic earthworms include invasion his- tory (e.g., frequency and duration of the introductions), site characteristics (e.g., climatic and edaphic conditions), and the characteristics of the species involved (see details in Hendrix et al. Native species only Habitat disturbance Invasion of exotic earthworms Natives only Disturbed ecosystem Native ecosystem Exotics and natives co-exist Natives only Reduction of native species Reduced competition from natives Exotics a nd natives co-exist Secondary succession Competitive exclusion of exotics Exotics only Extirpation of native species No competition with natives Decrease in native species a nd increase in exotic species Increase gradient of disturbance Fig. 1 Model illustrating the paths by which invasion of exotic

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