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Agriculture, Ecosystems and Environment 74 (1999) 137–155 The role of earthworms for assessment of sustainability and as bioindicators Maurizio G. Paoletti ∗ University of Padova, 35100-Padova, Italy Abstract Earthworms, which inhabit soils and litter layers in most landscapes, can offer an important tool to evaluate different environmental transformations and impacts. Agricultural landscapes, urban and industrialized habitats have some earthworms that represent interesting indicators to monitor different contaminations, to assess different farming practices and different landscape structures and transformations. Species number, abundance and biomass can give easily measurable elements. Ecological guilds can help in comparing different environments. Taxonomy is relatively well known, at least in temperate areas, where species identification is in general easily solved. CD-ROM based programs facilitate rapid identification of collected specimens. The substantial amount of research carried out on these invertebrates has made these soil organisms more promising for further improved and accurate work in assessing sustainability of different environments. In most cases earthworm biomass or abundance can offer a valuable tool to assess different environmental impacts such as tillage operations, soil pollution, different agricultural input, trampling, industrial plant pollution, etc. In rural environments different farming systems can be assessed using earthworm biomass and numbers. ©1999 Elsevier Science B.V. All rights reserved. Keywords: Bioindication; Earthworms; Rural landscape; Contamination; Reclamation; Soil quality; Sustainable farming; Lumbricidae; Pesticides; Heavy metals; Engineered crops 1. Introduction The Anellids have colonized marine, freshwater and terrestrial habitats. Most of the approximately 3500 species of so-called earthworms (Oligochaeta) inhabit soils, including suspended soil habitats on trees, especially in humid tropical forests; others live in submerged muds in freshwater bodies and marine bot∗ Present address: Dipartimento di Biologia, Università di Padova, via U. Bassi, 58/b, 35121-Padova, Italy; tel.: +39-049-8276304/5; fax: +39-049-8276300/8072213; web page: http://www.bio.unipd.it/agroecology/ E-mail address: [email protected] (M.G. Paoletti) toms, where they form a substantial part of the benthic fauna (Jamieson, 1988; Brinkhurst and Jamieson, 1971). This review concentrates on the earthworms, which are distributed among 18 families. The most extensively studied and widely distributed family of earthworms is represented by the Lumbricidae, which are especially numerous in the Palearctic region. Agricultural activities such as plowing, different tillage operations, fertilizing and application of chemical pesticides have dramatically influenced these animals. Most of the larger species (those over 18–25 cm long) have been displaced from cultivated areas in the tropics as well as in temperate rural areas or are present only in woodland and grassland patches remaining in 0167-8809/99/$ – see front matter ©1999 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 8 8 0 9 ( 9 9 ) 0 0 0 3 4 - 1 138 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 mosaic landscapes. The decline of larger earthworms in rural areas can be worsened as a result of high predation during and after tillage operations, e.g., by other invertebrates such as ground beetles, and by ravens, sea gulls (Cuendet, 1987) and other vertebrates. Earthworms traditionally have been considered to be convenient indicators of land use and soil fertility. For example, Tanara (1644) stated that the presence of birds such as ravens, magpies and others that are attracted to a freshly plowed field and scratch on the soil to uncover and eat the small invertebrates (mostly earthworms) gives a good indication of agrarian soil fertility. Their relatively large size, ranging from 1 to 80 cm or larger (Pop and Postolache, 1987), limited rapidity in soil displacement and slow recolonization are features that make earthworms easy to capture and sort and render them attractive as bioindicators. Substantial research in recent years and simple taxonomy (at least for common species in the temperate areas), also enhance their potential as useful tools (Lee, 1985; Bouché, 1996; Edwards and Bohlen, 1996; Paoletti and Bressan, 1996). 2. Taxonomy Identification of adult earthworms is based mainly on the position and shape of the clitellum, setae and internal organs such as seminal vesicles and spermathecae. Manuals are available for identification of earthworms in various countries, including France (Bouché, 1972); Germany (Graff, 1953), Italy (Paoletti and Gradenigo, 1996), the United Kingdom (Sims and Gerard, 1985), the United States and Canada (Reynolds, 1977; Schwert, 1990), Russia (Perel, 1976), and New Zealand (Springett, 1985); a system for identification of earthworms found in Italy is also available on CD-ROM (Paoletti and Gradenigo, 1996). Useful manuals dealing with earthworm biology, morphology and ecology include the works of Jamieson (1981), Satchell (1983), Wallwork (1983), Lee (1985) and Edwards and Bohlen (1996). 3. Earthworm abundance and distribution Fig. 1 summarizes earthworm density, biomass per m2 and species abundance in managed and unmanaged environments using data from surveys of about 350 study sites (found in the LOMBRI-ASSESS database). Differences in techniques, collection periods, territory scales and taxonomic expertise must be taken into consideration when evaluating these data. Nevertheless, it is reasonable to conclude the following: (1) pastures and meadows bear higher earthworm density and biomass; (2) deciduous forest have higher earthworm biomass and density than coniferous forests; (3) cultivated fields have lower densities than most orchards. Tropical habitats are not well represented in these figures but undoubtedly contain more species than indicated by the available data. 4. Collection systems The choice of earthworm collection methods depends on the aim of the sampling campaign, i.e., obtaining the maximum number of species in one area or estimating differences among various components or locations in a landscape. Sampling methods always represent a compromise between effort and labor (and funds) required and the desire for accurate quantitative and qualitative measurements and statistics. Earthworm sampling should preferably be carried out during cool and wet seasons; sampling of dry soils (or during dry seasons) or of frozen soils should always be avoided. In general sandy soils (over 70% sand), which easily become dry, and strongly acidic soils are inhospitable to earthworms and other soil organisms. In temperate areas, sampling studies in autumn, spring and some of the winter months give the best results if soil humidity is adequate. Although earthworms can live in litter, soil, wet mud, submerged mud, organic manure, composts, dung, under bark and on rotted wood, most earthworm species are adapted to a particular habitat. In the humid tropical forests (for instance, in the cloud forests in Venezuela) some species, sometimes the majority, are arboriculous and live in suspended soils, such as the soil that accumulates in the leaves rosette of bromeliads, in the tree canopy. These earthworms can be collected by photo-eclectors, a special traps that catch all moving invertebrates on the surface on trunks (Adis and Righi, 1989). One active collection system consists of hand sorting from soil cores of 25 × 25 or 30 × 30 cm2 dug to a depth of 20–50 cm with a spade. Although larger M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 139 Fig. 1. Earthworm density (a) fresh biomass (b) and species number (c) in managed and unmanaged environments. The data were obtained from 341, 274 and 172 different plots studied in the literature in different countries and climates (LOMBRI-ASSESS data base). 140 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 Fig. 1. (Continued). squares (sides: 50–100 cm) require much effort and therefore many workers, they are more efficient in gathering large, deep borrowing species (Lavelle, 1988). Digging deeper than 20–30 cm into the soil yields few specimens but sometimes reveals interesting deep-burrowing species that would be missed in shallow diggings. Sampling repetitions, possibly in a random design, are needed to assess population variability and to demonstrate statistical significance among the different prospected sites. Preliminary samplings can offer basic information and permit better design of the subsequent sampling campaign; the advice of a statistician can help in planning a valid sampling design. To assess populations of deep-burrowing and larger specimens, irritant solutions can be used to stimulate the earthworms to come to the soil surface, thereby facilitating collection. One particularly effective technique involves the application of 5–10 l of 0.2–0.5% aqueous formaldehyde solution onto 50 × 50 cm2 of soil; other irritant chemicals such as potassium permanganate and copper sulfate have been used with less success. Formaldehyde treatment is more effective on species producing vertical burrows, e.g., L. terrestris, than on those that dig meandering or horizontal burrows (e.g., Allolobophora rosea) (Bouché, 1975; Lee, 1985). Formaldehyde is not effective in inducing most tropical large burrowers to exit the soil, e.g., the Megascolecidae and the Glossoscolecidae: e.g., I obtained unsatisfactory results when formaldehyde solutions was used to collect large earthworms in rain forests and savannas in Venezuela, Ecuador and Vietnam. One must also keep in mind that formaldehyde is toxic to humans and other animals and burns plant root systems. Pitfall traps and soil baits have been successfully used in some earthworm sampling studies (Lee, 1985). Photo-eclectors arranged around the trunks of trees can also be used to collect earthworms, especially in the humid tropics (personal observations). Several electrical systems have been tested for the purpose of inducing earthworms to come to the soil surface (Edwards and Bohlen, 1996). For example, a system consisting of two electrodes inserted 1 m apart and M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 141 50 cm deep in the soil, with a Diesel engine producing 250 V and 2–4 A, has been demonstrated to be effective. As moisture is a prerequisite for electrical conductivity, this technique is suited only to humid soils, and becomes more efficient as the soil pH is lowered. 5. Ecological classification Categorizing living creatures based on their ecological characteristics is a limited and sometimes ambiguous way to operate, but clearly offers practical advantages such as the ability to assess different environments. Earthworms can be divided into the following general categories, which take into account basic features such as burrowing abilities, food preferences, and body color, shape and size (Bouché, 1977; Lee, 1985; Curry, 1994). 1. Epigés are surface-active, pigmented, and are in general non burrowing and dwell in litter. Some corticicoles living under rotted bark can be assigned to this category. 2. Anéciques are large, deep-burrowing forms that come to the soil surface when it is more humid, usually during the night, and draw the litter down into the lower strata. Sometimes they live in semi-permanent burrows. 3. Endogés live near the surface of soils in the organic horizons and produce mostly horizontal galleries. 4. Coprophagic species live in manure, e.g., Eisenia foetida (in the Holarctic), Dendrobaena veneta (originally described in northern Italy), and Metaphire schmardae (in China). 5. Arboricolous species live in suspended soils in humid tropical forests. Although similar to the epigés, they have large cocoons and can withstand long periods of immersion in water, e.g., in pools of water that accumulate in bromeliads in the cloud forests (Fig. 2). Interestingly, these earthworms have been reported to climb trees (Adis and Righi, 1989). Among these categories, epigés, aneciques and endogés are more often used in soil assessment compared to coprophagic and arboricolous species. Surface dwelling epigés such as Lumbricus rubellus and L. castaneus, which are most vulnerable to Fig. 2. Arboricolous Andiorrhinus spp. earthworms in suspended soils, on bromeliads, in cloud forests in Venezuela (Cordillera de la Costa, Paque Pittier). These arboricolous species produce large cocoons and support long immersion periods, in the water that accumulates in bromeliads. desiccation and predation, produce high numbers of cocoons each year (65–106); endogés such as Allolobophora chlorotica, A. caliginosa and A. rosea produce 8–27 cocoons per year. The deep-burrowing anécique species such as A. longa produce the lowest numbers of cocoons (3–8 per year) (Lavelle, 1981; Curry, 1994); the larger deep-burrowing species such as Eophila tellinii, which can reach 80 cm in length, may produce only 1 or 2 cocoons per year (Braida, 1994). Small numbers of cocoons have also been recorded for the largest specimens in Europe, which are found in the Carpathian mountains and can attain a length of up to 100–150 cm (Pop and Postolache, 1987; V. Pop, pers. comm., July, 1996). These reproductive data clearly explain why the larger deep-burrowing species would be the first earthworms to disappear from disturbed environments. For example, in a study of earthworm populations in natural and cultivated areas in the United States, Fender and McKey-Fender (1990) observed that although native Megascolecidae predominate in areas still dominated by native vegetation, the adventitious Lumbricidae become more numerous in agricultural and urban areas. 142 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 6. Agricultural activities and earthworms Intensification of cropping, annual tillage and other operations such as fertilization, irrigation and pesticide use consistently affect populations of earthworms and other invertebrates as well. A long history of rural landscape transformation has resulted in many changes in the distribution of earthworm species. Most large earthworms have disappeared from intensively tilled rural landscapes. In Europe, the large Octodrilus, Allolobophora, Eophila and Scheroteca species are relicts on hills, mountains and woodlot remnants in rural landscapes. Although large specimens also disappear from shifting agricultural gardens in tropical forests, they generally recolonize when the gardens are abandoned to fallow. Very little knowledge is available about the composition of species that colonized the earliest sites of cultivation such as the Fertile Crescent (i.e., 4000–14,000 BC). Most Lumbricidae species currently present in European rural landscapes probably adapted to rural environments and were passively spread by European peasants colonizing the United States, New Zealand, Australia and South America. Species such as Aporrectodea caliginosa, Lumbricus rubellus, L. terrestris, Octolasium lacteum, Allolobophora rosea, A. chlorotica and a few others undoubtedly have been dispersed by European colonists. In addition, active earthworm dissemination has been implemented by some farmers in order to improve pasture productivity, e.g., in New Zealand and Australia (Lee, 1991) and in reclaimed polders in Holland (Hoogerkamp, 1987). These introduced species overcome the native ones living in the forested areas. Some earthworm species have developed a mimetic yellow-green color (among Lumbricidae, Allolobophora chlorotica and A. smaragdina; among the Megascolecidae, most species living in rural areas of China (Fang et al., 1999) and in African savannas, possibly to avoid predation in grass-like dominated areas. In addition, some species such as Eisenia foetida and Dendrobaena veneta, which are found living in the cow manure that accumulates at dairy farms, have an annular color pattern that may serve to protect them from predators in manure heaps and other habitats (Fig. 3). A similar annular color pattern is shared by Eophila tellinii and Octodrilus mima, large species that are generally deep burrowers but also occasionally feed on soil surface litter when humidity in soil is high enough, e.g., in the deciduous forests of northeastern Italy (Paoletti, 1985). 7. Soil and litter type Native soils with organic matter of the mull and moder types generally present higher earthworm diversity and biomass. Sandy soils and sandy heaths usually support smaller populations of earthworms, as do acidic and mor soils (Ghilarov, 1979). Although most coniferous litter is unacceptable or marginally palatable to the majority of earthworms, even after weathering, earthworms seem to be an important element for regeneration of coniferous stands (Bernier and Ponge, 1994). In addition, most Eucalyptus spp., on which reforestation in temperate and many tropical countries is based, produce litter that is not attractive to earthworms and most soil invertebrates, and tends to lead to their disappearance (Curry, 1994). Fresh deciduous forest litter is generally attractive to earthworms only after some weathering and degradation by fungi and bacteria. The necessity for some initial breakdown of deciduous plant litter reflects the fact that earthworms are not well equipped to digest lignin and other products derived from cellulose; like other animals, they rely on symbiotic microflora to break down these and other substances that are abundant in plant materials (Neuhauser et al., 1978). 8. Tillage Long before its emergence in Western agriculture, the Chinese had developed the moldboard plow and introduced improved soil management methods, including turning down top soil and controlling weed pressure more efficiently. Tillage equipment, especially the machines developed to prepare a smooth seed bed after plowing, creates problems for the deep-burrowing species such as L. terrestris and A. longa, Octodrilus spp. and other larger earthworms found in most European rural landscapes and also sometimes significantly affects surface dwellers such as epigés. The larger Megascolecidae are also affected negatively by tillage in China and India. Larger species usually dis- M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 143 144 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 appear soon after transformation of a natural soil into a cultivated field, mostly because of tillage operations. Minimum tillage, no-tillage and ridge-tillage tend to reduce the loss of earthworm biomass living on the soil surface, in part because these less invasive soil mixing practices incorporate dead mulch and/or crop residues 10–15 cm below the surface of the topsoil, or allow it to stay on the soil surface, much like the litter found in woodlands (Stinner and House, 1990). Some organic farmers have obtained good earthworm management in fields and orchards using a chisel-type tiller that gently mixes the soil without the damaging cutting and slicing action associated with disc plows (Paoletti et al., 1995a). Tillage experiments carried out at Spray Farm in Ohio, USA demonstrated that, when confined to the soil surface, disc chisel tilling only moderately affects earthworm biomass in a 4-year rotation design (hay–corn–soybean–wheat) (personal observations) (Fig. 4). In addition, certain types of plows with rotary chisels that restrict tillage to the uppermost part of the soil are better at preserving earthworm populations than conventional moldboard plows (El Titi and Ipach, 1989). Crop residue left on the soil surface of non-tilled crops protects earthworms from desiccation and/or predation during dry periods (Paoletti, 1987); thus fields under no-tillage always exhibit higher earthworm biomass than conventionally tilled fields (House and Parmelee, 1985; Clapperton et al., 1997). Experiments carried out at Thompson Farm, IA, USA demonstrated that ridge tillage, which leaves most organic debris on the soil surface, is also less disruptive to earthworm biomass compared to conventional moldboard tillage (Fig. 4 (bottom), personal observations). 9. Fertilization and mulching Adding manure positively affects earthworm biomass and abundance both in grasslands and fields. Earthworms generally respond better to organic manure than to chemical fertilizers (Curry, 1994). However, liquid manure such as pig slurry can stress earthworm populations in grasslands and cultivated fields if applied in high quantities (e.g., 400 tons ha−1 ; Anderson, 1980). On several occasions the author have observed that farms that are frequently sprayed with liquid cow manure show dramatic decreases in earth- Fig. 4. (above) Conservation and no tillage systems associated with rotation and mulching reduce earthworm loss in most cases. Rotary chisel at Spay Farm, Ohio,USA, used for, reduced tillage. For instance, hay field is tilled in Fall just 10–12 cm on the surface. (bottom) Ridge tillage seeding machine that permits to directly forcast the seeds of crops such as corn and soybean directly on the sod. worm biomass (Paoletti, 1985). Given sufficient soil humidity, application of ‘living’ or ‘dead’ mulch can be expected to promote earthworm biomass. Incorporation of plant material such as crop residue or a cover crop (not too deep) into the soil improves earthworm activity and biomass, especially of endogé species. In apple orchards, Kuhle (1983) demonstrated that different mulching methods (grass cuttings, chopped wood residues and grass incorporation) can improve diversity, abundance and biomass of earthworms compared with bare soil. 10. Pesticides Although numerous studies have been devoted to toxicity of pesticides to earthworms, many products M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 have not been tested both in the laboratory and under field conditions. In addition to the direct effects of pesticides, one must consider the toxicity of the many breakdown products of pesticides that enter the soil; furthermore, the possible synergistic effects of pesticide cocktails are not well studied or understood. Pesticides can show both direct toxicity against earthworms and produce latent effects on their growth and fertility. In addition, pesticide-contaminated earthworms can represent a source of contamination of higher members of the food web, e.g., seagulls and other birds. Pesticides usually enter the soil as residues of sprays applied to crop plants from above ground, and are less frequently applied directly on soils, as is the case for nematicides and root pest control agents. Targets of root pest control agents include Diabrotica beetles, which are especially noxious to corn and soybean crops in the US, and larvae of beetles such as Elateridae and Alticinae, which attack the roots of sugarbeets and corn plantlets in Europe. Insecticides such as phorate and carbofuran are very deleterious to earthworms when applied to soil (Edwards and Bohlen, 1992). Pesticides usually reach the soil as mixtures of several products, especially in orchards. Upon entry into the soil, such mixtures are expected to have the greatest effects on earthworms feeding at the soil surface, i.e., epigeic, surface dwelling earthworms such as Lumbricus rubellus and L. castaneus. In orchards, grasslands and on row crops, slurries and sewage sludge are sometimes applied. These products create problems for the soil foodwebs. Soil toxicity resulting from introduction of contaminants such as heavy metals and PCBs can be monitored by earthworm numbers and dynamics (Kreis et al., 1987; Curry, 1994). 11. ‘Archeological’ pesticide residues High quantities of residues of ‘archeological’ pesticides can be found in many rural areas, especially those that traditionally have supported intensive orchards or industrial crops such as cotton or other industrial crops. Examples of such residues are: arsenic, a breakdown product of lead arsenites used at the beginning of this century and banned in Great Britain in 1960 (Sheail, 1985); DDT, banned in 1971 in the United States and most other countries but still used in 145 some areas, including China (Mellanby, 1992); copper, a component of bordeaux mixture (and similar compounds), especially common in vineyards in most European countries; and zinc, a component of carbamate fungicides. Despite the fact that some microorganisms are able to degrade arsenic compounds (Ahmann et al., 1994) and that organochloride compounds have been shown to be broken down in organic orchards (Paoletti et al., 1995a), their presence can still cause toxicity problems in intensively farmed rural landscapes. Although research on these contaminants has not yet been extensively pursued, the fact that these substances accumulate and persist in the soil suggests that earthworms and other invertebrates could be used to test such problems. For example, a study carried out by Fang et al. (1999) in subtropical China demonstrated an inverse correlation between the concentration of arsenic in the soil and abundance of Megascolecidae earthworms. 12. Fungicides Fungicides are generally highly toxic to earthworms, especially copper and zinc residues from copper sulfate and carbamates, respectively. Soil fumigants, nematicides and fungicides such as D–D mixture (dichloropropane : dichloropropene), metham-sodium and methyl bromide are highly toxic to earthworms. The majority of fumigants and contact nematicides are toxic to earthworms as well (Edwards and Bohlen, 1992). Carbamate fungicides such as benomyl and carbendazim are also highly toxic to earthworms. For example it has been reported that about 1.8 kg ha−1 per year of benomyl may destroy all the Lumbricus terrestris and most of the Allolobophora spp. present in an apple orchard in England (Stringer and Wright, 1976; Brown, 1978). The degree of toxicity of the more traditional copper sulfates is controversial. At the laboratory level, tests specifically developed for Eisenia foetida (a lumbricid species living only in manure) suggest copper sulfates are lethal only when applied at high doses (over 1000 ppm) (Malecki et al., 1982). However, this study is weakened by the fact that this species is completely absent from fields and is not representative of the earthworm fauna in rural landscapes. Some studies have demonstrated that the toxicity of copper 146 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 Fig. 5. Relationship between content of copper (a) and zinc (b) in soil and earthworm abundance in 72 orchards in Emilia Romagna, Italy under different practices and fruit crops (kiwi, apple, peach, grape). Copper is a residue from bordeaux mixture, applied as fungicide, and zinc is a residue linked to more recent use of carbamate fungicides such as ziram (from Paoletti et al., 1998). toward earthworms decreases as the quantity of organic matter in the soil increases (Jaggy and Streit, 1982). Direct tests have shown that concentrations of copper in the soil ranging between 100 and 150 ppm are in most cases sufficient to produce a consistent decrease in earthworm numbers (Fig. 5 (a)). Thus it is worrisome that higher concentrations of copper are found in the soil in many orchards around the world. As shown in Fig. 5 (b), zinc also has toxic effects on earthworms. M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 147 13. Insecticides 15. Heavy metals Earthworms are strongly affected by many types of insecticides, which may be applied directly to the soil or enter the soil from treated crops. The insecticides most commonly used in current agricultural practice include the following: Organochlorine insecticides: DDT, Aldrin, Dieldrin and BHC show low toxicity against earthworms; Heptachlor, Endosulfan, and Isobenzan are moderately toxic; Endrin and Chlordane, lindane are very toxic (Edwards and Bohlen, 1992; Slimax, 1997). Organophosphate insecticides: phorate, which is used as a granular soil insecticide to control certain soil pests, shows high toxicity against earthworms (Way and Scopes, 1968); other organophosphates are moderately toxic (Edwards and Bohlen, 1992). Carbamate insecticides (and fungicides): these products are generally highly toxic to earthworms; application of Carbofuran to soil has been shown to strongly affect earthworms (Haque and Ebing, 1983; Edwards and Bohlen, 1992). Natural and synthetic pyrethroids: those that have been tested do not appear to be toxic to earthworms (Edwards and Bohlen, 1992). However, in the author’s view additional research is needed in order to reach solid conclusions regarding the possible toxicity of this class of insecticides. Heavy metals can enter the soil from different sources. Fertilizers, pesticides, organic and inorganic amendants, wastes and sludge residues can contain variable amounts of these metals. Treatment of orchards and vineyards with copper sulfate strongly affects soil invertebrates, especially earthworms (Rhee, 1977a, 1977b; Ireland, 1979; Paoletti, 1985; Paoletti et al., 1988;) in terms of both biomass and species population response (Paoletti et al., 1988). Although their sensitivity to copper sulfate suggests that earthworms would be suitable as monitors of this source of soil contamination, such earthworm-based assessment is complicated by the fact that earthworms can develop tolerance to these pollutants, as documented in several studies of populations that have been in contact with high polluting sources over long periods (Bengtsson and Rundgren, 1992; Bengtsson et al., 1992; Fisher and Koszorus, 1992; Morgan and Morgan, 1992). The direct measurement of heavy metal concentrations in earthworm tissues could provide a means of assessing environmental pollution levels, given the demonstrated correlation between soil contamination and earthworm metal bioaccumulation (Motalib et al., 1997). However, in practice, many different residues accumulate in soils, and their many potential interactions are far from understood (Mari et al., 1997). 14. Herbicides 16. Engineered crops Although most herbicides are considered to exert little direct impact on earthworms (Edwards and Bohlen, 1996), the reduced weed cover resulting from their application obviously can render habitats less hospitable to earthworms. Laboratory tests have shown that the herbicides bentazon, bromphenoxin, bromoxynil, bromoxynil octaonate/ioxynil and atrazine are moderately toxic to earthworms (Pizl, 1988). Some large spectrum herbicides, e.g., glyphosate, are quite harmful to earthworms such as Aporrectodea caliginosa even at very low doses (Springett and Gray, 1992). Epigeic earthworms such as Allolobophora chlorotica and endogeic A. rosea seem to be negatively affected in grasslands spread with atrazine and pentachlorophenol (PCP) (Conrady, 1986). Agriculture was the first arena to support the development and practical application of genetic engineering to improve crop yields and quality. Over two thousand field trial releases of different transgenic crop plants have been carried out in various countries. Attributes of plants currently manipulated by genetic engineering include herbicide tolerance (47% of the transgenic plants generated to date); insect resistance (25%) altered product quality (20%); resistance to viruses (17%); and bacterial and fungal resistance (5%) (Gene Exchange, 1994). A growing list of Genetically Modified Organisms (GMOs), including microorganisms, animals and crop plants, are already available or will soon be introduced to the mar- 148 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 ketplace. For example, a genetically modified form of Agrobacterium radiobacter has been commercially available since 1988, at least in Australia. Engineered cotton and corn containing the Bacillus thuringiensis (BT) toxin, effective against some key lepidopteran pests, have been on the market since 1995, and crops such as engineered cotton, corn and soybeans that are resistant to the herbicide glyphosate, and cotton, corn and potatoes engineered with BT toxin will soon be commercially available. Risk assessment is a fundamental step in evaluating these new GMOs before large-scale release. The soil biota, and earthworms in particular, can offer a reliable tool for monitoring the possible effects of GMOs on non target soil organisms, especially in the case of transgenic plants exhibiting altered resistance to insects and viruses. For example, if it is expected that plants engineered with BT toxin would be incorporated into soils, then it would be useful to evaluate the impact of the toxin against non target organisms, earthworms included (Jepson et al., 1994; Paoletti and Pimentel, 1995; Paoletti and Pimentel, 1996). 17. Assessing environmental stress 17.1. Using earthworms to monitor the effects of fungicides Wood ashes, sulfur, lime, lime sulfate and copper sulfate have been applied for many years to plants attacked by fungi, including fruit crops such as grapes, apples, pears, peaches, apricots and citrus fruits (DeBach, 1974). These products have generally been considered to pose low toxicity to humans, vertebrates and non target beneficial insects such as predators and parasitoids (Pimentel, 1971; Brown, 1978). However, studies that take into consideration the agroecosystem as a whole rather than focusing on the organisms present at the canopy level have revealed that these substances are not entirely innocuous, especially among soil organisms. For example, detritivores such as earthworms are strongly affected by products containing copper. Those soils which contain over 100–150 ppm copper are severely damaging to earthworm populations, because only few species can survive in such conditions; these concentrations of copper are surpassed in numerous intensive and tradi- Fig. 6. Earthworm loss in a lowland agroecosystem (Pegolotte di Cona, Venezia, Italy) under different copper inputs (related to application of Bordeaux mixture) in five fields that were either uncultivated or supported vineyards. The copper concentration in the soils (C1–C5) was inversely related to earthworm numbers. Note that the endogeic species A. rosea was present in the very Cu-contaminated plot C5, albeit in low numbers (from Paoletti et al., 1995b). tional grape-growing areas in Europe (e.g., in France, Spain, Italy, Switzerland and Germany). Most endogeic species disappear from copper-contaminated soil (Paoletti et al., 1988), and the number of large burrowing species drastically decreases, e.g., Lumbricus terrestris. On the other hands some species are able to tolerate the presence of high levels of copper, including Aporrectodea (Allolobophora) rosea (Fig. 6) and some epigeic species such as Lumbricus castaneus and L. rubellus. These copper-polluted soils tend to accumulate undecomposed organic material at the surface and become less permeable; although these conditions are unfavorable to most soil biota, they sometimes produce an increase in the biomass of oribatids, collembola and dipteran larvae. Although comparatively little information is available regarding the impact of sulfur, lime and lime sulfate on earthworms, it has been demonstrated that modification of the soil pH by SO2 fallout can influence abundance of soil detritivores (possibly including earthworms) and other biota (Paoletti and Bressan, 1996). M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 149 Table 1 List of earthworm species collected by hand sorting soil cores (30 × 30 × 30 cm3 ). Mean number per m2 of four annual collections in an organic apple orchard, a conventional apple orchard and a nearby coppiced deciduous forest at Lagundo (B Z), Italy (modified from Paoletti et al., 1995a) Earthworms Conventional orchard Organic orchard Coppiced deciduous forest Lumbricus terrestris Lumbricus castaneus Lumbricus rubellus Lumbricus sp. (juveliles) Allolobophora rosea Aporrectodea caliginosa Allolobophora sp. (juveniles) Octolasium lacteum Octolasium sp. (juveniles) Eophila sp. (juveniles) Dendrodrilus rubidus rubidus 1.1 0.0 0.6 2.2 4.4 0.6 1.1 0.0 0.0 0.0 1.1 22.2 2.8 0.6 70.0 1.1 53.3 90.6 11.1 4.4 1.7 1.1 10.1 0.6 1.7 43.3 3.9 12.2 36.7 2.2 0.0 0.6 0.0 Total No. of specimens (m2 ) Total No. of species 11.1 5 258.9 8 111.2 7 Fig. 8. Lumbricus terrestris, at Lautenbach, Germany used as a good indicator of integrated vs. conventional farming. Integrated farming uses mostly shallow tillage (Fig. 6 (b)), and less pesticides compared with conventional farming, which involves plowing and relies more on pesticides. Fig. 7. Seasonal abundance of earthworms per m2 collected during 1 year by handsorting cores (30 × 30 cm2 ) at three sites: an organic apple orchard, a conventional (high input) orchard, and a nearby deciduous woodland (Lagundo, Bolzano, Italy) (from Paoletti et al., 1995a). 18. Assessing farming sustainability: organic versus conventional farms Earthworms are useful for monitoring different farming systems in order to assess comparatively agricultural practices and evaluate soil contamination and management practices (pesticide residues, tillage ef- fects, compaction, organic matter) (Buckerfield et al., 1997). We compared earthworm populations present in organic and conventional apple orchards and in a nearby deciduous woodland located in an intensive apple production area in Alto Adige, Italy (Paoletti et al., 1995a). We observed that both species number, and to a greater extent, population density, decreased from the organic to the conventional (high input) apple orchard (Table 1; Fig. 7). Both the deep-burrowing species Lumbricus terrestris and the surface-dwelling species L. castaneus practically disappeared from the conventional (high input) orchard, thus providing an indication that conventional orchard practices are 150 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 Fig. 9. Epigeic earthworm biomass and abundance in 72 orchards in Emilia Romagna, Italy under different practices and fruit crops (kiwi, apple, peach, grape); tillage differences: p < 0.0001 for biomass and abundance; treatment effect: p < 0.0001 for biomass and abundance (From Paoletti et al., 1998). harmful even to those species that are generally considered to be more resistant to disturbances. It was also noted that sorting earthworms to the species level only slightly improved comparative evaluation among different orchards. The finding that the evaluation of species numbers and population densities revealed the same trend shows that the latter approach, which does not require delving into taxonomy, can be an effective way to assess the impact of farming practices on earthworm populations. Earthworms recover more quickly in response to low input practices associated with organic farming compared with conventional, high input farming (Fig. 7) (Paoletti et al., 1995a). Total earthworm biomass per m2 has been used to evaluate different input farming systems in Switzerland, and demonstrated that integrated farming supports higher earthworm biomass and numbers (Hani, 1990; Matthey et al., 1990). Earthworm biomass, based on the key species Lumbricus terrestris, was the key element used to discriminate between conventional (35 cm moldboard plow) and integrated (20 cm minimum tillage) farming systems in Lautenbach, Germany (El Titi and Ipach, 1989) (Fig. 8). Earthworms have also been used to assess different farming systems at Rodale Research Station in Pennsylvania, USA (Werner and Dindal, 1989), in Japan to assess organic farming (Nakamura and Fujita, 1988) and in Italy to assess different input-orchards (Paoletti et al., 1995a, 1998). Earthworms cannot always respond in a significant way to application of reduced pesticide regimes in arable crops. Although 50% pesticide reduction after 2 years is not well marked by earthworms in a 6-year rotation in England, the comparison had been made considering very different locations and farms located in different soil classes (Tarrant et al., 1997). In practice, farm rotational practices and soil composition can influence the benefits expected to be gained by the limited use of pesticides. 19. Comparing different orchards in an intensive agricultural rural landscape Figs. 9–11 present results of a comparative study of 72 vineyards and kiwi, apple, and peach orchards in an intensive agricultural region (Emilia Romagna, Italy) that were maintained using different input systems, including non tillage and tillage. One general observation coming from these studies is that non tilled orchards have higher earthworm biomass and numbers of earthworm species (Fig. 9) especially if surface (epigeic) earthworm species are considered (e.g., Lumbricus rubellus and L. castaneus). Evaluation of endogeic species did not always reveal consistent differences among vineyards (Fig. 10). This demonstrates that endogeic earthworms and in particular A. caliginosa (Fig. 11) better support agroecosystem manage- M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 151 Fig. 10. Endogeic earthworm biomass and abundance in 72 orchards in Emilia Romagna, Italy under different practices and fruit crops (kiwi, apple, peach, grape); tillage differences: p < 0.0001 for biomass and abundance; treatment effect: p < 0.0001 for biomass and abundance (From Paoletti et al., 1998). Fig. 11. Total biomass and abundance of Aporrectodea caliginosa in 72 orchards in Emilia Romagna, Italy under different practices and fruit crops (apple, vineyard, peach, kiwi). Different letters indicate significant difference in values p < 0.05. ment. Nevertheless, considering total earthworm numbers, the difference between tilled versus non tilled orchards is still evident (Fig. 12). In this study the lowest number of earthworms was reported in the vineyards and was linked to higher amounts of pesticides used (especially copper) (see Fig. 5 (a) and Fig. 13). The highest earthworm biomass was linked to non-tillage associated with kiwi orchards requiring no pesticides. The best way to understand changes in earthworm populations in response to farming practices and/or pollution is to compare a variety of landscapes (Nakamura and Fujita, 1988; El Titi and Ipach, 1989; Werner and Dindal, 1989; Matthey et al., 1990; Paoletti et al., 1995a). Biomass, species number, and ecological groupings are the key factors that enter into comparative evaluations of different farming systems; in such studies, analysis of earthworm populations, in close to natural situations, in rural and disturbed landscapes provides useful reference data on which to base comparisons. Although species numbers can be expected to show a decline from natural forest to rural landscapes, individual species generally do not disappear if the scale of the study is sufficiently large, 152 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 Fig. 12. Total earthworm biomass and abundance in 72 orchards in Emilia Romagna, Italy under different practices and fruit crops (kiwi, apple, peach, grape) tillage differences: p < 0.0001 for biomass and abundance; treatment effect: p < 0.0001 for biomass and abundance (From Paoletti et al., 1998). Fig. 13. Copper and zinc concentrations in soil in 72 orchards in Emilia Romagna, Italy under different practices and fruit crops (kiwi, apple, peach, grape); tillage differences: p < 0.0001 for biomass and abundance; treatment effect: p < 0.0001 for biomass and abundance (From Paoletti et al., 1998). for example, covering cultivated fields and margins, forest plots and hedgerows (Paoletti, 1987). Normally more pronounced is the dramatic loss of numbers and biomass in intensively managed agroecosystems (Table 1) (Paoletti, 1985; Paoletti et al., 1995a). 20. Rural and urbanized landscapes Earthworms have also been utilized in assessments of larger landscapes in various countries, e.g., in an urbanized area of Belgium (Pizl and Josens, 1995) and in a rural area in the Veneto region of Italy (Paoletti, 1985; Paoletti et al., 1988; Paoletti and Sommaggio, 1996), and in forested areas in Belgium (Muys and Granval, 1997). Earthworms provide an accurate picture of contamination and environmental disturbance both in rural landscapes and marginal lands. Mosaic landscapes that include hedgerows, field margins and riverbanks still maintain some diversity of species even if the major portion of the area is under intensive cultivation. Extensive monocultures, conventional tillage and pesticide use are among the key factors that reduce numbers of earthworm species and overall biomass. M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155 Reduction of margins, hedgerows, wind breaks, natural fences and river banks also affects earthworm populations in landscapes. A combination of factors including rotation, mulching and cover crops, reduced tillage and reduced pesticide application are among the key factors permitting a consistent recovery of earthworm biomass and species numbers. 21. Conclusions Earthworms taxonomy is reasonably straightforward even for non experts, at least in temperate countries. Sometimes simple evaluation of numbers or biomass can be sufficiently useful measures. Sorting the earthworms to species, however, can better discriminate the populations into ecological guilds and facilitate more detailed assessments. Their limited mobility makes earthworms very suitable for monitoring the impact of pollutants, changes in soil structure and agricultural practices. Endogeic species are in some cases better able to support pesticide and heavy metal residues than some aneciques-deep borrowing species. Species living on manure, such as Eisenia foetida, support high levels of pesticide residues (like copper) a property that must be taken into consideration if they are to be used as sophisticated tools to monitor pesticides for environmental toxicity. Larger species frequently vanish from rural landscapes. 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