earthworms as bio indicators

Agriculture, Ecosystems and Environment 74 (1999) 137–155

The role of earthworms for assessment of sustainabilityand 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 differentenvironmental transformations and impacts. Agricultural landscapes, urban and industrialized habitats have some earthwormsthat represent interesting indicators to monitor different contaminations, to assess different farming practices and differentlandscape 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 forfurther improved and accurate work in assessing sustainability of different environments. In most cases earthworm biomassor 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 beassessed 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 andterrestrial habitats. Most of the approximately 3500species of so-called earthworms (Oligochaeta) inhabitsoils, including suspended soil habitats on trees, es-pecially in humid tropical forests; others live in sub-merged muds in freshwater bodies and marine bot-

∗ Present address: Dipartimento di Biologia, Universita diPadova, 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 ben-thic fauna (Jamieson, 1988; Brinkhurst and Jamieson,1971). This review concentrates on the earthworms,which are distributed among 18 families. The mostextensively studied and widely distributed family ofearthworms is represented by the Lumbricidae, whichare especially numerous in the Palearctic region. Agri-cultural activities such as plowing, different tillage op-erations, fertilizing and application of chemical pes-ticides have dramatically influenced these animals.Most of the larger species (those over 18–25 cm long)have been displaced from cultivated areas in the trop-ics as well as in temperate rural areas or are presentonly in woodland and grassland patches remaining in

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138 M.G. Paoletti / Agriculture, Ecosystems and Environment 74 (1999) 137–155

mosaic landscapes. The decline of larger earthwormsin rural areas can be worsened as a result of high pre-dation during and after tillage operations, e.g., by otherinvertebrates such as ground beetles, and by ravens,sea gulls (Cuendet, 1987) and other vertebrates.

Earthworms traditionally have been considered tobe convenient indicators of land use and soil fertility.For example, Tanara (1644) stated that the presenceof birds such as ravens, magpies and others that areattracted to a freshly plowed field and scratch on thesoil to uncover and eat the small invertebrates (mostlyearthworms) gives a good indication of agrarian soilfertility. Their relatively large size, ranging from 1 to80 cm or larger (Pop and Postolache, 1987), limitedrapidity in soil displacement and slow recolonizationare features that make earthworms easy to capture andsort and render them attractive as bioindicators. Sub-stantial 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; Paolettiand Bressan, 1996).

2. Taxonomy

Identification of adult earthworms is based mainlyon the position and shape of the clitellum, setae andinternal organs such as seminal vesicles and sper-mathecae. Manuals are available for identification ofearthworms in various countries, including France(Bouché, 1972); Germany (Graff, 1953), Italy (Pao-letti and Gradenigo, 1996), the United Kingdom (Simsand Gerard, 1985), the United States and Canada(Reynolds, 1977; Schwert, 1990), Russia (Perel,1976), and New Zealand (Springett, 1985); a sys-tem for identification of earthworms found in Italy isalso available on CD-ROM (Paoletti and Gradenigo,1996). Useful manuals dealing with earthworm biol-ogy, morphology and ecology include the works ofJamieson (1981), Satchell (1983), Wallwork (1983),Lee (1985) and Edwards and Bohlen (1996).

3. Earthworm abundance and distribution

Fig. 1 summarizes earthworm density, biomass perm2 and species abundance in managed and unmanaged

environments using data from surveys of about 350study sites (found in the LOMBRI-ASSESS database).

Differences in techniques, collection periods, ter-ritory scales and taxonomic expertise must be takeninto consideration when evaluating these data. Never-theless, it is reasonable to conclude the following: (1)pastures and meadows bear higher earthworm densityand biomass; (2) deciduous forest have higher earth-worm biomass and density than coniferous forests; (3)cultivated fields have lower densities than most or-chards. Tropical habitats are not well represented inthese figures but undoubtedly contain more speciesthan indicated by the available data.

4. Collection systems

The choice of earthworm collection methods de-pends on the aim of the sampling campaign, i.e., ob-taining the maximum number of species in one areaor estimating differences among various componentsor locations in a landscape. Sampling methods alwaysrepresent a compromise between effort and labor (andfunds) required and the desire for accurate quantita-tive and qualitative measurements and statistics. Earth-worm sampling should preferably be carried out dur-ing cool and wet seasons; sampling of dry soils (orduring dry seasons) or of frozen soils should alwaysbe avoided. In general sandy soils (over 70% sand),which easily become dry, and strongly acidic soils areinhospitable to earthworms and other soil organisms.In temperate areas, sampling studies in autumn, springand some of the winter months give the best results ifsoil humidity is adequate. Although earthworms canlive in litter, soil, wet mud, submerged mud, organicmanure, composts, dung, under bark and on rottedwood, most earthworm species are adapted to a partic-ular habitat. In the humid tropical forests (for instance,in the cloud forests in Venezuela) some species, some-times the majority, are arboriculous and live in sus-pended soils, such as the soil that accumulates in theleaves rosette of bromeliads, in the tree canopy. Theseearthworms can be collected by photo-eclectors, a spe-cial traps that catch all moving invertebrates on thesurface on trunks (Adis and Righi, 1989).

One active collection system consists of hand sort-ing from soil cores of 25× 25 or 30× 30 cm2 dug toa 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 obtainedfrom 341, 274 and 172 different plots studied in the literature in different countries and climates (LOMBRI-ASSESS data base).


Fig. 1. (Continued).

squares (sides: 50–100 cm) require much effort andtherefore many workers, they are more efficient ingathering large, deep borrowing species (Lavelle,1988). Digging deeper than 20–30 cm into the soilyields few specimens but sometimes reveals inter-esting deep-burrowing species that would be missedin shallow diggings. Sampling repetitions, possiblyin a random design, are needed to assess populationvariability and to demonstrate statistical significanceamong the different prospected sites. Preliminarysamplings can offer basic information and permit bet-ter design of the subsequent sampling campaign; theadvice of a statistician can help in planning a validsampling design.

To assess populations of deep-burrowing and largerspecimens, irritant solutions can be used to stimulatethe earthworms to come to the soil surface, therebyfacilitating collection. One particularly effective tech-nique involves the application of 5–10 l of 0.2–0.5%aqueous formaldehyde solution onto 50× 50 cm2 ofsoil; other irritant chemicals such as potassium per-manganate and copper sulfate have been used with

less success. Formaldehyde treatment is more effec-tive on species producing vertical burrows, e.g.,L. ter-restris, than on those that dig meandering or horizontalburrows (e.g.,Allolobophora rosea) (Bouché, 1975;Lee, 1985). Formaldehyde is not effective in inducingmost tropical large burrowers to exit the soil, e.g., theMegascolecidae and the Glossoscolecidae: e.g., I ob-tained unsatisfactory results when formaldehyde so-lutions was used to collect large earthworms in rainforests and savannas in Venezuela, Ecuador and Viet-nam. One must also keep in mind that formaldehydeis toxic to humans and other animals and burns plantroot systems.

Pitfall traps and soil baits have been successfullyused in some earthworm sampling studies (Lee, 1985).Photo-eclectors arranged around the trunks of treescan also be used to collect earthworms, especiallyin the humid tropics (personal observations). Severalelectrical systems have been tested for the purposeof inducing earthworms to come to the soil surface(Edwards and Bohlen, 1996). For example, a systemconsisting of two electrodes inserted 1 m apart and


50 cm deep in the soil, with a Diesel engine produc-ing 250 V and 2–4 A, has been demonstrated to beeffective. As moisture is a prerequisite for electricalconductivity, this technique is suited only to humidsoils, and becomes more efficient as the soil pH islowered.

5. Ecological classification

Categorizing living creatures based on their eco-logical characteristics is a limited and sometimes am-biguous way to operate, but clearly offers practicaladvantages such as the ability to assess different envi-ronments. Earthworms can be divided into the follow-ing general categories, which take into account basicfeatures 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. Somecorticicoles living under rotted bark can be as-signed to this category.

2. Anéciques are large, deep-burrowing forms thatcome to the soil surface when it is more humid,usually during the night, and draw the litter downinto the lower strata. Sometimes they live insemi-permanent burrows.

3. Endogés live near the surface of soils in the or-ganic horizons and produce mostly horizontal gal-leries.

4. Coprophagic species live in manure, e.g.,Eiseniafoetida (in the Holarctic),Dendrobaena veneta(originally described in northern Italy), andMetaphire schmardae(in China).

5. Arboricolous species live in suspended soils inhumid tropical forests.

Although similar to the epigés, they have large co-coons and can withstand long periods of immersionin water, e.g., in pools of water that accumulate inbromeliads 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 en-dogés are more often used in soil assessment com-pared to coprophagic and arboricolous species.

Surface dwelling epigés such asLumbricus rubel-lus and L. castaneus, which are most vulnerable to

Fig. 2. ArboricolousAndiorrhinusspp. earthworms in suspendedsoils, on bromeliads, in cloud forests in Venezuela (Cordillera dela Costa, Paque Pittier). These arboricolous species produce largecocoons and support long immersion periods, in the water thataccumulates in bromeliads.

desiccation and predation, produce high numbers ofcocoons each year (65–106); endogés such asAl-lolobophora chlorotica, A. caliginosaand A. roseaproduce 8–27 cocoons per year. The deep-burrowinganécique species such asA. longaproduce the low-est numbers of cocoons (3–8 per year) (Lavelle,1981; Curry, 1994); the larger deep-burrowing speciessuch asEophila tellinii, which can reach 80 cm inlength, may produce only 1 or 2 cocoons per year(Braida, 1994). Small numbers of cocoons have alsobeen recorded for the largest specimens in Europe,which are found in the Carpathian mountains andcan attain a length of up to 100–150 cm (Pop andPostolache, 1987; V. Pop, pers. comm., July, 1996).These reproductive data clearly explain why the largerdeep-burrowing species would be the first earthwormsto disappear from disturbed environments. For exam-ple, in a study of earthworm populations in naturaland cultivated areas in the United States, Fender andMcKey-Fender (1990) observed that although nativeMegascolecidae predominate in areas still dominatedby native vegetation, the adventitious Lumbricidaebecome more numerous in agricultural and urbanareas.


6. Agricultural activities and earthworms

Intensification of cropping, annual tillage and otheroperations such as fertilization, irrigation and pesti-cide use consistently affect populations of earthwormsand other invertebrates as well. A long history ofrural landscape transformation has resulted in manychanges in the distribution of earthworm species.Most large earthworms have disappeared from inten-sively tilled rural landscapes. In Europe, the largeOctodrilus, Allolobophora, Eophila and Scherotecaspecies are relicts on hills, mountains and woodlotremnants in rural landscapes. Although large speci-mens also disappear from shifting agricultural gardensin tropical forests, they generally recolonize when thegardens are abandoned to fallow. Very little knowl-edge is available about the composition of species thatcolonized the earliest sites of cultivation such as theFertile Crescent (i.e., 4000–14,000 BC). Most Lum-bricidae species currently present in European rurallandscapes probably adapted to rural environmentsand were passively spread by European peasants col-onizing the United States, New Zealand, Australiaand South America. Species such asAporrectodeacaliginosa, Lumbricus rubellus, L. terrestris, Octo-lasium lacteum, Allolobophora rosea, A. chloroticaand a few others undoubtedly have been dispersedby European colonists. In addition, active earthwormdissemination has been implemented by some farmersin order to improve pasture productivity, e.g., in NewZealand and Australia (Lee, 1991) and in reclaimedpolders in Holland (Hoogerkamp, 1987). These intro-duced species overcome the native ones living in theforested areas.

Some earthworm species have developed amimetic yellow-green color (among Lumbricidae,Allolobophora chloroticaandA. smaragdina; amongthe Megascolecidae, most species living in ruralareas of China (Fang et al., 1999) and in Africansavannas, possibly to avoid predation in grass-likedominated areas. In addition, some species such asEisenia foetidaand Dendrobaena veneta, which arefound living in the cow manure that accumulates atdairy farms, have an annular color pattern that mayserve to protect them from predators in manure heapsand other habitats (Fig. 3). A similar annular colorpattern is shared byEophila tellinii and Octodrilusmima, large species that are generally deep burrowers

but also occasionally feed on soil surface litter whenhumidity in soil is high enough, e.g., in the deciduousforests of northeastern Italy (Paoletti, 1985).

7. Soil and litter type

Native soils with organic matter of the mull andmoder types generally present higher earthworm di-versity and biomass. Sandy soils and sandy heaths usu-ally support smaller populations of earthworms, as doacidic and mor soils (Ghilarov, 1979). Although mostconiferous litter is unacceptable or marginally palat-able to the majority of earthworms, even after weath-ering, earthworms seem to be an important element forregeneration of coniferous stands (Bernier and Ponge,1994). In addition, mostEucalyptusspp., on which re-forestation in temperate and many tropical countriesis based, produce litter that is not attractive to earth-worms and most soil invertebrates, and tends to leadto their disappearance (Curry, 1994). Fresh deciduousforest litter is generally attractive to earthworms onlyafter some weathering and degradation by fungi andbacteria. The necessity for some initial breakdown ofdeciduous plant litter reflects the fact that earthwormsare not well equipped to digest lignin and other prod-ucts derived from cellulose; like other animals, theyrely on symbiotic microflora to break down these andother 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 in-troduced improved soil management methods, includ-ing turning down top soil and controlling weed pres-sure more efficiently. Tillage equipment, especially themachines developed to prepare a smooth seed bed af-ter plowing, creates problems for the deep-burrowingspecies such asL. terrestrisandA. longa, Octodrilusspp. and other larger earthworms found in most Eu-ropean rural landscapes and also sometimes signif-icantly affects surface dwellers such as epigés. Thelarger Megascolecidae are also affected negatively bytillage in China and India. Larger species usually dis-

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appear soon after transformation of a natural soil intoa cultivated field, mostly because of tillage operations.

Minimum tillage, no-tillage and ridge-tillage tendto reduce the loss of earthworm biomass living on thesoil surface, in part because these less invasive soilmixing practices incorporate dead mulch and/or cropresidues 10–15 cm below the surface of the topsoil,or allow it to stay on the soil surface, much like thelitter found in woodlands (Stinner and House, 1990).Some organic farmers have obtained good earthwormmanagement in fields and orchards using a chisel-typetiller that gently mixes the soil without the damagingcutting and slicing action associated with disc plows(Paoletti et al., 1995a). Tillage experiments carriedout at Spray Farm in Ohio, USA demonstrated that,when confined to the soil surface, disc chisel tillingonly moderately affects earthworm biomass in a 4-yearrotation design (hay–corn–soybean–wheat) (personalobservations) (Fig. 4). In addition, certain types ofplows with rotary chisels that restrict tillage to the up-permost part of the soil are better at preserving earth-worm populations than conventional moldboard plows(El Titi and Ipach, 1989). Crop residue left on the soilsurface of non-tilled crops protects earthworms fromdesiccation and/or predation during dry periods (Pao-letti, 1987); thus fields under no-tillage always exhibithigher earthworm biomass than conventionally tilledfields (House and Parmelee, 1985; Clapperton et al.,1997). Experiments carried out at Thompson Farm,IA, USA demonstrated that ridge tillage, which leavesmost organic debris on the soil surface, is also lessdisruptive to earthworm biomass compared to conven-tional moldboard tillage (Fig. 4 (bottom), personal ob-servations).

9. Fertilization and mulching

Adding manure positively affects earthwormbiomass and abundance both in grasslands and fields.Earthworms generally respond better to organic ma-nure than to chemical fertilizers (Curry, 1994). How-ever, liquid manure such as pig slurry can stress earth-worm populations in grasslands and cultivated fieldsif applied in high quantities (e.g., 400 tons ha−1; An-derson, 1980). On several occasions the author haveobserved that farms that are frequently sprayed withliquid cow manure show dramatic decreases in earth-

Fig. 4. (above) Conservation and no tillage systems associatedwith 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 directlyforcast the seeds of crops such as corn and soybean directly onthe sod.

worm biomass (Paoletti, 1985). Given sufficient soilhumidity, application of ‘living’ or ‘dead’ mulch canbe expected to promote earthworm biomass. Incorpo-ration of plant material such as crop residue or a covercrop (not too deep) into the soil improves earthwormactivity and biomass, especially of endogé species.

In apple orchards, Kuhle (1983) demonstrated thatdifferent mulching methods (grass cuttings, choppedwood residues and grass incorporation) can improvediversity, abundance and biomass of earthworms com-pared with bare soil.

10. Pesticides

Although numerous studies have been devoted totoxicity of pesticides to earthworms, many products


have not been tested both in the laboratory and un-der field conditions. In addition to the direct effects ofpesticides, one must consider the toxicity of the manybreakdown products of pesticides that enter the soil;furthermore, the possible synergistic effects of pesti-cide cocktails are not well studied or understood. Pesti-cides can show both direct toxicity against earthwormsand produce latent effects on their growth and fertility.In addition, pesticide-contaminated earthworms canrepresent a source of contamination of higher mem-bers of the food web, e.g., seagulls and other birds.Pesticides usually enter the soil as residues of spraysapplied to crop plants from above ground, and areless frequently applied directly on soils, as is the casefor nematicides and root pest control agents. Targetsof root pest control agents includeDiabrotica bee-tles, which are especially noxious to corn and soybeancrops in the US, and larvae of beetles such as Ela-teridae and Alticinae, which attack the roots of sugar-beets and corn plantlets in Europe. Insecticides such asphorate and carbofuran are very deleterious to earth-worms when applied to soil (Edwards and Bohlen,1992). Pesticides usually reach the soil as mixtures ofseveral products, especially in orchards. Upon entryinto the soil, such mixtures are expected to have thegreatest effects on earthworms feeding at the soil sur-face, i.e., epigeic, surface dwelling earthworms suchasLumbricus rubellusandL. castaneus.

In orchards, grasslands and on row crops, slurriesand sewage sludge are sometimes applied. Theseproducts create problems for the soil foodwebs. Soiltoxicity resulting from introduction of contaminantssuch as heavy metals and PCBs can be monitored byearthworm numbers and dynamics (Kreis et al., 1987;Curry, 1994).

11. ‘Archeological’ pesticide residues

High quantities of residues of ‘archeological’ pes-ticides can be found in many rural areas, especiallythose that traditionally have supported intensive or-chards or industrial crops such as cotton or other in-dustrial crops. Examples of such residues are: arsenic,a breakdown product of lead arsenites used at the be-ginning of this century and banned in Great Britainin 1960 (Sheail, 1985); DDT, banned in 1971 in theUnited States and most other countries but still used in

some areas, including China (Mellanby, 1992); cop-per, a component of bordeaux mixture (and similarcompounds), especially common in vineyards in mostEuropean countries; and zinc, a component of carba-mate fungicides. Despite the fact that some microor-ganisms are able to degrade arsenic compounds (Ah-mann et al., 1994) and that organochloride compoundshave been shown to be broken down in organic or-chards (Paoletti et al., 1995a), their presence can stillcause toxicity problems in intensively farmed rurallandscapes. Although research on these contaminantshas not yet been extensively pursued, the fact that thesesubstances accumulate and persist in the soil suggeststhat earthworms and other invertebrates could be usedto test such problems. For example, a study carriedout by Fang et al. (1999) in subtropical China demon-strated an inverse correlation between the concentra-tion of arsenic in the soil and abundance of Megas-colecidae earthworms.

12. Fungicides

Fungicides are generally highly toxic to earth-worms, especially copper and zinc residues fromcopper sulfate and carbamates, respectively. Soilfumigants, nematicides and fungicides such asD–D mixture (dichloropropane : dichloropropene),metham-sodium and methyl bromide are highly toxicto earthworms. The majority of fumigants and con-tact nematicides are toxic to earthworms as well(Edwards and Bohlen, 1992). Carbamate fungicidessuch as benomyl and carbendazim are also highlytoxic to earthworms. For example it has been re-ported that about 1.8 kg ha−1 per year of benomylmay destroy all theLumbricus terrestrisand most oftheAllolobophoraspp. present in an apple orchard inEngland (Stringer and Wright, 1976; Brown, 1978).The degree of toxicity of the more traditional coppersulfates is controversial. At the laboratory level, testsspecifically developed forEisenia foetida(a lumb-ricid species living only in manure) suggest coppersulfates 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 iscompletely absent from fields and is not representa-tive of the earthworm fauna in rural landscapes. Somestudies have demonstrated that the toxicity of copper


Fig. 5. Relationship between content of copper (a) and zinc (b) in soil and earthworm abundance in 72 orchards in Emilia Romagna, Italyunder different practices and fruit crops (kiwi, apple, peach, grape). Copper is a residue from bordeaux mixture, applied as fungicide, andzinc 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 or-ganic matter in the soil increases (Jaggy and Streit,1982). Direct tests have shown that concentrations ofcopper in the soil ranging between 100 and 150 ppmare in most cases sufficient to produce a consistent

decrease in earthworm numbers (Fig. 5 (a)). Thus itis worrisome that higher concentrations of copper arefound in the soil in many orchards around the world.As shown in Fig. 5 (b), zinc also has toxic effects onearthworms.


13. Insecticides

Earthworms are strongly affected by many types ofinsecticides, which may be applied directly to the soilor enter the soil from treated crops. The insecticidesmost commonly used in current agricultural practiceinclude the following:Organochlorine insecticides: DDT, Aldrin, Dieldrinand BHC show low toxicity against earthworms;Heptachlor, Endosulfan, and Isobenzan are moder-ately toxic; Endrin and Chlordane, lindane are verytoxic (Edwards and Bohlen, 1992; Slimax, 1997).

Organophosphate insecticides: phorate, which isused as a granular soil insecticide to control certainsoil pests, shows high toxicity against earthworms(Way and Scopes, 1968); other organophosphatesare moderately toxic (Edwards and Bohlen, 1992).

Carbamate insecticides (and fungicides): these prod-ucts are generally highly toxic to earthworms;application of Carbofuran to soil has been shownto strongly affect earthworms (Haque and Ebing,1983; Edwards and Bohlen, 1992).

Natural and synthetic pyrethroids: those that havebeen tested do not appear to be toxic to earthworms(Edwards and Bohlen, 1992). However, in the au-thor’s view additional research is needed in order toreach solid conclusions regarding the possible tox-icity of this class of insecticides.

14. Herbicides

Although most herbicides are considered to exert lit-tle direct impact on earthworms (Edwards and Bohlen,1996), the reduced weed cover resulting from their ap-plication obviously can render habitats less hospitableto earthworms. Laboratory tests have shown that theherbicides bentazon, bromphenoxin, bromoxynil, bro-moxynil octaonate/ioxynil and atrazine are moderatelytoxic to earthworms (Pizl, 1988). Some large spec-trum herbicides, e.g., glyphosate, are quite harmful toearthworms such asAporrectodea caliginosaeven atvery low doses (Springett and Gray, 1992).

Epigeic earthworms such asAllolobophora chlorot-ica and endogeicA. roseaseem to be negatively af-fected in grasslands spread with atrazine and pen-tachlorophenol (PCP) (Conrady, 1986).

15. Heavy metals

Heavy metals can enter the soil from differentsources. Fertilizers, pesticides, organic and inorganicamendants, wastes and sludge residues can containvariable amounts of these metals.

Treatment of orchards and vineyards with coppersulfate strongly affects soil invertebrates, especiallyearthworms (Rhee, 1977a, 1977b; Ireland, 1979; Pao-letti, 1985; Paoletti et al., 1988;) in terms of bothbiomass and species population response (Paoletti etal., 1988). Although their sensitivity to copper sul-fate suggests that earthworms would be suitable asmonitors of this source of soil contamination, suchearthworm-based assessment is complicated by thefact that earthworms can develop tolerance to thesepollutants, as documented in several studies of popu-lations that have been in contact with high pollutingsources over long periods (Bengtsson and Rundgren,1992; Bengtsson et al., 1992; Fisher and Koszorus,1992; Morgan and Morgan, 1992). The direct mea-surement of heavy metal concentrations in earthwormtissues could provide a means of assessing environ-mental pollution levels, given the demonstrated cor-relation between soil contamination and earthwormmetal bioaccumulation (Motalib et al., 1997). How-ever, in practice, many different residues accumulatein soils, and their many potential interactions are farfrom understood (Mari et al., 1997).

16. Engineered crops

Agriculture was the first arena to support the de-velopment and practical application of genetic engi-neering to improve crop yields and quality. Over twothousand field trial releases of different transgeniccrop plants have been carried out in various coun-tries. Attributes of plants currently manipulated bygenetic engineering include herbicide tolerance (47%of the transgenic plants generated to date); insect re-sistance (25%) altered product quality (20%); resis-tance to viruses (17%); and bacterial and fungal re-sistance (5%) (Gene Exchange, 1994). A growing listof Genetically Modified Organisms (GMOs), includ-ing microorganisms, animals and crop plants, are al-ready available or will soon be introduced to the mar-


ketplace. For example, a genetically modified formof Agrobacterium radiobacterhas been commerciallyavailable since 1988, at least in Australia. Engineeredcotton and corn containing theBacillus thuringiensis(BT) toxin, effective against some key lepidopteranpests, have been on the market since 1995, and cropssuch as engineered cotton, corn and soybeans that areresistant to the herbicide glyphosate, and cotton, cornand potatoes engineered with BT toxin will soon becommercially available. Risk assessment is a funda-mental step in evaluating these new GMOs beforelarge-scale release. The soil biota, and earthworms inparticular, can offer a reliable tool for monitoring thepossible effects of GMOs on non target soil organisms,especially in the case of transgenic plants exhibitingaltered resistance to insects and viruses. For exam-ple, if it is expected that plants engineered with BTtoxin would be incorporated into soils, then it wouldbe useful to evaluate the impact of the toxin againstnon target organisms, earthworms included (Jepsonet al., 1994; Paoletti and Pimentel, 1995; Paoletti andPimentel, 1996).

17. Assessing environmental stress

17.1. Using earthworms to monitor the effects offungicides

Wood ashes, sulfur, lime, lime sulfate and coppersulfate have been applied for many years to plants at-tacked by fungi, including fruit crops such as grapes,apples, pears, peaches, apricots and citrus fruits (De-Bach, 1974). These products have generally been con-sidered to pose low toxicity to humans, vertebratesand non target beneficial insects such as predatorsand parasitoids (Pimentel, 1971; Brown, 1978). How-ever, studies that take into consideration the agroe-cosystem as a whole rather than focusing on the or-ganisms present at the canopy level have revealedthat these substances are not entirely innocuous, es-pecially among soil organisms. For example, detri-tivores such as earthworms are strongly affected byproducts containing copper. Those soils which con-tain over 100–150 ppm copper are severely damagingto earthworm populations, because only few speciescan survive in such conditions; these concentrations ofcopper are surpassed in numerous intensive and tradi-

Fig. 6. Earthworm loss in a lowland agroecosystem (Pegolottedi Cona, Venezia, Italy) under different copper inputs (related toapplication of Bordeaux mixture) in five fields that were eitheruncultivated or supported vineyards. The copper concentration inthe soils (C1–C5) was inversely related to earthworm numbers.Note that the endogeic speciesA. roseawas present in the veryCu-contaminated plot C5, albeit in low numbers (from Paoletti etal., 1995b).

tional grape-growing areas in Europe (e.g., in France,Spain, Italy, Switzerland and Germany). Most endo-geic species disappear from copper-contaminated soil(Paoletti et al., 1988), and the number of large bur-rowing species drastically decreases, e.g.,Lumbricusterrestris. On the other hands some species are ableto tolerate the presence of high levels of copper, in-cluding Aporrectodea(Allolobophora) rosea(Fig. 6)and some epigeic species such asLumbricus castaneusand L. rubellus. These copper-polluted soils tend toaccumulate undecomposed organic material at the sur-face and become less permeable; although these con-ditions are unfavorable to most soil biota, they some-times produce an increase in the biomass of oribatids,collembola and dipteran larvae. Although compara-tively little information is available regarding the im-pact of sulfur, lime and lime sulfate on earthworms,it has been demonstrated that modification of the soilpH by SO2 fallout can influence abundance of soil de-tritivores (possibly including earthworms) and otherbiota (Paoletti and Bressan, 1996).


Table 1List of earthworm species collected by hand sorting soil cores (30× 30× 30 cm3). Mean number per m2of four annual collections inan organic apple orchard, a conventional apple orchard and a nearby coppiced deciduous forest at Lagundo (B Z), Italy (modified fromPaoletti et al., 1995a)

Earthworms Conventional orchard Organic orchard Coppiced deciduous forest

Lumbricus terrestris 1.1 22.2 10.1Lumbricus castaneus 0.0 2.8 0.6Lumbricus rubellus 0.6 0.6 1.7Lumbricussp. (juveliles) 2.2 70.0 43.3Allolobophora rosea 4.4 1.1 3.9Aporrectodea caliginosa 0.6 53.3 12.2Allolobophorasp. (juveniles) 1.1 90.6 36.7Octolasium lacteum 0.0 11.1 2.2Octolasiumsp. (juveniles) 0.0 4.4 0.0Eophila sp. (juveniles) 0.0 1.7 0.6Dendrodrilus rubidus rubidus 1.1 1.1 0.0

Total No. of specimens (m2) 11.1 258.9 111.2Total No. of species 5 8 7

Fig. 7. Seasonal abundance of earthworms per m2 collected during1 year by handsorting cores (30× 30 cm2) at three sites: an organicapple orchard, a conventional (high input) orchard, and a nearbydeciduous woodland (Lagundo, Bolzano, Italy) (from Paolettiet al., 1995a).

18. Assessing farming sustainability: organicversus conventional farms

Earthworms are useful for monitoring differentfarming systems in order to assess comparatively agri-cultural practices and evaluate soil contamination andmanagement practices (pesticide residues, tillage ef-

Fig. 8. Lumbricus terrestris, at Lautenbach, Germany used as agood indicator of integrated vs. conventional farming. Integratedfarming uses mostly shallow tillage (Fig. 6 (b)), and less pesticidescompared with conventional farming, which involves plowing andrelies more on pesticides.

fects, compaction, organic matter) (Buckerfield et al.,1997). We compared earthworm populations presentin organic and conventional apple orchards and in anearby deciduous woodland located in an intensiveapple production area in Alto Adige, Italy (Paolettiet al., 1995a). We observed that both species number,and to a greater extent, population density, decreasedfrom the organic to the conventional (high input) ap-ple orchard (Table 1; Fig. 7). Both the deep-burrowingspeciesLumbricus terrestrisand the surface-dwellingspeciesL. castaneuspractically disappeared fromthe conventional (high input) orchard, thus providingan indication that conventional orchard practices are


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 con-sidered to be more resistant to disturbances. It wasalso noted that sorting earthworms to the species levelonly slightly improved comparative evaluation amongdifferent orchards. The finding that the evaluation ofspecies numbers and population densities revealedthe same trend shows that the latter approach, whichdoes not require delving into taxonomy, can be an ef-fective way to assess the impact of farming practiceson earthworm populations. Earthworms recover morequickly in response to low input practices associatedwith organic farming compared with conventional,high input farming (Fig. 7) (Paoletti et al., 1995a).Total earthworm biomass per m2 has been used toevaluate different input farming systems in Switzer-land, and demonstrated that integrated farming sup-ports higher earthworm biomass and numbers (Hani,1990; Matthey et al., 1990). Earthworm biomass,based on the key speciesLumbricus terrestris, wasthe key element used to discriminate between conven-tional (35 cm moldboard plow) and integrated (20 cmminimum tillage) farming systems in Lautenbach,Germany (El Titi and Ipach, 1989) (Fig. 8). Earth-worms have also been used to assess different farmingsystems at Rodale Research Station in Pennsylvania,USA (Werner and Dindal, 1989), in Japan to assessorganic farming (Nakamura and Fujita, 1988) and inItaly to assess different input-orchards (Paoletti et al.,1995a, 1998).

Earthworms cannot always respond in a significantway to application of reduced pesticide regimes inarable crops. Although 50% pesticide reduction after2 years is not well marked by earthworms in a 6-yearrotation in England, the comparison had been madeconsidering very different locations and farms locatedin different soil classes (Tarrant et al., 1997). In prac-tice, farm rotational practices and soil composition caninfluence the benefits expected to be gained by thelimited use of pesticides.

19. Comparing different orchards in an intensiveagricultural rural landscape

Figs. 9–11 present results of a comparative studyof 72 vineyards and kiwi, apple, and peach orchardsin an intensive agricultural region (Emilia Romagna,Italy) that were maintained using different input sys-tems, including non tillage and tillage. One general ob-servation coming from these studies is that non tilledorchards have higher earthworm biomass and num-bers of earthworm species (Fig. 9) especially if sur-face (epigeic) earthworm species are considered (e.g.,Lumbricus rubellusandL. castaneus). Evaluation ofendogeic species did not always reveal consistent dif-ferences among vineyards (Fig. 10). This demonstratesthat endogeic earthworms and in particularA. caligi-nosa(Fig. 11) better support agroecosystem manage-


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 ofAporrectodea caliginosain 72 orchards in Emilia Romagna, Italy under different practices andfruit crops (apple, vineyard, peach, kiwi). Different letters indicate significant difference in valuesp< 0.05.

ment. Nevertheless, considering total earthworm num-bers, the difference between tilled versus non tilledorchards is still evident (Fig. 12).

In this study the lowest number of earthworms wasreported in the vineyards and was linked to higheramounts of pesticides used (especially copper) (seeFig. 5 (a) and Fig. 13). The highest earthworm biomasswas linked to non-tillage associated with kiwi orchardsrequiring no pesticides.

The best way to understand changes in earth-worm populations in response to farming practicesand/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; Pao-letti et al., 1995a). Biomass, species number, andecological groupings are the key factors that enter intocomparative evaluations of different farming systems;in such studies, analysis of earthworm populations,in close to natural situations, in rural and disturbedlandscapes provides useful reference data on whichto base comparisons. Although species numbers canbe expected to show a decline from natural forest torural landscapes, individual species generally do notdisappear if the scale of the study is sufficiently large,


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). Normallymore pronounced is the dramatic loss of numbersand biomass in intensively managed agroecosystems(Table 1) (Paoletti, 1985; Paoletti et al., 1995a).

20. Rural and urbanized landscapes

Earthworms have also been utilized in assessmentsof larger landscapes in various countries, e.g., in anurbanized 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 andGranval, 1997). Earthworms provide an accurate pic-ture of contamination and environmental disturbanceboth in rural landscapes and marginal lands. Mosaiclandscapes that include hedgerows, field margins andriverbanks still maintain some diversity of species evenif the major portion of the area is under intensive cul-tivation. Extensive monocultures, conventional tillageand pesticide use are among the key factors that reducenumbers of earthworm species and overall biomass.


Reduction of margins, hedgerows, wind breaks, nat-ural fences and river banks also affects earthwormpopulations in landscapes. A combination of factorsincluding rotation, mulching and cover crops, reducedtillage and reduced pesticide application are among thekey factors permitting a consistent recovery of earth-worm biomass and species numbers.

21. Conclusions

Earthworms taxonomy is reasonably straightfor-ward even for non experts, at least in temperatecountries. Sometimes simple evaluation of numbersor biomass can be sufficiently useful measures. Sort-ing the earthworms to species, however, can betterdiscriminate the populations into ecological guildsand facilitate more detailed assessments.

Their limited mobility makes earthworms verysuitable for monitoring the impact of pollutants,changes in soil structure and agricultural practices.Endogeic species are in some cases better able tosupport pesticide and heavy metal residues than someaneciques-deep borrowing species. Species living onmanure, such asEisenia foetida, support high levelsof pesticide residues (like copper) a property thatmust be taken into consideration if they are to beused as sophisticated tools to monitor pesticides forenvironmental toxicity.

Larger species frequently vanish from rural land-scapes. Among these large species, deep-borrowingspecies are dominant. The absence or presence of thelarge borrowing species in disturbed landscapes canserve as a useful indicator of environmental degrada-tion or rehabilitation.

Practices that are in general related to low inputfarming, improve earthworm abundance and diversityin rural landscapes.

Acknowledgements

The author thanks Donna D’Agostino for editing themanuscript and Patrick Lavelle, Lisa Lobry de Bruyn,Sam James, Joachim Adis, Daniele Sommaggio andJ.W. Sturrock for critically reading the manuscriptand offering suggestions for its improvement. Michele

Scarso helped with the LOMBRI-ASSESS data basecompilation.

References

Adis, J., Righi, G., 1989. Mass migration and life cycle adaptation— a survival strategy of terrestrial earthworms in centralAmazonian inundation forests. Amazoniana 11 (1), 23–30.

Ahmann, D., Robert, A.L., Krumholz, L.R., Morel, F.M.M., 1994.Microbe grows by reducing arsenic. Nature 371, 750.

Anderson, C., 1980. The influence of farmyard manure and slurryon the earthworm population (Lumbricidae) in arable soil. Proc.VIIth Int. Soil Zool. Colloq., Syracuse, NY, USA, pp. 325–335.

Bernier, N., Ponge, J.F., 1994. Humus form dynamics duringthe sylvogenetic cycle in a mountain spruce forest. Soil Biol.Biochem. 26 (2), 183–220.

Bouché, M.B., 1972. Lonbriciens de France. Ecologie etSystematique. Insitut Nationale de la Recherche Agronomique.

Bouché, M.B., 1975. Fonctions des lombriciens IV. Corrections etutilizations des distorsions causees par la methodes de capture.In: Vannek, J. (Ed.), Progress in Soil Zoology Junk. The HagueAcademia, Prague, pp. 571–582.

Bouché, M., 1977. Strategies lombriciemnnes. Ecol. Bull.,Stockholm 25, 122–132.

Braida, V., 1994. Ecologia e distribuzione geografica di unlombrico di grandi dimensioni: Eophila tellinii (Rosa, 1888).Tesi di Laurea, Dipartimento di Biologia, Università di Padovaa/a 1993/94.

Brinkhurst, R.O., Jamieson, B.G.M., 1971. Aquatic Oligochaetaof the World. University of Toronto Press, 860 pp.

Brown, A.W.A., 1978, Ecology of Pesticides. Wiley, New York.Buckerfield, J.C., Lee, K.E., Davoren, C.W., Hannay, J.N., 1997.

Earthworms as indicators of sustainable production in drylandcropping in southern Australia. Soil Biol. Biochem. 29 (3,4),547–554.

Clapperton, J.M., Miller, J.J., Larney, F.J., 1997. Earthwormpopulations as affected by longterm tillage practices in southernAlberta, Canada. Soil Biol. Biochem. 29 (3,4), 631–633.

Conrady, D., 1986. Okologische Untersuchungen uber dieWirkung von Umweltchemikalien auf die Tiergemeinschafteines Grunlandes. Pedobiologia 29, 273–284.

Cuendet, 1987. Some aspects of the ecology of earthworms inthe Alps. In Bonvicini Pagliai, A.M., Pmodeo, P. (Eds.), OnEarthworms, Mucchi, Modena, pp. 251–263.

Curry, J.P., 1994. Grassland Invertebrates. Chapman & Hall,London, 437 pp.

DeBach, P., 1974. Biological Control by Natural Enemies.Cambridge University Press, Cambridge, 323 pp.

Edwards, C.A., Bohlen, P.J., 1992. The effects of toxic chemicalson earthworms. Rev. Environ. Contam. Toxicol. 125, 23–99.

Edwards, C.A., Bohlen, P.J., 1996. Biology and Ecology ofEarthworms. Chapman & Hall, London, 426 pp.

El Titi, X., Ipach, U., 1989. Soil fauna in suastainable agriculture:results of an integrated farming system at Lautenbach, FRG.Agric. Ecosyst. Environ. 27, 561–572.


Fang, Ping, Wenliang, Wu, Qin, Xu, Jiahai, He, Chunru, Han,Paoletti, M.G., 1999. Assessing bioindication with earthwormsin an intensive rural landscape(Yuanqiao and Daqiao villages insubtropical China, Hubei Province), Crit. Rev. Plant Sciences,18 (3).

Fender, W.M., McKey-Fender, D., 1990. Oligochaeta: Mega-scolecidae and other earthworms from western North America.In: Dindal, D.L. (Ed.), Soil Biology Guide, pp. 357–378.

Ghilarov, M.S., 1979. Soil fauna of brown soil in the Caucasusbeech and fir mixed forests and some other communities.Pedobiologia 19, 408–424.

Graff, O., 1953. Die Re genwurmer Deutschlands. Schrift. Forsch.Land. Braunschweig-Volk 7, 81.

Hani, F., 1990. Farming systems research at Ipsach, Switzerland.The ‘third way’ project. Schweiz. Landw. Fo. RechercheAgronom. en Suisse 29 (4), 257–271.

Haque, A., Ebing, W., 1983. Toxicity determination of pesticidesto earthworms in the soil substrate. Z. PflanzenkrankPflanzenschutz 90, 395–408.

Hoogerkamp, M., 1987. Effect of earthworms on the productivityof grassland, an evaluation. In: Bonvicini Pagliai, A.M.,Omodeo, P. (Eds.), On Earthworms, Mucchi, Modena, pp.485–495.

House, G.J., Parmelee, R.W., 1985. Comparison of soilarthropods and earthworms from conventional and no-tillageagroecosystems. Soil Tillage Res. 5 (4), 351–360.

Jaggy, A., Streit, B., 1982. Toxic effects of soluble copper onOctolasium cyaneumSav. Rev. Suisse Zool. 4, 881–889.

Jamieson, B.G.M., 1981. The Ultrastructure of Oligochaeta.Academic Press, London, 462 pp.

Jamieson, B.G.M., 1988. On the phylogeny and higer classificationof the Oligochaeta. Cladistics 4 (4), 367–401.

Jepson, P.C., Croft, B.A., Pratt, G.E., 1994. Test systems todetermine the ecological risk posed by toxin release fromBacillus thuringensisgenes in croplands. NP Ecol. 3, 81–89.

Kreis, B., Edwards, P., Cuendet, G., Tarrandellas, J., 1987.The dynamics of RCBs between earthworm populations andagricultural soils. Pedobiologia 30, 379–388.

Kuhle, J.C., 1983. Adaptation of earthworm populations todifferent soil treatments in apple orchard. In: Lebrun, Ph.,Andre, H.M., De Medts, A., Gregoire-Wibo, C., Wauthy, G.(Eds.), Proc. VIII Int. Colloq. Soil Zool., Louvain-la-Neuve,OttinginesLouvain-la-Neuve, pp. 487–501.

Lavelle, P., 1981. Strategies de reproduction chez les vers de terre.Acta Oecologica, Oecologia Generalis 2, 117–133.

Lavelle, P., 1988. Assessing the abundance ane role of invertebratecommunities in tropical soils: aims and methods. J. Afr. Zool.102, 275–283.

Lee, K.E., 1985. Earthworms. Their Ecology and Relationshipswith soils and Land Use. Academic Press, Sydney, 411 pp.

Lee, K.E., 1991. The diversity of soil organisms. In:Hawksworth, D.L. (Ed.), The Biodiversity of Microorganismsand Invertebrates: Its Role in Sustainable Agriculture. CABInternational, pp. 73–87.

Malecki, M.R., Neuhauser, E.F., Goehr, R.C., 1982. The effects ofheavy metals on the growth and production ofEisenia foetida.Pedobiologia 24, 129–137.

Mari, P.J., Marinussen, J.P., Sjoerd, E.A., Van der Zee, T.M., 1997.Cu accumulation byLumbricus rubellusas affected by totalamount of Cu in soil, soil moisture, soil moisture and soilheterogeneity. Soil Biol. Biochem. 29 (3,4), 641–647.

Matthey, W., Zettel, J., Bieri, M., 1990. Invertebresbioindicateurs de la qualite de sols agricoles NationalenForschungsprogrammes ‘bonen’. Liebefeld-Bern, 141 pp.

Mellanby, K., 1992. The DDT Story. Unwin Brothers Limited,Old Working, Surrey, UK, 113 pp.

Morgan, J.E., Morgan, A.J., 1992. Heavy metal concentrationsin the tissues, ingesta, ingesta and faeces of physiologicallydifferent earthworm species. Soil Biol. Biochem. 24 (12), 1691–1697.

Motalib, A., Rida, M.A., Bouché, M.B., 1997. Heavy metallinkages with mineral, organic, organic and living soilcompartments. Soil Biol. Biochem. 29 (3,4), 649–655.

Muys, B., Granval, P., 1997. Earthworms as bio-indicators of forestsite quality. Soil Biol. Biochem. 29 (3,4), 323–328.

Nakamura, Y., Fujita, M., 1988. Abundance of lumbricidsand enchytraeids in an organically farmed field in northernHokkaido, Japan. Pedobiologia 32, 11–14.

Neuhauser, E.F., Hartenstein, R., Connors, W.J., 1978. Soilinvertebrates and the degradation of vanilin, cinnamic acid, andlignins. Soil Biol. Biochem. 10, 431–435.

Paoletti, M.G., 1985. Soil invertebrates in cultivated anduncultivated soils in northeast Italy. Redia 71, 501–563.

Paoletti, M.G., 1987. Soil tillage, soil predator dynamics, controlof cultivated plant pests. In: Striganova, B.R. (Ed.), Soil Faunaand Soil Fertility, Nauka, Moscow, pp. 417–422.

Paoletti, M.G., Bressan, M., 1996. Soil invertebrates asbioindicators of human disturbance. Crit. Rev. Plant Sci. 15(1), 21–62.

Paoletti, M.G., Gradenigo, C., 1996. Lombri Cd-ROM. An easyidentification key for italian earthworms. Padova University,Lapis, Padova. e-mail: [email protected]; web page:http://www.bio.unipd.it/∼paoletti/.

Paoletti, M.G., Pimentel, D., 1995. The environmental andeconomic costs of herbicide resistance and host-plant resistanceand host-plant resistance to plant pathogens and insects.Technological Forecasting and Social Change 50, 9–23.

Paoletti, M.G., Pimentel, D., 1996. Genetic engineering inagriculture and the environment. Bioscience 46 (9), 665–673.

Paoletti, M.G., Sommaggio, D., 1996. Biodiversity indicatorsfor sustainability. Assessment of rural landscapes. In: VanStraalen, N.M., Krivolutskii, D.A. (Eds.), New Approaches tothe Development of Bioindicator Systems for Soil Pollution.Kluwer Academic Publishers, in press.

Paoletti, M.G., Iovane, E., Cortese, M., 1988. Pedofaunabioindicators as heavy metals in five agroecosystems innorth-east Italy. Rev. Ecol. Biol. Sol. 25 (1), 33–58.

Paoletti, M.G., Schweigl, U., Favretto, M.R., 1995a.Soil microinvertebrates, heavy metals, heavy metals andorganochlorines in low and high input apple orchards andcoppiced woodland. Pedobiologia 39, 20–33.

Paoletti, M.G., Sommaggio, D., Petruzzelli, G., Pezzarossa, B.,Barbafieri, M., 1995b. Soil invertebrates as monitoring tools foragricultural sustainability. Polskie Pismo Entomologiczne 64,113–122.


Paoletti, M.G., Sommaggio, D., Favretto, M.R., Petruzzelli, G.,Pezzarossa, B., Barbafieri, M., 1998. Earthworms as usefulbioindicators of agroecosystem sustainability in different inpurorchards. Appl. Soil Ecol. 10, 137–150.

Perel, T.S., 1976. A critical analysis of the lumbricidae generasystem (with a key to the USSR fauna genera). Rev. Ecol. Biol.Sol. 13 (4), 635–644.

Pimentel, D., 1971. Ecological Effects of Pesticides on Non-targetSpecies. Executive Office of the President, US GovernmentPrinting Office, Washington, DC, 220 pp.

Pizl, V., 1988. Interactions between earthworms and herbicides 1.Toxicity of some herbicides to hearthworms in laboratory tests.Pedobiologia 32, 227–232.

Pizl, V., Josens, G., 1995. Earthworm communities along a gradientof urbanization. Environ. Pollut. 90 (1), 7–14.

Pop, V.V., Postolache, T., 1987. Giant earthworms build uo vermicmountain rendzinas. In: Bonvicini Pagliai, A., Omodeo, P. (Ed.),On Earthworms. Mucchi, Modena, pp. 141–150.

Rhee, J., 1977a. A study of the of the effect of earthworms onorchard productivity. Pedobiologia 17, 107–114.

Rhee, J., 1977b. Effects of soil pollution on earthworms.Pedobiologia 17, 201–208.

Reynolds, J.W., 1977. The Earthworms (Lumbricidae andSparganophilidae) (Anellidae Oligochaeta) of Ontario. Life Sci.Misc. Publ. R. Ont. Mus. pp. 1–144.

Satchell, J.E., 1983. Earthworm Ecology: From Darwin toVermiculture. Chapmann & Hall, London.

Schwert, D.P., 1990. Oligochaeta: Lumbricidae. In: Dindal, D.L.(Ed.), Soil Biology Guide, pp. 341–356.

Sheail, J., 1985. Pesticides and Nature Conservation. The BritishExperience 1950–1975. Clarendon press, Oxford, 276 pp.

Sims, R.W., Gerard, B.M., 1985. Earthworms: synopsis of Britishfauna. Nat Hist. Museum, London 31, 1–171.

Slimax, K.M., 1997. Avoidance response as sublethal effect ofpesticides onLumbricus terrestris(Oligochaeta). Soil Biol.Biochem. 29 (3,4), 713–715.

Springett, J.A., 1985. Soils: earthworms identification of commonspecies. Min. Agriculture Fisheries, Wellington, New Zeland,4 pp.

Springett, J.A., Gray, R.A.J., 1992. Effect of repeated lowdoses of biocides on the earthwormAporrectodea caliginosain laboratory culture. Soil Biol. Biochem. 24 (12), 1739–1744.

Stinner, B.R., House, G.J., 1990. Arthropods and otherinvertebrates in conservation-tillage agriculture. Ann. Rev.Entomol. 35, 299–318.

Stringer, A., Wright, M.A., 1976. The toxicity of Benomyland some related 2-substituted benzimidazoles to earthwormLumbricus terrestris. Pestic. Sci. 7, 459–464.

Tanara, V., 1644. L’economia del cittadino in villa, 10th ed. G.Bortoli, Venezia, 525 pp.

Tarrant, K.A., Field, S.A., Langton, S.D., Hart, A.D.M., 1997.Effects on earthworm populations of reducing pesticide use inarable crop rotations. Soil Biol. Biochem. 29 (3,4), 657–661.

Wallwork, J.A., 1983. Earthworm Biology. Edward Arnold,London, 58 pp.

Way, M.J., Scopes, N.E.A., 1968. Studies on the persistence andeffects on soil fauna of some soil-applied systemic insecticides.Ann. Appl. Biol. 62, 199–214.

Werner, M.R., Dindal, D.L., 1989. Earthworm communitydynamics in conventional and low-input agroecosystems. Rev.Écol. Biol. Sol. 26 (4), 427–437.

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