Download The role of earthworms for assessment of sustainability and as

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
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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
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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).
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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
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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.
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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-
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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
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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
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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-
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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,
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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. Among these large species, deep-borrowing
species are dominant. The absence or presence of the
large borrowing species in disturbed landscapes can
serve as a useful indicator of environmental degradation or rehabilitation.
Practices that are in general related to low input
farming, improve earthworm abundance and diversity
in rural landscapes.
Acknowledgements
The author thanks Donna D’Agostino for editing the
manuscript and Patrick Lavelle, Lisa Lobry de Bruyn,
Sam James, Joachim Adis, Daniele Sommaggio and
J.W. Sturrock for critically reading the manuscript
and offering suggestions for its improvement. Michele
153
Scarso helped with the LOMBRI-ASSESS data base
compilation.
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