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Environmental Pollution 107 (2000) 233±238
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Decomposer animals and bioremediation of soils
J. Haimi*
Department of Biological and Environmental Science, University of JyvaÈskylaÈ, PO Box 35, FIN-40351 JyvaÈskylaÈ, Finland
Received 29 August 1998; accepted 22 May 1999
``Capsule'': Soil animals do not themselves degrade soil contaminants, but they do have an important indirect role in these processes
performed by microbes.
Abstract
Although microorganisms are degrading the contaminants in bioremediation processes, soil animals can also have important Ð
while usually an indirect Ð role in these processes. Soil animals are useful indicators of soil contamination, both before and after
the bioremediation. Many toxicity and bioavailability assessment methods utilizing soil animals have been developed for hazard
and risk-assessment procedures. Not only the survival of the animals, but also more sensitive parameters like growth, reproduction
and community structure have often been taken into account in the assessment. The use of bioassays together with chemical analyses gives the most reliable results for risk analyses. This is because physical, chemical and biological properties of the remediated
soil may be changed during the process, and it is possible that transformation rather than mineralization of the contaminants has
taken place. In addition, the soil may contain other harmful substances than those searched in chemical analyses. Finally, because
the ultimate goal of the bioremediation should be Ð together with mineralization of the harmful substances Ð the ecological
recovery of the soil, development of diverse decomposer community as a basis of the functioning ecosystem should be ensured. Soil
animals, especially the large ones, can also actively take part in the ecological recovery processes through their own activity. The
potential risk of transfer of contaminants accumulated in soil animals to the above-ground food webs should be borne in mind.
# 2000 Published by Elsevier Science Ltd. All rights reserved.
Keywords: Soil contamination; Harmful chemicals; Bioremediation; Decomposer animals; Decomposition processes
1. Introduction
There are to two general approaches in remediating or
reclaiming severely degraded soils: (1) an engineering
approach; and (2) an ecological approach (Logan,
1992). The engineering approach relies exclusively on
external methods for soil restoration, while ecological
remediation involves the manipulation of inherent soil
processes to mobilize, immobilize, transform or degrade
contaminants. This manipulation may include, e.g. fertilization or liming of the soil, revegetation of the site
and the use of organic amendments to stimulate soil
biological activity. Bioremediation of contaminated
material is based on the ecological approach, microbes
being responsible for the degradation processes.
Bioremediation is usually recognized as an inexpensive, e€ective, and environmentally safe technology to
* Tel.: +358-14-2602303; fax: +358-14-2602321.
E-mail address: [email protected].® (J. Haimi).
clean up hazardous wastes or chemicals. The soil is considered remediated when concentrations of the contaminants have diminished to the recommended, directed
or appropriate levels. The ultimate goal of the process
is Ð or at least should be Ð full mineralization of the
harmful substances by their conversion into microbial
biomass and harmless products of metabolism, such as
water, carbon dioxide and inorganic salts. Once bioremediation treatment has been completed, the soil can
be utilized, e.g. as land®ll cover material.
Bioremediation techniques use biostimulation and/or
bioaugmentation in the degradation of various harmful
contaminants. Bioaugmentation involves the addition
of a microbial inoculum to a contaminated soil, whereas
biostimulation involves amendment, addition and/or
mechanical manipulation to stimulate indigenous
bacterial populations. Abiotic conditions are optimized
for biodegradation, that is, the functioning of desired
microbes. At the moment, the incomplete understanding
of biodegradation processes and the absence of diverse
engineering techniques required for applications are
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PII: S0269-7491(99)00142-6
234
J. Haimi / Environmental Pollution 107 (2000) 233±238
regarded as major problems in the development of
bioremediation (Pritchard et al., 1996).
There are both biological and environmental reasons to
extend the concept of bioremediation to ecological remediation. This approach requires Ð in addition to the
degradation of hazardous wastes Ð the establishment or
recovery of approriate microbial, plant and animal
communities to create a functioning ecosystem (Majer,
1989). The same ultimate goal is included in reclamation
processes of disturbed sites (Recher, 1989). Recreating
the original diverse and complex biota of the site is probably not possible or feasible in most cases, but a reasonable
approximation can generally be achieved. At the moment,
many other objectives, such as legislation, public opinion
and ®nancial considerations, are pursued when bioremediation processes and technology are designed.
2. Potential utilization of soil animals in bioremediation
Usually, abiotic conditions in the soil under bioremediation process are hostile for soil decomposer animals. The physical and chemical soil conditions may be
outside the tolerance limits of most species, or animals
may have been unable to colonize the soil due to limited
dispersal. In addition, because animals do not harbour
signi®cant metabolic ability to degrade the chemicals to
be treated, one may argue that decomposer animals are
not important in remediation processes. It should be
noticed, however, that when di€erent kinds of organic
wastes are composted, many soil animals, like earthworms, enchytraeids and mites, do have positive e€ects
on the process by utilizing organic compounds in their
own metabolism, and more importantly, by increasing
metabolic activity of soil microbes (Haimi and Huhta,
1987; Edwards, 1998). Stabilization of household wastes
may even be faster in vermicomposting (utilizing e€ec-
tively the earthworms) than in conventional composting
process (Haimi and Huhta, 1986).
Soil animals can also be exploited in remediation and
reclamation processes, principally in two ways. First,
they can take part in the process, increasing overall, and
especially microbial, metabolic activity of the soil. Second, soil animals can be used as indicators of soil contamination, either to assess the toxicity and risk of the
contaminated soil or to evaluate the ecacy of the
remediation process, that is, to evaluate the toxicity and
risk of the end product. Indeed, a number of methodologies with respect to pre-application testing, postapplication bioassays, monitoring, waste management
and risk assessment have been proposed and also
already utilized in environmental management (Table 1).
3. Soil animals as indicators of environmental contamination
Contaminated soils are usually characterized by complex chemical mixtures rather than single chemicals.
Moreover, soils may contain compounds that have not
been expected and not looked for in chemical analyses.
Transformation of the original harmful substances may
further complicate the situation. To determine the
environmental impact associated with complex contaminations, a toxicity-based approach rather than a
chemically-based approach should be adopted in risk
assessment (Callahan and Linder, 1992). It has been
emphasized that direct measurements of, e.g. heavy
metal concentrations in soils, has relatively little value,
whereas uptake into e.g. earthworms is a much more
sensitive and meaningful criterion (Morgan, 1986). Thus,
relevant biological information needs to be incorporated
into the toxicity and risk-assessment procedures.
Soil animals can for good reasons be used as indicators of soil contamination both before and after a
Table 1
A scheme for the use of soil decomposer animals in bioremediation processes
Phase of the process
Role/function of soil animals
Study of potentially contaminated soil
Preliminary toxicity testing
Monitoring the concentrations of contaminants in the tissues of animals
Contaminated soil
Testing of bioavailability and toxicity to organisms
Bioremediation processes
in situ
on site
ex situ
Increasing microbial activity
Monitoring the ecacy of the process
Soil after application
placing/use of the remediated soil
Post-application toxicity testing
Ecological reclamation with animals
organic amendments
liming, etc.
inoculation of animals
J. Haimi / Environmental Pollution 107 (2000) 233±238
bioremediation process. Di€erent kinds of bioassays
have been developed to determine bio-availability and
biological e€ects of harmful chemicals and contaminated soils. Together with chemical analyses, soil animal
studies will help in ®nding out the linkage between
actual contamination levels and adverse e€ects on biota.
Being important and large soil decomposer animals,
earthworms have gained acceptance for use in tests to
assess the e€ects of chemicals on soil organisms. The
survival test has been standardized (ISO, 1993), and it is
widely used to analyze toxicity of pure chemicals in
standardized soil. The survival test has further been
developed to a reproduction test (ISO, 1998), and to
a ®eld test (ISO, 1999). In addition to earthworms, a
collembolan reproduction test is in its ®nal stage of
standardization (ISO, 1997), and a proposal for an
enchytraeid worm reproduction test is under international evaluation at the moment (Table 2). While these
toxicity tests are very simple and done in quite arti®cial
conditions, their use in combination with more complex
bioassays is important to ®nd out causal explanations
for changes observed in animal densities and community structures in the ®eld.
Relevant information about the ecological consequences of chemicals in the soil is urgently needed. It
has been suggested that certain earthworm species could
be used in testing the toxicity of contaminated soils. The
test procedure has already been modi®ed from the
standardized arti®cial soil earthworm bioassay (Callahan and Linder, 1992). Gibbs et al. (1996) developed a
procedure that allows quanti®cation of the e€ects of soil
contaminants on earthworm (Eisenia fetida) growth and
reproduction. They applied the method both in evaluating the toxicity of compost-remediated soils and as a
fast-screening analysis for ®eld soils in a large-scale
ecological risk assessment. In the procedure, pairs of
earthworms are incubated in the studied soil, and total
biomass production (growth of the adults plus reproductive output) and several reproduction end points are
235
measured. The results showed that sublethal end points
are more sensitive and relevant than pure mortality
when evaluating ecological risk of potentially contaminated soils (Gibbs et al., 1996).
Salanitro et al. (1997) applied the traditional earthworm
toxicity test in evaluating the toxicity of crude oil-contaminated soils after bioremediation. Chang et al. (1997)
used the earthworm bioassay (test soils supplemented in
arti®cial soil in di€erent ratios) together with plant
bioassays to evaluate the remediation of a lead-contaminated soil. Tests revealed that the remediated soil
was clearly more toxic to earthworms than the original
soil. High salt levels generated during the remediation
process were concluded to be responsible for the
increased soil toxicity (Chang et al., 1997). Laine et al.
(1995) studied the bioavailability of organic halogen
compounds in contaminated sawmill soils using the
standard test species, Eisenia andrei, as a test species.
They found that higher soil organic matter diminished
the bioaccumulation potential of these chemicals in the
earthworms.
Some biomarkers measured in earthworms (like
enzyme and immune functions, hemoglobin content,
sperm production and fertility) have been developed
and proposed for the use in reliable toxicity testing (see
Reinecke and Reinecke, 1998). These parameters are
very sensitive and useful, but their use needs more
facilities and expertise than measurements of the more
simple individual-level parameters.
In addition, community and system-level ecotoxicological studies have proved to be valuable methods to
support ecological risk assessment procedures (Table 3).
However, the use of parameters of higher levels of biological organization as simple routine end points is
unrealistic because of large variation in community
structure in space and time, and large amount of labour
needed for reliable analyses (Salminen and Sulkava,
1997). However, Heimbach (1997) emphasized that
indirect e€ects of chemicals, like changes in food
Table 2
Decomposer animals frequently used (the procedure has been established or is under development) in the evaluation of toxicity of chemicals and
contaminated soils
Animal group
Species
Comments
Earthworms
Eisenia fetida/andrei
Standardized survival (ISO, 1993) and reproduction (ISO, 1998) tests in arti®cial
soil, tests also with contaminated soils
Common species in ®eld soils, used in several ecotoxicological studies
as above
Proposed standardized toxicity test in arti®cial soil, reproduction and survival
Standardized toxicity test (ISO, 1997) in arti®cial soil, reproduction and survival
Numerous studies in laboratories and in the ®eld
Enchytraeids
Collembola
Mites
Isopods
Nematodes
Protozoans
Aporrectodea caliginosa
Lumbricus terrestris
Enchytraeus albidus, also other species
Folsomia candida
several species, e.g. Folsomia ®metaria and
Orchesella cincta
Platynothrus peltifer
Porcellio scaber
Trichoniscus pusillus
e.g. Plectus parietinus
e.g. Colpoda cucullus
Long life cycle, used in many studies
Used in many studies, no standardization, nutrient mineralization also measured
In soil pore water, dicult to extrapolate to the ®eld, some studies
As above
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J. Haimi / Environmental Pollution 107 (2000) 233±238
Table 3
Organism groups and soil processes that should be considered in hazard and risk assessment of soil contamination (according to Eijsackers and
Lokke, 1992)
1. Taxonomic groups:
Microorganisms:
Invertebrates:
Higher plants
2. Functional groups:
Primary producers
Decomposers
Herbivores
Predators and parasites
3. Soil processes:
Decomposition, soil respiration
Nutrient mineralization, nitri®cation
Other enzyme activities
Saprotro®c fungi, mycorrhizal fungi, bacteria
Protozoa, Nematoda, Oligochaeta (earthworms, enchytraeids), microarthropods
(Collembola, Acarina etc.), macroinvertebrates (Isopoda, Diplopoda etc.), insects
and their larvae in soils
availability and soil structure, may be more important
in risk assessment than direct toxic e€ects of chemicals
on earthworms.
There are some complicating factors that make interpretation of the results from studies with soil animals
dicult. Resistance against the contaminant may
increase, at least in long lasting exposure. Resistance
may be physiologically and energetically expensive,
leading to a trade-o€ situation in animals. Posthuma et
al. (1992) and Donker et al. (1993) found changes in life
history characteristics of soil animals living at contaminated sites. These changes without doubt also have
e€ects at community and ecosystem levels. Another
factor hampering evaluation of the results is avoidance
behavior of soil animals. It has been observed that soil
animals are able to minimize their exposure by distinguishing contaminated substrate or food and actively
avoiding it (Haimi and Paavola, 1998). Thus, density of
individuals or concentrations in animal tissues may
necessarily not re¯ect the actual concentration in the
soil.
4. Promoting land reclamation and amelioration with
soil animals
When ecological rehabilitation of the soil is the reasonable ®nal goal, soil fauna can be very important for
biological activity of the soil after the more or less
technically driven bioremediation processes. Activity of
decomposer animals in the soil can result in faster
recovery of the site and ®nally in properly functioning
ecosystem. Especially larger soil animals, such as earthworms, are able to enhance soil physical properties
through their comminution and burrowing activity
(review by Edwards and Bohlen, 1996). In addition,
nutrient cycling at the site can be enhanced through the
soil animals' own metabolism and especially, through
the increased metabolic activity of soil microbes caused
by animal grazing. As most of the biologically cleaned
soils are used as a covering layer, e.g. on waste dumps,
ecological properties of these soils are considered to be
the most important part of the soil quality (Tamis and
Udo de Haes, 1995).
The success of reclamation of poor mineral soils,
polder soils, open-cast mining sites and areas of cutover
peats are often limited by poor soil structure, low
inherent soil fertility or high soil metal content. Also
here, large decomposer animals, especially earthworms,
have successfully been used in improving soils (Dunger,
1969; van Rhee, 1969; Curry and Cotton, 1983). Organic
matter incorporation has greatly been accelerated and
soil structure improved which has resulted in increased
soil fertility.
In many cases the faunal restoration processes should
have been supported by deliberate introductions of
earthworms (Dunger, 1969; van Rhee, 1969; Curry and
Cotton, 1983) and/or addition of organic amendments
onto the soils (Dunger, 1969). Usually, the sites with
remediated soils are small and have long edges in relation to their area, and therefore natural immigration
may play an important role in colonization by soil animals (Tamis and Udo de Haes, 1995). On the other
hand, Rundgren (1994) found out, when studying the
remediation of acidi®ed coniferous forest soils through
liming that remediation programme should include
earthworm inoculations, because the dispersal and
colonization abilities of these animals are low. The site
can be ameliorated in several ways to provide more
suitable habitat conditions for soil decomposer animals.
As mentioned earlier, these measures include liming to
counteract soil acidity and metal toxicity, addition of
organic amendments, and establishment of plant cover.
Spreading of clean soil can also provide as an inoculum
of diverse soil fauna.
More important than certain faunal structure with
particular species of the decomposers is the proper
functioning of the community and decomposition
J. Haimi / Environmental Pollution 107 (2000) 233±238
processes. However, all species do not have an equal
impact on ecosystem processes. Opportunistic colonizers and keystone species may be a prerequisite for the
successful development of the remediated soil (Lawton,
1994). These species are not necessarily among the best
species to recover after hostile conditions (Pimm, 1991).
While activity of earthworms has lead to enhanced
productivity at many reclaimed sites, amounts of metals
or other harmful substances have not been a€ected by
the animals. Martinucci et al. (1983) even observed that
burrowing and casting activity of earthworms brought
the highly hazardous substance TCDD, back to the soil
surface from the deeper soil layers. In laboratory
experiments, Haimi et al. (1992) showed that while
increasing overall soil microbial activity, earthworms
did not a€ect the amount of polychlorinated phenols in
the soil.
5. Soil animals as a risk Ð food web transfer of the
contaminants
In some cases soil animals may transfer contaminants
accumulated in them to the above-ground food webs.
Especially the earthworms, having considerable ability
to accumulate contaminants from soil into their bodies,
and having relatively low sensitivity to many of these
compounds, can be an important transfer route from
soil to the above ground ecosystems (Eijsackers, 1998).
Many vertebrate animals, like badgers, foxes and several
bird species, are frequently feeding on earthworms.
Because bioconcentration factors (concentration in
earthworms vs. that in soil) have been observed to be
quite high, it has been calculated that maximum permissible soil concentrations for e.g. heavy metals are
often exceeded, even in normal agricultural soils (Spurgeon and Hopkin, 1996).
In central Finland, earthworms have been found in
high numbers in several compost piles built for degradation of PCPs. Surprisingly, even the compost-living
species Eisenia andrei was very abundant in these piles
(consisting of sawdust and contaminated soil) which
indicate high microbial activity in the material (J. Haimi
and J. Salminen, unpublished information). These specimens contained high amounts of several polychlorinated compounds in their bodies, and also
compounds which were not found in measurable
amounts in the soil (Knuutinen et al., 1990). However,
because the total biomass of these earthworms was quite
small, and their distribution was very local, the real
threat to predators of the earthworms was limited.
Dense populations of several species of earthworms
were also found in highly PCP-contaminated soils at an
old saw-mill site in central Finland (Knuutinen et al.,
1990). Here, the earthworms had obviously avoided
high accumulation of PCP through their behavior,
237
because concentrations were signi®cantly lower than
could have been predicted from the soil concentrations
(Knuutinen et al., 1990).
As already pointed out earlier, the burrowing and
casting activity of earthworms can bring hazardous
chemicals from deeper soil layers back to the surface.
This has been observed in Seveso, Italy, in the case of
TCDD (Martinucci et al., 1983). Continuous mixing of
soil layers may easily lead to continuous exposure of
above-ground biota to the contaminants in the soil. In
addition, it should be noted that there is a potential risk
of contaminant transport down into deeper soil layers
or even to ground water by preferential ¯ow of rain
water along earthworm burrows.
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