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Review article
Earthworm assisted bioremediation of organic contaminants
Zachary A. Hickman, Brian J. Reid ⁎
School of Environmental Sciences, University of East Anglia, Norwich, UK, NR4 7TJ
article info abstract
Article history:
Received 30 August 2007
Accepted 27 February 2008
Available online 22 April 2008
Due to their biological, chemical and physical actions, earthworms can be directly employed within
bioremediation strategies to promote biodegradation of organic contaminants. Earthworms have been shown
to aerate and bioturbate soils and improve their nutritional status and fertility, which are variables known to
limit bioremediation. Earthworms have also been shown to retard the binding of organic contaminants to
soils, release previously soil-bound contaminants for subsequent degradation, and promote and disperse
organic contaminant degrading microorganisms.
This review discusses these earthworm actions upon the soil environment and how they might influence the
fate and behaviour of soil associated organic contaminants, subsequently improving bioremediation potential.
The latter part of this review considers organic compounds in the following order: agrochemicals, petroleum
and crude oil hydrocarbons, PAHs and PCBs.
© 2008 Elsevier Ltd. All rights reserved.
Keywords:
Bioremediation
Earthworms
Organic contaminants
Bioavailability/bioaccessibility
Biodegradation
Contents
1. Introduction . . . ........................................................ 1072
2. Theory: earthworm abiotic and biotic effects upon the soil environment ............................... 1073
2.1. Abiotic effects ....................................................... 1073
2.2. Biotic effects ....................................................... 1074
3. Practice: earthworm assisted bioremediation ............................................ 1074
3.1. Agrochemicals ...................................................... 1075
3.2. Petroleum and crude oil hydrocarbons ............................................ 1077
3.3. Polycyclic aromatic hydrocarbons (PAHs) ........................................... 1078
3.4. Polychlorinated biphenyls (PCBs) . ............................................. 1079
3.5. Other compounds ..................................................... 1079
4. Concluding remarks ....................................................... 1079
References .............................................................. 1080
1. Introduction
While literature exists with respect to the potential for earthworm
use in the remediation of soils contaminated with metals, this review is
specifically concerned with the application and potential use of earth-
worms for remediation of soils contaminated with organic compounds.
This review firstly considers the theoretical underpinning of such an
approach (Section 2) and its potential for application (Section 3).
A number of bioremediation methods exploit the ability of mi-
croorganisms to effectively degrade soil associated organic contami-
nants, such as composting, biopiling and landfarming. The success of
these microorganisms depends upon a wide array of variables and
conditions, which often limit effective bioremediation, and might
include oxygen and nutrient availability, pH, C:N ratio, presence,
number and activity of organic contaminant degrading microorgan-
isms, enzyme induction, temperature, toxic levels of contaminants,
presence of co-contaminants (determining added toxic effects or
preferential degradation), and presence of terminal electron acceptors
(Atlas, 1995; Boopathy, 2000; Romantschuck et al., 2000).
Within the soil environment, an earthworm's sphere of influence
is known as the drilosphere system (Brown et al., 2000). This
incorporates the burrow systems, surface and belowground earth-
worm casts, internal earthworm gut and processes, the earthworm
surface in contact with the soil, and associated biological, chemical
and physical interactions, in addition to the associated soil mi-
croorganisms (Brown and Doube, 2004). Earthworms promote
Environment International 34 (2008) 1072–1081
⁎Corresponding author. Tel.: +44 1603 592357; fax: +44 1603 591327.
E-mail address: b.reid@uea.ac.uk (B.J. Reid).
0160-4120/$ –see front matter © 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envint.2008.02.013
Contents lists available at ScienceDirect
Environment International
journal homepage: www.elsevier.com/locate/envint
favourable conditions within the soil, and theoretically, these may go
some way to positively enhancing the above mentioned variables, and
thus ultimately aid in bioremediation of organic contaminants.
In addition to such bioremediation limitations, the availability/
accessibility of the contaminants for, specifically microbial degra-
dation, is fundamental to successful biodegradation of organic con-
taminants within soils (Reid et al., 2000; Semple et al., 2003;
Volkering and Breure, 2003; Bamforth and Singleton, 2005). The
availability/accessibility of soil associated organic contaminants for
subsequent microbial degradation changes as soil/contaminant inter-
action time increases (ageing). The consequences and effects of this
‘ageing’process has been described elsewhere (Alexander, 2000; Reid
et al., 2000; Ehlers and Luthy, 2003; Semple et al., 2003; Volkering and
Breure, 2003; Bamforth and Singleton, 2005). Briefly, as time prog-
resses, contaminants become entrapped and sorbed onto and into soil
mineral and organic matter fractions, rendering them inaccessible,
and thus unavailable for microbial interaction. Significantly, earth-
worm activity has the potential to release these residues (Verma and
Pillai, 1991; Gevao et al., 2001) and could thus potentially further
enhance bioremediation performance. Bioavailability/accessibility of
chemicals and compounds to microorganisms and earthworms are
known to differ (Gevao et al., 2001), and whilst bioavailability/ac-
cessibility of chemicals and compounds to earthworms is pertinent,
the discussion of these activities and associated effects are not within
the scope of this review.
It is often the case that bioaugmentation of microorganisms to
contaminated soils is undertaken during bioremediation strategies
in the attempt to enhance both the contaminant degradation rate
and the ultimate endpoint concentrations (Vogel, 1996). Both single
strains and consortia of microorganisms added to contaminated
soils usually produce little added value in terms of degradative
ability over the soil's indigenous microorganisms (Catallo and
Portier, 1992; Allan et al., 2007), which are often only limited in
their contaminant degradation capacities due to the soil's sub-
optimal status. Promotion of the indigenous microorganisms is thus
a primary aim and would occur via optimisation and enhancement
of both abiotic and biotic conditions; something that earthworms
could enhance.
Earthworms have previously been utilised within land recovery or
rehabilitation of sub-optimal soils to aid in the improvement of soil
structure and fertility e.g. poor mineral soils, polder soils, open cast
mining sites and areas of cutover peats, (Edwards and Bohlen, 1996;
Butt et al., 1999; Haimi, 2000; Lowe and Butt, 2003; Butt et al., 20 04).
It is therefore surprising that limited investigations into the direct
application of earthworms for soil remediation have been undertaken.
Section 2 of this review will discuss the biological, chemical and
physical actions that earthworms exert upon their environment, thus
highlighting the theory behind their potential for use within
bioremediation. Additionally, the effects of these actions upon soil
microbiology with respect to bioremediation potential shall also be
discussed. Section 3, structured by contaminant type, will review
published work that has directly utilised earthworms within
bioremediation, or which have noted effects of earthworm presence
upon organic contaminant fate.
2. Theory: earthworm abiotic and biotic effects upon the soil
environment
It would be useful to gain an insight into the biological, chemical
and physical abiotic and biotic activities and effects that earthworms
have upon the soil environment. This section of the review will
investigate the underlying principles of these effects, and suggest how
they may go some way to aiding in bioremediation and offsetting
known bioremediation limitations (Table 1). It can be noted that there
are a number of bioremediation limitations, which may well benefit
from earthworm inclusion into their methodology.
2.1. Abiotic effects
Within bioremediation, it is often necessary to enhance and
maintain moisture, oxygen and nutrient levels, whilst also ensuring
they can be homogenously dissipated, especially if, for example,
dealing with deeper soils, compacted soils or soils rich in clay. Whilst
time consuming, labour intensive and expensive methods can be
utilised to aid in the optimisation of these variables, there might exist
a relatively low input, low technological tool available to undertake
this work. As earthworms move throughout the soil environment,
their resulting burrows (burrowing being species specific) act as input
points of, and preferential pathways for, water and particle movement
(Shipitalo and Le Bayon, 2004; Kretzshmar, 2004; Dominguez, 2004),
and nutrient flow and aeration (Dominguez 2004).
In addition, as burrowing occurs, and thus as earthworms ingest
and digest soil, a further positive effect upon the soil environment
occurs; that of the mechanical breakdown of soil particles (Edwards
and Bohlen, 1996; Bohlen et al., 2004; Kersante et al., 2006). Mckenzie
and Dexter (2004) and Shipitalo and Le Bayon (2004) both discuss the
forces applied to soil particles during earthworm gut passage and
their subsequent remoulding and reorganisation, as do Brown and
Doube (2004). For example, Ziegler and Zech (1992) noted that
earthworm (Eisenia fetida) digestion reduced soil organic matter
larger than 2000 μm by between 97 and 27% (200–2000 μm), whilst
Martin (1991) observed earthworm (Millsinia anomala) fractionation
of soil organic matter determined a size reduction of 25–30%. Such
research highlights the major role that earthworms have in reparti-
tioning soil litter into smaller aggregate sizes (Martin, 1991; Barois
et al., 1993; Bolan and Baskaran, 1996; Kretzshmar, 2004). It could be
hypothesised that herein might exist potential for earthworm assisted
release of soil associated (aged) organic contaminants (Barois et al.,
1993). In addition, such activities have also been shown to increase
soil organic matter surface area (Edwards and Bohlen, 1996), which
will have a bearing upon the fraction of material exposed for microbial
interaction (Dominguez, 2004), potentially resulting in increased
contaminant degradation. These aspects are worthy of serious
research and consideration with respect to increasing degradation
potential and offsetting the residual concentration problem, which
often limits final bioremediation success.
During the digestion and excretion (as earthworm casts) of the
now reworked ingested soil mineral and organic matter fractions, it is
known that there are many subsequent positive effects upon the
improvement of the soil environment and soil structure. These include
Table 1
Limitations to aerobic bioremediation and the main earthworm effects that minimise
the limitations
Bioremediation limitation Movement
and burrow
creation
Ingestion,
digestion and
excretion
Casts
Lack of oxygen, anaerobic conditions
Soil heterogeneity
Compacted soil
Inappropriate C:N ratio
Insufficiency of available nutrients
Low bioavailability of bound residues
Presence, number and activity of
degrader microorganisms
Contaminant concentrations too low
to induce catabolic ability
Toxic levels of contaminants, or
presence of co-contaminants
restricting induction of catabolic ability
Temperature
pH
Inappropriate moisture conditions
1073Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
increased soil porosity (Bolan and Baskaran, 1996; Shipitalo and Le
Bayon, 2004), increased oxygenation, moisture retention (Edwards
and Bohlen, 1996; Schaefer and Filser, 20 07), improved soil fertility via
accelerated organic matter decomposition, and improvement of the
availability of nutrients (Edwards and Bohlen, 1996; Lavelle et al.,
2004).
Earthworm casts are therefore nutritionally rich, and the deposi-
tion of these casts upon the burrow walls, within burrows or on the
soil surface can significantly differ in chemical and physical composi-
tion to the surrounding soil in terms of altered C:N ratios and higher
pH (Bolan and Baskaran, 1996; Edwards and Bohlen,1996; Brown and
Doube, 2004; Shipitalo and Le Bayon, 2004). There could thus be
potential for the use of earthworms casts (either directly applied to
contaminated soils, or being produced as earthworms reside within
contaminated soils) to firstly improve chemical conditions to aid bio-
remediation and, secondly, improve the overall soil condition. Some of
these effects upon the soil environment have been investigated within
soil/land rehabilitation (Lowe and Butt, 2003; Butt et al., 2004),
specifically the increases in soil fertility and structure, leading to
increased soil ‘health’. Thus, not only might soils benefit from earth-
worm input in terms of reduced contaminant concentrations, but also
from improved soil ‘health’; both aspects being fully in line with the
recently proposed EU Soil Framework Directive (2006).
2.2. Biotic effects
Although dependent upon earthworm species, it is known that
earthworms interact with soil microorganisms (fungi, bacteria and
actinomycetes) on three broad spatial scales (burrow linings, casts and
earthworm gut or intestine) (Brown and Doube, 2004). For example,
mucus and cast deposition on burrow walls, and other organic carbon
sources transferred through the burrow systems promote the increase
and distribution of microorganisms in earthworm burrows (Farenhorst
et al., 2001), whilst mucus, urine and glucose can result in increases in
microbial biomass (Scheu,1987). This is of relevance because increases
in microbial biomass is linked to increased microbial catabolic activity
(Meharg, 1996), and as Gevao et al. (2001) stated, such increased
activity, linked with potential increases in bioavailability due to
earthworm actions upon the soil within earthworm guts (Barois
et al., 1993) could potentially increase compound losses via microbial
mineralisation. Higher microbial numbers, diversity and activity are
also known to be related to passage of microorganisms through the
earthworm gut, as well as the promotion therein, and the ‘awakening’
of dormant gut flora (Brown et al., 2000; Brown and Doube, 20 04); this
is, however, very much related to gut passage time (Brown and Doube,
2004). Importantly, the increased gut associated microflora are then
excreted throughout the media within earthworm casts and via
microbial adheration to earthworm skin (Edwards and Bohlen, 1996),
whilst the transit and dispersal mechanisms associated with the water
flow (Kretzshmar, 2004) also help to further dissipate microorganisms.
Such actions are clearly relevant to any bioremediation methodology
desiring the spatial incorporation of microorganisms capable of
organic contaminant degradation.
Earthworm casts are therefore generally much richer in microbial
numbers in comparison to the initially ingested material; for example,
Scheu (1987) reported an increase of 90% in respiration rate in
fresh casts, whilst, Teotia et al. (1950) reported bacterial counts of
32 million/g compared to 6–9 million/g for the surrounding soil. This is
due not only to the aforementioned intestinal promotion of micro-
organisms but also to the inherently high soil organic matter levels,
resulting in further microbial activity and proliferation (Brown and
Doube, 2004). Dynamics and succession of microorganisms within
earthworm casts is complex, and relies heavily upon many factors such
as type of food ingested, gut passage time and ingested and inherent gut
microorganisms. Further discussion upon these factors, numbers of
microorganisms in earthworm casts, and the effect of earthworms upon
microorganisms on the meso and macroscale, are further discussed by
Edwards and Bohlen (1996),andBrown and Doube (2004).
It has also been noted that water soluble (Edwards and Bohlen,
1996) low molecular weight (Barrois and Lavelle, 1986; Lavelle et al.,
1993) organic compounds are added to earthworm gut contents
during digestion, such as enzymatic fluid and mucus based solutions
(Brown and Doube, 2004), which also subsequently stimulate
microbial activity both in the gut and in the egested casts (Edwards
and Bohlen, 1996). It is known that pre-exposure, or pre-induction of
microorganisms to contaminants, or groups of contaminants, can
result in subsequent increased degradation rates (Carmichael and
Pfaender, 1997; Reid et al., 2002). Therefore, these intestinal organic
compounds might help ‘prime’the microorganisms in the gut to break
down more complex organic compounds in the ingested soil.
Earthworm casts have had a strong presence within this particular
approach, and relevantly, the application of earthworms within waste
management involves the digestion of a wide range of organic wastes
(Edwards and Bohlen, 1996) into vermicast/compost. Vermidigestion is an
area rapidly increasing in interest and research due to the use of the
nutrient and microbially rich casts as plant growth media, plant pest and
disease suppressant and its use within horticulture (Edwards and Arancon,
2004). Such a material may well have a place within remediation, and will
be discussed subsequently. Pertinent reviews of earthworm feeding
ecology (Curry and Schmidt, 20 07) and vermidigestion, and the use of
earthworm casts have been undertaken elsewhere (Edwards and Bohlen,
1996; Dominguez, 2004; Edwards and Arancon, 2004).
This section has served two important functions; firstly, that of
undertaking a brief and general account of some aspects of earthworm
effects upon the soil environment, and secondly, that of providing the
theory for earthworm assisted bioremediation of organic contami-
nants. Thus, it should now be apparent that in theory, it is the
earthworm's combined mechanical activity upon the soil and
subsequent promotion of microorganisms that would be of most
benefit to remediation efforts, as opposed to uptake/accumulation of
organic contaminants. It has previously been shown that earthworm
body burdens of organic contaminants can typically be low (Kelsey
and Alexander, 1997; White et al., 1999; Gevao et al., 2001) and is
unlikely to prove to be a worthwhile tool in bioremediation.
Fig. 1 summarises the discussed positive earthworm actions upon
the soil environment, which might theoretically offset some of the
previously discussed bioremediation limitations.
In addition to the effects of earthworms uponmicrobial bioticeffects,
a number of studies have highlighted direct earthworm biotic effects in
the form of feeding behaviours upon contaminant fate. For example,
whilst Ma et al. (1995) noted that the effect of leaf litter food made only
minimal difference in polycyclic aromatic hydrocarbons (PAH) loss
extents, they did note that bioaccumulation of these PAHs was greatly
enhanced via food limitation, thus it is a possibility that earthworms
increase their oral intake of soil particles when driven by hunger stress.
When investigating total petroleum hydrocarbons (TPH) losses in with-
earthworm systems that either had or had not received food, Schaefer
et al. (2005) noted that residual TPH in the with-food systems was
greater, however, these were not significant values.
These results would suggest that if earthworms were applied to sub-
optimalcontaminated soils lacking in organic matter, a greaterdegree of
biological interaction might ensue resulting greater extents of loss. In
further support of this, Haimi et al. (1992) stated that the lower the
organic matter content, the higher the bioaccumulation, which
obviously implies increased soil association, a result confirmed by
Peters et al. (2007) who noted significantly greater uptake of p,p-DDE
from soil than compost by earthworms (E. fetida and L. rubellus).
3. Practice: earthworm assisted bioremediation
It must be stated that earthworms could only be applied to
contaminated soils that do not exert overly toxic effects. In relation to
1074 Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
this, there are inherent differences between earthworm niche types
which dictate responses and behaviour to soil type, contaminant type,
food availability and a number of other environmental parameters
(Edwards and Bohlen, 1996; Lavelle, 1998; Curry and Schmidt, 2007).
Therefore, care would be needed to select the correct earthworm
species for the correct intended conditions. Earthworm tolerances and
toxicity to contaminated soils have been discussed elsewhere
(Sheppard et al., 1998; Spurgeon et al., 2004).
It is envisaged that approaches for earthworm assisted bioreme-
diation might include:
1. Direct application of earthworms to contaminated soils (e.g.
Schaefer et al., 2005)
2. Co-application of earthworms to contaminated soils with another
organic media, such as compost. (e.g. Ceccanti et al., 2006)
3. Application of contaminated media to earthworms as part of a
feeding regime. (e.g. Getliff et al., 2002)
4. Indirect use of earthworms could occur via application of
vermidigested material. Such substrates could be hypothesised to
be high in promoted degraders and thus high in catabolic potential.
(e.g. Alvarez-Bernal et al., 2006)
A number of studies have investigated the use of earthworms
within bioremediation to enhance losses of organic contaminants
(Table 2). These include a broad range of contaminants, supporting the
wide applicability of earthworm use, such as insecticides (Verma et al.,
2006), herbicides (Farenhorst et al., 2001; Binet et al., 2006), crude oils
(Stom et al., 2003; Schaefer and Filser, 2007), PAHs (Eijsackers et al.,
2001), polychlorinated biphenyls (PCBs) (Singer et al., 2001), chlor-
ophenolic wood preservatives (Haimi et al., 1992) and 2,4,6-
trinitrotoluene (TNT) (Renoux et al., 2000).
It can be observed from Table 2 that a variety of earthworm species
were investigated, as were the effects of earthworms upon the be-
haviour, fate and loss of organic contaminants, with 35 studies being
discussed or referred to within the review. It can also be noted that a
variety of earthworm species are investigated, with E. fetida being by
far the most utilised. Prior to fuller discussion of the studies, it can be
observed that they are diverse in their investigation methods and
their observed earthworm effects. These range from the increased
sorption of compounds to earthworm burrows (Farenhorst et al.,
2001) and casts (Binet et al., 2006) to compound remobilisation
(Verma and Pillai, 1991) and the limiting of compound binding (Gevao
et al., 2001) to increased microbial promotion and subsequent
degradation (Schaefer, 2001). It should be noted that while some
studies offer mechanical insight, others report only approach taken
and effects observed.
3.1. Agrochemicals
A number of studies have investigated earthworm effects upon
agrochemicals. These are not necessarily with a view to enhancing
bioremediation potential, but to understand the governing mechanisms
in the field environment upon agrochemical fate and persistence.
However, these mechanisms are consistent with those pertinent to
applying earthworms to bioremediation of such compounds. Whilst
research (Eijsackers et al., 2001)hasidentified that earthworm assisted
bioremediation is likely to increase hydrocarbon availability, and has
been seen to remobilise dichlorodiphenyltrichloroethane (DDT) and
hexachlorocyclohexane (HCH) bound residues (Verma and Pillai, 1991),
such findings were in conflict with those of Bolan and Baskaran (1996)
who investigated the effect of earthworm (Lumbricus rubellus and Allo-
lobophora calignosa) casts upon the sorption and movement of
14
C-
atrazine,
14
C-2,4-dichlorophenoxy acetic acid (2,4-D) and
14
C-metsul-
foron methyl. They stated that the casts sorbed higher amounts of
herbicides than the source soil due to the higher levels of organic carbon
and fine size fractions, present due to earthworm grinding actions and
selective feeding. Clearly both theories are credible, and perhaps
highlight not only the differences in compound behaviour, experimental
set-up or earthworm species, but also the wide variability between the
effects of earthworm mechanics upon compound fate, and subsequent
earthworm casts upon compound fate.
Increased agrochemical sorption due to earthworm activity and/or
presence was also noted by Farenhorst et al. (2000a,b)when
earthworm (Lumbricus terrestris) activity, although effectively trans-
locating, distributing and mixing
14
C-atrazine, had resulted in its
persistence via sorption. Such sorption effects have been observed
for
14
C-atrazine and
14
C-metachlor to organic rich burrow linings
Fig. 1. Earthworm biological, chemical and physical effects within the soil environment.
1075Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
(Farenhorst et al., 2001), for atrazine to earthworm gut contents and
humic and colloidal rich casts (Binet et al., 2006) and for atrazine to
cast organic carbon content, when earthworm (Aporrectodea giardi)
presence was investigated in combination with an atrazine degrading
inoculum (Pseudomonas sp. strain ADP (DSM 11735) (Alekseeva et al.,
2006).
However, in contrast to these findings, Mallawatantri et al. (1996)
determined that the soil organic carbon amount related to the
Table 2
Overview of investigated organic compounds and earthworm species and effects
Compound Earthworm species Effect, or aspect of use Reference
Herbicides
Atrazine, 2,4-D and
Metsulforon methyl
L. rubellus and A. calignosa Casts increased sorption of compounds Bolan and Baskaran (1996)
Atrazine L. terrestris and A. calignosa Compound sorption to gut contents and casts. Earthworms
determined lower mineralisation.
Binet et al. (2006)
Atrazine L. terrestris Activity mixed and distributed compound, increased persistence,
reduced mineralisation, accelerated binding of residues
(Farenhorst et al. 2000a)
Atrazine L. terrestris Activity mixed and distributed compound, increased persistence,
reduced mineralisation, accelerated binding of residues
(Farenhorst et al. 2000b)
Atrazine and Metachlor L. terrestris Increased sorption of compound to burrow linings Farenhorst et al. (2001)
Atrazine L. terrestris Increased mineralisation and bioavailability Meharg (1996)
Atrazine A. giardi Burrows and casts increased compound sorption Alekseeva et al. (2006)
2,4-D, Carbofuran
and Metribuzin
Species unreported. Earthworm macropores increased sorption but increased
microbial mineralisation
Mallawatantri et al. (1996)
Isoproturon, Dicamba
and Atrazine
A. longa Released previously bound residues, limited formation of bound
residues, increased mineralisation
Gevao et al. (2001)
Atrazine L. terrestris and A. calignosa Reduced mineralisation and reduced microbial numbers,
increased sorption of compound
Kersante et al. (2006)
Atrazine and Metamitron Vermicompost No effect upon degradation Koocheki et al. (2005)
Insecticides
Endosulfan M. posthuma Gut microflora promoted as specific degraders Verma et al. (20 06)
Hexachlorohexane (HCH) P. posthuma Gut microflora promoted as specific degraders Ramteke and Hans (1992)
HCH and DDT Pheretima posthuma Released previously bound residues Verma and Pillai (1991)
Crude oils and petrochemicals
Oil refinery sludge E. fetida Promotion of microbial numbers, in combination with compost
increased TPH loss
Ceccanti et al. (2006)
Crude oil E. fetida Increased crude oil degraders and thus degradation Schaefer (2001)
Petroleum E. fetida No effect noted Callaham et al. (2002)
Crude oil L. terrestris, A. chlorotica and E. fetida Increased microbial respiration and taxanomic groups,
increased mineralisation
Schaefer et al. (2005)
Crude oil E. fetida Minimal losses, improved soil structure and porosity Stom et al. (2003)
Crude oil L. terrestris, A. chlorotica and E. fetida with
organic amendments.
Increased microbial respiration, increased TPH degradation in
some treatments.
Schaefer and Filser (2007)
Oil E. fetida Increased oil losses Tomoko et al. (2005)
Hydrocarbon drilling fluids
and drill cuttings
E. fetida fed contaminants with food mixture. Increased TPH losses Getliff et al. (2002)
Asphaltens E. fetida vermicompost Reduction in asphaltens, increased gut or vemicompost
microbial mineralisation rates
Martin-Gil et al. (2007)
PAHs
Phenanthrene
and Fluoranthene
L. rubellus Increased rates of loss Ma et al. (1995)
Phenanthrene
and Fluoranthene
E. fetida Increased PAH availability via consumption Eijsackers et al. (2001)
Anthracene, Phenanthrene and
Benzo(a)pyrene
E. fetida Increased losses Contreras-Ramos
et al. (2006)
Anthracene, Phenanthreneand
Benzo(a)pyrene
E. fetida vermicompost Increased rates of loss Alvarez-Bernal et al. (2006)
Chlorinated aromatics
Aroclor 1242 P. hawayana Increased losses due to burrowing and microbially rich casts,
effective mixing of compound
Singer et al. (2001)
Aroclor 1242 P. hawayana Effective mixing of compound and distribution of microorganisms,
some sorption effects, increased microbial activity.
Leupromchai et al. (2002)
Aroclor 1248 E. fetida Potential digestive activity and gut populations aided in losses,
high bioaccumulation
Tharakan et al. (2006)
Chlorophenolic
wood preservatives
A. calignosa and L. rubellus Bioaccumulation of compounds Haimi et al. (1992)
Other
2,4,6-trinitrotoluene E. Andrei Metabolised compound or promoted degraders Renoux et al. (2000)
di-(2-ethylhexyl) phthalate L. terrestris Hydrolyzing abilities Albro et al. (1993)
3-methylcholanthrene
and phenobarbitol
D. veneta No metabolic induction Milligan et al. (1986)
4-fluoroaniline
and 4-fluorobiphenyl
E. fetida No metabolism, and limited metabolism, respectively Bundy et al. (2002)
1076 Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
earthworm macropores (species unknown) was directly correlated to
microbial numbers and thus observed mineralisation of 2,4-D, carbo-
furan and metribuzin; organic carbon content not only appears to
determine sorption of agrochemicals, but also microbial mineralisation.
In relation to this, Binet et al. (2006) further suggested that
earthworm (L. terrestris and Aporrectodea calignosa) activity would
promote atrazine mineralisation by altering the size and diversity of
microbial communities. They then reported that earthworm presence,
albeit at low application density, (three earthworms per 1.8 kg
treatment) over 86 days, determined a lower mineralisation extent
(11.7%) in comparison to the without-earthworm treatments (15.3%).
This is in keeping with Farenhorst et al. (2000a) who also reported
reduced atrazine mineralisation in the presence of earthworms
(L. terrestris), whilst also noting the acceleration of the formation of
non-extractable residues in with-earthworm treatments (Farenhorst
et al., 2000a,b). However, these results are in conflict with those of
Meharg (1996) who determined that
14
C-atrazine mineralisation was
regulated by substrate availability on exchange sites, and in this
instance, earthworm (L. terrestris) presence, at high application
density (1 earthworm per 40 g) affected the binding of atrazine to
soil exchange sites over a 4 week period, with subsequent miner-
alisation of
14
C-atrazine by soil microorganisms being double that of
the control. Meharg (1996) concluded that this was due to increased
bioavailability on exchange sites attributed to the presence of worms,
thus further reinforcing the findings of Eijsackers et al. (2001). The
mechanisms for this were hypothesised to be earthworm mucilage
secretions and changes in soil structure and soil microflora.
In a contrasting study, Gevao et al. (20 01) applied earth-
worms (Aporrectodea longa) at a rate of 5 individuals per 2 kg to
soils contaminated with non-extractable pesticide (
14
C-isoproturon,
14
C-dicamba and
14
C-atrazine) residues for 28 days to evaluate
subsequent degradation, release and uptake. They determined that
due to earthworm physical activity, a greater degree of previously
bound pesticide residue in comparison to the without-earthworm
treatments was released. When the study was applied to freshly
added pesticides, it was noted that the formation of non-extractable
residues of
14
C-isoproturon,
14
C-dicamba and
14
C-atrazine were higher
by factors of 2, 2 and 4, respectively, in the without-earthworm
treatments. Thus, not only did earthworms limit the formation of
the bound fraction, they also promoted the release and mineral-
isation of bound residues. From a bioremediation perspective, this
clearly represents an overall beneficial scenario. The mechanisms
were attributed to the promotion of pesticide degraders in earthworm
gut being added to the soil, changes in carbon substrate availabili-
ty and changes in soil structure subsequently altering compound
availability.
Further to this study, Kersante et al. (2006) investigated the in-
teractions between earthworms (L. terrestris and A. calignosa) and
atrazine degraders (Pseudomonas sp. ADP) in soil microsites (earth-
worm gut contents, casts and burrow linings). They determined that
atrazine mineralisation was reduced in earthworm soil microsites and
that earthworms significantly altered the soil microbial structures by
reducing the size of the atrazine degrader communities. They also
suggested that low atrazine mineralisation, or loss, could be partly
explained by low effective mineralisation rates in the biostructures
due to sorption to the high organic carbon content, as previously
noted by Farenhorst et al. (2001),Alekseeva et al. (2006) and Binet
et al. (2006).
The effectiveness of earthworm gut microflora to effect soil
contaminant losses, or degradation, has previously been discussed.
For example, Verma et al. (2006) noted the growth potential of
earthworm (Mataphire posthuma) gut microorganisms to the pesticide
Endosulfan, whilst Ramteke and Hans (1992) isolated microorganisms
from the gut of Pheretima posthuma treated with HCH noting
significant subsequent HCH degradation. However, unlike Verma
et al. (2006), the authors noted that HCH degraders (in guts) gradually
increased over a 5 week period, replacing other gut microflora, in-
dicating the potential for specialised gut growth. However, as dis-
cussed by a number of authors (Edwards and Bohlen,1996; Brown and
Doube, 2004; Kersante et al., 2006; Curry and Schmidt, 2007)it
remains questionable whether (a) microorganisms are indigenous
to earthworm guts (b) earthworm gut microflora comes from the
surrounding soil and plant remains, or (c) whether specialised feeding
determines distinctive gut flora.
A number of studies relating to the application of earthworms, or
the effects of earthworms, upon soil associated agrochemicals have
been discussed. Whilst contradictory results have been observed,
especially with respect to compound sorption and release, it is ap-
parent that there are a number of potentially positive physical effects
upon agrochemical fate.
3.2. Petroleum and crude oil hydrocarbons
Whilst a relatively large amount of research has been undertaken
investigating the effects of earthworms upon agrochemicals, less has
been undertaken upon the effects to petroleum hydrocarbons
(petroleum and crude oil hydrocarbons). In contrast to the agrochem-
ical studies, many of the subsequent studies are descriptive investiga-
tions as opposed to mechanistic ones. However, to highlight the
increased interest of earthworm inclusion in bioremediation for
hydrocarbons, a recent paper elucidated upon the co-application of
compost and earthworms for bioremediation (Ceccanti et al., 2006).
Ceccanti et al. (2006) investigated biochemical processes, including
microbial enzyme activity and carbon dioxide evolution, which took
place during bioremediation treatment of oil refinery sludge with
(1) a mixture of microorganisms, enzymes and nutrients (2) compost
only, and (3) compost with earthworms (E. fetida; 10 per kg soil) for
3 months. Their aim was to use these treatments and variables to
stimulate soil microbial biomass and therefore degradation ability to
explain both microbial activity and the intensity of microbial metab-
olism. They concluded that the reduction in TPH of the oil refinery
sludge was greatest in the treatment with earthworms present
(reduction of 50.3%), followed by compost only (reduction of 39.5%),
highlighting the usefulness of the co-application of compost and
earthworms. Importantly, Ceccanti et al. (2006) stated that the result
could be due to earthworm action and/or soil microbial stimulation
via compost addition and earthworm casts.
An earlier study (Schaefer, 2001) had already concluded that
increased microbial catabolic activity due to E. fetida presence was
responsible for the loss of 91% (1074 mg kg
−1
to 96 mg kg
−1
) of crude
oil contamination when present for 56 days. This was in comparison to
the without-earthworm treatments, which showed no significant
difference in concentrations over the same period. Interestingly, it was
in the soils with the highest initial concentration that degradation was
fastest.
Such results are not always the rule, for example, Callaham et al.
(2002) observed no difference in TPH concentrations associated with
E. fetida or wheat treatments when applied to petroleum contami-
nated soils, whilst Stom et al. (2003), who investigated the effect of
earthworm (E. fetida) application (n=5) to crude oil contaminated
soils (25 g kg
−1
) for 40 days with the co-application of microorganisms
also observed minimal losses (~15 g kg
−1
loss for the microbial in-
oculation and earthworm co-application; ~9 g kg
−1
loss for the
microbial inoculum alone, and only ~3 g kg
−1
loss for earthworm only
treatments). However, in the treatments with earthworms, it was
noted that soil structure and porosity were improved, thus facilitating
oil losses via the introduced microorganisms. However, little meth-
odological data was provided, thus, full understanding of the under-
lying mechanisms cannot be discussed.
Schaefer et al. (2005) investigated the effects of differing earth-
worm species (10 worms/1 kg treatment) (L. terrestris,Allolobophora
chlorotica and E. fetida) on the microbial community within a crude oil
1077Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
contaminated soil (10,000 mg kg
−1
TPH) for 28 days. This is one of the
few studies that have been undertaken with a view to specifically
utilising earthworms for bioremediation of organic contaminants. It
was noted that both respiration and concentration of microbial
biomass was significantly enhanced, with observed changes not only
in microbial numbers and activity but of taxonomic groups, whilst
TPH concentrations were significantly reduced (TPH reduction of 30–
42% in samples with L. terrestris,31–37% in samples with E. fetida
and of 17–18% in samples with A. chlorotica with an average control
TPH concentration decrease of a non-significant 9–17% between test
start and test end). Whilst positive earthworm usefulness within
bioremediation was noted, there were differences in results between
earthworm species due to ecological behavioural differences, thus
reinforcing the importance of choosing species suited to specific en-
vironmental conditions.
Schaefer and Filser (2007) further reported upon their earlier
work (Schaefer et al., 2005), which utilised the three differing earth-
worm species to effect TPH losses in crude oil contaminated soils.
Interestingly, they noted that there was more degradation products
in the with-earthworm soils, indicating that degradation of the longer
chain aliphatics (C
29
–C
36
) had occurred, thus resulting in an increase
of shorter chain aliphatics (C
19
–C
29
). Such an observation was re-
ported by Prince et al. (2007), who stated that within a complex
mixed gasoline mixture; larger n-alkanes were more readily de-
graded than the smaller n-alkanes. Further to this, Schaefer and
Filser (2007) introduced organic additives (coffee grains, horticul-
tural waste (compost) and brewery mash) (as 10% mass) in combina-
tion with earthworms (L. terrestris) to assess microbial crude oil
(5000 mg kg
−1
) degradation over 28 days. Whilst increased micro-
bial respiration was observed in all treatments, only significant TPH
degradation was noted in the earthworm only treatments (decrease of
29%) and the mixed brewery mash treatment with earthworms (19%),
whilst the brewery mash without earthworms resulted in a decrease
of 35%. Other additives had no significant effects upon TPH degrada-
tion. It was noted by the authors that the earthworms did not interact
or feed on the additives, thus minimising the co-application potential.
They concluded that the microorganisms preferred the more eas-
ily degradable organic additives as opposed to the more complex
hydrocarbons.
Considering that compost proves to be useful in bioremediation
procedures and its use as a remediation amendment in combination
with earthworms has been demonstrated by Ceccanti et al. (2006),it
was surprising that the other additives did not determine any
significant TPH decreases. Tomoko et al. (2005) also investigated the
addition of the earthworm (E. fetida) and varying organic wastes to an
oil contaminated soil and found that earthworms alone significantly
decreased oil contents in comparison to the control.
Earthworm use to remediate hydrocarbon contaminated drilling
fluids and cuttings has been investigated (Getliff et al., 2002). How-
ever, as opposed to direct earthworm inclusion to hydrocarbon
impacted soils to effect remediation, the process described by Getliff
et al. (2002) involves adding the drilling wastes to other green wastes,
altering the C:N ratio and the moisture content and adding the
mixture to worm beds as feed. Worm beds were mounds 88 m× 3 m
and covered by polypropylene-backed felt mat, with moisture and
aeration capabilities. The drilling materials/green wastes were applied
to the mounds once a week at an average depth of 15–30 mm. The
worms (E. fetida) integrate with the applied material and consume it
within 5–7 days. Interestingly, the digested material (wormcast, or
vermicast/compost) can be harvested and packaged for fertilizer or as
a soil improver. Over an experimental period of 45 days and at
application of 30% w/w (drill cuttings/organic material), 50% w/w or
70% w/w, significant TPH reductions were observed. At 30% applica-
tion, TPH decreased from 1900 mg kg
−1
to less than 60 mg kg
−1
in
45 days, whilst at 50% application TPH decreased from 2100 mg kg
−1
to below detection limit and at 70% application, TPH decreased from
20,000 mg kg
−1
to 1500 mg kg
−1
. However at a tested application
of 100% drill cuttings, the earthworms did not associate with the
material and thus, degradation was minimal.
The difficulty in the removal of recalcitrant hydrocarbons and
the lack of biodegradability by inherent microorganisms of high
molecular weight compounds is known (Atlas, 1995; Alexander,
2000). This aspect of bioremediation is often a final limiting factor.
Martin-Gil et al. (2007) has recently investigated the use of earth-
worms (E. fetida) and vermicomposting in the treatment of the
high molecular weight hydrocarbons, asphaltens, from the Prestige
oil spill. Green waste (cow bed and potato peelings) (total mass
80%) was added to heavy fuel oil (20%), which then underwent a
composting process. Subsequent to the composting process, earth-
worms were added at a density of 330 g/m
2
(treatment vessel
0.40 × 0.50 × 0.12 m
3
) for 6 months. Definite values of asphaltens
reduction are not given, but they do state that their results reveal
that the microorganisms living in either the earthworm intestines
or vermicompost substrate can possibly mineralise and thus elim-
inate asphaltens.
3.3. Polycyclic aromatic hydrocarbons (PAHs)
PAHs are priority pollutants and cause a great deal of concern
with respect to human and ecological health. They are inherently
recalcitrant hydrocarbons, and the higher molecular weight PAHs can
be difficult to remediate. Thus, whilst soils have otherwise undergone
successful and extensive remediation, the high molecular weight
PAHs still have a presence due to their lack of degradability, and as
such, much work is undertaken to investigate the mechanisms for
their removal and degradation.
Achazi and Van-Gestel (2003) discussed the effects of earthworm
activity on PAH concentration in soils, recognising the fact that their
physical activity are likely to affect the concentrations of these
hydrophobic organic contaminants. They concluded that it was likely
that any improved degradation would be due to improved aerobic soil
conditions, intimate mixing of microorganisms with the soil in the
earthworm gut, and subsequent dispersal via castings, and general
improved working conditions for the microorganisms, as opposed to
any inherent earthworm metabolising capacities.
In support of the theory that earthworm digestion and grinding
actions would affect ingested contaminated material such that the
egested casts would have a greater degree of ‘available’contaminants
for subsequent degradation, Eijsackers et al. (2001) suggested that
earthworms living within PAH contaminated peat sediments have the
capacity to increase PAH availability by consuming the organic matter
and thus reducing the number of potential binding sites. In relation to
this, Gevao et al. (2001) stated that the presence of earthworms
(A. longa) retarded pesticide bound residue formation via their ac-
tivity, which is again in conflict with the previously discussed agro-
chemical results.
With respect to these theories, Ma et al. (1995) studied the in-
fluence of earthworms (L. rubellus) on the disappearance of spiked
phenanthrene and fluoranthene (100 μgkg
−1
) and concluded that
disappearance of both PAHs occurred at faster rates in soil with
earthworms, than soil without. The mechanistic actions behind these
losses remained still to be explored.
Eijsackers et al. (2001) undertook a similar laboratory based study
investigating the fate of phenanthrene and fluoranthene (10 mg kg
−1
)
in the presence and absence of earthworms E. fetida per 850 g of
artificial soil containaing10% or 40% organic matter. After 50 days,
highly significant differences in concentrations were observed be-
tween the with-earthworm and the without-earthworm treatments
due to earthworm activity improving the inherent conditions for
subsequent microbial degradation. In this instance, there were no
differences between the endpoint concentrations for the 10% and 40%
organic matter with-earthworm treatments.
1078 Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
More recently, Contreras-Ramos et al. (2006) studied the effects of
earthworms (E. fetida) (10 earthworms per 50 g soil) upon the removal
of PAHs (anthracene (200, 500 and 1000 mg kg
−1
), phenanthrene (50,
100 a nd 150 mg kg
−1
) and benzo(a)pyrene (50, 100 and 150 mg kg
−1
)).
The study lasted for an 11 week period, during which time it was
determined that the indigenous microorganisms removed an average
of 23%, 77% and 13% of anthracene, phenanthrene and benzo(a)pyrene,
respectively, whilst the with-earthworm treatments removed
averages of 51%, 100% and 47%. Whilst mechanisms for loss were not
studied, PAH losses were significant in terms of extent, which would
indicate a definite benefit to earthworm inclusion.
In relation to the study of Contreras-Ramos et al. (2006), co-
workers (Alvarez-Bernal et al., 2006) further investigated dissipa-
tion of soil associated phenanthrene (500 mg kg
−1
), anthracene
(350 mg kg
−1
) and benzo(a)pyrene (150 mg kg
−1
) when vermicom-
post (product of farm yard waste and E. fetida) was added (308 mg
vermicompost added to 250 mg soil) for 100 days. They noted that the
greatest losses of the three PAHs were apparent in the unsterilized
vermicompost and PAH-treated soil as well as in the PAH-treated soil
after 100 days of treatment. Whilst generally, the with-vermicompost
treatment determined a more rapid loss in the initial study period (0–
30 days), there was no significant difference in loss extents at study
end (100 days). Losses were almost 100% of the initially spiked com-
pounds, and whilst CO
2
measurements were highest in the vermi-
compost amended treatments, thus indicating increased microbial
activity, the authors suggest that this only had a minimal effect upon
PAH dissipation.
3.4. Polychlorinated biphenyls (PCBs)
In contrast to the oil and petroleum associated hydrocarbon con-
taminants already discussed, These chlorinated hydrocarbons show a
high thermodynamic stability and degradation mechanism generally
requires high heat or catalysis. As such, metabolic degradation
generally proceeds quite slowly relative to most other compounds.
Singer et al. (2001) investigated the use of earthworms (Pheretima
hawayana) to aid in the mixing and distribution of PCB-degrader
microorganisms when added to Aroclor 1242 contaminated soil
(100 mg kg
−1
) over an 18 week period (10 earthworms per 0.6 kg
treatment). The with-earthworm treatments resulted in significantly
greater PCB losses (average of all treatments: 52% loss), when com-
pared to the without-earthworm treatments (average of all treat-
ments: 41% loss). Further to this, the authors noted that the with-
earthworm treatments had more uniform distribution of residual PCB
due to earthworm bioturbation and mixing processes, a similar result
being stated by Binet et al. (2006) and Farenhorst et al. (2000a)
regarding earthworm redistribution of
14
C-atrazine within soil mi-
crocosms. The authors concluded that PCB losses were partly aided
by burrowing activity, thus allowing infiltration of microorganisms
and allowing gas exchange and diffusion (10-fold greater gas diffusion
in this case), and that deposition of nutrient rich casts maintained a
more metabolically active microbial community. It is important to
point out that the species of earthworm was chosen for its ecological
characteristics. This being an anecic earthworm thus suited to vertical
burrowing and the experimental approach undertaken.
A later study by Leupromchai et al. (2002) also investigated the
effectsofearthworms(P. hawayan a; two per treatment) and
introduced PCB degrading microorganisms (individually or in combi-
nation) upon the loss of Aroclor 1242 (100 ppm) added to 0.6 kg soil
over a nine week period. Again, extensive mixing of PCB residues
by earthworms was noted, with the most significant losses in the
earthworm and microorganism treatments (i.e. when in com-
bination). Soil sorption effects were not noted, but rather, it was
commented that the physical earthworm activity did aid in the
distribution of PCB degraders throughout the columns and their
presence contributed to increase the growth and activity of indigen-
ous PCB degraders, as was previously notedby Singer et al. (2001). The
control system resulted in an average loss of 20% whereas earthworms
in combination with the bioaugmented microorganisms resulted in an
average PCB loss of 54.7%. In addition, the bioaugmented microorgan-
isms on their own resulted in 33% PCB loss and earthworms on their
own also resulted in 33% PCB loss, however, these loss differences
were more pronounced within the top 3 cm of the soil column. It was
suggested that compounds associated with the earthworm casts were
potentially able to promote indigenous PCB degraders, and that
earthworm presence determined an 8 fold increase in indigenous PCB
degraders.
In a different scenario, Tharakan et al. (2006) investigated the use
of E. fetida (9 g) within vermicomposting bioreactors for 180 days for
the remediation of PCB contaminated sludge (N500 ppm Aroclor
1248). They noted that whilst there was a total PCB reduction of 55–
66%, the without-earthworm control also showed a reduction of 48–
68%. Whilst the earthworms in the vermicomposting bioreactor
did manage to eliminate and transform some of the PCBs due to
hypothesised microbial gut populations and digestive activity, the
authors concluded that losses from the sludge were mostly due to
bioaccumulation, leading to PCB concentrations as high as 313 ppm.
3.5. Other compounds
Earthworm metabolising capabilities of organic contaminants is
an area that has received even less research and highlights a po-
tentially more complex earthworm/contaminant interaction. It has
been suggested that earthworm metabolism of PAHs is weak and
hardly inducible (Berghout et al., 1991; Achazi et al., 1998; Ma et al.,
1998; Achazi and Van-Gestel, 2003), which is supported by Milli-
gan et al. (1986) who specifically noted that cytochrome P-450-
dependent monooxygenase activity was not induced in earthworms
(Dendrobaena veneta) by 3-methylcholanthrene or Phenobarbitol.
Bundy et al. (2002) further discusses the role of earthworm (E. veneta)
CYP450 activity in the metabolism of 4-fluoroaniline and 4-fluorobi-
phenyl, and they found no metabolism and limited metabolism,
respectively. Further to this, Renoux et al. (2000) observed that the
presence of E. Andrei either metabolised TNT or promoted TNT de-
grader microorganisms, and in an earlier paper, Sternerson (1984)
highlighted the potential importance of earthworms for the degrada-
tion of man-made chemicals via detoxication enzymes and reviews a
number of studies to support this. A slightly different earthworm
effect was observed by Albro et al. (1993), in that L. terrestris had the
ability to hydrolyze the plasticiser di-(2-ethylhexyl) phthalate, but
that losses by such methods were minimal and suggested no real
benefit to utilising earthworms in this way.
4. Concluding remarks
Through a combination of direct and indirect earthworm effects,
both upon the promotion of catabolically competent microorganisms,
and through earthworm biological, chemical and physical actions,
earthworm assisted bioremediation has been shown to be suited to a
wide range of organic compounds. This review has presented and
discussed a number of investigations that support earthworm assisted
bioremediation as a viable approach for the application to contami-
nants such as agrochemicals, crude oils, PAHs and PCBs.
Earthworm differences in terms of niche type (epigeic, endogeic and
anecic) dictate response and behaviour to soils, contaminants, food
availability and type, and a number of other environmental parameters.
Importantly, any earthworm assisted bioremediation procedure would
need to identify the correct earthworm species for the intended
methodology and conditions. This should involve the preliminary
assessment of suitability for conditions and toxicity assessment.
Earthworm potential for remediation of contaminated soils has
been noted by a number of authors within this review, with the main
1079Z.A. Hickman, B.J. Reid / Environment International 34 (2008) 1072–1081
beneficial areas being the mechanical development of the abiotic
systems in terms of burrowing, ingestion, grinding, digestion and
excretion of casts, and upon the biotic systems in terms of promoted
microorganisms. Additionally, following ingestion and re-working of
contaminated soils, it is plausible that the sequestered or sorbed
fraction of contaminants would undergo physical release, thus making
them available for subsequent microbial degradation; an area for
further research.
In relation to this, if earthworms were present within, for example,
hydrocarbon contaminated soils, then it could be hypothesised that
there would be a subsequent promotion of hydrocarbon degrading
microorganisms. In theory, this could achieve subsequent increased
rates of hydrocarbon mineralisation, with the extents of mineralisa-
tion being contributed to via optimised soil conditions. The subse-
quently inoculated, or pre-exposed, soil (or cast) could then be applied
as a remediation media, again aiding in increased rates, and poten-
tially extents of compound loss.
There would appear to be a number of advantages in the utilisation
of earthworms within organic contaminant bioremediation. For
example, they have been shown to both retard the binding of com-
pounds and increase compound availability, whilst increasing micro-
bial degradation and promoting favourable microbial conditions. Their
mechanical actions further optimise soil conditions, offsetting known
remediation limitations. However, not all research is corroborative;
both agrochemical and crude oil studies have shown that earthworm
presence and actions can increase compound sorption, and thus
persistence, with other studies noting no beneficial effect at all. It is
difficult to directly compare all studies due to the differences in
experimental set-up, soil types, compounds, earthworm species dif-
ferences and controlled variables. Furthermore, earthworms have the
potential to be employed not only in the recovery of contaminated
soils as part of a bioremediation strategy, but also in the subsequent
improvement of that soil, in terms of structure and nutritional status.
In relation to this, research should focus upon standardised compara-
tive studies and dedicated mechanistic studies. Regardless of this,
earthworm inclusion as a biotechnology has potential, and is worthy
of future research if a number of obstacles could be overcome, such as
toxicity issues and appropriate remediation strategies.
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