Applied Soil Ecology xxx (xxxx) xxxx

Contents lists available at ScienceDirect

Applied Soil Ecology

journal homepage: www.elsevier.com/locate/apsoil

Reviews

Vermiremediation of organically contaminated soils: Concepts, current

status, and future perspectives
Zhiming Shia,b, Jinghao Liua, Zhiwen Tanga, Yonghua Zhaob,*, Congying Wanga,b,**
a
College of Environmental and Resource Sciences, Shanxi University, Taiyuan, 030006, PR China
b
Shaanxi Key Laboratory of Land Consolidation, School of Earth Science and Resources, Chang’an University, Xi’an, 710064, PR China

A R T I C LE I N FO A B S T R A C T

Keywords: Vermiremediation is an expanding technology that uses earthworms to remediate organically contaminated soils
Earthworm and has been attracting attention from researchers gradually. This review outlines general aspects of vermir-
Drilosphere emediation, including its concepts, processing of organics-polluted soils, its advantages and limitations, the
Vermiextraction methods for enhancing vermiremediation, and other peripheral issues. Processes involved in vermiremediation
Vermitransformation
of soils contaminated by organic chemicals mainly include vermiaccumulation and vermiextraction, vermi-
Drilodegradation
transformation, and drilodegradation. Vermiaccumulation plays an important role in vermiremediation and
should be highlighted. Vermiremediation technology can be characterised as environmentally friendly, effective,
sustainable. Strategies for enhancing vermiremediation might include the use of surfactants, nutrient amend-
ments, management strategies, or combinations with other remediation technologies. Unlike previous reviews,
peripheral issues such as the inoculation and colonising of earthworms in contaminated field and methods for
harvest and disposal of earthworms used in vermiremediation are also discussed. However, there are many issues
need to be clarified, including i) the capacity, contribution, and mechanisms of different vermiremediation
processes; ii) the behaviour of organic pollutants in the drilosphere, iii) enhancement measures for vermir-
emediation and their side effects, and iv) earthworm collection methods in polluted soil and their post-harvest
disposal. This review gives a general outline of vermiremediation, which is expected to promote further studies
and practical application of vermiremediation in organically contaminated soils.

1. Introduction of organic contaminants in soil include chemical treatments and phy-

Due to the rapid and increasing process of industrialisation, China
and other regions around the world are suffering from serious soil
pollution from organic chemicals (Kang, 2014; Shi et al., 2017). Or-
ganic chemicals of particular concern in the environment generally
include petroleum hydrocarbons (PHCs), volatile organic compounds
(VOCs), polycyclic aromatic hydrocarbons (PAHs), halogenated hy-
drocarbons pesticides and polychlorinated biphenyls (PCBs), organic
solvents and others which are released by both natural and anthro-
pogenic sources, but mostly by the latter (Megharaj et al., 2011). As the
major sink for organic chemicals, soils containing organic pollutants
exert potential risks on humans and the overall ecological health (Shi
et al., 2017). Therefore, in recent decades, increasing attention has been
paid to the remediation of soils polluted with organic chemicals
(Megharaj et al., 2011; Kang, 2014).
Conventional remediation technologies for the treatment or removal
sical removal such as soil vapor extraction, soil washing, stabilisation
and solidification, electrokinetic remediation, thermal desorption, in
situ chemical oxidation, pumping and treatment, in situ flushing, and
monitored natural attenuation (Kang, 2014; Passatore et al., 2014;
Chirakkara et al., 2016). However, most of these technologies involve
intensive labour, high costs, disturbance of indigenous soil microflora,
and irreversible changes in soil physicochemical properties (Kang,
2014; Passatore et al., 2014; Chirakkara et al., 2016). As an alternative
technology, bioremediation has been developed and is considered to be
one of the most promising remediation options (Kang, 2014). Broadly,
bioremediation refers to the processes that use microorganisms, green
plants, soil fauna, or their enzymes to treat polluted sites to restore their
original condition (Wu et al., 2010). Among the forms of bioremedia-
tion, most studies have generally focused on phytoremediation and
microbial remediation (microremediation), while, by comparison, the
use of soil fauna such as earthworms to address soil contamination has

⁎
Corresponding author.
⁎⁎
Corresponding author at: College of Environmental and Resource Sciences, Shanxi University, Taiyuan, 030006, PR China.
E-mail addresses: yonghuaz@chd.edu.cn (Y. Zhao), wangcongying@sxu.edu.cn (C. Wang).

https://doi.org/10.1016/j.apsoil.2019.103377
Received 25 February 2019; Received in revised form 22 September 2019; Accepted 5 October 2019
0929-1393/ © 2019 Elsevier B.V. All rights reserved.

Please cite this article as: Zhiming Shi, et al., Applied Soil Ecology, https://doi.org/10.1016/j.apsoil.2019.103377
Z. Shi, et al. Applied Soil Ecology xxx (xxxx) xxxx

Fig. 1. Processes involved in vermiremediation of organically contaminated soils.

received relatively little attention (Wu et al., 2010). Considering the ‘vermiremediation’, and specifically focuses on the following: i) the
limitations of phytoremediation and its stagnant in real-world appli- concept of vermiremediation, the possible processes and mechanisms
cation (Mench et al., 2010; Gerhardt et al., 2017), focusing attention on involved and their definitions in the context of ‘vermiremediation’; ii)
the use of earthworms as a soil treatment technology may pay sig- the characteristics of vermiremediation; iii) the potential approaches
nificant dividends. for enhancing vermiremediation; and iv) several peripheral but un-
Earthworms acting as soil ecological engineers are well-known for avoidable issues that require attention prior to implementation of ver-
their profound effects on the chemical, physical, and biological pro- miremediation. This review might provide a framework and facilitate
cesses that occur in its immediate vicinity (Shi et al., 2017). In agri- further research on vermiremediation and promote its application in
cultural production, earthworms promote crop growth by improving real-world field tests.
the nutrient content of soil and reduce the toxicity of wastes and may
help detoxify contaminated soil (Singh et al., 2018). Given their key
2. The concepts and processes of vermiremediation for organics-
role in terrestrial ecosystems and unique biological advantages, earth-
contaminated soils
worms have been widely studied for a variety of purposes since the
1800s (Edwards, 2004; Shi et al., 2017). In the field of soil remediation,
2.1. Concept of vermiremediation
studies on their use might date back to 1980s (Sinha et al., 2010).
However, the rapid expansion in this field only began in the last decade,
The term ‘vermiremediation’ is a combination of two words: Latin
and the term ‘vermiremediation’ was only recently invoked (Sinha
vermis (meaning worm) and the Latin remedium (meaning to correct or
et al., 2008; Gupta and Garg, 2009; Rorat et al., 2017). To the best of
remove an evil). To the best of our knowledge, the term ‘vermir-
our knowledge, only four reviews concerned the application and po-
emediation’ was first used by Edwards and Arancon (2006) (based on
tential use of earthworms for remediation (vermiremediation) of soils
the research results from Google Scholar and Web of Science). How-
contaminated with organic compounds (Hickman and Reid, 2008;
ever, Rodriguez-Campos et al. (2014) might be the first authors who
Sinha et al., 2008; Dendooven et al., 2011; Rodriguez-Campos et al.,
defined the term, which states ‘the use of earthworms for removing
2014). In these reviews, earthworm abiotic and biotic effects upon the
contaminants from the soil or when earthworms help to degrade non-
soil environment, presence of earthworms in contaminated soils, me-
recyclable chemicals’. This definition appears to be somewhat vague,
chanism of vermiremediation (bio-accumulation and bio-transforma-
and, thus, a detailed definition was provided with caution here. Ver-
tion/bio-degradation, etc.), advantages of vermiremediation, removal
miremediation is an earthworm-based bioremediation technology that
of various contaminants (PAHs, petroleum and crude oil hydrocarbons,
makes use of use the earthworm’s life cycle (i.e., feeding, burrowing,
agrochemicals, and PCBs) from soil and other issues have been dis-
metabolism, secretion) or their interaction with other abiotic and biotic
cussed. However, up to now, a framework of vermiremediation still
factors to accumulate and extract, transform, or degrade contaminants
lacks considering that many aspects of vermiremediation, for example,
in the soil environment. According to the definition, the following
strategies and approaches to improve the efficiency of the earthworm-
terms might be used to describe possible processes and mechanisms
based remediation process, and methods for harvesting earthworm after
involved in vermiremediation: vermiextraction and vermiaccumula-
a round of remediation process etc., have not been fully discussed.
tion, vermitransformation, and drilodegradation. Fig. 1 depicts these
Besides, previous review on the description of mechanism of vermir-
processes.
emediation, i.e., bio-accumulation and bio-transformation/bio-de-
gradation, seems to be somewhat vague, general, incomplete and fea-
tureless (Sinha et al., 2008), which cannot highlight the role of 2.2. Vermiaccumulation of organic pollutants
earthworms in remediating polluted soil. Therefore, the processes and
mechanism involved in vermiremediation need to be further explored Vermiaccumulation and vermiextraction refer to the process in
and explicitly defined. which earthworms take up and, subsequently, store the contaminants in
Based on these critical aspects, this review aims to provide an their bodies and therefore reduce the amount of pollutants in soils.
overview of earthworm use in remediation of soils using Studies related to vermiaccumulation in the past decades largely em-
phasised the environmental behaviour of organic contaminants in soil-

2
Z. Shi, et al. Applied Soil Ecology xxx (xxxx) xxxx

Table 1
Models for predicting the vermiaccumulation of HOCs.
Models Equations Description References

Empirical models logBCF = alogK ow + b Plot log BCF versus log KOW, and obtain a regression which can be used as a (Jager, 1998; Mackay and Fraser,
predictive correlation. 2000; Meylan et al., 1999)
Equilibrium-partition Cworm =
BCF
Csoil Based on the assumption that only the dissolved fraction of the chemical in (Ma et al., 1998; Sijm et al.,
kd
models interstitial water is available for uptake by earthworms via passive diffusion. 2000)
k d = K oc foc
logK oc = alogK ow + b
Rate models Cworm =
ks Csoil + ki Cw Two routes of uptake are incorporated: uptake by passive diffusion from the (Belfroid et al., 1995)
k2 interstitial water and dietary uptake. Uptake and elimination processes follow first-
order one-compartment kinetics
Mechanical models Fwater + F lipid K ow Csoil When the solid phase, pore water, and organism are in thermodynamic equilibrium, (Jager, 1998; Jager et al., 2003)
Cworm =
ρworm kd the concentration in the organism is determined by the concentration in the solid
phase and the steady-state partition coefficients

BCF, bioconcentration factor, are expressed on a solution basis either on a fresh or dry weight basis; Kow, Koc and Kd are the octanol-water, organic carbon-normalized
and soil-water partition coefficients of HOCs; foc, content of organic carbon in soil (%); Cworm, Csoil and Cw are the concentrations of HOCs in earthworms, in soil solid
and in soil solution, respectively; Fwater and Flipid are the volume fraction of lipids and water in earthworms, respectively. ρworm is the bulk density of earthworms. ks,
ki and k2 are the dietary uptake rate constants, uptake rate constants from interstitial water and elimination rate constants.

earthworm systems, including three aspects: the pathways by which
organic contaminants can enter into earthworms (Belfroid et al., 1995;
Jager, 1998; Jager et al., 2003), the bioaccumulation and distribution
of organic contaminants in earthworms (Ma et al., 2012; Shi et al.,
2014; Chen et al., 2017; Li et al., 2017; Miao et al., 2018), and the
relevant models describing the uptake and accumulation of organic
contaminants (Jager, 1998; Jager et al., 2003).
2.2.1. Uptake, accumulation and distribution of hydrophobic organic
contaminants (HOCs) in earthworms
Earthworms take up organic chemicals through two pathways:
passive epidermal uptake and dietary uptake (Jager, 1998; Jager et al.,
2003; Shi et al., 2014). In the passive epidermal uptake pathway, up-
take passively occurs in the direction of decreasing chemical potential.
Then, the organic compounds dissolved in pore water or weakly asso-
ciated with the surfaces of particulate matter are adsorbed to the
bodywalls or absorbed by the bodywalls, pass through it and are,
subsequently, translocated within the body of the earthworm (Belfroid
et al., 1995; Jager, 1998; Shi et al., 2014). By contrast, the dietary
uptake pathways is essentially the result of earthworm feeding on soil
with organic compounds, which can be grounded, digested, and un-
dergo other processes associated with earthworm’s life activities, re-
sulting in the organic compounds within the soil being absorbed by the
intestinal tract and/or subsequently translocated to other earthworm
tissues (Jager, 1998; Shi et al., 2014). The process of vermiaccumula-
tion is correlated with the physiological characteristics of the earth-
worms such as the lipid content of their tissue, the levels of con-
taminants in the soil or sludge, and the physicochemical characteristics
of organic-like aqueous solubility and concentration (Rodriguez-
Campos et al., 2014). It is generally believed that the contributions of
the two routes differ; for hydrophobic chemicals that have a logKow < 5
(Kow is the octanol-water partition coefficient), epidermal uptake is the
dominant route (Jager et al., 2003).
The accumulation of organic contaminants in earthworms has been
widely studied during the past decades and parts of those studies were
summarized together in Table S1 as supplementary material. Relevant
contaminants included PAHs (Malev et al., 2016; Šmídová et al., 2017;
Zhang et al., 2017), PCBs (Yang et al., 2013; Xu et al., 2014), pesticides
(Nyholm et al., 2010; Miao et al., 2018), emerging organic con-
taminants (Wen et al., 2015; Navarro et al., 2016), and enantiomers of
some pesticides (Wang et al., 2014; Qin et al., 2015; Chang et al., 2016;
Ye et al., 2016). Most of these studies were designed to assess the
bioaccumulation of chemicals in the earthworms serving their regula-
tion and toxicity/risk assessment, the effect of environmental factors
(e.g., soil amendments, soil types, aging process, etc.) on the accumu-
lation of chemicals, bioavailability assessments, and enantioselectivity
toxicity and accumulation of enantiomers.
Regarding the distribution of organic contaminants in earthworms,
there are not as many as those on accumulation; however, some pro-
gress has been made on this issue. A hierarchic method has been de-
veloped for studying the distribution of organics in the earthworm,
which fractionated earthworm into different parts at three levels: sub-
organism (pre-clitellum, clitellum and post-clitellum), tissue (body
wall, gut, and bodyfluids) and subcellular (intracellular and extra-
cellular fractions) (Shi et al., 2014). The distribution of phenanthrene,
fluoranthene, tetrabromobis phenol A, hexabromocyclododecane dia-
stereoisomers (α-, β-, and γ-HBCDs) and lindane in earthworms have
been investigated (Shi et al., 2014; Ma et al., 2012; Chen et al., 2017; Li
et al., 2017; Miao et al., 2018). The results have indicated that the
distribution of contaminants is heterogeneous (Shi et al., 2014). For
example, at the tissue level, similar results were found, particularly that
the distribution of contaminants in gut fractions was higher than that in
bodywall (skin) fractions (Ma et al., 2012; Shi et al., 2014; Chen et al.,
2017; Li et al., 2017; Miao et al., 2018).
2.2.2. Models for describing and predicting the uptake and accumulation of
HOCs in earthworms
Since it is impossible to study each chemical and each earthworm
species under all possible conditions, relevant models describing and
predicting uptake and accumulation in earthworms have been devel-
oped. Empirical models, rate models, equilibrium-partition models,
mechanical models, and fugacity models have been developed succes-
sively (Table 1). However, it seems that these achievements were oc-
curred approximately 20 years ago, while little progress has been made
in recent years.
2.2.3. The potential of vermiaccumulation and vermiextraction in
remediating organics-polluted soils
Although there are many studies related to vermiaccumulation and
vermiextraction, its role in vermiremediation has not been well-ac-
knowledged, which may be due to the uncertainty about whether
earthworms accumulate large amounts of contaminants (Shi et al.,
2018). Studies concerning the bioaccumulation of organic pollutants in
earthworms during the past decades to address these issues have been
compiled (Table S1). Table S1 shows that the concentrations of HOCs in
earthworms varied greatly. Some studies showed that levels of organic
pollutants in earthworm are small (Liu et al., 2015; Khorram et al.,
2016; Deng and Zeng, 2017), while other results confirmed that the
concentrations of some chemicals in earthworms could be very high,
even when the concentration in the soil was rather low (Denyes et al.,
2013; Šmídová and Hofman, 2014). Furthermore, our previous study
results obtained from adsorption experiments also indicated that

3
Z. Shi, et al.
earthworms have the potential ability to carry a large amount of HOCs,
given their relatively high lipid content and that lipid fractions are the
main pool for organic contaminants (Shi et al., 2018).
It is noteworthy that in phytoremediation technology, hyper-
accumulator plants such as Thlaspi caerulescens, Alyssum bertolonii,
Arabidopsis helleri among others, for Cd, Co, Ni, Pb, Zn metals are well-
studied and acknowledged (Sarwar et al., 2017), while seemingly little
attention has been paid to the roles of earthworms as potential hyper-
accumulators for organic contaminants. Actually, under certain condi-
tions, the BSAFs (biota-to-soil accumulation factors, Ce/Cs, where Ce
and Cs are concentrations of test chemicals in earthworms and soil) of
some organic contaminants, which is used to describe the effectiveness
of earthworm take up and accumulation HOCs from soils due to uptake
from all exposure routes (Xu et al., 2014; Zhao et al., 2014), can be very
high. For example, the BSAFs of PCBs, phenanthrene, pyrene, lindane,
p,p’-DDT and PCBs153 in earthworms were as high as 26, 35, 52, 44, 62
and 39, respectively (Denyes et al., 2013; Šmídová et al., 2015). Fur-
thermore, a simple statistical analysis of Table S1 was made and it is
found that about 49.1% cases showed that concentrations of HOCs in
earthworms were much higher than that in soils. Based on all these
observations, the use of vermiaccumulation where earthworms act as
hyperaccumulators for organic pollutants might be feasible.
2.3. Vermitransformation and vermidegradation of organic pollutants
Vermitransformation and vermidegradation might be defined as the
processes by which organic pollutants in earthworms are degraded with
the help of enzymes such as CYP450 and peroxidise, or by gut microbes
(might be termed as ‘vermin-endophyte’, referring to microorganisms,
bacteria, or fungi, which live within earthworm tissues without causing
any disease), or by both. According to the definition, ‘vermi-
transformation/vermidegradation’ is one of the pathways of ‘vermi-
conversion’ and ‘vermicomposting’. Vermiconversion is termed as the
rapid conversion of slowly biodegradable solid wastes to valuable fer-
tiliser materials through the combined action of earthworms and mi-
croorganisms (Goswami et al., 2013; Sahariah et al., 2014). Vermi-
composting is also a biological decomposition of organic waste to
produce stabilized organic fertilizer, namely vermicompost (Lim et al.,
2016; Bhat et al., 2018). It seems that the two terms are describing a
similar bioconversion process. Therefore, vermiconversion and vermi-
composting includes the remediation of pollutants by default, the use of
the pollutant removal or detoxification ability of earthworms or
‘vermin-endophyte’. However, the target of vermiconversion and ver-
micomposting are biodegradable solid wastes while vermitransforma-
tion and vermidegradation directly focuses on the remedy of chemicals
(e.g., organic pollutants). At present, there exist studies related to
vermintransformation, which were focused mostly on the eco-tox-
icological effects of organic contaminants on earthworms (Lankadurai
et al., 2013; Zhao et al., 2016; Schmidt et al., 2017).
2.3.1. Detoxification of organic xenobiotics in earthworms
Earthworms can accumulate organic xenobiotics from polluted en-
vironments and detoxify them through their metabolic activities.
Table 2 lists studies related to vermitransformation. It can be found that
some earthworm species (mostly E. fetida) possess the capacity for
metabolising some organic pollutants such as 2, 4, 6-trinitrotoluene,
PAHs, herbicides and pesticides (Renoux et al., 2000; Duckett et al.,
2007; Zhang et al., 2016; Schmidt et al., 2017). In recent years, en-
antioselective degradation of enantiomer pesticides in earthworms has
also attracted the attention of scientists (Qu et al., 2014; Wang et al.,
2014). A few metabolites of organic contaminants in earthworms have
also been identified. 10:2 fluorotelomer alcohol could be transformed to
perfluorocarboxylic acids, perfluorononanate and perfluorodecanoate
in earthworms (Zhao and Zhu, 2017). N-ethyl perfluorooctane sulfo-
namide ethanol could be transformed to n-ethylperfluorooctane sulfo-
namide acetate, perfluorooctane sulfonamide acetate, perfluorooctane
4
Applied Soil Ecology xxx (xxxx) xxxx
sulfonamide, and perfluorooctane sulfonate in the soil, and n-ethyl-
perfluorooctane sulfonamide acetate was the predominant metabolite
of earthworms (Zhao et al., 2016). However, obviously, many meta-
bolites still need to be identified, indicative of the complexity of ver-
mitransformation and vermidegradation processes.
Regarding the biochemical metabolic processing of organic con-
taminants in earthworms, it has been described as a series of processes
that use enzymes catalysis (Saint-Denis et al., 1999). There are two
major biochemical processes by which metabolism occurs in eu-
karyotes: Phase I- transformation and Phase II – conjugation. In Phase I,
hydrophobic contaminants get transformed into chemically active,
more polarised, and more water-soluble compounds by the introduction
of a functional group, such as hydroxyl or sulphonyl groups, which
prepare the compound for Phase II reactions (Brown et al., 2004). Re-
actions, such as epoxidation, N-, O-, S-dealkylation, peroxidation, aro-
matic and aliphatic hydroxylation, sulphoxidation, and oxidative de-
sulphuration reactions might occur, but it seems focused reactions are
mostly oxidations catalysed by cytochrome P-450 s in Phase I pathways.
Cytochromes P450 (CYP450, P450, CYPs) are a super enzymatic family
widely distributed in living organisms from bacteria to mammals and
CYP450 are of central importance in the detoxification and bio-
transformation of xenobiotics (Li et al., 2018). CYP450 genes have been
identified in L. terrestris and E. fetida (Lankadurai et al., 2013; Schmidt
et al., 2017).
Phase II conversion involves either direct conjugation of organic
contaminants or conjugation of metabolites from Phase I reactions, with
glutathione, amino acids, or sugars (Brown et al., 2004). Conjugation
occurs by covalent linkages with any of these endogenous molecules,
thus, producing hydrophilic conjugates. For example, E. andrei pro-
duces three pyrene metabolites, all of which are conjugates of 1-hy-
droxypyrene (Stroomberg et al., 2004). In Phase II, glutathione S-
transferase (GST) was among the most studied because of its high
sensitivity and ecological relevance. GST catalyses the conjugation re-
action of GSH and electrophilic xenobiotics and, thus, contributes to the
removal of reactive electrophiles. Meanwhile, GST serves as an im-
portant Phase II detoxification enzyme to excrete and eliminate the
products of Phase I metabolism (Zhang et al., 2009b).
2.3.2. The current status of vermitransformation in vermiremediation
In vermiremediation, vermitransformation is also an important
process and mechanism. However, there are still many issues require
clarification: i) the vermitransformation capacity of organic con-
taminants in earthworms is unknown; ii) whether organic pollutants in
earthworms are degraded by earthworms themselves or gut microbes;
iii) the contribution of vermitransformation in vermiremediation.
However, like the contribution of phytodegradation in phytoremedia-
tion (Gan et al., 2009), it is speculated that vermitransformation is slow
considering that there is no clear evidence that the contribution of
metabolism of HOCs in earthworms is significant to their removal from
soil, as far as we know.
2.4. Drilodegradation of organic pollutants
2.4.1. The drilosphere effect and drilodegradation
Here, the drilosphere refers to the 2-mm-thick zone around earth-
worm burrow walls, which was first defined by Bouché (1975) ac-
cording to Brown et al. (2000). Drilospheric soil presents a substantially
different habitat for soil microbes from that of bulk soil, and is con-
sidered to be a critical microbial ‘hotspot’ (Hoang et al., 2016a;
Kuzyakov and Blagodatskaya, 2015). The drilosphere effect, whereby
earthworm excreta supply energy and nutrients to drilosphere micro-
organisms, promotes increased rates of biochemical processes, relative
to those found in un-burrowed soils. Specifically:
i) The drilosphere enriches in liable C and N due to excreta from
earthworm such as residues, mucus and casts as earthworms travel
along their burrowing systems; microbial growth is stimulated in the
Z. Shi, et al. Applied Soil Ecology xxx (xxxx) xxxx

Table 2
Some studies concerning vermitransformation of HOCs and their metabolites in earthworms.
No. Species Contaminants Metabolites References

1 L. terrestiris di-(2-ethylhexyl) phthalate mono-2-ethylhexyl phthalate and phthalic acid (Albro et al., 1993)
2 E. andrei TNT monoamino- (2-ADNT and 4-ADNT) and diamino-nitrotoluene (2,4-DANT and 2,6- (Renoux et al., 2000)
DANT)
3 E. veneta 4-fluoroaniline N-beta-glucoside conjugate (Bundy et al., 2002)
amma-glutamyl conjugate
4 E. veneta 3-trifluoromethylaniline (3-TFMA) alpha- and beta- glucoside conjugates (Lenz et al., 2002)
5 E. andrei Pyrene 3 conjugates of 1-hydroxypyrene (Stroomberg et al.,
2004)
6 E. veneta 2-fluoro-4-iodoaniline N-glutamyl and N-glucoside conjugates (Duckett et al., 2007)
7 E. fetida fenamiphos fenamiphos sulfoxide (Cáceres et al., 2011)
8 E. fetida Diniconazole 1, 2, 4-triazole, (E)-3-(1H-1, 2, 4-triazol-1-yl) acrylaldehyde, etc. (Wang et al., 2014)
9 E. fetida Perfluorooctane sulfonamide perfluorooctane sulfonic acid (Wen et al., 2015)
10 E. fetida lambad-cyhalothrin 3-phenoxybenzoic acid (Chang et al., 2016)
11 E. fetida Decaromodiphenyl ether (BDE209) BDE206, BDE208, etc. (Zhang et al., 2016)
12 E. fetida N-ethyl perfluorooctane sulfonamide n-ethylperfluorooctane sulfonamide acetate, perfluorooctane sulfonamide acetate, (Zhao et al., 2016)
ethanol perfluorooctane sulfonamide, and perfluorooctane sulfonate
13 M. guillelmi Tetrabromobisphenol A (TBBPA) mono- and dimethyl ethers (O- methylation products of TBBPA) (Chen et al., 2017)
E. fetida
14 E. fetida β- and γ- hexabromocyclododecane α- hexabromocyclododecane (Li et al., 2017)
15 E. fetida PAHs conjugated phase II metabolites (Schmidt et al., 2017)
16 E. fetida 10:2 fluorotelomer alcohol perfluorocarboxylic acids, perfluorononanate and perfluorodecanoate (Zhao and Zhu, 2017)
17 E. fetida Perfluorooctane sulfonamide perfluorooctane sulfonic acid (Zhao et al., 2018)
18 E. fetida N-ethyl perfluorooctane N-ethylperfluorooctane (Zhao et al., 2019)
sulfonamidoethanol sulfonamide acetate, N-ethyl perfluorooctane sulfonamide, perfluorooctane
sulfonamide
acetate, perfluorooctane sulfonamide and perfluorooctane sulfonate
19 E. fetida Perfluorooctane sulfonamide perfluorooctane sulfonic acid (Zhao et al., 2020)

drilosphere, which, subsequently, leads to the growth of eukaryotic
grazer populations such as protozoa and nematodes (Stromberger et al.,
2012). ii) Improved aeration status in the drilosphere through the for-
mation of air channels created when earthworms burrow enhance
aerobic bacterial metabolism (Liu et al., 2011; Kuzyakov and
Blagodatskaya, 2015). iii) The microbial load in drilospheric soil might
be improved, since earthworm mucus also provides nutrients, which are
mixtures of carbon-containing compounds including low-molecular
organic acids, amino acids, nucleic acid derivatives, carbohydrates,
phenolics, and enzymes (Zhang et al., 2009a). iv) The liable organic
carbon supply from earthworm excreta and the turnover of substrates
can sustain bacterial communities acting as readily utilisable sources of
energy (aerobic metabolism) or as electron donors (anaerobic meta-
bolism) (Tiunov and Scheu, 1999). vi) The drilosphere holds a higher
number of microbial populations due to the combined effects of the
above factors. All these effects indicate that drilospheric microorgan-
isms have great potential to mineralise and degrade organic pollutants.
A multitude of microbial processes might be activated in the drilo-
sphere, as described above by earthworm activities. Consequently, the
breaking down, elimination, or degradation of organic contaminants by
microorganisms in the zones might be trigged and enhanced (Monard
et al., 2010). Such processes might be defined as drilodegradation or
drilostimulation. Apart from the enhanced quantity and agility of
contaminant degraders, another way to stimulate drilodegradation is
potential enhanced bioavailability. Earthworms release a mass of
complicated glutinous mucus from their body wall, which contains
many compounds, such as dissolved organic carbon, amino acids and
glycerolipids, macromolecules including glycoproteins, mucopoly-
saccharides, lectins, and hemocyanin (Pan et al., 2010; Zhang et al.,
2009a). Some of these compounds might have surfactant properties and
have been known to enhance the apparent solubility hydrophobic or-
ganic compounds. Since the bioavailability of HOCs limits their uptake
and transformation, improved desorption in drilosphere serve as a
significant mechanism for driloremediation success (Katayama et al.,
2010).
2.4.2. Current status of drilodegradation in the view of vermiremediation
Although drilodegradation might be an important process and
mechanism for the vermiremediation of organic contaminants, few
studies have been conducted. Dallinger and Horn (2014) found that [U-
14C] 2, 4-Dichlorophenol (a metabolite of various herbicides) miner-
alisation was higher in cast, burrow wall, and soil from columns with as
opposed to earthworms (A. caliginosa). Data indicated a strong impact
of earthworms on the active microbial community. Liu et al. (2010,
2011) found that burrow walls and 0–5 cm depth bulk soil displayed
higher capacities to degrade 2-methyl-4-chlorophenoxyacetic acid, a
phenoxyalkanoic acid herbicide, than soil from 5 to 10 cm depth bulk
soil. Monard et al. (2010) reported that total bacterial abundance, atz
gene expression and herbicide atrazine mineralisation were induced in
the drilosphere.
Theoretically, the behaviour of organic pollutants in the drilosphere
should be distinct from that in bulk soil due to drilosphere effects.
However, such mechanisms have not been explained fully. The fol-
lowing issues should be explored to promote the use of drilodegradation
in control organically contaminated soil. First, whether the environ-
mental behaviour of organic pollutants in the drilosphere, e.g. bioa-
vailability, the degradation of organic pollutants, and the sorption and
desorption, etc. is different from that in bulk soil should be considered.
Second, whether biological characteristics under pollution stress con-
ditions in the drilosphere, e.g., the biotic community (microbial and
faunal communities), soil enzymes and their activities are different
from that in bulk soil is also an interesting issue requiring considera-
tion. Hoang et al. (2016b) have studied the distribution of enzyme
activities inside worm burrows and found that earthworm burrows are
microbial hotspots with a much higher and denser distribution of en-
zyme activities than reference soil.
3. Characteristics of vermiremediation
3.1. Advantages of vermiremediation
If vermiremediation proves to be technologically feasible after fur-
ther studies and exploration, it has several advantages over conven-
tional physicochemical methods. Primarily, vermiremediation is an
aesthetically pleasing, environmentally- and eco-friendly technology
similar to phytoremediation (Sinha et al., 2008). In general,

5
Z. Shi, et al.
earthworms treat contaminated lands without destroying the topsoil,
thus maintaining or improving soil utility and fertility. There is minimal
disruption of the environment.
Furthermore, it is useful for treating a broad range of environmental
contaminants. Rodriguez-Campos et al. (2014) reviewed that pesticides,
herbicides, PAHs, PCBs and crude oil in the soil can be removed in the
presence of earthworms. It is a relatively efficient technology compared
with phytoremediation technologies because the contribution of ver-
miaccumulation for organic pollutants might be significant, which is
different from phytoaccumulation (Wu et al., 2018). It is an en-
vironmentally sustainable in-situ approach to remediate sites con-
taminated with PAHs in less than a year, within several growth cycles
(Kuppusamy et al., 2017). Another benefit is that vermiremediation can
improve soil quality by enhancing organic matter, nutrient concentra-
tions, and biological activity (Sinha et al., 2008). Our previous also
showed that earthworms still play the role of ecosystem engineers even
in polluted soil (Shi et al., 2019).
3.2. Limitations of vermiremediation
The vermiremediation technique also has certain limitations like
any bioremediation technologies. Vermiremediation is only applicable
in slightly or moderately contaminated soils, which allow earthworm
survival. Severely contaminated soil may be toxic to earthworms, and
thus their survival may be affected by the toxicity of the contaminants
(Rodriguez-Campos et al., 2014; Shi et al., 2019). Furthermore, ver-
miremediation is only applicable to depths with earthworm activities,
which depends on the ecological groups of earthworm species used.
Based on their habitat preferences, earthworms are categorised as epi-
geic, anecic, and endogeic. Epigeic earthworms, e.g., E. fetida live on the
upper surface of soils to feed mainly on plant litter and other organic
debris on the soil surface and are also classified as detritivores ac-
cording to their feeding habit. Similarly, anecics and endogeic are
termed as phyto-geophagous and geophagous, respectively
(Bhattacharya and Kim, 2016). Therefore, vermiremediation potential
might also be restricted by food abundance, since it mainly relies on the
feeding preferences of the worm species (Bonkowski et al., 2000; Curry
and Schmidt, 2007). However, accumulated contaminants in earth-
worms can be transferred into the food chain in the case of misman-
agement or lack of proper disposal (Shi et al., 2014). Additionally, the
use of vermiremediation might require strict conditions. Earthworms
are sensitive species, and climate or seasonal conditions or other en-
vironmental factors may inhibit earthworm survival and subsequent
vermiremediation processes (Butt and Lowe, 2011).
4. Strategies for enhancing vermiremediation
4.1. General consideration for enhancement strategies
Two factors limiting vermiremediation are earthworm survival and
the mobility and bioavailability of HOCs. Earthworms growth can be
affected severely by poor quality soils and high levels of soil con-
taminants (Sinha et al., 2008). Lack of contaminant mobility and
bioavailability can prevent vermiremediation of organic contaminants
(Rodriguez-Campos et al., 2014). Therefore, enhancement of vermir-
emediation must deal with those two factors. Similar to phytor-
emediation, the vermiremediation of organics-contaminated soils can
be enhanced by several strategies (Megharaj et al., 2011; Gerhardt
et al., 2017; Hussain et al., 2018), including increased contaminant
mobility and bioavailability (using surfactants), increased overall
earthworm growth (and thus uptake capacity) via nutrient amendments
or management strategies, and combination with other remediation
technologies.
6
Applied Soil Ecology xxx (xxxx) xxxx
4.2. Surfactant enhanced vermiremediation
Surfactants are a group of natural and synthetic chemicals that can
desorb, solubilise, or emulsify poorly soluble substrates, and can play
an important role in soil pollution remediation due to their unique
characteristics for the desorption and mobilisation of organic con-
taminants (Chirakkara et al., 2016). Presently, the application of sur-
factants in microbial remediation and phytoremediation of organics-
polluted soil has been widely studied, and the underlying mechanisms
have been well-clarified (Liao et al., 2016; Mao et al., 2015;
Lamichhane et al., 2017; Liang et al., 2017). Many surfactants, such as
non-ionic surfactants (Brij30, Brij35, Tween80, and TX100), anionic
surfactants (sodium dodecyl sulphate, SDS) and cationic surfactants
(cetyltrimethylammonium bromide, CTMAB), have proven effective
bioremediation enhancers (Mao et al., 2015). However, their applica-
tion in vermiremediation has not been explored fully. Mass transfer and
the rate of earthworm uptake are the major factors that limit the ver-
miremediation of HOCs (Lanno et al., 2004). Therefore, theoretically,
surfactants can assist with the mobilisation of contaminants into the soil
solution, making contaminants more accessible and readily accumu-
lated by earthworms (Paria, 2008). Some studies have indicated that
surfactants significantly increased DDE bioaccumulation by earth-
worms; for example, Tween-80 and rhamnolipids increased DDE ac-
cumulation in L. terrestris by 74 and 36 fold, respectively (White et al.,
2007).
However, there are some possible adverse effects of surfactant use,
such as surfactant eco-toxicity and preferential biodegradation of the
surfactant itself by soil microflora (Cheng et al., 2018). The toxicity of
surfactants can be minimised by the use of biosurfactants: surfactants
produced by plants, animals, and many microorganisms, such as
rhamnolipids (Wu et al., 2018). Their merits over synthetic surfactants
include biodegradability, cost-effectiveness, and the potential for in-situ
production (Wu et al., 2018).
4.3. Enhancement of vermiremediation by promoting earthworms growth
Another way of augmenting the efficiency and uptake capacity of
vermiremedial systems is increasing the earthworm biomass by using
food and optimising inoculation conditions. Earthworms have shown a
dietary preference, which indicates that their growth might be im-
proved by improving the food quality (Bonkowski et al., 2000; Curry
and Schmidt, 2007). Increased earthworm growth leads to increased
rates of uptake and organic contaminant degradation in the soil due to
drilosphere effect. In addition, earthworms growth require suitable
survival environment, and, therefore, during vermiremediation pro-
cesses, maintaining optimal inoculation condition, such as temperature,
moisture, food quality, pH, etc., is also necessary to guarantee earth-
worms growth (Butt and Lowe, 2011).
4.4. Combination of vermiremediation with other technologies
Vermiremediation can be enhanced by exploiting microbe-earth-
worm interactions. Microbe-assisted vermiremediation couples earth-
worms with drilospheric microbes that enhance the remediation of
organics by increasing degradation and detoxification rates of con-
taminants, and affecting contaminant mobility, sequestration, and up-
take. Nneji et al. (2016) found that combined treatment with A. millisoni
and Bacillus spp. resulted in a significant reduction in total petroleum
hydrocarbons and increased total organic carbon and N in the soil
compared with other treatments. Sun et al. (2011) reported that the
percentage of pyrene removal in the presence of E. foetida was
45.5–91.0% after 14 d of incubation, which was 2.1–2.8 times greater
than that in treatments without the worms. Li et al. (2015) reported
that the inoculation with both earthworm species A. robustus Perrier
and E. fetida Savigny significantly enhanced soil pentachlorophenol
(PCP) disappearance and basal respiration, which suggests that
Z. Shi, et al.
earthworms can introduce functional bacteria into soils and increase
the population of PCP-degrading bacteria, thereby accelerating soil PCP
degradation. Muñiz et al. (2017) also found that a few days of earth-
worm (A. chlorotica) activity increased the extractability of hexa-
chlorocyclohexane (HCH) isomers (e.g., γ−HCH), facilitating the bio-
degradation of organochlorine compounds.
Vermiremediation can also be combined with phytoremediation.
Deng and Zeng (2017) reported that the removal rates for phenanthrene
in soil was 93% following a treatment of alfalfa + earthworms + white-
rot fungus, a result much higher than the controls containing only
earthworms, only alfalfa, earthworms + alfalfa, alfalfa + white-rot
fungus, which were 33, 48, 66, 74, and 85%, respectively.
Vermiremediation can also be used to clean up residual con-
taminants after the primary remedial treatment has been applied as a
final ‘polishing’ step. Along with residual contaminant clean up, it can
help recover the soil structure and texture after physical or chemical
treatment by providing organic nutrients and encouraging the growth
of microorganisms in the drilosphere (Sinha et al., 2008).
4.5. Use of agronomic practices and soil amendments
At contaminated sites, improving soil texture is often necessary for
earthworm growth because the soils are usually physically compacted,
low in dissolved oxygen, organic matter, and hydraulic conductivity
(Gerhardt et al., 2017). Tillage is important for homogenising soils to
eliminate ‘hot spots’ (i.e., areas with high concentrations of con-
taminants in heterogeneous soil) (Gerhardt et al., 2017), to break up
compact soils to facilitate earthworm movement, and to aerate soils
which can promote drilodegradation of organic compounds.
Increasing incubation densities, and, thus, biomass, can improve the
efficiency of remediation of HOCs. Additional amendments that can be
used for fertilisation include livestock manure, biosolids, biochar, ac-
tivated carbons, compost, sludge, and straw mulch can be used to im-
prove soil texture (Beesley et al., 2011; Denyes et al., 2012; Oleszczuk
et al., 2012; Navarro et al., 2016).
Amendments can also be used when contaminant mobility and
bioavailability increase the risk to biological receptors or hinder re-
mediation. For example, activated carbon can be added to soils to de-
crease the bioavailability and uptake of several organic compounds
(Paul and Ghosh, 2011; Oleszczuk et al., 2012). The use of biochar can
also decrease the bioavailability of some organic pollutants. For ex-
ample, the addition of biochar or activated carbons to the soils greatly
reduced the uptake of PCBs by earthworms (Denyes et al., 2013). Per-
haps the reduced bioavailability of pollutants is not beneficial for ver-
miaccumulation; however, such addition favours the survival of
earthworms, resulting in the enhancement of drilodegradation (Gomez-
Eyles et al., 2011).
Although there are many soil amendments that might have great
potential in enhancing the vermiremediation efficiency, it should be
noted that their effects on soil organisms, biochemical processes, and
soil biological properties must be assessed before they can be utilised
effectively.
5. Brief summary of key scientific issues in vermiremediation
To obtain a general impression on vermiremediation, a brief sum-
mary of the above discussion is depicted in Fig. 2. i) The environmental
behaviour of organic pollutants in soil, soil-earthworm interfaces and
earthworm bodies depend on the bioavailability of organic pollutants
(Lanno et al., 2004); ii) various factors, including physicochemical
properties of soil (e.g., soil organic matter, SOM), properties of HOCs
(e.g., Kow) (Jager, 1998), earthworm secretions (e.g., mucus and casts),
other soil organisms (e.g., microbe), among others, solely or jointly
exert effects on the bioavailability of HOCs in soil (Luo et al., 2012),
and consequently, on vermiremediation; iii) Therefore, various strate-
gies such as soil amendments, surfactants, agronomic practices, and
7
Applied Soil Ecology xxx (xxxx) xxxx
other practices, solely or jointly, indirectly play a role in the improve-
ment vermiremediation efficiency.
6. Peripheral issues needed to be considered prior to in
vermiremediation
6.1. Inoculation and colonisation of earthworm in polluted site
Vermiremediation might require a large number earthworms (Sinha
et al., 2008). Therefore, the first problem that must be solved is the
method of introducing earthworms into polluted soil to activate ver-
miremediation. Butt and Grigoropoulou (2010) reviewed earthworm
inoculation technologies, including turf cutting and relaying, chemical/
physical extraction with broadcasting and earthworm inoculation unit
method. In addition, their advantages and disadvantage were well de-
scribed. However, to confirm the colonisation and secure the applic-
ability of vermiremediation, the survival of earthworms at polluted site
needs to be assessed.
6.2. Harvest of earthworm biomass under polluted soil conditions
Extracting earthworms after finishing a cycle of vermiremediation is
an unavoidable issue. The sampling methods used in earthworm po-
pulation and abundance studies might offer valuable insights. To date,
earthworm sampling methods have been classified into ethological
methods and hand-sorting methods (Velki et al., 2012), which is sum-
marised in Table 3. Since a large number earthworms might be used in
vermiremediation, hand-sorting seems undesirable considering its in-
efficient nature, labor intensiveness, and physical disturbance of soil
system. Other sampling technologies, e.g., chemical extraction
methods, electroshocking, should be considered as potential harvest
methods of earthworm in vermiremediation (Butt and Grigoropoulou,
2010). What is more interesting is using electroshock equipment to
manipulate earthworms (Bohlen et al., 1995; Szlavecz et al., 2013),
which is promising for earthworm harvests. Recently, a simple push–-
pull/pull–pull strategy have been proved to be efficient for harvesting
the earthworms coconut leaf vermicompost produced in tanks, wherein
freshly ground mustard solution was used as repellant (push agent) and
cow dung (with or without bagasse/banana wastes) was used as an
attractant (‘pull’ agent) (Gopal and Gupta, 2019). The strategy might be
also used for the harvest of earthworms from vermiremediation. Al-
though published papers is limited, to the best of our knowledge, there
are many other noteworthy methods for collecting earthworms based
on earthworm biological traits, such as diet preference, sensitivity to
light, heat, temperature, and disturbance (Butt and Lowe, 2011). These
methods are mostly used on earthworm farms for separating and col-
lecting earthworms from substrates and might also be feasible in ver-
miremediation.
Although there are many earthworms sampling methods, their ef-
ficiencies depend on many factors, including the species, maturity stage
of the specimens, habitat type, soil properties, among others (Valckx
et al., 2011). Besides, it should be noticed that current studies on the
efficiency of earthworm sampling methods are conducted in clean soil
or media. However, many studies have confirmed that in contaminated
soil earthworm behaviors have been influenced (Shi et al., 2017),
therefore, whether earthworm sampling methods are still applicable in
contaminated soil remains to be studied further. Besides of sampling
efficiency, combined side effects of different samples methods on
earthworm survival, and pollution stress should be also clarified (Čoja
et al., 2008).
6.3. The fate of earthworms used for vermiremediation
Another important question is the fate of earthworms after used for
vermiremediation of organics-polluted soil. As discussed in Section
2.2.3, earthworms may accumulate a large amount of organic
Z. Shi, et al. Applied Soil Ecology xxx (xxxx) xxxx

Fig. 2. Key scientific issues involved in vermiremediation of organically contaminated soil.

NOTE: symbol "&/|" means that “and/or”, which indicates that various “Impact factors” and “Enhancement strategies” solely or jointly exert effect on bioavailability
of HOCs in soil, consequently, on the vermiremediation.

contaminants, therefore, earthworms used for vermiremediation should
be carefully handled. Similar to the post-treatment of plants used in
phytoremediation, a potentially simple method for disposal of earth-
worms safely is burning as hazardous waste in specialised dumps
(Sheoran et al., 2010; Ali et al., 2013). However, such issues are rarely
considered and need to be studied further to advance the use of ver-
miremediation.
7. Conclusions and prospects
Vermiremediation as an expanding technology available for the
treatment of organics-polluted soil have been acknowledged gradually.
Numerous studies related to vermiremediation have been conducted in
the past decade. Based on these studies, in this present, a framework
covering many aspects of vermiremediation was attempted to be es-
tablished. First, three terms describing the processes involved in ver-
miremediation of soils contaminated by organic chemicals, i.e., ver-
miaccumulation and vermiextraction, vermitransformation and
vermidegradation, and drilodegradation, were explicitly defined and
discussed. These definitions make the processes of vermiremediation
clear and distinctive, which stress the important role of earthworms in
remediating polluted soil. In these processes, vermiaccumulation plays
an important role in vermiremediation and should be highlighted;
Second, vermiremediation might be characterised as environmental
friendly compared with physiochemical remediation and it might be
relatively efficient compared with phytoremediation technologies;
Third, in order to exploit full potential of vermiremediation, enhance-
ment strategies should be employed by improving the bioavailability of
HOCs and earthworms growth. Surfactants, soil amendments, enhanced
biomass and agronomic practices, etc., have the potential to facilitate
vermiremediation; Four, peripheral issues, i.e., inoculation and colo-
nisation, harvest of earthworm and safe post-harvest disposal, are also
proposed and emphasised because these issues are unavoidable in real
vermiremediation practice.
In the future, more fundamental researches are needed considering
that many issues are unsolved to advance the widespread use of ver-
miremediation. The capacity, contribution, and mechanism of different
processes in vermiremediation should be fully clarified, and the beha-
viour of organic pollutants in the drilosphere should be understood
further. The enhancement measures for vermiremediation must be
verified, and attention should be paid to their possible side effects.
Peripheral considerations such as the effectiveness of earthworm

Table 3
Potential harvest methods of earthworms used in vermiremediation – based on the summary of earthworm sampling methods.
Classifications Expellants Characteristics References

Ethological methods Chemical methods Mustard or Non-destructive or “environmental friendly”; more effective on (Chan and Munro, 2001)
hot mustard anecic species; expensive (Lawrence and Bowers, 2002)
Formalin A standard method for the expulsion of earthworms; highly toxic to (Čoja et al., 2008)
soil organism.
Detergent Toxic. (East and Knight, 1998)
Allyl isothiocyanate (AITC) Environmental friendly; effective on deep-burrowing anecic (Zaborski, 2003)
species.
onion solution Environmental friendly. (Steffen et al., 2013)
electrical method Electroshocking Little damage. (Eisenhauer et al., 2008)
Hand-sorting – – Physical disturbance of soil system; labor intensive; time (Valckx et al., 2011)
consuming.
Mechanical separation – – Energy consuming. –

8
Z. Shi, et al.
collection methods from polluted soil and safe post-harvest disposal
should be considered seriously.
Conflict of interest
None.
Acknowledgments
This work was financed by the Natural Science Foundation of China
(Grant No. 41701286), the Fund Project of Shaanxi Key Laboratory of
Land Consolidation (Grant No. 2018-ZD05), and the Fundamental
Research Funds for the Central Universities, CHD (Project No.
300102279504). We also thank Dr. Andrey Zaitsev for his considerable
contribution for improving the manuscript.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.apsoil.2019.103377.
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