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Soil Meso- and Macrofauna Indicators of Restoration Success


in Rehabilitated Mine Sites
Sara Pelaez Sanchez1, Ronan Courtney1, and Olaf Schmidt2
1
Department of Biological Science, Faculty of Science & Engineering, Bernal Institute, University of Limerick, Limerick, Ireland
2
School of Agriculture and Food Science, University College Dublin, Dublin, Ireland

4.1 ­Introduction

Soil supports life on Earth and is a significant contributor to ecosystem services [1, 2]. The Status
of the World’s Soil Resources report identified soil pollution as one of the main threats affecting
soils and ecosystem services globally [3]. The problem is expected to worsen as the global popula-
tion continues to grow and, with it, demand for raw materials such as metals and minerals [4].
Notably, the mining of raw materials is among the worst anthropogenic perturbations as almost all
the components and attributes of the original ecosystem are destroyed [5]. Today, soil pollution is
a global concern due to the potentially hazardous impacts of these pollutants on soil quality, crop
yield and quality [6], and food safety and public health [7].

4.2  ­Restoration to Combat Land Degradation

Restoration allows the reestablishment of some attributes of a former ecosystem; it offers an oppor-
tunity for ecosystem habitat enhancement and an increase in the ecological value by creating new
ecosystem services [8]. In recent years, the science of restoration ecology has turned away from
accurate restoration to past conditions, instead of stressing future trajectories and the resilience of
(socio-)ecological systems  [9, 10]. Ecosystem restoration is increasingly taking place world-
wide [11] as an important contribution to urgently needed responses to environmental degrada-
tion, biodiversity loss, and anthropogenic climate change.
Restoration has evolved significantly over time and has multiple possible connotations [12, 13].
Rehabilitation is a generic term used for ecological repair activities that aim to restore ecosystem
functioning rather than the biodiversity and integrity of a designated native reference ecosystem.
When rehabilitation is used for mined lands or post-industrial sites, it is sometimes called reclama-
tion [13]. For ecosystem restoration in post-mining sites, the core focus is the restoration of soil
processes [8]. For the purposes of this chapter, we use restoration (terminology in McDonald [14]),
remediation, rehabilitation, reclamation, and ecosystem restoration as synonyms in the literature
search. The mining restoration literature encompasses an extensive collection of terminologies for
defining restoration practices [15–17].

Handbook of Ecological and Ecosystem Engineering, First Edition. Edited by Majeti Narasimha Vara Prasad.
© 2021 John Wiley & Sons Ltd. Published 2021 by John Wiley & Sons Ltd.
68 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

Herein, we highlight the current gaps in rehabilitation assessment, especially the role of inverte-
brates as indicators of restoration success, and present future research needs in metalliferous mine
tailings.

4.3  ­Mine Rehabilitation

4.3.1  Mine Tailings


Metalliferous mining produces waste of two distinct physical forms. Very coarse waste rock (usu-
ally 2–20 cm in diameter) consists mainly of unmineralized overburden rock, excavated to uncover
the ore-body, and rock from areas within the ore-body that contain metals at concentrations below
the cut-off grade. Mine tailings, on the other hand, are fine-grained (<2 mm) deposits from the
final stage separators. An estimated 10+ billion tons of mine tailings are produced per year world-
wide [18, 19]. Tailings management facilities are commonly constructed to store tailings. Tailings
sites can be susceptible to dusting and erosion, present a pollution risk, and require some form of
reclamation.

4.3.2  Rehabilitation of Mine Tailings


Historically, abandoned mine tailing sites have been prone to dusting or water erosion and are
therefore a potential source of contamination to the surrounding environment [20]. The absence
of environmental legislation (pre-1990s) limited rehabilitation after the termination of mining
operations and post-closure monitoring programs [21]. Today in Europe, mine waste facilities and
tailings disposal areas in most jurisdictions are operated under license from regulators that often
necessitate the implementation of closure strategies and rehabilitation (Council Directive
2006//21/EC [22]).
Phytoremediation may be an effective means for reducing metal loading in land reclaimed after
surface coal mining, such as in the UK [23]. According to Xie and Van Zyl [24], phytostabilization
stands out as the best potential phytoremediation technique for reducing metal(loid) mobility in
sulfidic tailings. Phytoremediation has also been proven effective for bauxite residue [25] and Pb/
Zn tailings in Ireland [20].

4.3.3  The Challenge of Metal Mine Rehabilitation


Degradation and landform modifications from mining activities produce some of the most difficult
landscapes to restore [16]. Self-regulation is the goal of post-mining ecological land rehabilitation,
where natural processes take over the control and management of the land and govern the devel-
opment of a self-sustaining system [26]. To achieve such endpoints, other challenges need to be
overcome; in particular, mine spoils and mine tailings pose very harsh conditions for plant estab-
lishment and growth due to low organic matter, heavy metal contents, and other unfavorable phys-
icochemical characteristics [27–29].
Herein, we understand the rehabilitated tailings from metal mining as novel ecosystems, and we
follow the definition proposed by Macdonald and King [30]: i.e. novel ecosystems are assemblages
of organisms and abiotic elements that form self-organizing systems that may not have historical
precedent. Rehabilitated mine tailings that have a residue as substrate – even when it is a type of
redeveloped soil or artificial soil (revegetated and amended) – cannot replicate the pre-disturbance
4.4  ­Restoration Success Assessment: Monitoring Diversity, Vegetation, and Ecological Processe 69

soil that develops slowly over long periods in natural systems [31]. We can accept that a certain
ecological abiotic or biotic threshold has been passed and can no longer be restored to a pre-­
disturbance state.
One of the primary challenges for practitioners when working with such sites is the uncertainty
of long-term resilience and the evolutionary and ecological implications  [32, 33]. It requires a
­better understanding of when and why an irreversible ecological threshold has caused an ecosys-
tem to shift to a new stable state [34]. At the same time, mine waste requiring rehabilitation repre-
sents an exciting research field and an opportunity to determine limiting factors for soil fauna and
vegetation colonization and establishment. Ultimately, we want to increase understanding of how
rehabilitated sites can support keystone soil fauna species that, in turn, can accelerate soil pro-
cesses and ecosystem development.
Post-mining rehabilitated sites present hostile conditions, such as lack of suitable food, adverse
physicochemical conditions, unfavorable moisture conditions, and large surface temperature fluc-
tuations  [35, 36]. However, primary succession can occur  [37, 38], and soil fauna communities
gradually develop even in these harsh conditions  [39]. In naturally and artificially revegetated
grassland and wetland soils from historical Irish mine sites, Good [40] observed that some tailings
sites had well-developed soil conditions to support Staphylinid assemblages. However, these areas
need careful study before definitive statements can be made regarding the sustainability of residue
rehabilitation strategies. More information is needed, and long-term field trials should be designed
to target soil faunal colonization and activity in mine wastes and their effects on ecosystem
function [41].
On top of the challenges emerging when working with novel ecosystems are tailings cover sys-
tems, which can be considered manufactured soils or so-called Technosols  [42]. Pedogenic pro-
cesses occurring in Technosols are similar to those occurring in natural soils [43]. However, the
ingredients used during their construction can significantly influence their formation, the result-
ing soil properties, and the soil’s capacity to provide ecosystem services. For mine tailings depos-
ited decades previously, some soil-forming processes may have initiated, leading to a certain level
of soil development [44]. It seems clear that in post-mining scenarios, assembling an entire geoeco-
logical system by applying the rehabilitation engineer approach (principally using machinery and
fertilizer) cannot replicate the pre-disturbance geosystem landscape [26]. For successful ecosystem
reconstruction, it is necessary to further understand the physical, chemical, and biological charac-
teristics of these Technosols. Research should move from simply evaluating vegetation establish-
ment techniques to a more comprehensive assessment of the ecological processes and developments,
including below ground [45, 46]. As part of this, improved knowledge of soil fauna recolonization
in post-mining sites is now considered crucial for meeting restoration objectives after mining [16]
and forming self-regulating ecosystems [45, 47].

4.4  ­Restoration Success Assessment: Monitoring Diversity,


Vegetation, and Ecological Processes

Evaluation of whether goals and objectives are achieved and assessment of the effects (biotic and
abiotic responses to management treatments) of restoration activities are currently missing from
many ecological restoration projects [13]. Such information will enhance conservation outcomes,
aid policy implementation, and boost further investment in restoration science [48]. As part of a
long-established practice, the mining industry has focused on compensation standards set for miti-
gation, which are often based only loosely on ecological criteria. Traditionally, assessment studies
70 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

in restoration projects can be categorized according to three majors attributes they focus on:
(i) diversity, (ii) vegetation, and (iii) ecological processes [48], which also correspond to the foun-
dation of the majority of management and restoration decisions in mine site rehabilitation world-
wide [15, 16, 20, 25, 45].

4.4.1  Monitoring Diversity


The use of species richness or diversity as an indicator of restoration success is a widespread prac-
tice in many cases; for example, in the late 1980s, Majer [49] suggested that local species richness
of particular taxa may indicate ecosystem quality and, consequently, the success of restoration
projects. Previous studies have used species diversity of some small mammals, birds, herpeto-
fauna [50, 51], and invertebrates – especially ants, which are easily surveyed with minimal time
and financial investment [45, 49, 52–55] – to evaluate restoration. However, several authors [56,
57] argue that using species alone as the indicator has several limitations since there is a strong
likelihood of missing rare, cryptic, migratory, or seasonally active species. In particular, the pres-
ence of a vertebrate community in restored areas could indicate temporal habitat sufficiency or
dispersion capacity for fauna but not site quality or habitat conditions to support resident fauna
communities in the long term [58].
Recently, some authors have criticized the viewpoint of a passive role for fauna in restoration
because animal–plant interactions frequently mediate life-history transitions that determine seed-
ling recruitment and other plant community processes. So, some fauna groups can drive the devel-
opmental trajectories of floristic diversity and composition during revegetation [58]. For example,
earthworm bioturbation activity can mediate the effect of tree species on soil development in post-
mining sites [59, 60]. Less attention is placed on studies in which the only goal is to assess site
biodiversity. Instead, there is an increasing trend to assess interactions of fauna with soil physico-
chemical properties.
In contrast to other faunal taxa mentioned, little is known about the colonization and commu-
nity development of soil invertebrate species and the soil food web in rehabilitated mine sites. An
initial characterization of a site using a diversity index could provide useful information about
rehabilitation stages and succession. For restoration efforts to be useful for all soil fauna groups,
assessments should move from using specific taxa as bioindicators to an extensive range of fauna
and their functional roles in the ecosystem [16]. However, the use of too many fauna groups could
be difficult to implement for restoration practitioners. Alternatively, using specific taxa that are
widely studied in mine sites and restored habitats elsewhere, such as by ecosystem engineers,
offers a promising opportunity to bring scientific knowledge into day-to-day rehabilitation prac-
tices for the mining industry.

4.4.2  Vegetation
Revegetation is one of the most common practices in mine site rehabilitation due to its effectiveness
in stabilizing soils, pollution control, and visual improvement [46, 61, 62]. Measures of vegetation
structure (e.g. ground cover, density, height, biomass, and litter) have been established as common
methods for assessing restoration success [63]. Surveying vegetation cover is also widely used as an
above-ground indicator for monitoring restoration success in rehabilitated mine sites [16, 45].
Some authors argue that if the vegetation structure is on a trajectory to be restored to a target,
it usually means a restoration of soil fauna will follow [39, 64]. However, De Deyn et al. [65] have
shown the role of below-ground diversity in above-ground plant development and succession;
4.4  ­Restoration Success Assessment: Monitoring Diversity, Vegetation, and Ecological Processe 71

therefore, regarding soil fauna only as passive respondents to vegetation restoration is not appro-
priate. Soil fauna strongly affect the composition of natural vegetation, and this knowledge might
improve the restoration and conservation of plant species diversity [66]. In post-mining restora-
tion, soil fauna can affect plants via trophic and non-trophic interactions or influence the micro-
bial soil community and physical or chemical properties of the soil  [59, 67]. In temperate
grasslands, earthworms can also influence above-ground vegetation structures by increasing the
spatial heterogeneity of grassland plant communities [68]. Earthworms’ engineering activity and
consequent development of topsoil layers may be an essential driver of plant community succes-
sion, enhances the bacterial food web channel (Frouz et al. [69]) while macrosaprophagous guilds
of soil fauna play an important role in litter decomposition and soil mixing in post-mining
sites [70, 71].

4.4.3  Ecological Processes


The sustainability of a restored system also depends on processes associated with carbon, nutri-
ent, and water cycles; yet most assessments of forest restoration employ indicators for composi-
tion, richness, and abundance of plant species, which are insufficient predictors for long-term
assessments. In an extensive literature review, Ruiz-Jaen and Mitchell Aide [72] found that meas-
ures of biological interactions were the most common ecological processes, followed by nutrient
pools and soil organic matter (SOM). In some restoration projects, the plant community composi-
tion is restored, but ecological processes on which the persistence of the plant communities
depend are not [73].
Soil indicators may be used for assessing the effectiveness of restoring ecosystem functioning
and services. However, selecting the most suitable soil indicators follows a clear identification of
the different and sometimes competing expectations for ecosystem services that the project aims to
restore [63, 74]. For example, detecting initial signs of ecosystem recovery may require decades in
gold and metalliferous tailings [40, 75]. The choice of a few easily measurable and unambiguous
indicators will increase the likelihood that the monitoring will continue for the expected life of the
project evaluation phase. There are many options of indicators (e.g. short-term and long-term), but
making them more uniform would help mutual comparisons among restoration projects [76]. The
relationship between ecological properties, patterns, and processes varies across ecosystems, mak-
ing it difficult to select global short-term and long-term indicators. These need to be ecosystem-
and site-specific indicators: for instance, in dryland ecosystems, soil fertility, water retention
capacity, and water availability are often crucial soil indicators  [63, 74]. According to Cohen-
Shacham et  al.  [77], soil indices such as soil stability, infiltration, and nutrient cycling provide
information on soil function that can be used to guide management decisions during restoration.
Costantini et al. [63] concluded that below-ground soil indicators might be used for assessing the
effectiveness of restoring ecosystem functioning and services. The use of below-ground indicators
for evaluating restoration success has been limited to physicochemical and microbiological indica-
tors, with less attention paid to soil fauna. A small number of studies have also considered methods
based on soil mesofauna composition (microarthropods) [78, 79] or have proposed macrofauna for
the evaluation of soil ecosystem services [63]. For example, the presence or absence of terrestrial
arthropods, mainly Coleoptera, can be used as a cost-effective restoration indicator for assessing
short-term environmental changes in coal mine spoil heaps [80]. However, even if soil biodiversity
is directly related to soil health, and healthy soils can offer a more extensive range of habitat niches
to fauna than poor soils, monitoring restoration success also requires looking at the role that soil
fauna play in soil functions [81].
72 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

4.5  ­Gaps in the Assessment of Restoration Success in Mine Sites

As mentioned previously, the three most common attributes in restoration assessment studies
(diversity, vegetation, and ecological processes) are essential for the long-term persistence of an
ecosystem [82]. Mining companies’ previous efforts to speed up ecosystem recovery have failed
when they focused on visual recovery rather than soil-related problems [80, 83]. Moreover, limited
studies have measured the reproducing population or evaluated the self-sustainability of ecosys-
tems because these are long-term attributes that can rarely be measured in the time frame of most
restoration projects  [13, 72, 84]. Few restoration projects predetermine criteria for success, and
even fewer quantitatively monitor project outcomes [48]. This is also the case for most assessments
of rehabilitation success in mine sites [16, 45, 46, 85]; literature relating to monitoring in mine site
restoration is difficult to access [16], and there is no agreement or standardization of which indica-
tors should be used to monitor development. Research has tended to focus on above-ground attrib-
ute assessment, typically plant communities and vegetation structures [72, 86, 87]. However, much
of this research lacks elucidation of the above/below-ground relationship in ecosystems [86]; eval-
uating the long-term success and self-sustainability of rehabilitation programs in mine sites has
also been neglected [41], and more studies are required across varying climatic regions [88]. Even
when methods and criteria to evaluate and assess restoration are available in open-pit mines such
as quarry rehabilitation, they are, in general, very specialized and time-consuming. A new perspec-
tive to assess mine site restoration success should move toward a simplified methodology that
enables the non-scientific public to evaluate restored areas [5]. Long-term rehabilitation programs
and assessments in metal mine tailing should develop a simplified methodology that could be
applied in mine sites across biomes.
It is worth mentioning the important role of assessing ecosystem complexity. When evaluated
separately from each other, individual attributes of the ecosystem, such as soil quality and vegeta-
tion performance, can be misleading for evaluating the sustainability of a rehabilitation strat-
egy  [25] because everything is part of the complex assemblage that contributes to ecosystem
functioning and resilience. Even landform reconstruction of mine sites [89] shows that spoil heaps
from brown coal mining mechanical terrain reshaping following overburden deposition affect the
nutrient distribution in soils, influencing plant community composition and the presence of soil
fauna and accelerating migration to sites. The concave-slope base sector, mimicking the landforms
of the surrounding undisturbed landscape, promotes soil formation and the establishment of self-
sustaining, functional ecosystems in restored quarries, contributing to habitat diversity and spon-
taneous arrival of vegetation [90].
Specific problems at mining sites include the lack of common biological indicators of ecosystem
restoration success across biomes and mineral spoil types; in addition, the soil fauna response has
been globally underestimated and disregarded [16]. An exception is efforts to assess macrofauna
(Lumbricidae, Collembola, Diplopoda, and Chilopoda) responses in Lignite post-mining sites in
Germany [91–93]. A considerable amount of literature has been published on Hymenoptera, espe-
cially Formicidae, as bioindicators [52, 75, 94, 95]. Ants have been widely used as indicators of
restoration processes in post-mining coal sites [53] and bauxite mining sites [96, 97]. There have
been few extensive studies of the role of ants in rehabilitated mine tailings, except Ribas et al. [75],
who showed that ant species can be used to evaluate the stage of the rehabilitation process in gold
tailings and that some species are indicative of later stages of succession. In Ireland, the findings
of Courtney et al. [45] indicate that bauxite residues can be successfully restored to a functioning
grassland-type ecosystem and that monitoring key arthropod species is recommended as part of
the restoration evaluation process.
4.6  ­Increasing Restoration Success by Enhancing Soil Biodiversity and Soil Multifunctionalit 73

When considering the vegetation structure and diversity monitoring approach, soil fauna are
viewed as passengers during restoration, responding passively to vegetation; it is assumed that
vegetation attributes reflect habitat adequacy for fauna and that animals will be capable of dispers-
ing to the restored habitat and establishing populations [58]. A substantial body of literature shows
that fauna can also drive the developmental trajectories in post-mining site restoration [59, 96–102].
Studies such as those of Frouz et  al.  [103] revealed that in addition to plant establishment,
successful colonization of post-mining sites by soil fauna is critical for soil development as a sub-
stantial part of newly formed soils consist of soil macrofauna feces.
Prach et al. [76] proposed that there are many options of indicators for mine rehabilitation, but
making them more uniform would allow comparisons among projects, assisting the mining indus-
try in assessing rehabilitation performance. There is more agreement about assessing soil physico-
chemical characteristics, and these remain the primary indicator of rehabilitation success, as in
bauxite residues [25, 104].
Gatica-Saavedra et al. [105] found that the three most commonly used ecosystem function indi-
cators were related to soils: chemical composition, physical characteristics, and assemblage of
bioindicators (soil organisms that are indicators of ecosystem processes). Vasconcellos et al. [106]
suggested that organic matter quality and physical soil attributes, in addition to management prac-
tices, can accelerate the forest recovery process during restoration. Given the functional impor-
tance of soil biodiversity and the role of soils in human wellbeing, soil biodiversity should be
considered further in policy agendas and conservation actions by adapting management practices
to sustain soil biodiversity [107]. The same general principle also applies to mine site restoration,
where soil biodiversity should be considered when designing restoration strategies and monitoring
and assessing mine site rehabilitation. To gain deeper insight into post-mining ecosystem evolu-
tion, the long-term study of soil and vegetation development and soil fauna assemblage in post-
mining land rehabilitation in mine tailing from different ages is crucial. To increase the knowledge
of soil multifunctionality and soil ecosystem services in these novel ecosystems, it is necessary to
look into the role of soil fauna.

4.6  ­Increasing Restoration Success by Enhancing Soil


Biodiversity and Soil Multifunctionality

Given that it is much easier to revive soil than it is to create it, salvaging and replacing topsoil is the
simplest and most effective means of restoring functional soil following disturbance. Practices that
ensure landform stability and enhance soil water-holding capacity, aeration, and accumulation of
organic matter and nutrients also make soils more conducive for soil microbial and faunal com-
munities [122]. Rehabilitation to restore degraded lands benefits both soil biodiversity and ecosys-
tem functioning  [107]. A growing body of literature suggests strongly that a functioning
below-ground ecosystem including diverse microbial and soil faunal communities is critical for
rehabilitation strategies to become sustainable [25, 85, 94, 99, 115, 123]. From all present knowl-
edge of mine-site restoration, it is clear that the success of amelioration depends on the waste
substratum characteristics [92]. However, modification of rehabilitation technologies in a way that
would support site colonization by saprophagous soil macrofauna might enhance soil mixing and
carbon storage in mineral sites [70].
Soil processes are controlled by a complex community of soil organisms and their environment,
such as the linkages between C and N mineralization, soil stability and structure, and activity of
soil fauna, microorganisms, and plant roots [124]. However, Scheu and Setälä [125] showed that
macrofauna and mesofauna play a stronger role in energy flow through predation, grazing, and
74 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

substrate processing than microbiota, despite their low metabolic contribution to soil pro-
cesses [126]. Findings from Briones (2014) support that meso- and macrofauna activity as biotur-
bators exert control over other organisms, creating favorable environments for colonization.
Soil microarthropods have been used as soil quality indicators since they play a vital role in
maintaining soil functions [78, 127–129]. Working in the context of mine site restoration, Majer
et al. [96] concluded that Hemiptera, Coleoptera, Araneae, and Hemiptera reflected biophysical
changes in the environment.
In Europe, previous studies on recovery, colonization, and succession of micro-, meso- and mac-
rofauna, have focused on coal and lignite sites, examples of which can be found in Table  4.1.
However, understanding soil fauna contributions to soil multifunctionality is still limited by many
factors: difficulties in taxonomic identification and the lack of taxonomic specialists, as molecular
information alone is insufficient for many ecological studies [81, 130].
One clear finding of research to date is that recovery cannot be adequately discerned by simple
measurement of total abundance or species richness within a higher taxon because richness often
recovers much faster than composition. To measure both the overall development of species com-
position in revegetated sites and their similarity to reference sites, a greater number of multitaxon
studies would be desirable, or grouping species into functional response guilds [58]. Regarding the
first option, this is not always feasible for logistic reasons in restoration assessment since there are
time and financial limitations [15]. Looking at functional response guilds based on their typical
habitat requirements or other ecological attributes and then how successful they seem to be is an
encouraging prospect to assess restoration in mine sites. Speaking about terrestrial ecosystems in
general, Brussaard et al. [131] highlighted that decomposition and production processes cannot be
understood and/or manipulated without explicitly addressing the composition and activity of the
soil food web. Similarly, it has been acknowledged that in terrestrial ecology, there is a need for a
more complete assessment of the role of the entire soil biological community and its interaction
with the above-ground components and mineral-organic matrix [132, 133]. These two fundamen-
tal insights also need to be applied to the restoration and rehabilitation of mine sites.

4.7  ­Using Keystone Species and Ecosystem Engineers in Restoration

Generally speaking, above-ground fauna can be passengers or drivers in revegetation; in the latter
case, fauna can play different roles such as dispersing seeds and pollinating  [58]. Considering
below-ground fauna, while the density of some mesofauna is closely related to the presence of
vegetation, there is no clear preference for vegetation type (e.g. grassy or woody vegetation) [120],
whereas earthworms have been linked with driving vegetation regeneration and soil develop-
ment [59, 70, 99]. Therefore, there is potential for developing novel restoration interventions that
manipulate fauna as a technique of initiating or accelerating revegetation [58]. So, identifying key
fauna groups that could potentially be used for field trial inoculation in rehabilitated mine sites
seems promising for the restoration of metal mining sites. This has been proved successful in pre-
vious research studies for post-mining coal mine sites  [116, 134–136], amended bauxite resi-
dues [85], and several landfills [83].
Herein, we follow the definition of Jones et al. [137] for ecosystem engineers, i.e. organisms that
directly or indirectly modulate the availability of resources to other species by causing physical
state changes in biotic or abiotic materials. Ecosystem engineers of any kind have the potential to
enhance ecosystem functions in soil, probably more than in any other ecological medium [138].
The concept of keystone species was introduced by Paine [139] and refers to species that have a
Table 4.1  Target invertebrate taxa studied as indicators (biological soil quality indicator) in mining restoration in Europe during the past 20 years.

Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Ireland Coleoptera: Relative abundance of Non-ferrous Not assessed Soil metal Stable soil moisture conditions Good [40]
Staphylinidae Coleoptera; metalliferous concentrations appear to be important for the
soil metal concentrations and Zn/Pb recolonization of metalliferous soils
by Staphylinidae.
Ireland Isopoda Monitor and evaluate Bauxite Not assessed pH, EC, C : N, Many species identified indicate Courtney
Chilopoda restoration success by residue concentrations later stages of succession. Bauxite et al. [45]
Diplopoda analyzing the (P, K, Na, Ca, residues can be successfully restored
colonization and Mg) to a functioning grassland-type
Araneae community development ecosystem.
Opiliones of soil macro-arthropods.
Collembola
Dermaptera
Hemiptera
Coleoptera,
Hymenoptera
Ireland Lumbricidae: Exposure tests to Bauxite Earthworm Soil pH, EC, Capability of the rehabilitated Courtney
A. chlorotica understand the potential residue survival and salinity, and residue to support earthworm et al. [85]
for rehabilitated residues population sodicity populations indicates the
to support earthworm viability development of a functioning soil
communities system in rehabilitated residues.
Ireland Lumbricidae: To investigate the ability Bauxite Growth and Soil pH, EC, Amendment improves the residue’s Finngean
E. fetida of keystone meso/ residue reproduction ESP, available physicochemical properties, and et al. [104]
Collembola: F. macrofauna to colonize tests for cations (Na, data revealed that both gypsum and
candida and establish populations Collembola Ca, K, and Mg) organic addition are required to
promote conditions favorable to
plant growth and mesofauna
establishment. Bauxite residue can
be transformed into a soil-like
medium capable of supporting
keystone species
(Continued)
Table 4.1  (Continued)

Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Ireland Lumbricidae: To investigate the effects Bauxite Earthworm Soil pH, EC, Earthworms exposed to soil Di Carlo
E. fetida of bauxite residue residue survival and salinity, and containing 10% residue took up and et al. [108]
properties on earthworm population sodicity accumulated elevated concentrations
survival and viability for viability of Al, As, Cr, and V in comparison to
future inoculation to the control earthworms.
accelerate rehabilitation
Germany Lumbricidae: Spontaneous Lignite Microbial NH4, NO3, PO4, In troughs, soil fauna directly Topp et al. [109]
D. octaedra colonization of soil fauna mining activity and N, organic enhanced microbial activity and
D. rubidus and implications for available litter layer indirectly increased the availability
microbial activity and macronutrients of macronutrients and improved soil
L. castaneus soil quality quality by increasing pH values,
L. rubellus increasing the ammonium–nitrogen
L. terrestris content, and decreasing the content
A. chlorotica of aluminum ions. A multiple-
A. caliginosa species system can improve soil
quality more effectively than a
Diplopoda single-species system.
Isopoda
Germany Lumbricidae: Species abundance; Lignite Decomposition SOM Soil faunal development allows Dunger and
D. dendrodrilus earthworm biomass mining and potential assessment of biological soil quality Voigtlander [92]
L. rubellus decomposition based on species composition,
level of biomass, metabolic activity of soil
Collembola saprophagous, animal groups, and the kind of
Actinedida respiration, competition for food supply (e.g.
Oribatida primary litter decomposition) between
Chilopoda production saprophagous groups.
Diplopoda
Gamasida
Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Germany Lumbricidae Species abundance, Lignite Decomposition SOM During succession of the mine site Dunger
Aranea earthworm biomass, mining and potential community, an interesting et al. [93]
Opilion microarthropod density, decomposition interrelationship between parts of
nematodes, and amoebae level of the soil fauna can be demonstrated,
Collembola density saprophagous, especially between lumbricids and
Diplopoda respiration, microarthropods (activity level of
Chilopoda primary saprophagous fauna).
Amoebae production
Nematoda
Oribatidae
Formicidae
Carabidae
Staphylinidae
UK Lumbricidae: To measure the effects on Coal mining Biomass-C, basal SOM The results emphasize the important Scullion and
L. terrestris soil organic matter and respiration, influence of earthworm activity on Malik [110]
A. longa associated soil dehydrogenase aggregate and organic matter
aggregation after nine activity, stabilization.
A. caliginosa years of earthworm metabolic
L. rubellus inoculation quotient,
A. chlorotica Cmic-to-Corg
ratio,
mineralization
constant
UK Lumbricidae: Compare soil properties Coal mining Productivity and WSA, SOM, Results suggest that earthworms, Marashi and
L. terrestris in inoculated areas with root content soil aggregates rather than plant roots, initiate Scullion [111]
A. longa those of controls to aggregation in severely degraded
evaluate the contribution grassland soils.
A. caliginosa of casts to bulk soil
L. rubellus aggregation, and SOM
A. chlorotica and root content
responses to earthworm
activity
(Continued)
Table 4.1  (Continued)

Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Czech Lumbricidae: Density and community Coal mining Decomposition Soil pH, Slower development of soil biota in Frouz
Republic D. octaedra composition of a wide rate thickness of initial stages of succession is caused et al. [112]
Germany L. rubellus spectrum of soil litter, by unfavorable physical and
organisms, direct counts fermentation, chemical conditions of heap
A. caliginosa of bacteria, rate of and humus substrates and by lower input and
A. rosea and cellulose decomposition, layers poor quality of litter in pine
O. lacteum and microstructure of plantations.
Enchytraeidae upper soil layers
Testacea
Collembola
Oribatida
Isopoda
Diplopoda
dipteran larvae
Czech Macrofauna The effect of macrofauna Coal mining Litter Accumulation The accumulation of C in the Frouz [113]
Republic on the removal of litter decomposition of C in the mineral layer resulted in the
from the soil surface and mineral layer long-term enhancement of microbial
accumulation of organic biomass and respiration. Macrofauna
matter in the mineral soil enhance C removal from the litter
layer layer through an effect on litter
fragmentation and its accumulation
on the mineral layer, but it does not
affect litter mineralization.
Czech Enchytraeus Toxicity test of E. Coal mining Survival and Soil pH, EC, Spoil with a pH below 3 did not Frouz
Republic crypticus crypticus to evaluate the population Na, Ca, K, Al, support the survival of E. crypticus. et al. [114]
Germany toxicity of brown coal growth Fe, loss of However, some alkaline spoils with
mining areas ignition, and high conductivity and ion
polyphenol concentration were also toxic.
contents
Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Czech Hymenoptera Abundance, species Coal mining Not assessed Fermentation A critical group of factors for ant Holec and
Republic richness, and diversity layer, humus community composition (plot age, Frouz [95]
index of ant communities layer depth depth of humus and fermentation
layers, cover of bare soil, and soil
substrate) corresponded to the
successional age of the plot and the
development of the soil.
Czech Hymenoptera: Describing the spatial Coal mining Not assessed Not assessed The results indicated that nesting and Holec
Republic Lasius patterns of nest foraging may differ in their et al. [100]
Formica distribution and epigeic microclimatic requirements, and the
activity of ants in relation formation of vegetation mosaics may be
Myrmica to the vegetation mosaic important to changes in the ant
and species abundance population during succession. Ant nest
significantly enriched soil by available P.
Czech Lumbricidae The effect of litter type Coal mining Microbial C : N ratio In reclaimed sites where macrofauna Frouz [70]
Republic Enchytraeidae and macrofauna respiration, was dominated by the sarcophagus,
Collembola community on litter decomposition mainly earthworms, the macrofauna
decomposition and rate increased soil mixing. In sites where
organic matter predators dominated, the
accumulation macrofauna exclusion probably
suppressed fragmentation and
mixing activity of the mesofauna.
Czech Lumbricidae: The effect of litter quality Coal mining Microbial SOM, C, and N Removal of litter from the litter layer Frouz
Republic D. octaedra and soil faunal respiration, litter concentrations and accumulation of C and N in the et al. [115]
D. rubidus composition on organic removal in the mineral mineral layer increased microbial Frouz et al. [99]
matter dynamics and litter layers respiration and biomass measured as
L. rubellus total PLFA.
Diplopoda
Microorganism
Collembola
dipteran larvae
Czech Lumbricidae: To study soil macrofauna Coal mining Soil fauna Formation of Besides plant establishment, Frouz
Republic D. octaedra density, species density and humus layer successful colonization of post- et al. [103]
D. rubidus composition, and the activity mining sites by soil fauna seems to be
distribution of critical for soil development as the
L. rubellus macrofauna feces in substantial part of newly formed soils
topsoil consisted of soil macrofauna feces.
(Continued)
Table 4.1  (Continued)

Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Czech Lumbricidae Guilds of soil fauna Coal mining Litter reserve on Soil pH, total Microstructure analysis indicated Frouz et al. [39]
Republic Enchytraeidae density in non-reclaimed the soil surface, C, and N, that earthworm activity, namely the
Testacea sites and implications for annual litter contents of mixing of organic and mineral
Oribatida soil development input herb available Ca, K, layers, played a principal role in
biomass and root and Na, WSP humus layer formation.
Collembola biomass, soil Macrosaprophagous guilds of soil
Tardigrades microstructure fauna, most important for litter
Nematodes decomposition and soil mixing,
attained their highest density in the
oldest sites.
Czech Lumbricidae: To investigate if the Coal mining Vegetation Soil pH; total Massive changes in plant Roubickova
Republic L. rubellus introduction of biomass N, Ca, and C; community composition occur et al. [116]
A. caliginosa earthworms into a exchangeable around 23 years of succession when
post-mining soil P, K the heaps are colonized by the
enhances the growth of earthworms.
late-succession plant
species
Czech Enchytraeidae To explore processes Coal mining Vegetation Soil pH; EC; The abundance of soil fauna was Frouz
Republic Formicidae responsible for biomass total C; total significantly related to microhabitat. et al. [117]
Chilopoda environmental available P, K, Maintaining the spatial
heterogeneity and Ca; heterogeneity created by the heaping
water-soluble P may enhance the spontaneous
re-vegetation of post-mining sites.
Czech Gastropoda To study the effects of Coal mining Not assessed Soil pH; C; The species richness of various Hendrychova
Republic Myriapoda pedological properties on total N; groups was affected by different soil et al. [118]
Diplopoda species richness exchangeable properties either independently of
inhabiting soil to shrub P, K, and Ca other variables or in interaction with
Isopoda content microclimatic conditions or
Heteroptera management history.
Coleoptera
Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Czech Microflora To study the parameters Coal mining Estimation of Soil pH, herb Biomass of the soil microflora Frouz et al. [71]
Republic Fungi characterizing the feeding rates in mass, fine root, (bacteria and fungi) is the best
Bacteria structure of the the soil food web litter input predictor of the thickness of the
decomposer food web, fermentation layer, which
Micro-meso- biomass of soil corresponds with changes in topsoil
macrofauna microflora microstructure driven by a
combination of plant organic matter
input and engineering effects of
earthworms.
Czech Lumbricidae: Test the effect of Coal mining Soil microbial Soil pH, C, Earthworms help drive succession of Mudrak
Republic L. rubellus earthworms on plants respiration, total N, and both plant and Collembola et al. [119]
A. caliginosa and Collembola microbial exchangeable P communities on post-mining sites.
Collembola biomass and K

Czech Lumbricidae To study the effects of Coal mining Microbial C : N ratio The results indicate that the effect of Frouz et al. [60]
Republic tree species on the respiration, tree species on soil development is
chemical, micro- microbial substantially mediated by soil fauna
morphological, and biomass activity and especially by earthworm
biological properties of bioturbation bioturbation.
soil and the role of soil activity
fauna
Czech Enchytraeidae To study variations in soil Coal mining Microbial Soil pH, total Patch type was the only plant-related Moradi
Republic Lumbricidae chemical properties, biomass, PLFA N, C, EC, and factor capable of explaining the et al. [120]
Lepidoptera microbial biomass, and analysis exchangeable P mesofauna community variations.
Araneae faunal populations as and K Epigeic macrofauna was found to
related to plant correlate more strongly with plant
Coleoptera functional traits, patch functional traits than endogeic
Aphids types, and successional macrofauna. The abundance of most
Hymenoptera stage fauna correlated positively with an
Thysanoptera increase in plant cover and litter
Orthoptera input and was significantly higher in
Dermaptera vegetated patches and old sites.
Chilopoda
Diplopoda

(Continued)
Table 4.1  (Continued)

Order/ Soil
Country Family/Species Target Mineral type Ecological process physicochemical Findings References

Czech Lepidoptera To study the effects of Coal mining Not assessed Not assessed Surface dozing should be applied Moradi
Republic Araneae micro-topographic only where the technical approaches et al. [121]
Coleoptera heterogeneity on are expedient. Micro-topographic
Hymenoptera biodiversity and heterogeneity is responsible for the
Orthoptera conservation potential of small-scale heterogeneity of various
Dermaptera arthropod communities environmental conditions that
support high biodiversity of groups
Chilopoda with various needs.
Diplopoda
Oniscidea
Czech Orabitidae Study the effect(s) of soil Coal mining Microbial C content, C : N Soil development of the spoil Moradi
Republic Lumbricidae transplantation on biomass, ratio, overburden might be even more et al. [38]
Diplopoda survival and colonization microbial pH and EC critical than the migration barrier.
respiration
Diptera
Coleoptera
Spain Coleoptera Analyze the potential use Coal mining Not assessed Not assessed Coleoptera may be useful as a Tizado and
of terrestrial arthropods cost-effective indicator for assessing Núñez-
as indicators of short-term environmental changes. Pérez [80]
successional restoration
stages
SOM, Soil organic matter; EC, electrical conductivity; ESP, exchangeable sodium percentage; WSA, water-stable aggregation; PLFA, fatty acid profiles of the phospholipids; WSP, water-
soluble phosphorus.
4.7  ­Using Keystone Species and Ecosystem Engineers in Restoratio 83

disproportionately large effect on ecosystem functioning in their environment relative to their bio-
mass. This concept partly overlaps with ecosystem engineers – an ecosystem engineer can be a
keystone species and vice versa. Earthworms, termites, and ants are considered the most essential
ecosystem engineers in soil  [67, 140, 141], followed by Collembola and mites  [142, 143]. These
groups also require, in general, less survey effort since they are relatively easy to sample, and there
is extensive literature available that facilitates their (morphological) identification.
Ecosystem engineers may increase restoration success and guide soil. For instance, Filser
et al. [144] reported that earthworms, Collembola, and other larger invertebrates strongly impact
carbon turnover, sometimes even turning C sinks into C sources or vice versa. Tuma et al. [145]
emphasized the importance, across all habitats, of termites for generating standing above-ground
soil structures and earthworms for short-term soil turnover. Some studies have effectively used soil
fauna or vegetation as ecosystem engineers by selecting adequate species and investigating the
functioning of the whole system (applying ecosystem-based management) for ecosystem restora-
tion [83, 146, 147]. Selected taxa will be discussed in more detail below. The use of selected soil
invertebrate taxa as bioindicators by mineral spoil and their functional roles in restored soils are
summarized in Figures 4.1 and 4.2, respectively.

4.7.1  Earthworms
Earthworms are one of the most studied groups of ecosystem engineers [148]. They are important
drivers for the formation of soil structures and SOM dynamics [149], and they drive nutrient turno-
ver and the functioning of detrital food webs and terrestrial ecosystems in general [81, 144, 150, 151].

Lignite Coal
Coal DE CZ
GB

Lignite
Coal DE
CZ Bauxite Bauxite
IE IE, AU

Bauxite Coal Taxa


AU CZ Bioindicators
Bauxite
AU

Bauxite
Lignite AU
DE
Coal
CZ Lignite
Coal DE
DE

Figure 4.1  Primary soil ecosystem engineers used as bioindicators in different mineral spoil types in mine
site rehabilitation worldwide. AU, Australia; CZ, Czech Republic; DE, Germany; GB, United Kingdom of Great
Britain and Northern Ireland; IE, Ireland (according to ISO 3166 country codes).
84 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

Figure 4.2  Primary ecosystem


engineers used as indicators or
Soil mixing drivers of restoration success and
Soil fertility their roles in modifying soil
Microbial physicochemical conditions in
dynamics post-mining sites. Both graphs
are based on the literature search
conducted for this chapter, which
Litter fragmentation
includes assessments in
Microbial activity rehabilitated coal mines, lignite,
Aggregation and bauxite site retrieved from
Soil fertility Table 4.1 and literature in
SOM Section 4.7.
Carbon
recycling
turnover

Bioturbation Soil mixing Decomposition


Decomposition Soil fertility
Nutrient cycling Plant-Fauna
Soil formation
succession
Decomposition

As detritivores, they are partially responsible for the breakdown and recycling of dead organic matter,
while soil passing through earthworms’ guts increases soil quality [83]. Marashi and Scullion [111]
found that earthworms, rather than plant roots, initiate aggregation in severely degraded grasslands.
In post-mining coal sites, Frouz et al. [60] observed that the effect of tree species on soil develop-
ment is substantially mediated by soil fauna activity and especially by earthworm bioturbation.
Roubickova et  al.  [116] showed that dramatic changes in plant community composition occurred
around year 23 of succession when the heaps were colonized by earthworms in post-mining coal sites.
The findings from Scullion and Malik [110] highlight the important influence of earthworm activity
on aggregate and organic matter stabilization in post-mining coal. Results from Mudrak et al. [119]
indicate that earthworms can promote other species and, therefore, the restoration of post-mining
sites, driving the succession of both Collembola and plants. In surfaces affected by coal mining, earth-
worm inoculation and subsequent activity and cast formation improved soil structure [111].
In metal mining tailings, the role of earthworms in soil development has been poorly investi-
gated. However, approaches of this kind are promising and have various implications for practice:
evaluation of soil inoculation necessity, an appropriate choice of species, timing, and inoculation
method; coordination with labor; and monitoring of the earthworms (species, numbers, and dis-
persal), preferably linked with measurements of developing soil properties [83, 146].

4.7.2 Ants
Ants play many important roles in directly and indirectly controlling resource availability for other
organisms. They are considered keystone species in many ecosystems, acting as important preda-
tors of insects and other invertebrates [152]. As Majer et al. [96] reported, Hemiptera are influenced
by both vegetation and soil factors, which makes them good bioindicators of environmental condi-
tions and biophysical changes. Ants have proved to be cost-effective to survey and potentially high
in information for restored bauxite mines [97]. Ant density has been found to increase due to higher
resource availability in restored lands [153]. Frouz et al. [154] confirmed that ants can also initiate
4.8  ­Conclusions and Further Perspective for the Restoration of Metalliferous Tailing 85

soil modification; ant nests induce chemical changes, as mixing due to excavation of deeper soil
layers, enrichment of substrate, and interactions of nests chemistry with other physical, chemical,
and microbial parameters could guide the restoration outcomes in post-mining sites.

4.7.3  Termites
Termites are among the principal macro-invertebrate decomposers in the tropics. Due to highly
evolved mutualism with microbes, termites play a significant role in decomposition processes and
nutrient recycling as soil ecosystem engineers impacting soil formation and fertility  [155, 156].
Termite-mediated processes are used to improve the soil–water balance  [157]. In rehabilitated
bauxite mines, forest development and the changing availability of food materials enabled coloni-
zation by termite groups. In restored bauxite mines, results showed that adding woody debris to
restored areas might accelerate the return of termites and the associated ecosystem processes,
decomposition, and nutrient recycling [96].

4.7.4  Collembola and Mites


Microarthropods, including mites (order Acari) and Collembolan (springtails, order Hexapoda),
are the most abundant and diverse soil mesofauna. They play an essential role in processing
organic matter via chemical, physical, and biological mechanisms, so they are considered neces-
sary in shaping ecosystems [158].
Collembola are involved in nutrient cycling, especially in litter decomposition, by controlling
microbial diversity and decomposition [159, 160] and play a role in the translocation of litter car-
bon to soil (Chamberlain et al. [161]). Meyer-Wolfarth et al. [162] demonstrated their potential as
biological regulators of plant pathogens. Moreover, Collembola community composition, which is
very sensitive to disturbances, was found to be a good environmental indicator in Anthrosols [78].
In coal waste deposits, Dunger and Voigtlaender  [91] found that Collembola succession was
dependent on rehabilitation age. In bauxite mines, collembolan populations mediate, or are at
least associated with, ecosystem decomposition and nutrient cycling [96].
Mites contribute to the formation of soil structure and increase the activity and distribution of
microorganisms, thereby enhancing decomposition processes [159]. Mites have essential impacts
on community dynamics, ecosystem processes, and biodiversity within many insect-fungus sys-
tems [163]. In restored bauxite mines, Majer et al. [96] found a strong positive correlation between
mite species richness and age of restoration.
Although some studies have evaluated the role of collembolans and mites as indicators of the
successional stage, few studies have focused on how they modify soil physicochemical conditions
and their effects on ecosystem function from rehabilitated metal mine sites.

4.8  ­Conclusions and Further Perspective for the Restoration


of Metalliferous Tailings

We agree with Cross et  al. (2019), who asserted that restoration assessment should move from
traditional evaluation toward a re-evaluation of regulatory standards and include soil fauna moni-
toring in mine restoration projects and its role in soil ecosystem services. Investing in soil fauna
assessments and the long-term evolution of rehabilitated mine sites will assist industry, promote
further investment in restoration science, and accelerate recovery of soil functions.
86 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

More research is needed to investigate the importance of metalliferous tailing properties on soil
fauna for future inoculation to accelerate rehabilitation. Mine restoration projects should imple-
ment common biological indicators to facilitate comparisons among projects [16] and simplified
methodologies to monitor ecosystem restoration  [5]. It may be reasonable to look at functional
response guilds or the soil food web rather than species diversity to avoid difficulties in taxonomic
identification. Identifying functional response guilds based on their typical habitat requirements
or other ecological attributes and then looking at how successful they are appears to be an encour-
aging prospect for metal mine rehabilitation.
In this chapter, we presented evidence supporting the idea that assessments and monitoring of
restoration success must target specific taxa, mainly those considered as ecosystem engineers and
their effects on ecosystem function, rather than focus on ease of survey effort or the use of single
taxa as biological indicators. Furthermore, identifying key fauna groups that could potentially be
used for field inoculations in rehabilitated mine sites offers a promising opportunity for enhancing
ecosystem restoration in metal mining sites. Even though inoculation with earthworms has been
proven successful in some sites, it is necessary to conduct more long-term field trials to test reha-
bilitation techniques, preferably linked with measurements of developing soil properties across
climatic regions, ecosystems, and mineral spoil types.

Acknowledgements

This work was supported by Science Foundation Ireland (SFI 17/CDA/4778).

­References

Dominati, E., Patterson, M., and Mackay, A. (2010). A framework for classifying and quantifying
1
the natural capital and ecosystem services of soils. Ecological Economics 69: 1858–1868.
2 Montanarella, L., Pennock, D.J., Mckenzie, N. et al. (2016). World’s soils are under threat. Soil 2: 79–82.
3 Rodríguez, N., Mclaughlin, M., and Pennock, D. (2018). Soil Pollution: A Hidden Reality. Rome:
Food and Agriculture Organization of the United Nations.
4 EUMICON & Franz Friesenbichler, A. H., Roman Stiftner, Sonja Bredl (2018). 25 Ideas For a
Future Made in Europe. European Mineral Resources Confederation.
5 Carabassa, V., Ortiz, O., and Alcaniz, J.M. (2019). Restoquarry: indicators for self-evaluation of
ecological restoration in open-pit mines. Ecological Indicators 102: 437–445.
6 Seleiman, M.F. and Kheir, A.M. (2018). Maize productivity, heavy metals uptake and their
availability in contaminated clay and sandy alkaline soils as affected by inorganic and organic
amendments. Chemosphere 204: 514–522.
7 Antoniadis, V., Golia, E.E., Shaheen, S.M., and Rinklebe, J. (2017). Bioavailability and health risk
assessment of potentially toxic elements in Thriasio Plain, near Athens, Greece. Environmental
Geochemistry and Health 39: 319–330.
8 Bradshaw, A. (1997). Restoration of mined lands – using natural processes. Ecological Engineering
8: 255–269.
9 Corlett, R.T. (2016). Restoration, reintroduction, and rewilding in a changing world. Trends in
Ecology & Evolution 31: 453–462.
10 Higgs, E., Falk, D.A., Guerrini, A. et al. (2014). The changing role of history in restoration ecology.
Frontiers in Ecology and the Environment 12: 499–506.
 ­Reference 87

1 Moreno-Mateos, D., Barbier, E.B., Jones, P.C. et al. (2017). Anthropogenic ecosystem disturbance
1
and the recovery debt. Nature Communications 8: 14163.
12 Anderson, R.M., Buitenwerf, R., Driessen, C. et al. (2019). Introducing rewilding to restoration to
expand the conservation effort: a response to Hayward et al. Biodiversity and Conservation 28:
3691–3693.
13 Gann, G.D., Mcdonald, T., Walder, B. et al. (2019). International principles and standards for the
practice of ecological restoration. Second edition. Restoration Ecology 27: S1–S46.
14 McDonald, T., Jonson, J., and Dixon, K.W. (2016). National standards for the practice of ecological
restoration in Australia. Restoration Ecology 24: S6–S32.
15 Cross, A.T., Young, R., Nevill, P. et al. (2018). Appropriate aspirations for effective post-mining
restoration and rehabilitation: a response to Kaźmierczak et al. Environmental Earth Sciences
77: 256.
16 Cross, S.L., Tomlinson, S., Craig, M.D. et al. (2019). Overlooked and undervalued: the neglected
role of fauna and a global bias in ecological restoration assessments. Pacific Conservation Biology
25: 331–341.
17 Kaźmierczak, U., Lorenc, M.W., and Strzałkowski, P. (2017). The analysis of the existing
terminology related to a post-mining land use: a proposal for new classification. Environmental
Earth Sciences 76: 693.
18 Jones, H. and Boger, D.V. (2012). Sustainability and waste management in the resource industries.
Indonesia 51: 10057–10065.
19 Tayebi-Khorami, M., Edraki, M., Corder, G., and Golev, A. (2019). Re-thinking mining waste
through an integrative approach led by circular economy aspirations. Minerals 9: 286.
20 Courtney, R. (2013). Mine tailings composition in a historic site: implications for ecological
restoration. Environmental Geochemistry and Health 35: 79–88.
21 Courtney, R. (2018). Irish mine site rehabilitation – a case study. In: Bio-Geotechnologies for Mine
Site Rehabilitation (eds. M.N.V. Prasad, P.J. De Campos Favas and S.K. Maiti), 439–456.
Amsterdam: Elsevier.
22 Council Directive (EC) 2006 2006/21/EC of the European Parliament and of the Council of
15 March 2006 on the management of waste from extractive industries and amending Directive
2004/35/EC. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:02006L0021-20090807
[accessed 20 May 2020].
23 Desai, M., Haigh, M., and Walkington, H. (2019). Phytoremediation: metal decontamination of
soils after the sequential forestation of former opencast coal land. Science of the Total Environment
656: 670–680.
24 Xie, L. and Van Zyl, D. (2020). Distinguishing reclamation, revegetation and phytoremediation,
and the importance of geochemical processes in the reclamation of sulfidic mine tailings: a review.
Chemosphere 252: 126446.
25 Di Carlo, E., Chen, C.R., Haynes, R.J. et al. (2019). Soil quality and vegetation performance
indicators for sustainable rehabilitation of bauxite residue disposal areas: a review. Soil Research
57: 419–446.
26 Haigh, M. (2018). Building a cradle for nature: a paradigm for environmental reconstruction. In:
Bio-Geotechnologies for Mine Site Rehabilitation (eds. M.N.V. Prasad, P.J.D.C. Favas and
S.K. Maiti), 593–615. Amsterdam: Elsevier.
27 Makineci, E., Gungor, B., and Kumbasli, M. (2011). Natural plant revegetation on reclaimed coal
mine landscapes in Agacli-Istanbul. African Journal of Biotechnology 10: 16. https://doi.
org/10.5897/AJB10.2499.
88 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

8 Tordoff, G.M., Baker, A.J.M., and Willis, A.J. (2000). Current approaches to the revegetation and
2
reclamation of metalliferous mine wastes. Chemosphere 41: 219–228.
29 Tripathi, P., Dwivedi, S., Mishra, A. et al. (2012). Arsenic accumulation in native plants of West
Bengal, India: prospects for phytoremediation but concerns with the use of medicinal plants.
Environmental Monitoring and Assessment 184: 2617–2631.
30 Macdonald, E. and King, E.G. (2018). Novel ecosystems: a bridging concept for the consilience of
cultural landscape conservation and ecological restoration. Landscape and Urban Planning 177:
148–159.
31 Macdonald, S.E., Landhausser, S.M., Skousen, J. et al. (2015). Forest restoration following surface
mining disturbance: challenges and solutions. New Forests 46: 703–732.
32 Belnap, J.Y.E., Ludwig, J.A., Wilcox, B.P. et al. (2012). Introduced and invasive species in novel
rangeland ecosystems: friends or foes? Rangeland Ecology & Management 65: 569–578.
33 Collier, M.J. and Devitt, C. (2016). Novel ecosystems: challenges and opportunities for the
Anthropocene. The Anthropocene Review 3: 231–242.
34 Murcia, C., Aronson, J., Kattan, G.H. et al. (2014). A critique of the ‘novel ecosystem’ concept.
Trends in Ecology & Evolution 29: 548–553.
35 Curry, J.P. and Boyle, K.E. (1995). Restoring soil fauna in reclaimed land, with particular reference
to earthworms in cutover peat. Acta Zoologica Fennica 196: 371–375.
36 Curry, J. and Good, J. (1992). Soil faunal degradation and restoration. In: Soil Restoration (eds.
R. Lal and B.A. Stewart), 171–215. New York: Springer.
37 Brady, V.J., Cardinale, B.J., Gathman, J.P., and Burton, T.M. (2002). Does facilitation of faunal
recruitment benefit ecosystem restoration? An experimental study of invertebrate assemblages in
wetland mesocosms. Restoration Ecology 10: 617–626.
38 Moradi, J., Vicentini, F., Simackova, H. et al. (2018). An investigation into the long-term effect of
soil transplant in bare spoil heaps on survival and migration of soil meso and macrofauna.
Ecological Engineering 110: 158–164.
39 Frouz, J., Prach, K., Pizl, V. et al. (2008). Interactions between soil development, vegetation and soil
fauna during spontaneous succession in post mining sites. European Journal of Soil Biology 44:
109–121.
40 Good, J.A. (1999). Recolonisation by Staphylinidae (Coleoptera) of old metalliferous tailings and
mine soils in Ireland. Biology and Environment: Proceedings of the Royal Irish Academy 99B: 27–35.
41 Di Carlo, E., Boullemant, A., and Courtney, R. (2019). A field assessment of bauxite residue
rehabilitation strategies. Science of the Total Environment 663: 915–926.
42 Carabassa, V., Domene, X., and Alcañiz, J.M. (2020). Soil restoration using compost-like-outputs
and digestates from non-source-separated urban waste as organic amendments: limitations and
opportunities. Journal of Environmental Management 255: 109909.
43 Leguédois, S., Séré, G., Auclerc, A. et al. (2016). Modelling pedogenesis of Technosols. Geoderma
262: 199–212.
44 You, F., Dalal, R., and Huang, L. (2018). Initiation of soil formation in weathered sulfidic Cu-Pb-Zn
tailings under subtropical and semi-arid climatic conditions. Chemosphere 204: 318–326.
45 Courtney, R., O’neill, N., Harrington, T., and Breen, J. (2010). Macro-arthropod succession in
grassland growing on bauxite residue. Ecological Engineering 36: 1666–1671.
46 Shu, W.S., Ye, Z.H., Zhang, Z.Q. et al. (2005). Natural colonization of plants on five lead/zinc mine
tailings in Southern China. Restoration Ecology 13: 49–60.
47 Gardner, J. (2001). Rehabilitating mines to meet land use objectives: bauxite mining in the jarrah
forest of Western Australia. Unasylva (FAO).
48 Suding, K.N. (2011). Toward an era of restoration in ecology: successes, failures, and opportunities
ahead. Annual Review of Ecology, Evolution, and Systematicsl 42: 465–487.
 ­Reference 89

9 Majer, J.D. (1989). Animals in Primary Succession: The Role of Fauna in Reclaimed Lands.
4
Cambridge: Cambridge University Press.
50 Parmenter, R.R. and Macmahon, J.A. (1990). Faunal community development on disturbed lands: an
indicator of reclamation success. In: Evaluating Reclamation Success: The Ecological Consideration
(eds. J.C. Chambers and G.L. Wade), 73–89. USDA, Forest Service, Northeastern Forest Station.
51 Slabova, M., Broumova, H., and Pecharova, E. (2008). Communities of small mammals as
indicators of biodiversity changes in reclaimed areas after coal mining. In: Rapantova, N. &Hrkal,
Z., eds., Mine Water and the Environment, Proceedings of the 10th International Mine Water
Association Congress, pp. 179–182. VSB – Technical University of Ostrava, Ostrava.
52 Andersen, A.N. and Sparling, G.P. (1997). Ants as indicators of restoration success: relationship
with soil microbial biomass in the Australian seasonal tropics. Restoration Ecology 5: 109–114.
53 Andersen, A.N., Hoffmann, B.D., Muller, W.J., and Griffiths, A.D. (2002). Using ants as
bioindicators in land management: simplifying assessment of ant community responses. Journal of
Applied Ecology 39: 8–17.
54 Crouzeilles, R. and Curran, M. (2016). Which landscape size best predicts the influence of forest
cover on restoration success? A global meta-analysis on the scale of effect. Journal of Applied
Ecology 53: 440–448.
55 O’Grady, A., Breen, J., Harrington, T.J., and Courtney, R. (2013). The seed bank in soil from the
nests of grassland ants in a unique limestone grassland community in Ireland. Ecological
Engineering 61: 58–64.
56 Chiarucci, A., Bacaro, G., and Scheiner, S.M. (2011). Old and new challenges in using species
diversity for assessing biodiversity. Philosophical Transactions of the Royal Society B-Biological
Sciences 366: 2426–2437.
57 Hejda, M., Pyšek, P., and Jarošík, V. (2009). Impact of invasive plants on the species richness,
diversity and composition of invaded communities. Journal of Ecology 97: 393–403.
58 Catterall, C.P. (2018). Fauna as passengers and drivers in vegetation restoration: a synthesis of
processes and evidence. Ecological Management & Restoration 19: 54–62.
59 Frouz, J. (2014). Soil Biota and Ecosystem Development in Post Mining Sites. Boca Raton: CRC Press.
60 Frouz, J., Liveckova, M., Albrechtova, J. et al. (2013). Is the effect of trees on soil properties mediated
by soil fauna? A case study from post-mining sites. Forest Ecology and Management 309: 87–95.
61 Wang, Y., Li, Y.-L., Shi, J.-H. et al. (2012). Effect of different vegetation restoration measures on the
species diversity and soil properties of iron tailings. Journal of Soil and Water Conservation 26:
112–117,183.
62 Wong, M.H. (2003). Ecological restoration of mine degraded soils, with emphasis on metal
contaminated soils. Chemosphere 50: 775–780.
63 Costantini, E.A.C., Branquinho, C., Nunes, A. et al. (2016). Soil indicators to assess the
effectiveness of restoration strategies in dryland ecosystems. Solid Earth 7: 397–414.
64 Dalle Laste, K.C., Durigan, G., and Andersen, A.N. (2019). Biodiversity responses to land-use and
restoration in a global biodiversity hotspot: ant communities in Brazilian Cerrado. Austral Ecology
44: 313–326.
65 De Deyn, G.B., Raaijmakers, C.E., and Van der Putten, W.H. (2004). Soil fauna enhances grassland
restoration. Levende Natuur 105: 10–12.
66 De Deyn, G.B., Raaijmakers, C.E., Zoomer, H.R. et al. (2003). Soil invertebrate fauna enhances
grassland succession and diversity. Nature 422: 711–713.
67 Anderson, J.M. (1988). Invertebrate-mediated transport processes in soils. Agriculture, Ecosystems
& Environment 24: 5–19.
68 Orgiazzi, A., Dunbar, M.B., Panagos, P. et al. (2015). Soil biodiversity and DNA barcodes:
opportunities and challenges. Soil Biology and Biochemistry 80: 244–250.
90 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

9 Frouz, J., Thebault, E., Pizl, V. et al. (2013). Soil food web changes during spontaneous succession
6
at post mining sites: a possible ecosystem engineering effect on food web organization? PLos One 8:
e79694. https://doi.org/10.1371/journal.pone.0079694.
70 Frouz, J. (2008). The effect of litter type and macrofauna community on litter decomposition and
organic matter accumulation in post-mining sites. Biologia 63: 249–253.
71 Frouz, J., Pižl, V., Tajovský, K. et al. (2014). Soil macro- and mesofauna succession in post-mining
sites and other disturbed areas. In: Soil Biota and Ecosystem Development in Post Mining Sites (ed.
J. Frouz), 104–131. Boca Raton: CRC Press.
72 Ruiz-Jaen, M.C. and Mitchell Aide, T. (2005). Restoration success: how is it being measured?
Restoration Ecology 13: 569–577.
73 Herrick, J.E., Schuman, G.E., and Rango, A. (2006). Monitoring ecological processes for restoration
projects. Journal for Nature Conservation (Jena) 14: 161–171.
74 Nunes, A., Oliveira, G., Mexia, T. et al. (2016). Ecological restoration across the Mediterranean
Basin as viewed by practitioners. Science of the Total Environment 566: 722–732.
75 Ribas, C.R., Schmidt, F.A., Solar, R.R.C. et al. (2012). Ants as indicators of the success of
rehabilitation efforts in deposits of gold mining tailings. Restoration Ecology 20: 712–720.
76 Prach, K., Durigan, G., Fennessy, S. et al. (2019). A primer on choosing goals and indicators to
evaluate ecological restoration success. Restoration Ecology 27: 917–923.
77 Cohen-Shacham, E., Andrade, A., Dalton, J. et al. (2019). Core principles for successfully
implementing and upscaling nature-based solutions. Environmental Science & Policy 98: 20–29.
78 Magro, S., Gutiérrez-López, M., Casado, M.A. et al. (2013). Soil functionality at the roadside: zooming
in on a microarthropod community in an anthropogenic soil. Ecological Engineering 60: 81–87.
79 Starý, J. (2002). Changes of oribatid mite communities (Acari: Oribatida) during primary
cussession on colliery spoil heaps near Sokolov, North-West Bohemia, Czech Republic. In: Studies
on Soil Fauna in Central Europe (eds. K. Tajovský, V. Balík and V. Pižl), 199–206. Ceské Budejovice:
Institute of Soil Biology, Academy of Sciences of the Czech Republic.
80 Tizado, E.J. and Núñez-Pérez, E. (2016). Terrestrial arthropods in the initial restoration stages of
anthracite coal mine spoil heaps in northwestern Spain: potential usefulness of higher taxa as
restoration indicators. Land Degradation & Development 27: 1131–1140.
81 Briones, M.J.I. (2014). Soil fauna and soil functions: a jigsaw puzzle. Frontiers in Environmental
Science 2: 7. https://doi.org/10.3389/fenvs.2014.00007.
82 Elmqvist, T., Setälä, H., Handel, S.N. et al. (2015). Benefits of restoring ecosystem services in urban
areas. Current Opinion in Environmental Sustainability 14: 101–108.
83 Butt, K.R. (2008). Earthworms in soil restoration: lessons learned from United Kingdom case
studies of land reclamation. Restoration Ecology 16: 637–641.
84 Cortina, J.W.B.G. (2018). SERE and the international standards for the practice of ecological
restoration. SERE (Society for Ecological Restoration Europe).
85 Courtney, R., Di Carlo, E., and Schmidt, O. (2018). Soil properties and earthworm populations
associated with bauxite residue rehabilitation strategies. Environmental Science and Pollution
Research 27 (27): 33401–33409.
86 Hasegawa, M., Fujii, S., Kaneda, S. et al. (2017). Recent progress in ecological studies of soil fauna.
Japanese Journal of Ecology (Otsu) 67: 95–118.
87 Koch, J.M., Grigg, A.H., Gordon, R.K., and Majer, J.D. (2010). Arthropods in coarse woody debris in
jarrah forest and rehabilitated bauxite mines in Western Australia. Annals of Forest Science 67: 106–106.
88 Frouz, J., Jilkova, V., Cajthaml, T. et al. (2013). Soil biota in post-mining sites along a climatic
gradient in the USA: simple communities in shortgrass prairie recover faster than complex
communities in tallgrass prairie and forest. Soil Biology & Biochemistry 67: 212–225.
 ­Reference 91

9 Walmsley Roubíčková, A., Vachová, P., and Vach, M. (2017). Topography of spoil heaps and its
8
role in plant succession and soil fauna presence. Scientia Agriculturae Bohemica 48: 30–38.
90 Martín-Duque, J.F., Sanz, M.A., Bodoque, J.M. et al. (2010). Restoring earth surface processes
through landform design. A 13-year monitoring of a geomorphic reclamation model for quarries
on slopes. Earth Surface Processes and Landforms 35: 531–548.
91 Dunger, W. and Voigtlaender, K. (2009). Soil fauna (Lumbricidae, Collembola, Diplopoda and
Chilopoda) as indicators of soil eco-subsystem development in post-mining sites of eastern
Germany – a review. Soil Organisms 81: 1–51.
92 Dunger, W. and Voigtlander, K. (2005). Assessment of biological soil quality in wooded reclaimed
mine sites. Geoderma 129: 32–44.
93 Dunger, W., Wanner, M., Hauser, H. et al. (2001). Development of soil fauna at mine sites during
46 years after afforestation. Pedobiologia 45: 243–271.
94 Courtney, R., Feeney, E., and O’Grady, A. (2014). An ecological assessment of rehabilitated
bauxite residue. Ecological Engineering 73: 373–379.
95 Holec, M. and Frouz, J. (2005). Ant (Hymenoptera: Formicidae) communities in reclaimed and
unreclaimed brown coal mining spoil dumps in the Czech Republic. Pedobiologia 49: 345–357.
96 Majer, J.D., Brennan, K.E.C., and Moir, M.L. (2007). Invertebrates and the restoration of a forest
ecosystem: 30 years of research following bauxite mining in Western Australia. Restoration
Ecology 15: S104–S115.
97 Orabi, G., Moir, M.L., and Majer, J.D. (2010). Assessing the success of mine restoration using
Hemiptera as indicators. Australian Journal of Zoology 58: 243–249.
98 Frouz, J. (2017). Effects of soil development time and litter quality on soil carbon sequestration:
assessing soil carbon saturation with a field transplant experiment along a post-mining
chronosequence. Land Degradation & Development 28: 664–672.
99 Frouz, J., Elhottova, D., Kuraz, V., and Sourkova, M. (2006). Effects of soil macrofauna on other
soil biota and soil formation in reclaimed and unreclaimed post mining sites: results of a field
microcosm experiment. Applied Soil Ecology 33: 308–320.
100 Holec, M., Frouz, J., and Pokorny, R. (2006). The influence of different vegetation patches on the
spatial distribution of nests and the epigeic activity of ants (Lasius niger) on a spoil dump after
brown coal mining (Czech Republic). European Journal of Soil Biology 42: 158–165.
101 Majer, J.D. (2009). Animals in the restoration process – progressing the trends. Restoration
Ecology 17: 315–319.
102 Moir, M.L., Brennan, K.E.C., Majer, J.D. et al. (2010). Plant species redundancy and the
restoration of faunal habitat: lessons from plant-dwelling bugs. Restoration Ecology 18: 136–147.
103 Frouz, J., Pižl, V., and Tajovský, K. (2007). The effect of earthworms and other saprophagous
macrofauna on soil microstructure in reclaimed and un-reclaimed post-mining sites in Central
Europe. European Journal of Soil Biology 43: S184–S189.
104 Finngean, G., O’Grady, A., and Courtney, R. (2018). Plant assays and avoidance tests with
collembola and earthworms demonstrate rehabilitation success in bauxite residue. Environmental
Science and Pollution Research 25: 2157–2166.
105 Gatica-Saavedra, P., Echeverria, C., and Nelson, C.R. (2017). Ecological indicators for assessing
ecological success of forest restoration: a world review. Restoration Ecology 25: 850–857.
106 Vasconcellos, R.L.F., Segat, J.C., Bonfim, J.A. et al. (2013). Soil macrofauna as an indicator of soil
quality in an undisturbed riparian forest and recovering sites of different ages. European Journal
of Soil Biology 58: 105–112.
107 Cameron, E., Martins, I., Lavelle, P. et al. (2019). Global mismatches in aboveground and
belowground biodiversity. Conservation Biology 33: 1187–1192.
92 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

08 Di Carlo, E., Boullemant, A., Poynton, H., and Courtney, R. (2020). Exposure of earthworm
1
(Eisenia fetida) to bauxite residue: implications for future rehabilitation programmes. Science of
The Total Environment 716: 137126.
109 Topp, W., Simon, M., Kautz, G. et al. (2001). Soil fauna of a reclaimed lignite open-cast mine of the
Rhineland: improvement of soil quality by surface pattern. Ecological Engineering 17: 307–322.
110 Scullion, J. and Malik, A. (2000). Earthworm activity affecting organic matter, aggregation and
microbial activity in soils restored after opencast mining for coal. Soil Biology and Biochemistry
32: 119–126.
111 Marashi, A.R.A. and Scullion, J. (2003). Earthworm casts form stable aggregates in physically
degraded soils. Biology and Fertility of Soils 37: 375–380.
112 Frouz, J., Keplin, B., Pizl, V. et al. (2001). Soil biota and upper soil layer development in two
contrasting post-mining chronosequences. Ecological Engineering 17: 275–284.
113 Frouz, J. (2002). The effect of soil macrofauna on litter decomposition and soil organic matter
accumulation during soil formation in spoil heaps after brown coal mining: a preliminary results.
Ekologia-Bratislava 21: 363–369.
114 Frouz, J., Kristufek, V., Bastl, J. et al. (2005). Determination of toxicity of spoil substrates after
brown coal mining using a laboratory reproduction test with Enchytraeus crypticus
(Oligochaeta). Water Air and Soil Pollution 162: 37–47.
115 Frouz, J., Elhottova, D., Pizl, V. et al. (2007). The effect of litter quality and soil faunal
composition on organic matter dynamics in post-mining soil: a laboratory study. Applied Soil
Ecology 37: 72–80.
116 Roubickova, A., Mudrak, O., and Frouz, J. (2009). Effect of earthworm on growth of late
succession plant species in postmining sites under laboratory and field conditions. Biology and
Fertility of Soils 45: 769–774.
117 Frouz, J., Kalcik, J., and Velichova, V. (2011). Factors causing spatial heterogeneity in soil
properties, plant cover, and soil fauna in a non-reclaimed post-mining site. Ecological Engineering
37: 1910–1913.
118 Hendrychova, M., Salek, M., Tajovsky, K., and Rehor, M. (2012). Soil properties and species
richness of invertebrates on afforested sites after brown coal mining. Restoration Ecology 20:
561–567.
119 Mudrak, O., Uteseny, K., and Frouz, J. (2012). Earthworms drive succession of both plant and
Collembola communities in post-mining sites. Applied Soil Ecology 62: 170–177.
120 Moradi, J., Mudrak, O., Kukla, J. et al. (2017). Variations in soil chemical properties, microbial
biomass, and faunal populations as related to plant functional traits, patch types, and
successional stages at Sokolov post-mining site – a case study. European Journal of Soil Biology
83: 58–64.
121 Moradi, J., Potocky, P., Kocarek, P. et al. (2018). Influence of surface flattening on biodiversity of
terrestrial arthropods during early stages of brown coal spoil heap restoration. Journal of
Environmental Management 220: 1–7.
122 Prescott, C.E., Frouz, J., Grayston, S.J. et al. (2019). Rehabilitating forest soils after disturbance.
In: Developments in Soil Science, vol. 36 (eds. M. Busse, C.P. Giardina, D.M. Morris and
D.S. Page-Dumroese), 309–343. Elsevier.
123 Biederman, L.A., Boutton, T.W., and Whisenant, S.G. (2008). Nematode community development
early in ecological restoration: the role of organic amendments. Soil Biology & Biochemistry 40:
2366–2374.
124 Six, J., Bossuyt, H., Degryze, S., and Denef, K. (2004). A history of research on the link between
(micro) aggregates, soil biota, and soil organic matter dynamics. Soil and Tillage Research 79: 7–31.
 ­Reference 93

25 Scheu, S. and Setälä, H. (2002). Multitrophic interactions in decomposer food-webs. In:


1
Multitrophic Level Interactions (eds. B.A. Hawkins and T. Tscharntke). Cambridge: Cambridge
University Press.
126 Petersen, H. and Luxton, M. (1982). A comparative analysis of soil fauna populations and their
role in decomposition processes. Oikos 39: 288–388.
127 Parisi, V., Menta, C., Gardi, C. et al. (2005). Microarthropod communities as a tool to assess soil
quality and biodiversity: a new approach in Italy. Agriculture, Ecosystems & Environment 105:
323–333.
128 Tsiafouli, M.A., Kallimanis, A.S., Katana, E. et al. (2005). Responses of soil microarthropods to
experimental short-term manipulations of soil moisture. Applied Soil Ecology 29: 17–26.
129 Van Straalen, N.M. (1998). Evaluation of bioindicator systems derived from soil arthropod
communities. Applied Soil Ecology 9: 429–437.
130 Coleman, D. and Callaham, M.C. Jr. (2017). Fundamentals of Soil Ecology, 3e. London:
Academic Press.
131 Brussaard, L., Pulleman, M.M., Ouédraogo, É. et al. (2007). Soil fauna and soil function in the
fabric of the food web. Pedobiologia 50: 447–462.
132 Harris, J. (2009). Soil microbial communities and restoration ecology: facilitators or followers?
Science 325: 573–574.
133 Harris, J.A., Hobbs, R.J., Higgs, E., and Aronson, J. (2006). Ecological restoration and global
climate change. Restoration Ecology 14: 170–176.
134 Scullion, J. (1991). Re-establishing earthworm populations on former opencast coal mining land.
In: Land Reclamation. An End to Dereliction? (ed. M.C.R. Davies), 377–386. London: Elsevier
Applied Sciences.
135 Scullion, J. (1994). Earthworms and soil rehabilitation after opencast mining for coal. Proceedings
of the 2nd International Symposium on Environmental Biotechnology, Brighton. Institution of
Chemical Engineers Symposium Series, 49–51.
136 Scullion, J., Mohammed, A.R.A., and Ramshaw, G.A. (1988). Changes in earthworm populations
following cultivation of undisturbed and former opencast coal-mining land. Agriculture,
Ecosystems & Environment 20: 289–302.
137 Jones, C., Lawton, J., and Shachak, M. (1994). Organisms as ecosystem engineers. Oikos 69: 373–386.
138 Lavelle, P., Decaens, T., Aubert, M. et al. (2006). Soil invertebrates and ecosystem services.
European Journal of Soil Biology 42: S3–S15.
139 Paine, R.T. (1969). A note on trophic complexity and community stability. The American
Naturalist 103: 91–93.
140 Jouquet, P., Dauber, J., Lagerlof, J. et al. (2006). Soil invertebrates as ecosystem engineers:
intended and accidental effects on soil and feedback loops. Applied Soil Ecology 32: 153–164.
141 Lavelle, P., Bignell, D., Lepage, M. et al. (1997). Soil function in a changing world: the role of
invertebrate ecosystem engineers. European Journal of Soil Science 33: 159–193.
142 Fournier, V., Rosenheim, J.A., Brodeur, J. et al. (2003). Herbivorous mites as ecological engineers:
indirect effects on arthropods inhabiting papaya foliage. Oecologia 135: 442–450.
143 Salmon, S., Geoffroy, J.-J., and Ponge, J.-F. (2005). Earthworms and collembola relationships:
effects of predatory centipedes and humus forms. Soil Biology and Biochemistry 37: 487–495.
144 Filser, J., Faber, J.H., Tiunov, A.V. et al. (2016). Soil fauna: key to new carbon models. Soil 2: 565–582.
145 Tuma, J., Fleiss, S., Eggleton, P. et al. (2019). Logging of rainforest and conversion to oil palm
reduces bioturbator diversity but not levels of bioturbation. Applied Soil Ecology 144: 123–133.
146 Butt, K.R., Frederickson, J., and Morris, R.M. (1995). An earthworm cultivation and soil
inoculation technique for land restoration. Ecological Engineering 4: 1–9.
94 4  Soil Meso- and Macrofauna Indicators of Restoration Success in Rehabilitated Mine Sites

147 Byers, J.E., Cuddington, K., Jones, C.G. et al. (2006). Using ecosystem engineers to restore
ecological systems. Trends in Ecology & Evolution 21: 493–500.
148 Angst, S., Mueller, C.W., Cajthaml, T. et al. (2017). Stabilization of soil organic matter by
earthworms is connected with physical protection rather than with chemical changes of organic
matter. Geoderma 289: 29–35.
149 Fonte, S.J., Quintero, D.C., Velásquez, E., and Lavelle, P. (2012). Interactive effects of plants and
earthworms on the physical stabilization of soil organic matter in aggregates. Plant and Soil 359:
205–214.
150 Bohlen, P.J. and Edwards, C.A. (1995). Earthworm effects on N dynamics and soil respiration
in microcosms receiving organic and inorganic nutrients. Soil Biology & Biochemistry 27:
341–348.
151 Uvarov, A.V., Ilieva-Makulec, K., Karaban, K. et al. (2019). Effects of intra- and interspecific
interactions in earthworm assemblages: a comparative study. Biology Bulletin 46: 475–482.
152 O’Grady, A., Schmidt, O., and Breen, J. (2010). Trophic relationships of grassland ants based on
stable isotopes. Pedobiologia 53: 221–225.
153 De Araújo, A.S.F., Eisenhauer, N., Nunes, L.A.P.L. et al. (2015). Soil surface-active fauna in
degraded and restored lands of Northeast Brazil. Land Degradation & Development 26: 1–8.
154 Frouz, J., Holec, M., and Kalcik, J. (2003). The effect of Lasius niger (Hymenoptera, Formicidae)
ant nest on selected soil chemical properties. Pedobiologia 47: 205–212.
155 König, H. (2006). Intestinal Microorganisms of Termites and Other Invertebrates. Springer
Science & Business Media.
156 Spain, A., Hinz, D., and Tibbett, M. Colonisation of rehabilitated lands by termites (Dictyoptera),
Rio Tinto Alcan Gove bauxite mine, Northern Territory, Australia. In: Fourie, A. B., Tibbett, M. &
Wiertz, J., eds., Proceedings Fifth International Conference on Mine Closure (Mine Closure 2010),
pp. 23–26.Australian Centre for Geomechanics.
157 Pardeshi, M. and Prusty, B.K. (2010). Termites as ecosystem engineers and potentials for soil
restoration. Current Science 99: 11.
158 Lee, K.E. and Foster, R.C. (1991). Soil fauna and soil structure. Australian Journal of Soil Research
29: 745–775.
159 Hättenschwiler, S., Tiunov, A.V., and Scheu, S. (2005). Biodiversity and litter decomposition in
terrestrial ecosystems. Annual Review of Ecology Evolution and Systematics 36: 191–218.
160 Jeffery, S., Gardi, C., Jones, A. et al. (2010). European Atlas of Soil Biodiversity. Brussels:
European Commission.
161 Chamberlain, P.M., McNamara, N.P., Chaplow, J. et al. (2006). Translocation of surface litter
carbon into soil by Collembola. Soil Biology and Biochemistry 38 (9): 2655–2664.
162 Meyer-Wolfarth, F., Schrader, S., Oldenburg, E. et al. (2017). Collembolans and soil nematodes as
biological regulators of the plant pathogen Fusarium culmorum. Journal of Plant Diseases and
Protection 124: 493–498.
163 Hofstetter, R. and Moser, J. (2014). The role of mites in insect-fungus associations. Annual Review
of Entomology 59: 537–557.

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