Review

Soil and Sediment Organisms as Bioindicators of Pollution

Samir Ghannem 1 , Ons Bacha 1 , Sondes Fkiri 2 , Sabri Kanzari 2, * , Abdelwaheb Aydi 3 and Samir Touaylia 1

1 Laboratory of Environment Biomonitoring, Life Sciences Department, Faculty of Sciences Bizerta, University
of Carthage, Zarzouna 7021, Tunisia; ghannemsamir7@gmail.com (S.G.); ons.bacha@fsb.u-carthage.tn (O.B.);
toysam2010@yahoo.fr (S.T.)
2 National Research Institute of Rural Engineering, Water and Forests, University of Carthage,
Ariana 2080, Tunisia; sondesfkiri@gmail.com
3 Department of Earth Sciences, Faculty of Sciences of Bizerte, University of Carthage, Bizerte 7021,Tunisia;
abdelwaheb_2000@yahoo.fr
* Correspondence: sabri.kanzari@gmail.com

Abstract: This review examines the role of soil and sediment organisms as bioindicators in envi-
ronmental pollution assessment. As fundamental elements of terrestrial ecosystems, soils harbour
a rich and diverse biodiversity that plays a key role in regulating ecological processes. The use of
bioindicators provides a sensitive and specific approach to detecting the effects of chemical, bio-
logical, and physical pollutants on soil health. The review presents a detailed analysis of the types
of contaminants commonly encountered, the soil organisms used as bioindicators, and the criteria
for selecting the most appropriate bioindicators. It also discusses assessment methods, including
soil sampling and analysis techniques, and the biological and ecological indices used to measure
contamination. Regional case studies illustrate the practical application of bioindicators for assessing
soil quality in different geographical contexts. The review also highlights current challenges to the
use of bioindicators, such as technical limitations and the variability of organism responses, and
suggests perspectives for future research, including technological innovation and the integration of
bioindicators into environmental policy.

Keywords: bioindicators; soil pollution; soil organisms; soil biodiversity; environmental assessment;
soil health; bioremediation
Citation: Ghannem, S.; Bacha, O.;
Fkiri, S.; Kanzari, S.; Aydi, A.;
Touaylia, S. Soil and Sediment
Organisms as Bioindicators of
Pollution. Ecologies 2024, 5, 679–696.
1. Introduction
https://doi.org/10.3390/ Soil is one of the fundamental elements of terrestrial ecosystems and plays a critical
ecologies5040040 role in sustaining life on Earth. It serves as the basis for plant growth, providing essential
nutrients, water, and physical support for roots. In addition to its role as a substrate for
Academic Editor: José
Ramón Arévalo Sierra
vegetation, soil is home to a wide range of living organisms, from microorganisms such as
bacteria and fungi to macroorganisms such as earthworms and insects. This below-ground
Received: 23 September 2024 biodiversity is essential for maintaining biogeochemical cycles, such as the carbon, nitrogen,
Revised: 12 December 2024 and phosphorus cycles, which are essential for ecosystem health [1,2]. As a regulator of
Accepted: 14 December 2024 ecological processes, soil acts as a buffer against environmental disturbances. It filters
Published: 18 December 2024
water, decomposes organic matter, and stores carbon, thus contributing to climate change
mitigation [3]. In addition, soil structure and composition influence the distribution of
natural habitats and above-ground biodiversity [4]. Today, however, soils are threatened by
Copyright: © 2024 by the authors.
various forms of pollution caused by human activities such as intensive agriculture, urbani-
Licensee MDPI, Basel, Switzerland. sation, and industrialisation. These activities lead to soil degradation, loss of biodiversity,
This article is an open access article and disruption of the ecosystem services they provide [5]. In this context, the study of soils
distributed under the terms and and their organisms is crucial to understanding and monitoring the effects of pollution.
conditions of the Creative Commons Indeed, soil can be an excellent bioindicator of pollution because it contains many living
Attribution (CC BY) license (https:// organisms and microorganisms that are sensitive to changes in their environment. What
creativecommons.org/licenses/by/ is more, pollutants in the air and water can accumulate in the soil and be taken up by the
4.0/). plants, animals, and microorganisms that live there. Furthermore, a number of studies

Ecologies 2024, 5, 679–696. https://doi.org/10.3390/ecologies5040040 https://www.mdpi.com/journal/ecologies

Ecologies 2024, 5 680

have suggested the use of sediments as environmental indicators to assess metal pollution
in aquatic environments [6–8]. In this sense, heavy metal concentrations in sediments are
constantly monitored to provide baseline information for environmental assessment [9]. As
soil is the main sink for airborne metals, measuring their levels in this medium is useful for
determining trends in abundance and their consequences due to natural and anthropogenic
changes [10]. Heavy metals have a significant impact on biological systems through a pro-
cess of biomagnification and bioaccumulation. They can affect the environment at different
levels of the trophic chain and are potentially harmful to ecosystems and humans [11,12].
In addition, metal speciation can help to assess how well metals are retained in the soil and
how easily they can be released into the soil solution [13]. By identifying changes in soil
biological communities, researchers can use these organisms as bioindicators to assess soil
health and the severity of contamination, which is essential for implementing sustainable
natural resource management strategies [14].
In this review, we aim to compile and present an overview of the different methods
used to assess changes in the soil and sediment environment using biological indicators.
We will also analyse the role of soil organisms, including soil fauna, bacteria, and fungi, as
bioindicators of pollution and ecosystem health. In addition, we will investigate how these
bioindicators can be used to detect and quantify the effects of pollution on soil and sediment
biodiversity. Another objective is to provide recommendations for integrating bioindicators
into natural resource management strategies to improve sustainability and environmental
protection. We will also identify gaps in current research on the use of bioindicators and sug-
gest avenues for future studies. Finally, we will highlight the importance of soil biodiversity
in maintaining ecosystem services and resilience to environmental perturbations.

2. Definition and Role of Bioindicators

A bioindicator is an organism or group of living organisms that responds in a pre-
dictable way to changes in the environment, particularly to chemical, biological, or physical
pollution. These responses can be observed at the molecular, physiological, behavioural,
population, and community levels [15]. As such, bioindicators make it possible to detect
and quantify the effects of environmental perturbations before they become visible by other
means. Bioindicators are used to monitor the quality of various media, including soil, water,
and air, and provide critical information for environmental management.

Advantages of Using Bioindicators in Pollution Assessment

The use of bioindicators offers several advantages in the assessment of environmen-
tal pressures:
a. Sensitivity to environmental changes: Bioindicators can respond rapidly to changes
in their environment, often before the changes are detectable by traditional physico-
chemical measurements [16]. This allows early detection of potential problems and
rapid intervention.
b. Representation of overall ecological quality: Unlike chemical indicators, which mea-
sure specific parameters, bioindicators integrate the cumulative effects of pollutants
on living organisms. They, therefore, reflect a more complete picture of the ecological
state of a given environment [17].
c. Cost-effectiveness: The use of bioindicators can be more cost-effective than complex
chemical analyses. For example, assessing macroinvertebrate biodiversity in soils
or streams requires less expensive technology while providing valuable data on
ecosystem health [18].
d. Applicability to different environments: bioindicators can be used in a variety of
environments, including soils, freshwater, marine waters, and even the atmosphere,
providing great flexibility for environmental studies [19].
Ecologies 2024, 5 681

3. Impact of Pollutants on Soil Biological Communities

Diversity of Soil Organisms
Soil is home to an incredible biodiversity of living organisms that play a crucial role
in maintaining the health of ecosystems. Soil organisms play a critical role in detecting
various types of pollutants, which is further explored in this review. These organisms
include a wide variety of microorganisms such as bacteria and fungi, as well as more
complex life forms such as microfauna (nematodes, mites) and macrofauna (earthworms,
insects, myriapods). Each group makes its own specific contribution to ecological processes,
including the decomposition of organic matter, the recycling of nutrients, and the formation
of soil structure [1,20].
Bacteria and fungi: Bacteria are ubiquitous in soils and are responsible for many
biochemical processes such as nitrogen fixation, decomposition of organic matter, and
humus formation. However, Kamble et al. [21] examined the impact of agricultural practices
on soil microbial biodiversity, highlighting that intensive use of pesticides and chemical
fertilisers leads to a significant reduction in the diversity of microbial communities. Their
study found that chemical-treated soils had a 40% reduction in the species richness of
beneficial bacteria compared to organically farmed soils. They also found that this loss
of biodiversity was correlated with a decline in soil fertility and an increase in plant
diseases. These findings highlight the importance of adopting sustainable farming practices
to maintain soil health and microbial biodiversity. Fungi, in turn, play a key role in the
breakdown of complex materials such as lignin and in the formation of mycorrhizae, which
help plants absorb nutrients [22,23]. They are crucial in terrestrial ecosystems by regulating
plant productivity, decomposing organic matter, and recycling nutrients. In particular,
mycorrhizal fungi form symbiotic associations with plant roots, enhancing the uptake of
limiting nutrients such as nitrogen (N) and phosphorus (P). In nutrient-poor ecosystems, up
to 90% of the N and P supply can come from these fungi. In addition, soil fungal diversity is
closely linked to the overall health of the ecosystem, as soils rich in fungal biodiversity are
generally more resilient to environmental disturbances. Fungi also influence competitive
interactions between plants, promoting the coexistence of plant species, and play a key role
in biogeochemical cycles, in particular by facilitating nitrogen fixation. In short, fungi are
essential players in maintaining plant productivity, soil health, and ecosystem biodiversity.
Microfauna: Consisting of nematodes, mites, and other small organisms that often
act as intermediaries in soil food chains, these organisms are sensitive to environmental
changes, making them particularly useful as bioindicators of soil health [24,25]. In a study
of nematode communities across eight sites from three river catchments, researchers inves-
tigated the genera composition, feeding types, and life-history strategies. The sampling
sites exhibited a gradient of anthropogenic contamination, with heavy metals and organic
pollutants being significant factors in differentiating the sites. Nematode community struc-
ture was closely related to sediment pollution and the hydro-morphological structure of
the sampling locations. Heavily contaminated sites were characterised by communities
with high relative abundances of omnivorous and predacious nematodes (Tobrilus, c–p 3;
Mononchus, c–p 4), while sites with low to medium contamination were dominated by
bacterivorous nematodes (Monhystera, Daptonema; c–p 2) or suction feeders (Dorylaimus,
c–p 4). The relatively high maturity index values in the heavily polluted sites were surpris-
ing. Overall, nematodes emerged as a suitable organism group for monitoring sediment
quality, with generic composition serving as the most accurate indicator for assessing dif-
ferences in nematode community structure. This underscores the importance of nematodes
not only in understanding the ecological impacts of pollution but also in providing valuable
insights into the health of aquatic ecosystems.
Macrofauna: Macrofauna, including earthworms, insects, and other large inverte-
brates, play an important role in soil aeration and mixing of organic matter, contributing
to the formation of a soil structure favourable to plant growth [26]. Earthworms, for
example, are often used as bioindicators because of their sensitivity to changes in soil
quality, such as the presence of heavy metals or pesticides [27]. Many experiments have
Ecologies 2024, 5 682

demonstrated how quickly soil that has been previously dispersed into units smaller than
2 mm can be enriched in large aggregates by endogenic earthworms. In tropical soils, this
effect can be particularly pronounced, with the entire soil of the upper 10 cm potentially
being bioturbated within just a few years. Consequently, the distribution of communi-
ties among different functional groups (for example, ‘compacting’ vs. ‘decompacting’)
becomes critical to soil functioning. In Amazonian oxisols near Manaus (Brazil), diverse
communities of soil engineers in natural forests create a wide variety of biogenic structures
(voids, pores, fabrics, and aggregates of all sizes), which endow these soils with highly
favorable hydraulic properties. However, when deforestation occurs, these soils tend
to lose much of this diversity, and invasive species may severely impair their physical
function by producing excessive amounts of a single type of structure. The effects of soil
invertebrate engineers have sometimes been described at a landscape scale. For instance,
in sloping environments in West Africa, earthworms have been reported to trigger soil
creep through the continuous erosion of surface casts and the downslope transport of their
materials. Jones et al. [22] detail the sophisticated contributions of isopods to the regulation
of physical (soil erosion) and chemical (soil desalinization) processes at the watershed
scale in the southern Negev Desert Highlands of Israel. Additionally, the roles of termites
and ants in shaping geomorphology and soil profiles at landscape levels have been well
documented, highlighting the significant impact of these organisms on soil health and
ecosystem functioning.
Soil biodiversity is closely linked to the overall health of the ecosystem. Biodiverse
soils are generally more resilient to environmental disturbances. They are able to main-
tain high productivity and ecological stability. Studies have shown that the loss of soil
biodiversity can lead to reduced soil fertility, increased erosion, and reduced capacity to
store carbon [28]. Consequently, soil biodiversity is often used as an indicator of soil health
and its ability to provide essential ecosystem services [29]. Certain species of land snails,
such as Papillifera papillaris, Eobonia vermiculata, or Arianta arbustorum, which are widely
distributed, have been recommended as bioindicators of metal contamination in soil [30,31].
The exposure of land snails to elevated levels of elements of concern can lead to various
symptoms of toxicity such as reduced growth, reproduction, mortality, normal metabolic
activities, etc. [32,33]. Extreme soil pollution can even eliminate the snail community [34].
In this context, the physiological, biochemical, genetic, and histological parameters of the
animals, the expression of indicators of oxidative stress (such as metallothionein synthesis),
and the alteration of enzymatic activity can be used to assess the harmful effects of the
elements at risk on the snail organism. Consequently, they can be used as suitable indices
for biomonitoring of the contaminated soil [33,35]. For example, significant correlations
between glutathione levels and acetylcholinesterase activity in the organism C. aspersus
and the levels of hazardous elements in the soil have been reported by Douafer et al. [36].
Similarly to land snails, various epigean beetles (Coleoptera) have been studied as possi-
ble bioindicators of soil pollution, in particular, due to their high sensitivity to changing
environmental conditions and rapid response to contamination [12,37]. For example,
Mukhtorova et al. [38] confirmed the ability of coleopterans (dominant species Philonthus
decorus, Staphylinidae, and Silpha obscura, Silphidae) to accumulate high-risk elements.

4. Soil Organisms as Bioindicators

4.1. Bioindicator Selection Criteria
4.1.1. Characteristics of Suitable Bioindicator Organisms
For an organism to be effective as a bioindicator, it must have several key character-
istics. First, it must be sensitive to environmental changes, including specific pollutants
or changes in abiotic conditions such as soil acidity or nutrient levels. This sensitivity
allows rapid detection of ecosystem perturbations [15]. Secondly, the organism must have
a wide geographical distribution, so that it can be used in different regions and soil types.
This makes it possible to compare different sites and make consistent assessments on a
regional or global scale [16]. Thirdly, it must be relatively easy to sample and identify, using
Ecologies 2024, 5 683

standardised analytical methods that ensure reliable and reproducible results. Finally, the
organism must have a well-understood ecology so that observed variation can be clearly
interpreted in relation to environmental conditions [18].

4.1.2. Examples of Commonly Used Bioindicators

Bioindicators play a crucial role in assessing environmental pollution, each providing
specific information about the health of ecosystems. Soil microorganisms, such as bacteria
and fungi, are sensitive indicators of changes in soil quality, as their diversity and activity
are often affected by pollution. They are assessed by analysing microbial biomass and
enzymatic activity, reflecting their role in biogeochemical cycles and pollutant degrada-
tion. Nematodes, for their part, are also sensitive to environmental variations and their
identification enables soil quality and trophic structure to be assessed [24]. Macroinverte-
brates, such as earthworms and insects, are important indicators of the health of terrestrial
ecosystems [12,17,27,39,40], their presence or absence signalling pollution levels. Their
assessment is based on an analysis of species diversity and abundance. Finally, mycorrhizal
fungi, which form symbiotic associations with plant roots, are sensitive to changes in soil
quality and their diversity and metabolic activity can indicate healthy soil. By combining
these different bioindicators, it is possible to obtain a more complete picture of ecosys-
tem health and soil quality, making it easier to implement sustainable natural resource
management strategies. The table below (Table 1) provides a summary of commonly used
bioindicators, detailing their respective groups, the types of pollution they help assess, and
their ecological roles in soil health evaluation.

Table 1. Commonly used bioindicators in soil and sediment pollution assessment and their ecological
roles (classified by taxonomic affiliation and body size where applicable).

Bioindication
Bioindicator Group Pollution Type Indicator Role References
Context
Soil health assessment,
Heavy metals,
Carabidae beetles Insects indicator of soil Soil [39,41]
pesticides
structure
Indicator of soil
Earthworms Heavy metals,
Annelids structure and Soil [42,43]
(Lumbricus sp.) organic pollutants
organic matter
Pesticides, Indicator of soil health
Nematodes Microfauna Soil [44,45]
heavy metals and contamination
Heavy metals, Indicator of soil
Mycorrhizal fungi Fungi Soil [46,47]
organic pollutants nutrient cycling
Bacteria (e.g., Indicator of organic
Microorganisms Organic pollutants Soil [48,49]
Pseudomonas) matter decomposition
Indicator of soil
Collembola Pesticides, structure,
Insects oil [50,51]
(springtails) heavy metals biodiversity, and
contamination levels
Indicator of organic
Fungi (e.g., pollution and soil
Fungi Organic pollution Soil [52,53]
Basidiomycota) health through
decomposition processes
Heavy Indicator of
River
Invertebrates Aquatic insects metals, sediment [54]
sediments
pesticides quality
Ecologies 2024, 5 684

As shown in Table 1, these bioindicators help assess soil health and pollution by re-
sponding to various contaminants through changes in population, diversity, and biological
processes, making them valuable tools for environmental monitoring.

5. Action Mechanisms of Pollutants in the Soil and Sediments

5.1. Soil Pollution Levels
We present a compilation of soil pollution levels that illustrates the concentrations of
various contaminants found in soils. Table 2 provides an overview of sediment pollution
levels, showcasing data from multiple published studies and highlighting the range of
contaminant concentrations observed across different geographical regions and types
of sediment.

Table 2. Compilation of sediment pollution levels according to published studies.

Pollution Level Regulatory

Pollutant Type of Site Reference
(mg/kg) Threshold (mg/kg)
Heavy Metals
River sediments
Lead (Pb) 70–120 100 [55]
(urbanised)
Cadmium (Cd) Lake sediments 0.2–0.8 0.5 [56]
Zinc (Zn) Estuary sediments 200–300 200 [57]
Mercury (Hg) Estuarine sediments 0.01–0.03 0.1 [57]
Lake sediments
Arsenic (As) 15–30 20 [58]
(mining areas)
Chromium (Cr) Fluvial sediment 50–150 100 [59]
Marine sediments
Copper (Cu) 70–110 100 [59]
(Türkiye)
Pesticides
DDT River sediments 0.02–0.05 0.01 [60]
Polluants Organiques
PAHs (Polycyclic Aromatic
Estuarine sediments 1.5–3.5 1.0 [57]
Hydrocarbons)
PCB (Polychlorinated
Urban sediments 0.02–0.09 0.05 [61]
biphenyls)
Plastic Pollutants
2.000–5.000
Microplastics Marine sediments N/A [62]
particles/kg
Nanoplastics Agricultural soils 50–150 particles/kg N/A [63]
Biological Pollutants
Agricultural soils
Microbial pathogens 103 –106 CFU/g N/A [64]
(fertilisers)

5.2. Types of Pollutants and Their Sources

5.2.1. Chemical Pollution: Heavy Metals, Pesticides
Chemical pollution of soil is mainly caused by the introduction of toxic substances such
as heavy metals and pesticides. Heavy metals such as lead, cadmium, and mercury often
come from industrial activities, vehicle emissions, and the use of agricultural chemicals.
These elements can persist in the soil for decades, bioaccumulating in living organisms and
causing long-term toxic effects on soil biodiversity and human health [65].
Ecologies 2024, 5 685

Meanwhile, pesticides are widely used in agriculture to control crop pests and dis-
eases. However, their intensive use can lead to soil contamination, where they can disrupt
microbial communities and affect non-target organisms such as earthworms and beneficial
insects. The slow degradation of some pesticides, such as organochlorines, can also prolong
their environmental impact [66].

5.2.2. Biological Pollution: Pathogenic Microorganisms

Biological contamination of soil involves the introduction of pathogenic microorgan-
isms, which can be of human, animal, or plant origin. These pathogens, such as certain
bacteria, viruses, or fungi, can enter the soil via wastewater, animal excreta, or untreated
organic waste. Once in the soil, these pathogens can contaminate crops, threaten plant,
animal, and human health, and disrupt ecosystems by reducing microbial biodiversity [67].

5.2.3. Physical Pollution: Plastic Waste

Physical pollution of soil, particularly from plastic waste, is a growing threat to
terrestrial ecosystems. Plastics, which make up a large proportion of solid waste, can
fragment into microplastics that accumulate in soils and disrupt soil structure, porosity,
and gas exchange. In addition, these microplastics can adsorb chemical contaminants and
introduce them into soil food webs, exacerbating environmental toxicity [68]. Other forms
of physical pollution include construction debris, mine tailings, and electronic waste, which
can not only alter the physical structure of the soil but also release toxic substances over
time, contributing to overall environmental degradation [69]. According to Scott et al. [70],
microplastic contamination was detected in seawater, coastal sediments, and mussels at
all sampling locations in the southwest region of the UK. All surface seawater samples
contained microplastic particles, with concentrations ranging from 1.97 to 3.38 particles
per cubic meter, showing no significant variation across different sites. The composition of
these particles included 51% microfibres, 47% fragments, and only 0.03% microbeads. In
contrast, microplastic contamination in intertidal sediment varied significantly by location,
with concentrations ranging from 33.9 particles per kilogram at Torquay to 402.0 particles
per kilogram at Whitsand Bay, predominantly consisting of microfibres (93%) (Figure 1).
Among the sampled mussels, 88.5% contained microplastic particles, with significant
differences in particle load per mussel across study sites. Mussels from Whitsand Bay had
the highest average load of 7.64 particles per individual, while those from Torquay had
the lowest at 1.43 particles per individual. The majority of particles found in mussels were
microfibres (87%), with only 12% being fragments and less than 1% microbeads. Overall,
the study highlights widespread microplastic contamination in marine environments and
its impact on local mussel populations.
Additionally, micro-FTIR spectroscopy was performed on 247 randomly selected par-
ticles from seawater, sediment, and mussel samples, revealing that 33.9% of these particles
were synthetic plastic polymers, primarily polystyrene, polyethylene, and polypropylene
(Figure 2). Particles of natural origin, accounting for 9.3% of the analysed items, and
those with low-match-quality spectra (below 70%) were excluded from the final results. A
significant portion of the particles (56.8%) were identified as semi-synthetic fibres made of
modified cellulose. These modified cellulose fibres, predominantly in black/blue or red
colours, are likely viscose or rayon fibres from textiles.
In addition, the study found that the size and shape of anthropogenic particles
significantly influence their uptake by mussels (Figure 3). There were notable differ-
ences in the sizes of particles found in mussels compared to those in the surrounding
seawater. Specifically, the average length of fibres in mussels was significantly shorter
than those in seawater, with the longest fibre recorded at 8.7 mm. This indicates that
while longer fibres can be ingested, they do not correlate with the abundance of longer
fibres in seawater. Additionally, the anthropogenic fragments ingested by mussels were
smaller than those found in surface sediments. Fibres constituted 67.6% of the particles
in mussel samples, compared to only 23.4% in water samples. The study also identified
Ecologies 2024, 5 686

both high-density and low-density plastic polymers in mussels, with a different rela-
tive abundance of polymer types compared to those in the overlying seawater. This
Ecologies 2024, 5, FOR PEER REVIEWanalysis underscores the prevalence of synthetic and semi-synthetic materials in marine
9
environments, reinforcing the importance of organisms as bioindicators for assessing
microplastic pollution.

Figure
Figure 1.
1. The
The average
average number
number ofof microplastic–like
microplastic–like particles,
particles, characterised
characterised according
according to
to shape
shape found
found
in
in (A) surface seawater (2018 data), (B) the surface 1 cm of sediment (2018 data), and (C) within
(A) surface seawater (2018 data), (B) the surface 1 cm of sediment (2018 data), and (C) within the
the
tissues of the mussel Mytilus edulis (2017 and 2018 data) at coastal sites in Devon and Cornwall, SW
tissues of the mussel Mytilus edulis (2017 and 2018 data) at coastal sites in Devon and Cornwall, SW
England. Data as mean ± standard error (limit of detection cross all samples of 50 µm) [70].
England. Data as mean ± standard error (limit of detection cross all samples of 50 µm) [70].

Additionally,
5.3. Impact micro-FTIR
of Pollutants spectroscopy was performed on 247 randomly selected
on Soil Organisms
particles from seawater, sediment,
5.3.1. Physiological and Behavioural and mussel
Effects on samples, revealing that 33.9% of these par-
Bioindicators
ticles were synthetic plastic polymers, primarily polystyrene, polyethylene, and polypro-
Soil contaminants can have adverse effects on soil-dwelling organisms. These effects
pylene (Figure 2). Particles of natural origin, accounting for 9.3% of the analysed items,
often take the form of physiological and behavioural changes (Table 3). For example,
and those with low-match-quality spectra (below 70%) were excluded from the final re-
exposure to heavy metals such as cadmium and lead can cause disturbances in the cellular
sults. A significant portion of the particles (56.8%) were identified as semi-synthetic fibres
processes of soil organisms, including oxidative stress, protein denaturation, and altered
made
enzyme of functions
modified cellulose. These modified
[71]. In earthworms, cellulose
studies fibres, predominantly
have shown in can
that these metals black/blue
reduce
or red colours,capacity,
reproductive are likely viscose
impair or rayon
growth, andfibres
reduce from textiles.
survival [72].
 Ecologies 2024, 5 687

Pesticides, such as organophosphates, can also cause behavioural effects in bioindica-

tors, such as changes in locomotor activity, reduced feeding capacity, and changes in social
interactions within communities of soil organisms. These behavioural effects are often early
indicators of sublethal toxicity before lethal effects become apparent [73]. Bioindicators
have the potential to discriminate different situations in different environments. In most
cases, pollution and landscape mismanagement create a loss of biodiversity. However, the
FOR PEER REVIEW species or group of species demonstrates the impact of a stressor on a biotic system
10 and is
used to monitor long-term stressor-induced change on biota (including habitat alteration,
fragmentation, and climate change).

Figure 2. Results of ATR/FT-IR spectral

Figure 2. Results analysis, showing
of ATR/FT-IR proportions
spectral analysis, of polymers
showing ofof
proportions anthropogenic
polymers of anthropogenic
particles present in (A) samples of seawater, (B) the surface 1 cm of sediment, (C) within
particles present in (A) samples of seawater, (B) the surface 1 cm of sediment, Mytilus
(C) within Mytilus
edulis, and (D) macroplastic beach
edulis, and debris frombeach
(D) macroplastic coastal sampling
debris sites in
from coastal Devon sites
sampling and in
Cornwall, SW
Devon and Cornwall, SW
England [70]. England [70].

Table
In addition, the 3. Quantitative
study found that and the
qualitative
size anddata shape
on bioindicator impacts in different
of anthropogenic environmental
particles sig- contexts.
nificantly influence their uptake by mussels (Figure 3). There were notable differences in
Bioindicateur Type of Impact Quantitative Measures Qualitative Measures References
the sizes of particles found in mussels compared to those in the surrounding seawater.
Oulema gallaeciana Heavy metal Bioaccumulation factor:
Specifically, the average
(Chrysomelidae) length of fibres in Fe
contamination mussels
= 2.15 was significantly shorter than those in
Morphological changes [12]
seawater, with the longest fibre recorded at 8.7 mm. This indicates that while longer fibres
Lachnaia paradoxa Heavy metal Bioaccumulation factor:
can be ingested, they
(Chrysomelidae) do not correlate with
contamination Fe the abundance ofMorphological
= 1.69 longer fibres changes
in seawater. [12]
Additionally,
Chlaenius olivieri the anthropogenic fragments ingested
Bioaccumulation by mussels
factor: were smaller
Morphological than those
changes,
found in surfacePollution
(Carabidae) sediments.des sols
Fibres constituted 67.6% of theReduced
Cd = 9.89 particles in mussel
mobility samples, [17]
and activity
compared to only 23.4% in water samples. The study also identified both high-density and
low-density plastic polymers in mussels, with a different relative abundance of polymer
types compared to those in the overlying seawater. This analysis underscores the preva-
lence of synthetic and semi-synthetic materials in marine environments, reinforcing the
importance of organisms as bioindicators for assessing microplastic pollution.
Ecologies 2024, 5 688

Table 3. Cont.

Bioindicateur Type of Impact Quantitative Measures Qualitative Measures References

40% decrease
Chemical pesticides in the specific richness Decreased soil fertility and
Soil bacteria [21]
and fertilisers of beneficial increased plant diseases
bacteria
7.64 particles per
individual
Moules (Mytilus edulis) Plastic pollution Obstruction digestive [70]
(87% microfibres
whilst 12% fragments).
Camponotus japonicus Heavy metal Labial gland disease, reduction
Cu = 59.6 ppm [74]
(Hymenoptera) contamination in body mass
Pterostichus Larvae mortality was
Reduction in body weight,
oblongopunctatus Effect of temperatures approximately 30% [75]
reduced size
(Carabidae) of total
Metal percentages in
Trachyderma hispida testicular tissues: Structural abnormalities in
Ceramic pollution [76]
(Tenebrionidae) p = 37.1, S = 35.7, testicular follicles
Na = 9.7
Learning abilities and memory
are affected, reducing
Honeybees and Chemical pollution
individual foraging efficiency,
bumblebees (Pesticide (insecticides Sublethal doses [77]
navigation ability, motor
(Hymenoptera) and fungicides))
function, and social behaviour
in the nest.
Carabus lefebvrei Heavy metal Bioaccumulation factor: Morphological changes,
[78]
(Carabidae) contamination As = 61.07, Hg = 1.5 Physiological alterations
Decrease in population density,
a reduction in body weight, an
Blaps polycresta Heavy metal Bioaccumulation factor: increase in mortality rate, an
[79]
(Tenebrionidae) contamination Cd = 95.16 increase in sex ratio of the
insects, and a decrease in
body length

5.3.2. Changes in Soil Organism Communities in Response to Pollution

Soil communities are also sensitive to contaminants, which can cause significant
changes in their structure and function. The presence of chemical contaminants such
as heavy metals and hydrocarbons can reduce soil biodiversity by eliminating the most
sensitive species, leading to a reduction in species richness and a simplification of food
webs [80]. For example, a reduction in nematode and microarthropod populations is
often observed in soils contaminated by heavy metals, disrupting decomposition and
nutrient recycling processes [2]. Similarly, fungicides can alter soil fungal communities,
reducing the efficiency of organic matter decomposition and affecting soil fertility [81].
The cumulative effects of pollution on soil communities can lead to a loss of efficiency in
terrestrial ecosystems, compromising essential ecological services such as plant production,
regulation of biogeochemical cycles, and filtration of pollutants [82].
 Ecologies
es 2024, 5, FOR PEER 2024, 5
REVIEW 11 689

Figure 3. Comparisons of the sizes of the two major categories, (A) fibres and (B) fragments, of
Figure 3. Comparisons of the sizes of the two major categories, (A) fibres and (B) fragments, of
observed anthropogenic particles in samples of Mytilus edulis, seawater, and the surface 1 cm of
observed anthropogenic particles in samples of Mytilus edulis, seawater, and the surface 1 cm of
sediment from coastal sites in Devon and Cornwall, SW England in 2018. Groups labelled with the
same number are sediment from different.
significantly coastal sites in Devon
(One-way and Cornwall,
ANOVA; SW<England
(1) p-value inp-value
0.001, (2) 2018. Groups
< 0.001,labelled with the
same number
(3) p-value < 0.001) [70]. are significantly different. (One-way ANOVA; (1) p-value < 0.001, (2) p-value < 0.001,
(3) p-value < 0.001) [70].
5.3. Impact of Pollutants on Soil Organisms
6. Methods for Assessing Pollution Using Bioindicators
5.3.1. Physiological and
6.1. Soil Behavioural
Sampling Effects on
and Analysis Bioindicators
Techniques
Soil contaminants
6.1.1. Soilcan have adverse
Organism effects
Sampling on soil-dwelling organisms. These effects
Methods
often take the formSampling
of physiological and behavioural
organisms is a crucial step changes (Table pollution
in assessing 3). For example, ex-
using bioindicators. For
posure to heavy metals such
macrofauna, as as
such cadmium and lead
earthworms can cause
and beetles, disturbances
common in methods
sampling the cellular
include squaring
processes of soil
andorganisms, including
hand extraction, oxidative
as well as thestress,
use ofprotein denaturation,
pitfall traps and
to capture alteredorganisms [83].
surface
enzyme functionsThese techniques allow the collection of representative samples of thereduce
[71]. In earthworms, studies have shown that these metals can populations present
reproductive capacity,
in a givenimpair growth, and
area, facilitating thereduce survival
analysis of the [72].
impact of pollution on soil biodiversity.
For soil microorganisms, such as bacteria and fungi, sterile soil sampling methods
using soil cores are often employed. These samples are then subjected to laboratory
Ecologies 2024, 5 690

analyses, including culture on selective media, DNA extraction for genomic analyses, or
measurement of enzymatic activity to assess the health of microbial communities [84].

6.1.2. Biomarker and Biological Indicator Analysis Techniques

The analysis of biomarkers and biological indicators is an essential part of soil con-
tamination assessment. Biomarkers can be biochemical, cellular, or molecular parameters
that indicate exposure to contaminants or a biological effect of these contaminants on soil
organisms. For example, the induction of metallothionein in earthworms may indicate
exposure to heavy metals, while changes in enzymatic activities such as dehydrogenase or
phosphatase may indicate disturbances in microbial communities [85]. Biomarker analysis
techniques include biochemical methods such as mass spectrometry and chromatography
for the detection of organic and inorganic compounds in organism tissues. Molecular biol-
ogy techniques, such as quantitative PCR (qPCR) and DNA microarrays, are used to assess
changes in gene expression related to environmental stress or contaminant toxicity [86]. In
addition, the analysis of biological indicators such as diversity indices, relative abundance
of sensitive species, or changes in community composition are commonly used to inter-
pret the ecological impact of pollution. These techniques not only detect the presence of
contaminants but also quantify their effects on soil ecosystems [87].

6.2. Indices and Assessment Tools

6.2.1. Overview of Biological and Ecological Indices Used to Measure Pollution
Biological and ecological indices are essential tools for assessing the impact of pollution
on soil ecosystems. Among the most commonly used indices is the nematode maturity
index (NMI), which assesses the ecological quality of soils based on the composition of
nematode communities. This index is particularly useful for detecting disturbances caused
by chemical pollutants and for monitoring long-term changes in agricultural and natural
soils [24].
Another key index is the Shannon diversity index (H’), which measures the diversity
of species present in a soil sample. A healthy soil generally has a high species diversity,
whereas a polluted soil tends to show a reduction in this diversity, often due to the dis-
appearance of species sensitive to pollutants [88]. The diversity index is often used in
combination with other indices to provide a complete picture of soil ecological status.
The global soil biological index (GSBI) is another powerful tool that integrates several
biological parameters, such as microbial activity, biomass, and macroorganism diversity,
to provide an overall assessment of soil quality [89]. This index is particularly useful for
environmental managers and researchers wishing to assess soils in natural and agricul-
tural environments.

6.2.2. Examples of Successful Applications in Different Regions and Soil Types

Biological and ecological indices have been successfully used in different regions
and soil types to assess the impact of pollution. For example, biological indicator (BLI)
has been used in agricultural soils of northern Europe to assess the effects of intensive
farming practices and heavy metal pollution [45]. The results showed that more polluted
soils had a lower NMI, indicating a reduction in ecological quality due to pollution [45].
In South America, the Shannon diversity index was used to assess soils contaminated
by pesticide residues in sugar cane crops in Brazil. The results showed a significant
decrease in soil microbial diversity in the most contaminated areas, suggesting a negative
impact of intensive agricultural practices on soil health [90]. In France, IBGS was used to
assess forest and grassland soils exposed to different levels of air pollution. This study
showed that soils near industrial areas showed a significant decrease in IBGS, reflecting
ecological degradation due to the deposition of air pollutants [89]. In Asia, a study in
China used mycorrhizal fungi to assess the effect of industrial pollutants on soil health
in the Yangtze River Delta region. The study found a significant decrease in mycorrhizal
colonisation in contaminated soils, which was associated with a reduction in soil fertility
Ecologies 2024, 5 691

and a deterioration in soil structure. This demonstrates the importance of mycorrhizal

fungi as bioindicators of soil contamination [47].

6.3. Remediation Strategies Based on Bioindicator Results

The results obtained from the use of bioindicators are invaluable in guiding reme-
diation strategies for polluted soils. For example, bioaugmentation, which involves the
introduction of microorganisms that specialise in contaminant degradation, can be targeted
according to the characteristics of the microbial communities present in the soil, as identi-
fied by bioindicators such as bacteria and fungi [91]. Phytoremediation, the use of plants
to extract, stabilise, or degrade contaminants, is another approach based on bioindicator
results. For example, certain mycorrhizal plants that form symbioses with mycorrhizal
fungi can be selected to remediate soils contaminated with heavy metals due to their ability
to tolerate and accumulate these elements [92]. These practices can be adapted according
to biological indicators to maximise remediation efficiency.

6.4. Sustainable Soil Management Policies and Practices

Bioindicator results also need to be integrated into soil management policies to en-
sure long-term sustainability. Integrated soil management, which combines continuous
monitoring of bioindicators with sustainable agricultural practices, can both prevent soil
degradation and maintain soil productivity. For example, crop rotation and the addition
of organic matter to the soil, such as composting, can improve soil health by promoting
microbial biodiversity, thereby reducing reliance on pesticides and chemical fertilisers [93].
Policies to limit the use of polluting substances such as pesticides and chemical fertilis-
ers need to be based on data from bioindicators, allowing for more precise management
adapted to local soil conditions [94]. In addition, ecological restoration, using bioindicators
to monitor progress, should be a priority in severely degraded areas to restore ecosystem
health and protect biodiversity.

7. Prospects and Challenges

7.1. Current Limits to the Use of Bioindicators
7.1.1. Technical Limitations
The use of bioindicators in soil pollution assessment has several technical limitations
that need to be considered. First, the complexity and diversity of soil ecosystems make it
difficult to identify and interpret bioindicator responses. Soils contain a wide variety of
organisms whose interactions are often poorly understood, complicating data analysis and
leading to misinterpretation [95]. In addition, the collection and analysis of bioindicators
often require specialised methods and expensive equipment, which can limit their use in
resource-limited areas. For example, the taxonomic identification of soil microorganisms
requires specialised skills and access to extensive databases, which can be a barrier for
researchers working in under-resourced environments [96].

7.1.2. Variability of Bioindicator Responses

Another important limitation of the use of bioindicators is the variability of observed
responses according to local environmental conditions. Bioindicators may respond dif-
ferently to the same contaminant depending on factors such as soil type, climate, or land
management practices. This variability makes it difficult to establish universal standards for
assessing soil contamination and can make it difficult to compare results between different
studies [97]. What is more, some bioindicators may have a tolerance to contaminants that
varies according to their stage of development or physiological state. For example, nema-
todes, which are often used as bioindicators, may have different responses to pollutants
depending on their age or life cycle, adding a layer of complexity to data interpretation [24].
Ecologies 2024, 5 692

7.1.3. Long-Term Assessment and Reliability

Finally, the reliability of bioindicators for long-term assessment of soil contamination
remains a challenge. Although bioindicators are useful for detecting immediate changes in
soil ecosystems, their ability to provide accurate assessments over long periods is limited
by the lack of longitudinal data and by changing environmental conditions. In addition,
natural resilience and recovery processes in ecosystems can mask the long-term effects of
pollution, making it difficult to identify its lasting impacts [98].

8. Conclusions
This review has highlighted the crucial role of bioindicators in the assessment of soil
pollution, emphasising their ability to provide detailed information on the state of health
of terrestrial ecosystems. Whether microorganisms, nematodes, or other soil organisms,
bioindicators provide a comprehensive view of the impact of chemical, biological, and
physical contaminants on soils. Despite the technical and methodological challenges
associated with their use, bioindicators remain essential tools for monitoring soil quality
and guiding remediation strategies.
The systematic integration of bioindicators into environmental management strategies
is essential to ensure effective long-term soil protection. By enabling continuous and
accurate soil monitoring, bioindicators can help to tailor environmental policies to local
specificities, promote sustainable management practices, and reduce the impact of human
activities on ecosystems. Their incorporation into regulatory frameworks and agricultural
practices is a necessary step towards preserving biodiversity and soil fertility. In order to
overcome current limitations and optimise the effectiveness of bioindicators, it is essential to
continue research in this field, in particular, through the development of new technologies
and analytical methods. In addition, interdisciplinary collaboration between ecologists,
agronomists, microbiologists, and policymakers is essential to translate scientific advances
into concrete soil management actions. Ultimately, soil conservation is a collective effort to
understand and preserve the vital functions of terrestrial ecosystems.

Author Contributions: S.G.: Writing—original draft, Methodology, Investigation, Data curation.

O.B.: Writing—review and editing, Funding acquisition, Formal analysis. S.F.: Resources, Formal
analysis. S.K.: Writing—review and editing, Investigation, Funding acquisition. A.A.: Supervision,
Formal analysis. S.T.: Writing—review and editing, Resources, Formal analysis. All authors have
read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Conflicts of Interest: The authors declare no conflicts of interest.

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