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Review

Soil and Sediment Organisms as Bioindicators of Pollution

by
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
2
National Research Institute of Rural Engineering, Water and Forests, University of Carthage, Ariana 2080, Tunisia
3
Department of Earth Sciences, Faculty of Sciences of Bizerte, University of Carthage, Bizerte 7021,Tunisia
*
Author to whom correspondence should be addressed.
Ecologies 2024, 5(4), 679-696; https://doi.org/10.3390/ecologies5040040
Submission received: 23 September 2024 / Revised: 12 December 2024 / Accepted: 14 December 2024 / Published: 18 December 2024
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Abstract

:
This review examines the role of soil and sediment organisms as bioindicators in environmental 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, biological, 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.

1. Introduction

Soil is one of the fundamental elements of terrestrial ecosystems and plays a critical 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 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 biodiversity is essential for maintaining biogeochemical cycles, such as the carbon, nitrogen, and phosphorus cycles, which are essential for ecosystem health [1,2]. As a regulator of ecological processes, soil acts as a buffer against environmental disturbances. It filters 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 various forms of pollution caused by human activities such as intensive agriculture, urbanisation, and industrialisation. These activities lead to soil degradation, loss of biodiversity, and disruption of the ecosystem services they provide [5]. In this context, the study of soils and their organisms is crucial to understanding and monitoring the effects of pollution. Indeed, soil can be an excellent bioindicator of pollution because it contains many living organisms and microorganisms that are sensitive to changes in their environment. What is more, pollutants in the air and water can accumulate in the soil and be taken up by the plants, animals, and microorganisms that live there. Furthermore, a number of studies have suggested the use of sediments as environmental indicators to assess metal pollution in aquatic environments [6,7,8]. 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 process 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 suggest 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 predictable 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 environmental pressures:
  • 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.
  • Representation of overall ecological quality: Unlike chemical indicators, which measure 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].
  • 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].
  • 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].

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 investigated 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 structure 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 surprising. Overall, nematodes emerged as a suitable organism group for monitoring sediment quality, with generic composition serving as the most accurate indicator for assessing differences 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 invertebrates, 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 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 communities 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 maintain 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 possible 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 characteristics. 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 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 degradation. Nematodes, for their part, are also sensitive to environmental variations and their identification enables soil quality and trophic structure to be assessed [24]. Macroinvertebrates, 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 ecosystem 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.
As shown in Table 1, these bioindicators help assess soil health and pollution by responding 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.

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].
Meanwhile, pesticides are widely used in agriculture to control crop pests and diseases. 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 microorganisms, 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 particles 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 differences 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 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 prevalence of synthetic and semi-synthetic materials in marine environments, reinforcing the importance of organisms as bioindicators for assessing microplastic pollution.

5.3. Impact of Pollutants on Soil Organisms

5.3.1. Physiological and Behavioural Effects on Bioindicators

Soil contaminants can have adverse effects on soil-dwelling organisms. These effects often take the form of physiological and behavioural changes (Table 3). For example, exposure to heavy metals such as cadmium and lead can cause disturbances in the cellular processes of soil organisms, including oxidative stress, protein denaturation, and altered enzyme functions [71]. In earthworms, studies have shown that these metals can reduce reproductive capacity, impair growth, and reduce survival [72].
Pesticides, such as organophosphates, can also cause behavioural effects in bioindicators, 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 species or group of species demonstrates the impact of a stressor on a biotic system and is used to monitor long-term stressor-induced change on biota (including habitat alteration, fragmentation, and climate change).
Table 3. Quantitative and qualitative data on bioindicator impacts in different environmental contexts.
Table 3. Quantitative and qualitative data on bioindicator impacts in different environmental contexts.
BioindicateurType of ImpactQuantitative MeasuresQualitative MeasuresReferences
Oulema gallaeciana
(Chrysomelidae)		Heavy metal contaminationBioaccumulation factor: Fe = 2.15Morphological changes [12]
Lachnaia paradoxa
(Chrysomelidae)		Heavy metal contaminationBioaccumulation factor: Fe = 1.69Morphological changes[12]
Chlaenius olivieri (Carabidae)Pollution des solsBioaccumulation factor: Cd = 9.89Morphological changes, Reduced mobility and activity[17]
Soil bacteriaChemical pesticides and fertilisers40% decrease in the specific richness of beneficial bacteriaDecreased soil fertility and increased plant diseases[21]
Moules (Mytilus edulis)Plastic pollution7.64 particles per individual (87% microfibres whilst 12% fragments).Obstruction digestive[70]
Camponotus japonicus (Hymenoptera)Heavy metal contaminationCu = 59.6 ppmLabial gland disease, reduction in body mass[74]
Pterostichus oblongopunctatus (Carabidae)Effect of temperaturesLarvae mortality was approximately 30% of totalReduction in body weight, reduced size[75]
Trachyderma hispida
(Tenebrionidae)		Ceramic pollutionMetal percentages in testicular tissues:
p = 37.1, S = 35.7, Na = 9.7		Structural abnormalities in testicular follicles[76]
Honeybees and bumblebees (Hymenoptera)Chemical pollution (Pesticide (insecticides and fungicides))Sublethal dosesLearning abilities and memory are affected, reducing individual foraging efficiency, navigation ability, motor function, and social behaviour in the nest.[77]
Carabus lefebvrei (Carabidae)Heavy metal contaminationBioaccumulation factor: As = 61.07, Hg = 1.5Morphological changes, Physiological alterations[78]
Blaps polycresta
(Tenebrionidae)		Heavy metal contaminationBioaccumulation factor: Cd = 95.16Decrease in population density, a reduction in body weight, an increase in mortality rate, an increase in sex ratio of the insects, and a decrease in body length[79]

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].

6. Methods for Assessing Pollution Using Bioindicators

6.1. Soil Sampling and Analysis Techniques

6.1.1. Soil Organism Sampling Methods

Sampling organisms is a crucial step in assessing pollution using bioindicators. For macrofauna, such as earthworms and beetles, common sampling methods include squaring and hand extraction, as well as the use of pitfall traps to capture surface organisms [83]. These techniques allow the collection of representative samples of the populations present in a given area, facilitating the analysis of the 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 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 contamination 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 biology 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 interpret 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 disappearance 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 agricultural 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 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 remediation 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 identified 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 ensure 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 fertilisers 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 differently 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, nematodes, 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].

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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Figure 1. The average number of microplastic–like particles, characterised according to shape found in (A) surface seawater (2018 data), (B) the surface 1 cm of sediment (2018 data), and (C) within the 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].
Figure 1. The average number of microplastic–like particles, characterised according to shape found in (A) surface seawater (2018 data), (B) the surface 1 cm of sediment (2018 data), and (C) within the 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].
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Figure 2. Results of ATR/FT-IR spectral analysis, showing proportions of polymers of anthropogenic particles present in (A) samples of seawater, (B) the surface 1 cm of sediment, (C) within Mytilus edulis, and (D) macroplastic beach debris from coastal sampling sites in Devon and Cornwall, SW England [70].
Figure 2. Results of ATR/FT-IR spectral analysis, showing proportions of polymers of anthropogenic particles present in (A) samples of seawater, (B) the surface 1 cm of sediment, (C) within Mytilus edulis, and (D) macroplastic beach debris from coastal sampling sites in Devon and Cornwall, SW England [70].
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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 sediment from coastal sites in Devon and Cornwall, SW England in 2018. Groups labelled with the same number are significantly different. (One-way ANOVA; (1) p-value < 0.001, (2) p-value < 0.001, (3) p-value < 0.001) [70].
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 sediment from coastal sites in Devon and Cornwall, SW England in 2018. Groups labelled with the same number are significantly different. (One-way ANOVA; (1) p-value < 0.001, (2) p-value < 0.001, (3) p-value < 0.001) [70].
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Table 1. Commonly used bioindicators in soil and sediment pollution assessment and their ecological roles (classified by taxonomic affiliation and body size where applicable).
Table 1. Commonly used bioindicators in soil and sediment pollution assessment and their ecological roles (classified by taxonomic affiliation and body size where applicable).
BioindicatorGroupPollution TypeIndicator RoleBioindication ContextReferences
Carabidae beetlesInsectsHeavy metals, pesticidesSoil health assessment, indicator of soil structureSoil[39,41]
Earthworms (Lumbricus sp.)AnnelidsHeavy metals, organic pollutantsIndicator of soil structure and organic matterSoil[42,43]
NematodesMicrofaunaPesticides, heavy metalsIndicator of soil health and contaminationSoil[44,45]
Mycorrhizal fungiFungiHeavy metals, organic pollutantsIndicator of soil nutrient cyclingSoil[46,47]
Bacteria (e.g., Pseudomonas)MicroorganismsOrganic pollutantsIndicator of organic matter decompositionSoil[48,49]
Collembola (springtails)InsectsPesticides, heavy metalsIndicator of soil structure, biodiversity, and contamination levelsoil[50,51]
Fungi (e.g., Basidiomycota)FungiOrganic pollutionIndicator of organic pollution and soil health through decomposition processesSoil[52,53]
InvertebratesAquatic insectsHeavy
metals,
pesticides		Indicator of
sediment
quality		River
sediments		[54]
Table 2. Compilation of sediment pollution levels according to published studies.
Table 2. Compilation of sediment pollution levels according to published studies.
PollutantType of SitePollution Level (mg/kg)Regulatory Threshold (mg/kg)Reference
Heavy Metals
Lead (Pb)River sediments (urbanised)70–120100[55]
Cadmium (Cd)Lake sediments0.2–0.80.5[56]
Zinc (Zn)Estuary sediments200–300200[57]
Mercury (Hg)Estuarine sediments0.01–0.030.1[57]
Arsenic (As)Lake sediments (mining areas)15–3020[58]
Chromium (Cr)Fluvial sediment50–150100[59]
Copper (Cu)Marine sediments (Türkiye)70–110100[59]
Pesticides
DDTRiver sediments0.02–0.050.01[60]
Polluants Organiques
PAHs (Polycyclic Aromatic Hydrocarbons)Estuarine sediments1.5–3.51.0[57]
PCB (Polychlorinated biphenyls)Urban sediments0.02–0.090.05[61]
Plastic Pollutants
MicroplasticsMarine sediments2.000–5.000 particles/kgN/A[62]
NanoplasticsAgricultural soils50–150 particles/kgN/A[63]
Biological Pollutants
Microbial pathogensAgricultural soils (fertilisers)103–106 CFU/gN/A[64]
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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. https://doi.org/10.3390/ecologies5040040

AMA Style

Ghannem S, Bacha O, Fkiri S, Kanzari S, Aydi A, Touaylia S. Soil and Sediment Organisms as Bioindicators of Pollution. Ecologies. 2024; 5(4):679-696. https://doi.org/10.3390/ecologies5040040

Chicago/Turabian Style

Ghannem, Samir, Ons Bacha, Sondes Fkiri, Sabri Kanzari, Abdelwaheb Aydi, and Samir Touaylia. 2024. "Soil and Sediment Organisms as Bioindicators of Pollution" Ecologies 5, no. 4: 679-696. https://doi.org/10.3390/ecologies5040040

APA Style

Ghannem, S., Bacha, O., Fkiri, S., Kanzari, S., Aydi, A., & Touaylia, S. (2024). Soil and Sediment Organisms as Bioindicators of Pollution. Ecologies, 5(4), 679-696. https://doi.org/10.3390/ecologies5040040

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