Ecological systems are exposed to various types of environmental stresses of different origin and duration (Bengtsson, 2002). Throughout evolution, organisms have developed effective strategies to survive and recolonize environments affected by such events (Egres et al., 2019). However, with increasing industrialization, human society introduced new types of disturbances to which native fauna and flora were not yet able to adapt (Kraft et al., 2015). The overall impact of the perturbation on the local fauna depends on the intensity, character or recurrence of the event, as well as on the actual resilience and stability of the local system and its subsystems. In terms of the recurrence of environmental disturbances, the effect could have an acute character, with a relatively short-term duration, or a chronic character, with more prolonged effects on the local ecosystem. Acute disturbances are usually a part of the system as a natural force for maintaining diversity by creating heterogeneity and new niches (Bengtsson, 2002). Chronic disturbances, on the other hand, are the result of long-term stress on ecosystem structures and are usually of anthropogenic origin, e.g. agricultural practices, climate change, introduction of various pollutants, etc. (Bengtsson, 2002; Höss et al., 2009; Šalamún et al., 2014; Šalamún et al., 2017).
Another important attribute is the rate of degradation/persistence of stressors in the environment. For example, pollutants, such as toxic heavy metals that have no natural degradation pathways, can cause stress for a relatively long time and alter the original structure and functions of the ecosystem (Alexander, 2000; Šalamún et al., 2017). In contrast, organic pollutants are degradable and therefore, at first glance, may not pose much of risk to native soil communities (Alexander, 2000). However, the half-life of degradation of these pollutants can vary from days to decades depending on their structure (molecular structure, functional groups present, etc.) and the general conditions in the soil (Navarro et al., 2007).
Persistent organic pollutants (POPs), including polycyclic aromatic hydrocarbons (PAHs), are compounds that are relatively difficult to degrade and pose a high risk to soil fauna. PAHs are suspected carcinogens and are produced by incomplete combustion of organic compounds, industry, the seepage of crude oil and volcanic activity. (Wang et al., 2007; Net et al., 2015). Their metabolism in soil carried out by living organisms is not always successful due to their resistance, and the transition and biomagnification of these xenobiotics towards the top of the food pyramid can be usually observed (Fig. 1). Therefore, a detailed knowledge of the toxic effects of PAHs at different levels of the food web is necessary to better understand their impact on soil processes and the proper functioning of the soil ecosystem (Langenbach, 2013).
This article provides a comprehensive overview of the different aspects of polycyclic aromatic hydrocarbons (PAHs) as hazardous pollutants with a particular focus on their impact on soil nematode communities, as they represent one of the most important groups of soil fauna and are involved in various soil processes (organic matter degradation, mineralization, pathogens regulation, etc.) and occupy various places in soil food webs (Ferris et al., 2001). The fate, behaviour and toxicity of PAHs in contaminated soils are discussed with particular attention to their direct and indirect effects on these invertebrates and their regulatory functions in soil processes. The relatively small number of publications and the lack of other sources of information focusing on PAHs in relation to soil nematodes suggest that much more attention should be paid to this problem. This article will serve as a valuable source for researchers in the environmental sciences.
This article does not contain any studies with human participants or animals by any of the authors.
Of the various features of soil, its ecology is one of the most vulnerable to pollutants and other forms of disturbances (Bongers, 1990). The actual condition of the soil can be described by the current conditions of soil flora and fauna, which can change under stress. Consequently, native soil communities are carefully studied by scientists seeking an effective tool to indicate soil disturbance. The spatial and temporal heterogeneity of soil provides myriads of habitats for a wide diversity of organisms that depend on each other through their involvement in the nutrient and energy cycling (Bongers & Ferris, 1999). Hence, understanding the structure and function of below-ground food webs in relation to the presence and abundance of their components is a basic requirement for deeper insight into the soil ecosystem. To condense the information and facilitate the interpretation of soil health in relation to the actual state of the soil food web, it is necessary to include as many food web links or functional groups as possible. Since a functional group is not restricted to a phylogenetic unit, representatives of any taxonomic group could be involved in the different functional groups responsible for various soil processes and functions. Nematodes fall into this category; with a wide variety of trophic preferences, life strategies and occupation of important aspects of the food web, their activity affects primary production, decomposition, energy flows and nutrient cycling, especially nitrogen (Bongers, 1990; Van den Hoogen et al., 2020). Furthermore, their high abundance, omnipresence in almost all aquatic and terrestrial ecosystems and good adaptation to a wide range of environmental conditions make them perfect model organisms for environmental assessment (Ferris et al., 2001).
The use of nematodes as soil condition transmitters initially benefited greatly from the mass of available information for plant-feeding nematodes as important agricultural pests (Bongers & Bongers, 1998). After gaining a deeper insight into nematode communities, scientists found that nematodes are one of the most important taxa in the soil ecosystem. Their distribution across different levels of the food web secure a relatively fast and stable response to a new food resources and changing environmental conditions, making them a suitable tool for the evaluation of soil conditions (Bongers & Bongers, 1998). Functional indices have been developed as a practical and effective tool not only for assessing the nematode community structure, but also for indirectly assessing the stability and health of the whole soil ecosystem. Using these new indication tools, soil scientists are able to look more closely at the responses of soil ecosystems and predict the possible pathways of their future development under the effect of compaction, acidification and the decline in soil fertility caused by toxic substances and erosion (Ferris et al., 2001; Hlava et al., 2017).
The main focus of indication capabilities in relation to soil nematodes has been on the effects of heavy metals (Georgieva et al., 2002; Šalamún et al., 2012), even though organic pollutants have also been introduced into the soil in large amounts. Although they are probably more of an acute disturbance to soil fauna and flora, their long-term introduction into the soil could pose a serious threat to the diversity and further development of the soil environment.
Polycyclic aromatic hydrocarbons (PAHs) enter the environment either from natural sources, e.g. plants, termites or early stages of diagenesis (Wilcke et al., 2000), or from anthropogenic sources and accidental spills. Production from more recent sources, such as combustion, transportation, oil or the wood processing industry is more important for the amount and variability of PAHs released. These contaminants are widespread in all components of the environment, including air, water, sediments and soil (Höss et al., 2007; Höss et al., 2009), and have been detected around the world from tropical to polar regions, even at sites far from industrial activities (Kuppusamy et al., 2017). PAHs are an important group of organic pollutants containing two or more unsubstituted benzene rings fused together when a pair of carbon atoms is shared between them (Duan et al., 2015). There are several hundred variants of PAHs, but only 24 compounds (shown in Fig. 2) have been preferentially monitored (Lerda, 2011). Depending on their molecular weight, PAHs are split into light molecular weight PAHs (LMW), which have 2 – 3 benzene rings, and high molecular weight PAHs (HMW) having 4 – 7 rings. LMW PAHs, such as naphthalene, fluorene or anthracene, have a shorter persistence in soil compared to the more recalcitrant and carcinogenic HMW PAHs, mainly due to their higher solubility, volatility and lower hydrophobicity (Duan et al., 2015; Kuppusamy et al., 2017). The higher hydrophobicity of HMW PAHs results in their higher tendency to be absorbed by the soil’s organic matter. Therefore, HMW PAHs, due to higher possible toxicity, low bioavailability and recalcitrance, represent 80 – 90 % of weathered PAHs in soils globally (Okere & Semple, 2011; Kuppusamy et al., 2017).
Soil appears to be the final deposition site for PAHs (> 90 % of total PAHs in the environment), with atmospheric deposition being the major pathway of entry (Agarwal et al, 2009). Depending on the nature of the PAHs, they can be eliminated from the soil by a number of physico-chemical and biological processes or leached into deeper soil layers including groundwater (Okere & Semple, 2011). The rate of PAHs degradation depends on numerous factors, e.g. soil properties (the redox-potential, organic matter and mineral content, temperature, moisture), individual PAHs properties (biodegradation half-life, toxicity, bioavailability) and the presence and activity of degrading soil organisms (Reid et al., 2000). The pace and extent of PAH degradation decreases over time. This is especially true for clay soils and soils with high organic matter content, where PAHs may be unreachable for biodegradation through sequestering into organic matter or diffusion into micropores (Okere & Semple, 2011). Thus, the bioavailability of PAHs to microorganisms represents a crucial factor for soil restoration and, at the same time, the most important way to remove PAHs from soils (Kuppusamy et al., 2017).
The interstitial life strategy (among soil particles) of nematodes gives them a unique ability to reflect direct and indirect influence of toxic organic compounds on the soil environment.
The most important factor for the degradation of PAHs in freshly contaminated soils is their hydrophobicity. The more soluble nature of LMW PAHs and their often higher concentrations in soil solutions compared to HMW PAHs influences the interstitial mesofauna directly through oral or transcuticular nutrient intake (Kammenga et al., 1994). Nematodes that are sensitive to toxicants (e.g. predators or omnivores) and have a relatively permeable cuticle are exposed to this risk immediately after the introduction of PAHs into the soil ecosystem. On the other hand, representatives of stress-resistant nematode genera (e.g. mostly bacterivores and fungivores) may benefit from the introduction of PAHs through, for example, a decrease in predation pressure or an increase in available food resources. The shift towards stress-resistant species in the nematode community structure has been well documented by Moreno et al. (2009) and Soto et al. (2017) in localities heavily polluted with PAHs, where nematode genera well-adapted to disturbed conditions significantly dominated. The replacing of sensitive nematode species by resistant ones can affect the food web from both bottom-up (food availability, overpopulation, etc.) and top-down effects (predation, pests’ control, etc.) and ultimately result in a lower ecosystem biomass despite constant population densities (Soto et al., 2017). Chen et al. (2009) also observed the decline of the environmental maturity level and simplification of the soil food web under the higher pressure of PAHs contaminants in the soil.
The toxic effect of contaminants on nematodes, which have a relatively permeable body surface may be reinforced by ingestion of food containing risky substances. Except omnivores and nematodes that consume the soil substrate itself, such as some diplogasterids, or
On the molecular level, PAHs induce multiple detoxification responses in nematodes, including the expression of cytochrome P450 genes responsible for the detoxification of xenobiotics. A concentration-dependent relationship was found between the intensity of expression of these genes and the benzo(a)pyrene added to the soil (Menzel et al., 2005). An even stronger induction of the P450 genes family was found in the use of fluoranthene (Menzel et al., 2001). Saint-Denis et al. (1999) pointed out that benzo(a) pyrene may also be activated by cytochrome P450-independent metabolic pathways. Alternative metabolic pathways of PAHs may include the generation of free radicals or the formation of reactive oxygen species as metabolic by-products, leading to oxidative stress (Penning, 2014). Wu et al. (2015) came to a similar conclusion in their study on oxidative stress in
The introduction of PAHs into an ecosystem can indirectly cause both positive and negative responses in nematode communities. The positive effects can be channeled through the ability of bacteria and fungi (decomposers, primary food sources for nematodes) to utilize various PAH compounds, including the most common PAHs – naphthalene, phenanthrene and pyrene – as sole carbon sources (Duan et al., 2015). This process is primarily controlled by the bioavailability of these compounds to microorganisms, even without the need for PAHs to be present in the soil solution (Alexander, 2000; Zhang et al., 2012). Depending on the nature of the PAHs introduced into the soil ecosystem and the decomposer channels used for their breakdown, soil communities respond distinctively by changes in the internal structure of their community. Bacteria can use LMW PAHs as a direct source of energy (Sack et al., 1997), but only fungi are able to degrade HMW PAHs, despite their recalcitrant and hydrophobic nature (Cerniglia, 1992). The increase of decomposer populations (bacteria and fungi) in the soil may act as a
Apart from this, the grazing of bacterivores keeps the population of soil bacteria at a reasonable level, thus preventing the inhibition of their growth caused by substrate shortage or the accumulation of toxic metabolites originating from the degradation. On the other hand, Näslund et al. (2010) found in marine sediments that, in the case of higher mesofaunal densities, naphthalene mineralization, as well as, the number of naphthalene-degrading bacteria, decreased. However, the authors pointed out that this phenomenon could be due to the higher predation pressure during the experiment in combination with significantly different bacterial diversity in treatments with different mesofaunal abundances.
The negative effects of PAH contamination on nematodes may be reflected, for example, in the availability of suitable microhabitat conditions. Given that the distribution of nematodes in the soil is largely dependent on their feeding habits and body size (Blakely et al., 2002), the intra-aggregate pore space could be an important determining factor for nematodes distribution. Therefore, increasing the bulk density of the soil by tightly bind PAHs to soil particles could significantly alter the actual conditions of microhabitats. This change may be a significant barrier to large-sized nematodes (e.g. Dorylaimida, or other omnivores and predators) using the intra-aggregate space as a refuge from other predators, or as a preferential place for reproduction and development (Briar et al., 2011). The decrease in soil pores diameter also means less oxygen and nutrient transportation through the soil microhabitats (Blakely et al., 2002). A lack of nutrition flow and suitable habitats for larger nematodes could lead to their decrease in the soil community. As larger nematodes represent mainly omnivores and carnivores, their decrease may significantly influence the top-bottom pressure in the habitat (Blakely et al., 2002; Sun et al., 2017). Nevertheless, Snow-Ashbrook and Erstfeld (1998) reported high abundance of omnivores/carnivores accompanied by a slight stimulatory effect of PAHs on the overall invertebrate community. Even though the genuine reason for the increased occurrence of sensitive nematodes in the most contaminated plots could not be explained from the study, Erstfeld and Snow-Ashbrook (1999) hypothesized that bottom-up effect regulation by the stimulated microflora, together with physico-chemical characteristics (organic carbon, soil moisture, pH and grain size) at the study sites, may play the key role.
As a result of rapidly growing urban land use, traditional agriculture or industrial activities, the environment is exposed to a variety of pollution discharges. With such pollution, environmental managers and decision-makers need a tool to better understand and manage the acute and chronic impacts on the local environment to protect, clean-up and restore it. The realization of the need to protect and restore affected ecosystems has led to a search for suitable environmental indicators. One possible option to distinguish affected soil ecosystems is the use of native soil communities that are able to reflect trends following contamination by various pollutants, including PAHs. Based on the literature collected, we have identified several research fields that could improve soil monitoring using native soil nematode communities in the future.
In the toxicological data collection and assessments of the impact of soil contamination, toxicological tests predominantly rely on a single-species laboratory test. For nematodes, the
As shown above, the outcomes of experimental studies can sometimes contradict each other, which means that no clear and relatively reasonable conclusions can be drawn about the impact of pollutants on nematodes. To obtain clear results under laboratory conditions, concentrations of pollutants beyond compare with real field conditions are often used. High levels of contamination indeed have an acute impact on nematode community structure, but this represents only a relatively short and partial effect of contaminants on the soil ecosystem, while contaminants availability in the system is still relatively high. On the other hand, the chronic phase lasting much longer (superseding the acute phase, when the availability of contaminants drops to a certain level) has possibly a stronger effect on the nematode community structure. In this phase, contamination does not shape the community directly but rather indirectly influences various physiological and behavioural aspects of nematode life.
Another problem closely associated with the chronic effects of contamination is the duration of exposure. Under controlled conditions, nematodes are exposed to pollutants for days or weeks, usually capturing the reaction of mostly a few following generations. The subacute exposure to foreign compounds leads to a transgenerational changes in nematode fitness (Yu & Liao, 2016). The induced multigenerational effects include additional mechanisms (cumulative damage, acclimatization, adaptation) that shape the nematode community and divert the direction of its development from that expected. Therefore, it is essential to consider the multigenerational effects to highlight the possible impacts of contamination over multiple generations and to include them in development predictions.
Although the understanding of soil ecosystem functioning has improved significantly in the last decades, due to the high heterogeneity and dynamics of the soil ecosystem and the absence of baseline input data, comparison and evaluation is often a challenge. One step towards improving the robustness of the experimental data obtained and the applicability of nematodes as a tool for bioindication of soil stress is the harmonization of different methods and approaches used in ecological studies of ecosystem pollution. Obstacles to harmonization of biological methods often lie in the requirement for “fresh” samples of nematode communities for analyses and the lack of reference control material as a data source (Faber et al., 2013). Therefore, standard methodological approaches, as can be found in other scientific fields, are usually not applicable in the field of soil biology. Instead, the way to compare the relative efficiency and reliability of different biological methods is in their application under the same experimental conditions, i.e. concurrently on the same set of plots or samples. The harmonization step is necessary as part of the effort to achieve standardized methods at national and international level and to make progress in the use of native soil indicators in actual monitoring.
Another issue hampering the engagement of nematodes in soil monitoring is the extremely time consuming taxonomic determination using traditional morphological methods (Donn et al., 2012). However, the recent increase in the development and use of molecular approaches, which are capable of processing large numbers of samples with high sensitivity in a relatively short time, should reduce the difficulties of identification based on morphology alone (Stone et al., 2016). The low resolutions of morphological methods often led to misconceptions in taxa distribution, through numerous cryptic species that are relatively site specific (Taylor et al., 2006). These subtle differences ultimately resulted in the incorrect assessment of the nematode community structure as well as an inability to recognize the uniqueness of each community and its proper reactions towards environmental conditions or stress (Stone et al., 2016)
However, it should be noted that molecular methods are still under development and may not currently be able to fully incorporate nematode identification and generate accurate representations of nematode community diversity in a single step. Therefore, it is necessary to employ more than one technique to obtain valid results (Lott et al., 2014). Stone et al. (2016) suggested that methods such as T-RFLP, which allow for quick but rather coarse analysis of large sample sets, could act as a sieve for selecting those to be analyzed in more detail at a later stage using additional methods. The main advantages of this approach lie in using rapid and cost-effective screening platforms without the considerable data processing and storage space requirements of most next-generation sequencing technologies, while yielding comparable resolution of community structure (Pilloni et al., 2012). Rapid analysis opens up the possibilities of studying nematode assemblages and their spatial and temporal dynamics in sample-intensive studies not only in polluted soils, but also in natural or disturbed soils and in different agricultural environments. Although the entire nematode community is used in soil monitoring, for specific purposes, these methods are able to restrict the analysis to groups of interest or to be expanded and applied to the entire food web or eukaryotic faunal community of the soil (Donn et al., 2012).
PAHs are an important class of environmental pollutants generated by both natural and anthropogenic processes. The importance of soil as a primary sink of PAHs means that they interact with soil and its constituents, leading either to their stabilization and persistence in the soil profile or to their loss, depending on the particular physical, chemical and biological conditions of the soil. Therefore, understanding the interactions between PAHs and soil should be one of the most important challenges in studying the impacts of organic pollutants in the soil environment. As this review shows, soil scientists are not always able to identify the negative impacts of PAHs on nematode communities, although many studies have observed negative effects on nematodes, including retarded development, reduced reproduction or activation of detoxification pathways in nematodes physiology. The ability of different nematode taxa to cope with the presence of contaminants in the soil usually results in altered species composition, which could significantly influence interactions within the nematode communities and interactions among other important soil taxa. The direct and indirect implications of soil contamination are that pollutants may be one of the driving forces of changes in the soil ecosystem, which could ultimately result in the alteration of entire communities and subsequently the entire ecosystem. Therefore, systematic and cost-effective monitoring of affected areas would greatly improve the possibilities of preventing negative developments in the soil ecosystem. This goes hand in hand with new techniques that open up new possibilities in analyzing large quantities of samples with relatively good resolution and will make it possible to detect threats more quickly and precisely.
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