Résumé

Cet article a examiné les articles publiés sur l'utilisation des arthropodes de la litière et du sol comme indicateurs biologiques de la qualité des sols depuis les années 1970. Notre revue montre que les arthropodes de litière et du sol sont des transformateurs de litière et des ingénieurs d'écosystèmes. Ils contribuent à la disponibilité de la matière organique. Leur diversité, leur abondance, leur biomasse et leur densité sont des mesures appropriées pour l'évaluation des effets naturels et / ou anthropiques sur le sol. Cependant, leur utilisation est remise en question par des difficultés dans les méthodes d'échantillonnage et l'identification de la diversité des arthropodes de la litière et du sol au niveau de l'espèce, et peu de projets de recherche combinent à la fois des facteurs abiotiques et biotiques. Nous recommandons que d'autres recherches explorent les méthodes les plus appropriées pour échantillonner les arthropodes de la litière et du sol et créent une classification des groupes dominants jusqu'au niveau de l'espèce qui, avec l'utilisation de méthodologies intégratives, constitueront des étapes précieuses vers une méthode généralisée et acceptée pour l’évaluation de la qualité du sol.

Abstract

This article reviewed published papers on the use of soil and litter arthropods as biological indicators of soil quality since the 1970s. Our review shows that soil and litter arthropods are litter transformers and ecosystem engineers. They contribute to the availability of organic matter. Their diversity, abundance, biomass, and density are suitable measures for the assessment of natural and/or anthropogenic effects on soil. However, their use is challenged by difficulties in sampling methods and the identification of soil and litter arthropod diversity up to species level, and few research projects combine both abiotic and biotic factors. We recommend further research to investigate the most suitable methods for sampling soil and litter arthropods, and create a classification of dominant groups up to species level which, along with the use of integrative methodologies, will be valuable steps towards a generalized and accepted method for the assessment of soil quality.

INTRODUCTION

1Soil is an integral component of ecosystem processes and biogeochemical cycles, comprised of solid, liquid and gaseous components which interact through a multitude of interrelated physicochemical and biological processes (Zornoza et al., 2015). Soil is a key resource for agriculture production and is a source of nutrients required for plant growth (Tsiafouli et al., 2015).  Soil is also the foundation and the essence of all terrestrial life (Lal, 2015). In relation to biodiversity, soil is inhabited by a range of organisms including fungi, algae, bacteria, protozoa, and invertebrates (Koehler, 1992), with soil and litter arthropods representing as much as 85% of all soil fauna (Culliney, 2013).

2Through history, soil has been essential to human well-being, and human dependence on soil is direct due to its contribution to food production and importance for economic development (Lal, 2015). However, intensive exploitation of soil can cause considerable decline in soil quality (Eswaran et al., 2016). Current estimations show that soil degradation affects around 33% of all soils in the world (FAO, 2017), and has strong consequences on soil ecosystem services and biodiversity conservation due to changes in the concentration of nutrients, loss of soil organic carbon, pollution, loss of soil biodiversity, wind and water erosions, desertification, acidification, salinization, increased greenhouse gas emissions, reduced water infiltration and purification, and perturbations of hydrological cycles (Zornoza et al., 2015).

3Although some authors consider soil quality to refer to soil functions while soil health represents the finite nonrenewable and dynamic living resource (Doran & Zeiss, 2000), soil quality and soil health are often used interchangeably and are defined as the ability of a specific soil to function within its capacity and within natural or managed ecosystem boundaries, to sustain productivity of plants and animals, maintain water and air quality, and support human health (Arshad & Martin, 2002). However, soil quality assessment has long been a challenging issue because soil presents high variability in properties and functions, and globally acceptable methodologies for assessing the soil quality are not yet in place (Laishram et al., 2012).

4The assessment of soil quality has long been based on various biological indicators (Vasconcellos et al., 2013), including indicators of biotic or abiotic conditions, indicators of various human activities (Basedow, 1990), or goal parameters deducted from nature conservation aims and translated into measurable factors such as species diversity (May, 1995). The use of soil invertebrate community as an indicator of soil quality has received more attention in recent years and soil mesofauna are the most studied organisms in soil quality assessment (Lavelle & Spain, 2001). Currently, the focus is on soil and litter arthropods (Bagyaraj et al., 2016), although little is known about the advantages and challenges of using these organisms in assessing soil quality.

5This paper reviews the use of soil and litter arthropods as biological indicators of the soil quality under forest plantations and agricultural lands. The focus on these land use is motivated by the fact that forest plantations become common landscapes across many parts of the world occupying around 264 million of hectares (7% of the total global forest area) (Jürgensen et al., 2014), while agricultural lands occupy around 1.6 billion of hectares (12%  of global land area) (FAO, 2011). Planted forests serve to restore degraded lands, to control soil erosion (Mishra et al., 2003), and together with natural forests, they provide benefits to human society such as timber, food, fuel wood, medicinal resources, opportunities for recreation, climate regulation, soil and water protection, biodiversity preservation and carbon sequestration (Campos et al., 2005; Dyck, 2003), while agriculture is the main source of food and money for humans (FAO, 2011).

6This review starts with a review of classical methods for soil quality assessment in forest plantations and agricultural lands, continues with a review of the dominant soil biodiversity of arthropods, their role in maintaining soil quality, and types of measures of soil and litter arthropods indicating soil quality. It concludes with recommendations on how soil and litter arthropods can be effectively used as biological indicators of soil quality.

LITERATURE

Classical and recent measures for soil quality assessment

7Quality of an indicator must correlate well with ecosystem processes, integrate soil physicochemical and biological processes and serve as basic inputs needed for estimation of soil properties or soil functions which are more difficult to measure directly (Doran & Safley, 1997). Furthermore, according to the same authors, an indicator must be relatively easy to use under field conditions and be assessable by both specialists and producers, be sensitive to variations in management and climate, and be components of existing soil data bases where possible. The need for basic soil quality and health indicators is reflected in the question such as: what measurements should I make or what can I observe that will help me evaluate the effects of management on soil function now and in the future (Doran & Safley, 1997)?

8Soil quality is assessed by considering soil properties that are sensitive to changes in land use (Andrews et al., 2004), and it has long been assessed by measuring physicochemical attributes (Table 1). The most commonly measured parameters include soil organic carbon and total nitrogen, soil pH, electrical conductivity, available nutrients, bulk density, and soil aggregation (Zornoza et al., 2015). In other studies, the choice of soil quality indicator considered land use and land management (Laishram et al., 2012) due to the interconnections of soil quality with other ecosystem components such as soil fertility, soil productivity and vegetation type (Doran, 2002).

9Table1: Soil physicochemical indicators for screening the condition and quality of soil (Adapted from: Doran & Parkin, 1994; Laishram et al., 2012; Cardoso et al., 2013).

10In agricultural systems, soil organic carbon has been used as the most important indicator of soil quality (Arias et al., 2005), as well as soil pH, electrical conductivity, and nutrient availability (Rahmanipour et al., 2014). Physical indicators are the most commonly used with the measurement of aggregate stability and bulk density (Rouseau et al., 2013). Soil microbial activity and diversity (Table 2) are also often used (Li et al., 2014), as they are more susceptible and can therefore clearly indicate changes in the environment more responsively than physicochemical attributes (Masto et al., 2009). Due to agricultural economic development, soil quality in agricultural lands can also be assessed using measures of crop productivity (Zornoza et al., 2015) and direct or indirect impacts of soil degradation on human health (Deng, 2011).  

11Table 2:Microbial indicators of soil quality: soil cycles they are involved in, and methods for assessment (Adapted from: Doran & Parkin, 1994; Cardoso et al., 2013).

12Researchers have applied biochemical indicators to assess soil quality (Table 3). Simple ratio measures including C:N ratios, metabolic quotient, enzyme activities/microbial biomass ratios, fungal/bacteria biomass ratios, soil organic carbon and nitrogen stratification ratios were commonly used (D’Hose et al., 2014; Zhao et al., 2014). Ratios are considered more effective than physicochemical and microbiological indicators for the assessment of soil quality in forest plantations due to their high correlations with soil organic carbon and higher response to changes in soil use and soil management (Miralles et al., 2009).

13Table 3: Enzyme indicators of soil quality and functions played in soil cycles (Adapted from: Cardoso et al., 2013).

14Recently, more emphasis has been given to soil fauna as indicators of soil quality in forest and agricultural land use (Eggleton et al., 2005). Their diversity, abundance, biomass, and density have been proven to be suitable indicators of natural or anthropogenic impacts on terrestrial ecosystems due to their correlation with physicochemical and microbiological properties and ecological changes (Paula et al., 2010). Soil fauna produce galleries, pores, and tunnels in soil that facilitate the flow of air and water in soil (Lavelle et al., 2006). Soil fauna are good decomposers of organic matter and participate in nutrient cycling (Moore & De Ruiter, 1991). The aggregation of soil particles and litter feeding processes enhance soil structures and accelerate dynamic production of organic matter through mineralization processes (Barrios, 2007).

15Protozoans, nematodes, and annelids are soil fauna of great importance in maintaining soil quality. Protozoans participate in the stimulation of mineralization of organic matter through microbial activities (Moore & De Ruiter, 1991). Nematodes including oligochaetes and enchytraeids are good litter transformers, and through their pellets, mineralization is enhanced in a short time, while annelids including earthworms are good ecosystem engineers, participating in the production of organomineral structures and formation of soil pores (Lavelle, 1996). The role of structures created by earthworms are essential to soil ecosystems as they offer the mineralization of C and N, denitrification, and facilitate water and air infiltration (Lavelle et al., 1997).

Soil arthropods and their role in maintaining soil quality

16Major groups of soil and litter arthropods including Acarina, Collembola, Myriapoda as well as various orders of the class Insecta are of significant importance in terrestrial ecosystems (Ogedegbe and Egwuonwu, 2014). They are recognized for their active role in organic matter decomposition, nutrient cycling, agricultural productivity, plant growth and improving physicochemical and biological soil conditions (Vasconcellos et al., 2013). By their digestive actions, soil and litter arthropods form stabilized aggregates and decompose resisting chemical substances, thereby improving nutrient availability for plants and microorganisms (Lavelle, 1997). Saprophagous arthropods affect decomposition through feeding on litter, mixing litter with soil and through the regulation of soil microflora (Suift et al., 1979).

17The class Insecta is the most dominant of all soil and litter arthropods. It is very diverse and highly susceptible to changes in soil characteristics, making it a good indicator group. The order of Diptera is among these insects. The main natural environmental factors affecting the distribution of Diptera are the inputs of dead organic matter into soil, changes in soil moisture content, litter depth and temperature as well as seasonal variation, and for agricultural systems, tillage, use of manure, fertilizers, and pesticide (Frouz, 1999). The community of soil-dwelling Diptera can serve as indicators of soil quality and environmental stress through an assessment of their distribution and abundance of their species in the community (Krebs, 1989). Lower taxonomic levels such from species to families are recommended to be used in this assessment (Frouz, 1999).

18Soil termites also form a very important group of the class Insecta, used as indicators of soil quality due to their effects on soil profiles and soil texture, distribution of organic matter, and plant nutrients and their construction of subterranean galleries (Stork & Eggleton, 1992). Termites’ foraging and activities create conditions promoting microbial populations and the mineralization of organic compounds (Culliney, 2013). Soils modified by termites showed higher microbial activity and were significantly more concentrated in ammonium, calcium, magnesium, and potassium cations and inorganic phosphorus (Ndiaye et al., 2004), available phosphorus, total nitrogen, bicarbonates, chloride and sulfate anions (Badawi, et al., 1982). The reduction of C:N ratios by fungi provide organic matter enriched in nitrogen to termite colonies and, by feeding on fungi, nutrients from the litter are incorporated into the biomass of termites with highly efficient assimilation of nitrogen (Lee, 1983).

19Hymenoptera, particularly ants, form another dominant group of the class Insecta in most terrestrial environments (Culliney, 2013). Mounds of ant species contain higher exchangeable cations including calcium, magnesium, potassium, sodium cations, and they are rich in trace elements including iron, manganese, and zinc (Wali & Kannowski, 1975). Ant mounds also contain higher concentrations of nitrate and ammonium salts (Amador & Görres, 2007), available phosphorus and potassium and showed higher levels of microbial activities than in uninhabited control soils (Czerwiński et al., 1971). The increase in soil nutrient and soil organic matter content in ant mounds are factors influencing the variation of soil pH (Frouz & Jilková, 2008).  

20In habitats with high anthropogenic activities, Coleoptera insects including carabid beetles are good indicators of changes in soil properties (Kromp, 1999), namely pH, sodium chloride levels and calcium content (Avgan & Luff, 2010). For sustainable agricultural systems, carabid beetles play the role of predators and prevent outbreaks of several pest insects (Luff, 1996). Scarabaeidae beetles are important in the breakdown of dung, carrion and leaf litter, and return nutrients to the soil (Greenslade, 1985). Communities of staphylinid can be used as bioindicators of human influence on soil ecosystems (Bohac, 1999), through the use of species diversity indices, and individual relative abundance in the sample (Ruzicka & Bohac, 1994).  

21Besides insects, collembolans form another group of soil and litter arthropods used as indicators of soil quality. They contribute to the decomposition of plant residues, increase mineralization by selective feeding on fungi, and help in the formation of humus by mixing organic material and mineral soil particles (van Amelsvoort et al., 1988). They form water-stable aggregates in the soil and strong inter-particle cohesive forces within fecal pellets (Siddiky et al., 2012).  Stimulatory effects of collembolans on fungal growth and respiration through grazing (Filser, 2002) results in mobilization of available nitrogen and calcium in soils (Ineson et al., 1982), and their feces contain more nitrate ions, increasing their availability on the forest floor (Teuben & Verhoef, 1992).

22Another group of soil and litter arthropods of interest in the assessment of the soil quality is Isopoda. They are sensitive to the application of pesticides and herbicides which can cause a rapid decrease of these soil and litter arthropods in intensively managed agricultural and forest plantations (Fischer et al., 1997). Isopoda biomass contributes to the storage of potassium, sodium, phosphate ions, and nitrogen and calcium ions in soil (Teuben & Verhoef, 1992). They constitute an important nutrient pool which immobilizes ions and prevents leaching from the soil (Zaady et al., 2003). Due to their tolerance to high-level metals, Isopoda indicate soil contamination by heavy metals especially copper (Hopkin et al., 1993), zinc, lead and cadmium (Prosi & Dallinger, 1988).  

23Soil quality assessment has been also done using mites, which are among the most species-rich and numerous soil and litter arthropods, having a positive influence on the decomposition rates of organic matter, bacterial and fungal colonizers. They produce fecal pellets which enhance further decay and contribute to improved soil structures by assisting the distribution of bacterial and fungal propagules through the soil and leaf litter (Maraun et al., 1998). In agricultural lands, the processes of cultivations, rotations, monocultures, and application of pesticides are the activities with negative effects on the community of mites (Tomlin & Miller, 1987). Mites give good results of soil status once the cause of the change in soil properties is known in advance (Linden et al., 1994).

24Diplopoda and Symphyla, the most important myriapods in soils, form another group of soil and litter arthropods used in the assessment of soil quality. They influence the distribution of microbial populations in soil (Szabó et al., 1983) and participate in the decomposition of plant material, which increases nutrients on the surface area and makes them available for bacteria and fungi (Paoletti et al., 2007). Diplopoda and Symphyla contribute to the decomposition of leaf litter by fragmentation and the addition of microflora through fecal pellets, and they release mineral nutrients into the soil by feeding and defecation which is essential for soil as this brings down C:N ratios. Furthermore, their feces have a relatively high pH which facilitates the growth and concentration of nitrogen-fixing bacteria (Bagyaraj et al., 2016).  

Types of measures of soil and litter arthropods indicating soil quality and their challenges

25Many soil and litter arthropods including collembolan, Oribatida, Isopoda and Diplopoda live a rather sedentary life and therefore reflect local conditions of a habitat (Van Straalen, 1998). These facts have been recognized for a long time, and relationships between soil types and soil and litter arthropods have been established in various studies (Rusek, 1989). Use of soil and litter arthropods as indicators of soil quality has commonly been done by measuring soil and litter arthropod biomass, density, abundance, species richness, and biological indices (Yeates & Bongers, 1997; Foissner, 1994) of either single taxon groups (Santarufo et al., 2012), or of the entire community (Aspetti et al., 2010).  

26Recently, a simplified ecomorphological index (EMI) based on the morphology of micro-arthropods has been introduced (Parisi & Menta, 2008). It is used to evaluate soil quality based on which groups are present in soil samples, where taxonomic groups receive an EMI score from 1 to 20 (Table 4), according to its adaptation to the soil environment. Deep soil living forms are given an EMI score of 20, intermediate forms are given a score proportional to their degree of specialization, while surface-living forms are scored with an EMI equal to 1 (Parisi et al., 2005). The Biological Quality of Soil Index (BQS) is calculated as the sum of EMI scores and soil quality correlates with the number of groups of arthropods with high EMI scores.

27Table 4:Ecomorphological indices (EMIs) of edaphic microarthropod groups (Adapted from: Parisi et al., 2005).

28However, a true theory of community composition of soil and litter arthropods in relation with other environmental factors still remains to be developed. Although diversity indices represent variables that can be measured independently of the difficulties involved in identification of soil and litter arthropods at species level, these measures represent a snapshot in time (Anderson et al., 1985). They give little information about the community structure, and changes in abundance can be related to other factors such as predation, grazing and mutualistic relationships. They can also be related to other abiotic and biotic factors (King et al., 1985), including climate variability and climate change, variations in temperature, moisture, soil salinity, soil pH, the type of vegetation, and land use (Schils et al., 2006).

29These are the reasons why measuring abundance, biomass, density, diversity and evenness is not enough for assessing the status of soil arthropods and hence soil quality. Some other factors including the relationship between biological parameters (species composition, life history diversity, feeding type and physiotype) and environmental parameters (soil type, microbial populations, soil pH, humidity, temperature, nutrients, heavy metals and pesticide residues) have to be studied (Van Straalen, 1998). Functional significance including fragmentation, soil aggregation, organic matter and nutrient distribution, mineralization rate, and nutrient mobility (Table 5), as well as spatial and temporal scales, have to be considered (Bagyaraj et al., 2016).

30Table 5: Classification of soil fauna according to their size and function (Adapted from: Schjønning et al., 2004; Faber, 1991).

31*Mites (Acari); spring tails (Collembola); **Spiders (Arachnida), Millipedes (Diplopoda); Termites (Isoptera); Slater (Isopoda); Centipedes (Chilopoda); Ants (Hymenoptera; and Beetles (Coleoptera).  

32Variations of soil and litter arthropods in samples may also depend on the sampling method used (Ferrer-Paris et al., 2013). Berlese-Tullgren funnels, pitfall traps, hand collection and Winkler extraction are the most used sampling methods for soil and litter arthropods (Tuf & Tvardik, 2003). However, less is known about the relative trapping efficiency of each of these sampling methods (Krell et al., 2005). The knowledge of the taxa that are most likely collected by each sampling method and the sampling method likely to collect the highest diversity of soil and litter arthropods remain the topic of interest, which has to be studied before generalization of any sampling-dependent findings (Sabu & Shiju, 2010).

CONCLUSIONS AND RECOMMENDATIONS     

33Even though community indicators meet most of the desired parameters to determine soil quality in the habitat under investigation, many other interesting criteria must be met, including soil physicochemical parameters, types of vegetation, soil microbial communities and enzymes (Van Straalen, 1998), soil ecological functions (Laishram et al., 2012) including availability of soil nutrients and soil structures (Culliney, 2013). Changes in these parameters may have varying effects on diversity and abundance of different species of soil and litter arthropods (Lavelle et al., 2006), so that the relationship between soil and litter arthropod biological parameters, and soil ecological functions played by soil and litter arthropods (Table 5) have to be studied (Cardoso et al., 2013) before making a general conclusion on soil status.

34Further research should explore the effect of combinations of various sampling and measuring methods. If both species diversity and abundance have to be used for assessing soil quality in different land use, we recommend that they be used together with other physicochemical parameters of soil, microbiological communities and enzymes as well as environmental factors such as seasonal variability and altitudinal variations (Sicardi et al., 2004). These studies should focus on the identification, comparison and testing different sampling methods for sampling soil and litter arthropods and the development of a hierarchy classification system up to species level for dominant soil and litter arthropod species. From our review, we propose that these steps could lead to a generalized and accepted approach for soil quality assessment using soil and litter arthropods.  

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