1. Quality Concept

Soil, water, and air quality are the components of environmental quality, but if we focus explicitly on soil resources, the quality is more complex to define due to its variety of components ^[1], and the enormous amount of interrelationships between its components. Chemical, physical, and biological parameters can be analyzed and integrated to form a soil quality index that allows comparisons between different uses or management practices ^[2]. Soil quality is usually focused on agricultural production ^[3], but is also a critical component in the maintenance of sustainability ^[4], and human and environmental health ^[2]. A soil’s quality is defined “as its ability to function within an ecosystem; to sustain or improve animal or plant productivity; to maintain and control environmental quality, and to support the habitability and health of man” ^[5].

The biological component is of great importance in assessing the management of land uses. This allows the implementation of agro-ecological management that favors agricultural production and biodiversity ^[4]. Some authors consider that for a soil to be considered high quality, it must meet criteria related to respiration, biomass, and its microbial activity ^[6], which correspond to biological parameters.

From a general point of view, the quality of the soils of the Ecuadorian Amazon is marked by fine clay textures, with good granular structure, on the surface horizon ^[7]. It has high OM content of low quality, low fertility, and acidic pH that limit the availability of nutrients, such as phosphorus and leaching of changeable bases (potassium, calcium, and magnesium), limiting its use ^[8][9][10]. A very thin superficial horizon with intense biological activity due to the accumulation of OM, and the presence of humidity, influences biogeochemical behavior ^[11]: phosphorus deficiency, the presence of sulfur, changeable bases ^[7][11], and high levels of iron and aluminum fixation ^[12]. As phosphorus is a critical macronutrient ^[13], low levels of native phosphorus represent one of the biggest obstacles to food production. In general, the dark colors on the ground are associated with OM and high biological activity ^[10], and reddish colors are associated with ferric minerals ^[9][14]; a characteristic behavior of Amazonian soils.

Consequently, when talking about soil quality, the most important thing is to know if the focus is from the point of view of agricultural productivity, or environmental or human health. In addition, the quality can refer to the physical, chemical, or biological components of the soil. It is much more frequent that indicators are considered for the evaluation of the quality of the soil. In the context of the Amazon, biological indicators or bioindicators are very useful.

2. Indicators

An indicator is a parameter that allows for the verification of the soil’s situation in relation to its state of conservation, pollution, productivity, or any other characteristic that provides information regarding its current and potential status ^[1][8][15]. These indicators are classified into four categories: visual, physical, chemical, and biological indicators to assess the quality of a soil ^[4].

Visual indicators are obtained with field visits, farmers’ perceptions, and local knowledge. These are based on observations and interpretations, such as the exposure of the subsoil, the color of the soil, the presence of gullies and weeds, the flooding, runoff, or poor vegetation development—all of these aspects are indications of alterations in soil quality ^[1][16][17]. Physical indicators are related to the structure of the soil, as is the case for porosity, bulk density, penetration resistance, water retention capacity, hydraulic conductivity, aggregate size, depth, and texture. These mainly reflect the limitations of root growth, seedling sprouting, infiltration, or movement of water within the soil profile, transfer and cycling of nutrients ^[4][16]. Chemical indicators include soil–plant properties, such as water quality and the availability of water, and nutrients for plants and microorganisms. Among the most common are pH, electrical conductivity, organic matter content, cation exchange capacity, and nutrients (total N, total phosphorus and potassium) ^[1][4][12].

Finally, biological indicators are related to the decomposition and incorporation of animal and plant residues in the soil by living organisms, controlling the supply of nutrients and humus to the ecosystem ^[18]. These indicators are based on soil respiration, microbial biomass, the amount of species and groups of edaphic fauna, as well as tests on enzymatic activities ^[19]. They act as early (microbiological and biochemical) signals of soil degradation or improvement due to their sensitivity ^[4][18]. The close relationship of the quality of the soil with the functions developed by the edaphic life has made them valuable indicators of disturbance, based on both their functions and their diversity, density, and abundance ^[4]. When the indicator is a living being, it is called a biological indicator, or bioindicator.

2.1. Biological Indicators (Bioindicators)

An edaphic bioindicator is every living being that responds easily to external (soil) stimuli through changes at the organism level ^[6]. Bioindicators need to belong to large, diverse taxonomic groups, of wide geographical and ecological distribution ^[11][20]. They must be easy to handle, visible at any time of the year, with easy reproduction, and be abundant and preferably sedentary. Depending on the presence/absence of changes against these soil variations (stimuli), bioindicators are called sensitive or tolerant ^[20][21][8].

We present below the most representative organisms of soil biota, considered to be bioindicators, with a special focus on the context of the Ecuadorian Amazon. The information and descriptions as functions, characteristics, and functionalities of each group are summarized in the entry called "Soil Biology in the Ecuadorian Amazon" published for this same author. Table 1 shows the applicability of some more representative organisms as edaphic bioindicators, depending on their abundance or absence. 

Table 1. Organisms used as edaphic bioindicators.

2.2. Biological Quality Indicators

These are parameters that serve to evaluate processes carried out by living beings in the soil, such as the transfer of nutrients from the soil to the plant, the dissolution of minerals that live in the mother rock, the mineralization of the OM, the stabilization of the soil structure that produces the OM, the cohesion of aggregates, and/or the formation of galleries that aerate and give porosity to the soil. As long as they can be measured, they can provide information on the condition and operation of the soil ^[4]. Table 2 summarizes the most important indicators, which we describe below.

Table 2. Biological quality indicators for Amazonian soils.

Organic matter (OM): the availability of OM is one of the main components of the soil. It is directly related to the different properties ^[7][6], such as the influence of temperature and humidity, which condition the mineralization in the microbial phase of the soil ^[40].

Organic carbon (OC) largely depends on the availability of OM and land use ^[41][47]. It is part of the different soil processes and is a source of food for edaphic organisms ^[47]. In pastures and crops, OC decreases by 65% compared to the forest ^[41], due to the low production of OM. It is among the five best carbon sinks ^[6].

Particulate organic matter refers to the youngest and most active portion of the OM. It is a reservoir of nutrients for the flora and fauna of the soil. It acts by increasing water carrying capacity and stabilizing aggregates. An analysis of this parameter allows the prediction of short-term nutrient availability ^[12][18].

Organic phosphorus is an important macronutrient for the functionality of plants. In tropical areas, availability limits plant growth ^[13], being one of the most sensitive nutrients in tropical soils ^[18].

Potentially mineralizable nitrogen is the amount of organic N in the soil that is transformed into soluble inorganic forms, such as NH₄⁺ and NO₃⁻, by microbial action. It is directly associated with the availability of OM and for its sensitivity it is considered as an indicator of nitrogen production or nitrogen contribution of a soil ^[18].

Microbial biomass (MB) is determined by the quantity and quality of OM that, at the same time, depends on the use of soil. Microbial characteristics are considered quality indicators ^[43]. Therefore, when MB is high, it indicates microbial diversity and an optimal environment. However, if they are at low levels, it is a sign of some kind of pollution ^[43] or due to changes in land use ^[18].

Carbon from microbial biomass (CMB) is related to the addition of OM to the soil. It indicates the biochemical and microbiological activity of soils. When it is high, it is considered an indicator of soil fertility ^[47]. It provides knowledge on the abundance and population structure of microorganisms, and is obtained from the difference between samples with C extracted and samples without C extracted ^[43], according to the fumigation-extraction method with chloroform. CMB is considered an indicator of soil quality ^[6][41].

Nitrogen from the microbial biomass (NMB), as well as CMB, depends on the MB and the amount of available OM ^[41]. It is obtained from the difference between fumigated (N extracted) and non-fumigated samples ^[43], according to the method of fumigation-extraction with chloroform. Actual NMB scores, similarly to CMB, are determined by the conversion factor (mineralized fraction for C and N) ^[42][43], applied to the general formula that determines the MB.

Soil respiration refers to the production of CO₂ as a result of microbial activity, roots, and macro and micro fauna. It is measured under anaerobic conditions and provides information on mineralizable substrates ^[6]. The larger the population, the greater the amount of CO₂. It also relates to the size of plant waste, litter, and biota in general ^[18], considered as an index of biological activity.

Metabolic or microbial ratio is the index of the relationship between growth and state of latency of BM. It measures the microbial change of the soil with respect to environmental limitations due to changes in use. An increase indicates unfavorable conditions for soil microbes (microbial stress) ^[41][45].

Geometric measurement of enzymatic activity (GMEa) is a common index to integrate data and information from various enzymes ^[19] and know the meaning of the enzymatic activity of a soil. Some authors ^[19][41][44] consider it a good index to estimate the quality of the soil. It can be related to physicochemical and biological properties.

Molecular markers—molecular techniques are capable of differentiating fungal microbial biomass, according to primers that are designed from the 16S and 18S rDNA genes ^[6]. The genomic study of soils from DNA shows the genetic potential to produce certain enzymes, motivating the study of RNA. These techniques show real information on the state of the soil and the environmental conditions to which microorganisms are subjected ^[6][46]. The genome of bacteria provides signals when there is some kind of impact on the soil. Currently, the determination of indicators of soil quality is based on the DNA and RNA of the species of soil organisms. It has great potential, speed, and provides more informative measurements of biota ^[1].

Enzymatic activity: Table 5 synthesizes some types of enzymatic activity that can be evaluated in soil samples. Their activity is affected by the change of land use, especially in the surface layer ^[6]. Low concentrations of enzyme activity indicate inactivity of microorganisms. High concentrations indicate the high decomposition of the OM and microbial activity ^[43]. In tropical soils, the marked variations are probably due to acidity ^[47], which are considered land degradation indicators, after deforestation ^[40][41], specifically, fertility and quality indicators ^[41],63]. Some research in Amazonian soils considers that enzymatic activity indicates ecological changes resulting from land use ^[43]. According to ^[19], these activities (Table 3) are the most sensitive indicators to assess the effects of restoration practices and effects of land use change. 

Table 3. Types of enzymatic activity that can be evaluated in soil samples.

3. Minimum Number of Indicators

In many cases, the limiting factor for measuring the soil quality through indicators is the cost, especially if biological parameters are included. Therefore, the total indicators contemplated to analyze the quality of the soil, at the initiative of several researchers, should be reduced to a minimum set of data ^[1].

The number of selected indicators usually varies between six and eight, and those that show the most relevant variations are chosen ^[1]. The selection and validation depends on the sensitivity and response to climatic changes, as well as their accessibility (sampling) ^[34]. The objectives of the investigation are also considered in selecting indicators ^[1].

The criterion for the selection of biological quality indicators is the score awarded by recognized researchers, frequency of use, reproducibility (essential aspect), and topicality in publications ^[1]. Under the reference a possible set of indicators applicable to the soil context of the Ecuadorian Amazon is proposed in Table 4.

Table 4. Example of a minimum number of indicators of soil biological quality. Source: ^[1].

4. Field Indicators

A project at the European level has developed simple and easy-to-use tools for farmers. The GROW Observatory project aims to provide services to citizens and non-profit science ^[49]. On the one hand, it allows for the measuring of soil parameters at high spatial resolution in large geographic areas. However, it has also opted for visual evaluations of soil in the field, a technique that is being implemented worldwide and is considered sensitive enough to assess the structure of a soil ^[14]. Most of the methods are based on observations of soil structure, and its relationship with crop productivity ^[49]. Other authors have affirmed that the visual evaluation of the soil is not sufficient to determine its state, the state of an ecosystem, or the services it provides ^[1]. They suggest that the indicators be preferably quantitative variables and propose the use of qualitative variables as valid and useful when there is no quantitative information, or when the costs of quantifiable parameters are high ^[4].

Studies in tropical soils of Venezuela have shown a strong relationship between visual evaluation scores, physical properties, and soil quality indicators measured in the laboratory ^[14]. Some variables taken into consideration in the visual evaluation are: (a) texture (tape method); (b) structure, by direct macromorphological observation and using a reference table (granular, laminar, or blocose); (c) depth of horizon (measured in the field); (d) color (Munsell table); (e) soil erosion (presence or absence of grooves); (f) slope (clinometer); and (g) height (GPS). Some authors have also proposed texture as an observable parameter in the field ^[11][50][51]. To understand the variation and to be able to relate the scores of the variables, they adjusted the data to a common numerical scale, facilitating interpretation.

However, the guiding approaches that are still provided by farmers or people who work the land strengthen knowledge through on-site practice (real time) ^[4]. They have the ability to measure the status of any agency or community. They manage to hold a discussion with researchers, relating practice to theory ^[1][34]. For example, the health of the soil can be determined from observations in the soil, plants, presence of animals, and water quality, and then related to laboratory analysis.

5. Relational Indicators Integrated Index

A correct evaluation of the soils takes into account the behavior and functionality of the organisms that inhabit it. Morphology, seasonality, and degree of sensitivity are also part of the evaluation process ^[29], showing the state of the soil. Some examples of relational indicators are shown in Table 5; they indicate sensitivity or adaptability depending on their densities.

Table 5. Examples of relational indicators.

6. Integrated Soil Quality Index

The Integrated Soil Quality Index is an integrated index based on a combination of indicators. This index clearly reflects the environmental quality of the soil and facilitates the comparison between different uses and management practices (same or different type of soil). In the countries of the Amazon, such as Brazil, Colombia, and Peru, its potential has been proven. It is obtained from the sum of three subscripts (physical, chemical, biological) of quality ^[2]. This index is developed in three steps: first, there is the selection of appropriate indicators, based on accessibility, ease of measurement, and sensitivity; second, the selected indicators are scored (more is better, optimal value and less is better); third, the integrated quality index is developed using a linear or additive model, combining the score of the indicators.

According to the attributes of the soil and the score, the indicators are grouped into subscripts of soil quality. In each subscript, the indicators are valued by the number of times each score is reached. The subscripts are divided by the number of indicators they contemplate, to integrate them (sum of subscripts) and normalize the equation of the integrated index ^[2]. It is important to avoid underestimating soil disciplines.