Artigo Qualidade Do Solo - Prof Elke

274
Cardoso et al. Scientia

Soil Agricola
health: looking for suitable indicators
Review
Soil health: looking for suitable indicators. What should be considered to assess the
effects of use and management on soil health?
Elke Jurandy Bran Nogueira Cardoso1*, Rafael Leandro Figueiredo Vasconcellos1, Daniel Bini1, Marina Yumi Horta Miyauchi1,
Cristiane Alcantara dos Santos1, Paulo Roger Lopes Alves1, Alessandra Monteiro de Paula2, André Shigueyoshi Nakatani1, Jamil
de Moraes Pereira1, Marco Antonio Nogueira3
USP/ESALQ – Depto. de Ciência do Solo, Lab. de

1
ABSTRACT: Soil Health refers to the ecological equilibrium and the functionality of a soil and its
Microbiologia do Solo, Av. Pádua Dias, 11, C.P. 09 – 13418- capacity to maintain a well balanced ecosystem with high biodiversity above and below surface,
900 – Piracicaba SP – Brasil. and productivity. To understand and use soil health as a tool for sustainability, physical, chemical,
UFPR, R. Pioneiro, 2153, Campus Palotina – 85950-000 –
2
and biological properties must be employed to verify which respond to the soil use and manage-
Palotina PR – Brasil. ment within a desired timescale. Attributes with a rapid response to natural or anthropogenic
The continued capacity of soil to function as a vital living system, within ecosystem and land-use
Embrapa Soja, Rod. Carlos João Strass, s/n, C.P. 231
3
–
boundaries, actions
to sustain are considered
biological goodthe
productivity, promote indicators of soil health. Among the physical indicators, soil texture,
quality of air and water environments, and maintain plant,
86001-970 – Londrina, PR – Brasil. animal and human aggregation,
health moisture, porosity, and bulk density have been used, while among chemical indica-
*Corresponding author <[email protected]> tors total C and N, mineral nutrients, organic matter, cation exchange capacity, among others
are well established. However, most of them generally have a slow response, when compared to
Edited by: Jussara Borges Regitano/Luís Reynaldo Ferracciú the biological ones, such as microbial biomass C and N, biodiversity, soil enzymes, soil respira-
Alleoni tion, etc., in addition to macro and mesofauna. Thus, a systemic approach based on different
kinds of indicators (physical, chemical and biological) in assessing soil health would be safer than
using only one kind of attribute. Many human activities have caused desertification, loss of bio-
diversity, disruption of aggregates, loss of organic matter and nutrients, among others. Today,
it is imperious to maintain soil health and productivity with increasing emphasis on reforestation
and recuperation of degraded areas through the use of organic amendments, reintroduction of
plants, soil fauna and microorganisms. This review focused on an integrative view on indicators
Received June 29, 2012 of soil health to be used as tools for prediction of sustainability in production systems.
Accepted February 18, 2013 Keywords: land-use, microbial community, soil fauna, soil quality, sustainability
Introduction and exert environmental functions, must be monitored

(Doran and Safley, 1997).
The concerns on the sustainability of agricultural Different land uses and management affect the
systems have increased recently because the agricultural soil as well as the sustainability of production systems.
edges have already expanded near to the maximum all Tillage systems based on plowing and disking (so-called
over the world. Feeding seven billion people with en- conventional tillage) in the tropical regions decrease soil
vironmental sustainability is a challenge for the next organic matter and increase the erosion process, leading
generations. In addition, pressures of public opinion and to chemical, physical, and biological changes in the soil
markets on the needs of environmental conservation, es- characteristics that enhance the dependence on exter-
pecially in the tropical region, claim for keeping forests nal inputs and consequently enhance production costs,
as reserve of biodiversity, provider of environmental ser- causing environmental impacts. On the other hand, less
vices, and needs for reclamation of degraded lands. impacting cropping systems like no-tillage and organic
Sustainable agriculture aims at meeting the needs farming are much more reliant on biological processes
of the present without compromising the productive po- for sustainability (Kaschuk et al., 2010).
tential for the next generations. Rational soil use practices Sustainable ecosystems, natural or agricultural,
must allow economically and environmentally sustain- rely on the flux of nutrients across trophic levels, which
able yields, which will only be reached with the mainte- are mainly intermediated by soil fauna and microorgan-
nance or recovery of the soil health. Thus, a healthy soil isms (Chen et al., 2003). Up to 95 % of the nitrogen re-
has been defined as “The continued capacity of soil to func- circulates in an almost closed soil-plant-microorganisms
tion as a vital living system, within ecosystem and land-use system in a climax forest (Rosswall, 1976). Nevertheless,
boundaries, to sustain biological productivity, promote the after removal of the vegetation and agricultural soil use,
quality of air and water environments, and maintain plant, the system becomes open and creates an external de-
animal and human health” (Doran and Safley, 1997). To mand for nutrients caused by harvests, leaching, and
assess the sustainability of a production system, changes erosion (Brussaard et al., 2004). The soil fauna and mi-
in chemical, physical, and biological properties, and the crobial community are considered critical in any eco-
effects on the soil’s capacity to support plant growth system, by acting on the decomposition of soil organic
Sci. Agric. v.70, n.4, p.274-289, July/August 2013

275
Cardoso et al. Soil health: looking for suitable indicators
matter, nutrient cycling, and affecting the soil chemical fects important functional processes in soil like the stor-
and physical properties, with direct effects on soil fertil- age of nutrients, mainly N, water holding capacity, and
ity and sustainability. The soil biota is very dynamic and stability of aggregates (Silva and Sá-Mendonça, 2007). In
promptly affected by soil use and management or any addition, the soil organic carbon also affects microbial
other disturbance, differently from most chemical and activity. Hence, this is a key component of soil fertil-
physical properties, which take longer to be changed. ity, especially in tropical conditions, which interacts
That is the reason why the edaphic organisms are good with chemical, physical, and biological soil properties
indicators of soil health, especially if the indicator cor- and must be considered in assessments of soil health.
responds to ecological processes occurring in soil. Although rarely mentioned, soil organic matter may also
Soil quality definition cannot be generalized for have negative effects on soil health. High organic mat-
all kinds of soil and soil-use as criticized by Sojka and ter contents reduce pesticide efficiency, increasing the
Upchurch (1999). Thus, indicators of soil quality must frequency of needed applications. Complexation with
be selected according to soil use and management, soil soluble organic matter facilitates pesticide sorption on
characteristics and environmental circumstances. There- organic fractions and transport through soil or ground-
fore, in this review, we discuss the general and most water (Sojka and Upchurch, 1999).
used chemical, physical and, mostly, biological indica- Nitrogen is the most required plant nutrient,
tors of soil health and also some special applications in which is found in several chemical forms in soil (Can-
case studies under tropical and subtropical conditions, tarella, 2007), resulting in a very dynamic behavior. Soil
especially in Brazil. nitrogen has been assessed mainly as mineral N, espe-
cially nitrate, organic N or potentially mineralizable N,
Chemical indicators as stored in the soil organic matter. Despite the impor-
Chemical attributes of soil health are correlated tance in plant nutrition and environment, the use of ni-
with the capacity to provide nutrients for plants and/or trogen as parameter for assessing soil health is subjected
retaining chemical elements or compounds harmful to to factors that affect its dynamics in soil, like climatic
the environment and plant growth. Soil pH, cation ex- conditions, turning inadequate the diagnosis of the real
change capacity (CEC), organic matter and nutrient lev- availability for plants, based on soil chemical analysis
els are the main chemical attributes used in soil health (Cantarella, 2007).
assessment, especially when considering the soil capac- Phosphorus (P) is also a key nutrient for agricul-
ity for supporting high yield crops (Kelly et al., 2009). tural yields and is essential in assessments of soil quality.
Chemical attributes have been correlated with plant Along with nitrogen, P is the main nutrient that limits the
yields and thus the variations of a particular indicator agricultural yields in tropical soils, especially in highly
are easily interpreted, and allow a quick improvement weathered, oxidic soils, where the major part of the total
of the soil chemical properties by liming and/or fertiliza- soil P is fixed in clay minerals and oxides. The available
tion. These soil chemical indicators can also be useful P in the soil solution is present as orthophosphates, but
in considering the soil’s capacity for sustaining forest the microbial P and organic-P are also stocks that can
production and sustainability, maintaining nutrient cy- rapidly become available. Procedures for assessment of
cling, plant biomass and organic matter (Schoenholtz et P availability have been well established (Pankhurst et
al., 2000). al., 2003; Zhang et al., 2006a).
Idowu et al. (2008) selected a set of parameters to Soil chemical parameters have been traditionally
characterize the soil health among 39 physical, chemical used for assessment of potentially available nutrients for
and biological attributes and correlated them with plant crops, and are based on worldwide well established ana-
growth and yield, in soils under different tillage, rota- lytical methodologies. Among them, organic matter, pH,
tion and cover cropping, in commercial production fields and available nutrients and also some potential hazard-
in New York State, USA. These authors concluded that ous chemicals have been used to establish levels of soil
the most important chemical parameters to be assessed health. These procedures do not fulfill the promises to
were pH, available P, K, Cu, Fe, Mn, and Zn. Soil pH is a help us to understand all factors associated to sustain-
key indicator because it correlates directly with nutrient ability, especially in relation to ecological processes. For
availability/solubility and also affects microbial activity. example, Melo and Marchiori (1999) reported very good
Thus, assessment of pH allows to predict the potential levels of chemical indicators in a field cropped with cot-
for nutrient availability in a given production system ton, but the biological indicators were far below the ones
(Sousa et al., 2007). However, under native vegetation, found in a native forest used as reference. Thus, the inte-
especially in the tropics, pH ranges in a very acidic range gration among indicators seems to be a more appropriate
(even < 3.5) (Chaer and Tótola, 2007), and nutrients, approach to assess soil health.
particularly P are scarce; nevertheless the ecosystem
works properly playing its environmental role. Physical indicators
Soil organic carbon is also a key attribute in assess- Physical indicators of soil health generally include
ing soil health, generally correlating positively with crop simple, fast and low-cost methodologies. Moreover, such
yield (Bennett et al., 2010). The soil organic carbon af- indicators like texture, bulk density, porosity, and ag-

276
gregate stability are also correlated with hydrological In particular, soil carbohydrates account for 5-25 % of
processes like erosion, aeration, runoff, infiltration rate, the soil organic matter and also act as stabilizers of the
and water holding capacity (Schoenholtz et al., 2000). soil aggregates (Spaccini et al., 2001).
In general, a soil is considered physically poor when it Soil aggregates affect aeration, permeability, nu-
shows low rates of water infiltration, enhanced surface trient cycling, and serve as refuge for microorganisms
runoff, poor cohesion, low aeration and root density, and and soil fauna in microsites. By turn, the soil biota (mi-
difficulty for mechanization (Dexter, 2004). croorganisms, fauna, and plants) affects the soil aggre-
Soil texture is an important factor affecting the bal- gates. Many organic substances as secretions, mucilages,
ance between water and gases, but it is very stable along mucigels, and cell lysates act as cementing substances
time, independently on the soil management. Therefore, produced by several organisms as earthworms, as repre-
bulk density and total porosity can better represent the sentatives of soil fauna (Figure 2-A), arbuscular mycor-
effects of soil use and management on the water/air rela- rhizal fungi (Figure 2-B), bacteria (Figure 2-C) and also
tionships (Beutler et al., 2002). the plants (Figure 2-D), in addition to their stimulation of
Lower bulk densities have been generally ob- microbial activity and action on soil aggregation (Preston
served in soils under less anthropogenic interferences et al., 2001).
like native forests (Bini et al., 2013), where the greater Organic matter and biological attributes shape the
levels of soil organic matter permit a better aggregation soil physical structure and consequently the hydrologi-
of soil particles, improving the soil structure. As a result, cal processes (erosion, drainage, runoff, and infiltration
an increase in soil macroporosity improves the soil per- rate). In addition, they are fundamental for water and
meability not only for water, but also for air and roots nutrients supply in soil. Humic substances increase the
(Tejada et al., 2006). soil capacity for water retention due to charges in their
The total soil porosity can be classified as textural, carboxylic and phenolic groups which attract the water
depending on the proportion of soil particles, and struc- molecule and thus reduce its percolation through the
tural, depending on biopores and as macro-structure. soil profile.
The second one is easily affected by soil use and man- As the content of available water is a determining
agement (Dexter, 2004), which may change the charac- factor of the microbial activity in soil, the soil physical
teristic soil water retention curve based on structural attributes affecting water availability and aeration will
pores (For further details, see Dexter, 2004). also affect the soil microbial activity, since the inverse
The structure corresponds to the arrangement of correlation between water availability and microbial ac-
the primary soil particles (sand, silt and clay) and is af- tivity has been described before (Geisseler et al., 2011).
fected by the cropping methods and compaction (Dex- Thus, the impairment of soil microbial activity due to
ter, 2004). The granular structure is considered the most water limitations can lead to losses of soil functionalities
suitable for plant growth, allowing for a better balance like synthesis and mineralization of soil organic matter
between macro and micropores, and consequently, be- and consequent effects on the biogeochemical cycles.
tween the air/water proportion. Structure is the major Nevertheless, different microbial groups are differently
soil physical attribute affected by organic matter, and affected by water restrictions in soil. For example, bac-
as a consequence other physical characteristics such as teria have restricted movement in drier soils in which
porosity, bulk density, aeration, water infiltration and re-
tention, are also affected.
Soil aggregates are formed by particles smaller
than 0.2 µm that group to form microaggregates (20-250
µm), and microaggregates are grouped to form macro-
aggregates (Figure 1). Microaggregates are more stable
and less affected by soil use and management. In addi-
tion, they are responsible for long-term stabilization of
soil organic carbon (Six et al., 2004). On the other hand,
macroaggregates are more susceptible to the soil use and
management, and are especially related to the dynamics
of the soil organic matter (Six et al., 2004). The disper-
sion of soil aggregates under intensive management is
usually less severe than in soils with more inputs of or-
ganic matter, which results in greater microbial activity
(Qin et al., 2010). On the other hand, the decrease of
soil organic matter followed by dispersion of aggregates Figure 1 – Formation of soil aggregates: non aggregated soil (left),
reduces the macroporosity and the soil oxygenation, and flocculation (center), that consists in the approximation of the soil
impairs the performance of decomposing microbiota particles, and cementation (right), that results from the direct
and their access to the organic material (Degens et al., interaction with soil organisms under influence of the soil organic
2000; Tejada et al., 2006; Chodak and Niklinska, 2010). carbon (By M.Y.H. Miyauchi).

277
Microbiological and biochemical indicators

Soil microbial activity and diversity play important
roles in the sustainability by keeping essential functions
in soil health, involving carbon and nutrient cycling (Jef-
fries et al., 2003; Izquierdo et al., 2005). Microbial indi-
cators are more susceptible than physical and chemical
attributes to changes imposed to the environment like
soil use and management (Melo and Marchiori, 1999;
Masto et al., 2009), and for this reason can early fore-
cast any disturbance in the sustainability of an environ-
ment.
The soil microbial biomass is the living part of the
soil organic matter, formed by fungi, bacteria, protozoa,
and algae, and represents an important source of nutri-
ents that may supply plant demands due to its rapid cy-
cling (Sicardi et al., 2004), being one of the main biologi-
cal attributes used in soil health studies.
In addition to microbial biomass, soil respira-
tion has been widely used as bioindicator of soil health
in either forestry or agricultural soils (Bastida et al.,
Figure 2 – Contribution of organisms to formation of soil aggregates: 2008). Changes in vegetation like deforestation reduce
earthworms by joining soil mineral particles and organic matter in the microbial respiration in the long-term (Bastida et
the intestinal tract (A), arbuscular mycorrhizal fungi with glomalin al., 2006) due to decrease in organic carbon inputs into
production (B), bacteria with exopolysaccharides (C), and plants, the soil via surface or rhizosphere (Bini et al., 2013). In
by action of roots and their exudates (D) (By M.Y.H. Miyauchi). agricultural systems, the soil management affects the
microbial activity, and in general, the less impacting
managements result in higher microbial activity (Ba-
the water film is more intensively interacting with the lota et al., 2003; Babujia et al., 2010). In this scenario,
soil particles (Wong and Griffin, 1976). Conversely, fungi the organic matter modulates the biological activity as
are favored under drier conditions, in which their hy- source of C, energy and nutrients that will be mineral-
phae explore the air-filled soil pores. Water availability ized to CO2 and minerals. However, the mineralization
in soil will depend not only on physical properties like rate will also depend on the quantity and quality of the
permeability, bulk density, texture, but also on chemical organic material in soil (Zhang et al., 2006b). Simulta-
properties like salinity and organic carbon content, in neously, the microbial biomass will immobilize C, N, P
addition to the climatic regime. and other nutrients that can be easily released for plant
In summary, physical soil attributes and soil mi- use due to its rapid turnover (Bayer and Mielniczuk,
crobial communities are co-influenced (Degens et al., 2008).
2000), and both are affected by soil organic matter. The metabolic quotient (qCO2) is an index given by
the amount of CO2-C released per unit of microbial bio-
Biological Indicators mass in time and represents the metabolic status of the
Understanding the complex interrelationships be- soil microorganisms (Anderson and Domsch, 1993), in
tween biological, physical, and chemical components which higher indices indicate more stressing conditions.
can be better achieved when studying the origins of nat- However, caution must be taken while interpreting the
ural processes and their fate in nature. For example, by qCO2 indexes, because higher values might not only be
means of photosynthesis, plants fix and transfer carbon attributed to microbial stress, but also to inputs of easily
as carbohydrates to the food web, which is the most im- degradable organic carbon that promptly stimulates the
portant biological process on earth. Along their lifecycle microbial activity (Dinesh et al., 2003).
and especially at the end, animal and plant debris are Soil microorganisms can be classified into func-
constantly deposited into the soil. Organic carbon and tional groups according to the biological process they
immobilized minerals must be recycled in the ecosystem play in an ecosystem. All microorganisms that act in
before being utilized by new organisms in a continuous the N cycle (e.g., diazotrophic, nitrifying, denitrifying,
and sustainable life-cycle (Schjønning et al., 2004). Thus, ammonifying and proteolytic bacteria, etc.) and C cycle
biological processes are essential for keeping the soil ca- (e.g., cellulolytics, amilolytics, proteolytics, etc.) are ex-
pacity for recycling carbon to the atmosphere and assure amples of functional groups. In this case, the individual
the continuance of photosynthesis, concomitantly with species is not the focus, but the function they play col-
nutrient mineralization for plant and microbial nutrition. lectively in an environment. A summary of microbial
Healthy soils have the capacity to keep these processes indicators related to the cycle in which they act and the
working in a sustainable way indefinitely. functions they play is shown (Table 1).

278
Table 1 – Microbial indicators of soil quality. The role they play in the soil cycles, and methods for assessment.
Indicator Cycle Function Measurement
Mainly C, but also N
Microbial Biomass Source and/or drain of C and nutrients C and nutrient stocks in cells
and P
Soil Respiration C Microbial mineralization of organic carbon CO2-C evolution
Amount of C-CO2 released per unit of
qCO2 index C Metabolic condition of the microbial community
microbial biomass in time
proteolytics, cellulolytics, amilolytics, proteolytics, Colony forming units (CFU) or most
Microbial functional groups C, N, P, etc. phosphate solubilizers and diazotrophic, nitrifying, probable number (MPN) on specific or
denitrifying and ammonifying bacteria. selective media
DNA extraction, amplification and
PCR-DGGE All Genetic diversity
separation
Fatty acids extraction and quantifica-
PLFA-profiling All Diversity and biomass
tion
Biolog All Metabolic diversity Matabolization of different C sources
A soil with high microbial diversity has more Facing these challenges, the use of multivariate statisti-
chance to keep the ecological processes after a distur- cal techniques is a useful tool for selecting attributes for
bance (Kennedy, 1999). Such capacity is defined as resil- assessment of soil health.
ience which means a biological buffering against distur- Lande-use changes affect the sooil carbon storage
bances in an ecosystem. We may usually state that the and cause changes quantitative and qualitativ
functional redundancy is higher in less degraded soils Land-use changes affect the soil carbon storage and
(Harris, 2003), but the composition of the plant commu- cause quantitative and qualitative changes on soil organic
nity may favor the prevalence or cause suppression of matter, and consequently on physical and chemical char-
certain microbial functional groups in soil (Matsumoto acteristics that directly affect the soil microorganisms,
et al., 2005). like humidity, porosity, density, among others (Bayer and
Besides microbial activity and biomass, biochemi- Mielniczuk, 2008). Consequently, these alterations will
cal indicators such as soil enzymes can also be useful also reflect on the nutrient cycling and availability of nu-
indicators of soil health (Table 2). They are involved in trients in soil. Different land-use systems like annual and
several metabolic processes and are also responsive to perennial crops, pastures and forests, generate different
changes in soil use and management (Nannipieri et al., residues whose dynamics and cycling will also be differ-
2002; Acosta-Martínez et al., 2007). Enzymes are cata- ent due to differences in composition (e.g., C/N ratio, cel-
lysts in different reactions during carbon and nutrient lulose and lignin contents, resins, monoterpenes, tannins
cycling in soil (Balota et al., 2004; Sicardi et al., 2004), etc.). In addition, more intense agricultural practices, with
and also represent the metabolic level of the soil micro- more soil stirring, can also affect the dynamics of organic
bial community. They may be free in soil as exoenzymes matter, speeding up the oxidation process and reduce the
excreted by plants, animals, and mainly microorganisms stable organic matter, and consequently the biological
(Weaver et al., 1994), linked to cell structures or inter- activity. More conservative agricultural practices like no-
nally in cells, but later released to the soil after cell ly- tillage and organic farming has been used to attenuate the
sis and death (Badiane et al., 2001). Hence, when the negative impact on soil health, thus keeping the system
soil microbial community is affected due to soil use and more balanced and sustainable.
management, changes in soil enzyme activities are also Besides the classical techniques for assessing the
expected (Nayak et al., 2007). soil biological quality, new approaches have been recent-
The main limitation of using individual biochemi- ly developed and are tools for helping us to understand
cal properties as indicators of soil quality is that they the changes in soil biological quality. For example, profil-
show a high degree of variability in response to climate, ing techniques consist of more specific tools that can be
season, geographical location and pedogenetic factors. used for assessment of variations in the soil microbial
This might result in contradictory conclusions in differ- community caused by land-use and management (Ken-
ent studies when describing the effects of a contaminant nedy and Smith, 1995).
or a given management on the soil quality (Gil-Sotres et The capacity of using different carbon sources has
al., 2005). Moreover, with the knowledge actually avail- been evaluated with the BiologEcoplate® method (Gar-
able, estimation of soil quality relying only on individual land and Mills, 1991) and allows to look for quantita-
biochemical properties, simple indexes or ratios, cannot tive and qualitative physiological profiles of the micro-
be considered reliable. Thus, a minimum data set of bio- bial community (Winding et al., 2005). Considering that
chemical properties capable of describing the complex- the metabolic diversity is consequence of the genetic
ity of the soil system is required for each situation, and diversity, environmental effects in gene expression,
it must be verified whether they are universally valid. and ecological interaction among different populations

279
Table 2 – Biochemical indicators of soil quality and functions played in soil cycles.
Enzyme Cycle Function Microorganisms
Electron transferences in the respiratory chain in living
Dehydrogenase C All aerobic
cells
β-glucosidase C C oxidation Several
Cellulase, amylase C Cellulose degradation with release of glucose Mainly fungi, but also bacteria
Urease, glutaminase, and Organic N mineralization to
N Several
asparaginase ammonia/ammonium
Phosphatases Alkaline phosphatases of microbial origin,
P Organic phosphorus cycling
(Acid and alkaline) and acid phosphatases with several origins
Arilsulphatase S Organic sulfur cycling Several
(Zak et al., 1994), the metabolic profiling can help us Faunal indicators
to understand changes in soil biological quality caused Recently, more importance has been given to
by anthropogenic activities or other interferences in the members of soil fauna as indicators of soil health. This
environment. group comprises the invertebrate community that lives
Phospholipids are found in membranes of all liv- totally or during at least a phase of the life cycle in the
ing cells and can be used as biomarkers. Phospholipid soil (Brown et al., 2009). They play roles in structuring
fatty acid (PLFA) profiling can be used to determine the processes of terrestrial ecosystems, fragmentation of
phenotypic structure of microbial communities based plant residues, and establishing relationships at differ-
on phylogenetic relations (Zelles, 1999). The PLFA tech- ent levels with microorganisms. Therefore, they actively
nique has also been used to elucidate different strate- take part in processes that influence the soil properties
gies employed by microorganisms to adapt to changes and quality, and for this reason are good indicators of
in environmental conditions due to land-use, climatic changes in the soil (Lavelle and Spain, 2001).
changes, and disturbances (Kandeler, 2007). Different As stated above, the decomposition and transfor-
microbial groups are characterized by fatty acids linked mations of organic materials in soil are predominantly
to specific phospholipid esters, and a change in the struc- carried out by microorganisms (Adl, 2003). Nevertheless,
ture of such communities is characterized by changes in the microbial processes are more effective when the or-
the patterns and composition of the PLFA in soil. Thus, ganic material is more accessible, i.e., more fragmented
the content of PLFA has been correlated with other mea- and distributed along the soil profile (Paul, 2007). Hence,
surements of microbial biomass in soil and therefore has the soil fauna is the main responsible for supplying pre-
been confirmed as a good indicator of changes in the mi- transformed organic material to the microorganisms af-
crobial community (Frostegard et al., 1993). In addition, ter fragmentation, resulting from their feeding process.
this technique also allows for assessing the physiological Besides increasing the contact surface, the fauna, espe-
status of the soil microbial communities. cially earthworms, promotes a distribution of organic
The development of methods based on recombi- material vertically or horizontally along the soil layers
nant DNA has represented great advances in the stud- (Kostina et al., 2011).
ies of soil biodiversity and microbial ecology (Torsvik The faunal activity also affects soil structure due
et al., 1990), mainly because these methods are not de- to the aggregation of soil particles, in addition to the mi-
pendent on cultivation in artificial media. Extraction and crobial effect (Belnap, 2003). Higher stability of soil ag-
amplification of a DNA fragment from soil samples by gregates has been observed in soil with higher microbial
PCR, employing universal or specific primers, followed and earthworm biomasses (Mäder et al., 2002). More-
by different fingerprinting methods like DGGE/TGGE, over, the faunal action mixes soil particles and produces
T-RFLP, ARDRA, RISA (Kirk et al., 2004) or by cloning galleries, pores, tunnels, and other biological compart-
and sequencing, can be used to analyze the microbial ments that make the air and water flow easier, which
community in time and space. also stimulates the microbial activity (Lavelle et al.,
The profiling techniques are powerful tools, how- 2006). Conversely, soils with low faunal activity show
ever cannot supply all the information alone, since each more compaction, which makes difficult the penetration
of them has intrinsic limitations. These limitations may of plant roots (Drewry et al., 2008).
cast doubts on the true relationship and contribution of The diversity, abundance, biomass and density of
the microbial diversity to the concept of soil quality. Thus, soil fauna has been used as indicator of natural or anthro-
polyphasic approaches are indicated to bring complemen- pogenic impacts on terrestrial ecosystems because they
tary information. The arising of novel methods must be are strictly correlated with physical, chemical, and mi-
considered as a progress and complementary to the tra- crobiological soil attributes (Decaëns et al., 2004; Eggle-
ditional methods, not a replacement. A minimal and dis- ton et al., 2005). This is a quite simple, easy, and econom-
tinct set of microbiological techniques is required for each ical procedure employed for assessment of the taxonomic
situation and type of study to assess soil health. diversity at order, class or key species level. Soil fauna

280
can be classified according to their food preference, mo- Despite the quick response of soil fauna to changes
bility, functional diversity, and mainly by size (Swift et in land-use and management, they are also very respon-
al., 1979) (Table 3). The most representative organisms sive to seasonality and climatic variations (Sicardi et al.,
normally studied as indicators of soil health belong to the 2004), thus indicating the necessity of a closer monitor-
mesofauna, which lives in soil macropores and spaces ing. In addition, the inference of an interpretative value
in the soil-litter interface, feeding on fungal hyphae and for biological attributes is not an easy task due to the
organic matter, and thus taking part in nutrient cycling huge amount of influences on soil organisms. For this
and soil aggregation (Lavelle and Spain, 2001). Studies reason, a compilation of studies in different environ-
under different environmental conditions have shown ments would be interesting, in order to try to establish
that some springtail species are good indicators of soil biological indices of soil quality, similarly to chemical
health (Ponge et al., 2003; Baretta et al., 2008). The mac- and physical indices already established.
rofauna includes bigger soil organisms which sometimes
are active in soil functioning (Lavelle et al., 2006). Case Studies
Changes in the environment may reflect differ-
ently on a species, family or functional group compo- Indicators of soil health under varying soil tillage
sition of the soil faunae (Wink et al., 2005; Lavelle et systems
al., 2006). Using functional groups as bioindicators has Different soil uses in agricultural systems regard-
been preferred instead of the total species diversity, due ing management, crop rotation, frequency of applica-
to the role they play in biological processes. The pres- tion or amounts of applied chemicals lead to changes
ence or absence of a particular species can be crucial in physical, chemical, and mainly biological soil prop-
for a given process in an ecosystem (Brussaard et al., erties. In this context, the conventional tillage system
1997), as can be seen when a biological process stops is considered to be more aggressive because the inten-
when a key species involved disappears (Schjønning et sive soil revolving disturbs some attributes associated
al., 2004). For example, after some earthworm species to soil health, e.g. decrease in organic matter (Grace et
had disappeared, the organic material accumulated on al., 1994), loss of structure (Bayer et al., 2001), increased
the soil surface, and thus the individual activity of the risk of erosion (Volk et al., 2004), in addition to losses of
species was considered limiting. Despite the existence of microbial diversity and activity (Gupta et al., 1994). Less
other functional groups of organisms, they were not able aggressive techniques of soil use, like minimum tillage
to replace the role previously played by the earthworm (Sun et al., 2010) and no-tillage (Balota et al., 2003; Babu-
species (Hoogerkamp et al., 1983). Nevertheless, the jia et al., 2010) have been identified as less impacting
presence or absence of a certain species may be limiting systems of soil management. In general, the no-tillage
for an ecosystem functioning (Huston et al., 2000), and system, in addition to adequate crop rotation, has shown
thus the richness index should be considered in assess- to improve attributes associated to soil health. A more
ments of soil quality. stable soil temperature and humidity due to the constant
soil mulching, greater inputs and maintenance of organ-
Table 3 – Classification of soil faunae according to their size and ic matter, protection against rain drops, thus preventing
function (Schjønning et al., 2004). soil erosion, do stimulate the soil microbial diversity
Size and activity, and consequent enhancement of nutrient
Function Micro- Meso- Macro-
cycling (Balota et al., 2003; Babujia et al., 2010; Kaschuk
fauna* fauna** fauna*** et al., 2010; Peixoto et al., 2010).
(< 0.20 (0.2 – (> 2.0 One of the main effects of no-tillage is the main-
mm) 2.0 mm) mm) tenance of soil structure. The adoption of no-tillage sys-
Fragmentation of residues X X tems in subtropical southern Brazil for 30 years has in-
Stimulate microbial activity X creased the concentrations of soil organic C especially
Organic matter/nutrient redistribution X at the 0-10 cm top layer, when compared to the conven-
Soil aggregation/biopores X X X tional tillage (Babujia et al., 2010). These findings have
Carbon sequestration X also been reported from several other geographic regions
Nutrient cycling, mineralization/
X X
under temperate and tropical conditions (Melero et al.,
immobilization 2008; Pandey et al., 2010; Sun et al., 2010).
Humification X X Despite serving as indicator of alterations due to
Feeding on fungal hyphae X X soil use, changes in soil organic C are usually of long-
Opening channels and galleries X term effect. Thus, more promptly responsive attributes
Regulate bacterial/fungal populations X X must be used to monitor changes in soil attributes caused
Mixing organic and mineral particles X by anthropogenic effects. In this particular, the soil mi-
*Protozoa (Protista); Nematodes (Nematoda); **Mites (Acari); Enchytraeids crobial biomass has been used as a promising indica-
(Enchytraeidae); Springtails (Collembola); ***Earthworms (Oligochaeta); tor of soil health due to its rapid response to changes in
Spiders (Arachnida); Millipedes (Diplopoda); Termites (Isoptera); Slater soil use and management (Nogueira et al., 2006). Un-
(Isopoda); Centipedes (Chilopoda); Ants (Hymenoptera); Beetles (Coleoptera). der tropical conditions, increases in C and N microbial

281
biomasses under no-tillage have been observed mainly As a result, soil use systems that keep organic ma-
at 0-10 cm of soil depth (Babujia et al., 2010; Balota et terial on the soil surface maintain higher levels of soil
al., 2003; Silva et al., 2010). Soil microbial biomass is af- microbial and biochemical activities, therefore pointing
fected not only by the soil management system, but also to greater environmental sustainability.
by the composition of plant species in the crop rotation
system (Silva et al., 2010). Indicators of soil health in forestry systems
Under semiarid conditions and different tillage Most of the forestry environments worldwide have
systems (disk ploughing, animal-drawn ploughing and undergone large losses in their floristic composition. Ap-
minimum tillage) in Mexico, the soil microbial biomass proximately 13 million ha of native forests have been
carbon and organic carbon were identified as a minimum converted into other land use systems or lost by natural
data set as potential indicators for soil health assessment disasters according to FAO’s biannual report (FAO, 2011).
(along with soil pH and exchangeable Mg2+) in Agave an- All these changes in natural landscapes have caused loss
gustifolia plantations, showing that these soil attributes of biodiversity, and increasing concerns associated to
are closely related and capable of distinguishing the sites emissions of greenhouse gases and soil degradation.
and their associated tillage systems (Bautista-Cruz et al., One of the main concerns regarding conversion of
2011). forest into agriculture is the decrease of C stocks in the
Under temperate conditions, comparisons be- soil with transference to the atmosphere as CO2 (Lemenih
tween conventional, minimum, and no-tillage soil man- et al., 2005). Comparing agricultural soil with a refer-
agement showed no differences among the total micro- ence site under native forest, the C stocks were 50-75 %
bial biomass based on phospholipids profiling (FAME) less in the agricultural soil (Spaccini et al., 2001). There-
techniques (Sun et al., 2010). Nevertheless, when fun- fore, it is very easy to lose the soil organic carbon due to
gal and bacterial biomasses were assessed separately, soil use and management, but the recovery back to the
only the fungal biomass had been favored under the original levels as found in the native forest is very dif-
more conservationist soil management. The favoring of ficult to be reached (Nogueira et al., 2006). The clear-cut
fungal biomass can be explained by the maintenance of a Mixedwood (Populus tremuloides-Picea glauca) stand
of the hyphal net in the system in which the soil is in Central Saskatchewan, Canada, showed no changes
less revolved (Frey et al., 1999). On the other hand, in the short-term (1-5 yr) in comparison with the mature
under more aggressive, stressing conditions, as gener- forest, but in the medium-term (6-20 yr), soil organic
ally observed under conventional tillage, the bacterial carbon and soil nitrogen decreased by 24 % and 27 %,
community prevailed in relation to the fungal commu- respectively, causing environmental concerns (Pennock
nity (Pankhurst et al., 2002). Thus, it is not rare to find and Van Kessel, 1997).
general increase of microbial biomass in soil under no- Another important indicator of soil health is the lev-
tillage in relation to conventional tillage (Helgason et el of soil microbial biodiversity. Environmentally friendly
al., 2010; Muruganandan et al., 2010), especially un- strategies of soil use and management must maintain or
der tropical conditions, where the microbial biomass increase the soil biodiversity and ultimately preserve the
is greater and activity is more intense (Kaschuk et al., soil ecological functions in the environment. Neverthe-
2010). less, assessment of soil microbial diversity is not an easy
Higher enzyme activities under conservationist task, because 95-99 % of soil microorganisms are not cul-
systems as compared to conventional tillage were also tivable on artificial media. Alternative tools independent
reported (Melero et al., 2008; Qin et al., 2010) in various of cultivation have been based on molecular biology and
countries, including Brazil (Mendes et al., 2003; Balota have brought new insights in studies on soil microbial di-
et al., 2004; Carneiro et al., 2004; Carneiro et al., 2009; versity. For example, the genetic diversity of the ribosomal
Peixoto et al., 2010; Lisboa et al., 2012). In general, high- gene 16S (16s rDNA) for bacteria based on the PCR-DG-
er activities of cellulase and amylase are associated with GE technique (polymerase chain reaction – denaturating
greater amounts of organic C at the topsoil layer. On the gradient gel electrophoresis) showed that sites reforested
other hand, enzymes like phosphatase may be inhibited with native species presented similar bacterial diversity
by phosphate fertilizers in a feedback effect (Melero et to the soil with native forest. Nevertheless, reforestation
al., 2008; Peixoto et al., 2010). with Eucalyptus resulted in less bacterial diversity in soil
Several other soil features have influence on en- (Nogueira et al., 2006). Card and Quideau (2010) found
zyme activity; for example, dehydrogenase correlated similar results and also observed that microbial diversity
negatively with soil pH, but correlated positively with in soil increased with the time elapsed after reforestation.
total soil C (Melero et al., 2008). Enhanced dehydroge- Vasconcellos et al. (2013) studied microbiological indica-
nase activity has often been observed at the 0-10 cm lay- tors of soil quality in a gradient of riparian forest reclama-
er in soil under no-tillage (Mikanová et al., 2009; Silva et tion in the Brazilian Atlantic forest biome and found that
al., 2010; Sun et al., 2010). A stimulation of soil micro- microbial biomass, urease activity and Bacteria commu-
bial activity is also expected to result in higher general nity structure followed the recovery process, emphasizing
enzyme activities (Nayak et al., 2007), because most of the need for more than 20 yr for the sites to recover the
the soil enzymes have microbial origin. similarities to the native riparian forest.

282
The replacement of native forests by exotic species logical indicators of soil health due to changes in the
leads to great changes in the soil properties and process- quantity and quality of vegetal residues deposited on
es like distribution of the soil organic matter along the the soil surface and directly inside the soil as rhizode-
soil horizons and on the composition of the soil fauna position (Fagotti et al., 2012; Bini et al., 2013). Thus,
(Córdova et al., 2009). Reforestation with exotic species the removal of native plant community firstly changes
of economical interest or conversion to pastures causes microbial communities and soil fauna, and later also
deep interferences in the structure and functionality of physical-chemical attributes like temperature, water
the ecosystem (Pankhurst et al., 1997). The soil fauna in availability, concentration of organic matter, nutrients,
native fields is more diverse than in reforestations with pH, etc. As reported by Bautista-Cruz et al. (2012), in a
Pinus taeda, P. elliottii, and Araucaria angustifolia (Córdo- forest recovery study after clearing in Mexico, chemical
va et al., 2009). Similar results were found for microbial indicators like pH, plant-available P and exchangeable
and biochemical processes related to N and C-cycling in Al3+, besides O horizon thickness, changed extremely
southern Brazil (Fagotti et al., 2012; Bini et al., 2013), slowly, in time spans estimated at 100 yr. Biological in-
in which reforestation with Pinus showed to impair the dicators, however, are much more sensitive to detect
microbial processes in soil as compared to reforestation alterations in soil health caused by land-use changes
with A. angustifolia, emphasizing that different indica- (Wink et al., 2005). In a forestry restoration chronose-
tors of soil health followed the same trend. quence after mining, the increase of soil organic carbon
The diversity of springtails decreased in refores- was only 1.7 % after 30 years, and even after 50 years of
tations in comparison with native fields, as the faunal restoration the ratio between microbial and total carbon
diversity in general (Deharveng, 1996). The intensity of did not reach the levels found in the native, reference
changes in the land-use system may eliminate some spe- site (Insam and Domsch, 1988). Substitution of native
cies essential for biochemical processes (Kouadio et al., vegetation by exotic species also decreased the micro-
2009), compromising the sustainability. Studies on abun- bial biomass and activity in soil (Rutigliano et al., 2004;
dance, diversity, and structure of the invertebrate com- Fagotti et al., 2012; Bini et al., 2013). The C/N ratio and
munity in soil have been useful indicators of soil health the recalcitrance of the organic molecules are the main
in forest environments. Decaëns et al. (2004) observed factors to define the availability of organic C for the soil
that conversion of native ecosystems in the Colombian biota. However, certain soil enzymes may be activated
tropical savanna into pastures did not change the taxo- by the presence of certain organic compounds, e.g. cel-
nomic richness and composition of organisms, while the lulase in the presence of cellulose with a high C to N
conversion of Brazilian rainforest caused deep changes ratio (Andersson et al., 2004; Bini et al., 2013).
in the macrofauna community, including substitution of Assessment of indicators of soil health in different
native earthworms by exogenous species. Even under strategies of soil use has shown increase of total organic
temperate conditions, the total abundance and species carbon and ammonification rate in forestry soils (Noguei-
composition decreased with the intensification of land ra et al., 2006). In addition, the C and N microbial bio-
use (Ponge et al., 2003). Similarly, Baretta et al. (2007) masses in the secondary and artificially reforested sites
reported that the diversity, abundance, and biomass of after 20 years tended to approximate values of the native
earthworms in native or reforested Brazil Pine (A. angus- forest, but in a site under Eucalyptus for 50 years, values
tifolia) forests were sensitive enough to distinguish the were similar to an agricultural fallow site. Assessments
sites under different land-use. of indicators of soil health are particularly important to
A spruce (Picea abies) forest in the Italian Alps evaluate the success of a given strategy for reclamation
(Salmon et al., 2008) revealed strong changes in com- of degraded forestry environments (Bastida et al., 2006;
position of organisms and also in soil C mineralization. Nogueira et al., 2006). Greater emphasis has been given
Great abundance of mites (Acari) was favored by the to biological and biochemical indicators due to their
recalcitrant plant residue, but there was low density of greater sensitivity (Wink et al., 2005). Soil enzyme ac-
springtails and absence of several other groups of soil tivities have also been widely employed in forestry soils
macrofauna. Conversely, during the different succes- to assess effects of changes in land use (Bastida et al.,
sional stages, there was a continuous up and down of 2008; Lucas-Borja et al., 2010; Fagotti et al., 2012; Bini et
several groups of invertebrates. The richness of the soil al., 2013). Despite their high sensitivity to environmen-
fauna was greater during the periods of revegetation, tal conditions, soil enzymes are also sensitive to seasonal
when the soil cover consisted of diverse growing trees variations. For example, dehydrogenase was the lowest
and abundant herbaceous vegetation. Similar results in the autumn due to low temperatures that restricted
were obtained by Lucas-Borja et al. (2010) in a study the soil microbial activities, while the activity of urease
with pine forests. was inversely correlated with the concentrations of am-
One of the most important factors affecting bio- monium in soil when both plants and microorganisms
logical indicators of soil health in forestry environments were less active. On the other hand, phosphatase and
is the C to N ratio of the plant residues. Thus, changes arylsulphatase were not affected by temperature, but de-
in the structure of plant community, like conversion pended on the amount of litter on the soil surface (Kang
of native forest to monocultures, deeply alters the bio- et al., 2009).

283
Assessment of C and N microbial biomass, soil res- Nowadays, several industrial and urban residues
piration and enzyme activities are correlated with the have also been applied as alternative sources of nutri-
content of soil organic matter and the age of successional ents in agriculture, but many times without the appro-
stages (Jiang et al., 2009) and are generally lower in ag- priate studies on their potential environmental impacts.
ricultural soils when compared to native forests, a fact Due to its capacity for cycling a large sort of residues,
attributed to less C inputs (Dinesh et al., 2003; Kaschuk soil has been seen as the receiving end of residues pro-
et al., 2010; Bini et al., 2013). Additionally, the enzyme duced by several activities. Nevertheless, depending on
activities also correlate with the soil microbial biomass the nature and amount of residues, the soil's biological
(Jiang et al., 2009). Forest cleaning, cropping and man- capacity for recycling may be exceeded, leading to soil
agement affect the soil microbial diversity and activity contamination and interruption of several ecological
(Degens et al., 2000, Stark et al., 2008). Decrease in mi- functions.
crobial activity in intensively managed soil in compari- Landfarming aiming at microbial degradation of
son to well managed pastures has been observed (Rif- the organic fraction of petrochemical residues is an
faldi et al., 2002). In general, the maintenance of soil example of soil use as an efficient bioreactor (Dua et
organic C is the main factor that favors the microbial al., 2002; Tyagi et al., 2011). Nevertheless, presence
activity (Lizarazo et al., 2005). of heavy metals, salts and recalcitrant compounds
In natural ecosystems, the rate between input and sometimes leads to reduction of soil microbial activity.
decomposition of organic material is under dynamic bal- Paula et al. (2006) observed that although total micro-
ance, with predominance of mineralization of nutrients. bial biomass, culturable bacteria and fungi were simi-
Bastida et al. (2006) observed less microbial and bio- lar among agricultural soils and landfarming of pet-
chemical activities in soils even after 15 years after de- rochemical residues, the metabolic coefficient (qCO2)
forestation and start of the vegetation reestablishment. and activities of β-glycosidase, acid phosphatase, and
Similar results were observed in a secondary forest un- urease indicated that the long-term soil use as land-
der regeneration for 20 years (Nogueira et al., 2006). In farming could lead to a loss of the soil's capacity to
general, the levels of soil organic carbon increase with degrade residues.
the vegetation recovery (Jiang et al., 2009; Chodak and The use of urban residues in agriculture, like sludge
Niklinska, 2010; Bautista-Cruz et al., 2012), but this is from sewage treatment plants, liquid effluent from treat-
generally a slow process. ed sludge, and composted domiciliary waste, has two
Besides the decreases in the soil organic carbon main environmental objectives: nutrient cycling and al-
levels, changes in other physical-chemical attributes also ternative destination of residues, instead of disposition
affect the microbial activity in degraded soils. Erosion is in sanitary landfills or discharge in surface waters. More-
one of the main factors affecting the physical soil con- over, these residues can also be used for reclamation of
ditions, in addition to soil compaction and decrease in degraded soils (Tamanini et al., 2008). Due to the general
aggregate stability (Hartanto et al., 2003). The increase predominance of organic matter, sewage sludge or com-
of the soil bulk density due to traffic of machines or ani- posted domiciliary wastes increase the soil organic mat-
mals and the loss of aggregate stability due to decrease ter, and consequently its water holding capacity and nu-
in the soil organic carbon directly affect the plant root trients, and stimulate the soil microbial activity (Oliveira
development and the water and air dynamics within the et al., 2002; Betiol and Fernandes, 2004). Nevertheless,
soil. the main concerns on the risks of using residues on soil
As observed, the main causes of changes in diver- health are the presence of high levels of heavy metals
sity and activity of microbial community and fauna in and other organic or inorganic contaminants (Lara et al.,
forest soils is the quantity and quality of residues that re- 1999). Despite established criteria for application of resi-
turn to the soil surface, and consequently, the soil organ- dues in soil (e.g., USEPA, 1995; CONAMA, 2006), most
ic matter levels. Nevertheless, in order to better under- of them are based on human health, whereas less atten-
stand the effects of use and management on soil health, tion has been given to the potential risks on soil health
physical, chemical, and biological attributes should be (Passuello et al., 2010).
assessed altogether because they are interconnected and The use of urban or industrial residues as irriga-
run mutual interferences, although they have different tion water and also as complementing source of nutri-
levels of responsiveness to changes. ents may represent risks for soil health, depending on
its characteristic (Toze, 2006). For this reason, monitor-
Indicators of soil health in soils amended with resi- ing of biological, chemical and physical indicators of
dues soil health is essential for safer strategies for the ap-
Residues like cattle, poultry, and pig dung have plication of residues. Fonseca et al. (2007) concluded
historically been used in agricultural soils. Besides act- that irrigation of crops with effluent from treated sew-
ing as source of nutrients, notably nitrogen and phos- age is economically and environmentally feasible, but
phorus, animal residues also contribute to improve soil the accumulation of sodium in the soil and losses of
physical and chemical properties (Haynes and Naidu, nitrogen by leaching or volatilization must be regularly
1998). monitored to avoid environmental risks. In addition to

284
chemical attributes, monitoring microbial activity can materials, avoiding environmental contamination of riv-
also provide essential information on the soil health ers, soil and atmosphere and minimizing the production
under a specific management, especially concerning to of greenhouse gases, thereby giving back to the soil over
nutrient cycling (Paula et al., 2010). Thus, the monitor- 90 % of the organic materials today being considered
ing of soil functions in sites used for receiving residues useless trash. Another decisive point is the development
is essential to prevent the soil degradation. In addition, of processes and methodologies to study ecotoxicological
monitoring of chemical or even biological contaminants aspects of all kinds of residues, independently of origin,
is also important to prevent any adverse effect on soil creating an interface with human health. Undoubtedly,
functions and plant growth and health. As a more com- we can claim that public health depends on healthy food,
prehensive strategy, a pool of indicators can be useful and this, in turn, is directly linked to the soil health. Fi-
for monitoring the impacts of application of residues on nally, soil health is the first requirement for agricultural
soil health. and environmental sustainability.
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Cardoso et al. Scientia

USP/ESALQ – Depto. de Ciência do Solo, Lab. de

Introduction and exert environmental functions, must be monitored

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Microbiological and biochemical indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Final remarks References

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

Cardoso et al. Soil health: looking for suitable indicators

Sci. Agric. v.70, n.4, p.274-289, July/August 2013

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