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Soil quality indicators under management systems in a Quilombola community in the Brazilian Cerrado

ABSTRACT:

Soil management systems exert different effects on soil attributes, especially on the organic matter content, and, consequently, the soil aggregation. The aim of this study was to evaluate the impact of different land uses practiced by quilombola family farmers on water stable aggregates, glomalin and organic carbon in soil aggregates. Soil samples were collected at depths of 0-10 and 10-20 cm from areas cultivated under the following management systems: 1) conventional corn plantation (MA), 2) cultivation of citrus trees intercropped with annual crops (AC) (a conservationist approach), 3) pasture of Brachiaria (Urochloa spp.) (PA), and, as reference, an area of the Cerrado (CR) free of any anthropogenic interference. The studied areas were evaluated in a completely randomized design, with five replications, in a subplot scheme. The plots were the management systems and the subplots the depths. Soil macro-aggregates were predominant at both depths and the aggregate stability indices were higher than 90 % for all management systems. Total organic carbon in the two aggregate classes (micro and macro-aggregates) correlated with the MWD (mean weight-diameter), but not with the easily extractable glomalin (EEG) related soil protein. Soil micro and macro-aggregates, EEG and MWD discriminated management systems and are important soil quality indicators. The carbon content in both micro-aggregates (C-MIC) and macro-aggregates (C-MAC) of the intercropped system (AC) was higher than in the CR. The soil attributes that best separated the areas were C-MIC, MWD and EEG in macro-aggregates for the depth of 0-10 cm, and EEG in micro-aggregates, together with MWD and C-MAC for the depth of 10-20 cm.

Keywords:
Rhodic Hapludox; water-stable aggregates; soil protein; quilombo

Introduction

In Brazil, the Cerrado is the second largest biome, after the Amazon, and much of it is located in the Central Plateau, consisting of flat areas, shrub vegetation and marked seasonality with abundant summer rains (Dec to Mar) and dry winters (May to Sept) (Buol, 2009Buol, S.W. 2009. Soils and agriculture in central-west and north Brazil. Scientia Agricola 66: 697-707.). In the Brazilian Cerrado, there are communities formed by ethnic-racial groups with a presumption of African ancestry, called quilombolas (INCRA, 2017Instituto Nacional de Colonização e Reforma Agrária [INCRA]. 2017. Quilombola Politics = Política Quilombola. Available at: http://www.incra.gov.br/quilombola [Accessed Jan 10, 2017] (in Portuguese).
http://www.incra.gov.br/quilombola...
). These communities practice family farming, based on giving due esteem to the local and traditional knowledge of farmers in order not to interfere with natural resources and processes. The agricultural management practices applied in quilombola communities do not have any technical assistance, which, in time, leads to a decrease in productivity. Thus, it is necessary to evaluate soil quality (SQ) indicators of the areas used by these communities in order to contribute to greater productivity (Nascimento et al., 2017Nascimento, R.S.M.P.; Ramos, M.L.G.; Figueiredo, C.C.; Silva, A.M.M.; Silva, S.B.; Batistella, G. 2017. Soil organic matter pools under management systems in Quilombola territory in Brazilian Cerrado. Revista Brasileira de Engenharia Agrícola e Ambiental 21: 254-260.).

SQ is the ability of soil to sustain productivity and biological diversity as well as promoting the health of the organisms that inhabit the area (Doran and Safley, 1997Doran, J.W.; Safley, M. 1997. Defining and assessing soil health and sustainable productivity. p. 1-28. In: Pankhurst, C.E.; Doube, B.M.; Gupta, V.V.S.R., eds. Biological indicators of soil health. CAB International, Wallingford, UK.), thus resulting in soil functionality and sustainability of the system consisting of soil, plants, and microorganisms (Cardoso et al., 2013Cardoso, E.J.B.N.; Vasconcellos, R.L.F.; Bini, D.; Miyauchi, M.Y.H.; Santos, C.A.; Alves, P.R.L.; Paula, A.M.; Nakatani, A.S.; Pereira, J.M.; Nogueira, M.A. 2013. Soil health: looking for suitable indicators; what should be considered to assess the effects of use and management on soil health? Scientia Agricola 70: 274-289.). Soil aggregates and the porous soil system integrated into the soil structure are key components of SQ (Pires et al., 2017Pires, L.F.; Borges, J.A.R.; Rosa, J.A.; Cooper, M.; Heck, R.J.; Passoni, S.; Roque, W.L. 2017. Soil structure changes induced by tillage systems. Soil and Tillage Research 165: 66-79.).

The formation and stability of aggregates results from the interaction between biotic and abiotic factors (Tisdall and Oades, 1982Tisdall, J.M.; Oades, J.M. 1982. Organic matter and water stable aggregates in soils. Journal of Soil Science 33: 141-163.). Among the factors that affect the formation of aggregates and their stability, are the arbuscular mycorrhizal fungi (AMF) (Rillig et al., 2015Rillig, M.C.; Aguilar-Trigueros, C.A.; Bergmann, J.; Verbruggen, E.; Veresoglou, S.D.; Lehmann, A. 2015. Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytologist 205: 1385-1388.) which, together with plant roots, form the symbiotic mycorrhizae. AMF synthesize in their hyphae a compound with a cementing function, consisting of a glycoprotein linked to nitrogen, called glomalin (EEG) (Wu et al., 2014Wu, Q.S.; Cao, M.Q.; Zou, Y.N.; He, X.H. 2014. Direct and indirect effects of glomalin, mycorrhizal hyphae, and roots on aggregate stability in rhizosphere of trifoliate orange. Scientific Reports 4: 5823.). The other factors that affect SQ are soil organic matter (Kimura and Scotti, 2016Kimura, A.C.; Scotti, M.R. 2016. Soil aggregation and arbuscular mycorrhizal fungal indicators of slope rehabilitation in the São Francisco River basin (Brazil). Soil and Water Research 11: 114-123.), soil texture (Gonçalves et al., 2017Gonçalves, D.R.P.; Sá, J.C.M.; Mishra, U.; Cerri, C.E.P.; Ferreira, L.A.; Furlan, F.J.F. 2017. Soil type and texture impacts on soil organic carbon storage in a sub-tropical agro-ecosystem. Geoderma 286: 88-97.), soil fauna (Jouquet et al., 2016Jouquet, P.; Chintakunta, S.; Bottinelli, N.; Subramanian, S.; Caner, L. 2016. The influence of fungus-growing termites on soil macro and micro-aggregates stability varies with soil type. Applied Soil Ecology 101: 117-123.), and plant and microorganism diversity (Gould et al., 2016Gould, I.J.; Quinton, J.N.; Weigelt, A.; De Deyn, G.B.; Bardgett, R.D. 2016. Plant diversity and root traits benefit physical properties key to soil function in grasslands. Ecology Letters 19: 1140-1149.), among others. Conventional management, with intense plowing and tilling, often lead to crop systems with low plant biomass diversity, resulting in changes in the soil physical, chemical and biological attributes (Ahmed et al., 2017Ahmed, E.H.; Anjum, S.I.; Zhang, M. 2017. Effects of fertilization on phosphorus distribution in water-stable aggregates of soils with different properties. Toxicological & Environmental Chemistry 2248: 32-47.).

Thus, the aim of the present study was to evaluate the effect of land uses employed by quilombola family farmers on soil properties and finally on soil quality.

Materials and Methods

The study was carried out in a quilombola community (Quilombo Mesquita) belonging to the municipality of Cidade Ocidental in the eastern region of the state of Goiás, Brazil (16°04’41” S and 47°52’05” W), at an altitude of 1014 m. The climate of the region, according to Köppen's classification, is type Cwa – high altitude tropical, with well-defined dry and rainy seasons. The mean annual temperature is 21 °C and the mean annual rainfall 1,500 mm (Alvares et al., 2013Alvares, C.A; Stape, J.L.; Sentelhas, P.C.; Gonçalves, J.L de M.; Sparovek, G. 2013. Köppen's climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728.).

The soil is a Rhodic Hapludox (Soil Survey Staff, 2010Soil Survey Staff. 2010. Keys to Soil Taxonomy. 11ed. USDANRCS, Washington, DC, USA.), and the physical and chemical soil properties have been described by Nascimento et al. (2017)Nascimento, R.S.M.P.; Ramos, M.L.G.; Figueiredo, C.C.; Silva, A.M.M.; Silva, S.B.; Batistella, G. 2017. Soil organic matter pools under management systems in Quilombola territory in Brazilian Cerrado. Revista Brasileira de Engenharia Agrícola e Ambiental 21: 254-260. (Table 1). Distinct historical management systems that were predominantly used by the quilombola community were selected (Table 2): 1) conventional corn planting (MA), 2) cultivation of citrus trees intercropped with annual crops (AC) (a conservationist approach), 3) Brachiaria (Urochloa spp.) pasture (PA). In addition to the cultivated areas, an area of the Cerrado (CR), free from any anthropogenic interference, was used as a reference.

Table 1
Soil particle size distribution and chemical characteristics under the investigated management systems at 0-20 cm depth.
Table 2
Description and history of the management systems.

We took soil samples along an imaginary diagonal line at depths of 0-10 and 10-20 cm in Jan 2016. The localization of the studied areas and the soil sampling points can be found in Figure 1. We obtained five subsamples at every 50 m to construct a composite sample. We collected samples in the row and between rows of the conventional corn cultivation system (MA) and in the shadow of treetops in the conservation system of citrus trees intercropped with annual crops (AC). The soil monoliths, collected to analyze the stability of the aggregates in water, were stored in plastic bags to maintain moisture and the stability of their structure. We fractioned all the soil making up the samples, according to points of weakness, so that the total sample volume would pass through an 8.0 mm sieve. Fragments of plants, cuttings and other residues that were retained on the sieve were excluded from the analysis. We used air-dried samples for subsequent analyses.

Figure 1
Localization of studied areas and points of soil collection in Quilombo Mesquita (CR = Native Cerrado; AC = Cultivation of citrus trees intercropped with annual crops; PA = Pasture of Brachiaria (Urochloa spp.); MA = Conventional corn planting).

Stability of the soil aggregates was determined by the vertical wet sieving method in a Yoder device (Yoder, 1936Yoder, R.E. 1936. A direct method of aggregate analysis of soil and a study of the physical nature of erosion losses. Agronomy Journal 28: 337-351.), which consists of separating the aggregates into size classes (Silva et al., 2016aSilva, A.N.; Figueiredo, C.C.; Carvalho, A.M.; Soares, D.S.; Santos, D.C.R.; Silva, V.G. 2016a. Effects of cover crops on the physical protection of organic matter and soil aggregation. Australian Journal of Crop Science 10: 1623-1629.). From the values of the aggregate masses, we calculated the following parameters: (1) the mean weight-diameter (MWD) and (2) the aggregate stability index (ASI).

(1) M W D = i = 1 n ( x i w i )
(2) A S I = ( D r y s a m p l e w e i g h t w p 25 s a n d D r y s a m p l e w e i g h t s a n d )

where: wi = proportion (%) of each class i in relation to the total aggregate weight; xi = mean diameter of class i, obtained by [(upper mesh + lower mesh):2]; and wp25 = weight of aggregates of the class < 250 µm.

The aggregates were subdivided into micro-aggregates (< 250 μm) and macro-aggregates (> 250 μm). The total organic carbon of each class of aggregates was quantified using oxidation by potassium dichromate according to the method of Walkley and Black (1934)Walkley, A.; Black, I.A. 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37: 29-38.. Easily extractable glomalin (EEG) related soil protein of each aggregate class was extracted from the soil according to the methodology of Wright and Upadhyaya (1998)Wright, S.F.; Upadhyaya, A. 1998. A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant and Soil 198: 97-107. and quantified by the Bradford test (Bradford, 1976Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72: 248-254.) using bovine serum albumin (BSA) as standard. We measured absorbance at 595 nm in a colorimeter (Carrizo et al., 2015Carrizo, M.E.; Alesso, C.A.; Cosentino, D.; Imhoff, S. 2015. Aggregation agents and structural stability in soils with different texture and organic carbon contents. Scientia Agricola 72: 75-82.).

The areas were analyzed in a completely randomized design, with five replications in subplots, where the plots were the management systems and the subplots the depths. The data were submitted to analysis of variance, after having met the normality criteria of the residues and homogeneity of variance, and subsequently multiple comparisons of the means were submitted to Tukey's test (p ≤ 0.05). We used canonical discriminant analysis (CDA) to separate the studied areas according to the analyzed variables. In addition, Pearson's correlation was plotted with the use of the program (R Core Team, 2017) and graphs were generated using MS Excel.

Results and Discussion

Distribution of water-stable aggregates

Soil macro-aggregates were predominant (around 90 %) at the depths evaluated in all systems (Figure 2). In areas of native Cerrado, we obtained similar results, with more than 90 % of macro-aggregates stable in water (Bertolin et al., 2016Bertolin, F.; Bono, J.A.M.; Macedo, M.C.M.; Araújo, A.R.; Pereira, F.A.R. 2016. Use and management of pasture in the Cerrado biome: impacts on aggregation of an oxisol. African Journal of Agricultural Research 11: 2139-2145.). This may be related to the high clay content found in all management systems (Table 1), because there is a positive correlation of clay content with soil aggregation (Liu et al., 2012Liu, X.H.; Han, F.P.; Zhang, X.C. 2012. Effect of biochar on soil aggregates in the Loess Plateau: results from incubation experiments. International Journal of Agriculture and Biology 14: 975-979.). Soils in tropical climates are highly influenced by electrostatic interactions between oxides and clay minerals of the 1:1 type in the aggregation process, forming micro-aggregates, which aggregate again by the action of biological agents, and form macro-aggregates (Costa Júnior et al., 2012Costa-Junior, C.; Píccolo, M.C.; Siqueira Neto, M.; Camargo, P.B.; Cerri, C.C.; Bernoux, M. 2012. Carbon in soil aggregates under native vegetation, pasture and agricultural systems in the Brazilian Savannah. Revista Brasileira de Ciência do Solo 36: 1311-1321 (in Portuguese, with abstract in English).).

Figure 2
Relative distribution of stable aggregates in water at depths of 0-10 cm and 10-20 cm submitted to the different management systems. CR = Native Cerrado; PA = Pasture of Brachiaria (Urochloa spp.); MA = Conventional corn planting; AC = Cultivation of citrus trees intercropped with annual crops.

There was no difference between the relative distribution of micro and macro-aggregates in the analyzed management systems (p < 0.05), suggesting that they do not interfere with the distribution of stable aggregates in water (Figure 2). Additionally, there were no changes in the percentage of micro and macro-aggregates in the MA system, where harrowing practices were applied; and this may be related to the effect of lime application in 2011 and continuous crop rotation with rice (Oryza sativa L.), beans (Phaseolus vulgaris L.), and corn (Zea mays L.), for 20 years (Table 2). Silva et al. (2016b)Silva, F.R.; Albuquerque, J.A.; Costa, A.; Fontoura, S.M.V.; Bayer, C.; Warmling, M.I. 2016b. Physical properties of a Hapludox after three decades under different soil management systems. Revista Brasileira de Ciência do Solo 40: e0140331. reported that the application of limestone into a Rhodic Hapludox (the same as the one used in our study), increased the growth of root biomass and, consequently, the increase in aggregate stability.

All management systems presented distribution of water-stable aggregates similar to the reference area (CR) (Figure 2), indicating that, after several years of different soil management systems, there was no alteration of aggregate distribution. Soil aggregation seems to be favored by greater soil microbial diversity and active root growth, which allows an increase in interactions between microorganisms, soil and plants (Six et al., 2002Six, J.; Feller, C.; Denef, K.; Ogle, S.M.; Moraes, J.C.; Albrecht, A. 2002. Soil organic matter, biota and aggregation in temperate and tropical soils: effects of no-tillage. Agronomie 22: 755-775.; Tivet et al., 2013Tivet, F.; Sá, J.C.M.; Lal, R.; Borszowskei, P.R.; Briedis, C.; Santos, J.B.; Sá, M.F.M.; Hartman, D.C.; Eurich, G.; Farias, A.; Bouzinac, S.; Séguy, L. 2013. Soil organic carbon fraction losses upon continuous plow-based tillage and its restoration by diverse biomass-C inputs under no-till in sub-tropical and tropical regions of Brazil. Geoderma 209-210: 214-225.). Consequently, there may be a greater release of organic exudates that act as cementing agents between soil particles (Wang et al., 2017Wang, Z.H.; Fang, H.; Chen, M. 2017. Effects of root exudates of woody species on the soil anti-erodibility in the rhizosphere in a karst region, China. Peer J 5: e3029.).

Mean weight-diameter (MWD)

The management system applied to the area with citrus trees intercropped with annual crops (AC) stood out from the other management systems evaluated for promoting significant variation (p < 0.05) in the MWD between the depths, with the highest values at 10-20 cm (Figure 3A). For the 0-10 cm depth, the AC, CR and PA systems presented the highest MWD values and did not differ between themselves (p < 0.05). For the depth of 10-20 cm, the AC system presented higher MWD and the MA was the management system with the lowest MWD.

Figure 3
A) Mean weight-diameter (MWD), B) aggregate stability index (ASI), C) total organic carbon in macro-aggregates (C-MAC), D) total organic carbon in micro-aggregates (C-MIC), E) easily extracted glomalin-related soil protein in macro-aggregates (EEG-MAC), F) and easily extracted glomalin-related soil protein in micro-aggregates (EEG-MIC) of soil submitted to different management systems. MA = Conventional corn planting; PA = Pasture of Brachiaria (Urochloa spp.); AC = Cultivation of citrus trees intercropped with annual crops; CR = Native Cerrado. Upper-case letters compare the depths within the same management system and lower-case letters compare a given depth among the different management systems by the Tukey's test at 5 % (p < 0.05) (n = 5).

For the last 10 years, the MA has been cultivated only with corn. The AC system was cultivated for 21 years with U. decumbens and fertilized with cattle manure. This same system was cultivated with C. reticulata intercropped with corn/beans/cassava for four years and in the last two years this area was intercropped only with cassava (Table 2). Soil management in AC promoted higher MWD, probably due to a higher biodiversity above and below the soil surface, which has the potential to restore soil health (Cardoso et al., 2013Cardoso, E.J.B.N.; Vasconcellos, R.L.F.; Bini, D.; Miyauchi, M.Y.H.; Santos, C.A.; Alves, P.R.L.; Paula, A.M.; Nakatani, A.S.; Pereira, J.M.; Nogueira, M.A. 2013. Soil health: looking for suitable indicators; what should be considered to assess the effects of use and management on soil health? Scientia Agricola 70: 274-289.).

The addition of plant biomass promotes the entry of easily decomposable carbon into the soil and favors an increase in the MWD. This effect is dependent on the quantity and quality of the organic material being supplied and may exhibit transient effects on the stability of aggregates (Lal, 2015Lal, R. 2015. Soil carbon sequestration and aggregation by cover cropping. Journal of Soil and Water Conservation 70: 329-339.). Moreover, the greater diversity of the planted species, especially grasses, due to their higher root biomass, increases the total organic carbon (TOC) and soil aggregate stability (Pérès et al., 2013Pérès, G.; Cluzeau, D.; Menasseri, S.; Soussana, J.F.; Bessler, H.; Engels, C.; Habekost, M.; Gleixner, G.; Weigelt, A.; Weisser, W.W.; Scheu, S.; Eisenhauer, N. 2013. Mechanisms linking plant community properties to soil aggregate stability in an experimental grassland plant diversity gradient. Plant and Soil 373: 285-299.). In the case of a Rhodic Hapludox, the organic-mineral interaction between carbohydrates and the mineral surface of clay is one of the most important mechanisms in the formation of soil aggregates (Hanke and Dick, 2017Hanke, D.; Dick, D.P. 2017. Aggregate stability in soil with humic and hystic horizons in a toposequence under araucaria forest. Revista Brasileira de Ciência do Solo 41: e0160369.).

We expected that the PA system would present higher MWD than the AC system, since it is known that areas under pasture have a greater tendency to present high levels of soil aggregation because of their fasciculate root system. They produce up to six Mg ha–1 of root biomass in the 0-30 cm layer (McNally et al., 2015McNally, S.R.; Laughlin, D.C.; Rutledge, S.; Dodd, M.B.; Six, J.; Schipper, L.A. 2015. Root carbon inputs under moderately diverse sward and conventional ryegrass-clover pasture: implications for soil carbon sequestration. Plant and Soil 392: 289-299.), and these are constantly renewed. However, in the present study, the MWD in the PA was lower than in the AC in the 10-20 cm layer (Figure 3A), which could also be associated with lower content of silt and clay in PA in the 0-20 cm layer (Table 2). Soil textures with a higher silt and clay content are capable of binding C to the primary organic-mineral complex into silt-sized aggregates (Tisdall and Oades, 1982Tisdall, J.M.; Oades, J.M. 1982. Organic matter and water stable aggregates in soils. Journal of Soil Science 33: 141-163.).

The MWD is dependent on plant root activity as well as on the quality and amount of metabolites which include organic acids and several other compounds secreted in the rhizosphere (Wang et al., 2017Wang, Z.H.; Fang, H.; Chen, M. 2017. Effects of root exudates of woody species on the soil anti-erodibility in the rhizosphere in a karst region, China. Peer J 5: e3029.).

Such metabolites also select groups of microorganisms well adapted to the make up of the soil biodiversity thus assisting in the formation of the soil structure (Xiao et al., 2017Xiao, S.; Zhang, W.; Ye, Y.; Zhao, J.; Wang, K. 2017. Soil aggregate mediates the impacts of land uses on organic carbon, total nitrogen, and microbial activity in a Karst ecosystem. Scientific Reports 7: 41402.).

We compared the general distribution of micro and macro-aggregates with the MWD, and found no influence on the distribution of stable macro and micro-aggregates in water (Figure 2). However, the MWD was lower in the MA system (Figure 3A) for both depths. This result may be related to the history of the area (Table 2) and the management system in which plowing and harrowing had been carried out every two years over the last 15 years.

Aggregate stability index (ASI)

There was no influence of ASI by soil use and management system (Figure 3B). Most of the aggregates were larger than 250 μm. However, their size distribution did not differ within management systems. The mineralogy of tropical soils is possibly the factor that results in increased stability of aggregates via the greater organic-mineral interaction (Madari et al., 2005Madari, B.E.; Machado, P.L.O.A.; Torres, E.; Andrade, A.G.; Valencia, L.I.O. 2005. No tillage and crop rotation effects on soil aggregation and organic carbon in a Rhodic Ferralsol from southern Brazil. Soil and Tillage Research 80: 185-200.; Hanke and Dick, 2017Hanke, D.; Dick, D.P. 2017. Aggregate stability in soil with humic and hystic horizons in a toposequence under araucaria forest. Revista Brasileira de Ciência do Solo 41: e0160369.). A higher ASI was expected in the system with greater species diversity (AC), including the reference area (CR), since both could promote a greater diversity of root exudates of different compositions, guaranteeing greater carbon source diversity in the soil system (Silva et al., 2016aSilva, A.N.; Figueiredo, C.C.; Carvalho, A.M.; Soares, D.S.; Santos, D.C.R.; Silva, V.G. 2016a. Effects of cover crops on the physical protection of organic matter and soil aggregation. Australian Journal of Crop Science 10: 1623-1629.). In addition to the biological diversity of natural systems that improves the stability of soil aggregates, another controversial aspect refers to spontaneous burning in the Cerrado that may or may not promote an increase in the stability of these aggregates (Thomaz, 2017Thomaz, E.L. 2017. High fire temperature changes soil aggregate stability in slash-and-burn agricultural systems. Scientia Agricola 74: 157-162.; Hobley et al., 2017Hobley, E.U.; Le Gay Brereton, A.J.; Wilson, B. 2017. Forest burning affects quality and quantity of soil organic matter. Science of the Total Environment 575: 41-49.; Zhang et al., 2017Zhang, M.; Cheng, G.; Feng, H.; Sun, B.; Zhao, Y.; Chen, H.; Chen, J.; Dyck, M.; Wang, X.; Zhang, J.; Zhang, A. 2017. Effects of straw and biochar amendments on aggregate stability, soil organic carbon, and enzyme activities in the Loess Plateau, China. Environmental Science and Pollution Research 24: 10108-10120.).

Despite this, the ASI value found for the management systems lies within the range commonly found for tropical soils (82 ± 6 %) (Thomaz, 2017Thomaz, E.L. 2017. High fire temperature changes soil aggregate stability in slash-and-burn agricultural systems. Scientia Agricola 74: 157-162.). This may also be indicative of high resilience of the soils in these areas, which, according to history, have been cultivated for at least 20 years (Table 2).

The total organic carbon in micro and macro-aggregates

The total organic carbon content (TOC) in both the micro (C-MIC) and macro-aggregates (C-MAC) of the soil differed between the depths (p < 0.05) only in the reference area (CR) (Figures 3C and D). At the depth of 0-10 cm, the C-MAC contents presented the following order: AC > CR > MA > PA (p < 0.05) (Figure 3D), while at that same depth the concentrations of C-MIC occurred in the following order: AC > CR = MA > PA (p < 0.05) (Figure 3C). At the 10-20 cm depth, the contents of C-MAC and C-MIC followed the same trend: AC > MA> PA = CR (p < 0.05) (Figures 3C and D).

The AC management system showed higher TOC in the micro and macro-aggregates, possibly due to intercropping with tangerine (Citrus reticulata L.) and cassava (Manihot esculenta L.), and fertilization with cattle manure and accumulation of plant residues on the soil surface in the AC system. Lack of soil disturbance including the continuous root growth promoted by intercropping are all factors that result in the improvement of aggregation and the supply of carbon (C) to the soil.

Carbon retained within the micro-aggregates seems to be protected physically and chemically as well as a predominance of iron and aluminum oxide in tropical soil. Thus, the micro-aggregates can present high stability and behave like sand particles, and increase the C reserves in the soil (Braida et al., 2011Braida, J.A.; Bayer, C.; Albuquerque, J.A.; Reichert, J.M. 2011. Organic matter and its effect on soil physics = Matéria orgânica e seu efeito na física do solo. p. 222-227. In: Filho, O.K.; Mafra, A.L.; Gatiboni, L.C., eds. Topics in Soil Science = Tópicos em Ciência do Solo. Sociedade Brasileira de Ciência do Solo, Viçosa, MG, Brazil (in Portuguese).; Silva et al., 2016aSilva, A.N.; Figueiredo, C.C.; Carvalho, A.M.; Soares, D.S.; Santos, D.C.R.; Silva, V.G. 2016a. Effects of cover crops on the physical protection of organic matter and soil aggregation. Australian Journal of Crop Science 10: 1623-1629.). In addition to protection in micro-aggregates, C may have some protection in the macro-aggregates, according to the pore sizes (Kravchenko et al., 2015Kravchenko, A.N.; Negassa, W.C.; Guber, A.K.; Rivers, M.L. 2015. Protection of soil carbon within macro-aggregates depends on intra-aggregate pore characteristics. Scientific Reports 5: 16261.).

TOC contents in macro and micro-aggregates, obtained in our work, were greater than the contents obtained by Silva et al. (2016aSilva, A.N.; Figueiredo, C.C.; Carvalho, A.M.; Soares, D.S.; Santos, D.C.R.; Silva, V.G. 2016a. Effects of cover crops on the physical protection of organic matter and soil aggregation. Australian Journal of Crop Science 10: 1623-1629.) in a clay-textured Rhodic Hapludox in the Cerrado, with a mean value of 18.94 g C kg–1 and 15.15 g C kg–1 for micro and macro-aggregates, respectively. The authors found no statistical differences in C content in soil cultivated with six cover crops in either micro or macro-aggregates.

It is known that the dynamics of C in soil is affected by different management practices (Nadal-Romero et al., 2016Nadal-Romero, E.; Cammeraat, E.; Pérez-Cardiel, E.; Lasanta, T. 2016. How do soil organic carbon stocks change after cropland abandonment in Mediterranean humid mountain areas? Science of the Total Environment 566-567: 741-752.), but it is still unclear which class of soil aggregates is more responsible for the accumulation of C and which soils, depths and management factors are decisive in this process (Fernández et al., 2010Fernández, R.; Quiroga, A.; Zorati, C.; Noellemeyer, E. 2010. Carbon contents and respiration rates of aggregate size fractions under no-till and conventional tillage. Soil and Tillage Research 109: 103-109.). The management systems promoted increases in TOC as compared to levels in the Cerrado (CR) at the 10-20 cm depth (except for PA C-MIC). However, in the 0-10 cm layer, only AC increased TOC when compared with CR (both in micro and macro-aggregates).

Easily extractable glomalin-related to soil protein in micro and macro-aggregates

The EEG content exhibited a behavior similar to the carbon content in micro and macro-aggregates of the soil (Figure 3E and F), which reinforces the concept that EEG is an important source of soil organic carbon (Zhang et al., 2017Zhang, M.; Cheng, G.; Feng, H.; Sun, B.; Zhao, Y.; Chen, H.; Chen, J.; Dyck, M.; Wang, X.; Zhang, J.; Zhang, A. 2017. Effects of straw and biochar amendments on aggregate stability, soil organic carbon, and enzyme activities in the Loess Plateau, China. Environmental Science and Pollution Research 24: 10108-10120.). The highest EEG levels were found in the AC system, differing between the depths evaluated only in the EEG-MAC (p < 0.05), and the systems with the least EEG were the MA and PA (Figure 3E). It has also been reported elsewhere in the literature that conservationist soil management with greater plant species diversity, associated with management practices that minimize degradation of the soil structure, presents a greater tendency to produce high EEG levels (Treseder and Turner, 2007Treseder, K.K.; Turner, K.M. 2007. Glomalin in ecosystems. Soil Science Society of America Journal 71: 1257.; Vasconcellos et al., 2016Vasconcellos, R.L.F.; Bonfim, J.A.; Baretta, D.; Cardoso, E.J.B.N. 2016. Arbuscular mycorrhizal fungi and glomalin-related soil protein as potential indicators of soil quality in a recuperation gradient of the Atlantic Forest in Brazil. Land Degradation and Development 27: 325-334.).

The AC presented higher EEG than the CR in the micro and macro-aggregates at both depths. The AC system is characterized for being a dynamic system with regard to the input of organic material, as plant residues and manure (Table 2). In addition, the establishment of the AC occurred five years ago as an integrated system and presented the largest accumulation of TOC in different fractions of the soil organic matter (Nascimento et al., 2017Nascimento, R.S.M.P.; Ramos, M.L.G.; Figueiredo, C.C.; Silva, A.M.M.; Silva, S.B.; Batistella, G. 2017. Soil organic matter pools under management systems in Quilombola territory in Brazilian Cerrado. Revista Brasileira de Engenharia Agrícola e Ambiental 21: 254-260.).

In the reference area (CR), the contribution of biomass may or may not have a different rate from the intercropped system. In other management systems, which were not evaluated in the present study, without soil disturbance, the EEG content may remain constant over time (Souza et al., 2016Souza, E.D.; Carneiro, M.A.C.; Paulino, H.B.; Ribeiro, D.O.; Bayer, C.; Rotta, L.A. 2016. Organic matter and soil aggregation after the conversion of “murundu fields” into a no-tillage system. Pesquisa Agropecuária Brasileira 51: 1194-1202 (in Portuguese, with abstract in English).), or vary due to the seasonality of precipitation (Buyer et al., 2011Buyer, J.S.; Zuberer, D.A.; Nichols, K.A.; Franzluebbers, A.J. 2011. Soil microbial community function, structure, and glomalin in response to tall fescue endophyte infection. Plant and Soil 339: 401-412.).

Macro-aggregates contained higher levels of EEG when compared to micro-aggregates, as had also been found by Vasconcellos et al. (2016)Vasconcellos, R.L.F.; Bonfim, J.A.; Baretta, D.; Cardoso, E.J.B.N. 2016. Arbuscular mycorrhizal fungi and glomalin-related soil protein as potential indicators of soil quality in a recuperation gradient of the Atlantic Forest in Brazil. Land Degradation and Development 27: 325-334., in areas of the Atlantic Forest Recovery in southeastern Brazil. In macro-aggregates, action of the fungal mycelium network provides greater stability of aggregates in water (Zou et al., 2015Zou, Y.N.; Srivastava, A.K.; Ni, Q.D.; Wu, Q.S. 2015. Disruption of mycorrhizal extraradical mycelium and changes in leaf water status and soil aggregate stability in rootbox-grown trifoliate orange. Frontiers in Microbiology 6: 1-9.) and this may be indicative of greater EEG synthesis (Kohler-Milleret et al., 2013Kohler-Milleret, R.; Le Bayon, R.C.; Chenu, C.; Gobat, J.M.; Boivin, P. 2013. Impact of two root systems, earthworms and mycorrhizae on the physical properties of an unstable silt loam Luvisol and plant production. Plant and Soil 370: 251-265.).

Relationship between the analyzed attributes

The Wilks’ Lambda multivariate test helps to discriminate between the significance of the studied attributes (Tables 3 and 4). The effect of the management system differed between the depths of 0-10 cm and 10-20 cm (Figures 4A and B). The canonical discriminant analysis (CDA) was selected to determine which attributes (or indicators) differentiate best the effect of the management systems. Contrary to principal component analysis (PCA), the CDA is a confirmatory evaluation whereas PCA is merely an exploratory analysis of the data, with no possibility of precisely determining the attributes that best distinguish the groups (Anderson and Willis, 2003Anderson, M.J.; Willis, T.J. 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-525.).

Figure 4
Relationships between the first and second canonical discriminant functions (CDF1 and CDF2) on the centroids of standardized canonical coefficients (SCC) for the attributes mean weight-diameter (MWD), aggregate stability index (ASI), organic carbon in micro and macro-aggregates (C-MIC and C-MAC) and easily extractable glomalin in micro and macro-aggregates (EEG-MIC and EEG-MAC) at depths of 0-10 cm (A) and 10-20 cm (B). CR = Native Cerrado; PA = Pasture of Brachiaria (Urochloa spp.); MA = Conventional corn planting and AC = Cultivation of citrus trees intercropped with annual crops; and (n = 5). *There is an overlapping of repetitions of the PA samples at the depth of 0-10 cm (A).
Table 3
Wilks’ Lambda test between mean weight-diameter (MWD), aggregate stability index (ASI), total organic carbon in macro-aggregates (C-MAC), total organic carbon in micro-aggregates (C-MIC), easily extractable glomalin-related soil protein in macro-aggregates (EEG-MAC) and easily extractable glomalin-related soil protein in micro-aggregates (EEG-MIC) at the depth of 0-10 cm.
Table 4
Wilks’ Lambda test between mean weight-diameter (MWD), aggregate stability index (ASI), total organic carbon in macro-aggregates (C-MAC), total organic carbon in micro-aggregates (C-MIC), easily extractable glomalin-related soil protein in macro-aggregates (EEG-MAC) and easily extractable glomalin-related soil protein in micro-aggregates (EEG-MIC) at the depth of 10-20 cm.

For the depth of 0-10 cm (Table 3), the attributes that best discriminated the areas according to the Wilks’ Lambda test were MWD (p < 0.001), C-MIC (p < 0.001), and EEG-MAC (p < 0.05). For the depth of 10-20 cm (Table 4), the attributes that best discriminated the areas were MWD (p < 0.001), C-MAC (p < 0.05) and EEG-MIC (p < 0.01). Thus, we observed that the common attribute between the two depths that best discriminated the management systems was the mean weight-diameter (MWD). At the depth of 10-20 cm the reference area (CR) and the PA system did not differ (p ≤ 0.05) in terms of the MWD, C-MIC, C-MAC, EEG-MAC and EEG-MIC (Figures 3A to F). The canonical discriminant function 1 (CDF1) explained the greatest total variability of the attributes for both depths, between 0-10 cm (62 %) and 10-20 cm (79 %), while the canonical discriminant function 2 (CDF2) explained 12 % and 16 %, respectively (Figures 4A and B).

EEG correlated with TOC, regardless of the class of aggregates (Table 5). It represents up to 52 % and 25 % of the total C content in organic and mineral soils, respectively (Schindler et al., 2007Schindler, F.V.; Mercer, E.J.; Rice, J.A. 2007. Chemical characteristics of glomalin-related soil protein (GRSP) extracted from soils of varying organic matter content. Soil Biology and Biochemistry 39: 320-329.). Thus, TOC is directly proportional to the amount of EEG present in the soil (Zhang et al., 2017Zhang, M.; Cheng, G.; Feng, H.; Sun, B.; Zhao, Y.; Chen, H.; Chen, J.; Dyck, M.; Wang, X.; Zhang, J.; Zhang, A. 2017. Effects of straw and biochar amendments on aggregate stability, soil organic carbon, and enzyme activities in the Loess Plateau, China. Environmental Science and Pollution Research 24: 10108-10120.), and studies have proven this relationship to be true in soil cultivated with crops such as citrus (Poncirus trifoliata (L.) Raf.) (Wu et al., 2015Wu, Q.S.; Li, Y.; Zou, Y.N.; He, X.H. 2015. Arbuscular mycorrhiza mediates glomalin-related soil protein production and soil enzyme activities in the rhizosphere of trifoliate orange grown under different P levels. Mycorrhiza 25: 121-130.) and corn (Zea mays L.) (Koide and Peoples, 2013Koide, R.T.; Peoples, M.S. 2013. Behavior of Bradford-reactive substances is consistent with predictions for glomalin. Applied Soil Ecology 63: 8-14.).

Table 5
Pearson's correlation among the attributes studied (MWD = mean weight-diameter, C-MIC = organic carbon in the micro-aggregates, C-MAC = organic carbon in the macro-aggregates, EEG-MIC = easily extractable glomalin-related soil protein in micro-aggregates and EEG-MAC = easily extractable glomalin-related soil protein in macro-aggregates).

The MWD did not correlate with the EEG-MAC or the EEG-MIC (Table 4), indicating that EEG contributed more to carbon storage than MWD in the present study.

Conclusions

Soil macro and micro-aggregates, EEG and MWD discriminated management systems, and are important indicators of soil quality.

The carbon content in macro-aggregates (C-MAC) and micro-aggregates (C-MIC) of the intercropped system (AC) was higher than that of the CR.

The attributes that best separated the areas were C-MIC, MWD and EEG in macro-aggregates at the depth of 0-10 cm, and EEG in micro-aggregates, MWD and C-MAC at the depth of 10-20 cm.

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Edited by

Edited by: Paulo Cesar Sentelhas

Publication Dates

  • Publication in this collection
    30 May 2019
  • Date of issue
    Nov-Dec 2019

History

  • Received
    15 Jan 2018
  • Accepted
    02 July 2018
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