Soil Quality Indicators in Agroecological Systems in the Cerrado of Minas Gerais, Brazil

Ana Flávia Brandão Rocha Ana Carolina Silva Siquieroli Adriane de Andrade Silva Amanda Mendes De Lima Carneiro Bruno Nery Fernandes Vasconcelos Danielle Davi Rodrigues Gondim About the authors

Abstract

Soil quality is its ability to function within the limits of the ecosystem and land use to ensure biological productivity, preserve environmental quality, and promote plant and animal health. Thus, the objective of this study was to select soil quality indicators sensitive to different agricultural practices adopted in areas of agroecological systems in the Cerrado of Minas Gerais, Brazil. Soil samples were collected in the 0-20 cm layer, at the end of the dry season, in three different rural properties dedicated to an agroecological system (AS) located in the municipalities of Romaria and Uberlândia, Minas Gerais, Brazil. Ten soil samples were evaluated, five from areas with agroecological management and five from pasture areas as reference. Chemical attributes, microbiota population, microbial biomass carbon (MBC), soil basal respiration (SBR), and activity of beta-glucosidase, phosphatase, and arylsulfatase enzymes were evaluated. The variables basal respiration, beta-glucosidase, pH, and bacterial and actinobacterial colonies were sensitive to different agroecological (AS) and pasture managements, so these variables can be used as indicators of soil quality. The mean values between the ratio of AS and pasture of these indicators were 1.69, 1.20, 3.57 and 2.44, respectively. Agroecological system areas showed a soil with better quality and, possibly, greater activity of its basic functions.

Keywords:
Agroforestry; Soil basal respiration; Microbial biomass carbon; Enzymatic activity

Resumo

A qualidade do solo é a sua capacidade de funcionar dentro dos limites do ecossistema e do uso da terra para assegurar a produtividade biológica, preservar a qualidade ambiental e promover a saúde dos vegetais e dos animais. Assim, o objetivo deste trabalho foi selecionar indicadores de qualidade de solo sensíveis às diferentes práticas agrícolas adotadas em áreas de sistemas agroecológicos na região do Cerrado Mineiro. As amostras de solos foram coletadas na camada de 0 a 20 cm da superfície, no final do período de seca, em três diferentes propriedades agrícolas familiares que se dedicam ao cultivo agroecológico (CA) localizadas nos municípios de Romaria e Uberlândia, Minas Gerais, Brasil. Foram avaliadas 10 amostras de solo, sendo cinco áreas com manejo agroecológico e cinco áreas de pasto, como referência. Foram avaliados os atributos químicos, população da microbiota, carbono da biomassa microbiana (CBM), respiração basal (RBS) e atividade das enzimas beta-glucosidase, fosfatase e arilsulfatase. As variáveis respiração basal, beta-glucosidase, pH, colônias de bactérias e de actinobactérias foram sensíveis aos diferentes manejos de cultivo agroecológico (CA) e pasto, podendo assim ser utilizadas como indicadores de qualidade de solo. Os valores médios entre a razão de CA e pasto destes indicadores foram 1,69, 1,20, 3,57 e 2,44, respectivamente. As áreas de cultivo agroecológico apresentaram um solo de melhor qualidade e, possivelmente, maior atividade das suas funções básicas.

Palavras-chave:
Agrofloresta; Respiração basal; Carbono da biomassa microbiana; Atividade enzimática

INTRODUCTION

Agroecology refers to principles of agricultural production practices that improve ecological systems. This includes nutrient recycling, soil improvement and increased interactions between different components. As an example, there may be the integration of animals and crops, planting of other crops, and also increased biodiversity (WACH, 2021WACH, E. Market Dependency as Prohibitive of Agroecology and Food Sovereignty-A Case Study of the Agrarian Transition in the Scottish Highlands. Sustainability, Basel, v. 13, n. 4, p. 1927, feb. 2021. https://doi.org/10.3390/su13041927.
https://doi.org/10.3390/su13041927....
). It provides the principles to manage productive agroecosystems and ensure the conservation of natural resources (ALTIERI; KOOHAFKAN, 2008ALTIERI, M.A.; KOOHAFKAN, P. Enduring Farms: climate change, Smallholders and Traditional Farming Communities. Penang: Third World Network, 2008.). This practice aims to redesign the food system, encompassing the ecological, economic and social dimensions of sustainability (CIACCIA et al., 2019CIACCIA, C. et al. Agroecological Practices and Agrobiodiversity: A Case Study on Organic Orange in Southern Italy. Agronomy, [s.l.], v. 9, n. 2, p. 85, fev. 2019. https://doi.org/10.3390/agronomy9020085.
https://doi.org/10.3390/agronomy9020085....
; WOOD et al., 2015WOOD, S. A. et al. Functional traits in agriculture: agrobiodiversity and ecosystem services. Trends in ecology & evolution, Cambridge, v. 30, n. 9, p. 531-539, sep. 2015. https://doi.org/10.1016/j.tree.2015.06.013.
https://doi.org/10.1016/j.tree.2015.06.0...
).

Alternative and sustainable agricultural models, such as agroecology, tend to reduce the adverse environmental or social effects of conventional agriculture that negatively affect rural areas (SKRZYPCZYŃSKI et al., 2021SKRZYPCZYŃSKI, R. et al. Beyond Supporting Access to Land in Socio-Technical Transitions. How Polish Grassroots Initiatives Help Farmers and New Entrants in Transitioning to Sustainable Models of Agriculture. Land, [s.l.], v. 10, n. 2, p. 214, feb. 2021. DOI: https://doi.org/10.3390/land10020214.
https://doi.org/10.3390/land10020214....
). The agroecological movement developed as opposed to the use of agrochemical inputs such as pesticides and inorganic fertilizers, mechanization and monocultures, since these practices deplete soils, reduce biodiversity, pollute watercourses and cause other types of environmental damage (WACH, 2021WACH, E. Market Dependency as Prohibitive of Agroecology and Food Sovereignty-A Case Study of the Agrarian Transition in the Scottish Highlands. Sustainability, Basel, v. 13, n. 4, p. 1927, feb. 2021. https://doi.org/10.3390/su13041927.
https://doi.org/10.3390/su13041927....
). The adoption of agroecological systems has been driven mainly by society’s demand for healthier foods and for production to result in lower negative environmental impacts (FERREIRA et al., 2017FERREIRA, E. P. B.; STONE, L. F.; MARTIN-DIDONET, C. C. G. População e atividade microbiana do solo em sistema agroecológico de produção. Revista Ciência Agronômica, Fortaleza, v. 48, n. 1, p. 22-31, jan.-mar. 2017. https://doi.org/10.5935/1806-6690.20170003.
https://doi.org/10.5935/1806-6690.201700...
; LIMA et al., 2020LIMA, S.K. et al. Produção e consumo de produtos orgânicos no mundo e no Brasil. Texto para discussão / Instituto de Pesquisa Econômica Aplicada, Brasília, Ipea, feb. 2020. Available: http://repositorio.ipea.gov.br/bitstream/11058/9678/1/TD_2538.pdf. Access in: 12 fev. 2021.
http://repositorio.ipea.gov.br/bitstream...
). An agroecological perspective links the nutritional value of food to the environmental impacts of food production. This reconnection between ecology and nutrition, which underlies the reconnection between agriculture, environment and food, raises fundamental ethical and ontological questions about our place as humans in the broader system, which, according to ecological theory, emphasizes the interconnection of different species and places humans as just one part of an ecosystem (LAMINE; DAWSON, 2018LAMINE, C.; DAWSON, J. The agroecology of food systems: Reconnecting agriculture, food, and the environment. Agroecology and Sustainable Food Systems, v. 42, n. 6, p. 629-636, feb. 2018. https://doi.org/10.1080/21683565.2018.1432517
https://doi.org/10.1080/21683565.2018.14...
).

According to Bünemann et al. (2018BÜNEMANN, E. K. et al. Soil quality-A critical review. Soil Biology and Biochemistry, [s.l.], v. 120, p. 105-125, feb. 2018. DOI: https://doi.org/10.1016/j.soilbio.2018.01.030
https://doi.org/10.1016/j.soilbio.2018.0...
), soil quality is measured by the soil’s ability to function within the boundaries of the ecosystem and land use to ensure biological productivity, preserve environmental quality and promote plant and animal health. The concept of soil quality was developed to enable the evaluation of the condition of a soil under a specific management (SARMIENTO et al., 2018SARMIENTO, E.; FANDINO, S.; GOMEZ, L. Indexes of soil quality. A systematic review. ECOSISTEMAS, Móstoles, v. 27, n. 3, p. 130-139, sep. 2018. https://doi.org/10.7818/ECOS.1598.
https://doi.org/10.7818/ECOS.1598....
). The relevance of using indicators is linked to the expression of soil functionality, which highlights the deficiencies of the evaluated areas and guides for soil recovery (CAVALCANTE et al., 2020CAVALCANTE, W. F. et al. Enzymatic activity of caatinga biome with and without anthropic action. Revista Caatinga, Mossoró, v. 33, n. 1, p. 142-150, 2020. https://doi.org/10.1590/1983-21252020v33n116rc.
https://doi.org/10.1590/1983-21252020v33...
).

Some examples of soil quality indicators are microbial biomass carbon, basal respiration and enzymatic activities, which are important for evaluating the effects of cultivation and land-use changes. In particular, soil microbial biomass and enzymes generally respond more rapidly to the disturbance caused by agricultural practices or changes in environmental conditions compared to other soil variables (RAIESI; BEHESHTI, 2014RAIESI, F.; BEHESHTI, A. Soil C turnover, microbial biomass and respiration, and enzymatic activities following rangeland conversion to wheat-alfalfa cropping in a semi-arid climate. Environmental Earth Sciences, Alemanha, v. 72, n. 12, p. 5073-5088, jun. 2014. https://doi.org/10.1007/s12665-014-3376-5.
https://doi.org/10.1007/s12665-014-3376-...
). In addition to biological and physical indicators, chemical indicators are also used to measure soil quality (ARAÚJO et al., 2012ARAÚJO, E. A. et al. Qualidade do solo: conceitos, indicadores e avaliação. Applied Research & Agrotechnology, Guarapuava, v. 5, n. 1, p. 187-206, jan.-apr. 2012. https://doi.org/10.5777/PAeT.V5.N1.12.
https://doi.org/10.5777/PAeT.V5.N1.12....
).

This study highlights the most appropriate soil quality indicators to be used in soil quality analyses in the Cerrado biome in the state of Minas Gerais, since there is a wide amount of variables that can be used to this end, but some of them do not generate significant results. Thus, the objective of this study was to select soil quality indicators for agroecological systems of family farming in the Brazilian Cerrado, in the municipalities of Uberlândia and Romaria.

MATERIAL AND METHODS

Characterization of the study area

In this study, three agroecological properties of family farming were analyzed, and properties 1 and 2 conduct agroecological systems within the same rural settlement in the city of Uberlândia-MG, which were implemented in 2015, and the transition to agroecological production was completed in 2017. The other agroecological rural property is located in the city of Romaria-MG. Properties 1 and 3 participate in Social Control Organizations (SCO), and their producers are certified as organic by the Ministério da Agricultura, Pecuária e Abastecimento (MAPA), which is the ministry responsible for agriculture in Brazil. Organic foods and agroecological foods do not use pesticides in their cultivation. One of the points that differentiate them is that agroecological food has an expanded ideology, which encompasses relationships with nature, trade and fair labor relations, review of consumption patterns and are based on family farming (WARMLING, 2014WARMLING, D. et al. Sentidos sobre agroecologia: a produção, distribuição e consumo de alimentos agroecológicos no município de Florianópolis/SC, 2014. 125 f. Dissertação (Pós-graduação em Saúde Coletiva), Centro de Ciências da Saúde, Universidade Federal de Santa Catarina, Florianópolis, 2014.). In addition, the certification of organic food is carried out by “audit” and the certification of agroecological food is “participatory” (ABREU et al., 2012ABREU, L. S. et al. Relações entre agricultura orgânica e agroecologia: desafios atuais em torno dos princípios da agroecologia. Desenvolvimento e Meio Ambiente, v. 26, p. 143-160, jul./dez 2012. http://dx.doi.org/10.5380/dma.v26i0.26865
http://dx.doi.org/10.5380/dma.v26i0.2686...
).

Family farming property 1, located in Uberlândia-MG, with geographic coordinates 19º04'05.0"S and 48º27'51.6"W (Figure 1), has a total area of 12.5 ha, being 2,493 m² occupied by an agroecological and agroforestry system (AS1) and a side area used for agroecological production (AS2). The agricultural and forest species found in the AS1 area were: papaya, mango, red angico, cecropia, jatobá, pink ipe, West Indian elm, pacara ear pod, guariroba, eucalyptus, castor bean, pigeon pea, elephant grass, Mexican sunflower, gliricidia, jack bean, velvet bean and signalgrass. In the AS2 area, the species found were: garlic, lemongrass, chives, coriander, lemon balm, mint, pepper, parsley, onion, acerola, banana, lemon, passion fruit, guava, blackberry, cashew, cowpea, corn, zucchini, eggplant, scarlet eggplant, cherry tomato, maroon cucumber, strawberry, lettuce, leek, chicory, purslane, broccoli, kale, spinach, mustard, cabbage, arugula, sweet potato, beetroot, arrowroot, carrot, radish, yam, cassava, yacon potato, and sunflower (SILVA, 2019SILVA, R. P. Análise integrada em sistemas agroflorestais de agricultores do assentamento Celso Lúcio, 2019. 84 f. Monografia (Graduação em Engenharia Ambiental), Instituto de Ciências Agrárias, Universidade Federal de Uberlândia, Uberlândia, 2019.).

The main aspect that differentiates the AS1 and AS2 areas of this property is that in AS2 there is a predominance of vegetables, while AS1 is mostly constituted by tree species. The rural producer of this property, for environmental reasons, left an area for agroforestry recomposition (AS1 area), with exploitation of crops that had already been planted before 2015, but without the reintroduction of vegetables, which would constantly depend on fertilization. In addition, AS2 has a greater diversity and quantity of plant species. The AS1 and AS2 areas of this property are irrigated with tilapia aquaculture effluent, which is rich in nutrients (SILVA, 2019SILVA, R. P. Análise integrada em sistemas agroflorestais de agricultores do assentamento Celso Lúcio, 2019. 84 f. Monografia (Graduação em Engenharia Ambiental), Instituto de Ciências Agrárias, Universidade Federal de Uberlândia, Uberlândia, 2019.). In addition, these two areas receive inputs of Yoorin, which also contains phosphorus, calcium, magnesium, silicon, dicalcium phosphate and other nutrients. The addition of these agricultural inputs is allowed by the regulations for agroecological/organic crops. Organic compounds, which are sources of macro and micronutrients, were also incorporated into the soil of these areas.

Figure 1
Location of the family farms. Properties 1 and 2: managed with agroecological system located in the municipality of Uberlândia, MG; Property 3: agroecological system, located in the municipality of Romaria, MG.

In property 1, two samples were collected as it had areas with distinct agricultural practices: AS1 corresponds to agroecological and agroforestry management implemented in 2015, and AS2 corresponds to agroecological management with the predominance of vegetables, implemented in 2017, in addition to the two pasture samples used as reference.

Table 1 shows the characteristics of the soils collected in the 3 rural properties for the 10 different samples. Soil classification was performed according to the methodology described by Teixeira (2017TEIXEIRA, P. C. et al. Manual de métodos de análise de solo. Rio de Janeiro: Embrapa, 2017.).

Table 1
Taxonomic classification of soils at the sampling sites.

Before the agroecological intervention, the main activity carried out in the lot of properties 1 and 2, by the former owner of the farm, was beef cattle farming, so most of the landscape is currently characterized by degraded pasture. Currently, there is rearing of some pigs in pigsty, cow, bull and chickens in the pasture area in the properties of the Celso Lúcio Settlement. The areas of Pasture 1 and Pasture 2 correspond to these pasture areas that have not suffered interference for a while.

Family farming property 2, with coordinates 19°04'59.5"S and 48°28'46.0"W, located in the municipality of Uberlândia, MG (Figure 1), has a total area of 13.2 ha, with 1,018 m2 intended for agroecological and agroforestry cultivation since 2015. In this area, vegetables and tree species are found. The plant species found on this property are coriander, lemon balm, ginger, mint, basil, pepper, parsley, common rue, saffron, boldo, fennel, onion, avocado, acerola, banana, lemon, papaya, mango, guava, cashew, orange, tangerine, cowpea, corn, zucchini, scarlet eggplant, bell pepper, okra, maroon cucumber, strawberry, watercress, lettuce, chicory, purslane, common chicory, kale, mustard, arugula, malanga, sweet potato, arrowroot, yam, cassava, guariroba, cambuí, eucalyptus, castor bean, pigeon pea, elephant grass, Mexican sunflower, gliricidia, jack bean, velvet bean and signalgrass (SILVA, 2019SILVA, R. P. Análise integrada em sistemas agroflorestais de agricultores do assentamento Celso Lúcio, 2019. 84 f. Monografia (Graduação em Engenharia Ambiental), Instituto de Ciências Agrárias, Universidade Federal de Uberlândia, Uberlândia, 2019.). In addition, the agricultural producer of this area incorporates organic matter in the soil of the beds.

Finally, there is the family agricultural property with coordinates 18°48'3.02"S 47°37'13.10" (Figure 1), located in the municipality of Romaria, MG. This producer has an agroecological system in the two areas of his property (AS4 and AS5), maintaining agroecological practices of recycling biomass from tree pruning, weeding and crop residues, use of mulch formed by straw and litter of native forest (Cerrado), crop rotation, green manure and other practices that promote nutrient recycling. In this property, in both areas, various plants are cultivated in full sun such as papaya, lemongrass, chives, coriander, lemon balm, mint, pepper, parsley, onion, acerola, banana, lemon, eggplant, scarlet eggplant, tomato, lettuce, leek, chicory, broccoli, kale, spinach, mustard, cabbage, arugula, sweet potato, beetroot, carrot, cassava and yacon potato.

Sampling

Soil samples were collected at a depth of 20 to 25 cm, with a hoe. Samples were collected randomly within the farmers’ cultivation systems. In addition, the samples were composed of five points per area and were collected after removing the litter and avoiding places near the trees.

The samples were collected between September and October 2019 (end of the dry season), in georeferenced points. Soil samples were also collected from areas used for pasture very close to the collection points to serve as a reference for the absence of agroecological management, representing neighboring areas, under the same climate and in similar soils, with another cultivation system and that did undergo intervention by farmers. The pasture samples of this study constitute a comparative treatment to the agroecological and agroforestry system.

Figure 2 shows the accumulated rainfall of the six months prior to the day of collection of soil samples in the municipalities of Uberlândia and Romaria, and Figure 3 shows the temperature in the month in which the samples were collected in these municipalities.

Figure 2
Accumulated daily rainfall (mm) in the six months prior to the collection of soil samples in the municipalities of Uberlândia and Romaria, MG.

Figure 3
Temperature (°C) in the month of collection of soil samples in the municipalities of Uberlândia and Romaria, MG.

The 10 samples evaluated in this study (Table 1) were sieved through a 2-mm mesh and used for chemical, microbial (colony forming units) and biochemical (enzymatic activity, biomass carbon and basal respiration) analyses.

Soil chemical, biochemical and microbial analyses

The fertility parameters pH (in water), phosphorus (P) - P meh-1 - Mehlich-1 Extractant, potassium (K) in which K = [0.05 mol L-1 HCl + 0.0125 mol L-1 H2SO4], calcium (Ca), magnesium (Mg), organic matter (OM) - Colorimetric method, effective cation exchange capacity (CEC) and base saturation (V %) were analyzed according to Teixeira (2017TEIXEIRA, P. C. et al. Manual de métodos de análise de solo. Rio de Janeiro: Embrapa, 2017.).

The number of colony-forming units (CFU) was determined in triplicate in selective culture media for bacteria and actinobacteria, using the method of serial dilution and spreading on a plate with a solid culture medium. For the cultivation of actinobacteria, SCN medium (TAVARES, 2019TAVARES, D. G. et al. Controle biológico de Meloidogyne incognita por isolados de actinomicetos. In: Colloquium Agrariae. ISSN: 1809-8215. 2019. p. 29-36. https://doi.org/10.5747/ca.2019.v15.n2.a282
https://doi.org/10.5747/ca.2019.v15.n2.a...
) supplemented with antifungal agent nystatin and antibiotic agent streptomycin was used. For the cultivation of bacteria, nutrient agar medium (CARDOSO, 2012CARDOSO, E. B.; LUQUINE, L. S.; SILVA, H. S. A. Aplicação conjunta de rizobactérias e bactérias endofíticas para o biocontrole do Fusarium oxysporum f. sp. Cubense. In: Embrapa Mandioca e Fruticultura-Resumo em anais de congresso (ALICE). In: JORNADA CIENTÍFICA EMBRAPA MANDIOCA E FRUTICULTURA, 6., 2012, Cruz das Almas. Anais... Cruz das Almas: Embrapa Mandioca e Fruticultura, 2012., 2012.) supplemented with nystatin was used. The plates were kept at a temperature of 25±2°C, under a photoperiod of 12 hours, for three days for actinobacteria and bacteria. The results were expressed in number of colony-forming units per 1g gram of soil.

The soils destined for the evaluation of microbial biomass carbon and basal respiration had their moisture content adjusted to 60% of the water retention capacity by the gravimetric method according to the methodology of Silva et al. (2007SILVA, E. E.; AZEVEDO, P. H. S.; DE-POLLY, H. Determinação da respiração basal (RBS) e quociente metabólico do solo (qCO2). Embrapa Agrobiologia-Comunicado Técnico (INFOTECA-E), Seropédica, 2007. Available: https://www.infoteca.cnptia.embrapa.br/bitstream/doc/627577/1/cot099.pdf. Access in: 15 jul. 2019.
https://www.infoteca.cnptia.embrapa.br/b...
). Microbial biomass carbon (MBC) was analyzed using the fumigation-extraction method (FE), which followed the methodology described by Souza et al. (2015SOUZA, L. M. et al. Carbono da biomassa microbiana em Latossolos determinado por oxidação úmida e combustão a temperatura elevada. Pesquisa Agropecuária Brasileira, Brasília, v. 50, n. 11, p. 1061-1070, nov. 2015. https://doi.org/10.1590/S0100-204X2015001100009.
https://doi.org/10.1590/S0100-204X201500...
). The quantification of carbon in extracts from the soil sample was performed according to the methodology of Mendonça and Da Matos (2005MENDONÇA, E. S, DA MATOS E. S. Matéria orgânica do solo: métodos de análises.Viçosa: UFV, 2005.). Basal respiration (SBR) was evaluated according to the procedure of Silva et al. (2007).

Activity of β-glucosidase (GLU) was determined according to the methodology of Eivazi and Tabatai (1988EIVAZI, F.; TABATABAI, M. A. Glucosidases and galactosidases in soils. Soil Biology and Biochemistry, Elmsford, v. 20, n. 5, p. 601-606, dec.1988. https://doi.org/10.1016/0038-0717(88)90141-1.
https://doi.org/10.1016/0038-0717(88)901...
), phosphatase (PHOS) was determined according to Tabatabai and Bremner (1969TABATABAI, M. A.; BREMNER, J. M. Arylsulfatase activity of soils. Soil Science Society of America Proceedings, Madison, v. 34, n. 2, p. 225-229, mar. 1969. https://doi.org/10.2136/sssaj1970.03615995003400020016x.
https://doi.org/10.2136/sssaj1970.036159...
) with modifications, and the arylsulfatase enzyme (ARYL) was determined according to Tabatabai and Bremner (1970). The results of this analysis were expressed in μg product released g dry soil−1 h−1.

The data of soil fertility, MBC, SBR, activity of enzymes and population of bacteria and actinobacteria were subjected to analysis of variance (ANOVA) and the means were compared by the Skott-Knott test at 5% significance level using the program SISVAR 5.7 (FERREIRA, 2019FERREIRA, D. F. Sisvar: a Computer Analysis System To Fixed Effects Split Plot Type Designs. Revista Brasileira De Biometria, v. 37, n. 4, p. 529-535, dec. 2019. https://doi.org/10.28951/rbb.v37i4.450
https://doi.org/10.28951/rbb.v37i4.450...
). In addition, principal component analysis (PCA), which is a linear ordering technique, was performed using CANOCO software version 4.5 (ter BRAAK; SMILAUER, 2002ter BRAAK, C. J. F.; SMILAUER, P. CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Ithaca: Microcomputer Power; 2002.).

The results of the bioindicators of this study were interpreted using the Fertbio model created by Mendes et al. (2018MENDES, I. C. et al. Bioanálise de solo: como acessar e interpretar a saúde do solo. Embrapa Cerrados-Circular Técnica (INFOTECA-E), Planaltina, 2018. Available: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/199833/1/CircTec-38-Ieda-Mendes.pdf. Access in: 12 feb. 2021.
https://ainfo.cnptia.embrapa.br/digital/...
), because this method incorporates microbial and fertility indicators in soil analyses in Brazil. Through this model, it is possible to interpret β-Glucosidase and Arylsulfatase indicators for clayey Latossolos (Oxisol) of the Cerrado, under annual crops for air-dried soil samples. Although not all properties have this type of soil, this interpretation model was used for all properties of the present study. The indicators were compared by the ratio of their values for each system. The higher the result, the greater the sensitivity of the bioindicator to changes in the management systems (MENDES et al., 2018MENDES, I. C. et al. Bioanálise de solo: como acessar e interpretar a saúde do solo. Embrapa Cerrados-Circular Técnica (INFOTECA-E), Planaltina, 2018. Available: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/199833/1/CircTec-38-Ieda-Mendes.pdf. Access in: 12 feb. 2021.
https://ainfo.cnptia.embrapa.br/digital/...
).

RESULTS AND DISCUSSION

According to the analysis of soil chemical attributes (Table 2), the variables pH, Ca, Mg, OM, effective CEC and V% are found in greater proportion in agroecological management systems than in pasture areas.

Table 2
Chemical attributes in soil samples collected in agroecological system (AS) and pasture areas.

The higher proportions of the attributes pH, Ca, Mg, OM, effective CEC and V% in the areas of AS are possibly due to the incorporation of organic matter and the diversity of species in these cultivation areas. OM was not significant probably because the litter was removed before sample collection. It is important to note that the chemical attributes may have changed due to the addition of agricultural inputs in properties 1 and 3.

Similar results were reported by Santiago et al. (2018SANTIAGO, F. S.; MONTENEGRO, S. M. G. L.; PINHEIRO, M. R. A P. Índice de qualidade do solo em cultivo agroecológico e convencional no semiárido potiguar, Brasil. Revista Verde de Agroecologia e Desenvolvimento Sustentável, v. 13, n. 1, p. 97-105, jan.-mar. 2018. http://dx.doi.org/10.18378/rvads.v13i1.5333
http://dx.doi.org/10.18378/rvads.v13i1.5...
), who observed that the pH in the 0 to 20 cm layer of soils in transition to agroecological systems showed positive correlations over the time of use, proving that the pH values tend to increase in these soils in transition. The present study also obtained results agreeing with those reported by Obeng and Aguilar (2015OBENG, E. A.; AGUILAR, F. X. Marginal effects on biodiversity, carbon sequestration and nutrient cycling of transitions from tropical forests to cacao farming systems. Agroforestry Systems, [s.l.], v. 89, n. 1, p. 19-35, sep. 2015.: https://doi.org/10.1007/s10457-014-9739-9.
https://doi.org/10.1007/s10457-014-9739-...
), who found that the soils of cocoa agroforests had higher concentrations of Ca and Mg than those of native forest areas in the region.

In a study conducted by Samani et al. (2020SAMANI, K. M. et al. Effect of land-use changes on chemical and physical properties of soil in western Iran (Zagros oak forests). Journal of Forestry Research, [s.l.], v. 31, n. 2, p. 637-647, oct. 2020. https://doi.org/10.1007/s11676-018-0799-y.
https://doi.org/10.1007/s11676-018-0799-...
), higher proportions of Mg were obtained in the soil of agroforestry systems than in soil samples from other cultivation systems. According to the authors, this may have occurred due to the treetops, which created adequate conditions for mineral weathering with ideal temperature and humidity, so greater amounts of Mg are released. This explains the lower concentrations of Mg in pasture areas.

According to Kassa (2018KASSA, H. et al. Agro-ecological implications of forest and agroforestry systems conversion to cereal-based farming systems in the White Nile Basin, Ethiopia. Agroecology and Sustainable Food Systems, Philadelphia, v. 42, n. 2, p. 149-168, nov. 2018. https://doi.org/10.1080/21683565.2017.1382425.
https://doi.org/10.1080/21683565.2017.13...
), higher pH and CEC values in agroforestry systems compared to monoculture areas are probably related to high levels of organic matter, linked to the fall of tree leaves and the protection against soil erosion provided by them. According to the author, higher soil CEC is related to high clay contents and organic matter. This is consistent with the results found in the present study, since the AS areas obtained a higher CEC than the pasture areas, probably due to the greater amount of plant residues present in the former. According to Teixeira (2013TEIXEIRA, V. G. Atribuição de tributos do solo e vegetação em sistema agroecológico. Trabalho de conclusão de curso (Ecologia) - Universidade Estadual Paulista, Instituto de Biociências de Rio Claro. UNESP, Rio Claro - SP, 2013.), V% is indicative of the general conditions of soil fertility, since it is a result of the sum of bases and effective CEC. Thus, it is possible to notice that the areas under agroecological management have higher fertility compared to pasture areas.

Regarding enzymatic analyses, it was found that the concentration of the enzyme β-glucosidase was significantly higher in the agroecological system samples than in the pasture soil samples (Figure 4). The higher concentration of this enzyme in AS areas is possibly due to the greater amount of plant residues in the soil, which come from the great diversity of perennial vegetation of this system and also due to the biomass recycling practices carried out used by rural producers.

Figure 4
Concentration of the enzymes β-glucosidase, phosphatase and Arylsulfatase in the management of Agroecological Systems and Pasture. The values of the enzymatic activities were expressed in μg product released g dry soil−1 h−1.

According to Paudel et al. (2011PAUDEL, B. R.; UDAWATTA, R. P.; ANDERSON, S. H. Agroforestry and grass buffer effects on soil quality parameters for grazed pasture and row-crop systems. Applied Soil Ecology, [s.l.], v. 48, n. 2, p. 125-132, jun. 2011. https://doi.org/10.1016/j.apsoil.2011.04.004.
https://doi.org/10.1016/j.apsoil.2011.04...
), the greater activity of certain soil enzymes is improved by conservation practices, such as agroecological system, which can raise other soil quality parameters, such as organic matter content, aggregation and water infiltration into the soil, as well as its sustainability and productivity.

Vallejo et al. (2010VALLEJO, V. E.; ROLDAN, F.; DICK, R. P. Soil enzymatic activities and microbial biomass in an integrated agroforestry chronosequence compared to monoculture and a native forest of Colombia. Biology and Fertility of Soils, Florença, v. 46, n. 6, p. 577-587, may 2010. https://doi.org/10.1007/s00374-010-0466-8.
https://doi.org/10.1007/s00374-010-0466-...
) analyzed the enzymatic activity of β-Glucosidase and found a higher concentration of these enzymes in the 12-year-old agroforestry system compared to the conventional pasture area. According to Paudel et al. (2011PAUDEL, B. R.; UDAWATTA, R. P.; ANDERSON, S. H. Agroforestry and grass buffer effects on soil quality parameters for grazed pasture and row-crop systems. Applied Soil Ecology, [s.l.], v. 48, n. 2, p. 125-132, jun. 2011. https://doi.org/10.1016/j.apsoil.2011.04.004.
https://doi.org/10.1016/j.apsoil.2011.04...
), the higher activity of the enzyme β-glucosidase in perennial vegetation treatments can be explained by the biomass accumulation of perennial vegetation in the soil.

In relation to the analysis of microorganisms, there was a significant increase in the amount of actinobacteria of the AS samples compared to the respective pasture areas (Figure 5). In addition, the colonies of actinobacteria found in the pasture were very small and white in color, while those found in the AS areas showed with yellow color. Actinobacteria population data are in accordance with those reported by Beule et al. (2020BEULE, L. et al. Poplar rows in temperate agroforestry croplands promote bacteria, fungi, and denitrification genes in soils. Frontiers in Microbiology, Lausanne, v. 10, p. 3108, jan. 2020. https://doi.org/10.3389/fmicb.2019.03108.
https://doi.org/10.3389/fmicb.2019.03108...
), who found that in general, these microorganisms were in greater abundance in AS soil samples than in monoculture soil samples. This was due to the increase in above-ground plant biomass and diversity, which increased litter input, and the increase in the amount and diversity of root exudates.

Figure 5
Biological indicators of soil quality (SBR, MBC, actinobacteria and bacteria) in soil samples collected at properties with agroecological system (AS) and pasture.

For the SBR values, the areas of agroecological system had significantly higher values than the pasture areas taken as a reference for each property (Figure 5). This result represents a higher activity of microorganisms in AS areas, which may have occurred due to the greater amount of colony-forming units of bacteria and actinobacteria in this soil, in addition to the greater amount of organic residues deposited.

Tian et al. (2013TIAN, Y.; CAO, F.; WANG, G. Soil microbiological properties and enzyme activity in Ginkgo-tea agroforestry compared with monoculture. Agroforestry systems, [s.l.], v. 87, n. 5, p. 1201-1210, aug. 2013. https://doi.org/10.1007/s10457-013-9630-0.
https://doi.org/10.1007/s10457-013-9630-...
) found that basal respiration was significantly higher in agroforestry systems than in monoculture systems. A higher rate of basal respiration in agroforests may be due to the existence of large availability of labile carbon substrates.

In the present study, bacteria were found in greater amount in AS areas than in the respective pasture areas. The samples with bacterial colony-forming units from the pasture areas showed a white color. On the other, the bacterial colonies found in the AS areas predominantly showed a yellow/orange color.

The results presented here are in accordance with those reported by Henneron et al. (2015HENNERON, L. et al. Fourteen years of evidence for positive effects of conservation agriculture and organic farming on soil life. Agronomy for Sustainable Development, [s.l.], v. 35, n. 1, p. 169-181, april 2015.: https://doi.org/10.1007/s13593-014-0215-8.
https://doi.org/10.1007/s13593-014-0215-...
), who stated that the amount of bacteria present in soil under organic system is significantly higher than in soils under conventional management. In addition, the abundance of certain bacterial genes was positively correlated with soil organic C, total N, available P in the plant and exchangeable K and Mg (BEULE et al., 2019BEULE, L. et al. Conversion of monoculture cropland and open grassland to agroforestry alters the abundance of soil bacteria, fungi and soil-N-cycling genes. PloS one, San Francisco, v. 14, n. 6, p. e0218779, jun. 2019. https://doi.org/10.1371/journal.pone.0218779.
https://doi.org/10.1371/journal.pone.021...
).

The biplot resulting from the principal component analysis (PCA), based on soil quality indicators and sampling subareas, clearly expresses the relationship between some enzymatic activities and the two types of management: agroecological system (AS) and pasture. According to the analysis, axis 1 explained 60.8% of the bioindicator-environment relationship and, together with axis 2, explained 16.5% of the data variation (Figure 6).

Figure 6
Biplot of the different management areas and soil quality indicators - ACT: actinobacteria, ARYL: Arylsulfatase; BAC: Bacteria; Ca: Calcium; MBC: Microbial Biomass Carbon; PHOS: Phosphatase, GLU: β-glucosidase; K: Potassium; Mg: Magnesium; OM: Organic Matter; P: Phosphorus; SBR: Soil Basal Respiration; V%: Base Saturation in potential CEC

It was possible to observe that the AS areas are more related to the higher values of soil quality variables, except for PHOS, which is an indication that these areas have higher quality. On the other hand, pasture areas are inversely related to soil quality indicators. Axis 1 is the one that most separates the types of management. Thus, the variables that most differentiate the AS from the pastures are Mg, Ca, bacteria, pH, CEC and actinobacteria. Possibly, the greater relationship of soil quality variables with AS was found because this management increases the amount of residues from several agricultural species and increases vegetation cover, avoiding nutrient leaching.

Soil samples from AS4 and AS5 showed a higher relationship with OM concentration and the activities of arylsulfatase and β-glucosidase. The enzymatic activity of these enzymes is positively related to the O.M concentration in the soil (WALMSLEY; SKLENIČKA, 2017WALMSLEY, A.; SKLENIČKA, P. Various effects of land tenure on soil biochemical parameters under organic and conventional farming− Implications for soil quality restoration. Ecological Engineering, [s.l.], v. 107, p. 137-143, oct. 2017. https://doi.org/10.1016/j.ecoleng.2017.07.006.
https://doi.org/10.1016/j.ecoleng.2017.0...
; PAUDEL et al., 2011PAUDEL, B. R.; UDAWATTA, R. P.; ANDERSON, S. H. Agroforestry and grass buffer effects on soil quality parameters for grazed pasture and row-crop systems. Applied Soil Ecology, [s.l.], v. 48, n. 2, p. 125-132, jun. 2011. https://doi.org/10.1016/j.apsoil.2011.04.004.
https://doi.org/10.1016/j.apsoil.2011.04...
). The greater relationship of these samples with organic matter can be explained by the practices that promote the recycling of nutrients carried out by the rural producer of property 3.

The soils evaluated in the present study have different typologies of Latossolos Vermelhos (Oxisols) (Table 1). Although there is this distinction between the classification of the soils, by comparing the obtained values of β-Glucosidase and Arylsulfatase with the data from the bioindicator interpretation table of Mendes et al. (2018MENDES, I. C. et al. Bioanálise de solo: como acessar e interpretar a saúde do solo. Embrapa Cerrados-Circular Técnica (INFOTECA-E), Planaltina, 2018. Available: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/199833/1/CircTec-38-Ieda-Mendes.pdf. Access in: 12 feb. 2021.
https://ainfo.cnptia.embrapa.br/digital/...
) (Table 3), it was possible to demonstrate that the samples collected in the areas of agroecological system showed a better class of interpretation than the pasture soil samples (Table 4).

Table 3
Interpretation of bioindicators for the activity of β-Glucosidase and Arylsulfatase enzymes in soil samples collected in properties with agroecological system (AS).

According to Mendes et al. (2018MENDES, I. C. et al. Bioanálise de solo: como acessar e interpretar a saúde do solo. Embrapa Cerrados-Circular Técnica (INFOTECA-E), Planaltina, 2018. Available: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/199833/1/CircTec-38-Ieda-Mendes.pdf. Access in: 12 feb. 2021.
https://ainfo.cnptia.embrapa.br/digital/...
), it is possible to interpret β-Glucosidase and Arylsulfatase indicators for clayey Latossolos Vermelhos (Oxisols) of the Cerrado, under annual crops for air-dried soil samples. According to these authors, low values of the indicators can demonstrate that inadequate management practices are being adopted in the area. On the other, higher values of these bioindicators can be understood as desirable values that must be maintained for the proper functioning of the soil. According to the bioindicator β-Glucosidase, soil quality in agroecological system areas is better than in pasture areas, while for Arylsulfatase there was no difference.

Table 4 shows the comparisons of the various soil quality indicators between the different areas of study (agroecological system and pasture).

Table 4
Ratio between soil variables collected in agroecological system (AS) areas and in adjacent pasture areas.

All variables, except for acid phosphatase enzyme activity, were higher in the AS areas compared to the pasture area, since values greater than 1 were obtained. The variables that obtained the most marked differences were K, P, Mg2+, Ca2+, CEC and bacterial colonies, which shows that these variables are more sensitive to changes according to the management system. The variables K, P, Mg2+, Ca2+, CEC of the AS had higher values possibly due to the addition of external inputs, which are allowed by the body that certifies organic products, during the management. The indicators SBR, actinobacterial colonies, MBC, Arylsulfatase, pH, OM and V% also stood out and were sensitive to the change in management.

Thus, the variables bacterial colonies, actinobacterial colonies, β-Glucosidase and pH present themselves as possible indicators of soil quality, because were sensitive (Table 4). In addition, these indicators mentioned above show a significant difference between the AS and Pasture samples in the means comparison test (Table 2, Figure 4 and Figure 5) and also there is greater relationship of these indicators with the AS areas, as shown in the PCA (Figure 6).

FINAL CONSIDERATIONS

The following soil quality variables proved to be sensitive to the difference in management between agroecological system and pasture areas: basal respiration, β-glucosidase, bacterial and actinobacterial colonies and pH, and it is possible to use these variables as indicators of soil quality. Other variables such as K, P, Mg2+, Ca2+ and CEC were not considered as good indicators in the present study because, possibly, they had undergone changes in their values due to the addition of external inputs by farmers, inputs that are allowed by the body that certifies organic products during management.

The indicators basal respiration, β-glucosidase, pH, and colonies of bacteria and actinobacteria proved to be able to identify changes in soil functioning in the areas of family farming. The higher soil quality in the agroecological system areas resulted in higher values of these variables. Possibly these managements have greater activities of their basic functions, such as movement and supply of water to soil and plants, nutrient cycling, resistance to organic and inorganic pollutants and high productivity.

ACKNOWLEDGMENTS

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

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Publication Dates

  • Publication in this collection
    22 Apr 2022
  • Date of issue
    2022

History

  • Received
    19 Aug 2021
  • Accepted
    05 Jan 2022
  • Published
    16 Feb 2022
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