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Conservation system improves soil microbial quality and increases soybean yield in the Northeastern Cerrado

ABSTRACT

The conservation tillage systems is based on the surface protection by crop residue and reduced soil disturbance. These two principles can favor the soil quality and promote sustainable agricultural systems. The study was developed with the objective of measure soil microbial biomass, soil basal respiration, enzymatic activity and soybean yield in conservation systems cultivated with cover crops species in the Northeastern Cerrado. The experiment was carried out in 2016/2017 and 2017/2018 cropping seasons, performed in a randomized blocks design. The treatments were soil tillage systems allocated in the main plots: no-tillage (NT) and minimum tillage (MT) and the cover crops were allocated in the subplots: Pennisetum glaucum (millet), Urochloa ruziziensis (brachiaria), Crotalaria spectabilis (C. spectabilis), Crotalaria ochroleuca (C. ochroleuca), Pennisetum glaucum + Crotalaria spectabilis (millet + C. spectabilis) and spontaneous plants with three replicates. The evaluated variables were dry mass (DM) production and nutrient accumulation in cover crops; soil biological properties, namely microbial biomass carbon and nitrogen (MBC and MBN, respectively), respiration, metabolic quotient (qCO2), dehydrogenase enzymatic activity (DH), fluorescein diacetate (FDA); and soybean yield. The higher production of dry mass and nutrient cycling occurs with the intercropping millet + C. spectabilis and single millet. The highest soybean yield occurs in succession to C. ochroleuca and intercropping of the millet + C. spectabilis. Cover crops in conservation systems improve soil microbial quality and increase soybean yield.

Key words
Glycine max L.; soil quality; no-tillage; nutrient cycling; microbial biomass

INTRODUCTION

The agricultural expansion in the Northeastern Cerrado is a result of good soil management practices, especially lime application, improved fertility through mineral fertilization and proper phytosanitary management, which make this region, partly situated in MATOPIBA, one of the last Brazil’s agricultural borders (Almeida et al. 2018Almeida, W. S., Panachuki, E., Oliveira, P. T. S., Menezes, S. R., Alves Sobrinho, T., and Carvalho, D. F. (2018). Effect of soil tillag., and vegetal cover on soil water infiltration. Soi., and Tillage Research, 175, 130-138. https://doi.org/10.1016/j.still.2017.07.009
https://doi.org/10.1016/j.still.2017.07....
). Soybean (Glycine max L. Merrill), which presents good adaptation and high yield, is the crop with the largest planted area in the Northeastern Cerrado. Due to the good profitability of soybean, the cultivation system is little diversified, resulting in large monoculture areas. In this production system, cover crops are rarely included, resulting in low production of crop residues and insufficient soil cover throughout the year (Merten et al. 2015Merten, G. H., Araújo, A. G., Biscaia, R. C. M., Barbosa, G. M. C., and Conte, O. (2015). No-till surface runof., and soil losses in southern Brazil. Soi., and Tillage Research, 152, 85-93. https://doi.org/10.1016/j.still.2015.03.014
https://doi.org/10.1016/j.still.2015.03....
).

Low soil cover may make no-tillage system unfeasible and low residue production compromises soil organic carbon stocks, nutrient cycling, microbiological activity and, consequently, soil quality (Pacheco et al. 2017Pacheco, L. P., Monteiro, M. M. S., Petter, F. A., Nóbrega, J. C. A., and Santos, A. S. (2017). Biomas., and nutrient cycling by cover crops in Brazilian Cerrado in the state of Piauí. Revista Caatinga, 30, 13-23. https://doi.org/10.1590/1983-21252017v30n102rc
https://doi.org/10.1590/1983-21252017v30...
; Derpsch et al. 2014Derpsch, R., Franzluebbers, A. J, Duiker, S. W., Reicosky, D. C., Koeller, K., Friedrich, T., Sturny, W. G., Sá, J. C. M., and Weiss, K. (2014). Why do we need to standardize no-tillage research? Soi., and Tillage Research, 137, 16-22. https://doi.org/10.1016/j.still.2013.10.002
https://doi.org/10.1016/j.still.2013.10....
). Thus, one of the current challenges for agriculture in the Northeastern Cerrado is to develop management practices that improve soil quality in order to ensure its sustainability. This can be achieved by using the conservation systems (used as synonym of conservation agriculture) with crop rotation plans, including cover crops to increase residue production and soil protection (Osterholz et al. 2020Osterholz, W. R., Culman, S. W., Herms, C., Oliveira, F. J., Robinson, A., and Doohan, D. (2020). Knowledge gaps in organic research: understanding interactions of cover crop., and tillage for weed contro., and soil health. Organic Agriculture. https://doi.org/10.1007/s13165-020-00313-3
https://doi.org/10.1007/s13165-020-00313...
).

The main characteristics of cover crops to their selection and use are soil and climate adaptation that are necessary to ensure sufficient mass production and proper nutrient cycling. Characteristics such as lignin content, rooting growth and ability to establish symbiosis with nitrogen fixing bacteria and their capacity to improve physical, chemical and microbiological soil properties should also be considered (Adler et al. 2020Adler, R. L., Singh, G., Nelson, K. A., Weirich, J., Motavalli, P. P., and Miles, R. J. (2020). Cover crop impact on crop productio., and nutrient loss in a no-till terrace topography. Journal of Soi., and Water Conservation, 75, 153-165. https://doi.org/10.2489/jswc.75.2.153
https://doi.org/10.2489/jswc.75.2.153...
; Amorim et al. 2020Amorim, S. P. N., Boechat, C. L., Duarte, L. S. L., Oliveira, D. F., Medeiros, J. C., and Arauco, A. M. S. (2020). Microbial responses to doses of cover plant straw in cerrado piauiense oxisol. Bioscience Journal, 36, 1146-1155. https://doi.org/10.14393/BJ-v36n4a2020-47963
https://doi.org/10.14393/BJ-v36n4a2020-4...
; Sousa et al. 2019Sousa, D. C., Medeiros, J. C., Lacerda, J. J. J., Dalla Rosa, J., Boechat, C. L., Souza, M. N. G., Rodrigues, P. C. F., Oliveira Filho, E. G., and Mafra, Á. L. (2019). Dry mass accumulation, nutrient., and decomposition of cover plants. Journal of Agricultural Science, 11, 152-160.).

Cover crop residues can improve water availability and thermal conditions, which favors growth and microbial activity and may increase soil carbon and nitrogen stocks (De Vincentis et al. 2020De Vincentis, A. J., Solis, S. S., Bruno, E. M., Leavitt, A., Gomes, A., Rice, S., and Zaccaria, D. (2020). Using cost-benefit analysis to understand adoption of winter cover cropping in California’s specialty crop systems. Journal of Environmental Management, 261, 110205. https://doi.org/10.1016/j.jenvman.2020.110205
https://doi.org/10.1016/j.jenvman.2020.1...
). Soil microbiota plays a fundamental role in organic matter decomposition and nutrient cycling, since the mineralization of crop residues depends on the presence and activity of these organisms (Castellano-Hinojosa and Strauss 2020Castellano-Hinojosa, A., and Strauss, S. L. (2020). Impact of cover crops on the soil microbiome of tree crops. Microorganisms, 8, 328. https://doi.org/10.3390/microorganisms8030328
https://doi.org/10.3390/microorganisms80...
; Mbuthia et al. 2015Mbuthia, L. W., Acosta-Martínez, V., Bruyn, J., Schaeffer, S., Tyler, D., Odoi, E., Mpheshea, M., and Eash, N. (2015). Long term tillage, cover cro., and fertilization effects on microbial community structure, activity: Implications for soil quality. Soil Biolog., and Biochemistry, 89, 24-34. https://doi.org/10.1016/j.soilbio.2015.06.016
https://doi.org/10.1016/j.soilbio.2015.0...
). In addition, biomass and soil microbial activity are important indicators of soil quality (Balota et al. 2014Balota, E. L., Calegari, A., Nakatani, A. S., and Coyne, M. S. (2014). Benefits of winter cover crop., and no-tillage for microbial parameters in a Brazilian oxisol: A long-term study. Agriculture Ecosystems & Environment, 197, 31-40. https://doi.org/10.1016/j.agee.2014.07.010
https://doi.org/10.1016/j.agee.2014.07.0...
). Thus, by using cover crops it is possible to improve soil microbial properties and increase crop yields over the years (Amorim et al. 2020Amorim, S. P. N., Boechat, C. L., Duarte, L. S. L., Oliveira, D. F., Medeiros, J. C., and Arauco, A. M. S. (2020). Microbial responses to doses of cover plant straw in cerrado piauiense oxisol. Bioscience Journal, 36, 1146-1155. https://doi.org/10.14393/BJ-v36n4a2020-47963
https://doi.org/10.14393/BJ-v36n4a2020-4...
; Chamberlain et al. 2020Chamberlain, L. A., Bolton, M. L., Cox, M. S., Suen, G., Conley, S. P., and Ané, J.-M. (2020). Crop rotation, but not cover crops, influenced soil bacterial community composition in a corn-soybean system in southern Wisconsin. Applied Soil Ecology, 154, 103603. https://doi.org/10.1016/j.apsoil.2020.103603
https://doi.org/10.1016/j.apsoil.2020.10...
). Long-term no-tillage and use of cover crops can improve structure, activity and conditions of the microbial community, with better C, N and P cycling that may increase crop yields compared to conventional soil plowing (Mbuthia et al. 2015Mbuthia, L. W., Acosta-Martínez, V., Bruyn, J., Schaeffer, S., Tyler, D., Odoi, E., Mpheshea, M., and Eash, N. (2015). Long term tillage, cover cro., and fertilization effects on microbial community structure, activity: Implications for soil quality. Soil Biolog., and Biochemistry, 89, 24-34. https://doi.org/10.1016/j.soilbio.2015.06.016
https://doi.org/10.1016/j.soilbio.2015.0...
). However, studies that relate conservation systems, cover crops, soil microbial and enzymatic activity and their effect on agricultural crop yields are still needed in the Northeastern Cerrado region.

The hypothesis tested in this study was that the use of cover crops in a no-tillage system improves soil quality and microbial activity, making it more efficient in nutrient cycling and, consequently, boosting soybean yield. The experiment was developed with the objective of measure soil microbial biomass, soil basal respiration, enzymatic activity and soybean yield in conservation systems cultivated with cover crops species in the Northeastern Cerrado.

MATERIAL AND METHODS

Experiment location

The experiment was carried out in the municipality of Bom Jesus, in Serra do Quilombo (Vô Desidério farm), with geographic coordinates of 09°16’20”S and 44°56’56”W. The average altitude of the experimental area is 610 m and the mean slope is 0.2%. The climate of the region is characterized as tropical with dry winter (Aw according to Köppen’s classification), with an average annual temperature of 26.6 °C and an average rainfall of 1,100 mm·year-1. There are two well-defined seasons in the year: a rainy season from November to April and a dry season from May to October, without rainfall (Andrade Junior et al. 2004Andrade Junior, A. S., Bastos, E. A., Silva, C. O., Gomes, A. A. N., and Figueredo Júnior, L. G. M. (2004). Atlas climatológico do estado do Piauí [Documentos 101]. Teresina: Embrapa Meio-Norte. [Accessed Feb. 10 2020]. Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/32199/1/atlas.pdf
https://ainfo.cnptia.embrapa.br/digital/...
). Data of air temperature and rainfall in the experimental area during soybean cropping season are described in Fig. 1.

Figure 1
Precipitation and air temperature (maximum, mean and minimum), in the 2017/2018 growing season, when the experiment was carried out at Vô Desidério Farm, Bom Jesus, PI.

The soil is a typical oxisol (Soil Survey Staff 2014Soil Survey Staff (2014). Keys to soil taxonomy. Washington: United States Department of Agriculture, Natural Resources Conservation Service.) with 220 g·kg-1 clay. Prior to the installation of the experiment, soil samples were collected in the 0–0.2 m and 0.2–0.4 m layers for soil chemical and particle size characterization (Table 1).

Table 1
Soil chemical properties and particle size distribution before the implementation of the experiment.

The experimental area has been cultivated in a no-tillage system for 11 years, using millet as an interseasonal cover crop. Soybean crops have been in the area for 18 years, and only in the 2013, cropping season there was intercropping corn + brachiaria.

Experimental design

The experiment was carried out in a randomized block design, in split-plot arrangement, using soil tillage in the main plot and cover crops in subplots, with three replicates. Conservation systems consisted of no-tillage (NT) and minimum tillage (MT) performed with a disking at a depth of 0.3 m, preceding the sowing of cover crops. The cover crops used were selected based on previous studies already made in the region (Sousa et al. 2019Sousa, D. C., Medeiros, J. C., Lacerda, J. J. J., Dalla Rosa, J., Boechat, C. L., Souza, M. N. G., Rodrigues, P. C. F., Oliveira Filho, E. G., and Mafra, Á. L. (2019). Dry mass accumulation, nutrient., and decomposition of cover plants. Journal of Agricultural Science, 11, 152-160.; Pacheco et al. 2017Pacheco, L. P., Monteiro, M. M. S., Petter, F. A., Nóbrega, J. C. A., and Santos, A. S. (2017). Biomas., and nutrient cycling by cover crops in Brazilian Cerrado in the state of Piauí. Revista Caatinga, 30, 13-23. https://doi.org/10.1590/1983-21252017v30n102rc
https://doi.org/10.1590/1983-21252017v30...
).

The cover crops were Pennisetum glaucum (millet), Urochloa ruziziensis (brachiaria), Crotalaria spectabilis (C. spectabilis), Crotalaria ochroleuca (C. ochroleuca), intercropping of Pennisetum glaucum + Crotalaria spectabilis (millet + C. spectabilis) and spontaneous plants, with predominance of the following species: Alternanther atenella L., Eleusine indica L., Cenchrus echinatus L. and Sida glaziovii L.

The area corresponding to each experimental block had 30 × 13 m and each plot 5 × 6.5 m. The cover crops were sown in both systems in mid-December 2016, manually and by broadcasting.

The quantities of seeds used were: millet: 30 kg·ha-1, brachiaria: 25 kg·ha-1; C. ochroleuca: 10 kg·ha-1; C. spectabilis: 20 kg·ha-1. Intercropping: 10 kg·ha-1 of millet + 15 kg·ha-1 of C. spectabilis. The plants were sown and incorporated with a light harrowing at a depth of 3 to 5 cm. Fertilization was not used to grow cover crops. A reseeding was required in mid-January 2017 due to germination failures.

Dry mass and nutritional analysis of cover crops

The evaluation of dry mass (DM) production of cover crops was performed at 105 days after the beginning of germination in March 2017. A 0.25 m2 metal frame was randomly launched at two plot sites. The above-ground plant material was cut, washed and then dried in a forced circulation oven at 65 °C until it reached constant mass. Dry mass results were expressed in kg·ha-1.

In the plant material, the chemical analysis of the tissue was performed for the elements: nitrogen (N); phosphorus (P); potassium (K); calcium (Ca); magnesium (Mg); sulfur (S); boron (B); copper (Cu); iron (Fe); manganese (Mn) and zinc (Zn). The methods used to analyze the nutrients after wet digestion (nitroperchloric) were: N –Kjeldahl method; P – colorimetry; K – flame photometry; Ca, Mg, Cu, Fe, Mn and Zn – atomic absorption spectrometry; B – Azomethine H procedure; S – BaCl2 method (Miyazawa et al. 2009Miyazawa, M., Pavan, M. A., Muraoka, T., Carmo, C. A. F. S., and Melo, W. J. (2009). Análise química de tecido vegetal. In: F. C. Silva (Org.), Manual de análises de solos, plantas e fertilizantes (p. 191-234). Brasília: Embrapa Informação Tecnológica.). The nutrient accumulation was estimated from the nutrient content present in each plant tissue and the total dry biomass.

Soybean cultivation, management and productivity

Soybean in the 2017/2018 cropping season was sown on December 13, 2017 after mulching by cover crops. The soybean cultivar used was M8808 IPRO, with a row spacing of 0.5 m, with a population of 200,000 plants·ha-1. Each plot consisted of 5 m in length and 11 soybean lines (for useful area, the end lines and 0.5 m of each row were disregarded). The fertilization used in planting was 300 kg·ha-1 of formula 10-30-10 (NPK) and 150 kg·ha-1 of KCl were top dressing applied. At sowing, soybean seeds were inoculated with Bradyrhizobium japonicum.

During the soybean cycle, the phytosanitary management consisted of two applications of the fungicides propiconazole + diphenoconazole (Score Flexi-150 mL·ha-1) were applied, one at 30 days after emergence (DAE) and one within 20 days after the first application. In addition, the fungicides azoxystrobin + ciproconazole (Priori Xtra-300 mL·ha-1) and mancozeb (Unizeb Gold) were applied at 70 DAE, with a second application of both 20 days later. The control of pests was performed with four applications of tiametoxam + lambda-cyhalothrin (Engeo Full S-300 mL·ha-1), being the first at 30 DAE, and three applications with an interval of 20 days each. Piriproxifem (Epingle-250 mL·ha-1) was applied at 90 DAE.

Grain yield was evaluated when soybean reached the harvest point at 115 days after emergence by collecting three rows of 2 m in length in each experimental unit, correcting grain moisture to 13% and estimated in kg·ha-1.

Sampling and microbial soil analysis

After soybean harvesting, soil samples were collected, one in each subplot, at a depth of 0-0.1 m, and sent to microbial analysis.

The soil microbial biomass carbon and nitrogen (MBC and MBN, respectively) were analyzed by the irradiation–extraction method and the soil basal respiration was determined by quantifying CO2 released after 7 days of incubation under aerobic conditions. The metabolic quotient (qCO2) was obtained by the relationship between soil basal respiration and MBC, according to the methodology described by Mendonça and Matos (2005)Mendonça, E. S., and Matos, E. S. (2005). Matéria orgânica do solo: Métodos de análises. Viçosa: UFV..

Enzyme activities were analyzed by the methodologies described by Frighetto and Valarini (2000)Frighetto, R. T. S., and Valarini, P. J. (2000). Indicadores biológicos e bioquímicos da qualidade do solo: manual técnico [Documento 21]. Jaguariúna: Embrapa Meio Ambiente. [Accessed Jun. 2 2020]. Available at: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/13251/1/2000DC01.pdf
https://www.infoteca.cnptia.embrapa.br/i...
, where enzymatic activities in the respiratory chain were obtained by fluorescein diacetate hydrolysis (FDA) and dehydrogenase activity (DH) analyzed after chloride addition triphenyltetrazolium (TTC) by spectrophotometry.

Statistical analysis

Results were submitted to analysis of variance and, when significant, the Scott–Knott grouping test was performed (p < 0.05) using the statistical program SISVAR (Ferreira 2014Ferreira, D. F. (2014). Sisvar: a guide for its bootstrap procedures in multiple comparisons. Ciência e Agrotecnologia, 38, 109-112. https://doi.org/10.1590/S1413-70542014000200001
https://doi.org/10.1590/S1413-7054201400...
). In order to observe the influence of soil tillage and cover crops use on microbial properties, nutrient cycling and soybean yield, multivariate analysis was performed using the principal component analysis (PCA) technique, presented by biplot graphics. Biplot graphs were prepared considering the first two main components with the largest variances and eigen values greater than 1.0 (Mora-Aguilera et al. 1993Mora-Aguilera, G., Nieto-Angel, D., Téliz, D., and Campbell, C. L. (1993). Development of a Prediction Model for Papaya Ringspot in Veracruz, Mexico.). In addition, the importance of variation factors was assessed by the amount of variation explained by each of them in relation to the total variation.

RESULTS AND DISCUSSION

Dry mass and nutrient accumulation by cover crops

There were no interaction effects considering the factors (soil tillage and cover crops) for dry mass production (DM) and nutrient accumulation (Table 2). There was significant effect of soil tillage for N, Ca, Mg and Cu, with higher values for minimum tillage (MT) with 116, 54.23 and 47 kg·ha-1 of these nutrients compared to no-tillage (NT) with 99, 45, 19 and 41 kg·ha-1, respectively (Table 2).

Table 2
Dry mass production and nutrient accumulation in the above ground mass of the cover plants cultivated in no-tillage and minimum tillage.

The higher accumulation of N, Ca, Mg and Cu in plants grown in MT in relation to NT is due to the disking tillage in the 0–0.3 m layer, which promotes root growth of cover crops during the first year of the experiment. Minimum tillage improves soil aeration, consequently water infiltration is increased and nutrient uptake by cultivated plants is favored (Calonego et al. 2017Calonego, J. C., Raphael, J. P. A., Rigon, J. P. G., Oliveira Neto, L., and Rosolem, C. A. (2017). Soil compaction managemen., and soybean yields with cover crops under no-til., and occasional chiseling. European Journal of Agronomy, 85, 31-37. https://doi.org/10.1016/j.eja.2017.02.001
https://doi.org/10.1016/j.eja.2017.02.00...
).

Cover plants differed in DM production and nutrient accumulation, except Ca and Mn (Table 2). Among the plants, millet and intercropping millet + C. spectabilis presented higher DM production, 8,034 and 8,186 kg·ha-1, respectively. In the same region of this study, Sousa et al. (2019)Sousa, D. C., Medeiros, J. C., Lacerda, J. J. J., Dalla Rosa, J., Boechat, C. L., Souza, M. N. G., Rodrigues, P. C. F., Oliveira Filho, E. G., and Mafra, Á. L. (2019). Dry mass accumulation, nutrient., and decomposition of cover plants. Journal of Agricultural Science, 11, 152-160. obtained similar values of DM and Pacheco et al. (2017)Pacheco, L. P., Monteiro, M. M. S., Petter, F. A., Nóbrega, J. C. A., and Santos, A. S. (2017). Biomas., and nutrient cycling by cover crops in Brazilian Cerrado in the state of Piauí. Revista Caatinga, 30, 13-23. https://doi.org/10.1590/1983-21252017v30n102rc
https://doi.org/10.1590/1983-21252017v30...
found higher values of approximately 11,000 kg·ha-1. Among other factors, the higher DM production of millet is associated with its better adaptation to local edaphoclimatic conditions and its rapid growth, expressing high potential for use in the region, with efficient cover by its residues and remaining longer on the soil surface in relation to the other cover crops (Borges et al. 2015Borges, W. L. B., Freitas, R. S., Mateus, G. P., Sá, M. E., and Alves, M. C. (2015). Produção de soja e milho cultivados sobre diferentes coberturas. Revista Ciência Agronômica, 46, 89-98. https://doi.org/10.1590/S1806-66902015000100011
https://doi.org/10.1590/S1806-6690201500...
; Sousa et al. 2019Sousa, D. C., Medeiros, J. C., Lacerda, J. J. J., Dalla Rosa, J., Boechat, C. L., Souza, M. N. G., Rodrigues, P. C. F., Oliveira Filho, E. G., and Mafra, Á. L. (2019). Dry mass accumulation, nutrient., and decomposition of cover plants. Journal of Agricultural Science, 11, 152-160.).

The intercropping of millet + C. spectabilis presented an increment of DM and accumulation of N, contrary to the results obtained by Sousa et al. (2019)Sousa, D. C., Medeiros, J. C., Lacerda, J. J. J., Dalla Rosa, J., Boechat, C. L., Souza, M. N. G., Rodrigues, P. C. F., Oliveira Filho, E. G., and Mafra, Á. L. (2019). Dry mass accumulation, nutrient., and decomposition of cover plants. Journal of Agricultural Science, 11, 152-160., who found lower values in this intercropping in the same region of this study. This occurs because other factors may influence the DM production of cover crops, such as: crop management, soil fertility, seed quality and germination, plant stand, and the cutting season. Despite the lower DM production in intercropping of millet + C. spectabilis, obtained by Sousa et al. (2019)Sousa, D. C., Medeiros, J. C., Lacerda, J. J. J., Dalla Rosa, J., Boechat, C. L., Souza, M. N. G., Rodrigues, P. C. F., Oliveira Filho, E. G., and Mafra, Á. L. (2019). Dry mass accumulation, nutrient., and decomposition of cover plants. Journal of Agricultural Science, 11, 152-160., the mulch produced presented lower decomposition rate, so the soil surface remained longer covered, suggesting this intercropping as an option to implement no-tillage in the region.

The largest accumulations of N and Mg occurred with the intercropping millet + C. spectabilis (136 and 28 kg·ha-1), millet (128 and 24 kg·ha-1) and C. ochroleuca (125 and 25 kg·ha-1), respectively. Millet accumulated N and Mg in lower amounts than found by Costa et al. (2015)Costa, N. R.., andreotti, M., Ulian, N. A., Costa, B. S., Pariz, C. M., and Teixeira Filho, M. C. M. (2015). Acúmulo de nutrientes e tempo de decomposição da palhada de espécies forrageiras em função de épocas de semeadura. Bioscience Journal, 31, 818-829. https://doi.org/10.14393/BJ-v31n3a2015-22434
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. These authors observed that in two consecutive crop years using millet as cover crop under oxisol, the accumulation of nutrients was 139 and 200 kg·ha-1 of N and 40 and 32 kg·ha-1 of Mg in both crop years, respectively.

The largest accumulations of P and K occurred with millet (26 and 171 kg·ha-1, respectively), and intercropping millet + C. spectabilis (23 and 158 kg·ha-1, respectively). Other studies already reported the ability of millet to accumulate K (Pacheco et al. 2013Pacheco, L. P., Barbosa, J. M., Leandro, W. M., Machado, P. L. O., Assis, R. L., Madari, B. E., and Petter, F. A. (2013). Ciclagem de nutrientes por plantas de cobertura e produtividade de soja e arroz em plantio direto. Pesquisa Agropecuária Brasileira, 48, 1228-1236. https://doi.org/10.1590/S0100-204X2013000900006
https://doi.org/10.1590/S0100-204X201300...
; 2017Pacheco, L. P., Monteiro, M. M. S., Petter, F. A., Nóbrega, J. C. A., and Santos, A. S. (2017). Biomas., and nutrient cycling by cover crops in Brazilian Cerrado in the state of Piauí. Revista Caatinga, 30, 13-23. https://doi.org/10.1590/1983-21252017v30n102rc
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) and this may be related, among other factors, to its high dry mass production in response to the good soil fertility conditions.

Among the micronutrients, only Mn showed similar accumulation among the evaluated plants. The highest accumulation of B and Fe occurred after brachiaria cultivation with 840 and 15,484 g·ha-1, respectively. However, this cover plant presented lower accumulated values for Cu (35 g·ha-1) and was similar to C. spectabilis, which in turn also presented smaller accumulation of Zn (168 g·ha-1). The results obtained for Fe corroborate those obtained by Pittelkow et al. (2012)Pittelkow, F. K., Scaramuzza, J. F., Weber, O. L. S., Maraschin, L., Valadão, F. C. A., and Oliveira, E. S. (2012). Produção de biomassa e acúmulo de nutrientes em plantas de cobertura sob diferentes sistemas de preparo do solo. Agrarian, 5, 212-222., who studied the accumulation of nutrients in different cover crops in a Brazilian Cerrado oxisol, observed higher Fe accumulation in the brachiaria (2,823 g·ha-1), although these values are lower than those obtained in the present study.

Soil microbial attributes

Interaction of cover crops and soil tillage was verified for all microbial attributes evaluated after the soybean harvest (Table 3).

Table 3
Analysis of variance for soil microbial biomass and enzymatic activity affected by tillage and cover crops.

Similar MBC was observed for cover crops grown in MT, however there was difference in the NT system (Table 4). The spontaneous plants in NT presented lower MBC value (142.6 g·kg-1), similar to C. ochroleuca (168.2 g·kg-1). However, the intercropping millet + C. spectabilis and single millet presented higher MBC values in NT compared to MT system, which may be related to the high dry mass production and available of nutrients in these treatments, associated with no soil disturbance, factors that favor microbial growth (Amorim et al. 2020Amorim, S. P. N., Boechat, C. L., Duarte, L. S. L., Oliveira, D. F., Medeiros, J. C., and Arauco, A. M. S. (2020). Microbial responses to doses of cover plant straw in cerrado piauiense oxisol. Bioscience Journal, 36, 1146-1155. https://doi.org/10.14393/BJ-v36n4a2020-47963
https://doi.org/10.14393/BJ-v36n4a2020-4...
).

Table 4
Interaction of cover crops and soil tillage on microbial biomass and enzymatic activity, in the soil depth of 0–0.1 m.

The associated use of cover crops in no-tillage system increased MBC values, regardless of the cover used and in minimum tillage, only legume cover crops increased MBC values (Quadros et al. 2012Quadros, P. D., Zhalnina, K., Davis-Richardson, A., Fagen, J. R., Drew, J., Bayer, C., and Triplett, E. W. (2012). The effect of tillage syste., and crop rotation on soil microbial diversit., and composition in a subtropical acrisol. Diversity, 4, 375-395. https://doi.org/10.3390/d4040375
https://doi.org/10.3390/d4040375...
). The lower microbial carbon biomass in disking tilled soil is probably due to disturbances caused by soil tillage by incorporating waste into the soil, increasing soil/waste contact and oxygen availability, stimulating faster degradation and decreasing the microbial community (Lange et al. 2014Lange, M., Habekost, M., Eisenhauer, N., Roscher, C., Bessler, H., Engels, C., Yvonne Oelmann, Y., Scheu, S., Wilcke, W., Schulze, E.-D., and Gleixner, G. (2014). Bioti., and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland. PLoSONE, 9, e96182. https://doi.org/10.1371/journal.pone.0096182
https://doi.org/10.1371/journal.pone.009...
).

For MBN, in both tillage systems, the spontaneous plants differed from other used plants, with the lowest values of 1.8 and 1.7 g·kg-1 in NT and MT, respectively. There was no difference between NT and MT and between the studied plants. Similarly, Santos et al. (2015)Santos, F. L., Paulino, H. B., Carneiro, M. A. C., Caetano, J. O., Benites, M. V., and Souza, E. D. (2015). Atributos bioquímicos do solo sob diferentes sistemas de produção no sudoeste goiano. Global Scienc., and Technology, 8, 74-86. https://doi.org/10.14688/1984-3801/gst.v8n2p74-86
https://doi.org/10.14688/1984-3801/gst.v...
evaluated cropping systems using soybean/Urochloa brizantha; soybean/spontaneous plants; soybean/corn; soybean/corn + Urochloa ruziziensis and also did not observe difference of MBN between the evaluated production systems.

The results present in this study also corroborate those obtained by Ferreira et al. (2017)Ferreira, E. P. B., Stone, L. F., and Martin-Didonet, C. C. G. (2017). População e atividade microbiana do solo em sistema agroecológico de produção. Revista Ciência Agronômica, 48, 22-31. https://doi.org/10.5935/1806-6690.20170003
https://doi.org/10.5935/1806-6690.201700...
, who observed similar soil microbial properties of rice crop in succession to cover crops, under no-tillage and minimum tillage systems. Although MBN is as an indicator of soil quality, the use of this variable is not the most appropriate for determining the metabolic status of soil microbial communities, and it can be necessary to consider other microbial indicators of soil quality.

Respiration values were changed by cover crops in both soil tillage systems (Table 4). In the NT system, C. ochroleuca and C. spectabilis presented the lowest respiration, differing from the other cover crops. In MT brachiaria cover had higher soil basal respiration (19.7 µg COg-1·day-1) and differed from other cover crops. The use of C. spectabilis and intercropping millet + C. spectabilis under MT presented the lowest soil basal respiration values (9.4 and 7.6 µg COg-1day, respectively). Comparing soil tillage, the lowest soil basal respiration values occurred in C. ochroleuca in NT (9.1 µg COg-1·day-1) and in intercropping the millet + C. spectabilis in MT (7.6 µg COg-1·day-1).

Alves et al. (2011)Alves, T. S., Campos, L. L., Elias Neto, N., Matsuoka, M., and Loureiro, M. F. (2011). Biomassa e atividade microbiana de solo sob vegetação nativa e diferentes sistemas de manejos. Acta Scientiarum. Agronomy, 33, 341-347. https://doi.org/10.402>5/actasciagron.v33i2.4841
https://doi.org/10.402>5/actasciagron.v3...
highlight that the efficiency of microbial biomass is related to the lower carbon lost as CO2 by soil basal respiration. Therefore, it is possible to state that C. ochroleuca and C. spectabilis were efficient in the microbial biomass accumulation, since a significant fraction of carbon is incorporated into the microbial biomass (Table 4).

The highest values of metabolic quotient (qCO2) were observed in spontaneous plants, in relation to the other cover crops, both in NT and MT system (0.13 and 0.10 mg COmg-1 CBM·day-1, respectively). In MT the spontaneous plant cover was similar to C. ochroleuca and brachiaria.

Differences between tillage systems were observed with C. ochroleuca cover which presented lower qCO2 when managed in NT. Intercropping millet + C. spectabilis in MT presented the lowest values.

High qCO2 values, as observed in this study for spontaneous plants, indicate higher energy use to maintain the microbial community, as a result of stress in the system, or the presence of microbial communities in early stages of development (Guimarães et al. 2017Guimarães, N. F., Gallo, A. S., Fontanetti, A., Meneghin, S. P., Souza, M. D. B., Morinigo, K. P. G., and Silva, R. F. (2017). Biomassa e atividade microbiana do solo em diferentes sistemas de cultivo do cafeeiro. Revista de Ciências Agrárias, 40, 34-44. https://doi.org/10.19084/RCA16041
https://doi.org/10.19084/RCA16041...
). Lower values of qCO2 indicate higher efficiency of microbial biomass, i.e. less carbon (C) is lost as CO2 and higher proportion of C is incorporated into microbial cells (Primieri et al. 2017Primieri, S., Muniz, A. W., and Lisboa, H. M. (2017). Dinâmica do carbono no solo em ecossistemas nativos e plantações florestais em Santa Catarina. Floresta e Ambiente, 24, e00110314. https://doi.org/10.1590/2179-8087.110314
https://doi.org/10.1590/2179-8087.110314...
).

The FDA is hydrolyzed by various enzymes (lipases, proteases and esterases) present in microorganisms, this way higher FDA values in NT indicate greater microbial activity in this system with the use of millet and intercropping the millet + C. spectabilis (30.3 µg·g-1 and 28.2 µg·g-1, respectively) compared to MT system (16.8 µg·g-1and 17.5 µg·g-1) (Table 4). For the heterotrophic potential of soil microbiota, represented by the activity of enzymes in FDA, grasses presented higher values, which shows a relationship with the higher dry mass production by these plants and, therefore, a higher carbon source favored greater enzymatic activity in these cover crops, corroborating the work of Santos et al. (2015)Santos, F. L., Paulino, H. B., Carneiro, M. A. C., Caetano, J. O., Benites, M. V., and Souza, E. D. (2015). Atributos bioquímicos do solo sob diferentes sistemas de produção no sudoeste goiano. Global Scienc., and Technology, 8, 74-86. https://doi.org/10.14688/1984-3801/gst.v8n2p74-86
https://doi.org/10.14688/1984-3801/gst.v...
, who obtained higher FDA value for brachiaria. The same authors also describe that the greater activity of enzymes in FDA is linked not only to the effects of accumulated residues and higher DM, but also to the presence of soil moisture, which stimulates microbial activity. In the present study, greater activity of enzymes in FDA occurred in no-tillage, possibly because this system provides greater soil moisture, which stimulates microbial processes.

The enzyme dehydrogenase (DH) in NT was higher with C. ochroleuca (3.4 µLg-1) and with consortium of millet + C. spectabilis (3.6 µLg-1), which differed from the other treatments. The lowest DH activity in NT occurred with millet cultivation (1.9 µLg-1).In MT all cover crops presented higher values than spontaneous plants. Except for C. spectabilis and brachiaria, the other cover plants differed between the SD and CM systems for DH.

Changes in soil physical and chemical properties cause variations in enzymatic activity and can be related to management practices or different dry mass production by cover crops. In this way, higher DH activity in the NT system is related to higher MBC values (Table 4) also found in this soil tillage system. The results obtained in the present study for DH activity corroborate those found by Quadros et al. (2012)Quadros, P. D., Zhalnina, K., Davis-Richardson, A., Fagen, J. R., Drew, J., Bayer, C., and Triplett, E. W. (2012). The effect of tillage syste., and crop rotation on soil microbial diversit., and composition in a subtropical acrisol. Diversity, 4, 375-395. https://doi.org/10.3390/d4040375
https://doi.org/10.3390/d4040375...
, in which the no-tillage presented higher enzymatic activity compared to conventional tillage.

The dehydrogenase enzyme plays an important role as an indicator of biochemical processes involved in soil organic matter decomposition and nutrient cycling and availability, in addition it can be used as indicator of soil fertility and quality. This enzyme also participates in the respiratory chain of microorganisms and is directly related to aeration conditions that are dependent on temperature and soil moisture, vegetation composition, management practices, soil pH and organic matter content (Andrighetti et al. 2014Andrighetti, M. S., Nachtigall, G. R., Queiroz, S. C. N., Ferracini, V. L., and Ayub, M. A. Z. (2014). Biodegradação de glifosato pela microbiota de solos cultivados com macieira. Revista Brasileira de Ciência do Solo, 38, 1643-1653. https://doi.org/10.1590/S0100-06832014000500029
https://doi.org/10.1590/S0100-0683201400...
).

Soybean yield

Soybean yield was influenced only by the cover crops (Fig. 2). The highest soybean yield was obtained after C. ochroleuca and the intercropping millet + C. spectabilis cover crops with values of 3,815 and 4,024 kg·ha-1, respectively, with no difference between these treatments. These results indicate that there are improvements in soil conditions in the treatments using legume cover crops. One of the benefits is due to the higher nitrogen accumulation provided by the cultivation of these plants, as shown in Table 2. Although soybean have symbiosis with nitrogen-fixing bacteria, this is the most required and exported nutrient by this crop (Borges et al. 2015Borges, W. L. B., Freitas, R. S., Mateus, G. P., Sá, M. E., and Alves, M. C. (2015). Produção de soja e milho cultivados sobre diferentes coberturas. Revista Ciência Agronômica, 46, 89-98. https://doi.org/10.1590/S1806-66902015000100011
https://doi.org/10.1590/S1806-6690201500...
). These legume cover species have low C:N ratio and low lignin concentration, which accelerates the decomposition of their residues, makes nutrients readily available in the soil solution and favors their utilization by the sequential crop (Carvalho et al. 2015Carvalho, A. M., Coser, T. R., Rein, T. A., Dantas, R. A., Silva, R. R., and Souza, K. W. (2015). Manejo de plantas de cobertura na floração e na maturação fisiológica e seu efeito na produtividade do milho. Pesquisa Agropecuária Brasileira, 50, 551-561. https://doi.org/10.1590/S0100-204X2015000700005
https://doi.org/10.1590/S0100-204X201500...
). The intercropping millet + C. spectabilis, besides higher nutrient cycling, also presented higher microbial biomass when cultivated under no-tillage. Therefore, is possible that these associated factors justify greater soybean productivity in this consortium. The millet, regardless of single or intercropping, provides sufficient K for the demand for soybeans, which for production of 3,600 kg of grain, requires an equivalent quantity of 114 kg·ha-1 of K (Embrapa, 2013[EMBRAPA] Empresa Brasileira de Pesquisa Agropecuária (2013). Tecnologias de produção de soja – Região Central do Brasil 2014. Londrina: Embrapa Soja. [Accessed Jun. 2 2020]. Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/95489/1/SP-16-online.pdf
https://ainfo.cnptia.embrapa.br/digital/...
). The amount of N and K in the millet residues indicates that, although it is not a legume, it has great nutritional potential to supply the following crops (Pacheco et al. 2017Pacheco, L. P., Monteiro, M. M. S., Petter, F. A., Nóbrega, J. C. A., and Santos, A. S. (2017). Biomas., and nutrient cycling by cover crops in Brazilian Cerrado in the state of Piauí. Revista Caatinga, 30, 13-23. https://doi.org/10.1590/1983-21252017v30n102rc
https://doi.org/10.1590/1983-21252017v30...
).

Figure 2
Soybean yield in succession to cover crops, in the Serra do Quilombo (Vô Desidério farm), Bom Jesus, PI.

However, these nutrients are in organic form and require mineralization to be available the soybean part of N and P is rapidly released at the initial stage of decomposition of plant residues (Costa et al. 2015Costa, N. R.., andreotti, M., Ulian, N. A., Costa, B. S., Pariz, C. M., and Teixeira Filho, M. C. M. (2015). Acúmulo de nutrientes e tempo de decomposição da palhada de espécies forrageiras em função de épocas de semeadura. Bioscience Journal, 31, 818-829. https://doi.org/10.14393/BJ-v31n3a2015-22434
https://doi.org/10.14393/BJ-v31n3a2015-2...
). Thus, it is important to highlight the high amounts of nutrients that can be released and used by crops in succession.

Crotalaria ochroleuca also showed higher productivity, was efficient in cycling nutrients similarly to the consortium and, cultivated under no-tillage, showed low soil basal respiration and qCO2 and high values of DH enzyme, which indicates the efficiency of the microbial community to assimilate carbon and use nutrients. In a long-term study, Mbuthia et al. (2015)Mbuthia, L. W., Acosta-Martínez, V., Bruyn, J., Schaeffer, S., Tyler, D., Odoi, E., Mpheshea, M., and Eash, N. (2015). Long term tillage, cover cro., and fertilization effects on microbial community structure, activity: Implications for soil quality. Soil Biolog., and Biochemistry, 89, 24-34. https://doi.org/10.1016/j.soilbio.2015.06.016
https://doi.org/10.1016/j.soilbio.2015.0...
also observed relationship of soil microbial quality and nutrient cycling in the increased cotton yield in no-tillage. The soybean yield was higher than that found by Nascente and Stone (2018)Nascente, A. S., and Stone, L. F. (2018). Cover crops as affecting soil chemica., and physical propertie., and development of upland ric., and soybean cultivated in rotation. Rice Science, 25, 340-349. https://doi.org/10.1016/j.rsci.2018.10.004
https://doi.org/10.1016/j.rsci.2018.10.0...
, who evaluated the effect of cover crops grown in the off-season and obtained 3,440 kg·ha-1 of soybean when cultivated after intercropping millet + C. ochroleuca under Cerrado conditions. Also, in the Northeastern Cerrado, Pacheco et al. (2017)Pacheco, L. P., Monteiro, M. M. S., Petter, F. A., Nóbrega, J. C. A., and Santos, A. S. (2017). Biomas., and nutrient cycling by cover crops in Brazilian Cerrado in the state of Piauí. Revista Caatinga, 30, 13-23. https://doi.org/10.1590/1983-21252017v30n102rc
https://doi.org/10.1590/1983-21252017v30...
obtained 3,874 kg·ha-1 of soybean, using millet preceding the soybean + brachiaria associated with soybean in the phenological phase R5.6.

Principal component analysis (PCA)

Principal component analysis (PCA) explained 61% of the total data variation, with 39% in the main component 1 (CP1) and 22% in the component 2 (CP2) (Fig. 3). Through CP1, DM, P, K and Mg were the variables that most influenced the dispersion of the data. And in CP2, the variables that contributed the most were Ca, qCO2 and FDA. It was observed that the use of exclusive millet and intercropping millet + C. spectabilis, regardless of the tillage system, presented higher dry mass production and nutrient accumulation, as observed in Table 2 and discussed above. In addition, the use of the intercropping of these species resulted in higher soybean yield (Fig. 2).

Figure 3
Principal component analysis (PCA), for soil microbial biomass and enzymatic activity, dry mass production, macronutrient cycling and soybean yield, after cover crops in soil tillage systems.

Soil microbial activity, represented by the variables BMC, MBN and DH, showed a positive correlation with soybean yield in this first evaluation after the introduction of cover crops. These observations demonstrate that biomass and soil microbial activity are important, not only as indicators of soil quality, but because they play an important role in nutrient supply to plants (Balota et al. 2014Balota, E. L., Calegari, A., Nakatani, A. S., and Coyne, M. S. (2014). Benefits of winter cover crop., and no-tillage for microbial parameters in a Brazilian oxisol: A long-term study. Agriculture Ecosystems & Environment, 197, 31-40. https://doi.org/10.1016/j.agee.2014.07.010
https://doi.org/10.1016/j.agee.2014.07.0...
) and these soil components can increase soybean yield. Evaluating long-term experiments, for 12 to 17 years, based on soybean and corn crop yield history, Lopes et al. (2013)Lopes, A. A. C., Sousa, D. M. G., Chaer, G. M., Reis Junior, F. B., Goedert, W. J., and Mendes, I. C. (2013). Interpretation of microbial soil indicators as a function of crop yiel., and organic carbon. Soil Science Society of America Journal, 77, 461-472. https://doi.org/10.2136/sssaj2012.0191
https://doi.org/10.2136/sssaj2012.0191...
found that highly productive soils also have high microbial biomass, soil basal respiration, and soil cellulase enzyme activity. Similarly, Mbuthia et al. (2015)Mbuthia, L. W., Acosta-Martínez, V., Bruyn, J., Schaeffer, S., Tyler, D., Odoi, E., Mpheshea, M., and Eash, N. (2015). Long term tillage, cover cro., and fertilization effects on microbial community structure, activity: Implications for soil quality. Soil Biolog., and Biochemistry, 89, 24-34. https://doi.org/10.1016/j.soilbio.2015.06.016
https://doi.org/10.1016/j.soilbio.2015.0...
, in a long-term study, also observed in addition to improved soil microbiological quality and nutrient cycling, increased yield in no-tillage and mulching compared to conventional tillage and bare soil.

The single millet and the consortium millet + C. spectabilis, in NT system favored MBC, which can be related to the high DM production by these plants (Table 2). Soil microbial biomass still depends on the characteristics of the crop residues, so residues with high C:N ratio, such as millet, need more time for decomposition of their biomass reflecting the presence of more active organic matter in the soil (Martínez-García et al. 2018Martínez-García, L. B., Korthals, G., Brussaard, L., Jørgense, H. B., and Deyn, G. B. (2018). Organic managemen., and cover crop species steer soil microbial community structur., and functionality along with soil organic matter properties. Agriculture Ecosystem., and Environment, 263, 7-17. https://doi.org/10.1016/j.agee.2018.04.018
https://doi.org/10.1016/j.agee.2018.04.0...
). Microbial biomass carbon is still closely related to respiration since low values of soil basal respiration combined with high MBC in millet cover show that the biomass of these residues was efficient in carbon accumulation, i.e., less carbon in the form of CO2 lost by respiration, and more incorporation of carbon into microbial tissues (Navroski et al. 2017Navroski, D., Moreira, A., Colozzi-Filho, A., and Grange L. (2017). Atributos microbiológicos do solo em diferentes sistemas de manejo no oeste paranaense. Agrotrópica, 29, 127-134.).

CONCLUSION

The highest dry mass production and nutrient cycling in this conservation system occurs with intercropping millet + C. spectabilis and single millet.

The soil microbial activity is promoted by millet, C. ochroleuca and intercropping of millet + C. spectabilis in no-tillage system. Cover crops in conservation systems improve soil microbial quality and increase grain yield even in the first soybean crop season.

ERRATA

  • In the article Conservation system improves soil microbial quality and increases soybean yield in the Northeastern Cerrado with DOI: https://doi.org/10.1590/1678-4499.20200117 published in Bragantia vol.79 no.4 Campinas Oct./Dec. 2020:
    • In the footline where is read Bragantia, Campinas, v. 79, n. 4, p.474-486, 2020

    • Should be read Bragantia, Campinas, v. 79, n. 4, p.599-611, 2020.

  • FUNDERS

    Embrapa
    Grant # 22.13.11.004.00.03.004
    CNPq
    Grant #442506/2014-7
    PQ fellowship
    Grant #307908/2017-8

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Edited by

Section Editor: Osvaldo Guedes Filho

Publication Dates

  • Publication in this collection
    18 Sept 2020
  • Date of issue
    Oct-Dec 2020

History

  • Received
    20 Mar 2020
  • Accepted
    21 July 2020
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