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Carbon Mineralization in Soil Aggregate Classes Under Leguminous Tree Planting in North Fluminense, Brazil

Abstract

The physical protection of soil organic matter through its occlusion in aggregates is a mechanism which reduces their accessibility by microorganisms. When the physically protected carbon (C) becomes accessible to the microbiota, it generates a flow of CO2. The objective of this study was to evaluate the C mineralization rate in macro and microaggregates of macerated and non-macerated soils under different leguminous tree, pasture, and secondary forest (capoeira). The CO2 mineralization curves showed that maceration increased the amount of C mineralized in macroaggregates, mainly in leguminous tree. Maceration provided an increase of approximately 50% and 47% in acacia and ingá, respectively, and 35% in sabiá. Capoeira and pasture did not respond to maceration.

Keywords:
microbial activity; physical protection; carbon lability; organic matter

There are only a few Atlantic Forest massif fragments in the North Fluminense region in Brazil. Part of the deforested area had its soil degraded by livestock farming, with frequent use of fire to renew pastures. Because of this, planting trees is an alternative for recovering these degraded lands (Gama-Rodrigues et al., 2008Gama-Rodrigues EF, Da Gama-Rodrigues AC, Paulino GM, Franco AA. Atributos químicos e microbianos de solos sob diferentes coberturas vegetais no norte do estado do Rio de Janeiro. Rev Bras Ciência Solo, 2008, 32: 1521-1530.). Due to the large plant residue deposition on the soil, forest systems are characterized as organic matter accumulator systems, and therefore are considered C reservoirs (Vicente et al., 2019Vicente LC, Gama-Rodrigues EF, Gama-Rodrigues AC, Marciano CR. Organic carbon within soil aggregates under forestry systems and pasture in Southeast region of Brazil. Catena, 2019, v.182, 104139. https://doi.org/10.1016/j.catena.2019.104139
https://doi.org/10.1016/j.catena.2019.10...
). For example, in addition to producing a significant amount of plant biomass, leguminous tree fix atmospheric N2, which guarantees higher organic matter and nitrogen levels incorporated into the soil (Figueiredo et al., 2016Figueiredo MA de, Oliveira DP, Soares B L, Morais AR de, Moreira FMDS, Andrade MJ B. Nitrogen and molybdenum fertilization and inoculation of common bean with Rhizobium spp. in two oxisols. Acta Scientiarum. Agronomy, 2016, 38(1), 85.).

Aggregates are secondary particles formed by combining mineral particles with organic and inorganic substances (Bronick and Lal 2005Bronick CJ, Lal R. Soil structure and management: a review. Geoderma, 2005, 124:3-22.). Depending on their size, they are classified into macroaggregates (2.00-0.25 mm) and microaggregates (0.25-0.053 mm). Macroaggregates are formed by temporary binding agents present in the soil such as carbohydrates released by the roots, fine roots, fungi hyphae, and organic matter (Tisdall and Oades 1982Tisdall JM, Oades JM. Organic matter and water-stable aggregates in soils. Journal of Soil Science, 1982, 33:141-163.). Conversely, microaggregate formation is related to the interaction between the surface of minerals and organic binders such as carbohydrates of vegetables and microbiological origin (Verchot et al. 2011Verchot LV, Dutaur L, Shepherd KD, Albrecht A. Organic matter stabilization in soil aggregates: understanding the biogeochemical mechanisms that determine the fate of carbon inputs in soils. Geoderma , 2011, 161:182-193. https://doi.org/10.1016/j.geoderma.2010.12.017
https://doi.org/10.1016/j.geoderma.2010....
).

The physical protection represents one of the most important mechanisms for soil organic matter stabilization (Monroe et al., 2022Monroe PHM, Gama-Rodrigues EF, Gama-Rodrigues AC, Vicente LC. Carbon and Nitrogen Occluded in Soil Aggregates Under Cacao-Based Agroforestry Systems in Southern Bahia, Brazil. J. Soil Sci. Plant Nutr, 2022, 22:1326-1339. https://doi.org/10.1007/s42729-021-00734-3
https://doi.org/10.1007/s42729-021-00734...
). The C mineralization within the aggregates can be obtained through the CO2 release curve in samples of macerated (submitted physical disaggregation) and non-macerated (did not undergo physical disaggregation) aggregates subjected to incubation. Maceration makes the organic matter that was protected in the aggregates available to the microbiota (Gárcia-Oliva et al., 2004García-Oliva F, Oliva M, Sveshtarova B. Effect of soil macroaggregates crushing on C mineralization in a tropical deciduous forest ecosystem. Plant and Soil, 2004, 259:297-305.). Furthermore, this procedure can also cause stress to the microbial community, due to the rupture of the aggregate, which can influence their activity. Thus, when the carbon becomes accessible to the microbiota, it generates a flow of CO2. The amount of CO2 released varies based on the lability level of organic matter within the aggregates. The objective of this work was to evaluate the C mineralization rate in macro and microaggregates of soils under different leguminous tree, pasture, and secondary forest on a site located in in the Southeast region of Brazil.

The soil was collected in the municipality of Conceição de Macabú, RJ, in an experimental area with five plant covers: Acacia auriculiformis (Acácia), Mimosa caesalpiniifolia (Sabiá) and Inga spp (Ingá), and two additional plant covers adjacent to the plantations used as reference, both approximately 40 years old: a degraded pasture, which represents the vegetation prior to planting tree species, with a predominance of molasses grass (Melinis minutiflora), paspalum grass (Paspalum maritimum) and satintail grass (Imperata brasiliensis); and a forest fragment of the Atlantic Forest in secondary succession (capoeira). Three field replications of each cover were collected at a depth of 0-10 cm. Before the samples were taken, the litter layer was removed. All of the samples were taken in a 1 m2 pit dug to a depth of 0.4 m. To minimize compression and to obtain a representative sample for the aggregation state of the soil, samples were taken using a bricklayer’s trowel inserted into the soil at the lower level of the sampling depth. The three composite samples were prepared in each land use system by compositing equal amounts of soils from ten pits for each replicate. The aggregate classes (2.00-0.25 mm; 0.25-0.053 mm) were obtained by dry screening: a set of sieves with different mesh diameters (2.00 mm; 0.25 mm and; 0.053 mm) were used (Gupta and Germida, 1988Gupta VVS R, Germida J J. Distribution of microbial biomass and its activity in different soil aggregation size classes as affected by cultivation. Soil Biol. Biochem., 1988, 20:777-786.). 150 g of soil from each composite sample from each plant cover was added to the set of sieves, considering 15 minutes of agitation in a shaking device. A fraction of of macro and microaggregates mass were manually macerated using gral until all aggregates were visibly broken. Sample moisture was standardized to 60% of the soil’s maximum saturation capacity (Grisi, 1995GRISI, BM. Biomassa e a atividade de microrganismos do solo: Revisão metodológica. R. Nordestina Biol., 1995, 10:1-22.).

Incubation was performed by placing each vial of soil in a glass jar that was kept hermetically sealed. Soil respiration was estimated by the amount of CO2 released initially every three days (in the first 10 days), and then every 5 days, for a total period of 40 days. Samples containing 40 g of different aggregate classes (macerated and non-macerated) + 1 g of fresh soil (representing the inoculum with a new population of microorganisms) were weighed. Each 3L glass jar contained a bottle with 10 mL of 1M NaOH and a bottle with water in order to maintain constant humidity until the end of incubation. At the end of each incubation period, the bottles with NaOH were titrated with 0.5 M HCl and 2 mL of barium chloride (BaCl2) was added to complete CO2 precipitation. The NaOH bottles were replaced for the new incubation period until the end time. The soil was weighed and the humidity was maintained at 60% of the saturation capacity to maintain the humidity of each treatment until the end of incubation (Azuaje et al., 2012Azuaje EI, Comerford NB, Harris WG, Iii JBR, Grunwald S. Loblolly and slash pine control organic carbon in soil aggregates and carbon mineralization. Forest Ecology and Management, 2012, 263: 1-8.).

The C mineralization process was tested using several models such as the Gompertz, Logistic, and Mitscherlich models including linear, quadratic, with and without intercept. The decision about the goodness of fit of the models was made based on information theory, as suggested by Burnham and Anderson (2004Burnham KP, Anderson DR. Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods & Research, 2004, 33:261-304. ). The goodness of fit was evaluated using the initial criterion of Akaike (1974Akaike, H. A new look at the statistical model identification. IEEE Transactions on Automatic Control, 1974, 19:716-723. ) corrected for the sample size, as recommended by Sugiura (1978Sugiura N. Further analysis of the data by Akaike’s information criterion and the finite corrections. Communications in Statistics - Theory and Methods, 1978, 7: 13-26.). Next, the goodness-of-fit measures derived from the corrected Akaike criterion were computed. These measures were calculated for all the models evaluated with or without random effects on the parameters. The models that challenged the traditional assumptions of homoscedasticity and independence of random errors were also evaluated. The data was analyzed using the SAS tool (Statistical Analysis System) and R Software.

The Gompertz model was considered the best choice to represent the reality contained in the data and also because it is efficient in biologically interpreting its parameters (Table 1). The curves of mineralized C in macro and microaggregates, macerated and non-macerated, of the different vegetation covers showed an exponentially increasing slope in the initial incubation period, followed by a regular and progressive increase in C mineralization from the 10th day onwards. The amount of mineralized C was greatest between the 35th and 40th incubation days (Figures 1 and 2). These results were similar to Araújo et al. (2001)Araujo AMS, Sampaio EVSB, Salcedo IH. Carbon and nitrogen mineralization in stored samples of soil planted with sugarcane with and without fertilization, over ten years. Rev. Bras. Ciênc. Solo, 2001, 25:43-53., Gonçalves et al. (2001Gonçalves JLM, Mendes KCFS, Sasaki CM. Nitrogen mineralization in natural and forest plantation ecosystems of São Paulo state. Rev Bras Cienc Solo , 2001, 25:601-616.) and Barreto et al. (2010Barreto PAB, Gama-Rodrigues EF, Gama-Rodrigues AC. Carbon and nitrogen mineralization in soils under an eucalyptus plantation chronosequence. Rev Bras Cienc Solo, 2010, 34:735-745.), who found that the amount of mineralized C was lower during the first incubation days. In the same vegetation cover as in the present study, Nunes et al. (2015Nunes DA, Gama-Rodrigues EF, Barreto PA, Gama-Rodrigues AC, Monroe PH. Carbon and nitrogen mineralization in soil of leguminous trees in a degraded pasture in northern Rio de Janeiro, Brazil. Journal of Forestry Research, 2015, 27, 91-99.) showed that the C mineralization curve fit the exponential model, and that there was still C available for mineralization by microorganisms after 20 weeks of incubation.

Table 1
Model adjustment coefficients.

Figure 1
Observed (symbols) and expected (lines) values of mineralized C according to incubation time in non-macerated macroaggregates (a) and macerated (b) of soils under different vegetation covers. ACA, acacia; ING, inga; CAP, capoeira; SAB, sabia; e PAS, pasture.

Figure 2
Observed (symbols) and expected (lines) values of mineralized C according to incubation time in non-macerated microaggregates (a) and macerated (b) of soils under different vegetation covers. ACA, acacia; ING, inga; CAP, capoeira; SAB, sabia; e PAS, pasture.

The curves also showed that maceration generally increased the amount of C mineralized in the macroaggregates. Maceration provided an increase of approximately 50% and 47% in acacia and ingá, respectively, and 35% in sabiá. Capoeira and pasture did not show responses to maceration (Figures 1a and 1b). The C mineralization curves after maceration suggest that leguminous tree modified the chemical composition of C in the soil aggregates studied and favored C mineralization, unlike the reference covers. Maceration increased the specific surface area of the aggregates and the accessibility to microbial attack by unprotecting the inaccessible soil organic C reservoir (Cadisch et al., 2006Cadisch G, Mutuo P, Mercado A, Hairiah K, Nyamugafata P, Boye A. Albrecht, A. Organic matter management in tropical agroforestry systems: Soil quality, soil C storage and soil atmosphere gas exchange. In: Gama-Rodrigues, A.C.; Barros, N.F.; Gama-Rodrigues, E.F.; Freitas, M.S.M.; Viana, A.P.; Jasmin, J.M.; Marciano, C.R. & Carneiro, J.G.A., eds. Sistemas Agroflorestais: Bases científicas para o desenvolvimento sustentável. Campos dos Goytacazes, 2006, p. 275-287.). Studies by Gupta and Germida (1988Gupta VVS R, Germida J J. Distribution of microbial biomass and its activity in different soil aggregation size classes as affected by cultivation. Soil Biol. Biochem., 1988, 20:777-786.) and Beare et al. (1994Beare MH, Hendrix PF, Cabrer ML, Coleman DC. Aggregate-Protected and Unprotected Organic Matter Pools in Conventional and No-Tillage Soils. Soil Sci Soc Am J, 1994, 58: 787.) also found a significant increase in C mineralization in aggregates after maceration. Additionally, maceration can potentially cause an imbalance in the microbial community due to the destruction of soil aggregates. This can lead to stress in this community, similar to what occurs in areas with conventional tillage systems. In these areas, management practices break up the aggregates, exposing organic matter to microbial and enzymatic attack, ultimately causing an imbalance. Furthermore, maceration can mix different organic matter fractions with varying levels of lability and transformation. This effect can be intensified in macroaggregates that arise from areas with leguminous tree species.

Maceration of microaggregates also promoted an increase in mineralized C during the 40 days of incubation in all vegetation covers (Figures 2a and 2b), which suggests the presence of organic matter available for action by the soil microbiota. The curves of mineralized C in non-macerated microaggregates varied little between vegetation covers (Figure 2a). When evaluating the chemical composition of C in different soil fractions (coarse fractions: air-dried fine earth; macro and micro-aggregates and fine fractions: occluded fractions of macro and micro-aggregates) using Fourier transform infrared spectroscopy, Lisboa et al. (2022Lisboa FM, Gama-Rodrigues EF, Gama-Rodrigues AC. Fluoridic Acid in the Infrared Spectroscopy Analysis of Chemical Composition of Organic Matter. FLORAM, 2022, 29(3): e20210098) showed that aromatic material was predominant in coarser fractions (less C protection from the action of the microbiota) and the fine fractions had a more aliphatic character. Due to the lower complexation of organic matter to the mineral fraction in the coarser fractions, the labile forms of C were the first used by microorganisms, which led to a proportional enrichment of aromatic C. This is in contrast to the fine fractions, which protect organic matter from microbiota action, in which there was an accumulation of more labile fractions. Likewise, when analyzing the chemical composition of C also using infrared spectroscopy, Vicente et al. (2023Vicente LC, Gama-Rodrigues EF, Aleixo S, Gama-Rodrigues AC, Andrade GRP. Chemical Composition of Organic Carbon in Aggregate Density Fractions Under Cacao Agroforestry Systems in South Bahia, Brazil. J. Soil Sci. Plant Nutr , 2023, published online. https://doi.org/10.1007/s42729-022-01083-5
https://doi.org/10.1007/s42729-022-01083...
) observed that the organic matter fraction associated with minerals (Cm < 53 µm) was the main reservoir of labile compounds.

In turn, Faustino et al. (2022Faustino LL, Gama-Rodrigues EF, Gama-Rodrigues AC, Barreto-Garcia PAB. Oxidizable organic carbon fractions in soils under leguminous nitrogen-fixing trees in a degraded pasture. Ciência Rural, 2022, 52: e20210488) observed that cultivation with leguminous tree favored the distribution of labile and moderately labile fractions along the soil profile when studying the lability of C using the chemical fractionation method of C by an oxidation gradient in the same areas of the present study. On the other hand, the reference covers contributed with a recalcitrant fraction below 20 cm deep.

The organic matter added to the soil after 13 years of conversion of degraded pasture into plantations with leguminous tree favored soil microbiota activity through the diversity of compounds with different lability levels. Although, its physical protection particularly in macroaggregates is a strategy for preserving C in the soil. The results also showed that the larger aggregate fraction was more responsive to changes provided by maceration. Thus, tree-based production systems which promote a significant input of organic matter and no-tillage are alternatives for maintaining C in the soil, and consequently for reducing CO2 emissions into the atmosphere.

REFERENCES

  • Akaike, H. A new look at the statistical model identification. IEEE Transactions on Automatic Control, 1974, 19:716-723.
  • Araujo AMS, Sampaio EVSB, Salcedo IH. Carbon and nitrogen mineralization in stored samples of soil planted with sugarcane with and without fertilization, over ten years. Rev. Bras. Ciênc. Solo, 2001, 25:43-53.
  • Azuaje EI, Comerford NB, Harris WG, Iii JBR, Grunwald S. Loblolly and slash pine control organic carbon in soil aggregates and carbon mineralization. Forest Ecology and Management, 2012, 263: 1-8.
  • Barreto PAB, Gama-Rodrigues EF, Gama-Rodrigues AC. Carbon and nitrogen mineralization in soils under an eucalyptus plantation chronosequence. Rev Bras Cienc Solo, 2010, 34:735-745.
  • Beare MH, Hendrix PF, Cabrer ML, Coleman DC. Aggregate-Protected and Unprotected Organic Matter Pools in Conventional and No-Tillage Soils. Soil Sci Soc Am J, 1994, 58: 787.
  • Bronick CJ, Lal R. Soil structure and management: a review. Geoderma, 2005, 124:3-22.
  • Burnham KP, Anderson DR. Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods & Research, 2004, 33:261-304.
  • Cadisch G, Mutuo P, Mercado A, Hairiah K, Nyamugafata P, Boye A. Albrecht, A. Organic matter management in tropical agroforestry systems: Soil quality, soil C storage and soil atmosphere gas exchange. In: Gama-Rodrigues, A.C.; Barros, N.F.; Gama-Rodrigues, E.F.; Freitas, M.S.M.; Viana, A.P.; Jasmin, J.M.; Marciano, C.R. & Carneiro, J.G.A., eds. Sistemas Agroflorestais: Bases científicas para o desenvolvimento sustentável. Campos dos Goytacazes, 2006, p. 275-287.
  • Faustino LL, Gama-Rodrigues EF, Gama-Rodrigues AC, Barreto-Garcia PAB. Oxidizable organic carbon fractions in soils under leguminous nitrogen-fixing trees in a degraded pasture. Ciência Rural, 2022, 52: e20210488
  • Figueiredo MA de, Oliveira DP, Soares B L, Morais AR de, Moreira FMDS, Andrade MJ B. Nitrogen and molybdenum fertilization and inoculation of common bean with Rhizobium spp. in two oxisols. Acta Scientiarum. Agronomy, 2016, 38(1), 85.
  • Gama-Rodrigues EF, Da Gama-Rodrigues AC, Paulino GM, Franco AA. Atributos químicos e microbianos de solos sob diferentes coberturas vegetais no norte do estado do Rio de Janeiro. Rev Bras Ciência Solo, 2008, 32: 1521-1530.
  • García-Oliva F, Oliva M, Sveshtarova B. Effect of soil macroaggregates crushing on C mineralization in a tropical deciduous forest ecosystem. Plant and Soil, 2004, 259:297-305.
  • Gonçalves JLM, Mendes KCFS, Sasaki CM. Nitrogen mineralization in natural and forest plantation ecosystems of São Paulo state. Rev Bras Cienc Solo , 2001, 25:601-616.
  • GRISI, BM. Biomassa e a atividade de microrganismos do solo: Revisão metodológica. R. Nordestina Biol., 1995, 10:1-22.
  • Gupta VVS R, Germida J J. Distribution of microbial biomass and its activity in different soil aggregation size classes as affected by cultivation. Soil Biol. Biochem., 1988, 20:777-786.
  • Lisboa FM, Gama-Rodrigues EF, Gama-Rodrigues AC. Fluoridic Acid in the Infrared Spectroscopy Analysis of Chemical Composition of Organic Matter. FLORAM, 2022, 29(3): e20210098
  • Monroe PHM, Gama-Rodrigues EF, Gama-Rodrigues AC, Vicente LC. Carbon and Nitrogen Occluded in Soil Aggregates Under Cacao-Based Agroforestry Systems in Southern Bahia, Brazil. J. Soil Sci. Plant Nutr, 2022, 22:1326-1339. https://doi.org/10.1007/s42729-021-00734-3
    » https://doi.org/10.1007/s42729-021-00734-3
  • Nunes DA, Gama-Rodrigues EF, Barreto PA, Gama-Rodrigues AC, Monroe PH. Carbon and nitrogen mineralization in soil of leguminous trees in a degraded pasture in northern Rio de Janeiro, Brazil. Journal of Forestry Research, 2015, 27, 91-99.
  • Sugiura N. Further analysis of the data by Akaike’s information criterion and the finite corrections. Communications in Statistics - Theory and Methods, 1978, 7: 13-26.
  • Tisdall JM, Oades JM. Organic matter and water-stable aggregates in soils. Journal of Soil Science, 1982, 33:141-163.
  • Verchot LV, Dutaur L, Shepherd KD, Albrecht A. Organic matter stabilization in soil aggregates: understanding the biogeochemical mechanisms that determine the fate of carbon inputs in soils. Geoderma , 2011, 161:182-193. https://doi.org/10.1016/j.geoderma.2010.12.017
    » https://doi.org/10.1016/j.geoderma.2010.12.017
  • Vicente LC, Gama-Rodrigues EF, Aleixo S, Gama-Rodrigues AC, Andrade GRP. Chemical Composition of Organic Carbon in Aggregate Density Fractions Under Cacao Agroforestry Systems in South Bahia, Brazil. J. Soil Sci. Plant Nutr , 2023, published online. https://doi.org/10.1007/s42729-022-01083-5
    » https://doi.org/10.1007/s42729-022-01083-5
  • Vicente LC, Gama-Rodrigues EF, Gama-Rodrigues AC, Marciano CR. Organic carbon within soil aggregates under forestry systems and pasture in Southeast region of Brazil. Catena, 2019, v.182, 104139. https://doi.org/10.1016/j.catena.2019.104139
    » https://doi.org/10.1016/j.catena.2019.104139

Edited by

Associate editor:

Marcos Gervásio Pereira http://orcid.org/0000-0002-1402-3612

Publication Dates

  • Publication in this collection
    15 Apr 2024
  • Date of issue
    2024

History

  • Received
    09 Oct 2023
  • Accepted
    23 Mar 2024
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