Acessibilidade / Reportar erro

Soil greenhouse gases emissions in a goat production system in the Brazilian semiarid region

Emissões de gases do efeito estufa do solo em sistema de produção de caprinos no semiárido brasileiro

ABSTRACT

In the climate change scenario, studying greenhouse gases (GHG) emissions and measures of mitigation in the Caatinga biome are strategic and may provide a basis for mitigation plans. This study aimed to evaluate the soil CO2, CH4 and N2O fluxes, as well as determining an annual baseline for GHG emissions, in a reference site of silvopastoral production system in the Brazilian semiarid region, in order to provide subsidies for future studies on GHG emissions mitigation. The GHG fluxes were monitored over one year, in a buffel grass pasture and in grazed and native Caatinga areas, which are components of a long-term silvopastoral system. The CO2 fluxes ranged from -19.98 to 179.12 mg m-2 h-1 of CO2-C, CH4 fluxes from -76.21 to 113.87 µg m-2 h-1 of CH4-C, N2O fluxes from -1,043.12 to 471.37 µg m-2 h-1 of N2O-N and the soil moisture was the main factor limiting the GHG fluxes. The total emissions converted to CO2-equivalent in the anthropized areas were lower than in the native area (65 % for the buffel grass pasture and 741 % for the grazed Caatinga). Therefore, it is possible to afrm that the GHG soil emissions from grazed areas in the Caatinga biome are not as high as in the native Caatinga, what is an important indication of the environmental sustainability of the evaluated silvopastoral system.

KEYWORDS
Cenchrus ciliaris L.; carbon dioxide; nitrous oxide; methane; silvopastoral system

RESUMO

No cenário das mudanças climáticas, o estudo das emissões de gases do efeito estufa (GEE) e de medidas de mitigação na Caatinga são estratégicos e podem fornecer a base para planos de mitigação. Objetivou-se avaliar os fluxos de CO2, CH4 e N2O do solo, bem como determinar uma linha de base anual para as emissões de GEE, em um sistema de produção silvipastoril de referência no semiárido brasileiro, a fim de fornecer subsídios para estudos futuros de mitigação das emissões de GEE. Os fluxos de GEE foram monitorados durante um ano, em pastagem de capim buffel e em área de Caatinga pastejada e nativa, as quais são componentes de um sistema silvipastoril de longa duração. Os fluxos de CO2 variaram de -19,98 a 179,12 mg m-2 h-1 de C-CO2, os de CH4 de -76,21 a 113,87 µg m-2 h-1 de C-CH4, os de N2O de -1.043,12 a 471,37 µg m-2 h-1 de N-N2O e a umidade do solo foi o principal fator limitante para os fluxos de GEE. As emissões totais convertidas para CO2-equivalente nas áreas antropizadas foram menores que na área de vegetação nativa (65 % para o capim buffel e 741 % para a Caatinga pastejada). Portanto, pode-se afrmar que as emissões de GEE nas áreas pastejadas no bioma Caatinga não são tão altas quanto na Caatinga nativa, o que é um importante indicador da sustentabilidade ambiental do sistema silvipastoril avaliado.

PALAVRAS-CHAVE
Cenchrus ciliaris L.; dióxido de carbono; óxido nitroso; metano; sistema silvipastoril

INTRODUCTION

The Brazilian Northeast region comprises the most populated semiarid area in the world (Assad et al. 2013ASSAD, E. D.; BUAINAIN, A. M.; PINTO, H. S.; DUARTE, V. S.; SOUSA, M. R. de. Climate changes: challenges for Brazil. In: DHIRENDRA, K. V. (ed.). Climate change, sustainable development & human security. Plymouth: Lexington Books, 2013. p. 169-199.) and is characterized by a semiarid climate, with a negative water balance. The native vegetation of this region is Caatinga, the largest continuous nucleus of the seasonally dry tropical forest and woodland biome in South America (Fernandes et al. 2020FERNANDES, M. F.; CARDOSO, D.; QUEIROZ, L. P. An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism. Journal of Arid Environments, v. 174, e104079, 2020.). Caatinga presents a high floristic diversity, with 3,347 species and 962 genera, of which 526 species and 29 genera are endemic (Fernandes et al. 2020FERNANDES, M. F.; CARDOSO, D.; QUEIROZ, L. P. An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism. Journal of Arid Environments, v. 174, e104079, 2020.). Historically, the Caatinga vegetation is used as an energy source, both in the form of frewood and charcoal, and as animal feed for goats and sheep, especially during the rainy season. Rainfall seasonality substantially affects water resources, agriculture and livestock farming, even in years in which the total rainfall volume is high (Moura et al. 2019MOURA, M. S. B.; ESPÍNOLA SOBRINHO, J.; SILVA, T. G. F.; SOUZA, W. M. Aspectos meteorológicos do semiárido brasileiro. In: XIMENES, L. F.; SILVA, M. S. L.; BRITO, L. T. L. (org.). Tecnologias de convivência com o semiárido brasileiro. Fortaleza: Banco do Nordeste do Brasil, 2019. p. 85-104.).

As in other semiarid regions of the world, livestock farming, especially of goats and sheep, is the main activity in the rural area of the region, in which there are 7.2 million goat heads, 8.6 million sheep heads and 14.2 million cattle heads, i.e., 8.2, 87.4 and 62.5 % of the national herd, respectively (IBGE 2017INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA (IBGE). Censo agropecuário. 2017. Available at: https://sidra.ibge.gov.br/pesquisa/censo-agropecuario/censo-agropecuario-2017. Access on: Mar. 10, 2022.
https://sidra.ibge.gov.br/pesquisa/censo...
). Livestock is based on the grazing of Caatinga native pastures. During the rainy period, the Caatinga phytomass is diverse at all strata, normally decreasing in the drought period, when the animals graze cultivated forage such as buffel grass (Cenchrus ciliaris L.) (Rangel et al. 2020RANGEL, J. H. A.; MORAES, S. A.; TONUCCI, R.; AMARAL, A. J.; ZONTA, J. H.; SOUZA, S. F.; SANTOS, R. D.; MUNIZ, E. N.; PIOVEZAN, U. Sistemas de integração lavoura-pecuária-foresta: uma análise temporal de sua utilização no semiárido brasileiro. Revista Científica de Produção Animal, v. 22, n. 2, p. 81-89, 2020.). However, the expansion in agriculture and livestock in the Caatinga biome is frequently associated with land degradation (Silva et al. 2020SILVA, M. V.; PANDORFI, H.; LOPES, P. M. O.; SILVA, J. L. B.; ALMEIDA, G. L. P.; SILVA, D. A. O.; SANTOS, A.; RODRIGUES, J. A. M.; BATISTA, P. H. D.; JARDIM, A. M. R. F. Pilot monitoring of Caatinga spatial-temporal dynamics through the action of agriculture and livestock in the Brazilian semiarid. Remote Sensing Applications: Society and Environment, v. 19, e100353, 2020.).

The concentration of the main greenhouse gases (GHG) in the Earth atmosphere are currently on the order of 410 ppm of CO2, 1,866 ppb of CH4 and 332 ppb of N2O (IPCC 2021INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE (IPCC). Climate change 2021: the physical science basis. Cambridge: Cambridge University Press, 2021.). The Brazilian national GHG emissions are approximately 1,305 million tons of CO2-equivalent, and the agriculture and energy sectors are the main responsible for these emissions (34 and 32 %, respectively) (Brasil 2020BRASIL. Ministério da Ciência, Tecnologia, Inovações e Comunicações. Coordenação Geral do Clima. Estimativas anuais de emissões de gases de efeito estufa no Brasil. 5. ed. Brasília, DF: Ministério da Ciência, Tecnologia, Inovações e Comunicações, 2020.). In the Brazilian agriculture sector, most emissions come from livestock farming, particularly due to the enteric fermentation of ruminants (56.5 % of the national emissions) and agricultural soils (36 % of the national emissions) (Brasil 2020BRASIL. Ministério da Ciência, Tecnologia, Inovações e Comunicações. Coordenação Geral do Clima. Estimativas anuais de emissões de gases de efeito estufa no Brasil. 5. ed. Brasília, DF: Ministério da Ciência, Tecnologia, Inovações e Comunicações, 2020.). In global terms, livestock farming is estimated to contribute with approximately 20 % of the anthropic emissions of GHG (IPCC 2014INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE (IPCC). Climate change 2014: impacts, adaptation, and vulnerability. Cambridge: Cambridge University Press, 2014.).

Despite this, few representative studies have been conducted to evaluate the GHG emissions in the Brazilian semiarid and also in the Caatinga biome. Ribeiro et al. (2016)RIBEIRO, K.; SOUZA-NETO, E. R.; CARVALHO JUNIOR, J. A.; LIMA, J. R. S.; MENEZES, R. S. C.; DUARTE-NETO, J.; GUERRA, G. S.; OMETTO, J. P. H. B. Land cover changes and greenhouse gas emissions in two diferent soil covers in the Brazilian Caatinga. Science of the Total Environment, v. 571, n. 1, p. 1048-1057, 2016. evaluated CO2, CH4 and N2O fluxes from soils in areas of native Caatinga and cultivated pasture (Brachiaria ssp.), during the dry and rainy seasons of 2013 and 2014, and claimed that the GHG emissions in the Caatinga are lower than in other Brazilian biomes. However, this information needs to be supported by other studies, also considering the diversity existing within the semiarid environment. In addition, in the context of climate change, it is estimated that, in the future, regions around the world will face an increase in the number of consecutive days of drought (Marengo et al. 2009MARENGO, J. A.; JONES, R.; ALVES, L. M.; VALVERDE, M. C. Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system. International Journal of Climatology, v. 29, n. 15, p. 2241-2255, 2009.), what makes the data on agricultural production systems in semiarid regions strategic for the development of measures of coexistence with climate change for other regions. Moreover, realistic and relatively easy-to-adopt farming management practices, such as improved livestock care management and rotational grazing, are important tools to mitigate GHG emissions per product sold in semiarid farms (Nieto et al. 2018NIETO, M. I.; BARRANTES, O.; PRIVITELLO, L.; REINÉ, R. Greenhouse gas emissions from beef grazing systems in semiarid rangelands of central Argentina. Susteinability, v. 10, e4228, 2018.).

Thus, this study aimed to evaluate CO2, CH4 and N2O fluxes from soil and determine an annual baseline of soil GHG emissions in a reference site of silvopastoral production system in the Brazilian semiarid region, in order to provide subsidies for future studies on GHG emissions mitigation.

MATERIAL AND METHODS

The study was conducted at the Caatinga experimental field of the Embrapa Semiárido, in Petrolina, Pernambuco state, Brazil (09º03’S, 40º19’W and altitude of 389 m). The system is a silvopastoral reference site in the Caatinga and is called Caatinga-Bufel-Legumes (CBL). This system was developed by the Embrapa Semiárido and is widely disseminated in the semiarid region, with a potential to be used in 62 % of Brazilian semiarid areas (Rangel et al. 2020RANGEL, J. H. A.; MORAES, S. A.; TONUCCI, R.; AMARAL, A. J.; ZONTA, J. H.; SOUZA, S. F.; SANTOS, R. D.; MUNIZ, E. N.; PIOVEZAN, U. Sistemas de integração lavoura-pecuária-foresta: uma análise temporal de sua utilização no semiárido brasileiro. Revista Científica de Produção Animal, v. 22, n. 2, p. 81-89, 2020.).

The meat goat production system is conducted in a 155-ha area and is divided into cultivated buffel grass pasture (C. ciliaris L.) (35-ha) and grazed Caatinga (120-ha) (Figure 1). The buffel grass is 50+ years old non-fertilized pasture. The grazed Caatinga is composed of native vegetation, rich in forage plants, divided into four paddocks of approximately 30 ha each, which are used under rotational grazing. In the experimental field, there is also a 160-ha area of never grazed, preserved Caatinga, which was evaluated as a reference site. In this silvopastoral system, during the dry season, the animals receive roughage and concentrate supplementation and graze on the buffel grass pasture. During the rainy season, they graze in the Caatinga area. Mineral supplementation occurs both in the rainy and dry seasons. A comprehensive list of Caatinga species is provided by Fernandes et al. (2020)FERNANDES, M. F.; CARDOSO, D.; QUEIROZ, L. P. An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism. Journal of Arid Environments, v. 174, e104079, 2020.. This biome is characterized by negative water balance, rainfalls lower than 800 mm concentrated from December to April, average insolation of 2,800 h year-1, average annual temperatures between 23 and 27 ºC, relative air humidity of approximately 50 % and evaporation rate of approximately 2,000 mm year-1 (Moura et al. 2019MOURA, M. S. B.; ESPÍNOLA SOBRINHO, J.; SILVA, T. G. F.; SOUZA, W. M. Aspectos meteorológicos do semiárido brasileiro. In: XIMENES, L. F.; SILVA, M. S. L.; BRITO, L. T. L. (org.). Tecnologias de convivência com o semiárido brasileiro. Fortaleza: Banco do Nordeste do Brasil, 2019. p. 85-104.).

Figure 1
Experimental sites with native Caatinga, grazed Caatinga and buffel grass pasture (Petrolina, Pernambuco state, Brazil).

The soil in the experimental field is Argissolo Vermelho-Amarelo (Santos et al. 2018SANTOS, H. G. dos; JACOMINE, P. K. T.; ANJOS, L. H. C. dos; OLIVEIRA, V. A. de; LUMBRERAS, J. F.; COELHO, M. R.; ALMEIDA, J. A. de; ARAUJO FILHO, J. C. de; OLIVEIRA, J. B. de; CUNHA, T. J. F. Sistema brasileiro de classificação de solos. 5. ed. Brasília, DF: Embrapa, 2018.) or Ultisol (USDA 2014UNITED STATES DEPARTMENT OF AGRICULTURE (USDA). Soil Survey Staf. Keys to soil taxonomy. 12. ed. Washington, DC: USDA-Natural Resources Conservation Service, 2014.). For the buffel grass pasture, the soil chemical and physical attributes are presented in Table 1.

Table 1
Soil attributes in native Caatinga, grazed Caatinga and buffel grass, in a Ultisol in the Brazilian semiarid.

The average temperature and rainfall in Petrolina (1981-2010) are 26.9 ºC and 482.6 mm, respectively, with rainfall concentrating from November to April (Brasil 2018BRASIL. Instituto Nacional de Meteorologia. Normais climatológicas do Brasil 1981-2010. 2018. Available at: https://portal.inmet.gov.br/normais. Access on: Mar. 01, 2022.
https://portal.inmet.gov.br/normais...
). The region’s climate is BSwh’, according to the Köppen classification, which characterizes a hot semiarid region. Climatic conditions during the experimental period are shown in Figure 2.

Figure 2
Monthly rainfall and maximum, average and minimum air temperature at a Caatinga experimental field in Petrolina (Pernambuco state, Brazil), during evaluations between February 2015 and February 2016.

The evaluations of GHG (CO2, CH4 and N2O) emitted by the soil were conducted from February 2015 to February 2016, in the three areas (buffel grass, grazed Caatinga and native Caatinga). The gases were collected using static chambers, consisting of two parts: a base and a lid (Rochette & Eriksen-Hamel 2008ROCHETTE, P.; ERIKSEN-HAMEL, N. S. Chamber measurements of soil nitrous oxide flux: are absolute values reliable? Soil Science Society of America Journal, v. 72, n. 2, p. 331-342, 2008.). Rectangular galvanized-steel bases (60 cm long x 40 cm wide) and galvanized-steel lids shaped as a frustum of a rectangular pyramid were used, with a total volume of 74 L, covered by aluminized polyethylene foam insulation (2-mm thick). Each chamber has one hole on its upper end to collect the gas samples and another to attach a digital thermometer. Four bases were installed in each area and maintained at the same site until the end of the evaluation period. At one week before the first gas collection, the bases were installed in the soil, at a depth of 0.05 m, and the lid was ftted onto the base during the collections only.

The GHG samples were collected monthly during the dry season and weekly during the wet season. During the collection, the lid was ftted onto the base and the gas samples were collected at four times: closure of the chamber (time zero) and at 10, 20 and 40 min after the chamber was closed. The samples were collected in 25-mL polypropylene syringes and transferred to glass vials closed with a rubber septum, manually sealed and previously evacuated (-80 KPa). The gas collections were always carried out in the morning (Alves et al. 2012ALVES, B. J. R.; SMITH, K. A.; FLORES, R. A.; CARDOSO, A. S.; OLIVEIRA, W. R. D.; JANTALIA, C. P.; URQUIAGA, S.; BODDEY, R. M. Selection of the most suitable sampling time for static chambers for the estimation of daily mean N2O flux from soils. Soil Biology and Biochemistry, v. 46, n. 1, p. 129-135, 2012.), and the lids were removed from the bases which were kept open until the next collection.

The samples were sent to the laboratory to determine the concentrations of CO2, CH4 and N2O by gas chromatography. The equipment used is an Agilent 7890A gas chromatograph, with injection oven working at 60 ºC. A FID detector (120 ºC) was used to determine the CO2 and CH4 concentrations in the gases samples and a µECD detector (300 ºC) was used to determine the concentrations of N2O. The calibration curve was done with four certified standard gases of known concentration (standard 1: 250 ppb N2O, 0.5 ppm CH4, 250 ppm CO2; standard 2: 500 ppb N2O, 1 ppm CH4, 500 ppm CO2; standard 3: 1,000 ppb N2O, 3 ppm CH4, 1,000 ppm CO2; standard 4: 2,000 ppb N2O, 5 ppm CH4, 2,000 ppm CO2).

For each day of evaluation, the CO2, CH4 and N2O concentrations in the samples were used to calculate the fluxes of these three gases in each chamber, using the following equation: F(µg N2O-N/CO2-C/CH4-C m-2 h-1) = (ΔC/Δt).(m/Vm).V/A, where, ΔC/Δt is the variation rate of the gas inside the chamber at a certain time (ppm h-1); m the molecular mass of each gas (g); Vm the molecular volume of the gas (1 mol occupies 22.4 L under normal conditions of temperature and pressure); V the chamber volume (L); and A the chamber area (m2). The molecular volume of the gases was corrected according to the temperature inside the chamber during the sampling, by multiplying 22.4 by (273 + T /273), where T is the average temperature inside the chamber (ºC) during the sampling. During all collections, the temperature was measured in the soil, in the air inside the chamber and in the air outside the chamber, using digital thermometers.

The GHG fluxes were tabulated onto a spreadsheet. As the studied areas do not constitute an experiment, but an observational study, with four replications within each of the three areas under evaluation, parametric statistics are not an adequate tool for our data analysis. Therefore, the results are presented with their descriptive statistics, with mean and standard error of the mean. The cumulative emissions along the evaluation period were calculated by mathematical integration of daily fluxes (Signor et al. 2013SIGNOR, D.; CERRI, C. E. P. Nitrous oxide in agricultural soils: a review. Pesquisa Agropecuária Tropical, v. 43, n. 3, p. 322-338, 2013.). Cumulative emissions of CH4 and N2O along the experimental period were converted to the CO2-equivalent unit and summed to CO2 accumulated emissions to estimate the total emissions of GHG in each of the three areas.

RESULTS AND DISCUSSION

The CO2 fluxes varied from -19.98 to 179.12 mg m-2 h-1 of CO2-C and were diferent (means ± standard error) among the areas only on January 26, 2016 (Figure 3). In all areas, the highest CO2 fluxes were observed in January and February, reffecting the increase in soil respiration due to the occurrence of rainfall events in the region (Figure 3).

Figure 3
CO2, CH4 and N2O fluxes (lines) and rainfall events (bars) in native Caatinga, grazed Caatinga and buffel grass in the Brazilian semiarid. For each gas, bars represent the standard error of the means (n = 4).

The CH4 fluxes varied from -76.21 to 113.87 µg m-2 h-1 of CH4-C (Figure 3). Diferences between the evaluated areas were observed on April 7 and May 27 (2015) and February 11 (2016). The native Caatinga often showed higher CH4 fluxes than other areas. The lowest CH4 fluxes were observed in the grazed Caatinga in February 2016, whereas, in the native Caatinga and buffel grass pasture, the lowest fluxes of this gas occurred in the driest months of the period (Figure 3).

The highest CO2 fluxes and the lowest CH4 fluxes associated with the highest rainfall events observed in this study suggest that, in this region, the soil moisture is the main limiting factor for decomposition, in agreement with Sharkhuu et al. (2016)SHARKHUU, A.; PLANTE, A. F.; ENKHMANDAL, O.; GONNEAU, C.; CASPER, B. B.; BOLDGIV, B.; PETRAITIS, S. Soil and ecosystem respiration responses to grazing, watering and experimental warming chamber treatments across topographical gradients in northern Mongolia. Geoderma, v. 269, n. 1, p. 91-98, 2016.. After the rainfall events, since the soil is well-drained, the decomposition of carbon compounds occurs through aerobic pathway with emission mainly of CO2. Brito et al. (2015)BRITO, L. F.; AZENHA, M. V.; JANUSCKIEWICZ, E. R.; CARDOSO, A. S.; MORGADO, E. S.; MALHEIROS, E. B.; LA SCALA JUNIOR, N.; REIS, R. A.; RUGGIERI, A. C. Seasonal fuctuation of soil carbon dioxide emission in diferently managed pastures. Agronomy Journal, v. 107, n. 3, p. 957-962, 2015. evaluated soil CO2 emissions in pastures and also observed higher emissions in the rainy and hot summers, when compared to the dry and cold winters, and those higher emissions were directly related to variations in the rainfall and soil temperature. According to these authors, during a rainy summer, precipitation events increase the soil moisture, enhancing the root respiration and microbial processes involved in the decay of soil labile organic matter, what favors the CO2 production and emission.

A similarity for CO2 fluxes among the studied areas, as well as the highest fluxes in the rainy season, as reported by Brito et al. (2015)BRITO, L. F.; AZENHA, M. V.; JANUSCKIEWICZ, E. R.; CARDOSO, A. S.; MORGADO, E. S.; MALHEIROS, E. B.; LA SCALA JUNIOR, N.; REIS, R. A.; RUGGIERI, A. C. Seasonal fuctuation of soil carbon dioxide emission in diferently managed pastures. Agronomy Journal, v. 107, n. 3, p. 957-962, 2015., were also observed by Ribeiro et al. (2016)RIBEIRO, K.; SOUZA-NETO, E. R.; CARVALHO JUNIOR, J. A.; LIMA, J. R. S.; MENEZES, R. S. C.; DUARTE-NETO, J.; GUERRA, G. S.; OMETTO, J. P. H. B. Land cover changes and greenhouse gas emissions in two diferent soil covers in the Brazilian Caatinga. Science of the Total Environment, v. 571, n. 1, p. 1048-1057, 2016., when comparing another site of native Caatinga with a brachiaria grazed field. Lima et al. (2020)LIMA, J. R. S.; SOUZA, R. M. S.; SANTOS, E. S.; SOUZA, E. S.; OLIVEIRA, J. E. S.; MEDEIROS, E. V.; PESSOA, L. G. M.; ANTONINO, A. C. D.; HAMMECKER, C. Impacts of land use changes on soil respiration in the semiarid region of Brazil. Revista Brasileira de Ciência do Solo, v. 44, e0200092, 2020. studied a native Caatinga and a degraded pasture in a Luvisol in the Pernambuco state and also reported a seasonal variation in the soil CO2 emissions, with higher emissions in the wet season. However, these authors observed higher soil respiration rates in the Caatinga than in degraded pasture, due to the higher soil carbon content and lower soil temperature in the native area. Grazing is frequently associated with increased soil CO2 emissions, because it stimulates the root development and microbial activity in the rhizosphere, increasing the soil respiration, as observed by Sharkhuu et al. (2016)SHARKHUU, A.; PLANTE, A. F.; ENKHMANDAL, O.; GONNEAU, C.; CASPER, B. B.; BOLDGIV, B.; PETRAITIS, S. Soil and ecosystem respiration responses to grazing, watering and experimental warming chamber treatments across topographical gradients in northern Mongolia. Geoderma, v. 269, n. 1, p. 91-98, 2016. in the semiarid region of Mongolia. The exclusion of grazing reduces the soil respiration mainly due to the increase of moisture and reduction of soil temperature (Chen et al. 2016CHEN, J.; ZHOU, X.; WANG, J.; HRUSKA, T.; SHI, W.; CAO, J.; ZHANG, B.; XU, G.; CHEN, Y.; LUO, Y. Grazing exclusion reduced soil respiration but increased its temperature sensitivity in a meadow grassland on the Tibetan plateau. Ecology and Evolution, v. 6, n. 3, p. 675-687, 2016.).

The CH4 formation in soils occurs mainly under anaerobic conditions, when organic matter is anaerobically digested by methanogenic microorganisms, and, in the presence of oxygen, it is directly decomposed to CO2 by methanotrofic microorganisms (Le Mer & Roger 2001LE MER, J.; ROGER, P. Production, oxidation, emission and consumption of methane by soils: a review. European Journal of Soil Biology, v. 37, n. 1, p. 25-50, 2001.). Factors such as soil moisture, soil and air temperatures, besides factors related to the management system and carbon availability in the soil, affect the soil CH4 production (Wu et al. 2010WU, X.; YAO, Z.; BRÜGGEMANN, N.; SHEN, Z. Y.; WOLF, B.; DANNENMANN, M.; ZHENG, X.; BUTTERBACH-BAHL, K. Effects of soil moisture and temperature on CO2 and CH4 soil-atmosphere exchange of various land use/cover types in a semiarid grassland in inner Mongolia, China. Soil Biology and Biochemistry, v. 42, n. 5, p. 773-787, 2010.). Despite the observed CO2 fluxes were higher than the CH4 fluxes, some positive CH4 fluxes from the soil in native Caatinga occurred in the present study (Figure 3). This may, at first, seems strange in a semiarid environment, where the soil remains under aerobic conditions most of the time. In native Caatinga areas, almost all the aboveground biomass material produced by plants during the rainy season is added to the soil as litter, i.e., it is not consumed by animals, as in the grazed Caatinga and buffel grass pasture areas. In both these grazed sites, part of the grazed material returns to the soil as urine or feces, although a significant amount of waste is deposited outside the grazing area, in the pen where the animals stay in the late afternoon and at night. Thus, the amount of organic material supplied to the soil every year in the native Caatinga is much larger than in those grazed areas. The peak litterfall in the Caatinga happens at the end of the rainy season and beginning of the dry season, and the litter production falls between 1,500 and 3,000 kg ha-1 year-1, on a dry matter basis (Lima et al. 2015LIMA, R. P.; FERNANDES, M. M.; FERNANDES, M. R. M.; MATRICARDI, E. A. T. Aporte e decomposição da serapilheira na Caatinga no sul do Piauí. Floresta e Ambiente, v. 22, n. 1, p. 42-49, 2015., Holanda et al. 2017HOLANDA, A.; LÍCIA, A.; FREIRE, F.; SOUSA, F.; RAMOS, S.; ALVES, A. Aporte de serapilheira e nutrientes em uma área de Caatinga. Ciência Florestal, v. 27, n. 2, p. 621-633, 2017.). These residues are accumulated on the soil surface and are slowly decomposed throughout the dry season, because water is the main limiting factor for this process in this environment, reducing the microbial population and thus the soil organic matter decomposition (Lima et al. 2020LIMA, J. R. S.; SOUZA, R. M. S.; SANTOS, E. S.; SOUZA, E. S.; OLIVEIRA, J. E. S.; MEDEIROS, E. V.; PESSOA, L. G. M.; ANTONINO, A. C. D.; HAMMECKER, C. Impacts of land use changes on soil respiration in the semiarid region of Brazil. Revista Brasileira de Ciência do Solo, v. 44, e0200092, 2020.). In the next rainy season, plant residues from the litter present in the native Caatinga, mainly composed of leaves (76.5 %, according to Lima et al. 2015LIMA, R. P.; FERNANDES, M. M.; FERNANDES, M. R. M.; MATRICARDI, E. A. T. Aporte e decomposição da serapilheira na Caatinga no sul do Piauí. Floresta e Ambiente, v. 22, n. 1, p. 42-49, 2015.), are readily decomposed by soil microorganisms, leading to the formation of many anaerobic sites in the soil. Under anaerobic conditions, carbon may be used as an electron acceptor, leading to the formation of CH4, what may explain the highest fluxes in the native Caatinga in some periods of the year, once in the grazed Caatinga and buffel grass pasture areas the availability of residues on the soil would be lower precisely because of the material removal by grazing.

Assouma et al. (2017)ASSOUMA, M. H.; SERÇA, D.; GUÉRIN, F.; BLANFORT, V.; LECOMTE, P.; TOURÉ, I.; ICKOWICKZ, A.; MANLAY, R. J.; BERNOUX, M.; VAYSSIÈRES, J. Livestock induces strong spatial heterogeneity of soil CO2, N2O and CH4 emissions within a semiarid sylvo-pastoral landscape in west Africa. Journal of Arid Land, v. 9, n. 2, p. 210-221, 2017., studying soil GHG emissions in a silvopastoral system in Ferlo, Senegal, also observed the occurrence of positive CH4 fluxes in grazed native area. The edaphoclimatic characteristics and rainfall distribution in the region of Ferlo are similar to those observed in the present study. In that study, the CH4 fluxes in the grazed native area were equivalent to 0.45 ± 0.3 mg m-2 day-1 of CH4-C, and the average flux of this gas in all areas comprising the silvopastoral system was 3.56 µg m-2 h-1 of CH4-C. Converting to the same unit, the fluxes observed in the present study were 0.09 mg m-2 day-1 of CH4-C, i.e., 43 % lower than that observed by Assouma et al. (2017)ASSOUMA, M. H.; SERÇA, D.; GUÉRIN, F.; BLANFORT, V.; LECOMTE, P.; TOURÉ, I.; ICKOWICKZ, A.; MANLAY, R. J.; BERNOUX, M.; VAYSSIÈRES, J. Livestock induces strong spatial heterogeneity of soil CO2, N2O and CH4 emissions within a semiarid sylvo-pastoral landscape in west Africa. Journal of Arid Land, v. 9, n. 2, p. 210-221, 2017. under similar edaphoclimatic conditions.

During the studied period, the N2O fluxes varied from -1,043.12 to 471.37 µg m-2 h-1 of N2O-N (Figure 3), and differences were observed among the areas after September 2016. In the dry season, the grazed Caatinga showed the lowest N2O fluxes, while, in the wet season, the grazed Caatinga presented the highest and positive N2O fluxes, while the other areas presented negative fluxes (Figure 2). The N2O fluxes were similar along the evaluation period for the native Caatinga and buffel grass pasture. Differences among the sampling dates occurred only in grazed Caatinga, with the lowest fluxes between September and December 2015 and the highest fluxes between January and February 2016, months with the largest volumes of cumulative rainfall during the studied period (Figure 2). In drylands, N2O fluxes are generally constant in the dry season and significantly increase with rainfall or irrigation events, and this pulse in N2O fluxes in a short period of the year may account for the majority of the N2O emissions of the year, making the drylands N2O emissions unique (Hu et al. 2017HU, H.; TRIVEDI, P.; HE, J.; SINGH, B. K. Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation. Environmental Microbiology, v. 19, n. 12, p. 4808-4828, 2017.).

N2O is formed in the soil mainly by the anaerobic biological process of denitrification, and, even in aerated soils, there are always some anaerobic sites where N2O may be produced (Signor & Cerri 2013SIGNOR, D.; CERRI, C. E. P.; CONANT, R. N2O emissions due to nitrogen fertilizer applications in two regions of sugarcane cultivation in Brazil. Environmental Research Letters, v. 8, e015013, 2013.). In dryland ecosystems, these biological processes are subjected to specific climatic conditions, such as scarcity of water and nutrients during the dry season and a pulse of water and nutrients in the wet season following rainfall, which may selectively favor some specific microbial groups like fungi (Hu et al. 2017HU, H.; TRIVEDI, P.; HE, J.; SINGH, B. K. Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation. Environmental Microbiology, v. 19, n. 12, p. 4808-4828, 2017.). There are some evidences that fungal denitrification may be a key mediator of N2O emissions during the dry seasons in drylands, while classic heterotrophic bacterial denitrification in anaerobic microsites is the main N2O source during the wet seasons (Hu et al. 2017HU, H.; TRIVEDI, P.; HE, J.; SINGH, B. K. Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation. Environmental Microbiology, v. 19, n. 12, p. 4808-4828, 2017.). Moreover, according to these authors, the nitrification process (the ammonia oxidation pathway and nitrifer denitrification pathway) is also an important source of N2O emissions in drylands.

Despite the episodes of rains, the N2O fluxes remained negative in the buffel grass pasture and native Caatinga in January and February 2016. Ribeiro et al. (2016)RIBEIRO, K.; SOUZA-NETO, E. R.; CARVALHO JUNIOR, J. A.; LIMA, J. R. S.; MENEZES, R. S. C.; DUARTE-NETO, J.; GUERRA, G. S.; OMETTO, J. P. H. B. Land cover changes and greenhouse gas emissions in two diferent soil covers in the Brazilian Caatinga. Science of the Total Environment, v. 571, n. 1, p. 1048-1057, 2016. also observed that N2O fluxes are similar between areas and negative or close to zero in native Caatinga and in brachiaria cultivated pasture during the rainy season, a fact that they associated to the low N content in the soil in both areas, what is consistent with the results of the present study.

Soil can consume or emit N2O to the atmosphere, and this consumption depends on its potential to reduce N2O to N2, difusion of N2O inside the soil profle and its capacity of dissolution in water within the soil (Chapuis-Lardy et al. 2007CHAPUIS-LARDY, L.; WRAGE, N.; METAY, A.; CHOTTE, J.; BERNOUX, M. Soils, a sink for N2O?: a review. Global Change Biology, v. 13, n. 1, p. 1-17, 2007.). The negative N2O fluxes observed in the present study, and also reported by Ribeiro et al. (2016)RIBEIRO, K.; SOUZA-NETO, E. R.; CARVALHO JUNIOR, J. A.; LIMA, J. R. S.; MENEZES, R. S. C.; DUARTE-NETO, J.; GUERRA, G. S.; OMETTO, J. P. H. B. Land cover changes and greenhouse gas emissions in two diferent soil covers in the Brazilian Caatinga. Science of the Total Environment, v. 571, n. 1, p. 1048-1057, 2016., even when rainfall events occurred in the Caatinga biome, may be related to the fast increase in the microbial activity due to the increment in soil moisture, because water is the main limiting factor for decomposition in semiarid regions (Sharkhuu et al. 2016SHARKHUU, A.; PLANTE, A. F.; ENKHMANDAL, O.; GONNEAU, C.; CASPER, B. B.; BOLDGIV, B.; PETRAITIS, S. Soil and ecosystem respiration responses to grazing, watering and experimental warming chamber treatments across topographical gradients in northern Mongolia. Geoderma, v. 269, n. 1, p. 91-98, 2016.). This intense microbial activity consumes CO2 and promotes the formation of some anaerobic sites in the soil, where the complete process of denitrification is favored and leads to higher emissions of N2 than N2O. Moreover, C/N and C/P ratios of Caatinga litter (33 and 431, respectively) are higher and may explain the low litter decomposition rates and the N immobilization in the soil during decomposition in this biome (Souto et al. 2009SOUTO, C.; SOUTO, J. S.; SANDOS, R. V.; BAKKE, I. A. Características químicas da serapilheira depositada em área de Caatinga. Revista Caatinga, v. 22, n. 1, p. 264-272, 2009.), what is another possibility to explain the small N2O fluxes in the Caatinga.

Moreover, in February 2016, negative CH4 fluxes and positive N2O fluxes were observed in the grazed Caatinga (Figure 2). Similar results were reported by Pan et al. (2021)PAN, H.; FENG, H.; LIU, Y.; LAI, C.; ZHUGE, Y.; ZHANG, Q.; TANG, C.; DI, H.; ZHONGJUN, J.; GUBRY-RANGIN, C.; LI, Y.; XU, J. Grazing weakens competitive interactions between active methanotrophs and nitrifers modulating greenhouse-gas emissions in grassland soils. ISME Communications, v. 1, e74, 2021., in a grazed site in Mongolia. According to Le Mer & Roger (2001)LE MER, J.; ROGER, P. Production, oxidation, emission and consumption of methane by soils: a review. European Journal of Soil Biology, v. 37, n. 1, p. 25-50, 2001., the methane consumption in the soil occurs through methanotrophic microorganisms, and it also significantly contributes to nitrification in the rhizosphere.

Therefore, the results of the present study suggest that soil moisture is the main factor limiting the GHG emissions in the Brazilian semiarid region. Thus, when rainfalls occur, under favorable moisture conditions, the residue decomposition by soil microorganisms occurs very intensely, and compounds containing C are decomposed through the aerobic pathway, emitting CO2 to the atmosphere. This CO2 fast production consumes soil O2, leading to the formation of anaerobic sites, which, with moisture still favorable to microbial reactions, allow the formation of CH4 and complete denitrification (higher emission of N2 to the detriment of N2O), even in the well-drained soil of the studied area.

The total CO2 emissions during the evaluated period were similar in all areas, while the native Caatinga showed the highest CH4 and N2O emissions (Table 2). In the present study, similar CO2 fluxes between the uses in most parts of the year and the increase in the fluxes due to the occurrence of rainfall (Figure 3), as well as the total similar emissions among the areas (Table 2), confirm that, in this region, the soil moisture is more important for soil respiration than the amount of material available for decomposition. This was also reported by Lima et al. (2020)LIMA, J. R. S.; SOUZA, R. M. S.; SANTOS, E. S.; SOUZA, E. S.; OLIVEIRA, J. E. S.; MEDEIROS, E. V.; PESSOA, L. G. M.; ANTONINO, A. C. D.; HAMMECKER, C. Impacts of land use changes on soil respiration in the semiarid region of Brazil. Revista Brasileira de Ciência do Solo, v. 44, e0200092, 2020., who highlighted that the soil CO2 emissions in the Brazilian semiarid region are similar to those in other semiarid areas of the world and vary mainly due to soil organic carbon contents, soil temperature and soil moisture.

Table 2
Cumulative emissions of CO2, CH4 and N2O, between February 2015 and February 2016, in native Caatinga, grazed Caatinga and buffel grass pasture in the Brazilian semiarid.

For the total CH4 emissions, the difference between native Caatinga and the anthropized areas was equivalent to 210.22 mg m-2 of CH4-C. The total N2O emissions were 1,398.48 mg m-2 of N2O-N higher in the native Caatinga than in the grazed Caatinga, during the same time. In addition, the highest cumulative N2O emissions observed in the native Caatinga (Table 2) may indicate that the N2O emissions in this area are caused by formation processes diferent from those observed in grazed areas, as suggested by Hu et al. (2017)HU, H.; TRIVEDI, P.; HE, J.; SINGH, B. K. Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation. Environmental Microbiology, v. 19, n. 12, p. 4808-4828, 2017.. According to Lima et al. (2015)LIMA, R. P.; FERNANDES, M. M.; FERNANDES, M. R. M.; MATRICARDI, E. A. T. Aporte e decomposição da serapilheira na Caatinga no sul do Piauí. Floresta e Ambiente, v. 22, n. 1, p. 42-49, 2015., the litterfall in the Caatinga contributes with almost 93 kg ha-1 year-1 of N, which can be available to plants and soil microorganisms to be denitrified and emitted to the atmosphere as N2O or N2.

The total emissions converted to CO2-equivalent in the anthropized areas were lower than those observed in the native area (Table 3). The buffel grass pasture area emitted 65 % less GHG than the native area, while the grazed Caatinga showed a reduction of 741 % in the soil GHG emissions in this period. Even if considered together, the anthropized sites showed lower GHG emissions than the native area. However, for the interpretation of total emissions, it is important to take into account that GHG emissions from the soil are dependent on soil organic matter content, and that the higher total emissions in the native Caatinga may also be explained by its higher soil organic matter content (Table 1). Despite the fact that the soil bulk density was not measured and that it was not possible to calculate the soil C stocks in the evaluated areas, it was possible to compare the soil organic matter content in these areas. Then, the native Caatinga soil organic matter content is 1.68 times higher than for buffel grass pasture and 2.50 times higher than for grazed Caatinga soil.

Table 3
Cumulative emissions (CO2-equivalent) of CO2, CH4 and N2O, between February 2015 and February 2016, in native Caatinga, grazed Caatinga and buffel grass pasture in the Brazilian semiarid.

Therefore, the data of the present study suggest that the GHG soil emissions from grazed areas in the Caatinga biome are not higher than in the native Caatinga, what is an important indication of the environmental sustainability of the evaluated agrosilvopastoral system. However, the C balance of this silvopastoral system must also consider the C stocks in the soil and the enteric CH4 emissions by the goats in the area. These aspects were not addressed in the present study, but should be considered in the future. Additionally, it is very important to take into account the GHG emissions in the pen where the goats spend the night, which is an important point for future investigation and represents a diferential for the Caatinga goat production system, in comparison with other animal production systems practiced in other Brazilian regions, in which the animals usually feed and spend the night in the same paddock.

Finally, Caatinga is a large and very diverse biome, in terms of floristic composition and edaphoclimatic conditions, and, as highlighted by Silva et al. (2020)SILVA, M. V.; PANDORFI, H.; LOPES, P. M. O.; SILVA, J. L. B.; ALMEIDA, G. L. P.; SILVA, D. A. O.; SANTOS, A.; RODRIGUES, J. A. M.; BATISTA, P. H. D.; JARDIM, A. M. R. F. Pilot monitoring of Caatinga spatial-temporal dynamics through the action of agriculture and livestock in the Brazilian semiarid. Remote Sensing Applications: Society and Environment, v. 19, e100353, 2020., it presents low resilience in periods of severe droughts. This diversity should be considered in future studies on GHG emissions both in native areas and in agroecosystems, and also in the development of mitigation practices, which have to be observed in order to avoid land degradation and desertification.

CONCLUSIONS

  1. Rainfall events in the Caatinga biome are associated with higher CO2 fluxes, lower CH4 fluxes and increments in N2O fluxes, and are the main factor limiting greenhouse gases (GHG) emissions in the Brazilian semiarid region;

  2. CO2 emissions are similar among native Caatinga, grazed Caatinga and buffel grass. Rain increments the N2O fluxes, but not sufficiently to make them positive in anthropized areas. Negative CH4 emissions are also observed in soils of grazed areas;

  3. For the Caatinga, areas under grazing (grazed Caatinga and buffel grass pasture) show lower GHG fluxes, when compared to the native Caatinga, being an important indication of the environmental sustainability of the silvopastoral activities in this biome.

ACKNOWLEDGMENTS

The authors thank the Embrapa Semiárido, the Post-Graduation Program in Animal Science of the Universidade Federal do Vale do São Francisco and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes). This study was supported by the Empresa Brasileira de Pesquisa Agropecuária (Embrapa) (grant number 01.10.06.001.09.00).

REFERENCES

  • ALVES, B. J. R.; SMITH, K. A.; FLORES, R. A.; CARDOSO, A. S.; OLIVEIRA, W. R. D.; JANTALIA, C. P.; URQUIAGA, S.; BODDEY, R. M. Selection of the most suitable sampling time for static chambers for the estimation of daily mean N2O flux from soils. Soil Biology and Biochemistry, v. 46, n. 1, p. 129-135, 2012.
  • ASSAD, E. D.; BUAINAIN, A. M.; PINTO, H. S.; DUARTE, V. S.; SOUSA, M. R. de. Climate changes: challenges for Brazil. In: DHIRENDRA, K. V. (ed.). Climate change, sustainable development & human security Plymouth: Lexington Books, 2013. p. 169-199.
  • ASSOUMA, M. H.; SERÇA, D.; GUÉRIN, F.; BLANFORT, V.; LECOMTE, P.; TOURÉ, I.; ICKOWICKZ, A.; MANLAY, R. J.; BERNOUX, M.; VAYSSIÈRES, J. Livestock induces strong spatial heterogeneity of soil CO2, N2O and CH4 emissions within a semiarid sylvo-pastoral landscape in west Africa. Journal of Arid Land, v. 9, n. 2, p. 210-221, 2017.
  • BRASIL. Instituto Nacional de Meteorologia. Normais climatológicas do Brasil 1981-2010 2018. Available at: https://portal.inmet.gov.br/normais Access on: Mar. 01, 2022.
    » https://portal.inmet.gov.br/normais
  • BRASIL. Ministério da Ciência, Tecnologia, Inovações e Comunicações. Coordenação Geral do Clima. Estimativas anuais de emissões de gases de efeito estufa no Brasil 5. ed. Brasília, DF: Ministério da Ciência, Tecnologia, Inovações e Comunicações, 2020.
  • BRITO, L. F.; AZENHA, M. V.; JANUSCKIEWICZ, E. R.; CARDOSO, A. S.; MORGADO, E. S.; MALHEIROS, E. B.; LA SCALA JUNIOR, N.; REIS, R. A.; RUGGIERI, A. C. Seasonal fuctuation of soil carbon dioxide emission in diferently managed pastures. Agronomy Journal, v. 107, n. 3, p. 957-962, 2015.
  • CHAPUIS-LARDY, L.; WRAGE, N.; METAY, A.; CHOTTE, J.; BERNOUX, M. Soils, a sink for N2O?: a review. Global Change Biology, v. 13, n. 1, p. 1-17, 2007.
  • CHEN, J.; ZHOU, X.; WANG, J.; HRUSKA, T.; SHI, W.; CAO, J.; ZHANG, B.; XU, G.; CHEN, Y.; LUO, Y. Grazing exclusion reduced soil respiration but increased its temperature sensitivity in a meadow grassland on the Tibetan plateau. Ecology and Evolution, v. 6, n. 3, p. 675-687, 2016.
  • FERNANDES, M. F.; CARDOSO, D.; QUEIROZ, L. P. An updated plant checklist of the Brazilian Caatinga seasonally dry forests and woodlands reveals high species richness and endemism. Journal of Arid Environments, v. 174, e104079, 2020.
  • HOLANDA, A.; LÍCIA, A.; FREIRE, F.; SOUSA, F.; RAMOS, S.; ALVES, A. Aporte de serapilheira e nutrientes em uma área de Caatinga. Ciência Florestal, v. 27, n. 2, p. 621-633, 2017.
  • HU, H.; TRIVEDI, P.; HE, J.; SINGH, B. K. Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation. Environmental Microbiology, v. 19, n. 12, p. 4808-4828, 2017.
  • INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA (IBGE). Censo agropecuário 2017. Available at: https://sidra.ibge.gov.br/pesquisa/censo-agropecuario/censo-agropecuario-2017 Access on: Mar. 10, 2022.
    » https://sidra.ibge.gov.br/pesquisa/censo-agropecuario/censo-agropecuario-2017
  • INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE (IPCC). Climate change 2021: the physical science basis. Cambridge: Cambridge University Press, 2021.
  • INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE (IPCC). Climate change 2014: impacts, adaptation, and vulnerability. Cambridge: Cambridge University Press, 2014.
  • LE MER, J.; ROGER, P. Production, oxidation, emission and consumption of methane by soils: a review. European Journal of Soil Biology, v. 37, n. 1, p. 25-50, 2001.
  • LIMA, J. R. S.; SOUZA, R. M. S.; SANTOS, E. S.; SOUZA, E. S.; OLIVEIRA, J. E. S.; MEDEIROS, E. V.; PESSOA, L. G. M.; ANTONINO, A. C. D.; HAMMECKER, C. Impacts of land use changes on soil respiration in the semiarid region of Brazil. Revista Brasileira de Ciência do Solo, v. 44, e0200092, 2020.
  • LIMA, R. P.; FERNANDES, M. M.; FERNANDES, M. R. M.; MATRICARDI, E. A. T. Aporte e decomposição da serapilheira na Caatinga no sul do Piauí. Floresta e Ambiente, v. 22, n. 1, p. 42-49, 2015.
  • MARENGO, J. A.; JONES, R.; ALVES, L. M.; VALVERDE, M. C. Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system. International Journal of Climatology, v. 29, n. 15, p. 2241-2255, 2009.
  • MOURA, M. S. B.; ESPÍNOLA SOBRINHO, J.; SILVA, T. G. F.; SOUZA, W. M. Aspectos meteorológicos do semiárido brasileiro. In: XIMENES, L. F.; SILVA, M. S. L.; BRITO, L. T. L. (org.). Tecnologias de convivência com o semiárido brasileiro Fortaleza: Banco do Nordeste do Brasil, 2019. p. 85-104.
  • NIETO, M. I.; BARRANTES, O.; PRIVITELLO, L.; REINÉ, R. Greenhouse gas emissions from beef grazing systems in semiarid rangelands of central Argentina. Susteinability, v. 10, e4228, 2018.
  • PAN, H.; FENG, H.; LIU, Y.; LAI, C.; ZHUGE, Y.; ZHANG, Q.; TANG, C.; DI, H.; ZHONGJUN, J.; GUBRY-RANGIN, C.; LI, Y.; XU, J. Grazing weakens competitive interactions between active methanotrophs and nitrifers modulating greenhouse-gas emissions in grassland soils. ISME Communications, v. 1, e74, 2021.
  • RANGEL, J. H. A.; MORAES, S. A.; TONUCCI, R.; AMARAL, A. J.; ZONTA, J. H.; SOUZA, S. F.; SANTOS, R. D.; MUNIZ, E. N.; PIOVEZAN, U. Sistemas de integração lavoura-pecuária-foresta: uma análise temporal de sua utilização no semiárido brasileiro. Revista Científica de Produção Animal, v. 22, n. 2, p. 81-89, 2020.
  • RIBEIRO, K.; SOUZA-NETO, E. R.; CARVALHO JUNIOR, J. A.; LIMA, J. R. S.; MENEZES, R. S. C.; DUARTE-NETO, J.; GUERRA, G. S.; OMETTO, J. P. H. B. Land cover changes and greenhouse gas emissions in two diferent soil covers in the Brazilian Caatinga. Science of the Total Environment, v. 571, n. 1, p. 1048-1057, 2016.
  • ROCHETTE, P.; ERIKSEN-HAMEL, N. S. Chamber measurements of soil nitrous oxide flux: are absolute values reliable? Soil Science Society of America Journal, v. 72, n. 2, p. 331-342, 2008.
  • SANTOS, H. G. dos; JACOMINE, P. K. T.; ANJOS, L. H. C. dos; OLIVEIRA, V. A. de; LUMBRERAS, J. F.; COELHO, M. R.; ALMEIDA, J. A. de; ARAUJO FILHO, J. C. de; OLIVEIRA, J. B. de; CUNHA, T. J. F. Sistema brasileiro de classificação de solos 5. ed. Brasília, DF: Embrapa, 2018.
  • SHARKHUU, A.; PLANTE, A. F.; ENKHMANDAL, O.; GONNEAU, C.; CASPER, B. B.; BOLDGIV, B.; PETRAITIS, S. Soil and ecosystem respiration responses to grazing, watering and experimental warming chamber treatments across topographical gradients in northern Mongolia. Geoderma, v. 269, n. 1, p. 91-98, 2016.
  • SIGNOR, D.; CERRI, C. E. P. Nitrous oxide in agricultural soils: a review. Pesquisa Agropecuária Tropical, v. 43, n. 3, p. 322-338, 2013.
  • SIGNOR, D.; CERRI, C. E. P.; CONANT, R. N2O emissions due to nitrogen fertilizer applications in two regions of sugarcane cultivation in Brazil. Environmental Research Letters, v. 8, e015013, 2013.
  • SILVA, M. V.; PANDORFI, H.; LOPES, P. M. O.; SILVA, J. L. B.; ALMEIDA, G. L. P.; SILVA, D. A. O.; SANTOS, A.; RODRIGUES, J. A. M.; BATISTA, P. H. D.; JARDIM, A. M. R. F. Pilot monitoring of Caatinga spatial-temporal dynamics through the action of agriculture and livestock in the Brazilian semiarid. Remote Sensing Applications: Society and Environment, v. 19, e100353, 2020.
  • SOUTO, C.; SOUTO, J. S.; SANDOS, R. V.; BAKKE, I. A. Características químicas da serapilheira depositada em área de Caatinga. Revista Caatinga, v. 22, n. 1, p. 264-272, 2009.
  • UNITED STATES DEPARTMENT OF AGRICULTURE (USDA). Soil Survey Staf. Keys to soil taxonomy 12. ed. Washington, DC: USDA-Natural Resources Conservation Service, 2014.
  • WU, X.; YAO, Z.; BRÜGGEMANN, N.; SHEN, Z. Y.; WOLF, B.; DANNENMANN, M.; ZHENG, X.; BUTTERBACH-BAHL, K. Effects of soil moisture and temperature on CO2 and CH4 soil-atmosphere exchange of various land use/cover types in a semiarid grassland in inner Mongolia, China. Soil Biology and Biochemistry, v. 42, n. 5, p. 773-787, 2010.

Publication Dates

  • Publication in this collection
    30 Sept 2022
  • Date of issue
    2022

History

  • Received
    30 Mar 2022
  • Accepted
    01 Aug 2022
  • Published
    30 Aug 2022
Escola de Agronomia/UFG Caixa Postal 131 - Campus II, 74001-970 Goiânia-GO / Brasil, 55 62 3521-1552 - Goiânia - GO - Brazil
E-mail: revistapat.agro@ufg.br