SciELO - Scientific Electronic Library Online

vol.78 issue1Assessing climate change effects on gladiola in Southern BrazilAgronomic responses of grapevine ‘Chenin Blanc’ as a function of training systems and rootstocks author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand



  • text new page (beta)
  • English (pdf)
  • Article in xml format
  • How to cite this article
  • SciELO Analytics
  • Curriculum ScienTI
  • Automatic translation


Related links


Scientia Agricola

On-line version ISSN 1678-992X

Sci. agric. (Piracicaba, Braz.) vol.78 no.1 Piracicaba  2021  Epub Mar 13, 2020 


CH4 and N2O fluxes from planted forests and native Cerrado ecosystems in Brazil

Alexsandra Duarte de Oliveira1  *

Fabiana Piontekowski Ribeiro2

Eloisa Aparecida Belleza Ferreira1

Juaci Vitoria Malaquias1

Alcides Gatto2

Diana Regazzi Zuim1

Luciano de Almeida Pinheiro1

Karina Pulrolnik1

João Paulo Guimarães Soares1

Arminda Moreira de Carvalho1

1Embrapa Cerrados, BR 020, km 18, C.P. 08223 – 73310-970 – Planaltina, DF – Brasil.

2Universidade de Brasília – Depto. de Ciências Florestais, Campus Universitário Darcy Ribeiro – 70910-900 – Brasília, DF – Brasil.


Forest soils are N2O sources and commonly act as CH4 sinks. This study evaluated the dynamics of the CH4 and N2O fluxes of soils under Eucalyptus plantations and native Cerrado vegetation, as well as possible interactions between environmental factors and fluxes. The study was carried out in the Distrito Federal, Brazil, during 26 months, in three areas: in two stands of the hybrid Eucalyptus urophylla × Eucalyptus grandis, planted in 2011 (E1), and in 2009 (E2) and native Cerrado vegetation (CE). Measurements to determine the fluxes in a closed static chamber were carried out from Oct 2013 to Nov 2015. Soil and climate factors were monitored. During the study period, the mean CH4 fluxes were –22.48, –8.38 and –1.31 μg CH4 m–2 h–1 and the mean N2O fluxes 5.45, 4.85 and 3.85 μg N2O m–2 h–1 from E1, E2 and CE, respectively. Seasonality affected plantations in the studied sites. Cumulative CH4 influxes were calculated (year-1: –1.86 to -0.63 kg ha–1 yr–1; year-2: –1.85 to –1.34 kg ha–1 yr–1). Cumulative N2O fluxes in the three sites were ≤ 0.85 kg ha–1 yr–1. The change in land use from Cerrado to Eucalyptus plantations did not significantly changed regarding greenhouse gases (GHG), compared to the native vegetation. Flux rates of both gases (N2O and CH4) were low. Temporal variations in GHG fluxes and different ages of the stands did not cause significant differences in cumulative annual fluxes.

Key words: Eucalyptus; greenhouse gases; forest stand age; savanna


Changes in land use have led tropical soils to estimated emissions of 0.2 Gt C yr1, accounting for 10-30 % of total C emissions from deforestation ( Houghton, 1999 ; Achard et al., 2004 ). In 2010, GHG emissions were estimated at 49 × 109 Mg CO2eq, of which 21 to 24 % were generated by agriculture, forestry, and other land uses ( Tubiello et al., 2013 ; IPCC, 2014 ). In the context of a low-carbon economy, forest stands can be an option to reduce pressure on the native vegetation and mitigate the effects of climate change ( Bonan, 2008 ). In forest stands, Eucalyptus is the second most commonly planted genus, due to its high adaptability, fast growth, and economic value ( Iglesias-Trabado et al., 2009 ). Moreover, nutrients released in forest litter may enhance stabilization mechanisms of soil organic carbon (SOC) ( Huang et al., 2011 ).

Land-use changes alter chemical, physical, and biological properties of the soil, modifying the GHG fluxes ( Kim and Kirschbaum, 2015 ). In addition, forest type ( Masaka et al., 2014 ) and soil management practices play an important role ( Kim et al., 2016 ), as well as water-filled pore space ( Santos et al., 2016 ; Smith, 2017 ), soil O2 contents, pH, plants, and N input ( Hickman et al., 2015 ; Carvalho et al., 2017 ). Moreover, long-term N inputs may favor soil C stocks, mainly in litter with a high lignin content ( Grandy and Neff, 2008 ). Microbial communities can be altered by climate warming, N fertilization, pH and the C:N ratio ( Högberg et al., 2007 ; Lucas et al., 2007 ). In particular, metabolic responses of the microbial community to N enrichment are complex and highly variable ( Michel and Matzner, 2003 ).

Native forests and commercial Eucalyptus stands of different ages have been little studied about the potential emission or consumption of GHG, but they are main drives for GHG fluxes in the Cerrado region. This study investigated GHG emissions with a two-year GHG monitoring program in natural and planted forests. The objectives were: (a) evaluate CH4 and N2O fluxes of soils under planted Eucalyptus forests of different ages (established in 2009 and 2011) and managements, and under native Cerrado vegetation, (b) describe fluxes and their interactions with seasonality and environmental variables, and (c) determine cumulative N2O and CH4 fluxes in soils of Eucalyptus forests of different ages and in native Cerrado vegetation.

Materials and Methods

Description of the study site

The three studied sites were located in the central region of Brazil (Central Plateau) in Paranoá, Distrito Federal ( Figure 1 ). The native forest consisted of an area of 3.5 ha of native Cerrado vegetation (CE) (Latitude 15o53’45.51” S, Longitude 47o38’40.69” W; Altitude 930 m a.s.l.) and belonged to the phytophysiognomic formation “cerradão”, a woodland savanna with short semideciduous forest, 10 to 15 m tall, of medium density ( FAO, 2001 ).

Figure 1 – Location of the study site, rural center Quebrada dos Neres, Paranoá, Distrito Federal, Brazil. Source: IBGE (2009). 

The planted forest consisted of, respectively, 12 and 19 ha, each with a Eucalyptus urophylla × Eucalyptus grandis hybrid stand: E1- clone EAC 1528 (Latitude 15o53’06.44” S, Longitude 47o39’37.10” W; 948 m a.s.l.) and E2 - clone GG100 (Latitude 15o53’48.24” S, Longitude 47o38’37.22” W; 946 m a.s.l.).

Tree seedlings were planted in E1 in Dec 2011, at 3.5 m × 1.7 m spacing in a site previously covered with native Cerrado vegetation. Soil tillage consisted of disking and subsoiling in the planting row to a depth of 1.2 m.

The tree seedlings in E2 were planted in Dec 2009 (3.5 m × 1.7 m). The site had previously been used for cropping soybean (2003 to 2005), sorghum (2006), and soybean again (2007-2009). Soil tillage consisted of heavy disk harrowing (width 1.5 m) and opening furrows in the center of the row to a depth of 25 cm.

In the Eucalyptus plantations (E1 and E2), soil acidity was corrected by incorporating dolomitic limestone (2.5 t ha1) to a depth of 20 cm and with 700 kg ha1agricultural gypsum applied on the soil surface two months later. Fertilization at planting consisted of NPK (5-25-15), corresponding to 16.52 kg N ha1. After one year, a side dressing of 60 kg K2O ha1 was applied in the form of potassium chloride, 50 kg N ha1 in the form of urea, and 1 g boron per plant in the form of borax. In Jan 2014, the application of 60 kg K2O ha1 was repeated.

The soil of the experimental site was classified as clayey Oxisol (Typic Haplustox) ( Soil Survey Staff, 2006 ). The soil chemical properties and density (0-5 and 5-10 cm depth) are listed in Table 1 . Table 2 shows the litter quality in E1, E2 and CE. The C:N ratio in the litter ranged from 66:1 to 75:1 and the lignin content, from 99.5 to 162.0

Table 1 – Soil chemical properties in two layers (0-5 and 5-10 cm) in Eucalyptus stands (E1, clone EAC 1528 planted in 2011 and E2, clone GG100 planted in 2009); and CE (native Cerrado vegetation), Distrito Federal, Brazil. 

Variables E1 E2 CE E1 E2 CE
Property Unit of measurement Soil depth 0-5 cm Soil depth 5-10 cm
Organic matter dag kg–1 3.3 3.0 3.8 2.9 2.6 3.2
pH (H2O) 5.0 5.4 5.1 4.9 5.3 5.1
P* mg dm–3 1.5 5.3 1.8 1.4 3.5 1.2
H+Al mg dm–3 8.2 7.0 9.5 8.3 7.1 8.6
SB mg dm–3 1.8 4.3 1.3 1.6 2.6 0.8
CEC mg dm–3 10.0 11.3 10.8 9.8 9.7 9.5
V % 17.7 38.0 11.8 15.8 26.7 8.7
B mg kg–1 0.5 1.1 0.5 0.5 0.9 0.5
Zn mg L–1 0.3 0.6 0.6 0.3 1.3 0.4
Soil density g cm–3 0.98 0.96 0.97 0.99 0.96 0.98

P* = phosphor Mehlich-1; H+Al = potential acidity; SB = sum of bases; CEC = cationic exchange capacity; V = base saturation; B = boron; Zn = zinc.

Table 2 – Litter quality in Eucalyptus stands (E1, clone EAC 1528 planted in 2011 and E2, clone GG100 planted in 2009); and CE (native Cerrado vegetation), Distrito Federal, Brazil. 

Area Ls K C N L C:N
Mg ha–1 ------------------------- g kg–1 --------------------------
E1 10.8 0.0012 463.4 6.15 99.5 75:1
E2 13.7 0.0009 465.7 7.04 114.6 66:1
CE 7.6 0.0021 460.0 6.53 162.0 70:1

Ls = litter stock; K = decomposition constant; C = carbon; N = nitrogen L = lignin.

The regional climate is Aw (rainy tropical), according to Köppen-Geiger classification ( Cardoso et al., 2014 ), with two well-defined seasons: dry season (May–Sept) and rainy season (Oct–Apr). The mean annual precipitation observed in the last 40 years was 1345.8 mm ( Silva et al., 2017b ). The precipitation in year-1 and year-2 was 1210.9 and 1305.6 mm, respectively, and > 94 % of the rain was concentrated in the rainy season. The average air temperature was 21.4 and 22.2 °C in year 1 and 2, respectively ( Figure 2 ).

Figure 2 – Precipitation (mm) and air temperature (ºC) from Oct 2013 to Nov 2015, Paranoá, Distrito Federal, Brazil. 

Measurements of CH4 and N2O fluxes

The CH4 and N2O fluxes were measured from Oct 2013 to Nov 2015, distinguished in year-1 (Oct 2013 to Sept 2014) and year-2 (Oct 2014 to Nov 2015). The years were analyzed separately to identify the behavior of GHG fluxes and contributions of the soil-climate variables.

The closed-chamber method was used for measurements ( Alves et al., 2012 ), with a sampling frequency of three times per month ( Zanatta et al., 2014 ), since the sites with fully established Eucalyptus trees were not fertilized with synthetic N. Three 30 m × 30 m plots were randomly delimited in each site. To ensure representativeness of the system, four closed chambers were installed per plot, two in the Eucalyptus rows and two in-between rows, spaced 10 m. The chambers in the rows did not receive N fertilization after the first experimental year. In CE, four static gas chambers were placed randomly in each plot, resulting in 36 chambers installed in the sites. Each closed chamber consisted of a metal base (0.38 m × 0.58 m) inserted into the soil, and an upper part of PVC (height 9.5 cm), coated with a thermal aluminum blanket, which, together with the metal base, sealed the space covered by the chamber, where the gases accumulated for later collection and determination.

A hole was drilled in the center of the top part of each chamber and connected to a rubber hose and a three-way valve, by which the gas outlet could be controlled at sampling. Digital thermometers were installed to monitor the air temperature within the chambers.

The soil temperature was measured at 5 cm deep with a digital thermometer at the sampling times. The gas samples were captured between 09h00 a.m. and 11h00 a.m., following the recommendation of Alves et al. (2012) , to best represent the daily average flux. The air trapped in the chambers was sampled at 0, 15, and 30 min after closing the device. A 60-mL polypropylene syringe was used, coupled with a three-way valve, in which 30 mL gas samples were collected and transferred to vials. In addition, one sample of atmospheric gas per plot was taken as reference to analyze gas samples. Before and after sampling, the vials were transported in ice-cooled thermal boxes and stored in a refrigerated environment at 16 ºC for measurements.

The CH4 and N2O concentrations were determined with a gas chromatograph (Trace 1310 GC ultra) equipped with a Porapak Q column at 65 °C, an electron capture detector (ECD) and a flame ionization detector (FID). The following standards were used: 200, 600, 1000 and 1500 ppb N2O; and 1000, 5000, 10000 and 50000 ppb CH4. The calculated detection limit was 51 ppb for N2O and 145 ppb for CH4 and the calculated quantification limit 154 ppb for N2O and 484 ppb for CH4. The CH4 and N2O fluxes were measured by the linear variation in gas concentration in relation to the incubation time in closed chambers, and calculated by Equation (1), as proposed by Bayer et al. (2015) :

Flux = δC/δt (V/A) m/Vm (1)

where in the flux (µg m2h1); dC/dt is the change in gas concentration (nmol N2O and CH4 h1) in the chamber in the incubation interval ( t ); V and A are, respectively, the chamber volume (m3) and the soil site covered by the chamber (m2); m is the molecular weight of N2O or CH4 (µg), and Vm is the molar volume at the sampling temperature.

The fluxes were calculated for the sampling times 0, 15, and 30 min, expressed in μg N2O m2 h1 and µg CH4 m2 h1. The average daily N2O and CH4 fluxes were calculated from the average value of the four chambers installed per plot. To determine the cumulative fluxes, the area under the curve was integrated, based on the daily N2O and CH4 soil fluxes ( Santos et al., 2016 ). The amount of equivalent carbon (C eq) required to mitigate the cumulative annual fluxes of CH4 and N2O was calculated by Equations 2 and 3, respectively.

CH4 = (CAI* 16/12) * GWP * F (2)

where: CAI is the cumulative annual influx (kg CH4 ha1 yr1); GWP is the global warming potential of CH4 (25 kg CO2, IPCC (2007) ); F is the factor 0.273 (used for the conversion from CO2 to C);

N2O = (CAF* 44/28) * GWP * F (3)

where: CAF is the cumulative annual flux (kg N2O ha1 yr1); GWP is the global warming potential of N2O (298 kg CO2, IPCC (2007) ); F is the factor 0.273(used for conversion from CO2 to C).

Environmental factors

For each gas sampling, soil samples from the 0-5 cm layer were also collected to determine mineral N in the forms of nitrate (NO3) and ammonium (NH4+), at eight points near the chambers, forming a composite sample. From each soil sample, a sub-sample was taken to determine gravimetric soil moisture. For the extraction of NO3 and NH4+, we used 50 mL of a solution of 2 mol L1 KCl , according to the methodology of Bremner and Mulvaney (1982) . The solution was analyzed by spectrophotometry with a system of flux injection analysis (FIA) ( Hambridge, 2007a , b ) to determine NO3 and NH4+ concentrations.

Soil particle density was determined by the ring and volumetric flask methods, respectively ( Embrapa, 1997 ). Soil moisture was calculated by oven-drying a soil sub-sample of known weight at 105 ºC for 48 h. From these variables, the water-filled pore space (WFPS in %) was calculated for each gas sampling date and determined by the equation:

WFPS = (gravimetric moisture × BD) / [1 (BD/PD)] × 100 (4)

where: the gravimetric moisture is expressed in %, BD is the bulk density (g cm3) and PD is the particle density (2.65 g cm3).

The meteorological data were recorded using a datalogger (CR 1000) installed near the study site.

Calculations and statistical analyses

The environmental variables were subjected to the descriptive statistical analysis and applied to the normality test (Shapiro-Wilk), followed by analysis of variance (ANOVA). The daily CH4 and N2O fluxes had a non-normal distribution; therefore, the nonparametric Kruskal-Wallis test of medians was performed at 5 % probability to find possible differences between the areas and years studied by comparisons.

The CH4 influxes and accumulated N2O fluxes for the sampling dates were calculated by linear interpolation. To compare sites and years, the data of accumulated fluxes and equivalent carbon were subjected to analysis of variance (ANOVA) and the Tukey test ( p < 0.05).

Another analysis evaluated the seasonality effect and the relationship between CH4 and N2O fluxes and the environmental variables by the Pearson’s correlation, using the FactoMineR package of program R (version 3.2.2). Only significant correlations are shown in the text.


Temporal variation in CH4 and N2O fluxes and environmental variables

Daily and seasonal CH4 fluxes for year-1 and year-2 in each site are presented in Figure 3A . Year-1 had annual average of CH4 fluxes of –35, –3 and –2 μg m2 h1, while year-2 had –22, –8 and –1 μg m2 h1 in E1, E2, and CE, respectively. Regarding the seasonality effect, the average CH4 fluxes were –32, –12 and 11 μg m2 h1 and –38, 9, and –20 μg m2 h1for year-1, and in year-2, –20, –5 and –6 μg m2 h1 and –29, –17 and –7 μg m2 h1 in the rainy and dry seasons in E1, E2, and CE, respectively ( Figure 3A ). In year-1, significant differences were observed between the environments, where the average CH4 flux in the rainy season was higher in CE than in E1 ( p = 0.0002) and E2 ( p = 0.0196). In the dry season, the average CH4 fluxes were higher in E2 ( p = 0.0191).

Figure 3 – (A) Soil fluxes of methane (CH4) and (B) nitrous oxide (N2O) in the Eucalyptus stands E1 (clone EAC 1528, planted in 2011) and E2 (clone GG100, planted in 2009); and in CE (native Cerrado vegetation), Paranoá, Distrito Federal, Brazil. 

The mean annual N2O fluxes were 4, 8, and 3 μg m2 h1 for year-1 and 5, 5, and 4 μg m2 h1 for year-2 in E1, E2, and CE, respectively ( Figure 3B ). Average N2O fluxes in the rainy season for E1, E2, and CE were, respectively, 1.00, 4.00, and 0.07 μg m2 h1 (year-1) and 7, 4, and 3 μg m2 h1(year-2), and in the dry season 10, 14, and 7 μg m2 h1 (year-1) and 3, 7, and 5 μg m2 h1 (year-2) ( Figure 3B ). In year-1, significant differences between N2O fluxes were observed in the rainy season, with the highest average N2O fluxes in E2 ( p = 0.0196). However, in year-2, differences were only significant in the rainy season between the average fluxes in E1 and CE ( p = 0.0273), which were higher for E1.

In all GHG evaluation, an uptake of CH4 was observed in 44 % of the evaluations in CE, but in 19 % in the Eucalyptus stands. For N2O, the average fluxes were 5, 6, and 4 μg m2 h1 in E1, E2, CE, respectively. In this study, the results of CH4 and N2O fluxes in the Eucalyptus rows and interrows were not shown, since the differences were not significant.

The environmental variables showed that the CH4 pulse in μg m2 h1 (64 ± 77 in Sept 2014, 131 ± 179 in June 2014 and 85 ± 131 in Sept 2014) coincided with WFPS values of 25 % for E1, 42 % for E2, and 33 % for CE in year-1. In year-2, CH4 pulses 266 ± 365 (May 2015), 104 ± 429 (Feb 2015), and 156 ± 292 μg m2 h1 (May 2015) coincided with WFPS values of 47 %, 40 %, and 68 % for E1, E2, and CE, respectively ( Figures 3A and 4A ). The N2O pulses of 39 ± 72 (May 2014), 108 ± 97 (Aug 2014), and 58 ± 87 μg m2 h1 (Sept 2014) coincided with WFPS values of approximately 33 % in all treatments in year-1, while in year-2, the N2O pulses 21 ± 81 (Feb 2015), 42 ± 65 (July 2015) and 27 ± 83 μg m2 h1 (May 2015) coincided with WFPS values of 37 %, 34 %, and 39 % for E1, E2, and CE, respectively ( Figures 3A and 4A ).

Figure 4 – (A) - Water-filled pore space (WFPS); (B) - nitrate NO3–; (C) - ammonium NH4+ and (D) - soil temperature from Oct 2013 to Nov 2015 in Eucalyptus stands (E1, clone EAC 1528 planted in 2011 and E2, clone GG100 planted in 2009); and CE (native Cerrado vegetation), Paranoá, Distrito Federal, Brazil. 

In year-1, the Cerrado was the only site with a correlation of 0.58 ( p = 0.0018) and –0.68 ( p = 0.0015) between the CH4 flux and WFPS, respectively, in the rainy and dry seasons. Only in E2, correlations were detected between N2O fluxes and WFPS in the rainy and dry seasons (0.63 ( p = 0.0005) and –0.59 ( p = 0.0041), respectively). In year-2, WFPS ranged from 19 % to 71 % in the rainy and from 30 % to 43 % in the dry season. With regard to correlations, CH4 and WFPS in CE positively correlated (0.84; p < 0.0001). For N2O, a correlation with WFPS of 0.62 ( p = 0.0190) was observed in E1, both correlations occurred in the dry season.

In year-1, the soil temperature in all sites remained between 17 and 24 ºC. The highest CH4 and N2O pulses occurred at soil temperatures ≥ 19 ºC. With regard to correlations, CH4 and soil temperature in CE positively correlated (0.65; p = 0.023). In year-2, the soil temperature ranged from 16 to 26 ºC and was correlated with CH4 flux in E2 (0.59; p = 0.024).

Soil mineral N dynamics

The highest soil NO3 and NH4+ concentrations were recorded in the rainy season in all sites ( p < 0.0240) ( Figures 4B and 4C ) and did not coincide with the GHG pulse. In the rainy season of year-1, a correlation of –0.68 between CH4 × NO3 ( p = 0.0004) in E1 was identified of 0.49 and 0.53 between N2O × NO3 ( p = 0.0033), and N2O × NH4+ ( p = 0.0023) in CE, while in the dry season, the correlation was 0.55 between CH4 and NO3 ( p = 0.0065) in CE.

The ammoniacal N was predominant ( Figure 4C ). The NO3concentrations were higher in the rainy season ( p < 0.0093). The N2O soil pulse coincided with NO3 concentrations < 0.50 mg kg1of soil and only in some moments, NO3 exceeded 2.00 mg kg1soil ( Figure 4B ). The seasonality effect on NH4+ concentrations differed only in CE, with higher soil concentrations in the dry season ( p < 0.0001), coinciding with higher N2O pulse in all studied sites. In year-2, NO3 and NH4+ soil concentrations were very close between the sites, except for E2, where concentrations were below 1 mg kg1of soil, from Feb 2015 onwards ( Figures 4B and 4C ). With regard to correlations, E1 was the only area in which N2O and NO3 concentrations negatively correlated (–0.63; p = 0.002) during the dry season.

Cumulative CH4 and N2O fluxes and carbon equivalent (C eq)

In the study period, cumulative fluxes were not influenced by annual variation, age of Eucalyptus stands, or by the replacement of native vegetation for Eucalyptus . For N2O, variations were 0.33 to 0.85 kg ha1 yr1 in year-1 and 0.32 to 0.43 kg ha1 yr1 in year-2 ( Table 3 ). The CH4values were negative, with cumulative influxes of –1.86 to –0.63 kg ha1 yr1 in year-1, and –1.85 to –1.34 kg ha1yr1in year-2 ( Table 3 ).

Table 3 – Cumulative fluxes and Carbon equivalent (C eq) of N2O and CH4 in Eucalyptus stands (E1, clone EAC 1528 planted in 2011 and E2, clone GG100 planted in 2009); and CE (native Cerrado vegetation) in year-1 and year-2; Distrito Federal, Brazil. 

Area Year-1*
N2O C equivalent CH4 C equivalent
------------------------------------- kg ha–1-----------------------------------------
E1 0.43 (± 0.26) 55 (± 33) –1.86 (± 0.26) –16 (± 12)
E2 0.85 (± 0.30) 108 (± 58) –0.98 (± 0.30) –8 (± 8)
CE 0.33 (± 0.20) 42 (± 25) –0.63 (± 0.20) –5 (± 5)
N 9 9 9 9
P 0.05 0.05 0.05 0.05
E1 0.39 (± 0.18) 52 (± 23) –1.34 (± 0.36) –11 (± 3)
E2 0.44 (± 0.01) 58 (± 11) –1.85 (± 1.40) –15 (± 11)
CE 0.32 (± 0.01) 43 (± 10) –1.55 (± 1.68) –13 (± 14)
N 9 9 9 9
P 0.05 0.05 0.05 0.05

*Year-1 = Oct 2013 to Sept 2014; Year-2 = Oct 2014 to Sept 2015.

The C eq ranged from 42 to 108 kg ha1 in year-1 and from 40 to 54 kg ha1 in year-2. However, on an annual basis, the cumulative C eq for CH4 was negative in all sites evaluated (–6 to –17 kg ha1 in year-1; –12 to –17 kg ha1 in year-2) ( Table 3 ).

The C eq ranged from 42 to 108 kg ha1 in year-1 and from 40 to 54 kg ha1 in year-2. However, on an annual basis, the cumulative C eq for CH4 was negative in all sites evaluated (–6 to –17 kg ha1 in year-1; –12 to –17 kg ha1 in year-2) ( Table 3 ).


Temporal variability of CH4 and N2O fluxes and environmental variables

The CH4 influxes were predominant in this study (81 % for E1 and E2, and 57 % for CE), reaffirming that forest soils are common sinks of this gas. The same behavior was observed in other studies ( Godoi et al., 2016 ; Liu et al., 2017 ). In general, well-drained soils consume atmospheric CH4 ( Ciais et al., 2013 ; IPCC, 2013 ) and indicate CH4 uptake from the atmosphere mediated essentially by methanotrophic bacteria due to reduced soil water content, favoring diffusion of atmospheric CH4 into soils ( Hiltbrunner et al., 2012 ). Other studies focused on savannas also mentioned these uptake conditions. In Eucalyptus globulus stands and Australian savanna vegetation, respectively, Livesley et al. (2009) recorded influxes of –7 and –16 μg m2 h1. In areas under cerradão, Siqueira-Neto et al. (2011) reported negative CH4 fluxes between –93 and –29 μg m2 h1.

The CH4 pulses in the three sites occurredin the dry season. Priano et al. (2014) found an inverse relation between CH4 emission rate and WFPS. The results of this study also indicate that wet soils can oxidize as much CH4 as relatively dry soils, with average WFPS values near 40 % in the study period. Previous reports also demonstrated that peaks of CH4 soil oxidation occur at some intermediate level of soil water content ( Khalil and Baggs, 2005 ). According to Humer and Lechner (1999) , the optimum saturation degree for oxidation is between 40 and 80 % (moisture content between 25 and 50 %). Moreover, measuring potential methane (CH4) oxidation rates in semiarid soil, Sullivan et al. (2013) observed that CH4 oxidation rates were higher in the wet than in the dry season.

During the assessed period, N2O fluxes in soil under native vegetation (CE) rarely exceeded 10 μg m2 h1. This is attributed to the very low amount of NO3 and to the predominant N form (NH4+) ( Figures 3B and 3C ) that did not induce high N2O emissions. These results were similar to previous descriptions in studies on Oxisols under native Cerrado vegetation, which reported few measurements above 10 μg m2 h1 and average fluxes between 0.6 and 16 μg N2O m2 h1 ( Siqueira-Neto et al., 2011 ; Santos et al., 2016 ; Carvalho et al., 2017 ).

In year-1, the N2O fluxes were higher in the dry than in the rainy season. Even under conditions in which fluxes are common (WFPS > 48 %, predominance of NH4+ and soil temperature > 21 ° C), very high fluxes were not observed in the entire dry season, but only in late Aug (08/28/2014). At this time, mineral N exceeded 5.0 mg kg1soil (lower than in the rainy season) and the soil temperature rose from 17 to 20.3 ºC. From Sept onwards, the soil temperature was 23 ºC. In this period, there was possibly a response in the N2O pulses to the increase in soil temperature in E1 and CE, however low (< 59 μg m2 h1).

Forest soils in the Cerrado biome usually have low N2O fluxes, which can be attributed to the physical, chemical, and biological characteristics of the system ( Martins et al., 2015a ; Martins et al., 2015b ; Santos et al., 2016 ). In general, N availability in tropical savanna ecosystems in Brazil is low, since 15 – 37 % of N is resorbed prior to leaf dehiscence ( Nardoto et al., 2006 ) and in the Cerrado, inorganic N is available by mineralization of SOM ( Catão et al., 2016 ). Under undisturbed conditions, N pools are at steady state and production and consumption are equal (Booth, 2005); thus, the annually mineralized inorganic N in unburned Cerrado does not exceed 15 kg ha1yr1( Nardoto et al., 2006 ). With these efficient cycling and use mechanisms, little N is lost by leaching or gas transformation ( Bustamante et al., 2006 ).

Under natural conditions, available N in Cerrado soils depends to a large extent on organic sources and litter ( Table 2 ). The equilibrium between mineralization and immobilization depends on the C: N ratio, which is high (> 65:1) in this study and on the material incorporated into the soil, which may induce N immobilization, showing that residue quality also influences N2O emissions. According to Alluvione et al. (2010), a high C:N ratio may increase N immobilization thus reducing the occurrence of denitrification and consequently of GHG emissions.

Another important factor to be considered is the cycling efficiency. If high, low values of mineral N can be established in the soil, and the N mineralized by decomposition can be absorbed quickly by the plant root system, after nitrification and denitrification ( Ugalde et al., 2007 ). Low rates of N2O and CH4 emissions were also documented in other studies on forests in Brazil, Australia, and China. Godoi et al. (2016) observed similar fluxes of CH4 (–22.7 and –24.4 mg CH4 m2 h1) and N2O (5.3 and 5.4 mg N2O m2 h1), for soils with Acacia and native vegetation, respectively. Werner et al. (2006) observed values near 7 mg N2O m2 h1in reforested areas in China, under tropical conditions, while Allen et al. (2009) reported a high CH4 uptake (–1 to –50 µg CH4 m2 h1) and low N2O fluxes (–5 to 50 μg N2O m2 h1) in subtropical Australian soils under Eucalyptus .

In general, when good drainage conditions, which reduce WFPS ( Baggs and Philippot, 2010 ), are combined to a low relative NO3 production, the mineral N concentrations rarely exceed the N demand of microorganisms and plant roots ( Martins et al., 2015b ). Although several studies reported correlations between GHGs and mineral N in the soil ( Siqueira-Neto et al., 2011 ; Santos et al., 2016 ; Carvalho et al., 2017 ), and in this study, some correlations between these N forms and gas fluxes were also observed, the gas emission pulses did not occur synchronously with the highest NO3 and NH4+ concentrations, which may have reduced the significance of relations.

In this study, the GHG fluxes were low, regardless of the season and year studied, which was mainly associated to WFPS < 50 % and NO3 concentrations < 8 mg kg1. In soils with high permeability, such as in the Oxisol of this study, both WFPS and texture are key factors in N2O emission. In soils with WFPS > 60 %, denitrification tends to be the predominant process ( Livesley et al., 2009 ; Gregorich et al., 2015) , while in low WFPS soils, ammonia oxidation is favored ( Bateman and Baggs, 2005) . These findings show that Eucalyptus stands of different ages and areas of native Cerrado vegetation probably contribute to reduce N2O emissions, where no external N sources are provided and the systems depend exclusively on internal nutrient cycling. Furthermore, based on the predominant form of mineral N (NH4+), it is assumed that the studied N2O emissions may result from nitrification rather than from denitrification processes.

However, it should be considered that transformations of N (immobilization or mineralization) in an ecosystem are coupled with C transformations, especially when organic carbon molecules are converted into CO2 by soil heterotrophic microbial populations ( McGill and Cole, 1981 ), which can reduce the partial pressure of oxygen and favor denitrification. Significant GHG pulse emissions following the first rains after a dry season, often with a short time lag, have been reported in different seasonally dry ecosystems. The pulses are generally preceded by significant GHG emissions immediately after the soil is re-moistened, due to water-induced activation of soil microbes ( Santos et al., 2016 ).

Studies show that soil moisture expressed by WFPS, soil temperature, and mineral N content are the main variables that control and express GHG emissions ( Bayer et al., 2015 ). Siqueira-Neto et al. (2011) reported divergent observations for native Cerrado vegetation, where lower N2O emissions were observed during the dry season, indicating that the seasonal variations occur due to the absence of rainfall and consequent reduction in soil moisture.

In this study, no environmental variable stood out as an environmental drive, despite variables with relevant effects on N2O emissions in agricultural systems found by our research group ( Santos et al., 2016 ; Carvalho et al., 2017 ; Sato et al., 2017 ). Therefore, these results indicate that the lack of consistent environmental effects may be due to both the intrinsic low GHS emission and the high spatial/temporal variability of native and cultivated forest environments in the Cerrado.

Cumulative CH4 and N2O fluxes

The cumulative annual CH4 fluxes were negative for the areas and years studied ( Figures 4B and 4D ). The cumulative CH4 flux from Eucalyptus under the conditions assessed shows the crop potential of methane mitigation. These cumulative CH4 influxes in Eucalyptus plantations and native savanna vegetation are in agreement with reports of emissions from forests and savannas ( Table 4 ) that indicate CH4 uptake from the atmosphere, since a greater amount was consumed by the environment than the effectively produced quantity ( Bustamante et al., 2012 ).

Table 4 – Literature review of annual or partial rates of CH4 and N2O fluxes in forest soils. 

Country Site CH4 N2O Reference
----- kg ha–1 -----
Brazil Woodland - –0.50 Carvalho et al. (2017)
Brazil Woodland - 0.07 Silva et al. (2017a)
Brazil Cerrado stricto sensu - 0.55 Sato et al. (2017)
Brazil Cerrado stricto sensu - 0.28 Santos et al. (2016)
Brazil Cerrado stricto sensu –4.4 0.40 Carvalho et al. (2014)
Brazil eucalyptus urograndis - 0.7 Coutinho et al. (2010)
Africa Savanna vegetation - 2.33 Castaldi et al. (2013)
Australia Native Forest (Savanna) –1.6 0.02 Grover et al. (2012)
Australia Native Forest (Savanna) –1.4 0.16 Livesley et al. (2009)
Australia Eucalyptus globulus –6.8 0.15 Livesley et al. (2009)
Australia Pinus radiata –5.0 0.12 Livesley et al. (2009)

Studies indicate that high soil N mineral contents may stimulate CH4 oxidation ( Bodelier and Laanbroek, 2004 ; Liu and Greaver, 2009 ). Mineral N seems to be a prerequisite for CH4 consumption, although the identification of relationships between N availability and CH4 consumption, as well as the bacteria involved, is still a challenge. For the time being, N must be treated as a potential inhibitor and as a beneficial factor for CH4 consumption in soils ( Bodelier and Laanbroek, 2004 ). Ammonium can compete with CH4 for the enzyme methane mono-oxygenase, effectively lowering CH4 oxidation by methanotrophs in the soil ( Hanson and Hanson, 1996 ).

The N2O emissions were below 0.86 kg ha1yr1for all areas studied ( Figures 4A and 4C ). Other studies also reported cumulative N2O fluxes below 1 kg ha1yr1( Table 4 ). To date, no studies have evaluated soil N2O fluxes for a period of two years under planted Eucalyptus systems in Brazil. In our study, mainly during the dry season in native Cerrado, N2O influxes and low nitrate levels were observed. The N2O influx under native vegetation may be associated to a low N mineral content, in predominantly ammoniacal N, a rapid drainage of soil water to the subsurface layers ( Martins et al., 2015b ; Santos et al., 2016 ; Carvalho et al., 2017 ; Sato et al., 2017 ), and low soil pH ( Lopes and Cox, 1977 ), since nitrification tends to decrease with increasing soil acidity ( Hickman et al., 2014 ).

In an integrated crop-livestock-forest system, Carvalho et al. (2017) observed N2O fluxes lower than in an integrated crop livestock system. The authors claimed that the presence of Eucalyptus plant residues in the system, which are rich in phenolic compounds and are acidic ( Soumare et al., 2015 ), inhibit the enzyme and microbial activity in the soil ( Chen et al., 2013 ).

Despite limitations of the static chambers in relation to the real conditions of free soil-atmosphere fluxes, these boxes are easy to construct and can be used under different conditions. Therefore, even low-magnitude flows can be detected and information on the spatial variability of emissions is provided, although no significant differences related to the position and no emission pattern could be observed in our study. Other drawbacks refer to variations in daily measurements that are commonly wide, the chamber measurements may be underestimated or overestimated, and the values of standard deviation are generally high. Possibly, the high spatial and temporal variability of the gas emissions was due to the quantity of variables that are interrelated and drive the flow dynamics. However, cumulative N2O emissions from forest soils and CH4 influxes were low (< 1.0 kg ha1), although their variability should not be left unmentioned. In evaluations at 15 positions in natural forests in Germany, Jungkunst et al. (2012) also found high variability and low spatial representativeness of the chambers, attributed to the C:N ratio, N input, and water availability by the authors. However, considering the variations observed, a random distribution of the chambers is suggested, since the measurements seem to be independent from the chamber position and distance from the Eucalyptus trees.

Planting Eucalyptus in areas of former native vegetation or previous agricultural use resulted in no marked differences between cumulative GHG fluxes. From the ecological and environmental viewpoint, greater biodiversity in areas of native vegetation stands out. This similarity in the cumulative GHG fluxes may be related to the stability observed in sites with Eucalyptus stands after planting.


The change in land use from Cerrado to Eucalyptus plantations did not induce significant changes in GHGs, compared to the native vegetation. The flux rates were low for both gases (N2O and CH4). The temporal variations in GHG fluxes and the different ages of stands caused no significant differences between cumulative annual fluxes. Our results may be an important contribution to a better understanding of the dynamics of GHG fluxes in commercial forest plantations in the Cerrado region.


The study was supported financially by Embrapa Cerrados (Contract Nº Project Emission of Greenhouse Gases, carbon stocks and environmental indicators in the Cerrado Biome (SALTUS) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).


Achard, F.; Eva, H.D.; Mayaux, P.; Stibig, H.J.; Belward, A. 2004. Improved estimates of net carbon emissions from land cover change in the tropics for the 1990s. Global Biogeochemical Cycles 18: GB2008. [ Links ]

Allen, D.E.; Mendham, D.S.; Singh, B.; Cowie, A.; Wang, W.; Dalal, R.C.; Raison, R.J. 2009. Nitrous oxide and methane emissions from soil are reduced following afforestation of pasture lands in three contrasting climatic zones. Australian Journal of Soil Research 47: 443-458. [ Links ]

Alluvione, F. 2010. Nitrous oxide and carbon dioxide emissions following green manure and compost fertilization in corn. Soil Science Society of America Journal 74: 384-395. [ Links ]

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. 2012. Selection of the most suitable sampling time for static chambers for the estimation of daily mean N2O flux from soils. Soil Biology and Biochemistry 46: 129-136. [ Links ]

Baggs, E.M.; Philippot, L. 2010. Microbial terrestrial pathways to nitrous oxide. p. 4-35. In: Smith, K., ed. Nitrous oxide and climate change. Earthscan, London, UK. [ Links ]

Bateman, E.J.; Baggs, E.M. 2005. Contributions of nitrification and denitrification to N2O emissions from soils at different water-filled pore space. Biology and Fertility of Soils 41: 379-388. [ Links ]

Bayer, C.; Gomes, J.; Zanatta, J.A.; Vieira, F.C.B.; Piccolo, M.C.; Dieckow, J.; Six, J. 2015. Soil nitrous oxide emissions as affected by long-term tillage, cropping systems and nitrogen fertilization in Southern Brazil. Soil & Tillage Research 146: 213-222. [ Links ]

Bodelier, P.L.E.; Laanbroek, H.J. 2004. Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiology Ecology 47: 265-277. [ Links ]

Booth, M.S.; Stark, J.M.; Rastetter, E. 2005. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecological Monographs 75: 139-57. [ Links ]

Bonan G.B. 2008. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320: 1444-1450. [ Links ]

Bremner, J.M.; Mulvaney, C.S. 1982. Total nitrogen. p. 1119-1123. In: Page, A.L.; Miller, R.H.; Keeny, D.R., eds. Methods of soil analysis, American Society of Agronomy, Madison, WI, USA. [ Links ]

Bustamante, M.M.C.; Medina, E.; Asner, G.P.; Nardoto, G.B.; Garcia-Montiel, D.C. 2006. Nitrogen cycling in tropical and temperate savannas. Biogeochemistry 79: 209-237. [ Links ]

Bustamante, M.M.C.; Nardoto, G.B.; Pinto, A.S.; Resende, J.C.F.; Takahashi, F.S.C.; Vieira, L.C.G. 2012. Potential impacts of climate change on biogeochemical functioning of Cerrado ecosystems. Brazilian Journal of Biology 72: 655-671. [ Links ]

Cardoso, M.R.D.; Marcuzzo, F.F.N.; Barros, J.R. 2014. Climatic classification of Köppen-Geiger for the state of Goiás and the Federal District. Acta Geográfica 8: 40-55 (in Portuguese, with abstract in English). [ Links ]

Carvalho, A.M.; Oliveira, W.R.D.; Ramos, M.L.G.; Coser. T.R.; Oliveira, A.D.; Pulrolnik, K.; Souza, K.W.; Vilela, L.; Marchão, L.R. 2017. Soil N2O fluxes in integrated production systems, continuous pasture and Cerrado. Nutrient Cycling in Agroecosystems 107: 1-15. [ Links ]

Carvalho, J.L.N.; Raucci, G.S.; Frazao, L.A.; Cerri, C.E.P.; Bernoux, M.; Cerri, C.C. 2014. Crop-pasture rotation: a strategy to reduce soil greenhouse gas emissions in the brazilian Cerrado. Agriculture, Ecosystems & Environment 183: 167-175. [ Links ]

Castaldi, S.; Bertolini, T.; Valente, A.; Chiti, T.; Valentini, R. 2013. Nitrous oxide emissions from soil of an African rain forest in Ghana. Biogeosciences 10: 4179-4187. [ Links ]

Catão, E.C.P.; Lopes, F.A.C.; Rubini, M.R.; Nardoto, G.B.; Prosser, J.I.; Krüger, R.H. 2016. Short-term impact of soybean management on ammonia oxidizers in a brazilian savanna under 69 restoration as revealed by coupling different techniques. Biology and Fertility of Soils 52: 401-412. [ Links ]

Chen, F.; Zheng, K.; Ouyang, Z.; Li, H.; Wu, B.; Shi, Q. 2013. Soil microbial community structure and function responses to successive planting of Eucalyptus. Journal of Environmental Sciences 25: 2102-2111. [ Links ]

Ciais, P.; Sabine, C.; Bala, G.; Bopp, L.; Brovkin, V.; Canadell, J.; Chhabra, A.; DeFries, R.; Galloway, J.; Heimann, M.; Jones, C.; Le Quéré, C.; Myneni, R.B.; Piao, S.; Thornton, P. 2013. Carbon and other Biogeochemical Cycles, in Climate Change 2013: The Physical Science Basis, Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland. [ Links ]

Coutinho, R.P.; Urquiaga, S.; Boddey, R.M.; Alves, B.J.R.; Torres, A.Q.A.; Jantalia, C. P. 2010. Carbon and nitrogen stock and N2O emission in different land uses in the Atlantic Forest. Pesquisa Agropecuária Brasileira 45: 195-203 (in Portuguese, with abstract in English). [ Links ]

Empresa Brasileira de Pesquisa Agropecuária [Embrapa]. 1997. Soil Analysis Methods Manual = Manual de Métodos de Análises de Solo. 2 ed. rev. atual, Rio de Janeiro, RJ, Brazil. 212p.: il. (Embrapa-CNPS. Documentos; 1) (in Portuguese). [ Links ]

Food and Agriculture Organization [FAO]. 2001. Global ecological zoning for the global forest resources assessment 2000. FAO, Rome, Italy. Available at: [Accessed Feb 23, 2017] [ Links ]

Godoi, S.G.; Neufeld, A.D.H.; Ibarr, M.A.; Ferreto, D.O.C.; Bayer, C.; Lorentz, L.H.; Vieira, F.C.B. 2016. The conversion of grassland to acacia forest as an effective option for net reduction in greenhouse gas emissions. Journal of Environmental Management 169: 91-102. [ Links ]

Grandy A.S.; Neff, J.C. 2008. Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Science of Total Environment 404: 297-307. [ Links ]

Gregorich, E.; Janzenx, H.H.; Helgason, B.; Ellertx, B. 2015. Nitrogenous gas emissions from soils and greenhouse gas effects. Advances in Agronomy 132: 39-74. [ Links ]

Grover, S.P.P.; Livesley, S.J.; Hutley, L.B.; Jamali, H.; Fest, B.; Beringer, J.; Butterbach-Bahl, K.; Arndt, S.K. 2012. Land use change and the impact on greenhouse gas exchange in north Australian savanna soils. Biogeosciences 9: 423-437. [ Links ]

Hambridge, J. 2007a. QuikChem method 12-107-04-1-J: determination of nitrate in 2M KCl soil extracts by flow injection analysis. Lachat Instruments, Milwaukee, WI, USA. [ Links ]

Hambridge, J. 2007b. QuikChem method 12-107-06-2-F: determination of ammonia (salicylate) in 2 M KCl soil extracts by flow injection analysis (high throughput). Lachat Instruments, Milwaukee, WI, USA. [ Links ]

Hanson, R.S.; Hanson, T.E. 1996. Methanotrophic bacteria. Microbiology Reviews 60: 439-471. [ Links ]

Hickman, J.E.; Palm, C.A.; Mutuo, P.; Melillo, J.M.; Tang, J. 2014. Nitrous oxide (N2O) emissions in response to increasing fertilizer addition in maize ( Zea mays L.) agriculture in western Kenya. Nutrient Cycling in Agroecosystems 100: 177-187. [ Links ]

Hickman, J.E.; Tully, K.L.; Groffman, P.M.; Diru, W.; Palm, C.A. 2015. A potential tipping point in tropical agriculture: avoiding rapid increases in nitrous oxide fluxes from agricultural intensification in Kenya. Journal Geophysical Research 12: 938-951. [ Links ]

Hiltbrunner, D.; Zimmermann, S.; Karbin, S.; Hagedorn, F.; Niklaus, P.A. 2012. Increasing soil methane sink along 120-year afforestation chronosequence is driven by soil moisture. Global Change Biology 18: 3664-3671. [ Links ]

Högberg, M.N.; Högberg, P.; Myrold, D.D. 2007. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150: 590-601. [ Links ]

Houghton, R.A. 1999. The annual net flux of carbon to the atmosphere from changes in land-use 1850-1990. Tellus Series B 51: 298-313. [ Links ]

Huang, Z.; Clinton P.W.; Baisden W.T.; Davis, M.R. 2011. Long-term nitrogen additions increased surface soil carbon concentration in a forest plantation despite elevated decomposition. Soil Biology and Biochemistry 43: 302-307. [ Links ]

Humer, M.; Lechner, P. 1999. Alternative approach to the elimination of greenhouse gases from old landfills. Waste Management Research 17: 443-452. [ Links ]

Iglesias-Trabado, G.; Carballeira-Tenreiro, R.; Folgueiro-Lozano, J. 2009. Eucalyptus universalis: global cultivated eucalyptus forests map, version 1.2. Git-Forestry, Charlotte, NC, USA. Available at: [Accessed Jun 19, 2018] [ Links ]

IPCC. 2007. Climate Change: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland. [ Links ]

IPCC. 2013. Climate Change: The Physical Science Basis: Working Group I Contribution to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland. [ Links ]

IPCC. 2014. Climate Change: The Physical Science. IPCC, Geneva Switzerland. [ Links ]

Jungkuns, H.; Bargsten, A.; Timme, M.; Glatzel, S. 2012. Spatial variability of nitrous emissions in an unmanaged old-growth beech forests. Journal of Plant Nutrition and Soil Science 175: 739-749. [ Links ]

Khalil, M.I.; Baggs, E.M. 2005. CH4oxidation and N2O emissions at varied soil water filled pore spaces and headspace CH4concentrations. Soil Biology and Biochemistry 37: 1785-1794. [ Links ]

Kim, D.G.; Kirschbaum, M.U. 2015.The effect of land-use change on the net exchange rates of greenhouse gases: a compilation of estimates. Agriculture, Ecosystems and Environment 208: 114-126. [ Links ]

Kim, D.G.; Thomas, A.D.; Pelster, D.; Rosenstock, T.S.; Sanz-Cobena, A. 2016. Greenhouse gas emissions from natural ecosystems and agricultural lands in sub-Saharan Africa: synthesis of available data and suggestions for further research. Biogeosciences 13: 4789-4809. [ Links ]

Liu, L.; Greaver, T.L. 2009. A review of nitrogen enrichment effects on three biogenic GHGs: the CO2sink may be largely offset by stimulated N2O and CH4emission. Ecology Letters 12: 1103-1117. [ Links ]

Liu, J.; Chen, H.; Yang, X.; Gong, Y.; Zheng, X.; Fan, M.; Kuzyakov, Y. 2017. Annual methane uptake from different land uses in an agro-pastoral ecotone of northern China. Agricultural and Forest Meteorology 236: 67-77. [ Links ]

Livesley, S.J.; Kiese, R.; Miehle, P.; Weston, C.J.; Butterbach-Bahl, K.; Arndt, S.K. 2009. Soil–atmosphere exchange of greenhouse gases in a Eucalyptus marginata woodland, a clover-grass pasture, and Pinus radiata and Eucalyptus globulus plantations. Global Change Biology 15: 425-440. [ Links ]

Lopes, A.S.; Cox, F.R. 1977. A survey of the fertility status of surface soils under cerrado vegetation in Brazil. Soil Science Society of America Journal 41: 742-747. [ Links ]

Lucas, R.W.; Casper, B.B; Jackson, J.K.; Balser, T.C. 2007. Soil microbial communities and extracellular enzyme activity in the New Jersey Pinelands. Soil Biology and Biochemistry 39: 2508-2519. [ Links ]

Martins, C.S.C.; Nazaries, L.; MacDonald, C.A.; Anderson, I.C.; Singh, B.K. 2015a. Water availability and abundance of microbial groups are key determinants of greenhouse gas fluxes in a dryland forest ecosystem. Soil Biology and Biochemistry 86: 5-16. [ Links ]

Martins, M.R.; Jantalaia, C.P.; Polidoro, J.C.; Batista, J.N.; Alves, B.J.R.; Boddey, R.M.; Urquiaga, S. 2015b. Nitrous oxide and ammonia emission from N fertilization of maize crop under no-till in Cerrado soil. Soil & Tillage Research 151: 75-81. [ Links ]

Masaka, J.; Nyamangara, J.; Wuta, M. 2014. Nitrous oxide emissions from wetland soil amended with inorganic and organic fertilizers. Archives of Agronomy and Soil Science 60: 1363-1387. [ Links ]

McGill, W.B.; Cole, C.V. 1981. Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26: 267-286. [ Links ]

Michel, K.; Matzner, E. 2003. Response of enzyme activities to nitrogen addition in forest 36 floors of different C-to-N ratios. Biology and Fertility of Soils 38: 102-109. [ Links ]

Nardoto, G.B.; Bustamante, M.M.C.; Pinto, A.S.; Klink, C.A. 2006. Nutrient use efficiency at ecosystem and species level in savanna areas of Central Brazil and impacts of fire. Journal of Tropical Ecology 22: 191-201. [ Links ]

Priano, M.E.; Fusé, V.S.; Gere, J.I.; Berkovic, A.M.; Williams, K.E.; Guzmán, S.A.; Gratton, R.; Juliarena, M.P. 2014. Tree plantations on a grassland region: effects on methane uptake by soils. Agroforestry Systems 88: 187-19. [ Links ]

Santos, I.L.; Oliveira, A.D.; Figueiredo, C.C.; Malaquias, J.V.; Santos Junior, J.D.G.; Ferreira, E.A.B.; Sa, M.A.C.; Carvalho, A.M. 2016. Soil N2O emissions from long-term agroecosystems: interactive effects of rainfall seasonality and crop rotation in the Brazilian Cerrado. Agriculture, Ecosystems and Environment 233: 111-120. [ Links ]

Sato, J.H.; Carvalho, A.M.; Figueiredo, C.C.; Coser, T.R.; Sousa, T.R.; Vilela, L.; Marchão, L.R. 2017. Nitrous oxide fluxes in a Brazilian clayey Oxisol after 24 years of integrated crop-livestock management. Nutrient Cycling in Agroecosystems 107:1-14. [ Links ]

Silva, J.F.; Carvalho, A.M.; Reinb, T.A.; Coser, T.R. Ribeiro-Júnior, W.Q.; Vieira, D.L.; Coomes D.A. 2017a. Nitrous oxide emissions from sugarcane fields in the Brazilian Cerrado. Agriculture, Ecosystems and Environment 246: 55-65. [ Links ]

Silva, F.M.A.; Evangelista, B.A.; Malaquias, J.V.; Muller, A.G.; Oliveira, A.D. 2017b. Time analyses of climate variables monitored between 1974 and 2003 at Embrapa Cerrados main station = Análise Temporal de Variáveis Climáticas Monitoradas entre 1974 e 2013 na Estação Principal da Embrapa Cerrados. Embrapa Cerrados, Planaltina, DF, Brazil. (Embrapa Cerrados. Boletim de Pesquisa e Desenvolvimento, 340) (in Portuguese). [ Links ]

Siqueira Neto, M.; Piccolo, M.C.; Costa Junior, C.; Cerri, C.C.; Bernoux, M.; 2011. Greenhouse gas emissions in different land uses in the Cerrado biome. Revista Brasileira de Ciência do Solo 35: 63-76 (in Portuguese, with abstract in English). [ Links ]

Smith, K.A. 2017. Changing views of nitrous oxide emissions from agricultural soil: key controlling processes and assessment at different spatial scales. European Journal of Soil Science 68:137-155. [ Links ]

Soil Survey Staff. 2006. Keys to Soil Taxonomy. 8ed. USDA-NRCS, Washington, DC, USA. [ Links ]

Soumare, A.; Manga, A.; Fall, S.; Hafidi, M.; Ndoye, I.; Duponnois, R. 2015. Effect of Eucalyptus camaldulensis amendment on soil chemical properties, enzymatic activity, Acacia species growth and roots symbioses. Agroforestry Systems 89: 97-106. [ Links ]

Sullivan, B.W.; Selmants, P.C.; Hart, S.C. 2013. Does dissolved organic carbon regulate biological methane oxidation in semiarid soils? Global Change Biology 19: 2149-2157. [ Links ]

Tubiello, F.N.; Salvatore, M.; Rossi, S.; Ferrara, A.; Fitton, N.; Smith, P. 2013. The FAOSTAT database of greenhouse gas emissions from agriculture. Environmental Research Letters 8: 015009, 10. [ Links ]

Ugalde, D.; Brungs, A.; Kaebernick, M.; McGregor, A.; Slattery, B. 2007. Implications of climate change for tillage practice in Australia. Soil Tillage Resources 97: 318-330. [ Links ]

Werner, C.; Zheng, X.; Tang, J.; Xie, B.; Liu, C.; Kiese, R.; Butterbach, K. 2006. N2O, CH4and CO2emissions from seasonal tropical rainforests and a rubber plantation in southwest China. Plant Soil 289: 335-353. [ Links ]

Zanatta, J.A.; Alves, B.J.R.; Bayer, C.; Tomazi, M.; Fernandes, A.H.B.M.; Costa, F.S.; Carvalho, A.M. 2014. Protocol for measuring greenhouse gases in the soil = Protocolo para medição de gases de efeito estufa no solo. Embrapa Florestas, Colombo, PR, Brazil. (Documentos. Embrapa Florestas, 265) (in Portuguese). [ Links ]

Received: October 18, 2018; Accepted: August 09, 2019

* Corresponding author

Edited by: Eduardo Alvarez Santos

Authors’ Contributions

Conceptualization : Oliveira, A.D. Data acquisition : Oliveira, A.D.; Ribeiro, F.P. Data analysis : Oliveira, A.D. ; Ribeiro, F.P.; Zuim, D.R.; Pinheiro, L.A.; Malaquias, J.V. Design of methodology : Oliveira, A.D.; Ribeiro, F.P. Writing and editing : Oliveira, A.D.; Ribeiro, F.P.; Ferreira, E.A.B.; Gatto, A.; Pulrolnik, K.; Soares, J.P.G.; Carvalho, A.M.

Creative Commons License  This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.