Agriculture, Ecosystems and Environment 135 (2010) 161–167

Inorganic nitrogen, microbial biomass and microbial activity of a sandyBrazilian Cerrado soil under different land uses

Leidivan Almeida Frazao a,*, Marisa de Cassia Piccolo a, Brigitte Josefine Feigl a,Carlos Clemente Cerri a, Carlos Eduardo Pellegrino Cerri b

a Centro de Energia Nuclear na Agricultura, Laboratorio de Biogeoquımica Ambiental, Av. Centenario 303, P.O. Box 96, 13416-000, Piracicaba, SP, Brazilb Escola Superior de Agricultura Luiz de Queiroz, Departamento de Solos e Nutricao de Plantas, Av. Padua Dias 11, P.O. Box 9, 13408-900, Piracicaba, SP, Brazil

A R T I C L E I N F O

Article history:

Received 16 January 2009

Received in revised form 8 September 2009

Accepted 10 September 2009

Available online 12 October 2009

Keywords:

Conventional system

Inorganic nitrogen

Metabolic quotient

No-till

Pasture

Soil microbial biomass

A B S T R A C T

The Brazilian Cerrado soils were incorporated into the agricultural production process in the 1970s. The

introduction of pastures and/or annual crops utilizing different management systems produced changes

in the dynamics of soil organic matter. This study evaluated the microbial attributes of a Typic

Quartzipsamment (Arenosols in FAO classification) in native vegetation, pastures, and soybean

cultivation under conventional (CT) and no-till (NT) systems. The soil samples (0–5, 5–10 and 10–20 cm

layers) were collected in July 2005 and February 2006 from different systems: native Cerrado (CE), CT for

4 years with soybean (CT4S), CT for 4 years with soybean in rotation with millet (CT4S/M), an area that has

been under pasture for 22 years (PA22), and an area that remained under pasture for 13 years, followed

by NT with soybean in rotation with millet for 5 years (NT5). Soil inorganic N (nitrate and ammonium),

microbial C and N and basal respiration were determined. The soil metabolic quotient (qCO2) and the

Cmic:Corg ratios were calculated. The predominant form of inorganic N in the native Cerrado (CE) and in

the pasture area (PA22) was ammonium, while the conventional system (CT4S/M) and no-till system

(NT5) areas presented higher nitrogen availability for crops in the form of nitrate. The microbial C and N

concentrations increased in the wet season, and the highest values were found in the Cerrado (CE) and in

pasture (PA22) areas, where the permanent soil cover and the lack of soil disturbance by agricultural

practices allowed more favorable conditions for microbial development. The CT4S area presented the

highest qCO2 index and the lowest Cmic:Ctotal ratio, indicating that the conversion of total carbon into

microbial carbon is less efficient in this system. Since sandy soils are more susceptible to degradation, the

use of more conservationist management systems promotes more favorable conditions to microbial

development and maintenance.

� 2009 Elsevier B.V. All rights reserved.

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1. Introduction

The deforestation of the Brazilian Cerrado started taking placein the 1970s as a consequence of the growing demand for newagricultural areas. Soils were initially occupied by pastures, andlater used for cropping (Ferreira et al., 2007). An area of over 12million hectares is cultivated with annual crops under differentsystems of soil management (Bayer et al., 2004).

The conversion of Cerrado to pastures and croplands is, for themost part, made by the slash-and-burn process, which causes majorimpacts on soil fertility. To improve soil cultivation conditions, rice isgenerally cultivated from 1 to 3 consecutive years before theestablishment of annual crops. Rice crops are also used to correct soilacidity and reduce the costs of forage grass (Vilela et al., 2002).

* Corresponding author. Tel.: +55 19 3429 4727; fax: +55 19 3429 4726.

E-mail address: lafrazao@esalq.usp.br (L.A. Frazao).

0167-8809/$ – see front matter � 2009 Elsevier B.V. All rights reserved.

doi:10.1016/j.agee.2009.09.003

Substantial changes in land use and soil management in theCerrado region were initiated in the 1980s. In order to improve soilconservation, maintain and increase crop productivity, a number ofpractices were introduced, such as the elimination of crop residuescaused by burning, the adoption of conservation tillage, and themanagement of crop residues (Mielniczuk et al., 1983). As aconsequence, the soil organic matter (SOM) increased not only dueto the reduction of losses caused by biological decomposition anderosion but also due to the increase of plant residues on the soilsurface (Bayer et al., 2000).

It is widely known that SOM improves soil structure (Fellerand Beare, 1997) and regulates soil biological activity (Bayer andMielniczuk, 1999) in addition to its role in water holdingcapacity and soil fertility maintenance (Dick, 1983). Thedynamics of SOM differs in clayey and sandy soils and it ishighly influenced by different management practices andclimate conditions in each region. The stocks of SOM decreasewhen the soil is exposed to intensive tillage systems because of

Table 1Soil physical and chemical characteristics (0–10 cm depth) in a sandy Brazilian Cerrado soil under different land uses and soil management systems.

Characteristics Systemsa

CE CT4S CT4S/M PA22 NT5

Bulk density (g cm�3) 1.33C 1.40BC 1.44ABC 1.53A 1.51AB

Clay content (g kg�1) 60C 50C 120A 50C 80B

pH H2O 6.01D 6.80A 6.26CD 6.48 BC 6.75AB

pH KCl 4.12C 6.30A 5.73B 5.75B 6.35A

H + Al (mmolc dm�3) 41.00A 14.10C 22.60BC 24.60B 14.30C

Al3+ (mmolc dm�3) 11.03A 0.51C 0.70C 4.05B 0.50C

CEC (mmolc dm�3) 43.35A 37.05AB 40.74A 27.87B 37.34AB

Available P (mg dm�3) 4.40B 8.70AB 5.10B 4.5B 17.70A

K+ (mmolc dm�3) 0.35B 0.55AB 0.64A 0.27B 0.74A

Ca2+ (mmolc dm�3) 1.00C 19.00A 9.80B 1.70C 17.60A

Mg2+ (mmolc dm�3) 1.00C 3.40B 7.70A 1.30C 4.80B

BS (%) 5.70C 61.43A 44.77B 11.67C 61.79A

The values represent the mean (n = 5). Means followed by the same letter for each attribute are not significantly different by the Tukey test (p<0.05).a CE: native Cerrado; CT4S: CT with soybean for 3 years; CT4S/M: CT with soybean/millet for 3 years; PA22: pasture for 22 years; NT5: NT with soybean/millet for 5 years.

Fig. 1. Monthly rainfall distribution for the period of July 2005 through June 2006,

and the 15-year average (1990–2005) in Comodoro, Mato Grosso State.Source:

Comodoro (2007).

L.A. Frazao et al. / Agriculture, Ecosystems and Environment 135 (2010) 161–167162

increasing losses caused by water erosion and microbialoxidation (Silva et al., 1994). However, little information isavailable about the effects of agricultural management practiceson the dynamics of SOM in the Cerrado region. In the same way,there is no information on the biological attributes of sandy soilssuch as microbial biomass. As far as Oxisols are concerned,studies showed a decrease in microbial attributes in managedsystems compared to the native systems (Neill et al., 1995;Roscoe et al., 2000; Matsuoka et al., 2003).

Microorganisms play a key role in SOM decomposition. Whentheir diversity or abundance is reduced, the nutrient cycling can behighly affected (Giller et al., 1998). The soil microbial community isgenerally influenced by variations in soil temperature, watercontent and aeration, rupture of aggregates, decrease in soil cover,nutrient availability, and organic substrates. These factors can bemodified by soil management systems as a function of crop residueincorporation and soil disturbance intensity (Vargas and Scholles,2000). Soil microorganisms present a high potential for use in soilquality assessments due to their abundance, biochemical andmetabolic activity, providing faster responses to environmentalchanges (Araujo and Monteiro, 2007).

Mineralization of organic N to ammonium (NH4+-N) takes

place through microbial transformation processes and it isthe main form in which N is made available for crops. Thepredominant form of mineral N in the native Cerrado and pasturesoils is NH4

+-N, with low nitrification rates (Nardoto andBustamante, 2003). However, the amount of nitrate (NO3

�-N)can exceed the amount of NH4

+-N when annual crops areintroduced (D’Andrea et al., 2004).

The soil microbial biomass (SMB), the living fraction of soilorganic matter, represents 1–4% of the soil organic carbon (C)(Anderson and Domsch, 1990; Sparling, 1992), 2–6% of the soiltotal nitrogen (N) (Jenkinson, 1998), and it is an N reservoir forplants. Nutrient release and immobilization depends on themicrobial dynamics, the quantity and quality of plant residues,on the carbon cycling and use efficiency of the soil microbialcommunity (Baudoin et al., 2003). Managed systems influencemicrobial C and N concentrations and conventional tillage reducesthe soil microbial biomass and microbial activity (Roscoe et al.,2000; Figueiredo et al., 2007). Due to its sensitivity to changesoccurring in the soil, SMB is considered to be a good soil qualityindicator (Jackson et al., 2003).

The objective of this study was to evaluate the effect ofconverting native Cerrado to pasture and agricultural systems inmicrobial attributes of a sandy soil and determine the changesrelated to soil management and climate seasonality in the Cerradoregion, in the State of Mato Grosso, Brazil.

2. Materials and methods

2.1. Study area

The field experiment was conducted in Santa Lurdes and SantaTereza farms (138500S, 598370W) located in Comodoro, in the Stateof Mato Grosso, Brazil. The soil type in both locations is a TypicQuartzipsamment (Neossolo Quartzarenico, under the Brazilianclassification, and Arenosols under FAO’s classification) withphysical and chemical characteristics as presented in Table 1.According to the Koppen classification, the local climate is Aw(Tropical Rainy) with rainfall concentration in the Summer(October through April). The dry season is well defined duringthe Winter (May through September). The mean annual rainfall forthe previous 15 years was 1900 mm year�1 (Fig. 1) and the meantemperature was 26 8C (Comodoro, 2007).

The study areas were selected taking into considerationrepresentative criteria of land use history and soil texture as theTypic Quartzipsamment was recently incorporated into theprocess of grain production in the Cerrado areas. In March 2005,the areas were seeded with soybean and fertilized with400 kg NPK ha�1 and 100 kg KCl ha�1.

The experiment consisted of five treatments with areas of100 m2 each, with completely randomized design:

� Native Cerrado (CE): reference situation, with a sensu stricto

typical Cerrado floristic composition, tree coverage of 50% andnative soil conditions.� Conventional tillage for 4 years (CT4S): after forest clearing, the

area was cultivated with rice (Oryza sativa L.) for 1 year and withsoybean (Glycine max L.) for 3 years under conventional tillage(CT).

Fig. 2. Soil water content (0–10 cm depth) in July (2005) and February (2006) in a

sandy Brazilian Cerrado soil different land and soil Management systems. The

values represent the mean (n = 10) �standard deviation.

L.A. Frazao et al. / Agriculture, Ecosystems and Environment 135 (2010) 161–167 163

� Conventional tillage for 4 years (CT4S/M): the area was cultivatedwith rice (O. sativa L.) for 1 year under CT, and with a cropsuccession of soybean (G. max L.) and millet (Pennisetum glaucum

L.) for 3 years.� Pasture (PA22): the area was cultivated with rice (O. sativa L.) for

1 year under CT and then occupied for 22 years with a lowproductivity pasture (Brachiaria decumbens Stapf.) withoutreplanting.� No-till for 5 years (NT5): the area was cultivated with rice for (O.

sativa L.) 1 year under CT, followed by 13 continuous years ofpasture, and then followed by 5 years of crops succession withsoybean (G. max L.) and millet (P. glaucum L.) under the no-tillsystem (NT).

2.2. Soil sampling and analytical procedures

With the purpose of verifying the influence of seasonal changesand different plant covers on the systems studied, soil sampleswere collected (0–5, 5–10 and 10–20 cm depth) in July 2005 (dryseason) and in February 2006 (rainy season). Five replicate soilsamples were collected from each treatment. Samples used formineral N (NH4

+ and NO3�) determination were bulked, and sieved

(2 mm sieve) to remove roots and gravel within 24 h of collection.Inorganic N was determined from 2 M KCl extractions (1:5 soilsolution ration). After a 24-h-incubation at a constant temperatureof 25 8C, this extract was filtered and preserved with phenylmercuric acetate at a final concentration of 0.5 mg L�1. Ammo-nium-N (NH4

+-N) and nitrate-N (NO3�-N) pools in the extraction

solution were determined colorimetrically using an automatedflow injection system (Ruzicka and Hansen, 1981) coupled with aconductivitymeter and a spectrometer. The NH4

+-N was analyzedwith a conductivitymeter using the Solorzano method, and theNO3

�-N was determined colorimetrically as NO2�-N following a

reduction with a cadmium catalyst (Neill et al., 1997). Thedetection limits were 0.10 mg L�1 for NH4

+-N and 0.010 mg L�1 forNO3

�-N.To determine soil microbial biomass and basal respiration,

subsamples were collected using a grid pattern at five pointswithin a 100 m2 quadrant for each treatment. The soil subsamplesfrom each treatment were bulked and thoroughly mixed in aplastic bag, and a composite sample was taken. The compositesamples, in five replicates for each treatment, were transported onice, in a cooler, to the laboratory. Field moist soils were sievedthrough a 2 mm screen, and immediately stored in sealed plasticbags at 4 8C.

The samples used for microbial biomass and determination ofsoil basal respiration (SBR) were adjusted to 55% of the fieldcapacity, considered the ideal soil water content for studyingmicrobial activity responses. The soil microbial biomass wasestimated by the fumigation–extraction method proposed byVance et al. (1987). Fumigated and non-fumigated soil sampleswere extracted with 0.5 M K2SO4 for 30 min (1:5 soil:extractionratio), filtered, and the aliquot was analyzed. The microbial Cconcentration in the extracts was obtained by a SHIMADZU TOC5000-A equipment. The microbial N was determined by theninhydrin reactive compound quantification method (Joergensenand Brookes, 1990) using the conversion factor kEN = 0.65(Sparling et al., 1993).

Soil basal respiration was obtained from measurement ofdioxide carbon (CO2) released from laboratory incubation at 25 8Cof 100 g moist soil in a 300 ml sealed jar wrapped in aluminumpaper to promote dark conditions. The released CO2 was capturedby a standard NaOH solution (0.5 mol L�1). The calibration methodassumes that a NaOH solution partially neutralized by CO2 may becompared to a mixture of standard solution of NaOH and Na2CO3.An aliquot of 20 ml of 0.50 mol L�1 NaOH was used for CO2

absorption, and a 0.25 mol L�1 Na2CO3 standard solution wasprepared to simulate the complete neutralization of the NaOHsolution by 220 mg CO2. Carbon dioxide released was quantified bythe electrical conductivity method (Rodella and Saboya, 1999).

The metabolic quotient (qCO2) was determined by the ratiobetween the basal respiration (mg CO2-C kg�1 of air-driedsoil day�1) and microbial C (g C kg�1 of air-dried soil).

2.3. Statistical analysis

This study was carried out in a completely randomized designwith five replicates and the data were submitted to the analysis ofvariance using the SAS program (SAS Institute, 1999). The meanswere compared by the Tukey test (p < 0.05) for each depthsampled and for each treatment between the sampling periods.

3. Results

The conversion of Cerrado into agricultural systems producedchanges in the physical and chemical characteristics of the soil(Table 1). Soil compaction was observed in the PA22 whencompared to CE. The lowest pH, available P, K, Ca and Mg valueswere observed in the pasture area, which had not been replantedand fertilized since its establishment. The CT and NT areaspresented improved soil fertility as compared to CE, with reducedsoil potential acidity and increased soil base saturation (BS) (Frazaoet al., 2008).

The period between May and September is characterized by lowrainfall in Comodoro (Mato Grosso State), while the periodbetween October and April is characterized by intense rainfall(Fig. 1). As expected, the soil water content was the highest in theFebruary 2006 sampling for all systems (Fig. 2).

3.1. Soil inorganic N

The NH4+-N quantities in all situations varied between 1.53 and

5.87 kg ha�1 in July 2005 and between 0.57 and 1.89 kg ha�1 inFebruary 2006 (Table 2). The only statistically significant (p < 0.05)differences in those two periods were found in the sampling data ofthe 0–5 cm layer, which may have resulted from the high standarddeviation in each situation studied. The highest values, in relationto the CE, were obtained in CT4S, PA22 and NT5. These three areaspresented a reduction in NH4

+-N concentrations in the rainyseason (February 2006).

Taking into account all the situations and depths studied,the NO3

�-N quantities varied between 0.05 and 3.94 kg ha�1 inJuly 2005 and between 0.04 and 1.73 kg ha�1 in February 2006(Table 2). In July 2005, the highest values in relation to the CEwere obtained in CT4S/M for all depths. All the areas, exceptfor the PA22, presented higher values than CE in the February2006 sampling. The CT4S/M was the only area where a reduction

Table 2Ammonium-N (NH4

+-N) and nitrate-N (NO3�-N) quantities and NH4

+-N: NO3�-N ratios in a sandy Brazilian Cerrado soil under different land uses and soil management

systems.

Systemsa NH4+-N (mg kg�1) NO3

�-N (mg kg�1) NH4+-N:NO3

�-N

July February July February July February

0–5 cm

CE 2.34Ba 1.53ABa 0.08Ba 0.06Ba 30.7 27.1

CT4S 3.75Aa 1.23ABb 1.06ABa 0.49Aa 3.5 2.5

CT4S/M 2.29Ba 2.18Aa 3.42Aa 0.10Bb 0.7 20.9

PA22 3.94Aa 0.82Bb 0.22Ba 0.24Aba 18.2 3.4

NT5 4.82Aa 0.79Bb 0.67ABa 0.51Aa 7.2 1.5

5–10 cm

CE 2.35Aa 0.93Aa 0.09Ba 0.03Ba 27.1 28.5

CT4S 2.52Aa 1.50Aa 0.75Ba 1.08Aba 3.4 1.4

CT4S/M 2.37Aa 2.57Aa 3.70Aa 1.53Ab 0.6 1.7

PA22 2.82Aa 1.40Aa 0.18Ba 0.63Aba 15.3 2.2

NT5 3.74Aa 1.53Aa 0.45Ba 1.17Aba 8.3 1.3

10–20 cm

CE 1.71Aa 0.86Ab 0.13Ba 0.06Ba 12.8 28.5

CT4S 2.41Aa 0.96Ab 1.07Ba 0.88Aba 2.3 1.1

CT4S/M 3.84Aa 1.10Ab 2.68Aa 0.82ABb 1.4 1.3

PA22 3.71Aa 0.64Ab 0.20Ba 0.10Ba 18.1 6.5

NT5 3.99Aa 0.91Ab 0.47Ba 1.18Aa 8.5 0.8

The values represent the mean (n = 5) for the samples collected in July 2005 (dry season) and February 2006 (rainy season). Means within each column of the same depth

followed by the same capital letter are not significantly different by the Tukey test (p<0.05). Means between sampling times within each row followed by the same small

letter are not significantly different by the Tukey test (p<0.05).a CE: native Cerrado; CT4S: CT with soybean for 3 years; CT4S/M: CT with soybean/millet for 3 years; PA22: pasture for 22 years; NT5: NT with soybean/millet for 5 years.

L.A. Frazao et al. / Agriculture, Ecosystems and Environment 135 (2010) 161–167164

in N-NO3� concentrations was observed during the rainy season,

in February 2006.The predominant inorganic N form down to 20 cm depth in CE

in the two sampling periods and PA22 in the July 2005 sampling,and 0–5 cm layer in CT4S/M in the February 2006 sampling wasammonium (NH4

+-N), with nitrate (NO3�-N) quantities close to

zero, indicating a high NH4+:NO3

� ratio (Table 2).

3.2. Total and microbial soil C and N

Considering all the areas and soil depths studied, the totalcarbon (C) concentration varied between 3.40 and 7.50 g kg�1, and

Table 3Total carbon (C) and (N) concentrations, microbial C (Cmic) and N (Nmic) concentrations an

management systems.

Systemsa C N Cmic (mg kg�1)

(g kg�1) July February

CE 6.74A 0.39B 101.4ABb 443.0Aa

CT4S 4.66B 0.36B 30.6Bb 212.1Ca

CT4S/M 7.50A 0.46A 111.0Ab 360.2Aba

PA22 4.52B 0.38B 113.9Ab 384.0Aa

NT5 4.82AB 0.40AB 69.7ABb 245.7Bca

CE 4.39C 0.33B 66.5Bb 237.2Ba

CT4S 4.80BC 0.33B 54.6Bb 235.0Ba

CT4S/M 7.35A 0.46A 40.6Bb 283.8Aba

PA22 4.02C 0.35B 160.9Ab 379.5Aa

NT5 5.15B 0.40AB 78.3Bb 295.8Aba

CE 3.58C 0.23C 113.2ABb 307.9Aa

CT4S 4.40AB 0.30B 33.6Cb 297.0Aa

CT4S/M 6.43A 0.40A 85.9BCb 224.9Bca

PA22 3.40C 0.24C 147.9Ab 247.5Aba

NT5 4.29BC 0.32AB 61.6BCb 187.1Ca

The values represent the mean (n = 5) of the samples collected in July 2005 (dry season)

2005 sampling. Means within each column of the same depth followed by the same capi

sampling times within each row followed by the same small letter are not significantla CE: native Cerrado; CT4S: CT with soybean for 3 years; CT4S/M: CT with soybean/mil

the total nitrogen (N) concentration varied between 0.23 and0.46 g kg�1 (Table 3). The highest values of these elements wereobserved in CT4S/M, since this situation was located in an area withhigher clay content than the other areas.

The microbial carbon (Cmic) presented values between 30.6 and160.9 mg kg�1 in July 2005 and between 187.1 and 434.0 mg kg�1

in February 2006 (Table 3). In the first sampling, the PA22 and CT4S/

M areas presented higher Cmic concentration in the 0–5 cm layerthan the CT4S area, which had no soil cover in that period.

Comparing all the situations in the 5–10 and 10–20 cm layers,the PA22 area presented higher Cmic concentrations, except for thelast layer of the CE area. The values varied less in February 2006,

d Cmic:Nmic ratios in a sandy Brazilian Cerrado soil under different land uses and soil

Nmic (mg kg�1) Cmic:Nmic

July February July February

0–5 cm

14.1Aa 52.7Aa 6.8Aa 7.9Aa

4.0Bb 21.0Ba 8.4Aa 10.5Aa

15.6Ab 30.3Ba 6.5Ab 11.7Aa

14.4Ab 34.9ABa 9.0Aa 11.3Aa

11.4Abb 22.0Ba 7.8Aa 9.4Aa

5–10 cm

10.8Abb 36.0Aa 6.6Ba 8.7Aa

5.2Cb 16.8Ba 10.9ABa 12.3Aa

7.1BCb 29.1Aa 6.3Ba 9.9Aa

13.0Ab 29.9Aa 12.6ABa 12.1Aa

4.7Cb 35.8Aa 16.8Aa 9.2Ab

10–20 cm

9.8 BCb 25.1ABa 11.4Aa 11.7Aa

3.2Cb 19.3Ba 7.5Aa 12.1Aa

10.8Abb 33.3Aa 10.2Aa 8.9Aa

13.7Ab 22.7Ba 9.7Aa 9.1Aa

8.4BCb 18.1Ba 7.8Aa 7.5Aa

and February 2006 (rainy season). The C and N concentrations refer only to the July

tal letter are not significantly different by the Tukey test (p<0.05). Means between

y different by the Tukey test (p<0.05).

let for 3 years; PA22: pasture for 22 years; NT5: NT with soybean/millet for 5 years.

L.A. Frazao et al. / Agriculture, Ecosystems and Environment 135 (2010) 161–167 165

but higher Cmic concentrations were observed in the PA22 and CEareas in relation to CT4S in the 0–5 cm layer.

When focusing on the sampling time, considering eachsituation and the soil depth, the February 2006 sampling hadthe highest Cmic concentrations (p < 0.05) (Table 3).

Taking into account all the situations and soil depths studied,the microbial N (Nmic) varied from 3.2 to 15.6 mg kg�1 in July2005 and between 16.8 and 52.7 mg kg�1 in February 2006(Table 3). The CT4S area presented lower values in the 0–5 and5–10 cm layers as compared to the CE on both samplingoccasions. In July 2005, the PA22 area also presented highervalues than CT4S in all depths.

Similarly to the Cmic data, when considering all situations andsoil layers, there were statistically significant differences (p < 0.05)between the sampling times for Nmic, with higher values inFebruary 2006, when an increase in soil moisture was observed.

The average C:N ratio of the SMB was between 6.3 and 16.8 inJuly 2005 and between 7.5 and 12.3 in February 2006 (Table 3).There were statistically significant differences (p < 0.05) betweenthe situations studied only in the 5–10 cm layer in July 2005, inwhich NT5 area presented a higher C:N ratio than CE and CT4S/M.The CT4S/M area in the 0–5 cm layer and NT5 area in the 5–10 cmlayer presented statistically significant differences betweensampling times.

The values obtained for the Cmic:Corg ratio varied between 0.6(CT4S/M) and 4.2% (PA22). The pasture system presented a higherratio than the native system in the 5–10 cm layer (Table 4). TheNmic:Ntotal ratio varied between 1.1 (CT4S) and 5.6% (PA22)(Table 4). The highest values for this ratio were observed in theCE and PA22 areas.

3.3. Soil basal respiration and qCO2

In the July 2005 sampling, the SBR rates were homogeneous inthe situations studied while a higher soil respiration was observedin the CE area in February 2006 (Table 4). Considering the soildepths studied, the respiration rates along the soil profile weresimilar, regardless of the management system adopted.

In July 2005, the qCO2 varied between 1.31 and 5.37 mg C-CO2 g Cmic day�1 while in February 2006 this index was between

Table 4Cmic:Corg and Nmic:Ntotal ratios, soil basal respiration (SRB) rates and metabolic quoti

management systems.

Systemsa Cmic:Corg Nmic:Ntotal SBR (

(%) July

CE 1.5AB 3.8A 188Ab

CT4S 0.7B 1.2B 202A

CT4S/M 1.3AB 2.8AB 192A

PA22 2.5A 3.8A 199A

NT5 1.4AB 2.9AB 197A

CE 1.6B 3.4A 200A

CT4S 1.7B 1.6B 207

CT4S/M 0.6C 1.2B 192

PA22 3.9A 3.8A 206

NT5 1.5B 1.2B 212

CE 3.2A 4.2A 195Ab

CT4S 0.9C 1.1C 203A

CT4S/M 1.6B 2.5B 191A

PA22 4.2A 5.6A 212A

NT5 1.5B 2.6B 201A

The values represent the mean (n = 5) of the samples collected in July 2005 (dry season) an

2005 sampling. Means within each column of the same depth followed by the same capi

sampling times within each row followed by the same small letter are not significantla CE: native Cerrado; CT4S: CT with soybean for 3 years; CT4S/M: CT with soybean/mill

0.25 and 1.26 mg C-CO2 g Cmic day�1. Comparing the data betweensampling times for a given situation and depth, the highest qCO2

values (p < 0.05) were observed in July 2005.

4. Discussion

4.1. Soil inorganic N availability

The results showed evidences of less NO3�-N in the CE and in

the PA22, indicating that the ion’s availability in the soil increaseswhen annual crops and use of fertilizers are introduced. This smallamount of NO3

�-N may be an indicator of a loss of this ion byleaching process due to small quantities of clay in this areas,denitrification and microbial immobilization of fertilizer applied aswell as an opportunity for the interaction between these factors(Amado et al., 2000). Another important characteristic is thedependency of the leaching on the soil type. Studies show thatsandy soils are more susceptible to leaching than clay soils (Niederet al., 1995; Beaudoin et al., 2005).

Studies developed on a forest to pasture conversion in a Ultisol,Neill et al. (1995) reported that the predominant inorganic N formin the pasture system was NH4

+-N. Various other studiesconducted in different types of soil in the Amazon showed similarresults (Piccolo et al., 1994; Neill et al., 1999; Passionato et al.,2003; Cerri et al., 2006).

Consistently with the data of this study, Carvalho (2006)verified that ammonium was the predominant inorganic N form ina Oxisol under different management systems in the Cerradoregion (Rondonia State). The CT4S/M situation presented the lowestNH4

+:NO3� ratio in July 2005, while the CT4S presented the highest

ratios in February 2006. This result indicates that these systemsincreased the availability of N-NO3

� for crops. D’Andrea et al.(2004) also reported higher values for nitrate than for ammoniumin annual crop systems in a Oxisol in the Cerrado region in the Stateof Goias.

4.2. Factors affecting soil microbial C and N concentrations

The permanent soil cover, as observed in the CE and PA22 areas,is an important factor for microbial maintenance with direct

ents (qCO2) in a sandy Brazilian Cerrado soil under different land uses and soil

mg CO2-C kg�1 soil day�1) qCO2 (mg CO2-C g Cmic day�1)

February July February

0–5 cm

254Aa 1.96Ba 0.68ABb

a 190ABa 5.37Aa 0.93Ab

a 105Bb 1.87Ba 0.30Cb

a 95Bb 2.00Ba 0.25Cb

a 102Bb 2.42Ba 0.39BCb

5–10 cma 268Aa 3.35Aa 1.26Ab

Aa 156ABa 3.62Aa 0.67Bb

Aa 108Bb 2.41ABa 0.39Cb

Aa 99Bb 1.31Ba 0.25Cb

Aa 113Bb 2.83ABa 0.40Cb

10–20 cm

253Aa 2.06Ba 1.16Ab

a 145Ba 4.37Aa 0.63ABb

a 108Bb 1.97Ba 0.43Bb

a 93Bb 1.51Ba 0.38Bb

a 116Bb 3.61ABa 0.64ABb

d February 2006 (rainy season). Cmic:Corg and Nmic:Ntotal ratios refer only to the July

tal letter are not significantly different by the Tukey test (p<0.05). Means between

y different by the Tukey test (p<0.05).

et for 3 years; PA22: pasture for 22 years; NT5: NT with soybean/millet for 5 years.

L.A. Frazao et al. / Agriculture, Ecosystems and Environment 135 (2010) 161–167166

impacts on the microbial C and N concentrations. Studies onannual crops in Oxisols demonstrated a reduction in microbial Cand N in these systems, as compared to the native Cerrado(Oliveira, 2000; Matsuoka et al., 2003).

The CT4S area had no plant cover in July 2005. This may explainthe low microbial C and N values Studies of different managementsystems provide evidence for microbial C reduction in CT whencompared to native vegetation (Roscoe et al., 2000; Matsuokaet al., 2003). This may result from the more favorable conditionsfor microorganisms as the soil is in its natural condition,undisturbed, and with its floristic diversity and soil fungalhyphae preserved. The reduction of the more active SOM fractionaffects the soil functions, which is fundamental far the aggrega-tion process, such as the maintenance of polysaccharide produc-tion (Golchin et al., 1997).

The pasture system (PA22) presented higher microbial C and Nconcentrations, with higher values than the CT and NT in somedepths. The results associated to the lower NO3

�-N values areindicative of N immobilization in this system (Vargas et al., 2005).It is important to highlight that this area has not been reformed for22 years and, according to Perez et al. (2005), the rate of Nmic

cycling is directly proportional to its concentration in the soil.The microbial C and N values can decrease or increase

depending on the type of crop (Conti et al., 1997), since Nfertilization and allocation to residue decomposition cause the soilmicrobial population activity to decrease. As the NT5 area had beenestablished recently, it did not present higher microbial C and Nvalues than the CT area under crop rotation (CT4S/M).

The soil water content is an important factor to consider as it isdirectly related to the soil microbial activity. Other studiesconducted in the Cerrado region are in agreement with the datapresented, with higher Cmic as soil water content increases(Nardoto and Bustamante, 2003; Gama-Rodrigues et al., 2005;Carvalho, 2006). The increase in Cmic and Nmic with higher soilwater content was also reported by Carvalho (2006) in an Oxisol inVilhena (Rondonia State).

Considering the high standard deviation in the situation means,the variations in Cmic and Nmic values are due to the influence ofseasonal differences, which increase as a direct result of the soilwater content. Several studies report the influence of seasonalfluctuations caused by the interaction between the soil watercontent and temperature, soil organic matter, soil texture, plantgrowth and other factors (Wardle and Parkinson, 1990; Kaiseret al., 1992; Srivastava, 1992; Wardle, 1992; Espindola et al., 2001).

The Cmic:Corg ratio is an index of the accumulation potential ofmicrobial biomass carbon relative to the organic carbon (Sparling,1992; Rodrigues, 1999) that can be used in the evaluation ofchanges caused by agricultural practices (Wardle, 1992). TheNmic:Ntotal ratio represents the mineralizable N fraction, i.e., itexpresses the potential of inorganic N available in the soil for thenext crop (McGill et al., 1988).

The values obtained for the Cmic:Corg ratio indicated higherefficiency in the conversion of organic C into microbial C in thepasture area (Alvarez et al., 1995; Xavier et al., 2007). The higherNmic:Ntotal values in the CE and PA22 areas represent higherinorganic N cycling efficiency and availability in the medium term(Xavier et al., 2007).

4.3. Soil basal respiration (SBR) and qCO2

The SBR results obtained in the Typic Quartzipsamment variedfrom the results reported by Alvarez et al. (1995), Balota et al.(1998), Mendes et al. (1999) and Vargas and Scholles (2000) indifferent soil types. Those authors observed a uniform release of C-CO2 in the 0–20 cm layer under CT, and higher levels for NT andreduced soil tillage surface layers. In this study, since the soil

texture is sandy, the SBR showed no differences among the systemsevaluated.

The respiration rate alone is not sufficient as an indicator toexplain the distinct behaviors between the situations studied. Highrespiration rates do not always indicate favorable conditions, sincethey signify rapid nutrient release for plants, as well as soil totalorganic C losses in the long term (D’Andrea, 2001).

The metabolic quotient (qCO2) is important to evaluate theeffect of the environmental conditions on the microbial population(Anderson and Domsch, 1990). In this study, the qCO2 was relevantto the analysis of the differences between different land usesystems. The index indicates the SBR rate by microbial carbon(Cmic) units. The results showed evidence of variations between thesituations and sampling times. The results indicated a high indexvalue in the CT4S system. According to Balota et al. (1998), the qCO2

decreases in more stable agroecosystems, but increases whenplant cover is removed and replaced, as plant residue decomposi-tion rates increase (Ocio and Brokes, 1990).

Due to the low Cmic values in July 2005, higher qCO2 values wereexpected, since there is an inverse relation between qCO2 and Cmic

(Prasad et al., 1994; Balota et al., 1998, 2004; Moreira and Malavolta,2004). The increase in soil water content in February 2006 favoredthe Cmic increase, and consequently the qCO2 decrease.

5. Conclusions

Changes in the land use for agricultural purposes in the Cerradousing different soil management systems promote alterations inthe microbial components of soil. The largest variations in theobserved values can be attributed more to climatic seasonalitythan to differences in the management systems.

Ammonium was the predominant inorganic N form in thenative Cerrado and pasture areas. The conventional tillage and no-till systems presented the highest nitrate values, indicating highernitrogen availability for crops in these systems, especially withcrop succession.

The microbial C and N concentrations also varied with climateseasonality.Thehighestvalues werefoundintheCerradoandpastureareas. The permanent soil cover and the lack of soil disturbance withthe absence of agricultural practices produced more favorableconditions for microbial development in those systems.

The qCO2 was higher in the dry season (July 2005) in allsituations evaluated with a higher index in the bare soil of theconventional tillage area (CT4S). The lowest Cmic:Corg ratio was alsoobtained in this area, indicating that the conversion of total C intomicrobial C is less efficient in this system.

In general, it is possible to conclude that sandy soils undernative system and agricultural practices with minimal disturbanceto the soil contribute to the adequate development and main-tenance of soil microbial attributes.

Acknowledgements

The authors thank FAPESP—Fundacao de Amparo a Pesquisa doEstado de Sao Paulo (The State of Sao Paulo Research Foundation)and CNPq—Conselho Nacional de Desenvolvimento Cientıfico eTecnologico (National Council for Scientific and TechnologicalDevelopment).

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