Spatial variability of microbial biomass and organic matter labile pools in a haplic planosol soil

Variabilidade espacial da biomassa microbiana e compartimentos lábeis da matéria orgânica de um planossolo háplico

Spatial variability of microbial biomass and organic matter labile pools in a haplic planosol soil

Variabilidade espacial da biomassa microbiana e compartimentos lábeis da matéria orgânica de um planossolo háplico

Diego Campana Loureiro^I; Helvécio De-Polli^II; Marcos Bacis CeddiaI, ^*; Adriana Maria de Aquino^II

^IUniversidade Federal Rural do Rio de Janeiro. E-mail: [e-mail]; [e-mail] ^IIEmbrapa Agrobiologia, km 7, Caixa Postal 74.505, 23890-000 Seropédica (RJ). E-mail: [e-mail]; [e-mail]

ABSTRACT

The objective of this work was to study the spatial variability of soil microbial biomass (SMB) and labile soil organic matter pools (labile SOM), under different management systems and plant cover. The experiment was conducted in a Haplic Planosol soil on an Integrated Agroecological Production System (SIPA), in Seropédica, Rio de Janeiro. The evaluated management systems were: alley cropping, pasture, and bush garden, the late one was used as reference area. Three grids of regular spacing of 2.5 x 2.5 meters were used for sampling, consisting of 25 georeferenced points each, where soil samples were taken at 0-10 cm depth. The following labile constituents of soil organic matter were determined: free light fraction (FLF), water soluble C and N, C and N of SMB (SMB-C and SMB-N), and glomalin content. The textural fractions (sand, silt, and clay), pH in water, and chemical attributes (organic C, total N, Ca, Mg, Al, P, K, and CEC-cation exchange capacity) were also determined. The areas of alley cropping and pasture showed spatial dependence to the attributes of SOM. The occurrence of high spatial dependence for the attributes associated to microbial biomass in the alley cropping system (C, FLF, SMB-N and respiration), probably was due to external factors related to management, such as: intensive rotational cropping system, diversity of crops and different inputs of organic matter to soil such as pruning material and organic compost.

Key words: organic carbon, geoestatistic, glomalin, precision agriculture.

RESUMO

O objetivo do trabalho foi estudar a variabilidade espacial da biomassa microbiana do solo (BMS) e dos constituintes lábeis da matéria orgânica do solo (MOS), sob diferentes sistemas de manejo e cobertura vegetal. O experimento foi instalado em um Planossolo Háplico no Sistema Integrado de Produção Agroecológica (SIPA), em Seropédica (RJ). Os sistemas de manejo avaliados foram: cultivo em aléias, pastagem e, horto florestal como área de referência. Para a amostragem utilizaram-se três grades regulares com espaçamento de 2,5 x 2,5 metros, composta de 25 pontos georreferenciados para cada grade, onde se coletou amostras de terra na profundidade de 0-10 cm. Em cada amostra determinaram-se os seguintes constituintes lábeis da MOS: fração leve livre, formas de C e N solúveis em água, C e N associado à BMS e teor de glomalina. Determinaram-se também as frações granulométricas areia, silte, argila, umidade gravimétrica, bem como os atributos químicos de rotina. Somente as áreas de cultivo em aléias e pastagem tiveram dependência espacial para os atributos da MOS. A ocorrência de maior dependência espacial dos parâmetros associados à BMS nas aléias (C, fração leve livre da MO, BMS-N e respiração), foi em decorrência de, provavelmente, de fatores extrínsicos relacionados ao manejo, tais como: intensa rotação e diversidade de culturas e aporte diferenciado de adubos orgânicos (material de poda e aplicação de compostos orgânico).

Palavras-chave: carbono orgânico, geoestatística, glomalina, agricultura de precisão.

INTRODUCTION

Several studies in the literature show the importance of monitoring the quantity and quality of soil organic matter (SOM) so as to produce more with less intensive use of land (SOUZA et al., 2006; HOPMANS et al., 2005; MOREIRA and MALAVOLTA, 2004; D'ANDREA et al., 2004; MARCHIORI JUNIOR and MELO, 2000). The microbial activity of soil and the fractions of labile SOM are considered important indicators of the sustainability of management systems (MALUCHE-BARETTA et al., 2006; FRAISSE et al., 1999; SWEZEY et al., 1998).

Most studies related to soil micro-biota use quantitative attributes such as soil microbial biomass (SMB), respiration and metabolic quotient (qCO₂) to establish a systematic interpretation of the quality of SOM. Other attributes of promptly metabolized fraction of SOM such as glomalin content, soluble carbon source, and free light fraction also aid in the interpretation of SOM quality. The interpretation of the interactions of these attributes can provide an indication of changes in the environment due to management practice.

Another aspect related to the study of SMB is that in most cases data are analyzed by means of classical statistics (test of means, variance, and coefficient of variation) and it is assumed that the data show normal distribution and random variance (MARTINAZZO et al., 2007; ASSISI JUNIOR et al., 2003; MARCHIORI JUNIOR and MELO, 2000; ALVARENGA et al., 1999). In general, soil attributes that are subject to temporal variation (microbial activity, moisture and soluble soil nutrients), are often subject to a high spatial variability (HALVORSON et al., 1997). In fact, attributes such as microbial biomass and labile fractions tend to an erratic behavior in the soil. However, in some cases, geostatistics analyses show spatial dependence for these attributes according to the system of management (STOYAN et al., 2000). EL SEBAI et al. (2007) found spatial dependence for microbial biomass carbon in long term wheat cropping area.

According to CARVALHO et al. (2003), the spatial variability of soil attributes can be influenced by their intrinsic factors (soil genesis, geologic origen, topography, climate, biota and time) and the extrinsic factors, normally related to the practices of management. PAZ-GONZÁLEZ et al. (2000), studying the spatial variability of soil properties (organic matter, nitrogen, phosphorus, cation exchange capacity, pH in H₂O, sand, silt, clay and gravel) in different land uses (area of natural vegetation and crop land) found that the area of natural vegetation was more diversified, providing evidence that the deforestation and long term of cropping promoted change in the pattern of spatial variability and increased the homogeneity of some soil attributes. The cultivated area presented, as beneficial changes, higher pH and Olsen-P, however, the loss of organic matter by cultivation was far from deleterious, but causes a significant CEC decrease, which was found to be the most detrimental change for sustainable soil use.

Considering that the spatial variability is important for better understanding of the relationship between management and dynamics of soil organic matter, the objective of this work was to study the spatial variability of microbial biomass and labile constituents of soil organic matter under different management systems and plant cover.

2. MATERIAL AND METHODS

The study of soil microbial biomass (SMB) and labile constituents of soil organic matter (SOM) was held in a Haplic Planosol soil on a 15-year-old Integrated Agroecological Production System (SIPA), in Seropédica, Rio de Janeiro. The management systems evaluated were: alley cropping, pasture, and bush garden as a reference area. The alley cropping system was composed of Gliricidia sepium rows of six meters apart where, until 2004, were grown in between rows several crops such as lettuce, chive, spinach, radishes, ginger, corn, and common bean. From 2005 to this sampling time tropical flowers (Heliconiaceas, Musaceas and Zingiberaceas) and black pepper were introduced. The pasture area was established in 1997 with Transvala grass (Digitaria decumbens Stent cv. Transvala). The bush garden was established in 1950 with Acacia spp., Mimosa spp., Cassia fistula, Anadenanthera sp., and palm trees.

For the study of spatial variability, in each management system, a regular grid of 100 m² (10x10 m) was settled. The sampling system used consisted of three grids of regular spacing of 2.5 meters, with 25 georeferenciated points in the UTM system with sub-metric precision (DGPS - Trimble-Pro XT model). At each point, soil samples were collected at the depth of 0-0.10 m. In each sample the following constituents of labile SOM were determined: free light fraction (FLF), forms of labile C and N soluble in water (Clab and Nlab) and content of glomalin. Besides, the textural fractions (sand, silt, and clay), pH in water, and chemical attributes (organic carbon, total N, Ca, Mg, Al, P, K, and CEC-cation exchange capacity) were also determined. The SMB and soil respiration were determined in 15 of the 25 points.

After collecting, soil samples were air dried, hand grinded, homogenized and sieved in 2.0 mm mesh for chemical, physical and biological analyses. The soil microbial biomass for carbon (SMB-C) and nitrogen (SMB-N) was determined using the method of fumigation extraction, proposed by VANCE et al. (1987) and TATE et al. (1988), with adjustments proposed by DE-POLLI and GUERRA (1999). Basal soil respiration was determined in accordance with the methodology proposed by JENKINSON and POWLSON (1976) through the quantification of the evolution of CO₂ accumulated during five days of incubation. The specific respiration or metabolic quotient (qCO₂ index) was determined according to ANDERSON and DOMSCH (1990).

The labile soil carbon and nitrogen components soluble in hot water were determined using the method of extraction in autoclave at 100 °C, adapted from SPARLING et al. (1998) and BAKER et al. (1998). The free light fraction of organic matter was obtained by the procedure proposed by SOHI et al. (2001), as suggested by JANZEN et al. (1992). The quantification of total glomalin, a glycoprotein found in mycorrhizal fungi, was performed using the test of BRADFORD (1976), modified by WRIGHT and UPADHYAYA (1998). Total glomalin-related soil protein (T-GRSP) was extracted by repeated cycles with 50 mM citrate of sodium, pH 8.0, by autoclaving at 121 ºC for 60 min. The extraction of glomalin continued until the supernatant content of glomalin was 2 mg ml^-1 (minimum level of detection). Extracts from each cycle were pooled and centrifuged at 10,000 g for 10 min to remove residual soil particles. Protein content was determined by Bradford assay (Sigma-Aldrich, Inc.) with bovine serum albumin as the standard. GRSP analyses were carried out on soil from two subsamples for each replicate.

The textural fractions (sand, silt, and clay), pH in water, and chemical attributes (organic carbon, Ca, Mg, Al, P, K, and CEC-Cation Exchange Capacity) was determined according to EMBRAPA (1997). The total N was determined by BREMNER and MULVANEY (1982).

To run the statistical analyses, first of all a descriptive analysis (minimum, maximum, mean, kurtosis, assimetry, CV, and standard error) was conducted to assess the pattern of distribution of data frequency, detecting anomalous values (Boxplot test) as well as the Pearson correlation between the variables through software XLSTAT 7.5 (ADINSOFT, 2004). GEOSTAT software (VIEIRA et al., 1983) was used to determine the spatial continuity (experimental semivariograms), to evaluating the most proper model to interpolation (cross-validation), as well as to interpolation by ordinary kriging. The maps generated by ordinary kriging covered an area of 100 m² with 1x1 m resolution. The file with interpolated data was exported to the program SURFER 7.02 (GOLDEN SOFTWARE, 2000) for better representation of the variability of attributes.

3. RESULTS AND DISCUSSION

Descriptive statistical analysis

The forest garden area presents the highest values of microbial biomass and labile constituents of soil organic matter (SOM) (Table 1). The lower range of temperature and humidity as well as the highest input of SOM, provides a more favorable environment for microbial activity and cycling of nutrients from the SOM in this kind of area (BANDICK and DICK, 1999; BOPAIAH and SHETTI, 1991; ORCHARD and COOK, 1983).

The mean of carbon content of soil microbial biomass (SMB-C) in the area of pasture is higher than in the area of alley cropping. The opposite occurs with the mean of nitrogen content in the soil microbial biomass (SMB-N), with higher values for the area of alley cropping. This result has influenced the mean of C/N ratio of the microbial biomass (C/Nmic), with lower relationship found in the alley cropping area (Table 1). This indicates higher conservation of nitrogen in this system through the incorporation of C and N in the microbial pool that can be a source of this nutrient for crops. Although the process of immobilization is sometimes considered a negative factor for crop production, in certain situations may be favorable because it is a temporary process and, therefore, consisting of potential reservoir of nutrients for plants (PAUL and CLARK, 1996). The microbial biomass has an active role on the immobilization-mineralization process increasing or reducing the availability of nutrients for plants (DUDA, 2000).

The mean of C/N ratio was higher in the area of pasture (Table 1). According to HEAL et al. (1997), this is a characteristic of this type of vegetation, with higher content of lignin, polyphenols and rigid structures. These characteristic also explain the higher amounts of free light fraction of SOM in pasture area than alley crops.

Evaluating the mean values of labile fractions (labile C, labile N and glomalin), stock of SOM (C and N) and CEC, the system of alley cropping showed higher levels than pasture and lower than forest garden (Table 1). Since the management history of the alley cropping area included soil plowing, the qCO₂ has remained higher than in areas of perennial crops (pasture and forest garden). Despite the fact that the system of alley cropping have a higher input of organic matter, reflecting positively on the stock of SOM including in its labile compartment, the efficiency of this management with intensive plowing can be questioned on the point of view of soil conservation since higher qCO₂ is an indicative of a certain instability in the C flow. Due to the above reasons, in general, the forest garden area showed higher mean value of free light fraction (FLF), stocks of SOM (C and N), CEC and labile constituents of soil organic matter (SMB-C, SMB-N, Clab, Nlab and glomalin) (Table 1).

The mean of clay content in the area of alley cropping and pasture was similar (4 and 2% respectively) being different from the orchard garden area (13%) (Table 1). It is worth emphasizing that in the area of forest garden, the highest amount of clay is strongly influenced by the occurrence of the activity of termites, which brings more material from deeper soil horizon to the surface layers. According to MOREIRA and SIQUEIRA (2002) a greater accumulation of microbial biomass is expected in soils with higher clay content (higher water and nutrient retention and less variation in temperature). Lower mean value of soil moisture (1.8%) in the pasture area (Table1) was observed. This is a consequence of its sandy texture combined with a period of low rainfall (Table 1). Similar values of soil moisture for this same area of pasture were found by VILLELA (2007).

According to WEBSTER (2001), attributes that have asymmetry ranging from 0 to around ±0.5 have normal distribution. Considering that criterion, it appears that the system of alley cropping probably presents greater number of attributes with distribution closer to the normal (SMB-C, SMB-N, labile C and N, respiration, qCO₂, C/N, soil moisture, glomalin, and CEC) (Table 1). Besides, it appears that except for sand content in the three management systems, and CEC in alley cropping, the coefficient of variation showed medium or high values (> 10%) (PIMENTEL-GOMES, 1984). The largest coefficient of variation (CV) values for the attributes related to microbial biomass and labile components of SOM are expected, since they have high sensitivity to edapho-climatic variation showing more erratic behavior.

Table 2 shows the linear correlation coefficients of Pearson (r), between the physical attributes and microbial biomass and constituents of labile SOM. In studies of spatial variability through geostatistics, the detection of significant correlation between the attributes is especially important to improve the interpolation of attributes of more difficult analyses (SMB and labile SOM) from others of easier analyses (organic carbon and texture) through ordinary co-kriging. At table 2 we can note that the organic C was the attribute, relatively easier to measure, which most significantly correlated with SMB and labile constituents (SMB-C, SMB-N, labile N and C, FLF, and glomalin), in alley crops and forest garden area. Among the systems evaluated pasture area is the one with fewer attributes for SMB and labile constituents of SOM correlated with organic C and texture. The forest garden showed greater number of values of SMB and labile SOM positively correlated with the clay content (Table 2). This behavior is expected, because in the forest garden area higher level of clay associated with the activity of termites was found, resulting also in higher values of soil CEC, specific surface, SMB and labile SOM. Although there are positive correlations between clay and SMB and labile constituents of SOM on the forest area, it should be noted that this kind of land use favors the highest levels of those attributes.

According to POWLSON et al. (1987), part of the observed variation in the quantity of microbial biomass is associated with input of organic matter to soil. From Tables 1 and 2 we can have an understanding on the variation of the attributes of microbial biomass and labile constituents of SOM. Areas with greater input of organic matter present higher values of SMB and labile constituents as well as greater correlation of these attributes with organic C.

Analysis of Spatial Variability

Table 3 shows the parameters for the models fitted to the experimental semivariograms of the attributes studied. In the area of alley cropping the attributes that showed spatial dependence were C, FLF, SMB-N and respiration, and the spherical model was fitted to these attributes. In the area of pasture C and microbial C/N ratio showed spatial dependence and the Gaussian model was fitted to these attributes. The range value for SMB-N was 5.5 m estimated by the semivariogram in the area of alley cropping (Table 3). This demonstrates high sensitivity of this variable to the applied management, where the spacing between rows of 6 m for Gliricidia, probably, influenced the pattern of spatial variability of SMB-N. Since Gliricidia is a N₂ fixing tree legume in association with rhizobium bacteria the falling leaves concentrates under-crown area generating a gradient of organic matter and SMB-N between the cropping rows.

The bush garden area did not show spatial dependence for the attributes of microbial biomass and labile constituents of SOM. The random pattern of variability of SMB and labile constituents in the area of bush garden is due, probably, to the random input to the soil of organic matter from forest litter (different species, size, and amount) where the trees were settled originally in the area in a random distribution. Also, with the soil protection provided by the trees the variation in temperature and humidity were lower reducing spots of variability in terms of soil moisture and temperature that would create extreme values of attributes that affect the SMB and the dynamics of SOM. These results corroborate with HARGREAVES et al. (2003) that studied the spatial variability of microbial biomass carbon in the jungle area converted to forest after being an arable field, also discovered that the results of the semivariogram analysis revealed no spatial dependence. PAZ-GONZÁLEZ et al. (2000) found lower nugget effect of variables Corg and cation exchange capacity (CEC) in crop area under rotational system with pasture than in areas under natural vegetation suggesting that the crop area has shows greater continuity in the semivariogram. This paper presents data similar to those found by these authors. The alley cropping area shows a higher number of variables of microbial biomass and labile components with spatial dependence and low nugget effect, indicating that the management as alley cropping is changing the pattern of spatial variability of these attributes (Figure 1).

However, the possibility of induction of spatial dependence through different managements, as the alley cropping system does not apply to all attributes related to soil organic matter. The content of glomalin, for example, did not present spatial dependence in any of managements evaluated.

Maps of spatial variability of clay, C, microbial biomass and labile constituents of SOM.

The maps of spatial variability of C, respiration, FLF, and SMB-N in the area of alley cropping are shown in Figures 2a, b and ^3a, ^b, respectively. Through visual assessment, we can see the similarity of behavior between C and SMB-N and that the respiration tends to behave in opposite manner. This pattern is most easily detected in the upper right corner of those maps, where local activities with greater microbial respiratory level present less C and SMB-N. The reverse pattern in this point of the area of alley cropping indicates that the efficiency of soil microbial activity is low and that the soil micro-organisms are under a factor of stress, since an efficient microbial biomass releases less carbon in the form of CO₂ by respiration (AQUINO et al., 2005). Regarding the FLF, it was not seen, visually, a pattern of systematic variability as seen in the other attributes.

The detection of regions with behavior directly and inversely proportional, such as C and SMB-N, and those with respiration, respectively, shows that the geostatistics tool extends the possibility of examining the phenomena in a given area.

Figure 4a, b refers to the maps of C and microbial C/N ratio (C/Nmic) respectively, in the area of pasture. There is a similar pattern of spatial variability of these attributes, or areas with higher levels of C promoted greater microbial C/N ratio. This site has been under pasture for about two decades and since then has not received other sort of management. This pattern of regular pasture cover could be the cause of the gradient of C and C/Nmic been well associated.

4. CONCLUSION

Some attributes of microbial biomass and labile constituents of soil organic matter had spatial dependence, specifically in the areas with the highest anthropogenic activity such as in alley cropping and pasture areas. Considering the relative homogeneity of soil and topography of the areas examined, this result confirms the hypothesis that selective management of soil (extrinsic factor) induces spatial variability, in this case some attributes related to soil organic matter.

ACKNOWLEDGEMENTS

To CAPES for the awarded scholarships to the first author and CNPq and FAPERJ for financial aid to the research.

Received for publication in September 18, 2008 and accepted in February 3, 2010.

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Corresponding author.

Publication Dates

• Publication in this collection
  14 Feb 2011
• Date of issue
  2010

History

• Received
  18 Sept 2008
• Accepted
  03 Feb 2010