AJCS 10(12):1623-1629 (2016) ISSN:1835-2707

doi: 10.21475/ajcs.2016.10.12.PNE164

Effects of cover crops on the physical protection of organic matter and soil aggregation

Alberto do Nascimento Silva1, Cícero Célio de Figueiredo1*, Arminda Moreira de Carvalho2, Daiane
dos Santos Soares1, Divina Cléia Resende dos Santos1, Vivian Galdino da Silva1
1
Faculty of Agronomy and Veterinary Medicine, University of Brasília (UnB), Brasília, Brazil
2
Brazilian Agricultural Research Corporation (EMBRAPA), Embrapa Cerrados, Planaltina, DF, Brazil

*Corresponding author: [email protected]

Abstract

The objective of this study was to evaluate the effects of cover crops grown under no-tillage on the aggregation and physical
protection of organic matter in soil macro and microaggregates. The experiment consisted of a randomized complete block design
with three replications. The following cover crops were investigated in corn rotation systems: T1 = Braquiária ruziziensis (Urochloa
ruziziensis), T2 = Canavalia brasiliensis Mart. ex Benth., T3 = Pigeon pea ‘BRS Mandarin’ [Cajanus cajan (L.) Millsp.], T4 = millet
‘BR05’ [Pennisetum glaucum (L.) R.Br.], T5 = turnip-forage (Raphanus sativus L.), T6 = velvet bean (Mucuna aterrima Merr.) and
T7 = native Cerrado vegetation as a reference environment. Soil was sampled at a depth of 0-10 cm in September 2015 for the
determination of organic matter fractions in macro and microaggregates. There was a reduction in aggregate size and its stability
when native Cerrado areas were converted into agricultural systems. Nevertheless, some cover crops such as velvet bean, millet and
turnip-forage favored restructuring the soil, forming stable aggregates similar to the native Cerrado. Among the cover crops, millet
was highlighted as presenting elevated capacity to accumulate labile organic carbon in macroaggregates (2.32 g C kg-1) and
microaggregates (2.34 g C kg-1). These values are, on average, 60% higher than those presented by turnip-forage. In general, the
conversion of land use under Cerrado vegetation to agroecosystems reduced the total organic carbon content, mainly due to
macroaggregate breakup, resulting in a lower physical protection of soil organic matter.

Keywords: soil organic carbon; no-tillage; Cerrado; organic matter pools; conservation tillage.
Abbreviations: C_Carbon; OM_Organic Matter; SOM_Soil Organic Matter; NTS_No Tillage System; LC_labile carbon;
MAC_Macroaggregates; MIC_Microaggregates; HS_Humic substances; FA_Fulvic Acid; HA_Humic Acid; HUM_Humin.

Introduction

Under the conditions of natural ecosystems, the formation of layers (Lima Filho et al., 2014; Ensinas et al., 2016), and
a well-defined soil structure is established over time due to consequently promotes increased stability of soil aggregates.
chemical interactions and the role of biological agents. This Cover crops in the NTS improve soil aggregation over the
good soil structure is dependent on and also protective of cultivation years and the plant species interfere differently on
organic matter (OM), representing an efficient form of carbon aggregate stability (Loss et al., 2011; Loss et al., 2014).
(C) protection in the soil. Changes to natural environments For the formation and subsequent stability of the
caused by human activities impose drastic changes to the soil aggregates, there occurs a plurality of interactions between
structure, reflecting the loss of OM and rupture of aggregates, the following factors: macro and mesofauna, soil
especially macroaggregates (Wendling et al., 2011; Winck et microorganisms, roots, inorganic agents, and environmental
al., 2014). variables (Bronick and Lal, 2005; Rillig and Mummey,
As an alternative to reduce the impacts on soil aggregation 2006). Among these factors, highlighted is the root system
promoted by the incorporation of native areas into that is directly related to aggregation and accumulation of C
agricultural ecosystems, the use of cover crops in the no- and nitrogen (N) in different classes of soil aggregates
tillage system (NTS) can reduce nutrient losses and increase (Kasper et al., 2009; Loss et al., 2015). Crops with aggressive
the content of soil organic matter (SOM) (Crusciol et al., root systems can minimize the negative effects of soil
2012; Nascente and Crusciol, 2012; Carvalho et al., 2012; degradation through improvements to its structure. However,
Ensinas et al., 2016). The SOM directly influences the information on the action of different cover crop species on
physical properties of the soil by increasing its aggregation the aggregation and accumulation SOM are still incomplete
and also promotes improvements in porosity, aeration, water (Lima et al., 2015).
infiltration and water retention in the soil (Garcia and To improve understanding of the relationship between OM
Rosolem, 2010). and soil aggregation, fractioning of the SOM and analysis of
The use of cover crops increases plant residue inputs on the the labile and recalcitrant fractions in different aggregates
surface which increases protection of the soil, reducing classes has been performed (Bimüller et al., 2016). Among
erosion (Guedes Filho et al., 2013). In addition to increasing the most recalcitrant fractions, humic substances are
the SOM, plant residues on the soil surface serve as a important in the process of formation and stability of
substrate for microbial activity, mainly in the upper soil aggregates due to its cementing action, which allows the

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formation of stable aggregates in water (Borges et al., 2015; protection provided by the plant residues of different soil
Gazolla et al., 2015; Li et al., 2015). In the case of Latosols covers, which protect the soil against disaggregation caused
from the Brazilian Cerrado, the presence of microstructures by the impact of rain and sudden changes in humidity. In
may represent an important form of protection to the OM and addition, the decomposition of cover plant residues enhances
they are generally neglected in evaluations of OM alterations microbial activity, the accumulation of nutrients and organic
promoted by soil management systems. matter on the soil surface layers, which favors greater
There are few studies that relate the use of different cover stability of the aggregates (Lima Filho et al., 2014).
plant with the formation of aggregates and the protection of
SOM. The hypothesis tested in this study was that different Effect of cover crops on the organic carbon fractions of the
species of cover crops differently alter the stability of soil in macro and microaggregates
aggregates and the physical protection of SOM. In this
context, the objective of this study was to evaluate the In general, the main form of labile carbon (LC) and total
influence of different cover crops in a long term no-tillage organic carbon (TOC) accumulation was observed in
system on the aggregation and protection of organic carbon in microaggregates (MIC) (Table 2). On average, the
soil macro and microaggregates. accumulation of LC and TOC in the macroaggregates (MAC)
was 21% and 31% higher, respectively, than in the MIC. This
Results and Discussion increased C accumulation in the MAC may be due to use of
the NTS, characterized by the absence of soil disturbance
Effect of cover crops on aggregate stability (Figueiredo et al., 2010). Similar results were obtained by
Costa et al. (2012).
The effects of different cover crops on the formation and The sequence of LC accumulation in the MIC by the cover
stability of aggregates, measured by the weighted average crops followed the following order: P. glaucum >native
diameter (WAD) and the aggregate stability index in water Cerrado= C. cajan = M. aterrima > R. sativus = B.
are shown in Figures 1 and 2. The WAD ranged from 0.91 ruziziensis. C. brasiliensis did not differ from M. aterrima, C.
mm in C. cajan to 1.5 mm in the native Cerrado (Figure 1). cajan, B. ruziziensis and R. sativus. Higher LC levels are
Three distinct groups were formed with regards to capacity of usually observed in areas where there is greater MOS input
the plants to form aggregates: the native cerrado vegetation from the crop residues (Leite et al., 2003). LC accumulation
presented the highest values, M. aterrima, R. sativus, B. is also influenced by the chemical composition of the ground
ruziziensis and P. glaucum had intermediate capacity, and C. cover crops (Silva and Mendonça, 2007; Zhongkui et al.,
cajan and C. brasiliensis indicated the lowest capacity. 2010). The addition of LC may be attributed to the
The largest WAD values in the area with native Cerrado are production plant residues with lower C/N and lignin/N ratios,
due to the higher quantity of plant material in that area and which more rapidly decompose and promote the increase of
the total absence of soil disturbance. The differences among this fraction in soil aggregates. The high values observed for
the groups with intermediate capacity (M. aterrima, R. P. glaucum may be explained by its low C/N ratio (9.19) and
sativus, B. ruziziensis and P. glaucum) and low capacity (C. low lignin/N ratio (1.95) when compared to the other species
cajan, C. brasiliensis) for aggregate formation are justified in studied. Unlike P. glaucum, R. sativus due to its C/N (16.67)
function of the specific characteristics of each plant, such as and lignin/N ratios (5.91), higher than the other species
aggressive root system and production of greater quantities of studied, showed lower LC values in macro and
exudates, factors that promote soil aggregation. Grasses, for microaggregates.
example, a group that includes B. ruziziensis and P. glaucum, The native Cerrado showed high LC content in MAC, not
are characterized by having a chemical aggregator effect due only significantly different from P. glaucum, but also
to higher root densities and better distribution of the root superior to the other cover crops (Table 2). These results
system in the soil which better distribute the root exudates indicate that the larger aggregates are those most affected by
and promote the union of small aggregates and formation of the mechanical destruction that occurs when replacing the
larger aggregates. However R. sativus, with its swiveling and native Cerrado with agroecosystems (Figueiredo et al., 2010).
aggressive root system, promotes a physical soil compaction Consequently, with the predominant rupture of
effect as its root system develops, thus favoring the formation macroaggregates, organic carbon that is physically protected
of larger and more stable aggregates (Guedes Filho et al., within this class is exposed to the action of microorganisms,
2013). M. aterrima, because it is a legume and produces a resulting in lower values in the cultivated areas (Loss et al.,
large amount of dry matter, contributes to the incorporation 2015). P. glaucum stood out as an LC accumulating species,
of C and nutrients in the soil, increasing the growth and both in MIC and in MAC, resulting from its chemical
activity of microorganisms, which may influence the composition with low C:N ratio.
aggregate diameter and stability (Loss et al., 2015). Analyzing the results of TOC in microaggregates, it was
Studies on the effect of cover crops regarding aggregate noticed that some plants (M. aterrima, R. sativus, B.
formation and stability have shown that with the use of B. ruziziensis, P. glaucum) were able to promote similar TOC
ruziziensis, R. sativus, M. aterrima and P. glaucum there levels to those found in the native Cerrado. These results
occurred increases in the WAD and aggregate stability (Loss demonstrated that the continuous supply of plant residues in
et al., 2011; Brandão and Silva 2012; Loss et al., 2015). different quantities and quality under the NTS makes TOC
Values of the aggregate stability index (ASI) were higher, accumulation possible in soil microaggregates (Guareschi et
ranging from 92% to 96% (Figure 2), indicating good soil al., 2012). Another explanation for the observed behavior
structure, which confirms the positive influence of cover refers to the ability of different species to influence the
plants with regards to aggregate stability. The plants R. formation of microaggregates. According to the hierarchical
sativus, M. aterrima and P. glaucum presented a high clustering model, macroaggregates are formed by the union
capacity to form stable aggregates in water, similar to the of microaggregates (Tisdall and Oades, 1982). Therefore,
Cerrado. C. cajan was the species that presented the lowest microaggregates are of fundamental importance in the
ASI. Similar results were found for the ASI by Torres et al. physical protection of C and the soil structure.
(2015), which justified the high ASI values as resulting from

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Table 1. C:N ratio and concentration of hemicellulose, cellulose and lignin (g kg-1) in the shoots of cover crops (average
concentrations of flowering and maturation).
Cover crops C:N Hemicellulose Cellulose Lignin Lignin:N
C. cajan 12.50 (±2.2) 160.6 (±10.2) bc 105.8 (±6.2) d 59.5 (±4.2) a 2.80 (±0.2) a
C. brasiliensis 12.41 (±3.2) 196.9 (±13.0) b 124.3 (±7.1) cd 38.1 (±2.1) bcd 1.89 (±0.3) bc
M. aterrima 8.38 (±1.8) 137.6 (±8.2) c 143.5 (±7.5) bc 55.6 (±4.5) ab 2.22 (±0.4) ab
P. glaucum 9.19 (±1.2) 302.0 (±15.2) a 178.2 (±9.2) a 34.0 (±2.4) cd 1.68 (±0.3) c
R. sativus 16.67 (±3.1) 123.6 (±32.2) c 164.6 (±8.2) ab 42.0 (±4.2) ab 3.33 (±0.6) a
B. ruziziensis 10.23 (±2.1) 319.3 (±11.2) a 105.7 (±6.3) d 17.5 (±1.5) d 0.85 (±0.1) d
Source: Carvalho et al. (2012). The values are expressed as means ± standard deviation. Means followed by the same letter in the column do not differ by the LSD test
(P≤0.05).

Fig 1. Weighted average diameter (WAD) of soil aggregates under cover crops and native Cerrado. Means followed by the same
letters do not present statistical difference by the LSD test (p≤0.05). (1) B. ruziziensis; (2) C. brasiliensis; (3) C. cajan; (4) P.
glaucum; (5) R. sativus; (6) M. aterrima; (7) native Cerrado.

Cover crops have differentiated capacity of soil aggregation in FA accumulation in microaggregates (Figure 3A). In
through the promotion of greater exudation of microaggregates all species presented higher quantities than
polysaccharides and formation of humic substances, resulting native Cerrado, which is attributed to the addition of plant
from decomposition of its residues. Soil polysaccharides are residues with the highest proportion of labile constituents in
mucilages resulting from the microbial metabolism and relation to those recalcitrant. In macroaggregates, C. cajan
decomposition of roots, plant and animal residues and root and B. ruziziensis showed higher C levels in FA than in the
exudation (Rangel et al., 2007). These substances act as native Cerrado, and there were no differences among the
transient bonding agents and are decomposed rapidly by other plants. Regarding HA accumulation in
microorganisms and associated predominantly with microaggregates, C. cajan stood out by presenting levels
macroaggregates (> 250 um), while humic substances higher than native Cerrado, M. aterrima and C. brasiliensis,
associated with iron, aluminum and aluminosilicates are and there was no difference between the other cover crops. In
persistent agents of microaggregates (<250 um) (Tisdall and general, the C contents in FA and HA were lower in the
Oades, 1982). Therefore, the species presenting TOC in MIC microaggregates compared to macroaggregates, confirming
similar to the native Cerrado may cause an increase in the results found by Passos et al. (2007). These results
humidification over time, which favors the formation of demonstrate that both the chemical and physical protection
microaggregates. have great importance in stabilizing these forms of C in the
The greatest impact of incorporating the Cerrado into soil (Passos et al., 2007).
agroecosystems was found in the loss of TOC in MAC. In Different from the behavior observed for FA and HA, the
this case, no cover crop was able to accumulate TOC in MAC native Cerrado showed higher HUM levels in MAC, greater
at the same levels of native Cerrado. Furthermore, cover than M. aterrima, B. ruziziensis and C. cajan (Figure 3A). In
crops do not differ in their ability to accumulate in TOC in several studies of tropical soils the predominance of HUM
MAC. The elevated capacity of the Cerrado in accumulating was also observed in relation to other humic fractions
carbon by means of the MAC was previously verified in (Conteh and Blair, 1998; Assis et al. 2006). A positive
other works (Figueiredo et al., 2010). relationship between soil aggregation and humin content was
The native Cerrado showed the lowest levels of FA in observed both in macro and microaggregates. This
microaggregates. Cover crops do not differ with regards to C relationship was also observed by Silva et al. (2014), where

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Table 2. Labile carbon (LC) and total organic carbon (TOC) in microaggregates (MIC) and macroaggregates (MAC), in the 0-10 cm
soil layer, for different land use systems.
LC TOC
Use system
MIC MAC MIC MAC
__________ g kg-1 _______ __________ g kg-1 __________
1 1.23 d 1.90 b 15.43 ab 19.33 bc
2 1.31 cd 1.97 b 14.24 b 18.97 bc
3 1.64 bc 1.95 b 14.57 b 17.25 c
4 2.34 a 2.32 ab 16.43 ab 20.22 bc
5 0.96 d 0.92 c 15.30 ab 18.71 bc
6 1.62 bc 2.19 b 15.02 ab 19.19 bc
7 1.83 b 2.53 a 17.83 a 22.83 a
Mean 1.56 1.97 15.54 22.4
(1) B. ruziziensis; (2) C. brasiliensis; (3) C. cajan; (4) P. glaucum; (5) R. sativus; (6) M. aterrima; (7) native Cerrado. Means
followed by the same letter in the column do not differ by the LSD test (P≤0.05).

Fig 2. Soil aggregate stability index (ASI) under the influence of different cover crops, in the depth of 0-10 cm. Means followed by
the same letters do not show statistical differences by the LSD test (p≤0.05). (1) B. ruziziensis; (2) C. brasiliensis; (3) C. cajan; (4)
P. glaucum; (5) R. sativus; (6) M. aterrima; (7) native Cerrado.

the predominance of humin in the Cerrado is related to its et al., 2013), with dry winters and wet summers. The average
insolubility and resistance to biodegradation, favored by the annual rainfall is 1400 mm and the average annual
formation of stable complexes (Fontana et al., 2006). The temperature is 21.3 °C. Soil of the experimental area is
relationship of macroaggregates and humic substances was classified as dystrophic Red Latosol, with clayey texture.
also observed by Borges et al. (2015). According to these The experiment was installed in an area with a history of
authors the high stability of humic substances is due to its corn cultivation in succession to cover crops in a NTS since
complex chemical structure and its interactions with clay 2005. At the time implementing the experiment, the soil of
minerals and metal cations; the humin fraction is more stable the 0-20 cm layer presented: pH (in water) = 6.0, OM = 21.7
when compared to fulvic and humic acids, which indicates g kg-1, PMehlich1= 0.9 mg kg-1, Al3+ = 0.1 cmolc kg-1,
greater recalcitrance and greater physical and chemical Ca2++Mg2+ = 2.9 cmolc kg-1, K+ = 0.1 cmolc kg-1. The
protection of carbon. This behavior demonstrates that the mineralogical composition of the soil horizon diagnosis is as
cover crops C. cajan, P. glaucum and C. brasiliensis favor follows: kaolin (320 g kg-1), gibbsite (496 g kg-1), hematite
the interaction between HUM and soil aggregation in these (142 g kg-1) and goethite (42 g kg-1), as described by Reatto
areas, presenting results similar to the natural conditions. et al. (2009).

Experimental design and plant materials

Materials and Methods
The treatments consisted of the following cover crops: T1 =
Experimental site and soil characteristics Braquiária ruziziensis, T2 = Canavalia brasiliensis Mart. ex
Benth., T3 = Pigeon pea ‘BRS Mandarin’ [Cajanus cajan
The experiment was conducted at the experimental station of (L.) Millsp.], T4 = millet ‘BR05’ [Pennisetum glaucum (L.)
Embrapa Cerrados, in Planaltina, DF, Brazil (latitude 15° 35 R.Br.], T5 = turnip-forage (Raphanus sativus L.), T6 = velvet
'30 "S, longitude 47º 42' 30" W). The regional climate, bean (Mucuna aterrima Merr.) and T7 = native Cerrado
according to the Köppen classification, is type Cwa (Alvares

1626
 (65 kg ha-1 N) when the plants emitted the fourth pair of
leaves (V4) and the same dose of N when plants emitted the
eighth pair of leaves (V6), totaling 150 kg ha-1 of N applied at
planting and in coverage. The species used as cover crops
were cut at the flowering stage.

Soil sampling and determination of aggregate size classes

In September 2015 the soil was sampled to determine

aggregate stability, total organic carbon (TOC), labile carbon
(LC), and carbon of the humic fractions (humic acid, fulvic
acid and humin). Three sub-samples were collected per plot,
in the 0-10 cm layer. The samples were appropriately packed
in plastic bags and sent to the laboratory. Then, the samples
were air dried, manually broken apart and passed through an
8 mm sieve for use in the separation of soil aggregate classes.
From this 100 g samples were weighed, which were
transferred to a 2 mm sieve, which comprised a set of sieves
with decreasing mesh diameter as follows: 2.00, 1.00, 0.50,
0.25 and 0.106 mm, according to EMBRAPA (1997). The
sample placed on the 2.00 mm sieve was moistened and
subsequently the sieve assembly was subjected to wet vertical
sieving for 30 minutes in a Yoder apparatus (Yoder, 1936).
After this time, the material retained on each sieve was
removed, placed in pre-weighed containers, identified and
placed in an oven at 60 °C to obtain a constant dry weight.
From the aggregate mass the weighted average diameter
(WAD) and the aggregate stability index (ASI) were
calculated.

The weighted average diameter (WAD) was calculated by the

formula:
𝑛
𝑊𝐴𝐷 = ∑ (𝑥𝑖. 𝑤𝑖)
𝑖=𝑙
Where: wi = proportion of each class in relation to the total;
xi = average diameter of the classes (mm);

The aggregate stability index in water was calculated by the

expression:
𝑊𝑒𝑖𝑔ℎ𝑡 𝑜𝑓 𝑡ℎ𝑒 𝑑𝑟𝑦 𝑠𝑎𝑚𝑝𝑙𝑒 − 𝑤𝑝25 − 𝑠𝑎𝑛𝑑
ASI = ( )
𝑊𝑒𝑖𝑔ℎ𝑡 𝑜𝑓 𝑡ℎ𝑒 𝑑𝑟𝑦 𝑠𝑎𝑚𝑝𝑙𝑒 − 𝑠𝑎𝑛𝑑

Fig 3. Carbon of the humin (HUM), humic acid (HA) and Where: wp25 = weight of the aggregates of the class < 0.25
fulvic acid (FA) fractions in macroaggregates (MAC) and mm.
microaggregates (MIC) at the depth of 0-10 cm, under the
effect of different cover crops. Means followed by the same After weighing and acquisition of the soil mass on each sieve,
letter in the same class of aggregates show no statistical the aggregates were grouped in two classes (macro- and
difference by the LSD test (p≤0.05). (1) B. ruziziensis; (2) C. micro-aggregates). The macroaggregates (MAC) were
brasiliensis; (3) C. cajan; (4) P. glaucum; (5) R. sativus; (6) considered those between 0.25 and 2.00 mm, obtained by
M. aterrima; (7) native Cerrado. combining the aggregate classes in this range. The
microaggregates (MIC) were considered those between 0.25
vegetation in an area adjacent to the experimental area. For and 0.106 mm.
C. cajan and U. ruziziensis, the sowing density was 20 plants
linear m-1 and 10 plants linear m-1 for other species. A Carbon analysis
spacing of 0.5 m between the sowing rows was used for all
species, as recommended by Carvalho and Amabile (2006). In the two aggregate classes (MAC and MIC) the CL and C
The treatments were arranged in a randomized block design levels were determined in the humic substances (HS).
with three replications. Each experimental plot, represented Quantitative chemical fractionation of HS was performed
by different cover crops, comprised 48 m2 (12m x 4 m). The according to Benites et al. (2003), using NaOH 1 mol L-1 as
chemical composition of the cover crops is presented in Table the extract. Obtained were the fractions of humic acid (HA),
1. The cover crops were sown in the first week of April in fulvic acids (FA) and humin (HUM), which was considered
succession to the corn crop, which was sown in the second the insoluble residue in acid and base. Carbon determinations
half of November. At corn planting, 20 kg ha-1 N, 150 kg ha-1 in extracts of the FA, HA and HUM fractions were performed
P2O5 and 80 kg ha-1 K2O were applied to the planting furrow, by oxidation with potassium dichromate and titration of the
and two applications of nitrogen were performed with urea

1627
excess with ammonium ferrous sulfate according to Yeomans Conteh A, Balir GJ (1998) The distribution and relative
and Bremner (1988). losses of soil organic carbon fractions in aggregate size
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Another procedure based on the oxidation of C in the samples CC, Bernoux M (2012) Carbono em agregados do solo sob
was performed according to Shang and Tiessen (1997), where vegetação nativa, pastagem e sistemas agrícolas no bioma
the LC is regarded as oxidizable C by the solution of KMnO4 Cerrado. Rev Bras Cienc Solo. 36: 1311–1321.
0.033 mol L-1. Crusciol CAC, Mateus GP, Nascente AS, Martins PO, Borghi
E, Pariz CM (2012) An innovative crop-forage intercrop
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C.C Figueiredo thanks CNPq (Conselho Nacional de Guareschi RF. Pereira MG, Perin A (2012) Deposição de
Desenvolvimento Científico e Tecnológico) for the Research resíduos vegetais, matéria orgânica leve, estoques de
Productivity Fellowship. carbono e nitrogênio e fósforo remanescente sob diferentes
sistemas de manejo no cerrado goiano. Rev Bras Cienc
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