Decomposition and nutrient release of leguminous plants in coffee agroforestry systems

Decomposição e liberação de nutrients de leguminosas herbáceas em cafezais sob sistemas agroflorestais

Eduardo da Silva Matos^I; Eduardo de Sá Mendonça^II; Irene Maria Cardoso^III; Paulo César de Lima^IV; Dirk Freese^V

^IResearcher, Embrapa Agrosilvopastoral, Av. dos Jacarandás 2639, 78550-003 Sinop (MT), Brazil. E-mail: eduardo.matos@embrapa.br ]]> ^IIProfessor, Plant Production Department, Agriculture Science Center, Federal University of Espírito Santo, 29500-000 Alegre (ES), Brazil. E-mail: esmjplia@gmail.com
^IIIProfessor, Soil Science Department, Federal University of Viçosa – UFV. CEP 36570-000 Viçosa (MG), Brazil. E-mail: irene@ufv.br
^IVResearcher, EPAMIG – Agriculture Research Institute of Minas Gerais. Vila Gianetti 46, 36570-000 Viçosa (MG), Brazil. E-mail: plima@epamig.ufv.br
^VResearcher, Chair of Soil Protection and Recultivation, Brandenburg University of Technology, 03046 Cottbus, Germany. E-mail: freese@tu-cottbus.de

SUMMARY

Leguminous plants used as green manure are an important nutrient source for coffee plantations, especially for soils with low nutrient levels. Field experiments were conducted in the Zona da Mata of Minas Gerais State, Brazil to evaluate the decomposition and nutrient release rates of four leguminous species used as green manures (Arachis pintoi, Calopogonium mucunoides, Stizolobium aterrimum and Stylosanthes guianensis) in a coffee agroforestry system under two different climate conditions. The initial N contents in plant residues varied from 25.7 to 37.0 g kg^-1 and P from 2.4 to 3.0 g kg^-1. The lignin/N, lignin/polyphenol and (lignin+polyphenol)/N ratios were low in all residues studied. Mass loss rates were highest in the first 15 days, when 25 % of the residues were decomposed. From 15 to 30 days, the decomposition rate decreased on both farms. On the farm in Pedra Dourada (PD), the decomposition constant k increased in the order C. mucunoides < S. aterrimum < S. guianensis < A. pintoi. On the farm in Araponga (ARA), there was no difference in the decomposition rate among leguminous plants. The N release rates varied from 0.0036 to 0.0096 d^-1. Around 32 % of the total N content in the plant material was released in the first 15 days. In ARA, the N concentration in the S. aterrimum residues was always significantly higher than in the other residues. At the end of 360 days, the N released was 78 % in ARA and 89 % in PD of the initial content. Phosphorus was the most rapidly released nutrient (k values from 0.0165 to 0.0394 d^-1). Residue decomposition and nutrient release did not correlate with initial residue chemistry and biochemistry, but differences in climatic conditions between the two study sites modified the decomposition rate constants.

Index terms: nutrient cycling, agroecology, plant residue, residue quality.

RESUMO

Termos de indexação: ciclagem de nutrientes, agroecologia, qualidade do resíduo vegetal.

INTRODUCTION

Efforts have been made to convert land use management systems with little or no addition of fertilizers into sustainable land uses that increase the efficiency of the nutrient cycling process and provide a valuable nutrient source for the development of sustainable smallholder farming systems in the Zona da Mata of Minas Gerais State. Leguminous plants used as green manure are a source of organic material with significant benefits for soil and crops, due to the high N₂ fixation capacity, nutrient cycling and contribution to soil cover (Cobo et al., 2002). Several studies have shown that leguminous plants can supply the crop demand for N and K (Mafongoya et al., 1998; Lupwayi & Haque, 1999), but are generally not effective in supplying sufficient P amounts to meet crop demands (Jones et al., 1996; Lupwayi & Haque, 1999; Lupwayi et al., 2007; Mukuralinda et al., 2009). However, decomposition of green manures have important residual effects on long-term P availability (Mafongoya et al., 1998) by releasing organic compounds that reduce the P fixation capacity of the soil (Andrade et al., 2003).

Leguminous species such as Stizolobium aterrimum, Arachis pintoi, Calopogonium mucunoides, and Stylosanthes guianensis have an outstanding capacity to produce high amounts of biomass and accumulate high nutrient concentrations (Matos et al., 2008), which become available to crops after residue decomposition. Decomposition and nutrient release depend on the residue quality, which is usually defined in relation to its chemical and biochemical composition (Thomas & Asakawa, 1993; Mendonça & Stott, 2003), because both influence the activity of decomposer communities (Thönnissen et al., 2000). High nutrient contents in plant materials have been correlated with high decomposition rates and nutrient release, which induce microbial growth and activity (Cobo et al., 2002). However, the relative importance of nutrient contents depends on the amounts of structural components such as lignin, cellulose, hemicellulose, and polyphenols as well as on the ratios C/P, C/N, lignin/N and polyphenol/N (Zaharah & Bah, 1999; Thönnissen et al., 2000; Hadas et al., 2004; Lupwayi et al., 2004).

The effects of climatic conditions can also greatly influence residue decomposition. Environmental factors such as temperature, moisture and aeration affect the microbial community and activity (Robertson & Morgan, 1996), and are therefore related to the decomposition process. Oliveira et al. (2003) observed significant effects on A. pintoi, when the residue decomposition process was evaluated in the wet and dry seasons. However, Zaharah & Bah (1999) observed no effects of rainfall on the decomposition and nutrient release rates of gliricidia (Gliricidia sepium).

The nutrient release rates are essential to plan the introduction of leguminous plants used as green manure, considering the crop demand and availability of critical nutrients (Mafongoya et al., 1998). Thus, it is necessary to know the constants related to these processes in order to: (1) establish effective management practices with green manure; and (2) plan the introduction of species to release nutrients and meet crop demand, improving nutrient use efficiency. The purpose of this study was to evaluate decomposition and nutrient release rates of leguminous plants used as green manure under two edaphic and climatic conditions in the Zona da Mata of Minas Gerais State, Atlantic Forest region, Brazil.

Study sites and experiment description

Leguminous plants (A. pintoi, C. mucunoides, S. aterrimum and S. guianensis) were grown in two experimental areas with coffee on two family farms, from December 2003 to April 2004. One experimental plot was located on a farm in Pedra Dourada (PD) at 20 º 50 ' S latitude, 42 º 08 ' W longitude and 690 m altitude, with highest and lowest mean annual temperatures, respectively, of 27.6 and 16.2 ºC, and 1,280 mm rainfall; the experimental area facing south. The second experiment was located on a farm in Araponga (ARA) (20 º 38 ' S latitude, 42 º 31 ' W longitude, 950 m asl, with highest mean annual temperature of 25.4 ºC and the lowest of 13.7 ºC, and 1,320 mm rainfall (Figure 1); the experimental area facing west. On both farms, the soils were classified as Red-Yellow Latosol (Brazilian taxonomy system), corresponding to a Typic Haplustox according to the U.S. soil taxonomy system. Some properties of the soils of both farms were described by Matos et al. (2008).

The three-year-old coffee trees were cultivated in agroforestry systems, spaced 3.0 x 0.8 m between rows and plants, respectively. The leguminous plants were grown in-between the coffee rows in a 2 x 2 m plot. Before the experiment, 1.20 Mg ha^-1 of lime, 300 kg ha^-1 of gypsum, 125 kg ha^-1 of potassium sulphate and 800 kg ha^-1 termophosphate was applied between the coffee rows in the PD area. In the ARA area, 0.26 Mg ha^-1 lime, 64 kg ha^-1 gypsum, 125 kg ha^-1 potassium sulphate and 800 kg ha^-1 termophosphate was applied. Seeds were sown at a depth of 1 cm, without Rhizobium inoculation. Approximately 120 days after sowing, the above-ground biomass was harvested, weighed and analyzed.

Chemical and biochemical characterization

Sub-samples of the entire plant material were dried (55 ºC), ground and sieved (< 1 mm) for chemical analysis. Total C and N were analyzed by dry combustion (Perkin Elmer CHNS/O 2400). Total P was determined by the ammonium molybdate-ascorbic method (Murphy & Riley, 1962), and total K was measured by flame spectrophotometry, after sample digestion with perchloric and nitric acids (Sarruge & Haag, 1974). Soluble polyphenols were extracted with 50 % aqueous methanol and measured using Folin-Dennis reagent with a tannic acid standard for the colorimetric method (Anderson & Ingram 1996). Lignin, cellulose and hemicellulose contents were determined by the acid-detergent fiber method (van Soest et al., 1991).

Sub-samples of the fresh material (100 g) were placed in 20 x 20 cm nylon litter-bags consisting of 2 mm mesh. The litter-bags were placed on the soil surface in the shade of a coffee tree, and were removed after 15, 30, 60, 120, 240 and 360 days. The remaining material was dried (55 ºC), weighed and analyzed each time. Total N, P and K were analyzed, as described above for the initial chemical content.

The experiment was arranged in a complete randomized 2 x 4 x 7 factorial block design (two farms, four residues and seven evaluations), with four replications.

To describe the decomposition and nutrient release rates, the percentage of the remaining dry biomass and N, P and K contents were adjusted to a single exponential equation:

where X_t is the dry weight or nutrient remaining at time t and the slope k, the decomposition or nutrient release constant. Constant X₀ is the initial quantity of dry biomass or nutrients.

The half-life (t_1/2) of the leguminous residues was calculated by the equation:

Linear regression coefficients were tested by the t test at 1, 5 and 10 % using SigmaPlot 8.0.

Chemical and biochemical properties of leguminous residues

The dry biomass (DB) varied from 0.95 to 2.88 Mg ha^-1 and from 0.94 to 3.21 Mg ha^-1 in PD and in ARA, respectively (Matos et al., 2008). The DB production of A. pintoi was lowest at both localities. In PD, the DB production of S. guianensis was highest (87 % higher than in ARA), while in ARA, S aterrimum produced most DB (85 % higher than in PD).

The initial N contents in plant residues varied from 25.7 to 37.0 g kg^-1 and P contents from 2.4 to 3.0 g kg^-1 (Table 1). Nitrogen values were lowest for A. pintoi on both farms. According to Mafongoya et al. (1998), the quality of plant residues with initial N and P concentrations of around 20 and 2.5 g kg^-1, respectively, is considered high. The C/N ratio varied from 12.2 to 15.9 and was lowest for S. aterrimum and C. mucunoides and highest for A. pintoi, but similar on both farms. The C/N ratio values of C. mucunoides, S. guianensis and S. aterrimum were around 8 % higher in ARA than in PD. For S. aterrimum the C/P ratio was highest in PD and the C/N ratio lowest in ARA. There was no difference in the C/P ratio of A. pintoi, C. mucunoides and S. guianensis in ARA, with values of around 170 (±3). According to Stevenson (1994), C/P ratio values < 200 in residues contribute to P mineralization, while the C/P ratio values that promote P mineralization vary widely in the literature (Baggie et al., 2004). The hemicellulose content varied from 12.1 to 16.9 %, and the cellulose content from 26.7 to 32.3 %. Except for C. mucunoides and S. aterrimum in PD, the variation in hemicellulose values was small (12.6 ±0.4) among leguminous species in both areas. Among the green manures, the lignin values of S. guianensis were lowest (4.8 % in PD and 6.1 % in ARA). The polyphenols content varied from 1.30 to 2.04 % in PD and from 1.19 to 1.86 % in ARA. C. mucunoides had the lowest value and S. aterrimum the highest value of polyphenols. Polyphenols can affect residue decomposition and nutrient release due to their ability to complex protein, reducing N availability to soil microorganisms (Hättenschwiler & Vitousek, 2000; Monteiro et al., 2002). On both farms, the LG/N and (LG/PP)/N ratios of A. pintoi were highest and of S. guianensis lowest. The concentration of structural compounds such as lignin, cellulose and hemicelluloses provides an important contribution to the decomposition rate as well as C/P, C/N, lignin/polyphenol, lignin/N, and polyphenol/N ratios, which are the main regulators of residue decomposition (Fox et al., 1990; Handayanto et al., 1995; Northup, 1995; Cobo et al., 2002; Mendonça & Stott, 2003). In general, the lignin/N, lignin/polyphenol and (lignin+polyphenol)/N ratios were low, indicating that the studied leguminous plants can be classified as residues with a high turnover rate (Thomas & Asakawa, 1993).

Decomposition

The mass loss rates were highest in the first 15 days when 25 % of the residues were decomposed in PD and ARA (Figure 2). From 15 to 30 days, the decomposition rate decreased on both farms. Except for the S. aterrimum, the mass loss of residues in PD was higher than in ARA. In ARA, S. aterrimum tended to present the lowest values of Remaining DB until 60 days (Figure 2). In a short term, decomposition rates are high due to the high content of fast decomposable components such as sugars, amino acids and proteins. In the later stages, decomposition rates tend to decrease due to the accumulation of recalcitrant components such as lignin, tannins and cellulose (Zaharah & Bah, 1999; Thönnissen et al., 2000; Hadas et al., 2004; Lupwayi et al., 2004).

In a comparison of the two farms, lower remaining DB values in PD (p < 0.01) throughout the decomposition period were observed, which increased the difference between the two farms at the end of the 360 days. This effect was probably related to the location of the experimental area, facing South in PD, resulting in greater humidity in the coffee rows than in ARA where the experimental area faces West.

In PD, the decomposition constant k increased in the order C. mucunoides < S. aterrimum < S. guianensis < A. pintoi (Table 2). No difference in the decomposition rate among leguminous plants (0.00220.0030 d^-1) was found in ARA. On average, the decomposition rates of all residues in ARA were 50.7 %, lower than in PD. Except for C. mucunoides, the half-life (t_1/2) of the leguminous plants in PD was 57 % shorter than in ARA. Differences in residue chemistry and biochemistry were not correlated with the decomposition rate constants of residues of both farms. Taking into account that the residues in our study presented similar composition, the edaphic and climatic factors apparently had more influence on residue decomposition than the chemical and biochemical composition. We suggest that the effects of plant constituents on the decomposition process should be more carefully evaluated in future studies involving heterogenic materials and that temperature and humidity should be controlled. Thönnissen et al. (2000) observed that the effects of residue chemistry and biochemistry on decomposition rates varied widely between seasons and locations.

The K release rate (k_K) varied from 0.0076 d^-1 for S. aterrimum in PD to 0.0145 d^-1 for A. pintoi in ARA. In general, the behavior of the curves of K concentration in the evaluation period was similar in both areas (Figure 3). Except for S. aterrimum, the t_1/2K of all leguminous residues tended to be similar on both farms. Potassium is considered a nutrient with highest release rates, since it is a non-structural component of the plants (Lupwayi & Haque, 1999; Cobo et al., 2002; Giacomini et al., 2003). Usually, the K rate depends on the rainfall during the decomposition process (Giacomini et al., 2003).

The rates of N release varied from 0.0056 to 0.0096 d^-1 in PD and from 0.0036 to 0.0048 d^-1. The rates of N release followed the same trend as mass loss. In PD, the k_N values were highest for A. pintoi and S. guianensis. Around 32 % of the total N in the plant material was released in the first 15 days. In comparison, the t_1/2 values of N were higher than of the other nutrients (72.1123.7 and 144.8192.5 days, respectively) in PD and ARA. In ARA, N concentrations in S. aterrimum residues were constantly higher than in the other residues (Figure 4). In PD, the behavior of S. aterrimum at the end of the evaluation period was similar. Following the same trend of DB losses, the values of turnover rates for N release were 50.2 % lower in ARA than PD. At the end of 360 days, the N released corresponded to 78 % of the initial content in ARA and 89 % in PD, indicating that a great part of N accumulated in the plant tissue had been released in the first days of decomposition. Zaharah & Bah (1999) observed a similar behavior of Gliricidia sepium, which released half of the initial N content in the initial stage.

Phosphorus was the most rapidly released nutrient (k values of 0.01650.0394 d^-1) (Table 2). A. pintoi had the highest k_P in PD and S. guianensis in ARA, consequently the t_1/2P of both leguminous residues was lowest (17.6 and 19.3 days, respectively). Oliveira et al. (2003) reported similar t_1/2P values of 16.1 days for A. pintoi. Unlike K, generally considered the nutrient with highest release rate, P participates in cell constituents, e.g., phospholipids, nucleic acids and DNA and RNA structures, and is also part of the ATP molecule (Jahnke, 1992; Ha et al., 2007). Phosphorus release is not directly related to rainfall, but to the total inorganic P content and soluble P in the residues, and to the effective action of microorganisms on the organic fractions (Giacomini et al., 2003). On average, 60 % of the total P in plant residues was released in the first 15 days when the P concentration in the residues was reduced to 50 % of the initial concentration on both farms (Figure 5). These results agree with Ha et al. (2007) who reported that 70 % of the initial P content was released from pea residues after 15 days of evaluation in a sandy soil with low P availability. Giacomini et al. (2003) observed that 64 % of P in Vicia sativa was released 30 days after cutting, and was correlated with soluble P. Gliricidia sepium released 55 % of the initial P content after 10 days of decomposition, and there was a remaining content of 11 % after 70 days of evaluation, which was related to recalcitrant fractions (Zaharah & Bah, 1999).

After 30 days of evaluation, the P release rate from all residues decreased, probably due to exhaustion of the inorganic P and labile organic P fractions, leaving only non-labile organic P fractions (Mueller-Harvey & Wild, 1986). Inorganic P is rapidly released to the soil after residue incorporation and can be quickly consumed by soil microorganisms (Oliveira et al., 2003; Ha et al., 2007). In the later stages of decomposition, P is released more slowly from residues by mineralization of organic forms (Ha et al., 2007). In ARA, the P contents of S. aterrimum were higher than of the other leguminous plants until 30 days of evaluation. In general, the P release rates from residues in PD were higher than from residues in ARA, which was related to the higher decomposition rates observed in PD, since the nutrient release constant can also be directly affected by residue mass loss.

The total nutrient release from leguminous plant residues after 360 days showed that S. aterrimum released the highest amounts in ARA (93.0 kg ha^-1 of N, 7.8 of P and 63.6 K) and S. guianensis in PD (86.2 kg ha^-1 N, 7.1 P and 50.4 K). Similar results were obtained by Silva et al. (2002), who reported 85.6 kg ha^-1 N, 8.2 P and 60.5 K released by S. aterrimum. Since our evaluation considered only the nutrient amounts in the shoot biomass, the contribution of green manures to the annual nutrient incorporation is likely to be higher, because the contribution of the roots to soil nutrient incorporation is essential (Weatherall et al., 2006).

CONCLUSIONS

2. Under field conditions, the initial chemical and biochemical composition of plant residues are not directly correlated with decomposition and nutrient release rates.

3. In the low nutrient availability soils of the Zona da Mata of Minas Gerais, P was the most rapidly released nutrient from leguminous residues.

4. The results of this study can be used as indicators of the potential amount and rate of nutrient supply of intercropped A. pintoi, C. mucunoides, S. aterrimum and S. Guianensis to coffee in agroforestry systems.

ACKNOWLEDGEMENTS

The authors thank Capes and Fapemig for the financial support and Epamig for the partnership in the project; Mr. José Brás for his attention and help with the laboratory analyses. We also thank the farmers "Jésus" and "Dadinho" for their participation in the field work.

LITERATURE CITED

ANDERSON, J.D. & INGAM J.S.I. Tropical soil biology and fertility: A handbook of methods. 2.ed. Wallingford, UK CAB International, 1996. 171p.         [ Links ]

ANDRADE, F.V.; MENDONÇA, E.S.; ALVAREZ V., V.H. & NOVAIS, R.F. Adição de ácidos orgânicos e húmicos em Latossolos e adsorção de fosfato. R. Bras. Ci. Solo, 27:1003-1011, 2003.         [ Links ]

BAGGIE, I.; ROWELL, D.L.; ROBINSON, J.S. & WARREN, G.P. Decomposition and phosphorus release from organic residues as affected by residue quality and added inorganic phosphorus. Agrofor. Syst., 63:125-131, 2004.         [ Links ]

COBO, J.G.; BARRIOS, E.; KASS, D.C.L. & THOMAS, R.J. Decomposition and nutrient release by green manure in a tropical hillside agroecossistem. Plant Soil, 240:331-342, 2002.         [ Links ]

FOX, R.H.; MYERS, R.J.K. & VALLIS, I. The nitrogen mineralization rate of legume in soil as influenced by their polyphenol, lignin and nitrogen contents. Plant Soil, 129:251-259, 1990.         [ Links ]

GIACOMINI, S.J.; AITA, C.; HÜBNER, A.P.; LUNKES, A.; GUIDINI, E. & AMARAL, E.B. Liberação de fósforo e potássio durante a decomposição de resíduos culturais em plantio direto. Pesq. Agropec. Bras., 38:1097-1104, 2003.         [ Links ]

HA, K.V.; MARSCHNER, P.; BÜNEMANN, E.K. & SMERNIK, R.J. Chemical changes and phosphorus release during decomposition of pea residues in soil. Soil Biol. Biochem., 39:2696-2699, 2007.         [ Links ]

HADAS, A.; KAUTSKY, L.; GOEK, M. & KARA, E.E. Rates of decomposition of plant residues and available nitrogen in soil, related to residue composition through simulation of carbon and nitrogen turnover. Soil Biol. Biochem., 36:255-266, 2004.         [ Links ]

HANDAYANTO, E.; CADISCH, G. & GILLER, K.E. Manipulation of quality and mineralization of tropical legume tree prunings by varying nitrogen supply. Plant Soil, 176:149-160, 1995.         [ Links ]

HÄTTENSCHWILER, S. & VITOUSEK, P.M. The role of polyphenols in terrestrial ecosystem nutrient cycling. Tree, 15:238-243, 2000.         [ Links ]

JAHNKE, R.A. The phosphorus cycle. In: BUTCHER, S.S.; CHARLSON, R.J.; ORIANS, G.H. & WOLFE, G.V. Global biogeochemical cycles. Sand Diego, 1992. p.301-315.         [ Links ]

JONES, R.B.; WENDT, J.W.; BUNDERSON, W.T. & ITIMU, O.A. Leucaena + maize alley cropping in Malawi. Part 1: Effects on N, P, and leaf application on maize yields and soil properties. Agrofor. Syst., 33:281-294, 1996.         [ Links ]

LUPWAYI, N.Z. & HAQUE, I. Leucaena hedgerow intercropping and cattle manure application in the Ethiopian highlands: I. Decomposition and nutrient release. Biol. Fert. Soils, 28:182-195, 1999.         [ Links ]

LUPWAYI, N.Z.; CLAYTON, G.W.; O'DONOVAN, J.T.; HARKER, K.N.; TURKINGTON, T.K. & RICE, W.A. Decomposition of crop residues under conventional and zero tillage. Can. J. Soil Sci., 84:403-410, 2004.         [ Links ]

LUPWAYI, N.Z.; CLAYTON, G.W.; O'DONOVAN, J.T.; HARKER, K.N.; TURKINGTON, T.K. & SOON, Y.K. Phosphorus release during decomposition of crop residues under conventional and zero tillage. Soil Till. Res., 95:231-239, 2007.         [ Links ]

MAFONGOYA, P.L.; GILLER, K.E. & PALM, C.A. Decomposition and nitrogen release patterns of tree prunings and litter. Agrofor. Syst., 38:77-97, 1998.         [ Links ]

MATOS, E.S.; MENDONÇA, E.S.; LIMA, P.C.; COELHO, M.S.; MATEUS, R.F. & CARDOSO, I.M. Green manure in coffee systems in the region of Zona da Mata, Minas Gerais: Characteristics and kinetics of carbon and nitrogen mineralization. R. Bras. Ci. Solo, 32:2027-2035, 2008.         [ Links ]

MENDONÇA, E.S. & STOTT, D.E. Characteristics and decomposition rates of pruning residues from a shaded coffee system in Southeastern Brazil. Agrofor. Syst., 57:117-125, 2003.         [ Links ]

MONTEIRO, H.C.F.; CANTARUTTI, R.B.; NASCIMENTO JR, D.; REGAZZI, A.J. & FONSECA, D.M. Dinâmica de decomposição e mineralização de nitrogênio em função da qualidade de resíduos de gramíneas e leguminosas forrageiras. R. Bras. Zootec., 31:1092-1102, 2002.         [ Links ]

MUELLER-HARVEY, I. & WILD, A. The nature and stability of organic phosphates in leaf litter and soil organic matter in Nigeria. Soil Biol. Biochem., 18:643-647, 1986.         [ Links ]

MUKURALINDA, A.; TENYWA, J.S.; VERCHOT, L.; OBUA, J. & NAMIREMBE, S. Decomposition and phosphorus release of agroforestry shrub residues and the effect on maize yield in acidic soils of Rubona, Southern Rwanda. Nutr. Cycl. Agroecosyst., 84:155-166, 2009.         [ Links ]

MURPHY, J. & RILEY, J.P. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta, 27:31-36, 1962.         [ Links ]

NORTHUP, R.R. Polyphenol control of nitrogen release from pine litter. Nature, 377:227-229, 1995.         [ Links ]

OLIVEIRA, A.O.; MUZZI, M.R.S.; PURCINO, H.A.; MARRIEL, I.E. & SÁ, N.M.H. Decomposition of Arachis pintoi and Hyparrhenia rufa litters in monoculture and intercropped systems under lowland soil. Pesq. Agropec. Bras., 38:1089-1095, 2003.         [ Links ]

ROBERTSON, F.A. & MORGAN, W.C. Effects of management history and legume green manure on soil microrganisms under organic vegetable production. Austr . J. Soil Res., 34:427-440, 1996.         [ Links ]

SARRUGE, J.R. & HAAG, H.P. Análises químicas em plantas. Piracicaba, Escola Superior de Agricultura "Luiz de Queiroz", 1974. 56p. (Boletim Técnico)         [ Links ]

SILVA, J.A.A.; VITTI, G.C.; STUCHI, E.S. & SEMPIONATO, O.R. Reciclagem e incorporação de nutrientes ao solo pelo cultivo intercalar de adubos verdes em pomar de larangeira-'pêra'. R. Bras. Frutic., 24:225-230, 2002.         [ Links ]

STEVENSON, F.J. Humus chemistry: Genesis, composition, reactions. 2.ed. New York, John Wiley, 1994. 496p.         [ Links ]

THOMAS, R.J. & ASAKAWA, N.M. Decomposition of leaf litter from tropical forage grasses and legumes. Soil Biol. Biochem., 25:1351-1361, 1993.         [ Links ]

THÖNNISSEN, C.; MIDMORE, D.J.; LADHA, J.K.; OLK, D.C. & SCHMIDHALTER, U. Legume decomposition and nitrogen release when applied as green manures to tropical vegetable production systems. Agron. J., 92:253-260, 2000.         [ Links ]

van SOEST, P.J.; ROBERTSON, J.B. & LEWIS, B.A. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci., 74:3583-3597, 1991.         [ Links ]

WEATHERALL, A.; PROE, M.F.; CRAIG, J.; CAMERON, A.D.; McKAY, H.M. & MIDWOOD, A.J. Tracing N, K, Mg and Ca released from decomposing biomass to new tree growth. Part II: A model system simulating root decomposition on clearfell sites. Biom. Bioenerg., 30:1060-1066, 2006.         [ Links ]

ZAHARAH, A.R. & BAH, A.R. Patterns of decomposition and nutrient release by fresh Gliciridia (Gliciridia sepium) leaves in an Ultisol. Nutr. Cycl. Agroecosyst., 55:269-277, 1999.         [ Links ]

Received for publication in March 2009 and approved in December 2010.