E ects of pig manure and wheat straw on growth of mung bean seedlings grown in aluminium toxicity soil

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1 Bioresource Technology 76 (2001) 235±240 E ects of pig manure and wheat straw on growth of mung bean seedlings grown in aluminium toxicity soil Q.R. Shen a, Z.G. Shen b, * a College of Resources and Environmental Sciences and MOA Key Laboratory of Crop Growth Regulation, Nanjing Agricultural University, Nanjing , People's Republic of China b Department of Agronomy and MOA Key Laboratory of Crop Growth Regulation, Nanjing Agricultural University, Nanjing , People's Republic of China Received 14 January 2000; received in revised form 2 July 2000; accepted 26 July 2000 Abstract Crop production in red soil areas may be limited by Al toxicity. A possible alternative to ameliorate Al toxicity is the application of such organic manure as crop straw and animal manure. A pot experiment was conducted to investigate the e ects of organic materials on the alleviation of Al toxicity in acid red soil. Ground wheat straw, pig manure or CaCO 3 were mixed with the soil and incubated, at 85% of water holding capacity and 25 C, for 8 weeks. After the incubation, 14 seedlings of mung bean (Phaseolus aures Roxb) were allowed to grow for 12 days. Results showed that application of organic material or CaCO 3 increased soil ph and decreased soil monomeric inorganic Al concentrations. Growth of mung bean seedling was improved substantially by the application of organic material or CaCO 3. Pig manure or wheat straw was more e ective in ameliorating Al toxicity than was CaCO 3. Mung bean plants receiving pig manure or wheat straw contained relatively high concentrations of P, Ca and K in their leaves. It is suggested that the bene cial e ect of organic manure on mung bean is likely due to decreasing concentrations of monomeric inorganic Al concentrations in soil solution and improvement of mineral nutrition. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Aluminium toxicity; Pig manure; Wheat straw; Mung bean; Red soil 1. Introduction Aluminium is the most abundant metal in the earth's crust and occurs in a number of di erent forms in the soil. It is generally accepted that Al toxicity is a primary factor limiting plant growth on acid soils (Kochian, 1995). Toxic e ects of Al on plant growth have been attributed to several physiological pathways, although the precise mechanism has not yet been understood. Proposed mechanisms of Al toxicity include Al interactions with the root cell wall, Al disruption of plasma membrane and the membrane transport processes, and Al inhibition of mineral uptake and metabolism, especially that of Ca and P (Clarkson, 1966; Clarkson and Sanderson, 1971; Bengtsson et al., 1988). Increasing Ca concentration in the nutrient solution (Alva et al., 1986; Shen et al., 1993) and liming (Bessho * Corresponding author. Tel.: ; fax: address: zgsheng@njau.edu.cn (Z.G. Shen). and Bell, 1992; Yu and Qin, 1998) had a bene cial e ect on plant growth under Al stress and alleviated Al toxicity of plants. Thus, liming is the usual method for ameliorating Al toxicity in the acid soil. However, it has been discovered that liming may also cause negative e ects on plant growth and soil properties (Ahmad and Tan, 1986). De ciencies, for example, of some nutrients such as P, Zn, B and Mn can be induced by lime application. Furthermore, the practice of liming is expensive in many areas of China. Organic material is a good source of plant nutrients and has a positive e ect on improvement of the soil physical structure. Bene cial e ects of organic matter application on aluminium detoxi cation have been demonstrated in acid soils and solution culture (Ahmad and Tan, 1986; Hue and Amien, 1989; Ostatek-Boczynski et al., 1995; Yu and Qin, 1998). Aluminium complexed by organic matter is not readily exchangeable and is non-phytotoxic (Hue et al., 1986). Dissolved organic matter could contribute e ective ligands to form complexes with aluminium in soil solution. Decomposition of organic matter in soils results in the microbial production of a number of /01/$ - see front matter Ó 2000 Elsevier Science Ltd. All rights reserved. PII: S ( 0 0 )

2 236 Q.R. Shen, Z.G. Shen / Bioresource Technology 76 (2001) 235±240 biochemical compounds such as aliphatic acids, phenols, phenolic acids and complex polymeric phenols (Wong et al., 1995). Application of organic materials increases ph of soil solution. An increase in ph could increase precipitation of soluble Al and complexation of Al by organic compounds (Bessho and Bell 1992). Red soil, which is acidic in reaction and contains a high level of Al and low content of organic matter, covers extensive areas of the humid regions in China. In these areas, Al toxicity is believed to be a very important agricultural problem. The main objective of the present study was to evaluate the e ects of organic manure on the amelioration of red soil. The response of mung bean (Phaseolus aures Roxb) was also investigated by measuring plant growth and element uptake. Table 2 Chemical properties of the test organic materials Chemical and physical properties Wheat straw Pig manure ph Organic matter (g kg 1 ) a Total N (g kg 1 ) Total K (g kg 1 ) Total Ca (g kg 1 ) Total Mg (g kg 1 ) Total P (g kg 1 ) Total Al (g kg 1 ) Total Cu (mg kg 1 ) Total Mn (mg kg 1 ) Total Zn (mg kg 1 ) a All concentrations are expressed on dry weight basis. 2. Methods Soil samples were collected from surface A horizons of red soil from Jianxu province, China. Selected soil characteristics are given in Table 1. The organic materials used in the present study were pig manure and wheat straw (stems and leaves). Pig manure, a combination of excreta, wasted feed and bedding materials, is rich in nitrogen and dissolved organic compounds and it represents a material expected to readily decompose in soils. In contrast, the wheat straw is characterized by high cellulose and lignin contents and high C/N ratio, and represents a material expected to be more resistant to decomposition in soil. These organic materials were ground to pass through a 0.25-mm sieve after air-drying. Chemical composition and ph of the two organic materials are given in Table 2. Soil ph was determined using a glass electrode and a 1:1 soil to water ratio. Total N was determined by Kjeldahl digestion and distillation. Samples of air-dried soil (800 g) were placed in plastic pots. The dry pig manure (PM) or wheat straw (WS) was added to the soil at rates of 10 and 30 g kg 1 soil, which were referred as PM10 and PM30 or WS10 and WS30, respectively. In terms of lime (L) and L + PM treatments, 1.5 g lime (CaCO 3 )kg 1 and 1.5 g lime + 30 g pig manure kg 1 were added, respectively. The soil that did not receive application of organic material or lime was used as control. Basal fertilizers applied were 100 mg N kg 1 dry soil as urea, 80 mg P kg 1 and 100 mg kg 1 KasKH 2 PO 4. The organic matter and fertilizers were applied to each of the pots and were mixed thoroughly with the soils. Soil moisture was raised to 85% of water holding capacity and maintained by daily addition of water after weighing every pot. Each treatment was replicated three times. These soils were incubated at 25 C for 8 weeks. About 350 g soil samples in each pot were collected and used to determine soil ph and extracted soil solution. The soil remaining in the pot was used for the pot experiment. Fifteen seeds of mung bean were sown in each pot (contained about 450 g dried soil). After germination, the seedlings were thinned to 10 plants per pot and grown for 14 days. Plants were harvested by cutting the shoots at the soil surface and roots were separated from the soil. Shoots and roots were washed with tap water and rinsed with deionized water, dried at 80 C for 24 h, and the dry matter measured. Plant materials were ground and digested with a mixture of HNO 3 /HClO 4 (Zhao et al., 1994), and the major and trace elements in the digests were determined using inductively coupled plasma atomic emission spectrometry (ICP-AES, Perkin±Elmer, 3300 DV). The soil solution was extracted by a centrifuge method. The supernatant solution was ltered through a 0.45 lm lter. Monomeric inorganic Al concentrations were determined by the pyrocatechol violet (PEV) method (Menzies et al., 1992). The concentrations of total Al, Ca, Mg, K, Mn, P, Fe and Zn in soil solution were determined by ICP-AES. Exchangeable cations were extracted with 1 mol l 1 NH 4 ±acetate (ph 7.0) and determined by ICP-AES. Table 1 Selected chemical and physical properties of the soil tested ph Organic C Total N Texture (%) Exchangeable cations (mg kg 1 ) (mg kg 1 ) a (mg kg 1 ) Clay Silt Sand Ca Mg K Na Al a All concentrations are expressed on dry weight basis.

3 Q.R. Shen, Z.G. Shen / Bioresource Technology 76 (2001) 235± Results and discussion 3.1. Soil ph The data show that the pig manure and wheat straw application increased soil ph (Fig. 1). The greater increase in soil ph in pig manure treatments than in wheat straw treatments probably resulted from the much higher amounts of K, Ca and Mg, especially Ca and Mg, in the pig manure (Table 2). These cations may increase the base saturation of the soil and result in increasing soil ph. This is in agreement with the observations of Wong et al. (1998), who found that the increased soil ph was directly proportional to the base cation (Ca, Mg and K) concentrations of the added organic material. Some reasons for such a soil ph increase have been advanced (Bessho and Bell, 1992), e.g., release of NH 3 from decomposing organic materials, production of OH by dissolution of solid Mn and Fe oxides in reduced conditions. But in the present experiment, we did not nd an increased concentration of Mn in solution of the soil treated with pig manure or wheat straw (Table 3). The concentration of Fe in soil solution was below the detection limit of ICP-AES (<1 lg l 1 ). Thus, it does not appear that the dissolution of Fe and Mn oxides contributed to the ph rise. The highest ph value of soil was found in the soil receiving 1.5 g kg 1 lime (CaCO 3 ). Compared to application of lime alone, combined application of lime and pig manure had no signi cant e ect on soil ph (Fig. 1) Total and monomeric inorganic Al concentrations in soil solution Liming markedly decreased total and monomeric inorganic Al concentrations in the soil solution (Fig. 2). The concentrations of total and monomeric inorganic Al in soil which received 1.5 g kg 1 lime were about 54% and 50% of those in the control soil without lime or organic materials added. Application of pig manure at 10 and 30 g kg 1 signi cantly decreased the concentrations of total and monomeric inorganic Al in soil solution (Fig. 2). Compared to the control, application of wheat straw decreased the concentrations of monomeric Al, but had no signi cant e ect on total Al concentration in soil solution. At the same rate of application, wheat straw treatments had much higher total and monomeric Al concentrations than pig manure treatments. The opposite was observed for the concentration of organically complexed Al. Bessho and Bell (1992) also reported that legume leaves and barley straw Fig. 1. The ph of soil incubated with pig manure (PM), wheat straw (WS) and lime (L) for 8 weeks. For treatments see Section 2. Fig. 2. Concentrations of total and monomeric Al in soil solution. Table 3 Chemical composition of solution of soil incubated with various levels of pig manure, wheat straw and CaCO 3 for 8 weeks a Treatment Ca (mmol l 1 ) K (mmol l 1 ) Mg (mmol l 1 ) Na (mmol l 1 ) Mn (lmol l 1 ) P (lmol l 1 ) Control 2.48a 0.68a 0.23a 0.97a 57c 6.2a WS a 1.17b 0.38a 1.78b 49c 11b WS a 2.00c 0.59b 2.37b 27b 16c PM b 1.87c 1.61c 2.42b 50c 13bc PM c 5.75e 4.98e 5.57c 34bc 35d L 4.79b 0.23a 0.20a 0.72a 0.01a < DL b L + PM c 4.92d 3.74d 5.00c 2a 65e a Means in the same column followed by di erent letters are signi cantly di erent at P < b DL: detection limit.

4 238 Q.R. Shen, Z.G. Shen / Bioresource Technology 76 (2001) 235±240 treatment decreased the concentrations of total and monomeric Al and increased the concentration of organically complexed Al. The decrease in monomeric Al concentration with addition of organic materials could have resulted from increases in ph and amount of organic material. An increase in ph could cause precipitation of soluble Al and increase the ability of native and added organic matter to complex Al. However, Wong et al. (1995) reported that the concentration of organically complexed Al in solution changed little with organic residue treatment and ranged from 0.04 to 0.05 mg Al l 1. They suggested that lowered Al solubility was the more likely cause for the lower concentration of monomeric inorganic Al measured in soil solution. In the present study, the concentration of organically complexed Al increased with increasing application of pig manure or wheat straw. This di erence could have been due to di erent application rates of organic materials. In their experiment, Wong et al., 1995 used much lower application rates of organic materials than we did Mineral element concentrations in the soil solution The concentrations of Ca, Mg and P in the soil solution increased with application of pig manure (Table 3). The highest Ca concentrations were found in the PM30 and L + PM30 treatments. This increase was attributed to the addition of soluble mineral elements in the pig manure. Wheat straw application also increased the concentrations of K, Mg and P in soil solution but had no signi cant e ect on the concentration of Ca. Application of CaCO 3 markedly increased Ca concentration and decreased the concentrations of P and Mn in soil solution Growth of plants Many experiments have shown that organic material application to Al-toxic soils may increase plant yield by decreasing the amount of toxic Al in the soil solution (Ahmad and Tan, 1986; Hue and Amien, 1989; Ostatek- Boczynski et al., 1995; Yu and Qin 1998). The present experiment demonstrated that application of pig manure or wheat straw increased signi cantly the height and dry weight of 15-day-old mung bean seedlings (Fig. 3). At the same application rates of organic materials, pig manure treatments produced signi cantly greater plant dry mass than did wheat straw. As expected, addition of lime at 1.5 g kg 1 markedly improved growth of mung bean seedlings, with height and dry weight increasing by 24.9% and 8.4%, respectively, compared with those of the control (Fig. 3). However, mixed treatment of pig manure and lime did not produce more dry matter than pig manure treatment alone, indicating that addition of lime may cause negative e ects on growth of mung bean in the presence of pig manure. It has also been con- Fig. 3. Height and dry weight of mung bean seedling as a ected by pig manure (PM), wheat straw (WS) and lime (L). rmed that adding N, P and K fertilizer alone to the same soil did not e ectively improve growth of mung bean (data not shown). This implies that both Al toxicity and nutrient de ciency are factors limiting plant growth in red soil. The relationships between yield of mung bean seedlings and various indices including soil ph, monomeric inorganic Al concentration, P concentration and Ca + Mg concentration in the soil solution are presented in Table 4. There was a signi cant relationship between the yield of mung bean seedlings and monomeric inorganic Al in the soil solution. The regression was improved by entering the concentrations of P in the soil solution. No signi cant relationship between the yield of mung bean seedlings and total Al concentration was found. Result suggested that the bene cial e ect of organic manure on mung bean growth is due to decreasing monomeric inorganic Al concentration and increasing P concentration in soil solution Al and mineral element concentrations in the leaves of mung bean There were large di erences between treatments in the Al concentration of mung bean leaves (Fig. 4). In L + PM treatment, leaf Al concentration was 356 mg kg 1, which was 39% of that in control plants. A higher correlation was obtained between Al concentration in the leaves of mung bean with monomeric inorganic Al concentration in the soil solution (Y ˆ 225:7 8:073x, r 2 ˆ 0:564 ; n ˆ 21) than that with total Al concentration in soil solution (Y ˆ 219:6 6:627x, r 2 ˆ 0:352 ; n ˆ 21). This suggested that monomeric inorganic Al in the soil might be a better index for Al toxicity than total Al in soil solution. Furthermore, a high Ca level in soil solution may reduce the uptake of Al from applications of organic materials or CaCO 3. Manganese toxicity is another important cause of poor crop growth on acid soils. Compared to the con-

5 Table 4 The relationships between yield of mung bean seedlings and various indices including soil ph, monomeric inorganic Al concentration, P concentration and Ca + Mg concentration in the soil solution Index Regression equation r 2 Soil ph y ˆ 0:843 0:02x a Total Al concentration y ˆ 1:03 1:4x a Monomeric inorganic Al concentration y ˆ 1:161 5:1x P concentration y ˆ 0:877 0:625x Ca + Mg concentration y ˆ 0:818 0:0194x a a NS: not signi cant. * P < ** P < Q.R. Shen, Z.G. Shen / Bioresource Technology 76 (2001) 235± Fig. 4. Aluminum concentration in the leaves of mung bean as a ected by pig manure (PM), wheat straw (WS) and lime (L). trol, a high rate of application of pig manure or wheat straw decreased leaf Mn concentration, but a low application rate had no signi cant e ect (Table 5). Liming or combining of lime and pig manure was more e ective in reducing leaf Mn concentration than application of organic materials (Table 5). One of the mechanisms of Al toxicity is Al disturbing mineral uptake and metabolism, especially that of P and Ca (Clarkson, 1966; Clarkson and Sanderson, 1971; Bengtsson et al., 1988). It is known that P, Ca and K de ciencies may occur under the high stress of Al toxicity. Mineral nutrient concentrations in leaves of 14-day-old seedlings were signi cantly a ected by the various treatments (Table 5). The concentration of P in mung bean leaves was lowest in the control and increased signi cantly with application of pig manure or wheat straw. Application of pig manure was more effective in increasing leaf P concentration than application of wheat straw. This is in accordance with the higher P concentration in the solution of soil treated with pig manure than in that of soil treated with wheat straw. A similar in uence of organic material such as millet straw and corncob compost on increasing P uptake has been reported (Kretzschmar et al., 1991; Chung and Wu, 1997). Phosphorus is the most growth-limiting mineral nutrient for plants in the red soil, due to the adsorption of P by Al and Fe±Mn oxides. Thus, it seems likely that the bene cial e ect of organic materials is related to improvement of P nutrition of mung bean, since organic materials increase solubility and thus mobility of P in the soil (Kretzschmar et al., 1991) by decreasing the adsorption of P onto the soil surface (Ohno and Erich, 1997). Toor and Bahl (1999) reported that poultry manure might chelate Al and Fe ions thereby transforming the mineral P towards higher solubility in the acidic soils. But, application of lime slightly decreased P concentration in leaves of mung bean. Kretzschmar et al. (1991) also found that liming Table 5 Mineral element concentrations in the leaves of 14-day-old mung bean grown on soil incubated with various levels of pig manure, wheat straw and CaCO 3 for 8 weeks a Treatment Ca (g kg 1 DM b ) K (g kg 1 DM) Mg (g kg 1 DM) P (g kg 1 DM) Mn (mg kg 1 DM) Control 14.0a 29.6a 2.39a 2.82a 786c 90b WS abc 36.7bc 2.95ab 2.55a 951c 98b WS ab 35.8b 3.65b 2.22a 323ab 76ab PM bc 40.1bc 5.23c 5.06b 745c 167c PM cd 42.5cd 6.89d 11.8d 525b 147c L 32.2e 23.9a 2.27a 3.27a 208a 57a L + PM d 48.1d 6.42d 8.88c 178a 98b a Means in the same column followed by di erent letters are signi cantly di erent at P < b DM: dry matter. Zn (mg kg 1 DM)

6 240 Q.R. Shen, Z.G. Shen / Bioresource Technology 76 (2001) 235±240 acid mineral soils or increasing ph by addition of organic materials did not necessarily lead to a short-term mobilization of soil P. A ph increase could result in a partial neutralization of exchangeable Al to hydroxy-al species and a precipitation of amorphous Al hydroxides, and thus in the formation of a highly active P adsorbing surface. The highest Ca concentration in leaves was found in the lime treatment (Table 5). Application of pig manure or wheat straw signi cantly increased the concentrations of K, Ca and Mg in mung bean leaves, with the e ect of pig manure being greater than that of wheat straw. This is in accordance with the higher concentrations of K, Ca and Mg in pig manure than in wheat straw (Table 2). The leaves of plants which received lime had the lowest K, Mg and Zn concentrations. Zn exhibited signi cantly higher leaf concentrations in the treatment with pig manure than in the treatments without organic materials added. Wheat straw application had no signi cant e ect on leaf Zn concentration. Poultry manure, crop straw, sewage sludge and compost have been used as organic fertilizers for centuries and have played an important role in increasing crop yield and maintaining the fertility of the soils in China. However, organic materials have been replaced greatly by chemical fertilizers over the last two decades. Recently, methods of treating poultry waste and crop straw have received considerable attention due to the rapid development of livestock and agriculture production. The present study demonstrated that organic material could be an economical alternative to chemical fertilizer to restore the soil nutrient balance and alleviate Al toxicity in red soil. The bene cial e ects of organic materials on crop growth and soil properties are directly related to the application rate and chemical composition of the organic manure. More experiments are needed to determine the optimum application rates of various organic materials under eld conditions. Acknowledgements This research was supported by National Natural Science Foundation of China ( ). References Ahmad, F., Tan, K.H., E ect of lime and organic matter on soybean seedlings grown in aluminum-toxic soil. Soil Sci. Soc. Am. J. 50, 656±661. Alva, A.K., Edwards, D.G., Asher, C.J., Blamey, F.P.C., E ects of phosphorus/aluminum molar ratio and calcium concentration on plant response to aluminum toxicity. Soil Sci. Soc. Am. J. 50, 133±137. Bengtsson, B., Asp, H., Jensen, P., Berggren, D., In uence of aluminum on phosphate and calcium uptake in beech (Fagus sglvaticee) grown in nutrient solution and soil solution. Physiol. Plant. 74, 299±305. Bessho, T., Bell, L.C., Soil solid and solution phase changes and mung bean response during amelioration of aluminum toxicity with organic matter. Plant Soil 140, 183±196. Chung, R.S., Wu, S.H., E ect of corncob compost on plant growth in an acid red soil. Commun. Soil Sci. Plant Anal. 28, 673± 683. Clarkson, D.T., E ect of aluminum on the uptake and metabolism of phosphorus by barley seedlings. Plant Physiol. 41, 165±172. Clarkson, D.T., Sanderson, J., Inhibition of the uptake and longdistance transport of calcium by aluminum and other polyvalent cations. J. Exp. Bot. 22, 837±851. Hue, N.V., Amien, I., Aluminum detoxi cation with green manures. Commun. Soil Sci. Plant Anal. 50, 1499±1511. Hue, N.V., Craddock, G.R., Adams, F., E ect of organic acids on aluminum toxicity in subsoils. Soil Sci. Soc. Am. J. 50, 28±34. Kochian, L.V., Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Physiol. Mol. Biol. 46, 237± 260. Kretzschmar, R.M., Hafner, H., Bationo, A., Marschner, H., Long- and short-term e ects of crop residues on aluminum toxicity, phosphorus availability and growth of pearl millet in an acid sandy soil. Plant Soil 136, 215±223. Menzies, N.W., Kerven, G.L., Bell, L.C., Edwards, D.G., Determination of total soluble aluminum in soil solution using pyrocatechol violet, lanthanum and iron to discriminate against microparticulates and organic ligands. Commun. Soil Sci. Plant Anal. 23, 2525±2545. Ohno, T., Erich, M.S., Inhibitory e ects of crop residue-derived organic ligands on phosphate adsorption kinetics. J. Environ. Qual. 26, 889±895. Ostatek-Boczynski, Z., Kerven, G.L., Blamey, F.P.C., Aluminium reactions with polygalacturonate and related organic ligands. Plant Soil 171, 41±45. Shen, Z.G., Wang, J.L., Guan, H.Y., E ect of aluminum and calcium on growth of wheat seedlings and germination of seeds. J Plant Nutr. 16, 2135±2148. Toor, G.S., Bahl, G.S, Kinetics of phosphate desorption from di erent soils as in uenced by application of poultry manure and fertilizer phosphorus and its uptake by soybean. Biores. Technol. 69, 117±121. Wong, M.T.F., Akyeampong, E., Nortcli, S., Rao, M.R., Swift, R.S., Initial responses of maize and beans to decreased concentrations of monomeric inorganic aluminum with application of manure or tree prunings to an Oxisol in Burundi. Plant Soil 171, 275±282. Wong, N.T.F., Nortcli, S., Swift, R.S., Method for determining the acid ameliorating capacity of plant residue compost, urban waste compost, framyard manure, and peat applied to tropical soils. Commun. Soil Sci. Plant Anal. 29, 2927±2937. Yu, G.T., Qin, S.C., E ect of organic manure on soil aluminum toxicity and nutrient absorption of winter wheat. Plant Nutr. Fert. Sci. 4, 57±62 (in Chinese). Zhao, F.J., McGrath, S.P., Crosland, A.R., Comparison of three wet digestion methods for the determination of plant sulphur by inductively coupled plasma atomic emission spectrometry (ICP- AES). Commun. Soil Sci. Plant Anal. 25, 407±418.

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