Microbial biomass, S mineralization and S uptake by African millet from soil amended with various composts

Soil Biology & Biochemistry 32 (2000) 845±852

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Microbial biomass, S mineralization and S uptake by African millet from soil amended with various composts Md. Akhter Hossain Chowdhury, Kenji Kouno*, Tadao Ando, Toshinori Nagaoka Faculty of Applied Biological Science, Hiroshima University, 1-4-4, Kagamiyama, Higashi-Hiroshima, 739-8528 Japan Accepted 15 November 1999

Abstract Microbial biomass growth, S mineralization after compost amendment (plant seeding) and S uptake by African millet at d 30, 60 and 120 (®rst, second, and third cutting, respectively) were monitored in an S-de®cient soil amended with cattle manure compost (CMC), saw dust compost (SDC) or rice husk compost (RHC) at the rate of 20 t haÿ1 in the presence or absence of growing African millet. A chemical fertilizer (CF) treatment at the rate of 30 mg gÿ1 soil along with a control (CT) was included for comparison. CMC produced a signi®cantly larger microbial biomass-C and -S than SDC or RHC. In the planted soil, during rapid growth of African millet, microbial biomass-S decreased more rapidly than in unplanted soil. Both biomass-C and biomass-S then showed a signi®cant ¯ush particularly at d 60±120 in all the treatments. CMC, RHC and SDC released 20, 10, and 8 mg CaCl2 extractable S gÿ1 soil, respectively, by d 5. Microbial biomass showed a marked increase in C-to-S ratio across the treatments which eventually reached 154 in the unplanted soil and 291 in the planted soil from an initial value of 64. Substantial mineralization of soil organic-S in all the treatments was observed during the period of greatest plant growth, but not in the absence of plants. Total S uptake was 37, 81 and 76% lower in the CMC, SDC and RHC amendment, respectively, than that of CF. CMC improved the S supplying potential of the soil, but addition of SDC or RHC (high C-to-S ratio) resulted in severe S de®ciency of plant due to S immobilization in soil. 7 2000 Elsevier Science Ltd. All rights reserved. Keywords: Microbial biomass; Compost; S mineralization; African millet; S uptake

1. Introduction Both plant and animal residues, either fresh or composted, are added to agricultural soils as a major source of organic inputs. These residues have a signi®cant role in maintaining soil organic matter content, microbial biomass and activity, and the size of the soil nutrient pool (Sanchez et al., 1989). Previous studies have shown large di€erences in S availability among residues. For example, cruciferous crops like rape provide a large and rapid release of available S (Wu et al.,

* Corresponding author. Tel.: +81-824-24-7966; fax: +81-824-240791. E-mail address: [email protected] (K. Kouno).

1993) but cereal residues release only minimal amounts of available S (Tabatabai and Chae, 1991; Wu et al., 1993). Lloyd (1994) concluded that animal manures are not a good source of plant available S. Incorporation of plant or animal residues of wide C-to-S ratios into soil normally immobilizes inorganic S, as the microbial biomass which develops on the decomposing material needs more S than is provided by the substrate (Chapman, 1997a). It is important to determine the e€ect of these residues on soil microbial biomass, S turnover and plant production. Goh and Gregg (1982) concluded that the major contributor to the actively cycling pool was S in plant residues and soil microorganisms. The mineralization of organic-S to SO4-S becomes critical for plant growth where atmospheric and fertili-

0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 2 1 4 - X

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zer S inputs are low. Recent studies suggest that the pattern of S mineralization from residues is very di€erent from that of N or other nutrients (Maynard, 1998). In many cases, S mineralization exhibits a rapid ¯ush of sulphate shortly after application of residues, followed by a very slow, linear phase of S release (Till et al., 1982). Most of the studies (e.g. Chapman, 1987b; Maynard et al., 1985; Tsuji and Goh, 1979) have indicated that S mineralization was increased in the presence of plants. In fact, sulphur immobilization together with the mineralization of organic-S regulates the accumulation and cycling of S in soil and a€ects S availability to plants (Freney and Williams, 1983; McGill and Cole, 1981). Assimilation and liberation of nutrients by and from the microbial biomass is supposed to make a considerable contribution to plant nutrition. The process of immobilization and mineralization are controlled by the dynamics of the conditions in the microbial environment. However, the dynamics of the immobilization process and the mechanisms through which immobilization is associated with microbial transformation remain poorly understood. Moreover, interrelationships between microbial biomass and the growing plant under which there are continuous inputs of C (Lynch and Whipps, 1990) and S (Rovira, 1969) from root exudation and root turnover have not been well studied. Organic S-containing compounds and biomass-S could be signi®cant and important sources of mineralizable-S (Banerjee and Chapman, 1996; Chapman, 1987a; Smith and Paul, 1990) particularly when the inorganic SO4-S content of the soil is very low but we have no clear understanding of their relative importance to plants. Cattle manure compost (CMC), saw dust compost (SDC) and rice husk compost (RHC) are common sources of organic amendment in the nutrient poor regosol of Japan. We used these three composts of di€erent C-to-S ratios to monitor: (1) the relationship between microbial growth and immobilization of S in the amended soils; (2) the release and subsequent availability of S from compost following incorporation into soil; and (3) the interrelationships between cropping, microbial biomass-S and S uptake by plant.

2. Materials and methods 2.1. Compost Three composts viz. cattle manure compost (CMC), saw dust compost (SDC) and rice husk compost (RHC), were obtained from Futaba Corporation, the Agriculture Center and the Agricultural Cooperative Association, respectively, Higashi-Hiroshima City, Japan. Some properties of the three compost are presented in Table 1. 2.2. Soil The soil used in the experiment was an S-de®cient sandy soil with 0.19% organic C, a C-to-N-to-S ratio of 43.7:9.5:1, CaCl2 extractable SO4-S 1.2 mg gÿ1 soil and pH (H2O) 4.2, collected from the Fukuyama Area of Hiroshima Prefecture, Japan. The soil had never received any fertilizer amendment. Bulk samples were air dried (208C), the undecomposed plant material removed and the soil sieved (2 mm). Samples were incubated aerobically at 258C and at 40% WHC for 10 days. This allowed the soil microbial population to stabilize, minimizing the e€ects of soil handling and preparation. 2.3. Pot experiment Fresh composts were added to the soil at the rate of 20 g kgÿ1 (oven dry basis) and then the equivalent of 4.2 kg oven-dried soil was placed in each Wagner pot (0.02 m2). Each treatment had four replications (two for planted and two for unplanted). The total number of pots were 100 {5(treatment)  2(planted)  2(unplanted)  5(samplings)}. Sulphur was applied as MgSO4.7H2O at the rate of 30 mg S kg ±1 soil. A basal dressing of 250 mg N (NH4NO3), 200 mg P and K (KH2PO4 or KCl), 10 mg Zn (ZnCl2), 2 mg Mn (MnCl2) 1 mg Cu (CuCl2) and 1 mg B (H3BO3) along with 2 g CaCO3 (to adjust soil pH at 6.0) kgÿ1 soil were added to each pot. Half of the pots were sown with 100 African millet (Eleusine coracana Gaertn, cv. Yukijirushi) seeds and half remained unplanted. The pots were incubated in a glasshouse maintained at 25±308C for 120 days

Table 1 Some characteristics of the cattle manure compost (CMC), saw dust compost (SDC) and rice husk compost (RHC) useda Compost

Organic C (%)

Total N (%)

Total S (mg gÿ1 compost)

Hot water soluble S (mg gÿ1 compost)

C:N:S ratio

CMC SDC RHC

36.3 43.3 37.2

1.81 1.89 0.97

4.2 1.7 1.3

1.40 0.13 0.06

86:4:1 255:11::1 286:7:1

a

All values expressed as oven dry basis and means of three replicate samples.

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between June and October, 1997. After 30 days, daytime temperatures tended to rise to 328C. The moisture content was maintained by daily additions of deionized water but varied between planted and unplanted soils. At intervals, four pots, two planted and two unplanted, were destructively sampled. As the plants were allowed to grow again after each cutting at d 30 and 60, the yields were added to the subsequent yield upon ®nal sampling. Soil samples were divided into two parts, one part was kept at 48C for 1 to 2 months for biomass analysis and the another was air dried and ®nely ground for total S analysis. Plant samples (shoot and root), except at d 10 where whole plant was used (due to very small size), were dried separately at 708C at least 48 h before weighing. The samples were then ®nely ground and stored for chemical analysis.

soil:water) and organic C of the air dried samples was determined using a carbon nitrogen analyzer (Yanaco MT 500). Total N was measured by the Kjeldahl method (Bremner and Mulvaney, 1982). All chemical analyses were made in triplicate and the results expressed on an oven dry weight basis.

2.4. Analytical

By d 5, the microbial biomass-C in the unplanted soil in the CMC, SDC and RHC amendments increased signi®cantly by 226, 178 and 165 mg C gÿ1 soil, respectively (Fig. 1a). However, in SDC, the microbial biomass-C had further increased by 19 mg C gÿ1 soil at d 10 and then gradually declined to an amount 69% greater than that in the unamended control by d 60. This amount was then maintained with a slight increase at the end of the experiment. There was no signi®cant di€erence of biomass-C between CF and control (CT) except a small increase in CF at d 5. Biomass-C in the planted soil behaved similarly to that of the unplanted soil until d 10. Thereafter, the growth of the African millet in¯uenced both microbial biomass and CaCl2 extractable-S. Biomass-C increased in all the treatments except SDC by d 30 and then declined at d 60 but maintained higher amounts compared to unplanted soil. At d 120, there was a sharp and signi®cant increase in biomass-C in all the treatments including control. The increase was most evident in CMC- and CF-treated pots (Fig. 1b).

Soil microbial biomass C (Wu et al., 1990) and S (Wu et al., 1994) were determined by the fumigation extraction (FE) method with 0.5 M K2SO4 and 10 mM CaCl2 as the extractant for biomass C and S, respectively. The microbial C (BC) was calculated from the equation: BC=2.22  EC where EC is (organic C extracted from the fumigated sample) minus (organic C extracted in the unfumigated samples). The extracted organic C was analyzed by a total organic C analyzer (Shimadzu TOC-5000). Biomass-S (BS) was calculated as BS=FS/KS, where FS is the di€erence between the S extracted from the fumigated and the S from the unfumigated soil and KS is the factor to convert FS to BS. The value of KS used was 0.31 (Wu et al., 1994). Total extractable S after H2O2 digestion and SO4-S following the removal of organic matter using activated charcoal (BDH Ltd DARCO G60; ca. 50 mg) were determined. The extractable organic-S was calculated from the di€erence between total extractable S and SO4-S. Hot water soluble S was extracted by hot water (1008C) for 1.5 h (Wu et al., 1993). Total S of soil was measured following the procedure of Steinbergs et al. (1962) but extracted with 10 mM CaCl2. Plants were digested by the method of Tabatabai (1992) for S analysis. Inorganic SO4-S in all soil extracts and plant digests was measured by ion chromatography (Toyosoda CM-8000) which was performed by resolving SO2ÿ 4 on a column (Toyosoda ICAnion-PW) using an eluent of 1.3 mM potassium gluconate, 30 mM boric acid, 1.3 mM sodium borate, 10% acetonitrile and 0.5% glycerol at a ¯ow rate of 1.2 ml minÿ1. The sample solution was ®ltered through a 0.45 mm cellulose acetate ®lter unit prior to injection into the ion chromatograph. Soil pH was measured with a glass electrode (1:2.5,

2.5. Statistical analysis A one-way ANOVA was performed to determine the signi®cant di€erences between treatments followed by test on LSD. 3. Results 3.1. Biomass C

3.2. Biomass-S Both in planted and unplanted soil, changes in microbial biomass-S in the compost amended soils followed the pattern similar to that of biomass-C. In the unplanted soil, the marked increase in the microbial biomass-S induced by the decomposition of compost resulted in the assimilation of 9.4, 3.5 and 4.2 mg S gÿ1 soil (Fig. 1c) in CMC, SDC and RHC treated pots respectively by d 5. From d 10 to the end of the incubation (120 days), biomass-S in all the compost amended soils and CF remained in amounts some 2 to 3.3 times greater than that in the control. In the planted soil, the pattern was similar until d 10, and then the biomass-S in all the treatments sharply declined below CT at d 30 and continued until d

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Fig. 1. Biomass C (a and b), biomass S (c and d) and biomass C-to-S ratio (e and f) as in¯uenced by cattle manure compost (CMC), saw dust compost (SDC), rice husk compost (RHC), chemical fertilizer (CF) and control (CT) in both unplanted and planted soil. Symbols for treatments: W, CMC; R, SDC; Q, RHC; *, CF; w, CT. Bars indicate LSD < 0.05.

60 (Fig. 1d). At d 120, there was again a signi®cant increase in biomass-S in the CMC, RHC and CF treatments except SDC where the biomass-S remained below control. 3.3. Biomass C-to-S ratio The biomass C-to-S ratio with an initial decrease either at d 5 or 10 in both planted and unplanted soil increased in all the treatments until d 60 and then decreased again at d 120. However, during the 120 days incubation, the C-to-S ratio of the biomass in the compost amended unplanted soil increased from 64 to 154:1 (Fig. 1e), in the planted soil from 64 to 291:1 (Fig. 1f). Although the C-to-S ratio in both planted and unplanted soil increased from 64 to over 290, that in the planted soil remained high until d 60. 3.4. CaCl2 extractable-S CaCl2 extractable total-S (SO4-S+org. S) in the

unplanted soil signi®cantly increased during the initial decomposition period following amendment (Fig. 2a). By d 5, the total CaCl2-extractable S in CMC, SDC and RHC treated pots were 19.9, 8.6 and 10.3 mg gÿ1 soil (Fig. 2a) of which the proportion of extractable organic-S was 31, 45 and 42% (data not shown) of the total, respectively. By d 10, the extractable total-S contents of all the compost amendments were signi®cantly

Fig. 2. CaCl2 extractable S in both unplanted (a) and planted (b) soil as in¯uenced by CMC, SDC, RHC, CF and CT. Symbols as for Fig. 1. Bars indicate LSD < 0.05.

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decreased and then remained constant until the end of the experiment except CF treatment where between d 30 and 60 extractable-S declined by a further 9 mg S gÿ1 soil (Fig. 2a). Between d 60 and 120, signi®cant increase in extractable-S was observed in CMC and CF treatments. In the planted soil, CaCl2 extractable-S, decreased rapidly between d 10 and 60, having fallen below 1 mg S gÿ1 soil in all the treatments except CMC where the amount was ca. 3 mg S gÿ1 soil which was maintained until the end of the experiment (Fig. 2b). 3.5. Dry matter yield, S concentration and uptake by African millet The yield of African millet shoots increased rapidly up to d 60 in CF and CMC treated pots and then slowly (Fig. 3a). But in RHC, the increase was slow and steady. In SDC, it was similar to control. However, the increase was 310, 269, 61, and 16% higher in CF, CMC, RHC and SDC than CT after 120 days. The root yield increased up to d 60 in CF and CMC and then decreased (Fig. 3b). In RHC, the increase was up to d 30 and then remained constant. But in SDC, it was parallel with CT until d 30 and then decreased at d 60 and remained constant up to d 120. The increase was 210 and 86% higher over control in CF and CMC, respectively at d 60. But at the same time the root yield decreased by 51 and 4% in the SDC and RHC treatment, respectively (Fig. 3b). The S concentration in the shoots of African millet in the CMC-treated pots increased rapidly up to d 10 and then slowly declined at d 60 and became constant thereafter (Fig. 3c). In the CF treatment, S concentration increased up to d 30 and then sharply declined at d 60. In RHC, SDC and CT, the increase was up to d 10, then sharply declined at d 30 and became constant until d 120. Root S concentration was sharply

Fig. 3. Shoot (a) and root (b) sulphur uptake by African millet as in¯uenced by CMC, SDC, RHC, CF and CT. Symbols as for Fig. 1. Bars indicate LSD < 0.05.

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increased in both CF and CMC but slowly in RHC, SDC and CT up to d 30 and then remained constant (Fig. 3d). Sulphur uptake was signi®cantly increased in both shoot and root treated with CF and CMC until d 30 and then slightly increased or decreased (Fig. 4a,b). In the RHC and SDC amendment, the uptake of S in shoot was not signi®cantly di€erent from control (CT) at any sampling time (Fig. 4a). The root uptake of S in the RHC amendment was signi®cantly higher over control until d 30 but in SDC, it was lower than that of control (Fig. 4b). However, the pattern was almost similar in both root and shoot from d 30 to 120. 4. Discussion 4.1. Biomass-C formation a€ected by compost amendment and plant growth The initial increase in biomass in amended soils (Fig. 1a±d) re¯ects the decomposition of the substrates during the early phase of incubation, although we could not measure CO2-C evolution in amended soils. The increase in biomass-C at d 5 is explained by the substrate added in the CMC, SDC and RHC treatment. The rate and extent of microbial assimilation of CMC-C and RHC-C is comparable to that found using starch amendments (Chapman, 1997b) while that of SDC with that of straw (Wu et al., 1993) or cellulose amendments (Saggar et al., 1981). The supply of carbon and energy from the decomposition of CMC or RHC to sustain the soil microbial biomass was reduced by d 10 resulting in a signi®cant decrease in biomass-C (88.6 and 100.6 mg C gÿ1 soil, respectively). On the other hand, though the initial increase in biomass-C in the SDC amendment was signi®cantly smaller over d 5, it was 30.5% higher than CMC by d 10 (Fig. 1a,b). This pattern of change in biomass-C in the SDC amended soil might be due to the gradual decomposition of SDC which provided a sustained supply of carbon and energy to maintain high amounts of microbial biomass over an extended period.

Fig. 4. Dry matter yield (a and b) and S concentration (c and d) of the shoot and root of African millet as in¯uenced by CMC, SDC, RHC, CF and CT. Symbols as for Fig. 1. Bars indicate LSD < 0.05 or 2SD.

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These results are in good agreement with those of Cogle et al. (1989) who explained that the labile fractions of straw were rapidly decomposed during the early phase and produced the labile microbial biomass. The resistant fractions (e.g. cellulose or hemicellulose) which were mineralized primarily during the later stages of incubation produced the slowly metabolizing microbial biomass. Though the C content of SDC and RHC is 7% and 1% higher than CMC (Table 1), the higher decomposition of CMC-C might be due to the lower C-to-S ratio (86:1). The higher amount of biomass-C in the planted soil (Fig. 1b) from d 30 onwards compared to unplanted soil might be due to root-derived available C during plant growth. Qian et al. (1997) reported that average daily production of root-derived available C was greatest during 4±8 weeks maize growth and 4±11% of the soil microbial biomass during that period and 15% at maturity came from this C source. Castellano and Dick (1991) also observed that cropping signi®cantly increased biomass-C over uncropped treatments. At d 120, the microbial biomass-C in all the treatments increased signi®cantly presumably by root exudates or root decay. There was evidence of root decay particularly in the CMC and CF treated pot after d 60 (Fig. 3b), possibly induced by the cut at d 30, though by this time the root system had fully explored the pot, making root recovery dicult. 4.2. Relationships between microbial biomass-S, available-S and S uptake by plant Increases in the biomass-S in the CMC, SDC and RHC amendments in the ®rst 5 days in the unplanted soil accounted for 11.2, 10.1 and 15.9% of the respective compost S added to soil (Table 1 and Fig. 1c). However, the release and subsequent immobilization of S largely depends on the C-to-S ratio of the added organic material (Chapman, 1997a) and their decomposability and S content. Each of the three composts irrespective of their decomposition rates, rapidly released S following incorporation into soil because major S-containing proteins and amino acids are very labile to soil microbial biomass and are decomposed prior to other resistant components (Wu et al., 1993). The increase was 23.7, 25.2 and 39.6% of the added CMC, SDC and RHC S, respectively (Table 1 and Fig. 2a,b). Fitzgerald and Andrew (1984) found that methionine S was rapidly converted to SO4-S and other forms of organic-S within 2 days of incorporation to soil. Fifty per cent of the CaCl2 extractable S in the SDC and RHC amendment and 30% in the CMC amendment was decreased by d 10 (Fig. 2a,b). Concomitantly, biomass-S was also decreased at the same time (Fig. 1c,d) which clearly suggests that some portion of

the extractable-S (mostly organic) was also incorporated by the declining biomass into the soil organic matter resulting in a net loss of plant available-S through microbial immobilization and transformation reactions. For the ®rst 10 days the biomass-S in the planted and unplanted soils behaved similarly. Subsequently, biomass-S in all the treatments declined between d 6 and 60 (Fig. 1c,d) which were not re¯ected by the increased concentrations of CaCl2 extractable-S over that period (Fig. 2a,b). Thus, our results support the ®ndings of Wu et al. (1993) and Eriksen (1997a) that once S was immobilized by the microbial biomass, it was directly transformed into soil organic-S and was not available to plants until it had been remineralized. Eriksen (1997b) found a rapid decrease in soil inorganic sulphate due to the addition of C equivalent to 10 t straw haÿ1. In the planted soil, during the rapid growth period of African millet from d 10 onwards until d 60, the decline in the biomass-S was much more prominent than the unplanted soil (Fig. 1d). It is likely that the biomass-S and CaCl2 extractable-S which were incorporated recently into soil organic matter between d 6 and 10 or 30 would remineralize between d 11 and 120 due to increased plant demand for S since recentlyformed organic-S is more readily mobilized than the bulk of organic-S in soils (Ghani et al., 1993). StankoGolden and Fitzgerald (1991) reported that the mobilization rates of very recently formed organic-S ranged from 27 to 57% dÿ1 in some tropical forest soils. In fact, soil organic-S was mineralized by 15.6, 4.8 and 10.7 mg S gÿ1 soil in the planted soil in CMC, SDC and RHC treated pots, respectively, between d 10 and 60 (data not shown) but not in the unplanted soil. However, this mineralized S was not re¯ected by the increase in CaCl2 extractable-S in the planted soil because of plant uptake (Fig. 2b). This con®rms observations that mineralization is increased by the presence of plants (Chapman, 1987b; Maynard et al., 1985) and at higher temperatures, usually more than 308C (Lee et al., 1985; Tabatabai and AL-Khafazi, 1980). The tendency for the planted soil to dry out more at higher temperature during growth period may have contributed to the plant e€ect. The signi®cant increase in biomass-S at d 120 (Fig. 1d) could be derived from root decomposition induced by the cut at d 30 or the presence of ®ne root materials which were undoubtedly left in the soil though roots were separated from the soil before analysis. Perrott and Sarathchandra (1990) found that such root material contributed to measured microbial biomass-S by 22%. Similarly, Perrott et al. (1992) reported a 19% contribution from roots and concluded that seasonal variations could be due to changes in root growth or amount of root material

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present in the soil. In our experiment, root dry matter was signi®cantly reduced at d 120 to almost half of the highest amounts at d 60 particularly in CF and CMC treatments (Fig. 3b). The initial decrease in biomass C-to-S ratio in both planted and unplanted soil at d 5 might be due to the immobilization of compost-S into the biomass. Thereafter the increase in biomass C-to-S ratio in the unplanted soil was small (Fig. 1e) and remained below control and probably does not indicate S de®ciency in the soil micro¯ora except SDC amendment. But in the planted soil, the biomass C-to-S ratio of the SDC treatment increased to 291 (Fig. 1f) at d 30 indicating possible severe S limitation for both biomass as well as plant. Actually, there is little information on what C-to-S ratio of the soil biomass might indicate S limitation. In our experiment, the biomass C-to-S ratio in the unplanted soil increased from 64 to 154 and in the planted soil up to 291. In a similar experiment with 35 S labelled ryegrass residues Chapman (1987b) found that the C-to-S ratio in the unplanted soil increased from 59 to a maximum of only 152 while that in the planted soil the C-to-S ratio reached a maximum of 262. Kouno and Ogata (1988) have given the critical concentration of SO4-S in plants associated with 60% of maximum yield of African millet as 160 mg gÿ1 while Smith et al. (1985) found the critical concentration to achieve 90% of maximum yield for S in perennial rye grass as 0.18%. Cowling and Jones (1970) reported that S concentrations of less than 0.2% were associated with de®ciency symptoms. In our experiment, this was reached in SDC and RHC by d 30 (Fig. 3c), hence S de®ciency appeared in both plant and microbial biomass in the SDC and RHC treated pots at approximately the same time. At d 30, in the planted soil, CaCl2 extractable total S (organic+SO4-S) had fallen to 0.53 mg gÿ1 (Fig. 2b) in both SDC and RHC treated soil which initiated S de®ciency in both biomass and African millet. Since all other nutrients were added in sucient amounts to the soil, the growth of the African millet in RHC, SDC and control treated pots were severely reduced by S de®ciency (Fig. 3c,d) because of the very low concentration (4.3, 2.5 and 3.0 mg S gÿ1 soil, respectively) of CaCl2-extractable S (Fig. 2b) from d 10 onwards. Thus, the total S uptake of African millet in RHC and SDC treated pots was 81 and 76% lower (Fig. 4a,b) at d 120 than that of the CF treatment where S was sucient. In a ®eld experiment, White (1984) reported decreased yield and S uptake of cereals as a result of S de®ciency induced by straw incorporation. Sulphur uptake by African millet in the CMC treated pot was signi®cantly higher among the compost treatments due to higher amounts (14.0 mg S gÿ1

851

soil) of extractable S and was only 37% lower than that of CF at the end of the experiment (Fig. 4a,b).

5. Conclusion The incorporation of CMC (C-to-S ratio: 86) into an S-de®cient soil would directly provide plant available S and improve the S supplying potential of the soil. In contrast, the addition of SDC or RHC (C-to-S ratio: 255, 286) could result in severe S de®ciency in soil and limitation of plant growth due to a net loss of plant available S through microbial immobilization and transformation reactions. It is, therefore, advisable to use supplemental S fertilizers during the incorporation of materials of high C-to-S ratio in soils of low available S contents to prevent S de®ciency.

Acknowledgements We would like to acknowledge the Ministry of Education, Science, Sports and Culture of the Government of Japan for ®nancial assistance.

References Banerjee, M.R., Chapman, S.J., 1996. The signi®cance of microbial biomass sulphur in soil. Biology and Fertility of Soils 22, 116± 125. Bremner, J.M., Mulvaney, C.S. 1982. Total nitrogen. In: Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis, 2nd ed. Soil Science Society of America, Madison, pp. 595±624 Part 2. Castellano, S.D., Dick, R.P., 1991. Cropping and sulphur fertilization in¯uence on sulphur transformations in soil. Soil Science Society of America Journal 55, 114±121. Chapman, S.J., 1987a. Microbial sulphur in some Scottish soils. Soil Biology & Biochemistry 19, 301±305. Chapman, S.J., 1987b. Partitioning of ryegrass residue sulphur between the soil microbial biomass, other soil sulphur pools and ryegrass (Lolium perenne L.). Biology and Fertility of Soils 5, 253±257. Chapman, S.J., 1997a. Barley straw decomposition and S immobilization. Soil Biology & Biochemistry 29, 109±114. Chapman, S.J., 1997b. Carbon substrate mineralization and S limitation. Soil Biology & Biochemistry 29, 115±122. Cogle, A.L., Sagna, P.G., Strong, W.M., 1989. Carbon transformations during wheat straw decomposition. Soil Biology & Biochemistry 21, 367±372. Cowling, D.W., Jones, L.H.P., 1970. A de®ciency in soil sulphur supplies for perennial ryegrass in England. Soil Science 110, 346± 354. Eriksen, J., 1997a. Sulphur cycling in Danish agricultural soils: Turnover in organic-S fractions. Soil Biology & Biochemistry 29, 1371±1377. Eriksen, J., 1997b. Sulphur cycling in Danish agricultural soils: Inorganic sulphate dynamics and plant uptake. Soil Biology & Biochemistry 29, 1379±1385. Fitzgerald, J.W., Andrew, T.L., 1984. Mineralization of methionine

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sulphur in soil and forest ¯oor layers. Soil Biology & Biochemistry 16, 556±570. Freney, J.R., Williams, C.H. 1983. The sulphur cycle in soil. In: Ivanov, M.V., Freney, J.R. (Eds.), The Global Biogeochemical Sulphur Cycle. SCOPE/UNEP Workshop, Pushchino, pp. 129± 201. Ghani, A., McLaren, R.G., Swift, R.S., 1993. Mobilization of recently formed soil organic sulphur. Soil Biology & Biochemistry 25, 1739±1744. Goh, K.M., Gregg, P.E.H., 1982. Field studies with radioactive sulphur-labelled gypsum-fertilizer. III. Sulphur pools and their signi®cance. New Zealand Journal of Science 25, 135±139. Kouno, K., Ogata, S., 1988. Sulphur-supplying capacity of soils and critical sulphur values of forage crops. Soil Science and Plant Nutrition 34, 327±339. Lee, R., Blackemore, L.C., Dale, B.K., Gibson, E.J., Speir, T.W., Orchard, V.A., 1985. Sulphur supply to ryegrass during a pot trial and correlation with soil biological activity: the in¯uence of two di€erent methods of determining the adsorbed sulphate status of soils. Communication in Soil Science and Plant Analysis 16, 97±117. Lloyd, A., 1994. E€ectiveness of cattle slurry as a sulphur source for grass cut for silage. Grass Forage Science 49, 203±208. Lynch, J.M., Whipps, J.M., 1990. Substrate ¯ow in the rhizosphere. Plant and Soil 129, 1±10. Maynard, D.G., 1998. Sulfur in the Environment. Marcel Dekker, New York, p. 16. Maynard, D.G., Stewart, J.W.B., Bettany, J.R., 1985. The e€ects of plants on soil sulphur transformations. Soil Biology & Biochemistry 17, 127±134. McGill, W.B., Cole, C.V., 1981. Comparative cycling of organic C, N, S and P through soil organic matter. Geoderma 26, 267±286. Perrott, K.W., Sarathchandra, S.U., 1990. Seasonal variations in soil S ¯ush and possible contributions from plant roots in the measurement of soil microbial sulphur, phosphorus, potassium and nitrogen. Australian Journal of Soil Research 28, 747±753. Perrott, K.W., Sarathchandra, S.U., Dow, B.W., 1992. Seasonal and fertilizer e€ects on the organic cycle and microbial biomass in a hill country soil under pasture. Australian Journal of Soil Research 30, 383±394. Qian, J.H., Doran, J.W., Walters, D.T., 1997. Maize plant contributions to root zone available carbon and microbial transformations of nitrogen. Soil Biology & Biochemistry 29, 1451±1462. Rovira, A.D., 1969. Plant root exudates. Botany Review 35, 35±57. Saggar, S., Bettany, J.R., Stewart, J.W.B., 1981. Sulphur transformations in relation to carbon and nitrogen in incubated soils. Soil Biology & Biochemistry 13, 499±511. Sanchez, P.A., Palm, C.A., Szott, L.T., Cuevas, E., Lal, R. 1989.

Organic input management in tropical agro-ecosystems. In: Coleman, D.C., Oades, J.M., Uehara, G. (Eds.), Dynamics of Soil Organic Matter in Tropical Ecosystem. NifTAL Project, University of Hawaii Press, Honolulu, pp. 125±152. Smith, J.L., Paul, E.A., 1990. The signi®cance of soil microbial biomass estimations. In: Bollag, J.M., Stotzky, G. (Eds.), Soil Biochemistry, vol. 6. Marcel Dekker, New York, pp. 357±396. Smith, J.S., Cornforth, I.S., Henderson, H.V., 1985. Critical leaf concentrations for de®ciencies of nitrogen, potassium, phosphorus, sulphur and magnesium in perennial ryegrass. New Phytologist 101, 393±410. Stanko-Golden, K.M., Fitzgerald, J.W., 1991. Sulphur transformations and pool sizes in tropical forest soils. Soil Biology & Biochemistry 23, 1053±1058. Steinbergs, A., Iismaa, O., Freney, J.R., Barrow, N.J., 1962. Determination of total S in soil and plant materials. Analytica Chemica Acta 27, 158±164. Tabatabai, M.A. 1992. Methods of measurement of sulphur in soils, plant materials and waters. In: Howarth, R.W., Stewart, J.W.B., Ivanov, M.V. (Eds.), Sulphur Cycling on the Continents, SCOPE 48. John Wiley, Chichester, pp. 307±344. Tabatabai, M.A., Al-Khafazi, A.A., 1980. Comparison of nitrogen and sulphur mineralization in soils. Soil Science Society of America Journal 44, 1000±1007. Tabatabai, M.A., Chae, Y.M., 1991. Mineralization of sulphur in soils amended with organic wastes. Journal of Environmental Quality 20, 684±690. Till, A.R., Blair, G.J., Dalal, R.C. 1982. Isotopic studies of the recycling of carbon, nitrogen, sulphur and phosphorus from plant material. In: Freney, J.R., Galbally, I.E. (Eds.), Cycling of Carbon, Nitrogen, Sulphur and Phosphorus in Terrestrial and Aquatic Ecosystems. Springer-Verlag, Berlin, pp. 51±59. Tsuji, T., Goh, K.M., 1979. Evaluation of soil sulphur fractions as sources of plant available sulphur using radioactive sulphur. New Zealand Journal of Agricultural Research 22, 595±602. White, P.J., 1984. E€ects of crop residue incorporation on soil properties and growth of subsequent crops. Australian Journal of Experimental Agriculture and Animal Husbandry 24, 1567±1573. Wu, J., Joergensen, R.G., Pommerening, B., Chaussod, R., Brookes, P.C., 1990. Measurement of soil microbial biomass by fumigation-extraction Ð an automated procedure. Soil Biology & Biochemistry 22, 1167±1169. Wu, J., O'Donnel, A.G., Syers, J.K., 1993. Microbial growth and sulphur immobilization following the incorporation of plant residues into soil. Soil Biology & Biochemistry 25, 1567±1573. Wu, J., O'Donnell, A.G., He, Z.L., Syers, J.K., 1994. Fumigationextraction method for the measurement of soil microbial biomass-S. Soil Biology & Biochemistry 26, 117±125.