Soil Bid.

Biochem.

Pergamon

0038-0717(94)00188-x

Vol. 21, No. 415. pp. 431-439, 1995 Copyright 0 1995Elsevier Science Ltd

Printed in Great Britain. All rights resewed 003%0717/95 59.50+0.00

EFFICIENT MANAGEMENT OF SOIL AND BIOLOGICALLY FIXED N2 IN INTENSIVELY-CULTIVATED RICE FIELDS

D. K. KUNDU and J. K. LADHA*
Soil and Water Sciences Division, International Rice Research Institute, P.O. Box 933, 1099 Manila, Philippines Summazy-A decline in productivity in wetland rice has been detected in some intensively-cultivated experimental farms in Asia since the early 1980s. Increased doses of fertilizer N are being used in both experimental and farmers fields to maintain the original yield levels. Little attention has been paid to judicious management of native soil N, which is the principal N source for rice, and to biological N2 fixation (BNF), which largely replenishes the soil N concentration. We review here various effects of long-term flooding and puddling associated with intensive cultivation of wetland rice on soil N availability and BNF. Some strategies are suggested to efficiently manage these two N sources to sustain high productivity of the ricelands.

INTRODUCIION Rice is the most important food crop of the developing world. It is the staple food for more than 2 x lo9 people in Asia and for many millions in Africa and Latin America. To feed the increasing global population, the world s annual rice production must increase from the present 520 x lo6 t to 760 x lo6 t by the year 2020. Because increased rice production must come from the same or even less land area, productivity (yield ha- ) must be enhanced. Yield stagnation-or even decline-has been observed in some rice-growing areas of Asia since the early 1980s. Such disturbing trends have been clearly detected on experimental farms where 2-3 crops of wetland rice are grown annually without adequate drying and thorough preparation of the fields (Flinn and De Datta, 1984; Cassman and Pingali, 1994). Cassman and Pingali (1994) have discussed the extrapolation of these experimental farm observations to farmers fields. They observed that yield declines are commonly associated with decreased crop N uptake and that increasing doses of fertilizer N must be applied to maintain original yield levels. The management of native soil N, which is the principal N source for rice, and biological N2 fixation (BNF) may play an important role in sustaining the soil N pool under intensive cropping. Reviews have dealt with the N-supplying capacity of flooded soils (Sahrawat, 1983; Zhu, 1989) and the roles of BNF in rice production (Roger and Watanabe, 1986; Ladha et al., 1993). The effects of long-term flooding and puddling associated with intensive cultivation of wetland rice on the availability of soil N

and on BNF have not been considered. We address these issues in this paper.
CONTRIBUTIONOF SOIL N TO WETLANDRICE

*Author for correspondence.

The total N content of almost 80% of rice growing soils surveyed in Asia ranged from 0.08 to 0.15% with 1.8-7.0% of the total soil N mineralized during the cropping season and made available to the rice crop (Table 1). The amount of N mineralized in rice soils during a cropping season ranged from 57 to 80 kg ha- in the Philippines (Shiga and Ventura, 1976) to 52-107 kg ha- in China (Lu, 1981). N supplied by the soil is sufficient to produce rice yields of 2-4 t grain ha- in most situations. In South and Southeast Asia, about 10% of 152 test sites yielded more than 5 t ha- without fertilizer N (Bouldin, 1986). In highly-productive rice fields, the soil N supply pattern matches the crop N uptake pattern. The yield benefits from high native soil N fertility are difficult to replace with increased fertilizer N. Cassman et al. (1994) reported that hybrid rice yields in China on a soil with low native N fertility, where 245 kg fertilizer N ha- was applied, was 2.2 t ha- less than that obtained on a soil of high native N fertility where only 54 kg fertilizer N ha- was used. Applying N fertilizer generally enhances the N mineralization rate in the soil (Broadbent, 1979; Bouldin, 1986) and soil N uptake by wetland rice [Table 2; see also De Datta and Broadbent (1990)]. Data obtained from several field experiments under diverse soil and climatic conditions showed that a wetland rice crop supplied with adequate fertilizer N took up 45-l 13 kg soil N ha- , constituting 5693% of total crop N uptake (Broadbent, 1984). A study in Japan indicated that the rice crop depends totally on the soil to meet its N requirements from heading to maturity (Table 2).

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D.

K. Kundu and J. K. Ladha permit any significant decrease in the bulk BNF activity of wetland soils. Although surface applied urea may cause a short-term decrease in Nz fixation by blue-green algae (BGA) in floodwaters, it could stimulate BNF in the soil and the rhizosphere (Ladha et al., 1989). BNF thus plays crucial role in maintaining soil N fertility.
EFFECTS OF CONTINUOUS SUBMERGENCE AND PUDDLING ON SOME SOIL PROPERTIES AND N AVAILABILITY TO RICE

Table 1. Total N contents and their mineralization rates in some irrigated rice soils of Asia [source: Kawaguchi and Kyuma (1977)) Samples analysed (No.) 53 16 73 44 84 41 16 54 33 80 Mean values of total N (% of air-dried soil) 0.13 0.10 0.08 0.12 0.29 0.28 0.10 0.15 0.13 0.09 Mean ammonification (% of total N) 4.5 5.1 3.9 12.4 6.5 6.3 1.8 10.8 7.0 6.6

Countrv Bangladesh Cambodia India Indonesia Japan Malaysia, W. Myanmar Philippines Sri Lanka Thailand

ROLE OF BNF IN REPLENISHING

THE SOIL N POOL

Assuming that rice plants assimilate about 80 kg soil N ha- every growing season, it may be difficult to continue rice cropping for many years in a field where the plough layer contains only about 2-3 t N ha- . However, in subsistence single-cropping systems, wetland rice in many lowland areas of tropical Asia has been grown continuously for centuries with no N fertilizer and with no apparent decline in soil N content. The plains of Thailand are one such area and Firth et al. (1973) estimated that inputs of at least 40 kg N ha- y-l are required to balance the N removed by the crop. Of this, 6 kg ha- was accounted for from N in irrigation water and 5-6 kg N ha- in rain water. They assumed that BNF supplied the remaining 28 kg ha- . Three rice crops y- in the same area, received 33 kg ha- crop- from BNF (Walcott et al., 1977). N balance data of selected sites are given in Table 3. In the Philippines two crops of wetland rice received an apparent contribution of N from BNF of 59-103 kg N ha- y-l, whereas in Japan a single wetland rice crop followed by a fallow received 19-38 kg N ha- y-l. The balance sheet, however, indicates very little gain and even net losses of N under the fertilizer N treatments; this is attributed more to the loss of applied fertilizer N than to smaller BNF contribution. The short residence time of fertilizer N due to its fast microbial transformation and volatilization, generally does not

Rice is preferably grown in flooded and puddled fields as there are fewer weeds, soilborne pests and diseases, higher water use efficiency and enhanced availability of some nutrient elements. Maintenance of flooding in rice fields through a growing season also considerably reduces the loss of soil N by nitrification and denitrification. In intensively-cultivated fields, where 2-3 crops of rice are grown annually, Ponnamperuma (1985) found it preferable to not allow soil to dry in order to conserve soil N. These soil and water management practices, considered ideal for N conservation in wetland rice, now appear to be inefficient in the maintenance of long-term productivity of the soils.
Suboptimum water percolation rate

Continuous flooding and repeated puddling of the soil without thorough dry tillage drastically reduces its water percolation rate, often to about zero. Permeability is important in maintaining long-term fertility of ricelands as the percolation water carries dissolved O2 to the active root zone and dilutes or eliminates the toxic substances, renewing the soil environment. The percolating water, however, may carry some nutrients away from the rooting zone, making proper permeability essential for rice fields, the actual rates dependent on local conditions. The water percolation rates of most high-yielding rice fields have been reported to range from 2&30 mm d- in Japan (Takai and Wada, 1977) to 9-l 5 mm d- in the Jiangsu and Shanghai provinces of China (Yang and

Table 2. Contribution of N from different sources to the total N in rice plants at different growth stages* Isource: Wada et al. ( 1986)I Contribution to total slant N Growth stage Transplanting to necknode initiation Origin Soil N Soil N by prtming effect of fertilizer Basal N fertilizer Soil N Soil N by priming effect of Fertilizer Topdressed N fertilizer Soil N Soil N by priming effect of fertilizer Topdressed N fertilizer Soil N Soil N Soil N by priming effect of fertdizer Fertilizer N
II

Necknode initiation to late spikelet initiation

Late spikelet initiation to headmg

3 8 18 63 11 26

Heading to maturity Total

*Fertilizer N used: basal at 70 kg N ha- and 2 topdressings each at 25 kg N ha-

Soil N and BNF management in rice

Table 3. N balance in some continuously-cultivated

433

wetland rice soils of Asia [adapted from App er al. (1984) and Watanabe and Roger (1984)] N input Soil N change Plant uptake Balance

Site Aomori, Japan (41N) Ishikawa, Japan (36N)

Annual cropping pattern Wetland rice Wetland rice

Duration (Y) 21 22

Fertilizer treatment PK NPK Unfertilized PK PKCa NPKCa Unfertilized Unfertilized Unfertilized 0 57 0 0 0 100 12 12* 12* -20 -35

kg- N y-l 45 66 53 64 12 119 116 71 91 +25 -25 +19 +34 +38 +4 +103 +59 +19

-34 -30 34 -15 30t 20t 30t

Los Banos, Philippines (14N)

Maligaya, Philippines (16N)

Two wetland rices (lst-24th crops) Two wetland (24th-33rd crops) Two wetland ricw

12 5 8.5

*Contributions of rain and irrigation water. tIgnored because a different laboratory sampled and analysed the soil at the start of the trial. $No change of soil N observed; value is 1 SE of analysis.

Chen, 1961; Anon., 1978). Obviously, the optimum percolation rate varies with organic matter content of the soils and the bioclimate of the regions. Rates for rice fields in many other regions of Asia are still not known.
Development of gley horizons within the plough layer

were significantly (Table 4).

less in gley than in normal soils

Accumulation of toxic substances in the root zone

In the absence of adequate water percolation, regular incorporation of rice stubble into the field following harvest makes the plough layer of the soil rich in easily-decomposable organic substances and excessively reduced with accumulation of toxic materials. Altogether, these conditions may help in the development of gley horizons within the plough layer. In one such field in a Chinese average redox potential of the soil in plough layer decreased from 260 to 173 mV and its permeability declined from 7.8 to 1Smm d-l (Hseung et al., 1980). According to 1958 and 1978 soil surveys, the areas of gley rice soils in China have increased. Grain yield on these soils is usually 1S-2.5 t ha- I lower than that on normal soils (Pan et al., 1986; He et al., 1986). Lower rate of soil N mineralization Very low rates of soil organic matter decomposition and N mineralization in poorly-drained rice fields (with water percolation rates <5 mm d-l) were observed due to excessively reduced conditions (Takai and Wada, 1977; Kanke and Kanazawa, 1986). The rates enhanced with improvement in the drainage and disappearance of the gley horizons. He et al. (1986) observed that the rate (the ratio of crop N uptake to total N reserve in the plough layer) and the capacity (total N uptake in above ground plant parts at maturity in the non-fertilized plot) of N mineralization in rice soils with a strong gley layer developed from the Yuan River alluvium were only 53 and 62%, respectively, of those in a normal rice soil developed from the same parent material in the same area. As there was less mineralization, the contributions of soil N to total N uptake by fertilized crop

Intensive reduction and anaerobic decomposition of organic matter lead to a large accumulation of reducing substances in the soils, and this may strongly inhibit the absorption of N by rice plants (Table 5). The reducing substances include ferrous iron, nitrites, sulphides, alcohols, aldehydes, ketones, reducing sugars, aliphatic hydroxy and unsaturated acids, mercaptans, organic sulphides, ferulic acid, sinapic acid and many other unknown compounds (Ponnamperuma, 1972). Tanaka et al. (1990) detected various aliphatic and aromatic acids in the soil solution of rice fields amended with straw, and some of these organic acids, especially the aromatic acids, inhibited rice root elongation by as much as 30-70%.
Restricted N contribution of the subsoil

Continuously-submerged lands often are not thoroughly ploughed due to poor trafficability. Fields are prepared every season by shallow hydrotilling by rotary plough and puddling. Continuous practice of such brief land preparation helps develop a hard impervious soil layer, often at 15-20 cm depth, which may prevent rice roots from using the subsoil N. At the
Table 4. Comparative soil and fertilizer N uptake by rice in gley and normal soils developed from Yuan River alluvium. Hanan, China [source: He er al. (198611 N uptake by rice plants (mg plot- )* Soil type Gley Normal LSD (P=O.O5)t N fertilizer used Ammonium sulphate Urea Ammonium sulphate Urea Soil N Fertilizer N Total 209 274 345 388 60 157 168 159 156 NS 366 442 504 545 ND

Microplots (bottomless plastic tubes of 29cm diax 33cm high inserted in soil to about 20 cm depth) and sN-labelled fertilizers used, sampling done at maturity. tNS = not significant, ND = not determined.

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D. K. Kundu

and J.

K.

Ladha

Table 5. Comparative N uptake by rice in gley and normal soils developed from the same parent materials in the same area: Hunan, China [source: Pan et al. (1986)] Parent material Red clay Slate Total N (%) 0.28 0.15 0.23 0.19 Total reducing substances (mequiv 100 g-l) 5.0 2.3 6.0 2.3 N uptake by rice (mg pot-) 294 786 432 959

Soil type Gley Normal Gley Normal

Directorate of Rice Research in Hyderabad, India, this was associated with a significant reduction in yield and N uptake of rice (D. K. Kundu et al., unpubl. data).
Thinner plough layer or reduced soil bulk densit~~

The development of a thick hard pan makes the plough layer thinner. Long-term flooding and repeated puddling apparently may keep the original soil depth unchanged but considerable reduction in the bulk density of the soil may occur. At the International Rice Research Institute (IRRI) Farm, during the early tillering stage of the rice crop, the bulk density of the soilat& cmdepthisoften0.55 gem- inplotsunder continuous submergence, compared with 0.85 g cm- in plots which were allowed to dry regularly through the pre-rice season. In these circumstances, the concentration of N measured in the soil at the plough layer depth may not be a good index of N availability to rice, unless the reduction in bulk density is also considered. The decreased availability of soil N in such cases may be proportional to the reduction in bulk density. In one field experiment, rice yields and N uptake were similar on two blocks with widely different soil N concentrations, obviously due to the influence of the soil bulk density on N availability to wetland rice (Table 6). Hard pans within the soil profile were detected at comparable depths in both of the blocks.
EFFICIENT MANAGEMENT OF SOIL N IN WETLAND RICE

proportion of the soil microorganisms may die during the drying and rewetting periods (Kieft et al., 1987; van Gestel et al., 1991) with dead microbial cells becoming available for decomposition (Marumoto et al., 1977). The youthful state of the microbial population that develops after rewetting can be responsible also for part of the enhanced N mineralization (Birch, 1958; Soulides and Allison, 1961). The N flush may be partly explained also by an increase in the availability of organic substrates through desorption from soil surfaces (Seneviratne and Wild, 1985) and through an increase in the organic surfaces exposed (Birch, 1959). Recent research results suggest that drying and rewetting not only generate an N pool but also increase the mineralization rate of the more stable N pool in soil (Inubushi and Wada, 1987; Cabrera, 1993). Subjecting soil to a drying period in intensively-cultivated wetland rice fields, may be a mechanism by which each soil N pool is replenished from successively more recalcitrant or physically-protected N pools. Seasonal drying of fields also can maintain optimum physical, chemical and microbiological properties of the soil.
Conservation andrecycling of N03-Nformedduringsoil drying

Drying of soil following harvest of a flooded rice crop favours nitrification. In a survey of 28 Philippine lowland soils, NO,-N before flooding for rice ranged from 5 to 39 mg kg- (Ponnamperuma, 1985). Dryland crops grown during the dry period can assimilate this NO,-N and prevent its loss through leaching and denitrification after flooding of the soil. The assimilated N can then be recycled to the subsequent rice crop by incorporating the plant residues. Quick-growing green manure crops can be used for this purpose, with legumes like Sesbania rostrata assuming a more positive role in the conservation and recycling of soil NO,-N (George et aI., 1992).
Adoption of rational cropping systems

Drying of thefields through pre-rice seasons

Several factors may contribute to the N mineralization that follows rewetting of dry soils. A significant
Table 6. Effect of soil bulk density on N availability to wetland rice: IRRI Farm, 1991 dry season [source: J. K. Ladha eta/. (unpubl. data)] Parameter Bulk density* (g cm I) Total N concentration* (% of dry soil) 2 M KCl-extractable N concentration* (mg kg- dry soil) Amount of total N in the O-20 cm layer (kg ha- ) Amount of KCI-extractable N in the t&20 cm layer (kg ha ) Rice grain yieldt (t ha-) Total croo N uotaket (ka ha ) Block M 0.675 +O.O06t 0.170 * 0.004 Block N 0.885iO.010 0.120+0.004

54.023.5 2295 + 53 72.014.6 5.40 k 0.64 77.0 -t 9.1

35 oi2.2 2124+66 62.Ok3.5 5.4OkO.59 74.0 + 8.1

*Pertains to the soil at O-20 cm depth. tValues are mean f SE. :Average of 40 medium-duranon genotypes.

Soil N availability in intensively-cultivated ricelands may be considerably improved by ensuring adequate soil drying through adoption of rational cropping systems. In triple-rice cropping areas, one rice crop may be replaced by a suitable upland crop. A continuous system of rice-rice-barley has maintained a high and stable grain yield level in the last 18 y in the southern coastal plain of Zhejiang, China (Li, 1993). In double-rice cropping areas, a field drying period of at least 60 days y- can be ensured by planting appropriate rice varieties. However, the desired degree of soil drying may not be achieved with continuous double-rice cropping, and in such areas practising a thorough wet-dry land rotation system using only one rice and an upland crop after every 2 y or so could be beneficial. To overcome the stagnation in productivity in continuously-cropped wetland rice fields, similar multiple-cropping systems focusing on wet-dry

Soil N and BNF management in rice rotation were introduced in some experimental farms in China in the 1980s. After 5-6 y of practising such systems, significant improvements in soil fertility were recorded: prevention of formation of secondary gley layers in soil; improvement of soil physical properties; promotion of the growth of N&xing microorganisms; and enhancement of N availability (Xie, 1992). Use of subsoil N A survey of 34 high-yielding rice fields and their neighbouring rice fields in Korea revealed the important role of the deeper soil layers in determining wetland rice productivity (Table 7). Growth of rice roots and the depth of their distribution in the soil are closely related to the thickness of the ploughed layer (Lin, 1965). Sharma et al. (1988) reported a significant positive correlation between subsoil root density and rice grain yield. Wetland rice can derive a significant part of its N requirements from the subsoil. Sekiya and Shiga (1977) determined the contribution of subsoil N (by difference in plant N uptake in microplots with and without tetron-made cloth placed between the top and subsoil layers) to total N in unfertilized rice plants and found it to range from 22-30% in alluvial and diluvial soils to 30-35% in peat soils and 5% in volcanic ash soil. In the N-fertilized fields, the contribution of subsoil N to the rice plants was almost 14% in the volcanic ash soil, 15% in the diluvial soil and 22% in the alluvial soil. In a microplot experiment at IRRI, Ventura and Watanabe (1984) observed that about 40% of total soil N absorbed by the unfertilized rice plants could come from soil below the O-20 cm layer. Similarly, in microplot experiments conducted in the Tai Lake region of China, Chen and Zhu (1986) recorded a subsoil contribution of 1649% to the total soil N supply to rice plants. A positive correlation was found between the subsoil N contribution and the ratio of total N content in the subsoil to that in the topsoil + subsoil. In continuously-flooded and puddled fields, however, rice plants largely fail to make use of N from deeper soil layers due to the formation of either a hard impervious pan below the surface soil or to a negligible water percolation rate. Ongoing field studies at IRRI revealed that deep tillage can break the hard layers,

435

reduce soil penetration resistance, enhance mineralization of subsoil N and promote root growth and entry into deeper soil layers, thereby helping to achieve efficient utilization of subsoil N in wetland rice (D. K. Kundu and J. K. Ladha, unpubl. data). However, the fields need to be dried to provide a thorough and deep tillage operation with the positive effects of the tillage treatment lasting for more than one cropping season. The carryover effects of deep tillage at the IRRI Farm are currently being monitored.
EFFICIENT MANAGEMENT OF BNF SYSTEMS IN WETLAND RICE

Indigenous BNF

Diverse kinds of N2-fixing microorganisms (aerobes, facultative and strict anaerobes, heterotrophs, phototrophs, free-living and symbiotic) grow in wetland rice fields. The major indigenous N2-fixing agents include the BGA and photosynthetic bacteria that inhabit the floodwater and soil surface, the heterotrophic bacteria found in the rice root zone, and those in soil outside of the rhizosphere. From N balance studies, the contribution of indigenous BNF to wetland rice has been estimated to be 14-50 kg N ha- crop- (Roger and Ladha, 1992). Low pH, phosphorus deficiency, grazer populations and a high concentration of N in floodwater, resulting from broadcasting of fertilizer N, often limit the growth and efficiency of photosynthetic Nrfixers in rice fields. Alleviation of such conditions by application of lime, phosphate, b&ides and deep placement of fertilizer N could stimulate BNF (Roger and Watanabe, 1986), although the economic viability of these technologies must be determined. Controlling the populations of the Ostracoda and Pulmonata in rice fields by applying b&ides like crushed neem seeds (Azadiruchtu indica) and Perthane + Bayluscide can enhance BGA biomass and thereby increase BNF (Grant et al., 1986). A fertile rice soil consists of both aerobic and anaerobic zones that form a mosaic structure and maintains a dynamic equilibrium between aerobic and anaerobic bacteria with oxidation and reduction of chemical components. Several changes in soil properties resulting from intensive cultivation of

Table 7. DitTerences in some soil physical properties between high-yielding and neighbowing irrigated rice fields: Korea [source: Jo and Urn (1990)) Penetration resistancet (kg co-*) Rice field High-yielding Year 1983 1984 Mean 1983 1984 Mean Depth of plough layer (cm) 20. I 18.4 19.3 13.5 14.8 14.2 Root zone (cm) 39.4 32.9 36.2 28. I 25.0 26.6 T 4.8 3.8 4.2 6.1 4.9 5.6 s 6.5 5.1 5.8 9.9 8.2 9.0 Grain yield (t ha- ) 8.1 8.2 8.1 4.4 4.6 4.5

Neighbowing

*Average of 34 fields surveyed. tT = topsoil, S = subsoil.

436

D.

K. Kundu and J. K. Ladha volatilization, and the development of high ostracod populations that graze on the BGA are a couple of examples. Shifting from continuous wetland rice cropping to multiple-cropping systems focusing on wet-dry rotation increased the population of Nz-fixing microorganisms in the soil of some Chinese farms (Xie, 1992).

wetland rice (e.g. water, OZ, organic nutrient and toxin content) might exert a strong influence on the appearance, distribution and efficiency of certain N&ing microorganisms. Takai and Wada (1977) observed that the number of total bacteria and sulphate-reducers in submerged soil with no water percolation was much less than that in soil with a percolation rate of 20 mm d- . They suggested that water percolation stimulates the microbial activities of submerged soil as long as easily-decomposable organic substances are available to the microorganisms. In China, microbial populations in some gley rice soils ranged from (350-420) x IO*g-l organic matter, being l/S to l/3 of that in the well-drained rice soils (Gong and Xu, 1990). Suzuki et al. (1969) investigated the effect of tillage operations on the vertical distribution of several groups of microorganisms in rice fields and found that their growth and O2 uptake were effectively accelerated. Maintenance of the oxidizing power of rice roots or low O2 consumption by rhizosphere organisms are important for active N2 fixation in the rhizosphere. Enumerations of aerobic and anaerobic N,-fixing bacteria revealed a predominance of aerobic organisms in the rhizosphere. They constitute a large portion of the total bacterial population (Trolldenier, 1977). For example, 8 x lo6 aerobic and 1 x lo6 anaerobic N&ixers g- fresh root were recorded in rice variety IR 20 in addition to 18 x IO6 total saprophytic aerobic bacteria at one sampling date. At another sampling date, 255 x lo6 total bacteria, 59 x lo6 aerobic Nz-fixers and only 23,000 anaerobic Nrfixing bacteria were observed on the roots of variety IR 8 (Trolldenier, 1981). As nitrogenase is inactivated by OZ, it is understandable that aerobic Nz-fixers fix N2 more efficiently at subatmospheric OZ tension. Trolldenier (1977) observed that intermediate oxidative conditions in the rhizosphere are more favourable for Nz-fixation than excessive aeration or absence of 02. In acetylene reduction assays, rice plants grown in fields and in solution culture were tested for nitrogenase activity by incubating fresh roots at different O2 pressures. The activity was high at 3% 02, low at 0% and far lower at 21%. Watanabe et al. (1977) also reported the N2-fixing process to be microaerophilic. These reports suggest that excessive reduction of the soil could adversely affect BNF in rice. The N balance sheet of the Los Bafios site in Table 3 supports this contention. The apparent contribution of BNF there decreased from 103 kg N ha- ymin the first 12 y to 59 kg N ha- y- during the next 5 y. Moreover, intensification of crop monoculture is likely to reduce the diversity of species in microbial populations and help certain individual species dominate the rice fields. thereby directly or indirectly affecting the growth and activity of the Nz-fixers (Roger and Kurihara, 1991). The appearance of green algal blooms that not only lack the capacity to fix NZ but also enhance losses of applied fertilizer N by

Exogenous BNF

The fallow period of 45-60 days between 2 rice crops can be used to grow fast-growing leguminous green-manure crops (e.g. Sesbaniu and Crotoluria) or short-duration grain legumes (e.g. cowpea and mungbean). They usually accumulate 80-120 kg N ha- , and at least 50% of this amount comes from BNF (Ladha et al., 1992). The legume seeds may be sown in the field upon harvest of a rice crop and grown as dryland crops until the following rice season. The green-manure legumes or residues of the grain-legume crops may then be incorporated into soil as sources of N for the subsequent rice crop. Agronomic efficiency of legume-fixed and fertilizer N in rice were found comparable in the wet season (Kundu et al., 1991). Kundu and Pillai (1992) have suggested that in many double-rice cropped areas of India a short-duration grain legume could be accommodated during the fallow period to increase the annual grain productivity by 1 t ha- and make a net saving of 30 kg N ha- . The N saving results from BNF by the legumes, residues of which are incorporated into soil after harvesting of grains or pods. The Nrfixing aquatic fern Azollu can be grown as a cover crop with rice to incorporate into the soil as topdressing. The fresh weight for a mat of Azoflu is commonly 10 t ha- , which releases 20-30 kg N, at least 70% of which is derived from the atmosphere through BNF (Roger and Ladha, 1992). Watanabe et al. (1989) reported comparable N recovery by rice plants from Azollu-N and urea-N. Maintaining Azolla inocula between cropping seasons is a major constraint to its wider adoption by rice farmers. The inoculum required varies from 30&500 kg to 2-5 t fresh biomass ha- . The problem of maintaining Azolh vegetatively would be eliminated if mass quantities of spores could be obtained. Technologies to induce mass sporulation and efficiently harvest the spores have not been developed, although some research addresses this (Toia et al., 1987). Selection of superior germplasm, development of improved Azolla hybrids, and an understanding of the mechanism for inducing sporulation continue to remain the priority areas of research. In a continuous-cropping experiment at IRRI, where 2 rice crops were separated by either a fallow or a green-manure crop of Sesbuniu or A--o/la, much higher contributions of BNF were recorded in Sesbania and Azollu than in urea-treated plots (W. Ventura and J. K. Ladha, unpubl. data). The N

Soil N and BNF management in rice balance in the O-SOcm soil profile after 8 y showed annual gains of 106 kg N ha- under no-N (control), 56 kg N ha- under urea, 84 kg N ha- under Sesbania and 148 kg N ha- under Azollu treatment. The higher N gains in the Azoflu-treated plots could be due to regular application of phosphatic fertilizer, which enhances the growth and Nr8xing capacity of free-living microorganisms. However, the continuing subsidy on N fertilizers and several socioeconomic constraints presently make adoption of BNF technologies, particularly those of Azolla and legume green-manures, less attractive to rice farmers.
ROLE OF RICE GENOTYPES

431

without use of additional inputs. Traits associated with larger N-use efficiency and BNF stimulation, however, are complex and therefore difficult to manipulate.

CONCLUDINGREMARKS

Varieties differ in their ability to efficiently use soil N (De Datta and Broadbent, 1988) and support associative BNF (App et al., 1986; Ladha et al., 1988). Although associative N2 fixation contributes almost 20% of the total N uptake by rice (Watanabe et al., 1987; Zhu, 1989), it occurs mostly during heading (Ladha et al., 1988) when the availability of both soil and fertilizer N is low. Generally, the longer-duration rice genotypes utilize soil N more efficiently and also support the BNF better. In field experiments, the genotypes IR 15323-78-1-3-1, IR 21912-56-3-1-2-2 and IR 18349-135-2-3-2-1 were found consistently to be more efficient than IR 8455-78-l-3-3, IR 50 and IR 36 in utilizing soil N (De Datta and Broadbent, 1988). In recent studies, the uptake of soil N by selected genotypes ranged from 60 to 100 kg ha- crop- and the use efficiency ranged from 40 to 75 kg grain kg- N uptake. In a field experiment at the IRRI Farm, 8 out of 12 test genotypes proved efficient users of subsoil N. In a separate greenhouse experiment, soil N mineralization in the presence of rice plants was, on average, 61% greater than in unplanted soil (D. K. Kundu and J. K. Ladha, unpubl. data). Soil and plant N balance studies by App et al. (1986) showed significant differences in the ability of rice genotypes to support a positive N balance. Positive balances equivalent to 70 kg N ha- crop- were observed, 55 kg of which could be attributed to a genotype effect on BNF support or stimulation. In a recent pot experiment at IRRI using 15N-stabilized soil, genotypes differed in BNF by up to 35% (Wu et al., 1994). The long-duration variety IR42 consistently exhibited the larger BNF. Although the bases for genotypic differences in soil N use efficiency are not well-understood, Ladha et al. (1993) speculated that some of the following traits might determine the efficiency: the plant s ability to utilize subsoil N; the rhizospheric effect on soil N mineralization; the synchrony of crop N demand and soil N supply; BNF resulting from interaction of the roots and diazotrophs; and the plant s ability to efficiently translocate, distribute and redistribute the absorbed N to various organs. Breeding varieties that can efficiently take up and use soil N and have a larger BNF potential should enhance rice productivity

The physical properties of soils are generally considered unimportant in determining the fertility of wetland rice fields. Available research data suggest that deterioration of soil physical properties could create unfavourable chemical and microbiological environments in intensively-cultivated ricelands, and thereby reduce the availability of soil and biologicallyfixed N. Since the water percolation rate is a simple and reliable index of the soil physical conditions, optimum percolation rates for rice soils of different regions and situations should be determined. A significant role of the subsoil in supplying N to rice plants in wetlands has been identified. The subsoil N contribution is expected to vary widely with soil type in terms of their vertical profile development and also with some cultural management practices such as tillage. Detailed studies on the factors determining the subsoil N availability to rice should be undertaken. Reliable estimates of BNF by individual systems are available, but the total BNF in a rice field has not yet been estimated by measuring simultaneously the contributions of various components in situ. It is not known whether the activities of the different BNF systems are independent or interrelated. A method for estimating the contribution of BNF to rice nutrition in situ is lacking, and should be urgently developed. The accumulation of excessive amounts of reducing substances in the soil adversely affects soil N mineralization, BNF and N absorption by rice plants. These reducing substances have not been identified individually; their identification could improve our understanding of the specific limiting factors of N availability to rice in continuously flooded soils. The excessively reduced condition of the soil created by prolonged submergence could alter the nature and composition of organic matter considerably (Wang et al., 1981; Pan et al., 1986). The direct influences of such changes on soil N mineralization and on the growth and activities of N2-fixing microorganisms merit investigation. Providing thorough, dry tillage is effective in maintaining the optimum physical, chemical and microbiological properties and in sustaining high N fertility of rice soils. The optimum frequencies and depth for dry-tillage operations in rice fields need to be determined.
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