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Published online 3 May 2006
Published in Agron J 98:698-704 (2006)
DOI: 10.2134/agronj2005.0173
© 2006 American Society of Agronomy
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Sugarcane

Microbial Biomass Turnover in Indian Subtropical Soils under Different Sugarcane Intercropping Systems

Archna Suman*, Menhi Lal, A. K. Singh and Asha Gaur

Division of Crop Production, Indian Inst. of Sugarcane Research, Rae-Barely Rd., P.O. Dilkusha, Lucknow-226 002 (UP), India

* Corresponding author (archsuman{at}yahoo.com)

Received for publication June 9, 2005.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Changes in soil organic C (Corg), total N (Nt), available nutrients, soil microbial biomass C (Cmic) and N (Nmic), and mineralizable C and N in the sugarcane (Saccharum officinarum L.) rhizosphere were evaluated under intensive sugarcane cropping systems with intercrops including wheat (Triticum aestivum L.), maize (Zea mays L.), rajmash (Phaseolus vulgaris L.), green gram [Vigna radiata (L.) R. Wilczek var. radiata], cowpea [Vign aunguiculata (L.) Walp.], lentil (Lens culinaris Medik.), mustard (Brassica rapa L.), potato (Solanum tuberosum L.), and sesbania (Sesbania rostrata Bremek. & Oberm.) in subtropical soils of India. Organic C increased significantly when maize (25%), wheat (24%), mustard (19%), potato (17%), and rajmash (13%) were intercropped with sugarcane, while legume intercrops substantially increased Nt and available N. Increase in microbial respiration was greater where maize (42%), wheat (37%), or mustard (31%) were intercropped compared with pulse crops. Soil microbial biomass C accounted for 2.7 to 3.3% of Corg content and Nmic accounted for 2.6 to 3.7% of Nt under different intercropping conditions. A higher CO2 evolution rate and wider Cmic/Nmic ratios were recorded with cereal and mustard intercrops, whereas higher N mineralization was recorded with pulse intercrops. Results indicate that intercropping with pulse crops and incorporation of their labile C substrate improved N mineralization. The build up of the C pool and Cmic in the case of cereals, mustard, and potato intercropping should promote long-term stability.

Abbreviations: Cmic, soil microbial biomass carbon • Corg, organic carbon • Nmic, soil microbial biomass nitrogen • Nt, total soil nitrogen • qCO2, metabolic quotient


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
SUGARCANE, an important agroindustrial crop in India, with a productivity level of 300 Tg from an area of 4.22 million ha, plays a pivotal role in the national economy; however, plateauing yield levels, declining productivity factors, increasing production costs, and slashed sugarcane prices in the industrial market in recent years pose a real concern and necessitate crop diversification in sugarcane-based production systems (Lal and Singh, 2004). Crop diversification increases resource use, reduces production costs, and improves or maintains soil quality in intensive agriculture systems (Andersen et al., 2004). In the subtropical belt of India, autumn sugarcane is planted at a 90-cm spacing. Due to the wider row spacing and initial slow growth rate of sugarcane, there is ample scope for intercropping in sugarcane. In addition, sugarcane generates income only one time due to its long crop duration. Therefore, inclusion of short duration, high value, and midseason income-generating intercrops should provide economic as well as nutritional security, especially for small and marginal cane growers. For management of intercrops in sugarcane, a World Bank funded NATP (National Agricultural Technology Project) study was undertaken at the Indian Institute of Sugarcane Research, Lucknow, India. Different intercrop options in sugarcane were studied, so that adoption of these techniques can make sugarcane production sustainable for improved yields and soil quality (Lal and Singh, 2004).

Phenological differences may allow crops to use resources at different times in the growing season (Fukai and Trenbath, 1993; Willey et al., 1983). Plants compete strongly for some nutrients, but intercrops can provide complementary and facilitating resource use and greater overall yields as opposed to single crops. Nitrogen fixation by legume intercrops or phosphate acquisition by intercrops with mychorrhizal associations are examples of the potential of complementary resource use by intercrops. Facilitation is the mechanism by which some plant species may have a positive impact on the performance of others. Such beneficial interaction could be the result of increased resource availability through root-induced changes in the rhizosphere (Ae et al., 1990; Horst and Waschkies, 1987; Marschner et al., 1986; Vandermeer, 1990), increased standing ability brought about by the physical support provided by one species to the other, reduced weed pressure through shading or allelopathic influence (Midmore, 1993), or reduced pest attack and pathogen infection through greater biological control in intercrops (Mitchell et al., 2002; Trenbath, 1993).

Soil quality has been defined as the capacity of a soil to function within ecosystem boundaries to sustain biological productivity, maintain environmental quality, and promote plant and animal health (Doran and Parkin, 1994; Staben et al., 1997). To evaluate soil quality, key biological and chemical indicators need to be evaluated for their sensitivity to changes in the management of disturbances. Soil microbial biomass is a sensitive indicator of soil quality and is influenced by many ecological factors such as plant community composition, soil organic matter level, moisture, and temperature (Jenkinson and Ladd, 1981; Wardle, 1992). Soil microbial biomass C comprises only 1 to 4% of Corg (Anderson and Domsch, 1989; Sparling, 1992) but, due to its fast turnover time, the microbial biomass plays a key role in controlling nutrient cycling and energy flow (Jenkinson and Ladd, 1981; Li and Chen, 2004). The microbial metabolic quotient (qCO2) has been used as a bioindicator of environmental stress on microbial communities (Anderson and Domsch, 1990, 1993), disturbances, and ecosystem development (Wardle and Ghani, 1995).

The quality and quantity of plant residues play an essential role in the cycling of nutrients in an agricultural ecosystem. Because sugarcane is nearly a 12-mo crop, it provides enough time for crop residue recycling, thus maintaining soil quality in terms of nutrients, microbial biomass, and activity in the soil. Knowledge is limited about how crop species diversity affects soil microbial activity and nutrient availability to a sugarcane crop. Under an NATP project, the present study was undertaken to monitor: (i) the effect of different intercrops on soil organic matter and nutrient availability; (ii) changes in microbial biomass and C and N mineralization in sugarcane soil; and (iii) and the interactions among different soil quality parameters under different sugarcane intercropping systems.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
The Site and Field Experiment
The study site, a research farm of the Indian Institute of Sugarcane Research, Lucknow, India, is located at 26°5' N, 80°6' E and 111 m above sea level. The local climate is characterized by two distinct seasons: a very hot summer from April to September with maximum temperatures up to 42°C, and a cool period from October to March with minimum temperatures as low as 7°C. Mean annual rainfall was ~908 mm in the year of this study and nearly 87% of total rainfall was received by northwest monsoons during June to September. The soil of the experimental site is noncalcareous sandy loam (13.3% clay, 24.5% silt, and 62.2% sand) of Indo-Gangetic alluvial origin, well drained, flat, and classified as a mixed, hyperthermic Udic Ustochrept with a pH of 7.2. Before planting sugarcane, in the second week of October, soil samples were drawn from the 0- to 15-cm soil layer by a core sampler of 8-cm diameter at six places in the experimental fields. The samples were thoroughly mixed and bulked, and a representative sample was drawn for initial biological and chemical analysis. The field experiment established to study the management of intercrops in sugarcane included wheat (cv. UP2338), maize (cv. Azad Uttam), rajmash (cv. PDR-14), green gram (cv. PM-11), cowpea (cv. Pusa komal), lentil (cv. DPl-15), mustard (cv. Pusa-Jaikisan), potato (cv. Kufri Ashoka), and sesbania as intercrops. The sugarcane crop was planted in October in a randomized complete block design with three replications for each treatment. Each plot was 5.4 by 6 m, with sugarcane planted at 90-cm row spacing, for which three budded sets of cv. CoS94257 were used. In between two rows of planted cane, two or three rows of an intercrop were sown. Sowing, harvesting, crop geometry, and fertilizer applications are given in Table 1.


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  		Table 1. Crop culturing summary for different intercrops.

 
Soil Sampling and Analysis
Soil sampling was done in September of the following year, which matches with growth maxima (grand growth stage) of the sugarcane crop. From each experimental plot, five soil samples were taken randomly from the 0- to 15-cm depth near the root zone of the standing crop using a core sampler of 8-cm diameter; the samples were thoroughly mixed and bulked. After removing visible plant residues and pebbles, a representative soil sample was passed through a 2-mm-mesh sieve and stored in plastic bags at 4°C. All measurements were conducted within 45 d of sampling. Before measuring microbial activities, soil moisture was adjusted to 60% of water holding capacity and samples were preincubated for 2 d at 28°C.

Soil samples were analyzed for total Corg by the Walkley and Black method, Nt by the micro-Kjeldahl method, extractable N using 2 M KCl, extractable P using 0.5 M NaHCO3, and extractable K using NH4OAc (1:6 soil/solution) following Page et al. (1982). Soil microbial biomass C and N were determined using the chloroform fumigation–incubation method (Jenkinson and Powlson, 1976). Mineralizable C (respiration rate) and N were estimated from the quantities of CO2–C and NH4+–N and NO3––N, respectively, that were mineralized from unfumigated samples during a 30-d incubation. All the incubation experiments were conducted at 28°C. To determine basal respiration, 50 g of unfumigated soil was incubated in 1-L air-tight sealed jars along with a small flask containing 10 mL of 1 M NaOH. Evolved CO2–C trapped in NaOH was measured after 10 d by titrating it with 1 M HCl. To determine N mineralization, pre- and postincubated samples were extracted with 2 M KCl and the soil extract was analyzed for mineral N using steam distillation and the micro-Kjeldahl technique (Bremner and Keeney, 1965). Net N mineralization rates were calculated by subtracting preincubation mineral N from the postincubation mineral N concentration and dividing the result by the number of incubation days.

Calculations and Statistical Analysis
Data are expressed on an oven-dry soil weight basis. Correlation coefficients were calculated to assess the interrelationships between the different parameters measured. One-way analysis of variance with Duncan's multiple-range test as a posthoc analysis was used to compare the means (Snedecor and Cochran, 1967).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Soluble Organic Carbon, Total Nitrogen, and Inorganic Nutrients
The amount of soil Corg was generally greater in all treatments than its initial status; however, it was not significant for sugarcane alone or with the sesbania intercrop. A significant increase in soil Corg was recorded in sugarcane plots where maize (25%), wheat (24%), mustard (19%), potato (17%), and rajmash (13%) were included as intercrops, compared with sugarcane alone (Table 2). There was no significant improvement in soil Corg where pulse crops (except rajmash) were included as intercrops, contrary to Nt, which increased significantly only in these treatments. There was an increase of 9 to 39% in Nt due to various intercrops compared with the initial status of Nt in the soil, whereas for sugarcane alone, Nt was reduced by 11%. The greatest increases in Nt were recorded in plots where rajmash (56%), lentil (51%), cowpea (46%), green gram, and sesbania (38.5%) were intercropped (Table 2). The decline in Nt under sugarcane alone might be due to the lack of the additional dose of chemical N given for the intercrop and also the resultant biomass due to various intercrops. Under intercropping conditions, Corg had a negative correlation with Nt (–0.030) but a positive correlation (0.229) with inorganic available N; however, a strong positive correlation (0.618) was found between Nt and available N (Table 4). This indicates that, with more Nt, the availability of available N had increased; during the buildup of Corg, however, Nt probably is being continuously used for degradation of plant residues. Although any permanent change in soil organic matter is a very slow process, the soluble and intermediate C pool is easily affected by cultivation, amendments, and weather conditions (Staben et al., 1997; VanVeen and Paul, 1981; Collins et al., 1992; Zaman and Chang, 2004; Salinas-Garcia et al., 1997). The higher Corg in maize, mustard, and potato is due to higher levels of biomass inputs than pulse crops. The narrow C/N ratio of pulse crop residues makes them more labile for supporting quick microbial growth and more easily decomposed than crops having wider C/N ratios. The pattern of accumulation of Corg and Nt in the rhizosphere of sugarcane due to intercrops is shown in Fig. 1 . Intercrops having a wider C/N ratio, a higher biomass input, or both resulted in a greater accumulation of Corg and a lesser accumulation of Nt. In contrast, a lesser accumulation of Corg and a greater accumulation of Nt were evident in the four pulse crops and sesbania. The soil C/N ratio narrowed with time in treatments where pulses were the intercrop. Since narrowing of the C/N ratio here is due to more Nt, more N is probably being mineralized.


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  		Table 2. Soil organic C (Corg), total N (Nt), and available N, P, and K in the sugarcane rhizosphere as affected by different intercrops.

 

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  		Table 4. Correlation among soil chemical and biological properties, including soil organic C (Corg), total N (nt), microbial biomass C (Cmic), microbial biomass N (Nmic), and the metabolic quotient (qCO2).

 

Figure 1
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  		Fig. 1. Variation in soil organic C (Corg) and total N (Nt) in the sugar cane rhizosphere due to intercrops. Bars denote SE.

 
Availability of N was significantly increased by 3 to 20% due to the different intercrops compared with sugarcane alone, with the maximum for lentil and rajmash followed by green gram, cowpea, and mustard (Table 2). The positive correlation of Nt with available N and higher Nt content in pulse intercrops justifies the greater availability of N in pulse intercrops compared with other intercrops. The availability of P also increased due to intercrops except rajmash, green gram, and potato. Recently, Cong and Mercky (2005), while reviewing the postulated mechanisms for improved availability of P due to green manuring and plant residue incorporation, have shown that an improved availability of P can be due to the release of P from the decomposition of amended residue, reduced P sorption due to blocking of P-sorption sites by organic compounds, complexing of Al by organic compounds leading to P release from Al–P complexes, or increased soil pH leading to an increased P concentration in the soil solution. There was also a significant change in the availability of K, with a maximum for potato (Table 2). No fixed trend could be found for different intercrops, but in pulse intercrops the availability of K was comparatively less.

Microbial Changes
Generally, respiration rate increased due to intercropping of different cereal and pulse crops, with a maximum in maize (42%), followed by wheat (37%) and mustard (31%), and then by the pulse crops (Table 3). The large amount of Cmic in maize, wheat, and mustard residues influenced the respiration activity. Raiesi (2004) has shown an increase, due to residue incorporation, of 6 to 35% in decomposition of the initial C present in a wheat system. Potato and sesbania intercropping did not influence the respiration rate in the sugarcane rhizosphere. Soil microbial biomass C increased the greatest when rajmash (35%) was intercropped, followed by maize (32%), mustard (27%), and wheat (22%). Soil Nmic increased significantly when pulse crops and sesbania were intercropped, resulting in a narrow Cmic/Nmic ratio compared with other intercrops. The wider Cmic/Nmic ratio in crops other than pulse crops is due to low Nmic, which might have been due to less Nt and available N in the soil of these treatments (Salinas-Garcia et al., 1997). The C/N ratio of the microbial biomass is also an indicator of the relative proportion of fungi to bacteria (Anderson and Domsch, 1980; Wheatley et al., 1990, Fauci and Dick, 1994). Consequently, the organic amendments with wider C/N ratio, such as the cereals and mustard in this study, probably lead to the colonization of fungal populations, which was evident from wider Cmic/Nmic ratio. Pulses having a narrow C/N ratio lead to higher bacterial activity, indicated by a narrow (near 10:1) Cmic/Nmic ratio (Filiminova, 1997; Wichern et al., 2004). This would also follow the observation that the inclusion of large biomass and reduced soil operations thereafter in the growing sugarcane crop favors the establishment and maintenance of fungal hyphal networks (Wardle, 1995).


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  		Table 3. Effect of intercrops on sugarcane rhizosphere soil biological properties, including microbial biomass C (Cmic), microbial biomass N (Nmic), total soil N (Nt), and the metabolic quotient (qCO2).

 
Intercropping treatments consistently had higher Corg and higher Cmic, which is consistent with reports that a higher Corg content stimulates microbial activity (Gaillard et al., 1999; Zaman et al., 1998; Zaman and Chang, 2004). The Cmic accounted for 2.7 to 3.3% of the Corg content under different intercropping conditions. These values are in agreement with reports that Cmic generally comprises 1 to 4% organic C and the Cmic/Corg percentage could be useful as a soil quality indicator to allow comparisons across soils with different organic matter contents (Anderson and Domsch, 1989; Sparling, 1992). Generally, if a soil is being degraded, the microbial-C pools will decline at a faster rate than organic matter and the Cmic/Corg percentage will decrease as well. The decrease in Cmic/Corg could be caused by decreased microbial biomass or a partially disabled function of its ability to mineralize the added organic matter, as a result of which, the turnover rate of organic matter decreases (He et al., 2003). This might create a calibrated soil quality indicator that could predict whether soils are accumulating or losing soil C. None of our intercropping treatments reduced Cmic/Corg, and there was a higher positive correlation of Cmic with Corg (Table 4, Fig. 2 ) than Nt, available N, or Nmic. These results agree with other studies (Insam and Haselwandter, 1989; Salinas-Garcia et al., 1997) and support the concepts that C usually is the limiting factor for microorganisms in agricultural soils and that the effect of N on Cmic is indirect via altered C input. Moreover, the substrate type has a marked impact on Cmic and Nmic, as evidenced by the effects of different crop residues and plant litter on a range of above- and belowground properties and processes (Nilsson et al., 1999). Crop residues like soybean [Glycine max (L.) Merr.] and other pulses support more microbial growth although they have less residue input to soils than cereals and other crops (Balota et al., 2003).


Figure 2
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  		Fig. 2. Variation in soil organic C (Corg) and microbial biomass C (Cmic) in the sugarcane rhizosphere due to intercrops. Bars denote SE.

 
The measured parameters related to the microbial N pool, such as Nmic and Nmic/Nt, showed variation with different intercrops (Table 3). Microbial N in this study accounted for 2.7 to 3.7% of Nt. The Nmic/Nt ratio increased when pulses and sesbania were intercropped, suggesting that microbes are more active than in other systems; this ratio is highly affected by organic matter substrate and moisture conditions (Insam, 1990; Li and Chen, 2004). Anderson and Domsch (1989) found that the relationships between Cmic or Nmic and Corg were more significant when the Corg content was <2.5%. Since our soils in the subtropical belt of India have Corg content up to only 1% (10 g Corg kg–1soil), Cmic and Nmic are very sensitive indicators of soil quality. The negative correlation of Nmic and Nmic/Nt with Corg and the strong positive correlation with Nt in this study contrasts with the statement of Wardle (1992) that both Nmic and Nmic/Nt ratios are influenced equally by soil Corg and N contents, and is in agreement with steppe soils, where Nmic is more positively related with Nt than with Corg (Li and Chen, 2004).

The qCO2, also called specific respiration, is defined as respiratory CO2 released per unit microbial biomass per unit time. Any change in metabolic quotient may indicate (i) changes in the substrate that an unchanged microbial community uses, (ii) a change of microbial community composition, (iii) a change in both substrate and microbial community, or (iv) no change in the substrate or the microbial community but a change in the physiological status of the community due to altered maintenance requirements (He et al., 2003). Odum (1985) postulated that, under stress, qCO2 increases due to diversion of energy from growth, maintenance, and reproduction, which was further extrapolated to the soil microbial community by Anderson and Domsch (1985, 1990, 1993). Therefore qCO2 was calculated for each intercrop and it was found that a higher qCO2 with wheat, maize, and mustard intercrops gives an indication of either variable microbial communities or stressful conditions due to variable quality and quantity of the crop residues compared with pulse crops. Andrews and Harris (1986) have given different strategies (r and k) for microbial communities, according to which fresh, easily decomposable substrate input favors microorganisms with an r strategy and a more complex substrate favors microbial communities with a k strategy. Strong positive correlations of qCO2 with Corg, Cmic, respiration rate, and CO2–C/Nmic were observed (Table 4); probably the variable qCO2 in this study is due to different substrate inputs. The CO2–C/Nmic ratio also showed a similar trend. Mader et al. (2002) have observed a lower qCO2 in a continuous organic system and have found a significant correlation between crop yield and qCO2. He et al. (2003) have also shown that qCO2 is lower under conservative management than the conventional management where different types of organic substrates are added to soil.

Nitrogen Mineralization
A significant increase in N mineralization was recorded when pulse crops the intercrop, with the maximum increase with green gram (34%) followed by lentil (29%), rajmash (24%), and cowpea (22%) (Table 3). Although C mineralization was higher with cereals than pulses, N mineralization was less with wheat, maize, mustard, and potato than pulses. Smith (1994) has shown that the ratio of C to N mineralization (CO2–C/N mineralized) can be tied to the C/N ratio of the soil, as a mineralized ratio above the soil C/N ratio indicates increased immobilization of N. In our study, the CO2–C/N mineralized ratio calculated for each intercrop treatment was low compared with the soil C/N ratio, indicating no or poor immobilization of N. Probably the N that is being mineralized with different intercropping treatments is being continuously taken up by the plant system, as sugarcane has a high N requirement. Among the different intercrops, the CO2–C/N mineralized ratio was narrow in the case of pulses, which also indicates that residues of pulses are easily decomposable and promote N mineralization. The positive correlation of N mineralization with Nt, available N, and Nmic in our study indicates further that microbial biomass did not act as a sink for N immobilization. Zaman and Chang (2004) have shown higher N mineralization rates due to above- and belowground residues of ryegrass (Lolium perenne L.) and lucerne (Medicago sativa L.) but, due to its negative correlation with Nmic, have hypothesized that the microbial biomass is acting as a sink for N. Holmes and Zak (1994) and Sierra and Marban (2000) found no relationship between net N minearlization and microbial biomass.

Soil quality, being an intricate interaction of chemical, biological, and physical components of the soil system, is indicated by several key factors, which are influenced by soil management practices. In this study, we have tried to measure potential soil quality indicators in different sugarcane intercropping systems. Our overall interpretation of this diverse set of data is that the sugarcane rhizosphere soil quality is affected by intercropping different crops. The incorporation of labile C substrates such as pulses led to improved yield (data not shown) and N mineralization. At the same time, the buildup of a secondary C pool and Cmic in the case of cereals, mustard, and potato intercropping should promote long-term stability.


   ACKNOWLEDGMENTS
 
We are grateful to the director of the IISR, Lucknow, for providing facilities and encouragement. Financial assistance by the World Bank under the NATP-PSR-21 project is duly acknowledged.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 





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