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Soil Science Society of America Journal 65:1442-1447 (2001)
© 2001 Soil Science Society of America

DIVISION S-4 - SOIL FERTILITY & PLANT NUTRITION

Enhancing the Mineralizable Nitrogen Pool Through Substrate Diversity in Long Term Cropping Systems

Jose E. Sanchez*,a, Thomas C. Willsonb, Kadir Kizilkayac, Elaine Parkera and Richard R. Harwooda

a Dep. of Crop and Soil Sciences, Michigan State University, East Lansing, MI 48824
b SW Kansas Research and Extension Center, Kansas State University, KS 67846
c Statistical Consulting Service, College of Agricultural and Natural Resources, Michigan State University

* Corresponding author (sanche22{at}msu.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
The development of sustainable N management systems requires a better understanding of the contribution of on-farm resources to the active N pool size and its mineralization. This study explores the effect of substrate diversity on improving N supply through mineralization. A "diverse system", consisting of a corn (Zea mays L.)-corn–soybean (Glycine max L.)-wheat (Triticum aestivum L.) rotation with cover crops and fertilized with composted manure was compared with a corn monoculture with conventional fertilizers. Nitrogen mineralization was measured in situ and in laboratory incubations as was the ability of each soil to mineralize added compost and red clover (Trifolium pratense) residue in the 6th and 7th yr of rotation. Net mineralized N in the diverse system was 90 and 40% higher than that in the monoculture at 70 and 150 d of laboratory incubations respectively. Comparable response was found in situ where a 70% higher net mineralization was observed in the diverse system at 70 d. The 70- and 150-d mineralizable N pools increased over time, but the ability of soil organisms to break down additional substrate did not change as a result of system diversity. At 150 d of laboratory incubation, a synergistic effect was observed when 5 Mg ha-1 of compost plus 5 Mgha-1 of clover was added to either soil. The combination of the two organic materials mineralized more N than the sum of their individual mineralization results. A more diverse cropping system may increase the soil's capacity to supply N to a growing crop while maintaining desirable levels of soil organic matter. This is essential for the overall long-term productivity and sustainability of agricultural systems.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 
NITROGEN MINERALIZATION is an important indicator of soil quality (Duxbury and Nkambule, 1994; Seybold et al., 1998), and its management could represent an excellent tool in achieving a sustainable N supply. Managing N mineralization efficiently is likely to result in a more synchronized N release, and has the potential to reduce N fertilizer dependence while promoting N recycling within agroecosystem boundaries.

Nitrogen mineralization is regulated by abiotic factors such as soil moisture, temperature, and texture; and by the supply of above- and below-ground substrates (Jenny, 1980). In a practical sense, managing N mineralization implies managing organic inputs. The way in which organic materials influence mineralization is closely related to their quality (Swift et al., 1979). The quality of a particular material is defined by its chemical composition, including C/N ratio, lignin, and polyphenol contents (Tian et al., 1997). Substrates with low N and high concentration of lignin and polyphenols decompose and release N slowly (Cornforth and Davis, 1968). In contrast, those rich in N with low lignin and polyphenol concentrations decompose rapidly (Handayanto et al., 1997). Therefore, a well-balanced diversity of materials entering the soil is expected to favor N availability for a growing crop while maintaining desirable levels of soil organic matter.

It is accepted from an ecological point of view that enhanced species richness is beneficial for ecosystem performance (Kareiva, 1996; Tilman et al., 1996), but the question remains whether that is the case for below-ground subsystems (Wardle and Giller, 1996). Substrate diversity can be primarily achieved with the use of crop rotations, cover crops, and application of organic amendments (Gliessman, 1998). In this work we investigated how substrate diversity influences N mineralization. Two cropping systems were selected according to their level of diversity. The "diverse system" received residues of corn, soybean, wheat, red clover, crimson clover (Trifolium incarnatum), and annual ryegrass (Lolium multiflorum), as well as composted manure during each rotation cycle. This system was compared with a continuous corn monoculture where commercial fertilizer was the fertility source. Specific objectives of this study were to determine if the first year corn of the diverse system would induce higher mineralization rates than the continuous corn monoculture, and to determine whether these two systems differ in their ability to mineralize added substrate. The first objective deals with the potential of the cropping system to supply N to a growing crop. The second asks whether there have been important changes in microbial performance relating to the decomposing ability of each microbial community.

In 1998 and 1999, laboratory and in situ incubation experiments were initiated to determine N mineralization potentials. Although in situ incubations were expected to generate data that more closely reflect actual field conditions, laboratory incubations require less effort and cost and produce data with less variability. A regression analysis of N mineralization over time was used to compare in situ and laboratory methods. Learning more about the relationship between the two methods has the potential to facilitate the calibration of predictive models based on commonly used laboratory incubations (Smith et al., 1977; Bhogal et al., 1999).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 CONCLUSIONS
 REFERENCES
 
Site Description
This study was conducted in the Living Field Laboratory (LFL), a long term experiment established in 1993 at the W.K. Kellogg Biological Station located in Southwest Michigan. The site experiences cold moist winters and warm humid summers. Average precipitation has been 860 mm yr-1 (1988–1999), and potential evapotranspiration typically exceeds precipitation from May through September. The soil is a mixture of Kalamazoo (fine-loamy, mixed, mesic Typic Hapludalfs) and Oshtemo (coarse-loamy, mixed, mesic Typic Hapludalfs) sandy loams. The depth of the Ap horizon is 20 to 25 cm, and pH ranges from 6.3 to 6.8. The LFL was designed to test various combinations of rotation and cover crops under several agronomic management regimes (Jones, 1996). The main goal is to test alternative strategies for achieving nutrient cycling efficiency and reducing chemical input requirements. The experimental design is a split-split-plot in four randomized complete blocks, with main plots for each management type. Both systems studied here used minimal application of pesticides, and banded herbicide plus cultivation for weed control. The main difference is in their fertility source and crop rotation: the monoculture system uses commercial fertilizer on continuous corn and the diverse system uses composted dairy manure to fertilize a corn-corn–soybean-wheat rotation. Red clover is frost-seeded into wheat, crimson clover is interseeded into first year corn, and annual ryegrass is interseeded into second year corn as cover crops. Before planting, approximately 4 Mg ha-1 (dry weight of non-sand material) of composted manure is added annually to all crops except soybean. Reduced tillage (chisel plow) is used throughout the LFL.

The crop rotation was selected as the diverse system because residues of six plant species in combination with composted manure are incorporated into the soil throughout the rotation cycle. These substrates have a wide range of C/N ratios. The lowest C/N ratio is provided by the red clover cover crop (14:1) and the highest by wheat stubble (80:1). This study used the 1st year corn (immediately following wheat + clover) plots because, historically, its grain yields have been comparable to those where fertilizer was used (Jones, 1996). In contrast, the continuous corn plots receive only corn residues (C/N ratio of 60:1) as organic substrate. These plots historically received P (triple superphosphate) and K (potassium chloride) before planting at a rate determined by a pre-planting soil test. Nitrogen was applied at planting (20–25 kg ha-1) and sidedressed (ammonium nitrate) as recommended by the pre-sidedress nitrate test (Magdoff et al., 1984). For clarity we will use the terms "diverse system" to describe the first year corn, and "monoculture" when referring to continuous corn. The C, N, and C/N ratios of soil from these cropping systems are described in Table 1.


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  		Table 1. Selected chemical properties of soil from the diverse and monoculture cropping systems, and the organic materials added in the laboratory and in situ incubations.

 
In early May 1998 and 1999, soil samples were taken from the diverse and monoculture cropping systems following tillage and immediately before planting and used in long-term laboratory incubations. Also in both years immediately after planting, microplots were established in the plots of the two cropping systems and were used for in situ incubations. No fertilizer was applied to microplots in the monoculture cropping system during the experimental period.

Laboratory Incubation
Soil samples were taken at 0–10 cm depth using a 1.9 cm diameter soil probe. Thirty cores from each plot were composited, placed in plastic bags, and stored at approximately 4°C until processed. Soils were sieved through a 6 mm screen and sub-sampled for moisture determination. Sixty-three 20-g dry weight equivalent aliquots of each sample were weighed into 100-mL plastic specimen cups. Treatments consisted of control, Com, 2Com, Clo, 2Clo, Com + Clo, Com + 2Clo, 2Com + Clo, and 2Com + 2Clo, where Com is 5 Mg ha-1 of composted manure and Clo is 2.5 Mg ha-1 of red clover. Both compost and clover were dried, finely ground, and sub-sampled for chemical analysis using the acid and neutral fiber detergent method (Goering and Van Soest, 1970). Selected chemical properties of added clover and compost are presented in Table 1. Calculations for the actual amount of material added to cups were based on a soil bulk density of 1.3 Mg m-3 and depth of 10 cm. The quantity of compost was based on dried weight of non-sand material. Following the additions, each cup was manually agitated to uniformly mix the soil and substrates. The soils were brought to 50% of water holding capacity. The specimen cups were stored in plastic storage containers that had a thin layer of water on the bottom to maintain humidity. These containers were then placed in a controlled temperature room at 25°C for 20, 30, 50, 70, 100, and 150 d. At the end of each incubation interval, the corresponding samples were removed and frozen temporarily to stop microbial activity. Nitrate-N and NH4-N concentrations were determined using the extraction technique described by Keeney and Nelson (1982) and a Lachat automated colorimetric analyzer (Lachat Instruments Inc. Milwaukee, WI).

In Situ Incubation
Four microplots of 2 m2 were established in each plot and used for in situ incubation experiments (Raison et al., 1987). Red clover (5 Mg ha-1, 2Clo), composted manure (10 Mg ha-1, 2Com), and the combination 2Com + 2Clo were used in this experiment along with control. The clover was dried, and applied unground. The treatments were randomly assigned to microplots, the materials uniformly added to the soil surface, and mostly incorporated in the 0–10 cm depth using a long-tined hand cultivator (Ben Meadows Co., Atlanta, GA). Fifteen PVC tubes (30-cm long and 5-cm i.d.) were inserted to a depth of 25 cm in the corn row of each microplot to prevent root in-growth. After tube insertion, soil samples were taken at 0–10 cm from each microplot to measure initial mineral N. Soil moisture was controlled in the cylinder by use of temporary rain shelters and periodic addition of water to prevent extreme wetting-drying events, and to minimize NO3 leaching and denitrification. Soil moisture was gravimetrically determined every two wk. The amount of water to be added was calculated by subtracting the actual soil moisture from the estimated water holding capacity for the 0–10 cm depth. Half of the calculated amount was added at each of two different days during the two-wk period.

On days 14, 28, 42, 56, and 70 after insertion, three cylinders from each microplot were randomly selected and removed. Samples were taken from 0–10 cm depth within each cylinder using a 1.9-cm-diam soil probe. Soils from the three cores were composited, placed in a plastic bag, and stored at approximately 4°C until processed. Mineral N was determined according to the method mentioned in the laboratory incubation section.

Mineralized Nitrogen Calculations
Net N mineralization using laboratory and in situ incubations was calculated using the difference between inorganic N content at the end of the incubation period and at day 0. For the in situ incubation we assumed that deep N leaching was prevented and gaseous N loss minimized. Linn and Doran (1984) reported that in a well drained soil the relative amount of anaerobic denitrification is negligible. Also, a recent long-term study in an adjacent field indicated that N loss due to denitrification ranged from 1.3 to 0.4 kg ha-1 per year (Robertson et al., 2000). Our agronomic treatments were nearly identical to that study.

The amount of net N mineralized from added substrate was calculated by subtracting the mineralized N of the control from the treatments with added substrate. The calculated amount is expressed as a percentage of the initial amounts of N added as clover and/or compost.

Data Analysis
The same statistical model was applied to the laboratory and in situ data sets. Factors used in the model were: year, replication, cropping system, treatment, and incubation time. We performed analysis of variance for each data set, using the SAS Mixed procedure (SAS Institute, 1999) in which the data from each incubation interval was treated as a repeated measurement of the corresponding experimental unit. The optimal covariance structure was determined using Schwarz's Bayesian Criterion (Littell et al., 1997). The laboratory incubation data set was appropriately explained by a compound symmetry (CS) covariance structure, while its heterogeneous version (CSH) better corresponded to the in situ data set. CS assumes constant variance and covariance, and CSH uses a different variance parameter for each diagonal element of the variance/covariance matrix, and assigns the square roots of these parameters in the off-diagonal entries (SAS Institute, 1999). The appropriateness of CSH for in situ data set may be related to the inherent variability commonly found in the field.

Since the analysis of variance indicated that N mineralization was not influenced by the year of sampling the results from both years were combined. We present results of 70- and 150-d N pools, obtained from mineralization at those dates. These incubation periods were selected due to their agronomic importance. The 70-d N pool was expected to closely represent the portion of organic-N available for mineralization during a growing season. The 150-d pool contains that of the 70-d plus a more resistant fraction.

In situ incubations were expected to generate data that more closely reflect actual field conditions, but laboratory incubations are more widely used. Regressions for the laboratory and in situ incubations were constructed using the least square means (LS-means) of common treatments at incubation periods less than 70 d.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
CONCLUSIONS
 REFERENCES
 
Laboratory Incubation
Net mineralized N in the diverse system was 90 and 40% higher than the monoculture at 70 and 150 d of laboratory incubation respectively (Fig. 1) . When substrates were added, the diverse system still mineralized more N than the monoculture when comparing the same treatment and incubation time. The net N mineralization was highest when 5 Mg ha-1 of clover was applied to this cropping system. The lowest net mineralization was observed in the monoculture without clover. The monoculture was able to produce as much mineral N as the diverse system when it received an extra 2.5 Mg ha-1 of clover. In general, the addition of compost did not significantly alter net mineralization.



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  		Fig. 1. Net mineralized N after 70 and 150 d of laboratory incubation for soil sampled from the diverse and monoculture cropping systems. Lower and upper case letters indicate significant differences in mineralized-N at Day 70 and 150, respectively (P < 0.05, Tukey-Kramer test).

 
The percentage of N (from added substrates) mineralized at 70 and 150 d of laboratory incubation were not significantly different between cropping systems (Table 2). Clover additions released considerable N during the first 70 d, and small amounts from 70-150 d of incubation. The proportion of N mineralized from each substrate remained constant as the rate of added substrate was doubled. At 150 d of incubation, the proportion of each substrate N mineralized increased, as calculated from weighted average calculation, when 5 Mg ha-1 of compost and 5 Mg ha-1 of clover were combined (calculation not shown).


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  		Table 2. Net mineralized N from added substrates for two cropping systems at two incubation dates, expressed as percentage of added N.

 
In Situ Incubation
The in situ net N mineralization in the diverse system was 70% higher than that of the monoculture after 70 d (Fig. 2) , agreeing with the pattern observed in the laboratory. When substrates were applied, the diverse system also produced more N than the monoculture. The highest N mineralizations were obtained when 5 Mg ha-1 of clover was added to the diverse system. The monoculture without clover produced the lowest net mineralized N but released N in comparable amount to the diverse system (in absence of clover) when 5 Mg ha-1 of clover was added. The addition of compost did not significantly increase mineralized N in either soil.



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  		Fig. 2. Net mineralized N after 70 d of in situ incubation for the diverse and monoculture cropping systems. Bars followed by the same letter are not significantly different (P < 0.05, Tukey-Kramer test).

 
The percentages of mineralized N in situ from the additions were consistent with those measured in the laboratory (Table 2). Thus, no significant differences between the two cropping systems in the % N mineralized of added materials were observed. The low mineralization rates of compost caused a dilution effect on the percentage of mineralized N from the combined materials.

Relating Laboratory and In Situ Incubations
Figure 3 indicates the level of agreement between laboratory and in situ incubation. Regardless of cropping history and addition of materials, net mineralized N at 70 d in situ was on average 90% of that in the laboratory.



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  		Fig. 3. Comparison between laboratory and in situ incubation across cropping systems and addition of organic materials. Individual data points are the LS-means of 32 observations.

 
DISCUSSION
The striking differences in net mineralization between the two cropping systems demonstrate the linkage between substrate diversity and the size of the active N pool. Swift et al. (1979) reported that quantitative variation in mineralized N occurs as a result of the variety of organic inputs. The mineralizable N pool size in the diverse system was undoubtedly enhanced by the incorporation of residues from the three legumes, three grasses, and composted manure. Individual contribution varies according to quantity and quality of the substrate. For instance, legumes with narrow C/N ratios and abundant soluble compounds are more likely to mineralize at higher rates than residues from grasses with high C/N ratios. Our data agree with those of Stanford and Smith (1972), Chang and Juma (1996), and Franco-Vizcaino (1997), showing that crop diversity including annual legumes increases the mineralizable N compared with monoculture. The higher mineralization rates in the diverse system with added clover and/or compost were influenced by the enhanced-input history of this soil. Despite the initial advantage of the diverse system, the corn monoculture showed that the presence of clover residue can dramatically increase its mineralization potential (Fig. 1 and 2). This may be an indication of microbial resilience, showing that incorporating a high quality substrate may cause a considerable improvement in soil fertility while increasing diversity.

Net mineralized N from the additions was expressed as a percentage of added N to facilitate the comparison between cropping systems. The similar ability of the corn monoculture and the diverse system to mineralize additional organic N may be an indicator of rapid changes in microbial activity and biomass. Nitrogen mineralization is a microbiologically-mediated process (Paul and Vorony, 1984), and the microbial biomass is largely controlled by organic C content and by recent substrate additions (Paul and Clark, 1996). It appears that regardless of its input history, the microbial biomass presumably reacts to the input of easily-decomposable compounds (e.g., from clover) by increasing its size and activity (immobilization and mineralization). The sizeable clover-N mineralized during the first 70 d and the small or undetected amount mineralized from 70–150 d (Table 2) suggest that N release may coincide with crop growth. Results of mineralized clover-N are comparable to those reported by Ladd et al. (1983), Bremer and van Kessel (1992), and Biederbeck et al. (1996). It is possible that the addition of compost did not stimulate the microbial biomass as may happen with clover. In a previous study at the same location and using similar type of compost, Willson et al. (2000) found that microbial biomass did not increase immediately following compost additions. Even though the C/N ratio of clover and compost were similar, decomposition rates may differ because different C compounds exhibit different decomposition rates (Somda et al., 1991). We suggest that the low, sometimes-negligible, release of compost-N was related to the presence of a large quantity of more recalcitrant nitrogenous compounds. During the composting process manure-N is stabilized through microbial assimilation and humification and thus the end product (compost) mineralizes N at a considerably slower rate (Castellanos and Pratt, 1981).

The combination of 5 Mg ha-1 of compost and 5 Mg ha-1 of clover mineralized more N than have been anticipated from the "weighted" means of their individual mineralization at 150 d of laboratory incubations (Table 2). We suggest the possibility of a synergistic relationship but this effect was not seen in the more limited in situ experiment. Enhanced mineralization of the compost could have resulted from the high level of labile N produced from mineralization of 5 Mg ha-1 of clover.

The results of the laboratory incubations were generally comparable to those of the in situ experiment. This can be explained by the similarity of their environmental conditions. Selected climatic data obtained from the nearby Long-Term Ecological Research weather station is shown in Table 3. Soil moisture was controlled in the laboratory and in situ experiments, and the average soil temperatures in the field and in the laboratory were also coincidently similar, although seasonal variation was greater in situ. The greater differences in N mineralization were observed early in the incubation period (Fig. 3). Early season lower average temperatures probably influenced the in situ N mineralization to be lower compared with those from the laboratory where temperature was kept constant. The similarity of results generated by these two methods agrees with those reported by Hadas et al. (1989).


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  		Table 3. Selected climatic data and amount of water added during the time period when in situ incubations were performed.

 
These laboratory and in situ incubations are not intended to represent actual field mineralization, but to provide evidence of how this process may be affected by substrate diversity, since in situ mineralizations excluded plant roots. Further studies are strongly recommended to quantify N release in presence of living roots. Growing roots not only affect N mineralization by exposing organic materials to decomposition and uptake of N, but rhizodeposit production represents a significant energy input to the soil microbial community (Bakken, 1990; Texier and Billes, 1990). Sanchez et al. (2000) in a previous study found that the presence of corn roots can dramatically increase N mineralization in soils with a large active N pool.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSIONS
REFERENCES
 
Farming practices promoting diversity have the potential to dramatically increase the mineralizable N pool and decrease fertilizer N requirement, because the use of diverse crop rotations, legume cover crops, and organic amendments from animal sources adds significant organic N to the soil. The ability of soil organisms to break down additional substrate did not change as a result of previous input diversity but it may have increased due to simultaneous input diversity. The additional gain in N mineralization by adding clover and compost combined was not definitely answered by this research. A possible synergistic effect was shown in the laboratory but was not found in situ where incubations were not as extensive as in the laboratory. Laboratory incubation is a reliable tool to estimate N mineralization in the field as long as plant roots are excluded. Further studies are needed to determine how mineralization of added substrates is affected by the presence of roots.


   ACKNOWLEDGMENTS
 
Our special thanks to the C.S. Mott Chair of Sustainable Agriculture and Michigan State Agricultural Experiment Station for their financial support that made this study possible.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 CONCLUSIONS
 REFERENCES
 




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