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Crop Science 43:631-638 (2003)
© 2003 Crop Science Society of America

TURFGRASS SCIENCE

Daily vs. Periodic Nitrogen Addition Affects Growth and Tissue Nitrogen in Perennial Ryegrass Turf

D. C. Bowman*

Dep. of Crop Sci., North Carolina State Univ., Raleigh, NC 27695

* Corresponding author (dan_bowman{at}ncsu.edu)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Nitrogen is typically supplied to turfgrasses either in large episodic pulses of readily available fertilizer N, or in relatively small, constant fluxes from mineralization, slow release fertilizers, or fertigation. There is little information on the comparative physiology and productivity resulting from each strategy. A greenhouse study was conducted to determine turfgrass productivity and N partitioning as a function of daily (near-constant) vs. intermittent N supply. Perennial ryegrass (Lolium perenne L.) was grown in solution culture and fertilized daily with KNO3 at rates ranging from 0.56 to 11.1 kg N ha-1 d-1 (daily N), or in pulses delivered every 8, 16, or 32 d to supply 50 kg N ha-1 mo-1 (intermittent N). Leaf growth rate, reduced N, and NO3–N content were relatively stable under daily N, with steady state values for each parameter strongly affected by N rate. Intermittent N caused fluctuations in growth and tissue N coincident with application. Nitrogen absorption was rapid and complete for all but the highest rate of daily N. Nitrogen supplied intermittently was absorbed quantitatively across a period of 8 to 36 h. Allocation to new leaf growth accounted for 88 to 119% of the absorbed N. Shoot biomass increased, whereas root biomass and length decreased with increasing daily N rate. The results indicate that while daily N supply produces relatively constant growth and stable tissue N pools, there is little benefit to long-term productivity and N use efficiency when compared with intermittent supply of N.

Abbreviations: PPFD, photosynthetic photon flux density


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
NITROGEN IS the most important nutrient in turfgrasses for maintaining color and density, and encouraging recovery from stress and damage. It is applied to turf systems not to maximize yields but rather to promote vigorous, healthy turf. In fact, fertility programs are designed specifically to moderate the supply of N to the turf and thus maintain turfgrass growth at submaximal levels. This implies that some degree of N deficiency is probably the normal state for turfgrass systems.

Turfgrass fertilizers fall into two general categories based on their pattern of N supply. The slow-release sources supply N continuously and at relatively low levels across a period of weeks to months. This pattern is somewhat analogous to N made available through mineralization of soil organic matter, although the mechanisms of release may be quite different. By contrast, fast-release sources of N are readily available and rapidly absorbed by N-deficient turf (Bowman and Paul, 1988). Leaf growth and color respond quickly to this periodic availability of N, but the response is often short-lived because the applied N is quickly exhausted.

Compared with a steady supply of N (slow-release fertilizers and mineralization), episodic pulses of fast-release N and the resulting fluctuations in tissue nutrient levels may represent an artifactual and inherently stressful situation. Ingestad (1980)( 1981), Ericsson (1981), and Ingestad and McDonald (1989) have reported that for a number of species, N deficiency symptoms were associated with fluctuating tissue nutrient status. When they abruptly altered the N addition rate, tissue N levels became unstable and leaf chlorosis quickly developed. However, once the growth rate adjusted to match the new addition rate, tissue N levels stabilized and the chlorosis disappeared. Interestingly, chlorosis was not a function of the absolute tissue concentration; it did not appear when levels dropped below a critical threshold. Rather, it was a function of internal nutrient instability.

In his research, Ingestad (1980)(1981) used young plants in the exponential stage of growth. Nitrogen was supplied exponentially to match the growth pattern; different relative addition rates resulted in stable tissue N levels and a predictable corresponding relative growth rate. By contrast (and assuming stable environmental conditions), a mature turfgrass system, having attained a steady state leaf area index, grows at a constant rate due to high canopy density and interplant competition. To maintain relatively stable tissue concentrations and uniform growth across time, it seems logical that N should thus be delivered to turfgrass systems also at a constant rate. However, there is little detailed information on turfgrass response to constant vs. intermittent N supply, which is somewhat surprising given the widespread acceptance and use of both delivery strategies. The objective of this study was to compare growth, N uptake, tissue N status, and N partitioning in perennial ryegrass turf when supplied with daily or periodic N additions. Detailed growth analysis was used to determine the efficiency of each strategy.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Plant Culture
An experiment was conducted in a greenhouse maintained at 23/15°C day/night under natural light; daily integrated light levels (PPFD, photosynthetic photon flux density) were recorded throughout the experiment. Perennial ryegrass ‘Manhattan II’ was grown as a turf in nutrient solution culture as previously described (Bowman and Paul, 1988). Briefly, individual culture units consisted of round plastic containers, 167 cm2 in area and containing 2.3 L of aerated nutrient solution. Seeds were sown at 400 kg ha-1 on glass wool sheeting supported by a rigid plastic mesh. Seedlings were established on 0.25 strength Hoagland's solution (Hoagland and Arnon, 1950), pH 6.0, for a period of 12 wk. The solutions were changed and the turf cultures were mowed at 4 cm every 4 to 7 d. This produced a dense, healthy turf with four to five tillers per plant.

Nitrogen Treatments
Treatments were initiated on 10 July and were designed to simulate constant N supply at rates ranging from suboptimal to excessive, and also N supplied in large, periodic pulses. Turf cultures were transferred from the plus-N solution used during establishment to a minus-N solution in which the NO3 salts were replaced with SO4 salts. Beginning the following day, KNO3 stock solution was added daily to supply 0.56, 1.67, 2.78, 5.56, or 11.1 kg N ha-1 d-1 (daily N, Treatments 1–5, respectively). These daily rates equate to 17, 50, 83, 167, and 333 kg N ha-1 mo-1, respectively. Initial solution N concentrations ranged from 31 to 620 µM. Treatment 2 (50 kg N ha-1 mo-1) approximates the standard N rate for perennial ryegrass during active growth. Intermittent additions were made every 8, 16, or 32 d (N pulse, Treatments 6, 7, and 8, respectively) to supply the equivalent of 50 kg N ha-1 mo-1, the same rate as in Treatment 2. Initial N concentrations were {approx}0.75, 1.5, and 3.0 mM for Treatments 6, 7, and 8, respectively.

Daily and intermittent N additions were continued for 19 weeks, during which solutions were changed and the cultures mowed approximately every 5 d. Supplemental Fe as FeSO4·7H2O was periodically added at a rate of 0.2 mg Fe L-1 to prevent chlorosis, and the pH was adjusted daily to 6.0 ± 0.5.

Tissue Analyses
Clippings from each mowing were collected, weighed fresh, dried, reweighed, and ground. Total N was determined by Kjeldahl digestion modified to exclude NO3 (Bowman et al., 1988). Tissue NO3 was extracted in deionized water under vacuum, and analyzed by the rapid diffusion method (Carlson, 1986). All turf cultures were harvested on 21 November. Roots were separated from shoots, and maximum root length and shoot density were measured. Tissues were processed and analyzed as for the clippings.

Nitrogen Uptake
During the experiment, aliquots of the nutrient solutions were periodically collected immediately before the daily N addition and analyzed for NO3. In all cases, the previous day's NO3 had been completely absorbed by the turf in Treatments 1-4 (data not shown). The addition rate in Treatment 5 exceeded uptake, which resulted in the accumulation of NO3 in the solution between changes.

A more detailed analysis of NO3 uptake was conducted following N additions on Day 68 (15 September). Aliquots of solution were collected for up to 36 h after N addition, and analyzed for NO3. Nitrogen uptake was calculated as NO3 depletion from solution.

The experiment was conducted as a randomized complete block design with three replicates. Harvest data were analyzed by ANOVA and means separated at P = 0.05 by the least significant difference test. Data for N allocation to leaf tissue were compared by ANOVA of the slope of the regression line.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Nitrogen treatments were designed to provide N either in intermittent pulses or in daily doses. Application in pulses, especially on a 32-d cycle, is fairly typical for granular turfgrass fertilizers. Daily N addition was chosen to simulate fertigation practices and approximate constant N supplied by slow-release fertilizers or through mineralization. This is fundamentally different from the previously cited work of Ingestad and others who supplied N as a relative, or exponential function. Relative nutrient addition is analogous to relative growth in that both increase exponentially with time. It should be noted that plant materials used in their studies were typically in an early, exponential stage of growth, for which an exponential addition of nutrients is logical. The mature turf systems used in this study had developed beyond the exponential and into a linear growth stage (data not shown), and it was thus more appropriate to use a linear, or daily N addition protocol.

Growth
Growth rate of perennial ryegrass, measured as clipping dry weight, responded quickly to daily N treatments (Fig. 1a). All treatments had an initial growth rate of {approx}200 kg ha-1 d-1, which is nearly identical to high values of productivity previously reported for ryegrass (Loomis et al., 1971). In Treatments 1 to 4, growth declined steadily for 20 to 40 d after switching to suboptimal daily N additions, and then leveled off at a rate reflecting the N addition rate. There was clear separation between all five daily N treatments during the first three months. Growth in Treatments 4 and 5 was nearly identical during the remainder of the experiment, with both declining to the level of Treatment 3. Growth reduction in Treatments 4 and 5 late in the experiment was likely due to reduced light levels; daily integrated PPFD declined substantially from highs of 25 to 30 mol m-2 d-1 during July and August to lows of 10 to 15 mol m-2 d-1 in November (Fig. 2).



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  		Fig. 1. Growth rate of perennial ryegrass turf with daily N additions (top) or intermittent N additions (bottom). Note the different ranges of the x-axes. Arrows indicate intermittent N additions, with long, intermediate, and short arrows representing the 32-d, 16-d, and 8-d additions, respectively. Values are means of three replicates. For clarity, error bars are absent; standard deviation averaged 7%.

 


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  		Fig. 2. Weekly values for integrated photosynthetic photon flux density (PPFD) in the greenhouse during the experiment.

 
Light level affected growth only at the two highest N rates, with similar responses noted for both treatments (Fig. 3). This is consistent with Ingestad and McDonald (1989), who reported that relative growth rate of birch (Betula pendula Roth.) seedlings responded to light levels only under conditions of high N nutrition.



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  		Fig. 3. Growth rate of perennial ryegrass treated with daily N as a function of photosynthetic photon flux density (PPFD). Values are means of three replicates. Slope values followed by the same letter are not significantly different at P = 0.05.

 
The slope of the curves comparing growth rate to PPFD provides an estimate of the efficiency of energy conversion at higher light levels. In the present case, Treatment 5 (nonlimiting N) had a slope of 0.41 g dry wt. mol-1 photons. On the basis of the simplifying assumption that dry leaf tissue contains 40% C by weight, all as glucose, the slope of the curve for Treatment 5 is equivalent to 0.014 mol C mol-1 photons, or a quantum yield of 1.4%. This conversion efficiency is limited to the upper half of the integrated PPFD range and does not account for productivity across the entire range of integrated PPFD. Conversion efficiency can also be calculated based on the growth rate at a given light level. Assuming a peak growth rate of 200 kg ha-1 d-1 (under nonlimiting N) at 25 mol m-2 d-1, the efficiency of energy conversion is {approx}2.7% when averaged across the entire integrated PPFD range. These values fall within the range for cultivated systems summarized in Loomis et al. (1971), but are somewhat lower than those reported by Ingestad and McDonald (1989). Growth rates at lower daily N (Treatments 1–3) were stable through the experiment, indicating that N was a more limiting resource than was light. This suggests that moderate seasonal variation in light intensity and duration is unlikely to cause significant changes in growth of perennial ryegrass turf.

Intermittent additions of N caused relatively large fluctuations in growth rate, especially with N applied on a 32-d cycle (Fig. 1b). Fluctuations were less pronounced with N applied every 16 d, and had essentially disappeared by the end of the experiment. There was little difference in growth patterns and no difference in cumulative clipping production between Treatments 6 (8-d N cycle) and 2 (daily N, same total rate as Treatment 6). From a practical standpoint, and based on this similarity in growth between daily and (approximately) weekly N additions, it may be possible to extend the interval between N applications applied through fertigation systems to once per week.

Tissue Nitrogen
Leaf reduced N followed a pattern similar to growth rates (Fig. 4a,b), with clear separation between the daily N treatments. Steady state levels increased from {approx}3% for the lowest addition rate to >5% for the highest N addition rate. A range of 3.3 to 5.1% N is considered to be sufficient for perennial ryegrass (Mills & Jones, 1996), which indicates that N supply in Treatments 1 to 3 was suboptimal, at least with regards to yield. As with growth rate, tissue reduced N fluctuated widely with the 32-d N cycle, ranging from 3.0 to 4.5% (Fig. 4b). Applications every 8 or 16 d resulted in relatively stable tissue N comparable with application every 32 d.



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  		Fig. 4. Concentration of reduced N in the clippings from perennial ryegrass turf grown with daily N additions (A) or intermittent N additions (B). Arrows indicate intermittent N additions, with long, intermediate, and short arrows representing the 32-d, 16-d, and 8-d additions, respectively. Values are means of three replicates. For clarity, error bars are absent; standard deviation averaged 3%.

 
Average growth rate data were regressed against tissue reduced N data from Days 30 through 99 (Fig. 5a,b). Day 30 was chosen as a starting point because the growth rates in Treatments 1 through 5 had stabilized at that time. With N added daily, growth rate was a linear function of tissue reduced N. This is similar to the linear relationship between relative growth rate and tissue N reported by Ingestad (1982)(and references therein). Extrapolation of the curve to the x-axis indicates a critical tissue level of 2.7% N, below which growth would be predicted to cease. The relationship between tissue N and growth in the intermittent treatments was also significant, with a slope approximately half that with daily N supply (slopes significantly different at P = 0.01). This is probably due to the intermittent N supply causing fluctuating tissue N levels. Although fluctuating tissue N levels have been associated with N deficiency symptoms (Ingestad and Lund, 1979; Ingestad, 1980, 1981), there was no apparent N chlorosis in any of the ryegrass cultures in this study.



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  		Fig. 5. Growth rate of perennial ryegrass grown with daily N additions (A) or intermittent N additions (B) as a function of reduced N concentration in the clippings. Values are means of three replicates.

 
Nitrate concentration in leaf tissue decreased from {approx}8000 to 100 µg N g-1 in Treatments 1 to 3 during the first 3 wk, with concentrations remaining low thereafter (Fig. 6a). The higher N rates in Treatments 4 and 5 resulted in relatively constant tissue NO3 concentrations of {approx}3000 and 7000 µg N g-1, respectively. These values represent 5 and 10% of total leaf N, respectively. All three intermittent N treatments resulted in relatively large fluctuations in tissue NO3 compared to Treatment 2 (Fig. 6b). Peak concentrations reached 1000 to 4000 µg N g-1 immediately after intermittent N additions, but these declined quickly to 100 to 300 µg N g-1. The presence of NO3 in clippings harvested from Treatments 6 to 8 is interpreted as an inefficient loss of absorbed N, at least in the short term. The NO3 had not been reduced, and thus could not have contributed to protein biosynthesis and plant productivity.



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  		Fig. 6. Concentration of NO3–N in the clippings from perennial ryegrass turf grown with daily N additions (A) or intermittent N additions (B). Symbols and arrows as in Fig. 1. Values are means of three replicates. For clarity, error bars are absent; standard deviation averaged 16%.

 
In perennial ryegrass grown with daily N supply, very little NO3 accumulated in leaf tissue having <4.3% reduced N; much higher NO3 concentrations, indicative of vacuolar storage, were found above this value (Fig. 7). These data correspond to Treatments 1 to 3 for values <4.3% N and Treatments 4 and 5 >4.3% N. Nitrate typically accumulates in tissues when supply exceeds requirements for growth (Millard, 1988), which would imply that maximum growth in ryegrass is approached at {approx}4.5% reduced N in the leaf tissue. Similar results were reported for tall fescue (Festuca arundinacea Schreb.), although the critical level of tissue N at which NO3 started to accumulate was 3.0% (Terman et al., 1976).



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  		Fig. 7. The relationship between NO3–N and reduced N in the clippings of perennial ryegrass turf grown with daily N additions. Data are compiled from all five daily N additions and are the means of three replicates.

 
Nitrogen Uptake and Allocation
A detailed analysis of NO3 uptake was conducted during Week 10. Nitrate supplied to Treatments 1 to 3 was rapidly depleted from solution, with complete absorption after 1.5, 2, and 3 h, respectively (Fig. 8a). This is consistent with previous work showing that N deprivation, even for relatively short periods, results in a substrate-inducible, high capacity uptake system in perennial ryegrass (Bowman and Paul, 1988). Uptake in Treatment 4 was less rapid and fairly constant through the 12-h period of depletion, indicating that these plants were physiologically N sufficient, or nearly so. There was no apparent lag period for NO3 uptake in the N deficient turf cultures, implying that the uptake system remained induced from the previous day's N addition. Nitrate uptake in Treatments 6 to 8 (intermittent supply) was 4- to 5-fold higher than in daily supply Treatment 5 (Fig. 8b). Treatments 6, 7, and 8 had absorbed the applied N by 8, 14, and 36 h, respectively. In contrast, Treatment 5 absorbed 90% of the daily N allocation by 24 h, at which time the next day's addition was made.



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  		Fig. 8. Nitrate uptake by perennial ryegrass turf grown with daily N additions (A) or intermittent N additions (B). Data from Treatment 5 (highest daily N) included in (B) for comparison. Values are means of three replicates; error bars are standard deviations.

 
It should be noted that although the N-replete ryegrass (Treatment 5) absorbed NO3 much more slowly than the N-deficient cultures, the rate for the N-replete ryegrass is equivalent to 10 kg N ha-1 d-1. At this rate, a typical 50 kg N ha-1 application using a soluble N source could be absorbed in 5 d. Obviously, turf is not managed to optimize growth potential, and the high N addition rates used in this experiment are not realistic. But the data do suggest that ryegrass turf has the capacity for both growth and N uptake far in excess of that normally associated with turfgrass management, assuming other factors are not limiting.

Nitrogen allocation to new leaf tissue was estimated by plotting cumulative total N (reduced plus NO3–N) harvested in the clippings against time (Days 33–98; Fig. 9), with the slope of the fitted linear function representing steady state N allocation. Slope values were compared with the N addition rate to calculate the percentage of applied N allocated to leaf growth during the long term. With the exception of the highest daily N rate, all daily N treatments had very high N allocation percentages, ranging from 88 to 119%. Allocation exceeded N supply for Treatment 1, indicating that the turf continued to remobilize preexistent tissue N throughout the experiment. This suggests that the lowest daily N rate was insufficient to support a maintenance growth level, forcing the turf to cannibalize internal N resources. Allocation closely approximated N supply (88–95%) for Treatments 2 to 4. Nitrogen allocation in the intermittent treatments were nearly identical, averaging 87% (data not shown).



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  		Fig. 9. Cumulative N harvested in clippings of perennial ryegrass turf grown with daily N additions. The percentage of absorbed N allocated to new leaf growth was calculated as the ratio of the slope of each curve to the daily N addition rate. Values are means of three replicates.

 
These data suggest that the root system and shoots were relatively static as N sinks. This does not preclude the possibility of considerable internal cycling of N, but rather describes a system in which, from a mass balance perspective, essentially all of the absorbed N was ultimately directed to produce new leaves. With N supply exceeding uptake in Treatment 5, allocation as a percentage of applied N was comparatively low.

Shoots and Roots
Nitrogen treatment had significant effects on biomass and N fractions in the shoots and roots harvested at the end of the experiment (Table 1). Shoot (canopy) dry weight decreased, whereas tiller density increased with increasing N rate. As a result, individual tiller dry weight was reduced by {approx}50% at the high compared with the low N rates. Shoot biomass in Treatment 2 was significantly greater than in Treatments 7 and 8, while tissue N concentrations were similar, averaging {approx}13 g N kg-1. Since these treatments all received the same total amount of N, on average, these data suggest that a daily N supply is more effective than intermittent supply at maintaining standing biomass. This difference between daily and intermittent N treatments may be due to lower per tiller biomass with intermittent N, since tiller number was not affected by the schedule of N supply.


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  		Table 1. Final harvest data for shoots (S) and roots (R) of perennial ryegrass (Lolium perenne L.) grown with daily N additions or intermittent N additions. Values are means of three replicates.

 
Root biomass and length declined with increasing N rate. Treatment 5 root biomass was reduced by two thirds compared with Treatment 1, while length was reduced by {approx}30%. Reductions in biomass were countered by increasing root tissue N, resulting in relatively constant total root biomass N across N rates. This is in contrast to shoot biomass N, which increased substantially with N rate. Assuming N allocation to the root system is constant across the range of N rates, it is intriguing that biomass (and by inference, C transport) varied threefold. Of course, greater root growth in response to nutrient limitation may be a strategy to access untapped soil nutrients (Ingestad and Agren, 1988). It is also conceivable that plants experiencing moderate to severe N deficiency use the root system as a convenient sink for fixed C (storage or new growth). This would prevent photoassimilate from concentrating in the leaves and avoid, at least temporarily, product inhibition of photosynthesis (Azcon-Bieto, 1983; Hirose, 1984; Layne and Flore, 1995).

Total standing biomass N (shoot + root) ranged from 87 to 147 kg N ha-1, roughly equivalent to 2 to 3 typical applications of 50 kg N ha-1. Perennial ryegrass is often fertilized monthly during active growth, with annual amounts totaling 200 to 250 kg N ha-1 for highly maintained turf. It is thus apparent that relatively little N is sequestered in the biomass compared with the amount applied. Rather, most N absorbed by a mature ryegrass stand is allocated, at least in the long term, to new leaf tissue, as shown in Fig. 9. Certainly, as noted above, there could be considerable cycling of internal N, and replacement by recently-absorbed N, but the net result is that incoming N is almost completely balanced by outflow through production of new leaves.

Daily vs. Intermittent Nitrogen Supply
One objective of this research was to determine if N supplied on a daily basis differed from intermittent N supply in terms of turf performance (compare daily N Treatment 2 to intermittent N Treatments 6–8). Tissue N undergoes wide fluctuations with intermittent N, in contrast to the internal stability achieved with N supplied daily at the same overall rate. Nutrient instability, according to Ingestad (1980)(1981), leads to deficiency symptoms and physiological stress. An examination of the data in Table 1 indicates that, in general, intermittent N supply resulted in shoot and root systems similar to those produced under more constant supply. Likewise, average N allocation to leaf tissue, determined as the slope of cumulative clipping dry wt. vs. time curves, was also very similar between treatments (Table 2). However, leaf dry weight production was affected by N supply strategy. Cumulative leaf dry weight was plotted against time for the period 38 to 134 d, and the slopes, representing average daily growth rate, were compared. There was a relatively small (13%) but significant reduction in growth rate with intermittent N supply, particularly Treatments 7 and 8, compared with daily N (Treatment 2). While this suggests that productivity may be somewhat greater under conditions of stable tissue N, there is the additional possibility that frequent mowing cuts short the period during which recently absorbed leaf N can affect growth processes. Fairly large pulses of N reach leaf tissue shortly after an intermittent N supply event, and conceivably it might take several days or more for the N to stimulate growth and have full value in the plant. With frequent mowing, the N may be removed before reaching full value. This would be especially true with frequent mowing, as in this study.


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  		Table 2. Average daily growth rate and N allocated to leaves as a function of constant vs. intermittent N supply. All cultures received the equivalent of 50 kg N ha-1 mo-1.

 
The results of this investigation provide a detailed analysis of N rate and supply strategy as a determinant of growth response and resource allocation in perennial ryegrass turf. Daily N addition resulted in stable growth and tissue N pools, with set points determined by N rate. Less frequent (weekly to monthly) N supply caused wide fluctuations in growth and tissue N pools, but had little or no effect on long-term productivity and N use efficiency compared with daily addition at the same total rate. It should be considered that the turf cultures in this study received N only from daily or intermittent application. Under field conditions, mineralization would also be a factor. This represents a more consistent source of N than that from periodic applications of soluble, quick release N fertilizers, and in combination would tend to diminish the fluctuations associated with episodic N supply.

Received for publication February 4, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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