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Division S-3—Soil Biology & Biochemistry

Soil Carbon and Nitrogen Pools in Response to Tall Fescue Endophyte Infection, Fertilization, and Cultivar

USDA-ARS, 1420 Experiment Station Road, Watkinsville, GA 30677-2373

^* Corresponding author (afranz{at}uga.edu)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Tall fescue (Festuca arundinacea Schreb.) is an important cool-season perennial forage used for grazing animals in the humid regions of the USA and throughout the world. The fungal endophyte Neotyphodium coenophialum Glenn, Bacon, & Hanlin naturally inhabits the majority of tall fescue stands producing a variety of alkaloids in leaf tissue that can cause animal health disorders on ingestion. We hypothesized that endophyte infection would modify the stock and activity of various soil C and N pools (total, particulate, microbial biomass, and mineralizable), but that fertilization (13.4–1.5–5.6 vs. 33.6–3.7–13.9 g N–P–K m^–2 yr^–1) and cultivar (‘Kentucky-31’, K-31; ‘AU-Triumph’; and ‘Johnstone’) might alter these responses. Soil organic C and total N at a depth of 0 to 20 cm under K-31 with high fertilization were greater with high (4197 g C m^–2 and 266 g N m^–2) than with low (3872 g C m^–2 and 242 g N m^–2) endophyte infection at the end of 20 yr. Under low fertilization, soil organic C and total N were not different between low and high endophyte infection. Differences in C and N pools among cultivars with low fertilization were as large as among K-31 fertilization-endophyte comparisons, but appeared to be related to factors other than endophyte infection frequency. Carbon and N contents of small macroaggregates (0.25–1.0 mm) were the only soil properties that were related (r = 0.70, P = 0.001) to endophyte infection frequency (range of 1–79%) across all treatments. Soil C and N pools can be modified by endophyte infection, but these results narrowed this phenomenon to (i) conditions of higher fertility and (ii) predominantly in small macroaggregates.

Abbreviations: K-31, ‘Kentucky-31’

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
TALL FESCUE is the most important cool-season perennial forage in the eastern USA (Stuedemann and Hoveland, 1988), grown on approximately 14 Mha (Buckner et al., 1979). A natural, mutualistic association with a fungus (N. coenophialum; formerly Acremonium coenophialum Morgan-Jones and Gams) results in improved persistence in the seasonally drought- and heat-stressed region of the southeastern USA (Hill et al., 1991; Bouton et al., 1993). Reasons for greater persistence have been attributed to physiological responses that confer greater drought tolerance (Belesky et al., 1987a; West et al., 1993) and production of ergot alkaloids that may reduce forage intake by grazing animals, thereby reducing grazing pressure (Hoveland et al., 1983; Read and Camp, 1986; Hill et al., 1990). Toxic effects of endophyte-infected tall fescue on grazing animals have been well documented (Stuedemann and Hoveland, 1988; Bacon and Hill, 1997). Ecologically, the presence of N. coenophialum may be important in deterring plant-parasitic nematode populations (West et al., 1988) and various plant diseases (Latch, 1997).

Another ecologically important characteristic of the tall fescue–endophyte association may be the potential for greater soil organic C sequestration. Soil organic C and N concentrations were significantly enhanced and potential soil microbial activity reduced in tall fescue stands with high compared with low frequency of endophyte infection (Franzluebbers et al., 1999). These data suggest that soil microbial activity may be sufficiently reduced in the presence of endophyte infection, as to eventually lead to greater accumulation of soil organic C and N. Alternatively, it is possible that plant production may be enhanced in the presence of the endophyte (Arachevaleta et al., 1989; Hill et al., 1990) or that changes in botanical composition of pastures with time might alter C inputs to soil. For example, tall fescue stands without endophyte association do not always persist as well as those with endophyte infection (Read and Camp, 1986; Bouton et al., 1993), which could result in encroachment by other plants leading to different quantity and quality of plant residues supplied to soil. Changes in botanical composition, such as tall fescue decline with bermudagrass (Cynodon dactylon L.) encroachment, could have either positive or negative consequences on soil C and N cycling (Wedin and Tilman, 1996).

The conditions under which endophyte infection of tall fescue might alter soil C and N cycling are currently limited to knowledge of endophyte effects on plant response variables (Malinowski and Belesky, 2000). Increased soil N availability may enhance accumulation of ergot alkaloids in tall fescue leaves (Lyons and Bacon, 1984; Belesky et al., 1988), and therefore could be expected to exacerbate differences in ergot alkaloid production between low- and high-endophyte-infected stands. In contrast, root and shoot dry matter production of endophyte-infected tall fescue plants responded less to increasing soil P availability than endophyte-free tall fescue plants (Malinowski et al., 1998). Therefore, the interaction of soil fertility with endophyte infection could be expected to have complex effects on soil C and N pools. In addition, the effects on soil C and N pools under pastures with varying levels of (i) endophyte infection frequency and (ii) ground cover due to natural pasture development are largely unknown.

Since soil microbial activity per unit of soil organic C was found to be inhibited by high compared with low endophyte infection (Franzluebbers et al., 1999), soil fractions rich in biologically active C and N pools could be expected to be altered most extensively. Water-stable macroaggregates (>0.25 mm) often contain higher quantities of mineralizable C and N than microaggregates (Elliott, 1986; Beare et al., 1994). Small macroaggregates (0.25–1.0 mm) are sometimes more enriched in biologically active C than large macroaggregates (1.0–4.75 mm) (Franzluebbers and Arshad, 1997).

We hypothesized that endophyte infection would increase the stock of soil organic C and N and decrease the size and activity of soil microbial biomass C and N, but that long-term differences in soil fertility might alter these responses. Further, difference in pasture composition due to progressive tall fescue decline in low-endophyte-infected plantings was hypothesized to partially explain changes in soil organic C and N pools in mature (>10 yr) tall fescue pastures. The objective of this investigation was to quantify soil C and N pools under 20-yr-old tall fescue pastures varying in endophyte infection frequency, fertilization history, and cultivar.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Site Characteristics
A field experiment was initiated in autumn 1981 near Watkinsville, GA (33°62' N, 83°25' W) on a Cecil sandy loam (clayey, kaolinitic, thermic Typic Kanhapludults). Long-term mean annual temperature for the area is 16.5°C, precipitation is 1250 mm, and pan evaporation is 1560 mm. During the period 1981 to 2001, yearly precipitation was 1220 ± 233 mm.

Experimental Setup and Management
The experimental design was a randomized complete block design with three replications of six treatments, as described earlier in Belesky et al. (1988). Treatments included (i) low-endophyte-infected K-31 tall fescue (<7% seed infection) with low fertilization (13.4–1.5–5.6 g N–P–K m^–2 yr^–1), (ii) low-endophyte-infected K-31 tall fescue with high fertilization (33.6–3.7–13.9 g N–P–K m^–2 yr^–1), (iii) high-endophyte-infected K-31 tall fescue (80% seed infection) with low fertilization, (iv) high-endophyte-infected K-31 tall fescue with high fertilization, (v) low-endophyte-infected AU-Triumph (Triumph) tall fescue with low fertilization, and (vi) low-endophyte-infected Johnstone tall fescue with low fertilization. Each of the 18 paddocks (0.7 ha) was grazed periodically with Angus cattle each year following establishment, primarily in spring and autumn, when growth of tall fescue was most vigorous. Paddock design was described in Wilkinson et al. (1989). All fertilization was suspended after 1997 to help avoid further accumulation of inorganic N in the soil profile below 0.3 m (Franzluebbers et al., 2000a). Termination of fertilizer application during the final 4 yr was not expected to greatly alter relative differences in soil organic C and N pools among treatments, which would have developed during the first 16 yr of this experiment.

Sampling and Analyses
Tall fescue tillers were collected yearly from 1983 to 1996 for determination of endophyte-infection frequency according to the procedure described in Belesky et al. (1987b). Six to 20 tillers per paddock were randomly collected during each of 7 ± 4 mo of the year. Although we did not measure alkaloid production throughout the course of the experiment, Belesky et al. (1988) showed that ergopeptine alkaloid levels in tall fescue leaf tissue were two- to threefold greater under high than low endophyte infection.

Basal ground cover (i.e., botanical composition of pasture) was evaluated in May 2001 from 30 areas (0.25 m² each) separated by >10 m in each paddock, all by the same experienced technician. Percentages of basal area (with separations in multiples of five) were calculated for the following six classes: (i) tall fescue, (ii) winter annual grass, (iii) bermudagrass, (iv) Paspalum spp., (v) broadleaves, and (vi) bare ground. None of the paddocks had measurable composition of Paspalum spp.

Soil was collected at depths of 0 to 3, 3 to 6, 6 to 12, and 12 to 20 cm in May 2002. Each paddock was divided into two zones for sampling: (i) a 0.5-ha area that included shade and water sources, and (ii) a 0.2-ha area farthest away from shade and water sources. Soil was composited from eight randomly located subsampling sites in Zone 1 and from five randomly located subsampling sites in Zone 2. Following removal of forage above 4 cm, surface residue from individual 0.04-m² subsampling sites was cut to the mineral surface with battery-powered hand shears, bagged, and dried at 55°C for several days. A 4-cm-diam. soil core was collected from each of the subsampling sites and sectioned into depth increments. Soil was oven-dried (55°C, 72 h), weighed, and gently crushed to pass a 4.75-mm screen to partially homogenize sample and remove stones (<1% of weight).

Soil bulk density was calculated from the oven-dried soil weight and pooled-core volume (1.88 to 8.04 x 10^–4 m³, depending on depth and zone). Soil for subsequent analyses was stored dried at ambient conditions. A subsample was ground in a ball mill to a fine powder and analyzed for total C and N with dry combustion (Leco CNS-2000, St. Joseph, MI).¹ It was assumed that total C was equivalent to organic C because soil pH was near 6.

Mineralizable C was determined from two subsamples of soil (27.5 g each for 0- to 3-cm depth, 48 g each for 3- to 6-cm depth, and 65 g each for 6- to 12- and 12- to 20-cm depths) wetted to 50% water-filled pore space (Franzluebbers, 1999), placed into a 1-L canning jar along with vials containing 10 mL of 1 M NaOH to trap evolved CO₂ and water to maintain humidity, and incubated at 25 ± 1°C for 24 d. Alkali traps were replaced at 3 and 10 d. Evolved CO₂ was calculated by titrating alkali with 1 M HCl to a phenolphthalein endpoint following precipitation of carbonate with excess BaCl₂. At 10 d of incubation, one of the subsamples was removed, fumigated for 24 h with CHCl₃, aerated, placed into a separate canning jar along with alkali and water, and incubated for 10 d at 25°C. Soil microbial biomass C was calculated from the quantity of CO₂ evolved during 10 d following fumigation divided by an efficiency factor of 0.41 (Voroney and Paul, 1984). Mineralizable N was determined from the same incubation as for C, representing the difference in inorganic N concentration between 0 and 24 d of incubation. Inorganic N (NH₄–N + NO₂–N + NO₃–N) was determined from the filtered extract of a 10-g subsample of oven-dried (55°C, 48 h) and sieved (<2 mm) soil shaken with 20 mL of 2 M KCl for 30 min using salicylate-nitroprusside and Cd-reduction autoanalyzer techniques (Bundy and Meisinger, 1994).

Particulate organic C and N were determined by shaking the oven-dried (55°C, 72 h) fumigated sample previously used for microbial biomass determination with 0.01 M Na₄P₂O₇ for 16 h, collecting the sand plus organic matter retained on a 0.053-mm screen, oven-drying (55°C, 72 h), weighing, grinding to a fine powder, and determining the C and N concentration using dry combustion as described previously.

For aggregate distribution and stability analyses, soil was initially oven-dried (55°C) and gently crushed to pass a 4.75-mm screen (Franzluebbers et al., 2000b). Dry aggregate distribution was determined by placing either a 50-g (0- to 3- and 3- to 6-cm depths) or a 100-g (6- to 12- and 12- to 20-cm depths) portion of soil on top of a nest of sieves (200-mm diam. with openings of 1.0, 0.25, and 0.053 mm), shaking for 1 min at Level 6 on a sieve shaker (CSC Scientific Company, Fairfax, VA, Catalogue No. 18480), and weighing soil retained on the screens and that passing the 0.053-mm screen. Water-stable aggregate distribution was determined from the reconstituted sample used for dry aggregate distribution placed on top of a nest of sieves (175-mm diam. with openings of 1.0 and 0.25 mm), immersed directly in water, and oscillated for 10 min (20-mm stroke length, 31 cycles min^–1). The two sieves were placed in an oven to dry (55°C, 24 h). Water and soil passing the 0.25-mm sieve was poured over a 0.053-mm sieve, with retained soil washed with a gentle stream of water and transferred into a drying bottle using a small stream of water. The <0.053-mm fraction was calculated as the difference between initial soil weight and summation of the other fractions. All fractions were oven-dried at 55°C for >24 h following visual dryness.

Mean-weight diameter of both dry- and water-stable aggregates was calculated by summing the products of aggregate fractions and mean diameter of aggregate classes. Macroaggregates were defined as soil retained on 1.0- and 0.25-mm sieves. Large macroaggregates were defined as soil retained on the 1.0-mm sieve. Stability of macroaggregates was calculated as the fraction of water-stable macroaggregates divided by the fraction of dry-stable macroaggregates. Stability of mean-weight diameter was calculated as water-stable mean-weight diameter divided by dry-stable mean-weight diameter.

Total C and N of the 1.0- to 4.75-, 0.25- to 1.0-, and 0.053- to 0.25-mm water-stable aggregate fractions were determined using dry combustion as described previously. The 1.0–4.75-mm fraction was ball milled to a fine powder before analysis, but other fractions were not.

Data from Zones 1 and 2 within a paddock were averaged and not considered a source of variation in the ANOVA using the general linear models procedure (SAS Institute, 1990). A priori orthogonal contrasts and unprotected least significant differences were used to separate means. Concentration of various soil properties (e.g., mg g^–1) was converted to content (g m^–2) using bulk density and soil volume. Analysis of variance for soil properties was conducted separately by cumulative-profile increments according to a randomized complete block design. Soil properties in cumulative-profile increments were from the sums of individual depth contents. Effects were considered significant at P < 0.1. Linear regression of endophyte-infection frequency on year of sampling was used to compute an average change. Correlations among soil and plant properties were determined using paddock means (n = 18) and declared significant only at P < 0.01.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Pasture Characteristics
Endophyte-infection frequency of tall fescue tillers was significantly greater in high- than in low-endophyte-infection paddocks, as was expected from the initial experimental setup (Table 1). However, there was a steady increase (P < 0.001) in endophyte-infection frequency with time in all treatments, except under (i) K-31 with low endophyte infection–high fertilization and (ii) Triumph (Fig. 1). The yearly change in endophyte-infection frequency was 1.9 and 1.2% yr^–1 (values different at P < 0.1) under K-31 with low and high endophyte infection–low fertilization, 0.6 and 2.3% yr^–1 (values different at P < 0.01) under K-31 with low and high endophyte infection–high fertilization, and 0.1 and 2.3% yr^–1 (values different at P < 0.001) under Triumph and Johnstone.

View larger version (32K): [in this window] [in a new window]   Fig. 1. Endophyte infection frequency of tall fescue tillers during the period of 1983 to 1996 as affected by endophyte infection level at planting (low = 7% seed infection, high = 80% seed infection), fertilization (low = 13.4–1.5–5.6 g N–P–K m–2 yr–1, high = 33.6–3.7–13.9 g N–P–K m–2 yr–1), and cultivar (Triumph and Johnstone). Lines represent linear regression, the results of which are specified in the text.

Whole-Soil Carbon and Nitrogen Pools
Endophyte Effect
Soil bulk density was not significantly different among pasture treatments at any soil depth (Table 2). However, soil bulk density did increase with depth in all pastures, as is typical for soils of this region (Franzluebbers et al., 2000b).

Particulate/total organic C and N were both reduced under high than under low endophyte infection of K-31 (Table 5). This observation partially contradicts previous findings of Franzluebbers et al. (1999). In this earlier study, particulate organic C and N were greater with high than with low endophyte infection, although the ratios of particulate/total organic C and total N were not significantly different. Particulate organic C and N below the residue-enriched surface soil can be considered an indicator of root proliferation, which would be expected to be greater under high than low endophyte infection (De Battista et al., 1990).

Fertilization Effect
The influence of long-term previous fertilization on soil C and N pools was limited. Increased fertilization resulted in significantly greater (8 ± 2%) soil organic C and total N at a depth of 0 to 12 and 0 to 20 cm (Tables 2 and 3). A similar fertilization effect was observed for particulate organic C, but not for particulate organic N. Residual inorganic N in surface soil was low in all pastures, but greater with increased fertilization under low endophyte infection (Table 3).

Soil organic C content at a depth of 0 to 12 cm was positively correlated with the area of bare ground (r = 0.60, P = 0.01). More bare ground may have been a result of at least two phenomena: (i) lush growth of tall fescue clumps at various times of the year due to high fertilization and high endophyte infection, which would have shaded neighboring areas and prevented a more complete distribution of plant bases, and (ii) greater number of dung pats that might have temporarily smothered plants in small areas. Both of these possibilities would have likely enhanced C input to soil. The only other whole-soil property that was significantly affected by pasture characteristics was the ratio of mineralizable/total N, which declined (r = –0.59, P = 0.01) with increasing area of broadleaves. Although residue quality of broadleaves might be different than that of various grasses, and therefore affect mineralizable N, the occurrence and persistence of broadleaves in pastures are not likely stable with time. Various other biotic and abiotic factors would also likely play roles in forming this association.

Cultivar Effect
Although both Triumph and Johnstone were planted with similarly low endophyte infection frequency, tall fescue tillers in Johnstone pastures increased in endophyte infection frequency with time while tillers in Triumph pastures remained low (Fig. 1). Using these two cultivars as a surrogate for differences in endophyte infection frequency, soil C and N pools did not respond the same as compared with K-31 endophyte infection treatments (Tables 2– 4). Particulate organic C at a depth of 0 to 6 cm was the only soil property that was significantly different between Triumph (2% infection) and Johnstone (43% infection). Besides differences in endophyte infection level, these two cultivars may have also differed in quantity, quality, timing, and architecture of various root and shoot properties that could have affected soil C and N properties.

The largest differences in soil organic C and total N among cultivars were between K-31 and Triumph, with soil under Triumph having 10 to 17% higher values. Because of the low basal area of tall fescue (28%) and low endophyte infection frequency (2%) in Triumph pastures, changes in soil C and N appear unlikely to have originated from a direct endophyte effect, but rather indirectly from changes in ground cover with time and forage quality. We did not measure forage quality among tall fescue cultivars before termination of the experiment in May 2002, but Hill et al. (1990) noted significant differences in forage quality among tall fescue genotypes. We observed a greater area of broadleaves and bare ground in Triumph pastures than in K-31 or Johnstone pastures (Table 1). The reason why Triumph pastures contained greater soil organic C and total N than the other two cultivars is not easily explained. If a greater percentage of bare area would have been derived from dung pats (not measured) that smothered forage, then there should have also been higher particulate organic C and N and residual inorganic N (Table 3). However, this was not observed.

Stability and Carbon and Nitrogen Content of Aggregates
Stability of macroaggregates (>0.25 mm) and stability of mean-weight diameter in water were both high in all pastures sampled (Table 6). Only at a depth of 12 to 20 cm did soil aggregates indicate any breakdown in water. These high aggregate stability indices under long-term tall fescue pastures are consistent with values reported for other conservation management systems in the same region (Franzluebbers et al., 2000b). Perhaps as a result of these overall high values, there were no differences in aggregate stability indices due to endophyte infection or fertilization.

Cultivar effects on soil C and N in aggregate fractions were also significant only for small macroaggregates (Table 7). Carbon and N contents of small macroaggregates were greater under K-31 than under Triumph and Johnstone pastures.

The only pasture characteristic associated with soil aggregate properties was endophyte infection frequency at the end of 1996, which was positively correlated (r = 0.70, P = 0.001) with C and N contents in small macroaggregates at a depth of 0 to 12 cm. The C and N contents in small macroaggregates were the only soil properties that were consistently related to endophyte infection frequency, irrespective of fertilization and cultivar differences.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Tall fescue pastures had levels of endophyte infection ranging from 1 to 79% and had naturalized during 20 yr of management into mixed stands of tall fescue (28–82% of basal area), bermudagrass (3–28%), winter annual grass (1–9%), and broadleaves (3–24%). Soil organic C and total N were greater with high than with low endophyte infection of K-31 tall fescue and greater under high fertility. Biologically active organic matter (i.e., soil microbial biomass and mineralizable C and N) per unit of soil organic C and total N were depressed under high compared with low endophyte infection of K-31, suggesting some inhibition of the active pools of organic C and N by endophyte-infected tall fescue. The effect of endophyte infection on soil C and N pools was stronger under high fertility. Carbon and N contents of small macroaggregates (0.25–1.0 mm) were the most consistent and sensitive organic matter pool to endophyte infection, irrespective of fertilization regime or cultivar of tall fescue pastures. Accumulation of C and N due to endophyte infection occurred preferentially in macroaggregates, suggesting a biophysical mechanism of protection that should be explored further.

	ACKNOWLEDGMENTS

 
This research was partially supported by the Office of Science (BER), U.S. Department of Energy, Grant No. DE-IA02-00ER63021. We appreciate the technical expertise of Steve Knapp, Eric Elsner, Devin Berry, Heather Hart, Kim Lyness, Dwight Seman, David Hildreth, Fred Hale, and Ned Dawson during various aspects of this research.

	NOTES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
¹ Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA.

Received for publication January 16, 2004.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

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