Published in Agron J 91:897-902 (1999)
© 1999 American Society of Agronomy
677 S. Segoe Rd., Madison, WI 53711 USA
Agronomy Journal 91:897-902 (1999)
© 1999 American Society of Agronomy
FORAGES
Fungal Endophyte Effects on Production of Legumes in Association with Tall Fescue
Carl S. Hovelanda,
Joseph H. Boutona and
Robert G. Durhama
a Dep. of Crop and Soil Sci., Univ. of Georgia, Athens, GA 30602 USA
hoveland{at}arches.uga.edu
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ABSTRACT
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The fungal endophyte, Neotyphodium coenophialum (Morgan-Jones & W. Gams) Glenn, Bacon & Hanlin (syn. Acremonium coenophialum Morgan-Jones & W. Gams) is generally considered to enhance the competitive ability of tall fescue (Festuca arundinacea Schreb.) with legumes, but substantiating field data are limited. Our objectives were to determine if endophyte infection of tall fescue affects stand density and forage production of (i) red clover (Trifolium pratense L.), ladino clover (T. repens L.), and alfalfa (Medicago sativa L.) harvested at 3-wk intervals and (ii) alfalfa at low and high seeding rates harvested at 3-wk and 9-wk intervals. The first study compared alfalfa, red clover, and ladino clover in association with `Jesup' E+ (endophyte-infected) and E- (endophyte-free) tall fescue, harvested at 3-wk intervals for 3 yr. The second study had alfalfa broadcast planted at 11.2 and 22.4 kg ha-1 with E+ and E- tall fescue planted broadcast at 11.2 and 22.4 kg ha-1 or in rows at 22.4 kg ha-1. This was harvested at 3-wk intervals for 3 yr, then at 5-wk intervals for 1 yr. In the first study, clovers and alfalfa cut at 3-wk intervals for 3 yr had similar (P > 0.05) legume yields when grown with both E+ and E- tall fescue. In the second study harvested at 3-wk intervals, E+ tall fescue adversely affected (P < 0.05) the associated alfalfa the second year, and by the third year the yield of alfalfa planted at 22.4 kg ha-1 in mixture with E+ tall fescue was only 71% of alfalfa with E- tall fescue (P < 0.05). Similar differences occurred the next year when cut at 5-wk intervals. Stands of alfalfa or tall fescue after 4 yr were not affected (P > 0.05) by endophyte. The results suggest that endophyte infection of tall fescue increases competition with legumes, but it may be modified by seeding rates or grass sod density.
Abbreviations: E+, endophyte-infected • E-, endophyte-free
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INTRODUCTION
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ENDOPHYTE INFECTION
of tall fescue is a major cause of reduced ruminant animal performance in the USA. Replanting with E- tall fescue is difficult and costly, so the most frequent method of ameliorating the toxicity problem is seeding legumes in E+ tall fescue pastures to dilute the toxic effects (Ball, 1997). With a strong legume component in the sward, this method can be effective, but maintaining an adequate amount of legume in the forage over much of the season is difficult and unreliable. Competition from associated grasses is associated with morphological and physiological differences that respond to changing environmental factors (Chamblee, 1972; Harper, 1978; Haynes, 1980). Tall fescue is highly competitive with alfalfa, red clover, and white clover (T. repens) (Fales et al., 1996). However, there is no way to ascertain the endophyte status of the grass in older literature. Legume persistence in tall fescue pastures is particularly difficult in the southeastern USA, where environmental stress from heat, drought, pests, and warm-season grass competition is greater than at higher latitudes (Hoveland, 1989).
Endophyte infection induces a number of physiological and morphological changes in tall fescue that confer several benefits, such as increased tillering and greater drought tolerance, improving competitiveness with other plant species (Bouton et al., 1993; Leuchtmann, 1997; Marks and Clay, 1996; Marks et al., 1991). These benefits should result in less legume growth in association with E+ than with E- tall fescue. Several studies in New Zealand comparing mixed swards of E+ and E- perennial ryegrass (Lolium perenne L.) found that white clover productivity was greater and plant survival was better in E- grass sod (Stevens and Hickey, 1990; Sutherland and Hoglund, 1989). Eerens et al. (1998) reported 40% more white clover in E- than E+ perennial ryegrass pasture during a drought year, but no difference during 4 yr with adequate rainfall. Prestridge et al. (1992) in New Zealand and Lewis (1992) in England reported no significant reduction in plant survival and growth of white clover in mixture with E+ infected perennial ryegrass. Marks and Clay (1996) also found no competitive advantage of E+ over E- perennial ryegrass with other grasses.
Research data on legume response to the endophyte of tall fescue in swards are limited. In a 3-yr Tennessee grazing study (Fribourg et al., 1991), ladino clover decreased in E+ tall fescue and increased in E- tall fescue during the first year, but this difference was not apparent in the next two years. This shift was attributed to preferential grazing of clover in the E+ tall fescue rather than to any competitive effects.
Shortening the cutting interval and lowering the cutting height decreased the legume component in grass mixtures with erect-growing legumes such as alfalfa and red clover, but had little effect on white clover–grass mixtures (Fales et al., 1996). During a 3-yr study with E- tall fescue–alfalfa mixtures, the legume percentage declined with more frequent cutting intervals of 6, 4, and 3 weeks (Hoveland et al., 1995). No similar data are available that compare E+ and E- tall fescue–legume mixtures. In a 3-yr Georgia study, there were no differences in stem population or first-year forage yield of alfalfa no-till planted in E+ and E- tall fescue sods (Hoveland et al., 1997). Thus, even though the competitive advantage of E+ over E- tall fescue in a mixture is well established (Hill et al., 1991; Marks et al., 1991; Clay, 1997), there is little evidence that this competitiveness affects stand persistence and productivity of associated legumes.
Our objectives were to determine if endophyte infection in tall fescue affects stand density and forage production of: (i) red clover, ladino clover, and alfalfa harvested at 3-wk intervals and (ii) alfalfa at low and high seeding rates harvested at 3-wk and 5-wk intervals.
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Materials and methods
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Clovers and Alfalfa
The experiment was established at the Plant Sciences Farm in the Piedmont area near Athens, GA (33°52' N 83°32' W, elevation 240 m), on Cecil coarse sandy loam soil (fine, kaolinitic, thermic Typic Kanhapludults). The land had been fallowed for about three months following a winter crop of wheat (Triticum aestivum L.). The treatments consisted of E+ and E- Jesup tall fescue in monoculture and in all combinations with `Alfagraze' alfalfa, `Redland III' red clover, and `Osceola' ladino clover. Each of the eight treatments had six replications of 1.2- by 6.1-m plots in a randomized complete block design. The soil pH was 6.6, and 24 kg ha-1 P and 186 kg ha-1 K were applied annually according to soil test recommendations. An application of 30 kg N ha-1 was made at planting, after which no additional N was applied. Tall fescue seed were planted in early October 1993 on a well-prepared seedbed in 23-cm rows at 17 kg ha-1. Legumes were broadcast planted at the same time with seeding rates of 2 kg ha-1 for ladino clover, 17 kg ha-1 for red clover, and 22.4 kg ha-1 for alfalfa. Tall fescue seed were grown in Georgia and were tested for endophyte infection level. Tall fescue endophyte levels were determined by microscopically examining stained leaf sheaths for presence of hyphae. Forage was harvested at 3-wk intervals from April until October during 1994 to 1996, resulting in 10 harvests. Percentage of legume in each plot was estimated visually prior to harvest. Hand separations were done twice each year, verifying that visual estimates were accurate. Samples of about 0.5 kg were taken from the harvested forage and dried for 48 h at 65°C in a forced-air oven for dry matter determinations.
Stands were sampled annually to determine changes in tall fescue and legume stand density. Alfalfa shoot and plant numbers and tall fescue tiller and plant numbers were counted in three 0.09-m quadrats randomly placed in each plot at each sampling date. The mean of the three quadrats was used for statistical analysis of the treatments.
Alfalfa
Jesup E+ and E- tall fescue were planted in early October 1993 with Alfagraze alfalfa utilizing three establishment treatments: (i) alfalfa broadcast at 11.2 kg ha-1 and tall fescue broadcast at 22.4 kg ha-1; (ii) alfalfa broadcast at 22.4 kg ha-1 and tall fescue broadcast at 11.2 kg ha-1; and (iii) alfalfa broadcast at 22.4 kg ha-1 and tall fescue in 15.2-cm rows at 22.4 kg ha-1. Each of the six treatment combinations had six replications of 1.2- by 6.1-m plots in a randomized complete block design. Planting and harvesting operations were similar to the previous experiment. After 3 yr of harvesting at 3-wk intervals, the study was continued for a fourth year, using 5-wk intervals to determine if endophyte effects on competition would be enhanced.
For both studies, analysis of variance (ANOVA) was conducted using the Statistical Analysis System (SAS Inst., 1988), with endophyte and legume or endophyte and planting rate considered fixed effects and blocks random effects. Differences in forage yield or plant populations between individual treatment means were evaluated using Fisher's protected least significant difference.
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Results
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Rainfall during the first year of the experiments was low in April and May, followed by above-normal moisture the remainder of the growing season. The second year, rainfall was low during this critical spring period, contributing to low forage yields. During the third year, rainfall was below normal from May through July and extremely low in October. In contrast, rainfall during the fourth year was much above normal and generally well distributed over the growing season. Endophyte levels were 0% for E- and 85% for E+ tall fescue during these experiments.
Clovers and Alfalfa
The tall fescue endophyte had no effect (P > 0.05), nor was there an endophyte x legume–grass interaction in any of the 3 yr on forage yield of legume or legume + tall fescue (Table 1) . Legume species differed (P < 0.05) in yield during the second and third years. Red and ladino clovers were more productive (P < 0.05) than alfalfa during these two years (Table 2)
. Although the yield of all three legumes generally showed a decline each year, the decline was much greater for alfalfa, which probably suffered more from competition. Yields of tall fescue monocultures (labeled as `none' in Table 2) were low and declined each year, probably a negative response to the absence of N fertilization. Endophyte also had no effect (P > 0.05) on tall fescue forage yield in the no-legume treatment (data not shown). In the mixtures, tall fescue was dominated by the legume species each year and generally made up much less than one-half of each sward (Table 2).
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Table 1 Analysis of variance of the effects of fungal endophyte (E), legume species (L), and year (Y) on forage yield of the legume component and legume + tall fescue mixture*
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Table 2 Forage dry matter yield of the cool season perennial legume (L) component and legume + tall fescue (TF) mixtures (mean of endophyte-infected and endophyte-free tall fescue) when harvested every 3 wk at Athens, GA
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Legume shoot numbers and tall fescue tillers or plant numbers were not affected (P > 0.05) by tall fescue endophyte infection, matching the trend observed for forage yield (Table 3)
. At the end of 3 yr, shoot numbers were highest (P < 0.05) on ladino clover (65 m-2), followed by alfalfa (33 m-2) and red clover (24 m-2). The loss in red clover shoot numbers is expected for this short-lived legume; however, tall fescue stands were depleted to a greater extent by red clover than alfalfa (P < 0.05).
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Table 3 Legume and tall fescue plant populations as affected by fungal endophyte (E-, endophyte-free; E+, endophyte-infected) in associated tall fescue
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Alfalfa
In the second experiment, endophyte infection had no effect (P > 0.05) on alfalfa forage yield the first year, but E+ significantly reduced alfalfa yield during the second (P < 0.05) and third (P < 0.01) years (Tables 4 and 5)
. Interactions between endophyte and planting method were not significant (P > 0.05). As in the previous experiment, alfalfa and alfalfa + tall fescue yields declined after the first year (Table 5). Alfalfa dominated swards the first year, but in succeeding years tall fescue generally constituted one-third to one-half of the sward or more. There were no differences (P > 0.05) in alfalfa yield between tall fescue planted in rows at the high seeding rate vs. broadcast at the low seeding rate when alfalfa was planted at the high rate (Table 6)
. Unfortunately, because of confounding, there is no way to determine if the lower alfalfa yields with tall fescue broadcast at the high rate and alfalfa at the low rate are a result of the low alfalfa or high tall fescue seeding rate.
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Table 4 Analysis of variance of the effects of fungal endophyte (E), planting method (P), and year (Y) on forage yield of the alfalfa component and alfalfa + tall fescue mixture
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Table 5 Forage dry matter yield of the alfalfa (A) component and alfalfa–tall fescue (TF) mixture as affected by fungal endophyte when harvested every 3 wk at Athens, GA. Values are averaged over three planting treatments
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Table 6 Forage dry matter yield of the alfalfa (A) component and alfalfa + tall fescue (TF) mixtures as affected by planting method when harvested every 3 wk at Athens, GA. Values are averaged over endophyte-free and endophyte-infected tall fescue
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Alfalfa and alfalfa + tall fescue forage yields in the fourth year (1997) were much higher than in the three previous years, a result of harvesting at 5-wk intervals (Table 7)
and much better rainfall. The endophyte effect and the endophyte x planting method interactions were highly significant (P < 0.01) for yields of both alfalfa and alfalfa + tall fescue in 1997 (Table 4). Yields of alfalfa associated with E+ were depressed 27 to 36%, compared with E- tall fescue, at the high alfalfa seeding rate, while there was no difference (P > 0.05) at the low alfalfa seeding rate, which also had a high tall fescue seeding rate (Table 7). Total alfalfa–grass yield trends were similar. Alfalfa dominated the swards in all cases, probably a result of the more favorable harvest intervals.
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Table 7 Forage dry matter yield of the alfalfa (A) component and alfalfa + tall fescue (TF) mixtures as affected by fungal endophyte when harvested every 5 wk for 1 yr at Athens, GA. Stands were harvested every 3 wk the previous 3 yr
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Alfalfa plant populations in all treatments declined over 4 yr (Table 8)
. At any planting method–rate combination, tall fescue endophyte infection had no effect (P > 0.05) on alfalfa plant numbers. However, at the last sampling date in broadcast planted tall fescue, tall fescue plant populations within an endophyte level were higher (P < 0.05) at the high than low seeding rate. Results of this experiment suggest that planting rate as well as harvest interval may influence alfalfa yield response to tall fescue fungal endophytes in mixtures with grass. However, this experiment does not provide conclusive evidence because of the confounding treatment effects.
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Table 8 Alfalfa and tall fescue plant populations as affected by fungal endophyte in associated tall fescue, Athens, GA
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Discussion
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The lower yield of alfalfa, relative to red and ladino clover, during the second and third years of the first study was likely a result of defoliation at 3-wk intervals, which probably reduced root carbohydrate reserves. In addition, with its very favorable leaf spatial arrangement and greater leaf area, alfalfa can intercept more light energy than the clovers with their planophile leaf orientation (Chamblee, 1972). Defoliation at 3-wk intervals penalized alfalfa by preventing accumulation of sufficient leaf area to reach its light interception potential. Thus, a longer cutting interval should favor alfalfa in competition with other species.
Our results of performance of legumes grown with tall fescue containing fungal endophytes was similar to the perennial ryegrass results of Prestridge et al. (1992) and Lewis (1992), but differ from the competitive effects of endophyte reported by Clay (1997), Stevens and Hickey (1990), and Sutherland and Hoglund (1989). Although less than normal rainfall occurred during April and May in each of the 3 yr of our study, white clover yield was not greater in E- than in E+ tall fescue, as had been reported for perennial ryegrass during a drought year in New Zealand (Eerens et al., 1998).
Alfalfa yield response to competition with E+ tall fescue in our two adjacent field experiments contrasts sharply, even though we used the same E+ and E- tall fescue germplasm. This may be related to the complexity of interspecies competition. Several reviewers have shown a large number of management and environmental factors that affect competition of grasses and legumes (Chamblee, 1972; Harper, 1978; Haynes, 1980). Thus, the potential competitive advantage of E+ tall fescue may vary among legume species and be diminished under particular production practices. In the clover–alfalfa study, the lower tall fescue seeding rate in wide rows may have provided less grass competition with the legumes than occurred in the separate study with alfalfa. In the alfalfa study, the competitive advantage of E+ tall fescue was not expressed until the second and third years, indicating that considerable time may be needed to effect botanical changes. This agrees with a previous study where endophyte infection level of tall fescue had no effect on the associated alfalfa during the first year (Hoveland et al., 1997).
Seeding rates affected the legume competitive response with E+ tall fescue in the sward in the fourth year. With a low alfalfa and high tall fescue seeding rate, alfalfa growth was similar (P > 0.05) in E+ and E- tall fescue (Table 7). With high alfalfa and low tall fescue seeding rates, however, there was increased (P < 0.05) alfalfa yield when grown with E- tall fescue. The higher (P < 0.05) alfalfa plant numbers at the high seeding rate during the final year may have furnished more competition for E- than with E+ tall fescue. This was especially noticeable when the harvest interval was increased from 3 wk to 5 wk (Table 7). Although tall fescue populations were greater (P < 0.05) at the high seeding rate, alfalfa was better able to compete with E- than with E+ tall fescue. The 5-wk cutting interval improved the competitive ability of alfalfa and demonstrated the depressing effect of the tall fescue endophyte on the associated legume to a greater extent than when cut at 3-wk intervals. The lack of response by all legumes to the competitive effects of E+ tall fescue in the clover–alfalfa experiment may be related to the associated tall fescue being row-planted at a lower planting rate than in the alfalfa experiment.
The nature of the competitive effect of E+ tall fescue on the associated alfalfa is an interesting question. Alfalfa and tall fescue plant numbers were similar (P > 0.05) regardless of the infection status of the tall fescue (Table 8). However, it is possible that greater plant vigor of E+ tall fescue may reduce space for the associated alfalfa, while better rooting of E+ tall fescue may favor drought tolerance and greater soil water extraction than is possible with E- grass (Bouton et al., 1993; Marks and Clay, 1996). Marks and Clay (1996) found that the photosynthetic rate of E- tall fescue decreased by about 25% at temperatures above 35°C, while E+ tall fescue had little decline. This suggests that the greater carbon exchange rate by E+ tall fescue at high temperature, possibly because of less photorespiration, may result in a higher plant growth rate than E- tall fescue and thus create more competition with the associated alfalfa. Since high summer temperatures are common in the southeastern USA, greater potential for growth by E+ tall fescue during this period would be expected to extract more soil water and place additional stress on the alfalfa. Even subtle advantages over time may give a competitive advantage to the E+ infected grass.
Results of these studies were mixed, but indicate that the greater competitive effects of E+, compared with E- tall fescue, under conditions that stress the grass (e.g., high alfalfa population and long harvest intervals) will adversely affect the associated legume over time. Many natural environmental and management factors probably influence the expression of this competitive advantage. However, it is likely that grass containing endophytes will affect persistence and productivity of legumes in dense mixed swards under stressful conditions.SAS Institute 1988
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NOTES
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Work supported by state and Hatch funds allocated to the Georgia Agric. Exp. Stn.
Received for publication November 2, 1998.
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REFERENCES
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- Ball D.M. Significance of endophyte toxicosis and current practices in dealing with the problem in the United States. In: Bacon C.W., Hill N.S., eds. Neotyphodium/grass interactions. New York: Plenum Press, 1997:395-410.
- Bouton J.H., Gates R.N., Belesky D.P., Owsley M. Yield and persistence of tall fescue in the southeastern Coastal Plain after removal of its endophyte. Agron. J. 1993;85:52-55.[Abstract/Free Full Text]
- Clay K. Consequences of endophyte-infected grasses on plant diversity. In: Bacon C.W., Hill N.S., eds. Neotyphodium/grass interactions. New York: Plenum Press, 1997:109-124.
- Chamblee D.S. Relationships with other species in a mixture. In: Hanson C.H., ed. Alfalfa science and technology. Madison, WI: ASA, 1972:211-228 Agron. Monogr. 15..
- Eerens J.P.J., Lucas R.J., Easton H.S., White J.G.H. Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool moist environment. N.Z. J. Agric. Res. 1998;41:39-48.
- Fales S.L., Laidlaw A.S., Lambert M.G. Cool-season grass ecosystems. In: Moser et al L.E., ed. Cool-season forage grasses. Madison, WI: ASA, CSSA, and SSSA, 1996:267-296 Agron. Monogr. 34..
- Fribourg H.A., Chestnut A.B., Thompson R.W., McLaren J.B., Carlisle R.J., Gwinn et al K.D. Steer performance in fescue–clover pastures with different levels of endophyte infestation. Agron. J. 1991;83:777-781.[Abstract/Free Full Text]
- Harper J.L. Plant relations in pastures. In: Wilson J.R., ed. Plant relations in pastures. Melbourne: CSIRO, 1978:3-14.
- Haynes R.J. Competitive aspects of the grass–legume association. Adv. Agron. 1980;33:227-261.
- Hill N.S., Belesky D.P., Stringer W.C. Competitiveness of tall fescue as influenced by Acremonium coenophialum. Crop Sci. 1991;31:185-190.[Abstract/Free Full Text]
- Hoveland C.S. Legume persistence under grazing in stressful environments of the United States. In: Marten G.C., ed. Persistence of forage legumes. Madison, WI: ASA, 1989:375-383.
- Hoveland C.S., Durham R.G., Bouton J.H. Management effects on productivity of Alfagraze alfalfa–tall fescue mixtures. J. Prod. Agric. 1995;8:244-248.
- Hoveland C.S., Durham R.G., Bouton J.H. Tall fescue response to clipping and competition with no-till seeded alfalfa as affected by fungal endophyte. Agron. J. 1997;89:119-125.[Abstract/Free Full Text]
- Leuchtmann A. Ecological diversity in Neotyphodium-infected grasses as influenced by host and fungus characteristics. In: Bacon C.W., Hill N.S., eds. Neotyphodium/grass interactions. New York: Plenum Press, 1997:93-108.
- Lewis G.C. Effect of ryegrass endophytes in mixed swards of perennial ryegrass and white clover under two levels of irrigation and pesticide treatment. Grass Forage Sci. 1992;47:302-305.
- Marks S., Clay K. Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol. 1996;133:727-733.[Web of Science]
- Marks S., Clay K., Chaplick G.P. Effects of fungal endophytes on interspecific and intraspecific competition in the grasses of Festuca arundinacea and Lolium perenne. J. Appl. Ecol. 1991;28:194-204.
- Prestridge R.A., Thom E.R., Marshall S.L., Taylor M.J., Willoughby B., Wildermoth D.D. Influence of Acremonium lolii infection in perennial ryegrass on germination, emergence, survival, and growth of white clover. N.Z. J. Agric. Res. 1992;35:225-234.
- SAS Institute. 1988. SAS/STAT user's guide. Release 6.03. SAS Inst., Cary, NC.
- Stevens D.R., Hickey M.J. Effects of endophytic ryegrass on white clover. In: Quisenberry S.S., Joost R.E., eds. Proc. Int. Symp. on Acremonium/Grass Interactions, 1st, New Orleans. 5–6 Nov. 1990. Baton Rouge: La. Agric. Exp. Stn, 1990:58-61.
- Sutherland B.L., Hoglund J.H. Effect of ryegrass containing the endophyte (Acremonium lolii) on the performance of associated white clovers and subsequent crops. Proc. N.Z. Grassl. Assoc. 1989;50:265-269.
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ABSTRACT
INTRODUCTION
