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Annals of Botany 81 : 483–488, 1998
Encroachment of Endophyte-infected on Endophyte-free Tall Fescue
N. S. H I L L*†, D. P. B E L E S K Y‡ and W. C. S T R I N G E R§
* Crop and Soil Sciences Department, UniŠersity of Georgia, Athens, GA, USA 30602, ‡ USDA-ARS Appalachian
Soil and Water ConserŠation Lab, Beckley, WV, USA 25802, and § Plant Sciences Department,
Clemson UniŠersity, Clemson, SC, USA 29631
Received : 3 July 1997
Returned for revision : 8 September 1997
Accepted : 4 December 1997
Persistence of endophyte-free (E®) tall fescue (Festuca arundinacea Schreb.) is erratic. Little information exists as to
how fast endophyte (Neotyphodium coenophialum)-infected (E­) tall fescue might encroach on E® tall fescue and
whether specific conditions might influence the speed of encroachment. Plots of E­ and E® tall fescue genotypes
7 and 17 were established using a modified Nelder’s design to compare performance of the E­ forms of the plants
in pure and mixed communities at different population densities. The plots were planted at the USDA Southern
Piedmont Conservation Research Laboratory in Watkinsville, Georgia, and the University of Georgia Plant Sciences
Farm in Bogart, Georgia. Plants were grown over a 5 year period and dry matter yield monitored 1, 3, and 5 years
after establishment. Relative crowding coefficients were calculated for each to establish trends of encroachment of the
E­ on the E® plants in the mixed communities. Generally, dry matter yields of E­ tall fescue were greater than
E® tall fescue regardless of whether they were grown in pure or mixed communities. As time progressed, the
difference in dry matter yield between E­ and E® tall fescue grown in mixed communities was greater than that of
the pure communities. Relative crowding coefficients increased as time progressed. Relative crowding coefficients at
the Watkinsville location were greater after 5 years than those at the Plant Sciences Farm. Therefore, site specific
conditions exist which affect the competitiveness of E® tall fescue and degree of encroachment by E­ tall fescue.
Research is needed to identify which biotic, abiotic and management variables exacerbate encroachment of E­ tall
fescue to better define the conditions which best suit E® tall fescue.
# 1998 Annals of Botany Company
Key words : Tall fescue, endophyte, Neotyphodium coenophialum, Festuca arundinacea, competition, population
density.
INTRODUCTION
One of the better defined mutualistic associations between
an endophytic fungus and its plant host is that between
Neotyphodium coenophialum (formerly called Acremonium
coenophialum) and tall fescue (Festuca arundinacea Schreb.)
(Hill, 1994). N. coenophialum increases root and shoot mass,
tiller number (Belesky, Stringer and Hill, 1989 ; Hill et al.,
1990) and drought resistance (West et al., 1993 ; Hill,
Pachon and Bacon, 1996), and provides chemical resistances
to insects (Clay, Hardy and Hammond, 1985) and nematodes (West and Gwinn, 1993). The collective effect of the
endophyte on physiology and morphology of tall fescue is a
population that is adapted over wide climatological and
geographical regimes (Hill et al., 1990).
Detrimental effects of toxins produced by N. coenophialum
make the use of endophyte-free (E®) tall fescue an attractive
option for livestock producers. However, removal of the
endophyte from the grassland ecosystem risks the loss of tall
fescue stands. Persistence of E® tall fescue is irregular.
Read and Camp (1986) and Bransby et al. (1988) found E®
pastures to be less persistent than endophyte-infected (E­)
pastures, while Hoveland and coworkers found little or no
difference in persistence of E® and E­ pastures or clipped
plots (Hoveland et al., 1983 ; Hoveland, 1994). Others have
found that E® pastures can be infested by E­ seed after
* For correspondence.
0305-7364}98}040483­06 $25.00}0
passing through the digestive tract of the grazing animal
(Shelby and Schmidt, 1991). Once infestation occurs, the
frequency of E­ plants may increase over time (Belesky et
al., 1987 ; Shelby and Dalrymple, 1993). Little information
exists on how often, how fast, or under what conditions E®
stands might convert to E­ once infestation has occurred.
Conceivably, aggressivity of E­ tall fescue on E® stands
could be affected by soil type, local geography and aspect,
soil moisture, nematode or insect populations. Therefore,
studies involving E­ and E® tall fescue are needed to
assess the competitiveness of the two forms.
Previously, we reported on the competitiveness between
E­ and E® forms of two tall fescue genotypes (Hill,
Belesky and Stringer, 1991). The original objective of the
study was to determine whether E­ and E® plant
genotypes varied in their competitive ability. We reported
that competitiveness of E­ and E® plants varied between
genotypes, and that competitiveness appeared to be site
specific during the establishment year. The plots were
subsequently maintained with the objective of evaluating
whether the competitive ability of the E­ and E® plants
remained constant or changed over time, location, or plant
genotype.
MATERIALS AND METHODS
Plant materials were collected from a population of E­
Kentucky 31 growing on the Simpson Experimental Farm in
bo980583
# 1998 Annals of Botany Company
484
Hill et al.—Encroachment of Endophyte-infected on Endophyte-free Tall Fescue
T     1. Mean dry matter yield (g per plant) of endophyte-infected (E­) and non-infected (E®) plants from two tall fescue
genotypes grown at two locations
1988
1992
Genotype
Location
Watkinsville
Infection
status
E­
E®
Mean
LSD (0±05)*
Genotype (G)
Infection (I)
G¬I
7
17
Mean
7
17
Mean
191
149
170
213
200
207
202
175
192
49
126
253
48
151
223
49
—
—
36
—
—
17
1989
1991
1993
Genotype
Plant Sciences
E­
E®
Mean
LSD (0±05)
Genotype (G)
Infection (I)
G¬I
7
17
Mean
7
17
Mean
7
17
Mean
396
277
337
397
309
352
397
292
460
266
363
628
241
435
544
254
175
82
129
194
87
141
185
85
—
—
18
—
—
48
n.s.
18
n.s.
* Least significant difference at the 0±05 level of probability.
Pendleton, South Carolina, USA. Plants were vegetatively
propagated and one half of the individuals from each were
treated to kill the endophyte (Hill et al., 1990). The plants in
this study were at least five vegetative generations beyond
endophyte removal to minimize chances of remnant fungicide effects. Plants were vegetatively propagated and grown
in 7±5¬10 cm plastic cups in the glasshouse prior to
establishment in the field as outlined by Hill et al. (1991).
Plots were established at the USDA Southern Piedmont
Conservation Laboratory in Watkinsville, Georgia, USA
on 4 Oct. 1987. The site was a Cecil sandy clay loam soil. A
second site was established on 4 Oct. 1988 at the University
of Georgia Plant Sciences Farm, located near Bogart
Georgia, USA, approx. 20 km from Watkinsville. The Plant
Sciences Farm site was a Pacolet sandy clay loam soil.
The soils at the two sites differ in that typical Cecil soils
have deeper A horizons (% 36 cm) with a greater water
holding capacity (C 2±2 cm) than the Pacolet series (A
horizon ! 15 cm, water holding capacity C 0±45 cm). Plots
were established in a modified Nelder’s systematic design
for spacing experiments (Nelder, 1962). The plots were in a
wagon wheel arrangement consisting of 16 spokes emanating
from the centre to the edge of the plot. Each wheel was
divided into four sections of four spokes each, and two
sections randomly assigned to pure stands of E­ or E®
plants. The remaining two sections were assigned to a
mixture of E­ and E® plants within and between spokes.
Each wheel was planted with one genotype. Each spoke had
11 plants. The four plants closest to the centre were planted
10 cm apart, the next four distal plants were planted 20 cm
apart, and the outside three plants were planted 40 cm
apart. Plants within spokes that were at the interface of
spacing distances were considered the border of the plot.
Hence planting density treatments were 4±7, 5±7, 13, 16, 21,
66 and 102 plants m−# (see schematic in Hill et al., 1991).
Three replications of each plant genotype were used, for a
total of six wagon wheels. Plots were fertilized with 90, 54
and 81 kg ha−" N, P and K, respectively, immediately after
planting and again in February of the following year. In
subsequent years the plants were fertilized every February
with 100, 59 and 90 kg ha−" N, P and K, respectively.
Plots were harvested for yield determinations at physiological maturity of the seed in early June during years 1, 3
and 5 following establishment. Plots were harvested by
hand-clipping the forage to a height of 7±5 cm. In alternate
years plots were mowed at late anthesis with a rotary mower
and the forage removed immediately after harvest. Except
for year 1, plots were mowed in February to remove residue
from the previous year. Harvested tissue was oven-dried at
65 °C for approx. 7 d. Relative crowding coefficients (RCC)
were calculated for all population densities within each year
to determine the competitiveness of the endophytic forms of
each genotype using eqn (1) (Harper, 1977) :
RCC ¯
DMYEIM}DMYNIM
DMYEIP}DMYNIP
(1)
where DMYEIM and DMYNIM are the dry matter yields
of E­ and E® plants, respectively, in mixed stands, and
DMYEIP and DMYNIP are the dry matter yields of E­
and E® plants, respectively, in pure stands.
Treatment variables were assigned to a split-strip plot
Hill et al.—Encroachment of Endophyte-infected on Endophyte-free Tall Fescue
design repeated over time (years), with genotype as the
whole plot, a complete factorial of stand type (mixed Šs.
pure) and endophyte infection status as the split, and
population density as the strip within each genotype. Since
locations were established in different years, data were
analysed within each location. Genotypes, infection status,
stand type and population density were considered fixed
effects, and years a random effect since environmental
conditions varied over years. The statistical model was
tested with the SAS general linear models program (SAS
Institute, Cary, NC).
Essentially all interactions between years and other
treatment variables were significant, so the data were reanalysed within years and locations using a split-strip-plot
model with genotype as the whole plot, a complete factorial
between infection status and stand as the split, and
population density as the strip within each genotype. The
PROC REG procedure of SAS (SAS Institute, Cary, NC)
was used to define relationships between dry matter yield or
RCCs (dependent variables) and population density. Linear,
quadratic and cubic regression models were tested and the
equation with significance (P % 0±05) of the highest order
regression coefficient (cubic " quadratic " linear) selected
to define the relationship between population density and
the dependent variables.
RESULTS
Plants grown at the two highest population densities could
not be distinguished from one another after the initial year
of growth. Therefore, data from the two highest population
485
1000
E+
1988
Watkinsville
E–
800
600
2
y = 452 – 40.64x + 1.18x
R2 = 0.96
Dry matter yield (g)
400
y = 394 – 35.41x + 1.00x2
R2 = 0.96
200
0
1992
Watkinsville
800
600
y = 479 – 35.78x + 1.09x
R2 = 0.99
2
400
y = 112 – 5.83x
R2 = 0.90
200
0
6
9
12
15
18
Plant density (plants m–2)
21
F. 1. Mean dry matter yield of endophyte-infected (E­) and
endophyte-free (E®) forms of two tall fescue genotypes at five different
population densities grown at Watkinsville, GA in 1988 and 1992.
T     2. Mean dry matter yield (g per plant) of endophyte-infected (E­) and non-infected (E®) tall fescue plants grown
in mixed or pure stands grown at two locations
1988
1992
Infection status
Location
Watkinsville
Stand type
Mixture
Pure
Mean
LSD (0±05)*
Stand type (S)
Infection (I)
S¬I
E­
E®
Mean
E­
E®
Mean
210
193
202
184
164
174
197
179
256
189
126
30
67
151
143
128
n.s.
22
n.s.
1989
—
—
17
1991
1993
Infection status
Plant Sciences
Mixture
Pure
Mean
LSD (0±05)
Stand type (S)
Infection (I)
S¬I
E­
E®
Mean
E­
E®
Mean
E­
E®
Mean
416
378
397
278
306
292
347
342
586
501
544
159
349
254
373
425
222
147
185
54
115
85
138
131
—
—
17
* Least significant difference at the 0±05 level of probability.
—
—
48
—
—
26
486
Hill et al.—Encroachment of Endophyte-infected on Endophyte-free Tall Fescue
1000
10
E+
800
E–
1989
Plant Sciences Farm
8
y = 874 – 68.49x + 1.65x2
R2 = 0.98
400
200
y = 581 – 23.7x
2
R = 0.94
Dry matter yield (g)
0
1991
Plant Sciences Farm
800
y = 1296 – 118.5x + 3.31x2
R2 = 0.97
600
400
200
40
200
6
y = 1.29 – 0.029x
R2 = 0.77
1992
Watkinsville
30
y = –13.35 + 2.635x
2
R = 0.97
y = 1.32 + 0.816x
2
R = 0.75
6
9
12
15
18
Plant density (plants m–2)
21
F. 3. Relative crowding coefficients of tall fescue genotypes 7 and 17
at five different population densities grown at Watkinsville, GA in 1988
and 1992.
600
0
0
0
1993
Plant Sciences Farm
y = 175 – 7.46x
2
R = 0.80
mean = 2.03
2
10
0
400
4
20
y = 498 – 22.6x
2
R = 0.93
800
Genotype 7 Genotype 17
6
Relative crowding coeffieient
600
1988
Watkinsville
y = 373 – 30.1x + 0.91x2
R2 = 0.97
9
12
15
18
–2
Plant density (plants m )
21
24
F. 2. Mean dry matter yield of endophyte-infected (E­) and
endophyte-free (E®) forms of two tall fescue genotypes at five different
population densities grown at the Plant Sciences Farm near Bogart
Georgia in 1989, 1991 and 1993.
densities were omitted during all years. In 1990, approximately one third of the samples collected at Watkinsville
were destroyed due to power failure during drying and,
therefore, no 1990 data will be presented for that location.
Dry matter yields varied from year to year, depending
largely upon spring rainfall. Growing conditions were
uncommonly dry in 1992 and 1993, with pan evaporation
exceeding precipitation after 1 April each year (Hill, Cabrera
and Agee, 1995). There were significant genotype¬
endophyte infection¬stand type¬population density¬
year interactions for dry matter yield at both the
Watkinsville and Plant Sciences Farm locations. To aid
interpretation of the five-way interaction, means of the
genotype¬infection status, stand type¬infection status,
and population density¬infection status interactions were
compared within years for each location.
Endophyte-infected (E­) genotype 7 had a greater dry
matter yield than the E® form, but the E­ and E®
genotype 17 did not differ from one another when averaged
across population densities and stand type at the
Watkinsville location in 1988 (Table 1). The E­ forms of
both tall fescue genotypes had a greater dry matter yield
than the E® forms when averaged across population
densities and stand type at the Watkinsville location in
1992. The E­ form of tall fescue genotype 17 had a greater
dry matter yield than E­ genotype 7, but dry matter yields
did not differ between the E® genotypes at the Watkinsville
location in 1992.
Dry matter yield of the E­ forms for both genotypes
were greater than the E® forms at the Plant Sciences Farm
in 1989. Dry matter yield of E® genotype 7 was less than
E® genotype 17 in that year. Dry matter yield of the E­
forms of the genotypes were greater than the E® forms at
the Plant Sciences Farm, and E­ genotype 17 was greater
than E­ genotype 7 in both 1991 and 1993. Dry matter
yield of the E® forms of the plant genotypes did not differ
from one another in either 1991 or 1993 at the Plant
Sciences Farm.
There was no difference in dry matter yield of E­ plants
when grown in mixtures with E® plants compared to pure
stands at Watkinsville in 1988 (Table 2). By 1992, E­
plants grown in mixtures had a greater dry matter yield than
E® plants grown in pure stands at Watkinsville. The E®
plants grown in pure stands had a greater yield than E®
plants grown in mixtures with E­ plants in 1992 at
Watkinsville. The E­ plants had a greater dry matter yield
when grown in mixtures with E® plants than when grown
in pure stands at the Plant Sciences Farm, regardless of
year. The E® plants had a greater dry matter yield when
grown in pure stands than when grown in mixtures with E­
plants at the Plant Sciences Farm, regardless of year.
Quadratic equations gave best fits when dry matter yield
was regressed with population density of E­ plants at both
locations (Figs 1 and 2). Linear equations gave best fits
Hill et al.—Encroachment of Endophyte-infected on Endophyte-free Tall Fescue
6
Two important trends occurred among the RCCs. First,
RCCs increased with time, especially at the Watkinsville
location and secondly, RCCs were greater for genotype 7 at
the Watkinsville location, but tended to be greater for
genotype 17 at the Plant Sciences Farm.
4
DISCUSSION
10
1989
Plant Sciences Farm
Genotype 7 Genotype 17
8
mean = 1.80
2
mean = 1.75
Relative crowding coefficient
487
0
1991
Plant Sciences Farm
8
6
4
mean = 3.61
2
y = 1.94 – 0.047x
R2 = 0.66
0
8
1993
Plant Sciences Farm
6
mean = 4.45
4
y = 2.09 – 0.119x
R2 = 0.64
2
0
6
9
12
15
18
Plant density (plants m–2)
21
F. 4. Relative crowding coefficients of tall fescue genotypes 7 and 17
at five different population densities grown at the Plant Sciences Farm
near Bogart Georgia in 1989, 1991 and 1993.
when dry matter yield was regressed with population density
of E® plants with the exception of those grown at
Watkinsville in 1988. Generally, dry matter yield of E­
plants was greater than E® plants regardless of population
density, year, or location, but yields were most similar
between E­ and E® plants during 1988 at Watkinsville
and 1989 at the Plant Sciences Farm, the years the plots
were established. Dry matter yield of E­ and E® tall
fescue genotypes was also most similar at the higher
population densities in all years when averaged over mixed
and pure stands.
Relative crowding coefficients were similar among all
population densities for genotype 7 at the Watkinsville
location in 1988, but genotype 17 showed a slight decrease
in RCC as population density increased (Fig. 3). Both
genotypes had linear increases in RCCs as population
density increased at Watkinsville in 1992. Relative crowding
coefficients did not differ within years and among population
densities for genotype 17 at the Plant Sciences Farm
location (Fig. 4). Relative crowding coefficients were similar
for all population densities for genotype 7 during 1989, but
showed a linear increase as population density increased in
1991 and 1993.
Since rainfall varied between years, it is difficult to interpret
a trend for the performance of E­ and E® during the
course of the experiment based upon dry matter yields.
Weights of E­ and E® tall fescue were most similar during
the establishment years, but as time progressed E­ plants
grown in mixtures had a greater mass than those grown in
pure stands. Also, E® plants grown in mixtures had a
smaller mass than those grown in pure stands as time
progressed. These data suggest that E­ plants encroached
upon E® plants (Table 2). However, interpretation of these
data is confounded since E® plants had a smaller mass than
E­ plants when grown in pure stands as well. Similarly, it
is difficult to interpret the competitiveness of the E­ and
E® forms for each genotype using dry matter yield data.
There was a genotype¬infection status interaction at the
Watkinsville location in 1988 and 1992. The mass of tall
fescue genotype 17 was similar regardless of endophyte
status in 1988 and E® genotype 17 had approx. 20 % of the
mass of the E­ form in 1992 (Table 1). There were
genotype¬infection status interactions for dry matter yield
for plants grown at the Plant Sciences Farm in 1989 and
1991, but the endophyte effect was significant only in 1993.
Consequently, comparisons of how E­ and E® plants
performed in mixtures relative to performance in pure
stands were necessary to properly interpret the data (Hill et
al., 1991).
Relative crowding coefficients compare the performance
of E­ and E® plants on a relative basis in mixed Šs. pure
stands at each population density (Harper, 1977 ; Hill et al.,
1991). An RCC " 1 indicates the E­ form was more
competitive and encroached on the E® form, while the
reverse is true if the RCC is ! 1. By definition, E­ tall
fescue genotypes were increasingly aggressive to the E®
form as the RCCs increased above 1.
Relative crowding coefficients were generally between 1
and 2 for genotype 7 but were 1 or less for genotype 17 in
1988 at the Watkinsville location (Fig. 3). Relative crowding
coefficients tended to be lower at the higher population
density, suggesting that E® genotype 17 encroached upon
the E­ form. Conversely, the data suggested that the E­
form of genotype 7 encroached on the E® form in 1988.
Relative crowding coefficients in 1992 suggested that the
E­ forms of both genotypes were encroaching on the E®
forms at the Watkinsville location, and that encroachment
was more pronounced at higher population densities.
Relative crowding coefficients were " 1 for both genotypes
at the Plant Sciences Farm in all years tested (Fig. 4),
indicating that E­ plants were encroaching on E® plants.
Trends in relative crowding coefficients were similar at
both locations in that they increased numerically over years.
Increases in relative crowding coefficients at the Plant
Sciences Farm were more subtle than at the Watkinsville
488
Hill et al.—Encroachment of Endophyte-infected on Endophyte-free Tall Fescue
location, but the genotypic ranking of relative crowding
coefficients changed among locations. These observations
suggest that encroachment of E­ tall fescue on the E®
forms is site and genotype specific. It is not surprising that
different genotypes perform differently at the two locations
depending upon infection status. The combination of plant
genotype and endophyte genotype seemingly increases
phenotypic variation in tall fescue plants (Hill et al., 1991).
Hence, the interaction of the two symbionts increases
plasticity in a tall fescue population (Schmid, 1985 ; Hill et
al., 1991), giving tall fescue its broad geographic adaptation.
The A horizon of the Cecil soil at Watkinsville was deeper
with a higher water holding capacity than the A horizon of
the Pacolet at the Plant Sciences Farm, suggesting that
Watkinsville would be a more hospitable site for the more
drought susceptible E® tall fescue. Indeed, the relative
crowding coefficients were approx. 1 or lower during the
establishment year suggesting Watkinsville was a more
hospitable site (Fig. 3). However, high RCCs 5 years after
establishment at the Watkinsville location make it clear that
this site was especially susceptible to encroachment by E­
tall fescue. This phenomenon demonstrates that a more
systematic ecological approach towards testing fitness of
E­ or E® tall fescue is needed to establish benchmarks for
recommendations concerning utilization of each.
Identification of abiotic variables (such as soil type,
climatic and fertility variables), biotic variables (such as
insect or disease pressures), and intensity, duration and type
of defoliation, are likely to lead to a better understanding of
the role each plays in encroachment of E­ on E® tall
fescue. There is an abundance of data in which each has
been observed as a component ; however, the interactions of
each need to be addressed in systems studies to establish
whether synergistic or antagonistic interactions exist among
those variables relative to the performance of E® tall
fescue. Such data could be useful when making recommendations concerning utilization of E­ or E® tall
fescue, and prescribe management variables to reduce the
probability of E­ encroachment.
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