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International Association for Ecology
Effects of Fungal Endophytes on the Seed and Seedling Biology of Lolium perenne and
Festuca arundinacea
Author(s): K. Clay
Source:
Oecologia,
Vol. 73, No. 3 (1987), pp. 358-362
Published by: Springer in cooperation with International Association for Ecology
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Oecologia
(Berlin)
(1987)
73:358-362
C
O7g1
C
Springer-Verlag
1987
Effects
of
fungal
endophytes
on
the
seed
and
seedling
biology
of
Lolium
perenne
and
Festuca
arundinacea
K.
Clay
Department of
Biology,
Indiana
University,
Bloomington,
IN
47405,
USA
Summary.
Many grasses
are
infected
by endophytic
fungi
that
grow
intercellularly
in
leaves, stems, and flowers
and
are transmitted
maternally by
hyphal growth into
ovules
and seeds.
The seed biology and
seedling growth of
endo-
phyte-infected and uninfected
perennial ryegrass
(Lolium
perenne)
and tall fescue (Festuca
arundinacea) were
investi-
gated
under controlled
environmental
conditions.
The
per-
centage
of
filled seeds produced
by infected tall fescue
was
over
twice
of uninfected tall
fescue; infected and
uninfected
perennial
ryegrass
had similar
percentages. Weights
of seeds
from
infected and uninfected
plants were similar in
both
species.
Seeds
from
infected
plants
of both
species
exhibited
a
higher rate of
germination
than seeds
from
uninfected
plants. Shoot
growth
in
the
greenhouse was
compared by
making three
sequential harvests
of
above-ground
plant
parts
from infected
and
uninfected
plants
of both
species.
Infected
perennial ryegrass
plants produced
significantly
more biomass
and tillers than
uninfected plants after 6
and
10 weeks of
growth
and
significantly
more
biomass
after
14
weeks of
growth. Infected
tall
fescue plants
produced
significantly
more biomass
and
tillers than
uninfected plants
after
10 and
14
weeks
of growth.
The
physiological
mecha-
nism of
enhancement of growth
is
not known. The
results
of this
study suggest
that
infected
plants may
have a
selec-
tive
advantage
in
populations
with
uninfected
members.
Key
words:
Lolium
perenne
-
Festuca
arundinacea
-
Leaf
endophytes
-
Seed
endophytes
-
Germination
-
Growth
A
common
theme in the
evolution of higher plants
has
been the
formation
of
symbiotic
associations
with
hetero-
trophic
microorganisms.
Plants infected
by
nitrogen-fixing
bacteria
or
mycorrhizal fungi
frequently
exhibit
increased
ability
to
acquire limiting
nutrients or
tolerate
physical
stresses (Lewis
1973). These
associations
arose
long
ago
and
are
essentially obligate
in
many plant groups, preclud-
ing experimental
attempts
to
quantify
the
ecological
advan-
tages
and
disadvantages
of
symbiosis.
The
ecological
ad-
vantages
of
symbiosis
between
plants
and
microorganisms
are best
studied
when the interaction
is
facultative and
exists
as a
polymorphism
in
host
plant
populations.
Many grasses
are
infected
by
clavicipitaceous fungi
that
occur
perennially
as
intercellular
endophytes (Clay
1986a).
While some
grass species appear
to be
ubiquitously
infected,
others are
not known
to
serve
as
hosts; many
other
species
fall between
these extremes
(Diehl 1950; Clay
1984, 1986a;
White
and Cole 1985,
1986). The widespread
grasses Lolium
perenne
(perennial
ryegrass) and
Festuca
arundinacea (tall
fescue)
often
are infected
by the imperfect
fungi Acremon-
ium
loliae and A.
coenophialum, respectively
(Morgan-Jones
and
Gams 1982; Latch et
al. 1984). These
fungi closely re-
semble
the asexual
(anamorphic) state of
Epichloe typhina
(Ascomycetes,
Clavicipitaceae) and probably
are derived
from
it (Sampson 1933;
Bacon et al. 1977;
White 1987).
Epichloe and closely
allied genera in the
tribe Balansiae
are related
to
the genus
Claviceps (Diehl 1950).
While Clavi-
ceps
species are transient
and localized
ovarian parasites
of
grasses and sedges, the
Balansiae fungi are
systemic and
perennial. Intercellular
hyphae of
A. loliae
and
A.
coeno-
phialum
can
be
observed
in
the meristematic
region,
in
the
mesophyll
of
leaves, in
the pith of flowering
culms, and
in
the
scutellum and
aleuron layer of seeds
(Neill 1940,
1941;
Bacon
et al.
1977;
Clark
et
al.
1983).
Fungal hyphae
do
not
occur
intracellularly or within roots.
The
endophytes of
perennial ryegrass and
tall
fescue
do
not
produce spores
in
their
hosts
(although they
can
in
pure culture) and do
not spread
contagiously; instead,
they
are
transmitted
from maternal
plant
to
progeny by
vegetative
growth of hyphae
into
the
developing ovule
or
seed
(Sampson 1933;
Neill
1941;
Bacon etal.
1977; Clay
1986a).
Therefore,
the
persistence
of the infection
in
natural
populations
depends upon
the effect
of the
fungi
on
the
survival, growth,
and
reproduction (i.e.,
fitness)
of their
hosts,
compared
to
uninfected
plants.
Previous
research
has
shown that
infected
plants
of
perennial ryegrass
and
tall
fescue exhibit
greater
resistance
to
some
insect
herbivores
and
greater
vigor
in
pastures
compare
to
uninfected
plants
(Bradshaw 1959; Funk et al.
1983; Clay
1986a; Clay
et
al.
1985).
Here
I
compare
the seed
and
seedling biology
of
infected and uninfected
plants of perennial
ryegrass and
tall
fescue
as an initial
step
in
estimating
the
effect
of
endo-
phyte-infection
on host
plant fitness.
Experiments
were
con-
ducted in a
controlled environment without
herbivores
to
distinguish
direct effects
of
endophyte-infection
on
shoot
growth
from
indirect
effects on
growth
due
to differential
herbivory.
Materials and
methods
Seeds of
perennial ryegrass
(Lolium perenne
L.)
were
ob-
tained from a
commercial
seed
company (Loft's
Seed
Co.,
Bound
Brook,
NJ, USA).
Seeds of the cultivar
"Repell"
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359
have a
high
frequency
of infection
by
the
endophyte
Acre-
monium
loliae
Latch,
Christensen & Samuels while
seeds
of the cultivar "Yorktown"
have a low
frequency
of
infec-
tion.
I
determined the
frequency
of infected
plants by
micro-
scopically
examining
leaf sheaths of 25
plants
raised
from
seed for each
cultivar. The two cultivars are advanced
gen-
eration
selections from the same
parental
stock and
are
genetically
similar
(pers.
comm.,
R.
Hurley,
Loft's
Seed
Co.).
Seeds
of tall fescue
(Festuca
arundinacea
Schreb.)
were
bulk collected from
a
stand
containing
a
high
frequency
of infected
plants
and
from
a stand
containing
a low fre-
quency
of infected
plants
located
in
a
garden
on the Lou-
isiana State
University
campus (Baton
Rouge, LA,
USA).
The stands
of tall
fescue were
originally planted
with
lots
of seeds of cultivar
"
KY-31"
differing
in
infection level
of Acremonium
coenophialum
Morgan-Jones
and
Gams
(provided by
Dr.
Malcolm
Siegel,
University
of
Kentucky).
To confirm levels of infection I examined leaf
sheaths of
25 plants
raised from
seed collected from each stand.
Abundant hyphae of
A.
loliae were observed in the leaf
sheaths of 23 of 25
(92%)
Repell perennial
ryegrass
plants;
no
hyphae
were
observed
in
the leaf sheaths of Yorktown
perennial
ryegrass plants. The leaf sheaths of all 25 tall
fescue
plants
collected as seed from the infected stand
con-
tained
hyphae
of A.
coenophialum;
3 of
25
(12%)
plants
collected as seed from the
uninfected stand were found to
contain
hyphae
in
the
leaf sheaths. Hereafter
I
refer
to the
seeds and
plants
originating
from the different
seed lots
as either infected or
uninfected,
recognizing
that low levels
of contamination
may
be
present.
Individual seeds
and
plants
used in
experiments were not examined for
infection
but were
presumed to resemble the
frequencies
found in
the above
subsamples.
Statistical tests
comparing
infected
and uninfected
plants
are therefore
conservative.
The
percentage of filled
seeds was
estimated by
taking
a random
sample
of 200
from
each of the four
catagories:
infected
and
uninfected
perennial
ryegrass,
and
infected and
uninfected tall fescue. Each seed was
pressed
individually
on a
glass
plate
with the
fingertip
to detect a
caryopsis
within the
lemma
and
palea.
A
sample
of
approximately
100 filled seeds
(caryopsis, lemma,
and
palea)
in
each cate-
gory
were
weighed
individually
on
an electronic balance
to the nearest 0.01
mg.
Germination
was
compared by
planting 100
seeds of
infected
ryegrass (ten seeds each in ten
pots) and
100 seeds
of
uninfected
ryegrass.
Each 10
cm2
pot was
filled with
a
soil mixture
(one part
sterile
potting
soil,
one
part
peat,
one
part
perlite,
one
part
sand).
The
pots
were
placed
in
an environmental
growth
chamber
with a diurnal
light/tem-
peratue cycle
(14
h
light/24
C,
10
h
dark/20 C)
and
the soil
was
kept
constantly
moist.
Emergent
seedlings
were
counted
every day
until
new
seedlings
ceased to
appear.
Germination tests of tall fescue
were conducted in a similar
manner
except
there were 250 seeds each
from
infected and
uninfected
plants (25 per
pot).
The
higher sample
size
was
used because it
was felt that
germination levels
might
be
lower than in commercial
cultivars of
perennial
ryegrass.
Growth
comparisons
were made
using seedlings from
seeds
germinated
in
plastic
trays.
Individual
seedlings
were
washed
free of
soil,
blotted
dry,
and
weighed
for
subsequent
use as a covariate
in
statistical
analyses. Each
seedling was
planted in sterile
soil into individual
cavities of
"Speedling
Trays"
(Speedling, Inc., Sun City,
FL, USA),
styrofoam
trays with
72 inverted
pyramidal cavities 5 cm2 at
the
open-
ing,
7.5 cm
deep, and
approximately 62 cm3
in
volume.
Each
tray
was divided
into two blocks of 36 cavities
each
and
either
seedlings
from
infected or uninfected seeds were
planted in
each
block. A
total
of
eight blocks were
planted
with
infected
seedlings
and
eight
with
uninfected
seedlings,
for each
grass
species.
The
trays
were
randomly
arranged
on benches in the
greenhouse
and rotated
biweekly.
All
plants
were
watered
daily
and fertilized
weekly
with a
dilute
liquid
fertilizer
(Peters
20-20-20,
1
g
per
1);
insecticidal
soap
(Safer,
10
ml
per
l) was
sprayed
on all
plants
biweekly
to
prevent
colonization
by
aphids. Dead
plants
were
not re-
placed.
Two
blocks
of infected
plants
and
two of infected
plants, for
both
species,
were
harvested after six weeks
by
clipping
at the soil
surface. The number of
tillers were
counted
and
dried at 80 C for
48
h
and then
weighed.
An-
other harvest was
conducted at 10 weeks
by
sampling
two
additional
blocks from each
category
in the same manner.
The
remaining four
blocks
in
each
category
were
harvested
at
14
weeks.
Non-parametric
chi-square
tests were utilized to
com-
pare
the
percentages
of
filled seeds and
germination
of in-
fected
and
uninfected seeds
of
each
species
(Siegel
1956).
One-way
analysis of
variance
was used
to
compare seed
weights
and
analysis
of
covariance was
used
to
compare
tiller numbers
and
weights
of
harvested
plants, between in-
fected and
uninfected
plants of the same
species.
Infection
status of
the
plants
was
considered a fixed
main
effect while
original
seedling
weight
was considered as
a
covariate. Un-
transformed and
log-transformed
weights and
tiller
numbers were
analyzed,
and
because
tranformation of
de-
pendent
variables did not
increase
the amount of
variation
explained
by
the
model
(and in
some
cases
decreased
it),
only
the results from
untransformed
variables
are
presented
here.
Results
Seeds from
infected
and
uninfected
perennial
ryegrass
were
similar
with
respect
to the
percentage
of filled
seeds
and
seed
weight
(Table
1).
In
contrast,
the
percentage
of
filled
tall
fescue seeds
from
infected
plants
was
over
twice
that
from uninfected
plants, a
highly
significant
difference (X2
=
20.8,
P<0.0005).
However,
the
weights
of
filled
seeds
were
equal
(Table
1).
The
germination
of
seeds
of
both
species
followed a
similar course.
There
was a
flush
of
germination
over a
Table 1.
Percentage
seed set
(sample of
200) and
seed weights
(mg)
of infected and uninfected
perennial
ryegrass
and tall fescue.
Aster-
isk
indicates
a
significant
difference
(P<0.05)
based on
a chi-
square
test.
Mean seed
weights+
one
standard error are
presented
(sample sizes in
parentheses)
Species
Type
%
Filled Seeds Mean Seed
Weight
Perennial
Infected 88% 1.90 + 0.05
Ryegrass
(98)
Uninfected
90%
1.86 +
0.05
(102)
Tall
Fescue
Infected
44%*
2.13 +0.05
(98)
Uninfected
19%
2.13
+0.06
(102)
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360
100
N
0
|.
-
TALL
FESCUE
N
80
-
zcI
60
*~~~~
PERENNIAL
RYEGRASS
6 0
-
w
40
z
w
0
2
4
6 8
10
22
DAYS SINCE
SOWING
Fig.
1. Percent
germination of
endophyte-infected (I) and unin-
fected
NI
seeds of
perennial ryegrass
and
tall
fescue
three or four
day period
after which few additional
seeds
germinated
(Fig. 1). For
both species
there was a
consistent
trend
for seeds from infected
plants,
which themselves were
endophyte-infected,
to
germinate
at a
higher frequency
at
each sample
point and
in total. Approximately
10%
more
infected seeds
than uninfected
seeds
germinated
for both
perennial
ryegrass
and tall fescue
(Fig.
1).
Given the
sample
size,
a
chi-square
test for
differences
in total seed
germina-
tion was not significant
for eight species.
However,
infected
seeds of both species
had higher germination
than
unin-
fected
seeds at each of five
sample
dates (P<0.05,
sign
test).
For both species,
the number of
tillers and above-
ground biomass
produced by infected and
uninfected indi-
viduals
grown
in
the
greenhouse
differed significantly in
most
cases (Table 2). In
perennial ryegrass
there was a trend
for the
differences in
tiller number and
dry weight to be
greatest earlier and
decrease later. This
trend was paralleled
by
the
decreasing effect
over time of the
covariate (seedling
weight) and the amount
of variation
explained by the AN-
COVA model
(Table 2).
In
contrast,
infected and unin-
fected
plants
of tall fescue
exhibited no
significant differ-
ences at the first harvest
but
highly
significant differences
in tiller number and
dry weight at the second and final
harvests.
These results
were paralleled
by
an increase in
the
amount of variation
explained by
the ANCOVA
model
over time
(Table 2).
The
covariate
was
significant only once
for
dry weight
at
week
10.
Tiller numbers of
infected perennial
ryegrass were 50%
higher
than those of uninfected
perennial
ryegrass
at week
6 and
10
but were
slightly
lower at week
14
(Table 3).
Above-ground
biomass was
significantly
higher
for infected
perennial
ryegrass plants
at all
three harvest
dates;
the
great-
est
proportional
difference in
dry weight
occurred at week
6. While
dry weights
of both infected and uninfected
peren-
nial
ryegrass increased
from week 6 to
14,
tiller numbers
of infected
perennial
ryegrass
first increased then
declined;
tiller numbers of uninfected
perennial
ryegrass
increased
from
week 6 to
14
(Table
3).
Tiller numbers of infected and uninfected tall
fescue
were identical
at week
6,
but infected
plants
had
produced
18%
and 42%
more tillers than uninfected
plants
at week
Table 2. Summary
of analysis
of covariance.
Tiller
number (TL)
and dry weight
(DW) were
analyzed separately
for each species
and
harvest date.
The infection
status of
the plant was
analyzed as
a fixed main
effect and initial
seedling
weight was analyzed
as a
covariate.
Transforming
the data did
not increase
the explained
variance so only
the results
of untransformed data are
presented.
One, two,
and three asterisks
signify P<0.05,
0.005,
and
0.0005,
respectively
Perennial
Ryegrass
Tall Fescue
Week
6
Week 10
Week 14
Week 6
Week 10
Week
14
DF TL
DW
TL DW
TL
DW
TL DW
TL DW
TL
DW
Model
2 **
*
*
**
NS
*
NS NS
* ** ***
***
Inf 1 *
*
*
NS
*
NS NS
* * ***
***
Cov
I
**
*
NS * NS
*
NS NS NS
*
NS
NS
R
2
0.32 0.49 0.32 0.10
0.01
0.08 0.04 0.00
0.05 0.14
0.22
0.45
Table 3. Numbers of tillers
and above-ground
biomass of infected and uninfected perennial
ryegrass
and tall fescue raised
in the greenhouse.
Means
+
one
standard error
are presented
(sample sizes
in
parentheses).
Weights are
in
milligrams
Week
6
Week 10
Week
14
Tillers
Dry
Weight
Tillers
Dry Weight
Tillers
Dry
Weight
Perennial Ryegrass
Infected
14.5+0.6
502.9
+
19.8 19.1 +0.7
544.9+19.2 16.7+0.5
710.3+
19.5
(58)
(59)
(111)
Uninfected
9.6
+
0.5
291.0 + 16.0 12.3
+
0.6
478.8 + 23.8 17.6
+ 0.9 607.5
+
23.6
(50)
(56)
(96)
Tall Fescue
Infected
4.6+ 0.2
700.0+30.8
4.7+0.3
1066.7+ 55.8
5.1 +0.2 1547.2+ 33.5
(49)
(46)
(94)
Uninfected
4.6+0.2
786.0
+
29.2
4.0 +0.2 862.4+48.3
3.6+0.1
979.8 + 33.0
(50)
(37)
(89)
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361
10
and
14,
respectively
(Table
3).
Above-ground
biomass
of
infected
plants was lower than
that of
uninfected
plants
at
the
first harvest but was
24%
greater
at
week 10
and
58%
greater at
week 14.
As
in
perennial
ryegrass,
dry
weight
increased
from week
6 to
14 for
both
infected
and
uninfected tall
fescue.
Tiller
numbers of
infected tall
fescue
increased from
week
6 to
14
but
declined
in
uninfected
tall fescue over
the
same
period.
Discussion
The
results of
this
and
other
studies
generally
support
the
idea
that the
relationship
between
tall
fescue
and
perennial
ryegrass
and
their
endophytes
is
mutualistic.
Increased
sur-
vival
and
growth of
other
grasses
and
sedges
infected
by
related
fungi has been
reported
previously
(Bradshaw
1959;
Clay
1984,
1986b;
Antonovics et al.
1987;
Stovall
and
Clay
unpublished
work). The
experimental
technique
of
compar-
ing
identical or
closely
related
host
genotypes
with
and
without
the
endophyte
allows a
direct
assesment
of
the ef-
fect of
the
fungus
on
its
host.
Latch
et
al.
(1985)
compared
the
growth of
infected and
uninfected
clones
of
perennial
ryegrass
(cultivar
"Grasslands
Ruanui
").
Endophyte-in-
fected
clones
produced 38%
more
biomass than
uninfected
clones
after
eight
weeks in a
controlled-environment
room,
a
significant
difference.
Gaynor
and
Hunt
(1983)
and
Mor-
timer
and
di
Menna
(1983)
reported
increased
forage
yields
of
endophyte-infected
perennial
ryegrass
pastures
but it is
not
clear
whether
the
differences
resulted
from
increased
growth
or
decreased
herbivory
of
infected
plants.
However,
Neill
(1941,
1952)
observed
no
differences
between
infected
and
uninfected
ryegrass.
Read
and
Camp
(1986)
have re-
cently
reported
that
infected tall
fescue
pastures
yielded
more
forage
than
uninfected
pastures in
the
absence
of
graz-
ing
and
exhibited
greater
persistence
under
drought
condi-
tions.
In
constrast,
Siegel
et al.
(1984)
observed
no
differ-
ences in
forage
production
between
infected and
uninfected
tall
fescue.
Differences
reported
here in
seed
set
(in
tall
fescue)
and
germination
have not
been
noted
previously.
The
increased
vigor
of
infected
plants
also
appears
to
be
expressed
during
flowering
and
seed set
of
maternal
plants
and
during
seed
germination.
One
possible
basis for
greater
growth
of
infected
plants
in
nature
is
their
increased
resistance
to
herbivory.
Several
studies
have
demonstrated
that
endophyte-infected
grasses
are
discriminated
against
by
herbivorous
insects
and
if
they
are
consumed,
insects
suffer
reduced
survival
and
growth
compared
to
those
reared
on
uninfected
conspecifics
(Funk
et al.
1983;
Clay
et
al.
1985;
Johnson
et
al.
1985; Stewart
1985).
The
results
of
this
study
and
those of
Latch
et
al.
(1985)
cannot
be
ascribed to
differential
herbivory
because
plants
were
grown
in
herbivore-free
environments; the
fungi
appear
to
enhance
growth of
their
hosts
directly.
The
physiological basis
for the
increased
growth
of
en-
dophyte-infected
perennial
ryegrass and
tall
fescue is
un-
known.
Porter
et al.
(1985)
have
recently
demonstrated
that
Balansia
epichloe
produces
auxin
in
vitro.
The
sedge
Cyper-
us
virens often
produces
viviparous
plantlets
when
infected
by
B.
cyperi,
a
phenomenon
often
associated
with
hormonal
imbalances
(Clay
1986b).
The
concentration
of
fungal hy-
phae
around
meristematic
regions
of
their
hosts
might
facil-
itate
hormonal
regulation
of
cell
division
and
differentia-
tion.
Possible
hormonal
differences
between
infected
and
uninfected
perennial
ryegrass
and tall fescue
should be
in-
vestigated
in
relation to
their
observed
growth
differences.
Endophyte
infection
has
obvious
implications
for
the
ecology
of
host
populations
and
grassland communities.
While this
study
was
conducted
in
an
artificial
environment
and
over
a short
time
span,
the
results
suggest
infected
plants
may
possess
advantages
over
uninfected
plants
in
seed
set,
germination,
and
seedling
growth. Insect
herbivory
was
shown
to
significantly decrease
the
survival of
unin-
fected
perennial
ryegrass
seedlings
compared
to
infected
seedlings,
which
suffered
little
herbivory
(Stewart
1985).
Differences
in
plant
growth
and size
are
frequently
corre-
lated
with
fecundity
differences
(Harper
1977).
Infected
plants
may
also
exhibit
greater
interspecific
competitive
ability,
as shown
in
the
grass
Danthonia
spicata
infected
by
a
related
Balansiae
fungus
(Kelley
and
Clay
1987).
In
many
areas
endophyte-infected
perennial
ryegrass
and
tall
fescue
plants
comprise
the
majority
of the
popula-
tion
(Neill
1940;
Funk et
al.
1983;
Rycyk
and
Sharpe
1984;
Siegel
et al.
1985).
Recent
studies have
revealed the
presence
of
endophytic
fungi
resembling
those
of
perennial
ryegrass
and tall
fescue in
many
additional
grasses
(White
and
Cole
1985;
White
1987;
Latch
1987).
Thus,
the
symbiotic
associ-
ation
between
grasses
and
fungal
endophytes
appears to
be
widespread. Because
these
fungi
are
not
known to
spread
contagiously
from
infected to
uninfected
plants,
alternative
hypotheses
explaining
the
high
frequency
of
infected
plants
are
required.
The
results
of
this
study
suggest
that
endo-
phyte-infection
may
enhance
host
plant
fitness,
thereby in-
creasing
the
frequency
of
infected
plants
in
the next
genera-
tion.
The
question
arises
why
uninfected
plants
still
exist.
Populations
consisting
of
uninfected
plants
will
remain
so
because
infection
is
maternally
inherited,
barring
immigra-
tion
of
infected
seeds.
Within
mixed
populations
uninfected
plants
may
persist
if
there is
little or
no
selection
against
them.
For
example,
the
disadvantage of
being
uninfected
may
be
minimal
in low
density
populations
lacking herbi-
vory.
Infected
plants
may
also
lose
the
endophyte.
While
adult
plants are
not
known to
become
uninfected if
pre-
viously
infected,
the
same is
not true
of
seeds.
Endophyte
viability
decreases
more
rapidly than
seed
viability
so
pro-
longed
seed
dormancy
may result in
seeds
without
viable
endophyte
(Neill
1940;
Welty and
Azevedo
1985;
Latch
1987).
However,
the
importance of
regneration
from
seed
banks is
not known
for
many
wild
grasses.
Perennial
rye-
grass
and
tall
fescue
are
native
to
Europe but
have
been
disseminated
worldwide
by
man.
Latch
(1987)
surveyed
col-
lections of
Lolium
and
Festuca
species from
natural
habitats
and
long
established
pastures
in
Europe
and
found
that
the
frequency
of
endophyte-infection
was
much
higher than
in
commercial
cultivars.
He
suggested
that
endophyte-free
plants have
become
common
only
following
the
develop-
ment of
modern
agriculture
involving
seed
harvesting
and
storage.
Acknowledgements.
I thank
Mary
Stovall
and
David
Guaicara
for
help
with
the
plants
and
Gregory
P.
Cheplick
and
an
anonymous
reviewer for
comments
on
the
manuscript.
This
research
was
sup-
ported
by
NSF
Grant
BSR-8400163.
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Received December 22, 1986
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