CROP SCIENCE, VOL. 51, MAY–JUNE 2011 1291
T [Schedonorus arundinaceus (Schreb.) Dumort =
Lolium arundinaceum (Schreb.) Darbysh.], formerly Festuca
arundinacea Schreb., is one of the most widely grown cool-sea-
son grasses in the United States. Its popularity is due to its long
growing season, its relatively high yield for a cool-season peren-
nial grass, and its ability to withstand extreme biotic and abiotic
stresses (Fribourg et al., 2009).
Despite its popularity, tall fescue can be toxic to livestock. Its
toxicity is the result of its hosting an endophytic fungus, Neoty-
phodium coenophialum (Morgan-Jones and Gams) Glenn, Bacon,
and Hanlin comb. nov. (Bacon et al., 1977; Glenn et al., 1996).
Common strains of N. coenophialum produce ergot alkaloids that
cause fescue toxicosis, an animal disorder that costs American
livestock producers between US$600 million and $1 billion each
year (Fribourg and Waller, 2005; Roberts and Andrae, 2010).
Seasonal Fluctuation of Ergovaline
and Total Ergot Alkaloid Concentrations
in Tall Fescue Regrowth
Wendi M. Rogers, Craig A. Roberts,* John G. Andrae, David K. Davis, George E. Rottinghaus,
Nicholas S. Hill, Robert L. Kallenbach, and Don E. Spiers
Common cultivars of tall fescue [Schedonorus
arundinaceus (Schreb.) Dumort = Lolium arun-
dinaceum (Schreb.) Darbysh.] host a fungal
endophyte that produces ergot alkaloids. These
alkaloids are linked to fescue toxicosis, a seri-
ous livestock disorder in the United States. This
study was conducted to determine how ergot
alkaloid concentrations uctuate throughout the
growing season in tall fescue regrowth. In 2005,
plots were established in pastures of endo-
phyte-infected tall fescue growing in Missouri,
Georgia, and South Carolina. Each month of the
growing season, plots were clipped and forage
allowed to regrow; regrowth was sampled from
April through October 2006 and analyzed for
ergovaline and total ergot alkaloid concentra-
tions. At all three sites, ergovaline concentration
was lowest during the spring, increasing slightly
through the summer months and then sharply
in the early autumn. This pattern of ergovaline
uctuation did not mimic data published from
experiments in which tall fescue was grazed or
was allowed to grow without defoliation. Total
ergot alkaloid concentration followed a bimodal
curve, with highest concentration in the spring
and fall and lowest concentration in the summer.
We conclude that common cultivars of endo-
phyte-infected tall fescue should be regarded
as highly toxic in the autumn and less toxic in
the summer, even if pastures are clipped. We
also conclude that the toxicity potential of tall
fescue regrowth in the spring depends on which
ergot alkaloids prove most responsible for fes-
W.M. Rogers, Graduate Assistant, Division of Plant Sciences, Univ. of
Missouri, Columbia, MO 65211; C.A. Roberts and R.L. Kallenbach,
Professor, Division of Plant Sciences, Univ. of Missouri, Columbia, MO
65211; J.G. Andrae, Associate Professor, Dep. of Entomology, Soils, &
Plant Sciences, Clemson Univ., Clemson, SC, 29634-0315; D.K. Davis,
Superintendent, Univ. of Missouri Forage Systems Research Center,
Linneus, MO; G.E. Rottinghaus, Clinical Professor, College of Veteri-
nary Medicine, Univ. of Missouri, Columbia, MO, 65211; N.S. Hill,
Professor, Dep. of Crop and Soil Sciences, Univ. of Georgia, Athens,
GA 30602; D.E. Spiers, Professor, Division of Animal Sciences, Univ.
of Missouri, Columbia, MO 65211; Received 8 July 2010. *Corre-
sponding author (RobertsCr@missouri.edu).
Abbreviations: DM, dry matter; ELISA, enzyme-linked immunosor-
Published in Crop Sci. 51:1291–1296 (2011).
Published online 14 Mar. 2011.
© Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA
All rights reserved. No part of this periodical may be reproduced or transmitted in any
form or by any means, electronic or mechanical, including photocopying, recording,
or any information storage and retrieval system, without permission in writing from
the publisher. Permission for pr inting and for repr inting the material contained herein
has been obtained by the publisher.
Published May, 2011
1292 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, MAY–JUNE 2011
Livestock producers can reduce the toxicity of tall fes-
cue by adopting modern management strategies such as
incremental alleviation and alkaloid management (Rob-
erts and Andrae, 2010). These strategies are designed to
limit the amount of ergot alkaloids produced by indi-
vidual plants, o ered in the mixed pasture, preserved in
stored forage, and ultimately ingested by the grazing ani-
mal. Before producers can adopt such management strate-
gies, however, they must acquire knowledge of toxicity;
some of this knowledge includes awareness of periods in
which a tall fescue pasture contains high amounts of toxic
Early work has shown that ergot alkaloid concentra-
tions in tall fescue uctuate throughout the growing sea-
son. In grazing studies by Belesky et al. (1988), ergopeptine
alkaloid concentrat ions increased in late spr ing to coincide
with anthesis, decreased in the summer as plants enter dor-
mancy, and increased again to maximum concentration
in early autumn at the initiation of fall regrowth. This
bimodal curve, reported in Georgia (Belesky et al., 1988),
was also found by Missouri researchers (Rottinghaus et
al., 1991), who reported extremely high concentrations of
ergovaline in the spring followed by low concentrations in
the summer and high concentrations again in the autumn.
The Missouri workers also showed that the high concen-
trations in the spring were due primarily to reproductive
maturity, as concentrations were three times higher in the
seedhead than in the leaf blade.
While these studies have proved valuable, they have
not provided information regarding alkaloid concentra-
tions in tall fescue kept in a vegetative stage of maturity
throughout the entire growing season. Such information is
needed. It is possible that vegetative tall fescue, as accom-
plished by complete removal of seedheads and regular
clipping of foliage, might contain moderate to low con-
centrations of ergot alkaloids. In this case, management
practices could be developed that would partially detoxify
tall fescue in its otherwise most toxic period ofyear.
The objective of this study was to determine con-
centrations of ergovaline and total ergot alkaloids in tall
fescue regrowth throughout the growing season (April
MATERIALS AND METHODS
This study was conducted in 2006 in established pastures of
tall fescue at three sites: the Forage Systems Research Center at
Linneus, MO, the University of Georgia Plant Sciences Farm
at Watkinsville, GA, and the Clemson University Simpson
Research Farm at Pendleton, SC; these three sites are hereafter
referred to as the Missouri, Georgia, and South Carolina loca-
tions. Pastures at these sites were old stands of ‘Kentucky 31’
that had been planted at least 15 yr earlier. Before plots were
marked on these sites, tillers were tested by Agrinostics, Ltd.,
(Watkinsville, GA) for Neotyphodium infection and were deter-
mined to contain >90% infected tillers at all three locations.
The three sites o ered extremes in latitude and longitude,
soil type, and temperature and precipitation within the “fescue
belt,” the region of primary tall fescue use in the United States
(Buckner and Bush, 1979; West, 1998). The Missouri site was
located at 39°51’ N, 93°8’ W, and elevation 242 m, the Georgia
site at 33°58’ N, 83°43’ W, and elevation 293 m, and the South
Carolina site at 34°3’ N, 82°42’ W, and elevation 256 m. The
Missou ri soi l was a n Arm strong clay loam ( ne, smectitic, mesic
Aquertic Hapludalfs); the South Carolina and Georgia soils are
Cecil clay loam ( ne, kaolinitic, thermic Typic Kanhapludults).
All three sites experienced a wide range of di erences in tem-
perature and precipitation, as shown in Tables 1 and 2.
Plot Layout and Maintenance
In December 2005, four 10 × 10-m plots were marked at each
site, which served as four replications per site. After being
marked, plots were mowed and mowed plant material discarded
o site. Plots were fertilized one time with 33 kg N ha–1 the fol-
lowing March. As detailed below, plots were mowed monthly
after each sampling. The monthly mowing and fertilization
used in this study were plot maintenance practices necessary to
provide regrowth material and prevent chlorosis.
Sample Collection and Laboratory Analysis
Plots were sampled in April 2006 and at monthly intervals
through October 2006, resulting in seven harvests. A 100-g
sample was collected by randomly selecting tillers and hand clip-
ping them at soil surface. The purpose for collecting tillers at soil
surface was to determine the concentration of ergot alkaloids in
the whole tiller, not the tiller at a given height of defoliation; it
should be remembered that defoliation height varies among hay
harvesting practices and among classes of livestock. Immediately
after sampling, tillers were stored at –5°C, and plots were mowed
to a height of 10 cm and the mowed materialdiscarded.
Tillers were freeze dried and ground through a 2-mm
screen then through a 1-mm screen using a cyclone-type mill.
Ground samples were analyzed for ergovaline concentration by
high performance liquid chromatography (HPLC) according
to the procedure of Rottinghaus et al. (1991) with modi ca-
tions reported by Hill et al. (1993). Samples were also analyzed
for total ergot alkaloid concentration by enzyme-linked immu-
nosorbent assay (ELISA) following the procedure of Hill and
Ergovaline and total ergot alkaloid concentrations were ana-
lyzed as a randomized complete block with three locations,
seven harvests (months), and four replications as described by
Steel and Torrie (1980). Months and interactions with months
were considered as xed e ects, and location was considered as
a random e ect. The model used included location and block
as main plots, months as subplots, and all possible interactions.
Repeated measures ANOVA procedures were used to test
e ects of months. The SAS (SAS Institute, 2009) procedure,
PROC MIXED, was used assuming rst-order autoregressive
correlation among the repeated measures.
CROP SCIENCE, VOL. 51, MAY–JUNE 2011 WWW.CROPS.ORG 1293
is 10-fold higher than during the summer months (Rot-
tinghaus et al., 1991). In our study, the absence of a spring
peak in ergovaline concentration can be explained in terms
of anatomy, morphology, and possibly physiology. Regard-
ing anatomy and morphology, there were no seedheads
present in any stage of development, including what would
normally be the boot stage. This is because reproductive
development was suppressed; plots were mowed every
month to a 10-cm stubble height, which prevented repro-
duction from progressing beyond early stem elongation.
In other studies, such has not been the case. One
grazing trial that reported ergopeptine concentrations
described only partial control of reproductive develop-
ment, as accomplished by livestock pressure (Belesky et
al., 1988). Another grazing trial allowed the pasture to
mature beyond anthesis before mowing (Peters et al.,
1992). In both cases, ergovaline concentration increased
in the spring then decreased in the summer; this spring
peak was likely the result of seedheads and/or reproduc-
tive stems, which are known to contain high concentra-
tions of endophytic mycelia and ergovaline (Christensen
and Voisey, 2009; Rottinghaus et al., 1991).
With regard to a physiological explanation, the lack
of a spring peak in ergovaline concentration may re ect
restrictions in ergovaline biosynthesis. Because plots in
this study were mowed monthly, plants may have allo-
cated resources with a priority on leaf growth (Wilhelm
and Nelson, 1978) and hyphal extension (Christensen et
al., 2008; Schmid et al., 2000; Tan et al., 2001) rather than
on fungal secondary metabolite production. Other physi-
ological explanations may involve altered phytohormone
production and signaling in the host plant as a result of
suppressing reproductive development; explanations such
as these will require further study.
After the gradual increase from spring through sum-
mer, ergovaline concentration peaked in the fall. This peak
RESULTS AND DISCUSSION
Mean ergovaline concentration among the locations and
months of the growing season (April to October) ranged
from 75 to 1038 µg ergovaline kg–1 dry matter (DM) (Fig.
1). There was a signi cant month × location interaction,
so data were not pooled.
At each location, ergovaline concentration was lowest
in early spring (Fig. 1). At the Missouri location, ergovaline
concentration was only 75 µg kg–1 DM in April; this was
three times lower than ergovaline at the Georgia and South
Carol in a locations i n Apr il , where co ncentr ations were nearly
identical (Fig. 1) at 283 and 277 µg kg–1 DM, respectively.
The ergovaline concentrations in April coincided
with ambient temperatures. The Missouri location was
Linneus, MO, which is not far from the Iowa border;
the high temperature for April averaged 11.5°C. At both
southern locations, the April temperature reached 18.2°C
(Table 1). The low ergovaline concentrations in April
were expected for Missouri, as concentrations are low-
est during late winter and only begin to increase during
the rst month after winter dormancy (Curtis and Kal-
lenbach, 2007; Ka llenbach et a l., 2003). The fact that April
concentrations were lower in Missouri than in Georgia or
South Carolina relates to the di erence in mean monthly
temperatures between the northern and southern loca-
tions. According to Ju et al. (2006), the minimum tem-
perature for Neotyphodium growth is 5°C warmer than for
tall fescue growth. Thus, warmer temperatures in Geor-
gia and South Carolina would induce greater endophyte
growth and therefore increase alkaloid concentrations.
What was not expected was the low ergovaline con-
centration that was sustained throughout the entire spring
and summer months (Fig. 1). In grazed pastures, ergovaline
reportedly peaks during late spring then decreases by half in
the late summer months (Belesky et al., 1988; Peters et al.,
1992). In nongrazed pastures, this spring peak is more pro-
nounced because no seedheads are removed and ergovaline
Table 1. Monthly average high and low air temperatures for
the growing season (March through October) of 2006 at the
University of Georgia Plant Sciences Farm, Watkinsville, GA,
the Forage Systems Research Center, Linneus, MO, and the
Clemson University Simpson Research Farm, Pendleton, SC.
Average ambient temperatures (°C)
Georgia Missouri South Carolina
Month High Low High Low High Low
March 13.8 0.8 5.3 –7.5 12.2 –0.1
April 18. 2 4.1 11.5 –0 .5 18 . 2 3 . 4
May 23.2 8.1 21.4 7.2 25.5 9.9
June 27.0 12.6 22.7 10.9 25.1 10.6
July 30.1 16.8 28.0 16 .1 31.1 16 .8
August 31.6 19.0 32.2 19.5 32.3 19.8
September 31.0 18.6 29.7 18.9 32.9 20.5
October 27.8 15.7 23.7 9.0 26.8 15.4
Table 2. Monthly precipitation for 2006 at the University of
Georgia Plant Sciences Farm, Watkinsville, GA, the Forage
Systems Research Center, Linneus, MO, and the Clemson
University Simpson Research Farm, Pendleton, SC.
2006 precipitation (mm)
Month Georgia Missouri South Carolina
January 135 47 112
February 110 1 60
March 146 88 46
April 112 77 58
May 103 67 54
June 102 110 152
July 109 104 41
August 95 135 77
September 95 31 99
October 91 77 104
November 90 51 65
December 97 42 94
1294 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, MAY–JUNE 2011
could have been expected for ergovaline, as it has occurred
in early autumn in both Missouri (Rottinghaus et al., 1991)
and North Carolina (Burns et al., 2006). This late autumn
peak has also occurred in Georgia (Belesky et al., 1988).
Total Ergot Alkaloid Concentration
Total ergot alkaloid concentration ranged from 327 to 2411
µg kg–1 DM among the three locations (Fig. 2). Concentra-
tions varied across months (Fig. 2), and there was a month ×
location interaction. Therefore data were not pooled.
In general, total ergot alkaloid concentration uctu-
ated according to a bimodal pattern throughout the grow-
ing season (Fig. 2). Concentrations were high in the spring,
lower in the summer, and higher again in the autumn. This
bimodal pattern was most clear at the Georgia and South
Carolina sites, as these locations revealed a prolonged period
of low ergot alkaloid concentration through the summer
months. A summer decrease in concentration coincides
with semidormant state of tall fescue, which occurs over
a much longer period than would occur in northern Mis-
souri. The low summer concentrations also coincide with
temperatures for endophyte growth; according to Li et al.
(2008), the optimum growing temperature for Neotyphodium
gansuense Li et Nan, the symbiont hosted by Achnatherum
inebrians (Hance) Keng, is 25°C, and growth ceases at 35°C.
Total ergot alkaloid concentration during April was
551 µg kg–1 DM at the Missouri location; this was approx-
imately two-thirds lower than concentrations at the Geor-
gia and South Carolina locations for April (Fig. 2). Again,
the low concentrations during April in Missouri probably
re ect limited fungal activity at cold temperatures (Table
1), as tall fescue growth is accelerating but Neotyphodium
growth is not (Ju et al., 2006).
Toward the end of the growing season, total ergot
alkaloid concentration increased to its highest level (Fig.
Figure 1. Ergovaline concentration in Neotyphodium-infected
‘Kentucky-31’ tall fescue regrowth. Plants were harvested in 2006
at the University of Georgia Plant Sciences Farm at Watkinsville,
GA, the University of Missouri Forage Systems Research Center
at Linneus, MO, and the Clemson University Simpson Research
Farm at Pendleton, SC. Bars are averaged across ﬁ eld replications,
and error bars represent 2 SE. DM, dry matter.
Figure 2. Total ergot alkaloid concentration in Neotyphodium-
infected ‘Kentucky-31’ tall fescue regrowth. Plants were harvested
in 2006 at the University of Georgia Plant Sciences Farm at
Watkinsville, GA, the University of Missouri Forage Systems
Research Center at Linneus, MO, and the Clemson University
Simpson Research Farm at Pendleton, SC. Bars are averaged
across ﬁ eld replications, and error bars represent 2 SE. DM,
CROP SCIENCE, VOL. 51, MAY–JUNE 2011 WWW.CROPS.ORG 1295
2). Concentration in October in Missouri was 2411 µg
kg–1 DM, in Georgia was 1972 µg kg–1 DM, and in South
Carolina was 2038 µg kg
–1 DM. This increase in the
autumn mirrored the increase of ergovaline concentration
in the autumn (Fig. 1).
Concentrations of total ergot alkaloids likely re ect
compounds produced by Neotyphodium. They would not
include compounds produced by Claviceps purpurpea (Fr.)
Tul., the surface fungus that inoculates seedheads. Because
plots were clipped monthly, there were no seedheads pres-
ent. Therefore, the only ergot alkaloids present would be
those produced by fungi in or on the vegetative material.
To date, the literature would indicate the primary fungus
would be Neotyphodium, whose alkaloids are found in the
leaf blade, sheath, and culm (Burns et al., 2006; Spiering et
al., 2005; Christensen et al., 1997; Keogh et al., 1996; Lyons
et al., 1986), not just the seedhead.
Concentrations for total ergot alkaloids (Fig. 2) fol-
lowed the same trend as ergovaline concentrations in the
summer and autumn (Fig. 1) but not the spring. Total
ergot alkaloids were determined by ELISA, which detects
compounds known to be precursors in ergovaline synthe-
sis (Schardl and Panaccione, 2005). The ELISA method
may also be detecting derivative products of ergovaline
breakdown that could have occurred over the previous
winter (Kallenbach et al., 2003).
When tall fescue is kept in a stage of vegetative regrowth,
ergovaline concentration is low in the spring, increases
gradually through the spring and summer months, and
increases sharply in the autumn months. This pattern of
ergovaline uctuation was consistent across all three sites,
even with the variation in geographical location, soil type,
temperature, and precipitation. This pattern of uctua-
tion, particularly during the spring months, is not similar
to patterns of uctuation published from grazing trials or
from experiments in which tall fescue is not defoliated.
Other studies report that ergovaline concentration during
the spring reaches a peak, the magnitude of which appears
to be related to extent of defoliation.
One reason for the low concentration during the
spring in this study was probably because host plants were
not allowed to develop ergovaline-rich seedheads. Another
reason might have been because as plants were repeatedly
stressed, they were forced to prioritize resources toward leaf
growth instead of fungal secondary metabolite production.
Also in tall fescue clipped monthly, total ergot alkaloid
concentration generally followed a bimodal curve, with
highest concentrations in the spring and autumn. These
concentrations likely included a wide range of compounds
in addition to ergovaline.
At present, the question remains regarding which
alkaloid measurements best re ects toxicity, whether the
causative agent includes ergovaline primarily or ergovaline
and the entire class of ergot alkaloids (Hill, 2005). If at least
one of the primary causative agents is ergovaline, this study
shows that tall fescue can be partially detoxi ed in the late
spring, which is otherwise the most toxic time of year. If the
causative agents include all ergot alkaloids, the study shows
that the spring and autumn are by far the most toxic times
of the year, even if the pasture is clipped repeatedly. Under
extreme temperatures and poor management, this potential
toxicity would readily translate into fescue toxicosis.
Follow-up research should examine the vertical distri-
bution of ergovaline and ergot alkaloids within the vege-
tative canopy, as this study merely reported concentrat ions
in whole tillers. Future research should also include a clip-
ping study to determine the minimum number of clipping
events required to eliminate the ergovaline peak in the
spring months, as a monthly clipping regime would not
likely prove to be economically justi able.
We express our gratitude to Mr. Greg Durham, University
of Georgia, for sample collection and plot maintenance at the
Georgia location. We also express gratitude to Ms. Valerie Tate,
at the Forage Systems Research Center, University of Missouri,
for her assistance at the Missouri location.
This paper is based on work supported by the U.S. Department
of Agriculture, under Agreement No. 58-6227-3-016. Any
opinions, ndings, conclusion, or recommendations expressed
in this publication are those of the author(s) and do not neces-
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