Published November 25, 2014
Effects of fescue toxicosis on bull growth,
semen characteristics, and breeding soundness evaluation1
H. M. Stowe,* M. Miller,* M. G. Burns,* S. M. Calcatera,* J. G. Andrae,*
G.E. Aiken,† F. N. Schrick,‡ T. Cushing,§ W. C. Bridges,* and S. L. Pratt*2
*Department of Animal and Veterinary Sciences, Clemson University, Clemson, SC 29634; †USDA-ARS-Forage-Animal
Production Research Unit, University of Kentucky Campus, Lexington 40546; ‡Department of Animal Science,
University of Tennessee, Knoxville 37996; and §Livestock and Poultry Health, Clemson University, Columbia, SC 29229
Abstract: Tall fescue possesses heat, drought, and
pest resistance conferred to the plant by its mutualistic
relationship with the ergot alkaloid producing fungal
endophyte, Neotyphodium coenophialum. The objective of this study was to evaluate the impact of ergot
alkaloid consumption on growth, scrotal circumference
(SC), and semen quality. The SC measurement and
percentage of motile and normal sperm were used to
determine if a bull passed the breeding soundness exam
(BSE) requirements. Bulls (n = 14) between 13 and 16
mo of age exhibiting ≥32 cm SC and having passed a
BSE were assigned to 1 of 2 dietary treatments accounting for BCS and BW. Bulls were fed the treatment diet
containing toxic tall fescue seed (E+; 0.8 μg of ergovaline and ergovalanine/g DM) or the control diet containing endophyte-free nontoxic tall fescue seed (E–) for
126 d. Blood samples were collected and BSE and BCS
accessed at the start of the test (d 0) and every 21 d to
the end of test (d 126). Weights were obtained on d 0
and d 126. Serum prolactin (PRL) concentrations were
affected by treatment × day interactions (P = 0.04) verifying the effectiveness of the E+ diet. Bulls consuming
the E+ diet exhibited declining PRL concentrations from
250 ± 52.1 ng/mL on d 0 to 30.6 ± 46.9 ng/mL by d 126
whereas bulls receiving the E– ration maintained serum
PRL concentrations greater than or equal to 226.7 ± 50.4
ng/mL across the 126-d study. Body condition score
(P = 0.4) and BW (P = 0.4) were not different between
treatments. No difference due to treatment was observed
for the percentage of bulls passing a standard BSE exam
(P = 0.6) and no treatment effect was observed for any
semen characteristic measured by computer-assisted
semen analysis (CASA; P ≥ 0.2). The SC was negatively affected by treatment × day interaction (P = 0.04)
with E– bulls exhibiting a larger SC at d 126 compared
with E+ bulls of 36.7 ± 0.8 versus 34.3 ± 0.8 cm, respectively. Within treatment, E+ bulls exhibited a decrease
in SC (P = 0.0001) with a d 0 SC of 37.3 ± 0.8 cm and
dropping to 34.3 ± 0.8 by d 126. Theoretically, reduced
SC would negatively impact semen quality, but this was
not observed. However, CASA and BSE evaluation data
are consistent with recent reports indicating that bulls
grazing E+ tall fescue exhibited only subtle, if any, differences on semen characteristics.
Key words: breeding soundness exam, computer assisted semen analysis, fescue toxicosis,
scrotal circumference
© 2013 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2013.91:3686–3692
doi:10.2527/jas2012-6078
Introduction
1This material is based on work supported by NIFA/USDA, under
project number SC-1700376, and was supported by National Research
Initiative Competitive Grant no. 2010-38942-20745 from the USDA
National Institute of Food and Agriculture and the Cooperative
State Research, Education and Extension Service and has been assigned Technical Contribution No. 6092 of the Clemson University
Experiment Station.
2Corresponding author: scottp@clemson.edu
Received November 7, 2012.
Accepted May 3, 2013.
Tall fescue [Schedonorus phoenix (Scop.) Holub]
is present on approximately 16 million ha in the
mid-Atlantic and southern regions of the United
States (Hoveland, 1993) and serves as a forage for
approximately 8.5 million cattle, making this species the
dominant cool-season perennial grass in the region. The
vast majority of this forage is infected with the endophyte
Neotyphodium coenophialum, with the grass existing
in a mutualistic relationship with the ergot alkaloid
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Fescue Toxicosis and Semen Quality
producing endophyte conferring disease, drought, grazing
tolerance, and insect resistance to tall fescue (Hoveland,
1993). Ergot alkaloids negatively impact growth and/or
reproductive performance of animals grazing tall fescue
containing the wild-type endophyte. Accumulation of the
ergot alkaloids within the system of the animal result in
the syndrome of fescue toxicosis, which is characterized
by rough hair coat, increased core body temperature,
decreased blood flow to body extremities, and poor
growth and reproductive performance (Thompson and
Porter, 1990; Porter and Thompson, 1992). Estimates for
lost beef production due to fescue toxicosis were US$600
million (Hoveland, 1993); however, more recent reviews
estimate that total to be approaching $1 billion lost per
year for cattle and small ruminants (Allen and Segarra,
2001; Strickland et al., 2011).
The most studied aspects of fescue toxicosis are the
effects on animal performance (Browning, 2004; Gunter
and Beck, 2004; Watson et al., 2004; Johnson et al., 2012),
with more limited documentation of the effects of fescue
toxicosis on reproductive function (Burke et al., 2001;
Jones et al., 2003). Little information is available describing
the effects of fescue toxicosis on bovine male reproduction
(Jones et al., 2004; Schuenemann et al., 2005a,b; Looper
et al., 2009). The objectives of this study were to evaluate
semen characteristics of yearling beef bulls being fed
a defined, constant amount of ergot alkaloid in a highconcentrate ration to delineate toxic effects of the ergot
alkaloids from possible reduced body condition and plane
of nutrition of animals grazing tall fescue pastures.
Materials and Methods
All animal research was approved by the Clemson
University Institutional Animal Care and Use Committee
(IACUC; IACUC protocol number ARC2010-68).
Experimental Design
All reagents were purchased from Sigma Scientific
(St. Louis, MO) unless stated otherwise. Fourteen Angus
(n = 8) and Hereford (n = 6) bulls between 13 and 16 mo
of age exhibiting ≥32 cm scrotal circumference (SC) and
passed a breeding soundness exam (BSE) were stratified
by breed, BW, and BCS and allotted to 1 of 2 treatments.
One bull [allotted to control diet containing endophytefree nontoxic tall fescue seed lacking ergot alkaloids
(E–) treatment] did not tolerate semen collection but
remained in the study for collection of data on other
measurable variables including growth data, BCS, and
serum prolactin (PRL) concentration. A second bull
[allotted to treatment diet containing toxic tall fescue
seed possessing ergot alkaloids (E+; 0.8 g of ergovaline
and ergovalanine/g DM)(E+) treatment] failed the
3687
initial BSE but was used to evaluate nonreproductive
variables and the testes of a third bull (allotted to E+
treatment) were injured midway through the study. The
reproductive data of the third bull before injury and
growth data postinjury are included in the study as no
adverse effects were noted for growth and BCS. All bulls
were evaluated at 21-d intervals for reproductive and
growth parameters. The study duration was designed to
monitor bulls through 2 full spermatogenic cycles.
Treatment
Dietary treatments contained fescue seed that either
contained ergot alkaloid (E+) or was negative for ergot
alkaloid (E–). The total concentration of ergovaline and
ergovalanine for the E+ and E– seed were 2.1 mg/kg DM
and 0 mg/kg DM, respectively, as assayed by USDAARS-Forage-Animal Production Research Unit using
HPLC procedures as described in Johnson et al. (2012).
The diet (including seed) was formulated to meet energy,
CP, and mineral requirements (85% DM, 68% TDN, and
12.7% CP on DM basis) of the bulls and fed to provide
adequate nutrients for 1.0 kg/d BW gain (NRC, 1996). All
bulls were adjusted to the concentrate diet before initiation
of the study. Bulls were fed within treatment with 2 pens
per treatment once daily at 0800 h. During this 2-wk time
period, the diet contained only E– seed. The E+ ration
contained 0.8 μg of ergovaline and ergovalanine/g DM. At
the start of the test, bulls were weighed, BCS and BSE
were determined, and then bulls were allotted to diets
and remained on E+ or E– diets for the remainder of the
126-d study (April 6, 2011 to August 10, 2011). To verify
that bulls were responding to treatment, blood samples
were obtained via the caudal artery at the start of test and
every 21 d to the end of test and assayed for serum PRL.
Serum was harvested from whole blood by centrifugation
at 2,000 × g for 15 min at 4°C, placed in vials, and stored
at –20°C until used in RIA for PRL. Prolactin assays were
performed by the F. Neal Schrick laboratory as previously
described (Bernard et al., 1993) with mean inter- and intraassay CV of 9.7 and 6.0%, respectively.
Breeding Soundness Exam and Semen Evaluation
Bulls were restrained in standard animal handling
chutes and subjected to electro-ejaculation using the
Pulsator IV electro-ejaculator (Agtech, Manhattan, KS)
on the preprogrammed collection mode. The ejaculate
volume was recorded and semen quality variables were
estimated using computer-assisted semen analysis
(CASA) using the SQA-Vb (A-Tech, Los Angeles, CA).
Each sample had CASA performed in duplicate, and if
motility and/or morphology were below 30 and 70%,
respectively, a second collection was obtained within 7 d
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Stowe et al.
of the first sample. If both samples were below 30 and 70%,
respectively, the greatest rated collection for the bull was
used in subsequent analysis. Variables evaluated by CASA
were sperm cell concentration (M/mL), percent motility,
percent progressive motility, motile sperm concentration
(M/mL; percent motility × sample concentration),
progressive motile sperm concentration (M/mL; percent
progressive motility × sample concentration), sperm
velocity (μM/sec), total sperm number (sample volume ×
sample concentration), total motile sperm concentration
(sample volume × motile sperm concentration), and total
progressive motile sperm concentration (sample volume ×
progressive motile sperm concentration). In addition, each
sample was subjected to estimations of morphology using
standard staining and microscopic examinations. Bulls
failed BSE if their semen samples from both collections
exhibited <30% motility, <70% normal morphology, or a
SC lower than recommend for their respective age range
using the 1993 Society for Theriogenology guidelines
(Spitzer and Hopkins, 1997) for BSE.
Statistical Analysis
The GLIMMIX procedure (SAS Inst. Inc., Cary, NC)
was used to perform an ANOVA to test for the main effects
and main effect interactions for all semen parameters and
BCS. The model included fixed effects for treatment (E+
vs. E–), day, and treatment × day. To adjust for the effects
of breed, the model also included fixed effects of breed,
breed by treatment, breed × day, and day × treatment ×
breed. To correct for the repeated measures, a whole plot
error term was used to test treatment, and a subplot error
term was used to test day and treatment × day. To adjust
for the effects of BW, the model also included BW as a
covariate. We also attempted to adjust for breed, BCS,
and BW experimentally by creating “blocks” based
on breed, BCS, and BW and allotting treatments with
the “blocks.” The GLM procedure in SAS was used to
assess the main effects of treatment, breed, day, and all
interactions on BW, total BW gain, and ADG. Treatment
× day combination means for all SAS procedures were
generated and compared using Fisher’s LSD test.
Differences in the ability of a bull to pass a BSE due to
treatment were evaluated by χ2 analysis.
Pathology
Immediately after the feedlot portion of this study, 8
bulls (n = 4, for E– and E+, consisting of 3 Angus and 1
Hereford, per treatment) were slaughtered at a USDA
inspected abattoir. Testes and the pampiniform plexus
were collected from these animals and fixed in 10%
neutral buffered formalin (Merck, Darmstadt, Germany).
Formalin-fixed samples were processed in a Leica ASP300S
Figure 1. Comparison of serum prolactin (PRL) concentrations between
bulls receiving a diet containing ergot alkaloids (E+) or negative for ergot
alkaloids (E–) across a 126-d trial. Mean PRL values are given in ng/mL (y-axis)
for each treatment × day combination. The day of treatment blood samples were
obtained for analysis is given on the x-axis. The * denotes significance (P ≤ 0.02)
between treatments. a–dSuperscripts within the E+ treatment denotes differences
due to day (P = 0.01).
(Bannockburn, IL) using this regimen: 1 h formalin, 2 h
formalin, 45 min 50% ethanol, 45 min 70% ethanol, 45 min
90% ethanol, 45 min 90% ethanol, 45 min 100% ethanol,
45 min 100% ethanol, 45 min xylene, 45 min xylene, 30
min paraffin wax, 3 min paraffin wax, and 30 min paraffin
wax. Samples were embedded in paraffin and stored until
sectioning occurred. Samples were trimmed to 4 to 5 μm
thickness and stained with hematoxylin and eosin. The
slides were examined by an American College of Veterinary
Pathologists board-certified pathologist who was blinded to
the treatment groups.
Results
Induction of Fescue Toxicosis
Blood samples were collected for each bull at the
start of test and every 21 d over the 126-d experiment
and serum samples were assayed for circulating
PRL concentrations. Figure 1 shows serum PRL
concentrations for E+ and E– bulls across the 126d experiment. Serum PRL concentrations for the E–
group ranged from 226.7 ± 50.4 to 321.0 ± 45.7 ng/mL.
Analysis revealed a treatment × day interaction (P <
0.04). Serum PRL concentrations differed at d 63, 84,
105, and 126 between the E+ and E– treatments with
values of 321.0 ± 45.7, 276.2 ± 48.7, 226.7 ± 50.4, and
263.5 ± 51.7 for the E– group and 159.4 ± 45.7, 64.4 ±
46.2, 47.3 ± 46.2 and 30.6 ± 49.6 ng/mL for the E+
group (P ≤ 0.02). Additionally, within the E+ treatment,
PRL concentrations were lower at d 84, 105, and 126
than at the start of test (251.5 ± 52.1 ng/mL; P = 0.008).
3689
Fescue Toxicosis and Semen Quality
Table 1. Mean BW, total BW gain, and ADG per treatment group for the start of the experiment (d 0) and the end of
the experiment (d 126) for bulls receiving a diet containing ergot alkaloids (E+) or negative for ergot alkaloids (E–)
Breed
Angus
(n = 8)
Treatment
d 0, kg
d 126, kg
E–
522.6 ± 39.9a
654.3 ± 43.5a
E+
495.6 ± 39.9a
624.7 ± 43.5a
Hereford
E–
498.5 ± 46.1a
648.9 ± 50.2a
(n = 6)
E+
488.8 ± 46.1a
590.9 ± 50.2a
a,bMeans within column possessing different superscripted lowercase letters differ (P ≤ 0.04).
Consumption of Toxic Tall Fescue
Seed Effects on Bull Growth
Total BW gain for bulls on the 126-d test are given in
Table 1. No difference was observed for BW between the
E+ and E– bulls on d 0 (P = 0.7) as bulls were stratified
based on BW before allotment to treatment. In addition,
BW did not differ between groups on d 126 (P = 0.4).
However, treatment × breed effects (P = 0.04) were
observed for total BW gain and ADG (P = 0.04) across the
126-d trial with Hereford bulls on the E+ diet exhibiting
decreased BW gains compared with Hereford bulls on E–
diet and both treatments of Angus bulls. No difference
was observed due to treatment (P = 0.4) or breed (P = 0.1)
for BCS; however, day (P = 0.0001) impacted BCS. The
mean BCS values were 5.6 ± 01, 5.4 ± 0.1, 5.3 ± 0.1, 5.4 ±
0.1, 5.8 ± 0.1, 5.9 ± 0.1, and 6.0 ± 0.1 for d 0, 21, 42, 63,
84, 105, and 126, respectively.
Effects of Consumption of Toxic Tall
Fescue Seed on Reproductive Variables
No effects due to treatment, day, or treatment × day
interaction were observed for ejaculate volume, sperm
concentration, morphology, percent motile sperm,
percent progressively motile sperm, or derivative
data generated from those parameters such as motile
sperm concentration, progressively motile sperm
concentration, total sperm, total motile sperm, or total
progressively motile sperm (P ≥ 0.1; Table 2). Day
effect was observed for sample volume (P = 0.002),
motility (P = 0.01), progressive motility (P = 0.004),
and velocity (P = 0.002; Table 2). No differences were
observed for the number of bulls passing a BSE at any
time during the 126-d evaluation due to treatment (P =
0.6). Interestingly, of the 12 animals that were collected
every 21 d, treatment × day interaction impacted SC (P =
0.0001; Fig. 2). The SC was less for E+ bulls at d 126
(34.3 ± 0.8 cm) than for E– bulls at d 0, 21, 42, 63, 84,
105, and 126 (P = 0.02; values ranged from 36.6 ± 0.8
to 37.4 ± 0.8 cm). In addition, within treatment, E+ bulls
showed a reduction in SC across the test, with decreased
SC values observed by d 105 and d 126 compared with
earlier measurements (P = 0.0001). To evaluate the
possibility of testicular degeneration as the causative
Total BW gain, kg
131.6 ± 9.1a
129.1 ± 9.1a
150.4 ± 10.5a
102.1 ± 10.5b
ADG, kg
1.0 ± 0.1a
1.0 ± 0.1a
1.2 ± 0.1a
0.8 ± 0.1b
effect of decreasing SC in the E+ bulls, testes from
E– and E+ bulls were fixed, sectioned, and stained and
sections were subjected to histological evaluation. Four
bulls from each treatment were euthanized and testis
samples collected. Evaluation of the testis tissue samples
of the 8 bulls was unremarkable. Seven of the 8 bulls
(4 E+ and 3 E–) exhibited minimal to mild depletion of
spermatocytic cells (spermatocytes and spermatogonia).
One E– bull exhibited a mild to moderate decrease in
spermatogenic epithelium. No significant changes to the
vascular endothelium, vessel wall, or perivascular soft
tissues were identified to suggest vasculitis, vascular
necrosis, or vascular compromise leading to edema of
the pampiniform plexus.
Discussion
Prolactin serum concentrations for bulls on this study
tend to agree with those reported by the laboratory of
Schrick for bulls grazing tall fescue, with the exception that
the E– groups PRL concentrations were slightly greater in
this study than in previous reports, but the E+ values were
nearly identical between the 2 studies (Schuenemann et
al., 2005b). Interestingly, PRL values from our data are
inconsistent with those reported for bulls being fed a
silage-based ration containing ergotamine tartrate as they
observed no differences in PRL values for bulls being
fed ergotamine tartrate and controls (Schuenemann et al.,
2005a). Additionally, PRL values for E+ bulls in our study
do not seem to decrease as rapidly or to the depressed
concentrations observed in cows and steers (Lipham et
al., 1989; Browning et al., 1997; Samford-Grigsby et al.,
1997; Browning, 2000; Aiken et al., 2007). However, the
decrease in PRL over time observed in our study validates
that tall fescue toxicosis was established in the E+ group.
Furthermore, any observed differences in the physiological
parameters evaluated were most likely due to toxicosis or
perhaps toxicosis by environment interactions such as heat
stress as reported for other aspects of animal physiology
(Gadberry et al., 2003; Spiers et al., 2012). In fact, heat
stress has been shown to negatively impact bull semen
quality (Brito et al., 2003; Rahman et al., 2011); however,
little if any literature exists examining the interaction of
tall fescue toxicosis and heat stress affecting bull fertility
in vivo. Limited nutrition or energy levels were most likely
3690
Stowe et al.
Table 2. Means for semen quality variables of bulls receiving a diet containing ergot alkaloids (E+) or negative for
ergot alkaloids (E–) for the 126-d experiment
Parameter
†Ejaculate
volume, mL
Treatment
d0
d 21
d 42
d 63
d 84
d 105
d 126
E–
3.3 ± 1.0d
5.2 ± 1.0d
5.0 ± 1.0cd
5.9 ± 1.0cd
6.5 ± 1.1ab
5.7 ± 1.1bc
8.5 ± 1.1a
E+
3.3 ± 1.1d
3.6 ± 1.0d
4.8 ± 1.0cd
4.3 ± 1.0cd
7.7 ± 1.0ab
7.4 ± 1.0bc
9.0 ± 1.0a
Concentration,
E–
578.4 ± 145.3a 572.0 ± 128.9a 518.2 ± 131.1a 549.4 ± 138.5a 624.6 ± 140.0a 720.8 ± 146.2a 397.0 ± 149.2a
M/mL
E+
481.3 ± 147.6a 473.4 ± 136.9a 391.1 ± 136.9a 395.0 ± 133.9a 392.2 ± 138.2a 549.4 ± 138.5a 340.5 ± 143.2a
†Motility,
E–
68.3 ± 5.9b
85.2 ± 5.8a
90.4 ± 5.7a
76.9 ± 5.6a
87.1 ± 6.5a
80.4 ± 6.6ab
92.5 ± 6.6a
%
E+
66.1 ± 6.2b
80.7 ± 6.0a
90.3 ± 6.0a
83.6 ± 6.0a
91.5 ± 6.0a
76.2 ± 6.0ab
74.3 ± 6.1a
†Progressive
E–
58.5 ± 5.3d
71.1 ± 5.1abc
78.1 ± 5.1a
64.1 ± 5.1bcd
76.3 ± 5.8ab
77.4 ± 5.9abc
76.0 ± 5.9cd
motility, %
E+
56.1 ± 5.5d
66.1 ± 5.4abc
77.8 ± 5.4a
69.4 ± 5.4bcd
79.0 ± 5.4ab
68.6 ± 5.4abc
55.4 ± 5.5cd
Morphology,
E–
77.8 ± 6.8a
76.9 ± 6.1a
73.4 ± 6.2a
84.4 ± 6.1a
84.0 ± 6.9a
79.6 ± 7.1a
81.6 ± 7.2a
%
E+
78.0 ± 6.8a
91.1 ± 6.6a
86.6 ± 6.5a
84.2 ± 6.4a
81.6 ± 6.5a
72.9 ± 6.6a
63.7 ± 6.7 a
Motile sperm concentration,E–
400.9 ± 102.6a 463.4 ± 91.9a 461.4 ± 92.6a 404.5 ± 89.2a 544.4 ± 99.0a 514.8 ± 103.6a 347.0 ± 105.6a
M/mL
E+
323.8 ± 104.3a 364.4 ± 98.2a 350.6 ± 96.8a 309.5 ± 94.6a 360.5 ± 97.7a 348.6 ± 97.9a 247.4 ± 101.1a
Progressive motile sperm E–
337.0 ± 90.7a 399.1 ± 80.6a 396.7 ± 82.0a 351.0 ± 78.9a 468.8 ± 87.7a 445.2 ± 91.8a 294.3 ± 93.4a
concentration, M/mL
E+
272.2 ± 92.2a 313.7 ± 86.9a 302.4 ± 85.6a 266.4 ± 83.8a 307.6 ± 86.4a 290.9 ± 86.6a 191.46 ± 89.4a
†Velocity,
E–
54.4 ± 8.2b
67.5 ± 7.6ab
72.1 ± 7.7a
79.2 ± 7.5a
74.9 ± 8.6a
73.5 ± 8.8ab
57.3 ± 8.9b
mic1/s
E+
48.8 ± 8.4b
65.1 ± 8.1ab
76.4 ± 8.0a
71.8 ± 7.9a
65.0 ± 8.1a
52.8 ± 8.1ab
42.3 ± 8.3b
a–dMeans within the same row possessing different suprscripted lowercase letters differ (P < or = 0.04) due to day within treatment. the (symbol) to the left
denotes which semen quality variables differed due to day (P < 0.02).
1mic = micron.
not involved in any observed differences in this report as
bulls on E– and E+ treatments were in a positive energy
balance as exhibited by both BW gain and BCS. However,
breed × treatment interactions were observed for ADG.
Others have established that ergot alkaloids in the
diet can negatively impact bovine male fertility measured
using in vitro systems (Schuenemann et al., 2005a,b).
These observations are further supported by the negative
impact of E+ diets on male mouse reproduction (Wagner
et al., 2000; Ross et al., 2004). The laboratory of Schrick
reported a consistent observation of reduced cleavage rates
by approximately 10 to 17% during in vitro fertilization
(Schuenemann et al., 2005a,b); however, at this time it is
unclear if this depressed cleavage rate is due to a lack of
sperm penetration or pronuclear formation or a failure to
activate the oocyte after fertilization. The E+ treatment
in male mice from inbred lines deemed susceptible to
fescue toxicosis exhibited reduced litter size, but litter size
was significantly increased in the inbred fescue toxicosis
resistant line (Ross et al., 2004). An assessment of male
fertility was not conducted in this study; however, the data
presented here show that semen quality in this report is
similar to those previously reported for Zebu influence and
British breed bulls during similar times of the year in the
southern portion of the United States (Jones et al., 2004;
Schuenemann et al., 2005a,b; Looper et al., 2009). We
observed similar nonsignificant trends, but semen quality
variables measured were only significantly impacted
by day and our data are in agreement with others using
English breed based bulls in the southeastern United
States (Schuenemann et al., 2005a,b). Furthermore, the
observations reported here were obtained from bulls on a
concentrate ration; therefore, energy in the diet most likely
differed between the previous reports and our investigation.
The major observation shown in this report, which could
significantly decrease semen quality and production over
time, was the reduction in SC in the E+ bulls by d 105
and 126 of the study. Scrotal circumference is an indirect
assessment of testicular weight (Hahn et al., 1969; Coulter
and Foote, 1976; Coulter and Keller, 1982) with both SC
(Almquist et al., 1976; Gipson et al., 1985) and testicular
weight (Almquist and Amann, 1961; Killian and Amann,
1972) being positively correlated to sperm production
and therefore the reason and importance of acceptable
SC for individual bulls in the BSE. The reduction in SC
observed in this experiment is in contrast to previous
reports (Schuenemann et al., 2005a,b; Looper et al., 2009).
Figure 2. Effect of a diet containing ergot alkaloids (E+) on scrotal
circumference (SC) across the 126-d trial. Scrotal circumference is shown in
centimeters (y-axis) and day of treatment the measurements were taken is on
the x-axis. The * denotes significance (P = 0.02) between groups and ŧ signifies
significance between day within group (P = 0.0001). Fig. 2.
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Fescue Toxicosis and Semen Quality
However, a similar observation was previously reported in
a case study for Angus bulls consuming an E+ diet (Jones et
al., 2004). The data presented here show a marked decline
in SC of bulls consuming the E+ ration within treatment
at the end of the study in comparison with the previous
data, and this difference could be due to the length of the
study (126 d compared with 60 d) or the time of year at
which the study was conducted. Because ergot alkaloids
are known vasoconstrictor (Aiken et al., 2007; Klotz et al.,
2007; Foote et al., 2012), it is reasonable to speculate that
over 126 d of constant exposure to the E+ containing highconcentrate ration, the testicular vein becomes constricted
and reduces blood flow to the testes, producing an ischemic
state as reported for other tissues (Schoning et al., 2001;
Foote et al., 2011), which may lead to increased cell death
and reduced cellular proliferation. Bioaccumulation of
E+ may also occur in the testes as in other tissues (Klotz
et al., 2007, 2009) and may affect spermatogenesis and/
or spermatozoa function directly. We conducted a blind
histological analysis on the pampiniform plexus and testis
of 4 E– and 4 E+ bulls. No erosion of the vasculature or
degeneration of the testicle was observed, as may have
been indicated by the reduction in SC. Although bulls
(E+ and E–) did exhibit Sertoli cells only, Sertoli cells and
spermatogonia, or Sertoli, spermatogonia, and depleted
numbers of spermatocytes, Sertoli only tubules should not
always be assumed to be the result of toxicity or immaturity,
as single tubules or segmental/multifocal Sertoli only
tubules have been found in control animals in various rat
studies (Foley, 2001). In light of our data of both control
and E+ bulls exhibiting normal sperm morphology, it is
likely the observed alterations do not represent testicular
degeneration. One possible scenario for the difference in
the SC observation is that the earlier studies maintained
bulls on the E+ treatment for similar (Looper et al., 2009)
or longer time frames (Schuenemann et al., 2005b);
however, these bulls were maintained on forage, not fed a
concentrate ration. Forage concentrations of ergot alkaloids
vary throughout the season (Rogers et al., 2011), and it is
likely that consumption of the E+ seed in the concentrate
ration resulted in maintained and/or increased toxin levels
in our bulls compared with these studies.
A concern of all studies reported to date is that bulls
regularly pass the requirements of the BSE regardless
of exposure to E+ or E– tall fescue. Therefore, if the
observations of reduced bull fertility on E+ diets continue
to be repeated (Schuenemann et al., 2005a,b), the reduction
in the fertility of these males cannot or will not be detected
using standard BSE procedures. Furthermore, it has been
suggested in rodent models (Ross et al., 2004) and cattle
(J.G. Andrea, Clemson University, S.L. Pratt, Clemson
University, F.N. Schrick, University of Tennessee, and
M.G. Burns, Clemson University) that there is a significant
negative synergistic effect on pregnancy rates when both
the male and female are consuming E+ rations. Future
work verifying the negative effect of ergot alkaloids
on bull fertility, cow fertility, their putative negative
interactions, and how to best manage the male and female
for optimal pregnancy rates when grazing the tall fescue
cultivar Kentucky 31 is required.
Literature Cited
Aiken, G. E., B. H. Kirch, J. R. Strickland, L. P. Bush, M. L. Looper, and
F. N. Schrick. 2007. Hemodynamic responses of the caudal artery
to toxic tall fescue in beef heifers. J. Anim. Sci. 85:2337–2345.
Allen, V. G., and E. Segarra. 2001. Anti-quality components in forage: Overview, significance, and economic impact. J. Range
Manage. 54:409–412.
Almquist, J. O., and R. P. Amann. 1961. Reproductive capacity of
dairy bulls. II. Gonadal and extra-gonadal sperm reserves as determined by direct counts and depletion trials; dimensions and
weight of genitalia. J. Dairy Sci. 44:1668–1678.
Almquist, J. O., R. J. Branas, and K. A. Barber. 1976. Postpuberal
changes in semen production of Charolais bulls ejaculated at
high frequency and the relation between testicular measurements and sperm output. J. Anim. Sci. 42:670–676.
Bernard, J. K., A. B. Chestnut, B. H. Erickson, and F. M. Kelly. 1993.
Effects of prepartum consumption of endophyte-infested tall
fescue on serum prolactin and subsequent milk-production of
Holstein cows. J. Dairy Sci. 76:1928–1933.
Brito, L. F., A. E. Silva, R. T. Barbosa, M. M. Unanian, and J. P.
Kastelic. 2003. Effects of scrotal insulation on sperm production, semen quality, and testicular echotexture in Bos indicus
and Bos indicus × Bos taurus bulls. Anim. Reprod. Sci. 79:1–15.
Browning, R., Jr. 2000. Physiological responses of Brahman and
Hereford steers to an acute ergotamine challenge. J. Anim. Sci.
78:124–130.
Browning, R., Jr. 2004. Effects of endophyte-infected tall fescue on
indicators of thermal status and growth in Hereford and Senepol
steers. J. Anim. Sci. 82:634–643.
Browning, R., Jr., F. N. Thompson, J. L. Sartin, and M. L. LeiteBrowning. 1997. Plasma concentrations of prolactin, growth
hormone, and luteinizing hormone in steers administered ergotamine or ergonovine. J. Anim. Sci. 75:796–802.
Burke, J. M., R. W. Rorie, E. L. Piper, and W. G. Jackson. 2001. Reproductive responses to grazing endophyte-infected tall fescue
by postpartum beef cows. Theriogenology 56:357–369.
Coulter, G. H., and R. H. Foote. 1976. Relationship of testicular
weight to age and scrotal circumference of Holstein bulls. J.
Dairy Sci. 59:730–732.
Coulter, G. H., and D. G. Keller. 1982. Scrotal circumference of
young beef bulls: Relationship to paired testes weight, effect of
breed, and predictability. Can. J. Anim. Sci. 62:133–139.
Foley, G. L. 2001. Overview of male reproductive pathology. Toxicol. Pathol. 29:49–63.
Foote, A. P., D. L. Harmon, K. R. Brown, J. R. Strickland, K. R.
McLeod, L. P. Bush, and J. L. Klotz. 2012. Constriction of bovine vasculature caused by endophyte-infected tall fescue seed
extract is similar to pure ergovaline. J. Anim. Sci. 90:1603–1609.
Foote, A. P., D. L. Harmon, J. R. Strickland, L. P. Bush, and J. L.
Klotz. 2011. Effect of ergot alkaloids on contractility of bovine
right ruminal artery and vein. J. Anim. Sci. 89:2944–2949.
Gadberry, M. S., T. M. Denard, D. E. Spiers, and E. L. Piper. 2003.
Effects of feeding ergovaline on lamb performance in a heat
stress environment. J. Anim. Sci. 81:1538–1545.
3692
Stowe et al.
Gipson, T. A., D. W. Vogt, J. W. Massey, and M. R. Ellersieck. 1985.
Associations of scrotal circumference with semen traits in
young beef bulls. Theriogenology 24:217–225.
Gunter, S. A., and P. A. Beck. 2004. Novel endophyte-infected tall fescue for growing beef cattle. J. Anim. Sci. 82 (E-Suppl.):E75–82.
Hahn, J., R. H. Foote, and G. E. Seidel Jr. 1969. Testicular growth
and related sperm output in dairy bulls. J. Anim. Sci. 29:41–47.
Hoveland, C. S. 1993. Importance and economic-significance of the
Acremonium endophytes to performance of animals and grass
plant. Agric. Ecosyst. Environ. 44:3–12.
Johnson, J. M., G. E. Aiken, T. D. Phillips, M. Barrett, J. L. Klotz,
and F. N. Schrick. 2012. Steer and pasture responses for a novel
endophyte tall fescue developed for the upper transition zone. J.
Anim. Sci. 90:2402–2409.
Jones, K. L., S. S. King, K. E. Griswold, D. Cazac, and D. L. Cross.
2003. Domperidone can ameliorate deleterious reproductive effects and reduced weight gain associated with fescue toxicosis
in heifers. J. Anim. Sci. 81:2568–2574.
Jones, K. L., C. R. McCleary, S. S. King, G. A. Apgar, and K. E. Griswold. 2004. Consumption of toxic fescue impairs bull reproductive parameters. Prof. Anim. Sci. 20:437–442.
Killian, G. J., and R. P. Amann. 1972. Reproductive capacity of dairy
bulls. IX. Changes in reproductive organ weights and semen
characteristics of Holstein bulls during the first thirty weeks after puberty. J. Dairy Sci. 55:1631–1635.
Klotz, J. L., L. P. Bush, D. L. Smith, W. D. Shafer, L. L. Smith, B.
C. Arrington, and J. R. Strickland. 2007. Ergovaline-induced
vasoconstriction in an isolated bovine lateral saphenous vein
bioassay. J. Anim. Sci. 85:2330–2336.
Klotz, J. L., B. H. Kirch, G. E. Aiken, L. P. Bush, and J. R. Strickland.
2009. Bioaccumulation of ergovaline in bovine lateral saphenous veins in vitro. J. Anim. Sci. 87:2437–2447.
Lipham, L. B., F. N. Thompson, J. A. Stuedemann, and J. L. Sartin.
1989. Effects of metoclopramide on steers grazing endophyteinfected fescue. J. Anim. Sci. 67:1090–1097.
Looper, M. L., R. W. Rorie, C. N. Person, T. D. Lester, D. M. Hallford, G. E. Aiken, C. A. Roberts, G. E. Rottinghaus, and C. F.
Rosenkrans Jr. 2009. Influence of toxic endophyte-infected fescue on sperm characteristics and endocrine factors of yearling
Brahman-influenced bulls. J. Anim. Sci. 87:1184–1191.
NRC. 1996. Nutrient requirements of beef cattle. National Academy
Press, Washington, DC.
Porter, J. K., and F. N. Thompson Jr. 1992. Effects of fescue toxicosis
on reproduction in livestock. J. Anim. Sci. 70:1594–1603.
Rahman, M. B., L. Vandaele, T. Rijsselaere, D. Maes, M. Hoogewijs,
A. Frijters, J. Noordman, A. Granados, E. Dernelle, M. Shamsuddin, J. J. Parrish, and A. Van Soom. 2011. Scrotal insulation and its relationship to abnormal morphology, chromatin
protamination and nuclear shape of spermatozoa in HolsteinFriesian and Belgian Blue bulls. Theriogenology 76:1246–1257.
Rogers, W. M., C. A. Roberts, J. G. Andrae, D. K. Davis, G. E. Rottinghaus, N. S. Hill, R. L. Kallenbach, and D. E. Spiers. 2011.
Seasonal fluctuation of ergovaline and total ergot alkaloid concentrations in tall fescue regrowth. Crop Sci. 51:1291–1296.
Ross, M. K., W. D. Hohenboken, R. G. Saacke, and L. A. Kuehn. 2004.
Effects of feeding endophyte-infected fescue seed on reproductive traits of male mice divergently selected for resistance or susceptibility to fescue toxicosis. Theriogenology 61:651–662.
Samford-Grigsby, M. D., B. T. Larson, J. C. Forcherio, D. M. Lucas,
J. A. Paterson, and M. S. Kerley. 1997. Injection of a dopamine
antagonist into Holstein steers to relieve symptoms of fescue
toxicosis. J. Anim. Sci. 75:1026–1031.
Schoning, C., M. Flieger, and H. H. Pertz. 2001. Complex interaction of ergovaline with 5–HT2A, 5–HT1B/1D, and alpha1 receptors in isolated arteries of rat and guinea pig. J. Anim. Sci.
79:2202–2209.
Schuenemann, G. M., J. L. Edwards, M. D. Davis, H. E. Blackmon,
F. N. Scenna, N. R. Rohrbach, A. M. Saxton, H. S. Adair, F. M.
Hopkins, J. C. Waller, and F. N. Schrick. 2005a. Effects of administration of ergotamine tartrate on fertility of yearling beef
bulls. Theriogenology 63:1407–1418.
Schuenemann, G. M., J. L. Edwards, F. M. Hopkins, N. R. Rohrbach,
H. S. Adair, F. N. Scenna, J. C. Waller, J. W. Oliver, A. M. Saxton, and F. N. Schrick. 2005b. Fertility aspects in yearling beef
bulls grazing endophyte-infected tall fescue pastures. Reprod.
Fertil. Dev. 17:479–486.
Spiers, D. E., L. E. Wax, P. A. Eichen, G. E. Rottinghaus, T. J. Evans, D. H. Keisler, and M. R. Ellersieck. 2012. Use of different
levels of ground endophyte-infected tall fescue seed during heat
stress to separate characteristics of fescue toxicosis. J. Anim.
Sci. 90:3457–3467.
Spitzer, J. C., and F. M. Hopkins. 1997. Breeding soundness evaluation of yearling bulls. Vet Clin North Am Food Anim Pract.
13(2):295-304.
Strickland, J. R., M. L. Looper, J. C. Matthews, C. F. Rosenkrans Jr.,
M. D. Flythe, and K. R. Brown. 2011. Board-invited review: St.
Anthony’s Fire in livestock: Causes, mechanisms, and potential
solutions. J. Anim. Sci. 89:1603–1626.
Thompson, F. N., and J. K. Porter. 1990. Tall fescue toxicosis in
cattle: Could there be a public health problem here? Vet. Hum.
Toxicol. 32 (Suppl.):51–56, discussion 56–57.
Wagner, C. R., T. M. Howell, W. D. Hohenboken, and D. J. Blodgett.
2000. Impacts of an endophyte-infected fescue seed diet on
traits of mouse lines divergently selected for response to that
same diet. J. Anim. Sci. 78:1191–1198.
Watson, R. H., M. A. McCann, J. A. Parish, C. S. Hoveland, F. N.
Thompson, and J. H. Bouton. 2004. Productivity of cow-calf
pairs grazing tall fescue pastures infected with either the wildtype endophyte or a nonergot alkaloid-producing endophyte
strain, AR542. J. Anim. Sci. 82:3388–3393.