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Biology of Reproduction 65, 260-268 (2001)
© 2001 Society for the Study of Reproduction, Inc.

Regular Article

Interaction of Endophyte-Infected Fescue and Heat Stress on Ovarian Function in the Beef Heifer1

J.M. Burke2,a, D.E. Spiersb, F.N. Kojimab, G.A. Perryb, B.E. Salfenb, S.L. Woodb, D.J. Pattersonb, M.F. Smithb, M.C. Lucyb, W.G. Jacksona, and E.L. Piperc

a United States Department of Agriculture, Agricultural Research Service, Booneville, Arkansas 72927 b Department of Animal Science, University of Missouri, Columbia, Missouri 65211 c Department of Animal Science, University of Arkansas, Fayetteville, Arkansas 72701

ABSTRACT

The objective of the experiment was to examine the interaction of endophyte-infected tall fescue and environmental temperature on follicular and luteal development and function in beef heifers. Heifers were fed endophyte-free or endophyte-infected tall fescue seed at thermoneutral or heat stress temperatures (n = 6/treatment) 4 wk before and 3 wk after synchronized ovulation. All heifers were subjected to thermoneutral conditions (19°C, 50% relative humidity) from Days -7 to -2; temperature increased incrementally from Days -1 to 0 and cycled between 25°C and 31°C between Days 1 and 20 for heat-stressed heifers. Serum was collected and ovaries monitored every other day after induced luteolysis between Days 1 and 23 or until ovulation. Size and location of follicles >4 mm and corpora lutea were recorded. Serum concentrations of prolactin were reduced in heat-stressed heifers fed infected seed and both heat stress and infected seed decreased total cholesterol. Rectal temperature and respiration rate were greatest in heifers fed the infected seed when exposed to maximal temperatures. Heat stress led to reduced diameter of the corpus luteum and serum progesterone compared with thermoneutral conditions. Progesterone was reduced more so in heifers fed infected seed. The combination of infected seed and heat stress was associated with reduced diameter of the preovulatory dominant follicle, and consumption of infected seed led to fewer large follicles during the estrous cycle. Both stressors led to reduced serum estradiol. Impaired follicle function may explain reduced pregnancy rates commonly observed in heifers grazing infected tall fescue pasture.

corpus luteum function, environment, follicle, ovary, stress

INTRODUCTION

Grazing endophyte-infected tall fescue leads to negative responses in breeding livestock, such as decreased circulating prolactin, pregnancy and calving rates [1], impaired luteal function in heifers [2, 3], and delayed conception [4, 5]. Serum cholesterol was also reduced [6, 7], which may be important because it is the precursor to progesterone produced by the corpus luteum. In fact, progesterone production was reduced in heifers fed endophyte-infected fescue [2, 3], although this was prevented by high energy supplemental diets [2]. In addition, follicle number was decreased in beef heifers grazing endophyte-infected fescue [8, 9], as well as eCG-induced or GnRH agonist-induced estradiol production [8–10].

During summer months, when core body temperature is elevated [11–14], fescue toxicosis elicits its greatest effect on grazing animals. The effect of heat stress on reproduction in beef heifers affected by fescue toxicosis is not understood. Aside from the effects of endophyte-infected fescue on reproductive responses, heat stress may cause other problems, such as decreased pregnancy and conception rates [15, 16], and changes in follicular dynamics [12–14]. In an attempt to understand the interaction between heat stress and endophyte-infected fescue on reproductive responses during the estrous cycle, heifers in this study were exposed to thermoneutral temperatures or controlled heat stress while consuming endophyte-free or endophyte-infected fescue seed. Follicular and luteal dynamics were examined using ultrasound for a synchronized estrous cycle. Serum progesterone and estradiol were measured on days of ultrasound scanning.

MATERIALS AND METHODS

Animals and Treatments

All experimental procedures were reviewed and accepted by the Agricultural Research Service Animal Care and Use Committee in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals. Pain and stress to animals was minimized throughout the experimental period.

Twenty-four Angus or Angus x Hereford heifers between 10 and 18 mo of age, weighing approximately 350 kg, determined by ultrasound to have a corpus luteum, received either endophyte-free seed (EF) or endophyte-infected seed (EI) in a mixed feed ration and thermoneutral (TN) or heat stress (HS) temperatures resulting in four treatment combinations (EF-TN, EF-HS, EI-TN, and EI-HS; n = four Angus and two Angus x Hereford heifers per treatment). Dietary treatments were initiated 28 days before synchronized ovulation. In individual tie stalls inside the Brody Climatic Laboratory at the University of Missouri, all heifers underwent TN treatment (19°C, 50% relative humidity) from Days -7 to -2. For heifers in the HS treatment, temperature increased incrementally between Days -1 and 0 and cycled between 25°C and 31°C (minimum and maximum temperatures were maintained for a period of 4 h each day) from Days 1 to 20, whereas the TN-treated heifers remained at 19°C (Fig. 1). The laboratory contains a set of four identical environmental chambers with a capacity of six heifers per chamber. One heifer from the EF-TN group was removed because of aggressive behavior in the environmental chambers. Respiration rate and rectal temperature were measured daily at 0600 and 1600 h. Serum prolactin and total cholesterol were analyzed from blood collected on Day 17 (heifers were expected to be in luteal phase of estrous cycle) of the experiment to confirm toxicity from endophyte-infected fescue diet.



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  		FIG. 1. Experimental time line depicting dietary and heat stress treatment and estrus synchronization protocol. Diet of endophyte-free (EF) or endophyte-infected (EI) tall fescue seed began on Day -27 and ended on Day -20. Heifers were exposed to thermoneutral (TN) environmental chambers between Days -7 and -2. Temperature for heat-stressed (HS) heifers increased between Days -1 and 0 and were maximal (cycled between 25 and 31°C) between Days 1 and 20

Diet

EI tall fescue seed (Grande variety; Seed Research of Oregon, Corvallis, OR) contained 1.9 µg g-1 of ergovaline, and EF seed (Teton variety; Cascade International Seed Company, Aumsville, OR) contained 0 µg g-1 of ergovaline. Ergovaline concentration in seed was determined by high-performance liquid chromatography (HPLC) [17]. Heifers consumed a total mixed ration throughout the experiment (as a percentage of dry matter: 39.4% corn; 20.5% soybean hulls; 18.4% fescue seed; 10% cotton seed hulls; 4.5% soybean meal; 6% molasses; 0.25% trace mineralized salt; 0.25% salt; 0.6% limestone; 0.035% vitamins A, D, and E premix; and 0.025% vitamin E premix) and daily feed intake was measured. Initially, all heifers were fed 1.75% of body weight (on a dry-matter basis), which was formulated for a 0.68-kg gain day-1. However, because 30% of the heifers had lost weight after 19 days of feeding, heifers were then offered 2.5% of body weight of feed (dry matter basis). Once heifers entered the heat stress/thermoneutral period, feed offered to EF heifers was reduced to the average intake of EI heifers, as a percentage of body weight, from the previous day for TN and HS treatments, so that intake between diets was similar.

Estrus Synchronization and Reproductive Responses

Seven days after dietary treatment was initiated, melengestrol acetate (0.5 mg MGA-200 day-1; Pharmacia Inc., Kalamazoo, MI) was fed for 7 days. An injection of PGF2{alpha} (25 mg lutalyse i.m.; Pharmacia Inc.) was administered on the last day of MGA feeding followed by injections of GnRH (100 µg cystorelin i.m.; Rhone Merieux Inc., Athens, GA) 4 days and PGF2{alpha} 11 days later ([18]; Fig. 1). Ovaries were monitored by transrectal ultrasonography (Aloka SSD 500V ultrasound scanner equipped with a 7.5 MHz linear array transrectal transducer; Aloka Co. Ltd, Japan) on each Monday, Wednesday, and Friday beginning on Day -2 and daily from Days 17 to 23 or until ovulation (Day 0 = day of expected ovulation; Fig. 1). The size and number of ovarian follicles >4 mm, their position, and position and size of corpora lutea were recorded. Ovulation was determined by the disappearance of the largest follicle and subsequent development of a corpus luteum in the respective location on the ovary. Blood was collected for serum concentrations of progesterone and estradiol on days of ultrasound scanning and daily from Days 17 to 23 or until ovulation. In addition, serum concentrations of progesterone were determined on the day of GnRH and second PGF2{alpha} treatment (Days -10 and -3, respectively, relative to the day of experiment).

Two heifers (one EF-TN, one EI-TN) were not included in analyses of reproduction responses because they were acyclic (serum concentrations of progesterone were <1 ng ml-1 on days measured throughout the study).

Assays

Blood was collected from a coccygeal vessel on days of ultrasound monitoring. Samples were allowed to clot at room temperature (outside of chambers) for 60 min and then were centrifuged (3000 x g for 20 min at 4°C). Serum was collected and stored at -20°C until analyzed. Serum concentrations of prolactin were determined in a single assay, using a modification of Henson et al. [19]. The intraassay coefficient of variation (CV) was 16.8%. Serum concentrations of total cholesterol were analyzed in a single assay by the procedure of Wybenga et al. [20]. The intraassay CV was 1.9%.

Serum concentrations of progesterone run in a single assay (Coat-A-Count Progesterone; Diagnostic Products Corp., Los Angeles, CA, validated by Srikandakumar et al. [21]) and estradiol [22] were determined from blood collected after ultrasonography. The intraassay CV for progesterone was 9.8% and intraassay and interassay CVs for estradiol were 3.4 and 8.5%, respectively.

Statistical Analysis

Data were analyzed by least squares ANOVA and mixed models procedures of the Statistical Analysis System [23]. The experiment was designed as a 2 x 2 factorial repeated measures with diet and environmental temperature as the main effects. The mathematical model that was used to analyze respiration rate, rectal temperature, and feed intake included the following: diet, temperature and breed, the interactions of diet by temperature, diet by breed, temperature by breed, and diet by temperature by breed and heifer within diet by temperature by breed as the error term. Day and time (0600 h vs. 1600 h) were repeated effects. The model for serum concentrations of prolactin and total cholesterol included diet, temperature, breed, and their interactions. Regression analysis [23] was used to determine whether treatments affected the relationship between a response variable (respiration rate, rectal temperature, feed intake) and day of experiment to the order of significance [24]. These models were adjusted for the appropriate independent variables described previously.

Four heifers (two EF-HS; one EI-TN; one EI-HS) did not respond to synchronization and ovulated between Days 9 and 16. All but three of the heifers that did synchronize ovulated between Days 18 and 22. The remaining three heifers (two EF-HS; one EF-TN) had not ovulated by Day 22, but the uterus had estrus tone. Therefore, analysis of reproduction responses considered 1) day of experiment (Fig. 1), as well as 2) days before final ovulation as Day 1 for all heifers. Further, because day of final ovulation was determined retrospectively, there were missing heifer-day cells for the latter. Heterogeneity of regression [23] was used to examine treatment effects on the relationship between response variables (number or diameter of follicles or corpora lutea and serum concentrations of progesterone or estradiol) and days before ovulation (determined retrospectively) or day of experiment (Days 0 until ovulation; [24]). These models were adjusted for the appropriate independent variables described previously. For the analysis with days before ovulation as the covariate, data included up to Day 21 to Day 1 for diameter of the corpus luteum, serum concentrations of progesterone, and numbers of medium and large follicles. Because we were interested in increasing serum concentrations of estradiol in the presence of the preovulatory follicle, Days 10 to 1 were included for estradiol and preovulatory follicle diameter analyses when days before ovulation was the covariate. Heterogeneity of regression and mixed model analyses as described previously were performed for reproductive responses after removal of two EI-HS heifers with aberrant cycles to compare responses with and without these animals.

RESULTS

Feed intake was reduced under HS conditions (P < 0.001; Fig. 2). Respiration rate and rectal temperature were similar among treatments before heat stress was imposed. Respiration rate increased for heifers consuming EI diets under heat stress conditions (diet x temperature x day x time [0600 vs. 1600 h], P < 0.001; Fig. 3, A and B). By the end of the experiment, respiration rate was similar between dietary treatments for both TN and HS heifer groups. Rectal temperature increased in HS heifers exposed to EI relative to EF diets at 0600 and 1600 h (diet x temperature x day x time, P < 0.001; Fig. 3, C and D). Serum concentrations of prolactin were reduced in EI-treated heifers under HS, but not TN conditions (diet x temperature, P < 0.003; Table 1). Both EI diet and HS treatment led to a reduction in serum concentrations of total cholesterol (diet, P < 0.04; temperature, P < 0.003; Table 1).



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  		FIG. 2. Feed intake (kg d-1) for heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 5) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 6) or heat-stressed temperatures (black squares, EI-HS; n = 6). The least squares means are presented for each day from Days -6 to 20 and with an estimated standard error of 0.64 kg d-1. Heat stress conditions were initiated on Day -1 as arrow indicates



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  		FIG. 3. Respiration rate (breaths/min-1) and rectal temperature (°C) determined at 0600 h (A, C) and 1600 h (B, D) for heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 5) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 6) or heat-stressed temperatures (black squares, EI-HS; n = 6). The least squares means (± SEM) are presented for each day from Days -6 to 20. Heat stress conditions were initiated on Day -1 as arrow indicates


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  		TABLE 1. Mean serum concentrations of prolactin and total cholesterol in beef heifers fed endophyte-free or endophyte-infected fescue seed diets and exposed to thermoneutral or heat stress conditions

There was no effect of diet on diameter of the corpus luteum, but diameter was reduced in HS heifers (x = day before ovulation: temperature x day, P < 0.07, R2model = 0.13, Fig. 4A; x = day of experiment: temperature x day, P < 0.05, R2model = 0.15; least squares means: temperature x day, P = 0.33, Fig. 4B). Similarly, serum progesterone was reduced in HS heifers and to a greater extent in EI-HS heifers (x = days before final ovulation: diet x temperature x day, P < 0.004, R2model = 0.34, Fig. 5A; x = day of experiment: diet x temperature x day, P < 0.004, R2model = 0.22, Fig. 5B; least squares means: diet x day, P < 0.08, Fig. 5C).



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  		FIG. 4. Diameter of the corpus luteum for heifers at thermoneutral (open triangles, TN; n = 9) or heat stress temperatures (black stars, HS; n = 12) analyzed by heterogeneity of regression with predicted values presented for each day before final ovulation (A) or mixed models procedure with least squares means presented for each day before final ovulation and an estimated standard error for dietary and temperature treatment of 2.8 mm (B)



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  		FIG. 5. Serum concentrations of progesterone for heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 4) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 5) or heat-stressed temperatures (black squares, EI-HS; n = 6). Regression lines are presented for each treatment from Days -19 to -1 relative to day of final ovulation (A) or for each day of experiment (B) with predicted values presented for each day. Serum progesterone expressed as least squares means for each day of experiment for all cyclic heifers with an estimated standard error of 0.88 ng ml-1 (C) and with two heifers with aberrant cycles removed with an estimated standard error of 0.99 ng ml-1 (D)

Serum concentrations of progesterone were below the detection level during the experimental estrous cycle in two of six EI-HS heifers for all but one sample (1.5 ng ml-1 in the early luteal phase) and each had a corpus luteum that appeared normal by ultrasound examination. Because serum concentrations of progesterone were greater than 1 ng ml-1 for one of two samples collected 7 days apart before heat stress conditions were initiated and characteristics of the preovulatory follicle and serum estradiol appeared normal, these heifers were considered cyclic. However, data were analyzed with and without these animals for reproductive responses. Serum concentrations of progesterone were not different among treatments when these heifers were removed (regression: diet x temperature x day, P = 0.16; mixed models: diet x temperature x day, P = 0.66, Fig. 5D). One heifer, interestingly, ovulated between Days 18 and 20 of the study (Day 0 was the day of expected ovulation) and the other heifer had not ovulated by Day 22.

The diameter of the preovulatory dominant follicle was reduced in EI-HS heifers relative to other treatments (x = days before ovulation: diet x temperature, P < 0.008, R2model = 0.52, Fig. 6A; x = day of experiment: diet x temperature, P = 0.11, R2model = 0.22; least squares means: diet x temperature, P = 0.27, temperature, P = 0.08, Fig. 6B). Heat stress led to decreased serum concentrations of estradiol and under TN conditions, estradiol was reduced for EI-treated compared with EF-treated heifers (x = days before final ovulation: diet x temperature x day, P < 0.01, R2model = 0.28, Fig. 7A; least squares means: diet x day, P < 0.05, Fig. 7B; x = day of experiment: diet x temperature x day, P < 0.001, R2model = 0.17, Fig. 7C; least squares means: temperature x day, P < 0.001, Fig. 7D). Serum concentrations of estradiol for the two heifers with negligible progesterone in the blood ranged between 0.8 and 3.1 pg ml-1 and 1.9 and 2.2 pg ml-1, similar to that of other EI or HS heifers. After these heifers were removed from the data, the diameter of the preovulatory dominant follicle was not different among treatments (Fig. 8A). However, serum concentrations of estradiol were still decreased for stressed heifers (x = days before final ovulation: diet x temperature x day, P < 0.005, R2model = 0.32; least squares means: diet x day, P < 0.003, Fig. 8B; x = day of experiment: diet x temperature x day, P < 0.001, R2model = 0.18). The number of large follicles was reduced in heifers that consumed EI diets whether or not the two heifers with negligible progesterone concentrations were removed from data (x = day before final ovulation with all cyclic heifers: P < 0.07, R2model = 0.05, Fig. 9A; least squares means: diet x day, P < 0.02, temperature x day, P < 0.04, Fig. 9B; x = day of experiment: P < 0.04, R2model = 0.12; x = day before final ovulation with two heifers removed: P < 0.05, R2model = 0.15; least squares means with two heifers removed: P > 0.10, Fig. 9C), but large follicle numbers were not altered by heat stress. Diet or temperature did not affect number of medium follicles during monitored estrous cycle.



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  		FIG. 6. Diameter of the preovulatory dominant follicle analyzed by heterogeneity of regression with regression line presented for each treatment from Days -10 to -1 relative to day of final ovulation and predicted values presented for each day (A). Diameter of the preovulatory dominant follicle analyzed by mixed models procedure with least squares means presented for each day before final ovulation and an estimated standard error of 1.4 mm (B) for heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 4) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 5) or heat-stressed temperatures (black squares, EI-HS; n = 6)



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  		FIG. 7. Serum concentrations of estradiol analyzed by heterogeneity of regression (A, C) with regression line (predicted values presented for each day) for each treatment from Days -10 to -1 relative to day of final ovulation (A) or for each experimental day (C). Serum concentrations of estradiol analyzed by mixed models procedure (B, D) with least squares means presented for each day before final ovulation and an estimated standard error of 1.1 pg ml-1 (B) or for each experimental day with an estimated standard error of 0.9 pg ml-1. Treatments include heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 4) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 5) or heat-stressed environment (black squares, EI-HS; n = 6)



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  		FIG. 8. Diameter of the preovulatory dominant follicle (A) and serum concentrations of estradiol (B) with least squares means presented for each day before final ovulation for heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 4) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 5) or heat-stressed environment (black squares, EI-HS; n = 4). Heifers with aberrant cycles were removed from data analysis. Estimated standard errors are 1.48 mm and 1.01 pg ml-1, respectively



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  		FIG. 9. Number of large follicles for heifers consuming endophyte-free seed diet (open triangles, EF; n = 10) or endophyte-infected seed diet (black hexagons, EI; n = 12; A). Regression lines are presented for each dietary treatment from Days -21 to -1 relative to day of final ovulation with predicted diameter presented for each day. Numbers of large follicles analyzed by mixed models procedure for heifers consuming endophyte-free seed diet at thermoneutral (open circles, EF-TN; n = 4) or heat-stressed environment (open squares, EF-HS; n = 6) and endophyte-infected seed diet at thermoneutral (black circles, EI-TN; n = 5), or heat-stressed environment (black squares, EI-HS; n = 6); least squares means are presented for each day before final ovulation with an estimated standard error of 0.41 mm for all cycling heifers (B) and 0.41 mm for heifers with aberrant cycles removed (C)

DISCUSSION

By reducing the intake of EF-HS treated heifers to that of EI-HS treated heifers, the effects of decreased intake typically observed for endophyte-infected fescue-fed animals [25, 26] were minimized in the current study. Daily feed consumption by cattle is approximately 2–3% of body weight. The concentration of ergovaline, an indicator of endophyte infection, in endophyte-infected tall fescue seed and forage ranges from 0.1 to 6.0 µg g-1 [27–29]. Based on a 350-kg heifer consuming 1.75% of body weight, a normal range of ergovaline consumption would be 1.75–105 µg kg-1 of body weight per day. In the current study, heifers that weighed 350 kg and fed endophyte-infected fescue diets received 6.1 (feed intake at 1.75% body weight) to 8.7 (feed intake at 2.5% body weight) µg kg-1 body weight of ergovaline per day. Mizinga et al. [30] administered 2.6–9.75 µg ergovaline kg-1 body weight per day to 338-kg heifers by feeding endophyte-infected fescue seed during the months of April and May, before animals likely were heat stressed, and observed no difference in serum prolactin between these heifers and those fed endophyte-free fescue seed. However, serum prolactin decreased in endophyte-infected, fescue-treated heifers after ergovaline administration was increased above 9.75 µg kg-1 body weight. Although we would have liked to have administered a higher dose of ergovaline through diet in the current study, greater than 19% seed in the ration may have reduced intake or palatability for all heifers. It was not surprising then that serum concentrations of prolactin in the current study were not different between endophyte-free and endophyte-infected, fescue-fed cows at thermoneutral conditions. In contrast, concentrations of prolactin were reduced in endophyte-infected, fescue-fed heifers under heat stress conditions. Similarly, other signs of fescue toxicosis were present in endophyte-infected, fescue-fed cows only under heat stress conditions. Rectal temperature and respiration rate increased in endophyte-infected fescue-fed heifers under heat stress conditions. These observations correspond with that of Hemken et al. [25] who observed an increase in rectal temperature and respiration rate in steers fed endophyte-infected tall fescue under heat stress conditions, but not cooler temperatures. Interestingly, heat-stressed heifers may have adjusted to the effects of the endophyte-infected fescue in the diet, as evidenced by similar respiration rate between dietary groups of heifers by Day 20 of the study.

The greatest decrease in serum concentrations of progesterone occurred in heifers fed the endophyte-infected fescue under heat stress conditions, although heifers with aberrant cycles may have contributed to this. Others reported a decrease in circulating progesterone in heifers fed endophyte-infected fescue [2, 3]. A decrease in total cholesterol in the blood can lead to decreased progesterone [31, 32]. In ruminants, the cholesterol used in steroidogenesis by the corpus luteum is derived from serum low-density lipoproteins, high-density lipoproteins, or both [33–35]. In the current study, there was indeed a decrease in serum concentrations of total cholesterol in endophyte-infected, fescue-fed heifers, as others have observed [5–7], which may have led to decreased steroidogenesis.

There was a greater frequency of heat-stressed, endophyte-infected fescue-fed heifers observed with dysfunctional corpora lutea (a corpus luteum that failed to produce progesterone) in the present study. Similarly, others reported a greater frequency of dysfunctional corpora lutea in heifers grazing endophyte-infected fescue pastures [2, 3, 36]. Development of the corpus luteum appears normal, but function may be impaired in endophyte-infected fescue-fed animals. In the two endophyte-infected fescue-treated heifers with undetectable concentrations of progesterone, circulating estradiol was not increased and the life span of the dominant follicle appeared normal. This is surprising, because typically, in the presence of low progesterone, circulating estradiol increases relative to that of cows with normal luteal function [37]. This may suggest altered hormonal feedback mechanisms between the ovary and the hypothalamus and or pituitary. In addition, circulating concentrations of LH may be reduced in endophyte-infected fescue-treated cows [38], which in turn, could lead to decreased luteal function. On the other hand, others reported no changes in LH concentration in heifers or cows exposed to endophyte-infected fescue [30, 39], but the concentration of ergovaline administered to these animals in these studies may not have been great enough to observe a change in LH activity.

There appeared to be an earlier rise in serum progesterone in both thermoneutral and heat-stressed heifers exposed to endophyte-infected fescue seed, although heifers that did not respond to estrus synchronization may have contributed to this anomaly. Similarly, production of progesterone may have ceased earlier in heat-stressed heifers fed infected fescue seed, even after heifers with aberrant cycles were removed from data set. In addition, in the presence of the preovulatory follicle, estradiol production of infected fescue-fed heifers may peak and then decline at least 1 day after that of endophyte-free fescue-fed heifers. There have been no other reports, to the authors' knowledge, of potential reproductive hormonal asynchrony in association with endophyte-infected fescue.

In the thermoneutral environment, preovulatory serum estradiol was decreased in endophyte-infected fescue-fed heifers in the present study, in agreement with McKenzie and Erickson [8] and McLane et al. [10]. Similarly, estradiol also was decreased in heat-stressed heifers. However, endophyte-infected fescue seed did not lead to a further decrease in estradiol under heat stress conditions, suggesting that the two stressors were not additive to follicular function. During chronic [40] or acute heat stress [13, 14, 40], follicular or serum estradiol production was reduced relative to thermoneutral conditions. Decreased estradiol production may have been due to impaired follicle growth in endophyte-infected fescue-fed heifers in the current study as evidenced by decreased diameter and number of large follicles, which agrees with McKenzie and Erickson [8, 9]. Others reported no changes in follicle diameter or number of large follicles in heifers fed ergotamine [41], but these heifers were not exposed to the combination of ergot alkaloids present in endophyte-infected fescue. Consistent with Seals et al. [41], there was no observed change in medium follicle numbers in heifers fed endophyte-infected fescue seed (current study) or ergotamine vs. control diet.

Beef heifers and cows are typically bred during late spring and early summer months, often on fescue-based pastures in the southeastern and midwestern United States. Lower fertility in heifers that graze endophyte-infected fescue could be explained by decreased luteal function resulting in early embryonic loss, which has been observed in sheep [5]. Alternatively, there could be an asynchrony of reproductive hormones between the dam and the conceptus as evidenced by the earlier rise in serum progesterone and delayed rise in estradiol production in endophyte-infected fescue-fed heifers in the current study. Altered follicular function occurs when heifers are heat-stressed and exposed to endophyte-infected fescue, which contributes to poorer fertility. The inability to regulate body temperature, triggered by fescue toxicosis, predisposes the animal to heat stress, which by itself, is associated with reduced conception rates.

Lack of a negative response of endophyte-infected fescue-fed heifers under thermoneutral conditions, with the exception of decreased circulating estradiol, indicates that signs of fescue toxicosis are certainly less severe when heifers are not heat stressed. This may explain lack of consistent results to treatment with endophyte-infected fescue as reported in the literature. Some researchers reported no decrease in reproduction responses in association with endophyte-infected fescue (similar conception rates [42], increased progesterone [43], similar pregnancy rates; unpublished data). This strongly suggests that optimal conditions to breed heifers grazing endophyte-infected fescue pastures would be in the absence of heat stress. The level of heat stress that induces signs of fescue toxicosis leading to decreased fertility warrants further investigation.

ACKNOWLEDGMENTS

The authors thank J. Cherry, G. Robson, and M. Leonard for technical assistance; and D. Jones, T. Preston, J. Bader, and University of Missouri student aid for help with handling animals. Thanks to T. Popham for statistical advice, G. Rottinghaus for ergovaline analysis, and K. Coffey for ration formulation. Appreciation is extended to Pharmacia Inc. for supplying Lutalyse and MGA-200.

FOOTNOTES

First decision: 29 December 2000.

1 Mention of trade names or commercial products in this manuscript is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. Back

2 Correspondence: J.M. Burke, 6883 South State Highway 23, Booneville, AR 72927. FAX: 501 675 2940; jmburke{at}spa.ars.usda.gov Back

Accepted: March 1, 2001.

Received: December 4, 2000.

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