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Effects of feeding ergovaline on lamb performance in a heat stress environment

M. S. Gadberry^*, T. M. Denard, D. E. Spiers and E. L. Piper^,1

^* University of Arkansas, Cooperative Extension Service, Little Rock 72203; and Department of Animal Science, University of Arkansas, Fayetteville 72701; and and Department of Animal Science, University of Missouri, Columbia 65211

¹ Correspondence:
AFLS B114 (phone: 501-750-4410; fax: 479-575-7294; E-mail:
epiper{at}uark.edu).

	Abstract

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Lambs exposed to a heat-stressed environment (33°C, 50% relative humidity) were used in three experiments to determine whether ergovaline (EV) is the primary toxin involved in fescue toxicosis. The first study evaluated the effects of feeding diets containing increasing levels of endophyte-infected tall fescue seed (E+) and decreasing levels of endophyte-free tall fescue seed (E-). The second and third study evaluated the response to a diet that contained synthetic EV added to an E- diet and the response to a diet containing endophyte-infected ryegrass seed (R+) with an elevated concentration of EV. In Exp. 1, lambs were fed diets of: 1) 10% E- and 0% E+, 2) 5% E- and 5% E+, or 3) 0% E- and 10% E+. Increasing the percentage of E+ in the diet resulted in a linear decrease (P < 0.01) in feed intake (as-fed basis), skin temperature, thermocirculation index (TCI), and serum prolactin. Body weight gain also decreased (P < 0.06). Respiratory rate and core body temperature were not affected by the 5 or 10% E+ diets. In Exp. 2, lambs were fed diets that contained: 1) 10% E-, 2) 10% E- with synthetic EV added at a level equivalent to the 10% E+ diet, or 3) 10% E+. Feed intake (as-fed basis), body weight gain, and skin temperature did not differ for lambs fed the E- and EV diets. The EV diet elicited a decrease (P < 0.05) in TCI and prolactin compared with the E- diet. The TCI for lambs fed EV did not differ (P > 0.10) from the E+ lambs; however, serum prolactin was lower (P < 0.05) for lambs on the E+ diet than for those fed EV. Core body temperature was not affected (P > 0.10) by feeding EV or E+ fescue seed in Exp. 2. In Exp. 3, lambs were fed diets that contained: 1) 10% E-, 2) 3.24% R+ and 6.76% E-, which added an equivalent amount of EV to E+ diets but reduced concentrations of other ergot alkaloids, or 3) 10% E+. Lambs fed the E+ diet and maintained at 33°C had lowered feed intake (as-fed basis), skin temperature, and TCI compared with lambs fed the E- or R+ diets (P < 0.05). Lambs fed the E+ diet had increased rectal temperatures and lowered serum prolactin compared with lambs on the R+ diet (P < 0.05). Lambs on the R+ diet had a greater rectal temperature and lower serum prolactin than lambs on the E- diet (P < 0.05). These results suggest that EV is a fescue toxin; however, other alkaloids might work synergistically with EV, causing the full expression of fescue toxicosis.

Key Words: Alkaloids • Festuca arundinacea • Lambs • Toxicity

	Introduction

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Livestock that graze endophyte (Neotyphodium coenophialum)-infected (Glenn et al., 1996) tall fescue (Festuca arundinacea) develop symptoms collectively known as fescue toxicosis (Stuedemann and Hoveland, 1988). The toxicosis is caused by alkaloids produced in endophyte-infected tall fescue swards (Porter, 1995). Ergovaline (EV), the primary ergopeptine alkaloid, and other ergot alkaloids (Lyons et al., 1986), are found in endophyte-infected fescue.

The effects of pure EV isolated from tall fescue seed on performance has been studied by injecting the compound into animals (McCollough et al., 1994; Spiers et al., 1995) and by in vitro techniques (Denard et al., 1994;Strickland et al., 1994;Larson et al., 1995; HREF="#LARSON-ETAL-1999">1999). Results from these studies support the hypothesis that EV contributes to fescue toxicosis. Garner et al. (1993) likewise noted that EV is a fescue toxin, and concluded that trials in which purified EV is fed must be conducted to determine the role EV and other alkaloids in the production of symptoms associated with fescue toxicosis.

The objectives of the following studies were: 1) to evaluate the symptoms of fescue toxicosis expressed by heat-stressed lambs fed increasing levels of endophyte-infected fescue seed (E+), and 2) to reveal the role of EV as a fescue toxin by feeding a diet that contained either synthesized EV (F. Smith, Auburn University) or endophyte-infected ryegrass seed (R+) (Ag Research, Ruakura, New Zealand) with high concentrations of EV and reduced concentrations of other ergot alkaloids.

	Materials and Methods

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All experiments were approved by and followed the guidelines of the Animal Care and Use Committee at each institution.

Experiment 1
The purpose of Exp. 1 was to evaluate the physiological responses of lambs to diets containing increasing levels of E+ seed. Twenty-four Rambouillet wethers (21 ± 2.0 kg) were randomly assigned to one of three diets. Diets included 10% endophyte-free fescue seed (E-) (cultivar Trophy, MFA Inc., Rogers, AR), 5% E- plus 5% E+ (cultivar SR8200, Seed Research of Oregon, Inc., Corvallis, OR), or 10% E+ seed (Table 1). Dietary ingredients in this study were similar to those used by Debessai et al. (1993). Debessai et al. (1993) reported decreases in lamb performance with diets containing E+ tall fescue seed at a minimal level of 10%. Analysis by HPLC determined the E- seed had no detectable level of EV, and that the E+ seed contained 6.4 ppm of combined EV and ergovalinine. Therefore, the calculated concentrations for the E-, 5% E+, and 10% E+ diets were 0, 320, and 640 ppb, respectively. The E- and E+ fescue seed lots were tested for ergot (Claviceps purpureum) contamination by HPLC analysis of the ergot alkaloids: ergotamine, ergosine, and ergocryptine. No ergot contamination was detected. Visual examination of seed samples also revealed no ergot bodies.

All lambs were given ad libitum access to feed and water, housed in individual pens (1.2 m x 1.2 m), and subjected to 14 h of light and 10 h of dark within a single chamber. The chamber temperature was maintained at 21°C, 60% relative humidity from d 0 to d 5. At 1030 on d 5, 6, 7, and 8, the room temperature was raised to 24, 28, 31, and 33°C, respectively. The chambers remained at 33°C and 50% relative humidity through d 14.

Core body temperature was collected every 30 min on each animal from d 0 to 15. Skin temperature (Ts) of the medial area of the caudal side of the ear and room temperature (Ta) were measured at 900, 1400, and 1900 daily. Skin temperature was measured using an Everest infrared thermometer (Everest Interscience, Inc., Tucson, AZ). Skin temperature, Tco, and Ta were used to calculate the thermocirculation index (TCI), defined as TCI = (Ts - Ta)/(Tco - Ts) (Burton and Edholm, 1955). The steady-state condition required for this calculation was used throughout the study.

Lambs were weighed on d 14, and blood was sampled for prolactin analysis. Room temperature was returned to 21°C, and lambs were taken off food and water 12 h before d 15. Temperature transmitters were removed from lambs on d 15.

Failure to recover from surgeries resulted in one lamb being removed from the 5% E+ treatment in trial one and one lamb being removed from the 0% E+ treatment in trial two.

Experiment 2
Experiment 2 was conducted to determine if lambs fed a diet containing synthetic EV would exhibit fescue toxicosis symptoms similar to those of lambs fed a diet containing E+ seed. Twenty-four Rambouillet lambs (21.5 ± 2.6 kg) were used in the experiment. The diets in Exp. 2 consisted of the following: 1) 10% E- fescue seed diet, 2) a 10% E- fescue seed diet containing pure EV (EV diet), and 3) a 10% E+ fescue seed diet. The EV diet consisted of the 10% E- fescue seed diet with added EV obtained from F. Smith, Auburn University. Soybean meal was used as a carrier for EV in the EV diet. Ergovaline (58.7 mg) was dissolved in 350 mL of acetone, and then dried onto 300 g of soybean meal via rotary evaporation. The calculated concentration of EV in the EV diet was 645 ppb. The soybean meal-ergovaline mix was spread on a tray and placed in the dark at room temperature until no odor of acetone was detected. A similar amount of acetone–washed soybean meal, which contained no EV, was substituted for nonwashed soybean meal in the E- and E+ fescue seed diets.

As in the first experiment, two trials were conducted with 12 lambs per trial. All procedures in Exp. 2 were the same as those in Exp. 1. Due to battery failure of temperature transmitters, Tco data was missing from one lamb on the EV diet in trial one, one lamb on the 0% E+ diet, and one lamb on the EV diet in trial two.

Experiment 3
Experiment 3 was conducted to determine if a diet containing R+ seed, formulated to contain a level of EV similar to a diet containing E+ fescue seed, would elicit responses similar to those from the diet containing E+ seed. Twenty-four black-faced, crossbred lambs (25.0 ± 1.8 kg) were randomly assigned to two trials with three replicated treatments per trial.

Treatment diets contained: 1) E- fescue seed, 2) E- seed plus R+ seed, or 3) E+ seed. The diets were formulated in a manner similar to that of the previous experiments.

The E+ tall fescue seed contained 5.2 ppm of EV and ergovalinine, and no alkaloids were detected in the E- tall fescue seed. Both lots of seed were obtained from the same sources cited in Exp. 1. The ryegrass seed, obtained from Ag Research, contained 16.1 ppm of EV plus ergovalinine.

The predicted composition of EV in the E+ fescue seed diet was 520 ppb. The R+ seed diet required mixing 32.4 parts ryegrass seed with 67.6 parts E- fescue seed. The mixture resulted in a final EV concentration of 520 ppb while maintaining a 10% grass seed content of the endophyte-infected ryegrass diet.

Lambs were adapted to the seed diets by feeding the E- diet for 4 d before entering the environmental chamber (d 1). After an overnight fast without water, the lambs were weighed and moved to the environmental chambers. Lambs were started on the experimental diets and maintained at 21°C, 60% relative humidity to d 4. On d 4, 5, 6, and 7, chamber Ta was raised to 24, 28, 31, and 33°C, 50% relative humidity, and maintained until d 14. Unlike Exp. 1 and 2, temperature transmitters were not implanted, and rectal temperature (Tr) and infrared skin temperatures were measured twice daily at 1400 and 1900 on d 8 to 12 with model 450 and model OS-610 thermometers (Omega Engineering, Stamford, CT). Daily feed intake was measured, and lambs were maintained on a lighting regime similar to Exp. 1. On d 14, the lambs were weighed, a blood sample was drawn from the jugular, and serum was frozen for prolactin, enzyme, and lipid analyses.

Serum Analysis
Serum prolactin was analyzed by RIA (Henson et al., 1987). Intra- and interassay CV were 10.83 and 13.83%, respectively. In Exp. 3, assays for serum alkaline phosphatase (AP), aspartic transaminase (AST), lactate dehydrogenase (LDH), cholesterol, and triglycerides were measured on a Ciba-Corning model 550 Express (Oberlin, Ohio).

Alkaloid Analysis
Fescue seed samples were analyzed for EV and ergovalinine concentration using an Isco model 2360 HPLC gradient programmer and an Isco model 2350 HPLC pump (Isco, Inc., Lincoln, NE) connected to a Shimadzu RF-550 fluorescence detector (Shimadzu Corp., Kyoto, Japan). A tertiary gradient delivered the mobile phase, which consisted of acetonitrile, 2.1 mM ammonium carbonate, and 1:1 methanol/water (Moubarak et al., 1993). Samples were separated on a Perkin Elmer 3.3-cm CR18 column (Perkin Elmer, Norwalk, CT). Seed samples (0.5 g), were extracted by shaking in 10 mL of methanol for 30 min and soaking overnight, followed by a second 30-min shake, filtration, and analysis. Lysergic acid (ergine) concentrations were measured by HPLC, and total ergot alkaloids were estimated by an ELISA procedure (Hill and Agee, 1994) in seed samples from Exp. 3.

Statistical Analysis
A randomized experimental design was used for all experiments. Body temperature data was analyzed from d 9 to 14 for Exp. 1 and 2, and from d 8 to 12 for Exp. 3, when Ta was held constant at 33°C. Feed intake is reported for d 9 to 14 in Exp. 1 and 2, and for d 3 to 6 and d 7 to 14 in Exp. 3. Respiratory rates are reported only for the heat stress period. The univariate approach to repeated-measures ANOVA using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC) was used to test treatment effects on average daily Tco (Exp. 1 and 2) or Tr (Exp. 3), feed intake, Ts, and TCI. Diet, trial, and diet x trial interaction effects were tested using the mean square for lamb within diet x trial. Day and diet x day effects were tested using the residual mean square. Orthogonal contrasts were used to determine linear effects of diet in Exp. 1. Weight change and serum prolactin concentration were analyzed for diet, trial, and diet x trial interaction effects using the residual mean square for the error term. Since weights were taken at the beginning and end of the study, and blood samples were taken at the end of the study, the reported values represent the overall effect (with and without heat stress). Least squares means were generated for all studies and are reported throughout.

	Results and Discussion

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Experiment 1
Feed intake of lambs decreased linearly (P < 0.01) as the percentage of E+ seed in the diet increased (Table 2). Fiorito et al. (1991), Rhodes et al. (1991), and Aldrich et al. (1993) also reported decreases in feed intake of lambs consuming an E+ diet. Weight gain tended to decrease (P = 0.06) as the level of E+ in the diet increased. Although initial body weight did not differ between trials (P = 0.62), a significant trial effect existed for weight gain. Lambs in trial one gained more weight than lambs in trial two; however, weight loss due to the E+ seed showed the same trends in both trials.

Skin temperature and TCI decreased linearly (P < 0.01) with increasing levels of E+ fescue seed in the diet. The TCI was developed by Burton and Edholm (1955) to identify a steady-state difference in vasomotor tone that is associated with peripheral heat transfer. Decreases in both Ts and TCI indicated that feeding E+ caused peripheral vasoconstriction in lambs. Rhodes et al. (1991) reported a decrease in blood flow to skin covering the inner hind leg in lambs and skin covering the ribs in steers. Aldrich et al. (1993) recognized a reduction in skin temperature over the ribs of lambs, and Osborn et al. (1992) reported that E+ fescue caused a lowering of peripheral temperatures in cattle.

A linear reduction (P < 0.01) in serum prolactin concentration was measured in lambs fed increasing levels of E+. Reduced serum prolactin concentration was previously reported in sheep consuming E+ fescue (Elsasser and Bolt, 1987;Henson et al., 1987).

Lambs fed the 10% E+ diet had a 22, 1.7, 42.8, and 93.6% reduction in feed intake, Ts, TCI, and prolactin, respectively, compared to lambs fed the E- diet. These results suggest that changes in prolactin are more sensitive to fescue toxins than feed intake, Ts, and TCI. A day effect (P < 0.01) existed for feed intake, respiratory rate, Tco, Ts, and TCI. The day effect may be a reflection of lamb adaptation to heat (33°C). The 10% E+ diet more effectively produced fescue toxicosis symptoms than did the 5% E+ diet; therefore, the 10% E+ diet was used in for Exp. 2.

Experiment 2
As in Exp. 1, feed intake was significantly affected by diet (P < 0.01) (Table 3). Voluntary intake was reduced in lambs consuming the E+ diet compared with the lambs on the E- (P < 0.01) and EV diets (P = 0.02). There was no difference (P = 0.12) in intake between the lambs consuming the E- and EV diets. Unlike Exp. 1, weight gain was affected by diet (P < 0.01). Total weight gain over the 15-d experiment was less for lambs consuming the E+ diet compared with the gain of lambs on the E- (P < 0.01) and EV (P = 0.02) diets. The lowered weight gain was due in part to lower feed intake of the E+ lambs. Gain tended to be lower (P = 0.10) for lambs consuming the EV diet than the lambs on the E- diet.

Skin temperature, TCI, and prolactin concentration of lambs were affected by diet (P < 0.01). Skin temperature of lambs consuming the E+ diet was 0.8 and 0.4°C less than (P < 0.01) the skin temperatures of the lambs fed E- and EV. Although Ts was lower for EV-fed lambs than E- lambs, the difference between the EV and E- lambs was not significant. However, TCI values for lambs fed the EV and E+ diets were lower (P < 0.05) than those for lambs fed the E- diet. The TCI for EV and E+ lambs did not differ (P = 0.12). As indicated in Exp. 1, the E+ diet significantly lowered Ts and TCI, which suggested that E+ fescue caused peripheral vasoconstriction. Although the EV diet did not cause a significant change in Ts, feeding the EV diet did result in a significant reduction in TCI. Thermocirculation index may better represent a vascular response to fescue toxicosis since its value takes into consideration differences in Ta, Ts, and Tco. This would suggest that EV, when fed to lambs, has significant vasoconstrictive properties.

Lambs that consumed the EV diet exhibited a lower (P < 0.01) serum prolactin concentration compared with the E- lambs. Pure EV can reduce prolactin concentrations when injected into cattle (McCollough et al., 1994), added to a pituitary culture system (Denard et al., 1994;Strickland et al., 1994), and, as the present study shows, when added to the diet of animals. The prolactin concentration of the E+ lambs was substantially less (P < 0.01) than that of the lambs fed the EV diet. Although the EV diet caused a 34.1% reduction in prolactin below that of lambs on the E- diet, the E+ diet caused a 94.3% decrease compared to the E- lambs. This suggests that the E+ diet contained additional compounds that augmented the reduction of prolactin or that the EV in the EV diet was degraded more rapidly or assimilated differently than the EV in the E+ seed matrix.

As in Exp. 1, a day effect existed for average Ts and TCI. The day effect may be a result of thermal adaptation of lambs to their noncyclic environment (33°C, 50% relative humidity). A trial effect (data not shown) was detected for Ts, TCI, and serum prolactin. The least squares means for the three variables had similar trends in both trials; however, the magnitude of the response was greater in trial 2 than in trial 1. The reason for this difference is unclear.

Although the EV diet contained a concentration of EV similar to that of the E+ diet, there was no significant difference in feed intake, weight gain, or body temperature of lambs fed the EV diet compared with lambs on the E- diet. However, lambs fed the E+ diet had a significant reduction in feed intake, weight gain, and Ts. Lambs fed the EV diet showed a significant reduction in TCI, suggesting a reduction in peripheral blood flow, as well as a significant reduction in prolactin concentrations compared with lambs fed the E- diet. However, reduction in prolactin caused by the EV diet was not as great as the reduction caused by the E+ diet. Overall, the EV diet was not as effective as the E+ diet in producing fescue toxicosis symptoms. The result suggests that EV is a fescue toxin, but additional alkaloids may contribute to the full fescue toxicosis response.

Experiment 3
Concentration of ergot alkaloids in the seed and estimated concentration in the diets for Exp. 3 are shown in Table 4. Predicted concentration of EV, based on HPLC analysis of the original seed sources, was 520 ppb for the E+ and R+ diets. Analysis of dietary grab samples taken from bags in which each diet was stored demonstrated that EV concentrations in R+ diets (0.61 ppm) were at least as great as EV concentrations in the E+ diets (0.53 ppm). Total ergot alkaloids estimated by ELISA in the seed were 0, 1.32, and 2.69 ppm, for E-, R+, and E+, respectively. Considerably more EV was measured by HPLC in the R+ seed than in the E+ seed; however, an inverse relationship was seen with the ergot alkaloids as estimated by the ELISA procedure. The monoclonal antibody used in the ELISA procedure was produced by immunizing mice against lysergol/BSA. The antibody not only cross-reacts with EV, but also with other lysergic acid derivatives (Hill and Agee, 1994). As measured by HPLC, lysergic acid amide concentration was greater in the E+ vs. R+ seeds (2.50 vs.1.26 ppm), which corresponds with the ELISA estimates. The water-based extraction procedures used in the ELISA assay may be more effective in extracting the more water-soluble lysergic acid derivatives than lipophilic ergopeptides, such as EV. The concentration of EV in the E+ and R+ diets was similar. However, the predicted concentration of total ergot alkaloid in the E+ diet was six times higher than the level in the R+ diet. The presence of high concentrations of loline alkaloids in E+ and its absence in R+ (Porter, 1995) probably has little bearing on this study since loline alkaloids have not been shown to affect grazing animals (Fletcher et al., 2000). Loline alkaloids alone are not implicated to cause fescue toxicosis; however, potential synergistic effects between loline and ergot alkaloids may exist and should be addressed in future research delineating the compounds involved in fescue toxicosis.

Rectal temperature during the continuous heat stress was higher (P < 0.05) for lambs on the E+ diet than for lambs on the R+ or the E- diets. In addition, Tr of lambs fed the R+ diet was 0.31°C higher (P = 0.03) than lambs on the E- diet. As shown in Table 5, the Ts for E+ lambs was lower (P < 0.01) than for lambs fed the E- or R+ diets, the Ts of which were not different (P = 0.4). The TCI indicated that lambs on the E+ diet had reduced (P < 0.01) peripheral blood flow compared with lambs on E- or R+ diets. However, TCI of lambs on the R+ diet was somewhat lower (P < 0.07) than lambs on the E- diet. These data would suggest that EV, which was common to both E+ and R+ diets, may have contributed to the reduction in peripheral blood flow and heat loss, causing an elevation of internal body temperature. Total ergot alkaloids were higher in the E+ diets than in the R+ diets, and other ergot alkaloids (ergine and the clavines, Porter, 1995) found in E+ forage have vasoactive properties (Solomons et al., 1989), which indicates that these alkaloids, along with EV, may be producing some of the toxicosis symptoms.

Lambs on the R+ diet had a lower (P < 0.01) serum prolactin concentration compared with lambs on the E- diet, and lambs on the E+ diet had lower (P < 0.02) serum prolactin than lambs on the R+ diet. In Exp. 2, addition of EV to the E- diet lowered serum prolactin compared with the E- control lambs, but it was not as effective at lowering serum prolactin as feeding the E+ diet. Experiments 2 and 3 demonstrate that EV fed to lambs lowers serum prolactin; however, other ergot alkaloids may play a role. As shown in Table 5, lambs fed the E+ diet had a reduction of serum AP and an elevation of serum AST, LDH, cholesterol, and triglycerides compared with the lambs fed the E- diet. Lambs on the R+ diet were either similar to lambs fed the E- control diet (serum AST and cholesterol) or had intermediate concentrations (serum AP, LDH, and triglycerides) between the E- and E+ treatment groups. Changes in these enzyme and lipid constituents of lambs on the E+ diet are similar to reports of cattle grazing endophyte-infected fescue (Oliver et al., 2000). The lack of an intermediate response of lambs on the R+ diet suggests that ergot alkaloids other than EV may play an important role in altering these constituents.

	Implications

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Lambs fed a diet containing ergovaline as a supplement (Exp. 2) or as the primary ergot alkaloid (Exp. 3) developed some symptoms of fescue toxicosis; however, the endophyte-infected seed diets that contained comparable concentrations of ergovaline in addition to other ergot alkaloids were more effective in producing fescue toxicosis symptoms. These studies indicate that ergovaline produces some symptoms of fescue toxicosis (e.g., decreased prolactin), and that it works in concert with other ergot alkaloids.

Received for publication October 2, 2002. Accepted for publication January 20, 2003.

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Top Abstract Introduction Materials and Methods Results and Discussion Implications Literature Cited

 


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