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Use of nonergot alkaloid-producing endophytes for alleviating tall fescue toxicosis in sheep^1,2

J. A. Parish^*,3, M. A. McCann^*,4, R. H. Watson^*, C. S. Hoveland, L. L. Hawkins^,5, N. S. Hill and J. H. Bouton

^* Department of Animal and Dairy Science; and Department of Crop and Soil Sciences; and and College of Veterinary Medicine, The University of Georgia, Athens 30602-7385

³ Correspondence:
2301 S. University Ave., P. O. Box 391, Little Rock, AR 72203 (phone: 501-671-2162; fax: 501-671-2185; E-mail:
jparish{at}uaex.edu).

	Abstract

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Nonergot alkaloid-producing endophytes from New Zealand were inserted into tall fescue (Festuca arundinacea) cultivars in an attempt to address the problem of fescue toxicosis in grazing sheep. A 3-yr grazing study was conducted to determine lamb performance and to evaluate toxicosis in lambs grazing nonergot alkaloid-producing endophyte-infected (AR542 or AR502), endophyte-free (E–), or wild-type toxic endophyte-infected (E+) Jesup tall fescue or nonergot alkaloid-producing endophyte-infected (AR542) Georgia-5 tall fescue. Replicated 0.11-ha tall fescue paddocks were established at the central Georgia Branch Station during September 1997 and stocked with lambs from spring 1998 through autumn 2000. Mean ergot alkaloid concentrations were higher (P < 0.01) in E+ forage than in AR542, AR502, and E– tall fescue, and ergot alkaloid concentrations in E– plants and plants infected with AR542 and AR502 were low. Forage availability did not differ (P = 0.92) across treatments during autumn and was higher (P < 0.05) in Georgia-5 AR542 than in Jesup AR502 and E+ pastures. Initial serum prolactin (PRL) concentrations did not differ (P = 0.58) across treatments during autumn, but were higher on Jesup AR542 than E+ during spring. Post-treatment serum PRL concentrations were depressed (P < 0.01) on E+ compared with AR542, AR502, and E– in both spring and autumn. Signs of heat stress were observed in E+ lambs during periods of high ambient temperatures. Mean post-treatment rectal temperature and mean stocking rate exhibited treatment x year interactions (P < 0.05). Lamb ADG was higher (P < 0.05) on AR542, AR502, and E– than on E+ tall fescue. Similarly, gain/hectare was higher (P < 0.015) on AR542, AR502, and E– than on E+. Tall fescue pastures containing AR542 and AR502 endophytes yielded lamb performance that did not differ from that on E– tall fescue and which was superior to performance on E+ tall fescue. Depressed PRL concentrations and elevated rectal temperatures as indicators of toxicosis were evident only in lambs grazing E+ tall fescue, suggesting that nonergot alkaloid-producing endophyte-infected tall fescue is a viable alternative for alleviating tall fescue toxicosis.

Key Words: Endophytes • Ergot Alkaloids • Festuca arundinacea • Grazing • Lambs • Toxicosis

	Introduction

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Tall fescue (Festuca arundinacea) is a cool-season grass widely used as pasture or hay in the southeastern United States. Despite attributes making it a desirable forage crop, consumption of tall fescue often results in fescue toxicosis, a condition that adversely affects grazing livestock performance (Stuedemann and Hoveland, 1988) and production profitability (Thompson et al., 2001). Toxicosis problems in livestock are the result of grazing wild-type endophyte-infected (E+) tall fescue. Tall fescue endophytes (Neotyphodium coenophialum) reside within the plants, imparting positive agronomic qualities, such as enhanced drought tolerance (Thompson et al., 2001) and improved vigor (Stuedemann and Hoveland, 1988). However, the E+ produces ergot alkaloids associated with fescue toxicosis (Hill et al., 1994). Plant breeders have developed endophyte-free (E–) cultivars, which are nontoxic to livestock, but plant persistence is sacrificed (Hill et al., 1991).

Nonergot alkaloid-producing endophytes (AR542 and AR502) have been incorporated into E- Jesup and Georgia-5 tall fescue. These cultivars with AR542 and AR502 endophyte strains produce extremely low concentrations of ergot alkaloids and have better stand survival than Jesup and Georgia-5 E- controls; also, survival did not differ from Jesup and Georgia-5 E+ controls when subjected to close grazing in bermudagrass (Cynodon dactylon) sod (Bouton et al., 2002). Initial animal toxicosis evaluation was conducted in lambs since tall fescue seed supplies with AR542 and AR502 were limited and lambs required a smaller grazing area per animal than cattle. Other researchers have found lambs to be good models for assessing fescue toxicosis in ruminants (Aldrich et al., 1993; Fletcher et al., 2000). The objectives of the present study were to determine growth performance and evaluate toxicosis in lambs grazing nonergot alkaloid-producing endophyte-infected Jesup and Georgia-5, Jesup E-, and Jesup E+ tall fescue.

	Materials and Methods

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Pasture Establishment and Management

Five pasture treatments: 1) Georgia-5 AR542-infected tall fescue, 2) Jesup AR542-infected tall fescue, 3) Jesup AR502-infected tall fescue, 4) Jesup E- tall fescue, and 5) Jesup E+ tall fescue were compared for lamb toxicity and performance for 3 yr. The experiment had a randomized complete block design with two blocks of each paddock treatment. The blocks were assigned based on paddock slope and drainage. The 0.11-ha paddocks were tall fescue monocultures established at the Central Georgia Branch Station near Eatonton, GA (33.3972°N lat; 83.4883°W long; elevation = 167 m) in September 1997. Seed supplied by J. H. Bouton was drilled into well-prepared Mecklenburg sandy loam soil at a seeding rate of 33.6 kg/ha. The paddocks were fertilized uniformly with 67 kg of N/ha and P and K according to soil tests at establishment and in February and September of each subsequent year.

Lamb and Grazing Management

The lambs in this study were managed under protocol A2000-10092 approved by the University of Georgia Animal Care and Use Committee. Rambouillet-Suffolk crossbred ewe and wether lambs (mean BW = 23 kg) were randomly assigned to the treatment paddocks. Paddock fencing consisted of 0.91-m Flexinet electric netting (Horizont UK, Ltd., Gloucester, U.K.). The lambs were supplied at all times with fresh water, free-choice copper-free mineral blocks (Godfrey’s Warehouse, Madison, GA) (Table 1), and shade in each paddock. The lambs were shorn, ear-tagged, paint branded, and treated orally for internal parasites with Valbazen (active ingredient is 11.36% albendazole) (Pfizer Animal Health, Exton, PA) at a rate of 7.5 mg/kg of BW at the initiation of each grazing season. In an attempt to maintain forage availability levels that did not differ among the paddocks, a put-and-take method of stocking was used. Two lambs in each paddock were designated as testers, and the remaining lambs were designated as grazers. Based on forage availability, stocking rate was adjusted by removing or adding grazer lambs while tester lambs remained on the paddocks for the duration of the grazing season. Paddocks were restocked with new lambs at the onset of each grazing season. Grazing dates and the number of lambs per grazing period appear in Table 2. The spring grazing seasons averaged 75 d, whereas the autumn grazing seasons averaged 66 d. Grazing began later in the spring of the first year than in succeeding years to ensure that new forage plantings were vigorous and well established. Grazing was initiated when there was approximately 2,600 kg of DM/ha of available forage and continued until forage availability dropped below approximately 1,800 kg of DM/ha.

At the beginning of grazing and at 2-wk intervals thereafter, paddocks were sampled for available forage by clipping herbage to a 5.08-cm stubble height within a 0.09-m² quadrant from 10 randomly selected sites within each paddock. The material was dried in a forced-air oven at 60°C, weighed, and the amount of DM (kg/ha) was calculated. The rate of endophyte infection was assayed on tall fescue tillers near the onset and conclusion of each grazing season using the immunoblot procedure of Hiatt et al. (1997). Tillers were collected on the same sampling schedule as available forage samples at 10 randomly selected sites within each paddock, lyophilized, ground through a 1 mm screen in a Wiley mill (Arthur A. Thomas, Philadelphia, PA), and analyzed for total ergot alkaloid concentration using an ELISA procedure described by Adcock et al. (1997).

Lamb weights, blood samples, and rectal temperatures were collected at the onset of each grazing season and at 14-d intervals. Initial and final lamb weights were collected on two consecutive days and averaged. On weigh dates, lambs were gathered from all paddocks at approximately 0900, sampled in random order, and returned to paddocks within approximately 2 h. After autumn 1999, lambs were gathered from all paddocks for data collection at approximately 1300. Approximately 7 mL of blood was collected from each lamb via jugular venipuncture. Blood samples were centrifuged at 3,000 x g to separate and harvest serum that was then frozen (0°C). Analysis was then performed to determine serum prolactin (PRL) concentrations according to the RIA procedure of Mizinga et al. (1992). The intraassay and interassay CV were 9.4 and 15.5%, respectively. Post-treatment PRL concentrations and rectal temperatures were averaged from d 14 through the end of the grazing season.

Lamb days were calculated as the sum of the days tester and grazer lambs remained on each paddock treatment. Tester lambs remained on the treatment paddocks for the entire duration of the grazing season, and lamb ADG represents the gains for tester lambs only. Lamb ADG was computed by dividing mean tester lamb gain in a given paddock by the number of days in the grazing period. Gain per hectare was calculated as the number of lamb days for both grazer and tester lambs multiplied by the ADG of testers. Mean stocking rate was computed by dividing lamb days by the duration of the grazing season in days.

Statistical Analysis

The PROC GLM/LSMEANS of SAS (SAS Inst., Inc., Cary, NC) was used to analyze the available forage and lamb data. A randomized complete block experimental design was used with paddock as the experimental unit and paddock slope as the blocking factor. Each treatment occurred once in each of the two blocks. Main effects were endophyte treatment, season, year, and block. The model included main effects and their interactions. Orthogonal contrasts among treatments included: E+ vs. all other treatments, E- vs. nonergot alkaloid-producing endophyte treatments, AR502 vs. AR542, and Jesup AR542 vs. Georgia-5 AR542. Ergot alkaloid concentration and serum PRL means showed nonhomogeneity among their variances due to some treatments having near-zero values and others possessing values in the hundreds or even thousands. Thus, these data were subjected to square root transformations to address data abnormality prior to statistical analysis, and nontransformed least square means are reported. Because the ergot alkaloid and serum PRL data were not normally distributed, the variations around the means are not reported.

	Results and Discussion

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Ergot Alkaloid Production, Forage Availability, and Forage Quality

Rates of endophyte infection in nonergot alkaloid-producing and E+ pastures were at least 68 and 80%, respectively, throughout the duration of the study. Mean ergot alkaloid concentrations were higher (P < 0.01) in E+ forage than in AR542, AR502, and E- tall fescue (Table 3). Along with E- tall fescue, plants infected with AR542 and AR502 endophytes produced extremely low concentrations of ergot alkaloids. Using put-and-take grazing management, average forage availability was maintained at levels that did not differ (P = 0.92) among treatments during autumn. During spring, mean available forage levels were higher (P < 0.05) in Georgia-5 AR542 than in Jesup AR502 and Jesup E+ pastures. Average forage availability was higher (P < 0.01) in the autumn compared with the spring (2,648 vs. 2,246 ± 90 kg of DM/ha). This resulted from stockpiling forage to target at least 60 d of autumn grazing each year. There was a year effect (P < 0.01) for available forage. Least squares means were 2,158, 2,247, and 2,936 ± 111 kg of DM/ha for 1998, 1999, and 2000, respectively. This trend of increasing annual forage availability over time was related to improved plant vigor as tall fescue stands matured. Root development likely played a role in this enhanced plant productivity over time. Forage IVDMD did not differ among pasture treatments in spring (P = 0.98) or autumn (P = 0.59), and CP concentrations did not differ (P = 0.40) across treatments during spring. Autumn CP was higher (P < 0.05) in AR542 and AR502 pastures compared with E+ pastures.

Depressed PRL concentrations are widely accepted as an indicator of fescue toxicosis (Hoveland et al., 1983; Fribourg et al., 1991; Rice et al., 1997). Initial pretreatment PRL concentrations (d 0) did not differ (P = 0.58) among treatments during autumn, however, initial PRL concentrations were higher (P < 0.05) in lambs assigned to Jesup AR542 than to E+ tall fescue during spring (Table 4). In addition, there was a season effect (P < 0.01) for initial PRL concentrations with spring concentrations exceeding autumn concentrations. There was a treatment season interaction (P < 0.01) for post-treatment PRL concentrations that may be associated with photoperiod influencing PRL concentrations to different degrees based on whether they are subject to the effects of ergot alkaloid consumption (Table 4). Mean post-treatment PRL concentrations were depressed (P < 0.05) in E+ compared with AR542, AR502, and E- tall fescue during spring and autumn grazing. This treatment response of serum PRL concentrations is consistent with the findings of Fletcher et al. (2000) for lambs grazing nonergot alkaloid-producing (AR501), E-, and E+ tall fescue. In addition, the upper PRL values reported in the current study are within the range of values reported by Fletcher et al. (2000). Spring d-0 and post-treatment PRL concentrations were higher (P < 0.01) than corresponding autumn values. This seasonal difference in d-0 and post-treatment PRL concentrations is likely related to the photoperiod. Sheep are seasonal breeders and have been shown to have increased PRL concentrations during periods of increasing day length (spring) and decreased PRL concentrations over periods of decreasing day length (autumn) (Foldes et al., 1991; Cerna et al., 2000; Lincoln and Clarke, 2000).

No treatment effects were observed for initial (d-0) rectal temperatures during spring (P = 0.40) or autumn (P = 0.51) (Table 5), but there were year (P < 0.01) and season (P < 0.10) effects, as well as a year x season interaction (P < 0.01). These differences were likely due to environmental conditions, the use of different lambs each grazing season, and time of day when measurements were taken. In addition, rectal temperature measurements were subject to confounding variables, such as lamb handling and stress, ambient temperature, humidity, and exposure to sunlight. After autumn 1999, rectal temperature collections were moved from the morning hours to the afternoon hours in order to record lamb temperatures during periods of higher ambient temperatures in an attempt to increase the likelihood of capturing treatment differences. No treatment effects (P = 0.32) were observed for post-treatment rectal temperatures during autumn, but post-treatment rectal temperatures were elevated in lambs grazing E+ tall fescue over lambs grazing Jesup AR542 and AR502 tall fescue (Table 5). There was a year x treatment interaction (P < 0.05) for post-treatment rectal temperatures. Lamb rectal temperatures were elevated to a greater extent during 1999 and 2000 on E+ pastures over AR542, AR502, and E- pastures than during 1998. Moving rectal temperature collections from morning to afternoon hours may have influenced annual post-treatment rectal temperatures to a greater degree on the E+ than on the other treatments, contributing to the significance of this interaction. Lambs on E+ tall fescue were observed exhibiting signs of heat stress (e.g., panting and lying under shade, whereas lambs on the E- and nontoxic endophyte treatments were grazing) during periods of elevated environmental temperatures. Higher temperatures have been documented on E+ tall fescue over E- tall fescue in cattle (Hoveland et al., 1983; Schmidt et al., 1983) and over E- and AR501 tall fescue in sheep (Fletcher et al., 2000).

There was a year x treatment interaction (P < 0.05) for stocking rate that may be explained by the more pronounced impacts that the lamb has on E- grass over time in conjunction with ergot alkaloid-based negative feedback on forage intake by lambs in the E+ paddocks (Figure 1). Lower forage intake has been documented in E+ vs. E- tall fescue in steers (Stuedemann et al., 1989), cows (Peters et al., 1992), and lambs (Aldrich et al., 1993). The difference between mean stocking rates on E+ and E- was particularly pronounced in 1999, when rainfall totals during the grazing seasons were moderate relative to spring 1998 and autumn 2000 (Figure 2a).

View larger version (13K): [in this window] [in a new window]   Figure 1. Least squares means of treatment x year interaction for mean stocking rate in Georgia-5 AR542 nonergot alkaloid-producing endophyte-infected (G542); Jesup AR542 nonergot alkaloid-producing endophyte-infected (J542); Jesup AR502 nonergot alkaloid-producing endophyte-infected (J502); Jesup endophyte-free (JE–); and Jesup wild-type endophyte-infected (JE+) tall fescue pastures, 1998 to 2000. SE = 0.86. Two observations per mean.

View larger version (49K): [in this window] [in a new window]   Figure 2. Total rainfall (2a) and average maximal and minimal daily terperatures (2b) at the Central Georgia Branch Station from spring 1998 to autumn 2000.

Lamb ADG was higher on AR542, AR502, and E- vs. E+ pastures during spring (P = 0.0007) and autumn (P = 0.0148) (Table 6). This agrees with the findings of Fletcher et al. (2000) in lambs grazing AR501, E-, and E+ tall fescue. A year effect (P < 0.01) was observed for ADG with least squares means of 116, 137, and 77 ± 6 g for 1998, 1999, and 2000, respectively. There was an inverse relationship between annual ADG and annual grazing days that may have contributed to the year effect.

Gain per hectare was higher on AR542, AR502, and E- than on E+ tall fescue during both spring (P = 0.0003) and autumn (P = 0.0107) (Table 6). There was a seasonal effect for gain/ha, with values being higher (P < 0.01) in spring than in autumn. This finding is not unexpected since there were 222 d of spring grazing compared with only 197 d of autumn grazing. A gain/ha year effect (P < 0.01) was found with least squares means of 253, 282, and 202 ± 13 kg for 1998, 1999, and 2000, respectively. As with ADG, the number of annual grazing days may have influenced the gain/ha year effect.

	Implications

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The removal of ergot alkaloids alleviated negative lamb responses associated with fescue toxicosis regardless of the nonergot alkaloid-producing endophyte strain or tall fescue cultivar host. Nonergot alkaloid-producing endophytes seem to be a viable alternative to endophyte-free tall fescue for good lamb performance without toxicity problems. The implications of alleviating tall fescue toxicosis include improved lamb health and performance and improved profitability, which should serve to improve the sustainability of forage-based livestock production.

	Footnotes

 
¹ The authors thank the following people for their technical assistance throughout this research effort: D. Wood, V. Calvert, F. Newsome, N. Paiva, T. Kormanik, J. Wood, A. Bunce, and B. Bramwell.

² This research was supported by state and Hatch funds allocated to the Georgia Agric. Exp. Stn., as well as funding from AgResearch (Palmerston North, New Zealand), Pennington Seed, Inc. (Madison, GA), and the Southern Region Sustainable Agriculture Research and Education Program.

⁴ Present address: Dept. of Animal and Poultry Sciences, Virginia Polytechnic Institute and State Univ., Blacksburg 24061.

⁵ Present address: Bayer Corp., Athens, GA 30605.

Received for publication August 20, 2002. Accepted for publication January 17, 2003.

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