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ANIMAL PRODUCTION |
* Department of Animal Science and
and
Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville 72701;
and
Southwest Research Center, University of Missouri, Mount Vernon 65712; and
and
Department of Agronomy and
and
¶ Department of Animal Science, University of Missouri, Columbia 65211
Abstract
Cattle grazing tall fescue (Festuca arundinacea Schreb.) often develop fescue toxicosis. This condition is thought to be caused by ergot alkaloids produced by the endophyte Neotyphodium coenophialum. Endophytes from wild tall fescue plants, which do not produce ergot alkaloids, were transferred into the endophyte-free tall fescue germplasm, HiMag. The novel associations also lacked the ability to produce ergot alkaloids. Our objective was to determine whether cattle grazing these novel endophyte associations showed signs of fescue toxicosis. At the Fayetteville, Arkansas location, tester steers (n = 72) were assigned to one of four pasture treatments: endophyte-free HiMag tall fescue (HiMag-); ‘Kentucky-31’ tall fescue infected with its native, toxic endophyte (KY+); and two novel endophyte-infected tall fescue associations, HiMag4 and HiMag9. At the Mount Vernon, Missouri location, steers (n = 54) were used to test three of the four cultivars (HiMag9 was not tested). Ergot alkaloid concentrations in the forage of HiMag4 and HiMag9 were low or undetectable. Respiration rate, rectal temperature, ADG, and hair scores were measured during the grazing period. Blood was collected via jugular venipuncture and used for prolactin, aspartate aminotransferase, alkaline phosphatase (ALP), lactate dehydrogenase (LDH), cholesterol, triglyceride, and creatinine analysis. Weight gains by steers grazing HiMag4 and HiMag9 did not differ from those of steers grazing HiMag-, but were greater than gains (P < 0.05) by steers on the KY+ treatment. Steers grazing KY+ had higher (P < 0.05) respiration rates, rectal temperatures, and hair scores than did steers grazing novel endophyte and HiMag- pastures. Prolactin, ALP, cholesterol, LDH, and triglycerides all were suppressed (P < 0.05) in steers grazing KY+ compared with steers grazing novel endophyte and HiMag- pastures. Steers grazing the novel endophyte tall fescues did not suffer from the decreased weight gains and toxicities associated with fescue toxicosis, resulting in enhanced animal production.
Key Words: Cattle • Ergot Alkaloids • Fescue Toxicosis • Novel Endophyte
Introduction
Cattle grazing endophyte-infected tall fescue (Festuca arundinacea Schreb.) typically suffer from symptoms of fescue toxicosis (Stuedemann and Hoveland, 1988
). Fescue toxicosis appears to be caused by alkaloids produced by the endophytic fungus Neotyphodium coenophialum (Hill et al., 1994; Glenn et al., 1996). That same endophyte can enhance host-plant persistence and competitiveness when compared with endophyte-free tall fescue (Clay, 1988; West, 1994).
Selecting endophyte strains that lack the toxins that are deleterious to livestock but that promote plant persistence was shown to be successful in perennial ryegrass (Fletcher and Easton, 1997) and has stimulated strong interest in applying this technology to tall fescue in the United States. Bouton et al. (2002) reported on trials using nonergot-alkaloid-producing endophyte strains in combinations with tall fescue cultivars ‘Jesup’ and ‘Georgia-5.’ Lambs grazing these cultivars containing endophyte strain AR542 gained at a rate similar to that of lambs grazing endophyte-free (E-) versions of the same cultivars, all of which averaged an approximately 60% greater rate of gain than Jesup containing the toxic, wild-type endophyte. Forage yield and stand persistence with the novel endophyte were greater than that with E- and the same as that with the wild-type endophyte. Parish et al. (2003) reported that beef steers grazing tall fescue with strain AR542 or E- averaged a 70% greater rate of gain and gain per hectare compared with tall fescue with the wild-type endophyte.
An analogous Arkansas-Missouri effort was carried out involving the selection of ergopeptine-deficient endophytes (West et al., 1998) and their introduction into HiMag, a population of tall fescue with a low risk of causing grass tetany (Sleper et al., 2002). The objective of this trial was to determine if cattle grazing tall fescue containing ergopeptine-deficient endophytes develop symptoms of fescue toxicosis.
Materials and Methods
A 2-yr grazing study using growing steers was conducted at the University of Arkansas in Fayetteville and the University of Missouri Southwest Research Center near Mount Vernon.
Fayetteville
Pastures were established by drilling seed at 19 kg/ha of pure live seed into prepared seedbeds in October 1998. Two 1.62-ha pasture replicates were prepared for each of the four fescue treatments. A third replicate was seeded in October 1999 for grazing in 2000. Treatments comprised two novel (ergovaline-deficient) endophyte selections in HiMag tall fescue (HiMag4 and HiMag9), toxic endophyte-infected Kentucky 31 tall fescue (KY+), and endophyte-free HiMag tall fescue (HiMag-). Endophyte infection levels of pastures were verified by sampling 25 tiller bases from each pasture using a tissue-print immunoblot (Gwinn et al., 1992). All pastures were fertilized and limed before planting according to soil test recommendations for establishment. Nitrogen fertilizer was applied in two applications of 67 kg/ha in 1999 and 2000. One of the KY+ pastures was overtaken by annual ryegrass (Lolium multiforum Lam.); therefore, that pasture was removed from the trial, leaving only one KY+ replicate in 1999 and two in 2000.
On May 21, 1999 and April 17, 2000, four crossbred tester steers (240 ± 1.8 kg) were weighed and assigned to each pasture. Steers were weighed at 28-d intervals until October of each year and had access to a mesh-covered shade (4 m2 per tester steer). A combination of mowing and using put-and-take grazer steers was used to control excess forage accumulation and equalize forage availability among treatments from grazing initiation through the end of June. The minimum available DM of forage was 2,200 kg/ha.
Mount Vernon
Nine 0.81-ha pastures were planted in September 1998 with three tall fescue treatments, HiMag4, HiMag-, and KY+, in three replications. Pasture establishment and fertilization practices were the same as those used at Fayetteville. Each pasture was stocked with three crossbred tester steers (234 ± 3.2 kg). Steers were weighed and bled via jugular venipuncture at 28-d intervals until October of each year. Mowing and put-and-take grazers were used as in Fayetteville to control forage availability through June of each year. Steers had no access to shade.
Serum cholesterol, creatinine, triglycerides, lactate dehydrogenase (LDH), alkaline phosphatase (ALP), and aspartate aminotransferase (AST) were determined by a 550 Express Clinical Chemistry Analyzer (Ciba Corning Diagnostics Corp., Alameda, CA). Serum prolactin was analyzed by a RIA procedure (Henson et al., 1987).
Animal and Pasture Treatment for Both Locations
Husbandry of the steers was in accordance with guidelines recommended by the Consortium (1988). All steers were given ad libitum access to a mineral supplement and fresh water. Tester steers were visually scored for hair coat at weighing using the following system: 1) slick short hair (less than 1.5 cm in length); 2) some medium length hair (1.5 cm to 2.5 cm); 3) medium length hair covering most of the body; 4) medium length hair plus some rough, long, dead hair; and 5) rough, long, dead hair covering most of the body. On days when ambient temperature exceeded 32°C, steers were gathered at midday and penned in a shaded area. Steers were allowed to rest for 1 h before determining rectal temperature via digital thermometer. In addition, respiration rate was determined by recording number of breaths taken per 30-s period. Twelve observations were made over the trial period for 1999, and five observations were taken for 2000. Ambient temperature and humidity in the shade and black globe temperatures were continually monitored by use of the HOBO Boxcar Pro data logger (Onset Computer Corp., Bourne, MA).
Fifty leaf blades that were suitable for grazing were detached and composited from each pasture for alkaloid determination on May 24, July 25, October 1, and October 21, 1999, and April 21, May 31, and July 27, 2000 at Fayetteville. At Mount Vernon, sampling occurred on May 6, June 2, June 18, and October 20, 1999, and on June 7, 2000. Forage samples were lyophilized and ergovaline concentrations were determined by HPLC and expressed as the sum of ergovaline and its epimer ergovalinine (Moubarak et al., 1996). Forage loline levels were also determined from collection of each pasture on May 24, 1999 and May 31, 2000 at Fayetteville. At Mount Vernon, sampling occurred on May 6, 1999 and June 7, 2000. Loline concentrations were determined by GLC, using the extraction procedure of Bush et al. (1982) and a capillary HPLC procedure from Yates et al. (1989). Forage CP, ADF, and NDF were determined using near infrared reflectance spectroscopy on the Fayetteville May and July samplings.
Initial stand density was determined in 1999 by recording the percentage frequency of live tall fescue plants at 50 points spaced 0.2 m apart along fixed, 10-m transects, six per pasture at Fayetteville and four per pasture at Mount Vernon. A final reading was performed in 2002; however, the disappearance of transect markers at Fayetteville prevented repeat readings in the same locations. Therefore, final stand counts were based on grid-frame quadrat readings. The quadrat consisted of a 0.76 x 0.76 m steel-wire frame divided into 25, 0.15 x 0.15 m cells. The percentage of cells containing at least one live tall fescue crown (or partial crown, not overhanging leaves) was averaged across 50 random throws per pasture in the fall of 2002 to determine long-term stand persistence.
Statistics
Data for live weight gain (ADG), respiration rate, rectal temperature, and hair score were averaged among testers within pasture units. The experimental unit was the group of tester steers in an individual pasture. Data were combined across locations and years and analyzed as a 2 x 2 x 4 (location x year x forage) factorial arrangement using PROC GLM from SAS (SAS Inst., Inc., Cary, NC) in an unbalanced design. Main effects of year, location, forage, and their interactions were tested for significance (
= 0.05). Serum component data were analyzed using PROC GLM with effects of year and forage and the year x forage interaction in the model. In both analyses, means were separated using the PDIFF function of SAS. Percentage ground cover was analyzed by ANOVA within sampling times and locations, using a completely randomized design.
Results
No significant year x location, forage x location, or forage x year interactions were observed for performance data; therefore, data were presented as least squares means for combined years and locations. Steers grazing HiMag4 and HiMag9 had ADG similar to those of steers grazing HiMag- but exceeded (P < 0.05) those of steers grazing KY+ (Table 1). Mean respiration rate, rectal temperature, and hair coat score for cattle grazing HiMag4 and HiMag9 were not different from those of cattle grazing HiMag- and were lower (P < 0.05) than for cattle grazing KY+ pastures.
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. N-Acetyl and N-formyl loline concentrations were present in KY+, HiMag4, and HiMag9 pastures and are reported in Table 3. Crude protein concentrations ranged from 12.8 to 16.9% across sampling dates, ADF ranged from 27.8 to 30.0%, and NDF ranged from 52.8 to 56.4%, with no trends associated with tall fescue treatments.
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). There was no treatment effect on AST activity. Serum triglyceride concentrations were highest in steers on HiMag4, lowest in KY+, and intermediate in the HiMag- treatment. Creatinine concentrations were similar in steers grazing HiMag4 and HiMag- but were higher (P < 0.05) in steers grazing KY+.
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Discussion
Steers grazing novel endophyte and endophyte-free tall fescue forage had the greatest ADG. The increase in ADG may have been due to an increased forage intake. Goetsch et al. (1987) observed decreased intake when cows consumed toxic endophyte-infected (E+) tall fescue compared with steers consuming endophyte-free (E-) tall fescue forage in hot weather. Similar observations were made with heat stressed lambs (Aldrich et al., 1993). Although behavior data were not collected, we observed that steers grazing KY+ pastures spent more time in the shade or standing at the waterer than did steers grazing E- and novel endophyte pastures, particularly during hot weather. Those observations would be consistent with lowered intake, and with previously reported behavior (Bondurant et al., 2001).
Studies comparing cattle grazing E+ tall fescue and E- tall fescue have found that cattle grazing E+ tall fescue have elevated body temperature and respiratory rates compared with cattle grazing E- tall fescue (Hemken et al., 1979, 1981; Hoveland et al., 1983; Strahan et al., 1987). Steers grazing HiMag4, HiMag9, and HiMag- pastures in our study had normal rectal temperatures, whereas the steers grazing KY+ pastures were heat stressed as indicated by observed behaviors, elevated rectal temperatures, and increased respiration rates. Elevated body temperature for steers grazing E+ may be due to the peripheral vasoconstriction induced by ergot alkaloids (Strickland et al., 1993; Oliver, 1997). Because cattle lose metabolic heat via the respiratory tract (Finch, 1986), elevated body temperature may be responsible for the increase in respiration rate.
Prolactin was suppressed in steers grazing KY+ pastures but not in steers grazing novel and E- tall fescue pastures. Those results are consistent with previous studies that found prolactin release to be suppressed or blocked by animals receiving ergot alkaloids (Karg and Schams, 1974; Smith et al., 1974; Browning et al., 1997).
Cattle grazing E+ tall fescue typically retain their winter hair coat, resulting in summer hair coats that are long, rough, and bronze in appearance (Stuedemann and Hoveland, 1988). In the present study, steers grazing KY+ had long and rough hair coats, whereas steers grazing the HiMag pastures with or without endophytes had slick and smooth hair coats. Ergot alkaloids cause decreases in peripheral blood flow (Oliver, 1997). Reduction in peripheral blood flow, as well as seasonal changes in prolactin or melatonin secretion (Porter and Thompson, 1992), may affect normal hair follicle function (Milne et al., 1990).
Steers grazing toxic KY+ tall fescue had decreased serum levels of ALP, AST, and LDH and increased levels of creatinine compared with steers grazing HiMag tall fescues. Data are congruent with results from other studies in which cattle consuming E+ tall fescue had lower enzymatic activities in their sera (Jackson et al., 1984; Oliver et al., 2000). The precise mechanism by which those enzymes are related to fescue toxicosis is not known.
Cholesterol concentrations were reduced in steers that grazed KY+ pastures compared with steers that grazed HiMag pastures, as reported by Oliver et al. (2000). Ergot alkaloids affect lipid metabolism by causing a lowering of fat stores, cholesterol, and triglyceride concentration in blood (Cincotta and Meier, 1989; Barnett et al., 1991). However, a recent report indicates that cows may have elevated cholesterol and triglyceride concentrations immediately following an intravenous challenge with ergotamine (Browning, 2003).
Cattle grazing E+ tall fescue have been shown to have reduced ADG and altered physiology and body composition when compared with cattle grazing E- tall fescue. In the present study, steer grazing novel E+ tall fescue had weight gains and physiological markers that were similar to steers grazing E- tall fescue grass. Steers on KY+ pastures gained less weight and had elevated or lowered levels of most physiological markers than animals on HiMag-, HiMag4, or HiMag9.
Implications
Toxic alkaloids produced by endophytes associated with tall fescue result in production losses for grazing livestock; however, beneficial aspects of the endophyte to the plant are important for stand establishment and survivability. Results from this study demonstrate that associations between novel endophytes, which are void of the ergot alkaloids, and tall fescue could be used as a management tool to decrease or prevent fescue toxicosis. Tall fescue pastures infested with these novel endophytes support animal production as well as endophyte-free tall fescue while maintaining the potential to protect the plant from environmental stressors.
1 Correspondence: B107E AFLS (phone: 479-575-4376; fax: 479-575-7294; e-mail: crosenkr{at}uark.edu).
Received for publication September 3, 2002. Accepted for publication November 10, 2003.
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