Reproductive responses to grazing endophyte-infected tall fescue by postpartum beef cows

ELSEVIER

REPRODUCTIVE RESPONSES TO GRAZING ENDOPHYTE-INFECTED TALL FESCUE BY POSTPARTUM BEEF COWS J.M. Burke, la R.W. Rorie, 2 E.L. Piper 2 and W.G. Jackson 1 IDale Bumpers Small Farms Research Center, ARS, USDA, Booneville, AR, USA 2Department of Animal Sciences, University of Arkansas, FayetteviIle, AR, USA Received for publication: November 14, 2000 Accepted: March 5, 2001 ABSTRACT The objective was to determine pregnancy rate and stage of embryonic loss in response to grazing endophyte-free (E-; n = 20) or infected (E+; n = 30) tall fescue in postpartum beef cows with calves. Three weeks before estrus synchronization, cow-calfpairs were introduced to pastures (April 1999). Cows were synchronized and bred by AI after detected estrus for a period of 6 d and then by natural service for 62 d. Bulls were rotated weekly to minimize effects o f fescue toxicosis on male fertility. Fetal development was monitored weekly between 30 and 60 d of pregnancy and at weaning using transrectal ultrasound. Respiration rate (52.0 ± 1.4 vs 46.6 breaths/min; P < 0.02) and rectal temperature (39.6 + .09 vs 38.8 ± .12°C; P < 0.001) increased in E+ cows and serum concentrations ofprolactin (7.2 vs 57.4 ± 4.4 ng/mL; P < 0.001), total cholesterol (123.2 vs 149.6 + 3.6 mg/dL; P < 0.001 ), body condition (3.8 vs 5.2 ± 0.15; P < 0.001; 1 = thin, 9 = fat) and adjusted weaning weight of calves (195.8 vs 210.8 ± 4.5 kg; P < 0.02) were reduced compared to that of Ecows. Differences were not detected (E- vs E+) for estrus detection rate (84.9 ± 10.6% vs 80.2 ± 8.4%), pregnancy rate to synchronized estrus (41.7 ± 11.8% vs 46.8 ± 9.5%), overall pregnancy rate 30 d postbreeding (93.8 ± 6.2% vs 93.5 ± 5.1%), overall pregnancy rate at 60 d postbreeding (86.7 ± 10.1% vs 81.2 ± 8.3%), or serum concentrations of progesterone on day of PGF2a treatment (4.5 ± 0.7 vs 4.5 ± 0.8 ng/mL). Pregnancy losses that occurred between 30 and 60 d gestation were 6.0 (E-) vs 15.0 (E+) ± 8.0% (P > 0.10) and occurred after environmental temperatures rose above 37.8°C for three weeks. Total pregnancy losses that occurred by weaning (between 70 and 126 d of gestation) were 5.5 (E-) vs 17.6 (E+) ± 8.0% (P > 0.10). Pregnancy rate and embryonic losses were not different between cows grazing E- and E+ tall fescue under these management conditions. Published by ElsevierScience Inc.

Key words: beef, fescue toxicosis, reproduction Acknowledgments Authors express their appreciation to T. Lester for assistance with AI and ultrasound, J. Cherry, G. Robson, D. Jones, and T. Preston for technical assistance, and to T. Popham for statistical consultation. Thanks to Pharmacia Inc. of Kalamazoo, MI for the unconditional gift ofLutalyse. 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. aCorrespondence and reprint requests. Theriogenology 56:357-369, 2001 Published by Elsevier Science Inc.

O093-691X/O1/$-see front matter PII: S0093-691X(01 )00569-6

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INTRODUCTION Consumption of endophyte-infected tall fescue may lead to hyperthermia, a reduction in feed intake and weight gain, and decreased circulating prolactin (22, 25). Reproductive responses to endophyte-infected fescue include decreased pregnancy (7, 8, 9, 13) and calving rates, and delayed conception (25). Collectively, these related problems have been termed fescue toxicosis or summer slump. A fungus, Acremonium neotvphodium, resides in the endophyte-infected tall fescue grass that produces ergot alkaloids, which, when consumed by the animal, may lead to fescue toxicosis. The most apparent signs of fescue toxicosis occur during periods of heat stress. Total losses to the cattle industry attributed to fescue toxicosis have been estimated to exceed 600 million dollars (15), whereas those due to decreased reproductive performance have been estimated to be more than 300 million dollars. It is not well understood at what stage of the reproductive cycle consumption of endophyteinfected fescue leads to decreased pregnancy rates in cattle. Follicular dynamics may be affected as evidenced by reduced follicle number or size in beef heifers exposed to endophyte-infected fescue (11, 18, 19) and reduced estradiol production (11, 18, 19, 20). Luteal function may be impaired in cycling heifers grazing endophyte-infected fescue (11, 12, 16). Decreased conception rate in ewes grazing endophyte-infected fescue was attributed to delayed conception, or more specifically, increased embryonic loss and later onset ofestrus (5). However, in cattle, Rorie et al. (29) observed no differences in fertilization rate or embryonic development through the second week of gestation in heifers consuming endophyte-infected fescue seed. The sensitive stage of pregnancy to endophyte-infected rescue may occur after placentation and to a greater extent during heat stress. The current study examined pregnancy rates and stage of embryonic losses in early pregnancy in cows grazing endophyte-free or endophyte-infected tall fescue during summer months. MATERIALS AND METHODS Mature beef cow-calf pairs were randomly assigned to graze endophyte-free tall fescue (E-; n = 20; 16 ha paddock) or endophyte-infected tall fescue (E+; n = 30; 24 ha paddock) for 45 d before synchronized estrus until weaning of current calf(mid-October 1999). Before this, all but nine cows had been exposed to bermudagrass pasture. The nine cows (6 E-, 3 E+) grazed E+ pastures for more than 5 mo, but grazed bermudagrass pasture for 14 d before randomly assigned to treatment. Breeds grazing E- pasture included 6 Angus, 10 Hereford, 4 Angus × Hereford and in the E+ pasture 8 Angus, 17 Hereford, 5 Angus × Hereford. Forage availability was never limited for either pasture for the duration of the experiment, based on weekly visual examination of grass. Pastures were fertilized with an equal amount (63.9 kg/ha) of nitrogen, phosphorus and potassium in late February. Reproductive tracts of cows were palpated per rectum and determined normal before start of treatment. Body condition score (BCS; 1 = thin, 9 = fat) was estimated in April, May, June, and August. Intramuscular fat at hip and rib was estimated using ultrasound (Aloka SSD 500V ultrasound scanner equipped with a 3.5 MHz linear array transducer) during the first week on pasture and in late August. In order to evaluate fescue toxicosis, respiration rate and rectal temperatures were measured between 0730 and 0830 for both treatments on the day of PGF2a treatment (luteal phase of estrous cycle) and serum was collected for analysis of prolactin, total cholesterol, and progesterone.

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Cows were fed melengestrol acetate (MGA) grain carrier (0.91 kg/cow/d) without MGA for 14 d followed by carder with MGA (0.5 mg/cow/day) for 14 d. Seventeen days later cows were treated with PGF2a (25 mg Lutalyse im; Pharmacia Inc., Kalamazoo, MI; 6, 24). Cows were monitored for standing estrus using an electronic heat detection system (HeatWatch System, DDx, Inc., Denver, CO). The system was downloaded to computer twice daily for 7 d after treatment with PGF2w then daily until removal of bull. Cows were bred by AI with Angus semen (from two halfsib sires distributed randomly among the cows) 8 to 26 h after onset of standing estrus. Angus bulls were maintained on bermudagrass pastures free of endophyte-infected fescue and introduced 7 d after PGF2a treatment for a 62 d natural service period. Bulls passed a breeding soundness examination for sperm motility, viability, and abnormalities 7 d before introduced to cows. A total of three bulls were rotated weekly from E- to E t to bermudagrass pasture to minimize confounding effects of pasture and bull fertility. During natural service, there was 1 bull per 20 E- cows and 1 bull per 30 E+ cows. Thirty to 36 d after breeding, the uterus of pregnant cows was monitored every 7 to 14 d by transrectal ultrasound scanning (Aloka SSD 500V ultrasound scanner equipped with a 5.0 MHz linear array transrectal transducer; Aloka Co. Ltd, Japan) to examine embryo viability. Conception date was estimated by ultrasound (fetal size) and estrus detection data. Blood was collected from a coccygeal vessel or jugular vein and samples held continuously on ice until centrifuged (3000 g for 20 min at 4°C). Serum was collected and stored at -20°C until analyzed for prolactin, total cholesterol, and progesterone on day of PGF2a treatment and for progesterone at 30 d of gestation. Administration of PGF2a occurred after blood was collected. Concentrations of progesterone were analyzed in a single assay from non-extracted serum using a solid-phase 125I RIA kit (Coat-A-Count®, DPC, Los Angeles, CA) validated by Srikandakumar et al. (35). Sensitivity of the assay was 0.10 ng/mL. Intra-assay CV was 4.0%. Serum concentrations of total cholesterol were measured by the procedure of Wybenga et al. (40). Absorbance was measured at 560 nm wavelength. Intra-assay CV was 1.0%. Serum was analyzed for prolactin using a modification of procedures of Henson et al. (14) in a single RIA. Intra-assay CV was 8.4%. Data were analyzed using the GLM and Mixed Models procedure of SAS (31). The mathematical model used for data collected at one time point included pasture treatment, breed, and the interaction. Covariance was used in some models to correct for physiological differences among cows. To account for variations due to number of days postpartum, this continuous variable was included as a covariate for estrus detection and pregnancy rates and serum concentrations of progesterone. Time of measurement (first, second, and third 20 min interval) was included in the mathematical model for respiration rate and rectal temperature because of potential heat stress to cows waiting for measurement. The April BCS was used as a covariate for subsequent BCS measurements because BCS in April was greater for E- treated cows (6.2 vs 5.3 ± 0.27; P < 0.01). For BCS and body weight, heterogeneity of regression analyses were used to analyze differences between curves of E- and E+ cows from April to August; and included pasture treatment, breed, cow within month and month to the second order (38). Similarly, for calf weights, heterogeneity of regression was used to analyze differences between curves of E- and E+ treated calves from April to September, and included pasture treatment, breed, sex, calf within day of age and day of age to the second order. One cow from the E+ group was culled and removed from the data set after

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synchronized breeding for feet and leg problems incurred before the study began. A second cow from the E- group became infected with actinobacillus lignieresei infection between 30 and 60 d of pregnancy, did not respond to antibiotic treatment, and became emaciated. Therefore, this cow was removed from the data set after 30 d of pregnancy. Calving rate was determined in spring of 2000 and reflects differences due to treatment that occurred in early pregnancy. After fall weaning there was a cow from the E+ treatment that died of bloat. The three cows removed from the data set after death or culling were treated as missing values for subsequent analyses. In order to account for influence of previous forage exposure (i.e., 9 cows exposed to E+ fescue before randomly assigned to treatments), this fixed variable and interactions were included in the GLM model described previously. Because significance and differences between treatment means were unaffected, least squares means from the model that included treatment and breed were included in results. RESULTS Signs of fescue toxicosis existed in cows grazing endophyte-infected fescue pastures. Respiration rate and rectal temperature increased in E+ cows and serum concentrations ofprolactin, total cholesterol, BCS by late August; and adjusted weaning weights of calves were reduced (Table 1). Change in BCS between April and August was different as determined by regression analysis. Equations were YE- = 11.91 - 1.94x + 0.14x z and YE+ = 7.19 - 0.45x + (3.8 x 10-~)xz (P < 0.001), where y = BCS and x = month. Although cows were assigned randomly to treatments, BCS was greater for E- cows in April (P < 0.01). Therefore, the April BCS was used as a covariate to analyze BCS estimated in May, June, and August (Figure 1). Calf weight gains were different between pasture treatments: YE- = 9.56 + 1.47x - 0.0024x 2 and YE+ = 31 51 + 0.85x - (2.0 x 10-4)x2, where y = body weight (kg) and x = day of age (P < 0.001; Figure 2). Differences were not detected between treatments for estrus detection, pregnancy or calving rates or serum concentrations of progesterone on day of PGF2, treatment or at 30 d gestation (Table 2). Calving rate (Hereford, 65.3 + 8.0; Angus, 100.0 + 10.7; Angus x Hereford, 90.0 :L 12.8%; P < 0.04) and serum concentrations of progesterone (Hereford, 5.9 + 0.4; Angus, 7.7 + 0.6; Angus x Hereford, 8.4 + 0.8 ng/mL; P < 0.01) were lower in Hereford compared with Angus or Angus x Hereford cows. Mean day of conception for cows that responded to synchronization was not different (157.6 vs 157.3; P > 0.10). However, 68% of cows on E+ pasture were detected in estrus within 3 d of PGF2a treatment vs 31% of cows on E- (Figure 3).

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Table 1. Physiological responses of cows with calves grazing endophyte-free or infected tall fescue. Values represent least squares mean ± pooled standard error adjusted for treatment and breed effects. E -a

E+ b

Pooled SE

Respiration rate, breaths/min

46.6 c

52.0

1.5

Rectal temperature, oC

38.8 d

39.6

0.1

Prolactin, ng/mL

57.4 d

7.2

4.4

Serum cholesterol, mg/dL

149.6 d

123.2

3.6

Body weight (April), kg

536.8

549.7

10.8

Body weight (September), kg e

551.1

528.6

10.1

14.2 d

-24.0

3.1

BCS (August)

5.2 d

3.8

0.15

Backfat at rump (August), cm

0.84

0.62

0.08

Backfat at rib (August), cm

0.48

0.37

0.04

Change in body weight, kg e

Adjusted calf weaning weight, kg e

210.8 c

195.8

4.5

aEndophyte-free rescue (n = 20). bEndophyte-infected fescue (n = 30). Cp < 0.02. d p < 0.001. eOne cow from E+ group removed (n = 29).

Pregnancy losses that occurred between 30 and 60 d pregnancy were 6.0 (E-) vs 15.0 (E+) + 8.0% (P > 0.10). Losses for two cows grazing E+ occurred between 56 and 60 d pregnancy, whereas the remaining losses occurred between 30 and 45 d pregnancy. All of these losses occurred after environmental temperatures rose above 37.8°C for three weeks (Figure 4). Daily maximum and minimum temperatures for August were recorded at the Booneville Human Development Center, which is located within 7 km from the research site to aid in interpretation of data (NOAA; 21; Figure 4). Total pregnancy losses that occurred by weaning (between 70 and 126 d pregnancy) were 5.5 (E-) vs 17.6 (E+) ± 8.0% (P > 0.10). Pregnancy losses at this time tended to be greater for Hereford compared with Angus or Angus × Hereford cows (Hereford, 28.0 ± 7.4%; Angus, 7.2 :~ 10.4%; Angus x Hereford, 0 ± 12.6%; P < 0.09). All but one of the cows that lost an embryo became pregnant again before the bull was removed. Interestingly, a negative relationship existed between serum concentrations of progesterone on day of PGF2a treatment and pregnancy loss for both treatments: y = 59.5 - 7.6x (P < 0.01), where y = pregnancy loss and x = serum progesterone. In other words, for every 1 ng/mL increase in progesterone, embryo loss decreased by 7.6%.

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6.5 --O-- E6.0 5.5 5.0 4.5 4.0 3.5 5/l/99

7/1/99

9/l/99

Month Figure 1. Least squares means and standard error of body condition scores of cows grazing endophyte-free (E-) or infected (E+) rescue between April and August.

240 --G-- E200 oO e"

160 120

O

80 40 50

100

150

200

250

Day of age Figure 2. Body weights of calves with cows grazing endophyte-free (E-) or infected (E+) fescue between April and August. Symbols represent predicted body weight per day of age.

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Table 2. Reproductive responses among cows on endophyte-free (E-) or infected (E+) tall fescue pastures. Values represent least squares mean + pooled standard error adjusted for treatment and breed effects for the number of cows in parenthesis. E-

E+

84.9 (20)

80.2 (30)

9.3

Pregnancy rate to synchronized estrus, %

41.7 (20)

46.8 (30)

10.4

Pregnancy rate at 30 days, %

93.8 (20)

93.5 (29)

5.5

Pregnancy rate at 60 days, %

86.7 (20)

81.2 (29)

9.0

Pregnancy rate at weaning a, %

89.7 (19)

84.8 (29)

8.3

Calving rate, %

85.1 (19)

85.0(28)

8.6

Serum progesterone on d of PGF2~ treatment, ng/mL

4.5 (20)

4.5 (30)

0.7

Serum progesterone, 30 d pregnancy, 7.8 (19) ng/mL aGestation length at weaning was between 70 and 126 d.

6.9 (25)

0.5

Estrus detection rate, %

Pooled SE

7O L

60

i E- ( n = 16) E+ (n = 22)

5O @ %.. 0

40 30

E 20

10 nl 0 0

2

3

4

5

6

Day after PGF treatment Figure 3. Percent of cows that responded to synchronization for each day after PGF2a treatment.

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45

40 35 "U 30 25 20 15 5

10

15

20

25

30

August 1999 Figure 4. Daily high and low air temperature for month of August. Arrows indicate approximate days where embryo losses occurred. DISCUSSION Cows and calves that grazed endophyte-infected tall fescue exhibited signs of fescue toxicosis (increased respiration rate and rectal temperature, decreased serum concentrations of prolactin and total cholesterol, body condition, and calf growth) as others have observed (for review see 22, 25). Despite this, pregnancy rates were not reduced in these cows. The authors are aware of two research locations, including the current one, with peer-reviewed reports of the negative impact of endophyte-infected fescue on pregnancy rates in English breed cattle (7, 8, 9, 13). In addition, there are several non peer-reviewed reports of decreased pregnancy or calving rates in heifers or cows grazing endophyte-infected fescue (2, 4, 19, 27, 33, 36, 37; Table 3). However, there are studies that found no decrease in pregnancy rate in cows grazing endophyte-infected fescue (16, 29) or exposed to ergotamine (3) or a decrease some years, but not others (9, 36, 37) or in some breeds of cattle (Angus), but not others (Brahman or Brahman cross; 8, 9, 10). Most studies reported relatively low numbers of heifers or cows used to determine pregnancy or calving rates (Table 3). Experiments used bulls for the entire breeding season (33), or rotated bulls to minimize confounding effects of male fertility and fescue toxicosis (4, 8, 9, 10, 13) while others used AI or ET (3, 13, 27, 29, 36, 37). In addition, environmental and management conditions among the studies were diverse, yielding pregnancy or calving rates that ranged from poor to acceptable for both pasture treatments. Differences in environmental temperature may contribute to a variable response of pregnancy rate to grazing endophyte-infected fescue. The response of an individual to heat stress may vary, as seen by a difference in rectal temperature among heat stressed heifers consuming a similar diet of 1.2°C (Burke, unpublished data). Embryonic development was greatly reduced when dairy cows were exposed to heat stress that caused rectal temperatures to rise to 41.1 °C (26). An animal that is more

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Table 3. Summary of pregnancy, conception, or calving rates on control forage vs endophyteinfected pasture reported in the literature. Number of animals per treatment is included in parenthesis when reported. Pregnancy, conception, or calving rate (number of animals) Report

Control pasture

E+ pasture d

Schmidt et al. (33)

96 a

55

Alabama

Ashley et al. (2)

100 b

54

Tennessee

Beers & Piper (4)

90 c'f (20)

80 (20)

Arkansas

Gay et al. (13)

94.6 a (74)

55.4 (92)

Kentucky

Washburn et al. (37)

74 b

78

McKenzie et al. (19)

85 a (20)

60 (20)

Tennessee

Rahe et al. (27)

73a'f (15)

57 (14)

Alabama

Rahe et al. (27)

72 a (15)

31 (16)

Alabama

Washburn & Green (36)

68 a (57)

47 (57)

North Carolina

82.1 i 3.2 c'e (167)

77.8 + 2.3 (153)

35.0a'f (20)

21.0 (19)

Brown et al. (7)

91.9 + 5. I c,e (87)

78.6 + 5.2 (86)

Arkansas

Barnett et al. (3)

32a'f (25)

50 (20)

Tennessee

Rorie et al. (29)

74 b'f

78

Arkansas

56.4 ± 7.2 (27)

Arkansas

Brown et al. (9) Mahmood et al. (16)

Brown et al. (8) 93.0 + 6.5 c'e (38) aPregnancy rate. b Concepnon rate. CCalving rate. dEndophyte-infected fescue. e Includes only Angus cows. fNot significant.

Geographic location

North Carolina

Arkansas Illinois

susceptible to heat stress may be more likely to lose an embryo under heat stress conditions. In addition, response of cattle to acute vs chronic or mild vs severe heat stress also may influence the degree of embryonic loss in a herd, contributing to differences in pregnancy rate among the studies (Table 3). Serum concentrations of total cholesterol were measured because cholesterol from the blood is used as a substrate for progesterone synthesis in the corpus luteum (23, 32, 39). Ryan et al. (30)

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reported decreased serum cholesterol in very thin cows (BCS 3) compared with cows in higher body condition for up to 12 d post-calving, but no differences existed by 16 d post-calving. Serum cholesterol was decreased in heifers fed endophyte-infected rescue seed compared with endophytefree fescue seed while condition among the heifers was similar (11). Similarly, concentrations of cholesterol were reduced in cows grazing endophyte-infected fescue pasture in the current study likely due to pasture treatment rather than decreased body condition. However, this did not lead to a change in serum concentrations of progesterone between the two treatments. Similarly, there was no change in progesterone in heifers fed ergotamine tartrate (36) or grazing endophyte-infected fescue 13 d after treatment with PGF_~,(1). In contrast, Estienne et al. (12) and Mahrnood et al. (16) observed a decrease in progesterone in heifers grazing endophyte-infected fescue. Burke et al. (11 ) reported no change in serum concentrations of progesterone between heifers fed endophyte-free or infected fescue seed under thermoneutral conditions. However, during heat stress, there was a decrease in progesterone in endophyte-infected fescue fed heifers. This suggests that differences in circulating progesterone between endophyte-free and infected fescue fed animals observed in the literature may be attributed to environmental temperatures that the animals were exposed to during sampling. Also, blood volume may become diluted, concentrated, or unchanged during heat stress (17, 28), which could alter steroid hormone concentrations in blood. Notably, the reduced serum progesterone at 30 d gestation in Hereford compared with Angus or Angus × Hereford cows likely led to increased pregnancy losses between 70 and 126 d gestation. A greater proportion of cows grazing E+ rescue responded to estrus synchronization 3 d after treatment with PGF2, compared with 4 d for cows grazing E- pasture. This could indicate a change in luteal dynamics due to consumption of E+ fescue. If PGF2Q production is increased in cows grazing endophyte-infected fescue as Browning et al. (10) observed after treatment with ergonovine or ergotamine, this could lead to increased rate of luteal regression. This may create a more susceptible environment for the corpus luteum to endogenous or exogenous PGF2,. However, serum concentrations of progesterone were not different on day of PGF2, treatment, suggesting that function of the corpus luteum was not impaired due to grazing endophyte-infected fescue. Hoveland (15) determined that annual economic loss to the cattle industry for reproductive reasons due to fescue toxicosis was more than $300 million. These losses were attributed to a 20% decrease in calving rate of cows grazing tall fescue in 21 tall fescue-growing states. Other factors may be involved in decreased calving rates in these states, including climate, environment, and management. The current study demonstrated that under good management conditions (animals and forage), pregnancy rate was not reduced for cows grazing endophyte-infected fescue. Further studies that focus on defining management conditions for ruminants grazing endophyte-infected tall fescue that yield acceptable pregnancy rates are necessary.

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