The Estrous Cycle of the Ewe Is Resistant to Disruption by Repeated, Acute Psychosocial Stress1

Abstract

Five experiments were conducted to test the hypothesis that psychosocial stress interferes with the estrous cycle of sheep. In experiment 1, ewes were repeatedly isolated during the follicular phase. Timing, amplitude, and duration of the preovulatory luteinizing hormone (LH) surge were not affected. In experiment 2, follicular-phase ewes were subjected twice to a "layered stress" paradigm consisting of sequential, hourly application of isolation, restraint, blindfold, and predator cues. This reduced the LH pulse amplitude but did not affect the LH surge. In experiment 3, different acute stressors were given sequentially within the follicular phase: food denial plus unfamiliar noises and forced exercise, layered stress, exercise around midnight, and transportation. This, too, did not affect the LH surge. In experiment 4, variable acute psychosocial stress was given every 1-2 days for two entire estrous cycles; this did not disrupt any parameter of the cycle monitored. Lastly, experiment 5 examined whether the psychosocial stress paradigms of experiment 4 would disrupt the cycle and estrous behavior if sheep were metabolically stressed by chronic food restriction. Thirty percent of the food-restricted ewes exhibited deterioration of estrous cycle parameters followed by cessation of cycles and failure to express estrous behavior. However, disruption was not more evident in ewes that also encountered psychosocial stress. Collectively, these findings indicate the estrous cycle of sheep is remarkably resistant to disruption by acute bouts of psychosocial stress applied intermittently during either a single follicular phase or repeatedly over two estrous cycles.

Influences of the stress endocrine system on the reproductive endocrine axis in sheep (Ovis aries)

“…This study also found that ewes subjected to a variety of acute stressors during the follicular phase, such as food denial, unfamiliar noises, exercise and transportation, had no effect on the LH surge (Wagenmaker et al 2010). There was no difference in the mean latent period to the LH surge in the stressed ewes compared with the control ewes of this study (Wagenmaker et al 2010). This suggests that the type or intensity of the acute stressor may determine the effect of reproductive dysfunction in sheep; however, it contradicts the effects of transportation stress on the preovulatory LH surge observed in other research.…”

“…However, both acute and chronic stress-like levels of cortisol had no effect on sexual attractivity and proceptivity behaviours in this study (Papargiris et al 2011). On the contrary, another study found that the repeated exposure of ewes to acute psychosocial stressors over two oestrous cycles did not alter the incidence, timing, amplitude or duration of the preovulatory LH surge (Wagenmaker et al 2010). This study also found that ewes subjected to a variety of acute stressors during the follicular phase, such as food denial, unfamiliar noises, exercise and transportation, had no effect on the LH surge (Wagenmaker et al 2010).…”

“…On the contrary, another study found that the repeated exposure of ewes to acute psychosocial stressors over two oestrous cycles did not alter the incidence, timing, amplitude or duration of the preovulatory LH surge (Wagenmaker et al 2010). This study also found that ewes subjected to a variety of acute stressors during the follicular phase, such as food denial, unfamiliar noises, exercise and transportation, had no effect on the LH surge (Wagenmaker et al 2010). There was no difference in the mean latent period to the LH surge in the stressed ewes compared with the control ewes of this study (Wagenmaker et al 2010).…”

“…Stress-induced reproductive dysfunction is more likely attributed to chronic stress rather than acute stress and involves neuroendocrine action at the level of the hypothalamus, pituitary glands and gonads. Chronic stress is one of the major challenges in livestock production, as it can result in immune suppression, increased susceptibility to disease and reproductive dysfunction, potentially leading to undesired fitness consequences and failure to meet full genetic potential (Wagenmaker et al 2010). Macfarlane et al (2000) suggested that stresslike concentrations of cortisol may actually arrest follicular development prior to maturation, which could lead to stress related infertility in ewes.…”

Impact of psychosocial stress on gonadotrophins and sexual behaviour in females: role for cortisol?

“…There have been many studies in a range of species to show that various stressors interfere with the LH surge and these have been extensively reviewed (Dobson & Smith 2000, Smith & Dobson 2002, Tilbrook et al 2002, Turner et al 2002a, 2005, Breen & Karsch 2006b, Dobson et al 2012. These stressors include (1) transportation that delays or attenuates the LH surge in sheep and cows (Dobson 1987, Nanda et al 1990, Dobson et al 1999, (2) injection of insulin that delayed the LH surge in ewes (Saifullizam et al 2010), (3) metabolic stress caused by caloric restriction that can disrupt and stop oestrous cycles in ewes (Wagenmaker et al 2010), (4) restraint that can block the preovulatory surge in rats (Roozendaal et al 1997a,b) and (5) immune/inflammatory stress that suppresses pulsatile LH secretion during the preovulatory period in sheep (Battaglia et al 2000) and delays or blocks the LH surge in follicular phase ewes, cows and monkeys (Peter et al 1989, Xiao et al 1998, Battaglia et al 2000. With respect to immune stress, endotoxin was shown to disrupt the oestradiol-induced LH surge in ovariectomized ewes by interfering with the early activating effects of the oestradiol signal (Battaglia et al 1999) and by acting centrally to suppress the secretion of GNRH (Breen et al 2004a).…”