The estrous cycle of the ewe is resistant to disruption by repeated, acute psychosocial stress

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.

FIG. 1.

LH and cortisol profiles for one representative ewe kept under nonstress conditions (A) or exposed to the layered stress paradigm (B) on two occasions in experiment 2. The layered stress paradigm is depicted at the top in B and consisted of sequential hourly application of isolation, restraint, blindfold, and predator cues.

FIG. 2.

Mean prestress (closed circles) and immediate poststress (open and shaded squares) plasma cortisol concentrations in stress ewes in experiment 4 (A) and experiment 5 (B). The numbers above the poststress values depict the stressor used: 1 = barking dog, 2 = circadian stress, 3 = layered stress, 4 = mock shear, 5 = transport, 6 = noise/exercise, 7 = isolation, and 8 = blindfold/barking dog CD. Poststress values indicated by shaded squares denote a significant difference between pre- and poststress values as determined by paired t-test (P < 0.05, n = 6 ewes in experiment 4 and n = 8 ewes in experiment 5).

FIG. 3.

Mean daily plasma progesterone values in experiment 4 (A) for nonstress control (closed circles) and stress ewes (open circles), and in experiment 5 (B) for nonstress control (closed circles), diet-only (gray circles), and diet-plus-stress (open circles) ewes. The period of stress is depicted at the top of each panel. In experiment 4 (A), values from one stress ewe that expressed an abnormal luteal phase in cycle 3 were excluded. In experiment 5 (B), values were excluded once ewes ceased to express estrous cycles. In experiment 4 (A), n = 5–6 ewes/group, and in experiment 5 (B), n = 5–8 ewes/group.

FIG. 4.

Mean daily plasma progesterone profiles of three diet-only and two diet-plus-stress ewes that ceased to express estrous cycles during experiment 5. Sampling ended in ewe 12 (diet only) after the first missed estrous cycle.

FIG. 5.

Mean estrous cycle parameters in controls (open bars; n = 8), diet-restricted animals (with or without psychosocial stress) that continued to cycle (hashed bars; n = 11), and diet-restricted animals that subsequently ceased to cycle (closed bars; n = 5) in experiment 5. Once an animal displayed disrupted cyclicity, values were excluded from the analysis (ANOVA). *P < 0.02, **P < 0.01 compared to control and diet-restricted animals that continued to have normal cycles.