The present study examined the effects of first pregnancy and nursing behavior on postpartum infertility in seasonally breeding rhesus monkeys to assess whether prolonged lactational infertility observed in adolescent mothers is due to a particular pattern of nursing or to decrements in body growth rates. After a successful first pregnancy, a significant percentage of the lactating adolescent mothers (57.1%; n = 8) failed to exhibit an ovulation with normal luteal phase during the subsequent breeding season. In contrast, the remaining lactating adolescents (42.9%, n = 6) and all of the adult mothers (100%, n = 6) exhibited ovulations with a normal luteal phase. Age alone was not the critical variable, since all nonlactating adolescents exhibited ovulations with normal luteal phase parameters in the subsequent breeding season. The luteal phase abnormalities exhibited by the subset of lactating adolescent females were characterized by an inadequate luteal phase (ILP) and by significantly lower serum levels of progesterone, estradiol, and bioactive luteinizing hormone. The occurrence of these ILP ovulations was associated with more frequent nursing bouts prior to ovulation and during the subsequent luteal phase. In contrast, nursing patterns for adult females who had ovulations with normal luteal phases were more similar to those of the infertile lactating adolescents exhibiting significantly longer and more frequent nursing bouts, suggesting that fully adult females may be less sensitive to the inhibitory aspects of a suckling stimulus. Differences in luteal phase function among lactating adolescents were not related to differential rates of ponderal or skeletal growth. A still-developing neuroendocrine system may thus render a significant proportion of adolescent females more sensitive to suckling-induced suppression of gonadotropin secretion.
Rhesus monkeys housed outdoors exhibit a distinct breeding season limited to the fall and winter months. Four groups of female rhesus monkeys, multiparous nonlactating (MNL; n = 8), multiparous lactating (ML; n = 6), primiparous lactating (PL; n = 3) and nulliparous first-time ovulators (N; n = 6) were studied to investigate the influence of age, parity, and social dominance rank on the parameters of the breeding season. MNL exhibited the longest season (146 days), and PL the shortest (70 days), with N (106 days) and ML (89 days) intermediate. PL females also had a significantly reduced percentage of normal ovulations compared to other groups. Neither body weight nor estimates of body fat were related to either the timing of the ovulatory season or the quality of ovulations within the season. Parity and social dominance rank were significantly related to the percentage of normal ovulations (r = 0.85), with low-ranking, primiparous females exhibiting the fewest normal ovulations. These data indicate that the presence of a suckling infant acts synergistically with environmental factors to determine the parameters of the breeding season. Furthermore, postpubertal females may be more responsive to those factors that terminate the breeding season, and some factor independent of body weight but associated with low social dominance rank and/or primiparity renders females less capable of normal luteal function during the breeding season.
Rhesus monkeys housed in an outdoor environment are seasonal breeders, with ovulations and concomitant sexual behavior limited to the fall and winter months. To determine if there is a seasonal difference in the capacity of physiological levels of estradiol (E2) to induce sexual behavior in ovariectomized rhesus monkeys housed outdoors, subjects living in a social group were treated with subcutaneous E2 implants in a counter-balanced design during the nonbreeding season (May-July) and during the breeding season (September-November). Serum E2 levels were monitored by obtaining blood samples twice a week. Three levels of E2 were studied: baseline (less than 30 pg/ml), follicular (100 pg/ml), and periovulatory (200 pg/ml). Two of five adult males in the group were injected with human chorionic gonadotropin (hCG) twice a week to insure that males with high testosterone levels were present during each season. Focal observations of behavior of 15 minutes' duration on each subject were conducted 5 days per week, with frequencies and durations of social, sexual, and solitary behaviors recorded. Concomitant 2-h group scans were made to record all occurrences of mounting behavior. Neither heterosexual serial mounting nor seminal plugs were ever observed in E2-treated females during the summer months. In contrast, copulation and seminal plugs were observed in subjects at both treatment levels during the fall. While E2-treated females engaged in homosexual mounting behavior during both summer and fall, E2 treatment resulted in heterosexual copulation only during the fall. Changes in patterns of social behavior paralleled changes in sexual behavior and were significantly affected by treatment and season, with more male-female interactions during the fall months.(ABSTRACT TRUNCATED AT 250 WORDS)
The seasonal restriction of ovulations in rhesus monkeys is thought to be due to enhanced estradiol (E2)-negative feedback suppression of luteinizing hormone (LH) during the spring and summer anovulatory months. This hypothesis was examined in seven ovariectomized monkeys housed in an outdoor environment and treated with various doses of E2 in a counterbalanced design during both the anovulatory season (May-Jul) and the breeding season (Sep-Nov). Subcutaneous implants of E2 produced levels that mimicked late follicular (LF-100 pg/ml) or periovulatory concentrations (PO-190 pg/ml). Analyses of twice weekly serum samples revealed that during the period of no E2 treatment (NT), basal levels of bioactive LH were significantly lower in the summer than the fall. Although treatment with both doses of E2 lowered basal LH levels during both seasons, the decrease in LH was significantly greater during the summer. Samples collected at 15-min intervals for 2 h revealed that during NT, LH pulses were significantly slower during the summer than in the fall, whereas pulse amplitude did not differ between seasons. Treatment with both doses of E2 either abolished or significantly reduced both LH pulse amplitude and frequency in the summer. In contrast, LH pulses during the fall were not affected by E2 treatment. Response to treatment with LH-releasing hormone (5 micrograms/kg i.v.) revealed that release was significantly reduced during E2 treatment in the summer. These data indicate that seasonal changes in the environment influence both nongonadal control and E2-negative feedback inhibition of LH secretion. The reduced ability of E2 to maximally suppress LH release in the fall can thus account for the seasonally delimited pattern of ovulations observed in rhesus monkeys.
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