Maternal aggression in hamsters: effects of stage of lactation, presence of pups, and repeated testing

This study investigated maternal aggression in hamsters and examined the effects of early versus late lactation, presence or absence of the litters during the tests, and prior aggressive encounters. There was a total of six experimental groups. Two groups were tested in the presence of their litters on both Days 5 and 15 of lactation; two groups were presented with intruders after a 6-hr interval of mother-litter separation on Days 5 and 15 of lactation. The last two experimental groups were tested on Day 15 only in the presence of their litters or after a 6-hr separation from their litters. Estrous-cycling animals were also tested twice (10 days apart) or once to control for periods of social isolation. Animals were tested in their home cages for 10 min with weight-matched estrous-cycling intruders. Sexually receptive females were not used as controls or intruders. Measures of aggression included fights, attacks, chases, and intruder retreats. Lactating animals initiated significantly higher levels of all measures of aggression than cycling controls. There were no differences in aggression between Days 5 and 15 of lactation or between the groups tested in the presence or absence of their litters. Prior testing on Day 5 had little effect on aggressive responses on Day 15. The results are discussed in terms of comparisons to other species and the factors responsible for high levels of aggression during lactation.     

Short-day increases in aggression are independent of circulating gonadal steroids in female Siberian hamsters (Phodopus sungorus)

Among the suite of adaptations displayed by seasonally-breeding rodents, individuals of most species display reproductive regression and concomitant decreases in gonadal steroids during the winter. In addition, some species display increased aggression in short "winter-like" days compared with long "summer-like" day lengths. For example, male Syrian and Siberian hamsters held in short days express heightened levels of aggression that are independent of gonadal steroids. Virtually nothing is known, however, regarding seasonal aggression in female Siberian hamsters (Phodopus sungorus). Studies were undertaken to determine female levels of aggression in long and short days as well as the role of gonadal steroids in mediating this behavior. In Experiment 1, females were housed in long or short days for 10 weeks and resident-intruder aggression was assessed. Prior to testing, estrous cycle stages were determined by vaginal cytology and females were tested during both Diestrus I and Proestrus. In Experiment 2, hormone levels were experimentally manipulated; long-day females were ovariectomized (OVx) or given sham surgeries whereas short-day females were implanted with capsules containing 17beta-estradiol (E(2)) or Progesterone (P). In Experiment 3, both long- and short-day females were ovariectomized and implanted with either an exogenous E(2) or blank capsule, or given a sham surgery. Short-day hamsters displayed increased aggression relative to long-day females. Aggression was not affected by estrous stage. There was no difference in aggression between long-day OVx and sham animals. Furthermore, neither exogenous E(2) nor P had any significant effect on aggression. These results support previous findings of increased non-breeding aggression and suggest that short-day aggression is not likely mediated by circulating levels of gonadal steroids. These results also suggest that the endocrine regulation of seasonal aggression may be similar between the sexes.     

Effects of ergocornine and prolactin on aggression in the postpartum golden hamster

The effects on aggressive behavior of prolactin (PRL) and ergocornine hydrogen maleate, an inhibitor of PRL secretion, were investigated in the female golden hamster. Because high aggression and PRL levels are associated with lactation in hamsters, postpartum females were used as subjects. In the first experiment, three groups of ovariectomized and hysterectomized females were compared: normally lactating, ergocornine-treated, and ergocornine plus replacement PRL treated. Normally lactating mothers were typically aggressive towards males in an arena, whereas females given ergocornine were not. Females given both ergocornine and PRL showed an intermediate level of aggression. Although ergocornine suppressed aggression towards adult males, attacks on pups increased. A second experiment sought to determine if ergocornine would depress aggression when PRL involvement was unlikely. At least 30 days following pup removal, females from the first experiment were “trained” to attack home-cage intruders consistently. After ergocornine administration, home-cage attacks by these experienced females were not diminished. Since PRL levels were probably low in these animals, it was concluded that the effects of ergocornine on aggression were limited to instances in which PRL was involved, and that PRL probably can facilitate aggression.     

Enhancement and suppression of ultradian and circadian rhythms across the female hamster reproductive cycle

The impact of ovarian hormones on hamster ultradian rhythms (URs) is unknown. We concurrently monitored URs and circadian rhythms (CRs) of home cage locomotor activity during the estrous cycle, pregnancy, and lactation of Syrian hamsters. URs with a mean period of 4-5 h were evident during the dark phase in more than 90% of females on days 1 and 2 of the estrous cycle but were significantly less prevalent on cycle days 3 and 4. The period of the UR did not vary as a function of estrous cycle stage, but at all stages, the UR period was longer in the dark than the light phase. The UR acrophase occurred significantly earlier on cycle day 4 than on days 1 and 2, and UR robustness and amplitude were reduced on days 3 and 4. Robustness, mesor, and amplitude of CRs were greater during cycle days 3 and 4; timing of the CR acrophase was delayed on day 4 relative to all other cycle days. Effects of the estrous cycle on URs were evident only during the dark phase. The proportion of hamsters displaying dark phase URs increased significantly during early and late gestation and decreased during lactation. Pregnancy significantly increased UR complexity, robustness, and amplitude. The emergence of URs over gestation was paralleled by decrements in the robustness and amplitude of CRs, which also were absent in a significant proportion of dams during lactation but re-emerged at weaning of litters. The changing endocrine profile of the estrous cycle, hormonal dynamics of pregnancy and lactation, and nursing demands placed on dams are each associated with alterations in the expression of ultradian and circadian locomotor rhythms. Diminution of CRs and augmentation of URs may afford greater behavioral flexibility during life stages when interactions with mates and offspring are less predictable.     

Lack of sexual experience does not reduce the responses of LH, estrus or fertility in anestrous goats exposed to sexually active males

We investigated whether LH secretion, estrous behavior and fertility would differ between sexually inexperienced and experienced anestrous goats exposed to the males. Male goats were rendered sexually active during the reproductive rest season by exposure to 2.5 months of artificial long days. Two groups of anovulatory sexually inexperienced and sexually experienced does were exposed to males during 15 days (n = 20 per group). LH pulsatility was determined every 15 min from 4 h before to 8 h after introducing males (Day 0). Estrous behavior was recorded twice daily. Pregnancy rates were determined on Day 50. Fertility was determined at parturition. Male sexual behavior was registered on days 1 and 2 during 1 h. Before introducing the males, the number of LH pulses did not differ between groups. After introduction of the males, all females increased their LH pulsatility, but the number of pulses did not differ between sexually inexperienced and experienced goats. The proportion of females displaying estrous behavior with a high pregnancy rate and fertility did not differ between inexperienced and experienced goats. The sexual behavior of the males did not differ significantly between those interacting with sexually inexperienced or experienced goats. We conclude that goats can show substantial endocrine and reproductive responses to males, even in the absence of previous sexual experience, when sexually active bucks are used.     

An acute social defeat stressor in early puberty increases susceptibility to social defeat in adulthood

Syrian hamsters readily display territorial aggression. If they lose even a single agonistic encounter, however, hamsters show striking reductions in aggressive behavior and increases in submissive behavior, a distinct behavioral change that we have previously termed conditioned defeat. This acute social defeat stressor is primarily psychological and is effective in both males and females. Therefore, we maintain that this procedure presents an ideal model for studying behavioral and physiological responses to social stress. Here, we demonstrate that social avoidance following social defeat is a particularly useful dependent measure because of its sensitivity and stability between sexes and across the estrous cycle. In addition, we demonstrate that peripubertal hamsters exposed to a single, 15 min social defeat exhibit significantly more social avoidance 24 h later when compared with no-defeat controls. Later, defeated and non-defeated hamsters display similar agonistic behavior in adulthood indicating that the peripubertal defeat does not alter adult territorial aggression. After experiencing an additional social defeat in adulthood, however, the hamsters that experienced the pubertal defeat respond to the adult defeat with increased social avoidance when compared with hamsters that were defeated only in adulthood and with no-defeat controls. These data are the first to show that a single social defeat in puberty increases susceptibility to later social defeat in both males and females.     

Olfactory preferences, scent marking, and "proceptivity" in female hamsters

Two appetitive sexual behaviors of female hamsters, attraction to odors of males and vaginal scent marking, were investigated and the correlations of each to reproductive states were determined. Both estrous and diestrous females were more attracted to the odors of intact males than to the odors of females or castrated males; this differential attraction was more pronounced for estrous females. Lactating females, but not pregnant females, were also preferentially attracted to odors of intact males. Thus, odors alone provided sufficient information to allow sexual discrimination by females, and estrous, diestrous, and lactating females were preferentially attracted to odors of intact males whereas pregnant females were not. Reproductive condition had no influence on responses to odors of castrated males or diestrous females. Vaginal scent marking was strongly influenced by reproductive state: Marking frequency was low in estrous, pregnant, and early lactation females, but high in late lactation and diestrous females, suggesting a function of advertisement of approaching receptivity. Thus sexual preferences based on olfactory cues and vaginal scent-marking frequency differed in their relationships to reproductive conditions. It is suggested that in other species such relationships between appetitive sexual behaviors and reproductive condition will depend on the species social organization, ecological niche, and taxonomic group, and consequently that the concept of preceptive behaviors should be broadened to include all appetitive sexual behaviors of females, not just those that are correlated with the hormonal state characterizing estrus.     

Changes in tissue histamine during the estrous cycle, pregnancy and pseudopregnancy in the golden hamster

The histamine content of reproductive tissues and skeletal muscle was determined in the golden hamster during the estrous cycle, pregnancy, and pseudopregnancy. Histidine decarboxylase activity was measured in uterine implantation sites and intersites from Day 4 to Day 10 of pregnancy. Histidine decarboxylase was also measured in mesometria and placentas on selected days of gestation. During the estrous cycle, uterine and skeletal muscle histamine levels were highest on Day 2 and lowest on Day 4 of the cycle. The ovarian histamine content did not change significantly among the different stages of the cycle. While the histamine content of uterine implantation sites of attachment was high on Days 4 and measurable on Days 5 and 6 of pregnancy, the levels were below the limits of detection by Day 7. On the other hand, the highest levels of histamine were in the uterine interimplantation sites on Days 8 and 9. The ovarian levels of histamine were highest on Day 13 of pregnancy. Histamine in skeletal muscle did not change significantly during pregnancy. The histidine decarboxylase activity in the implantation sites began rising on Day 9 and increased dramatically on Day 10. Placental histidine decarboxylase activity was very high on Days 13 and 15. Overall, we observed changes in uterine and skeletal muscle histamine during the estrous cycle that may be explainable in light of previously reported changes in mast cell numbers and circulating estrogens. During pregnancy, histamine levels of implantation sites and implantation intersites varied, as did the histamine content of ovarian tissue. Histidine decarboxylase activity rises in the uterus and placental tissue after the formation of the placenta.     

Sex and estrous cycle differences in the display of conditioned defeat in Syrian hamsters

We have reported that there is a sex difference in the behavioral response to social defeat in hamsters. While previously defeated male hamsters fail to display normal territorial aggression and instead produce submissive/defensive behavior, a phenomenon that we have termed conditioned defeat (CD), only a small portion of previously defeated females exhibit CD. In Experiment 1, we tested the hypothesis that CD varies over the estrous cycle and found that previously defeated female hamsters tested on diestrus 2 and proestrus were more likely to exhibit CD than were females tested on diestrus 1 and estrus. In Experiment 2, we found that regardless of hormonal status, non-defeated females displayed normal territorial aggression, indicating that the behavioral changes observed in Experiment 1 were not due to a cyclic variation in submissive behavior independent of a previous defeat encounter. In Experiment 3, we found that females tested 4 days after defeat responded similarly to those tested 1 day after defeat suggesting that the hormonal status of females on the day of testing is a more important determinant of the behavioral response to defeat than is the hormonal status on the day of defeat training. Finally, in Experiment 4, we monitored anxiety-like behaviors in diestrous 1 and proestrous females in an open field arena and found that there was no effect of cycle on any of the observed behavioral measures, suggesting that the observed differences in CD are not the result of differences in generalized anxiety-like behaviors across the estrous cycle.     

Circulating immunoreactive inhibin, gonadotropin, and prolactin levels during pregnancy, lactation, and postweaning estrous cycle in the rat

Serum inhibin levels were measured by heterologous RIA during pregnancy, lactation, and the post-weaning estrous cycle in the rat and correlated with changes in serum FSH and LH and prolactin. Blood was serially collected by cardiac puncture under light ether anesthesia from adult Sprague-Dawley rats on alternate days throughout the experimental period. For the first 8 days of pregnancy, immunoreactive inhibin levels remained high, then gradually decreased to reach a nadir at Day 16, and subsequently rose steeply until parturition. The pattern of serum immunoreactive inhibin levels during early pregnancy does not support a corpus luteum source and the dramatic rise from Day 16 to Day 22 correlates with the recommencement of follicular development in the ovary. Inhibin levels decreased rapidly on the day after birth and were suppressed until Day 8 of lactation, slowly increasing thereafter to reach a plateau from Day 14 until weaning (Day 22.5 of lactation). These changes in inhibin levels positively correlated with LH and FSH and negatively with prolactin, and are consistent with an ovarian source for inhibin associated with the recommencement of follicular development resulting from the diminution of the suckling stimulus. Immediately after weaning, serum immunoreactive inhibin levels showed a 4-day cyclic pattern corresponding to the estrous cycle identified by vaginal smear. Inhibin levels peaked on the day of proestrus, reached a nadir on the day of estrus, and rose slowly during metestrus and diestrus to a new peak at proestrus. Serum FSH levels showed an inverse correlation to inhibin levels consistent with a feedback relationship with inhibin.     

Changes in hypothalamic and pituitary content of immunoreactive alpha-melanocyte-stimulating hormone during the gestational and postpartum periods in the rat

alpha-Melanocyte-stimulating hormone (alpha-MSH) was measured in the mediobasal hypothalamus (MH), median eminence (ME), preoptic-suprachiasmatic area (POA-SCN), anterior (AL), and posterior lobes (PL) of the pituitary gland during the gestational and postpartum periods in the rat. The content of alpha-MSH in the MH and POA-SCN compared to estrous levels was lower during the later days of gestation and decreased further in the MH during lactation in association with the elevated plasma prolactin (Prl). Distinct increases in the ME content of alpha-MSH compared to estrous levels occurred on Days 8 and 12 of the gestational period and Day 14 of the postpartum period. A significant increase in PL content of alpha-MSH compared to Days 5-11 and 17-20 occurred on Day 4 of gestation, and no significant changes were detected in the AP concentration of alpha-MSH throughout the period studied. In vitro, PLs and ALs from females on Day 4 of gestation secreted more alpha-MSH into the incubation medium than tissues from animals on Day 20. These results suggest that alpha-MSH of both brain and pituitary origin may play a role in mediating some of the physiological changes which occur during pregnancy and lactation.     

Male aggression and the sexual behavior of Japanese monkeys

The factors that regulate male aggressive behavior towards females during the mating season and their relationship to the sexual behavior of Japanese monkeys were investigated. Observations were made on the Shiga A troop in Nagano Prefecture for 132 days during both the non-mating and mating seasons in three successive years. As a result, chasing towards females was observed in males older than 4 years. The frequencies of this type of behavior increased in the mating season. The chasing rank of the individual males did not correlate with the male dominance rank but with the tree-shaking rank. Chasing was directed not only at estrous females but also at non-estrous females. Pairs of both sexes in which chasing was observed, tended to have sexual interactions. Both hormonal and social factors should be considered in the regulation of chasing. The role of aggression in the formation of new male-female bonds in discussed.     

Changes in plasma progesterone and prolactin concentrations during the annual cycle and the role of prolactin in the maintenance of lactation and luteal development in the Antarctic fur seal (Arctocephalus gazella)

Progesterone in Antarctic fur seals was undetectable from 1-2 days before parturition to 4-6 days after parturition. There was a rapid increase in progesterone to 20 ng/ml between 6 and 10 days post partum and this increase coincided with peak concentrations of oestradiol-17 beta at the time normally associated with oestrus and mating in this species. Newly formed corpora lutea were present in the ovaries by Day 9 post partum even though the seals had been isolated in an enclosure and not mated. Thereafter, progesterone remained detectable, but at a low concentration (5 ng/ml) throughout embryonic diapause. A similar pattern was observed in unmated females which suggests they enter a period of pseudopregnancy. Progesterone increased to 35 ng/ml between late February and mid-March, indicating activation of the corpus luteum at the end of diapause, and then declined slowly through the remainder of gestation. Plasma prolactin, measured against a human prolactin standard, was elevated from 1-2 days before parturition and peaked at 0-3 days post partum. It then declined slowly throughout the post-partum period and remained at a low level throughout embryonic diapause. Prolactin concentration declined to undetectable at the end of diapause and before the end of lactation. Reduction of prolactin secretion by injections of bromocriptine from Days 3 to 5 post-partum terminated lactation. Mothers, which normally leave their pups to feed at sea on about Day 7 post partum, did not continue to lactate beyond Day 7 although this did not appear to be associated with reduced prolactin secretion. Bromocriptine treatment appeared to prevent the post-ovulatory surge of progesterone although there was no long-term effect of bromocriptine on progesterone secretion during the early stages of embryonic diapause/pseudopregnancy. This study has shown that prolactin is an important hormone for maintaining early lactation in the fur seal and it probably also has a role in the control of ovulation and luteal development. Prolactin does not appear to be implicated in the control of lactation cycles in fur seals. Changes in plasma progesterone during the annual cycle show that the pattern in fur seals resembles that of some carnivores with embryonic diapause.     

Effects of reproductive state on vocalizations in squirrel monkeys (Saimiri sciureus)

Vocalizations and behavior of a group of 6 squirrel monkeys, 2 males and 4 females, were recorded during the nonbreeding and breeding seasons. Behavioral and physical criteria were used to determine the presence of estrus. During the breeding season the types of vocalizations uttered by estrous females changed, and the adult male increased his rate of vocalizing. Err vocalizations by estrous females were associated with increased following and initiation of affiliative behavior with the adult male, and may have functioned to facilitate these interactions. Errs appeared to be related to changes in female reproductive state rather than to the behavior of others. The adult male increased vocalizations associated with sexual and aggressive behavior (squeals and cackles), primarily in response to the estrous females' persistent initiation of interactions with him. We concluded that certain vocalizations in Saimiri reflected changes in the reproductive state of males and females, and functioned to mediate changes in social bonding during the breeding season.     

Lactation reduces prolactin levels in reproductively experienced female rats

Long-term alterations in prolactin (PRL) secretion following reproductive experience have been demonstrated in both women and female rats. In the rat, these changes include decreased PRL secretion in response to a dopamine antagonist challenge following ovariectomy, decreased post-coital diurnal and nocturnal prolactin surges in multigravid versus primigravid females, as well as decreased suckling-induced prolactin release in multiparous versus primiparous females. To date, there have been no studies examining PRL secretion following reproductive experience in cycling female rats. Studies in women, however, have demonstrated a reduction in basal PRL secretion during the menstrual cycle. The purpose of the present work was to determine whether similar changes occur in the rat during the estrous cycle and to what extent lactation is involved in these effects. In addition to examining PRL, potential parity-induced changes in estradiol secretion were also studied. The findings revealed a significant decrease in PRL levels during the afternoon of proestrus, which was only observed in primiparous females that had lactated. Significant differences in estradiol secretion were not detected following reproductive experience. Thus, a reduction in the PRL surge on the afternoon of proestrus is a consequence of reproductive experience that requires both pregnancy and lactation.     

Sexual behavior of the female porcupine Hystrix africaeaustralis

Porcupines are sexually active throughout the estrous cycle, and sexual behavior is not affected by the reproductive status and hormonal milieu of females. Increased female-male interactions during estrus are the only indications of behavioral changes during estrus. The lack of aggression shown by females to known males as opposed to aggression shown to strange males, the greater interest shown by males toward certain females, and the superior breeding success of these females suggest a pair-bonding mating system. Limited changes in female receptivity throughout the cycle might be of importance in maintaining the pair-bond.     

Patterns of sexual receptivity in the female musk shrew (Suncus murinus)

Female musk shrews (Suncus murinus) were tested daily to examine patterns of sexual receptivity. When only mounting was used as a criterion (to avoid pregnancy), nonpregnant females remained sexually receptive to males every day for 14 consecutive days. When insemination was allowed, most females continued to copulate for the first 5 days of pregnancy. Receptivity declined markedly around Day 10 of gestation, but a few females were receptive even into late pregnancy. Lactating females copulated with males 5 and 10 days after parturition. In general, unlike most mammals studied in the laboratory, the nonpregnant female musk shrew has no behavioral estrous cycle. Musk shrews are ready to mate anytime except in mild to late pregnancy, and even then occasionally mating is found.     

The estrogenic arousal of aggressive behavior in female mice

Experiments were conducted to determine the conditions under which estrogen would promote male-like aggressive behavior in female mice. The results of the first experiment showed that most females chronically exposed to testosterone propionate (TP) in adulthood fought, whereas females similarly treated with estradiol benzoate (EB) did not display aggression. Another experiment found that, when either TP or EB was administered on the day of birth, adult females displayed aggression in response to daily EB injections during adult life. Also, the potentiating effect of neonatal hormone exposure declined over the first 12 days postpartum, as 100% of the Day 0, 75% of the Day 6, and 0% of the Day 12 and 18 TP-treated females fought in response to daily injections of 40 μg of EB in adulthood. The final study showed that, under the test conditions employed, the failure of a chronic adult EB regimen to promote aggression was not due to a competing tendency to display female sexual behavior.     

Sexual behavior in female western lowland gorillas (Gorilla gorilla gorilla): evidence for sexual competition

Previous research in gorillas suggests that females engage in post‐conception mating as a form of sexual competition designed to improve their own reproductive success. This study focused on sexual behaviors in a newly formed group of western lowland gorillas (Gorilla gorilla gorilla) housed at Zoo Atlanta. All females engaged in mating outside their conceptive periods, although there was individual variation in the frequency of the behavior. An analysis of the presence/absence of sexual behavior found females, regardless of reproductive condition, were more likely to engage in sexual behavior on days when other females were sexually active. On these “co‐occurrence” days, females were significantly more likely to solicit the silverback, but copulations did not differ from expectation. The results find further evidence for sexual competition among female gorillas and suggest that this may occur throughout their reproductive cycle rather than only during pregnancy. Am. J. Primatol. 71:587–593, 2009. © 2009 Wiley‐Liss, Inc.     

Differential hormonal control of aggression and sexual behavior in female Syrian hamsters

These experiments were designed to test the effects of chronic estradiol treatment on aggression and sexual behavior in female hamsters. Isolated female hamsters were ovariectomized and tested for their behavioral responses to a group-housed, ovariectomized female hamster (aggression test) and a group-housed, intact male hamster (sexual behavior test). Following these baseline tests, the experimental females were implanted sc with Silastic capsules containing different concentrations of estradiol (100, 25, 10, or 0%) diluted with cholesterol and retested 3, 7, 10, and 14 days after implantation. High levels of aggression were observed on the baseline test, with no changes in aggression toward an intruder female observed for any implant group on subsequent tests. Despite these high levels of aggression toward another female, most of the estradiol-treated females (80% at 14 days) were sexually responsive in the presence of a male. There was no effect of Silastic estradiol concentration on sexual behavior, even though a range of serum estradiol levels (39–105 pg/ml) resulted. Lordosis latencies decreased and lordosis durations increased over the extent of estradiol treatment. Seventeen days after Silastic implantation, all females were injected with progesterone and retested. Estradiol-treated females showed an extreme reduction in aggression toward a stimulus female, as well as a further stimulation of sexual behavior after progesterone treatment. High levels of aggression in cholesterol-treated females (0% estradiol) were maintained even after progesterone injection, and these females never displayed any sexual responsivity. These results suggest that sexual behavior in the female hamster is sensitive to estradiol alone, whereas the inhibition of aggression requires the combination of estradiol plus progesterone.