Interactions of partners in family pairs,care of the offspring,and the role of tactile stimulation in formation of parental behavior of the Mongolian gerbil (<Emphasis Type="Italic">Meriones unguiculatus</Emphasis>) under laboratory conditions

The interactions of sexual partners and care of the offspring in male and female Mongolian gerbils reared in biparental and uniparental family groups (without an adult male) were compared. In individuals reared in biparental family groups, sexual differences related to the manifestation of parental care were small and statistically insignificant. In individuals reared in uniparental groups, the interactions of sexual partners related to grooming changed; the duration in males decreased threefold, as compared to the norm; indices of parental behavior of females and, especially of males, related to tactile stimulation of pups (huddling with pups in the nest and duration of licking pups) also decreased. The importance of the parental contribution of males, especially of tactile stimulation, in the evolution of the family-group mode of life is discussed.     

Marking behavior is innate and not learned in the Mongolian gerbil.

We studied whether marking behavior in Mongolian gerbils would be innate or learned behavior. The marking behavior was defined as "animals rubbing their abdominal scent glands on small protruding objects". Between 21 and 90 days of age, Mongolian gerbils, which were kept under such conditions that they would be unable to learn this behavior, were observed at intervals of 5-15 days to find out if there were signs of the behavior or not. Six male and four female Mongolian gerbils were used for observing. Neonate Mongolian gerbils during the age of 3 to 28 days were fostered by ICR mother mice. Weaning Mongolian gerbils were then individually kept away from the others. Marking behavior was observed in 2 out of 6 males at 50 days of age and 2 of 4 females at 60 days and the mean frequency of the marking behavior for 10 min was 3.5 in the males and 5.0 in the females. These results suggest that marking behavior was innate and not learned behavior in Mongolian gerbils.     

Lifespan ontogeny of breeding and reproductive success in Mongolian gerbils

An analysis was made of demographic data collected from a colony of Mongolian gerbils (Meriones unguiculatus). The data on births of over 3800 gerbils provide evidence on several aspects of development and fecundity. Approximately 4% more females than males survived to weaning. Mean number of pups per dam per year was estimated to be 48.3, greater reproductive success than reported previously. The shortest period of gestation resulting in viable pups was 25 days. Implantation was delayed by the presence of suckling pups. When gestation was prolonged, there was a direct relationship between the number of pups being suckled concurrently and the length of the delay. Length of gestation did not affect the size of the subsequent litter. Female gerbils gave birth as early as 72 days of age. Gerbils continued to reproduce until after 2 years of age in some cases. There were fewer pups per litter born to older females, fewer pups per litter with increasing parity, and longer intervals between litters with increasing age.     

Hormonal Responses of Male Gerbils to Stimuli from Their Mate and Pups

Following copulation and cohabitation with a pregnant female, male gerbils show high levels of parental behavior toward their pups. The initiation of male parental behavior may be the result of neuroendocrine changes induced by cohabiting with the pregnant female or by pup stimuli. Experiment 1 examines the changes in androgen and prolactin levels in male gerbils cohabiting with females over the reproductive cycle. Gerbils were mated and blood samples taken from males for hormone analysis 1, 10, and 20 days after pairing and 3, 10, and 20 days after pups were born. A group of unmated male gerbils served as controls. Plasma prolactin levels of males were elevated throughout the female's pregnancy and lactation periods, but were only statistically significantly higher than those of unmated males 20 days after pups were born. Androgen levels rose during pregnancy and dropped significantly after the birth of the pups. These hormonal changes are similar to those found in males of monogamous birds and differ from those found in males of polygynous rodents such as the rat. Experiment 2 examined the hormonal responses of male and female gerbils to pup replacement after 4 hr of parent–pup separation. Female gerbils showed a significant elevation of prolactin levels 1 hr after pup replacement, but males did not. Males with pups returned showed no difference in androgen levels from males who did not have pups returned. Thus, male gerbils show neuroendocrine changes following long-term cohabitation with their mate and pups, but do not show acute hormone responses to pup removal and replacement. These results indicate that parental males have neuroendocrine changes associated with parental behavior and these differ from the neuroendocrine changes underlying female parental behavior.     

Paternal experience and stress responses in California mice (Peromyscus californicus)

Paternal behavior greatly affects the survival, social development, and cognitive development of infants. Nevertheless, little research has been done to assess how paternal experience modifies the behavioral characteristics of fathers, including fear and stress responses to a novel environment. We investigated long-term behavioral and physiologic effects of parental experience in mice (Peromyscus californicus) and how this response activates the hypothalamic-pituitary-adrenal axis (as measured by corticosterone and dehydroepiandrosterone [DHEA] levels) and interacts with anxiety-related behaviors. Three groups of adult males were tested--fathers exposed to pups, virgins exposed to pups, and virgins never exposed to pups--in 2 environments designed to elicit anxiety response: an open field with a novel object placed in the center and a closed cage containing a sample of a component of fox feces. Behavioral responses were measured by using traditional methods (duration and frequency) and behavioral-chain sequences. Results indicated that paternal experience significantly modifies a male mouse's behavioral and physiologic responses to stress-provoking stimuli. Compared with inexperienced male mice, experienced male mice had a significant decrease in the occurrence of incomplete behavioral chains during the exposure to the novel object, an index of reduced stress. Further, even moderate pup exposure induced behavioral modifications in virgin male mice. These behavioral responses were correlated with changes in corticosterone and DHEA levels. Together, these data provide evidence that interactions between male mice and offspring may have mutually beneficial long-term behavioral and physiologic effects.     

Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles

This study examined whether neonatal paternal deprivation (PD: father was removed and pups were raised just by mother) or early deprivation (ED: pups were raised by both parents except separated from not only the dam but also the peers for three hours a day from PND 0 to 13) has long-term effects on anxiety and social behaviors of adult mandarin voles. Newborn mandarin voles of F2 generation were randomly assigned to one of three groups: bi-parental care (PC: pups were raised by both parents), PD and ED. The parental care behaviors of F1 generation were observed at the age of 0, 13 and 21 days (PND 0, 13, 21) of F2 generation of PC and PD groups. Moreover, each mandarin vole of F2 generation received an open field test and a social interaction test on PND 70 and PND 75, respectively. No significant differences of parental behavior were observed between mothers and fathers from PC families, showing typical parental behavior of socially monogamous rodents. In addition, no significant differences of maternal behaviors were found between mothers from PC and PD families, indicating no maternal compensation towards pups for the absence of the paternal care. In the open field test, mandarin voles from both PD and ED families displayed higher levels of anxiety and lower locomotor activity, relative to offspring of PC family. In the social interaction test, both PD and ED mandarin voles also showed lower levels of social behavior and higher levels of anxiety. Thus, both PD and ED significantly increase anxiety and reduce social behavior of adult mandarin voles, suggesting that variation in parental investment may lead to variation in anxiety and social behaviors in rodents with different mating systems.     

The Roles of Stimuli from Young, Previous Breeding Experience, and Prolactin in Regulating Parental Behavior in Ring Doves (Streptopelia risoria)

In addition to stimulating crop "milk" formation in ring doves, prolactin (PRL) may promote the parental regurgitation behavior that transfers this "milk" to the young at the time of hatching. Although earlier studies suggest that previous breeding experience is an important modulator of PRL-induced parental regurgitation behavior in ring doves, the ways in which experience, hormones, and stimuli from young interact to promote parental behavior have not been well characterized in this species. In the first study, untreated, nonbreeding female doves with and without previous breeding experience were given 10 daily parental behavior tests (2 h/day) with a hungry 5- to 10-day-old foster squab. Experienced females exhibited a higher incidence of regurgitation behavior, defensive behavior, and crouching or sitting in the nest than did inexperienced females. In a second study, nonbreeding females were given 10 daily tests for parental behavior while they received sc injections of ovine PRL or vehicle. Prolactin reduced squab-directed aggression and increased the incidence of regurgitation feeding behavior of foster squabs in both experienced and inexperienced females. However, the average number of regurgitation feeding acts displayed by those PRL-treated females that showed the behavior was over eight times higher in experienced females than in inexperienced females. Previous experience also enhanced the stimulatory effects of PRL on defensive behavior and crouching or sitting in the nest. The parental behavior exhibited by nonbreeding, PRL-treated experienced females was qualitatively and quantitatively similar to that observed in normally breeding females during a single test with their own hungry 5- to 10-day-old squabs. These findings indicate that PRL and previous breeding experience both enhance the parental responsiveness of nonbreeding female doves and that under optimal hormonal, experiential, and squab exposure conditions, nonbreeding doves exhibit levels of parental activity that rival those of normally breeding parents.     

食物诱导长爪沙鼠集群贮食的野外实验设计及其在社群研究中的应用

长爪沙鼠为典型的群居性鼠类。在自然条件下该鼠的集群贮食活动随时可为人工投放的种子食物所导引。本文依据组群个体合作贮食的习性,并结合剪趾和染毛双重标记的重捕跟踪方法设计了着重观测社群结构、群内个体序位、领域边界及相关社群行为的野外实验。据2(X)2年5月对4个相邻洞群的观测结果分析表明,应用此法便于在复杂的社群环境中直接确认组群成员及其属性,亦便于分辨同一组群或不同组群成员之间发生的行为事件及相关过程,且能在重复实验中得以验证。为在野外条件下定量研究长爪沙鼠社群行为提供了一种便捷可靠的观测方法。     

Parental behaviour in Mongolian gerbils (Meriones unguiculatus). II. Parental interactions

Twelve pairs of Mongolian gerbils were observed raising 15 litters. Both parents performed parental activities. Within pairs, associations were found between the behaviours of the parents. If one parent was active outside the nest, the other was likely to be relatively inactive in the nest. These non-random behavioural associations existed even though overall activity tendencies of members of pairs were similar. As a consequence of these patterns of behaviour, the pups were seldom left unattended, and the adaptive significance of parental presence is discussed.     

不同生活史阶段长爪沙鼠尿标记行为的遗传和空间距离效应

气味标记普遍存在于哺乳动物类群中,它能向同类传达领地占有、社会等级及繁殖状态等多种信息。2014年4月至10月,我们在内蒙古锡林郭勒正蓝旗对长爪沙鼠 (Meriones unguiculatus) 野外种群进行了标志重捕,采用中立场的方式测定了不同社群间同性别长爪沙鼠的尿标记行为。通过建立洞群样地坐标后用勾股弦方法计算群间距离,并用微卫星DNA分子标记估算个体间的亲缘系数,以探讨野生动物标记行为是否受个体间空间和遗传距离的影响。广义线性混合效应分析显示,雄鼠间的尿标记强度在繁殖期和贮食期受空间距离或遗传距离的影响均不显著。繁殖期雌鼠间的尿标记强度受空间或遗传距离的影响亦不明显,但在贮食期,遗传距离对雌鼠间标记的强度有显著影响,且遗传距离与空间距离对标记强度有明显的交互作用。本研究结果暗示亲缘关系和空间距离对长爪沙鼠的尿标记行为具有一定影响,这与长爪沙鼠的繁殖或贮食行为相适应。     

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)

In the laboratory rat and mouse, neonatal handling enhances hippocampal-dependent learning in adulthood, an effect mediated by changes in maternal behavior toward the handled young. In the present study, we examined the interaction between neonatal handling and biparental care during the early postnatal period and its effect on cognitive function in adult California mice (Peromyscus californicus). We characterized the parental behavior of handled and nonhandled father-present and father-absent families over the first 15 days of life. We then assessed cognitive performance of male and female offspring in the Barnes maze and object recognition test after they were 60 days of age. We found that the amount of licking and grooming received by pups was decreased in father-absent families. By postnatal days 12-15, licking and grooming in handled, father-absent families were equivalent to that of nonhandled, father-present families. Handling enhanced novel object recognition in father-present male mice with no effect in females. In the nonhandled group, the presence of the father had no effect on object recognition learning in male or female mice. Handling also enhanced spatial learning in the Barnes maze. In nonhandled families, the presence of the father appeared to have no effect on spatial learning in the male offspring. Interestingly, spatial learning in nonhandled, father-absent, female offspring was similar to that of handled animals. The average amount of licking and grooming received by pups was negatively correlated with the average number of errors made on the first day of reversal training in the Barnes maze. These data support previous findings that neonatal handling facilitates learning and memory in adulthood, suggest that under certain environmental conditions, there is a sex difference in the response of pups to paternal care, and further demonstrate the importance of active parental investment for offspring cognitive development.     

Mongolian gerbil fathers avoid newborn male pups, but not newborn female pups: olfactory control of early paternal behaviour

We examined effects on the parental behaviour of male Mongolian gerbils, Meriones unguiculatus, of the sex and number of pups in a litter. Recent fathers interacting with foster litters consisting entirely of newborn males decreased the time that they spent in contact with a litter the greater the number of pups it contained. However, fathers that interacted with litters composed entirely of newborn females showed no change in the time they spent in contact with a litter as a function of its size. Fathers responded similarly to litters of 1- and 3-day-old female pups, but their responses to male pups changed from avoidance to approach as the age of males increased from 1 day to 3 days, and fathers made anosmic by intranasal administration of zinc-sulfate solution did not avoid neonatal litters. Results of a correlational study revealed that the more time males spent with newborn young during a 30-min test, the greater their latency to mate with their partners in postpartum oestrus and the shorter the duration of their mating effort during the 24 h immediately after parturition. We discuss these findings as consistent with the view that androgen-mediated olfactory stimuli produced by newborn male Mongolian gerbils make them unattractive to fathers, possibly functioning to increase the time that recent fathers mate-guard while their partners are in postpartum oestrus.     

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.     

Corticotropin-releasing hormone inhibits maternal behavior and induces pup-killing

Behavioral responses to stressors and the effects of stressors on maternal behavior change with mothering experience. Corticotropin-releasing hormone (CRH) is released by stressors and produces stress-like behavioral effects. We tested the effects of ICV infusion of ovine CRH (0.5-4 ug) on pup-directed behaviors in ovariectomized, ovarian steroid-treated virgin rats that were either naive to pups or that had three days of mothering experience. CRH inhibited maternal behavior in naive and experienced rats in a dose-related manner. The magnitude and duration of inhibition, especially at the 1 ug dose, were less in rats with mothering experience. Higher doses of CRH (1 - 4 ug) significantly increased pup-killing in rats that were naive to pups. In contrast, CRH produced no pup-killing in rats with mothering experience.     

Alloparenting experience affects future parental behavior and reproductive success in prairie voles (Microtus ochrogaster)

Various hypotheses have been proposed to explain the function of alloparental behavior in cooperatively breeding species. We examined whether alloparental experience as juveniles enhanced later parental care and reproductive success in the prairie vole (Microtus ochrogaster), a cooperatively breeding rodent. Juveniles cared for one litter of siblings (1EX), two litters of siblings (2EX) or no siblings (0EX). As adults, these individuals were mated to other 0EX, 1EX or 2EX voles, yielding seven different pair combinations, and we recorded measures of parental behaviors, reproductive success, and pup development. As juveniles, individuals caring for siblings for the first time were more alloparental; and as adults, 0EX females paired with 0EX males spent more time in the nest with their pups. Taken together, these results suggest that inexperienced animals spend more time in infant care. As parents, 1EX males spent more time licking their pups than 2EX and 0EX males. Pups with either a 1EX or 2EX parent gained weight faster than pups with 0EX parents during certain developmental periods. While inexperienced animals may spend more time in pup care, long-term benefits of alloparenting may become apparent in the display of certain, particularly important parental behaviors such as licking pups, and in faster weight gain of offspring.     

Social suppression of female reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils

In several cooperatively breeding species, reproductively suppressed, nonbreeding females are attracted to infants and routinely provide alloparental care, while breeding females may attack or kill other females' infants. The mechanisms underlying the transition from alloparental to infanticidal behavior are unknown. In this study, we tested the hypothesis that this transition is associated with cessation of reproductive suppression and onset of ovarian activity in the Mongolian gerbil (Meriones unguiculatus), a cooperatively breeding rodent. Young female gerbils were housed with their natal family (FH), with a female pairmate (PH) or singly (SH). When females were either 11-13 or 16-18 weeks of age, we characterized their behavioral responses to an unfamiliar pup, reproductive development, and plasma progesterone, cortisol, and prolactin concentrations. In both age groups, FH females were significantly less likely to attack pups than PH or SH females and in fact never did so. FH females also had smaller ovaries and uteri, less developed scent glands, and lower progesterone levels, and were more likely to be anovulatory than PH or SH females, especially in the 11- to 13-week-old age group. Prolactin concentrations did not differ with reproductive status but were significantly higher in females that did not attack pups than in those that did. We found no other significant associations, however, between reproductive or endocrine measures and behavioral responses to pups. These results suggest that cohabitation with the natal family inhibits both infanticidal behavior and reproductive maturation in young female gerbils but that these two effects may not be causally related.     

Parental behaviour in the Mongolian gerbil (Meriones unguiculatus). I. Retrieval

Twelve pairs of Mongolian gerbils rearing 15 litters were tested for their responses to their own pups placed outside the nest area. All females and 3 of 12 males retrieved pups. Fewer pups were retrieved and more returned to the nest by themselves as the pups matured. The female's latency to retrieve pups also increased as the pups grew older. Due to retrieval by both parents and the spontaneous return of pups, few pups were left outside the nest after scattering. The possible mechanisms by which parental retrieval is elicited are discussed.     

Paternal behavior in the Mongolian gerbil (Meriones unguiculatus): Estrogenic and androgenic regulation

Here, we analyzed the effects of testosterone (T) and its metabolites, estradiol (E₂) and dihydrotestosterone (DHT), on the onset of paternal behavior in virgin male Mongolian gerbils (Meriones unguiculatus). We hypothesized that T and E₂, but not DHT, would facilitate the onset of paternal behavior. Seventy males displaying aggression toward pups were selected through a paternal behavior screening test. Forty males were bilaterally castrated. Of them, 10 were implanted with T, 10 with E₂, and 10 with DHT, and 10 received no treatment. Another 30 males underwent a sham procedure. In these gerbils, T, E₂ and DHT were measured to obtain the basal levels of these hormones. After treatment, the paternal behavior test was conducted again. Blood samples were obtained immediately after the administration of the test for the quantification of T, E₂ and DHT by radioimmunoassay. Surprisingly, 100% of the males that received T, E₂ and DHT implants stopped being aggressive and became paternal. Castrated and sham-operated males displayed no changes in their aggressive behaviors. This is the first report that T and its metabolites are involved in neuroendocrine mechanisms that inhibit aggression toward pups and facilitate paternal behavior in virgin male Mongolian gerbils. In addition, this is the first report of regulation of paternal behavior in a rodent by estrogenic and androgenic pathways.     

棕色田鼠幼仔对父鼠的早期识别及条件位置偏爱

群居性动物的幼仔对亲本的识别有利于获得最大化的亲本抚育。雄性棕色田鼠对幼仔具有较高水平的父本投资,那么幼仔在断乳前是否能够识别父鼠并形成条件位置偏爱(Conditioned place preference,CPP)呢?本研究通过双向选择测试、社会互作测试以及CPP 测试探讨了这一问题。双向选择结果显示,与陌生雄鼠相比,出生后14 d 和21 d 的幼仔对父鼠访问的持续时间及潜伏期有显著性差异(P < 0.05);社会互作结果表明,14 d幼仔对父鼠的跟随行为较陌生雄鼠多,但探究行为及亲密行为没有显著性差异(P > 0.05),21 d 幼仔对父鼠的探究行为较少、跟随行为和亲密行为较多(P < 0.05)。CPP 结果表明,在连续4 d (出生后13 ～ 16 d;19 ～ 22 d)的父鼠强化后,第17 d 和第23 d 的幼仔不能形成对父鼠的位置偏爱(P > 0.05)。这些结果说明断乳前的棕色田鼠幼仔已能够识别父鼠和陌生雄鼠,但不能形成对父鼠的位置偏爱。     

Effects of repeated pup exposure on behavioral,neural, and adrenocortical responses to pups in male California mice (Peromyscus californicus)

In biparental mammals, the factors facilitating the onset of male parental behavior are not well understood. While hormonal changes in fathers may play a role, prior experience with pups has also been implicated. We evaluated effects of prior exposure to pups on paternal responsiveness in the biparental California mouse (Peromyscus californicus). We analyzed behavioral, neural, and corticosterone responses to pups in adult virgin males that were interacting with a pup for the first time, adult virgin males that had been exposed to pups 3 times for 20 min each in the previous week, and new fathers. Control groups of virgins were similarly tested with a novel object (marble). Previous exposure to pups decreased virgins' latency to approach pups and initiate paternal care, and increased time spent in paternal care. Responses to pups did not differ between virgins with repeated exposure to pups and new fathers. In contrast, repeated exposure to a marble had no effects. Neither basal corticosterone levels nor corticosterone levels following acute pup or marble exposure differed among groups. Finally, Fos expression in the medial preoptic area, ventral and dorsal bed nucleus of the stria terminalis was higher following exposure to a pup than to a marble. Fos expression was not, however, affected by previous exposure to these stimuli. These results suggest that previous experience with pups can facilitate the onset of parental behavior in male California mice, similar to findings in female rodents, and that this effect is not associated with a general reduction in neophobia.