Reproduction in the crowned lemur (Lemur coronatus) in captivity

Four pairs of captive crowned lemurs (Lemur coronatus) were studied during their annual breeding season in order to obtain baseline data on their reproductive biology for comparison with other Lemur species and to enhance their captive breeding success. Vaginal smears, testicular measurements, and records of the Duke University Primate Center provided the presented data. During a single breeding season, females cycled an average of three times, with an average cycle length of 34 days. Cycles were detected between November and March. Vaginal estrus and copulations were limited to one day per cycle. After 125 days of gestation females gave birth to one or two young. Both sexes attained sexual maturity at an age of about 20 months. Mean male testis size peaked in late December; at the same time, three of the females experienced their first estrus. Based on all available data, there was a significant positive correlation between cycle length and gestation length in the genus Lemur.     

Breeding performance of a captive colony of rhesus macaques (Macaca mulatta)

For most of the 18 years recorded, fewer than 50% of the adult females gave birth in any one year. The colony, of 6 social groups, showed a clear-cut breeding season. Female parity and dominance had no effect on breeding rate, though 1st infants were born earlier in the year than 2nd-born ones. Only when females gave birth in successive years were the months of giving birth correlated. Mothers and daughters may tend to give birth closer in time within a breeding season than do other females.     

Social control of reproduction in banded mongooses

Recent theoretical work suggests that the distribution of reproduction, or degree of reproductive skew, in animal societies depends crucially on (1) whether dominant individuals can fully control subordinate reproduction, and (2) how subordinate reproduction affects the fitness of dominants. I investigated these two factors in cooperatively breeding banded mongooses, Mungos mungo. Female packmates entered oestrus together and were closely guarded by dominant males. These males were aggressive to subordinate males who attempted to mate, but females still managed to mate with males other than their mate guard. Older females were guarded and mated a few days before their younger packmates, yet all females usually gave birth on the same day, suggesting that older females may have a longer gestation period. Moreover, older females carried more fetuses. Overall, ca. 83% of adult females conceived in each breeding attempt and 71% carried to term. These results indicate that, among males, dominant individuals did not have full control over the mating attempts of subordinates (since they could not fully control the mating behaviour of the females they guarded), while among females there was little or no attempt to prevent subordinates from breeding (at least, prior to parturition). Two within-group infanticides by males suggested that some control over reproduction may be exercised postpartum. Per capita survivorship of young in the den increased with the number of females who gave birth. Thus, dominant females may benefit from subordinate reproduction, providing a possible explanation for the lack of reproductive suppression among females in this species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Artificial induction of superfetation in the European hare (<Emphasis Type="Italic">Lepus europaeus</Emphasis>)

The aim of this study was to induce superfetation in hares. On day 37 or 39 of pregnancy, female hares were treated with GnRH analogue and artificially inseminated with fresh semen. Ultrasonographic examination showed that pregnant females had follicles on the ovary on 37 days of pregnancy. After a few days from insemination performed during pregnancy, all females gave birth to healthy young, and one of the females inseminated on day 37 of pregnancy gave birth to two healthy young 42 days after insemination performed during pregnancy (39 days post first delivery). The same female in the next year gave birth to two healthy young 43 days after second insemination that was performed on the day 37 during pregnancy. The obtained results confirm that superfetation is possible to occur in hares.     

Mother-infant cannibalism in thick-tailed bushbabies (Galago crassicaudatus umbrosus)

Mother-infant cannibalism in species of galagos as in several other species of non-human primates is a common phenomenon. In non-human primates kept in laboratory conditions many of the observed cases of cannibalism were not associated with starvation and with infanticide. Cannibalism in galagos was observed in at least five different species. In several laboratories, like the Duke University Primate Center, the frequencies of cannibalism in galagos species in captivity have been reduced by the isolation of pregnant female before the parturition from her companions, especially adult males. At the Primate Behaviour Research Group (University of Witwatersrand, Johannesburg, South Africa) three cases of cannibalism were observed in twoGalago crassicaudatus umbrosus' mothers before the end of the third day after birth. To understand the reasons why the mothers cannibalize their own infants, it was decided to analyze the mother-infant interaction which preceded the death of the infants. InGalago crassicaudatus twin and triplet births are very common. In one of our two observed mothers who cannibalized their infants, there was one triplet birth. In this study the two pregnant females were isolated in two separated cages ten days before giving birth. One of the two observed mothers gave birth to triplets, the other had a single birth. At the end all four infants were cannibalized. In all cases the cannibalization started after the infant's death. The infants' deaths were caused by lack of maternal care which caused them to starve. The results show that the triplet's mother differed in some of her behaviour towards her infants. In one of the cannibalized infants behaviours such asNipple andMother Passive Prevent were never seen before death. In our cases it seems that cannibalism was probably due to the laboratory condition that for generation to generation caused stress to the mothers and changed their maternal behaviours, which lead to the death of the offspring which after death became a consumable resource.     

Lactation and care for unrelated infants in forest-living ringtailed Lemurs

An adult female ringtailed lemur (Lemur catta) known not to have been pregnant showed spontaneous lactation in response to twin infants born to an unrelated female. The females had met only 7 months earlier, when they and two other unrelated adult females were released from separate locations in a forest enclosure to form a new social group. Three months after release, an adult male from an adjacent enclosure gained access to the new group for 1 day, the day of one female's estrus. No males had access to the females throughout the remainder of the breeding season. Within 2 weeks of the birth of the twins, one of the other adult females began carrying the infants frequently, typically one at a time. All three females were checked for lactation when the infants were two months old. Both their mother and the unrelated adult who had been carrying the infants were producing milk. The third adult female, who never carried either infant, had no milk. The third adult female, who never carried either infant, had no milk. This female, however, like the two maternal females, frequently attacked unfamiliar immigrating adult males when the males approached the infants. Potential implications of these observations concerning the social organization of ringtailed lemurs are discussed.     

Role of early experience in social behaviour of laboratory-bred female rats

Social relationships among female laboratory-bred rats in a community are influenced by their early life history. When the rats were born and kept until adulthood under conventional breeding conditions, i.e. in single cages, and then used to form a community in which they gave birth, one female assumed the dominant role, with all others subordinate. The dominant female herded all young rats born in the community, irrespective of their age, in a single litter and suckled them. She accumulated food and wood shavings from other parts of the community near the nest and prevented access to the nest to all other community members including other females that had given birth. Subordinate females ceased to show maternal behaviour, including lactation, within 24 h (occasionally within 48 h). The mortality of the young until 15 days of age was high. This type of behaviour in a community was observed both with randomly chosen female rats and with rats selected as dominant and subordinate types in preceding experiments. Female rats born and reared in a community and rats living in a community from 15 to 30 days of age did not differentiate into dominant and subordinate types. All females retained their maternal behaviour, including lactation. Mortality of young rats was minimal. In most cases the females built one common nest; sometimes each female built her own nest. The results point to the decisive role of early experience in the development of maternal behaviour and in the occurrence of communal rearing of the young.     

Reproduction in captive lion tamarins (Leontopithecus): Seasonality,infant survival,and sex ratios

Diversity in reproductive and social systems characterizes the primate family Callitrichidae. This paper contributes to our appreciation of this diversity by presenting the first detailed comparative analysis of captive breeding in three species of lion tamarins (Leontopithecus chrysomelas, L. chrysopygus, and L. rosalia) housed at the Centro de Primatologia do Rio de Janeiro. The annual pattern of reproduction in all three species of Leontopithecus was markedly seasonal, with births occurring during the spring, summer, and fall months from August through March. While modal number of litters produced per female per year was 1, approximately 20% of breeding females produced two litters per year. The onset of breeding activity in years when two litters are produced was significantly earlier than in years when only one litter was produced. The cumulative number of offspring surviving to 3 months of age did not differ between years with one vs. two breeding attempts. Like other callitrichids, postnatal mortality was highest during the first week of life, and there were pronounced species differences in offspring survival through 1 year, with significantly lower survivorship in L. chrysomelas. Infant survivorship was affected by a number of experiential factors. Survivorship up to 30 days of life was higher in groups in which the breeding female had previous experience with infants as a nonbreeding helper than in groups in which the female lacked previous helping experience. Likewise, survivorship to 30 days of life was higher for infants born to multiparous females than for infants born to primiparous females. When parity and previous helping experience were analyzed concurrently, the lowest survivorship was associated with offspring produced by inexperienced primiparous females. Genus-wide, there was no significant departure from a 50:50 sex ratio at any point during the first year of life, nor was there evidence for differential mortality for male and female infants. However, L. chrysopygus produced significantly more male infants at birth (65:44) and had male-biased litters (approximately 60% males) throughout the first year of life, while L. chrysomelas showed a nonsignificant tendency toward female-biased litters. © 1996 Wiley-Liss, Inc.     

An analysis of birth sex ratio bias in captive prosimian species

The extent to which sex ratio bias is a common reproductive characteristic of prosimians has not been well established. The present study analyzed reproduction in 13 breeding groups of captive prosimians for evidence of birth sex ratio bias. A substantial male bias was demonstrated in nongregarious, but not gregarious, breeding groups. Analyses of birth sex ratios of individual mothers suggested that the observed bias did not result from the tendency of a few mothers to overproduce males, but rather from a small but reliable excess of male births in general. An examination of infant mortality revealed that male Otolemur garnettii and Microcebus murinus infants were more vulnerable to preweaning mortality, whereas female Eulemur fulvus albifrons infants were more vulnerable. An analysis of birth order by sex found that mothers of one group (O. garnettii) tended to produce males initially and females later. Additionally, a distinct pattern of birth seasonality was noted among Malagasy prosimians that was absent in the African prosimians. Greater length of period of sexual receptivity for nongregarious females as compared to gregarious females is proposed as a possible mechanism of male birth sex ratio bias. © 1996 Wiley-Liss, Inc.     

Chimpanzee triplets born in captivity

A female chimpanzee (Pan troglodytes) gave birth to triplets at the Lincoln Park Zoological Gardens, Chicago, Illinois. Of the three infants born, only one survived. The other two, both sexed as males, were dead when they were discovered. When pathology was done on these infants, it was found that aside from being underweight, chimpanzee No. 1 was 930 g and chimpanzee No. 2, 630 g, the animals had never developed a brain. The female nursed the surviving male infant for six days till it was taken for hand-rearing. The infant was in a weakened condition and weighed 890 g. He died on the next day. This is possibly the first birth of triplet chimpanzees in a North American zoological garden.     

The reproductive biology of female Père David's deer (Elaphurus davidianus)

Data for this study came from breeding records of 27 Père David's (Elaphurus davidianus) hinds maintained in large pastures and from estrous records of four hand-reared nulliparous hinds. The mean estrous cycle length ranged from 17.5 to 19.6 days. Standing estrus resembled that of other cervids, except that a low, moaning vocalization was given in response to contact, and activity (as measured by pedometers) did not increase. Mean gestation length was 183.38 ± SD 6.11 days (n = 21), and nearly all females conceived in the second and third years. The median interbirth interval was 362 days. The median birth date was April 8, and 80% of the births occurred over a 9.5-week period. Multiparous hinds gave birth an average of 20.5 days earlier in the season than primiparous hinds. There was no dimorphism in birth weight. The results are discussed in light of comparative data for other species.     

Birth sex ratios and maternal social rank in a captive colony of rhesus monkeys (Macaca mulatta)

Data from a 35-year study of rhesus macaques (Macaca mulatta) at Madingley, Cambridge, were used to investigate sex ratio biases associated with maternal rank. Data were available from two colonies, the Old colony (1960–81) and New colony (1982–93). Overall, top-ranking mothers gave birth to 30.9% sons, while non-top mothers gave birth to 58.4% sons. Among non-top mothers, middle- and bottom-ranking ones had 59.0 and 55.0% sons, respectively. Top mothers' daughter biases were strongest in matrilines with two adult females in the year the infants were conceived (15.4 sons and 14.3% sons in Old and New colonies). Non-top mothers' son biases (88.9 and 71.0% in Old and New colonies) were strongest in matrilines with 3 females. The findings are discussed in relation to the colonies' small matriline sizes and data on breeding performance and infant survival, which indicate the costs to mothers of different rank of having different sex infants. Overall, top-ranking mothers were more likely to breed in two successive years (78.6%) than non-top mothers (56.7%). Infant survival to 7 days was significantly higher in the New colony (89.0%) than the Old colony (75.3%), with daughters born to Old colony mothers doing especially poorly. We point out that between-group and between-species comparisons of sex ratio effects depend critically on how females are assigned to rank categories, and require information about divergences of sex ratios from 50:50 in each category. © 1996 Wiley-Liss, Inc.     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

Characteristic features of the reproduction of Koshima monkeys,Macaca fuscata fuscata: A summary of thirty-four years of observation

The reproductive data for Japanese monkeys,Macaca fuscata fuscata, which had been recorded for the 34 years from 1952 to 1986 on Koshima, were analyzed in terms of the influence of changes in artificial food supplies, the differences in reproductive success between females, the timing of births, and the secondary sex ratio. Koshima monkeys increased in number until 1971 when the population density was still small and artificial provisioning was copious. As described byMori (1979b), the severe reduction in artificial food supplies, which began in 1972, had an enormous deleterious effect on reproduction: the birth ratio of adult females of 5 years of age or more fell from 57% to 25%; the rate of infant mortality within 1 year of birth rose from 19% to 45%; primiparous age rose from 6 to 9 years old on average; and there was an increased death rate among adult and juvenile females. The prolonged influence of “starvation” may be seen in the significantly delayed first births of those females that were born just before the change in food supplies. When reproductive parameters are compared between the females who belonged to six lineages in the group during these periods, they were found to be rather consistent, although some individual differences can be recognized among females and subgroups. The apparent trend was that some of the most dominant females retained superior reproductive success while that of the second-ranked females has tended to diminish over the years since 1972. Such opposing trends were seen only in the most dominant lineage group and such a difference was not recognized among the females of other lineages. The difference in reproductive success is discussed in relation to both the different situations that arise because of the artificial food supplies and differences in feeding strategies. Multiparous females, after a sterile year, gave birth somewhat earlier than those who reared infants in the preceding year and, when artificial provisioning was intense, they tended to give birth a little earlier than during other periods. There is some evidence that the mortality of later-born infants was higher than that of earlier-born infants after 1972. However, this difference may not be responsible for the differential reproductive success of females since the timing of births did not differ among lineages. Furthermore, during the time when many females gave birth continuously, prior to 1972, the infant mortality did not differ with respect to the timing of births. The differences in infant mortality were not correlated with the reproductive history, parity or age of the mother, or with the sex of the infant. The secondary sex ratio varied by only a small amount, from slightly male-biased ratio (114: 100) when correlated with reproductive history, parity, age of mother, sex and survival ratio for preceding infants, timing of birth, and lineage of the female. Furthermore, the change in artificial food supplies did not cause any modifications of the secondary sex ratios, despite its enormous deleterious effect on reproduction. The secondary sex ratio of Japanese monkeys may not be influenced by the social factors mentioned.     

BREEDING BIOLOGY OF SOUTHERN ELEPHANT SEALS IN PATAGONIA

Abstract: Elephant seals breed in Patagonia (Península Valdés, Argentina) from late August to early November, reaching peak numbers during the first week in October. Observations of this population over the past ten years yielded similar results. Eighty percent of the pups were born by 2 October. Most (96%) of 663 females marked during three breeding seasons gave birth to a pup. Females stayed on land a mean of 28 d, gave birth 6 d after arrival, nursed their pups for 22 d, and copulated a mean of 2.5 times 20 d after parturition and 2 d before departure. Copulations peaked during the third week in October. Males spent 57–80 d on land fasting and defending harems of up to 134 females (median 11–13 females, depending on year). Most (96%) marked females that gave birth ( n = 636) also weaned their pups successfully. Pup sex ratio was unity. Harems were smaller and breeding occurred about three weeks earlier in Patagonia than in other colonies. Thermal conditions, day length and food availability may explain clines in the timing of breeding events between populations, Other parameters of the breeding season for the expanding Patagonia colony are similar to those for declining southern elephant seal populations elsewhere.     

Fecal endocrine monitoring of reproduction in female snow leopards (Uncia uncia)

Although the snow leopard (Uncia uncia) is a common endangered felid species in zoos, little is known about the complex endocrine interactions controlling ovarian function and conception in this species. The goal of this work was to characterize ovarian activity throughout the estrous cycle, nonpregnant luteal phase (pseudopregnancy), and gestation in female snow leopards. This goal was accomplished using an enzyme immunoassay to measure fecal concentrations of estrogen metabolites (E) and progesterone metabolites (P). Fecal samples were collected from 12 female snow leopards (ages 18 months to 18 years) during one to three breeding seasons. In each breeding season, the majority of females (78%, 88%, and 100%, respectively) began to exhibit ovarian activity in December or January. The estrous cycle, defined by the first day of estrus (E ≥ 2 × basal concentration) to the first day of the subsequent estrus, was 12.7 ± 0.6 days (n = 145 cycles). Estrus lasted 4.3 ± 0.4 days with mean concentrations of fecal E during the follicular phase (1661 ± 139 ng/g feces) increasing 3.2-fold above basal concentrations (515 ± 32 ng/g feces). No spontaneous ovulations were observed in any of the cycling females. Nonpregnant luteal phases were observed in eight females that bred but did not become pregnant. The length of the nonpregnant luteal phase ranged from 11 to 72 days (45.7 ± 5.7 days; n = 10) with mean concentrations of fecal P during the luteal phase (12.46 ± 1.7 μg/g feces) increasing 6.2-fold above basal concentrations of P (2.01 ± 0.2 μg/g feces). Three of the females in the study became pregnant and gave birth after a gestation of 93 (n = 2) and 95 (n = 1) days. Fecal P concentrations during pregnancy increased to 11.64 ± 1.3 μg/g feces, or 5.8-fold above basal concentrations. The results of this study provide a comprehensive characterization of reproductive endocrinology in snow leopards, and confirm that fecal hormone monitoring is an effective way to monitor female snow leopards throughout the breeding season.     

The social grooming of captive female rhesus monkeys: Effects of the births of their infants

We observed the grooming interactions of 13 female rhesus monkeys (Macaca mulatta)before and for 12 weeks after the births of their infants. Mothers groomed for similar amounts of time before and after the birth of their infants, but after the birth, the grooming they directed to their infants may have been at the expense of that directed to other partners. Lactating females did not receive more grooming from other females but were approached more often, suggesting that they were more attractive. Mothers that groomed their infants most groomed others least, as if grooming time was limited for each mother or as if she was trying to compensate for avoiding interactions with other partners. Mothers of male infants groomed others more than mothers with female infants did, which might be due to mothers with daughters receiving more aggression and therefore avoiding interaction. Experienced and high-ranking mothers groomed their newborn infants considerably more than primiparous mothers did in the 24 hr following birth. Grooming was preferentially directed at close kin before the births of the infants. Mothers tended to groom higher-ranked partners more than they were groomed by them, and they tended to receive more grooming from lower-ranked partners than they gave, as suggested in models of rank attractiveness.     

Reproductive biology of captive Arabian oryx (Oryx leucoryx) in Saudi Arabia

Reproductive data on captive Arabian oryx (Oryx leucoryx) were collected from June 1986 through April 1992 at the National Wildlife Research Center (Taif, Saudi Arabia). Oryx females are polyestrous. The estrous cycle averaged 22 days and mean gestation length was 260 ± 5.5 days (S.D). Sex ratio at birth was unbiased and mean weight was 6.5 ± 0.7 kg (S.D.), with no difference between sexes. Under captive breeding conditions, births occurred throughout the year. Females gave birth to a single calf at any time during the day and produced 1.03 young per year. Abortion rate was 3.6%. Mortality rate of young was 6.1% before weaning at 3 months of age. The interbirth interval averaged 295 ± 42 days (S.D.), with 53% lasting between 270 and 279 days. Females reached sexual maturity at the age of 13 months. © 1996 Wiley-Liss, Inc.     

Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.