Patterns of reproduction in Malayan silvered leaf monkeys at the Bronx Zoo

Within phylogenetic limits reproductive characteristics of a given species may vary between populations in response to ecological and social factors. For instance, in environments where high quality nutrition is readily available, the onset and speed of reproduction are often accelerated. Other influencing factors might be maternal experience or the sex of the infant. Here we present data on reproductive characteristics for the silvered leaf monkey (Trachypithecus cristatus), a medium‐sized Asian colobine housed at the Wildlife Conservation Society's Bronx Zoo as a one‐male group. To place the species into an appropriate phylogenetic context, we limited our comparison to other colobine species. Demographic data span 21.4 years (October 1985 to March 2007) and derive from 30 adult females (128.0 female years). Detailed behavioral data stem from a 2.2 years study (November 2002 to January 2005; 734 days, 4,225 hr). As in other Asian colobines, receptive periods were short (mean=4.3 days, n=68). This is expected for one‐male groups where receptivity likely indicates, rather than conceals, ovulation. Gestation length was estimated based on a change in the pattern of sexual behavior (mean=194.6 days, n=7). It fell within the range reported for the taxon. Births occurred year round, at an early age (mean=2.9 years, n=8), at short intervals (mean=14.9 months, n=59) in combination with a short lactation (mean 12.1 months, n=9) likely due to the nearly unlimited availability of nutrition in this zoo setting. Primiparous females tended to have a longer first interbirth interval but infant survival rates were similar to multipara possibly due to the absence of predators. Maternal investment was independent of the infant's sex and birth sex ratio was even. Our results emphasize that when interpreted with caution, zoo populations yield realistic reproductive characteristics that can help fill the gap in our knowledge about colobine life history. Am. J. Primatol. 71:852–859, 2009. © 2009 Wiley‐Liss, Inc.     

Reproductive parameters of wild female Rhinopithecus roxellana

On the basis on 6 years of observation, we estimated the reproductive parameters of a Golden snub-nosed monkey (Rhinopithecus roxellana) group in the Qinling Mountains, China. We observed 88 births in 47 females from 2001 to 2006. Two methods were used to calculate the birthrate. The first method is based on the number of births observed in a year, giving 0.49+/-0.07 (mean+/-SD), and the second method is based on the female-years of observation, giving 0.49+/-0.17 births per female per year in this troop. The mean interbirth interval is 21.88+/-6.01 months (mean+/-SD). The mortality of infant born between 2002 and 2005 was 22.4%. The interbirth intervals of females that had lost an infant before the age of 6 months were significantly shorter than that of females whose infants survived for more than 6 months. A female usually gives birth once every 2 years if the previous offspring survives to a weaning age of 5-6 months, or will give birth in the next year if the previous young dies before reaching an age of 6 months. Births were significantly concentrated during March to May of each year. The mean birth date was on April 14, median was April 12; and the standard deviation was 13.98 days. Birth peak occurs 6-7 months after mating peak. From observations on 15 individuals that gave birth for the first time, we concluded that the wild female Golden snub-nosed monkeys in Qinling Mountains start giving birth at an age of 5 or 6 years. We suggest that the seasonal reproductive pattern is an adaptive response to the availability of seasonal food. Our results are consistent with the hypothesis that these reproductive characteristics are a result of adaptation to the seasonality of mountain climate and food resources.     

Reproductive biology of captive and free-ranging spider monkeys

Records from 42 zoos and from long-term studies of wild populations were analysed to describe the reproductive biology of spider monkeys (Ateles spp.). Both data sets suggested that spider monkey females typically have their first infant between 7 and 8 years of age with an interbirth interval of approximately 32–36 months. Infant sex ratio for zoo populations was approximately 1 male to 1 female; infant sex ratios from wild populations were variable. Zoo records provided adequate sample size to suggest that interbirth interval was not influenced by the sex of the infant produced, and that the sex ratio and the probability of infant survival did not change with the number of infants the mother had produced. The findings of this study have implications with respect to the conservation of New World primate species. Since spider monkeys take a long time to reach sexual maturity and their interbirth interval is longer than that expected based on their body size, their populations may be slow to recover following disturbances. Thus, particular care should be taken for the protection of these species.     

Reproduction of the owl monkey (Aotus spp.) in captivity

Abstract: The reproduction performance of captive owl monkeys, a breed used extensively in biomedical research, was observed at the Battelle Primate Facility (BPF). The colony grew through captive breeding, imports from the Peruvian Primatological Project, and others to a peak size of 730. It included seven karyotypes of Aotus sp. Results showed that owl monkeys can breed successfully in a laboratory in numbers sufficient to sustain modest research programs. Reproductive success increases when pairs are compatible, of the same karyotype, and stabilized; however, mated pairs of different karyotype are also productive. Under conditions of controlled lighting and heating, owl monkeys at BPF showed no birth peak nor birth season.     

Reproductive life history of Thornicroft’s giraffe in Zambia

Knowledge of the reproductive life history of giraffe in the wild is sparse. Giraffe have two fairly unusual reproductive patterns among large mammals: they can become pregnant while lactating, and calf mortality is extremely high. Longitudinal records are largely absent, so tracking reproductive parameters tends to combine information from captive and field studies. In this study, we examine longitudinal data obtained over a 33‐year period in one population of Thornicroft’s giraffe in order to chart their reproductive careers. We found that age at first parturition was 6.4 years, or slightly later than in captivity. Giraffe bred throughout the year, with cows producing offspring on average every 677.7 days. About half of the calves died before one year of age, but death of a calf did not reduce interbirth interval. We conclude that the lifetime reproductive success of giraffe is more dependent on longevity and calf survivorship than on reproductive rate.     

Diffuse nodular hyperplasia and fibrosis of the liver in lead-poisoned mandrills

Two sibling mandrills with clinical evidence of lead intoxication showed previously unreported hepatic alterations. The younger animal had high lead concentrations in blood, kidneys, and liver and characteristic intranuclear inclusions in renal tubules and hepatocytes. The liver showed diffuse nodular regenerative hyperplasia. The older mandrill had high lead concentrations in blood only and resolving intranuclear inclusions in liver and kidneys. The liver showed prominent portal fibrosis with evidence of resolving diffuse nodular hyperplasia. Occipital horn hydrocephalus was also present.     

Reproductive parameters in Guizhou snub‐nosed monkeys (Rhinopithecus brelichi)

In this study, we present data on reproductive parameters and birth seasonality of Guizhou snub‐nosed monkeys (Rhinopithecus brelichi). Our analyses are based on data from a small captive population collected over 15 years and on 5 years of observations of free‐ranging snub‐nosed monkeys. Captive females (n=4) mature at an age of 70.8±6.7 months and reproduce for the first time at 103.4±7.5 months. The mean interbirth interval was 38.2±4.4 months if the infant survived more than 6 months, which is longer than that in R. roxellana and R. bieti. In the wild and in captivity, births are very seasonal and occur only in a period from the end of March to the end of April. Our data suggest that population growth in Guizhou snub‐nosed monkeys is slow compared with the other two Chinese snub‐nosed monkey species. The risk of extinction is therefore particularly high in this species, given the small overall population size and slow population recovery potential. Am. J. Primatol. 71:266–270, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

Reproductive Characters and Mating Behaviour of Wild Nomascus hainanus

We report for the first time the reproductive behaviors of Hainan gibbons (Nomascus hainanus), based on 29 mo of field observations. Receptive females initiated courtship displays. Copulatory patterns involved the male mounting dorsoventrally from above and behind. Multiple intromissions with thrusting were brief, lasting <10 s per copulation. We observed multiple copulations ≤4 times/d, but could not confirm multiple ejaculations. We also observed postconception proceptivity and copulations in sexually active females. We estimated the gestation period to be 136–173 d. Infants became independent at 1.5 yr, and the natal group could drive out maturing offspring at ca. 5.5 yr. The interbirth interval is ca. 24 mo. Our limited data also suggest that mating activities peak in the rainy season. The Hainan gibbons are polygynous, with a 1 male-2 females mating system. We hypothesize that suboptimal habitat quality and limited forest area may contribute to the current mating structure, but more work needs to be done over a longer period to understand better the sociosexual behaviors of this critically endangered species.     

Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques

Primate life histories are strongly influenced by both body and brain mass and are mediated by food availability and perhaps dietary adaptations. It has been suggested that folivorous primates mature and reproduce more slowly than frugivores due to lower basal metabolic rates as well as to greater degrees of arboreality, which can lower mortality and thus fecundity. However, the opposite has also been proposed: faster life histories in folivores due to a diet of abundant, protein-rich leaves. We compared two primate taxa often found in sympatry: Asian colobines (folivores, 11 species) and Asian macaques (frugivores, 12 species). We first described new data for a little-known colobine (Phayre's leaf monkeys, Trachypithecus phayrei crepusculus) from Phu Khieo Wildlife Sanctuary, Thailand. We then compared gestation periods, ages at first birth, and interbirth intervals in colobines and macaques. We predicted that heavier species would have slower life histories, provisioned populations would have faster life histories, and folivores would have slower life histories than frugivores. We calculated general regression models using log body mass, nutritional regime, and taxon as predictor variables. Body mass and nutritional regime had the predicted effects for all three traits. We found taxonomic differences only for gestation, which was significantly longer in colobines, supporting the idea of slower fetal growth (lower maternal energy) compared to macaques and/or advanced dental or gut development. Ages at first birth and interbirth intervals were similar between taxa, perhaps due to additional factors (e.g., allomothering, dispersal). Our results emphasize the need for additional data from wild populations and for establishing whether growth data for provisioned animals (folivores in particular) are representative of wild ones.     

Demographic parameters and life history of chimpanzees at Bossou, Guinea

Demographic parameters of wild chimpanzees at Bossou, Guinea, are presented and compared with those of other populations. The population size of Bossou chimpanzees has been stable over the last 26 years, except during two incidents of partial deforestation. The annual birth rate for a female (mean = 0.194, but 0.165 when the infant survived more than 4 years) and interbirth interval are not much different from those of other study sites. The primiparous age of Bossou chimpanzees, however, is far younger (mean = 10.9 years) than for all other known wild chimpanzee populations. The infant and juvenile survival rate is also the highest (female = 0.64, male = 0.52 for the first 8 years). As a result, the lifetime reproductive success of Bossou chimpanzees is estimated to be highest among long-term study sites. The rate of disappearance from Bossou dramatically increases during the adolescent stage, and most young chimpanzees disappear before or around maturation. Probably because the environmental capacity for chimpanzees at Bossou is at its limit, many young independent males, as well as females, have to disperse, though others may die. For chimpanzee alpha males of other populations, mature males may be needed as collaborators to defend resources. In the case of Bossou, however, a lack of adjacent groups, conspecific competitors, predators, and perhaps medium-sized mammals as prey for group hunting may eliminate this need of the alpha male for other males. The reasons why all males of other chimpanzee populations persist in being philopatric for life and maintain kin-related male bonds differing from most mammal species, including humans, are discussed.     

Reproductive parameters of wild Trachypithecus leucocephalus: seasonality,infant mortality and interbirth interval

Understanding the reproductive parameters of endangered primate species is vital for evaluating the status of populations and developing adequate conservation measures. This study provides the first detailed analysis of the reproductive parameters of wild white‐headed langurs (Trachypithecus leucocephalus), based on demographic data collected over an 8‐year period in the Nongguan Karst Hills in Chongzuo County, Guangxi, China. From 1998 to 2002, a total of 133 live births were recorded in the population based on systematic censuses. Births occurred throughout the year, but the temporal pattern was highly correlated with seasonal variation in temperature and rainfall, with the birth peak coinciding with the dry and cold months of November–March. The average birthrate was 0.47±0.13 births per female per year and mortality for infants younger than 20 months was 15.8%. From 1998 to 2006, 14 females gave birth to 41 infants in four focal groups. The average age at first birth for female langurs was 5–6 years (n=5) and the interbirth interval (IBI) was 23.2±5.2 months (median=24.5 months, n=27). Infants are weaned at 19–21 months of age. The IBI for females with infant loss before weaning was significantly shorter than those for females whose infants survived. It appears that birth seasonality in the white‐headed langurs is influenced by seasonal changes in food availability. The timing of conceptions was found to coincide with peak food availability. The reproductive parameters for white‐headed langurs reported here are quite similar to those reported for other colobine species. One major difference is our observation of lower infant mortality in Trachypithecus. Am. J. Primatol. 71:558–566, 2009. © 2009 Wiley‐Liss, Inc.     

Demographic and Female Life History Parameters of Free-Ranging Chimpanzees at the Chimpanzee Rehabilitation Project, River Gambia National Park

We analyzed fertility and mortality records for 113 provisioned, free-ranging chimpanzees at the River Gambia National Park, The Gambia. The chimpanzees are rehabilitated orphans released by the Chimpanzee Rehabilitation Project (CRP), and their descendants born in a natural environment. Females experienced their 1st births at an average age of 14.3 yr, with average interbirth intervals of 68 mo. Despite limited provisioning, reproductive parameters in both released and 1st-generation females resembled those of wild chimpanzees and showed seasonal fluctuations. Mortality rates were low compared to those for wild chimpanzees, particularly for infants and juveniles; life expectancy at birth was 23.6 yr for females and 18 yr for males. The results have implications for our understanding of variation in reproductive parameters between captive and wild chimpanzees. We also discuss issues related to chimpanzee conservation and captive rearing.     

Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

Annual Reproductive Behavior of Rhinopithecus roxellana

Ren conducted year-round observations on sexual behaviors of Sichuan snub-nosed monkeys in Shanghai Wild Animal Park from May 2000 to May 2001, which confirmed quantitatively that the species is a rigorous seasonal breeder with a single birth season between late March and early June. Lactation continues until the infant reaches about 1.5 years or it dies. Accordingly, the interbirth interval is ca. 18–20 mo. The results also confirm that females regulate the timing of reproduction. To avoid mating competition their conception times differ from one another, and they conceive between October and December. Three focal females maintained proceptive activities with significant durations due to their different ages and mating choice. If new babies died in the same year the mothers resumed sexual activity on different days. Apart from female peak mating times there is no significant difference among them regarding the regularity of their sexual activities. Temporal differences in birth peaks at different locations might be due to latitude.     

Interbirth interval variation in three sympatric species of neotropical monkey

Relatively few papers have focused on interbirth intervals in primates, even though the spacing between births is one of the primary determinants of female reproductive success in long-lived mammals. We present life history data from a ten-year field study of Costa Rican capuchins (Cebus capucinus), howlers (Alouatta palliata), and spidei monkeys (Ateles geoffroyi). Analyses of intraspecific variability found no significant differences attributable to individual variation in age, parity, weight, or maternal rank. Loss of an infant significantly shortened the interbirth interval in all three species. There was no correlation between annual rainfall and birth rates, but there was a significant clustering of births in the dry season. Survival analyses demonstrated a significant difference between the median interbirth intervals of the three species. Howlers have the shortest intervals (19.9 months), capuchins exhibit longer intervals (26.36 months), and spider monkeys have the longest intervals (34.72 months;. This comparative pattern does not correspond to relative body weights of the three species, but does correspond to relative brain weights. Comparisons to other primates with similar life history characteristics demonstrate that interbirth intervals are best examined at the level of their three component phases: gestation, lactation, and cycling to re-conception. © 1995 Wiley-Liss, Inc.