Reproduction of the mongoose lemur (Lemur mongoz) in captivity

Responses to questionnaires sent to 20 institutions holding Lemur mongoz did not reveal which aspects of management or husbandry could account for reproductive failure in the captive population, but allowed some qualitative comparisons with data compiled for captive and wild animals. In general, reproduction has occurred initially among wild-caught specimens before tapering off, and rarely occurs in the captive F₁ generation. Data compiled by the International Species Inventory System and the International Zoo Yearbook revealed an aging captive population with no recent reproduction. No aspect of group composition, activity patterns, seasonal light regime, reproductive cycles, or diet could be linked to the lack of reproduction; and among lemurs subjected to the same conditions, some were known to reproduce while others did not. Lack of knowledge about this species and the threat of extinction for both captive and wild populations make an investigation of reproductive biology imperative. Recommendations for a research program are given.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Evidence for social enhancement of reproduction in two Eulemur species

Across the past 20 years, captive reproduction has declined steeply in mongoose lemurs (Eulemur mongoz) and has been only moderately successful in black lemurs (E. macaco). At the same time, reproduction has been so successful in brown lemurs (E. fulvus) that contraception has been used since 1987 to limit captive numbers. No obvious cause for the differential reproductive success has been identified. Our experience with a pair of unrelated mongoose lemurs at the Philadelphia Zoological Garden suggested that they reproduced in only those years when they were caged in close proximity to another nonreproductive, full-sibling pair of mongoose lemurs. Examination of the worldwide pattern of captive reproduction by Eulemur species during the past two decades revealed that female black and mongoose lemurs housed in institutions with either additional conspecific males or additional conspecific pairs had a higher rate of reproduction than those maintained as an isolated pair. Black lemurs also had higher rates of reproduction when additional conspecific females were present. No similar pattern was found for brown lemurs or for two comparable mammals, the pudu (Pudu pudu) and the okapi (Okapia johnstoni). The evidence presented for the black and mongoose lemurs supports the existence of the Allee effect in these two species, namely, that reproduction is enhanced by the presence of conspecifics. © 1996 Wiley-Liss, Inc.     

A preliminary study of olfactory behavior of captiveLemur coronatus during the breeding season

The olfactory behavior of a captive population of crowned lemurs (Lemur coronatus)was studied during their annual breeding season in order to investigate its possible role in the fine-tuning of mating synchrony after photoperiodic initiation of reproductive activity. The frequencies of five stereotyped olfactory behavior patterns were recorded in four male-female groups during 315 1-hr observation sessions between October and March. The mean total scent-marking frequency of all males was positively correlated with their mean testicular size. Male anogenital-, head-, and allomarking frequencies decreased during the breeding season, whereas hand-marking frequencies remained constant. Male head-marking increased significantly in the 5 days preceding female vaginal estrus. Furthermore, males responded to many female scents by olfactory investigation and/or overmarking, whereas females never showed an observable behavioral response to male scent marks. The marking frequencies of two females did not change significantly during the breeding season, while those of two others decreased significantly. These results suggest qualitative changes of female scents during estrus and a less important role of male scents in intersexual communication in the context of reproduction than previously thought.     

Endocrine Monitoring of Wild Dominant and Subordinate Female Leontopithecus rosalia

In captive callitrichid primates, female reproductive function tends to vary with social status. However, little is known about the interplay between these factors in wild groups. We report observations on normative ovarian function in dominant and subordinate female golden lion tamarins (Leontopithecus rosalia) living in wild groups. We monitored ovarian status by measuring, via enzyme immunoassay, concentrations of excreted pregnanediol glucuronide (PdG) and estrone conjugates (E₁C) in fecal samples collected noninvasively from individuals in social groups in the Poço das Antas Biological Reserve, Rio de Janeiro State, Brazil. Dominant breeding females demonstrated steroid levels similar to those previously reported for wild cotton-top tamarin females, with statistically significant rises during pregnancy. The duration of elevation of fecal steroids in breeding females was ca. 4 mo, which corresponds with estimates of gestation from captive studies. Low steroid concentrations from December to June suggest a seasonally-related period of infertility in female golden lion tamarins. Dominant and subordinate females demonstrated several differences in endocrine function. In general, younger females living in intact natal family groups showed no evidence of ovarian cyclicity. We noted endocrine profiles consistent with ovulation and subsequent pregnancy for behaviorally subordinate females living in groups with unrelated males or in which a reversal in female dominance status occurred. Results suggest that in addition to changes in female reproductive endocrinology associated with puberty, the regulation of reproduction in females in wild callitrichid groups can be sensitive to status and relatedness to breeding males.     

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.     

Predatory behavior in captive Lemur spp

Lemur fulvus mayottensis, L catta, and L mongoz mongoz at the Jersey Wildlife Preservation Trust readily catch and consume proffered crickets and locusts. Lf mayottensis and L m mongoz also readily catch and consume small birds and mice, whilst these are ignored by L catta and L variegatus. These differences probably reflect real differences in the predatory behavior of these species, though they may also relate to cage specifications or to the history of the particular groups. These captive lemurs are either perpetuating previously unsuspected wild habits or else innovating in captivity. Observed Lemur predation resembles that of other primate species in being primarily accomplished by dominant individuals (in lemurs, generally adult females), and involving group excitement, as well as snatching and begging by subordinates, which could lead to traditions of predatory behavior.     

Serum 17β-estradiol and progesterone associated with mating behavior during early pregnancy in female rhesus monkeys

The phenomenon of postconception mating behavior was examined in a social group of rhesus monkeys living in an outdoor compound. Periodic blood samples and daily vaginal swabs were obtained from nine females beginning several weeks prior to conception and continuing through 6 weeks of pregnancy to permit an assessment of ovarian hormonal events associated with mating during early pregnancy. Each of the females showed a discrete period of copulatory activity during the periovulatory period which ceased within several days after the 17β-estradiol (E₂) ovulatory peak. In agreement with earlier reports, only a percentage of subjects (44%) exhibited a period of postconception mating, with copulatory activity beginning 19.8 (± 1.9) days following the E₂ peak and continuing for 9.5 (± 1.3 days). Implantation bleeding was detected in all of the subjects with the onset 19.5 (± 0.68) days after the E₂ peak. The interval between the E₂ peak and the onset of implantation bleeding was similar for all females. However, the duration of implantation bleeding was significantly shorter in females who exhibited postconception mating. The females who displayed postconception copulatory activity had significantly lower mean serum progesterone concentrations (2.33 ± 0.24 ng/ml vs. 3.64 ± 0.37 ng/ml) during the period associated with implantation bleeding and copulatory behavior. Although both groups had elevated concentrations of serum E₂ during this period, levels in the females who displayed postconception mating were significantly lower (173.8 ± 19.2 pg/ml vs 223.9 ± 28.8 pg/ml). These data demonstrate that the occurrence of postconception mating behavior in this environment is associated with a distinct pattern of ovarian hormonal events, and analysis suggests that differences in steroid concentrations probably account for the observed differences in implantation bleeding and copulatory behavior during pregnancy.     

Abnormal behaviors,with a special focus on rocking,and reproductive competence in a large sample of captive chimpanzees (Pan troglodytes)

Chimpanzees (Pan troglodytes) are endangered in the wild and may no longer be imported into the United States. Of those animals presently in captivity, candidates for breeding programs must be identified to insure a self-sustaining captive population. Some have suggested that poor reproductive performance might be linked to the performance of abnormal behaviors. In Study 1, three institutions housing breeding colonies of chimpanzees (86 males, 103 females) surveyed their animals for abnormal behaviors, copulatory performance, and, for females, maternal competence. In neither sex was there a positive association between absence of copulation and the presence of any of 18 forms of abnormal behavior. No one abnormal behavior was positively associated with inadequate maternal performance. Contrary to expectations, in both sexes (significantly for females), copulators exhibited more forms of abnormal behaviors than did noncopulators. In contrast, good mothers did show slightly fewer different forms of abnormal behaviors than did inadequate mothers. No specific combination of abnormal behaviors was associated with lack of copulatory performance in either sex or with inadequacy of maternal behavior. Significant sex differences occurred only in 2 of the 18 abnormal behaviors (coprophagy and self-clinging), both with females showing the higher prevalence. In Study 2, the rate of rocking in 5 male and 14 female chimpanzees at the Primate Foundation of Arizona was found to be relatively high among some reproductively competent subjects. Some rocking had forms and contexts indicative of aggressive displays. We conclude that chimpanzees should not be disregarded as potential breeders or as candidates for resocialization and breeding programs solely because they exhibit abnormal behaviors. Anyone involved in assessing well-being needs to be aware of individual differences among animals in the stimuli that may elicit rocking behavior. If they are strangers, they may elicit display rocking which does not indicate a lack of well-being. © 1992 Wiley-Liss, Inc.     

Reproduction in free-ranging Propithecus verreauxi: Estrus and the relationship between multiple partner matings and fertilization

Female sifaka mate selectively with one or more resident and/or non-resident males during the breeding season. Various adaptive explanations have been advanced to explain why female primates mate with multiple males including that 1) females seek to confuse paternity and thereby forestall male infanticide and/or ensure male infant care or 2) females seek to ensure fertilization. Assessing the power of fertilization insurance to explain mating patterns in females requires information on the temporal relationship between mating and ovarian hormones. The hormonal correlates of reproduction and mating in free-ranging Propithecus verreauxi were investigated using excreted steroids as indices of reproductive state. Solid-phase extraction and radioimmunoassay techniques were used to measure unconjugated estradiol (E₃) and progesterone (P₄) in 485 desiccated fecal samples collected from five female sifaka before and during the breeding season at Beza Mahafaly, Madagascar. Results suggest that behavioral estrus was characterized by 10- to 15-day elevations in E₂; hormonal activity was observed to be similar to pseudo-estrus reported for other lemur species; apparent conception was associated with sustained P₄ elevations beginning 1 to 3 days post-estrus with gestational phase elevations of E₂ beginning 42 to 45 days post-conception; and mating with multiple partners appeared not to be a prerequisite to fertilization, as conception resulted from both monoandrous and polyandrous matings. These preliminary data suggest that fertilization insurance is not adequate to explain polyandrous mating in sifaka at Beza Mahafaly. © 1996 Wiley-Liss, Inc.     

Demographics of captive De Brazza's guenons

Survival and fertility rates of captive De Bràzza's guenons (Cercopithecus neglectus), based on the 575 known captive animals in 70 zoos and institutions worldwide, were calculated. The results suggest that the high level of infant mortality (males: dx_{(day 1-yr 1)} = 0.73 males; females; dx_{(day 1-yr 1)} = 0.51), low fertility rate (Σ m′_x = 1.69), and differential mortality due to the incidence of stillbirths (males: dx_{(day 1)} = 0.676, females: dx_{(day 1)} = 0.442) may threaten the viability of this population. Possible causes of differential mortality rates are discussed and questions requiring additional research are identified.     

Reproductive and thyroid hormone profiles in captive Western fence lizards (Sceloporus occidentalis) after a period of brumation

Seasonal fluctuation in serum concentrations of sex steroid (testosterone [T] and 17β‐estradiol [E₂]) and thyroid (triiodothyronine [T₃] and thyroxine [T₄]) hormones was determined in captive Western fence lizards (Sceloporus occidentalis). Samples were collected from male and female breeding pairs weekly for a 4‐month period after their emergence from artificial brumation. Circulating levels of E₂ corresponded with the expected vitellogenic and ovulatory cycles in females, and surprisingly, E₂ in males followed a similar pattern, indicating a possible role in breeding behavior. Serum T was elevated in male lizards for the first 6 weeks after emergence from brumation, possibly related to an increase in the onset of active spermatogenesis. Thyroid hormones showed little cyclical activity throughout the breeding period, with the exception of small increases of T₃ at weeks 8 and 16, possibly implying an active role of this hormone with ovulation in females. Overall, these baseline hormone data are not only useful in developing this animal as a laboratory reptile model for assessment of endocrine‐mediated toxicity, but also of value for understanding herpetological endocrinology and for application in the conservation of threatened species. Zoo Biol 27:36–48, 2008. © 2007 Wiley‐Liss, Inc.     

Use of behavioral measures to assess reproductive status in maned wolves (Chrysocyon brachyurus)

Captive breeding efforts of the threatened maned wolf (Chrysocyon brachyurus) have been plagued by a lack of reliable reproduction and a high rate of neonatal mortality. A particular problem for animal managers has been the ability to detect pregnancy in a noninvasive manner. Pseudopregnancies are common, and many staff hours are expended preparing for a birth that may not occur. The objectives of our study were to document changes in behavior during the breeding season in captive maned wolves in order to determine if behaviors other than sexual (i.e., copulation) could be used to distinguish nonbreeding from breeding pairs and, further, whether successful breeding pairs (young born) could be distinguished behaviorally from breeding pairs that did not produce young (pseudopregnant). Between 1988 and 1994, behavioral data were collected during the annual reproductive season from 52 maned wolf pairings (27 males, 26 females) housed at 17 North American institutions. Breeding animals showed significant increases in rates of affiliative behaviors (approach, friendly) and the amount of time spent in close association (social) during the estrous period, compared to pre- and post-estrous periods. In contrast, the behavior of nonbreeding pairs varied little throughout the breeding season. Discriminant function analysis (DFA) showed that several behavioral measurements during certain reproductive periods were useful in discriminating between nonbreeding and breeding animals (rates of friendly and social behavior for males, marking and social behavior for females). Unsuccessful (pseudopregnant) and successful breeding pairs could be further distinguished on the basis of agonistic and approach behavior frequencies (successful females showed higher rates of agonistic and lower rates of approach behavior during certain periods; successful males had higher rates of both behaviors). Discriminant equations for key behavioral measurements and examples of their practical application are presented. DFA provides animal managers with an effective, noninvasive technique for assessing the reproductive status of maned wolf pairs. © 1996 Wiley-Liss, Inc.     

Testicular Volume and Reproductive Status of Wild <Emphasis Type="Italic">Callithrix jacchus</Emphasis>

The social relationship dynamic among callitrichid females is well known. Breeding exclusivity by dominant females involves female-female competition, usually resulting in the inhibition of subordinate reproduction. However, the strategies to maintain the male breeding position are still unclear. Researchers have observed no overt aggression between males, and differences in testosterone levels between dominant and subordinate individuals do not correlate with differences in reproductive success. In Callithrix monogamy is the predominant mating system, and testicular size is compatible with the absence of sperm competition. We analyzed testicular volume during development in 95 individuals at different ages (infant n = 12, juvenile n = 9, subadult n = 15, and adult n = 59). We also investigated if the ratio between testicular volume and body mass correlates with breeding position in the social group. The ratio was significantly higher in breeding males and a positive correlation between body mass and testicular volume is significant only for nonbreeding males. The findings suggest that testicular size varies with male reproductive status in the social group and that the enlargement of testicular volume in breeding common marmoset males seems to be a result of proximate causes and to depend on social and reproductive contexts acting together or separately.     

Effects of age,lactation, and repeated cycles on rhesus monkey copulatory intervals

Young, sexually mature female rhesus monkeys copulate on more days prior to conception than do older females, and this prolonged discrete mating period is associated with an earlier rise in serum estradiol prior to the first ovulation of the breeding season. The influence of repeated ovulatory cycles and the presence of a suckling infant on the copulatory patterns were examined in two separate analyses. Extending previous work, young, nulliparous females copulated on more days at the first ovulation of the breeding season than did older, multiparous females. However, the duration of the copulatory period at the second ovulation of the breeding season was similar and significantly shorter for both age groups. Furthermore, the presence of a suckling infant did not influence the duration of the mating periods in adult, multiparous females. The onset of copulatory behavior for all females was associated with serum estradiol concentrations of approximately 90 pg/ml, indicating that the age and cycle differences in the duration of the copulatory periods are due to the time course of serum estradiol prior to ovulation. A separate, longitudinal analysis of the duration of the mating period associated with the first ovulation of three successive breeding seasons indicated that females copulated on more days during their first ovulatory cycle of their first breeding season. These data indicate that the copulatory interval is longer for females during the first ovulation of the breeding season, and this pattern is accentuated in young, sexually mature animals.     

Reproductive behavior of the captive Sunda pangolin (Manis javanica Desmarest, 1822)

Understanding reproductive behavior is important for the conservation of endangered species, but research on the reproductive behavior of Sunda pangolins (Manis javanica Desmarest, 1822) is still very scarce. In this study, we used focal animal sampling and all-occurrence recording by an infrared monitor to observe the behaviors of two Sunda pangolins during a 5-day breeding period at the Pangolin Research Base for Artificial Rescue and Conservation Breeding of South China Normal University (PRB-SCNU). The behavioral characteristics and breeding strategies were analyzed, and the results were discussed together with information on other captive Sunda pangolin pairs at PRB-SCNU. The results found that there was no obvious estrus behavior in the captive female, while the male could exhibit sexual excitement and courtship behavior after a brief introduction period. Repeated copulation continued over many days after the female accepted the courtship. The average duration of copulatory behavior was 248.9 ± 148.7 s (n = 25), and all copulation occurred between 20:00 and 08:00 hr in the natural day–night photoperiod. The mating position of Sunda pangolins was lateral–ventral and was classified as the ninth or eleventh pattern under both Dewsbury's and Dixson's classification systems. This study can provide scientific guidance for the captive breeding and management of Sunda pangolins and other pangolin species, which is of great significance for ex situ conservation tactics.     

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.     

Serum and fecal steroid analysis of ovulation,pregnancy, and parturition in the black rhinoceros (Diceros bicornis)

Studies were conducted to determine: (1) if fecal hormone metabolite concentrations correlated with serum estrogen and progesterone concentrations, follicular activity and reproductive behavior in the black rhinoceros (Diceros bicornis) and (2) if threshold values of respective fecal metabolite concentrations correlated with pregnancy. Blood and fecal samples were collected, in conjunction with transrectal ultrasound and behavior observations, for an 18-month period from one black rhinoceros female. Subsequently, serial fecal samples were collected from 13 females in 10 zoos. Quantitative analysis of serum progesterone (P₄) and estradiol (E₂) was performed by radioimmunoassay (RIA): analysis of fecal estrogen metabolites (E) and fecal progesterone metabolites (P) were performed by enzyme immunoassay (EIA). Serum P₂ concentrations identified two luteal phase patterns and two nadirs which corresponded with behavioral estrus. Fecal E patterns indicated a sharp peak which corresponded with breeding. concentrations of fecal P illustrated identifiable nadirs and several peaks which corresponded to serum P₄ nadirs and luteal phases. Serum P₄ concentrations were not different between the luteal phase and pregnancy. Fecal P concentrations started to rise above luteal phase concentrations approximately 150 days postbreeding and remained elevated until immediately before parturition. Serum E₂ and fecal E concentrations rose and subsequently declined after parturition. In the fecal samples from seven pregnant females, fecal P concentrations were similarly elevated compared to six nonpregnant females. Results indicated that fecal steroid metabolites accurately reflected serum steroid hormone concentrations and that the measurement of P and E concentrations permitted the characterization of the estrous cycle, the diagnosis of pregnancy, and the onset of parturition. Zoo Biol 16:121–132, 1997. © 1997 Wiley-Liss, Inc.     

Prosimian juvenile mortality in zoos and primate centers

I review literature on juvenile mortality of captive prosimians in order to evaluate the available information on captive breeding. Juvenile mortality includes abortion, premature mortality, stillbirth, and death of the unweaned young. Prosimian juvenile mortality ranges between 25 and 45% in captive populations. It is generally lower in the Lemuroidea, particularly the Cheirogaleidae, than in the Lorisoidea. Mortality is particularly high in the Lorisinae. Most mortality, including a high stillbirth rate, occurs on the first day and during the first 10 days thereafter. Stress, maternal neglect and traumatic insults, not infrequently linked to each other, are the most frequently reported causes of death. The percentage of congenital malformations tends to be high in some colonies. Sex of the infant and parity seem to be important risk factors for juvenile mortality, whereas litter size does not appear to be important. Based on few data, wild- caught females appear to have higher breeding success than those born in captivity. Synchronized births in lemuroids and isolated births in Galagoare more likely to result in successfully weaned infants.     

Long-term Study of Group Dynamics and Female Reproduction in Venezuelan Pithecia pithecia

White-faced sakis (Pithecia pithecia) are well known for their specialized feeding strategy and dependence on seed-eating, but we know less about social dynamics and reproduction. I summarize data from 1990 to 2001 on sakis inhabiting a small island in Lago Guri, Venezuela that includes changes in group composition, aggressive behavior, and female reproductive histories. Though the characteristic group size and typical mating system are still uncertain for wild, free-ranging Pithecia spp., size of the study group ranged from 2–3 adult females and 1–4 adult males. My group and I collected fecal samples from adult females, which we dried and assayed for estrogen (E₁C) and progesterone (PdG) conjugates to document reproductive cycles and female development. During the study, as many as 3 females were either cycling or pregnant at the same time. Ten infants were born during the study, 4 of which survived to adulthood. Five interbirth intervals after weaning an infant ranged from 12 to 36 mo. Though researchers often assume Pithecia spp. are monogamous, multiple breeding females can coexist in groups without evidence of reproductive suppression. Within the pitheciine clade, Pithecia spp. exhibit a mosaic of behavioral and morphological traits intermediate between bearded sakis and uakaris on the one hand and their sister-group, the pair-bonded titis, on the other.