Color changes in the haircoat of patas monkeys (Erythrocebus patas)

Caged patas monkeys were evaluated monthly to determine changes in the color of their hair during infancy, adolescence, pregnancy and lactation. From birth until 3 months of age the facial and anterior crown hairs were short, sparse, and completely black. The body fur was a fine, short, fawn-colored hair mixed with longer black hairs which produced a black-tipped effect. During the second 3 months of life the body fur and anterior crown fur became coarser, longer, and changed to a red-brown color. The facial hairs thickened and became longer, but remained totally black. A thin line of black hairs outlined the brow and temple. The black chin hairs were gradually replaced by white from 7 to 24 months of age, and the upper lip hairs changed from black to white during the second year of life. Color changes related to pregnancy and lactation were confined to the nosepatch, cheek, and browline hair. The nosepatch and cheek hair changed from black or grey to completely white, and the browline faded to the approximate color of the body fur. These changes began approximately at the end of the second trimester of pregnancy, maximized during the third month of lactation, began to darken 1 to 2 months later, and returned completely to the black, nonpregnant colors approximately 1 year postpartum. In one nonlactating female, the darkening was delayed until 500 days postpartum and in one female ovariectomized in the light color phase, the darkening was complete 200 days later. The cause of these changes is believed to be hormonal, resulting from altered endocrine function during maturation and pregnancy, which may alter melanocyte stimulating hormone activity.     

Life-history parameters of a wild group of West African patas monkeys (Erythrocebus patas patas)

Based on long-term, although intermittent, observations (2 years 4 months of 14 years), we present data on birth seasonality, age at first birth, interbirth intervals, mortality rates, age at first emigration, and population change of a wild population of West African patas monkeys (Etythrocebus patas patas) in northern Cameroon. Birth season was from the end of December until the middle of February, corresponding to the mid-dry season. In spite of large body size, the patas females had the earliest age at first birth (36.5 monthsold) and the shortest interbirth intervals (12 months) compared to the closely related wild forest guenons. Age at first emigration of the males was considered to occur between 2.5 and 4.5 years. The group size of the focal group drastically decreased between 1984 and 1987, and steadily increased until 1994, then decreased again in 1997. The neighboring group also showed a similar trend in group size. The population decreases were likely to be caused by drought over 3 years. Annual crude adult mortality rate was 4% during population increase periods (PIP) between 1987 and 1994. It rose to 22% during all the periods (AP), including drought over 3 years. Despite their smaller body size, the rate of the wild forest guenons (Cercopithecus mitis) (4%) was the same and much lower than those of the patas during PIP and AP, respectively. The annual average juvenile mortality rate was 13% during PIP and it also rose to 37% during AP. That of wild forest guenons (C. ascanius) (10–12%) was a little lower and much lower than those of the patas during PIP and AP, respectively. These findings were consistent with Charnov's theoretical model of mammalian life-history evolution in that patas with high adult and juvenile mortality showed early and frequent reproduction in spite of large body size. Charnov also considered high adult mortality as a selective force and high juvenile mortality as a density-dependent consequence of high fecundity. Our results support the former but not the latter research findings.     

Influence of age,sex, and caging on joint mobility in the patas monkey (Erythrocebus patas)

Normal range of joint mobility in the extremities of the patas monkey, Erythrocebus patas, was established for a free-ranging colony of 64 animals at La Parguera, Puerto Rico (Caribbean Primate Research Center). Eighty-five animals that had been caged (30″ × 30″ cages) for up to 5 years were used for comparison. Passive joint mobility of anesthetized animals was measured with a goniometer. Nine parameters (five on the forelimb and four on the hindlimb) were measured on each animal. The data were sorted into subsets according to the animal's age, sex, place of birth, and type of confinement, if any. The number of animals in each subset was recorded and the mean (in degrees) and standard deviation for each parameter were calculated. A P?0.05 on two-tailed Student's t-tests was considered significant. Comparisons between free-ranging males and females showed significant differences in one or two parameters for all age groups. A cross-sectional sample of free-ranging animals of both sexes showed that significant changes in joint mobility occurred only in the first 18 months of life. Joint mobility of all caged animals, however, was highly variable, and even between the more mature animals there were significant differences in several parameters. Almost all comparisons of subsets of the same age and sex showed significant differences between caged and free-ranging animals in at least one parameter. When the caged animals were laboratory-born, however, these differences were significant in five out of nine parameters. The results suggest that, although caging itself affects joint mobility, the age of first confinement may have an even greater effect than the length of the confinement.     

Reproduction and social rank in female stumptail Macaques (Macaca arctoides)

Reproductive physiology was studied in female stumptail macaques. Initially the monkeys were housed indoors (individually and in small groups) and later as one large (92 individuals) social group in an outdoor cage. Most data were collected during the 4-year outdoor period. Plasma progesterone determination in blood samples taken at weekly intervals allowed estimation of ovulation and conception dates. The age at first ovulation (X =3.73 years) was positively correlated with body weight at 3 years of age. The average age at first birth was 4.90 years. Gestation lengths averaged 176.6 days. Following a live birth ovulations returned after a mean interval of 11 months but following an abortion or still birth this interval was 1 month. Usually a number of ovulatory cycles (X =2.37) preceded a conception. Interbirth intervals (IBIs) in the outdoor cage (X =619.4 days) were significantly longer than IBIs during the indoor period (X =523.1), because indoors the infants were weaned at the age of 7 months, while outdoors weaning occurred more naturally. IBIs following abortions or still births (X =291.9 days) were significantly shorter than IBIs following live births. Age at first ovulation, age at first birth, IBIs, and infant production rates were not correlated with dominance rank. Ovarian cycle lengths (X =30.2 days, mode = 28 days) were comparable to previously reported data from laboratory-housed stumptails. No systematic seasonal fluctuations were found in the onset of sexual maturity, in ovarian cycle lengths, in copulation frequencies, and in distribution of births.     

Embryonic development in Erythrocebus patas

The developmental stages of 12 Erythrocebus patas embryos, ranging in gestational age from 30 to 50 days, is described. The pattern of embryogenesis in E. patas closely parallels the anatomic characteristics of human and other nonhuman primate embryos between stages 12 and 23. However, there is a delay in development in E. patas similar to that observed in human embryos which differs from the macaques and baboons. This temporal difference in the embryonic period is an important factor in the design and analysis of early pregnancy studies in this species.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Allomaternal behavior in a group of free-ranging patas monkeys

A free-ranging group of patas monkeys (Erythrocebus patas) containing 18 individually identifiable adult females was observed for approximately 400 hours, equally distributed over two two-month periods corresponding to the breeding and birth seasons, at the La Parguera facility of the Caribbean Primate Research Center. The large number of infants born in the spring and early summer (n = 14) allowed for detailed observations of alloparental behaviors, with a focus on allomothering by the adult females. Seven types of alloparental behaviors were recorded: contact, nuzzling, grooming, agonism, close visual inspection, attempted kidnapping, and kidnapping. Adult females emitted the vast majority of allomaternal behavior, the patterning and frequency of which closely resembled the patterning and frequency of inter-adult female social grooming. Relative dominance status of the participants did not consistently predict the directionality of allomothering. The most commonly observed allomaternal behaviors were contact and nuzzling, which are primarily affiliative behaviors; agonism was rare. Successful kidnapping occurred eight times. Immature monkeys (n = 22) emitted an additional 32 alloparental acts. A propensity towards allomothering by experienced females would be most beneficial to patas infants due to the patas' tendency towards dispersed foraging and rapid flight in the presence of danger. It is possible that direct competition with groups of rhesus macaques for available resources on the island served as a proximal cause for the allomothering observed in this patas group.     

Development and mother-infant relations among captive patas monkeys

Generalizations about the rate of behavioral development and mother-infant relations in nonhuman primates are often based largely on observations of a few closely related species of macaques. Patas monkeys (Erythrocebus patas)are sufficiently distant phylogenetically and distinct in their social and ecological adaptations from the well-studied macaque species that observations of their patterns of infant development and mother-infant relations may indicate to what extent macaque patterns are typical of Old World monkey species. Eight patas infants living with their mothers in an established captive group were observed for 960 hr over the first year of life. These infants showed a rapid rate of behavioral development and attainment of independence from mothers. Patas also have one of the fastest rates of sexual maturation of any Old World monkey species. This pattern of rapid social and sexual development can be viewed as a response to a highly seasonal savannah environment in which there is a premium on ability to achieve nutritional, locomotor, and social self-sufficiency as quickly as possible and to reproduce as early and as often as developmental constraints will permit. Patterns of infant development and mother-infant relations may be best understood as an integral part of a species’ overall life history pattern.     

Housing conditions and breeding success of chimpanzees at the primate center TNO

Results of rearing and breeding chimpanzees at the Primate Center TNO are presented. The colony was built up from 1964 to 1971 by the acquisition of mostly young chimpanzees; thereafter, it was increased by local breeding. The ages at which the animals became reproductive were between 6 and 11 years for the males and between 7 and 15 years for the females. Seventy-six percent of the pregnancies (N = 132) were carried to full term and 87% of these were live births. Fifty-five percent of the babies were nursed by their mothers for 2–10 months. The next pregnancy after an abortion occurred on the average after 7 months; after a carriage to term, this occurred after 11.9 months. The difference was not influenced by the duration of the weaning period. Animals of 2 years or more that had been weaned within a month were more likely to show body rocking than animals weaned later. Cases of disturbed social or reproductive behavior were rare; the first locally bred animals have become reproductively active.     

Reproduction of the greater bushbaby (Galago crassicaudatus panganiensis) under laboratory conditions

A breeding colony of Galago crassicaudatus panganiensis was maintained under laboratory conditions for four years, August 1971 to July 1975. The estrous cycle and the gestation period averaged 39 and 132 days in length, respectively. Twinning occurred in 14.5% of the pregnancies. No postpartum estrus was observed, although 1.2 conceptions per female per year were recorded. Breeding occurred throughout the year. Puberty occurred between ten and 18 months of age, the first conception occurred between 15 and 18 months of age, and reproductive capability decreased rapidly between ten and 12 years of age.     

Longitudinal study of dominance relations among captive patas monkeys

Eight and a half years of dominance relations within a captive group of patas monkeys were analyzed. It was found that matrilineal kinship significantly influenced individuals' ranks. In contrast, with the exception of certain intramatriline changes, increasing age had no predictable effect on overall rank, at least for females (this was untestable for males). Offspring typically challenged maternal dominance and in eight of twelve dyads, offspring either rose fully over their mothers (three cases, all daughters) or at least achieved dominance ambiguity with them. Additionally, two of the four younger sisters with an opportunity to rise in rank over an older sister did so. The group dominance hierarchy was unstable for 75% of the study due to a combination of agonistically induced and demographically induced rank changes. Concentration of the highest ranks in a single matriline showed a stronger association with group hierarchy stability than did the presence of an adult, nonnatal male. Group hierarchy stability was associated with increased affiliation (sitting close and sitting touching), but otherwise there were no behavioral correlations. Individuals' ranks within the group hierarchy were unrelated to their chances of being wounded or having diarrhea. Adult females' ranks were over twice as stable as the group hierarchy (57.1% stability), but stability/instability was not correlated with any behavioral changes. Available evidence suggests that dominance relations play only a minor role in the organization of patas monkeys' intragroup behavior. Am. J. Primatol. 42:41–51, 1997. © 1997 Wiley-Liss, Inc.     

Growth and reproduction in captive tufted capuchins (Cebus apella)

We present data on weight and reproduction from a colony of tufted capuchins monkeys (Cebus apella) over a 12 year period. The data constitute a normative record for this species. Weight at birth averages 210 g, and infants gain weight rapidly. Females typically first conceived just after their fifth birthday, and males were fertile by 4 years, 5 months. Interbirth intervals average 576 days. Eighty-seven percent of live-born infants survived past 6 months. Three of eight live-born infants that died prior to 6 months succumbed from trauma inflicted by cage mates. Am. J. Primatol. 44:197–203, 1998. © 1998 Wiley-Liss, Inc.     

Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata)

In this study we investigated the reproductive characteristics of wild female Japanese macaques (Macaca fuscata fuscata) in 2 nonconsecutive years using noninvasive methods to monitor physiological events. We detected ovulation dates and ascertained conceptions from fecal hormone profiles. First ovulations occurred from middle October to early November in 1997, and from middle to late November in 1999. Most females conceived during their first ovarian cycle. On average, postconception bleeding occurred 18.4 days after ovulation, and menstruation occurred 13.7 days after ovulation. The average gestation length was 176.3 days. The average degree of facial redness and the percentage of females that copulated synchronously changed across the ovarian cycle and peaked in the periovulatory period. Although prolonged periods of postconception copulation have been reported in previous studies, they did not occur in this study, which suggests that such behavior may not be a species-typical characteristic. Female fertility varied between the 2 years. The copulation rates of females with no infant <1 year of age were 100% (14/14) in 1997 and 45.5% (5/11) in 1999. The ovulation rates of the female subjects that we chose for hormonal assays were 100% (9/9) in 1997 and 50.0% (3/6) in 1999. Th conception rates of these selected females were 100% (9/9) in 1997 and 16.7% (1/6) in 1999. The birth rates (the number of females that delivered divided by the total number of adult females in the troop) were 73.3% (11/15) in 1998 and 6.7% (1/15) in 2000. The modified birth rates (the number of females that delivered /the number of adult females with no infant <1 year of age) x 100 were 78.6% (11/14) in 1998 and 9.1% (1/11) in 2000.     

Correlation of perineal swelling with serum ovarian hormone levels,vaginal cytology,and ovarian follicular development during the baboon reproductive cycle

Perineal swelling was correlated with changes in vaginal cytology and serum ovarian hormone levels and with development of the ovarian follicle. The average length of 66 menstrual cycles as seen in 12 mature baboons was 35.7±.66 days with a range of 25 to 47 days. Laparoscopic observations and photographic documentation of follicular development were made as early as 13 days prior to ovulation with the most rapid follicular maturation occurring 24 to 48 hours before ovulation. In 38.5% of the cycles ovulation occurred on the last day of maximal perineal tumescence with 26.9% of the ovulations occurring one day after initial detumescence. In 17.8% ovulations occurred two to five days prior to detumescence while the remaining 17.8% occurred two to three days following first observed detumescence. The mean progesterone level during the follicular phase was significantly less than that in the luteal phase, 1.6 and 6.7 ng/ml respectively (p<0.01). The level of estrogen detected during the periods of maximal tumescence was significantly higher (p<0.05) than that detected in the remainder of the cycle, 19.8 and 5.9 pg/ml respectively. Vaginal smears were stained, observed microscopically, and found to correlate with perineal swelling, hormone levels, and laparoscopic observations.     

Reproduction and population growth in free-ranging mantled howling monkeys

Free-ranging mantled howling monkey (Alouatta palliata Gray) females experienced a regular estrus cycle averaging 16.3 days, demonstrated sexual skin changes, and participated in multiple matings before becoming pregnant. Gestation averaged 186 days. The average interval between births was 22.5 months. Sexual maturity occurred at approximately 36 and 42 months for females and males, respectively. Female age at first birth was about 3½ years. Births were scattered during some years and clustered during others. The age, rank, and parity of the females affected infant survival. More female than male infants survived to one year of age. Increased population size was the result of immigration rather than births.     

Initiation of feeding by provisioned patas monkeys: Evidence for the protection hypothesis

The applicability of the baboon-based protection hypothesis was tested with data from a provisioned, free-ranging group of Erythrocebus patas.The age/sex class of the individual which first approached and fed from one of the food hoppers during early morning feeding sessions was noted for 114 mornings. The presence of an observer, and periodically, rhesus monkeys,near the hopper made these approaches analogous to progressions described for feral baboons. Adult patas of both sexes approached and ate first significantly more frequently than was expected based on their respective proportions in the group, and immature monkeys less often. For adult females,initiating feeding was not correlated with dominance rank, although females in the middle and lower thirds of the hierarchy (n = 6 in each third) initiated feeding more frequently than did the females in the top third. The protection hypothesis accounts for the observed behavioral pattern, while explanations based on competitive exclusion and dominance relationships do not adequately account for the results.     

Social and environmental determinants of reproductive cycles in patas monkeys

The menstrual cycles of a captive group of patas monkeys were followed for 15 months by taking vaginal smears and lavages three times a week. Without an adult male in the group, menstrual cycles still showed the expected qualitative changes previously associated with the onset and with the end of a mating period. The addition of an adult male to the female group, once mating season cycles were evident, did not result in further changes in erythrocytes or sediment levels in vaginal samples or cycle regularity. Menstrual-cycle onsets for related females were significantly more synchronized than onsets for unrelated females. Preliminary observations on adult male patas housed separately from the females indicate that they too undergo seasonal changes in physiology and behavior.     

Long-term data on basic reproductive parameters and evaluation of endocrine,morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana)

Cycle and gestation lengths, menstruation patterns, female genital swelling characteristics, and male-female consortship durations are reported in a semifree-ranging group of Tonkean macaques (Macaca tonkeana) studied over a 12 year period. In addition, profiles of urinary estrone conjugates (E1C) and immunoreactive pregnanediol glucuronide (PdG) throughout four complete menstrual cycles in two females and three full-term pregnancies are presented. Based on intermenstrual intervals, a mean cycle length of 37–41 days (n = 55 cycles in 10 females) was found. Gestation length averaged 173 days (n = 27 pregnancies in eight females). Measurement of PdG immunoreactivity in urine revealed a cyclic pattern with a 5–15-fold increase between follicular and luteal phase concentrations, suggesting that PdG is a reliable indicator of ovarian cyclicity and luteal function. In contrast to PdG, E1C excretion showed no clear pattern throughout the cycle; however, highest values of E1C were usually found shortly before the onset of the luteal phase PdG rise at the presumed time of ovulation. Levels of both hormones were elevated during the first half of gestation and showed a marked increase throughout the second half, with maximum E1C concentrations being up to 100-fold higher than nonpregnant levels. Consortships by the male and occurrence of female genital swelling were long lasting (on average 5–10 days and 13 days, respectively) and were restricted to the follicular phase of the cycle. The day of maximal swelling and day of detumescence as well as the end of male consortship were closely associated with the periovulatory period. Swellings and consortships were longer following lactational ammenorhea than for subsequent cycles. The evolutionary significance of the cyclical changes undergone by females upon their relations with males is discussed. © 1996 Wiley-Liss, Inc.     

Mating strategy and reproductive success of male patas monkeys (Erythrocebus patas)

Mating behavior and paternity of offspring of wild patas monkeys were studied at Kala Maloue National Park, Cameroon. Observation of patas groups over three years revealed that multi-male situations occurred after takeover of the position of a resident male. Direct observation of behavior showed that resident males (harem males) occupied only 31% of mating in multi-male situations and 100% in one-male situations. DNA-typing revealed that resident males sired two of four of infants in the one-male situation and four of five in the multi-male situation. Under the two years cycle of the one-male situation and the multi-male situation, calculation shows that resident males sired more offspring than sneakers both in observation and paternity testing. Sneak mating occurred during both one-male and multi-male situations, and resident males performed compensatory mating, with dilution of sneaker sperm; these activities explain the discrepancy found between observation of mating and results of paternity discrimination.     

Reproduction in the slow loris (Nycticebus coucang)

The reproductive biology of the slow loris (Nycticebus coucang) is poorly documented because of infrequent captive breeding success and the absence of field studies of this species. Reproductive data were collected from a breeding colony of slow lorises held at the Duke University Primate Center for the past 10 years. Nineteen infants were born, with a sex ratio of 1:1 and a neonatal mortality rate of 15.8%. In all cases, litter size was one. Females born in the colony copulated for the first time between 18 and 24 months of age. A male that reached sexual maturity in the colony sired his first offspring at the age of 17 months. Estrous cycles ranged in duration from 29–45 days, with copulations usually occurring for 1 day of estrus. Gestation length averaged 192.2 days. Although a postpartum estrus was observed in three cases of infant death, no conceptions resulted. Lactation lasted approximately 6 months. A clear birth peak was observed, with 12 out of 19 births occurring in March, April, and May. The comparatively low basal metabolic rate of this species may account for the unusually low reproductive rate of the slow loris in comparison with other prosimian primates.