Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas)

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.     

Age at first reproduction in philopatric female muriquis (<Emphasis Type="Italic">Brachyteles arachnoides hypoxanthus</Emphasis>)

Female northern muriquis (Brachyteles arachnoides hypoxanthus or B. hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA, Minas Gerais, Brazil typically disperse from their natal groups at an average age of 6.1±0.6 years (median =6.0 years, range =5.3–7.8 years, n =22), prior to the onset of puberty and sexual activity. Immigrants do not conceive until at least their second mating season, and the minimum interval from immigration to first reproduction has been 2.0 years. Age at first reproduction in dispersing females, previously estimated at 8.9 years, has now been documented at 9.0 and 9.25 years for two females whose birth dates are known. This is older than the 7.5 years at which the only female previously known to have reproduced in her natal group gave birth. Here, we present new data from a second female that reproduced in her natal group. This female (BA) was first observed to copulate at 5.5 years, and gave birth to her first infant at 7.25 years of age. Her 1.75-year cycling-to-first conception delay was only slightly shorter than the minimum recorded for immigrant females, and thus was not responsible for her young age at first reproduction compared to dispersing females. Although our sample size is small, our findings suggest that early puberty may permit females to reproduce in their natal group, implying a possible link between life history trade-offs and dispersal patterns. Because the only two females that have reproduced in their natal group were maternal sisters, it is also possible that maternal effects on age at puberty can impact dispersal patterns, particularly in small populations of primates.     

Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus).

We monitored the birth patterns of sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus) during a 4‐yr period from October 1996 to August 2000 at the Estação Biológica de Caratinga, Minas Gerais, Brazil. Brown howler monkey births (n = 34) occurred throughout the year, and birth frequencies did not differ between rainy and dry season months. The aseasonal birth patterns of the howler monkeys differed significantly from the dry season concentration and dry month peak in muriqui births (n = 23). We found no effects of infant sex or the number of females on interbirth intervals (IBIs) in our 10 howler monkey study troops. IBIs of brown howler monkeys averaged 21.2 ± 2.5 mo (n = 8, median = 21.0 mo), and were significantly shorter following dry season births than rainy season births. Their IBIs and yearling survivorship (74%) were similar to those reported for other species of howler monkeys, but yearling survivorship was much lower than that of muriquis (94%), whose IBIs were more than 12 mo longer than those of the howler monkeys. Our study extends comparative knowledge of birth patterns in Alouatta to a poorly known species, and provides insights into the different ways in which diet and life history may affect the timing of births in large‐bodied platyrrhines under the same seasonal ecological conditions. Am. J. Primatol. 55:87–100, 2001. © 2001 Wiley‐Liss, Inc.     

Age of the Jeju pony (Equus caballus) at first reproduction: potential costs for foals and mothers that first reproduce early in life

In a related paper, we showed that mares that reproduced early in life tended to have higher fecundity because of a decrease in the duration of inter-birth intervals relative to mares that reproduced later in life. However, we know that young mares are subordinate to older mares. Hence, costs associated with low dominance rank might offset the benefits of earlier reproduction. We compared harassment of foals of female Jeju ponies that first reproduced at three years of age with that of foals of females that first reproduced at five years of age. As a consequence of their positions in the linear dominance hierarchy, foals born to and guarded by young mares were harassed more frequently than foals whose mothers were older when they first reproduced. A mare that reproduced early in life guarded her offspring more closely and intervened between her foal and neighboring mares more frequently than those mares which first reproduced when older. This need to guard their foals and the harm that might ensue from frequent harassment might counter-balance selection towards earlier reproduction in mares.     

Male Relationships and Infant Deaths in Red Howler Monkeys (Alouatta seniculus)

For decades howler monkeys were considered to be among the most peaceful animals. Recent investigators, however, have noted that, although male aggression is rare, it may be extremely severe; the criteria used to quantify howler relationships should therefore be different from those used for other primates. This paper describes the pattern of male relationships in the red howler monkey Alouatta seniculus, and examines its effect on reproductive success within the troop and the ability of troop males to resist intrusion by competing males. 4 of the 8 infants born during the study period were killed or disappeared when change occurred in relative status between two adult males.     

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five-year period in a population of bats in south-west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.     

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.     

Life-history characteristics of a wild population of vervets (Cercopithecus aethiops sabaeus) in Barbados,West Indies

Life history data are presented for a population of vervets, Cercopithecusaethiops sabaeus, in Barbados, West Indies. The data were obtained from two habituated troops and from vervets captured during a large-scale trapping program. Individuals of known age from one troop were weighed periodically, and separate growth curves generated for males and females. The mean weight of captured adult females was 3.3 kg; that of adult males, 5.3 kg. The average age at sexual maturity is estimated at 34 months for females and 60 months for males. Vervets give birth throughout the year, but most infants are born between April and July. The average interbirth interval following a surviving infant is 11.8 months. The mortality of juveniles is heaviest between birth and 2 years of age and decreases thereafter. Males emigrate from their natal troops at sexual maturity and one incident of a juvenile female emigrating is reported.     

THE EFFECT OF BIRTH DATE ON FITNESS OF FEMALE DWARF PERCH,MICROMETRUS MINIMUS (PERCIFORMES: EMBIOTOCIDAE)

Lifetime reproductive success may vary considerably with birth date. I measured phenotypic selection on female birth date in a viviparous teleost fish (Embiotocidae: Micrometrus minimus) by sampling birth-date cohorts over time in Tomales Bay, California. Four episodes of selection were measured: survival from birth to first reproduction, reproductive success in the first breeding season, survival to second reproduction, and reproductive success in the second season. Birth date had a significant impact on fitness in the first two episodes. Early born females were more successful in their first breeding season than late born females (directional selection on birth date), but early born females were less likely to survive the period between birth and first reproduction, relative to females born in the middle of the season (stabilizing selection on birth date). The final two episodes of selection had no detectable effect on birth date. Because of the relationship between birth date and survival in the first year, overall selection on female birth date was stabilizing.     

Parental behavior and infant development in ruffed lemurs (Varecia variegata) in a northeast Madagascar rain forest

Parental behavior and infant development of black and white ruffed lemurs (Varecia variegata) were studied on Nosy Mangabe Island in northeast Madagascar. Ruffed lemur females produced twins, prepared nests for neonates in the trees, transported infants by mouth, and parked them in the trees. During two consecutive birth seasons, the average birth rate for nine females was 0.58. Two females reproduced in one social group. Lactating females spent most of their time resting with their infants or foraging for food. Infants developed rapidly and were fully mobile by 3–4 months. No female reproduced successfully in 2 consecutive years. In 1988, infant mortality within 3 months of birth was very high (64%). Accidental falls may have been one major cause. Adults of both sexes, including a reproductive female, exhibited alloparental behavior such as guarding infants and nonmaternal nursing. Alloparental care may increase the likelihood of infant survival. Some of these observations are not compatible with the idea that ruffed lemurs live in small pair-bonded groups, as other researchers have suggested.     

Reproductive efficiency of captive Chinese- and Indian-origin rhesus macaque (Macaca mulatta) females

Reproductive and survival records (n=2,913) from 313 Chinese-origin and 365 Indian-derived rhesus macaques at the Tulane National Primate Research Center (TNPRC) spanning three generations were studied. Least-squares analysis of variance procedures were used to compare reproductive and infant survival traits while proportional hazards regression procedures were used to study female age at death, number of infants born per female, and time from last birth to death. Chinese females were older at first parturition than Indian females because they were older when placed with males, but the two subspecies had similar first postpartum birth interval (1st PPBI) and lifetime postpartum birth interval (LPPBI). Females that gave birth to stillborn infants had shorter first postpartum birth intervals (1st PPBI) than females giving birth to live infants. Postpartum birth intervals decreased in females from age 3 to 12 but then increased again with advancing age. Chinese infants had a greater survival rate than Indian infants at 30 days, 6 months, and 1 year of age. Five hundred and forty-three females (80.01%) had uncensored, or true records for age at death, number of infants born per female, and time from the birth until death whereas 135 females (19.91%) had censored records for these traits. Low- and high-uncensored observations for age at death were 3 and 26 years for Chinese, and 3 and 23 years for Indian females. Uncensored number of infants born per female ranged from 1 to 15 for Chinese females and 1 to 18 for Indian females. Each of these traits was significantly influenced by the origin×generation interaction in the proportional hazards regression analyses, indicating that probabilities associated with age at death, number of infants born per female, and time from last birth to death for Chinese and Indian females did not rank the same across generations.     

On the virtue of being the first born: the influence of date of birth on fitness in the mosquitofish, Gambusia affinis

We found in an earlier study that mosquitofish (Gambusia affinis and G. holbrooki) ceased reproduction in the late summer, long before the end of warm weather, stored fat, then utilized reserves to survive the winter and initiate reproduction the following spring. We hypothesized that this pattern of fat utilization was a life history adaptation that enabled the fish to acquire food resources in the autumn then allocate them to reproduction the following spring when the fitness of the young would be greater. Here we evaluate one aspect of this hypothesis by evaluating the probability of survival to maturity and fecundity of young as a function of date of birth. We placed cohorts comprising eight to ten litters of young born early‐, mid‐ or late in the reproductive season in replicate field enclosures. The entire experiment was repeated in two different years. Early‐born young had a significantly higher probability of survival to maturity but did not differ in fecundity relative to the last cohort of the season. Early‐born young also attained maturity early enough to reproduce in their year of birth while late‐born young had to overwinter before reproduction. The fitness consequences to the mother of either producing one more litter of young at the end of the season, versus instead storing fat and reproducing the following spring are not as determinate as are the effects of date of birth on offspring fitness. Females most often gain fitness by not producing one last litter and instead over‐wintering. If, however, the overwinter survival of offspring is not influenced by their size at the end of the season, then a female's fitness could be enhanced by producing one more litter late in the season. If instead the probability of overwinter survival is strongly influenced by the size of offspring at the end of the season, then our results suggest that a female gains more by deferring reproduction and storing for overwinter survival and reproduction the following spring.     

Reproduction in wild female olive baboons

The purpose of this paper is to evaluate several factors that influence female reproduction in a large troop of wild olive baboons (Papio cynocephalus anubis) based on 4 consecutive years of demographic data. Interbirth intervals were significantly shorter for females whose infants died before their next conception than for females whose infants survived. High-ranking mothers of surviving infants had significantly shorter birth intervals than comparable low-ranking mothers, independent of maternal age. This occurred mainly because the interval from resumption of cycling to conception was significantly shorter for high-vs. low-ranking females. Dominance rank did not influence sex ratio at birth, infant survival in the first 2 years, or adult female mortality. Age was also significantly related to interbirth intervals, with older females having shorter intervals. Primiparous females had consistently longer reproductive intervals than did multiparous females, but this difference reached statistical significance only for females whose infants died before the next conception. Primiparous females also experienced significantly higher infant mortality. Data on body size and estrous cycle length indicated no differences between high- and low-ranking females. Nutritional and stress-related mechanisms that may underlie the reproductive advantages of high rank are discussed.     

Deaths in a desert baboon troop

Over a 4-year period, three of 22 infants born in a desert-dwelling chacma baboon troop (Papio ursinus) survived to more than 6 months of age. Tick infestation and infant kidnapping by adult females were the main causes of infant death. The high neonatal mortality resulted in a rapid birth rate through a decrease in duration of interbirth intervals for mature females. There were more adult male deaths in the troop than adult female deaths. Males died from canine inflicted wounds sustained during fights.     

Growth and reproduction of two species of Akodon and their hybrids

Growth and reproduction of Akodon molinae (A.m.), A. dolores (A.d.) (Rodentia: Cricetidae), and their hybrids are described. A.d. showed less fertility under animal room conditions, fewer "successful" matings, similar litter sizes, and an altered sex proportion as compared to A.m.; A.d. ovulatory index is supposed to be higher than mean litter size. X-linked lethal gene(s) and chromosome polymorphisms are possible causes of these variations. Interspecific crosses showed a marked seasonal (summer) tendency in parturitions. Intraspecific matings also produced young during winter. F1 hybrids showed a reversed tendency, while F2 matings returned to the parental pattern. A.d. male X A.m. female and F1 crosses presented larger litter sizes than the other pairings. A.m. exhibited sexual differences in weight after 60 days of age. A.d. and F1 hybrids did not show significant differences in weight of both sexes at any age. A.m. males and females were heavier than A.d. individuals except 12 months after birth. F1 hybrids born to A.m. male were heavier at birth than the A.d. female s interspecific offspring, and may be interpreted as a maternal influence of the A.m. females. Hybrids were heavier than their parents at birth and some of them were also heavier at 21 days, and probably is due to pseudoheterosis. The comparison of body measurements between sexes of both species did not give conclusive results. A.m. females were larger than females of A.d. Males of both species showed similar total lengths; A.m. males had larger body lengths and shorter tails. Body measurements were not related to weight variations. However, differences in weight and measurements between sexes appeared simultaneously at 2-6 months. This probably reflected the attainment of maturity.     

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same‐age siblings have been less‐studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938–2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter‐born peers and they significantly outperform litter‐born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed‐sex litter outperform isosexually‐born individuals (i.e., those born in all‐male or all‐female litters), suggesting that same‐sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male‐biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same‐age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.     

Factor affecting body mass of young fat dormics (Glis glis) at weaning and by hibernation

This paper describes the factors affecting body mass at weaning and by hibernation of young fat dormice (Glis glis) We studied a free-living population in 1991 and 1992 in a mixed forest where 100 nest-boxes were placed. In the two years, 128 females used the nest-boxes to give birth and rear their litters and more than 900 dormice have been individually marked. Body mass of young at weaning was positively correlated to body mass of the mother in both years and to birth date in 1991, while litter size was negatively correlated to body mass of the young in 1992 only, when birth took place about two weeks later than in 1991. On the contrary, by the time of hibernation, young born later weighed significantly less than those born earlier in the season, and heavier young at weaning remained heavier by hibernation, while maternal body mass and litter size did not significantly affect body mass of young at this stage. Body mass of the mother was negatively related to the date of parturition and early breeding females lost weight during lactation, while females that bred later did not. It seems, therefore, that early breeding carries a cost that only females in good condition can afford. It appears that females may follow two strategies: those in poor body condition will delay pregnancy so that lactation occurs when environmental feeding conditions are at their best; those in good condition will breed earlier, since they can afford to lose weight during lactation. Their young will have more time to grow before hibernation and the mothers themselves will have a longer period of time for restoring their fat reserves.     

Lower birth weight of offspring born after self-poisoning of parent.

Birth weight was evaluated in 777 and 217 livebirths, respectively, of index females and female partners of index males born before and after severe self-poisoning with drugs. Birth weight was also evaluated in matched controls. Babies born to index females months or years after an attempted self-poisoning were found to have a lower birth weight than before this suicide attempt. The difference in the birth weight of subsequent pregnancies of index and control females was also highly significant. A similar trend was observed in livebirths of female partners of index males. However, the differences were not significant between previous and subsequent pregnancies and between index cases and matched controls.     

Reproductive biology of captive alpine ibex (Capra i. ibex)

We studied the reproductive biology of alpine ibex bred at the Peter & Paul Wildlife Park, St. Gallen, Switzerland, from 1930 through 1943 and 1968 through 1983. Peter & Paul Wildlife Park had supplied most of the original stock used to reestablish ibex populations in the European Alps after they had become extinct. Ibex females were seasonally polyestrous. Their estrous cycle averaged 20 days, and their gestation period averaged 167 days. Females between 1 and 15 years of age on average produced 0.78 young per year; females between 3 and 13 years of age produced 0.99 young per year. The average age at which captive ibex females gave birth was 8.44 years. Sex ratio at birth was unbiased. More singletons than twins were born, but the proportion of twins born during the years 1968 through 1983 was higher than during the earlier study period. There were no differences in the survival rates of male or female and single or twin offspring.     

Reproductive Coordination in a Nonseasonally Breeding Primate Species,Macaca silenus

Varying types of reproductive coordination among females have been described for several mammals. Among nonhuman primates, female reproductive coordination has usually been described as breeding seasonality, or in few cases, closer synchrony within the breeding or birth season. We examined birth records from a large captive colony of lion-tailed macaques, Macaca silenus, a nonseasonally breeding species, in order to determine the degree of female reproductive synchrony in this population. Births were nonrandomly distributed over the 10-year study period. Of the total of 28 births, the majority (21 or 75 %) of births occurred in cohorts, in spite of wide variations in interbirth intervals among cohort birth mothers. Cohorts consisted of two to five infants born within a 90-d period or less. Of the remaining 7 “isolated” births, four were in the three years in which only one or two births occurred. The pattern of cohort births was nonrandomly distributed according to mother's parity: three of the isolated births were to primiparous mothers, whereas only one of the 21 cohort births was to a primiparous mother. Estrous synchrony results showed that females in the longer-established of two groups exhibited greater synchrony, suggesting social facilitation of reproductive coordination. It is thus suggested that synchrony in this sample was the result of social rather than ecological mechanisms, as has been hypothesized for some other mammalian species.