Management and husbandry of ruffed lemurs,Varecia variegata,at the San Diego Zoo. I. Captive population,San Diego Zoo housing and diet

The captive history of the ruffed lemur is presented with concentration on taxonomy, captive population and husbandry of the San Diego Zoo population. At the conclusion of 1985, the living population of black and white ruffed lemurs numbered 358; red ruffed lemurs totaled 125. The San Diego Zoo population, established between 1965 and 1970, began with two pairs of each subspecies. Intensive breeding at the Primate Propagation Center resulted in the birth of 135 black and white ruffed lemur infants and 95 red ruffed lemur infants as of January 7, 1986. Housing specifications are presented for the off-exhibit 96-unit breeding facility, describing enclosure size, material, nest box composition, and enclosure furniture. The diet is described, which emphasizes high-protein, high-fiber foods and leaves.     

Inbreeding effects in captive populations of ruffed lemurs

The two subspecies of ruffed lemurs (Vareica variegata variegata andVarecia variegata rubra) have been maintained in captivity since 1959 and all institutions which hold ruffed lemurs have contributed data to theVarecia International Studbook. Studbook data were used to analyze inbreeding effects on survival in both subspecies ofVarecia. Several variables, including offspring's inbreeding coefficient, litter size, mother's inbreeding coefficient, and mother's age, were examined for significant associations with percent survivorship per litter. Percent survivorship per litter was negatively correlated to the offspring inbreeding coefficient in the black and white ruffed lemurs (p<0.001) but no significant association was found for red ruffed lemurs. Although emphasis has been put towards the status of the red ruffed lemurs due to the small founder size, the black and white ruffed lemurs should also be managed with care due to the lower tolerance to inbreeding in captivity.     

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.     

The breeding system of wild red ruffed lemurs (<Emphasis Type="Italic">Varecia rubra</Emphasis>): a preliminary report

Captive studies have shown that ruffed lemurs (Varecia) have an unusual suite of reproductive traits combined with extremely high maternal reproductive costs. These traits include the bearing of litters, nesting of altricial young, and absentee parenting. To characterize the breeding system of this enigmatic lemur, reproductive traits must be contextualized in the wild. Here, I provide a preliminary report of mating and infant care in one community of wild red ruffed lemurs (Varecia rubra). Observations span a 15-month period covering two birth seasons and one mating season on the Masoala Peninsula, Madagascar. Factors that are not possible to replicate in captivity are reported, such as mating pattern, natality and mortality rates, the location of nests within the home range, and the structuring of infant care within a natural community. V. rubra at Andranobe have a fission-fusion, multifemale-multimale grouping pattern and a polygamous mating system. They do not mate monogamously or live strictly in family-based groups as suggested by previous workers. During the first 2 months of life, nests and infant stashing localities are situated within each mother's respective core area, and inhabitants of each core area within the communal home range provide care for young. As part of their absentee parenting system, infants are left in concealed, protected, and supportive spots high in the canopy, while mothers travel distantly. This practice is termed 'infant stashing'. Alloparenting appears to be an integral part of V. rubra's overall reproductive strategy in the wild, as it was performed by all age-sex classes. Among the alloparental behaviors observed were infant guarding, co-stashing, infant transport, and allonursing. Alloparenting and absentee parenting may mitigate high maternal reproductive costs. Furthermore, V. rubra may have a breeding system in which genetic partners (i.e., mating partners) do not always correspond to infant care-providers. Combined with recently available information on the behavioral ecology of wild ruffed lemurs, this preliminary report suggests directions for in-depth studies on Varecia's breeding system.     

Aspects of reproduction in ruffed lemurs (Lemur variegatus).

Results of breeding of ruffed lemurs (Lemur variegatus) at the Duke Primate Facility provide information concerning estrous cycle, sexual behavior, age of first conception, gestation period, parturition, litter size. L. variegatus differs from other Lemur species in these respects.     

A retrospective study of infant mortality of cotton-top tamarins (Saguinus oedipus) in captive breeding

Fifty of 156 (32%) colony bred cotton-top tamarins were stillborn, and 31 (20%) died within the first week after birth. The stillbirth rate was related to litter size and parity in captivity. A higher percent of single births were stillborn (69%) compared to those of twin births (26%) (p less than 0.005). A higher percent of infants born of the first litter in captivity (42%) were stillborn than those of subsequent litters (23%) (p less than 0.025). Stillbirths were not related to season of birth or sex of infant. Survival of live infants was unrelated to season of birth, sex, litter size, or number of litters.     

Reproductive patterns and birth seasonality in a South-American breeding colony of common marmosets,Callithrix jacchus

We analyzed data on captive-born and wild-caught females housed under natural conditions in a colony located in northeastern Brazil. No differences in reproductive performance were found between captive-born and wild-caught females. Twins were the most frequent litter size, followed by triplets and singletons. No parity effect was observed, with similar infant survival for nulliparous and multiparous females. No significant departures in sex ratio were detected for births and mortality of the male and female infants. The age of the females at the time of pairing showed a negative correlation with pairing-parturition length, but did not affect infant survival. The prolongation in pairing-parturition interval (PPI) and interbirth interval (IBI) was related to birth seasonality. The births were clustered in the second half of the dry season and the beginning of the wet season (November–March), and the time of pairing and the time of infant birth influenced the PPI and IBI, respectively. The use of outdoor cages, which allowed the animals to be aware of the seasonal variations in photo-period and rainfall seems to be sufficient to time the reproductive activity, even when the animals are maintained on a constant food supply.     

Simultaneous recordings from two physiologically different types of relay neurons, mitral cells and ruffed cells, in the olfactory bulb of goldfish.

Anatomical differences characterizing mitral cells and ruffed cells were published by Kosaka and Hama in three teleost species. Physiological responses from both different types of relay neurons were recorded extracellularly and simultaneously in the plexiform layer using a single tungsten microelectrode. During interstimulus intervals mitral cells responded with higher, frequently burst-like impulse rates triggered by the activity of epithelial receptor neurons. The mitral cell activity could be totally suppressed during local anesthesia of the olfactory epithelium. Ruffed cell impulse rates were low, and each action potential triggered a long-lasting (3-5 ms), continuously variable, summed up granule cell potential. In contrast to mitral cells, blockade of epithelial receptor cells significantly increased the activity of ruffed cells. I.e., the ruffed cells, which have no input from the olfactory epithelium, are spontaneously active, and are laterally inhibited by granule cells activated by mitral cells. During olfactory stimulation contrasting interactions between mitral cells and ruffed cells resulting in a drastic intensification of centrally transmitted information, frequently were recorded. An excitation of mitral cells activity via granule cells laterally inhibited the ruffed cells activity, and an inhibition of mitral cells activity simultaneously "released" an excitation of ruffed cells. This is the first physiological determination of different types of relay neurons in the olfactory bulb of fish.     

Reproductive output, maternal age, and survivorship in captive common marmoset females (Callithrix jacchus)

Common marmosets (Callithrix jacchus) demonstrate significant variation in reproductive output on both a yearly and lifetime basis in comparison to other anthropoid primates. We explore the factors that may be most important in determining reproductive variation in captive common marmosets. Studies have found that maternal age, maternal condition, and dam survivorship are related to reproductive output; however, these reports are not in agreement and are far from conclusive. With the use of a large, multicolony, demographic database pooling data across five marmoset colonies, we examined litter information for 1,649 litters, and reproductive summaries for 400 dams to assess 1) how reproductive output variation (total production, total weaned production) is determined by litter size, interbirth interval (IBI), age at first birth, and dam survival age; 2) the relationship between maternal age and reproductive output variables; and 3) relationship between the reproductive output variables and survival. We used stepwise regression procedures to describe the amount of variation in lifetime reproductive output among dams, and found that mean litter size accounted for 18% of the variance in total production, survival age accounted for 10.6%, age at first birth accounted for 8.8%, and mean IBI accounted for 5%. For total (nonzero) weaned production, survival age accounted for 7.6% of variance, age at first birth accounted for 7.2%, mean IBI accounted for 2%, and mean litter size accounted for 1.6%. We identified significant effects (P<0.05) of maternal age on litter size and IBI length, but no effect of dam age on weaned litter size. Cox proportional hazards regression analyses revealed significant effects (P<0.01) of number of litters, age at first birth, and site on dam survivorship. Dams that produced more litters showed higher survivorship. Age at first birth showed a positive relationship with dam survivorship, i.e., dams that delayed first reproduction had higher survival. Our findings about reproductive variation in marmosets may have practical applications for the management of marmoset breeding colonies.     

Relations among birth condition, maternal condition, and postnatal growth in captive common marmoset monkeys (Callithrix jacchus)

The present study characterizes the relations among maternal condition, litter size, birth condition, and growth in body weight for a population of common marmosets. The subjects of the study were marmosets born into a single colony between 1994 and 2001. Three sets of analyses were conducted to answer the following questions: 1) Is there a relationship between litter size, maternal condition, and birth condition? In the study population, maternal body weight, maternal age, litter size, and birth condition were related in a complex fashion. Birth weight and prenatal long‐bone growth, as reflected in knee–heel length, were both related to maternal age, with older mothers supporting higher prenatal growth. Age and maternal condition appeared to interact as determinants of long‐bone growth, as the combination of older and larger mothers resulted in significantly longer knee–heel lengths in their offspring. 2) Is there a relationship between birth condition or maternal condition and subsequent growth or final adult size? The early growth rate in this population was similar to early growth rates reported for three different marmoset colonies, suggesting that early growth may be relatively inflexible in this species. However, within this population, the variation that did occur in early growth rate was related to birth weight and maternal weight. Later growth and adult weight were related to birth weight and litter size: small twin infants displayed slower later growth rates and were smaller as adults than twins that began life at a higher birth weight, while the birth weight of triplets was not related to adult size. In these marmosets, small infants that were the result of increased litter size differed from small infants whose small birth size resulted from other factors. This reinforces the proposal that the causes of low birth weight will be relevant to the development of the marmoset as a model of prenatal environmental effects. Am. J. Primatol. 62:83–94, 2004. © 2004 Wiley‐Liss, Inc.     

Effects of litter size on maternal care, body weight and infant development in golden hamsters (Mesocricetus auratus)

The effects of litter size on maternal care, body weight and infant development of golden hamsters were investigated from a longitudinal perspective. Litters were culled to 1,3,6 and 9 pups, and the behavior and body weight of mothers and pups were recorded from the 5th to the 25th postpartum day. We noted that the time spent by mothers in bodily interactions with pups decreased as a function of litter size; maternal pup retrievals reached their maximum around the 13-15th day, which coincided with the increased locomotor activity of pups at this time; the total number of pup retrievals by the mother increased as a function of the litter size, but mothers of larger litters were more 'efficient' (i.e. they failed less frequently in exhibiting a full sequence of retrievals) and exhibited a low litter-size proportional mean number of retrievals. All mothers gradually lost body mass throughout lactation, and decrease in body weight was significantly related to litter size. The mean body weight gain (%) by pups decreased as a function of litter size, but we also noted that single and larger litter pups exhibited a decreased body mass (grams) by the 15th day, suggesting that infant development may be impaired at both extremes of experimental conditions. We concluded that the behavior of mothers and pups was affected by the litter size, and it appeared that the litter had an optimal size-not so large as to overlap the mother's physical capacity, and not so small as to fail to compensate for the parental investment.     

Mammalian reproductive strategies: A generalized relation of litter size to body size

Summary A generalized relationship of litter size to mammalian body size was predicted by a graph model. The model was used to generate hypotheses explaining specific features of variation in gestation time, relative litter weight, birth weight, and reproductive capacity. The predictions were tested by means of data from the literature.Mammals were assumed to maximize neonatal survival of offspring to the limits allowed by litter weight per female body weight. Gestation time correlated negatively with the foetal growth rate of relative litter weight. Gestation time did not correlate with the foetal growth rate of individual offspring.Relative litter weight correlated negatively with adult body weight. This relationship was explained by the higher assimilation rate per unit weight relative to metabolic rate in small mammals.Birth weight correlated positively with body weight. However, small mammals produce larger offspring than predicted by the linear relationship of birth weight to body weight in large mammals. There is obviously a minimum birth weight which cannot be decreased without special arrangements for parental care.The prediction of the relationship of litter size to body size was derived from the relations of relative litter weight and birth weight to body weight. In small mammals (less than 1 kg) litter the correlation was negative. When litter size was compared with body length, the correlation was positive in small mammals (less than 30 cm) and negative in large mammals. In both sets of data there was a negative overall correlation between litter size and body size.Reproductive capacity, defined as the number of offspring per season, correlated negatively with life-span.     

Cotton-top tamarins (Saguinus (o.) oedipus) in a semi-naturalistic captive colony

To test the prediction that the breeding success of captive cotton-top tamarins (Saguinus (o.) oedipus) could be improved by maintaining them in groups whose size and age-sex composition resembled those of wild groups, data were collated from 6.5 years of records from a breeding colony that otherwise had housing and husbandry procedures similar to those of other successful colonies. Group size and composition in the colony closely resembled those of wild groups, and infant survival was the highest yet reported for the species, with 69% of the 124 infants born reared by their parents to adulthood, and a mean surviving litter size of 1.5 infants. Abortion, stillbirth, and parental neglect of infants were rare. Parity had several effects on reproduction: mean litter size decreased, but percentage infant survival increased; interbirth intervals decreased in length; and seasonality in reproduction was more pronounced for the first four litters born to breeding females than for their subsequent litters, with a birth peak in the spring. Although a spacious and complex physical environment, retention of offspring in their natal families until experience of several sets of infant siblings had been obtained, and non-invasive husbandry and research techniques may all have contributed to the colony's success, it seems possible that the improvement over other colonies is due to the resemblance of group composition to those of wild tamarins.     

Genetic parameters for early piglet weight,litter traits and number of functional teats in organic pigs

Knowledge remains limited on genetic variation and genetic correlations for traits in sows and piglets that are reared in an organic or outdoor setting. Here, we estimated genetic variance components for individual piglet weight, litter weight, litter size traits, and number of functional teats in a pig population raised under outdoor organic conditions. Data were collected from the largest organic multiplier farm in Denmark. Individual piglet weight was recorded at birth and on day 10. Number of live and dead piglets were recorded at birth, day 4, and day 11. Mean and total litter weight were calculated based on the individual weight of living piglets at birth and on day 10. The estimated heritability was highest for the number of functional teats (0.49), mean weight of a litter at birth (0.33) and on day 10 (0.25). In contrast, heritability was lowest for litter size traits (0.04–0.08) and piglet weight (0.06–0.07). Maternal heritability was much higher for individual piglet weight than direct heritability. The results showed that selection for higher mean weight results in smaller litters. Also, selection for individual birth weight of piglets results in heavier piglets at 10 days. In conclusion, this study confirmed that there is genetic variation in individual piglet weight, litter traits, and number of functional teats in organically and outdoor-reared pigs.     

Reproductive factors affecting survivorship in captive Callitrichidae

Efforts to breed Callitrichidae in captivity have resulted in high fertility accompanied by high infant mortality. This paper investigates the relationship between reproductive characteristics and survivorship in the Oak Ridge and Associated Universities (ORAU) callitrichid colony. Records of 2,834 individuals were analyzed using Cox Proportional Hazards regression to investigate factors affecting infant survivorship. Species and birth cohort were found to have a significant (P less than 0.05) effect on survivorship. Litter size also was an important factor in determining survivorship. Individuals born into singlet and twin litters had significantly (P less than 0.001) higher survivorship than triplets. Factors which affect survivorship perinatally (0-1 months of age), prior to breeding age and subsequent to the first month of life were then investigated. Litter size was a significant (P less than 0.05) factor in determining survivorship perinatally, with twins having significantly higher survivorship than both singlets and triplets. After the first month of life, litter size no longer showed a significant effect on survivorship. Records of 145 dams were analyzed using the same procedures to investigate reproductive characteristics associated with survivorship. Age at first litter showed a significant (P less than 0.01) positive relationship with dam survivorship. These results suggest various factors affect survivorship at specific temporal points during development, and also suggest selection for survivorship perinatally to be strongly associated with litter size, possibly through sibling competition and maternal effects.     

Effect of empty uterine space on birth intervals and fetal and placental development in pigs

A substantial loss of embryos occurs between Days 30 and 40 of pregnancy in the pig under crowded intrauterine conditions, but it is not clear whether this loss affects the growth of adjacent conceptuses. Birth intervals are known to increase with decreasing litter size, but the factors responsible are unknown. Two possibilities are that increased birth weight associated with reduced litter size and the empty uterine space and resulting constricted uterine regions that occur in pigs with small litters may impair piglet delivery. To address these, pregnant gilts were laparotomized on Day 35 of pregnancy and one or two fetuses were manually crushed through the uterine wall on the ovarian or cervical end of each uterine horn to create an empty uterine space behind or in front of the litter of piglets, respectively, in relation to the route of delivery from the uterus. A subset of gilts was slaughtered at 105 days of gestation to confirm that the empty uterine spaces were successfully created and to determine their effects on placental and fetal weights of adjacent conceptuses. At slaughter, the lengths of all externally visible empty constricted regions of the uterus were measured. The uterine horns were opened and the lengths of each placenta were measured from the umbilicus toward the ovary and toward the cervix to assess whether placentas developed symmetrically, and then each fetus and placenta was weighed. Fetal crushing successfully created constricted empty uterine regions on the ovarian and cervical ends of the uterine horns. Ovarian-side placental lengths were greater than cervical-side for conceptuses adjacent to fetuses crushed on the ovarian end of the horn. Cervical-side placental lengths were greater than ovarian-side for conceptuses adjacent to fetuses crushed on the cervical end. Both placental and fetal weights were greater (10% and 6%, respectively, P<0.05) for conceptuses adjacent to crushed fetuses compared to nonadjacent conceptuses. Remaining gilts were farrowed to determine the effect of litter size, average birth weights, and treatment on birth intervals of piglets, which were monitored using 24-h video surveillance. The negative association between number of piglets born alive and average birth interval was confirmed and was not explained by litter size-induced reduction in litter average birth weights. Birth intervals and stillbirth rate did not differ between cervically- and ovarian-treated gilts. These results indicate that conceptus loss on Day 35 of gestation can benefit the growth of adjacent placentas and fetuses, but the benefit is small. Increased average birth weight and the presence of empty uterine space that occurs when litter size is reduced does not fully explain the effect of litter size on birth intervals.     

A description of nesting behaviors,including factors impacting nest site selection,in black‐and‐white ruffed lemurs (Varecia variegata)

Nest site selection is at once fundamental to reproduction and a poorly understood component of many organisms’ reproductive investment. This study investigates the nesting behaviors of black‐and‐white ruffed lemurs, Varecia variegata, a litter‐bearing primate from the southeastern rainforests of Madagascar. Using a combination of behavioral, geospatial, and demographic data, I test the hypotheses that environmental and social cues influence nest site selection and that these decisions ultimately impact maternal reproductive success. Gestating females built multiple large nests throughout their territories. Of these, females used only a fraction of the originally constructed nests, as well as several parking locations as infants aged. Nest construction was best predicted by environmental cues, including the size of the nesting tree and density of feeding trees within a 75 m radius of the nest, whereas nest use depended largely on the size and average distance to feeding trees within that same area. Microhabitat characteristics were unrelated to whether females built or used nests. Although unrelated to nest site selection, social cues, specifically the average distance to conspecifics’ nest and park sites, were related to maternal reproductive success; mothers whose litters were parked in closer proximity to others’ nests experienced higher infant survival than those whose nests were more isolated. This is likely because nesting proximity facilitated communal crèche use by neighboring females. Together, these results suggest a complex pattern of nesting behaviors that involves females strategically building nests in areas with high potential resource abundance, using nests in areas according to their realized productivity, and communally rearing infants within a network of nests distributed throughout the larger communal territory.     

Infant survival and litter size in primigravid and multigravid Galagos

Eighteen years of birth records for three species of Galago at the Duke University Primate Center were examined to determine the effect of gravidity status on neonatal mortality and litter size. Multiparous Galago senegalensis moholi and G crassicaudatus, but not G garnettii, had significantly higher infant survival rates. Gravidity status had no effect on the percentage of multiple births for any of the three species of Galago.     

Hormonal manipulation of offspring number: maternal effort and reproductive costs

We used exogenous gonadotropin hormones to physiologically enlarge litter size in the bank vole (Clethrionomys glareolus). This method allowed the study design to include possible production costs of reproduction and a trade-off between offspring number and body size at birth. Furthermore, progeny rearing and survival and postpartum survival of the females took place in outdoor enclosures to capture salient naturalistic effects that might be present during the fall and early winter. The aim of the study was to assess the effects of the manipulation on the growth and survival of the offspring and on the reproductive effort, survival, and future fecundity of the mothers. Mean offspring body size was smaller in enlarged litters compared to control litters at weaning, but the differences disappeared by the winter. Differences in litter sizes disappeared before weaning age due to higher mortality in enlarged litters. In addition to the effects of the litter size, offspring performance was probably also influenced by the ability of the mother to support the litter. Experimental females had higher reproductive effort at birth, and they also tended to have higher mortality during nursing. Combined effects of high reproductive effort at birth and high investment in nursing the litter entailed costs for the experimental females in terms of decreased probability of producing a second litter and a decreased body mass gain. Thus, enlarged litter size had both survival and fecundity costs for the mothers. Our results suggest that the evolution of litter size and reproductive effort is determined by reproductive costs for the mothers as well as by a trade-off between offspring number and quality.     

Litter size and infant survivorship in wild groups of cotton‐top tamarins (Saguinus oedipus) in Colombia

Cotton‐top tamains (Saguinus oedipus) are a critically endangered primate found only in Colombia. Efforts to conserve this species are centered on developing effective management plans that integrate biological information regarding population dynamics and factors that influence their survival. This study documented infants born to wild cotton‐top tamarin females from 1994–2008 at two distinct field sites in northern Colombia. Our studies have shown that wild cotton‐top tamarins typically give birth to one litter each year and infant survival to 6 months of age was greater in the wild than has been reported in captive colonies. However, similar to reports from captive colonies, litter size of wild cotton‐top tamarins ranges from 1–3 infants, with twin litters most common. Here we report the first occurrence of triplet litters in nearly 20 years of observing wild cotton‐top tamarin groups. Over the first 3 months of life, wild‐born infants exhibited highest mortality during the first week of life, similar to reports from captive colonies. Infant survival in the wild also increases with successive litters as it does in captivity. However, inter‐birth interval, group size, and the number of adult males in the group did not appear to influence infant survival in the wild. The value of such long‐term data from field studies aids in the information that can be used to model future population trends and develop effective conservation plans for this critically endangered primate. Am. J. Primatol. 71:707–711, 2009. © 2009 Wiley‐Liss, Inc.