Body weights of ruffed lemurs (Varecia variegata) in European zoos with reference to the problem of obesity

Qualitative observations in several European zoos revealed a high proportion of obese individuals in different species of lemurs. This phenomenon was examined in both subspecies of the ruffed lemur (Varecia variegata variegata and Varecia variegata rubra). Data on body weight were obtained from 43 animals in 13 European zoos and were compared with body weights of wild ruffed lemurs. The captive individuals’ mean weight was significantly higher than either of two different samples of wild V. variegata variegata. Using a weight‐based definition of obesity, 46.5% of the individuals in our sample were obese. Neither significant differences in body weight between the two subspecies nor between sexes could be found. Body weight did not correlate with age. The findings are discussed with reference to the feeding ecology of ruffed lemurs and their nutrition in captivity and to implications for captive breeding programs for this species. Zoo Biol 20:261–269, 2001. © 2001 Wiley‐Liss, Inc.     

Induction of a fertile mating in a red ruffed lemur (Varecia variegata rubra) using pregnant mare serum gonadotropin

Pregnant mare serum gonadotropin (PMSG) was administered to an adult female red ruffed lemur (Varecia variegata rubra) as part of a medical evaluation to determine the cause of reproductive failure. Successful fertilization, pregnancy, and parturition occurred following PMSG treatment. This report documents an approach to evaluating reproductive failure in an endangered primate species and illustrates the value of collecting objective data on all individuals in a colony for retrospective and comparative analysis. Data from basic and applied research on a variety of species were synthesized to establish a logical protocol for fertility evaluation of an individual. The use of PMSG to induce estrus, ovulation, or fertilization has not been documented for an endangered primate species.     

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.     

Laterality in semi‐free‐ranging black and white ruffed lemurs (Varecia variegata variegata): head‐tilt correlates with hand use during feeding

Previous studies in human and chimpanzee infants have identified a predictive relationship between early rightward head orientation and later right hand use. Data from lemurs suggest a leftward bias in hand preference, but there are no data on head positioning. The purpose of this study was to examine the relationship between head and hand preferences in the black and white ruffed lemur (Varecia variegata variegata). Ruffed lemurs rotate the head vertically during chewing in a behavior called head‐tilting. Frequency of head‐tilting and bouts of unimanual hand use were measured during normal feeding in a semi‐free‐ranging population of lemurs. Subjects were provisioned at feeding platforms twice daily with fresh fruits, vegetables, and other food items. Sampling was spontaneous and all observations were videotaped. No group‐level bias was found for head‐tilting, but a left hand bias emerged for hand use. A positive relationship was found between direction of head‐tilting preference and direction of hand use preference such that left head‐tilts increased as left hand use increased. Furthermore, left head‐tilts increased as the degree of hand preference lateralization increased. When the hand used to bring food to the mouth just before head‐tilting was examined, there was a strong bias for the left hand to precede left head‐tilts. For right head‐tilts, however, lemurs were equally likely to use either hand before head‐tilting. Overall a strong relationship was found between the left hand and left head‐tilting in black and white ruffed lemurs, suggesting a common link between these behaviors. However, the direction of bias was different from that seen in human and chimpanzee studies. Additional studies on patterns of laterality would be informative for understanding how laterality has changed across the primate order and the adaptive significance of laterality in primates. Am. J. Primatol. 71:1032–1040, 2009. © 2009 Wiley‐Liss, Inc.     

Management and husbandry of ruffed lemurs,Varecia variegata,at the San Diego Zoo. III. Medical considerations and population management

Medical aspects of maintaining the ruffed lemurs, Varecia variegata, at the San Diego Zoo and recommendations for population management of the species are presented. Common clinical problems include diarrhea, hair balls, chapped feet in young animals, and canine-tooth abscesses. Congenital abnormalities in animals at San Diego involve scoliosis, incomplete skull formation, internal organ anomalies, and neuromuscular disease, all of which may be related to the small number of founders. Population-management recommendations vary in complexity with the subspecies. Of primary importance for Varecia v. variegata is equalization of founder contributions and controlled breeding. Critical issues for Varecia v. rubra include acquisition of wild-born stock, equalization of founder representation, increased population, and the location of captive habitat. The creation of four or five major breeding centers for Varecia is proposed; the centers would be designed to house wild-born and underrepresented founder lines that could be genetically manipulated and rapidly expanded over a short time period. The creation of a self-sustaining population of ruffed lemurs in captivity depends on international cooperation and the development of a ruffed lemur master plan.     

Sex ratio affects sex-specific innovation and learning in captive ruffed lemurs (Varecia variegata and Varecia rubra)

Recent years have witnessed extensive research into problem solving and innovation in primates, yet lemurs have not been subjected to the same level of attention as apes and monkeys, and the social context in which novel behavior appears has rarely been considered. We gave novel foraging puzzlebox devices to seven groups of ruffed lemurs (Varecia variegata and Varecia rubra) to examine the factors affecting rates of innovation and social learning. We found, across a range of group sex ratios, that animals of the less-represented sex were more likely to contact and solve the puzzlebox sooner than those of the more-represented sex. We established that while some individuals were able to solve the puzzleboxes there was no evidence of social learning. Our findings are consistent with previously reported male deference as a sexual strategy, but we conclude that the need for male deference diminishes when, within a group, males are rare.     

The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae)

A stable social group of 7 semifree-ranging black-and-white ruffed lemurs (Varecia variegata variegata) was studied for 4 months to catalog the behavioral repertoire of this species. Observations focussed on particular aspects of behavior were conducted before and after this 4-month period to supplement information gathered. Behavior in 11 major categories is detailed: postures, terrestrial locomotion, arboreal locomotion, feeding behavior, vocalizations, scent-marking, affinitive social behavior, agonistic social behavior, play behavior, sexual behavior, and parental behavior. Ruffed lemurs frequently used body positions and locomotor patterns unusual among lemurids, including bipedal hanging and long-descent leaps. These behaviors reinforce dental evidence that Varecia are among the most frugivorous of the Malagasy lemurs. Low intragroup cohesion, infrequent social interaction, and antiphonal use of several long-distance vocalizations suggest that ruffed lemurs naturally exhibit fission-fusion sociality. Social structure based on interindividual familiarity probably extends across foraging parties for several of the diurnally active lemurs; however, thus far only Varecia seems likely to exhibit fission-fusion sociality analogous to that seen in spider monkeys and chimpanzees.     

Functional Analysis of Aggression in a Black-and-White Ruffed Lemur (Varecia variegata variegata)

A functional analysis was conducted to assess the antecedent and reinforcing conditions underlying aggressive behavior in a female lemur in captivity. Results showed that her aggression was primarily the result of human attention. A replacement behavior-training program was introduced, and the lemur's aggression was successfully eliminated. These results demonstrate the utility of using functional assessment and analyses in zoos with captive wild nonhuman animals.     

Hematology and serum chemistry values of juvenile and adult ruffed lemurs (Varecia variegata)

Hematologic and serum chemistry values are presented for adult and juvenile red ruffed lemurs (Varecia variegata rubra) and black and white ruffed lemurs (Varecia variegata variegata) maintained in a zoological collection. Hematologic and serum chemical values are compared between age groups and subspecies and with other primate species. Elevated hematocrit, total protein, and serum albumin values were noted. Significant differences in cholesterol, total protein, and serum albumin values between the two age groups are discussed.     

Patch size and isolation influence genetic patterns in black-and-white ruffed lemur (Varecia variegata) populations

Land use in Madagascar has resulted in extensive deforestation and forest fragmentation. Endemic species, such as the black-and-white ruffed lemur (Varecia variegata), may be vulnerable to habitat fragmentation due to patchy geographic distributions and sensitivities to forest disturbance. We tested for genetic differentiation among black-and-white ruffed lemur groups in two sites in a large forest patch and three sites in smaller patches. We also investigated the relationship between the genetic diversity of populations and patch configuration (size and isolation), as well as the presence or absence of past genetic bottlenecks. We collected blood (n = 22 individuals) or fecal (n = 33) samples from lemurs and genotyped the extracted DNA for 16 polymorphic microsatellites. Bayesian cluster analysis and F_ST assigned individuals to three populations: Ranomafana (two sites in continuous forest), Kianjavato (two fragments separated by 60 m of non-forest), and Vatovavy (a single fragment, more isolated in time and space). Vatovavy showed significantly lower allelic richness than Ranomafana. Kianjavato also appeared to have lower allelic richness than Ranomafana, though the difference was not significant. Vatovavy was also the only population with a genetic bottleneck indicated under more than one mutation model and a significant F_IS value, showing excess heterozygosity. These results indicate that a small geographic separation may not be sufficient for genetic differentiation of black-and-white ruffed lemur populations and that patch size may influence the rapidity with which genetic diversity is lost following patch isolation.     

Use of desferoxamine and S-adenosylmethionine to treat hemochromatosis in a red ruffed lemur (Varecia variegata ruber)

Hemochromatosis was diagnosed in a 14-year-old, male, red ruffed lemur (Varecia variegata ruber) on the basis of abnormal results of serum biochemical analysis, including high serum ferritin and transferrin saturation values, and of liver biopsy. Therapy included chelation, using desferoxamine to remove excess iron and S-adenosylmethionine to improve liver function, and monthly peripheral blood removal by phlebotomy to reduce total body iron content. Response to treatment was assessed by changes in the lemur's attitude and appetite, as well as variations in serum biochemical and iron panel values. Initial improvement was associated with the onset of therapy. After 56 days of treatment, results of serum biochemical analysis indicated a decrease in iron panel values. Treatment was temporarily discontinued from days 56 to 65, and the lemur's condition worsened, so therapy was re-instituted. However, the lemur died of hepatocellular carcinoma on day 110 of treatment.     

Diet and feeding behaviour of the black-and-white ruffed lemur (Varecia variegata variegata) in the Betampona Reserve, eastern Madagascar

The feeding behaviour and diet of the black-and-white ruffed lemur (Varecia variegata variegata) was investigated in the Betampona Reserve, eastern Madagascar. The highly frugivorous diet of this subspecies was confirmed - feeding on fruits accounting for 92.0% of feeding records. Most feeding at Betampona was observed at 10-25 m above the forest floor amongst flexible, small (0.5-5.0 cm diameter) and oblique/horizontal (0-45 degrees ) supports. The Varecia spent on average 21.7% (+/- 1.5) of their daily activity budget feeding and employ a variety of postures that enable them to harvest fruits in the rain forest canopy. The suspensory postures were the most important in allowing Varecia to compete with other smaller-bodied frugivores.     

Diurnal distribution of loud calls in sympatric wild indris (Indri indri) and ruffed lemurs (Varecia variegata): implications for call functions

We carried out a short study on the diurnal call distribution of two sympatric lemurs in the Réserve Naturelle Intégrale Zahamena (eastern Madagascar). Whereas indris (Indri) song bouts were clearly concentrated in the early morning hours, the roar/shriek choruses of ruffed lemurs (Varecia) exhibited a much more even distribution throughout the day. These differences in distribution pattern support earlier claims that indri song bouts are more likely to serve territorial functions, whereas ruffed lemur loud calls may serve both spacing and/or alarm call functions.     

Reproductive activity of ruffed lemurs (Varecia variegata variegata) in a Madagascar rain forest

Mating activity was observed during four breeding seasons in two groups of black and white ruffed lemurs (Varecia variegata variegata) living in lowland rain forest on Nosy Mangabe island, Madagascar. The onset of the May-July breeding season was signalled by behavioral changes in adult males. Males made forays outside their usual home ranges, were more aggressive to other males, and performed appetitive and other sex-specific behaviors more frequently. Females showed receptive and proceptive behaviors during a 1-2 day behavioral estrus. Ruffed lemurs mated monogamously, polyandrously, and polygynously. These observations do not support previous assertions that they live only in monogamous families. Limited evidence suggests females exercised mate choice and may have preferred familiar males. © 1993 Wiley-Liss, Inc.     

Some observations of two kinds of lemuridae (Varecia variegata variegata andLemur fulvus albifrons) in the reserve of Nosy Mangabe

A total of nine groups of ruffed lemurs (Varecia variegata variegata), as well as one solitary individual, were observed on Nosy Mangabe, an island located off the eastern coast of Madagascar, for a total 536 min between November 30 and December 8, 1983. The average group size was 2.8 animals (N=5), and the population density was 175 animals/km², as estimated from direct observation and location of vocalization. During the same period, nine groups of brown lemurs (Lemur fulvus albifrons) and one solitary individual were observed for a total 320 min. One group of brown lemurs was composed of eight animals (two adult males and females, one male juvenile, two infants, and one individual of undetermined age and sex). Feeding competition occurred between the two species, with whichVarecia variegata variegata dominating.     

Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata)

Although many studies have examined social learning capabilities in apes and monkeys, experiments involving prosimians remain largely absent. We investigated the potential for social learning in black-and-white ruffed lemurs using a two-action foraging task. Eight individuals were divided into two experimental groups and exposed to conspecifics using one of two techniques to access food. Subjects were then given access to the apparatus and their retrieval techniques were recorded and compared. All subjects made their first retrieval using the technique they observed being demonstrated, and there were significant differences between the two groups in their overall response patterns. These results suggest that prosimians are capable of social learning and that additional long-term field studies may reveal the presence of behavioural traditions similar to those found in other primates.     

Epidemiologic assessment of reproductive success and infant mortality in ruffed lemurs (Varecia variegata)

Retrospective epidemiologic evaluation of 27 years of colony data (1966–1993) from a large breeding center for ruffed lemurs (Varecia variegata) was used to quantitatively assess the risk imposed by different management variables on reproductive success (littering) and infant viability (litter death). Logistic regression analysis was used, both with and without a term to account for extra-binomial variation in the data (random effects) associated with repeated assessments of individual lemur dams during the study period. Population-based littering rates are defined and shown not to fluctuate substantially over time, although the proportion of females given the opportunity to breed was drastically reduced in 1986 due to changes in the species management strategy and limited breeding center space resources. No management-related factors were found to be associated with littering success. However, young age of dam (odds ratio = 4.3, P = 0.016) and housing in natural habitat enclosures (odds ratio = 6.5, P = 0.003) significantly predicted complete litter mortality by 48 hr post-partum. Varecia females >15 years of age (8 dams, 42 observation-years) produced 18 litters and 37 infants, 31 of which survived at least 48 hr. Use of established epidemiologic methods to analyze data from existing colony records should be used to help direct the management of this endangered species toward maximally efficient goals, especially in light of current conservation resource limitations. © 1994 Wiley-Liss, Inc.     

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 re-stocking of captive-bred ruffed lemurs (Varecia variegata variegata) into the Betampona Reserve, Madagascar: methodology and recommendations

Since November 1997 the Madagascar Fauna Group has released 13 captive-bred black and white ruffed lemurs (Varecia variegata variegata) into the Betampona Reserve in eastern Madagascar. The release programme has three major aims: (1) to assess the ability of captive-bred V. v. variegata to adapt to life in their natural habitat; (2) to investigate the contribution that such a release programme can make to reinforcing the existing small wild population of V. v. variegata in Betampona; and (3) to contribute to the long-term protection and conservation of the reserve. Criteria for the selection of release candidates, veterinary screening and pre-release experience in naturalistic environments are described and discussed. Methods for post-release monitoring of health and behaviour are covered in detail. The importance of considering the social dynamics of the species involved is emphasised. The survival of five of the releasees, plus successful reproduction and integration with the wild population have led to the conclusion that the release was a success.     

Species‐level view of population structure and gene flow for a critically endangered primate (Varecia variegata)

Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remaining V. variegata range. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNA sequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of the Mangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNA haplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high average F_ST (0.247) and Φ_ST (0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.