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.     

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.     

Encouraging natural feeding behavior in captive-bred black and white ruffed lemurs (Varecia variegata variegata)

Captive breeding of endangered species is commonly proposed as a means of conserving biodiversity. The suggestion is that captive populations can be built up to provide individuals to reinforce or re-establish wild populations. However, there is evidence to suggest that captive-bred animals lack the skills necessary for survival in their natural habitat. This research was designed to assess whether a group of captive-bred Varecia variegata variegata exhibit such behavioral deficiencies in relation to feeding behavior compared to two wild groups. A further aim was to determine which of four methods of food presentation and two captive environments were most effective in encouraging the exhibition of natural feeding behavior. An identical focal animal, instantaneous time-sampling technique was used to collect data from the wild groups in the Betampona Reserve, Madagascar, and the captive group at Chester, UK. Results from Betampona confirm the highly frugivorous and arboreal nature of V. v. variegata. Under all captive conditions, except the rooftop feed in the cage environment, the captive V. v. variegata spent significantly less time feeding than their wild conspecifics. Suspensory feeding postures are an important adaptation enabling wild V. v. variegata to harvest fruit in the small-branch setting. Similar frequencies of use of such postures to those observed at Betampona were most effectively encouraged among captive V. v. variegata in the cage environment by the rooftop food presentation method and on a naturalistic island exhibit by the suspended method of food presentation. Differences in feeding behavior between the wild and captive V. v.variegata can be explained in terms of structural differences between their environments. As naturalistic captive environments allow lemurs to experience the challenges associated with feeding in the wild, it is strongly recommended that zoos endeavor to provide them with such conditions. Zoo Biol 17:379–392, 1998. © 1998 Wiley-Liss, Inc.     

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.     

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.     

Subspecific divergence in a loud call of the ruffed lemur (Varecia variegata)

A loud call of the ruffed lemur (Varecia variegata) was analyzed for subspecific and gender differences according to four variables: pulse rate, median pulse duration, median high frequency, and median low frequency. These vocalizations of black-and-white and red ruffed lemurs and one hybrid ruffed lemur were recorded at the Duke University Primate Center (Durham, NC). Significant differences were found between subspecies but not between the sexes. Quantitative differences in this loud call of ruffed lemur subspecies indicate that these prosimians exhibit subspeciation trends similar to anthropoid primates for which comparable data exist. Preliminary data are presented that support the hypothesis that the vocalization functions as a terrestrial predator alarm call.     

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.     

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.     

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.     

Preliminary biomedical evaluation of wild ruffed lemurs (Varecia variegata and V. rubra)

Complete medical examinations were performed on 11 wild ruffed lemurs (Varecia variegata and V. rubra) from three sites in Madagascar. Each animal received a complete physical examination, several physiological parameters were analyzed (complete blood count, serum biochemical profile, and fecal bacterial culture), and the animals were examined for endo-, ecto-, and hemoparasites. Additional tests were performed as samples were available, including fat-soluble vitamin analysis, trace mineral analysis, toxoplasmosis serology, and viral serology. We found that the ruffed lemurs were in good health, harbored a low endoparasite load, and frequently had external parasites (e.g., ticks (Haemophysalis lemuris)). Statistically significant differences between captive and wild lemurs were found for the following serum biochemical and blood count parameters: alanine aminotransferase (ALT), total protein (TP), albumin, blood urea nitrogen, cholesterol, glucose, amylase, band neutrophil count, and eosinophil count. Low blood urea nitrogen (BUN) and serum cholesterol values in wild lemurs (compared to those of North American captive zoo ruffed lemurs) may suggest differences between diets in the wild and captivity.     

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.     

Social organization of free-ranging ruffed lemurs,Varecia variegata variegata: mother-adult daughter relationship

The relationship between a mother and an adult daughter is examined in a group of free-ranging ruffed lemurs (Varecia variegata) at the Duke University Primate Center (DUPC). Although the two females were affiliative during the birth season, interactions during the mating season were predominantly agonistic. The maturing daughter was dominant to the mother, as has been observed in many caged social groups at the DUPC. Although both mother and daughter produced offspring in the same group, the daughter subsequently aggressively evicted the mother from the enclosure. It was not possible to maintain more than one long-term resident breeding female in the same social group. This pattern contrasts with observations of affiliation among breeding females in the wild. © 1992 Wiley-Liss, Inc.     

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.     

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.     

Environmental enrichment to address behavioral differences between wild and captive black-and-white ruffed lemurs (Varecia variegata)

I compared the behaviors of wild Varecia variegata living in a Malagasy rain forest with those of caged groups living in zoos in the United Kingdom in order to design environmental enrichment to encourage more natural behaviors. Comparisons were made between wild and captive animals in terms of activity budgets (instantaneously sampled at 1-min intervals) and social and solitary behaviors, which were continuously recorded for focal individuals. I followed the same sampling protocol during behavioral enrichment experiments, with additional monitoring of the amount and type of food consumed, and with more detailed observations of feeding behavior. No significant differences were found in resting or moving between wild and captive V. variegata. However, captive V. variegata spent more time on self-grooming and social behaviors, and less time feeding than wild V. variegata. There was also a lack of manual manipulation of food items. Behavioral enrichment experiments were carried out in which whole rather than chopped fruit was provided and presented in a more naturalistic manner. With this method of dietary presentation, manual manipulation of dietary items increased. Time spent feeding also increased significantly. Captive conservation breeding programs should not be wholly concerned with maintaining a diverse gene pool-they should also be concerned with conserving species-typical behaviors, especially if they are to produce behaviorally intact captive animals that can be reintroduced to the wild with minimal training, financial resources, and loss of individuals.