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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Nutrient composition of plants consumed by black and white ruffed lemurs,Varecia variegata,in the Betampona Natural Reserve,Madagascar

The purpose of this study was to quantify the concentrations of crude protein, fat, ash, neutral detergent fiber, acid detergent fiber, lignin, nonstructural carbohydrates, and gross energy in plant foods consumed by wild black and white ruffed lemurs (Varecia variegata). Calcium, phosphorous, magnesium, potassium, sodium, iron, zinc, copper, manganese, molybdenum, and selenium concentrations were also determined. A total of 122 samples from 33 plant families and more than 60 species were collected and analyzed for their nutritional content. The specific nutrient needs of black and white ruffed lemurs are unknown, but quantifying the nutritional composition of the foods they consume in the wild will help nutritionists and veterinarians formulate more appropriate diets for captive ruffed lemurs. This information will also supply information on how man‐induced habitat changes affect the nutritional composition of foods consumed by free‐ranging lemurs. Zoo Biol 29:375–396, 2010. © 2009 Wiley‐Liss, Inc.     

How Many Red Ruffed Lemurs Are Left?

I surveyed the Anaovandrano River Watershed to assess whether large tracts of primary lowland rain forest still occur there and to what extent red ruffed lemurs (Varecia variegata rubra) populate the interior of the Masoala Peninsula. These data permit an informed estimate of the remaining population size for this subspecies. I located large tracts of primary lowland rain forest in the interior, but fragmentation has begun. Red ruffed lemurs appear to be less dense in the interior than they are in remaining lowland coastal rain forest. I estimate the remaining population size to be between 29,682 and 51,115 individuals. Breeding population size is substantially smaller, probably <14,841 individuals.     

Management imperatives forVarecia in captivity

A review of the captive history and status ofVarecia is presented followed by specific management recommendations for bothVarecia v. variegata andVarecia v. rubra. The total living captive population for the nominate form numbers 398 animals while that for the red and black form numbers 148 individuals as of 31 December 1986.Varecia v. variegata is reported to be a rapidly growing population originating from a founder population (wildborn animals which have produced offspring) of 21 animals. Management direction for this subspecies includes equalization of founder representation and controlled reproduction.Varecia v. rubra is reported to be more highly inbred with 79.35% of the captive population originating from 3 of 8 founders. The management imperatives for this subspecies include: 1) acquisition of a small number of wildborn red ruffed lemurs to be infused into the captive population over an extended period of time; 2) increase population; 3) equalize founder representation; 4) locate space. Encouragement ofin situ research and conservation activities is strongly advocated. Formerly: International Ruffed Lemur Studbook Keeper San Diego Zoo Box 551, San Diego, California 92112     

Seasonal differences in hair growth rates of captive aye-aye,red ruffed,and black-and-white ruffed lemurs

Hair can be an important source of biological information, providing a record of such things as pollutant exposure, hormonal levels, and stable isotope ratios. Hair as a biological sample is easily accessible, easily stored, and resists degradation. Analysis of hair is particularly useful when studying rare and endangered species, such as lemurs, since it can be sampled noninvasively. However, to better interpret the results of stable isotope or other analyses, it is important to understand hair growth rates. We measured hair growth rates in captive aye-ayes (Daubentonia madagascariensis), red ruffed lemurs (Varecia rubra), and black-and-white ruffed lemurs (Varecia variegata), both in winter (December 23, 2013, to January 13, 2014) and summer (July 10–31, 2013) at the Duke Lemur Center. Hair growth per week in all three species of lemurs differed significantly between the boreal summer and boreal winter. The aye-aye, black-and-white ruffed lemur, red ruffed lemur had a mean weekly hair growth of 0.195, 0.209, and 0.232 cm, respectively, in the summer. While the aye-aye, black-and-white ruffed lemur, and red ruffed lemur had a mean weekly hair growth of 0.239, 0.464, and 0.479 cm, respectively, in winter. We found no effect of age on hair growth rates, neither in the boreal summer, nor in the boreal winter for black-and-white ruffed lemurs and red ruffed lemurs. A pregnant black-and-white ruffed female displayed negligible hair growth during the northern winter, suggesting that pregnancy may affect the partitioning of resources away from such things as hair growth.     

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.     

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.     

Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores

For captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber-limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubra and V. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social-group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur's own baseline, an effect that became stronger as the study progressed. In the final study days, Ruminococcaceae UCG-008 and Akkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce-provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.     

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.     

Preface: Biology of skates

Synopsis Skates have become a concern in recent years due to the preponderance of these elasmobranchs that are caught as bycatch or as a directed fishery. This has raised concern because skates have life history characteristics that may make them vulnerable to over-exploitation. It was due to this increasing awareness and concern about these batoids that prompted us to organize an international symposium on the “Biology of Skates”. The aims and goals of the symposium were to bring together an international group of researchers to meet, discuss, perhaps develop collaborations, and present their most recent findings. The symposium was held over two days, on 13–14 July, 2006, in conjunction with the 22nd annual meeting of the American Elasmobranch Society in New Orleans, LA. A total of 31 authors from four countries contributed 16 papers that appear in this special issue. The papers are broadly arranged into four separate categories: systematics and biogeography, diet and feeding ecology, reproductive biology, and age and growth. To the best of our knowledge this is the first dedicated book on the biology of skates. We hope that readers will find this issue of interest and that it helps encourage and stimulate future research into these fascinating fishes.     

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.