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.     

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     

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.     

Wichtige veterinärmedizinische Aspekte der Lemurenhaltung im Tierpark Berlin

The author describes diseases in lemurs, which occurred in the last ten years at Tierpark Berlin. After a short introduction of the importance of lemur husbandry and breeding in zoological gardens a review of the following diseases is given: periarticular hyperostosis in black lemurs, acute alkaloid intoxication in black lemurs, amoebiasis in ruffed lemurs and obesity in mongoose lemurs. Clinical symptoms, diagnosis, therapy and post mortem findings are explained in detail.     

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.     

Detection of virus-like particles in the liver of black and white ruffed lemurs with hepatitis

Two young black and white ruffed lemurs (Varecia variegata variegata) died at the San Diego Zoo (San Diego, California, USA) with extensive liver lesions suggestive of acute viral infection. Immunoassays performed to detect hepatitis B virus (HBV) markers were negative. Polymerase chain reaction (PCR) primers overlapping the HBV core gene produced an amplicon of approximately 411 base pairs (bp) from serum DNA of a HBV-positive western lowland gorilla (Gorilla gorilla gorilla) but not from serum DNA of either lemur. Cesium chloride gradient fractions of liver homogenates from both lemurs contained a peak protein fraction with a density of 1.18 g/cm3. Electron microscopic analysis of fraction contents, concentrated by ultracentrifulgation, revealed numerous pleomorphic, spherical particles varying in diameter from 16-25 nm. In one of the lemurs, this peak fraction also contained a double-shelled virus-like particle 47-50 nm in diameter. The size, morphology, and density of these particles suggest they are members of the Hepadnaviridae, a group of hepatotropic DNA-genome viruses for which HBV is the prototype.     

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.     

Pathogenesis of hemosiderosis in lemurs: Role of dietary iron,tannin, and ascorbic acid

Clinical disease associated with excess iron deposition (hemosiderosis) in the duodenum, liver, and spleen occurs in captive lemurs. In this report we review the occurrence of hemosiderosis and related disease in the Zoological Society of San Diego lemur collection; we then define and describe potential pathogenic factors with the goal of establishing rational husbandry methods to limit or prevent the disease. At the San Diego Zoo, all 49 lemurs necropsied since 1968 were hemosiderotic, the severity increasing with increasing age; liver and kidney disease were common. Our review of iron metabolism, current knowledge on the pathogenesis of hemosiderosis in humans, and the diets of captive and wild lemurs reveals several key dietary substances that may contribute to lemur hemosiderosis: iron, tannins, and ascorbic acid. In captivity, excess dietary iron (commercial monkey chow) and high levels of ascorbic acid (citrus fruits) lead to enhanced iron uptake and increased toxicity of stored iron due to free radical formation. In the wild, lemurs have an unusual preference for leaves, fruits, and bark high in tannin, a polyphenolic secondary plant compound that rapidly chelates iron, protein, and minerals in the gastrointestinal (GI) tract, preventing their absorption. These findings suggest that hemosiderosis in captive lemurs results from a diet high in iron, high in ascorbic acid, and lacking in tannin. Immediate correction of captive diets may limit hemosiderosis in lemurs in the future.     

Hemosiderosis in lemurs

In the late 1960s, pathologists at the San Diego Zoo began to notice iron storage in the internal organs of captive lemurs. Hemosiderin was found in liver, spleen, lymph nodes, duodenum, and occasionally other organs. This was most pronounced in Lemur macaco, least pronounced in Lemur catta, with the severity in Lemur variegatus variegatus and Lemur variegatus ruber falling somewhere in between. Since 1968, 20 of 29 necropsied lemurs had hemosiderosis, three with hepatomas, three with cholangiomas, and one with a metastatic pheochromocytoma. In a preliminary attempt to compare their iron absorption, five black-and-white ruffed lemur (Lemur variegatus variegatus) weanlings and five rhesus monkey weanlings were each given ～500 nmol/kg FeCI₃ (27.9 μg iron/kg) containing 5 μCi of ⁵⁹Fe in 0.1 M HCl via a nasogastric tube. Retained ⁵⁹Fe was measured by whole body gamma counting and found to be roughly the same in the two groups, possibly because insufficient quantities of iron were administered and/or excessive iron absorption becomes apparent only in older animals. Our conclusions were the following: (1) Hemosiderosis in lemurs is associated with tissue damage similar to that seen in humans with idiopathic hemochromatosis. (2) Because iron deposits occur both in parenchymal cells and reticuloendothelial cells, hemosiderosis in lemurs is probably not a model for idiopathic hemochromatosis in a pure sense.     

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.     

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.     

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.     

Cryptococcosis in columbiformes at the San Diego Zoo.

Two cases of cryptococcosis in columbiformes exhibited at the San Diego Zoo are described. The organism isolated from the first case had morphological, chemical and temperature growth characteristics of C. neoformans. The culture from case 2 died before it could be examined biochemically or by mouse inoculation.     

Can Black‐and‐White Ruffed Lemurs (Varecia variegata) Solve Object Permanence Tasks?

We examined object permanence in black‐and‐white‐ruffed lemurs (Varecia variegata) at Zoo Atlanta. A series of visible and invisible displacement tasks with suitable controls were presented to five adult subjects. Subjects performed significantly above chance on all regular tasks, except for the double invisible displacements. Subjects failed visible and invisible controls. Failure on the control trials did not appear to be because subjects used the “last box touched” strategy (subjects did not choose the last box touched significantly more than expected by chance). However, a substantial percentage of choices was made to the last box touched by the experimenter. There was no significant difference between this percentage, and the percentage of choices made to the baited box (on both visible and invisible controls), which indicates that subjects were drawn to both boxes which the experimenter visited/touched, and thus failed the controls. Based on the results from the present study, we believe that there is no evidence that black‐and‐white ruffed lemurs understand visible and invisible tasks in the traditional object permanence battery. Am. J. Primatol. 75:376‐386, 2013. © 2013 Wiley Periodicals, Inc.     

Extensive variability in the gut microbiome of a highly‐specialized and critically endangered lemur species across sites

Deforestation continues to jeopardize Malagasy primates as viable habitats become smaller, more fragmented, and more disturbed. This deforestation can lead to changes in diet, microhabitat, and gene flow between populations of endangered species, and it remains unclear how these changes may affect gut microbiome (GM) characteristics. The black‐and‐white ruffed lemur (Varecia variegata), which is among Madagascar's most threatened lemur species, provides a critical model for understanding the relationships between historical and on‐going deforestation (habitat disturbance), feeding ecology, and GM composition and diversity. We studied four populations inhabiting two rainforests (relatively pristine vs. highly disturbed) in southeastern Madagascar. We conducted full‐day focal animal behavioral follows and collected fecal samples opportunistically across a three‐month period. Our results indicate that lemurs inhabiting sites characterized by habitat disturbance and low dietary diversity exhibited reduced gut microbial alpha diversity. We also show that these same factors were associated with high community dissimilarity using weighted and unweighted UniFrac metrics. Finally, an indicator species analysis showed that the most pristine site was characterized by an abundance of methanogenic archaea. While it is impossible to disentangle the relative contributions of each confounding variable presented by our sampling design, these results provide crucial information about GM variability, thereby underscoring the importance of monitoring endangered species at the population‐level.     

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.     

The social behaviour of doucs (Pygathrix nemaeus nemaeus) at San Diego Zoo

A group of six doucs was observed for 200 hours at San Diego Zoo. Patterns of social behaviour (including communicatory patterns) are described and compared with those of other colobine monkeys. Most aspects of the douc's social behaviour appear to be typical for colobines, although an eyelid display may be unique within the sub-family and the copulatory patterns are at least unusual.     

Feeding enrichment by self‐operated food boxes for white‐fronted lemurs (Eulemur fulvus albifrons) in the Masoala exhibit of the Zurich Zoo

In the new Masoala exhibit of the Zurich Zoo four self‐operated food boxes were installed to encourage arboreal behavior and higher activity levels, and to increase the attractiveness to visitors of a group of three white‐fronted lemurs (Eulemur fulvus albifrons) and one Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data obtained by direct observations with and without food boxes present were compared. In addition, visitors were surveyed to investigate attractiveness of the lemurs. Overall activity and locomotor behavior increased due to food box presentation. Furthermore, the visitor survey documented that the lemurs were spotted more often in trees when the food boxes were present. Because behavior patterns of the subjects approached natural levels with food boxes, the presentation of self‐operated food boxes seems a valuable tool to improve the captive environment of lemurs. Zoo Biol 0:1–10, 2005. © 2005 Wiley‐Liss, Inc.     

Strike-induced chemosensory searching in old world vipers and new world pit vipers at San Diego Zoo

Rattlesnakes (Crotalus unicolor, C vegrandis) and Russell's vipers (Vipera russelli) at San Diego Zoo exhibited sustained high rates of tongue flicking after striking mice (Mus musculus) but not after seeing, smelling, and/or detecting thermal cues arising from mice. Called strike-induced chemosensory searching (SICS), this phenomenon contributes to poststrike trailing of envenomated prey. Because these zoo-raised snakes had always been offered dead rodents, and because these prey were usually ingested without first being struck, the present snakes had rarely exercised their innate predatory repertoire (ie, ambush tactics including striking, releasing, and trailing). Indeed, most specimens had never before struck a mouse and, hence, had never exhibited SICS. The occurrence of SICS in the present study clearly indicates that this important aspect of the predatory repertoire had not been degraded as a consequence of long-term captive husbandry.