Free-ranging Lemurs Research Articles

The effects of environmental and visitor variables on the behavior of free-ranging ring-tailed lemurs (Lemur catta) in captivity.

The effect of the zoo environment on captive animals is an increasingly studied area of zoo research, with visitor effects and exhibit design recognized as two of the factors that can contribute to animal welfare in captivity. It is known that in some situations, visitors may be stressful to zoo-housed primates, and this may be compounded by environmental factors such as the weather, the time of day, and zoo husbandry routines. Exhibit design and proximity of the public are also known to influence behavioral response of primates to visitors; however, there is minimal research on free-ranging zoo animals, even though they are potentially subjected to intense interactions with visitors. The current study explores the effect of the zoo environment, several visitor variables and specific animal-visitor interactions on the behavior of free-ranging ring-tailed lemurs (Lemur catta) at Fota Wildlife Park, Ireland. Data were obtained through scan samples collected over 18 months (n = 12,263) and analyzed using a range of statistical tests, including general estimating equations (GEE). Results demonstrate that the free-ranging lemurs' behavior at Fota Wildlife Park is affected by season, weather and time of day. Similarities in feeding behavior exist between the free-ranging group and lemurs in the wild when resources are plentiful. Visitor variables had a limited effect on lemur behavior and behavioral diversity level. Lemurs rarely reacted to visitors when specific interactions were considered. Generally, the results indicate that the ring-tailed lemurs in this study have adapted well to the zoo environment and habituated to visitors.

Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar

We detected Cryptosporidium sp. by direct immunofluorescence in fecal samples from greater bamboo lemurs (Prolemur simus) and eastern rufous mouse lemurs (Microcebus rufus) inhabiting the Ranomafana National Park, Madagascar. This is the first report of an occurrence of these potentially zoonotic parasites in free-ranging lemurs in the rain forest of Madagascar.

Survey of Minerals and Fat-Soluble Vitamins in Captive Black and White Ruffed Lemurs (Varecia variegata)

Serum and whole blood samples from 64 clinically normal captive black and white ruffed lemurs (Varecia variegata), aged 6 mo to 32 yr, were analyzed to survey mineral and fat-soluble vitamin concentrations. All animals were fed a commercial primate food and a wide range of fruits and vegetables. Specific commercial diet information was available for 52 animals that were fed one of 10 different diets. Data analysis showed no differences in the analytes attributable to sex or access to natural ultraviolet light. Serum phosphorus (range: 1.4-3.1 mmol/L) was significantly higher and retinol (range: 0.38-1.23 micromol/L) was significantly lower in young animals (< or =4 yr). Iron (range: 17.2-77.0 micromol/L) and copper (range: 10.7-53.3 micromol/L) were much higher than concentrations reported in other free-ranging lemur species, and in some animals were at levels considered potentially toxic in domestic animals. Magnesium (range: 0.66-2.04 mmol/L), sodium (range: 111-201 mmol/L), and potassium (range: 2.0-6.8 mmol/L) ranged both lower and higher than concentrations considered adequate for a mammal, but were similar to concentrations reported in wild red ruffed lemurs (Varecia rubra), a closely related species. Selenium (range: 3.5-7.7 micromol/L) was within the range expected for a mammal, but higher than concentrations reported in wild V rubra. Zinc (range: 9.2-62.7 micromol/L) was similar to concentrations reported in V. rubra. Calcidiol (range: <12.5-144.8 nmol/L) and retinol (range: 0.38-2.95 micromol/L) were both lower and higher than concentrations reported in V. rubra. Lower serum calcidiol concentration correlated with lower commercial dietary vitamin D3. Alpha-tocopherol (range: 1.2-17.6 micromol/L) and y-tocopherol (range: 0.3-3.9 micromol/L) were within a range expected in a captive frugivorous primate but higher than concentrations found in wild V. rubra.

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.

BIOMEDICAL EVALUATION OF FREE-RANGING RING-TAILED LEMURS (LEMUR CATTA) IN THREE HABITATS AT THE BEZA MAHAFALY SPECIAL RESERVE, MADAGASCAR

Complete physical examinations and biomedical sample collection were performed on 70 free-ranging ring-tailed lemurs (Lemur catta) from three different habitats in the Beza Mahfaly Special Reserve (BMSR), in southern Madagascar, to assess the impact of humans and habitat on lemur health. Lemurs were chemically immobilized with ketamine and diazepam administered via blow darts for concurrent biomedical, morphometric, and behavioral studies. Subsets of the animals had blood analyzed for hematology, serum chemistry, micronutrients, fat-soluble vitamins (vitamins A, D, and E), measures of iron metabolism, and polymerase chain reaction assays (PCR) for Toxoplasma gondii, Hemoplasma spp., Bartonella spp., Ehrlichia spp., Anaplasma phagocytophilum, and Neorickettsia risticii. Results were compared on the basis of gender and the habitats at the study site: reserve (intact gallery forest), degraded (human inhabited and altered), and marginal (dry didieracea forest with heavy grazing and tree cutting). Levels of vitamin D, triglycerides, and cholesterol, and measures of iron metabolism for BMSR lemurs were greater than those previously reported for a free-ranging lemur population (Tsimanampetsotsa Strict Nature Reserve, Madagascar) with less access to foods of anthropogenic origin. BMSR ring-tailed lemurs from a habitat with less water (marginal) had higher sodium (P = 0.051), chloride (P = 0.045), osmolality (P = 0.010), and amylase (P = 0.05) levels than lemurs from other BMSR habitats, suggesting that these lemurs were less hydrated. Vitamin D levels of male lemurs were higher (P = 0.011) than those of females at BMSR, possibly because of differences in sunning behavior or differential selection of food items. The biological significance is uncertain for other parameters with statistically significant differences. All samples tested (n = 20) were negative for the pathogens tested using PCR assays. Continued concurrent biomedical and ecological research is needed at BMSR to confirm these results and determine their association with population mortality and fecundity rates.

Male Mate Choice in Lemur catta

Though females are generally more selective in mate choice, males may also derive reproductive benefits from exercising mate selectivity if one or more factors limit male reproductive success and females differ in reproductive potential. I used male mating effort as a proxy for male mate choice in ring-tailed lemurs (Lemur catta). I calculated mating effort as the rate of male-male agonism during each female's estrous period 30 min before and 30 min after the first and last mountings with intromission. I collected data on 1 free-ranging Lemur catta troop during 2 consecutive breeding seasons on St. Catherines Island, USA. In both yrs, male mating effort differed significantly among troop females once I adjusted male-male agonistic rates to reflect agonistic intensity, and I corrected for the number of observed mates per female (2000: χ2 = 27.43, df = 3, p < 0.0001; 2001: χ2 = 21.10, df = 3, p < 0.001). Results strongly suggest male mate choice. Contrary to expectation, males did not expend the greatest mating effort for females with the highest dominance status nor the highest reproductive success. Males preferred females that either: (1) belonged to the age class in which fecundity and infant survival is the highest at this site (4–9 yrs), or 2) were older females (≥10 yrs) with high reproductive success. Female reproductive potential appears to be an important variable determining male mating effort in Lemur catta.

MOLECULAR AND SEROLOGIC EVIDENCE OF TICK-BORNE EHRLICHIAE IN THREE SPECIES OF LEMURS FROM ST. CATHERINES ISLAND, GEORGIA, USA

In recent years, several species of ehrlichiae have been recognized as tick-borne disease agents of veterinary and medical importance. Clinically normal free-ranging or previously free-ranging lemurs, including 46 ring-tailed lemurs (Lemur catta), six blue-eyed black lemurs (Eulemur macaco flavifrons), and four black and white ruffed lemurs (Varecia variegata variegata) from St. Catherines Island, Georgia, were tested for evidence of exposure to tick-borne ehrlichiae. All 52 adult lemurs were serologically tested for exposure to Ehrlichia chaffeensis and Anaplasma phagocytophilum. Polymerase chain reaction (PCR) assays for E. chaffeensis, A. phagocytophilum, Ehrlichia ewingii, and Ehrlichia canis were conducted on blood samples from all 56 lemurs. Blood from all lemurs was inoculated into DH82 cell cultures for E. chaffeensis isolation. Of the adult lemurs, 20 (38.5%) and 16 (30.8%) had antibodies reactive (> or =1:128) for E. chaffeensis and A. phagocytophilum, respectively. Two ring-tailed lemurs were PCR and culture positive for E. chaffeensis. Molecular characterization of the two E. chaffeensis isolates showed that both contained 5-repeat variants of the variable-length PCR target (VLPT) antigen gene and 3-repeat variants of the 120-kDa antigen gene. Sequencing of the VLPT genes revealed a novel amino acid repeat unit (type-9). One lemur infected with E. chaffeensis was slightly hypoproteinemic and had moderately elevated serum alanine aminotransferase (ALT) levels. These lemurs from St. Catherines Island have been exposed to or infected with tick-borne ehrlichiae, or both, but showed no clinical disease.

Alloparental Care in Free-Ranging Lemur catta at Berenty Reserve, Madagascar

Alloparental care was examined in three free-ranging groups of Lemur catta. Group members of all age/sex classes were found to participate to varying degrees in alloparental care of infants, and some types of care were performed significantly more frequently by animals of particular age/sex classes. Adult males, previously reported not to interact with infants, were found to groom and play with them occasionally. Rank or sex of the infant did not affect the amount of alloparental care it received. It is suggested that individuals of all age/sex classes can benefit from receiving or performing alloparental care. Infants can develop social skills and receive protection from alloparents; mothers gain free time to forage and rest; prereproductive females can learn parental skills; all adult females and prereproductive animals are aiding kin by alloparental care, and adult males, by interacting with infants, may have the opportunity to establish a relationship with the mother which could enhance future reproductive success.