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.     

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.     

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.     

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.     

What is Communicated in the Antipredator Calls of Lemurs: Evidence from Playback Experiments with Ringtailed and Ruffed Lemurs

Two hypotheses of signal specificity in antipredator calls (“referential signalling” and “response urgency”) are discussed in light of prior research on ground squirrels and vervet monkeys. These hypotheses then are examined with data on responses of semi-captive ringtailed and ruffed lemurs to antipredator call playbacks. Although the responses of ringtailed lemurs support a referential-signalling interpretation of their antipredator calls, those of ruffed lemurs do not conform well to either hypothesis. Rather, ruffed lemur antipredator calls seem best viewed as “affective” signals that may only reflect underlying emotional/motivational states.     

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.     

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.     

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.     

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.     

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.     

An Interactive Playback Experiment Shows Song Bout Size Discrimination in the Suboscine Vermilion Flycatcher (Pyrocephalus rubinus)

Many aspects of the social behaviour of birds are mediated by vocal displays, and variation in song output or song structure conveys different information to receivers. After nest construction begins, when vermilion flycatcher (Pyrocephalus rubinus) females are potentially fertile, males increase their song rate during the dawn chorus. A previous study failed to give evidence that males discriminate among song rates. However, males sing in sequences of songs (song bouts), and an increase in song rate may be achieved by increasing the number of bouts, the number of songs in each bout (bout size) or both. Studying a vermilion flycatcher population in Mexico City, we evaluated whether dawn song rate is related to song bout size or to number of bouts. Bout size correlated with song rate and differed among males. We hypothesized that longer bouts are more threatening signals than shorter ones and predicted a stronger response by males towards the former. We exposed each male to three playback treatments: (1) Long song bout (Long), in which we replied to the male with twice the number of songs he sang in the bout, (2) Short song bout (Short), in which we played half the number of songs sung by the male and (3) Control, this was the same as the Long treatment but we used songs from a related species, the tropical kingbird (Tyrannus melancholicus). Males responded with a higher proportion of calls near the speaker when exposed to the Long treatment than during the Short or Control treatments, indicating that they discriminate among song bouts differing in size, that they may perceive longer bouts as more threatening and that they use calls rather than songs to address threatening situations. Our results suggest that song bout size is a relevant song attribute that conveys information during intrasexual interactions.     

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.     

Acoustic adaptations to anthropogenic noise in the cicada Cryptotympana takasagona Kato (Hemiptera: Cicadidae)

Anthropogenic noise produced by human activities affects acoustic communication in animals living in urban habitats. We recorded the calling songs of the cicada Cryptotympana takasagona in the Kaohsiung metropolitan areas of southern Taiwan to investigate possible acoustic adaptations to anthropogenic noise. C. takasagona did not call more in noise gaps. Acoustic features (peak frequency, quartile 25%, quartile 50%, and quartile 75%) of calling songs significantly increased with ambient noise levels. C. takasagona shifted the energy distribution of calling songs to higher frequencies in the presence of higher noise levels. We suggest that the acoustic adaptation by which song frequencies increase with levels of anthropogenic noise in C. takasagona may result from a size-dependent calling strategy in which small-sized males call more in noise conditions or large-sized males adjust their song frequency by changing their abdominal cavities.     

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.     

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.     

Sexual Selection and Information Content in Gibbon Song Bouts

Male and female gibbons (Hylobates) produce sexually dimorphic song bouts which appear to serve to guard mates and defend territories respectively. On the basis of differences in both the familiarity and the costs of conflict between sender and receiver, males but not females are hypothesized to use high-energy assessment signals to advertise resource-holding potential. This hypothesis is tested by examining the evidence for differential energy constraints in the production of male and female song bouts across 21 gibbon populations. The results indicate that song performance is reduced when the availability of high-energy foods is reduced and that this effect is greatest in males. Male song bout frequency also declines in populations where the energetic costs of thermoregulation are likely to be greater (i.e. in high-latitude populations). Females do not show this pattern. Females appear to perform the minimum number of songs per bout required for signal transmission and may perform bouts less often when more songs are required. In contrast, males sing for longer periods the more frequently bouts are performed. Overall, these results support the hypothesis that the song bouts of males but not females act as assessment signals. Observational and experimental studies which would provide a more powerful test of this hypothesis are briefly outlined.     

Song characterization in the spectacled warbler (Sylvia conspicillata): a circum-Mediterranean species with a complex song structure

The spectacled warbler (Sylvia conspicillata) is a small passerine with a patchy distribution throughout the circum-Mediterranean region, including the North Atlantic archipelagos of Madeira, Canary Islands and Cape Verde. Here we characterize the species song structure on the island of Fuerteventura, quantifying repertoire size, inter- and intra-individual spectrographic variation, to determine whether acoustic variation occurred within an island population. Male song display was organized in song bouts of a variable number of song phrases, which in turn were made up of 4–69 syllables. We classified syllable types to derive a measure of repertoire size (number of different syllables) per song bout, and then used rarefaction methods to calculate the estimated repertoire size for our population of males. Three categories of song bout length were considered in analyses: short song bouts of 10 phrases, average bouts of 19 phrases and long bouts of ≥ 29 phrases. The observed and estimated repertoire size per male (between 43 and 126 syllables per male) increased with song bout duration, although the relationship was not significant for the estimated values. To test whether songs could be individually specific, we measured 11 spectrotemporal parameters of the song. A discriminant analysis using these variables performed poorly in classifying songs to the individuals that uttered them, but we found less variation in the individual than in the population for three out of the 11 variables. These individually specific variables, involving the first or the most common syllable of the song, the trill, were the duration of the first syllable of the phrase, the duration and the dominant frequency of the trill syllable. Our study emphasizes the complexity of spectacled warbler songs, in which males continuously add novel syllables over the entire song bout. This complexity appears to be determined by individual innovation capabilities rather than by the behaviour of copying neighbour repertoires, since songs of close birds were not more similar than songs from far-away territories.     

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.     

The song structure and seasonal patterns of vocal behavior of male and female bellbirds (Anthornis melanura)

The bellbird (Anthornis melanura) is a honeyeater endemic to New Zealand, which uses song to defend breeding territories and/or food resources year round. Both sexes sing and the song structure and singing behavior have not yet been quantified. The number of song types, spectral structure, repertoire size, and singing behavior of male and female bellbirds was investigated for a large island population. Song types differed between the sexes with males singing a number of structurally distinct song types and females producing song types that overlapped in structure. Singing behavior also differed between the sexes; males often sung long series of songs while females sung each song at relatively long and variable intervals. Singing by both sexes occurred year round but the frequency of male and female singing bouts showed contrasting seasonal patterns. The frequency of female singing bouts increased as the breeding season progressed, whereas male singing bouts decreased. In contrast to almost all studied passerines, female bellbirds exhibited significant singing behavior and sung songs of complex structure and variety that parallel male song. These results provide a quantitative foundation for further research of song in bellbirds and in particular the function of female vocal behavior.     

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.