Aspects of reproduction in ruffed lemurs (Lemur variegatus).

Results of breeding of ruffed lemurs (Lemur variegatus) at the Duke Primate Facility provide information concerning estrous cycle, sexual behavior, age of first conception, gestation period, parturition, litter size. L. variegatus differs from other Lemur species in these respects.     

Reproduction of the mongoose lemur (Lemur mongoz) in captivity

Responses to questionnaires sent to 20 institutions holding Lemur mongoz did not reveal which aspects of management or husbandry could account for reproductive failure in the captive population, but allowed some qualitative comparisons with data compiled for captive and wild animals. In general, reproduction has occurred initially among wild-caught specimens before tapering off, and rarely occurs in the captive F₁ generation. Data compiled by the International Species Inventory System and the International Zoo Yearbook revealed an aging captive population with no recent reproduction. No aspect of group composition, activity patterns, seasonal light regime, reproductive cycles, or diet could be linked to the lack of reproduction; and among lemurs subjected to the same conditions, some were known to reproduce while others did not. Lack of knowledge about this species and the threat of extinction for both captive and wild populations make an investigation of reproductive biology imperative. Recommendations for a research program are given.     

Reproduction in the crowned lemur (Lemur coronatus) in captivity

Four pairs of captive crowned lemurs (Lemur coronatus) were studied during their annual breeding season in order to obtain baseline data on their reproductive biology for comparison with other Lemur species and to enhance their captive breeding success. Vaginal smears, testicular measurements, and records of the Duke University Primate Center provided the presented data. During a single breeding season, females cycled an average of three times, with an average cycle length of 34 days. Cycles were detected between November and March. Vaginal estrus and copulations were limited to one day per cycle. After 125 days of gestation females gave birth to one or two young. Both sexes attained sexual maturity at an age of about 20 months. Mean male testis size peaked in late December; at the same time, three of the females experienced their first estrus. Based on all available data, there was a significant positive correlation between cycle length and gestation length in the genus Lemur.     

Endocrine correlates of pregnancy in the ring-tailed lemur (Lemur catta): implications for the masculinization of daughters

Female ring-tailed lemurs (Lemur catta) are Malagasy primates that are size monomorphic with males, socially dominate males, and exhibit a long, pendulous clitoris, channeled by the urethra. These masculine traits evoke certain attributes of female spotted hyenas (Crocuta crocuta) and draw attention to the potential role of androgens in lemur sexual differentiation. Here, hormonal correlates of prenatal development were assessed to explore the possibility that maternal androgens may shape the masculine morphological and behavioral features of developing female lemurs. Maternal serum 17α-hydroxyprogesterone, dehydroepiandrosterone sulphate (DHEA-S), ?⁴ androstenedione (androst-4-ene-3,17,dione), testosterone, and 17β-estradiol were charted throughout the 19 pregnancies of 11 ring-tailed lemurs. As in spotted hyenas, lemur pregnancies were associated with an immediate increase in androgen concentrations (implicating early maternal derivation), followed by continued increases across stages of gestation. Pregnancies that produced singleton males, twin males, or mixed-sex twins were marked by greater androgen and estrogen concentrations than were pregnancies that produced singleton or twin females, especially in the third trimester, implicating the fetal testes in late-term steroid profiles. Concentrations of DHEA-S were mostly below detectable limits, suggesting a minor role for the adrenals in androgen biosynthesis. Androgen concentrations of pregnant lemurs bearing female fetuses, although less than those of pregnant hyenas, exceeded preconception and postpartum values and peaked in the third trimester. Although a maternal (and, on occasion, fraternal) source of androgen may exist for fetal lemurs, further research is required to confirm that these steroids would reach the developing female and contribute to her masculinization.     

Disseminated toxoplasmosis in a captive ring-tailed lemur (Lemur catta)

A 3-yr-old secundiparous female ring-tailed lemur presented to the Auburn University Small Animal Clinic with signs of dyspnea, lethargy, and anorexia. The animal died before she could be examined, and a full necropsy was immediately performed. Provisional necropsy findings included moderate pneumonia and hepatopathy. Acute interstitial pneumonia and focal hepatocellular necrosis were confirmed histologically. Lung impression smears, histopathology, electron microscopy, immunohistochemistry, and tissue culture isolation resulted in a diagnosis of acute disseminated Toxoplasma gondii infection, which was confirmed by polymerase chain reaction. The isolate of T. gondii was avirulent for mice and was named AU Tgl and genetically is type II. The source of the infection remains unclear, but speculation suggests contaminated fruit or blackbirds (Passeriformes: Icteridae) acting as transport hosts for oocysts from nondomestic felids and feral cats on the property.     

Individuality in a contact call of the ringtailed lemur (Lemur catta)

A vocalization of the ringtailed lemur (Lemur catta) was examined for individual differences according to several temporal- and frequency-dependent variables. Vocalizations were tape recorded at the Duke University Primate Center (Durham, NC) and spectrographically analyzed. Significant differences were found in pair-wise comparisons of call structure among the study subjects, thus providing the physical basis for individual discrimination. A separate analysis comparing degree of kinship and vocal similarity revealed a positive but nonsignificant correlation between these two variables. This study represents an initial examination of vocal individuality in prosimian 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.     

Black lemur (Lemur macaco) hand preference in food reaching

The present study assessed the hand preferences exhibited by 33 black lemurs during routine feeding. Individual animals displayed hand preferences that were consistent across observations separated by as much as seven months. Within this population, 20 were left hand preferent, 12 right preferent, and 1 was ambidextrous. Correlational analysis of age and percentage left hand use indicated an inverse relationship in which younger animals tended towards the preferential use of the left hand and older animals the preferential use of the right hand. Similar analysis found no relationship between either sex and hand preference or familial relationship and hand preference. The skewed distribution of age in this sample renders tentative conclusions regarding age-related variations in hand preference. It is suggested that if the hand preferences of the black lemur are not age-related, then this species may be characterized as having a bias towards the preferential use of the left hand for food reaching.     

Selected aspects of Lemur variegatus reproductive biology

Results from data collected during the 1978–1979 breeding season on the reproduction of Lemur variegatus at the San Diego Zoo provide information which generally supports previously published reports on this species. Comparison of selected results from these data to a larger data base of which they are a part makes it possible to resolve some of the discrepancies between reports. Certain aspects of the reproductive biology of this species may then be generally characterized with confidence: The onset of seasonal breeding as evidenced by estrous behavior begins as early as mid-December in the northern hemisphere and may continue through March; genital changes associated with estrus in females last 9.85 ± 1.67 days (± SD); female receptivity occurs 7.0 ± 1.53 days after the onset of these genital changes and lasts 12-24 hours, during which breeding occurs; gestation averages 99.47 ± 4.19 days; the peak birth season is April–May; litters normally contain two to three offspring, with full-term neonates weighing an average of 104.63 ± 19.10 grams. In addition, L variegatus appears to be highly resistant to the impact of captivity on both its reproductive physiology and behavior, as indicated by the 100% breeding success of the diversely reared and managed groups of study animals.     

Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus)

Physiologically related features of muscle morphology are considered with regard to functional adaptation for locomotor and postural behavior in the brown lemur (Lemur fulvus). Reduced physiological cross-sectional area, estimated maximum excursion of the tendon of insertion, length of tendon per muscle fasciculus, and areal fiber type composition were examined in the quadriceps femoris in order to assess the extent of a "division of labor" among four apparent synergists. Each of these four muscles in this prosimian primate displays a distinguishing constellation of morphological features that implies functional specialization during posture and normal locomotion (walk/run, galloping, leaping). Vastus medialis is best suited for rapid whole muscle recruitment and may be reserved for relatively vigorous activities such as galloping and leaping (e.g., small cross-sectional area per mass, long excursion, predominance of fast-low oxidative fibers, relatively little tendon per fasciculus). In theory, rectus femoris could be employed isometrically in order to store elastic strain energy during all phasic activities (e.g., large cross-sectional area per mass, short excursion, predominance of fast-high oxidative fibers, large amount of tendon per fasciculus). Vastus intermedius exhibits an overall morphology indicative of a typical postural muscle (e.g., substantial cross-sectional area, short excursion, predominance of slow-high oxidative fibers, large amount of tendon per fasciculus). The construction of vastus lateralis reflects an adaptation for high force, relatively high velocity, and resistance to fatigue (e.g., large cross-sectional area, long excursion, most heterogeneous distribution of fiber types, large amount of tendon per fasciculus); this muscle is probably the primary contributor to a wide range of locomotor behaviors in lemurs. Marked dramatic architectural disparity among the four bellies, coupled with relative overall fiber type heterogeneity, suggests the potential for exceptional flexibility in muscle recruitment within this mass. One interpretation of this relatively complex neuromuscular organization in the brown lemur is that it represents an adaptation for the exploitation of a three-dimensional arboreal environment by rapid quadrupedalism and leaping among irregular and spatially disordered substrates.     

Avian nest predation by a semi-captive collared lemur (Lemur fulvus collaris)

A lemur (Lemur fulvus collaris) in a semi-captive group of six animals at the Duke University Primate Center (DUPC) was observed eating an egg from the nest of a mourning dove (Zenaida macroura). The manner in which the animal had been foraging prior to this incident, and the fact that wild birds at the DUPC frequently direct antipredator behaviors, such as mobbing toward thisL. f. collaris group, suggest that nest predation is part of normal foraging behavior in these animals.     

The Behavior of Lemur variegatus Kerr 1792

This paper reports the social behavior of two groups of captive Lemur variegates. An intensive three-month study provided baseline data. This was supplemented by two years of follow-up observations. Various components of the captive behavioral repertoire are described. Data on feeding behavior, vocalizations, grooming, agonistic interactions, sexual behavior and infant development were collected.     

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.     

Spontaneous cholangiocarcinoma in a ring-tailed lemur (Lemur catta).

A cholangiocarcinoma in the liver with metastasis to the regional lymph nodes was found in a male ring-tailed lemur (Lemur catta). The liver was partially replaced by a gray-white, coarsely lobulated mass. Microscopically, the tumor consisted of well circumscribed lobules of anaplastic, low cuboidal cells occasionally arranged in duct-like structures. The tumor did not involve the gallbladder.     

Contact calling behaviour in the male ring‐tailed lemur (Lemur catta)

The ring‐tailed lemur (Lemur catta) is a group‐living strepsirhine primate endemic to Madagascar that has a complex vocal repertoire including affiliative moan and hmm calls. Past research has suggested that both vocalisations may be contact calls, and we assessed their usage in addition to examining the effect of individual differences and social factors on male calling behaviour. We tested three hypotheses: the group cohesion, preferred companion and individual differences hypotheses. From March to July 2010, 565 h of focal animal data were collected on 31 males aged ≥1 year at the Beza Mahafaly Special Reserve, Madagascar. Focal males were observed for 30 min, with vocalisations, allogrooming and agonistic interactions noted using one‐zero sampling, and general behaviour, nearest neighbour identity and distance noted using instantaneous point sampling, all at 2.5 min intervals. We found support for the group cohesion hypothesis for both vocalisations, and support for the preferred companion and individual differences hypotheses for the hmm but not the moan vocalisation. Moan and hmm calls maintained the distance between a male and his nearest neighbour, and were made at higher rates during behaviours which may lead to separation from conspecifics, such as travel and vigilance. Males made hmm calls at higher rates when they were low‐ranking, and/or when the nearest neighbour of a male or a preferred companion of either sex. Low‐ranking males may hmm call to maintain proximity to specific individuals within social groups who will show them increased tolerance, with the hmm signalling peaceful intent. Ring‐tailed lemurs are one of the best living models of gregarious primate ancestors, and gaining a better knowledge of the function and range of usage of their contact calls informs our understanding of the evolution of primate cognition.     

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.