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Ecology and conservation of the crowned lemur, Lemur coronatus, at Ankarana, n. Madagascar. With notes on Sanford's lemur, other sympatrics and subfossil lemurs.

Forests of Ankarana limestone massif in northern Madagascar support one of the largest and least disturbed populations of Crowned Lemurs, Lemur coronatus. This paper reports a preliminary study of the ecology of this species in the Ankarana Special Reserve conducted at the end of the dry season in 1986, with additional information collected a year later. Crowned Lemurs occur in very high densities in the semi-deciduous canopy forest and this probably represents a dry season refuge for the species. They also use more open habitats, including sparsely vegetated limestone and degraded forest. Sanford's Lemur, Lemur fulvus sanfordi, also inhabits the Ankarana forests but is most abundant in degraded habitats. Crowned and Sanford's Lemurs had similar patterns of activity, which included nocturnal travelling and feeding bouts. Crowned Lemurs proved to be unusual among Lemur species in displaying low spatial troop cohesion and a lack of obvious troop hierarchy. Stronglyoides-like enteric helminths infested about one third of Crowned Lemurs but were apparently not causing disease. Crowned Lemurs fall prey to the Fosa, Cryptoprocta ferox, and the young possibly also to the largest raptors. A total of seven living lemur species (including the very rare Propithecus diadema perrieri and Daubentonia madagascariensis) were confirmed at Ankarana by the authors, and three further species have been reported by other observers. In addition to these ten extant lemurs, four subfossil species have been discovered: three of them (Hapalemur simus, Palaeopropithecus and Mesopropithecus) by the authors. The possibility that all 14 lemurs were once sympatric is discussed. For the present, the lemurs of Ankarana are protected from hunting by local taboo. Nevertheless they are under severe threat from habitat destruction, despite Ankarana's Special Reserve status. Given the very restricted distributions of Crowned and Sanford's Lemurs, both must be considered as threatened with extinction.

Animals

Multiple measures of hand-use lateralization in the ring-tailed lemur (Lemur catta).

Evaluated a free-ranging matriline of 13 ring-tailed lemurs (Lemur catta) from videotaped records for lateralized hand use with 2 tasks and 4 measures: food reaching, feeding posture, duration of food holding, and manipulation of food between mouth and hand while eating. Binomial z scores determined 7 lemurs to be left preferent in reaching, 3 right, and 3 ambipreferent. Ideographic analyses suggested possible sex-linked and early experience twin effects. When compared to right and ambipreferent lemurs, left reach preferent lemurs used the left hand more but bimanuals grasped less in food holding and also engaged in less hand-mouth food manipulation. The tendency to manipulate food was not correlated with bimanual holding but was inversely related to left hand holding and directly related to right hand holding. These patterns are discussed as possible precursors of human bimanual manipulation.

Animals

Chromosomal evolution in Malagasy lemurs. II. Meiosis in intra- and interspecific hybrids in the genus Lemur.

The chromosome analysis of meiosis in four lemurs, Lemur fulvus fulvus, L. f. collaris, L. f. albocollaris, and L. macaco, and particular hybrid crosses is reported. In metaphase I, trivalents and chain elements were detected and identified with T-banding. The study largely confirms our previous work on mitotic karyotype comparisons in the genus Lemur. The absence of chain multivalents elements in the pachytene stages of hybrid meiosis, where a chain is detected later in diakinesis, may offer evidence on the possible existence of a two-step pairing mechanism in meiotic homolog pairing. Considerations about the role of the chromosome rearrangements in establishing a gametic barrier in speciation are developed.

Animals

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.

Animals

Arboviruses and lemurs in Madagascar: experimental infection of Lemur fulvus with yellow fever and West Nile viruses.

In previous serological surveys of lemurs in Madagascar, antibodies against flaviviruses were frequently detected. To examine the epidemiological role of Lemur fulvus, experimental infections with yellow fever (YF) virus and West Nile (WN) virus were performed. YF and WN infections were clinically unapparent. A 3 to 4-day-long viremia, with moderate levels was observed with YF virus. WN virus, especially the strain isolated in Madagascar, provoked a 4 to 6-day-long viremia sufficient to infect Aedes aegypti. In all experiments, the antibody response was studied during the following weeks by 3 methods. The results led to the conclusion that Malagasy lemurs could act as amplifying hosts for WN virus present in Madagascar, and as hosts for YF virus if it were introduced on the island. The epidemiological role of these primates is discussed according to their ecology and their contact with potential mosquito vectors in forest areas of Madagascar.

Aedes

Amino acid sequences of the alpha and beta chains of adult hemoglobin of the brown lemur, Lemur fulvus fulvus.

Globin prepared from hemoglobin of the brown lemur (Lemur fulvus fulvus) was separated into alpha and beta chains by chromatography on a CM 52 column. The S-aminoethylated alpha and beta chains were each digested with trypsin and resulting peptides were isolated. The amino acid sequences of the tryptic peptides were established. The ordering of these peptides in the alpha and beta chains was deduced from the homology of their amino acid sequences with that of human adult hemoglobin. The primary structure of brown lemur hemoglobin thus obtained differs from that of human hemoglobin in 15 amino acids in the alpha chain and 26 in the beta chain.

Amino Acid Sequence

[Reactions to mirror in three species of lemurs (Lemur fulvus, L. macaco, L. catta)].

Reactions when confronted with their own reflection in a mirror were observed in three captive groups of lemurs: L. fulvus, L. macaco and L. catta. The ability of a mirror to induce social facilitation of drinking was also studied in one individual of each species. As previously observed in monkeys, the three groups of lemurs showed much more attention to the mirror than to a non-reflective surface, especially nasal contacts. Only L. fulvus showed habituation to the mirror with successive presentations. No social behaviours were directed towards the reflection, in contrast to descriptions of mirror-image reactions in monkeys, and the mirror did not produce an effect of social facilitation. The results suggest that the mirror elicits a diminished social reaction in lemurs compared to monkeys, perhaps due to the absence of relevant olfactory stimuli.

Animals

Analyses of feeding lateralization in the small-eared bushbaby (Otolemur garnettii): a comparison with the ring-tailed lemur (Lemur catta).

Feeding related lateralization was examined in a population of 23 small-eared bushbabies (Otolemur garnettii). The three measures used to determine lateralization were food reaching, holding, and manipulation. Sex and age differences were found, with adult females showing a strong right bias and adult males a left bias. Juvenile males were weakly lateralized and less consistent across measures than adult animals. The use of standard scores to assess lateralization allowed species comparisons to be made. The results of this study were compared with results from a previous study on lateralization in the ring-tailed lemur (Lemur catta). Species comparisons found sex differences to be a stronger factor in lateralization than species differences.

Animals

Chromosomal evolution in Malagasy lemurs. I. Chromosome banding studies in the genuses Lemur and Micrcebus.

The successive use of several banding methods permitted us to compare the karyotypes of six Malagasy lemurs: Microcebus murinus, Lemur fulvus fulvus, L. f. collaris, L. f. albocollaris, L. macaco, and L. mongoz. A correspondence can be found among all clearly identifiable chromosomes. Based on rearrangements of some of the chromosomes, the karyotype of M. murinus seems to be closest to that of the hypothetical common ancestor. The karyotype of L. f fulvus, which is nearly identical to that of M. murinus, gives rise to those of other forms by several rearrangements.

Animals

Chromosomal evolution in Malagasy lemurs. III. Chromosome banding studies in the genus Hapalemur and the species Lemur catta.

The karyotypes of five Malagasy lemurs are described and compared after the successive use of various banding methods. Phylogenic relationships appear to exist between the respective ancestors of Lemur catta, Hapalemur simus, H. griseus occidentalis, H. griseus ssp, and H. griseus griseus. Their karyotypes can be derived from that of L. fulvus fulvus by chromosomal rearrangements affecting mainly chromosomes 1 and X. Intense staining of juxtacentromeric heterochromatin was detected among the different subspecies of H. griseus.

Animals

Confirmation, via in situ hybridization, of the occurrence of Robertsonian translocations during lemur evolution by localization of GLUDP1 DNA sequences on lemur chromosomes.

A human genomic DNA sequence derived from glutamate dehydrogenase pseudogene 1 was used as a probe for in situ hybridization to the chromosomes of three lemur species, Eulemur fulvus mayottensis (EFU), E. macaco macaco (EMA), and E. coronatus (ECO). This sequence, which is 98% homologous to the nucleotide sequence of the gene for human glutamate dehydrogenase (GLUD), was found on homologous bands of three morphologically similar chromosome segments, EFU14, EMA5p, and ECO8q, confirming that different Robertsonian translocations occurred during the evolution of these three species. These loci on the lemur chromosomes probably correspond to the human GLUD locus.

Animals

The oestrous cycle of the brown lemur, Lemur fulvus.

Examination of vaginal smears and observations of the colour and tumescence of the genitalia and discharge of mucus of 9 brown lemurs indicated that the oestrous cycle lasted for 30 days and that cycles occurred between September and July. The timing of cycles of females housed in visual isolation differed from that of females able to see other lemurs, indicating that the oestrous cycle in this species can be influenced by different housing conditions.

Animals

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.

Adenoma, Bile Duct

Chromosomal evolution in Malagasy lemurs. IV. Chromosome banding studies in the genuses Phaner, Varecia, Lemur, Microcebus, and Cheirogaleus.

The karotypes of five species of Malagasy lemurs are described and compared with those of 12 previously studied species or subspecies. Based on these studies, phylogenetic relationships among nearly all the species of Cheirogaleidae and Lemuridae are proposed. The karyotype of the common ancestor is identical or very similar to that of Microcebus. Nearly 60 chromosomal changes, including five intrachromosomal rearrangements of the X chromosome, have been detected during the evolution of these two families. The possible evolutionary role of the different chromosomal rearrangements is discussed.

Animals

Patterns of maternal care in lemurs. III. Lemur variegatus.

Lemur fulvus, L. catta, and L. variegatus differ markedly in the details of mother-infant relations. Do these differences account for those seen in adult life? We hope to determine this through interspecific cross-fostering. Here we describe the normal pattern of rearing of 5 infants among two groups of 2 and 5 adult L. variegatus, reared in the laboratory. The descriptions cover the first 7 months of life, and include the effects of maternal separation at 150 days of age, when estrus normally disrupts maternal care. The principal finding is that in the mother's absence young turn more to other adults than to their siblings, who are, apparently, not adequate social substitutes for adults.

Animals