Cytogenetic study of Hapalemur aureus

The karyotype of Hapalemur aureus was compared with those of other Hapalemur species, allowing us to determine the phylogenetic position of this species on the evolutionary tree of the Lemuridae.     

Chromosomes of lemuriformes. I. A chromosome complement of Lepilemur mustelinus (I. Geoffroy 1851)

The diploid chromosome number of two specimens of Lepilemur mustelinus (I. Geoffroy 1851) is 2N = 20. All of the chromosomes, except the Y chromosome, are metacentric or submetacentric; the Y chromosome is acrocentric and is the shortest chromosome in the complement. Satellites on autosomal pair 5 provide marked chromosomes for the animals studied and may be a marked pair for the species.     

Cytogenetic study of Allocebus trichotis,a Malagasy prosimian

A cytogenetic study of a female Allocebus trichotis was conducted using R-, G-, and C-banding. Its karyotype does not differ from those of the other Cheirogaleinae (Microcebus, Cheirogaleus, and Mirza). The absence of chromosomal rearrangement in speciation in this group is discussed. © 1995 Wiley-Liss, Inc.     

The food habits of a Malagasy Giant: Hipposideros commersoni (E. Geoffroy, 1813)

Hipposideros commersoni is a large microchiropteran bat endemic to Madagascar. We analysed fragments of its prey from faeces and from underneath feeding perches to describe its diet from four sites. Diet was similar across sites and Coleoptera was the main prey item by percentage volume (75%), followed by Hemiptera (13%). Carabidae and Scarabidae were the most frequent coleopterans found in the diet. Direct observations (n = 3) were made of bats flying short distances from perches along forest trails to prey on Cicadidae ( c. 20 mm in length) located on tree trunks. There were differences in the composition of faecal samples collected form netted bats and pellets collected under feeding perches, with the latter consisting of more Blattoptera (Blattellidae 'cockroaches'). Hipposideros commersoni appears to have a unique foraging behaviour and diet among Malagasy microchiropterans and its preference for certain Coleoptera and other large invertebrates may account for reported seasonal variation in body fattening and activity.     

Social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis)

Knowledge of the social organization of lemurs is still limited for most species. Where there is sufficient information, it has been shown that lemur social organization differs in essential points from that of other primates. In the field study reported here, demographic structure and life-history processes were investigated in order to characterize the social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data were obtained through captures and observations. Alaotran gentle lemurs were found in small groups of up to nine individuals. Although most groups contained just one breeding female, a substantial proportion of groups (35%) had two breeding females. Therefore, Alaotran gentle lemurs cannot be classed as being organized in monogamous family groups. An extended birth season was found, and groups with two breeding females had significantly higher breeding output per adult than groups with a single adult female. Limited data suggest that females emigrate from their natal group while still subadult, whereas males can stay in the natal group until they are fully grown and disperse as adults. Variability in group composition, significantly higher reproductive output per adult in groups with two breeding females, and delayed dispersal of males suggest that Alaotran gentle lemurs pursue a resource-defense mating strategy, rather than a female-defense mating strategy. The suggestion that extant social lemurs may have evolved from a monogamous system, could explain the differences between lemur social systems and those of other primates.     

Cytogenetic study of the endemic Malagasy lemurs subfamily Cheirogaleinae Gregory 1915

Karyotypes were determined on 27 lemurs from six species of what has been called the “subfamily” of Cheirogaleinae : Microcebus murinus murinus (2), M. murinus rufus (2), M. coquereli (5), Phaner furcifer (6), Cheirogaleus medius (9), and C. major (3). The cytogenetic study of these animals reveals that this “subfamily” contains in fact two groups, (a) — Microcebus and Cheirogaleus, and (b) — Phaner. The karyotype of the first two genera has a fundamental number (FN) equal to 66 and the karyotype of the third genus has an FN equal to 62. This result and the fact that Phaner has a particular scent-marking gland, knuckle pads, and finger prints markedly different from those of other genera agree with the view that this animal belongs to a special subfamily, Phanerinae, while the two other genera constitute the subfamily of Cheirogaleinae. These two subfamilies constitute the family of Cheirogaleidae.     

Assessing the function of geophagy in a Malagasy rain forest lemur

Geophagy has been observed in nearly every long‐term study of folivorous primates. Yet despite frequent observations of this behavior, conclusive explanations for soil consumption remain ambiguous. This study tests the most frequently proposed hypotheses for geophagy using data collected on the geophagic behavior of the Milne‐Edwards’ sifaka (Propithecus edwardsi) living in two forests with varying levels of disturbance within Ranomafana National Park, Madagascar. Field data were collected from December 2002 to November 2003, during which time soil samples were collected for mineral analyses from 102 sites selected for geophagy and 42 control sites at which no geophagy was recorded. Results indicate that control soils differ significantly between the two study sites and that this difference is primarily attributable to varying levels of habitat disturbance. The frequency of soil consumption also does not vary significantly by sex or between logged and unlogged habitats. Soil consumption significantly correlated with fruit/seed consumption overall, but to a lesser degree in logged compared with unlogged sites. Clay minerals found in soils likely prevent absorption of dietary toxins in the gut and/or may mediate gut pH. This provides strong evidence for the protection hypothesis for geophagy, which may be especially important in areas where logging, or other forms of habitat disturbance, has been experienced. Abstract in French is available with online material.     

Early Holocene chronology and environment of Ampasambazimba,A Malagasy subfossil lemur site

According to a traditional but hitherto untested reconstruction of Madagascar’s Holocene environment, continuous forest preceded the monotonous grassland formations that now cover most of the island’s interior. Preliminary analyses of pollen samples collected near¹⁴C-dated horizons at Ampasambazimba (central Madagascar) indicate that a mosaic of woodlands, bushlands, and savanna existed close to this important vertebrate subfossil site around 7000–8000 BP. Although most members of Madagascar’s recently extinct “subfossil” fauna are thought to have been forest dwellers, several may have preferred a more open habitat like the one inferred for the region of Ampasambazimba. Dry savanna-woodland burns more readily than does dense forest and may have been more severely affected by the forces which transformed the Malagasy environment during the later Holocene. If so, the loss of savanna-woodland, not dense forest, may have been an important factor in the subfossil extinctions.     

Extreme Endemic Radiation of the Malagasy Vangas (Aves: Passeriformes)

Phylogenetic relationships of the family Vangidae and representatives of several other passeriform families were inferred from 882 base positions of mitochondrial DNA sequences of 12S and 16S rRNA genes. Results indicated the monophyly of the Vangidae, which includes the genus Tylas, hitherto often placed in the family Pycnonotidae. Our results also revealed the Malagasy endemic Newtonia, a genus never previously assigned to the Vangidae, to be a member of this family. These results suggest the occurrence of an extensive in situ radiation of this family within Madagascar, and that the extant high diversity of this family is not the result of multiple colonizations from outside. The extremely high morphological and ecological diversification of the family seems to have been enhanced through the use and ultimate occupancy of vacant niches in this island. Received: 8 September 2000 / Accepted: 13 February 2001     

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.     

Parasite burden and constitution of major histocompatibility complex in the Malagasy mouse lemur, Microcebus murinus

We investigated the importance of the major histocompatibility complex (MHC) constitution on the parasite burden of free-ranging mouse lemurs (Microcebus murinus) in four littoral forest fragments in southeastern Madagascar. Fourteen different MHC class II DRB-exon 2 alleles were found in 228 individuals with high levels of sequence divergence between alleles. More nonsynonymous than synonymous substitutions in the functional important antigen recognition and binding sites indicated selection processes maintaining MHC polymorphism. Animals from the four forest fragments differed in their infection status (being infected or not), in the number of different nematode morphotypes per individual (NNI) as well as in the fecal egg counts (FEC) values. Heterozygosity in general was uncorrelated with any of these measures of infection. However, a positive relationship was found between specific alleles and parasite load. Whereas the common allele Mimu-DRB*1 was more frequently found in infected individuals and in individuals with high NNI and FEC values (high parasite load), the rare alleles Mimu-DRB*6 and 10 were more prevalent in uninfected individuals and in individuals with low NNI and FEC values (low parasite load). These three alleles associated with parasite load had unique amino acid motifs in the antigen binding sites. This distinguished them from the remaining 11 Mimu-DRB alleles. Our results support the hypothesis that MHC polymorphism in M. murinus is maintained through pathogen-driven selection acting by frequency-dependent selection. This is the first study of the association of MHC variation and parasite burden in a free-ranging primate.     

Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta

The objective of this project was to better define the similarities and differences in gastrointestinal morphology present in lemur species. Measurements of the gastrointestinal tract of lemurs were obtained at necropsy from the captive population at Duke University Primate Center. Measurements of body length and weight, as well as gastrointestinal length, were recorded from five prosimian species: Propithecus tattersalli, Propithecus verreauxi, Varecia variegata, Hapalemur griseus, and Lemur catta. Photographs and measurements were used to obtain illustrations. Preliminary results suggest differences in gastrointestinal morphology among lemur species that coincide with differences in diet. Distinct sacculations in either the cecum or the colon were present for H. griseus, L. catta, P. verreauxi, and P. tattersalli, but not for V. variegata. The Propithecus specimens possessed a much greater ratio of gastrointestinal length to body length than the other three species. A short, blunt cecum and a shortened and sacculated colon were unique characteristics of the H. griseus specimens. These differences correlate well with a dietary shift from consumption of large amounts of structural plant cell wall (Propithecus sp.) to consumption of variable or moderate amounts (H. griseus, L. catta, and V. variegata). They also suggest that captive groups would benefit from further diet refinement in captivity.     

Characterization of 14 microsatellite marker loci in the grey bamboo lemur (Hapalemur griseus)

Fourteen nuclear microsatellite loci were isolated from a genomic DNA library derived from a free‐ranging bamboo lemur (Hapalemur griseus griseus) from Ranomafana National Park, Madagascar. Expected and observed heterozygosity levels were determined for populations of bamboo lemurs from Ranomafana National Park and a nonprotected area near Tsinjoarivo, Madagascar. Although genotype frequencies for all but one marker were within Hardy–Weinberg expectations for the Tsinjoarivo population, this was not the case for the Ranomafana samples. It is probable that the deviation of genotype frequencies from Hardy–Weinberg expectations in Ranomafana was precipitated by the presence of two taxa within the sample population.     

Relative efficiency of preferred and nonpreferred patterns of lateralized foraging in the gentle lemur (Hapalemur griseus)

Lateralized patterns of hand use in species-typical bamboo shoot foraging were evaluated for efficiency in five female and six male gentle lemurs (Hapalemur griseus sp.). Efficiency was defined as amount of time required to complete a foraging response sequence. The foraging pattern consisted of four component movements: PULL-IN, COUNTERFORCE, TURN, and FEED-IN. These component movements had been shown in a previous study to incorporate lateral hand biases that formed subsets of patterns that were characteristic for each gentle lemur. The duration of each foraging sequence was measured from the beginning of the first component to the initiation of the terminal component. Frequency of use scores were employed to divide the pattern sequences of each subject into preferred and nonpreferred categories. A within-subjects comparison of the mean durations of preferred patterns (M = 2.56 sec) with those of non- preferred patterns (M = 3.02 sec) found that preferred patterns were executed more rapidly, t(10) = 3.36, P = .007. A multiple regression showed that order of pattern preference accounted for 89% of the variance in mean duration of response time (R² = .89, P = .056). Thus, the use of preferred lateralized hand patterns resulted in more rapid bamboo shoot harvesting. Speed in foraging may be regarded as an adaptive strategy for a species that subsists on a high bulk, low nutrient density food such as bamboo. © 1995 Wiley-Liss, Inc.     

Social system of the Alaotran gentle lemur (Hapalemur griseus alaotrensis): genetic characterization of group composition and mating system

Group composition and mating system were investigated in wild Alaotran gentle lemurs (Hapalemur griseus alaotrensis) using genetic markers. These small-bodied herbivorous and cathemeral primates are endemic to the reed and papyrus beds around Lac Alaotra in Madagascar. They live in small groups in small, defended territories. Data were collected during the rainy seasons in 1996, 1997, and 1999, and include 99 individuals from 22 neighboring social groups and an additional 30 animals from other areas representing most of the geographic range. Animals were located by researchers canoeing in the marshes bordering the lake. After a group's size was determined by direct observation, all individuals were captured, marked, and released. During handling each individual was weighed and sexed, and hair samples for DNA extraction were collected. A 342 bp mtDNA control region sequence and 10 nuclear microsatellite loci provided multilocus genotypes that were used to assess pedigree relations and population structure. Alaotran gentle lemurs were found in groups of two to nine individuals (mean: 4.3), comprising one or two breeding females, their offspring, and one reproducing male. Solitary individuals of both sexes were encountered rarely. Breeding females were the permanent core of the social groups, whereas intergroup transfer of reproductive males was relatively frequent. Forty percent of all reproducing groups contained two breeding females, which were related to each other as closely as mother-daughter or full sisters. Parentage assessment revealed a variable mating system ranging from serial monogamy to polygyny within social groups. At least 8% of paternities involved extragroup males. Additional data on life history and reproduction are presented, and the social system of the Alaotran gentle lemur is discussed in the light of the new genetic findings.     

Molecular and cytogenetic evidence for cryptic speciation within a rare endemic Malagasy lemur, the Northern Sportive Lemur (Lepilemur septentrionalis)

Evolutionary relationships of different populations of the threatened malagasy lemur Lepilemur septentrionalis were assessed by sequence analysis of mitochondrial DNA (D-loop region and partial Cyt b gene). One hundred and fifty nine samples were collected from five main different localities in the northern part of Madagascar. We applied the phylogenetic species concept based on fixed diagnostic differences to determine the status of different geographical populations. No nucleotide site diagnoses Ankarana from Andrafiamena or Analamera. However, numerous fixed differences separate Sahafary from all other populations. These results were corroborated by phylogenetic trees. As previous cytogenetic studies, our molecular data suggest that two cryptic species of Lepilemur occur in the extreme north of Madagascar. This speciation is probably caused by chromosomal rearrangements in at least one of the evolutionary lineages. Our study comprises another striking example of how molecular genetic assay can detect phylogenetic discontinuities that are not reflected in traditional morphologically based taxonomies. Our study indicates that the Sahafary population is a hitherto undescribed endangered endemic species which urgently needs conservation efforts.