Pair-specific usage of sleeping sites and their implications for social organization in a nocturnal Malagasy primate, the Milne Edwards' sportive lemur (Lepilemur edwardsi)

Safe sleeping sites may be a limited resource crucial for survival. In order to investigate their potential significance for social organization in nocturnal primates, we analyzed the spatial distribution of daily sleeping sites, their characteristics, their usage, and sleeping group compositions in the nocturnal Milne Edwards' sportive lemur during a 6-month field study in the dry deciduous forest of northwestern Madagascar. Sexes did not differ either in body size or in body mass. Sleeping sites were used almost exclusively by adult male-female pairs. Individuals showed a high sleeping-site fidelity limited to 2-3 different sleeping sites in close vicinity during the whole study period. Most females showed a higher fidelity to one distinct sleeping site than their male partners. Sleeping groups consisted of one adult male and one adult female and remained stable in composition over the whole study period. Exclusive pair-specific usage of sleeping sites suggests sleeping site related territoriality of male-female pairs, perhaps influenced by inter- and intrasexual resource competition. Results give first insights into the distribution patterns and social organization of this species. They imply dispersed monogamy for the Milne Edwards' sportive lemur, with sleeping sites as a potentially restricted and defendable resource.     

Isolation of sixteen autosomal loci and a sex-linked polymorphic microsatellite locus from the Milne-Edwards' sportive lemur (Lepilemur edwardsi)

We isolated 21 microsatellites from the Milne-Edwards' sportive lemur, Lepilemur edwardsi. Eighteen microsatellite sequences possessed sufficient flanking DNA for primer design. Seventeen loci amplified and were found to be polymorphic displaying two to 17 alleles in 32 unrelated individuals from a population from the National Park of Ankarafantsika in northwest Madagascar. One locus (Led-12) was found to be sex linked located on the X chromosome and can be used to sex-type 40% of female L. edwardsi lemurs. These 17 loci were characterized to investigate family structure and the phylogeography of L. edwardsi.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Infanticide by a Male Milne-Edwards' Sportive Lemur (Lepilemur edwardsi) in Ampijoroa,NW-Madagascar

During a long-term field study on the behavioral ecology and communication of a population of the monogamous Milne-Edwards' sportive lemur (Lepilemur edwardsi) in NW-Madagascar, we recorded for the first time an infanticide in a nocturnal lemur. A male newcomer killed the infant of a female whose male partner had left her recently. Both the social-pathology and the sexual-selection hypotheses may explain infanticidal behavior in Lepilemur edwardsi.     

Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar

Thermoregulation, energetics and patterns of torpor in the pygmy mouse lemur, Microcebus myoxinus, were investigated under natural conditions of photoperiod and temperature in the Kirindy/CFPF Forest in western Madagascar. M. myoxinus entered torpor spontaneously during the cool dry season. Torpor only occurred on a daily basis and torpor bout duration was on average 9.6 h, and ranged from 4.6 h to 19.2 h. Metabolic rates during torpor were reduced to about 86% of the normothermic value. Minimum body temperature during daily torpor was 6.8 °C at an ambient temperature of 6.3 °C. Entry into torpor occurred randomly between 2000 and 0620 hours, whereas arousals from torpor were clustered around 1300 hours within a narrow time window of less than 4 h. Arousal from torpor was a two-step process with a first passive climb of body temperature to a mean of 27 °C, carried by the daily increase of ambient temperature when oxygen consumption remained more or less constant, followed by a second active increase of oxygen consumption to further raise the body temperature to normothermic values. In conclusion, daily body temperature rhythms in M. myoxinus further reduce the energetic costs of daily torpor seen in other species: they extend to unusually low body temperatures and consequently low metabolic rates in torpor, and they employ passive warming to reduce the energetic costs of arousal. Thus, these energy-conserving adaptations may represent an important energetic aid to the pygmy mouse lemur and help to promote their individual fitness. Accepted: 2 November 1999     

Evolutionary significance of the variation in acoustic communication of a cryptic nocturnal primate radiation (Microcebus spp.)

Acoustic phenotypic variation is of major importance for speciation and the evolution of species diversity. Whereas selective and stochastic forces shaping the acoustic divergence of signaling systems are well studied in insects, frogs, and birds, knowledge on the processes driving acoustic phenotypic evolution in mammals is limited. We quantified the acoustic variation of a call type exchanged during agonistic encounters across eight distinct species of the smallest‐bodied nocturnal primate radiation, the Malagasy mouse lemurs. The species live in two different habitats (dry forest vs. humid forest), differ in geographic distance to each other, and belong to four distinct phylogenetic clades within the genus. Genetically defined species were discriminated reliably on the phenotypic level based on their acoustic distinctiveness in a discriminant function analysis. Acoustic variation was explained by genetic distance, whereas differences in morphology, forest type, or geographic distance had no effect. The strong impact of genetics was supported by a correlation between acoustic and genetic distance and the high agreement in branching pattern between the acoustic and molecular phylogenetic trees. In sum, stochastic factors such as genetic drift best explained acoustic diversification in a social communication call of mouse lemurs.     

Sleeping site ecology in a rain-forest dwelling nocturnal lemur (Lepilemur mustelinus): implications for sociality and conservation

Suitable sleeping sites as potentially restricted resources are suggested to shape sociality in primates. We investigated sleeping site ecology of a rain-forest dwelling sportive lemur in eastern Madagascar for the first time. Using radiotelemetry, we characterized the type, quality and usage of sleeping sites as well as social sleeping habits of 11 focal individuals of the weasel sportive lemur (Lepilemur mustelinus) during the dry and the onset of the rainy season. Morphometric measurements provided additional information. The sexes showed an unusual sexual dimorphism for primates. Males and females did not differ in body length, but females surpassed males in body mass suggesting female dominance. Both sexes used dense vegetation and holes in hollow trees high above the ground as shelters for sleeping during the day. No sex difference in the quality of tree holes was found, but focal individuals used tree holes more often than open sleeping sites in dense vegetation. Both sexes showed high sleeping site fidelity limited to two to six different sites that they used primarily solitarily. The results imply that suitable sleeping sites are limited and survival of this species will strongly depend on the availability of mature rain forests with suitable hollow trees. Furthermore, these findings provide evidence of a solitary sleeping and ranging system in this rain-forest dwelling sportive lemur with suitable sleeping sites as defendable resources.     

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.     

Geographic variation in loud calls of sportive lemurs (Lepilemur ssp.) and their implications for conservation

Bioacoustical studies in nonhuman primates have shown that loud calls can be reliably used as a noninvasive diagnostic tool for discriminating cryptic taxa, for their monitoring in the field as well as for the reconstruction of their phylogeny. To date, it is unknown, whether loud calls can be used for these purposes in sportive lemurs, for which current genetic studies suggest the existence of at least 24 cryptic species. The aim of this study was to compare the structure of loud calls of populations of sportive lemurs to characterize informative acoustic traits for taxa discrimination and to establish a phylogenetic tree based on acoustic structure. We have based our study on Inter-River-Systems (IRSs) as operational taxonomic units. Samples were collected from nine different localities of four IRSs along a transect from northwestern to northern Madagascar. Two call types, the ouah and the high-pitched call, were present in almost all IRSs. Six temporal and eight spectral parameters were measured in 196 calls of the best quality given by 21 different males. Variation within and between IRSs was assessed by multivariate statistics. Loud calls differed significantly among the different IRSs. The IRSs varied most in spectral parameters, whereas temporal parameters were less variable. Phylogenetic analysis using parsimony yielded 11 out of 17 acoustic characters as phylogenetically informative. The acoustic tree had an average branch support of 78%. Its topology coincided less with geographic distances than with genetic tree topology. Altogether our findings revealed that loud calls separated geographically isolated populations of sportive lemurs specifically. Based on these results, noninvasive tools for diagnosis and monitoring of cryptic species in nature can be developed for conservation management.     

Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar

Understanding ecological niche evolution over evolutionary timescales is crucial to elucidating the biogeographic history of organisms. Here, we used, for the first time, climate‐based ecological niche models (ENMs) to test hypotheses about ecological divergence and speciation processes between sister species pairs of lemurs (genus Eulemur) in Madagascar. We produced ENMs for eight species, all of which had significant validation support. Among the four sister species pairs, we found nonequivalent niches between sisters, varying degrees of niche overlap in ecological and geographic space, and support for multiple divergence processes. Specifically, three sister‐pair comparisons supported the null model that niches are no more divergent than the available background region. These findings are consistent with an allopatric speciation model, and for two sister pairs (E. collaris–E. cinereiceps and E. rufus–E. rufifrons), a riverine barrier has been previously proposed for driving allopatric speciation. However, for the fourth sister pair E. flavifrons–E. macaco, we found support for significant niche divergence, and consistent with their parapatric distribution on an ecotone and the lack of obvious geographic barriers, these findings most strongly support a parapatric model of speciation. These analyses thus suggest that various speciation processes have led to diversification among closely related Eulemur species.     

Does nonnutritive tree gouging in a rainforest‐dwelling lemur convey resource ownership as does loud calling in a dry forest‐dwelling lemur?

Nonhuman primates may defend crucial resources using acoustic or chemical signals. When essential resources are limited, ownership display for a resource may be enhanced. Defending resources may depend on population density and habitat characteristics. Using the Milne Edwards' sportive lemurs (Lepilemur edwardsi) and weasel sportive lemurs (L. mustelinus) as models, we tested whether two cryptic nocturnal lemur species differing in population density and habitat show differences in their vocal and chemical communication for signaling ownership of resources. L. edwardsi inhabits a western dry deciduous forest in a high‐density population, whereas L. mustelinus is found in an eastern rainforest in low density. We followed ten L. edwardsi (six males and four females) and nine L. mustelinus (four males and five females) for 215 hr during the early evening (06:00–10:00 p.m.) and the early morning (02:00–05:00 a.m.) and recorded their behavior using focal animal sampling. We found that both species differed in their vocal and chemical communication. L. edwardsi was highly vocal and displayed loud calling in the mornings and evenings while feeding or in the vicinity of resting places. In contrast, L. mustelinus never vocalized during observations, but displayed tree‐gouging behavior that was never observed in L. edwardsi. Tree gouging occurred more often during early evening sessions than early morning sessions. Subjects gouged trees after leaving their sleeping hole and before moving around. We suggest that, in weasel sportive lemurs, non‐nutritive tree gouging is used as a scent‐marking behavior in order to display ownership of sleeping sites. Altogether, our findings provide first empirical evidence on the evolution of different communication systems in two cryptic nocturnal primate species contrasting in habitat quality and population density. Further investigations are needed to provide more insight into the underlying mechanisms. Am. J. Primatol. 72:1062–1072, 2010. © 2010 Wiley‐Liss, Inc.     

Attacks on a wild infant ring-tailed lemur (Lemur catta) by immigrant males at Berenty, Madagascar: interpreting infanticide by males

An orphaned infant ring-tailed lemur (Lemur catta) was attacked persistently by immigrant males and disappeared with severe wounds at Berenty Reserve, Madagascar. Prior to the attacks, two troop members disappeared. On 20 November 1998, the only resident male in Troop C2B disappeared suddenly. After the disappearance, nine males from three neighboring troops approached, but only six males continued to shadow the troop. Of the females, the one lactating female attacked the males the most frequently. On 21 January 1999, the lactating female disappeared and her infant was orphaned. Subsequently, five attacks on the infant by immigrant males were observed for five consecutive days from January 23 to 27. The aggression was persistent and specifically targeted the infant, suggesting that the attacks were purposeful aggression, rather than redirected or accidental aggression. The primary attacker was the most dominant of the immigrant males, and mated with females in the next mating season.     

Species‐level view of population structure and gene flow for a critically endangered primate (Varecia variegata)

Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remaining V. variegata range. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNA sequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of the Mangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNA haplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high average F_ST (0.247) and Φ_ST (0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.     

Female social dominance and basal metabolism in a malagasy primate,Propithecus verreauxi

Tight energetic constraints on reproductively active females are hypothesized to be an important determinant of the phenomenon of female dominance in Propithecus verreauxi, a primate endemic to Madagascar. Five wild sifakas were captured in the Beza Mahafaly Special Reserve in southern Madagascar, and resting metabolic rates (RMR) were measured. Levels were low, as predicted, with the exception of a possibly pregnant female.; Although the data were not conclusive, they were consistent with the hypothesis.     

Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: a comparison of the golden brown mouse lemur ( Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur ( Microcebus rufus) in Eastern Madagascar

To investigate for the first time the relationship between contrasting patterns of seasonal changes of the environment and activity, body mass and reproduction for small nocturnal primates in nature, we compared a population of golden brown mouse lemur (Microcebus ravelobensis) in a dry deciduous forest of northwestern Madagascar and of the brown mouse lemur (Microcebus rufus) in an evergreen rain forest of eastern Madagascar. Both species live under similar photoperiodic conditions. Golden brown mouse lemurs (GBML) were active during the whole period (May to December) irrespective of changing environmental conditions. In contrast, a part of the population of brown mouse lemurs (BML) showed prolonged seasonal torpor, related to body mass during periods of short day length and low ambient temperatures. Differences between species might be due to differences in ambient temperature and food supply. Body weight and tail thickness (adipose tissue reserve) did not show prominent differences between short and long photoperiods in GBML, whereas both differ significantly in BML, suggesting species-specific differences in the photoperiodically driven control of metabolism. Both species showed a seasonal reproduction. The rate of growth and size of the testes were similar and preceded estrous onset in both species suggesting a photoperiodic control of reproduction in males. The estrous onset in females occurred earlier in GBML than in BML. Estrous females were observed over at least 4 months in the former, but in only 1 month in the latter species. Intraspecific variation of estrous onset in GBML may be explained by body mass. Interspecific variation of female reproduction indicates species-specific differences in the control of reproduction. Thus, environmentally related differences in annual rhythms between closely related small nocturnal lemurs emerged that allow them to cope with contrasting patterns of seasonal changes in their habitats.     

Characterization of 20 microsatellite marker loci in the red‐bellied brown lemur (Eulemur rubriventer)

Twenty nuclear microsatellite loci were isolated from a genomic DNA library derived from a free‐ranging red‐bellied brown lemur (Eulemur rubriventer), from the Ranomafana National Park, Madagascar. Population genetic parameters were estimated as baseline values from samples collected from populations harboured in the Ranomafana and Andringitra National Parks. The marker suite will be used in a future study on the population dynamics of this species.     

Distribution and morphological characters of intermediate forms between the black lemur (Eulemur macaco macaco) and the Sclater's lemur (E. m. flavifrons)

A study of intermediate forms betweenEulemur macaco macaco andE. m. flavifrons was performed on animals in different areas located to the north, south, and east of the known limits of distribution in Maromandia. A large hybridization zone was defined and morphological and dermatoglyphic comparisons were done on the different animals.