Woolly Lemur Research Articles

Depth of Edge Influence in a Madagascar Lowland Rainforest and Its Effects on Lemurs’ Abundance

Edge effects result from interactions between adjacent habitats, which can modify abiotic and biotic conditions and produce various negative effects on biodiversity. Given the high degree of forest fragmentation in Madagascar, understanding lemur responses to edges is a conservation priority. We aim to determine the depth of edge influence in a continuous low-land rainforest of south-eastern Madagascar and identify the response of six lemur species. We surveyed lemur abundance along nine 1 km transects from May 2015 to July 2016 totaling 112.2 km of survey effort during the day and 88.5 km at night. We characterized the habitat structure via 33 plots centered along the line transects. We used Generalized Additive Models and Generalized Linear Models to test the effect of distance from the forest edge on vegetation parameters and animal encounter rates. Edge effect on the vegetation structure can be detected up to around 100 m in terms of tree diversity and density. We found a negative edge response for Madame Fleurette’s sportive lemurs (Lepilemur fleuretae) and collared brown lemurs (Eulemur collaris), and a positive edge response for Anosy mouse lemurs (Microcebus tanosi), Southern bamboo lemurs (Hapalemur meridionalis) and Southern woolly lemurs (Avahi meridionalis). Since around half of the forested areas in Madagascar are within 100 m of forest edge, taking into account edge effect is vital when producing estimates of population sizes and informing conservation management.

Are sleeping site ecology and season linked to intestinal helminth prevalence and diversity in two sympatric, nocturnal and arboreal primate hosts (Lepilemur edwardsi and Avahi occidentalis)?

BackgroundVarious factors, such as climate, body size and sociality are often linked to parasitism. This constrains the identification of other determinants driving parasite infections. Here, we investigate for the first time intestinal parasites in two sympatric arboreal primate species, which share similar activity patterns, feeding ecology, body size and sociality, and cope with the same climate conditions, but differ in sleeping site ecology: the Milne-Edward’s sportive lemur (Lepilemur edwardsi) and the Western woolly lemur (Avahi occidentalis). Comparison of these two species aimed to test whether differences in sleeping sites are related to differences in parasite infection patterns. Additionally, gender and seasonal factors were taken into account. Animals were radio-collared to record their sleeping site dynamics and to collect fecal samples to assess intestinal parasitism during both the dry and the rainy season.ResultsOnly low parasite diversity was detected, which is attributable to the strict arboreal lifestyle of these lemurs, limiting their contact with infective parasite stages. L. edwardsi, which sleeps in tree holes and repeatedly uses the same sleeping site, excreted eggs of strongyle and oxyurid nematodes, whereby strongyles always occurred in coinfection with oxyurids. In contrast, A. occidentalis, which sleeps on open branches and frequently changes sleeping sites, only excreted eggs of strongyle nematodes. This difference can be attributed to a potential favorable environment presented by tree holes for infective stages, facilitating parasitic transmission. Additionally, Strongylida in A. occidentalis were only observed in the rainy season, suggesting an arrested development during the dry season in the nematodes’ life cycle. Males and females of both lemur species showed the same frequency of parasitism. No differences in body mass of infected and non-infected individuals were observed, indicating that the animals’ body condition remains unaffected by the detected gastrointestinal parasites.ConclusionsThe comparison of two primate hosts with a very similar lifestyle suggests an influence of the sleeping site ecology on intestinal parasites. In A. occidentalis there was a clear seasonal difference in strongyle egg excretion. These results improve our understanding of the parasite ecology in these endangered primate species, which may be critical in the light of species conservation.

Sleeping site ecology, but not sex, affect ecto- and hemoparasite risk, in sympatric, arboreal primates (Avahi occidentalis and Lepilemur edwardsi)

BackgroundA central question in evolutionary parasitology is to what extent ecology impacts patterns of parasitism in wild host populations. In this study, we aim to disentangle factors influencing the risk of parasite exposure by exploring the impact of sleeping site ecology on infection with ectoparasites and vector-borne hemoparasites in two sympatric primates endemic to Madagascar. Both species live in the same dry deciduous forest of northwestern Madagascar and cope with the same climatic constraints, they are arboreal, nocturnal, cat-sized and pair-living but differ prominently in sleeping site ecology. The Western woolly lemur (Avahi occidentalis) sleeps on open branches and frequently changes sleeping sites, whereas the Milne-Edward’s sportive lemur (Lepilemur edwardsi) uses tree holes, displaying strong sleeping site fidelity. Sleeping in tree holes should confer protection from mosquito-borne hemoparasites, but should enhance the risk for ectoparasite infestation with mites and nest-adapted ticks. Sex may affect parasite risk in both species comparably, with males bearing a higher risk than females due to an immunosuppressive effect of higher testosterone levels in males or to sex-specific behavior. To explore these hypotheses, ectoparasites and blood samples were collected from 22 individuals of A. occidentalis and 26 individuals of L. edwardsi during the dry and rainy season.ResultsL. edwardsi, but not A. occidentalis, harbored ectoparasites, namely ticks (Haemaphysalis lemuris [Ixodidae], Ornithodoros sp. [Argasidae]) and mites (Aetholaelaps trilyssa, [Laelapidae]), suggesting that sleeping in tree holes promotes infestation with ectoparasites. Interestingly, ectoparasites were found solely in the hot, rainy season with a prevalence of 75% (N = 16 animals). Blood smears were screened for the presence and infection intensity of hemoparasites. Microfilariae were detected in both species. Morphological characteristics suggested that each lemur species harbored two different filarial species. Prevalence of microfilarial infection was significantly lower in L. edwardsi than in A. occidentalis. No significant difference in infection intensity between the two host species, and no effect of season, daytime of sampling or sex on prevalence or infection intensity was found. In neither host species, parasite infection showed an influence on body weight as an indicator for body condition.ConclusionsOur findings support that sleeping site ecology affects ectoparasite infestation in nocturnal, arboreal mammalian hosts in the tropics, whereas there is no significant effect of host sex. The influence of sleeping site ecology to vector-borne hemoparasite risk is less pronounced. The observed parasite infections did not affect body condition and thus may be of minor importance for shaping reproductive fitness. Findings provide first evidence for the specific relevance of sleeping site ecology on parasitism in arboreal and social mammals. Further, our results increase the sparse knowledge on ecological drivers of primate host-parasite interactions and transmission pathways in natural tropical environments.

Feeding Patterns and Dietary Profile of Nocturnal Southern Woolly Lemurs (Avahi meridionalis) in Southeast Madagascar

Folivory has evolved in all primate radiations but the relative importance of resource quantity and nutritional quality of food is controversial. To understand how food abundance and different nutrients affect a folivorous diet, we investigated food composition of the leaf-eating lemur Avahi meridionalis. From June to December 2004, we conducted 26 nights of focal observation (256.1 h) in Sainte Luce pluvial littoral forest (southeast Madagascar) and recorded feeding behavior of 4 radiocollared individuals. Within the subjects’ home ranges, we recorded vegetation characteristics (morphospecies, phenology, diameter at breast height) and sampled food and nonfood items for chemical analyses. A. meridionalis did not eat fruit but only leaves and flowers and did not base their choice on food abundance. Adult leaves eaten were higher in easily soluble protein than adult leaves that were not consumed. The subjects ate young leaves and flowers as soon as they became available. These young leaves contained the same concentrations of soluble protein, higher concentrations of crude protein, and lower concentrations of acid detergent fiber and sugar than mature food leaves. A. meridionalis ate leaves with condensed tannins, alkaloids, and intermediate concentrations of polyphenolics. Contrary to previous studies that considered Avahi spp. a specialist, A. meridionalis acted as leaf-eating generalists with moderate selectivity, based on nutritional quality and tolerance of a wide array of plant secondary metabolites. This illustrates the dietary flexibility within a single genus of primates that seems to be driven by environmental constraints rather than morphological or physiological adaptations.

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.

Conservation Assessment of the Recently Described John Cleese's Woolly Lemur, Avahi cleesei (Lemuriformes, Indridae)

Abstract John Cleese's woolly lemur (Avahi cleesei) was discovered in 1990 and officially defined and named in 2005. This nocturnal lemur is known to occur only in the Tsingy de Bemaraha Strict Nature Reserve, a UNESCO World Heritage Site in central western Madagascar. In this article we summarize available relevant information on morphology, distribution, habitat, and behavior including vocalizations to assess the conservation status and facilitate future investigations, surveys in particular. According to the IUCN Red List categories, A. cleesei is clearly in the category Endangered. Further studies might show, however, that the species should be classified as Critically Endangered, because of its very limited distribution and particularly specialized biological requirements.

New species of woolly lemurAvahi (primates: lemuriformes) in Bemaraha (Central Western Madagascar)

There are at least three distinct taxa of woolly lemurs (genus Avahi) in western Madagascar. The range of Avahi occidentalis extends north and east of the Betsiboka River to the Bay of Narinda. Avahi unicolor occurs well to the north, including the Ampasindava peninsula and the Manongarivo Special Reserve. Here we describe a third Avahi population in central western Madagascar, which was discovered in the Bemaraha Strict Nature Reserve in the Tsingy de Bemaraha region, north of the Manambolo River. The description is based on a released type individual from which we obtained hair samples, photographs, and tape and video recordings. Its entire range is believed to be less than 5,000 km(2), and forest loss, along with an observed continuing decline in numbers, indicates that this species should be considered Endangered or even Critically Endangered, according to the Red List criteria of the World Conservation Union-IUCN.

Characterization of 22 microsatellite loci developed from the genome of the Woolly Lemur (Avahi laniger)

AbstractTwenty‐two polymorphic microsatellite loci were isolated and characterized from the Avahi laniger genome. All were polymorphic in both the Eastern Woolly Lemur (A. laniger) and the Western Woolly Lemur (A. occidentalis). One locus, WOOL157, harboured allele structures that were species‐specific. This marker suite will be used in future studies to establish the ranges and population structures of the two Avahi species on the island of Madagascar.

Distribution and Geographic Variation in the Western Woolly Lemur (Avahi occidentalis) with Description of a New Species (A. unicolor)

The western woolly lemur is distributed through central western, northwestern and possibly northern Madagascar and is traditionally viewed as a monotypic species (Avahi occidentalis) or as a subspecies of A. laniger. We present new data on body weights of Avahi which, together with previously available body weights, provide additional evidence for recognizing eastern and western woolly lemurs as two distinct species. We then reexamine the distributions of, and chromatic variation within and between, populations of western woolly lemurs. A comparative study of wild subjects and museum skins reveals that several geographically discrete morphs exist in western Avahi, which is clearly polytypic. Marked differences between populations in fur coloration suggest that ≥3 distinct taxa should be recognized. The populations differ considerably in their habitat structure. In addition, field observations suggest clear differences in population density between ≥2 of the populations. We describe and name one new species.