The study of sleeping site selection in primates is fundamental to the development of appropriate conservation strategies. Here we present data on the characteristics and usage of sleeping sites of the northern sportive lemurs (Lepilemur septentrionalis) at Montagne des Français, Madagascar. The study was conducted on three individuals over a period of seven months from December 2018 to June 2019. The research objective is to describe the sleeping site characteristics and usage patterns of L. septentrionalis in the dry forest of Montagne des Français. The northern sportive lemurs in this study used three types of sleeping sites: tree holes, vine tangles, and branches. Among the tree species used as sleeping sites by L. septentrionalis, Strychnos madagascariensis was used most frequently, and most of these sleeping sites were food trees. We most often observed L. septentrionalis using tall trees with large diameters at breast height. Tree holes are generally found in living trees rather than in dead or partially dead trees. We observed a significant difference in the frequency of sleeping sites reuse, with repeated use of tree holes being particularly noticeable. There is no variation in distance between the different types of sleeping sites and the first or last feeding trees. The results of this study suggest that L. septentrionalis depends primarily on large trees with tree holes. The reuse of sleeping sites may serve as a strategy for predator avoidance or for easy access to food resources, while the use of food trees as sleeping sites may be a strategy to reduce the cost of travel to access food resources. Sampling efforts must be considered to better understand the sleeping sites selection preferences of this species.
Aye-ayes possess an unusual suite of morphological characteristics that are used to locate and extract xylophagous invertebrates. A growing body of evidence supports the long-held claim that xylophagous invertebrates comprise a significant portion of aye-aye diets; however, several aye-aye features are also used to harvest endosperm from seeds of Canarium spp., another important aye-aye resource. Using continuous focal animal sampling, we collected feeding data on a female aye-aye in Madagascar's Ihofa Forest from January 2016 to December 2017 to better elucidate resource preference. We used aye-aye feeding traces in woody substrates as a proxy for xylophagous invertebrate presence to estimate xylophagous invertebrate abundance along 20 transects (10 m × 100 m). During observational follows, we also counted each trace made during feeding. Using the same transects, we also estimated Canarium seed abundance based on fruit in the canopy and fruit on the ground. There were more aye-aye feeding traces in woody substrates for xylophagous invertebrates (3206) than for Canarium seeds (2153). A Wilcoxon signed-rank test found no significant difference in the number of xylophagous invertebrates and Canarium seeds consumed during this study ( p = 0.317); however, a two-item preference index indicated that xylophagous invertebrates were the preferred resource monthly and annually. Our results indicated that the aye-aye in this study preferentially consumed xylophagous invertebrates. This provides further evidence that the aye-aye's highly derived morphology is specifically adapted for extracting insect larvae from structurally defended substrates. The use of some of these morphological autapomorphies for Canarium seed feeding may be an example of an exaptation.
Food transfer occurs when part or all of a food item is passed from one individual to another. Adult transfer of solid food to infants has been reported in 45 primate species. For aye-ayes, this behaviour was recorded in captivity where individuals were provisioned, but little is known about this behaviour in the wild. Wild aye-ayes consume hard-to-process foods that are inaccessible to infants such as wood-boring larvae embedded in trees and the endosperm of Canarium spp. seeds which are protected by a hard coat. Learning to process these food resources may be essential for aye-aye development. We used ad libitum sampling to record the social activities and behaviours of a mother and her male infant from January to December 2020 in Sangasanga Forest, Kianjavato, Madagascar. We collected in total 4 hours 57 minutes and 57 seconds of social behaviours. Over two days in December, we observed eight occurrences of the 11-month-old infant usurping Canarium sp. seeds from his mother. Our findings suggest that, due to physical limitations, the infant aye-aye primarily resorted to food transfer via theft to obtain hard-to-process food. Transfer of larvae, their main resource, was not observed, though it may occur until young aye-aye have the bite force needed to gouge holes in substrates and the coordination to retrieve and extract wood-boring larvae. Future research should explore if food transfer differs across individuals' sex, sites and type of food as well as the effects of anthropogenic disturbances on foraging.
studied an adult female and a juvenile male aye-aye (Daubentonia madagascariensis) in Madagascar's Ihofa forest from May to December 2017 to investigate whether the postural diversity of this lemur varied with age, maintenance activity, and habitat use. We used bout sampling (female N = 488, male N = 355) to record postures during feeding and resting and tested for differences using chi 2. For both individuals, bimanual and unimanual cling were the most common postures used during feeding (78.4% and 82.9%) and these behaviors were strongly associated with the use of vertical supports-trunks and bamboo-in the main canopy. When feeding on branches and boughs, pronograde postures such as tri-pedal crouch and crouch were most common. Most rest occurred on horizontal branches using primarily pronograde postures. Our data indicate that although aye-ayes exploit multiple forest strata, the great majority of feeding is accomplished using orthograde postures from vertical supports, even in forest strata dominated by horizontal supports. These findings support recent arguments about the significance of vertically oriented behaviors in the evolution of early mammalian arboreal quadrupeds.
The concept of “facilitated restoration” aims at native biodiversity reinstatement with the help of animal seed dispersers attracted by fruiting trees. Yet, large-crowned trees will have to develop in the early stages of restoration; therefore, seed dispersal provided by small generalist mammals and birds that use rapidly growing herbs, shrubs, and small trees at early stages of forest succession would accelerate biodiversity restoration. Due to the elusive lifestyle of these small animals, it is unclear what species can contribute to the early stages of this process. Using the primate genus Microcebus (adult body mass about 60 g) as an example, we illustrate that these small generalists are possible seed dispersers in the early stages of forest restoration, not yet used by larger frugivores. We show that Microcebus spp. dispersed more seeds from herbs, shrubs, and small trees than large frugivorous primate species. These plants tend to have smaller seeds than large tree species and are often pioneer species not considered in forest restoration projects. Facilitating the colonization of restoration plots by generalist small seed dispersers that use shrubby habitats may improve plant diversity by adding a more natural sequence of successional stages towards mature forests in Madagascar and elsewhere in the tropics.
La perte d’habitat due à l’activité humaine est une menace qui affecte tous les primates à Madagascar. Les lémuriens, primates arboricoles, ont des réponses variées face au changement de leur habitat. La présente recherche vise à déterminer le lien entre la dégradation forestière, la masse et les caractères morphologiques des lémuriens nocturnes de Menabe Sud : Lepilemur ruficaudatus et Microcebus murinus. L’étude a été effectuée dans cinq sites dont deux sites sont des forêts primaires et trois autres sont des forêts perturbées. La capture et la mesure des caractères morphologiques des lémuriens ont été réalisées entre novembre et décembre 2014, puis entre juillet et septembre 2015. Des parcelles botaniques (5m x 5m) ont été utilisées pour décrire les caractéristiques des sites dont l’abondance des arbres, le diamètre à hauteur de poitrine ou la hauteur et le diamètre de la couronne. La masse de M. murinus n’était pas influencée par la saison de capture (P > 0,05), mais elle variait avec le sexe (P < 0,005) et le site (P < 0,001). Tous les caractères morphologiques de M. murinus dans les deux forêts primaires étaient similaires (P > 0,05). Par contre, dans les forêts perturbées, les femelles de M. murinus étaient plus lourdes et avaient des corps plus longs que les mâles (P < 0,05). La masse et la longueur du corps de L. ruficaudatus entre les différents sites étaient similaires (P > 0,05). Comparé à L. ruficaudatus, M. murinus répondrait advantage à la dégradation forestière. Comprendre l’étendue de la réponse morphologique des lémuriens face à la dégradation de leur habitat pourrait être utilisé comme outil pour prioriser leur conservation. English Abstract Forest structure effects primate morphology because it determines the availability and characteristics of resources, such as substrates for locomotion, sleeping trees, and trees food. However, forest degradation may alter environmental condition of habitats and influence lemur behavior and morphology. We evaluated the links between forest degradation, lemur body mass, and lemur morphometric. We surveyed red-tailed sportive lemurs (Lepilemur ruficaudatus) and gray mouse lemurs (Microcebus murinus) in the dry, deciduous forest of southern Menabe, Morondava, Madagascar. The study was conducted in the dry season in 2014 (November–December) and 2015 (July– September). Lemur captures were conducted in five forest sites: two primary forest and three disturbed forest. Sherman and Tomahawk style traps were used to capture mouse lemurs. We conducted three capture sessions in site B in 2014 and three capture sessions for each site in 2015, for a total of 5616 night traps. During each capture session, 80 Sherman traps and 24 Tomahawk traps were installed for three consecutive nights. To capture the red-tailed sportive lemur, we used a gun (Dan Inject Model JM air rifle) with a tranquillizer dart to immobilize the animal. We collected morphometric measurements from 232 mouse lemurs and 31 red-tailed sportive lemurs. Botanic plots (5m x 5m) allowed us to characterize the forest characteristics: tree diameter at breast height (DBH), tree height, tree abundance, tree crown height and diameter. Tree abundance with DBH ≥ 5 cm and trees diversity varied significantly between sites (P < 0.001). Mouse lemur body mass did not vary with seasonality of the capture (P > 0.05). For mouse lemurs, all morphometric from two populations in the pristine forest were similar (P > 0.05). Mouse lemurs in one disturbed habitat had greater body length and body mass than mouse lemurs in the pristine forest (P < 0.05). The difference may be linked with fruit abundance of two trees species (Tamarindus indica and Ziziphus mauritiana) and more insect availability in the disturbed site. In the altered habitat, mouse lemur females had longest body size and heavier than males (P < 0.05). Red-tailed sportive lemur body mass and length did not change between sites (P > 0.05). Our study is consistent with the hypothesis that lemur morphometric and body mass may change with forest degradation in southern forest of Menabe. Additionally, the range of the response varies between species and sex: mouse lemurs had a wider reaction norm to the habitat disturbance than did red-tailed sportive lemurs. Mouse lemurs may have higher ecological flexibility and tolerance for forest changes, specifically the alteration of forest habitats. Understanding how lemur morphology responds to habitat disturbance may be used as a tool to prioritize lemur conservation.
Forest loss and degradation due to land cover changes imperil biodiversity worldwide. Subtropical and tropical ecosystems experience high deforestation rates, negatively affecting species like primates. Madagascar's endemic lemurs face exceptionally high risks of population declines and extirpation. We examined how short-term land cover changes within a fragmented landscape in southeastern Madagascar impacted the density of lemur species. Using line transects, we assessed density changes in nine lemur species across five forest fragments. Diurnal surveys were conducted monthly from 2015 to 2019 on 35 transects (total effort = 1268 km). Additionally, 21 transects were surveyed nocturnally in 2015 and 2016 (total effort = 107.5 km). To quantify forest cover changes, we generated land use/land cover (LULC) maps from Sentinel-2 imagery using supervised classification for each year. For the LULC maps, we overlayed species-specific buffers around all transects and calculated the proportion of land cover classes within them. We observed declines in the annual densities of four diurnal and cathemeral lemur species between 2015 and 2019, with species-specific declines of up to 80% (Varecia variegata). While the density of two nocturnal species decreased, one increased fivefold (Cheirogaleus major) between 2015 and 2016. By 2019, Grassland was the dominant land type (50%), while Paddy Fields had the smallest coverage (1.03%). Mature Agricultural Land increased the most (63.37%), while New Agricultural Land decreased the most (-66.36%). Unexpectedly, we did not find evidence that higher forest cover supported a higher lemur population density within sampled areas, but we found support for the negative impact of degraded land cover types on three lemur species. Our study underscores the urgent need to address land-use changes and their repercussions for primate populations in tropical ecosystems. The diverse responses of lemur species to modified habitats highlight the complexity of these impacts and emphasize the importance of targeted conservation efforts.
The mode of reproduction most often seen in snakes is sexual, but studies have noted facultative parthenogenesis in at least six families. Here, we provide evidence for the first observed case of facultative parthenogenesis in a captive Jamaican boa (Chilabothrus subflavus). A 7-year-old female Jamaican boa, isolated since birth, was found to have produced a litter of 15 offspring. To provide molecular DNA evidence of parthenogenesis, 13 new microsatellite loci were isolated in the species. All offspring were found to be homozygous at each locus and only possess alleles found in the dam, implicating that they were born from asexual reproduction. Several developmental abnormalities, including stillbirths and spinal deformities, were noted in the litter which may be explained by their increased level of homozygosity. To preserve genetic diversity in the captive population, research should be conducted to understand the prevalence of this mode of reproduction and to guide future management decisions of this IUCN listed Vulnerable species.
Global biodiversity is under accelerating threats, and species are succumbing to extinction before being described. Madagascar’s biota represents an extreme example of this scenario, with the added complication that much of its endemic biodiversity is cryptic. Here we illustrate best practices for clarifying cryptic diversification processes by presenting an integrative framework that leverages multiple lines of evidence and taxon-informed cut-offs for species delimitation, while placing special emphasis on identifying patterns of isolation by distance. We systematically apply this framework to an entire taxonomically controversial primate clade, the mouse lemurs (genus Microcebus, family Cheirogaleidae). We demonstrate that species diversity has been overestimated primarily due to the interpretation of geographic variation as speciation, potentially biasing inference of the underlying processes of evolutionary diversification. Following a revised classification, we find that crypsis within the genus is best explained by a model of morphological stasis imposed by stabilizing selection and a neutral process of niche diversification. Finally, by clarifying species limits and defining evolutionarily significant units, we provide new conservation priorities, bridging fundamental and applied objectives in a generalizable framework. A spatial taxonomic framework integrating genomic, morphological, ecological, life history and acoustic data is used to clarify the cryptic evolution of the taxonomically controversial mouse lemur complex, with a view to aiding future conservation of this and other similarly cryptic clades.
The degree of dietary flexibility in primates is species specific; some incorporate a wider array of resources than others. Extreme interannual weather variability in Madagascar results in seasonal resource scarcity which has been linked to specialized behaviors in lemurs. Prolemur simus , for example, has been considered an obligate specialist on large culm bamboo with >60% of its diet composed of woody bamboos requiring morphological and physiological adaptations to process. Recent studies reported an ever-expanding list of dietary items, suggesting that this species may not be an obligate specialist. However, long-term quantitative feeding data are unavailable across this species’ range. To explore the dietary flexibility of P. simus , we collected data at two northern sites, Ambalafary and Sahavola, and one southern site, Vatovavy, from September 2010 to January 2016 and May 2017 to September 2018, respectively. In total, we recorded 4022 h of behavioral data using instantaneous sampling of adult males and females from one group in Ambalafary, and two groups each in Sahavola and Vatovavy. We recorded 45 plant species eaten by P. simus over 7 years. We also observed significant differences in seasonal dietary composition between study sites. In Ambalafary, bamboo was the most frequently observed resource consumed (92.2%); however, non-bamboo resources comprised nearly one-third of the diet of P. simus in Sahavola and over 60% in Vatovavy. Consumption of all bamboo resources increased during the dry season at Ambalafary and during the wet season at Vatovavy, but never exceeded non-bamboo feeding at the latter. Culm pith feeding was only observed at Ambalafary, where it was more common during the dry season. We identify P. simus as a bamboo facultative specialist capable of adjusting its feeding behavior to its environment, indicating greater dietary flexibility than previously documented, which may enable the species to survive in increasingly degraded habitats.
Abstract Conservation funding is currently limited; cost‐effective conservation solutions are essential. We suggest that the thousands of field stations worldwide can play key roles at the frontline of biodiversity conservation and have high intrinsic value. We assessed field stations’ conservation return on investment and explored the impact of COVID‐19. We surveyed leaders of field stations across tropical regions that host primate research; 157 field stations in 56 countries responded. Respondents reported improved habitat quality and reduced hunting rates at over 80% of field stations and lower operational costs per km2 than protected areas, yet half of those surveyed have less funding now than in 2019. Spatial analyses support field station presence as reducing deforestation. These “earth observatories” provide a high return on investment; we advocate for increased support of field station programs and for governments to support their vital conservation efforts by investing accordingly.
Madagascar exhibits exceptionally high levels of biodiversity and endemism. Models to explain the diversification and distribution of species in Madagascar stress the importance of historical variability in climate conditions which may have led to the formation of geographic barriers by changing water and habitat availability. The relative importance of these models for the diversification of the various forest-adapted taxa of Madagascar has yet to be understood. Here, we reconstructed the phylogeographic history of Gerp's mouse lemur (Microcebus gerpi) to identify relevant mechanisms and drivers of diversification in Madagascar's humid rainforests. We used restriction site associated DNA (RAD) markers and applied population genomic and coalescent-based techniques to estimate genetic diversity, population structure, gene flow and divergence times among M. gerpi populations and its two sister species M. jollyae and M. marohita. Genomic results were complemented with ecological niche models to better understand the relative barrier function of rivers and altitude. We show that M. gerpi diversified during the late Pleistocene. The inferred ecological niche, patterns of gene flow and genetic differentiation in M. gerpi suggest that the potential for rivers to act as biogeographic barriers depended on both size and elevation of headwaters. Populations on opposite sides of the largest river in the area with headwaters that extend far into the highlands show particularly high genetic differentiation, whereas rivers with lower elevation headwaters have weaker barrier functions, indicated by higher migration rates and admixture. We conclude that M. gerpi likely diversified through repeated cycles of dispersal punctuated by isolation to refugia as a result of paleoclimatic fluctuations during the Pleistocene. We argue that this diversification scenario serves as a model of diversification for other rainforest taxa that are similarly limited by geographic factors. In addition, we highlight conservation implications for this critically endangered species, which faces extreme habitat loss and fragmentation.
Based on sequences of three mitochondrial and two nuclear-encoded genes, we examine genetic variation in the leaf tailed geckos Uroplatus sameiti and U. sikorae, and morphological and chromatic characteristics of the genetic clusters identified. The mitochondrial phylogeny reveals a puzzling diversity of 16 deep lineages (4 in U. sameiti and 12 in U. siko- rae) differing by 2.9-9.9% uncorrected pairwise distance in a fragment of the 16S rRNA gene. Populations from Analalava in the North and Zahamena in the Northern Central East form two mitochondrial lineages clustering with U. sameiti but being deeply divergent (>8% 16S distance); however, no information on their morphology is available. In U. sikorae, the mitochondrial lineages identified form several major geographic clades, two of which (from the northernmost and south- ernmost populations, respectively) received substantial support in the phylogenetic analysis. No instance of sympatry of two or more mitochondrial lineages was observed, precluding an unambiguous assessment of species status under the bio- logical species criterion without experimental approaches or detailed hybrid zone analyses. In the fragment of the nuclear encoded gene SACS we observed haplotype sharing between species and mitochondrial lineages, while in the fragment of KIAA1239 no haplotype sharing was detected although neither species nor mitochondrial lineages formed coherent phylo- groups in the respective network A screening of colour patterns from live photos, partly of the genotyped individuals, confirmed a large variation within species and populations, with a possible sexual dichromatism where a longitudinally striped phenotype is restricted to males. All individuals from populations of the U. sikorae clade from the Southern Central East and South East had an unpigmented oral mucosa just like U. sameiti, while all other U. sikorae populations are char- acterized by a black oral mucosa pigmentation. The extremely strong phylogeographic structure in the U. sikorae complex without obvious species-level divergences is unprecedented for large-sized squamates in Madagascar and calls for further taxonomic scrutiny using phylogenomic approaches; and it exemplifies how the loss of any major block of the remain- ing rainforests in Madagascar will inevitably lead to a substantial loss of genetic diversity - even if often intraspecific - in rainforest-specialized species.
Objectives: The investigation of morphological variation in animals is widely used in taxonomy, ecology, and evolution. Using large datasets for meta-analyses has dramatically increased, raising concerns about dataset compatibilities and biases introduced by contributions of multiple researchers.Materials and Methods: We compiled morphological data on 13 variables for 3073 individual mouse lemurs (Cheirogaleidae, Microcebus spp.) from 25 taxa and 153 different sampling locations, measured by 48 different researchers. We introduced and applied a filtering pipeline and quantified improvements in data quality (Shapiro-Francia statistic, skewness, and excess kurtosis). The filtered dataset was then used to test for genus-wide sexual size dimorphism and the applicability of Rensch's, Allen's, and Bergmann's rules.Results: Our pipeline reduced inter-observer bias (i.e., increased normality of data distributions). Inter-observer reliability of measurements was notably variable, highlighting the need to reduce data collection biases. Although subtle, we found a consistent pattern of sexual size dimorphism across Microcebus, with females being the larger (but not heavier) sex. Sexual size dimorphism was isometric, providing no support for Rensch's rule. Variations in tail length but not in ear size were consistent with the predictions of Allen's rule. Body mass and length followed a pattern contrary to predictions of Bergmann's rule.Discussion: We highlighted the usefulness of large multi-researcher datasets for testing ecological hypotheses after correcting for inter-observer biases. Using genus-wide tests, we outlined generalizable patterns of morphological variability across all mouse lemurs. This new methodological toolkit aims to facilitate future large-scale morphological comparisons for a wide range of taxa and applications.
Forest fragmentation may lead to substantial declines in food availability for primary consumers, especially presenting a challenge for frugivores, such as the Critically Endangered black-and-white ruffed lemur (Varecia variegata). We investigated how forest fragmentation impacts the diet and activity budgets of V. variegata across three forest fragments—71 ha, 232 ha, and 597 ha—in Kianjavato, Madagascar. We collected phenological and lemur behavioural data over 17 months. We found that in both small fragments (< 500 ha), there was lower tree basal area, tree species diversity, and availability of fruit from large tree species compared to the largest fragment. Despite overall lower fruit availability, we found that individuals in the smallest forest maintained a high degree of frugivory year-round but had high measures of dietary diversity. In contrast, individuals in the other small-fragment consumed large proportions of flowers seasonally and showed low dietary diversity. These individuals consumed nectar from the traveller’s tree (Ravenala sp.) for more than 40
Madagascar's Central Highlands are largely composed of grasslands, interspersed with patches of forest. The historical perspective was that Madagascar's grasslands had anthropogenic origins, but emerging evidence suggests that grasslands were a component of the pre-human Central Highlands vegetation. Consequently, there is now vigorous debate regarding the extent to which these grasslands have expanded due to anthropogenic pressures. Here, we shed light on the temporal dynamics of Madagascar's vegetative composition by conducting a population genomic investigation of Goodman's mouse lemur (Microcebus lehilahytsara; Cheirogaleidae). These small-bodied primates occur both in Madagascar's eastern rainforests and in the Central Highlands, making them a valuable indicator species. Population divergences among forest-dwelling mammals will reflect changes to their habitat, including fragmentation, whereas patterns of post-divergence gene flow can reveal formerly wooded migration corridors. To explore these patterns, we used RADseq data to infer population genetic structure, demographic models of post-divergence gene flow, and population size change through time. The results offer evidence that open habitats are an ancient component of the Central Highlands, and that widespread forest fragmentation occurred naturally during a period of decreased precipitation near the last glacial maximum. Models of gene flow suggest that migration across the Central Highlands has been possible from the Pleistocene through the recent Holocene via riparian corridors. Though our findings support the hypothesis that Central Highland grasslands predate human arrival, we also find evidence for human-mediated population declines. This highlights the extent to which species imminently threatened by human-mediated deforestation may already be vulnerable from paleoclimatic conditions.