Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar

In this paper, I provide data on the possible effects of group size and seasonal changes in food availability on the activity and habitat use patterns of two species of prosimian primate: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). General and subtle seasonal differences were observed between lemur species in (1) group size and composition, (2) activity profiles, and (3) habitat use. Rufous lemur groups were larger (mean = 8 individuals) and contained more adults than red-bellied lemur groups (mean = 3 individuals). The overall degree and distribution of diurnal activity differed between lemur species and varied within species with seasonal changes in food availability. In general, rufous lemurs traveled more often than red-bellied lemurs. During food scarcity, both species increased the amount of time spent feeding, although peak feeding and traveling times differed. Both species also preferred horizontal substrates; however, during food scarcity, red-bellied lemurs used terminal branches more often while feeding than rufous lemurs. In addition, red-bellied lemurs used the lower middle story forest and rested in taller, upper canopy trees more often than rufous lemurs. Differences in activity and habitat use patterns between lemur species were more related to seasonal changes in food availability than overall differences in group size. These behavioral patterns may represent different strategies used by each lemur species to avoid directly competing for similar resources during times of food scarcity. © 1996 Wiley-Liss, Inc.     

Behavioral thermoregulation in a gregarious lemur, Eulemur collaris: effects of climatic and dietary-related factors

Primates deal with fluctuations of the thermal environment by both physiological and behavioral mechanisms of thermoregulation. In this article we focus on non-hibernating lemurs, which are hypometabolic and have to cope with a seasonal environment. Behavioral thermoregulation has received little attention compared with specific physiological adaptations to seasonality, i.e., hibernation and torpor, which characterize a number of lemurs. We investigated the role of seasonality and dietary-related factors in determining frequencies of resting, social and postural thermoregulation, and microhabitat selection in collared lemurs, Eulemur collaris. We observed two groups of collared lemurs over a 14-month period in the littoral forest of Sainte Luce, Southern Madagascar. Frequencies of total resting and time spent in huddling, prone, and curled postures were collected via 5-min instantaneous sampling. Microhabitat selection was evaluated as the proportion of time spent in the upper canopy as compared with other layers. Climatic variables were recorded by automatic data loggers, while dietary variables were derived from phenological data and nutritional analyses of the ingested food items. We weighted the combined effects of climatic and dietary variables on the different types of behavioral thermoregulation by means of canonical correlation analysis. The model with the strongest canonical correlation included a first root representing mainly feeding time, day length, and ambient temperature and a second root representing diet quality and height of feeding trees. The output indicated that collared lemurs adapt to thermal and dietary-related metabolic stress by adjusting resting time, social, and postural thermoregulation.     

High Energy or Protein Concentrations in Food as Possible Offsets for Cyanide Consumption by Specialized Bamboo Lemurs in Madagascar

Plants producing toxic plant secondary metabolites (PSMs) deter folivores from feeding on them. Animals that can cope with noxious PSMs have a niche with a competitive advantage over other species. However, the ability to cope with toxic PSMs incurs the costs of detoxification. To assess possible compensations for the ingestion of toxic PSMs, we compare the chemical quality of plants consumed by bamboo lemurs (genera Hapalemur and Prolemur; strepsirrhine primates of Madagascar) in areas with and without bamboo. Some bamboo lemurs consume bamboo containing concentrations of cyanogenic substances 10–50 times above the average lethal dosage for mammals, and we postulate that animals consuming cyanogenic substances need supplementary protein or readily available energy for detoxification. We compared the chemical composition of food consumed by three species of bamboo lemurs that feed mainly (>80% of their time) on bamboo in the evergreen rainforest of Ranomafana (Madagascar) with published data of the diets of bamboo lemurs at two sites without highly cyanogenic plants (reed beds of Lac Alaotra and the evergreen littoral forest of Mandena) and with food of sympatric folivorous lemur species that do not feed on bamboo. Lemurs feeding on bamboo consumed up to twice as much protein as bamboo lemurs in areas without bamboo and sympatric lemur species that feed on leaves of trees. Concentrations of nonstructural carbohydrates (a source of energy) showed the opposite trend. This result supports the hypothesis that feeding on cyanogenic plants is linked to high protein intake, either as a source of protein or for sulfur-containing amino acids that can be used for detoxification. Owing to the high protein concentrations in bamboo, however, we cannot distinguish between the hypothesis that lemurs that eat bamboo target additional food items with higher protein from the hypothesis that lemurs feeding on bamboo unavoidably obtain higher concentrations of protein than animals feeding on leaves of trees, without an added nutritional benefit.     

Effects of Habitat Quality and Seasonality on Ranging Patterns of Collared Brown Lemur (Eulemur collaris) in Littoral Forest Fragments

Degraded forest habitats typically show low fruit availability and scattered fruit tree distribution. This has been shown to force frugivorous primates either to move further in search of food, resulting in large home ranges, or to use energy saving strategies. Malagasy lemurs are known to face pronounced seasonality and resource unpredictability, which is amplified by the overall reduction in food availability due to the human-driven habitat disturbance on the island. To explore lemur flexibility to habitat disturbance, we examined the ranging behavior of collared brown lemurs (Eulemur collaris) in two differently degraded fragments of littoral forest of southeastern Madagascar. We collected data from February 2011 to January 2012 on two groups living in a degraded area and two groups living in a less disturbed forest. We calculated annual ranges, monthly ranges, and daily distance traveled. We then ran repeated measures ANOVAs using seasonality as dichotomous, intrasubject factor and site/group as intersubject nested factors. In the degraded forest, the lemurs had larger monthly ranges, and their annual ranges were either fragmented or characterized by multiple core areas. They were able to use a habitat mosaic that also included nonforested areas and swamps. In addition, they shortened their daily path length, possibly to preserve energy, and used different areas of their annual home ranges seasonally. Although a number of possible confounding factors may have been responsible for the observed differences between sites, our findings highlight the ranging flexibility of collared brown lemurs in littoral forest fragments.     

Long-term genetic monitoring of a translocated population of collared brown lemurs

Post-release monitoring is important to improve translocation success because it provides an opportunity to identify factors relevant to the survival of local populations. We studied a population of the endangered collared brown lemur (Eulemur collaris) translocated from a degraded forest fragment to a nearby littoral forest within the Mandena Conservation Area in southeast Madagascar from 2000–2011. We compared genetic surveys of mitochondrial and nuclear markers with the genetic profile of nearby populations to examine the dispersal capacity of the collared brown lemur. We also performed a landscape analysis to assess changes in connectivity between forest fragments. There was a fluctuating trend characterized by a phase of demographic and genetic stability shortly after translocation, followed by an increase in genetic diversity coinciding with a population decrease and a gradual recovery of initial conditions. These results demonstrated the ability of the collared brown lemur to disperse through unfavorable landscapes and to recover after translocation. Our study revealed the importance of monitoring translocated populations over time using a multidisciplinary approach.     

The Use of an Invasive Species Habitat by a Small Folivorous Primate: Implications for Lemur Conservation in Madagascar

The lemurs of Madagascar are among the most threatened mammalian taxa in the world, with habitat loss due to shifting cultivation and timber harvest heavily contributing to their precarious state. Deforestation often leads to fragmentation, resulting in mixed-habitat matrices throughout a landscape where disturbed areas are prone to invasion by exotic plants. Our study site, the Mandena littoral forest (southeast Madagascar), is a matrix of littoral forest, littoral swamp, and Melaleuca swamp habitats. Here, Melaleuca quinquenervia has invaded the wetland ecosystem, creating a mono-dominant habitat that currently provides the only potential habitat corridor between forest fragments. We sought to understand the role of this invasive Melaleuca swamp on the behavioral ecology of a threatened, small-bodied folivore, the southern bamboo lemur (Hapalemur meridionalis). We collected botanical and behavioral data on four groups of H. meridionalis between January and December 2013. Our results confirm Melaleuca swamp as an important part of their home range: while lemurs seasonally limited activities to certain habitats, all groups were capable of utilizing this invasive habitat for feeding and resting. Furthermore, the fact that Hapalemur use an invasive plant species as a dispersal corridor increases our knowledge of their ecological flexibility, and may be useful in the conservation management of remaining threatened populations.     

Habitat Degradation and Seasonality Affect Physiological Stress Levels of Eulemur collaris in Littoral Forest Fragments

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.     

Sleeping and Ranging Behavior of the Sambirano Mouse Lemur, <Emphasis Type="Italic">Microcebus sambiranensis</Emphasis>

Primates require secure sleeping sites for periods of rest, but despite their importance, the characteristics of desired sleeping sites are poorly known. Here we investigated the sleeping ecology of a radio-collared population of the Sambirano mouse lemur, Microcebus sambiranensis, during the nonreproductive season in the Anabohazo forest, northwestern Madagascar. We also investigated their ranging behavior and examined the spatial distribution of sleeping sites within the home ranges of the collared individuals. We took measurements of the sleeping tree’s physical characteristics and recorded the number of collared individuals using each sleeping site. We found that M. sambiranensis generally use foliage sleeping sites more frequently than tree holes and individuals slept more frequently in densely foliated trees than in sparsely foliated trees, often alone. We observed no significant differences in home range size or nightly travel distance between males and females; however, home ranges were smaller than those described for other mouse lemur species. Finally, we found that M. sambiranensis sleep peripherally and forage centrally within their home ranges, a behavior not previously described for mouse lemurs. Our results indicate profound differences in the social organization between M. sambiranensis and other mouse lemur species described in the literature, suggesting species-specificity in mouse lemur ecology. Understanding the sleeping ecology and ranging behavior of mouse lemurs is of great importance to their conservation, as these data facilitate the planning of long-term reforestation, habitat management, and population assessment.     

Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar

The lemurs of Madagascar are known for their extraordinary species diversity. The mechanisms that allow the coexistence of these species are still poorly known. Here feeding patterns were investigated for three small nocturnal lemur species of Cheirogaleidae ( Microcebus murinus , Cheirogaleus medius and Cheirogaleus major ) occurring sympatrically in a littoral rainforest in south-east Madagascar. During three rainy seasons, the plant species eaten by these three lemurs were described in relation to morphological and biochemical characteristics. All three species were mainly frugivorous and fed on 68 different plant species with small- and medium-sized fruits. A total of 91% of these forage plant species was visited by all three lemur species. Fruits larger than 25–30 mm were avoided. Seeds of a total of 51 food plant species were swallowed and passed the gut unharmed. Thus, even these smaller lemur species play an important role in seed dispersal. There were no differences in the morphological and biochemical characteristics of fruits eaten between the three species, but the feeding height was significantly different between the species. Thus, competition avoidance and niche separation are presumably not based on different feeding patterns of M. murinus , C. medius and C. major in the littoral rainforest, but on different habitat utilization.     

Pilot survey of avahi population (woolly lemurs) in littoral forest fragments of southeast Madagascar

This study presents a pilot survey of the avahis (pair-living, nocturnal prosimians) living in threatened littoral forest fragments of southeastern Madagascar. In the period of October–December 2004, I evaluated the density of adult and newborn avahis (carried by the mothers) by counting the individuals encountered during 58 night walks in seven fragments of Sainte Luce and Mandena forests, along one trail/fragment. Along each trail, I used random plots (5 m²) for a preliminary characterization of the vegetation. The density of the population was not correlated with fragment size and number of plant morphospecies, while it was correlated with large tree availability. Possibly due to a low energy diet based on leaves and to specialized and energetically expensive vertical leaping, the loss of large trees by selective logging seems to affect avahi populations more than other variables.     

Ecological correlates to social structure in two lemur species in Madagascar

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity. © 1996 Wiley-Liss, Inc.     

Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates

Among primates, catarrhines (Old World monkeys and apes) andcertain platyrrhines (New World monkeys) possess trichromaticcolor vision, which might confer important evolutionary advantages,particularly during foraging. Recently, a polymorphism has beenshown to shift the spectral sensitivity of the X-linked opsinprotein in certain strepsirrhines (e.g., Malagasy lemurs); however,its behavioral significance remains unknown. We assign genotypesat the X-linked variant to 45 lemurs, representing 4 species,and test if the genetic capacity for trichromacy impacts foragingperformance, particularly under green camouflage conditionsin which red detection can be advantageous. We confirm polymorphismat the critical site in sifakas and ruffed lemurs and fail tofind this polymorphism in collared lemurs and ring-tailed lemurs.We show that this polymorphism may be linked to "behavioraltrichromacy" in heterozygous ruffed lemurs but find no comparableevidence in a single heterozygous sifaka. Despite their putativedichromatic vision, female collared lemurs were surprisinglyefficient at retrieving both red and green food items undercamouflage conditions. Thus, species-specific feeding ecologiesmay be as important as trichromacy in influencing foraging behavior.Although the lemur opsin polymorphism produced measurable behavioraleffects in at least one species, the ruffed lemur, these effectswere modest, consistent with the modest shift in spectral sensitivity.Additionally, the magnitude of these effects varied across individualsof the same genotype, emphasizing the need for combined geneticand behavioral studies of trichromatic vision. We conclude thattrichromacy may be only one of several routes toward increasedforaging efficiency in visually complex environments.     

Influence of abiotic factors on cathemeral activity: the case of Eulemur fulvus collaris in the littoral forest of Madagascar

The role environmental factors play in influencing circadian rhythms in natural habitats is still poorly described in primates, especially for those taxa with an activity cycle extended over the 24-hour cycle. In this paper, we elucidate the importance of abiotic factors in entraining the activity of cathemeral primates, focussing on results from a long-term study of Eulemur fulvus collaris (collared brown lemur) in south-eastern Malagasy littoral forest. Two groups of lemurs were followed for 60 whole-day and 59 whole-night observation periods over 14 months. Diurnal and nocturnal observations were equally distributed among moon phases and seasons. Temperature and humidity were recorded hourly by automatic data loggers. The littoral forest has a climatic environment where rainfall and humidity are uncorrelated with temperature and photoperiod. Diurnal and nocturnal activity varied seasonally, with the former increasing significantly with extended day length and the latter increasing significantly with shortened day length. Dusk seemed to act as a primary zeitgeber for these lemurs, coordinating the onset of evening activity throughout the entire year. Lunar phase and the nocturnal luminosity index correlated positively with the duration of nocturnal activity and negatively with the length of diurnal activity. Temperature was positively associated with diurnal activity but did not seem to influence lemur rhythms at night. Finally, lemur nocturnal activity significantly decreased when levels of humidity and rainfall were high. Cathemeral biorhythm is triggered by zeitgebers and influenced by masking factors. The activity of collared brown lemurs appears to be seasonally influenced by photoperiod and directly modulated by nocturnal ambient luminosity. These results are discussed by comparing data from other cathemeral species living in various climatic situations.     

Coping with low-quality diets: a first account of the feeding ecology of the southern gentle lemur, <Emphasis Type="Italic">Hapalemur meridionalis</Emphasis>, in the Mandena littoral forest,southeast Madagascar

Malagasy primates of the genus Hapalemur are exceptional in their exhibition of specialisations allowing for a folivorous diet despite their small body size. Members of this group are well known for their preference for specific parts of woody bamboo, the primary food resource throughout much of their range. The southern gentle lemur (H. meridionalis), however, inhabits littoral forests that contain little or no woody bamboo. Similar to its closely related congener, the Alaotran gentle lemur (H. alaotrensis), the question is raised as to how these lemurs subsist in this ecological context. The aim of this study was to gain an initial understanding of the ecological niche of the southern gentle lemur in the threatened ecosystem of the littoral forest of southeastern Madagascar. Lemurs were habituated and observed over a 3-month period during the austral winter, allowing for collection of both continuous and instantaneous focal data on their feeding ecology. Preferred food species were identified and collected, and biochemical analyses determined macronutrient and secondary compound values for consumed food items. The diet of the southern gentle lemur was found to be of low nutritional quality, as evaluated through the low protein-to-fibre ratio, especially when compared with other folivores. This lemur is also unique in spending a majority of its time grazing on terrestrial grasses (family Poaceae) during the resource-poor winter months. Our data indicate that Hapalemur spp. possess a behavioural flexibility, and possibly, digestive abilities, higher than previously thought for an animal of its small body size.     

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.     

Delimiting Species without Nuclear Monophyly in Madagascar's Mouse Lemurs

Background

Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters—including morphological differences, reproductive isolation, and gene tree monophyly—that are typically used as evidence for separately evolving lineages.

Methodology

In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed.

Conclusions

The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa, as well as newly resolved patterns of micro-endemism revealed through expanded field sampling into previously poorly and well-sampled regions.     

Geographic Variation in Populations of Microcebus murinus in Madagascar: Resource Seasonality or Bergmann's Rule?

Gray mouse lemurs (Microcebus murinus) occur in western Madagascar from the evergreen littoral rain forests at the southern tip of the island to the seasonal dry deciduous forests of the west and northwest. The wide geographic distribution allows researchers to investigate whether ecogeographic variations reflect adaptations to ambient temperatures, as a proxy for constraints of thermoregulation, or to rainfall, as a proxy of food availability. We compared body mass, number of litters/yr, and longevity for 3 populations: 1 from the evergreen littoral rain forest of the south (Mandena: annual mean temperature 23°C, 1600 mm rain/yr), 1 from the dry deciduous forest of the west (Kirindy/CFPF: 25°C, 800 mm), and 1 from the dry deciduous forest of northwestern Madagascar (Ampijoroa: 27°C, 1200 mm). Body mass decreases with increasing ambient temperature from south to north (Mandena > Kirindy/CFPF > Ampijoroa). The number of litters/yr was highest in the littoral rain forest (2 or 3 litters/yr) and decreased with decreasing rainfall (Mandena > Ampijoroa > Kirindy/CFPF). Life expectancy is lowest in the littoral forest (13% recaptures of mouse lemurs between years) and high (ca. 30–40% recaptures between years) in the dry forests (Mandena < Kirindy/CFPF and Ampijoroa). We postulate that constraints of thermoregulation result in the latitudinal gradient of body mass. Reduced resource productivity or seasonality is reflected in differences in reproductive rates, which seemed to be traded off against longevity. Thus body mass, longevity, and reproductive parameters respond differently to ambient conditions.     

Ecological Flexibility as Measured by the Use of Pioneer and Exotic Plants by Two Lemurids: <Emphasis Type="BoldItalic">Eulemur collaris</Emphasis> and <Emphasis Type="BoldItalic">Hapalemur meridionalis</Emphasis>

Primate responses to habitat alteration vary depending on the species’ dietary guild and forest type. Leaves from secondary vegetation can provide nutritious resources to folivorous primates, whereas frugivores, burdened with a scattered spatial and temporal distribution of fruiting resources, require larger home ranges, potentially limiting their ability to cope with altered landscapes. Within coastal southeastern Madagascar, we sought to determine whether two lemur species occupying contrasting ecological niches respond differently to the changing features of their degraded and fragmented habitat. We conducted behavioral observations between 2011 and 2013 on frugivorous collared brown lemurs (Eulemur collaris) and folivorous southern bamboo lemurs (Hapalemur meridionalis). To estimate the ability of lemurs to use pioneer species, we categorized all plants used for feeding and resting as fast growing, mid-growing, or slow growing. We fitted general linear mixed-effects models, one for each plant growth category with monthly proportional use rates as the dependent variable, and included species (E. collaris and H. meridionalis), activity (feeding and resting), and season (dry and wet) as fixed effects. Our results show that E. collaris used both slow- and mid-growing plant species most often, while H. meridionalis were more likely to use fast-growing plants, which indicated an ability to use secondary/disturbed vegetation. Frugivorous E. collaris appear more limited by climax plants, while folivorous H. meridionalis appear to be slightly more adaptable, a finding that is consistent with that for other primate folivores.     

Life in a fragment: Evolution of foraging strategies of translocated collared brown lemurs,Eulemur collaris,over an 18-year period

While the drivers of primate persistence in forest fragments have been often considered at the population level, the strategies to persist in these habitats have been little investigated at the individual or group level. Considering the rapid variation of fragment characteristics over time, longitudinal data on primates living in fragmented habitats are necessary to understand the key elements for their persistence. Since translocated animals have to cope with unfamiliar areas and face unknown fluctuations in food abundance, they offer the opportunity to study the factors contributing to successful migration between fragments. Here, we illustrated the evolution of the foraging strategies of translocated collared brown lemurs (Eulemur collaris) over an 18-year period in the Mandena Conservation Zone, south-east Madagascar. Our aim was to explore the ability of these frugivorous lemurs to adjust to recently colonized fragmented forests. Although the lemurs remained mainly frugivorous throughout the study period, over the years we identified a reduction in the consumption of leaves and exotic/pioneer plant species. These adjustments were expected in frugivorous primates living in a degraded area, but we hypothesize that they may also reflect the initial need to cope with an unfamiliar environment after the translocation. Since fragmentation is often associated with the loss of large trees and native vegetation, we suggest that the availability of exotic and/or pioneer plant species can provide an easy-to-access, nonseasonal food resource and be a key factor for persistence during the initial stage of the recolonization.