Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.     

Effects of seasonality on brain size evolution: evidence from strepsirrhine primates

Seasonal changes in energy supply impose energetic constraints that affect many physiological and behavioral characteristics of organisms. As brains are costly, we predict brain size to be relatively small in species that experience a higher degree of seasonality (expensive brain framework). Alternatively, it has been argued that larger brains give animals the behavioral flexibility to buffer the effects of habitat seasonality (cognitive buffer hypothesis). Here, we test these two hypotheses in a comparative study on strepsirrhine primates (African lorises and Malagasy lemurs) that experience widely varying degrees of seasonality. We found that experienced seasonality is negatively correlated with relative brain size in both groups, controlling for the effect of phylogenetic relationships and possible confounding variables such as the extent of folivory. However, relatively larger-brained lemur species tend to experience less variation in their dietary intake than indicated by the seasonality of their habitat. In conclusion, we found clear support for the hypothesis that seasonality restricts brain size in strepsirrhines as predicted by the expensive brain framework and weak support for the cognitive buffer hypothesis in lemurs.     

Seasonal Fluctuations in Body Fat and Activity Levels in a Rain-Forest Species of Mouse Lemur,Microcebus rufus

Seasonal fattening in preparation for the dry season followed by torpor characterizes some members of the family Cheirogaleidae, a group of < 600-g nocturnal Malagasy primates. These behaviors are associated with extreme seasonality in dry forests, where most studies have been conducted. I aimed to determine if the brown mouse lemur (Microcebus rufus), a rain-forest species of cheirogaleid, exhibited similar changes. Between January 1993 and May 1994 I conducted a mark-recapture study on Microcebus rufus in the rain forest of Ranomafana National Park. I monitored body weight and tail circumference for body fat fluctuations and inferred changes in activity levels from presence or absence in the traps. Some individuals of both sexes increased body fat and entered torpor as suggested by their absence from traps for at least 1 month of the dry season. Activity was resumed with body weight reduced by 5–35 g, and tail circumference by 0.4–1.2 cm. Population-level analysis supports these results; highest weight and tail circumference values occurred just before and at the onset of the dry season. Other individuals, predominantly male, exhibited no change in body fat or activity level, and some mouse lemurs increased their body fat over the course of the dry season. Age, social status, and individual response may influence seasonal behavioral strategies. Dry and rain-forest species of mouse lemur adopt similar behaviors to cope with environmental stresses. Mouse lemurs resemble nonprimate, small-bodied mammals, in which behavioral changes related to maintaining energy balance occur during seasonally unfavorable conditions.     

Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a malagasy primate community

Understanding the mechanisms maintaining local species richness is a major topic in tropical ecology. In ecological communities of Madagascar, primates represent a major part of mammalian diversity and, thus, are a suitable taxon to study these mechanisms. Previous research suggested that ecological niche differentiation facilitates the coexistence of lemurs. However, detailed data on all species making up diverse local primate assemblages is rarely available, hampering community‐wide tests of niche differentiation among Malagasy mammals. Here, we took an indirect approach and used stable isotopes as long‐term indicators of individuals' diets to answer the question of whether trophic patterns and food‐related mechanisms stabilize coexistence in a species‐rich lemur community. We analyzed stable carbon and nitrogen isotopes in hair collected from eight syntopic lemurs in Kirindy Forest. We found that lemur species were well separated into trophic niches and ranged over two trophic levels. Furthermore, species were densely packed in isotopic space suggesting that past competitive interactions between species are a major structuring force of this dry forest lemur community. Results of other comparative studies on primates and our findings underline that—in contrast to communities worldwide—the structure and composition of lemur communities follow predictions of ecological niche theory. Patterns of competitive interactions might be more clearly revealed in Malagasy primate communities than elsewhere because lemurs represent a large fraction of ecologically interacting species in these communities. The pronounced trophic niche differentiation among lemurs is most likely due to intense competition in the past as is characteristic for adaptive radiations. Am J Phys Anthropol 153:249–259, 2014. © 2013 Wiley Periodicals, Inc.     

Conservation biology of Malagasy strepsirhines: a phylogenetic approach

The phylogenetic diversity of extant lemurs represents one of the most important but least studied aspects of the conservation biology of primates. The phylogenetic diversity of a species is inversely proportional to the relative number and closeness of its phylogenetic relatives. Phylogenetic diversity can then be used to determine conservation priorities for specific biogeographic regions. Although Malagasy strepsirhines represent the highest phylogenetic diversity among primates at the global level, there are few phylogenetic data on species-specific and regional conservation plans for lemurs in Madagascar. Therefore, in this paper the following questions are addressed for extant lemurs: 1) how does the measure of taxonomic uniqueness used by Mittermeier et al. (1992 Lemurs of Madagascar; Gland, Switzerland: IUCN) equate with an index of phylogenetic diversity, 2) what are the regional conservation priorities based on analyses of phylogenetic diversity in extant lemurs, and 3) what conservation recommendations can be made based on analyses of phylogenetic diversity in lemurs? Taxonomic endemicity standardized weight (TESW) indices of phylogenetic diversity were used to determine the evolutionary component of biodiversity and to prioritize regions for conserving lemur taxa. TESW refers to the standardization of phylogenetic diversity indices for widespread taxa and endemicity of species. The phylogenetic data came from recent genetic studies of Malagasy strepsirhines at the species level. Lemur species were assigned as being either present or absent in six biogeographic regions. TESW indices were combined with data on lemur complementarity and protected areas to assign conservation priorities at the regional level. Although there were no overall differences between taxonomic ranks and phylogenetic rankings, there were significant differences for the top-ranked taxa. The phylogenetic component of lemur diversity is greatest for Daubentonia madagascariensis, Allocebus trichotis, Lepilemur septentrionalis, Indri indri, and Mirza coquereli. Regional conservation priorities are highest for lemurs that range into northeast humid forests and western dry forests. Expansion of existing protected areas in these regions may provide the most rapid method for preserving lemurs. In the long term, new protected areas must be created because there are lemur species that: 1) are not found in existing protected areas, 2) exist only in one or two protected areas, and 3) are still being discovered outside the current network of protected areas. Data on the population dynamics and feeding ecology of phylogenetically important species are needed to ensure that protected areas adequately conserve lemur populations in Madagascar.     

PHYLOGENETIC,ECOLOGICAL, AND ALLOMETRIC CORRELATES OF CRANIAL SHAPE IN MALAGASY LEMURIFORMS

Adaptive radiations provide important insights into many aspects of evolution, including the relationship between ecology and morphological diversification as well as between ecology and speciation. Many such radiations include divergence along a dietary axis, although other ecological variables may also drive diversification, including differences in diel activity patterns. This study examines the role of two key ecological variables, diet and activity patterns, in shaping the radiation of a diverse clade of primates, the Malagasy lemurs. When phylogeny was ignored, activity pattern and several dietary variables predicted a significant proportion of cranial shape variation. However, when phylogeny was taken into account, only typical diet accounted for a significant proportion of shape variation. One possible explanation for this discrepancy is that this radiation was characterized by a relatively small number of dietary shifts (and possibly changes in body size) that occurred in conjunction with the divergence of major clades. This pattern may be difficult to detect with the phylogenetic comparative methods used here, but may characterize not just lemurs but other mammals.     

Comparison of Reproductive Characteristics and Changes in Body Weight Between Captive Populations of Rufous and Gray Mouse Lemurs

The nocturnal Malagasy mouse lemurs are among the smallest primates worldwide. Several sibling species are known. Of these, the rufous and the gray mouse lemur differ with respect to morphology, genetics, and communication. They might also differ in seasonal reproduction and body weight changes. We investigated and compared reproductive activities and changes in monthly body weight in males and females of successfully breeding colonies of both species under the same photoperiodic conditions. Females of both species showed estrous cycles only during the long-day period. Rufous mouse lemur females seemed to have a shorter gestation than their sibling species (57 vs. 62 days). The number of estrous cycles (2.25 vs. 2.5/season) and their lengths (59 vs. 52 days) were similar. Litter size (2) seemed to be similar. Latency of estrous occurrence after photoperiodic stimulation was longer in Microcebus rufus than in its sibling species (71.6 and 42.3 days). The same was true for the onset of the growth of the testes. The rate of growth and size of the testes were similar, and precede the estrous onset in both species. The reproductive activity was shorter in both sexes of the rufous than of the gray mouse lemurs. In both species, body weight showed similar seasonal changes. Males lost more weight during the breeding season than females did. In rufous mouse lemurs, body weight was similar in both sexes during the nonbreeding season. In gray mouse lemurs, sexes differed throughout the year.     

Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates

The goals of this study were to analyze the origin and function of sex differences in the size of canine teeth among Malagasy lemurs and other strepsirhine primates. These analyses allowed me to illuminate interactions between different mechanisms of sexual selection and to elucidate constraints on this sexually-selected trait. In contrast to central predictions of sexual selection theory, polygynous lemurs lack both sexual dimorphism in body size and male social dominance, but the degree of sexual dimorphism in the size of their canines is not known. A comparison of male and female canine size in 31 species of lemurs and lorises revealed significant male-biased canine dimorphism in only 6 of 13 polygynous lemur species. This result is in contrast to predictions of a hypothesis that would explain the lack of size dimorphism in lemurs as a result of high viability costs because canine teeth presumably have low maintenance costs and because they are used as weapons in male-male combat. Moreover, because females had significantly larger maxillary canines than males in only one lemur species, female dominance is not generally based on female physical superiority and selective forces favoring female dominance do not constrain sexual canine dimorphism in the sense of a pleiotropic effect. Contrary to predictions of sexual selection theory, species differences in canine dimorphism across strepsirhines were neither associated with differences in mating system, nor with the potential frequency of aggression. Variation in canine dimorphism was also unrelated to differences in body size, but there were significant differences among families, pointing to strong phylogenetic constraints. This study demonstrated that polygynous lemurs are at most subject to weak intrasexual selection on dental traits used in male combat and that traits thought to be under intense sexual selection are strongly influenced by phylogenetic factors.     

Group Size, Home Range Use, and Seasonal Variation in the Ecology of Eulemur mongoz

We collected data during a 10-month study carried out on the mongoose lemur, Eulemur mongoz, at Anjamena in northwestern Madagascar, which provide baseline information on seasonal variation in the ecology, home range use and some aspects of the behavior of two neighboring groups. We monitored group size of nine groups in the study area and assessed them for seasonal variation. We present additional information collected during short-term surveys in other areas before and during the study for comparison. The study groups were small family units, and changes in group size were limited to births and emigrations of sexually mature progeny. In spite of clear seasonal changes in climate and vegetation, there is no variation in grouping patterns, so it is not possible to correlate variation in group size with seasonal variation of ecological variables. Comparison with ecological data from other field studies on lemurids reveals differences in food resource distribution in western forests versus other types of Malagasy forest. This distribution of food resources may predict home range size in mixed frugivorous–folivorous lemurs. Small home ranges, mainly in the West, could be correlated with a uniform distribution of food resources. Finally, we suggest that the dry season in the West may not present frugivorous–folivorous lemurs with major problems in finding an adequate food supply. This is supported by the lack of seasonal differences in ranging behavior of mongoose lemurs.     

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.     

Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo, southwestern Madagascar

Variation in body size is well documented for both extant and extinct Malagasy primates, and appears to be correlated with geographic patterns of resource seasonality. Less attention has been paid to extant lemurs in subfossil collections, although it has been suggested that subfossil forms of extant species are characterized by greater size than their modern counterpart. This trend of phyletic size change has been related to climate change, habitat fragmentation, or human hunting. However, space- and time-averaging in the subfossil samples of previous studies may have obscured more general ecogeographic patterns underlying these size differences. Our objective is to examine size variation in subfossil still-extant primates within a regional comparative context to determine if subfossil and living forms conform to similar ecogeographic patterns. We report on the subfossil still-extant primate assemblage from Ankilitelo, southwestern Madagascar (approximately 500 yr BP) to test this hypothesis. The Ankilitelo primates were compared with museum specimens of known locality. Extant taxa were assigned to one of five distinct ecogeographic regions, including spiny thicket, dry deciduous forest, succulent woodland, lowland and subhumid rainforest. Comparisons of tooth size in extant lemurs reveal significant geographical patterns of variation within genera. In general, the primates from Ankilitelo are indeed larger than their modern counterpart. However, these differences fit an ecoregional model of size variation, whereby Ankilitelo species are comparable in size to living forms inhabiting ecoregions present near the cave today. This suggests that Malagasy primates have been subjected to similar patterns of resource seasonality for at least 500 years.     

Use of Vocal Fingerprinting for Specific Discrimination of Gray (Microcebus murinus) and Rufous Mouse Lemurs (Microcebus rufus)

Advertisement calls are often important noninvasive tools for discriminating cryptic species and for assessing specific diversity and speciation patterns in nature. We investigated the contribution of these calls to uncover specific diversity in nocturnal Malagasy lemurs. We compared sexual advertisement and predator advertisement calls of two mouse lemur species, western gray and eastern rufous mouse lemurs (Microcebus murinus and M. rufus, respectively) living in two contrasting habitats (dry deciduous vs. rain forest), and analyzed them statistically. Both species emitted several highly variable whistle calls in the context of predator-avoidance. Intrapopulation variation was high and overlapped interspecific variation. Sexual advertisement calls, given in the mating context, displayed a totally distinct, species-specific acoustic structure. Whereas gray mouse lemurs produced rapidly multifrequency modulated, long trill calls, rufous mouse lemurs gave slowly frequency-modulated short chirp calls. Our results suggest specific status for gray and rufous mouse lemurs and indicate the importance of predation and social needs in shaping vocal communication.     

Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs

Following human arrival, Madagascar suffered well-documented megafaunal extinctions and widespread deforestation. Although humans are widely considered to be the primary cause of the extinctions, the relative contributions of climate change and human activities to this ecological transformation remain uncertain. Reconstructing the habitats of the giant lemurs of Madagascar can provide key information for understanding the evolutionary mechanisms involved in their extinction. In this study, I present a faunal analysis of the subfossil assemblage from Ankilitelo Cave, southwestern Madagascar. This assemblage documents the latest known occurrence of five species of extinct giant lemur, in association with abundant well-preserved small mammal remains. I compared the small mammal fauna at Ankilitelo with 27 extant Malagasy mammal communities spanning the range of Madagascar's habitat types. Similarities in species composition between modern communities and Ankilitelo were assessed using cluster analysis. Ecological similarities were examined by assigning each species to dietary, locomotor, activity pattern, and body size categories. Multiple discriminant analysis was then used to classify Ankilitelo relative to modern habitat types in Madagascar, based on the ecological structure of the subfossil fauna. Results indicate that the habitat surrounding Ankilitelo during the late Holocene was similar to the succulent woodlands of modern southwestern Madagascar. This suggests that approximately 500 yr BP, these semi-arid habitats supported a subfossil lemur community that included the highly-suspensory Palaeopropithecus, and deliberate slow-climber Megaladapis, as well as Archaeolemur, Pachylemur, and Daubentonia robusta. In such environments, these giant lemurs would likely have been highly vulnerable to increasing human pressure in southwestern Madagascar.     

Molecular Evidence of Reproductive Isolation in Sympatric Sibling Species of Mouse Lemurs

Recent morphological and molecular phylogenetic studies of mouse lemurs (Microcebus) living in the western and southern regions of Madagascar have shown that specific diversity had been considerably underestimated. In large part, this underestimate was due to the lack of sufficient specimens from given localities to assess properly the level of phenotypic variation within and between populations. The accurate delineation of specific boundaries has no doubt been confounded by the diminutive size, nocturnal habits, and subtle morphological variation characteristic of mouse lemurs, which can make field identification of individuals problematic. We illustrate the use of molecular phylogenetic analysis to reveal reproductive isolation in two sympatric mouse lemur species, Microcebus murinus and M. griseorufus. Their documentation in the Berenty Private Reserve in the extreme south of Madagascar verifies the historically-broad distribution of Microcebus griseorufus, a species recently resurrected from synonomy.     

Mhc-DRB genes evolution in lemurs

Partial exon 2 sequences (202 bp) of the lemur Mhc-DRB genes were sequenced. A total of 137 novel sequences were detected in 66 lemurs, representing four out of the five extant families. Trans-species polymorphisms and even identical sequences were observed not only among genera but also among families. Based on the time-scale of lemur evolution, these findings suggest that some identical sequences have been maintained for more than 40 million years. This is in contrast to the evolutionary mode of simian DRB genes, where such identical sequences have been retained for at most several million years. To explore the reasons behind these unexpected findings, the degree of recombination and the synonymous substitution rate in lemurs and simians were examined. We found that (1) little difference existed in the extent of recombination, (2) frequent recombination occurred within the alpha-helix as well as between the beta-pleated sheet and the alpha-helix, and (3) the synonymous substitution rate was significantly reduced in lemur lineages. Upon phylogenetic analysis, lemur DRB genes were clustered by themselves and separated from the other primate DRB genes (simians and non-Malagasy prosimians). This result suggests that the DRB variations in extant lemur populations have been generated after the divergence of the lemurs from the remaining primates. This mode of substitution accumulation is also supported by a pattern of mismatch distribution among lemur DRB genes. These observations correspond with the postulation that a severe bottleneck occurred when the ancestors of lemurs settled into Madagascar from the African continent.     

Monogamy as a Rule Rather than Exception in Nocturnal Lemurs: the Case of the Fat-tailed Dwarf Lemur, Cheirogaleus medius

According to present hypotheses on the evolution of life history traits and social systems in Malagasy lemurs, nocturnality and infant parking are associated with a solitary lifestyle and a polygynous mating system. However, theoretically extreme seasonality of reproduction could limit the number of females that can be monopolized by a given male and thus hinder the evolution of polygyny. The aim of this ongoing study is to test these contrasting expectations by looking at the social and mating system of the fat-tailed dwarf lemur Cheirogaleus medius . This species hibernates for up to 7 mo, so that time for breeding and raising offspring is extremely limited.
A mark-recapture study in western Madagascar was combined with observations and radio-tracking of 36 individuals during the rainy seasons from 1995 to 1998. According to these data, fat-tailed dwarf lemurs live in permanent sleeping groups consisting of a male and a female (n = 8) or one male and two females (n = 1). One or two offspring from the previous year were frequently observed to sleep together with an adult pair. Members of each sleeping group were the exclusive users of their nest holes and home ranges. During the birth season, males and females took turns at baby-sitting their offspring. Females without paternal help were unable to raise their offspring successfully. Since females did not exhibit oestrus synchrony, the ultimate selective factor favouring pair-living could be obligate paternal investment. The results, together with the lack of sexual size dimorphism and relatively small testis size, suggest that the fat-tailed dwarf lemur lives in family groups with a monogamous mating system. A review of the mating systems of nocturnal lemurs shows that monogamy appears to be the rule rather the exception.     

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.     

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.