Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

I examined the vigilance behavior of adult males and females in two groups of ring-tailed lemurs(Lemur catta)during the birth and lactation season at the Beza-Mahafaly Reserve, southwestern Madagascar. I found no sex difference with respect to the rates of overall vigilance, rates of vigilance toward a potential predator or unfamiliar sound, or rates of vigilance toward conspecifics from other social groups, nor were there sex differences in the percentage of time spent vigilant in any of the above categories. Higher-ranking females were vigilant significantly more often toward predators or potential predators than lower-ranking females were. I detected no relationship between vigilance behavior and dominance rank among adult males. The alpha female in each group exhibited significantly more vigilance behavior than all other members of her group. It was predicted that males should exhibit more vigilance behavior than females do, particularly during the birth and lactation season, when predator pressure is high, if they are benefiting females in this respect. I discuss the results in the context of this prediction and in terms of how ring-tailed lemur males benefit females, and why they may be tolerated in social groups.     

The nature and frequency of agonism in free-ranging and semi-free-ranging brown lemurs,Eulemur fulvus

Agonistic behaviour was studied in three groups each of free-ranging and semi-free-ranging brown lemurs (Eulemur fulvus) at Berenty, Madagascar and the Duke University Primate Center (DUPC) respectively. The purpose of the study was to answer questions arising from the work of other researchers regarding the frequency and intensity of agonism in this species. Authors of field studies generally concluded that agonism was rare and mild, whereas those who had studied semi-free-ranging or captive animals at the DUPC reported intense agonism during the peaks of the mating and birth seasons, with sometimes fatal wounding occurring among captive animals. I recorded 30 agonistic behaviours or “signals” which I grouped into seven general categories — cuffs, other physical contact, threats, chases, third party intervention, unprovoked submissive signals, and reciprocal aggression. The seven categories represent the types of signals which initiated or otherwise defined agonistic interactions, regardless of whether or not there was a submissive response to aggression. The relative percentages of all agonism constituted by the seven categories were not found to be significantly different between study sites. Agonistic signals were also classified as either subtle or obvious, a classification which crosscut the seven categories. At both study sites, the majority of agonistic signals initiating or defining interactions were subtle. Rates of agonism for the Berenty groups, studied during the birth season only, were significantly lower than those for the DUPC groups during the birth season, possibly due to (1) easier observation conditions at the DUPC, and (2) the impossibility of successful emigration at the DUPC, which might have resulted in social stresses translating into higher rates of agonism. In only one DUPC group was there significant variation in rates of agonism between seasons. I found agonistic behaviour to be mild, at both study sites, in the senses of subtlety of both aggressive and submissive signals, unlikelihood of response to aggression, and virtual absence of wounding; and I noted that serious wounding during other studies at the DUPC involved animals captive in caged runs. Comparing rates of the study groups with rates reported in other research for brown lemurs, other lemuriform species, and some New and Old World anthropoid species, I concluded thatE. fulvus agonism was in fact not rare except in comparison to baboons and macaques.     

Dental use wear in extinct lemurs: evidence of diet and niche differentiation

A new technique for molar use-wear analysis is applied to samples of all 16 species of extinct lemurs with known dentitions, as well as to a large comparative sample of extant primates. This technique, which relies on the light refractive properties of wear pits and scratches as seen under a standard stereoscopic microscope, has shown itself to be effective in distinguishing the diets of ungulates and extant primates. We draw dietary inferences for each of the 16 extinct lemur species in our database. There is a strong phylogenetic signal, with the Palaeopropithecidae showing use-wear signatures similar to those of the Indriidae; extinct lemurids (Pachylemur spp.) showing striking similarities to extant lemurids (except Hapalemur spp.); and Megaladapis showing similarities to Lepilemur spp. Only the Archaeolemuridae have dietary signatures unlike those of any extant lemurs, with the partial exception of Daubentonia. We conclude that the Archaeolemuridae were hard-object feeders; the Palaeopropithecidae were seed predators, consuming a mixed diet of foliage and fruit to varying degrees; Pachylemur was a fruit-dominated mixed feeder, but not a seed predator; and all Megaladapis were leaf browsers. There is no molar use wear evidence that any of the extinct lemurs relied on terrestrial foods (C4 grasses, tubers, rhizomes). This has possible implications for the role of the disappearance of wooded habitats in the extinction of lemurs.     

Dental and general health in a population of wild ring-tailed lemurs: a life history approach

Data are presented on dental and general health for seven groups of wild ring-tailed lemurs, Lemur catta, from the Beza Mahafaly Reserve, in southern Madagascar. As part of a study of population demography, adults were captured, collared, and tagged, and biometric measurements, dental casts, and analyses of dental and general health were made. Results indicate that patterns of dental health vary by individual, age, sex, and habitat. Prime adults show more dental attrition than young adults. Prime males living in more marginal habitats show greater mean attrition than those living in richer habitats. Dental damage, specifically to the toothcomb, indicates that mechanical stresses to this region may include the initial harvesting of foods, in addition to grooming. Males exhibit more evidence of past trauma, including scars and chipped teeth. These results indicate that environmental as well as social factors, such as female dominance, may lead to sex differences in health patterns among lemurs.     

Patterns of female dominance in Propithecus diadema edwardsi of Ranomafana National Park, Madagascar

Many lemur species are characterized by some form of female dominance, ranging from female feeding priority to complete female dominance, although this is a rare trait in primates and other mammals. The status of the Milne-Edwards' sifaka (Propithecus diadema edwardsi), a diurnal lemur, is ambiguous. Some short-term studies have found little or no aggression. The aim of the current, long-term study was to quantify the intersexual-dominance patterns of this sifaka. The distribution, outcome, and context of aggressive interactions were studied in four groups of wild sifakas. The majority of intersexual aggressive interactions were decided, with the loser expressing submissive behavior. Intersexual aggressive interactions occurred in all social contexts, and within all social contexts the females won the vast majority (92.7-96.0%) of aggressive interactions. While aggression rates were low (0.22/hr), this evidence suggests female dominance. We propose that female dominance exists because it provides a fitness advantage to both males and females.     

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.     

Nutritional correlates of the “lean season”: Effects of seasonality and frugivory on the nutritional ecology of diademed sifakas

Primate field studies often identify “lean seasons,” when preferred foods are scarce, and lower‐quality, abundant foods (fallback foods) are consumed. Here, we quantify the nutritional implications of these terms for two diademed sifaka groups (Propithecus diadema) in Madagascar, using detailed feeding observations and chemical analyses of foods. In particular, we sought to understand 1) how macronutrient and energy intakes vary seasonally, including whether these intakes respond in similar or divergent ways; 2) how the amount of food ingested varies seasonally (including whether changes in amount eaten may compensate for altered food quality); and 3) correlations between these variables and the degree of frugivory. In the lean season, sifakas shifted to non‐fruit foods (leaves and flowers), which tended to be high in protein while low in other macronutrients and energy, but the average composition of the most used foods in each season was similar. They also showed dramatic decreases in feeding time, food ingested, and consequently, daily intake of macronutrients and energy. The degree of frugivory in the daily diet was a strong positive predictor of feeding time, amount ingested and all macronutrient and energy intakes, though season had an independent effect. These results suggest that factors restricting how much food can be eaten (e.g., handling time, availability, or intrinsic characteristics like fiber and plant secondary metabolites) can be more important than the nutritional composition of foods themselves in determining nutritional outcomes—a finding with relevance for understanding seasonal changes in behavior, life history strategies, competitive regimes, and conservation planning. Am J Phys Anthropol 153:78–91, 2014. © 2013 Wiley Periodicals, Inc.     

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.     

Body size and scaling of the hands and feet of prosimian primates

The hands and feet of primates fulfill a variety of biological roles linked with food acquisition and positional behavior. Current explanations of shape differences in cheiridial morphology among prosimians are closely tied to body size differences. Although numerous studies have examined the relationships between body mass and limb morphology in prosimians, no scaling analysis has specifically considered hand and foot dimensions and intrinsic proportions. In this study, we present such an analysis for a sample of 270 skeletal specimens distributed over eight prosimian families. The degree of association between size and shape was assessed using nonparametric correlational techniques, while the relationship between each ray element length and body mass (from published data and a body mass surrogate) was tested for allometric scaling. Since tarsiers and strepsirrhines encompass many taxa of varying degrees of phylogenetic relatedness, effective degrees of freedom were calculated, and comparisons between families were performed to partially address the problem of statistical nonindependence and "phylogenetic inertia." Correlational analyses indicate negative allometry between relative phalangeal length (as reflected by phalangeal indices) and body mass, except for the pollex and hallux. Thus, as size increases, there is a significant decrease in the relative length of the digits when considering all prosimian taxa sampled. Regression analyses show that while the digital portion of the rays scales isometrically with body mass, the palmar/plantar portion of the rays often scales with positive allometry. Some but not all of these broadly interspecific allometric patterns remain statistically significant when effective degrees of freedom are taken into account. As is often the case in interspecific scaling, comparisons within families show different scaling trends in the cheiridia than those seen across families (i.e., lorisids, indriids, and lemurids exhibit rather different allometries). The interspecific pattern of positive allometry that appears to best characterize the metapodials of prosimians, especially those of the foot, parallels differences found in the morphology of the volar skin. Indeed, relatively longer metapodials appear to covary with flatter and more coalesced volar pads, which in turn slightly improve frictional force for animals that are at a comparative disadvantage while climbing because of their larger mass. Despite the essentially isometric relationship found between digit length and body mass across prosimians, examination of the residual variation reveals that tarsiers and Daubentonia possess, relative to their body sizes, remarkably long fingers. Such marked departures between body size and finger length observed in these particular primates are closely linked with specialized modes of prey acquisition and manipulation involving the hands.     

The secrets of lemur teeth

New tools are available for teasing out aspects of life‐history variation among extinct species. Here we summarize research on the life histories of the extinct lemurs of Madagascar. There is a wide range of variation in dental developmental timing among these species, from among the most accelerated (Palaeopropithecus) to among the most prolonged (Hadropithecus) within the Order Primates. Rather than reflecting variation in body size, this diversity appears to relate to niche characteristics and encephalization.