Life history of Eulemur fulvus rufus from 1988-1998 in southeastern Madagascar

In this study, we compare the life-history patterns of male and female Eulemur fulvus rufus based on longitudinal data collected on individuals from two study groups from 1988-1998 in southeastern Madagascar. Mean group size was 9.5 individuals, and groups either contained more adult males than females or equal numbers of both sexes. Females reproduced for the first time between 2 and 4 years of age and reproduced each year, although the mean interbirth interval between surviving offspring was 2.1 years. An average of two adult females reproduced annually in each social group, and age and body weight may positively influence reproductive success. Females also appear to be philopatric but not female-bonded. Young natal males immigrated between 3 and 4.5 years of age and may join a new group within 612 months based on the age of emigrants. Once in a social group, they remained until old age, although a male's spatial position in the social group varied with age. Young nonnatal males were members of the social core and had the first opportunity to mate with all estrous females. Older males were peripheral to the social group and mated with females later in their cycle. We hypothesize that group size, the number of females in the group, and individual variation in reproductive success is influenced by several ecological conditions at this site: extreme variability in food availability during reproductive periods, the lack of large food patches, low plant species diversity, and small numbers of important aseasonal food sources such as Ficus species.     

Effects of Transect Selection and Seasonality on Lemur Density Estimates in Southeastern Madagascar

I investigated how transect type (trails vs. cut transects) and seasonality influenced density estimates for 5 lemur taxa (Avahi laniger, Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus) in the Vohibola III Classified Forest in SE Madagascar. I surveyed tree height and diameter and lemur populations from June 1 to December 28, 2004 along 2 1250-m trails local people used and 2 1250-m transects cut parallel to the trails in primary rain forest. Despite dendrometric variations within and between trails and transects, only density estimates of Hapalemur griseus griseus differed significantly by transect type. The spatial variation may be a result of removal by local people of giant bamboo, which is the main food for Hapalemur griseus griseus, along trails. Conversely, seasonality influenced density estimates for Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus. The temporal variations may be related to seasonal torpor for Cheirogaleus major and increased detection probabilities during periods of fruit exploitation for Eulemur rubriventer, Microcebus rufus, and Hapalemur griseus griseus. Transect type and seasonality did not affect density estimates for Avahi laniger, which may be related to the highly folivorous and low-energy diet of the nocturnal lemur. Researchers surveying lemurs along line transects should be aware that transect selection may influence density estimates for Hapalemur griseus griseus and that seasonality may influence density estimates for Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, and Microcebus rufus.     

Sexual Dichromatism and Female Preference in Eulemur fulvus Subspecies

We experimentally tested the hypothesis that sexual dichromatism in the subspecies of Eulemur fulvus is the evolutionary result of female preference for brightly colored males. Ten female lemurs representing 6 different subspecies of Eulemur fulvus were subjects in the experiment; controls were 4 females of non-sexually dichromatic lemurid taxa. For each taxon we presented photographs of the face of a male of that taxon whose colors had been digitally altered to make him less and more colourful. Median viewing times of the pooled female Eulemur fulvus are significantly correlated with colorfulness. Viewing times in the control females are not correlated with color or brightness of the stimulus photographs. We concluded that the females of the Eulemur fulvus sspp. preferred to view photographs of more colorful males, which is consistent with the predictions of sexual selection theory.     

Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences

The brown lemurs (Eulemur fulvus) include seven subspecies, whose evolutionary relationships remain contentious. In particular, it is unclear whether the Malagasy and Comorian E. f. fulvus populations are differentiated at the subspecific level (E. f. mayottensis). Furthermore, it has been suggested that E. f. collaris and E. f. albocollaris are separate species. Analyses of approximately 2400 bp of mitochondrial DNA sequence data from part of the COIII gene, together with complete genes for ND3, ND4L, and ND4 and 5 tRNAs, resolved 34 E. fulvus specimens into six clades: ((albocollaris, collaris) (rufus (rufus (fulvus/mayottensis (albifrons/fulvus/sanfordi))))). Based on the information available and our analyses we conclude that E. f. albocollaris and E. f. collaris do not represent species distinct from E. fulvus and that Comorian brown lemurs do not deserve subspecific rank. No genetic differentiation was detected between E. f. albifrons and E. f. sanfordi; on the other hand, there are obviously two separate lineages of E. f. rufus.     

Spatial memory during foraging in prosimian primates: Propithecus edwardsi and Eulemur fulvus rufus

A variety of anthropoids travel efficiently from one food source to another, although there is disagreement over how this is accomplished over large-scale space. Mental maps, for example, require that animals internally represent space, geometrically locate landmarks, use true distance and direction, and generate novel shortcuts to resources. Alternately, topological or route-based maps are based on a network of fixed points, landmarks and routes so that one food patch can be linked with another. In this study we describe travel patterns between food sources for two prosimian species found in southeastern Madagascar, Propithecus edwardsi and Eulemur fulvus rufus. Both species are dependent on fruit and have large home range sizes. By comparing interpatch distances, patch size and turning angles, we found that both species prefer nearest neighbor food patches and P. edwardsi travels in relatively straight lines. The amount of backtracking seen in E. f. rufus may be linked to their large group size and dependence on large-crowned fruit trees. We suggest that the goal-oriented foraging of both prosimian species is dependent on a topological or route-based map. These are rare behavioral data relevant to ecological and social contexts of primate cognitive evolution.     

Habitat use and social structure of a brown lemur hybrid population in the Berenty Reserve, Madagascar

The population of brown lemurs has rapidly grown since their founders were introduced to the Berenty Reserve. The founders consist of two species (Eulemur fulvus rufus and E. collaris). To characterize the behavior of the population and to examine whether these characteristics affect population growth, I investigated the habitat use and social structure of the population of brown lemurs at Berenty (Berenty Eulemur). Behavior data were collected focusing on horizontal and vertical habitat use, activity rhythms, and intergroup relationships. These data were compared with the data of E. fulvus in other areas, with the previous studies done at Berenty, and with data on Berenty Lemur catta. Berenty Eulemur maintained a home range size comparable to E. f. rufus in the western deciduous dry forest, but was found at a lower level of the forest and had larger overlapping home ranges. Berenty Eulemur use food resources earlier in the morning than L. catta, intergroup conflict was avoided by vocal communication, and Berenty Eulemur made suitable use of their limited habitat. I suggest that a number of behavioral characteristics of Berenty Eulemur may contribute to their population growth.     

Surveys of sympatric lemurs at Anjamena, north-west Madagascar

In order to assess the status of lemurs along the lower reaches of the Mahavavy in north-west Madagascar, we carried out transect line sampling at Anjamena between April and August 1995. These data were complemented by additional absence–presence surveys conducted in 1994 and 1995 in many of the remaining forested areas of the region. This is the first study of lemur population density estimates for the faunal subregion between the rivers Mahavavy and Betisboka. Six sympatric lemurs are found at Anjamena: Cheirogaleus medius, Eulemur fulvus rufus, E. mongoz, Lepilemur sp., Microcebus murinus and Propithecus verreauxi coronatus. Data suggest that in some parts of the region large numbers of lemurs may still be found (E. f. rufus 121 individuals per km², E. mongoz (45), Lepilemur sp. (110), M. murinus (85) and P. v. coronatus (173)). No density data are provided for C. medius. In conclusion, as high lemur population densities may still be found and, in particular, P. v. coronatus is not known to exist in any protected area, Anjamena could serve as an important addition to the protected area system of north-west Madagascar.     

Edge effects and their influence on lemur density and distribution in Southeast Madagascar

Edge effects are caused by the penetration of abiotic and biotic conditions from the matrix into forest interiors. Although edge effects influence the biogeography of many tropical organisms, they have not been studied directly in primates. Edge effects are particularly relevant to lemurs due to the loss of 80-90% of forests in Madagascar. In this study, data are presented on how biotic edge effects influenced the distribution and density of lemurs in the Vohibola III Classified Forest in southeastern Madagascar. In total, 415 lemur surveys were conducted during June-October 2003 and May-September 2004 along six 1,250-m transects that ran perpendicular to the forest edge. Data were also collected on lemur food trees along the six transects (density, height, diameter at breast height, area, volume, and distance to forest edge). Four nocturnal species (Avahi laniger, Cheirogaleus major, Lepilemur microdon, and Microcebus rufus) and four diurnal species (Eulemur rubriventer, Eulemur fulvus rufus, Hapalemur grisesus griseus, and Propithecus diadema edwardsi) were sighted during surveys. Regression analyses of lemur densities as a function of distance to forest edge provided edge tolerances for A. laniger (edge-tolerant), M. rufus (edge-tolerant), E. rubriventer (edge-tolerant or omnipresent), and H. g. griseus (omnipresent). The density and distribution of M. rufus and their foods trees were correlated. Edge-related variations in food quality and predation pressures may also be influencing lemurs in Vohibola III. Tolerance for edge effects may explain, in part, how lemurs have survived extreme habitat loss and forest fragmentation in southeastern Madagascar.     

Female dominance in blue-eyed black lemurs(Eulemur macaco flavifrons)

Female dominance is unusual among mammals and has been described in detail for only a handful of species. Here we present data on the frequency and outcome of dominance interactions in seven semi-free ranging and captive groups of blue-eyed black lemurs (Eulemur macaco flavifrons) housed at the Duke University Primate Center. We collected over 260 hours of focal data during which all occurrences of dominant-subordinate interactions were recorded. We collected data outside the typical breeding and birthing seasons for this species, thus eliminating possible confounding factors and increased aggression associated with these periods. We found that females were dominant over males in all seven groups, with females winning 99% of all dominance interactions.E. m. flavifrons used aggressive dominance (e.g. chase, cuff, bite) in 81% of all interactions, with the remainder of interactions being decided using social dominance (e.g. deference in the form of supplants or cowers). Older females were dominant over younger females in two out of three multi-female groups (in each case, younger females were daughters), and younger males (sons of the dominant female) received less aggression from females than did older males (n = 2 groups). Caging and group size appear to play a minimal role in the expression of female dominance. While confirmation must await further observations on free-ranging groups ofE. m. flavifrons, our data strongly suggest that this subspecies can be characterized as female dominant.     

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.     

Female reproductive competition in Eulemur rufifrons: eviction and reproductive restraint in a plurally breeding Malagasy primate

In mammals with female philopatry, co-resident females inevitably compete with each other for resources or reproductive opportunities, thereby reducing the kin-selected benefits of altruism towards relatives. These counteracting forces of cooperation and competition among kin should be particularly pronounced in plurally breeding species with limited alternative breeding opportunities outside the natal group. However, little is still known about the costs of reproductive competition on females' fitness and the victims' potential counter-strategies. Here we summarize long-term behavioural, demographic and genetic data collected on a plurally breeding primate from Madagascar to illuminate mechanisms and effects of female reproductive competition, focusing on forcible eviction and potential reproductive restraint. The main results of our study indicate that females in groups of redfronted lemurs (Eulemur rufifrons) above a critical size suffer from competition from their close relatives: females in larger groups face an increased probability of not giving birth as well as a higher probability of being evicted, especially during the annual mating and birth seasons. Eviction is not predicted by the number of adult females, the number of close female relatives, female age or inter-annual variation in rainfall but only by total group size. Thus, eviction in this species is clearly linked with reproductive competition, it cannot be forestalled by reproductive restraint or having many relatives in the group, and it occurs in the absence of a clear dominance hierarchy. Our study therefore also underscores the notion that potential inclusive fitness benefits from living with relatives may have been generally over-rated and should not be taken for granted.     

Dietary and dental variations in the genus Lemur, with comments concerning dietary-dental correlations among Malagasy primates.

Field studies of feeding in the lemur subspecies Lemur fulvus rufus and L. f. mayottensis have revealed that feeding patterns within a single species can be markedly different, both regionally and seasonally. Thus L. f. rufus is a dietary specialist (3 plant species accounting for 80-90% of feeding time), and is highly folivorous, especially during the dry season (90% of feeding time spent eating leaves during the dry season, and 53% during the wet season). On the other hand, L. f. mayottensis is more generalized dietarily (the parts of 12 plant species accounting for 90% of feeding time), and is primarily frugivorous (64% of feeding time spent eating fruit, with a monthly maximum during the wet season of 79%. In both these respects, L. f. mayottensis resembles L. catta are more closely thant it does L. f. rufus. When size differences are corrected for, Lemur fulvus rufus has significantly longer second lower molar shearing crests than does L. f. mayottensis. Other folivorous Malagasy strepsirhines also tend to have long shearing crests than frugivorous forms. Some data on cheirogaleines also suggest that the more insectivorous species have better developed molar crests than frugivorous species. Some apparent exceptions to this pattern are noted, especially for Lemur catta, which in certain functional respects dentally more closely resembles L. f. rufus than L. f. mayottensis. The problems of dietary classifications are discussed.     

Demography, range use, and behavior in black lemurs (Eulemur macaco macaco) at Ampasikely, northwest Madagascar

We studied a black lemur population over a 2-year period (1992-1993) and 8 years later (2000) in a 50-ha secondary forest in northwest Madagascar. All of the animals were marked to investigate population dynamics and seasonal variation in ranging and behavior, and new data on black lemurs were obtained. Our data on demographic characteristics were expanded to include other forest sites and contrasted with those collected in other Eulemur macaco macaco field studies, in relation to human activity and the presence of introduced and cultivated plant species. Density is affected by deforestation and hunting. Group size and home range depend on the composition of the forest and probably food patches. Sex ratio at birth varies according to the number of females per group, a result that fits the local resource competition model. Groups are multimale-multifemale, and adult females form the core of the groups. Reproductive parameters indicate sharply defined seasonal breeding, a high female reproductive rate, and birth synchrony. Changes in group composition reveal male and female juvenile dispersal, male transfer between groups at the time of mating, and adult female transfer and group fission when groups exceed a critical size. At mating and birth, intergroup agonistic encounters occurred at home-range boundaries, and larger groups were dominant over smaller groups. Patterns of intragroup interactions suggest that males compete for access to groups of females during the mating season, and that females may compete for food resources during the birth season. Our study also reports female social dominance and lack of sexual weight dimorphism in this species.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

Phylogeny and character behavior in the family Lemuridae

A phylogenetic analysis of the family Lemuridae was accomplished using multiple gene partitions and morphological characters. The results of the study suggest that several nodes in the lemurid phylogeny can be robustly resolved; however, the relationships of the species within the genus Eulemur are problematically nonrobust. The genus Varecia is strongly supported as the basal genus in the family. Hapalemur and Lemur catta are strongly supported as sister taxa and together are the sister group to the genus Eulemur. E. mongoz is the most basal species in the genus Eulemur. E. fulvus subspecies form a monophyletic group with three distinct lineages. E. coronatus is strongly supported as the sister taxon to E. macaco. The relationships of E. rubriventer, E. fulvus, and the E. macaco-E. coronatus pair are unresolved. Our combined molecular and morphological analysis demonstrates the lack of influence that morphology has on the simultaneous analysis tree when these two kinds of data are given equal weight. The effects of several extreme weighting schemes (removal of transitions and of third positions in protein-coding regions) and maximum-likelihood analysis were also explored. We suggest that these other forms of inference add little to resolving the problematic relationships of the species in the genus Eulemur.     

Social thermoregulation in redfronted lemurs (Eulemur fulvus rufus)

Pronounced seasonality, with temperatures dropping as low as 5 degrees C during the dry season, has led to the hypothesis that Malagasy lemurs face cold stress and respond to this by inactivity and social thermoregulation, i.e. resting in tight body contact with conspecifics. Compared to anthropoids, lemur groups are comprised of an unusually high number of males, leading to an even or slightly male-biased adult sex ratio. According to one hypothesis, females may benefit from these surplus males in their groups if males huddle with females. The results of this study on redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest, Madagascar revealed that the animals indeed responded to cold ambient temperatures by increased inactivity and the formation of huddling groups. However, surplus males did not participate more frequently than expected in huddling groups with females and females do not, therefore, benefit from the high number of males in their groups by increased social thermoregulation.     

Genetic assessment of a white-collared x red-fronted lemur hybrid zone at Andringitra,Madagascar

We examined a purported lemur (Eulemur fulvus rufusxE. albocollaris) hybrid zone at Andringitra, Madagascar, using sequences from five genes (one mitochondrial gene (d-loop) and four nuclear introns (hemopexin, malic enzyme, ceruloplasmin, and microsatellite 26 flanking region)), from 60 individuals (E. albocollaris (n = 16), E.f. rufus (n = 14), E. collaris (n = 9), and purported hybrids from Andringitra (n = 21)). Diagnostic (d-loop and microsatellite 26) and private sites (all other genes) were found in all gene regions for E. albocollaris and E.f. rufus. Also, private sites were found for the purported hybrid population in two gene regions (d-loop and ceruloplasmin). When the putative hybrids were examined for diagnostic and private markers, 18 of 21 were found to contain markers from both E. albocollaris and E.f. rufus populations. The remaining three individuals were found to contain only markers for E. albocollaris. These results indicate that the population at Andringitra is a hybrid population between E. albocollaris and E.f. rufus.     

Spatial variations in Eulemur fulvus rufus and Lepilemur mustelinus densities in Madagascar

I present data on variations in Eulemur fulvus rufus and Lepilemur mustelinus densities as well as tree characteristics (height, diameter and stem frequency) between edge and interior forest habitats in southeastern Madagascar. Line transect surveys were conducted from June 2003 to November 2005 in edge and interior forest habitats in the Vohibola III Classified Forest. Although E. f. rufus densities were significantly lower in edge habitats than in interior habitats, density estimates for L. mustelinus did not differ significantly between habitats. Trees in edge habitats were significantly shorter, had smaller diameters and had lower stem frequencies (for those >25 cm in diameter) than trees in interior habitats. Spatial characteristics of food abundance and quality may explain lemur density patterns in Vohibola III. Low E. f. rufus densities may reduce seed dispersal in edge habitats, which has important consequences for the long-term viability of forest ecosystems in Madagascar.     

Female Coordination of Group Travel in Wild Propithecus and Eulemur

Coordination of primate group movements by individual group members is generally categorized as leadership behavior, which entails several steps: deciding where to move next, initiating travel, and leading a group between food, water sources, and rest sites. Presumably, leaders are able to influence their daily foraging efficiency and nutritional intake, which could influence an individual's feeding ecology and long-term reproductive success. Within anthropoid species, females lead group movements in most female-bonded groups, while males lead groups in most nonfemale-bonded groups. Group leadership has not been described for social prosimians, which are typically not female-bonded. We describe group movements in two nonfemale-bonded, lemurid species living in southeastern Madagascar, Propithecus diadema edwardsi and Eulemur fulvus rufus. Although several social lemurids exhibit female dominance Eulemur fulvus rufus does not, and evidence for female dominance is equivocal in Propithecus diadema edwardsi. Given the ecological stresses that females face during reproduction, we predict that females in these two species will implement alternative behavioral strategies such as group leadership in conjunction with, or in the absence of, dominance interactions to improve access to food. We found that females in both species initiated and led group movements significantly more often than males did. In groups with multiple females, one female was primarily responsible for initiating and leading group movements. We conclude that female nutritional needs may determine ranging behavior to a large extent in these prosimian species, at least during months of gestation and lactation.     

Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs

Data collected on the feeding behavior, food intake, and chemical analyses of plant foods were used to document seasonal variation in diet and nutrition in Eulemur mongoz in northwestern Madagascar. E. mongoz conforms to the general Eulemur dietary pattern, with a predominantly frugivorous diet supplemented mainly by leaves, flowers, and nectar. Phytochemical analysis revealed high water contents in all the main plant foods; mature fruit and flowers contained the most water-soluble carbohydrates; immature leaves were richest in protein and essential amino acids; the limiting amino acids in all plant foods were methionine and cystine; ash (mineral) content was highest in petioles and mature leaves; crude lipid content was highest in seeds; and crude fiber content was indistinguishable between immature and mature fruit and leaves. High-fiber foods were eaten during both seasons; the wet season diet was dominated by high-energy foods (mature fruit, nectar, and seeds), while the dry season diet contained foods high in energy (mature fruit and flowers) and high in protein (immature leaves) and minerals (mature leaves and petioles). However, nutrient intake did not vary between seasons, implying that nutrient requirements are met throughout the year. These results suggest we draw more conservative conclusions when interpreting dietary variability in the absence of chemical analysis, and also draw into question the idea that nutritional stress is a factor in the timing of reproduction in lemurs and, by extension, is linked to the prevalence of female dominance and small group size in lemurs.