Eulemur Fulvus Research Articles

THIS ARTICLE HAS BEEN RETRACTED: Enumeration of objects and substances in non‐human primates: experiments with brown lemurs (Eulemur fulvus)

AbstractBoth human infants and adult non‐human primates share the capacity to track small numbers of objects across time and occlusion. The question now facing developmental and comparative psychologists is whether similar mechanisms give rise to this capacity across the two populations. Here, we explore whether non‐human primates’ object tracking abilities are subject to the same constraints as those of human infants. In particular, we examine whether one primate species, the brown lemur (Eulemur fulvus), also fails to represent and enumerate objects when they behave non‐rigidly or non‐cohesively. We presented lemurs with a series of expectancy violation studies involving simple 1 + 1 addition events in which we varied the entities to be enumerated. Like infants, lemurs successfully enumerated the two objects when those objects were rigid, cohesive individuals, but failed to enumerate similar‐looking non‐rigid piles of sand. In contrast to human infants, however, lemurs successfully enumerated non‐cohesive objects that broke into multiple pieces. These results are discussed in light of recent theories about object processing in human infants and adults.

Individual Facial Coloration in Male Eulemur fulvus rufus: A Condition-dependent Ornament?

Researchers studying individual variation in conspicuous skin coloration in primates have suggested that color indicates male quality. Although primate fur color can also be flamboyant, the potential condition dependence and thus signaling function of fur remains poorly studied. We studied sources of variation in sexually dichromatic facial hair coloration in red-fronted lemurs (Eulemur fulvus rufus). We collected data on 13 adult males in Kirindy Forest, Madagascar, during two study periods in 2006 and 2007, to determine whether variation in facial hair coloration correlates with male age, rank, androgen status, and reproductive success. We quantified facial hair coloration via standardized digital photographs of each male, assessed androgen status using fecal hormone measurements, and obtained data on reproductive success through genetic paternity analyses. Male facial hair coloration showed high individual variation, and baseline coloration was related to individual androgen status but not to any other parameter tested. Color did not reflect rapid androgen changes during the mating season. However, pronounced long-term changes in androgen levels between years were accompanied by changes in facial hair coloration. Our data suggest that facial hair coloration in red-fronted lemur males is under proximate control of androgens and may provide some information about male quality, but it does not correlate with dominance rank or male reproductive success.

Behavior and diet of the Critically Endangered Eulemur cinereiceps in Manombo forest, southeast Madagascar

Manombo Special Reserve is a parcel of rainforest along the southeastern coast of Madagascar, containing eight lemur species, including the White-collared brown lemur (Eulemur cinereiceps [Eulemur albocollaris]). Following a drastic cyclone in the region in January of 1997, the population of E. cinereiceps at Manombo was reduced by half. Results indicate that individuals of this critically endangered species at Manombo consume a total of 54 plant species belonging to 24 families, with over two - thirds of the diet comprised of ripe and unripe fruits. White - collared brown lemurs also opportunistically feed on novel food items and invasive plants in their recovering habitat. We report the first record of E. cinereiceps consuming a shelf fungus species growing on invasive trees. During feeding, lemurs tore pieces of the fungus from the trees with their hands and mouth (chewing cycle duration mean 0.28 s; SD 0.01). White - collared brown lemurs also consumed spicy fruits of a non - native plant species (Aframomum angustifolium) growing in highly disturbed open areas. Feeding bouts typically began by stripping away the outer covering with the anterior dentition, with pulp and seeds then consumed (chewing cycle duration mean 0.22 s; SD 0.005). This is the first record of consumption of either of these resources for any lemur species at Manombo. Ability to feed on items like A. angustifolium may permit E. cinereiceps to avoid competition with other species in this highly degraded forest environment.

Bushmeat hunting and use in the Makira Forest, north-eastern Madagascar: a conservation and livelihoods issue

In the 2003 Durban Vision the Malagasy government committed to tripling the amount of protected areas in Madagascar by 2009. This extensive expansion needs to involve an assessment of the potential impacts on the people who rely on forest resources for subsistence. Wildlife for human consumption (bushmeat) is one such resource that has received great attention on mainland Africa but has largely been ignored in Madagascar until recently. In terms of biomass, hunting in Madagascar appears to be on a lesser scale compared to areas of mainland Africa. However, because of the life-history characteristics associated with hunted primate and carnivore species in Madagascar even small-scale hunting is a major threat to long-term conservation. In this study I used semi-structured interviews to quantify annual rates of bushmeat harvest in 14 villages adjacent to the Makira Forest in north-eastern Madagascar. Interviews revealed that 23 mammal species were hunted for consumption, providing a new insight into the scale and frequency of bushmeat use. Harvest data and life-history information were sufficient to allow quantitative assessments of sustainability for four species of lemur (black and white ruffed lemur Varecia variegata, indri Indri indri, eastern bamboo lemur Hapalemur griseus and white-fronted brown lemur Eulemur albifrons) and a species of the carnivore family Eupleridae (fossa Cryptoprocta ferox). Model results suggest hunting of these species is probably unsustainable. This research presents clear evidence that hunting is a major conservation and livelihoods issue in Madagascar and needs to be considered in the planning stages of protected area development to address better the needs of local people.

Anatomy and ultrasonography of the normal kidney in brown lemurs:Eulemur fulvus

The purpose of this study is to describe the anatomy and obtain echographic measurements of normal kidneys in brown lemurs (Eulemur fulvus). The anatomical findings show that brown lemur kidneys are comparable to those of rats except for an elongated papilla. The kidneys of 16 (7 females and 9 males) lemurs were examined with two-dimensional and power Doppler ultrasonography under general anesthesia. Morphometrically, the left and right kidney surface areas are comparable (3.29 and 3.51 cm(2)). Kidney area has a significant linear correlation with body weight. Echo-Doppler findings show that the mean renal arterial blood flow speeds for the left and right kidneys are comparable (0.70 and 0.73 m/s). However, flow speed is higher in the male (0.79 m/s) than in the female (0.60 m/s). The renal arterial diameters are between 1.0 and 1.8 mm. The fact that anesthesia can have hemodynamic effects on renal vasculature should be taken into consideration when assessing these echographic results.

Assessing reproductive profiles in female brown mouse lemurs (Microcebus rufus) from Ranomafana National Park, southeast Madagascar, using fecal hormone analysis

Studies on reproductive endocrinology in wild primate populations have greatly increased in the last decades owing to the development of noninvasive techniques that can be applied under field conditions. However, small-bodied nocturnal species are not well represented on the long list of primates surveyed in the wild, and reproductive inferences regarding these animals in their natural habitats have not benefited from direct observations of hormonal changes. We collected fecal samples from female brown mouse lemurs (Microcebus rufus) in a southeastern rainforest of Madagascar in order to determine whether or not fecally excreted steroid levels show a consistent pattern of change during the reproductive season and are a useful complement to reproductive observations in wild-trapped individuals. Initial data show variation in reproductive hormone levels before and after estrus and estimated day of parturition. Elevated levels of excreted estradiol (E(2)) were observed around the time of estrus, whereas high levels of fecal progesterone (P) were seen during later stages of pregnancy and around parturition. A more complete picture of reproductive profiles in female mouse lemurs, and how they may change over the life span, can be obtained if hormone analyses are used to supplement field observations.

Genetic analysis of hybridization and introgression between wild mongoose and brown lemurs

BackgroundHybrid zones generally represent areas of secondary contact after speciation. The nature of the interaction between genes of individuals in a hybrid zone is of interest in the study of evolutionary processes. In this study, data from nuclear microsatellites and mitochondrial DNA sequences were used to genetically characterize hybridization between wild mongoose lemurs (Eulemur mongoz) and brown lemurs (E. fulvus) at Anjamena in west Madagascar.ResultsTwo segments of mtDNA have been sequenced and 12 microsatellite loci screened in 162 brown lemurs and mongoose lemurs. Among the mongoose lemur population at Anjamena, we identified two F1 hybrids (one also having the mtDNA haplotype of E. fulvus) and six other individuals with putative introgressed alleles in their genotype. Principal component analysis groups both hybrids as intermediate between E. mongoz and E. fulvus and admixture analyses revealed an admixed genotype for both animals. Paternity testing proved one F1 hybrid to be fertile. Of the eight brown lemurs genotyped, all have either putative introgressed microsatellite alleles and/or the mtDNA haplotype of E. mongoz.ConclusionIntrogression is bidirectional for the two species, with an indication that it is more frequent in brown lemurs than in mongoose lemurs. We conclude that this hybridization occurs because mongoose lemurs have expanded their range relatively recently. Introgressive hybridization may play an important role in the unique lemur radiation, as has already been shown in other rapidly evolving animals.

Sociogenetic structures, dispersal and the risk of inbreeding in a small nocturnal lemur, the golden–brown mouse lemur (Microcebus ravelobensis)

Summary Natal dispersal reduces the risk of inbreeding, since it is typically biased towards one sex. Golden-brown mouse lemurs {Microcebus ravelobensis) form mixed-sex sleeping groups whose genetic composition is not yet known. This study investigates the composition of eight sleeping groups and the dispersal pattern in a free-living population of this nocturnal primate. Genetic relatedness and parentage was calculated for 101 individuals (43 males, 58 females) based on microsatellite analyses. Matrilinear relatedness played a major role in the composition of sleeping groups. Co-sleepers were significantly more closely related than members of different sleeping groups. Dispersal was not strongly biased towards one sex. More than 50% of all potential sons (N = 19) and daughters (N = 26) remained in their natal range well into their first mating season, but potential sons disappeared more frequently than daughters lateron. These data indicate that many sons may have delayed their dispersal. This delayed dispersal may have increased the risk of inbreeding, since closely related males and females stayed within one home range diameter of each other quite regularly in the mating season. In fact, two definite cases of inbreeding were detected. The likely benefits of delayed dispersal are discussed in view of the confirmed cases of inbreeding.

Gaze following and gaze priming in lemurs

Although primates have often been found to co-orient visually with other individuals, members of these same species have usually failed to use co-orientation to find hidden food in object-choice experiments. This presents an evolutionary puzzle: what is the function of co-orientation if it is not used for a function as basic as locating resources? Co-orientation responses have not been systematically investigated in object-choice experiments, and requiring co-orientation with humans (as is typical in object-choice tasks) may underestimate other species' abilities. Using an object-choice task with conspecific models depicted in photographs, we provide experimental evidence that two lemur species (Eulemur fulvus, n = 4, and Eulemur macaco, n = 2) co-orient with conspecifics. Secondly, by analysing together two measures that have traditionally been examined separately, we show that lemurs' gaze following behaviour and ultimate choice are closely linked. Individuals were more likely to choose correctly after having looked in the same direction as the model, and thus chose objects correctly more often than chance. We propose a candidate system for the evolutionary origins of more complex gaze following: 'gaze priming.'

Comparison of Biomedical Evaluation for White-Fronted Brown Lemurs (Eulemur fulvus albifrons) from Four Sites in Madagascar

Health and nutritional assessments of wildlife are important management tools and can provide a means to evaluate ecosystem health. Such examinations were performed on 37 white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar. Comparison of health parameters between sites revealed statistically significant differences in body weight, body temperature, respiratory rate, hematology parameters (white cell count, hematocrit, segmented neutrophil count, and lymphocyte count), serum chemistry parameters (aspartate aminotransferase, alanine aminotransferase, serum alkaline phosphatase, total protein, albumin, phosphorus, calcium, sodium, chloride, and creatinine phosphokinase), and nutrition parameters (copper, zinc, ferritin, retinol, tocopherol, and 25-hydroxycholecalciferol). Two of 10 lemurs tested were positive for toxoplasmosis; none of 10 were positive for Cryptosporidium or Giardia. Enteric bacteria and endo- and ectoparasites were typical. Statistically different values in hematology and chemistry values probably do not reflect clinically significant differences, whereas nutrition parameter differences are likely related to season, soil, and forage availability.

Forelimb proportions and kinematics: how are small primates different from other small mammals?

The crouched limb posture of small mammals enables them to react to unexpected irregularities in the support. Small arboreal primates would benefit from these kinematics in their arboreal habitat but it has been demonstrated that primates display certain differences in forelimb kinematics to other mammals. The objective of this paper is to find out whether these changes in forelimb kinematics are related to changes in body size and limb proportions. As primates descended from small ancestors, a comparison between living small primates and other small mammals makes it possible to determine the polarity of character transformations for kinematic and morphometric features proposed to be unique to primates. Walking kinematics of mouse lemurs, brown lemurs, cotton-top tamarins and squirrel monkeys was investigated using cineradiography. Morphometry was conducted on a sample of 110 mammals comprising of primates, marsupials, rodents and carnivores. It has been shown that forelimb kinematics change with increasing body size in such a way that limb protraction increases but retraction decreases. Total forelimb excursion, therefore, is almost independent of body size. Kinematic changes are linked to changes in forelimb proportions towards greater asymmetry between scapula and radius. Due to the spatial restriction inherent in the diagonal footfall sequence of primates, forelimb excursion is influenced by the excursion of the elongated hind limb. Hindlimb geometry, however, is highly conserved, as has been previously shown. The initial changes in forelimb kinematics might, therefore, be explained as solutions to a constraint rather than as adaptations to the particular demands of arboreal locomotion.

Mother-Young Feeding Synchrony and Early Food Selection Differences in Eulemur fulvus

I tested the hypothesis that mother-young cofeeding correlates with a systematic similar food selection in wild Mayotte brown lemurs (Eulemur fulvus). I simultaneously recorded the feeding behavior of 4 maternal dyad members, from infant birth to weaning, and 10–12 mo of juvenile age, during 10-min focal periods, each separated by 5-min intervals over 10 mo. I recorded the solid food items selected for each feeding behavior at the level of specific plant part, along with the distance between the 2 individuals. I considered feeding behaviors simultaneous (between the young lemurs and their mothers) when the young began to eat a food item while the mother was already eating, regardless of the separation distance. During their first year, most of the feeding events of the young brown lemurs were initiated by their mothers. However, infants also selected different food items from those chosen by their mothers in almost one-third of cases, and the food selection dissimilarity was not attributable to an increase in the distance of separation. For juveniles, dissimilar food selection was significantly lower and linked to an increase in mother-juvenile separation distance. Thus, the substantial proportion of dissimilarity in solid foods selected by the infant during the synchronized feeding behaviors strongly suggests that social influences were not food-specific and might instead drive the acquisition of group feeding activity rhythm rather than food selection habits.

Proximate and ultimate determinants of cathemeral activity in brown lemurs

Among primates, only two lemur genera, Eulemur and Hapalemur, and a population of the platyrrhine Aotus azarai are known to be cathemeral (i.e. show a mixture of daytime and night-time activity). Given the rarity of this phenomenon in primates except for Malagasy lemurs, its proximate and ultimate factors are still debated. The adaptive reasons for this apparently odd lifestyle are mainly based on four not mutually exclusive hypotheses: thermoregulatory benefits, antipredator strategy, competition avoidance and metabolic dietary-related needs. However, little effort has been made to tease apart proximate cues from potential ultimate factors in the multivariate context of activity correlates. To investigate these hypotheses, we compared the year-round cathemeral activity of two groups of Eulemur collaris and one group of hybrids E. collaris × Eulemur fulvus rufus in a humid littoral and in a dry gallery forest of southern Madagascar. Data were collected using a 5 min instantaneous method, with sampling equally distributed between day and night. We weighted the different effects of proximate and ultimate factors via the ANCOVA analysis using as the dependent variable the ratio between diurnal and nocturnal activity. Photoperiodic changes and nocturnal luminosity were the two proximate factors that accounted for most of the variability at the two sites. Diet quality was the only ultimate factor that had a significant effect on the diurnality index of the two lemur populations, suggesting a role of metabolic dietary-related needs in determining cathemeral activity in these lemurs.

A natural history of the brown mouse lemur

A natural history of the brown mouse lemur

Market effects offset the reciprocation of grooming in free-ranging redfronted lemurs, Eulemur fulvus rufus

Social grooming is a commonly observed affiliative behaviour in primates. Grooming has been suggested to represent a service in a biological marketplace, exchanged either for grooming or for other social commodities or services. Accordingly, grooming is predicted to be approximately reciprocated within a dyad when no other services are being exchanged, but it should be more asymmetrical if partners have different quantities of other services to offer. We analysed 412 grooming bouts observed in four groups of free-ranging redfronted lemurs to test this prediction. Grooming in this species seems to take place in a highly reciprocal manner because partners usually alternate in the roles of groomer and gromee within a grooming bout. However, within dyads there were asymmetries in the duration of grooming given and received. In both sexes, more grooming was directed from low-ranking towards high-ranking individuals than vice versa, and in males this asymmetry became more pronounced as the number of subordinates per group increased. Grooming in bisexual dyads was generally skewed in favour of males, but patterns of grooming between the sexes were less clear than within the sexes. In addition, aggression occurred at high frequencies between classes of individuals that were characterized by nonreciprocal grooming, suggesting that grooming may serve as a means to reduce aggression in dyads with a high potential for conflicts. Taken together, our results indicate that a strict reciprocation of grooming can be offset by power differentials between partners, where grooming appears to be traded by subordinates in exchange for the tolerance of dominants.

Object permanence in lemurs

Object permanence, the ability to mentally represent objects that have disappeared from view, should be advantageous to animals in their interaction with the natural world. The objective of this study was to examine whether lemurs possess object permanence. Thirteen adult subjects representing four species of diurnal lemur (Eulemur fulvus rufus, Eulemur mongoz, Lemur catta and Hapalemur griseus) were presented with seven standard Piagetian visible and invisible object displacement tests, plus one single visible test where the subject had to wait predetermined times before allowed to search, and two invisible tests where each hiding place was made visually unique. In all visible tests lemurs were able to find an object that had been in clear view before being hidden. However, when lemurs were not allowed to search for up to 25-s, performance declined with increasing time-delay. Subjects did not outperform chance on any invisible displacements regardless of whether hiding places were visually uniform or unique, therefore the upper limit of object permanence observed was Stage 5b. Lemur species in this study eat stationary foods and are not subject to stalking predators, thus Stage 5 object permanence is probably sufficient to solve most problems encountered in the wild.

Berenty 2006: Census of Propithecus verreauxi and Possible Evidence of Population Stress

We provide a survey of a folivorous lemur, Propithecus verreauxi (sifaka), in the Berenty Reserve, southern Madagascar. Higher densities of folivores in small patches occur in either high-quality food areas or in less disturbed refugia. The skewness of sex ratio, which in lemurs is often male-biased, can be critically exacerbated in population stress. We predicted that sifaka would show higher densities in areas where protein-rich food is abundant (prediction 1a) and in refugium areas (prediction 1b). Owing to increased competition by brown and ring-tailed lemurs and decreased food production by tamarind trees, we expected an extremely male-biased sex ratio (prediction 2). In November–December 2006, we counted and sexed 206 adult/subadult sifaka (49 groups) during daily walks in different forest zones (Ankoba secondary forest, to the north, Malaza gallery/scrub areas, and spiny forest, to the south). Sifaka may have decreased in the gallery forest to concentrate in Ankoba (in a sort of out-of-Malaza). The area contains protein-rich food (prediction 1a confirmed). Sifaka are proportionally more concentrated in the spiny area than in the degraded scrub forest (prediction 1b confirmed). The sex ratio is extremely male biased, possibly due to either high sifaka density, in Ankoba, or food availability reduction, in Malaza (prediction 2 confirmed). The sifaka population seems to be under stress: researchers need to resume demographic studies, interrupted in Berenty in the mid-1980s, to preserve in situ a species that is difficult to protect ex situ.

What is it going to be? Pattern and potential function of natal coat change in sexually dichromatic redfronted lemurs (Eulemur fulvus rufus)

In some primate species, pelage colorations at birth contrast with adult colorations. The intensity of natal coats and their phylogenetic distribution is highly variable within primates. Natal coat coloration seems to change to adult coloration in most species when infants become independent from their mothers, but an accepted functional explanation for natal coats is not available. Here we describe pelage coloration change in sexually dichromatic redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest, and propose a new functional hypothesis for this phenomenon. In this species, infants are born with adult male coloration and female infants subsequently undergo a change in coloration. Using digital pictures and behavioral data collected on eight mother-offspring dyads from birth until the end of the coloration change, we 1) described timing and pattern of pelage developmentin redfronted lemur infants and 2) examined behavioral developmental correlates of the coloration change. The color change took place between 7 and 17 weeks of age and coincided with advanced physical independence; a pattern also found in monochromatic primate species with natal coats. No behavioral differences between male and female infants were found. Hypotheses about the ultimate function of natal coats focusing on enhanced infant care or reduced infanticide risk did not explain the pelage change in redfronted lemurs. The natal pelage pattern in this species may instead serve as sexual mimicry. Accordingly, female infants may mimic males during the most vulnerable developmental phase to avoid sex-specific aggression by adult females in a species with intense female-female aggression and competition.

Diurnality and nocturnality in nonhuman primates: comparative chronobiological studies in laboratory and nature

Looking for differences in circadian clock characteristics of diurnal and nocturnal nonhuman primates, this article summarizes results of chronobiological studies carried out in various nocturnal, diurnal, and cathemeral prosimian and anthropoid primate species under controlled laboratory conditions, under seminatural conditions, and in the wild. In almost all circadian parameters investigated, no differences were discernible between the two main chrono-ecotypes, either in circadian period length and the influence upon it of after-effects, of light intensity, and ambient temperature, or in the PRC, re-entrainment behavior, rhythm splitting, and internal desynchronization. Diurnal and nocturnal or cathemeral species differed only in the phase of artificial or natural LDs to which their circadian activity phase was adjusted as well as in the characteristics of masking activity upon the rhythms produced by the direct inhibiting or enhancing effects of light. Pronounced lunar periodicity—observed in the activity rhythm of nocturnal neotropical owl monkeys, genus Aotus, in seminatural and natural environments as well as in wild cathemeral Malagasy lemurs, genus Eulemur—is shown to result from masking effects of moonlight. In captive Eulemur fulvus albifrons, a change from dark-active over cathemeral to light-active behavior, without concurrently changing the circadian phase-setting of activity to D, was produced by direct masking effects of a stepwise reduction of darktime luminosity on an LD 12:12 cycle. Long-term activity recordings carried out in wild diurnal Malagasy sifakas (Propithecus verreauxi) and cathemeral redfronted lemurs (Eulemur fulvus rufus), as well as in wild nocturnal owl monkeys (Aotus a. azarai) of the North Argentinean Chaco, yielded in all species distinct bimodal long- and short-day activity patterns with pronounced peaks during dusk and dawn. Applying Pittendrigh's two-oscillator concept to these results, it is hypothesized that the differences in chrono-ecotype behavior may result from variations in internal coupling and external phase-setting of morning and evening oscillators (m, e) to dawn and dusk, interacting with direct masking effects of light.

The influence of social organisation on leadership in brown lemurs (Eulemur fulvus fulvus) in a controlled environment

Studies on leadership during group movements in several lemur species showed that females were responsible for the travelling choices concerning time and direction. Interestingly, in these species females are dominant over males. We investigated the influence of social organisation upon leadership processes by studying a lemur species in which social organisation is characterized by the absence of female dominance: the brown lemur (Eulemur fulvus fulvus). The study was conducted on a semi-free ranging group of 11 individuals and the analysis performed on 69 group movements showed that all the individuals could initiate a group movement. In 34 cases, the whole group moved. There was no significant difference in the number of start attempts or in the number of group members involved from one initiator to another. Moreover, there was no effect of sex or age of the initiator on the number of individuals following it or on the speed of the joining process. Therefore, the leadership observed is widely distributed to all group members. These results support the hypothesis of an influence of social organisation upon the decision-making processes but still remain to be studied in a more relevant ecological context.