Adult Male Scent-Marking in Lemur catta and Eulemur fulvus rufus

Scent-marking and olfactory communication are used extensively by prosimians and can provide spatial and temporal records of group movement and behavior. We compare rates of male scent-marking in relation to reproductive seasons, male dominance rank, and habitat use in two related prosimians: Lemur catta and Eulemur fulvus rufus. We collected scent-marking data on adult male Lemur catta at Beza-Mahafaly Reserve (dry forest), and on Eulemur fulvus rufus at Ranomafana National Park (rainforest), Madagascar. In Lemur, rates of overall scent-marking differed significantly by reproductive season, with higher rates occurring in mating and lactation/migration periods, whereas in Eulemur, reproductive season did not appear to affect scent-marking rates. Dominance rank of male Lemur catta did not affect rates of scent-marking. Among male Eulemur fulvus, dominance relations were not apparent; however, 2 of the 5 focal males scent-marked somewhat more frequently during the mating season and also experienced greater mating success. In Lemur catta, higher rates of scent-marking in the mating season may relate to indirect reproductive competition during a period of high aggression, while such mating competition was not as marked in Eulemur fulvus. Furthermore, higher rates of marking in resident male Lemur catta during male migration may correlate with vigilance toward immigrating males. Greater overall scent-marking rates in ring-tailed lemurs may relate to extensive intergroup home range overlap and no area of exclusive use, whereas the red-fronted lemur groups tended to forage in areas of their home range where little-to-no intergroup overlap occurred.     

Freeze-mark techniques applied to mammals at the Santa Barbara Zoo

Dichlorodifluoromethane (CCl₂F₂) was evaluated as a means of freeze-marketing ring-tailed lemurs (Lemur catta), brown lemurs (L. fulvus), and Parma wallabys (Wallabia parma). Application times of 3–6 sec on unshaven lemurs resulted in successful markings, but the wallabys failed to respond with growth of white hair to application times of 3–10 sec. The freeze-marking process caused little physical discomfort when applied to fleshy regions, and the marks appear to be permanent.     

Pitch control and speed limitation during overground deceleration in lemurid primates

An animal's fitness is influenced by the ability to move safely through its environment. Recent models have shown that aspects of body geometry, for example, limb length and center of mass (COM) position, appear to set limits for pitch control in cursorial quadrupeds. Models of pitch control predict that the body shape of these and certain other primates, with short forelimbs and posteriorly positioned COM, should allow them to decelerate rapidly while minimizing the risk of pitching forward. We chose to test these models in two non-cursorial lemurs: Lemur catta, the highly terrestrial ring-tailed lemur, and Eulemur fulvus, the highly arboreal brown lemur. We modeled the effects of changes in limb length and COM position on maximum decelerative potential for both species, as well as collecting data on maximal decelerations across whole strides. In both species, maximum measured decelerations fell below the range of pitch-limited deceleration values predicted by the geometric model, with the ring-tailed lemur approaching its pitch limit more closely. Both lemurs showed decelerative potential equivalent to or higher than horses, the only comparative model currently available. These data reinforce the hypothesis that a relatively simple model of body geometry can predict aspects of maximum performance in animals. In this case, it appears that the body geometry of primates is skewed toward avoiding forward pitch in maximal decelerations.     

Operant conditioning of scratching in lemurs

An adult femaleLemur catta and an adult femaleEulemur fulvus were given edible rewards for scratching. Both subjects learned to scratch in order to obtain the rewards, showed diminished rates of scratching during periods of extinction, and learned to scratch preferentially with one foot when required. TheLemur catta subject was more responsive to the changing experimental conditions than theEulemur fulvus. The conditionability of scratching in primates does not appear to be directly related to the widespread occurrence of scratching in simian social contexts.     

Chemical Properties of the Diets of Two Lemur Species in Southwestern Madagascar

Seasonal dietary variations demonstrate the importance of certain plant parts during the year. A parallel analysis of their nutritional constituents provides further information on underlying patterns of consumption of the plant parts and the relative importance of key nutrients. I studied the diets of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas), for 9 mo over a 13-mo period in the highly seasonal tropical dry forest site of Beza Mahafaly in southwestern Madagascar. I tested dietary plant parts for nutrients—protein, free amino acids, and sugars—and for 2 potential deterrents, phenolics and tannins, using plant extracts prepared in the field. I compared consumption of nutrients and secondary compounds throughout the year and between seasons. Nutrients are balanced throughout the year. The 2 lemur species do not appear nutrient-starved in either season, though actual quantities of nutrients and contributing food parts differ for each species. Lemur catta consumes high levels of sugar throughout the year, whereas Propithecus takes in higher levels of protein. The effects of phenolics and tannins are quantitative, and they appear to deter consumption of plant parts only past a certain threshold. Sifakas consume them in greater quantities than those of ring-tailed lemurs, which appear more sensitive to their effects. Sifakas may have a higher tolerance for secondary plant metabolites, which is consistent with reports for other folivores. The overall stability of nutrients throughout the year indicates no lean period that coincides with the decline in food abundance during the dry season, though actual caloric intake probably decreases.     

Photopigments underlying color vision in ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus)

A recent examination of color vision in the ringtail lemur produced evidence that these prosimians could make color discriminations consistent with a diagnosis of trichromatic color vision. However, it was unclear if this behavior reflected the presence of three classes of cone or whether lemurs might be able to utilize signals from rods in conjunction with those from only two classes of cone. To resolve that issue, spectral sensitivity functions were obtained from ringtail lemurs (Lemur catta) and brown lemurs (Eulemur fulvus) using a noninvasive electrophysiological procedure, electroretinographic flicker photometry. Results from experiments involving chromatic adaptation indicate that these lemurs routinely have only a single class of cone photopigment in the middle to long wavelengths (peak sensitivity of about 545 nm); they also have a short-wavelengthsensitive cone pigment with peak of about 437 nm. The earlier behavioral results are suggested to have resulted from the ability of lemurs to jointly utilize signals from rods and cones. The cone pigment complements of these lemurs differ distinctly from those seen among the anthropoids. © 1993 Wiley-Liss, Inc.     

Soil Consumption of Two Groups of Semi-free-ranging Lemurs {Lemur catta and Lemur fulvus)

Soil consumption of two Malagasy lemurs, Lemur catta and Lemur fulvus was observed in an enclosure simulating a natural habitat at Duke University Primate Center (Durham, USA). Soil eaten by L. catta contained more Na than random soil samples. Concentrations of the four major minerals in soil eaten by L. fulvus did not differ from random samples. L. fulvus stopped soil ingestion in summer when they ate large amounts of foliage rich in K and Mg, also in winters after being fed with MgCl₂. It is suggested that, in this study, soil was consumed in relation to its mineral content and not for physical properties related to its structure. Some non physiological factors that might influence food selection are discussed.     

Copulatory Plug Displacement Evidences Sperm Competition in Lemur catta

Male displacement of copulatory (sperm) plugs from female vaginas provides further evidence for sperm competition in ring-tailed lemurs (Lemur catta), a gregarious prosimian species with a multimale, multifemale mating system. During two mating seasons, I studied two groups of free-ranging ring-tailed lemurs on St. Catherines Island, GA, USA. I observed 22 mating pairs in which males achieved penile intromission. Copulatory plug displacement by males occurred in 9 cases. Plugs were displaced during copulation by male penes upon withdrawl following deep vaginal thrusting. In every case of copulatory plug displacement, the male displacing a plug mated to ejaculation with the estrous female. In a mating system in which females typically mate with more than one male during estrous, often in succession, copulatory plug displacement may function to disrupt or preclude other males' successful insemination of estrous females. The effects of sperm plug displacement on paternity in Lemur catta are unknown, as no study had heretofore documented copulatory plug displacement in this species. The first-male mating advantage suggested for Lemur catta should be re-evaluated where mating order is known, and copulatory plug displacement during mating, or lack thereof, is identified. Because there is a tendency for first-mating males to mate-guard for longer periods of time in Lemur catta, the latency period between the first mate's ejaculation and that of subsequent mates may be an important determinant of male fertilization success.     

Total Energy Expenditure and Body Composition in Two Free-Living Sympatric Lemurs

Background

Evolutionary theories that account for the unusual socio-ecological traits and life history features of group-living prosimians, compared with other primates, predict behavioral and physiological mechanisms to conserve energy. Low energy output and possible fattening mechanisms are expected, as either an adaptive response to drastic seasonal fluctuations of food supplies in Madagascar, or persisting traits from previously nocturnal hypometabolic ancestors. Free ranging ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur sp.) of southern Madagascar have different socio-ecological characteristics which allow a test of these theories: Both gregarious primates have a phytophagous diet but different circadian activity rhythms, degree of arboreality, social systems, and slightly different body size.

Methodology and Results

Daily total energy expenditure and body composition were measured in the field with the doubly labeled water procedure. High body fat content was observed at the end of the rainy season, which supports the notion that individuals need to attain a sufficient physical condition prior to the long dry season. However, ring-tailed lemurs exhibited lower water flux rates and energy expenditure than brown lemurs after controlling for body mass differences. The difference was interpreted to reflect higher efficiency for coping with seasonally low quality foods and water scarcity. Daily energy expenditure of both species was much less than the field metabolic rates predicted by various scaling relationships found across mammals.

Discussion

We argue that low energy output in these species is mainly accounted for by low basal metabolic rate and reflects adaptation to harsh, unpredictable environments. The absence of observed sex differences in body weight, fat content, and daily energy expenditure converge with earlier investigations of physical activity levels in ring-tailed lemurs to suggest the absence of a relationship between energy constraints and the evolution of female dominance over males among lemurs. Nevertheless, additional seasonal data are required to provide a definitive conclusion.     

Feeding behavior ofLemur catta andLemur fulvus

The feeding behavior of two sympatric species of lemurs, Lemur cattaand Lemur fulvus,was studied in an enclosure simulating a natural habitat at the Duke University Primate Center. L. fulvusspent less time feeding during the day than L. catta.But the former species ate more fruit and had longer feeding bouts on preferred food items than L. catta.They also had a shorter food passage time than L. cattaand their choice of resting places was more influenced by food distribution. Furthermore, the two lemur species ate parts of different plant species and showed different reactions to chemical plant components. According to these results, L. fulvusis a more conservative feeder than L. catta.These interspecific differences in feeding behavior may be one of a number of differences that allow the two species to coexist. In allopatry, however, L. fulvusmay also adopt feeding patterns similar to those of L. catta.But L. cattawas never found to change its feeding strategies in different areas. It may be this option of L. fulvusto adopt different feeding strategies in different situations that allows this species to have the widest range of all Malagasy lemurs. Duke University Primate Center Publication No. 259.     

Effects of spatial proximity and alliances on dominance relations among female ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar

In the present study, we describe a change in the dominance rank of the top-ranking female in a wild troop of ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. After the top-ranking female fell to the bottom-ranking position, she was able to outrank a low-ranking female with the support of her adult daughter or an unrelated high-ranking female. These results indicate that, as in cercopithecine monkeys such as macaques and baboons, close proximity and alliances influence dominance relations among adult females in a wild troop of ring-tailed lemurs.     

Galactose-1-phosphate uridyltransferase of lemurs: A comparison of four species

Erythrocyte galactose-1-phosphate uridyltransferase (Gal-1-PUT) was studied in four species of lemurs. Electrophoretic phenotypes of Lemur fulvusand Lemur macacowere indistinguishable and different from the phenotypes of Lemur cattaand Lemur variegatus,which were different from each other. Enzymatic activity of hemolysates was species specific, with that of Lemur variegatusabout twice that of either Lemur fulvusor Lemur macacoand almost three times that of Lemur catta.Only minor interspecific differences were demonstrated in pH optima and k_m for galactose-1-phosphate; however, thermal stability varied considerably with phenotype. Antibody inhibition studies indicated that differences in enzyme activity of hemolysates from these species are probably due to differences in enzyme concentration.     

Measuring social tolerance: An experimental approach in two lemurid primates

Social tolerance crucially affects the life of group‐living animals as it can influence, among other things, their competitive regimes, access to food, learning behavior, and recruitment. However, social tolerance tests were mainly conducted in semi‐free or captive populations, and we know little about the behavioral mechanisms and consequences of social tolerance under natural conditions. We therefore developed a co‐feeding experiment to measure social tolerance in groups of wild and captive animals across two primate species. Specifically, we recorded the social tolerance level of redfronted lemurs (Eulemur rufifrons, four wild, one captive group) and ringtailed lemurs (Lemur catta, three wild, three captive groups) by presenting a clumped food resource in an experimental arena, and recorded patterns of resource use during the experiment. Because redfronted lemurs exhibit lower levels of decided conflicts than ringtailed lemurs, we predicted that they would be socially more tolerant. The probability for an individual to feed in the arena was higher in redfronted lemurs than in ringtailed lemurs. In addition, in both species, the probability for an individual to feed in the arena was higher in the captive populations than in their wild counterparts, suggesting that proximate factors, such as a relaxation of feeding competition in captivity, may adapt species‐specific levels of social tolerance to local levels of food availability. Hence, the number of individuals co‐feeding on a valuable food resource appears to be a useful proxy of social tolerance that could be measured with this experimental setup in other wild and captive species as well.     

Diets of Two Lemur Species in Different Microhabitats in Beza Mahafaly Special Reserve,Madagascar

Studies of primate diets usually focus on differences that distinguish species or populations. However, variation in diet can occur at a more local level of groups within a population, especially in a non-homogeneous habitat. I compared dietary variation in food composition and toughness across groups of 2 lemur species in Beza Mahafaly special reserve, Madagascar. Beza Mahafaly contains an 80-ha reserve (Parcel 1) that, while small, hosts a dense population of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas). Microhabitats in the eastern vs. western sides of the parcel are structurally and floristically distinct. Sifakas in this parcel have small, discrete home ranges and are morphological folivores. For these reasons, I expected that the 6 groups studied would eat a different menu of food plants but with similar toughness values. Ring-tailed lemurs have comparatively large, overlapping home ranges, and I expected that the 5 study groups would eat similar foods. Despite living in different microhabitats across the parcel, sifakas exhibit high dietary uniformity both in dietary plant species composition and the toughness of the foods. Food selection in sifakas operates on two distinct levels. Sifaka groups share many key food species that appear independent of local abundances, but the ranking of the foods within each group appears related to availability. Ring-tailed lemur groups are more heterogeneous in the composition of their diets relative to sifakas, though the time spent feeding on individual foods reveals a marked preference for the fruits of Tamarindus indica by all groups. Food toughness is consistent across the parcel with the exception of the most western group. Ring-tailed lemurs are highly specific feeders, but indiscriminate nibblers. Sifakas are targeted, balanced feeders. There does not appear to be a consistent microhabitat effect operating across species. Differences within sifaka and ring-tailed lemur populations in food composition and toughness, however, correspond to an east-west microhabitat gradient. Measures of dietary flexibility must take into account not only the plant species consumed and the different parts eaten but also their associated food properties and proportion of time spent feeding on them.     

The impact of fallback foods on wild ring-tailed lemur biology: A comparison of intact and anthropogenically disturbed habitats

Fallback foods are often viewed as central in shaping primate morphology, and influencing adaptive shifts in hominin and other primate evolution. Here we argue that fruit of the tamarind tree (Tamarindus indica) qualifies as a fallback food of ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Special Reserve (BMSR), Madagascar. Contrary to predictions that fallback foods may select for dental and masticatory morphologies adapted to processing these foods, consumption of tamarind fruit by these lemurs leaves a distinct pattern of dental pathology among ring-tailed lemurs at BMSR. Specifically, the physical and mechanical properties of tamarind fruit likely result in a high frequency of severe tooth wear, and subsequent antemortem tooth loss, in this lemur population. This pattern of dental pathology is amplified among lemurs living in disturbed areas at Beza Mahafaly, resulting from a disproportionate emphasis on challenging tamarind fruit, due to few other fruits being available. This is in part caused by a reduction in ground cover and other plants due to livestock grazing. As such, tamarind trees remain one of the few food resources in many areas. Dental pathologies are also associated with the use of a nonendemic leaf resource Argemone mexicana, an important food during the latter part of the dry season when overall food availability is reduced. Such dental pathologies at Beza Mahafaly, resulting from the use or overemphasis of fallback foods for which they are not biologically adapted, indicate that anthropogenic factors must be considered when examining fallback foods. Am J Phys Anthropol 140:671–686, 2009. © 2009 Wiley-Liss, Inc.     

Plants Consumed by Eulemur fulvus in Comoros Islands (Mayotte) and Potential Effects on Intestinal Parasites

The study of self-medication among animals—zoopharmacognosy—is founded on observations that suggest that wild animals use plants with specific biological properties that may be beneficial to them. To verify whether self-vermifugation occurs among Eulemur fulvus in the wild, we studied their feeding behavior in both the dry and humid forests of Mayotte (Comoros Islands). We used the focal individual sampling method over an annual cycle. We conducted a complementary study during the 2-mo mating season, via the scan sampling method (at 10-min intervals). Among the 29 plant species brown lemurs consumed, we tested 16 in vitro as antiparasitic agents on 3 experimental parasite models (Rhabditis pseudoelongata, Trichomonas vaginalis, Entamoeba invadens). We obtained crude extracts to be tested after 2 successive chemical extractions (ethyl acetate and methanol), and 7 of them, belonging to 4 different plant species, showed an antiparasitic property: lemurs consumed Annona squamosa and Mimusops comorensis in large amounts, but ingested Ixora cremixora and Syzygium jambos sporadically. The 4 plants were active on the flagellate but only one of them (Ixora cremixora) also demonstrated antinematode properties. Humans use 2 of the plants as intestinal antiparasitic agents in traditional medicine and include numerous other plants in the diet. The relative lake of amoebas and flagellates in stools of Eulemur fulvus may be related to the consumption of plants with antiprotozoal properties. Nevertheless, in the absence of specific behavior that could be linked to a voluntary therapeutic action during our study, self-vermifugation in Eulemur fulvus remains elusive.     

Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate

Background  

Like other vertebrates, primates recognize their relatives, primarily to minimize inbreeding, but also to facilitate nepotism. Although associative, social learning is typically credited for discrimination of familiar kin, discrimination of unfamiliar kin remains unexplained. As sex-biased dispersal in long-lived species cannot consistently prevent encounters between unfamiliar kin, inbreeding remains a threat and mechanisms to avoid it beg explanation. Using a molecular approach that combined analyses of biochemical and microsatellite markers in 17 female and 19 male ring-tailed lemurs (Lemur catta), we describe odor-gene covariance to establish the feasibility of olfactory-mediated kin recognition.     

Brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human head orientation as a cue to gaze direction in a food choice task

Whilst the ability to follow human gaze has been demonstrated in monkeys and apes, there is little evidence that prosimians share this ability. The current study used a food choice paradigm to assess whether captive brown (Eulemur fulvus) and ring-tailed lemurs (Lemur catta) use human gaze direction as a cue when choosing between an attending or non-attending human. Four experiments assessed the use of body, head and eye cues by the lemurs. In experiment 1, the non-attending human stood with her back to a food item; 3 of the 5 lemurs preferentially chose the attending human with an equivalent food item in view. In experiments 2 and 3, which used head angles of 90°, 4 out of 5 lemurs preferentially chose the attending human. In experiment 4, in which the humans differed only by whether their eyes were open or shut, no significant preferences were found. This study provides the first tentative evidence that lemurs are capable of discriminating human gaze direction and can use both body and head direction to do so.     

Phylogenetic relationships among Malagasy lemurs as revealed by mitochondrial DNA sequence analysis

Systematics and evolution of Malagasy lemurs has been analyzed using morphological characters, fossil evidence, ecological/ethological data, and chromosomal banding patterns. Recent developments in DNA technology have provided evolutionary biologists with additional and powerful tools for making phylogenetic inference. In the last years several studies concerning highly repeated DNA sequences (hrDNA) provided new insights about the systematic relationships among the different species of Lemuridae and Cheirogaleidae. Here, a reconstruction of molecular phylogeny of extant Malagasy lemurs based on the comparison of cytochrome-b mitochondrial DNA sequences is presented. With the Polymerase Chain Reaction (PCR) and direct sequencing of amplified DNA fragments, both the phylogenetic range and resolving power of comparative analysis can be extended. These techniques allow to gather sequence data useful to evaluate the pattern of molecular evolution offering opportunities for phylogenetic purposes. A 290-bp fragment of cytochrome-b gene has been amplified and sequenced from the following species:Tupaia glis, Galago alleni, Daubentonia madagascariensis, Indri indri, Varecia variegata, Eulemur fulvus, Eulemur coronatus, Eulemur rubriventer, Eulemur mongoz, Eulemur macaco, Lemur catta, andHapalemur griseus griseus. The phylogenetic trees obtained show the relationships among the Eulemur species and confirm the karyological and hrDNA results of a separated clade forL. catta/Hapalemur. The separation ofVarecia variegata from the other genus of the family Lemuridae is discussed.