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.     

Food Intake and Dietary Overlap in Native Lemur catta and Propithecus verreauxi and Introduced Eulemur fulvus at Berenty,Southern Madagascar

The introduction of Eulemur fulvus in 1975 into the Berenty Reserve and their recent attainment of population densities comparable to those of Lemur catta led us to analyze food partitioning among the 3 large prosimian species in the gallery forest. We assessed the diets of ring-tailed lemurs (Lemur catta), brown lemurs (Eulemur fulvus) and sifakas (Propithecus verreauxi) from food intake measurements during 3 successive short-term studies. All species exhibited marked seasonal changes in their major food categories. Dietary overlap was very high between ring-tailed lemurs and brown lemurs during 2 of 3 seasons, including the middle of the dry season. During the latter period, Eulemur appeared to compensate for a low quality diet by increasing the amount of food eaten. In contrast, Lemur fed on lower amounts of food and seemed more efficient at coping with fibrous plant materials. There is low dietary overlap of Lemur catta and Eulemur fulvus versus Propithecus, which exhibit by far the highest dietary diversity of the 3 species. We discuss sustainable coexistence among them, based on respective dietary adaptations and potential for dietary flexibility.     

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.     

Highly repeated DNA analysis and systematics of the Lemuridae,a family of Malagasy prosimians

Hybridization of highly repeated DNA sequences ofEulemur fulvus mayottensis, Lemur catta, andVarecia has been performed on blots of different species of Lemuridae (L. catta, Hapalemur griseus, Varecia variegata variegata, V. v. rubra, E. macaco macaco, E. coronatus, E. mongoz, andE. rubriventer). The probe ofE. fulvus only hybridized with the differentEulemur species, whereas that ofVarecia hybridized with the two subspecies ofVarecia and that ofL. catta with bothL. catta andHapalemur. These results were used to confirm the classification ofVarecia in a separate genus and to review the separation of theL. catta/Hapalemur group from the other species ofEulemur. Comparison of the migration patterns from DNA fragments of these different species has been used to propose a cladogram of the differentEulemur species.     

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.     

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.     

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.     

Chromosome variability in the Lemuridae

Chromosome studies have been conducted in Lemur catta, L. macaco, L. mongoz, L. fulvus fulvus, and a hybrid L. fulvus fulvus x L. fulvus albifrons. Comparative analysis shows that inter- and intraspecific chromosome variability is a common finding in Lemurs. The Lemuridae are divided into three groups according to the characteristics of their chromosome complement. A reclassification of L. catta with the Hapalemurs is suggested, based on chromosomal and nonchromosomal data.     

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.     

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.     

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.     

Isolation of 10 microsatellite markers for mongoose lemurs (Eulemur mongoz)

We present here 10 new microsatellite markers for the mongoose lemur (Eulemur mongoz), nine of which were isolated from E. mongoz and one from Lemur catta. At least 60 individuals were genotyped for each of the 10 loci. Mendelian inheritance at each locus was tested by genotyping five captive families with known pedigrees. All loci were polymorphic and demonstrated simple Mendelian inheritance. The microsatellite markers presented here will be useful for genetic surveys of wild E. mongoz, to gain insights into the genetic background of the captive population, and to aid in the conservation of the species’ genetic diversity.     

A model for comparison of masticatory effectiveness in primates

A model is presented to express how effectively animals increase the exposed surface area of their food by chewing. It includes a coefficient of masticatory effectiveness (E) the value of which increases with effectiveness of exposing new food surface area with each chew. Humans and other species of primates differ significantly in their values of E; among the nonhuman primates studies, Lemur catta has a higher coefficient than Lemur fulvus, and both have higher coefficients than either Varecia variegatus or Galago crassicaudatus argentatus. The differences among the coefficients to these prosimians are correlated with variations in specific features of the molar morphology. Of six lower molar shearing crests considered, the relative length of the post-metacristid correlates most highly with the coefficient of masticatory effectiveness for the prosimian species. Also, among comparable-sized prosimians, E correlates significantly with the absolute postmetacristid length. Both these findings indicate that the relative size of molar shearing crests is related significantly to how effectively an animal chews its food. There are also implications for an adaptation to a high-fiber diet.     

Can lemurs (<Emphasis Type="Italic">Eulemur fulvus</Emphasis> and <Emphasis Type="Italic">E. macaco</Emphasis>) use abstract representations of quantities to master the reverse-reward contingency task?

In previous studies we demonstrated that brown and black lemurs (Eulemur fulvus and E. macaco) showed self-control abilities under a reverse-reward contingency. They were able to significantly select the smaller quantity of food to be rewarded with the larger one and to generalize this ability when presented with two rewards that differed in quality. In the present study, previously trained subjects had to choose between graphic representations of two different quantities of food under the reverse-reward contingency. Three out of four subjects learned to associate a graphic representation of the reward with the corresponding quantity. Only one subject consistently selected the representation of the smaller quantity to be rewarded with the larger quantity of food and therefore showed abstraction as well as relative numerousness skills. Indeed, she was able to discriminate between representations of different quantities and to ordinate them. We discuss how primates mentally represent food quantities and how self-control is involved in foraging strategies.     

Male life history and intergroup mobility among ringtailed lemurs (Lemur catta)

Lemur catta shares a male-biased dispersal pattern with most primate species and the majority of mammals. Individuals in a free-ranging population of ringtailed lemurs were captured, marked, released, and monitored for a 40-month period. Sixty-four percent of the males (43 of 67) migrated or were missing within this period and all nine censused groups were affected by migration. Males migrate from their natal group and then may migrate again after reaching full adult body weight. Full-sized adult males migrate at a rate of 0.28 per year or once every 3.5 years and may change groups a number of times during their life. Migrations occurred within a 6-month period, ending just after the mating season. However, there is no direct connection between mating success and male migration. Females mate with transferring males, with group males, and with visitors from adjacent groups. The age-related pattern of male migration and the occurrence of extragroup mating inLemur catta is similar to that described for several species of macaques.     

Differences in male-female interaction betweenLemur fulvus andL. macaco

Interspecific differences were found betweenLemur fulvus andLemur macaco in heterosexual pair-tests.L. fulvus showed more mutual grooming and were more active in exploration thanL. macaco. The absence of a naked anal region inL. macaco females causes a virtual absence of foreheadmarking on this region by males.L. macaco males have a stronger tendency to mark the body of the female with their anogenital region after a nose-anogenital contact thanL. fulvus, indicating that the behaviour is more ritualized inL. macaco males.     

A comparative banding analysis of chromosomes in three species of lemurs (Primates,Lemuridae)

Banded karyotypes were compared in 3 species of lemurs,Lemur catta (2n=56),L. f. fulvus (2n=60) andL. mongoz (2n=60). The karyotypes of the latter 2 species were indistinguishable from each other in both Q-band and G-band patterns, except thatL. mongoz had an unusually large Y chromosome. The karyotypic differences betweenL. catta and the other 2 species were mainly explained by centric fusions (or fissions) and pericentric inversions. Contrary to the general similarity in Q-band and G-band patterns, the C-band patterns were highly variable among the 3 species. All chromosomes ofL. fulvus had a distinctive C-band in the centromeric region, whileL. mongoz had only a few chromosomes with an apparent C-band.L. catta was remarkable by showing interstitial and terminal C-bands in some elements, in addition to the centromeric band which was observed in about 20 pairs.     

Codominant autosomal inheritance of polymorphic red cell acid phosphatases of lemurs and some properties of the enzymes

Red cell acid phosphatase phenotypes of 207 captive animals of the genera Lemur, Hapalemur, and Propithecus were determined by starch gel electrophoresis and phosphatase-specific staining. In Lemur fulvus, three phenotypes, designated A, B, and AB, were observed. In each of the species L. catta, L. macaco, L. mongoz, and L. variegatus, a single phenotype was observed. In Hapalemur griseus, three phenotypes were found: A, B, and AB. In Propithecus verreauxi, a single phenotype was found. Examination of breeding records in conjunction with the results of the electrophoretic analyses supports the conclusion that the erythrocytic acid phosphatases in this group of nonhuman primates are the products of at least two codominant autosomal alleles. There is a wide range of specific activities of the acid phosphatases as determined by colorimetric assays. The values range from 60.6 moles of p-nitrophenol released per gram of hemoglobin per 30 min in Lemur catta to 429.1 moles in Propithecus verreauxi. The enzymes of L. fulvus and P. verreauxi were purified approximately 400-fold, and Michaelis-Menten constants were determined on the purified preparations. For L. fulvus phenotype A, K _m =0.8 mM; for L. fulvus phenotype B, K _m =0.8 mM; and for P. verreauxi, K _m =0.6 mM; the substrate in each case was p-nitrophenylphosphate.The work reported here was taken in part from a doctoral dissertation submitted by G.A.M. to the Graduate School of Duke University in partial fulfillment of the requirements for the Doctor of Philosophy degree. This work was supported by grants from the National Science Foundation (Nos. GS 39635X and BNS-74-02504), the USPHS (fellowship to G.A.M., No. GM-02007), and the Wenner-Gren Foundation (No. 2697).