An eco-ethological comparison ofLemur fulvus andLemur macaco

Classification problems withLemur fulvu andL. macaco are at the origin of research on the eco-ethology of these two species. Interspecific differences were observed in dominance and in sniffing, marking and rubbingbehaviour. It is hypothesised thatL. macaco uses more visual cues in communication thanL. fulvus. The post-copulatory barrier appears however to be more important than the pre-copulatory one.     

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.     

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.     

Meat eating and predation in captive-born semi-free-ranging Lemur fulvus and caged Lemur macaco

A group of brown lemurs, Lemur fulvus, and a group of black lemurs, Lemur macaco, at the Duke University Center for the Study of Primate Biology and History have been observed to capture and eat birds and lizards. Although vertebrate prey are not unusual for many carnivorous prosimians, folivorous prosimians never have been observed to take vertebrates in the wild and rarely even insects.     

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.     

Responses of Lemur fulvus to Scents of Different Subspecies of L. fulvus and to Scents of Different Species of Lemuriformes

Captive Lemur fulvus were presented with scents of their own subspecies, scents of other subspecies of L. fulvus, and scents of other species of sympatric Lemuriformes. The results suggest that L. fulvus do not distinguish between scents of different subspecies of L. fulvus, and that they do distinguish between scents of their own species and other sympatric species of Lemuriformes.     

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.     

Discrimination by male ring-tailed Lemurs (Lemur catta) between the scent marks of male and those of female conspecifics

Olfaction plays an important role in the social communication of all prosimians. (The experiment reported in this paper forms part of an intensive chemobehavioral study of olfaction in Lemur catta (ring-tailed lemur) being carried out in this laboratory.) Five male Lemur cattawere tested on their behavioral responses to paired scent stimuli. Responses measured were (1) total investigation time, (2) arm-marking, (3) ABO/BO rubbing, and (4) flehmen. Males showed a strong discrimination between the scent stimuli,giving higher levels of response to female scent on measures 1, 3, and 4. This response suggests an olfactory-related preference by males for female scent under controlled conditions. This preference may be a consequence of the females’ dominance over males and the brevity of estrus in L. catta,both of which would favor such choice behavior.     

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).     

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.     

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.     

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.     

Cytogenetic study of a female Lemur coronatus × Lemur macaco hybrid

Two species of lemur, Lemur macaco and Lemur coronatus, which do not hybridize in the wild, have produced a first, “definite” female hybrid in captivity. Its karyotype contains one haploid set from each parent. The analogy with the parental chromosomes is such that the pairing of the corresponding chromosomal arms leads to the formation of an open chain and a ring. The difficulty in obtaining hybrids between these two species could reflect the existence of a prezygotic barrier. The presence of multivalents, with probably a negative action on the gametogenesis, would introduce a postzygotic barrier.     

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.     

Seasonal ultrastructural modifications of the seminiferous epithelium in twoEulemur species:E. fulvus andE. macaco

A comparative ultrastructural study of the seminiferous epithelium was conducted during the mating and non-mating seasons of twoEulemur species:E. fulvus andE. macaco. The ultrastructure of the junctional complexes of the Sertoli cells, and the modifications in the spermatids during spermiogenesis are reported. Acridine orange staining of the sperm cells of these animals showed that the chromatin compaction was complete in all spermatozoa.     

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.     

Hemosiderosis in lemurs

In the late 1960s, pathologists at the San Diego Zoo began to notice iron storage in the internal organs of captive lemurs. Hemosiderin was found in liver, spleen, lymph nodes, duodenum, and occasionally other organs. This was most pronounced in Lemur macaco, least pronounced in Lemur catta, with the severity in Lemur variegatus variegatus and Lemur variegatus ruber falling somewhere in between. Since 1968, 20 of 29 necropsied lemurs had hemosiderosis, three with hepatomas, three with cholangiomas, and one with a metastatic pheochromocytoma. In a preliminary attempt to compare their iron absorption, five black-and-white ruffed lemur (Lemur variegatus variegatus) weanlings and five rhesus monkey weanlings were each given ～500 nmol/kg FeCI₃ (27.9 μg iron/kg) containing 5 μCi of ⁵⁹Fe in 0.1 M HCl via a nasogastric tube. Retained ⁵⁹Fe was measured by whole body gamma counting and found to be roughly the same in the two groups, possibly because insufficient quantities of iron were administered and/or excessive iron absorption becomes apparent only in older animals. Our conclusions were the following: (1) Hemosiderosis in lemurs is associated with tissue damage similar to that seen in humans with idiopathic hemochromatosis. (2) Because iron deposits occur both in parenchymal cells and reticuloendothelial cells, hemosiderosis in lemurs is probably not a model for idiopathic hemochromatosis in a pure sense.     

Discrimination between individuals by scent in Lemur fulvus

When a captive Lemur fulvus is habituated to the scent of another L. fulvus by repeatedly presenting it with that individual's scent, and is then presented with the scent of a second individual, the amount of sniffing of the scents increases, indicating that it discriminated between the scents of the two individuals. The two individuals' scents were significantly discriminated in eight of eleven different combinations of scent receiver and pair of scent donors. The two scent donors were always of the same sex and subspecies, and they could be discriminated by members of their own or of another sex or subspecies.     

Gross structure and function of the quadriceps femoris in Lemur fulvus: An analysis based on telemetered Electromyography

Analysis based on telemetered electromyography from the quadriceps femoris of Lemur fulvus, a Malagasy prosimian, during walking, galloping, leaping, and a variety of postural behaviors partially confirms and partially contradicts earlier hypothesized functions of this musculoskeletal complex. As predicted on the basis of morphological criteria (large physiological cross-section and long parallel fibers), the vastus lateralis is of special functional significance in leaping. This relatively large muscle consistently initiates the leap and frequently undergoes a very long period of force enhancement via active stretch. By contrast, the vastus intermedius fails to exhibit increased electrical activity and undergoes little or no active stretch during jumps. The myological details of vastus intermedius (short fibers, no fusion with other components), therefore, cannot be accounted for as adaptations to leaping. Rather, a primary postural role is indicated for the vastus intermedius, because in normal resting postures, with the knee quite flexed, it alone is continuously active. The existence of a fibrocartilaginous superior patella in the tendon of vastus intermedius, however, is most plausibly related to the complex tensile and compressive stresses generated in the tendon during the completely hyperflexed phase of leaping. The phasic patterning of the quadriceps femoris of Lemur fulvus does not point to any special role of the vastus lateralis or vastus intermedius during walking and galloping; it does indicate very different patterns of muscle recruitment in comparison to those in nonprimate mammals and some anthropoid primates. The forward cross walk (diagonal sequence, diagonal couplets) of primates versus the backward cross gait (lateral sequence) of most other mammals probably accounts for some of these differences. Lemur fulvus lacks the degree of elastic storage and release of kinetic energy in the quadriceps femoris that characterizes the gallop of dogs, cats, and Erythrocebus patas.