Black Lemurs Research Articles

Cathemeral activity patterns of the blue-eyed black lemur Eulemur macaco flavifrons in intact and degraded forest fragments

This study describes the activity pattern of the blue-eyed black lemur Eulemur macaco flavifrons for the first time and investigates the parameters, such as season or habitat, that may influ- ence the distribution of activity over the 24 h cycle. Four groups of E. m. flavifrons in 2 forest frag- ments with different degrees of degradation were followed for 24 h mo -1 over a 7 mo period between July 2004 and July 2005. Blue-eyed black lemurs exhibited a bimodal activity pattern which peaked during the morning and evening twilight. The groups consistently showed activity bouts both during the day and at night, a behaviour that corresponds to Tattersall's (1987) definition of cathemerality. The proportion of illuminated lunar disc and the nocturnal illumination index were positively associ- ated with the amount of nocturnal activity. Total activity, both diurnal and nocturnal, was signifi- cantly higher in the secondary than in the primary forest. In view of our results, the cathemeral behaviour of E. m. flavifrons may best be explained as flexible responses to a framework of varying environmental factors, each of which may enhance or inhibit activity within the lemurs' range of adaptability. This temporal behavioural plasticity may be an adaptation to an erratic and severe climate with frequent droughts and cyclones and unpredictable resource availability.

Seroprevalence of Toxoplasma gondii, Sarcocystis neurona, and Encephalitozoon cuniculi in three species of lemurs from St. Catherines Island, GA, USA

In the current study, we determined the seroprevalence of Toxoplasma gondii, Sarcocystis neurona, and Encephalitozoon cuniculi in three species of lemurs from St. Catherines Island, Georgia. Serum samples were tested from 52 ring-tailed lemurs ( Lemur catta), six blue-eyed black lemurs ( Eulemur macaco flavifrons), and four black and white ruffed lemurs ( Varecia variegata variegata) using an agglutination assay. Three ring-tailed lemurs (5.8%) were positive for T. gondii (titer of 1:50); one ring-tailed lemur (1.9%) and one black and white ruffed lemur (25%) were positive for S. neurona (titers of 1:1000); and one ring-tailed lemur (1.9%) was positive for E. cuniculi (titer of 1:400). All blue-eyed black lemurs were negative for antibodies to T. gondii, S. neurona, and E. cuniculi. This is the first detection of antibodies to T. gondii in ring-tailed lemurs and antibodies to S. neurona and E. cuniculi in any species of prosimian.

Asymptomatic Enterocytozoon bieneusi microsporidiosis in captive mammals

Human microsporidiosis, a serious disease of immunocompetent and immunosuppressed people, can be due to zoonotic transmission of microsporidian spores. A survey utilizing chromotrope 2R stain and fluorescent in situ hybridization techniques for testing feces from 193 captive mammals demonstrated that 3 animals (1.6%) shed Encephalitozoon bieneusi spores. These include two critically endangered species (i.e., black lemurs, Eulemur macaco flavifrons; and Visayan warty pig, Sus cebifrons negrinus) and a threatened species (mongoose lemur, Eulemur mongoz). The concentration of spores varied from 2.7 x 10(5) to 5.7 x 10(5)/g of feces, and all infections were asymptomatic. The study demonstrates that E. bieneusi spores can originate from captive animals, which is of particular epidemiologic importance because the close containment of zoological gardens can facilitate pathogen spread to other animals and also to people such as zoo personnel and visitors.

Effects of Three Food Enrichment Items on the Behavior of Black Lemurs (Eulemur macaco macaco) and Ringtail Lemurs (Lemur catta) at the Henson Robinson Zoo, Springfield, Illinois

This study tested 3 food enrichment items mentioned in a laboratory primate newsletter with 6 adult Eulemur macaco and 3 adult Lemur catta to examine whether the items would affect the behavior of the lemurs. The results suggest that Food Enrichment Item 3 (a wire box filled with whole grapes, apples, or both hidden in straw hung from a branch within the enclosure) caused a significant decrease in the incidence of resting and a significant increase in the incidences of playing and grooming, with no significant effect on the incidence of feeding or foraging. The lemurs' behavior appeared to be most affected by the food enrichment item that required the most manipulation, closely followed by an enrichment that required a moderate amount of manipulation. The order of the exposure to the food enrichment items and the day of the week appear to have an attenuation effect on these behaviors and did affect the incidence of 3 stereotypic behaviors exhibited by a male L. catta such that 3 behaviors declined in occurrence as the study progressed.

Can lemurs learn to deceive? A study in the black lemur (eulemur macaco).

Deceptive behavior in primates has been the focus of a number of studies. Nevertheless, such abilities have never been demonstrated in prosimians. The authors' goal was to analyze possible deception in lemurs according to a paradigm used with simians. Three black lemurs were trained to communicate about the location of a hidden reward with a cooperative trainer. Afterward, when a 2nd trainer and lemurs competed to gain access to the reward, each subject differentially adapted its learned behavior to the context. Their performances with the cooperative trainer remained stable while they showed various behavioral adjustments when faced to the competitive trainer: 1 subject refused to participate, another preferentially withheld information, and the 3rd sometimes pointed deceptively to obtain the reward.

FIBER DIGESTIBILITY BY BLACK LEMURS (EULEMUR MACACO MACACO)

Black lemurs, Eulemur macaco, are classified as generalist feeders, consuming a proportion of fruits and leaves that varies with seasonal availability. It is hypothesized that black lemurs are capable of using neutral detergent fiber (NDF) as a source of energy through fiber fermentation in the cecum and large intestine. In captivity, they are typically fed a diet of commercially available primate biscuits and readily available produce, both of which are limited in NDE Digestibility trials were conducted on 14 black lemurs; 12 were housed in groups (four, three, three, and two) and 2 were individually housed. The lemurs were fed four manufactured feeds differing in fiber form and content. A commercially available primate biscuit, containing approximately 27% NDF, served as the control diet. The second diet contained the same primate biscuits, which were ground and then incorporated into a fiber-based gel matrix. The third and fourth diets were formulated using soybean hulls or ground corncobs as the fiber source, resulting in 53% and 47% NDF, respectively. Produce was added to the diet at 36% (dry matter basis). Dry matter digestibility differed significantly among all diets. Neutral detergent fiber digestibility was highest for the ground biscuit in gel and lowest for the two high-fiber gel diets, with biscuit digestibility values falling between the two extremes. The high-fiber gel diets were successful in increasing the NDF concentrations of the primate diets; however, black lemurs were capable of only limited fiber digestion.

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

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

MOLECULAR AND SEROLOGIC EVIDENCE OF TICK-BORNE EHRLICHIAE IN THREE SPECIES OF LEMURS FROM ST. CATHERINES ISLAND, GEORGIA, USA

In recent years, several species of ehrlichiae have been recognized as tick-borne disease agents of veterinary and medical importance. Clinically normal free-ranging or previously free-ranging lemurs, including 46 ring-tailed lemurs (Lemur catta), six blue-eyed black lemurs (Eulemur macaco flavifrons), and four black and white ruffed lemurs (Varecia variegata variegata) from St. Catherines Island, Georgia, were tested for evidence of exposure to tick-borne ehrlichiae. All 52 adult lemurs were serologically tested for exposure to Ehrlichia chaffeensis and Anaplasma phagocytophilum. Polymerase chain reaction (PCR) assays for E. chaffeensis, A. phagocytophilum, Ehrlichia ewingii, and Ehrlichia canis were conducted on blood samples from all 56 lemurs. Blood from all lemurs was inoculated into DH82 cell cultures for E. chaffeensis isolation. Of the adult lemurs, 20 (38.5%) and 16 (30.8%) had antibodies reactive (> or =1:128) for E. chaffeensis and A. phagocytophilum, respectively. Two ring-tailed lemurs were PCR and culture positive for E. chaffeensis. Molecular characterization of the two E. chaffeensis isolates showed that both contained 5-repeat variants of the variable-length PCR target (VLPT) antigen gene and 3-repeat variants of the 120-kDa antigen gene. Sequencing of the VLPT genes revealed a novel amino acid repeat unit (type-9). One lemur infected with E. chaffeensis was slightly hypoproteinemic and had moderately elevated serum alanine aminotransferase (ALT) levels. These lemurs from St. Catherines Island have been exposed to or infected with tick-borne ehrlichiae, or both, but showed no clinical disease.

Evolutionary History of Chromosome 20

The evolutionary history of human chromosome 20 in primates was investigated using a panel of human BAC/PAC probes spaced along the chromosome. Oligonucleotide primers derived from the sequence of each human clone were used to screen horse, cat, pig, and black lemur BAC libraries to assemble, for each species, a panel of probes mapping to chromosomal loci orthologous to the loci encompassed by the human BACs. This approach facilitated marker-order comparison aimed at defining marker arrangement in primate ancestor. To this goal, we also took advantage of the mouse and rat draft sequences. The almost perfect colinearity of chromosome 20 sequence in humans and mouse could be interpreted as evidence that their form was ancestral to primates. Contrary to this view, we found that horse, macaque, and two New World monkeys share the same marker-order arrangement from which the human and mouse forms can be derived, assuming similar but distinct inversions that fully account for the small difference in marker arrangement between humans and mouse. The evolutionary history of this chromosome unveiled also two centromere repositioning events in New World monkey species.

Urinary Progestogen and Estrogen Excretion During Pregnancy in Eulemur macaco flavifrons, E. rubriventer, and Hapalemur griseus occidentalis

Via a non-invasive approach, we aimed to provide comparative data on the presence and relative abundance of progestogen and estrogen metabolites excreted into the urine of Eulemur rubriventer, E. macaco flavifrons and Hapalemur griseus occidentalis and to characterize the patterns of progestogen and estrogen excretion during pregnancy. We found that estrone is the major urinary estrogen in Eulemur macaco flavifrons and Hapalemur griseus occidentalis, while 16α-hydroxyestrone appeared to be the predominant estrogen in the urine of E. rubriventer. Estradiol-17s was either absent (Hapalemur) or present in very low amounts. HPLC of progestogens had high levels of immunoreactivity in an assay against 5α-pregnane-3α-ol-20-one (5-P-3OH) in each species, though the nature of the progestogens measured by the 5-P-3OH assay differed among species. During pregnancy, 5-P-3OH levels remained relatively low in Eulemur rubriventer, whereas in E. macaco flavifrons and Hapalemur griseus occidentalis, a sustained elevation in levels occurred from mid-pregnancy until the final weeks before parturition. Estrogen excretion differed depending on the sex of the fetus in each species, with only females carrying male infants showing clearly elevated estrogen levels during the last 6–8 weeks of gestation. In conclusion, we demonstrate both species similarities and differences in the metabolism and urinary excretion patterns of reproductive hormones throughout gestation in the Lemuridae. The data not only extend our knowledge on the reproductive physiology of lemurs but also show that more studies on other lemur taxa are needed to provide a broader basis for interspecific comparison.

Learning to suppress responses to the larger of two rewards in two species of lemurs, Eulemur fulvus and E. macaco

Six brown lemurs and four black lemurs were presented with two stimulus arrays of one and four raisins. Under a reverse-reward contingency, they received the array they did not choose. All subjects showed a strong preference for the larger array and developed a strong side preference bias. When a large-or-none reward contingency was applied (i.e. no reward followed the choice of the larger array, but this array was given for the choice of the smaller array), six of the 10 subjects overcame their side bias and learned to select the smaller array. When a correction procedure was added, all the remaining subjects mastered the task. Performance was maintained when the original reverse-reward contingency was rerun, and when novel array pairs were presented. Several months after the study, six subjects retained a significant preference for choosing the smaller of the two arrays. The results demonstrate a form of self-control in two prosimian species.

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

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

Acoustic structure and contexts of emission of vocal signals by black lemurs

We investigated the vocal repertoire of a Malagasy primate: the black lemur (Eulemur macaco macaco). The first study allowed the characterization of 16 different vocal signals on the basis of acoustic parameters. Black lemurs emit sparse harmonic sounds, dense harmonic sounds, spectrally structured noise (Beeman, 1998) and a wide variety of grunts. The second study focused on the behavioral context of emission of these signals and used the pre- and post-event histogram method (Douglass and Sudd, 1980; Preuschoft, 1995a). It provides statistical demonstration of the association between a signal and other behaviors of the emitter, thus giving insight into the latter’s motivations. Four signals are linked to affiliative and agonistic interactions. Three signals express a state of alarm, and two appear related to discomfort. Most grunts are linked to contact and signal precisely the emitter’s level of vigilance. Other interdisciplinary communication studies could benefit from methodology and software used here.

Conflict and postconflict behaviour in two lemur species with different social organizations (Eulemur fulvus and Eulemur macaco): A study on captive groups

AbstractAlthough the brown lemur (Eulemur fulvus) and the black lemur (Eulemur macaco) share many life parameters and are genetically closed, they show considerable difference in social organization. Dominance relationships with no systematic effect of gender characterize the former, whereas the latter is based on female dominance. The present study was done on two captive groups of brown lemurs and one semi–free‐ranging group of black lemurs. To reveal links between the specific pattern of social organization and agonistic behaviors, agonistic interactions were analyzed for each species as for their context of occurrence, symmetry, initiation, and outcome. The effect of gender in the initiation of conflicts appeared as the only notable interspecific difference, aggression being mostly initiated by females in E. macaco and by males in E. fulvus. Conflict outcome was generally in favor of the initiator, regardless of gender in both species. The analysis of postconflict behaviors revealed conciliatory processes in the brown lemur, whereas reconciliation seemed to be absent in the black lemur, a characteristic shared with the ring‐tailed lemur (Lemur catta), another lemur species with female dominance. Aggr. Behav. 28:62–74, 2002. © 2002 Wiley‐Liss, Inc.

Fruit Characteristics of Species Dispersed by the Black Lemur (Eulemur macaco) in the Lokobe Forest, Madagascar.

ABSTRACTI describe the fruit characteristics of species closely associated with black lemur seed dispersal (i.e., species that are often dispersed by die black lemur and only dispersed by the black lemur in die Lokobe Forest). A black lemur group was habituated and observed during the day and night for all months of die year (total 1272 h). When fruits were eaten, die plant species was identified, die maturity of the fruit and treatment of the seeds noted, and the fruit described in terms of ripe fruit color, husk thickness, fruit length, and seed length and width. Black lemur feces were searched for seeds; these were identified and signs of damage noted. Other potential dispersers feeding on the fruits of species eaten by the black lemur were also noted. The black lemurs were seen eating die fruits of 70 species. Of these, 51 species were defined as closely associated with black lemur dispersal and 16 species had seeds that were either often preyed upon or wasted by the black lemur, or were seen being eaten by other potential seed dispersers. Fruits of species in the former group were often dull colored (94% of species); rarely less than 1 cm long (6%); rarely had seeds less than 0.1 cm long or less than 0.1 cm wide (2 and 4%, respectively); never had seeds more than 4 cm long or greater than 2 cm wide; and quite often had either thick husks (49%) or thin husks (51%). In contrast, the fruits of the latter group were often brightly colored (75% of species) and nearly always had a thin husk (94%). Also, this latter group included more small and very large fruits and seeds than the former group. Fruit characteristics significantly associated with the former group were: dull color, thick husk, fruit length greater than 2 cm, seed length 1–4 cm, and seed width 1–2 cm. The extent to which these traits are the result of coevolution between plants and the guild of lemur dispersers that includes the black lemur is not clear, but a coevolved lemur–fruit syndrome remains a possibility.RESUMESCette étude porte sur la description des caracteristiques des fruits appartenant aux espèces dont la dissemination des graines est étroitement liée au Eulemur macaco. Ces espèces sont definies comme étant souvent disséminees par E. macaco et uniquement disséminées par E. macaco dans la for○t de Lokobe. Dans le but d'identifier ces espéces, un groupe de E. macaco a été habituéà la présence humaine et observé jour et nuit pendant tous les mois de 1'année (en total 1272 h). Une fois le fruit consommé, I'espèce était identifyée, la maturityé du fruit ainsi que le traitement de la graine notés et le fruit était dàcrit en termé de couleur á maturityé, d'épaisseur de I'enveloppe, de longueur de fruit et de longueur et de largeur de graine. Par la suite, les féces sont recherchés afin d'identifier les graines qu'ils contiennent et routes signes d'endommagement de celles‐ci sont notés. Les autres agents de dissémination potentiels, consomma‐teurs des fruits appartenant aux espèces consommées par E. macaco, ont étéégalement notés. Les E. macaco ont été vu consommer les fruits de 70 espèces. De ces dernières, 51 espèces étaient définies comm.éaetant étroitement liées à la dissémination par E. macaco et les graines de 16 espèces sont soit consommées, soit gaspillées par E. macaco, soit ont été vu consommées par d'autres agents de dissémination potentiels. Les fruits des espèces appartenant au groupe précédent sont souvent d'une couleur sombre (94% des espèces), d'une longueur rarement < 1 cm (6%), avaient rarement des fruits < 0.1 cm de long ou < 0.1 cm de large (2 et 4% respectivement) et n'ont jamais des graines > 4 cm de long ou > 2 cm de large, et presque souvent avaient une enveloppe épaisse (49%) et presque souvent une enveloppe mince (51%). Par contre, les fruits du dernier groupe sont souvent d'une couleur claire (75% des espèces) 'et presque toujours ont une enveloppe mince (94%). De plus, ce groupe inclut plus de petits et de très larges fruits et graines que le premier groupe. Les classes des caractéristiques des fruits significativement associées au premier groupe sont: couleur sombre, enveloppe épaisse, longueur de fruit >2 cm, longueur de graine 1‐4 cm, et largeur de graine 1‐2 cm. Cependant, 1'importance du ro̧le joué par la coévolution entre les plantes et le groupe des lémuriens disséminateurs, comprennant Eulemur m., dans le développement des caractéristiques de ces fruits n'est pas connue.

Factors affecting feeding decisions in a group of black lemurs confronted with novel food

The behavior of black lemurs presented with novel and familiar food in the presence or absence of the dominant female was analyzed in order to examine the influence of the latter on feeding decisions at a group level. Results showed that individual learning occurred with high quality food, while the dominant female influenced the eating behavior of other group members when food was of low attractiveness or unfamiliar.

Fruit Characteristics of Species Dispersed by the Black Lemur (Eulemur macaco) in the Lokobe Forest, Madagascar1

I describe the fruit characteristics of species closely associated with black lemur seed dispersal (i.e., species that are often dispersed by the black lemur and only dispersed by the black lemur in the Lokobe Forest). A black lemur group was habituated and observed during the day and night for all months of the year (total 1272 h). When fruits were eaten, the plant species was identified, the maturity of the fruit and treatment of the seeds noted, and the fruit described in terms of ripe fruit color, husk thickness, fruit length, and seed length and width. Black lemur feces were searched for seeds; these were identified and signs of damage noted. Other potential dispersers feeding on the fruits of species eaten by the black lemur were also noted. The black lemurs were seen eating the fruits of 70 species. Of these, 51 species were defined as closely associated with black lemur dispersal and 16 species had seeds that were either often preyed upon or wasted by the black lemur, or were seen being eaten by other potential seed dispersers. Fruits of species in the former group were often dull colored (94% of species); rarely less than 1 cm long (6%); rarely had seeds less than 0.1 cm long or less than 0.1 cm wide (2 and 4%, respectively); never had seeds more than 4 cm long or greater than 2 cm wide; and quite often had either thick husks (49%) or thin husks (51%). In contrast, the fruits of the latter group were often brightly colored (75% of species) and nearly always had a thin husk (94%). Also, this latter group included more small and very large fruits and seeds than the former group. Fruit characteristics significantly associated with the former group were: dull color, thick husk, fruit length greater than 2 cm, seed length 1–4 cm, and seed width 1–2 cm. The extent to which these traits are the result of coevolution between plants and the guild of lemur dispersers that includes the black lemur is not clear, but a coevolved lemur–fruit syndrome remains a possibility.

Genetic comparison between different populations of Eulemur macaco flavifrons in northwest Madagascar using RAPD markers

Eulemur macaco flavifrons, the Sclater's black lemur, is a critically endangered subspecies of northwest Madagascar, which is not yet protected by any reserve. In order to study the feasibility of creating such a reserve, an area of outstanding biological importance was selected in the region of Maromandia-Sahamalaza, which is probably the only remaining place which would permit the long-term survival of the Sclater's black lemur. To determine if genetic management is needed for the Sahamalaza black lemur population, its genetic variability was estimated with random amplified polymorphic DNA (RAPD) markers and compared with other populations. These comparisons demonstrate that the Sahamalaza black lemurs have a genetic variability equivalent to those in other areas. Thus, we conclude that no genetic management is required at the present time. Am. J. Primatol. 51:249–255, 2000. © 2000 Wiley-Liss, Inc.

Colour and Shape Discrimination in Black Lemurs (Eulemur macaco)

Colour and Shape Discrimination in Black Lemurs (Eulemur macaco)

Genetic Variation in Prosimian Species

Scheffrahn et al. (1998a,b) aimed to outline the possible contributions of genetics to conservation biology: the determination of genetic variation of wild groups and its use as a guideline in breeding programs. Unfortunately, the amount of genetic variation within wild groups of nonhuman primates is rarely known. In particular, this observation holds for prosimians. Average heterozygosity is widely considered to be a good indicator of the magnitude of intraspecific variation. We provide some values of average heterozygosity of wild populations of Otolemur garnettii, Eulemur macaco macaco and E. m. flavifrons.