Habitat shifting by the common brown lemur (Eulemur fulvus fulvus): a response to food scarcity

During periods of food scarcity, most primates display behavioral responses, such as dietary switching or adjustment of traveling and foraging efforts, within home ranges. In rare cases, several primate species leave their home ranges for other remote habitats to seek alternative resources; this migration-like behavior is termed “habitat shifting.” Reports of habitat shifting have concentrated on platyrrhines, but this behavior has rarely been observed among prosimians. During 1 year of observation of a troop of common brown lemurs (Eulemur fulvus fulvus) in Ankarafantsika National Park, northwestern Madagascar, habitat shifting occurred twice. To understand the causes of this behavior, I examined the seasonal availability of fruit resources in the range continuously used by the troop during the year (defined as the annual range) and compared feeding activities and vegetation types between the annual range and new areas. The troop usually stayed within a 38.7-ha annual range, defined by a 95 % fixed kernel analysis based on GPS location data collected at 5-min intervals. In April 2007, the lemurs suddenly moved to a habitat 1.0–1.5 km south of their annual range and concentrated on the consumption of Grewia triflora fruits for 2 weeks. In November 2007, they visited a habitat 0.8–1.7 km southeast of the annual range and exploited fruits of Landolphia myrtifolia. These new areas were open habitats with high densities of the respective fruit species. The density of fruiting trees was low in the annual range during these periods; thus, habitat shifting to areas with different phenological productivity appeared to be an effective response to fruit scarcity. Brown lemurs are generally categorized as a nonterritorial species, and the lemurs observed here showed no agonistic behavior in intergroup encounters during range shifting. Such nonterritoriality may allow brown lemurs to shift habitats, a behavior resulting in long-term absence from their annual range.     

Feeding behavior of lactating brown lemur females (Eulemur fulvus) in Mayotte: influence of infant age and plant phenology

Altmann [Baboon Mothers and Infants, University of Chicago Press, 1980] and Dunbar and Dunbar [Animal Behavior 36:970-980, 1988] provided a model that predicts the amount of time spent feeding by lactating baboon females, as related to infant age. Dunbar's model further suggests that food quality affects the amount of time that females devote to feeding activity, and is predictable from rainfall and temperature data. In this study the model was tested with data recorded from births of the Mayotte brown lemur from four maternal dyads (Eulemur fulvus). This study also examines the correlation between female activity budget, quantities of fresh plant matter ingested, and suckling duration using data collected from focal animal samples on the mother-infant dyads. The relationships among rainfall, food supply, and food quality were also tested. It appears that female brown lemurs do not devote more time to feeding during the infant growth period. The data show that female brown lemurs increased their food intake during the early-lactating period when the frequency of suckling is the highest, and before infants begin to eat substantial amounts of solid foods. Thus, the frequency of feeding reflects the cost of lactation better than suckling duration. Furthermore, females did not appear to select foods according to their availability or rainfall levels. I hypothesize that the lack of convergence between lemur data and baboon observations is due to differences between their respective environments and their feeding ecology. These data also indicate that the most significant lactating cost for the brown lemur occurs during the early lactation period.     

Cathemerality in the mongoose lemur, Eulemur mongoz

Results of a 10 month study of the mongoose lemur (Eulemur mongoz) at Anjamena are presented. The activity pattern is documented in detail for both wet and dry seasons based on observations conducted over the entire 24 h period. E. mongoz was found to be cathemeral throughout the year but exhibited shifts towards more diurnal activity in the wet season and more nocturnal activity in the dry season. The cathemeral activity pattern in the mongoose lemur appears to be coordinated with sunrise, sunset, and day length and modulated by an inhibitory effect of low nocturnal light intensity in the forest during the wet season, resulting in mainly diurnal activity. Temperature and rainfall may also influence the activity pattern. Few advantages to food-related behavior appear to derive from this activity pattern, although resource accessibility may be enhanced by nocturnal behavior in the dry season, leading to reduction in interspecific competition. Cathemerality may also represent a behavioral thermoregulatory mechanism allowing the mongoose lemur to conserve energy by being active during the cool nights of the dry season. In addition, nocturnal behavior in the dry season probably allows avoidance of predation by raptors at the time of year when least protection is afforded by vegetation.     

Cineradiographic study of forelimb movements during quadrupedal walking in the brown lemur (Eulemur fulvus, Primates: Lemuridae)

Movements of forelimb joints and segments during walking in the brown lemur (Eulemur fulvus) were analyzed using cineradiography (150 frames/sec). Metric gait parameters, forelimb kinematics, and intralimb coordination are described. Calculation of contribution of segment displacements to stance propulsion shows that scapular retroversion in a fulcrum near the vertebral border causes more than 60% of propulsion. The contribution by the shoulder joint is 30%, elbow joint 5%, and wrist joint 1%. Correlation analysis was applied to reveal the interdependency between metric and kinematic parameters. Only the effective angular movement of the elbow joint during stance is speed-dependent. Movements of all other forelimb joints and segments are independent of speed and influence, mainly, linear gait parameters (stride length, stance length). Perhaps the most important result is the hitherto unknown and unexpected degree of scapular mobility. Scapular movements consist of ante-/retroversion, adduction/abduction, and scapular rotation about the longitudinal axis. Inside rotation of the scapula (60 degrees -70 degrees ), together with flexion in the shoulder joint, mediates abduction of the humerus, which is not achieved in the shoulder joint, and is therefore strikingly different from humeral abduction in man. Movements of the shoulder joint are restricted to flexion and extension. At touch down, the shoulder joint of the brown lemur is more extended compared to that of other small mammals. The relatively long humerus and forearm, characteristic for primates, are thus effectively converted into stride length. Observed asymmetries in metric and kinematic behavior of the left and right forelimb are caused by an unequal lateral bending of the spinal column.     

Aggressive and neutral interventions in conflicts in captive groups of brown lemurs (Eulemur fulvus fulvus)

Third-party interventions in conflicts have revealed complexity in primate social relationships. This type of intervention has seldom been analyzed in prosimians, although many of these species exhibit complex (multimale/multifemale) social organizations. The present study on captive brown lemurs (Eulemur fulvus fulvus) shows that dominant individuals were more likely to intervene in conflicts. Both males and females intervened aggressively in conflicts. Female aggressive interventions occurred mainly on behalf of close kin, whereas males mainly intervened on behalf of juveniles. This study also provides the first record of neutral or peaceful interventions in lemurs. Although females intervened neutrally, almost all neutral interventions were by dominant males. Dominant males intervened in conflicts neutrally more often than aggressively, principally in conflicts between adults and juveniles or between juveniles. Neutral interventions by males always ended the conflicts and were often followed by affiliative contacts between participants (intervenors and opponents). In lemurs, female interventions can be explained by kin selection, while the nature of dominant males' interventions suggests a control role. Interventions by males on behalf of juveniles may increase the formers' fitness.     

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.     

Ontogeny of Feeding Behavior of Eulemur fulvus in the Dry Forest of Mayotte

Captive data show that juvenile mammals usually reproduce the diet of the adult. However, it is not known whether, in natural environments, the process of feeding maturation varies according to available foods and to adult choices. I examined the feeding ontogeny of Mayotte brown lemurs (Eulemur fulvus), a presumed introduced species, from birth to 12 mo old in the southern dry forest of Mayotte. The study focused on activities and diets of 4 mothers and their juveniles from 2 groups in 1999 and 2000. In 2001, we also observed 2 other dyads from each group for 2 mo (March/April). I assessed plant phenology in each group's home range. There are 4 phases of feeding ontogeny: (1) the 3 mo following birth are characterized by lactation, early bouts of exploration, and consumption; (2) the next 2 mo are characterized by feeding and social weaning; (3) during the sixth and seventh mo, the daily feeding activity rhythms of the mother and her juvenile are synchronized and diets largely overlap; (4) at 10–12 mo of age, the feeding juvenile is closer to other group members than to its mother. During their first year of life, especially before being weaned, juveniles eat several food items that are not ingested by their mothers. It appeared that the progressive overlap in dietary items and feeding synchrony between mother and juvenile depends on several types of leaming. There is a correlation between the availability of particular food resources with high nutritional quality and timing of reproduction and infant maturation.     

Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences

The brown lemurs (Eulemur fulvus) include seven subspecies, whose evolutionary relationships remain contentious. In particular, it is unclear whether the Malagasy and Comorian E. f. fulvus populations are differentiated at the subspecific level (E. f. mayottensis). Furthermore, it has been suggested that E. f. collaris and E. f. albocollaris are separate species. Analyses of approximately 2400 bp of mitochondrial DNA sequence data from part of the COIII gene, together with complete genes for ND3, ND4L, and ND4 and 5 tRNAs, resolved 34 E. fulvus specimens into six clades: ((albocollaris, collaris) (rufus (rufus (fulvus/mayottensis (albifrons/fulvus/sanfordi))))). Based on the information available and our analyses we conclude that E. f. albocollaris and E. f. collaris do not represent species distinct from E. fulvus and that Comorian brown lemurs do not deserve subspecific rank. No genetic differentiation was detected between E. f. albifrons and E. f. sanfordi; on the other hand, there are obviously two separate lineages of E. f. rufus.     

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

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

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

The purpose of this study is to describe the anatomy and obtain echographic measurements of normal kidneys in brown lemurs (Eulemur fulvus). The anatomical findings show that brown lemur kidneys are comparable to those of rats except for an elongated papilla. The kidneys of 16 (7 females and 9 males) lemurs were examined with two‐dimensional and power Doppler ultrasonography under general anesthesia. Morphometrically, the left and right kidney surface areas are comparable (3.29 and 3.51 cm²). Kidney area has a significant linear correlation with body weight. Echo‐Doppler findings show that the mean renal arterial blood flow speeds for the left and right kidneys are comparable (0.70 and 0.73 m/s). However, flow speed is higher in the male (0.79 m/s) than in the female (0.60 m/s). The renal arterial diameters are between 1.0 and 1.8 mm. The fact that anesthesia can have hemodynamic effects on renal vasculature should be taken into consideration when assessing these echographic results. Am. J. Primatol. 71:647–653, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus)

Physiologically related features of muscle morphology are considered with regard to functional adaptation for locomotor and postural behavior in the brown lemur (Lemur fulvus). Reduced physiological cross-sectional area, estimated maximum excursion of the tendon of insertion, length of tendon per muscle fasciculus, and areal fiber type composition were examined in the quadriceps femoris in order to assess the extent of a "division of labor" among four apparent synergists. Each of these four muscles in this prosimian primate displays a distinguishing constellation of morphological features that implies functional specialization during posture and normal locomotion (walk/run, galloping, leaping). Vastus medialis is best suited for rapid whole muscle recruitment and may be reserved for relatively vigorous activities such as galloping and leaping (e.g., small cross-sectional area per mass, long excursion, predominance of fast-low oxidative fibers, relatively little tendon per fasciculus). In theory, rectus femoris could be employed isometrically in order to store elastic strain energy during all phasic activities (e.g., large cross-sectional area per mass, short excursion, predominance of fast-high oxidative fibers, large amount of tendon per fasciculus). Vastus intermedius exhibits an overall morphology indicative of a typical postural muscle (e.g., substantial cross-sectional area, short excursion, predominance of slow-high oxidative fibers, large amount of tendon per fasciculus). The construction of vastus lateralis reflects an adaptation for high force, relatively high velocity, and resistance to fatigue (e.g., large cross-sectional area, long excursion, most heterogeneous distribution of fiber types, large amount of tendon per fasciculus); this muscle is probably the primary contributor to a wide range of locomotor behaviors in lemurs. Marked dramatic architectural disparity among the four bellies, coupled with relative overall fiber type heterogeneity, suggests the potential for exceptional flexibility in muscle recruitment within this mass. One interpretation of this relatively complex neuromuscular organization in the brown lemur is that it represents an adaptation for the exploitation of a three-dimensional arboreal environment by rapid quadrupedalism and leaping among irregular and spatially disordered substrates.     

Interlimb coordination and gait in the brown lemur (Lemur fulvus) and the talapoin monkey (Miopithecus talapoin)

Patterns of interlimb coordination based on telemetered electromyography of extensor muscles are described for the brown lemur (Lemur fulvus) and the talapoin monkey (Miopithecus talapoin) in order to address the issue of possible motor programs for quadrupedal stepping in primates. Differences in modal patterns of ipsilateral limb coupling (phase intervals) between walking and galloping indicate that gait-specific programs do exist in primates, especially for symmetrical gaits. These preferred patterns distinguish primates from most other mammals (e.g., the domestic cat), but do not rule out the possibility of subtle differences among primates in species-specific mechanisms of neural control. Variability about the preferred modes is better interpreted as an expression of the flexibility or facultative capabilities of the neural mechanisms controlling locomotion than as “errors” in the motor program.     

Testing brown lemurs (Eulemur fulvus) on the reverse-reward contingency task without a modified procedure

A common paradigm used to study inhibitory control is the reverse-reward contingency task in which the subject is presented with a choice between two different quantities of food and is rewarded with the non-chosen item. Most animals have problems inhibiting their impulsive choice towards the larger quantity, and need correction procedures to master the reverse-reward task. Recent studies have nonetheless shown that rhesus macaques and white crowned mangabeys were able to master the task without correction procedures after a large number of trials were applied.We previously demonstrated that, similar to other primates tested under the reverse-reward contingency task, lemurs initially showed an impulsive bias towards the larger quantity of food. But following introduction of a large-or-none contingency, all the subjects learned to reliably select the smaller quantity in order to gain access to the larger one. Here, we assessed the possibility that, similar to rhesus macaques and mangabeys, lemurs could master the reverse-reward task, without a modified procedure, by presenting a large number of trials. One of 5 subjects was able to master the task and then generalize performance to novel food arrays.     

Nocturnal activity in the cathemeral red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse

Several ecological and physiological factors have been suggested to structure circadian activity in cathemeral primates, i.e., those that are regularly active both day and night, but their relative importance remains controversial. We studied the nocturnal activity of a group of cathemeral redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest in Western Madagascar to examine its relationship with one environmental factor, ambient light levels, in detail. To this end, nightly travel distances and moon luminosity were determined between March and June 1996. During this transitional period between the wet and dry seasons these red-fronted lemurs were regularly active at night, and traveled significantly larger distances during full-moon nights compared to new-moon nights. The importance of ambient luminosity for nocturnal activity was highlighted by observations during a total lunar eclipse (i.e., during a full-moon night), which caused abrupt cessation of the animal's activity. Our results support the hypothesis that nocturnal activity of these cathemeral lemurs is regulated also by changes in ambient light levels.