Group Composition, Home Range Size, and Diet of Three Sympatric Bamboo Lemur Species (Genus Hapalemur) in Ranomafana National Park, Madagascar

This is the first long-term, simultaneous, comparative study of three bamboo lemur species (Hapalemur griseus, H. aureus, and H. simus) at a site in southeastern-central Madagascar where they occur in sympatry. At Talatakely, Ranomafana National Park, the three Hapalemur spp. share overlapping home ranges. Hapalemur griseus has flexible group sizes, varying from three to nine individuals (n = 6). The home range of Hapalemur griseus averages 15 ha (n = 2). Hapalemur aureus forms family groups of 4 individuals (n = 3); they have a home range on average of 26 ha (n = 2). The single group of Hapalemur simus is composed of one or three adult males, two adult females, and their offspring; they occupy a home range of 62 ha. The three species of Hapalemur are year-round bamboo specialists: >88% of their diets consist of bamboo and grass in the Family Poaceae. Contrary to earlier findings, all three Hapalemur spp. consume the cynogenic parts—young leaf bases, young pseudopetioles, and young shoots—of the giant bamboo, Cathariostachys madagascariensis. They rely heavily on this plant, which comprises 72–95% of their diets. Hapalemur griseus and H. aureus consume similar proportions of bamboo vs. nonbamboo plants, though they differ in the species of bamboo they prefer. Hapalemur simus has the most distinct diet of the three bamboo lemurs. They exploit the young shoots of Cathariostachys madagascariensis during the austral summer rainy season, between November and April. From June to November, Hapalemur simus shifts its diet to eating the mature culm pith of Cathariostachys madagascariensis; the proportion of pith represented in their diet reaches a maximum of 89% in October. Seasonal availability of food resources, feeding competition, and factors related to body size may provide clues to the understanding of diet selection among the three sympatric Hapalemur spp.     

Lemur habitat and dental senescence in Ranomafana National Park, Madagascar

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.     

Patterns of male scent-marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

Scent-marking behavior has been well documented in many primate species. Three common functions attributed to scent-marking in males of multi-male/multi-female lemur species include: 1) advertisement of individual identity, 2) territorial defense, and 3) reproductive suppression. We examined the average number of scent-marks per hour exhibited daily by adult male sifakas (Propithecus edwardsi) and found that patterns of scent-marking changed with season, natal status, and dominance status. Males in single-male groups scent-marked at the highest rate, followed by dominant males, males of equal status, and subordinate males. Non-natal males generally scent-marked at higher rates than natal males, and adult males living in a natal group without a parent marked at higher rates than males living with a parent. All males scent-marked at higher rates in the migration season compared to the other seasons. These patterns were consistent with territorial defense and advertisement to females, and the suggestion that these chemical signals impart information concerning status. Since scent-marking behavior tracked seasons and varied with both dominance and natal status, it may serve multiple functions in males.     

The Effects of Habitat Disturbance on Lemurs at Ranomafana National Park, Madagascar

The alarming rate of deforestation in Madagascar is driving some endemic primates to extinction. Surprisingly, anthropogenic habitat disturbance is not always deleterious. The effect of disturbance on lemur abundance may be related to diet, with frugivorous species more prone to population declines than folivores or insectivores. To test the effects of disturbance on lemur abundance and group size, we surveyed 2 sites within contiguous forest at Ranomafana National Park, 1 lightly disturbed primary forest (Vato) and 1 heavily logged forest (Tala). We quantified forest structure variables along 6 survey routes and conducted 68 diurnal and 42 nocturnal lemur surveys. Canopy closure, canopy height, and understory visibility were greater in Vato than in Tala. We encountered 2 frugivorous lemurs (Eulemur rufifrons, Varecia variegata) and 1 folivore (Avahi peyrierasi) significantly more frequently in Vato than in Tala, whereas the opposite was true for the insectivorous Microcebus rufus. Rates did not differ statistically for 1 frugivore (Eulemur rubriventer) and 2 folivores (Propithecus edwardsi, Hapalemur griseus). Comparisons across the 6 survey routes suggest that the abundance was heterogeneous within as well as between sites. Neither group size nor composition differed between sites. Encounter rates for Varecia variegata were positively related to canopy closure, and encounter rates for Avahi peyrierasi were positively related to canopy height. Encounter rates for Microcebus rufus were negatively related to canopy closure, height, and understory visibility. Similar to other studies, the results suggest that some lemurs, including folivores, may cope with anthropogenic disturbance better than others, including some frugivores. Lemur abundance is heterogeneous, though, even on small spatial scales.     

Patterns of female dominance in Propithecus diadema edwardsi of Ranomafana National Park, Madagascar

Many lemur species are characterized by some form of female dominance, ranging from female feeding priority to complete female dominance, although this is a rare trait in primates and other mammals. The status of the Milne-Edwards' sifaka (Propithecus diadema edwardsi), a diurnal lemur, is ambiguous. Some short-term studies have found little or no aggression. The aim of the current, long-term study was to quantify the intersexual-dominance patterns of this sifaka. The distribution, outcome, and context of aggressive interactions were studied in four groups of wild sifakas. The majority of intersexual aggressive interactions were decided, with the loser expressing submissive behavior. Intersexual aggressive interactions occurred in all social contexts, and within all social contexts the females won the vast majority (92.7-96.0%) of aggressive interactions. While aggression rates were low (0.22/hr), this evidence suggests female dominance. We propose that female dominance exists because it provides a fitness advantage to both males and females.     

Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

In this study we compared the scent-marking rates of females with those of males. Specifically, we examined the ability of season, dominance status, and natal status to explain the frequency of scent marking in female sifakas living wild in Ranomafana National Park, Madagascar, and compared the results with those published for males [Pochron et al., American Journal of Primatology, in press]. We also sought to determine whether vulnerability to infanticide affects marking frequency in adults of either sex, and whether female reproductive status affects female marking behavior. We found that males marked at twice the rate of females, and like males, females in single-female groups marked at the highest rates. Dominant females and non-natal females marked at higher rates than did subordinate females and natal females, a pattern also seen in males. This suggests that scent marks may convey important information about status. Neither females nor males varied their marking frequency with the presence of vulnerable infants. Females did not alter marking frequency with reproductive state, and like males, they marked at higher rates in the period prior to the mating season than they did in the mating season itself. This implies that females may use scent marks more for intrasexual aggression or territoriality than for mate attraction.     

Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park,Madagascar

We investigated mechanical dietary properties of sympatric bamboo lemurs, Hapalemur g. griseus, H. aureus, and H. (Prolemur) simus, in Ranomafana National Park, Madagascar. Each lemur species relies on bamboo, though previous behavioral observations found that they specialize on different parts of a common resource (Tan: Int J Primatol 20 1999 547–566; Tan: PhD dissertation 2000 State University of New York, Stony Brook). On the basis of these earlier behavioral ecology studies, we hypothesized that specialization on bamboo is related to differences in mechanical properties of specific parts. We quantified mechanical properties of individual plant parts from the diets of the bamboo lemur species using a portable tester. The diets of the Hapalemur spp. exhibited high levels of mechanical heterogeneity. The lemurs, however, could be segregated based on the most challenging (i.e., mechanically demanding) foods. Giant bamboo culm pith was the toughest and stiffest food eaten, and its sole lemur consumer, H. simus, had the most challenging diet. However, the mechanical dietary properties of H. simus and H. aureus overlapped considerably. In the cases where lemur species converged on the same bamboo part, the size of the part eaten increased with body size. Plant parts that were harvested orally but not necessarily masticated were the most demanding, indicating that food preparation may place significant loads on the masticatory apparatus. Finally, we describe how mechanical properties can influence feeding behavior. The elaborate procurement processes of H. simus feeding on culm pith and H. griseus and H. aureus feeding on young leaf bases are related to the toughnesses of protective coverings and the lemurs' exploitation of mechanical vulnerabilities in these plants. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Timely estrus in wild brown mouse lemur females at Ranomafana National Park, southeastern Madagascar

The small-bodied nocturnal mouse lemurs (genus Microcebus) occupy a variety of habitats in Madagascar. Gray (M. murinus) and brown (M. rufus) mouse lemurs have been widely studied both in the wild and captivity. Whereas captive studies revealed an endogenous regulation of reproduction entrained by photoperiod, field studies have suggested that reproductive activation could be affected by additional climatic, physical, or social conditions. I collected data on wild brown mouse lemur females at Ranomafana between 2004 and 2008 to determine: 1) the timing of estrus and estrous periodicities across multiple seasons, and 2) whether additional factors such as body mass, age, or rainfall are correlated with onset of reproduction. In mouse lemur females at Ranomafana, the first seasonal estrus occurs 3-4 weeks after the vernal equinox. I report ~1 month's intra-population variation in the timing of estrus and inter-annual estrous intervals with periodicities of ~365 days. There were significant differences between the onset of reproduction across years. Estrous onset was uncorrelated with body mass, but there was an apparent age effect. There was a significant negative correlation between August rainfall and onset of reproduction when 2004 data were removed from the analysis. Results from this study are consistent with the notion that timing of estrus is photoperiod-dependent. As in captivity, intra-population variation in estrous onset is ~4 weeks in length. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments. In the wild, variation in estrous onset and polyestry (multiple reproductive opportunities per year) appear to be favored under the highly unpredictable conditions of Madagascar's environments.     

The Role of Demography and Markets in Determining Deforestation Rates Near Ranomafana National Park,Madagascar

The highland forests of Madagascar are home to some of the world''s most unique and diverse flora and fauna and to some of its poorest people. This juxtaposition of poverty and biodiversity is continually reinforced by rapid population growth, which results in increasing pressure on the remaining forest habitat in the highland region, and the biodiversity therein. Here we derive a mathematical expression for the subsistence of households to assess the role of markets and household demography on deforestation near Ranomafana National Park. In villages closest to urban rice markets, households were likely to clear less land than our model predicted, presumably because they were purchasing food at market. This effect was offset by the large number of migrant households who cleared significantly more land between 1989–2003 than did residents throughout the region. Deforestation by migrant households typically occurred after a mean time lag of 9 years. Analyses suggest that while local conservation efforts in Madagascar have been successful at reducing the footprint of individual households, large-scale conservation must rely on policies that can reduce the establishment of new households in remaining forested areas.     

Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar

This study investigated the effects of habitat on the diet, population density, and social structure of a small-bodied folivore, Hapalemur griseus. Three groups of H. griseus were followed at two study sites (Tala and Vato) within Ranomafana National Park in southeastern Madagascar. These two sites differed in degree of habitat disturbance, forest composition, and forest structure, as determined by botanical plots (50 x 10 m) which were monitored twice monthly in the home ranges of three study groups (group T, n = 4; group V1, n = 4; group V2, n = 2). Tala has experienced more habitat disturbance compared to Vato, and this appeared to influence population density and group size. The H. griseus that inhabit Tala occur at much higher densities and in larger social groups than the H. griseus at Vato. These results may be attributable to: 1) a greater number of potential food sources, 2) a more dense resource base, and/or 3) higher-quality resources at Tala for this folivore. In general, dietary diversity for all groups was low, and groups exploited similar plant species. However, within this small range of food sources, each study group specialized in food sources found in the highest abundance within their home range. This resulted in dietary differences between groups within sites, as well as differences between sites. Introduced tree species such as Chinese guava (Psidium cattleyanum) may have greatly impacted the diet and social structure of those groups at Tala, whose home ranges included this food source. In contrast, Vato group 1 ingested more new and mature leaves of Ficus spp., and Vato group 2 primarily ate spider bamboo (Nastus elongatus). In conclusion, it seems that microhabitat differences, which may be related to habitat disturbance and/or other factors such as topography, influenced the food species ingested by H. griseus. Overall habitat quality, which is likely also affected by habitat disturbance, influenced general diet, population density, and group size.     

Diet of the Brown Mouse Lemur (Microcebus rufus) in Ranomafana National Park, Madagascar

The conventional notion is that small-bodied primates should be highly insectivorous in order to obtain protein and other nutrients from a food source that is more easily digestible than plant matter. I studied feeding behavior of Microcebus rufus for 16 months in the east coast rainforest of Ranomafana National Park. I determined the diet primarily through analysis of 334 fecal samples from live-trapped individuals. They consumed a mixed diet basically of fruit and insects year-round. I identified 24 fruits, while 40–52 remain unidentified. Bakerella, a high-lipid epiphytic semiparasitic plant, was in 58% of fecal samples that contained fruit seeds, and was consumed year-round irrespective of general resource availability. It served both as a staple and keystone resource. Fruit was less frequently totally absent from fecal samples of individual mouse lemurs than insect matter was. For Microcebus rufus, fruit may be a primary source of energy, not just complementary to insects. Fruit consumption increased in quantity and diversity during the latter part of the rainy season and the very early part of the dry season, when fruit production was relatively high. This pattern in fruit feeding is similar to that for mouse lemurs in the west coast dry forests and is related to specific nutritional needs dictated by the highly seasonal character of the life cycle. Coleoptera were present in 67% of samples examined and were consumed year-round by the subjects, but insect consumption did not increase during the rainy season when insect abundance was highest.     

Olfactory predator recognition in the brown mouse lemur (Microcebus rufus) in Ranomafana National Park,Madagascar

Predator odors such as urine and feces are known to elicit antipredator behaviors in prey including avoidance, fear, and curiosity. We measured how wild brown mouse lemurs (Microcebus rufus) responded to odors of mammalian, avian, and snake predators as well as nonpredator controls. The first experiment took place under controlled conditions in a laboratory where we recorded the occurrence of four behavioral categories (ignore, curiosity, alert, and fear) in response to a single odor. Subjects exhibited behavioral change significantly more often in response to the predator than to control stimuli, but did not distinguish between familiar and unfamiliar predators. Mammalian predator urine and feces were most likely to elicit behavioral change. The owl was the only predator to never elicit behavioral change, possibly because owls do not provide relevant odor cues. A second experiment employing live traps in the forest found that neither predator nor control odors affected the likelihood of capture. Due to their longevity, odors do not provide accurate information of spatial and temporal risk, and while mouse lemurs may have initially hesitated to enter a trap, in the absence of additional information about risk, they may have eventually ignored the stimuli. This study found that brown mouse lemurs are able to distinguish between predator and nonpredator odors, and that risk assessment may be affected by the experience, as well as predator and sensory stimulus quality.     

Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar

We present a summary of a long-term field study that examined the effects of forest disturbance on the availability of palatable fruit and its utilization by V. variegata. Forest structure and tree species composition were measured in three adjacent study areas, with different histories of disturbance, in Ranomafana National Park (RNP), Madagascar. V. variegata abundance was monitored by frequent encounters with resident groups and periodic censuses conducted along trails. Finally, the abundance of mature fruit in species used by V. variegata was scored monthly at representative trees at several locations. V. variegata abundance was most consistent in the least anthropogenically disturbed site, while no established lemur groups were observed in the heavily logged site for over a decade post-harvest. Lemur abundance was variable in the selectively logged site. The presence of select food trees, particularly specimens with voluminous crowns capable of producing abundant fruit crops, appears to be key to the establishment and expansion of V. variegata groups. Our analysis of year-long fruit utilization revealed a high degree of preference for several species of trees. Two species exhibited mature fruit in a low percentage of stems but were available for a protracted period of time, while two additional species showed high intraspecific fruiting synchrony and were available for a shorter period of time. These contrasting phenologies, rather than the individual tree species, may be most important to V. variegata due to their coincident timing of fruit maturation with key lemur life-history events. Any disturbance-natural or anthropogenic-that disrupts the phenology cycles of food trees has the potential to impact lemur abundance and dispersion. Intense disturbances, such as heavy logging or severe cyclones, have long-lasting impacts on fruit production, while selective logging or moderate cyclonic windthrow cause more transient impacts. V. variegata is adapted to deal with an intrinsically erratic food supply by virtue of its reproductive biology and social behavior.     

Ecological Flexibility of Propithecus edwardsi in Two Forest Habitats with Different Logging Histories in Ranomafana National Park,Madagascar

International Journal of Primatology - In the face of global change, where anthropogenic practices, such as logging, alter the structure and composition of forest habitats and impact...     

Similarities,differences, and seasonal patterns in the diets ofEulemur rubriventer andEulemur fulvus rufus in the Ranomafana National Park,Madagascar

I studied the diets of two sympatric species ofEulemur (E. fulvus rufus andE. rubriventer) in the Ranomafana National Part in southeastern Madagascar from July 1988 through August 1989. Both species were highly frugivorous throughout the year and devoted similar amounts of time to feeding daily; the composition of their diets were similar. Three aspects of both lemur species' diets were correlated with seasonal food availability: changes in interspecific dietary overlap, the length of feeding bouts, and the amount of time devoted to feeding daily. Throughout the year neither species had a more diverse or more folivorous diet than its sympatric congener. However, there were several consistent year-round differences between their diets.E. f. rufus initiated more feeding bouts daily that were shorter in duration than those ofE. rubriventer. E. f. rufus also consistently exploited more unripe fruits and mature leaves thanE. rubriventer did throughout the study.E. f. rufus migrated from the study site during a period of fruit scarcity. These dietary patterns are discussed here in regard to feeding patterns observed in other sympatric congeneric primate species, whether these dietary differences can contribute to these two species' ability to coexist, and how differences in diet may be influenced by differences in social structure. I suggest that subtle, consistent differences in diet and seasonal dietary differences are sufficient to allow these two species to coexist.     

Demography, life history, and social structure in Propithecus diadema edwardsi from 1986-2000 in Ranomafana National Park, Madagascar

Prosimian lemurs differ fundamentally from anthropoid primates in many traits related to social structure. By exploring the demography of Milne-Edwards' sifakas (Propithecus diadema edwardsi), and comparing it to other well-studied primates, we explore the effect of demographic and life-history factors on social structure. Specifically, we compare lemur survivorship and fertility patterns to two published composite models: one created for New World and another created for Old World monkeys. Using longitudinal data collected on individual Propithecus diadema edwardsi from four study groups from 1986-2000 in Ranomafana National Park, Madagascar, we quantify 1) group composition, 2) birth seasonality, 3) interbirth interval, 4) life-table values, and 5) population growth estimates. The mortality, survivorship, and life-expectancy schedules indicate high infant and juvenile mortality. Fertility remains high until death. The intrinsic rate of increase and net reproductive rate indicate a shrinking population. We suggest that high mortality rather than low fertility causes the observed population decline. While sifaka survivorship closely resembles New World patterns, fertility resembles Old World patterns, i.e., like New World monkeys, few sifakas survive to reproductive age, and those that do, reproduce at a slow rate resembling the Old World pattern. This necessarily impacts social structure. An adult sifaka at the end of her lifespan will have one only daughter who survives to reproductive age, compared to 3.4 for New World or 2.7 for Old World monkeys. Demography limits the formation of large kin-based groups for sifakas, and survivorship and fertility patterns do not easily permit sifakas to form large same-sex family groups.     

Comparing aye-aye (Daubentonia madagascariensis) presence and distribution between degraded and non-degraded forest within Ranomafana National Park, Madagascar

The aye-aye is considered the most widely distributed lemur in Madagascar; however, the effect of forest quality on aye-aye abundance is unknown. We compared aye-aye presence across degraded and non-degraded forest at Ranomafana National Park, Madagascar. We used secondary signs (feeding sites, high activity sites) as indirect cues of aye-aye presence and Canarium trees as an indicator of resource availability. All 3 measured variables indicated higher aye-aye abundance within non-degraded forest; however, the differences across forest type were not significant. Both degraded and non-degraded forests showed a positive correlation between feeding sites and high activity sites. We found that Canarium, an important aye-aye food source, was rare and had limited dispersal, particularly across degraded forest. This preliminary study provides baseline data for aye-aye activity and resource utilization across degraded and non-degraded forests.     

Feeding Ecology of Sympatric Mouse Lemur Species in Northwestern Madagascar

We performed a comparative pilot study on vertical space use and feeding ecology of 2 closely related sympatric mouse lemur species in northwestern Madagascar. We recorded feeding behavior and the use of vertical forest strata for 6 gray and 4 golden-brown mouse lemur females that we followed for 120 h. We carried out feeding experiments and analyzed fecal samples for food remains. Both species showed no significant difference in use of forest strata. They had a similar overall diet, with insect secretions and gum as main plant food resources; arthropod remains occurred in about half of all fecal samples. Both lemurs used in common >50% of the plant species that each consumed, which accounts for ≥70% of all individual plants used. However, both species used >40% of their feeding plant species exclusively and seemed to differ in their degree of specialization on certain plant species.