Edge effects and their influence on lemur density and distribution in Southeast Madagascar

Edge effects are caused by the penetration of abiotic and biotic conditions from the matrix into forest interiors. Although edge effects influence the biogeography of many tropical organisms, they have not been studied directly in primates. Edge effects are particularly relevant to lemurs due to the loss of 80-90% of forests in Madagascar. In this study, data are presented on how biotic edge effects influenced the distribution and density of lemurs in the Vohibola III Classified Forest in southeastern Madagascar. In total, 415 lemur surveys were conducted during June-October 2003 and May-September 2004 along six 1,250-m transects that ran perpendicular to the forest edge. Data were also collected on lemur food trees along the six transects (density, height, diameter at breast height, area, volume, and distance to forest edge). Four nocturnal species (Avahi laniger, Cheirogaleus major, Lepilemur microdon, and Microcebus rufus) and four diurnal species (Eulemur rubriventer, Eulemur fulvus rufus, Hapalemur grisesus griseus, and Propithecus diadema edwardsi) were sighted during surveys. Regression analyses of lemur densities as a function of distance to forest edge provided edge tolerances for A. laniger (edge-tolerant), M. rufus (edge-tolerant), E. rubriventer (edge-tolerant or omnipresent), and H. g. griseus (omnipresent). The density and distribution of M. rufus and their foods trees were correlated. Edge-related variations in food quality and predation pressures may also be influencing lemurs in Vohibola III. Tolerance for edge effects may explain, in part, how lemurs have survived extreme habitat loss and forest fragmentation in southeastern Madagascar.     

Lemur responses to edge effects in the Vohibola III classified forest, Madagascar

Forest edges are dynamic zones characterized by the penetration (to varying depths and intensities) of conditions from the surrounding environment (matrix) into the forest interior. Although edge effects influence many tropical organisms, they have not been studied directly in primates. Edge effects are particularly relevant to lemurs because of the highly fragmented forest landscapes found in Madagascar. In this study, data are presented regarding how the densities of six lemur species (Avahi laniger, Cheirogaleus major, Eulemur rubriventer, Hapalemur griseus griseus, Microcebus rufus, and Propithecus diadema edwardsi) varied between six 500-m interior transects and six 500-m edge transects in the Vohibola III Classified Forest in SE Madagascar. Diurnal (n = 433) and nocturnal (n = 128) lemur surveys were conducted during June-October 2003 and May-November 2004. A. laniger, E. rubriventer, and H. g. griseus exhibited a neutral edge response (no differences in densities between habitats). M. rufus and P. d. edwardsi had a positive edge response (higher densities in edge habitats), which may be related to edge-related variations in food abundance and quality. Positive edge responses by M. rufus and P. d. edwardsi may ultimately be detrimental due to edge-related anthropogenic factors (e.g., hunting by local people). The negative edge response exhibited by C. major (lower densities in edge habitats) may result from heightened ambient temperatures that inhibit torpor in edge habitats.     

Direct and Indirect Impacts of Raptor Predation on Lemurs in Southeastern Madagascar

I calculated rates of predation by 2 species of diurnal raptors, Polyboroides radiatus and Accipiter henstii, on the lemur community of Ranomafana National Park, Madagascar from 2700 h of observation and 470 prey deliveries at 7 nests of each hawk species. The 2 hawks consumed 7 of 12 lemurs found in the park region, with a body mass of 63–3500 g and including diurnal and nocturnal species of all group sizes. Calculations of predation rates indicate that raptor predation is a significant cause of mortality for lemur populations relative to other causes. Minimum rates of predation by Polyboroides radiatus and Accipiter henstii on Microcebus rufus, Cheirogaleus major, Avahi laniger, Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, and Varecia variegata resulted in the raptors removing of 1–21% of the population per yr, similar to other rates of predation on primates documented in the literature. Modeling of lemur populations under varying levels of raptor predation pressure that I calculated found that one may attribute 3–17% of adult, juvenile, and infant mortality for nocturnal lemurs and 2–66% of adult, juvenile, and infant mortality for diurnal lemurs to diurnal raptor predation. Raptor predation may significantly depress intrinsic growth rates and carrying capacity of Avahi laniger, Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, and Varecia variegata owing to their low fecundities, long life spans, and long age to sexual maturation. Nocturnal lemurs may best avoid predation by diurnal raptors by exhibiting a solitary lifestyle and cryptic antipredator tactics, whereas, diurnal lemurs benefit less by increasing group size than by using specific antipredator tactics.     

Ecological Correlates to Lemur Community Structure in Southeast Madagascar

The Fandriana-Marolambo forest corridor is one of the largest (ca. 250,000 ha) and least explored tracts of unprotected forest in southeast Madagascar. Although published range maps show continuous distributions for many lemurs throughout the region, there are few data on lemur community structure in the corridor. We aimed to determine lemur community structure, with its ecological correlates (altitude, agriculture, selective logging, and hunting), in the Fandriana-Marolambo forest corridor. We surveyed 7 sites and sighted 4 nocturnal taxa (Avahi laniger, Cheirogaleus major, Lepilemur mustelinus, and Microcebus rufus) and 6 diurnal taxa (Eulemur rubriventer, E. fulvus rufus, E. f. fulvus, Propithecus diadema edwardsi, Hapalemur griseus griseus, and Varecia variegata variegata). Composition of the lemur community was broadly similar to that of nearby protected areas (Ranomafana and Mantadia National Parks). However, we sighted no Hapalemur aureus, H. simus, or Indri indri, and observed Propithecus diadema edwardsi and Varecia variegata variegata at only 1 site each. We sighted an apparent hybrid form of Eulemur fulvus fulvus and E. f. rufus that may represent a new hybrid zone for lemurs. After testing for spatial autocorrelation, lemur diversity correlates negatively with altitude and agricultural intensity. Though the Government of Madagascar is assessing the corridor as a new national park, we suggest conservation plans for local lemurs are complicated by population isolation and lack of data on minimum viable size of the proposed protected area.     

Surveys of sympatric lemurs at Anjamena, north-west Madagascar

In order to assess the status of lemurs along the lower reaches of the Mahavavy in north-west Madagascar, we carried out transect line sampling at Anjamena between April and August 1995. These data were complemented by additional absence–presence surveys conducted in 1994 and 1995 in many of the remaining forested areas of the region. This is the first study of lemur population density estimates for the faunal subregion between the rivers Mahavavy and Betisboka. Six sympatric lemurs are found at Anjamena: Cheirogaleus medius, Eulemur fulvus rufus, E. mongoz, Lepilemur sp., Microcebus murinus and Propithecus verreauxi coronatus. Data suggest that in some parts of the region large numbers of lemurs may still be found (E. f. rufus 121 individuals per km², E. mongoz (45), Lepilemur sp. (110), M. murinus (85) and P. v. coronatus (173)). No density data are provided for C. medius. In conclusion, as high lemur population densities may still be found and, in particular, P. v. coronatus is not known to exist in any protected area, Anjamena could serve as an important addition to the protected area system of north-west Madagascar.     

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.     

A possible role of plantations for primate conservation in Madagascar

The utilization of eucalyptus plantations by seven sympatric species of prosimians was studied in the eastern rainforest of Madagascar. The species were Avahi laniger, Cheirogaleus major, Hapalemur griseus, Indri indri, Lemur fulvus, Lepilemur mustelinus, and Microcebus rufus. None of the lemurs was ever found in young eucalyptus plantations with little undergrowth. This was mainly due to the lack of travel opportunities within the shrub layer and between the shrubs and the canopy. Food (mainly berries) is seasonally available in the shrub layer but cannot be exploited because frugivorous lemurs cannot reach it. Old eucalyptus plantations with dense undergrowth are used by all prosimian species. They provide food as well as travel and resting facilities. Mixed tree plantations in the western part of Madagascar were used by groups of Lemur fulvus, Lepilemur mustelinus, and Propithecus verreauxi. According to these results, old eucalyptus plantations and mixed tree species plantations could be used to provide firewood and construction wood for the human population. They also might extend the habitat for lemurs and serve as buffers against human disturbance.     

Variation in the leaping of lemurs

Locomotor diversity among lemurids has been ignored by placing most species into a category of arboreal quadrupeds. Recent field studies have shown that leaping behaviors comprise a relatively large amount of their travel. In this contribution I detail a study of captive lemurs locomoting on a designed support network and/or in outdoor enclosures. Associations between support context, leaping behaviors, and landing kinematics are detailed for Hapalemur griseus, Eulemur rubriventer, Eulemur fulvus, Eulemur mongoz, and Varecia variegata. In-air body position, including the amount and location of trunk flexion, coupled with the extent of shoulder and hip flexion dictates limb use at landing. Limb strike pattern when landing onto the same support type varies interspecifically. The kinematic variation in leaping behaviors may well have implications for functional analyses of the postcranium. © 1996 Wiley-Liss, Inc.     

Phylogenetic relationships among Malagasy lemurs as revealed by mitochondrial DNA sequence analysis

Systematics and evolution of Malagasy lemurs has been analyzed using morphological characters, fossil evidence, ecological/ethological data, and chromosomal banding patterns. Recent developments in DNA technology have provided evolutionary biologists with additional and powerful tools for making phylogenetic inference. In the last years several studies concerning highly repeated DNA sequences (hrDNA) provided new insights about the systematic relationships among the different species of Lemuridae and Cheirogaleidae. Here, a reconstruction of molecular phylogeny of extant Malagasy lemurs based on the comparison of cytochrome-b mitochondrial DNA sequences is presented. With the Polymerase Chain Reaction (PCR) and direct sequencing of amplified DNA fragments, both the phylogenetic range and resolving power of comparative analysis can be extended. These techniques allow to gather sequence data useful to evaluate the pattern of molecular evolution offering opportunities for phylogenetic purposes. A 290-bp fragment of cytochrome-b gene has been amplified and sequenced from the following species:Tupaia glis, Galago alleni, Daubentonia madagascariensis, Indri indri, Varecia variegata, Eulemur fulvus, Eulemur coronatus, Eulemur rubriventer, Eulemur mongoz, Eulemur macaco, Lemur catta, andHapalemur griseus griseus. The phylogenetic trees obtained show the relationships among the Eulemur species and confirm the karyological and hrDNA results of a separated clade forL. catta/Hapalemur. The separation ofVarecia variegata from the other genus of the family Lemuridae is discussed.     

Census of brown lemurs (Eulemur fulvus sspp.) in southeastern Madagascar: Methods‐testing and conservation implications

Four forest areas were censused in southeastern Madagascar from June–August 1995 to estimate local population densities and habitat conditions for two threatened subspecies of brown lemur (Eulemur fulvus collaris and Eulemur fulvus albocollaris). Survey transects varied in length (1–3.5 km) and in surveillance frequency (three to seven times). Additional test surveys were conducted at the Parc National de Ranomafana to compare transect methods in an area with known population densities of Eulemur fulvus. Based on these tests, we demonstrate that the use of existing trails for transects can result in a close estimate of local population size, although more replications and longer transects increase precision. Results from regional surveys indicate considerably smaller population densities for E. f. albocollaris (0.086 animals/ha). In contrast, E. f. collaris densities were relatively high (.107 animals/ha) at Midongy‐Sud. We also noted variation among sites in the density of lianas, which was positively correlated with local population density (a possible indication of habitat degradation). More generally, habitats in E. f. albocollaris's range suffered from fragmentation, reduction in forest area, logging, and potentially greater hunting pressure. Based on these results, it is apparent that more immediate steps are necessary to preserve E. f. albocollaris populations and habitats. Am. J. Primatol. 47:51–60, 1999. © 1999 Wiley‐Liss, Inc.     

Spatial variations in Eulemur fulvus rufus and Lepilemur mustelinus densities in Madagascar

I present data on variations in Eulemur fulvus rufus and Lepilemur mustelinus densities as well as tree characteristics (height, diameter and stem frequency) between edge and interior forest habitats in southeastern Madagascar. Line transect surveys were conducted from June 2003 to November 2005 in edge and interior forest habitats in the Vohibola III Classified Forest. Although E. f. rufus densities were significantly lower in edge habitats than in interior habitats, density estimates for L. mustelinus did not differ significantly between habitats. Trees in edge habitats were significantly shorter, had smaller diameters and had lower stem frequencies (for those >25 cm in diameter) than trees in interior habitats. Spatial characteristics of food abundance and quality may explain lemur density patterns in Vohibola III. Low E. f. rufus densities may reduce seed dispersal in edge habitats, which has important consequences for the long-term viability of forest ecosystems in Madagascar.     

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 16-hydroxyestrone appeared to be the predominant estrogen in the urine of E. rubriventer. Estradiol-17ß was either absent (Hapalemur) or present in very low amounts. HPLC of progestogens had high levels of immunoreactivity in an assay against 5-pregnane-3-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.     

Characterization of 14 microsatellite marker loci in the grey bamboo lemur (Hapalemur griseus)

Fourteen nuclear microsatellite loci were isolated from a genomic DNA library derived from a free‐ranging bamboo lemur (Hapalemur griseus griseus) from Ranomafana National Park, Madagascar. Expected and observed heterozygosity levels were determined for populations of bamboo lemurs from Ranomafana National Park and a nonprotected area near Tsinjoarivo, Madagascar. Although genotype frequencies for all but one marker were within Hardy–Weinberg expectations for the Tsinjoarivo population, this was not the case for the Ranomafana samples. It is probable that the deviation of genotype frequencies from Hardy–Weinberg expectations in Ranomafana was precipitated by the presence of two taxa within the sample population.     

Phylogenetic relationships among Lemuridae (Primates): evidence from mtDNA

The family Lemuridae includes four genera: Eulemur, Hapalemur, Lemur,Varecia. Taxonomy and phylogenetic relationships between L. catta, Eulemur and Hapalemur, and of Varecia to these other lemurids, continue to be hotly debated. Nodal relationships among the five Eulemur species also remain contentious. A mitochondrial DNA sequence dataset from the ND 3, ND 4 L, ND 4 genes and five tRNAs (Gly, Arg, His, Ser, Leu) was generated to try to clarify phylogenetic relationships w ithin the Lemuridae. Samples (n=39) from all ten lemurid species were collected and analysed. Three Daubentonia madagascariensis were included as outgroup taxa. The approximately 2400 bp sequences were analysed using maximum parsimony, neighbor-joining and maximum likelihood methods. The results support monophyly of Eulemur, a basal divergence of Varecia, and a sister-group relationship for Lemur/Hapalemur. Based on tree topology, bootstrap values, and pairwise distance comparisons, we conclude thatVarecia and Eulemur both represent distinct genera separate from L. catta. H. griseus andH. aureus form a clade with strong support, but the sequence data do not permit robust resolution of the trichotomy involving H. simus, H. aureus/H. griseus and L. catta. Within Eulemur there is strong support for a clade containing E. fulvus, E. mongoz and E. rubriventer. However, analyses failed to clearly resolve relationships among those three species or with the more distantly related E. coronatus and E. macaco. Our sequencing data support the current subspecific status of E.m. macaco and E.m. flavifrons, and that of V.v. variegata and V.v. rubra. However, tree topology and relatively large genetic distances among individual V.v. variegata indicate that there may be more phylogenetic structure within this taxon than is indicated by current taxonomy.     

Edge Effects on the Density of Cheirogaleus major

We investigated how greater dwarf lemur (Cheirogaleus major) densities, ambient air temperature, and dendrometrics (tree height and diameter) varied along forest edge-interior gradients in the Vohibola III Classified Forest in SE Madagascar. We also assessed if spatial variations in densities of Cheirogaleus major provide indirect evidence of increased predation pressure in the transition zone between edge and interior forest habitats, i.e., an ecological trap. We conducted diurnal temperature surveys (N = 394) and nocturnal surveys of Cheirogaleus major (N = 182) over 2 yr along 4 1250-m transects that ran perpendicular to the forest edge in Vohibola III. We did not see Cheirogaleus major from May to mid-September, and the highest sighting frequency occurred during October–November. Cheirogaleus major exhibited a negative edge response because densities ranged from low levels in edge habitats to higher levels in the forest interior. After we tested for spatial autocorrelation, edge-related variations in densities of Cheirogaleus major covaried most strongly with tree diameter. Edge responses of Cheirogaleus major may reflect spatial variations in fruit and liana abundance, though data are needed on the precise relationship between tree diameter and food production to confirm the relationship. Edge-related variations in densities of Cheirogaleus major may also provide indirect evidence of an ecological trap. Testing and controlling for spatial autocorrelation should be important components of future studies of primate conservation biology and ecology.     

Prosimian hemoglobins--V. The primary structures of the alpha-I, alpha-II and beta-hemoglobin chains of Hapalemur griseus, with a note on the classification of Microcebus

1. The duplicated adult hemoglobins were isolated from a mature Hapalemur griseus and the constituent chains prepared. Sequence analysis of the isolated alpha-globins showed that the alpha-I and alpha-II chains differed by a glycine for lysine substitution at position 15. 2. The complete amino acid sequence of the single adult beta-globin of Hapalemur griseus was determined. The beta-globin sequence of Hapalemur griseus clusters with those of other authentic lemurs, and is clearly separated from the sequences characteristic of lorisiform primates. 3. Partial sequence analysis of the beta-globin of Microcebus murinus showed only a single amino acid difference when compared to the Hapalemur globin. 4. Partial sequence analysis of the alpha-globin of Microcebus murinus showed only three amino acid residues that are not found in other lemuriform alpha-globins; two of these are unique to Microcebus among all known prosimian alpha-globin sequences. 5. The Microcebus alpha- and beta-globins are more similar to the homologous lemuriform sequences than they are to lorisiform sequences.     

Maintenance of female dominance in blue‐eyed black lemurs (Eulemur macaco flavifrons) and gray bamboo lemurs (Hapalemur griseus griseus) under semi‐free‐ranging and captive conditions

Several species of Malagasy prosimians are characterized by female dominance, an unusual trait among mammals. We compare the extent to which female dominance is displayed and the mechanisms that are used to maintain dominance in the frugivorous blue‐eyed black lemurs (Eulemur macaco flavifrons) and the folivorous gray bamboo lemurs (Hapalemur griseus griseus) housed at the Duke Lemur Center. All dominant–submissive interactions were recorded during 448 hr of focal animal observations. Both species of lemurs exhibited clear patterns of female dominance. However, the two species used aggressive dominance (defined as aggression+submission) and social dominance (defined as submission in the absence of aggression) to different extents in maintaining hierarchies within each group. The adult female blue‐eyed black lemurs used aggressive dominance (e.g., chase, cuff, bite) in more of their dominance interactions (66%) than did the adult female gray bamboo lemurs (40%). In both species, rates of aggressive dominance interactions were higher during feeding versus nonfeeding periods and while in smaller outdoor runs versus larger natural habitat enclosures, but the differences were not significant. Overall blue‐eyed black lemurs exhibit a more aggressive form of female dominance compared to the gray bamboo lemur. Zoo Biol 26:345–361, 2007. © 2007 Wiley‐Liss, Inc.     

Confirmation of the specific status ofHapalemur aureus (Primates,Strepsirhini) by restriction genomic DNA banding patterns

This study confirms, on the basis of our molecular biology results and in accordance with cytogenetic, morphological and ethological data, the specific status ofHapalemur aureus. Furthermore, it appears clearly thatHapalemr simus began its differentiation fromHapalemur griseus griseus andHapalemur aureus (wich have a common branch) shortly after the separation ofLemur catta from the phylogenetic tree of theL. catta/ Hapalemur group.     

Seasonal Fluctuations in Body Fat and Activity Levels in a Rain-Forest Species of Mouse Lemur,Microcebus rufus

Seasonal fattening in preparation for the dry season followed by torpor characterizes some members of the family Cheirogaleidae, a group of < 600-g nocturnal Malagasy primates. These behaviors are associated with extreme seasonality in dry forests, where most studies have been conducted. I aimed to determine if the brown mouse lemur (Microcebus rufus), a rain-forest species of cheirogaleid, exhibited similar changes. Between January 1993 and May 1994 I conducted a mark-recapture study on Microcebus rufus in the rain forest of Ranomafana National Park. I monitored body weight and tail circumference for body fat fluctuations and inferred changes in activity levels from presence or absence in the traps. Some individuals of both sexes increased body fat and entered torpor as suggested by their absence from traps for at least 1 month of the dry season. Activity was resumed with body weight reduced by 5–35 g, and tail circumference by 0.4–1.2 cm. Population-level analysis supports these results; highest weight and tail circumference values occurred just before and at the onset of the dry season. Other individuals, predominantly male, exhibited no change in body fat or activity level, and some mouse lemurs increased their body fat over the course of the dry season. Age, social status, and individual response may influence seasonal behavioral strategies. Dry and rain-forest species of mouse lemur adopt similar behaviors to cope with environmental stresses. Mouse lemurs resemble nonprimate, small-bodied mammals, in which behavioral changes related to maintaining energy balance occur during seasonally unfavorable conditions.