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.     

New hand bones of Hadropithecus stenognathus: implications for the paleobiology of the Archaeolemuridae

A partial, associated skeleton of Hadropithecus stenognathus (AHA-I) was discovered in 2003 at Andrahomana Cave in southeastern Madagascar. Among the postcranial elements found were the first hand bones (right scaphoid, right hamate, left first metacarpal, and right and left fifth metacarpals) attributed to this rare subfossil lemur. These hand bones were compared to those of extant strepsirrhines and catarrhines in order to infer the positional adaptations of Hadropithecus, and they were compared to those of Archaeolemur in order to assess variation in hand morphology among archaeolemurids. The scaphoid tubercle does not project palmarly as in suspensory and climbing taxa, and the hamate has no hook at all (just a small tubercle), which also points to a poorly developed carpal tunnel. There is a distinctive, radioulnarly directed "spiral" facet for articulation with the triquetrum that is most similar in orientation to that of more terrestrial primates (i.e., Lemur catta, Papio, and Gorilla). The first metacarpal is very reduced and represents only 48% of the length of metacarpal V, as in Archaeolemur, which suggests that pollical grasping of arboreal supports was not important. Compared to Archaeolemur, the shaft of metacarpal V is gracile, and the head has no dorsal ridge and lacks characteristics functionally associated with digitigrade, extended metacarpophalangeal joint postures. Proximally, the articular facet for the hamate is oriented more dorsally. Thus, the carpometacarpal joint V appears to have a distinctive hyperextended set, which has no analog among living or extinct primates. The carpals of Hadropithecus are diagnostic of a pronograde, arboreal and terrestrial (although not digitigrade) locomotor repertoire that typifies Lemur catta and some Old World monkeys. No clinging, suspensory, or climbing specializations that characterize indriids or lorises can be found in the hand of this subfossil lemur. The hand of Hadropithecus likely had similar ranges of movement at the radiocarpal and midcarpal joints as of those of pronograde primates, such as lemurids, for which the hand is held in a more extended, pronated, and neutral (i.e., showing less ulnar deviation) position during locomotion in comparison to that of vertical clingers or slow climbers. Although highly autapomorphic, the hand of Hadropithecus resembles that of its sister taxon, Archaeolemur, in having a very reduced pollex and an articular facet on the scaphoid for a sizeable prepollex. These unusual hand features reinforce the monophyly of the Archaeolemuridae.     

Diets of Two Lemur Species in Different Microhabitats in Beza Mahafaly Special Reserve,Madagascar

Studies of primate diets usually focus on differences that distinguish species or populations. However, variation in diet can occur at a more local level of groups within a population, especially in a non-homogeneous habitat. I compared dietary variation in food composition and toughness across groups of 2 lemur species in Beza Mahafaly special reserve, Madagascar. Beza Mahafaly contains an 80-ha reserve (Parcel 1) that, while small, hosts a dense population of Lemur catta (ring-tailed lemurs) and Propithecus verreauxi verreauxi (sifakas). Microhabitats in the eastern vs. western sides of the parcel are structurally and floristically distinct. Sifakas in this parcel have small, discrete home ranges and are morphological folivores. For these reasons, I expected that the 6 groups studied would eat a different menu of food plants but with similar toughness values. Ring-tailed lemurs have comparatively large, overlapping home ranges, and I expected that the 5 study groups would eat similar foods. Despite living in different microhabitats across the parcel, sifakas exhibit high dietary uniformity both in dietary plant species composition and the toughness of the foods. Food selection in sifakas operates on two distinct levels. Sifaka groups share many key food species that appear independent of local abundances, but the ranking of the foods within each group appears related to availability. Ring-tailed lemur groups are more heterogeneous in the composition of their diets relative to sifakas, though the time spent feeding on individual foods reveals a marked preference for the fruits of Tamarindus indica by all groups. Food toughness is consistent across the parcel with the exception of the most western group. Ring-tailed lemurs are highly specific feeders, but indiscriminate nibblers. Sifakas are targeted, balanced feeders. There does not appear to be a consistent microhabitat effect operating across species. Differences within sifaka and ring-tailed lemur populations in food composition and toughness, however, correspond to an east-west microhabitat gradient. Measures of dietary flexibility must take into account not only the plant species consumed and the different parts eaten but also their associated food properties and proportion of time spent feeding on them.     

Isolation of 10 microsatellite markers for mongoose lemurs (Eulemur mongoz)

We present here 10 new microsatellite markers for the mongoose lemur (Eulemur mongoz), nine of which were isolated from E. mongoz and one from Lemur catta. At least 60 individuals were genotyped for each of the 10 loci. Mendelian inheritance at each locus was tested by genotyping five captive families with known pedigrees. All loci were polymorphic and demonstrated simple Mendelian inheritance. The microsatellite markers presented here will be useful for genetic surveys of wild E. mongoz, to gain insights into the genetic background of the captive population, and to aid in the conservation of the species’ genetic diversity.     

Phylogeny of the Lemuridae: Effects of Character and Taxon Sampling on Resolution of Species Relationships within Eulemur

DNA sequences from three mitochondrial genes and one nuclear gene were analyzed to determine the phylogeny of the Malagasy primate family Lemuridae. Whether analyzed separately or in combination, the data consistently indicate that Eulemur species comprise a clade that is sister to a Lemur catta plus Hapalemur clade. The genus Varecia is basal to both. Resolution of cladogenic events within Eulemur was found to be extremely problematic with a total of six alternative arrangements offered by various data sets and weighting regimes. We attempt to determine the best arrangement of Eulemur taxa through a variety of character and taxon sampling strategies. Because our study includes all but one Eulemur species, increased taxon sampling is probably not an option for enhancing phylogenetic accuracy. We find, however, that the combined genetic data set is more robust to changes in taxon sample than are any of the individual data sets, suggesting that increased character sampling stabilizes phylogenetic resolution. Nonetheless, due to the difficult nature of the problem, we may have to accept certain aspects of Eulemur interrelationships as uncertain.     

Semi‐quantitative tests of cyanide in foods and excreta of Three Hapalemur species in Madagascar

Three sympatric Hapalemur species (H. g. griseus, H. aureus, and H. (Prolemur) simus) in Ranomafana National Park, Madagascar are known to eat bamboo food parts that contain cyanide. How these lemurs avoid cyanide poisoning remains unknown. In this study, we tested for the presence/absence of cyanide in bamboo lemur foods and excreta to (1) document patterns of cyanide consumption among species with respect to diet, (2) identify routes of elimination of cyanide from the gastrointestinal tract, and (3) determine whether cyanide is absorbed from the diet. We tested 102 food, urine, and fecal samples for hydrogen cyanide (HCN) during two “pre‐dry” seasons (April 2006, May 2007) using commercially available Cyantesmo test strips. The test strips changed color in the presence of HCN, and we recorded color change on a scale of 0 (no change) to 5 (cobalt) at preset intervals with a final score taken at 24 hr. We detected cyanide in bamboo food parts and urine of all three Hapalemur species. Time to color change of the test strips ranged from almost instantaneous to >12 hr incubation. Of the foods tested, only bamboo contained cyanide, but results differed among bamboo species and plant parts of the same species. Specifically, branch shoot and culm pith of the giant bamboo produced strong, immediate reactions to the test paper, whereas parts of liana bamboos produced either weak or no color change. Cyanide was present in almost all urine samples but rarely in fecal samples. This suggests that dietary cyanide is absorbed in the gastrointestinal tract of the Hapalemur species and excreted, at least in part, by the kidneys. Samples from H. griseus exhibited lower, though still detectable, cyanide levels compared with H. simus and H. aureus. Differences among lemur species appear to be related to the specific bamboo parts consumed. Am. J. Primatol. 72:56–61, 2010. © 2009 Wiley‐Liss, Inc.     

Organization of white adipose tissue in lemuridae

The gross anatomy of white adipose tissue was studied in seven carcasses representing three lemurid species (Lemur catta, Eulemur fulvus, E. mongoz) to validate in vivo methods of assessing fatness, and to contribute to a comprehensive database on the organization of adipose tissue in Mammalia. During the years preceding their deaths, subjects had been either caged or semi-provisioned under semi-captive conditions, and their body masses had been recorded several times annually. All specimens were as fat or fatter than anthropoid primates maintained for long periods under comparable conditions. At least eight superficial, four intra-abdominal, and two intermuscular adipose depots were described, all of which were comparable to those described previously for macaques and humans. All typical mammalian depots were present. Many superficial depots adhered tightly to the skin and/or underlying muscles. The superficial “paunch” depot on the outer ventral wall of the abdomen, characteristic of anthropoid primates, was found in all specimens. The existence of this depot in lemurs suggests that it evolved early in Primates. As in monkeys and humans, the paunch was very variable in size, massive in obese specimens but almost absent in moderately lean ones, confirming that extensive accumulation and selective depletion of adipose tissue at this depot is a special feature of Primates. In some obese specimens, adipose tissue on the ventral and lateral thorax and on the inner dorsal wall of the abdomen, extending around the kidneys and into the pelvic canal, was also massive. The investigation allowed for improvement of protocols for external measurement in ongoing research on growth, mass, and fatness in ringtailed and redfronted lemurs. Comparisons of subjects' ranges of body mass change during adult life with masses of adipose tissue found upon dissection suggested that much of lemurs' predictable seasonal change in body mass is due to changes in the mass of white adipose tissue. © 1995 Wiley-Liss, Inc.     

New discoveries of skeletal elements of Hadropithecus stenognathus from Andrahomana Cave, southeastern Madagascar

Remains of what appears to be a single, subadult Hadropithecus stenognathus were recovered from a previously unexcavated site at Andrahomana Cave (southeastern Madagascar). Specimens found comprise isolated teeth and cranial fragments (including the frontal processes of the orbits), as well as a partial postcranial skeleton. They include the first associated fore- and hind-limb bones, confirming the hind-limb attributions made by Godfrey and co-workers in 1997, and refuting earlier attributions by Lamberton in 1937/1938. Of particular interest here are the previously unknown elements, including a sacrum, other vertebrae and ribs, some hand bones, and the distal epiphysis of a femur. We briefly discuss the functional implications of previously unknown elements. Hadropithecus displayed a combination of characters reminiscent of lemurids, others more like those of the larger-bodied Old World monkeys, and still others more like those of African apes. Yet other characteristics appear unique. Lemurid-like postcranial characteristics may be primitive for the Archaeolemuridae. Hadropithecus diverges from the Lemuridae in the direction of Archaeolemur, but more extremely so. Thus, for example, it exhibits a stronger reduction in the size of the hamulus of the hamate, greater anteroposterior compression of the femoral shaft, and greater asymmetry of the femoral condyles. Nothing in its postcranial anatomy signals a close relationship to either the Indriidae or the Palaeopropithecidae.