New wrist bones of the Malagasy giant subfossil lemurs

Recently discovered wrist bones of the Malagasy subfossil lemurs Babakotia radofilai, Palaeopropithecus ingens, Mesopropithecus dolichobrachion, and Megaladapis madagascariensis shed new light on the postcranial morphologies and positional behaviors that characterized these extinct primates. Wrist bones of P. ingens resemble those of certain modern hominoids in having a relatively enlarged ulnar head and dorsally extended articular surface on the hamate, features related to a large range of rotation at the inferior radioulnar and midcarpal joints. The scaphoid of P. ingens is also similar to that of the extant tree sloth Choloepus in having an elongate, palmarly directed tubercle forming a deep radial margin of the carpal tunnel for the passage of large digital flexors. In contrast, wrist remains of Megaladapis edwardsi and M. madagascariensis exhibit traits observed in the hands of extant pronograde, arboreal primates; these include a dorsopalmarly expanded pisiform and well-developed "spiral" facet on the hamate. Moreover, Megaladapis spp. and Mesopropithecus dolichobrachion possess bony tubercles (e.g., scaphoid tubercle and hamate hamulus) forming the carpal tunnel that are relatively similar in length to those of modern pronograde lemurs. Babakotia and Mesopropithecus differ from Megaladapis in exhibiting features of the midcarpal joint related to frequent supination and radioulnar deviation of the hand characteristic of animals that use vertical and quadrumanous climbing in their foraging behaviors. Comparative analysis of subfossil lemur wrist morphology complements and expands upon prior inferences based on other regions of the postcranial skeleton, and suggests a considerable degree of locomotor and postural heterogeneity among these recently extinct primates.     

Morphometric analysis of lumbar vertebrae in extinct Malagasy strepsirrhines

Previous research on subfossil lemurs has revealed much about the positional behavior of these extinct strepsirrhines, but a thorough quantitative analysis of their vertebral form and function has not been performed. In this study, 156 lumbar vertebrae of Pachylemur, Archaeolemur, Megaladapis, Mesopropithecus, Babakotia, and Palaeopropithecus (11 species in all) were compared to those of 26 species of extant strepsirrhines and haplorhines. Lumbar shape was compared among species, using a principal components analysis (PCA) in conjunction with selected vertebral indices. The first principal component revealed strong separation between Palaeopropithecus at one extreme, and Archaeolemur/Pachylemur at the other, with Babakotia, Mesopropithecus, and Megaladapis in an intermediate position. Palaeopropithecus has markedly shorter spinous processes and wider laminae than do the other subfossil taxa, consistent with sloth-like, inverted suspensory postures. The moderately reduced lumbar spinous processes of Babakotia, Mesopropithecus, and Megaladapis are convergent with those of lorisids and Pongo, reflecting antipronogrady, but a less specialized adaptation than that of Palaeopropithecus. Archaeolemur and Pachylemur share relatively elongated spinous processes, in conjunction with other features (e.g., transverse process orientation and relatively short vertebral bodies) indicative of pronograde, quadrupedal locomotion characterized by reduced agility. All subfossil taxa exhibit adaptations emphasizing lumbar spinal stability (e.g., relatively short vertebral bodies, and transverse processes that are not oriented ventrally); we believe this probably reflects convergent mechanical demands connected to large body size, irrespective of specific locomotor mode. Reconstructions of positional behavior in subfossil lemurs based on lumbar vertebrae are largely consistent with those based on other aspects of the postcrania.     

Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.     

Dental topography indicates ecological contraction of lemur communities

Understanding the paleoecology of extinct subfossil lemurs requires reconstruction of dietary preferences. Tooth morphology is strongly correlated with diet in living primates and is appropriate for inferring dietary ecology. Recently, dental topographic analysis has shown great promise in reconstructing diet from molar tooth form. Compared with traditionally used shearing metrics, dental topography is better suited for the extraordinary diversity of tooth form among subfossil lemurs and has been shown to be less sensitive to phylogenetic sources of shape variation. Specifically, we computed orientation patch counts rotated (OPCR) and Dirichlet normal energy (DNE) of molar teeth belonging to 14 species of subfossil lemurs and compared these values to those of an extant lemur sample. The two metrics succeeded in separating species in a manner that provides insights into both food processing and diet. We used them to examine the changes in lemur community ecology in Southern and Southwestern Madagascar that accompanied the extinction of giant lemurs. We show that the poverty of Madagascar's frugivore community is a long-standing phenomenon and that extinction of large-bodied lemurs in the South and Southwest resulted not merely in a loss of guild elements but also, most likely, in changes in the ecology of extant lemurs.     

Can low-magnification stereomicroscopy reveal diet?

A new method of scoring dental microscopic use wear, initially developed for and applied to extant and extinct ungulates, is here applied to primates, and the efficacy of the method as a tool for diagnosing diet in both ungulates and primates is established. The method employs standard refractive light microscopy instead of scanning electron microscopy (SEM), and all use-wear features are counted or scored under low magnification (35 x). We use measurement systems analysis (variance components analysis of sources of measurement error) to evaluate the consistency and reproducibility of measurements using this method. The method is shown to have low intra- and inter-observer measurement error, and to effectively distinguish among graminivores, folivores, and frugivores. It can also be used to identify seed predators and to diagnose hard-object feeding. The method is also shown to be robust to the selection of measurement site; it works equally well when applied to upper or to lower molars. Finally, we use analysis of variance to examine the consistency of the signals across mammalian orders, and discriminant function analysis to develop dietary diagnostic tools for a set of "classified" primates with known diets. We test the success of these tools not merely by examining their a posteriori classification "success," but by using them to construct predicted dietary profiles for a sample of unclassified extant primate species, again with known diets.     

Dental development in Megaladapis edwardsi (Primates, Lemuriformes): implications for understanding life history variation in subfossil lemurs

Teeth grow incrementally and preserve within them a record of that incremental growth in the form of microscopic growth lines. Studying dental development in extinct and extant primates, and its relationship to adult brain and body size as well as other life history and ecological parameters (e.g., diet, somatic growth rates, gestation length, age at weaning), holds the potential to yield unparalleled insights into the life history profiles of fossil primates. Here, we address the absolute pace of dental development in Megaladapis edwardsi, a giant extinct lemur of Madagascar. By examining the microstructure of the first and developing second molars in a juvenile individual, we establish a chronology of molar crown development for this specimen (M1 CFT = 1.04 years; M2 CFT = 1.42 years) and determine its age at death (1.39 years). Microstructural data on prenatal M1 crown formation time allow us to calculate a minimum gestation length of 0.54 years for this species. Postnatal crown and root formation data allow us to estimate its age at M1 emergence (approximately 0.9 years) and to establish a minimum age for M2 emergence (>1.39 years). Finally, using reconstructions or estimates (drawn elsewhere) of adult body mass, brain size, and diet in Megaladapis, as well as the eruption sequence of its permanent teeth, we explore the efficacy of these variables in predicting the absolute pace of dental development in this fossil species. We test competing explanations of variation in crown formation timing across the order Primates. Brain size is the best single predictor of crown formation time in primates, but other variables help to explain the variation.     

Reconstructing the Diet of an Extinct Hominin Taxon: The Role of Extant Primate Models

Modern humans represent the only surviving species of an otherwise extinct clade of primates, the hominins. As the closest living relatives to extinct hominins, extant primates are an important source of comparative information for the reconstruction of the diets of extinct hominins. Methods such as comparative and functional morphology, finite element analysis, dental wear, dental topographic analysis, and stable isotope biogeochemistry must be validated and tested within extant populations before they can be applied to extinct taxa. Here we review how these methods have and might be used to reconstruct the diet of a particular extinct hominin, Paranthropus boisei, which has no extant analogue for its highly derived masticatory morphology. Our review emphasizes the potential and limitations of using extant primates as models for the reconstruction of extinct hominin diets. We encourage paleoanthropologists and those who study the feeding behaviors of extant primates to work together to investigate and validate methods for interpreting the diets of all extinct primates, including hominins.     

DNA from extinct giant lemurs links archaeolemurids to extant indriids

Background  

Although today 15% of living primates are endemic to Madagascar, their diversity was even greater in the recent past since dozens of extinct species have been recovered from Holocene excavation sites. Among them were the so-called "giant lemurs" some of which weighed up to 160 kg. Although extensively studied, the phylogenetic relationships between extinct and extant lemurs are still difficult to decipher, mainly due to morphological specializations that reflect ecology more than phylogeny, resulting in rampant homoplasy.     

The functional significance of skeletal allometry in Megaladapis in comparison to living prosimians

Slow vertical climbing and clinging are the dominant positional behaviors of the most convincing reconstruction of the primary spatial niche of Megaladapis, a giant extinct prosimian from Madagascar. The vertical support model of Cartmill ('74) predicts that clawless mammals should exhibit relatively elongated forelimbs in expanded size ranges. The allometric corollaries of this model are tested on closely related interspecific samples of Megaladapis and selected extant prosimians. Megaladapis and indriids (vertical leapers and clingers) conform to the structural predictions of the model, and are clearly distinguished from the more pronograde lemurids and cheirogaleids. Extreme hindlimb reduction (negative allometry) is coupled with moderate forelimb elongation (positive allometry) in Megaladapis. These body proportions effectively optimize pedal friction during vertical climbing and minimize the moment of body weight pulling the animal away from the trunk. Positive forelimb allometry occurs in the indriids, while isometry obtains for the hindlimb. The adaptive significance of these morphological strategies are discussed, as are possible selective mechanisms which effect the extreme hindlimb reduction in Megaladapis. Body weight estimates are also presented for Megaladapis edwardsi and Megaladapis grandidieri (50–100 kg and 40–75 kg, respectively).     

Limb joint surface areas and their ratios in Malagasy lemurs and other mammals

Surface areas of humeral and femoral heads scale largely as a function of body size. However, differences in the relative sizes of these articular surfaces are correlated with differential joint mobility and force transmission through fore- and hindlimbs. They can therefore assist interpretation of the positional behavior of extinct species. In this paper, we document variation in ratios of humeral head surface area to femoral head surface area among extant primates and other mammals. We then examine a group of extinct primates: the subfossil lemurs of Madagascar. Many Malagasy le murs, including some giant extinct species with very long forelimbs and short hindlimbs, have relatively small humeral heads and large femoral heads. We explore the adaptive implications of this pattern. © 1995 Wiley-Liss, Inc.     

Molar microwear of subfossil lemurs: improving the resolution of dietary inferences

In this study we use molar microwear analyses to examine the trophic distinctions among various taxa of Malagasy subfossil lemurs. High resolution casts of the teeth of Megaladapis, Archaeolemur, Palaeopropithecus, Babakotia, and Hadropithecus were examined under a scanning electron microscope. Megaladapis was undoubtedly a browsing folivore, but there are significant differences between species of this genus. However, dietary specialists appear to be the exception; for example, Palaeopropithecus and Babakotia probably supplemented their leaf-eating with substantial amounts of seed-predation, much like modern indrids. Hadropithecus was decidedly not like the modern gelada baboon, but probably did feed on hard objects. Evidence from microwear and coprolites suggests that Archaeolemur probably had an eclectic diet that differed regionally and perhaps seasonally. Substantial trophic diversity within Madgascar's primate community was diminished by the late Quaternary extinctions of the large-bodied species (>9 kg).     

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.     

A chronology for late prehistoric Madagascar

A database has been assembled with 278 age determinations for Madagascar. Materials 14C dated include pretreated sediments and plant macrofossils from cores and excavations throughout the island, and bones, teeth, or eggshells of most of the extinct megafaunal taxa, including the giant lemurs, hippopotami, and ratites. Additional measurements come from uranium-series dates on speleothems and thermoluminescence dating of pottery. Changes documented include late Pleistocene climatic events and, in the late Holocene, the apparently human-caused transformation of the environment. Multiple lines of evidence point to the earliest human presence at ca. 2300 14C yr BP (350 cal yr BC). A decline in megafauna, inferred from a drastic decrease in spores of the coprophilous fungus Sporormiella spp. in sediments at 1720+/-40 14C yr BP (230-410 cal yr AD), is followed by large increases in charcoal particles in sediment cores, beginning in the SW part of the island, and spreading to other coasts and the interior over the next millennium. The record of human occupation is initially sparse, but shows large human populations throughout the island by the beginning of the Second Millennium AD. Dating of the "subfossil" megafauna, including pygmy hippos, elephant birds, giant tortoises, and large lemurs, demonstrates that most if not all the extinct taxa were still present on the island when humans arrived. Many taxa overlapped chronologically with humans for a millennium or more. The extinct lemurs Hadropithecus stenognathus, Pachylemur insignis, Mesopropithecus pithecoides, and Daubentonia robusta, and the elephant birds Aepyornis spp. and Mullerornis spp., were still present near the end of the First Millennium AD. Palaeopropithecus ingens, Megaladapis edwardsi, and Archaeolemur sp. (cf. edwardsi) may have survived until the middle of the Second Millennium A.D. One specimen of Hippopotamus of unknown provenance dates to the period of European colonization.     

The extinct sloth lemurs of Madagascar

Paleontological expeditions to Madagascar over the past two decades have yielded large quantities of bones of extinct lemurs. These include abundant postcranial and cranial remains of new species belonging to a group of giant extinct lemurs that we have called sloth lemurs due to their remarkable postcranial convergence with arboreal sloths. New fossils have come from a variety of locations in Madagascar, including caves in the Northwest (Anjohibe) and the Ankarana Massif, located in the extreme north, as well as pits in the karstic plains near Toliara in southwestern Madagascar. The most spectacular of these is the extremely deep pit (>100 m) called Ankilitelo, the “place of the three kily trees.” These new materials provide insights into the adaptive diversity and evolution of sloth lemurs. New carpal and pedal bones, as well as vertebrae and other portions of the axial skeletons, allow better reconstruction of the positional behavior of these animals. New analytical tools have begun to unlock the secrets of life‐history adaptations of the Palaeopropithecidae, making explicit exactly what they had in common with their relatives, the Indriidae. Paleoecological research has elucidated the contexts in which they lived and the likely causes of their disappearance.     

Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo, southwestern Madagascar

Variation in body size is well documented for both extant and extinct Malagasy primates, and appears to be correlated with geographic patterns of resource seasonality. Less attention has been paid to extant lemurs in subfossil collections, although it has been suggested that subfossil forms of extant species are characterized by greater size than their modern counterpart. This trend of phyletic size change has been related to climate change, habitat fragmentation, or human hunting. However, space- and time-averaging in the subfossil samples of previous studies may have obscured more general ecogeographic patterns underlying these size differences. Our objective is to examine size variation in subfossil still-extant primates within a regional comparative context to determine if subfossil and living forms conform to similar ecogeographic patterns. We report on the subfossil still-extant primate assemblage from Ankilitelo, southwestern Madagascar (approximately 500 yr BP) to test this hypothesis. The Ankilitelo primates were compared with museum specimens of known locality. Extant taxa were assigned to one of five distinct ecogeographic regions, including spiny thicket, dry deciduous forest, succulent woodland, lowland and subhumid rainforest. Comparisons of tooth size in extant lemurs reveal significant geographical patterns of variation within genera. In general, the primates from Ankilitelo are indeed larger than their modern counterpart. However, these differences fit an ecoregional model of size variation, whereby Ankilitelo species are comparable in size to living forms inhabiting ecoregions present near the cave today. This suggests that Malagasy primates have been subjected to similar patterns of resource seasonality for at least 500 years.     

Antipredator behavior in lemurs: Evidence of an extinct eagle on Madagascar or something else?

Goodman (1994) related the antipredator response exhibited by two species of lemurs from southwestern Madagascar against extant birds of prey to the predatory efforts of an extinct eagle, inhabiting the same region about 4000 years ago. He argued that today’s smaller raptors, hunting young individuals perhaps only occasionally, represent marginal danger to lemurs. Nevertheless,their activity would be sufficient to impose a continuous reinforcement to a strong antipredator response. I question such an interpretation and instead suggest that extant birds of prey may indeed represent a strong threat to lemurs and that the same might not have been necessarily true for the extinct eagle. In addition, I propose four optional hypotheses, all of which encompass a marginal role for the extinct eagle.     

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.     

Dental wear among cercopithecid monkeys of the Taï forest,Côte d'Ivoire

Studies of dental macrowear can be useful for understanding masticatory and ingestive behavior, life history, and for inferring dietary information from the skeletal material of extinct and extant primates. Such studies to date have tended to focus on one or two teeth, potentially missing information that can be garnered through examination of wear patterns across the tooth row. Our study measured macrowear in the postcanine teeth of three sympatric cercopithecid species from the Taï Forest, Côte d'Ivoire (Cercocebus atys, Procolobus badius, and Colobus polykomos), whose diets have been well‐described. Inter‐specific analyses suggest that different diets and ingestive behaviors are characterized by different patterns of wear across the molar row, with Cercocebus atys emphasizing tooth use near P₄‐M₁, P. badius emphasizing a large amount of tooth use near M₂‐M₃, and Colobus polykomos exhibiting wear more evenly across the postcanine teeth. Information regarding differential tooth use across the molar row may be more informative than macrowear analysis of isolated teeth for making inferences about primate feeding behavior. Am J Phys Anthropol 150:655–665, 2013. © 2013 Wiley Periodicals, 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.