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.     

The enigma of antipredator behavior in lemurs: Evidence of a large extinct eagle on Madagascar

Numerous zoologists who study diurnal lemurs on Madagascar have noted that they react strongly to the presence of birds of prey. For two of the most intensively studied lemurs, Propithecus verreauxiand Lemur catta,there are few documented cases of raptor predation. Thus, the maintenance of this stereotypic response is enigmatic. Bird bones recovered from cave surface deposits in southwestern Madagascar include the remains of an eagle (Aquila),a genus that has disappeared from Madagascar and that would have been capable of hunting animals the size of adult P. verreauxi and L. catta.The stereotypic response of these two lemurs toward raptors may have been retained from the period when this extinct eagle inhabited the island and is reinforced by rare acts of predation by extant birds of prey.     

Evidence of early butchery of giant lemurs in Madagascar

We report here definitive evidence of butchery, most probably associated with hunting, of giant extinct lemurs by early human settlers in Madagascar. Specimens of Palaeopropithecus ingens and Pachylemur insignis from two sites in southwestern Madagascar, Taolambiby and Tsirave, show classic signs of butchering. We compared these to the bones (also from Taolambiby) of butchered Propithecus verreauxi, a lemur still living in the region. The characteristics of the tool-induced extinct-lemur bone alterations (sharp cuts and chop marks near joints, oblique cuts along the shafts, spiral fractures, and percussion striae) suggest skinning, disarticulation, and filleting. Conclusive evidence of megafaunal modification by humans in Madagascar was limited previously to a few hippo and elephant bird bones and one extinct aye-aye tooth. New evidence comes not from archaeological sites, but from specimens collected in the early 1900s, without stratigraphic records, at "subfossil" sites (i.e., sites renowned for their late Pleistocene or Holocene fossils, often lacking human artifacts). Whereas these are hardly the most ideal samples for analysis of this kind, careful scrutiny of the characteristics of the cut marks has allowed us to document butchery beyond any reasonable doubt. One bone with definitive cut marks has been dated to the very earliest part of the human period in Madagascar. Continued, careful research on the bones in subfossil collections is warranted.     

The secrets of lemur teeth

New tools are available for teasing out aspects of life‐history variation among extinct species. Here we summarize research on the life histories of the extinct lemurs of Madagascar. There is a wide range of variation in dental developmental timing among these species, from among the most accelerated (Palaeopropithecus) to among the most prolonged (Hadropithecus) within the Order Primates. Rather than reflecting variation in body size, this diversity appears to relate to niche characteristics and encephalization.     

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.     

Motivations for the Ownership of Captive Lemurs in Madagascar

The live capture of primates is occurring throughout the tropics and can be a threat to their conservation. Primates are owned as pets for a variety of reasons. Studies of the motivations for primate ownership have been conducted in several countries where they are endemic, but no study has examined this issue in Madagascar. Madagascar is home to the highest number of threatened primate taxa in any one country, and an estimated 28,000 lemurs were kept in illegal captivity from 2010 to mid-2013. We aimed to expand knowledge about the motivations of lemur ownership in Madagascar. Data were collected via a web-based survey (n = 229 respondents) and from the websites and social media pages of 25 hotels. We found that many lemurs (45%) were seen on the premises of a business or in a private home (27%). Many lemurs were perceived to be kept as personal pets (37%) or for money-making or tourism purposes (20%). When lemurs were used for money-making, owners could receive indirect (72% of the time) and direct benefits (28%). Hotels showing photographs of captive lemurs on their websites and social media sites charged USD 25.69 more per night for a standard room than hotels that did not show such photographs. We found little evidence that captive lemurs are kept as a social status symbol, for captive breeding, or as a fallback food. These findings provide evidence that the motivations for the ownership of, usually illegal, captive lemurs is typically linked with money-making or with the desire to have a lemur as a pet. These data can help target new outreach programs.     

Extinction and ecological retreat in a community of primates

The lemurs of Madagascar represent a prodigious adaptive radiation. At least 17 species ranging from 11 to 160 kg have become extinct during the past 2000 years. The effect of this loss on contemporary lemurs is unknown. The concept of competitive release favours the expansion of living species into vacant niches. Alternatively, factors that triggered the extinction of some species could have also reduced community-wide niche breadth. Here, we use radiocarbon and stable isotope data to examine temporal shifts in the niches of extant lemur species following the extinction of eight large-bodied species. We focus on southwestern Madagascar and report profound isotopic shifts, both from the time when now-extinct lemurs abounded and from the time immediately following their decline to the present. Unexpectedly, the past environments exploited by lemurs were drier than the protected (albeit often degraded) riparian habitats assumed to be ideal for lemurs today. Neither competitive release nor niche contraction can explain these observed trends. We develop an alternative hypothesis: ecological retreat, which suggests that factors surrounding extinction may force surviving species into marginal or previously unfilled niches.     

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 semicircular canal system and locomotion: The case of extinct lemuroids and lorisoids

Paleontologists reconstruct the locomotor and postural behavior of extinct species by analogy with living forms and biomechanical analyses. In rare cases, behavioral evidence such as footprints can be used to confirm fossil‐based reconstructions for predominantly terrestrial orders of mammals. For instance, the chalicothere prints from Laetoli show that these perissodactyls supported their body weight on the metacarpals, as previously reconstructed. 1 Unfortunately, primates are mostly arboreal and rarely leave footprints. The cercopithecid and hominin prints at Laetoli are a rare exception. We have recently shown that the semicircular canal system can be used to test and augment locomotor reconstructions based on postcranial material or to provide first estimations of locomotor behavior for taxa not known from the postcranium. Using a sample of modern primates, we have been able to demonstrate that the radii of curvature of the semicircular canals are significantly correlated with both body mass and agility of locomotion. 2 This paper reviews those results and examines the relationship between semicircular canal morphology and other evidence in efforts to reconstruct locomotor behavior in subfossil lemurs from the Holocene of Madagascar and fossil lorisoids from the Miocene of Africa.     

Origins,Diversity and Relationships of Lemurs

I review new evidence on origins and adaptive radiation of Malagasy lemurs, a remarkably diverse group containing 13% of living primate species. The number of recognized lemur species has increased significantly, partly due to research revealing specific subdivisions within known populations but mainly because of discovery of new populations through fieldwork. Some species feared to be extinct have also been rediscovered. Specific numbers have increased particularly in small-bodied, cryptic genera for which continued research will surely reveal even more species.Adaptative radiation of lemurs has been essentially confined to Madagascar. The high density of lemur species on that island, associated with very small geographical ranges, has major implications both for their evolutionary divergence and for conservation. Reconstructions of phylogenetic relationships among primates have been considerably enhanced by DNA sequence data. Sufficient data are now available from both nuclear and mitochondrial sequences to examine relationships among and within the major groups of living primates. Most studies have confirmed that lemurs constitute a monophyletic sister-group of the lorisiform clade and all exclude a specific relationship between cheirogaleids and lorisiforms repeatedly inferred from morphological evidence. However, some analyses indicate that the aye-aye may have branched away before the divergence between other lemurs and lorisiforms. DNA sequence analyses have also yielded a broad consensus for relationships between Eulemur, Hapalemur, Lemur and Varecia: Varecia branched away first, while Lemur is more closely related to Hapalemur than to Eulemur. As debate about phylogenetic relationships among lemurs and other primates seems to have been settled in favor of lemur monophyly (possibly excluding the aye-aye), only a single invasion of Madagascar is required; but it must still be explained how ancestral lemurs could have migrated there at an appropriate time. Separation between Madagascar and Africa was apparently complete by about 120 Ma, too far in the past for direct overland migration. A recent hypothesis suggested that uplifted land in the Mozambique Channel assisted colonization of Madagascar 26-45 Ma, seemingly agreeing with an estimated date of about 40 Ma for divergence of lemurs from other primates. However, mounting evidence suggests that divergence occurred significantly earlier. Because the earliest known fossil representatives of several modern orders of placental mammals (including primates) are dated no earlier than the early Tertiary, it is widely accepted that their divergence took place after the Cretaceous/Tertiary mass extinction. Yet the known fossil record can only yield minimum divergence times; if sampling is poor and/or biased there may be a considerable discrepancy between minimum and actual dates. There is, for example, virtually no known fossil record for lemurs in Madagascar and the earliest known representatives are subfossil lemurs, so in this case a direct reading of the fossil record would indicate that the lemurs first originated just a few thousand years ago! Examination of underestimation of times of origin because of poor sampling in the fossil record has confirmed previous suggestions that primates originated considerably earlier than generally believed. Several recent phylogenetic reconstructions based on DNA sequence data and using calibration dates derived from groups other than primates provide independent support for this inference. Overall, it now seems that primates originated at around 90 Ma rather than the 55 Ma indicated by direct reading of the known fossil record. Hence, colonization of Madagascar by lemurs would have taken place at about 80 Ma, double the date usually accepted, and should be interpreted in terms of contemporary continental relationships.     

A new species ofMesopropithecus (Primates,Palaeopropithecidae) from Northern Madagascar

We diagnose new subfossil specimens belonging to the extinct palaeopropithecid, Mesopropithecus,from several caves at the Ankarana massif in northern Madagascar. They include three partial crania with mandibles, and the first vertebrae, ribs, clavicle, pelvis, ulna, and hand and foot bones of Mesopropithecusever found. Several other postcranial elements are known for this northern variant of Mesopropithecusand for previously described species from central and southern Madagascar. The new materials cannot be accommodated in either currently recognized species of this genus and are,hereby, given the name Mesopropithecus dolichobrachion. M. dolichobrachionis the second new species of extinct subfossil lemur to be found in the caves of Ankarana. It is unlike the two previously described species of this genus primarily in its larger size, different limb proportions, and aspects of its long bone morphology. Most notable is the fact that this is the only species of Mesopropithecuswith the forelimb longer than the hind limb— hence the name, the “long-armed” Mesopropithecus.Various characteristics place M. dolichobrachionphenetically closest (of species belonging to Mesopropithecus)to Babakotia radofilai, Archaeoindris,and Palaeopropithecus.If these similarities are derived specializations rather than primitive for palaeopropithecids, a new generic name will be required.     

Talar morphology of azibiids, strepsirhine-related primates from the Eocene of Algeria: phylogenetic affinities and locomotor adaptation

The HGL-50 locality, situated on the Glib Zegdou outlier in the Gour Lazib of Algeria (Hammada du Dra), is famous for having yielded several dental remains of primates dating from the late Early to the early Middle Eocene. These primates include Algeripithecus minutus, Azibius trerki and a new species of cf. Azibius (not described yet). Algeripithecus was widely acknowledged to be one of the oldest known anthropoids from Africa. However, very recent discoveries strongly suggest that Algeripithecus is closely related to Azibius and that both taxa are phylogenetically remote from the clade Anthropoidea. Algeripithecus and Azibius make up the family Azibiidae and appear as stem strepsirhines. Here we describe and analyse two ankle bones (tali) found in HGL-50. UM/HGL50-466 is a small left talus, which is appropriate in size to belong to A. trerki, while UM/HGL50-467 is a right talus, which is significantly larger and appropriate in size to belong to the new large species of cf. Azibius. Both tali exhibit a suite of features that resemble conditions primarily found in extinct and extant strepsirhine and adapiform primates; conditions that are consistent with the strepsirhine-like dentition characterizing azibiids. Functionally, these two tali indicate that Azibius species were engaged in a form of active arboreal quadrupedalism with some ability to climb and leap. Azibiids were rather small-bodied primates, approximating the size of some modern dwarf lemurs (Cheirogaleidae) and sportive lemurs (Lepilemuridae) from Madagascar. Given their small body-size and their talar morphology, living cheirogaleid lemurs, which are agile arboreal quadrupeds (with climbing, springing and branch running activities), might appear as good analogues for azibiids in terms of locomotor behaviour.     

Locomotor behaviour in Plio-Pleistocene sabre-tooth cats: a biomechanical analysis

The locomotor behaviour of some large extinct carnivores, including several species of Plio-Pleistocene sabre-tooth cats, is here reconstructed, based on a comparison of the cross-sectional geometric properties and linear dimensions of their femora and humeri with those of large modern carnivores. The long bones are modelled as simple beams, thereby allowing the use of basic beam theory in assessing relevant functional parameters such as second moments of area of the diaphyses when subjected to compressive and bending stresses. Three Pleistocene carnivores, Smilodon fatalis, Homotherium serum , and Panthera atrox seem to have had ecological and functional equivalents among the late Miocene-Early Pliocene genera, Barbourofelis, Machairodus , and Nimravides , respectively. Barbourofelis and Smilodon were 'cat-like'in dental morphology but some structural characteristics of their limb bones had 'bear-like'affinities. Machairodus and Homotherium were cursorial, whereas Nimravides and P. atrox display the limb morphology of true ambush predators. Various aspects of the postcranial skeleton of some of these extinct carnivores suggest that they may have employed locomotory gaits that lack modern analogs.     

Computed tomography and biomechanical analysis of fossil long bones.

Computerized transverse axial scanning (computed tomography) is a relatively new radiographic technique designed to recover precise cross-sectional images (tomograms) of 3-dimensional objects. This highly sensitive process permits tissues of similar density to be separated and displayed unambiguously. These special features are, therefore, ideal for analyzing the cross-sectional geometry of intact fossil long bones, even when they are highly mineralized and their medullary cavities are occluded by matrix. In order to demonstrate the utility of this method in assessing the complex relationship between fossil structure and probable function, geometrical and biomechanical properties of midshaft tomograms of femora and tibiae have been analyzed for a comparative primate sample consisting of Megaladapis edwardsi (an extinct giant prosimian from Madagascar), Indri indri (the largest extant prosimian), and Homo sapiens.     

A new species of Mesopropithecus (Primates, Palaeopropithecidae) from Northern Madagascar

We diagnose new subfossil specimens belonging to the extinct palaeopropithecid, Mesopropithecus,from several caves at the Ankarana massif in northern Madagascar. They include three partial crania with mandibles, and the first vertebrae, ribs, clavicle, pelvis, ulna, and hand and foot bones of Mesopropithecusever found. Several other postcranial elements are known for this northern variant of Mesopropithecusand for previously described species from central and southern Madagascar. The new materials cannot be accommodated in either currently recognized species of this genus and are,hereby, given the name Mesopropithecus dolichobrachion. M. dolichobrachionis the second new species of extinct subfossil lemur to be found in the caves of Ankarana. It is unlike the two previously described species of this genus primarily in its larger size, different limb proportions, and aspects of its long bone morphology. Most notable is the fact that this is the only species of Mesopropithecuswith the forelimb longer than the hind limb— hence the name, the “long-armed” Mesopropithecus.Various characteristics place M. dolichobrachionphenetically closest (of species belonging to Mesopropithecus)to Babakotia radofilai, Archaeoindris,and Palaeopropithecus.If these similarities are derived specializations rather than primitive for palaeopropithecids, a new generic name will be required.     

Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs

Following human arrival, Madagascar suffered well-documented megafaunal extinctions and widespread deforestation. Although humans are widely considered to be the primary cause of the extinctions, the relative contributions of climate change and human activities to this ecological transformation remain uncertain. Reconstructing the habitats of the giant lemurs of Madagascar can provide key information for understanding the evolutionary mechanisms involved in their extinction. In this study, I present a faunal analysis of the subfossil assemblage from Ankilitelo Cave, southwestern Madagascar. This assemblage documents the latest known occurrence of five species of extinct giant lemur, in association with abundant well-preserved small mammal remains. I compared the small mammal fauna at Ankilitelo with 27 extant Malagasy mammal communities spanning the range of Madagascar's habitat types. Similarities in species composition between modern communities and Ankilitelo were assessed using cluster analysis. Ecological similarities were examined by assigning each species to dietary, locomotor, activity pattern, and body size categories. Multiple discriminant analysis was then used to classify Ankilitelo relative to modern habitat types in Madagascar, based on the ecological structure of the subfossil fauna. Results indicate that the habitat surrounding Ankilitelo during the late Holocene was similar to the succulent woodlands of modern southwestern Madagascar. This suggests that approximately 500 yr BP, these semi-arid habitats supported a subfossil lemur community that included the highly-suspensory Palaeopropithecus, and deliberate slow-climber Megaladapis, as well as Archaeolemur, Pachylemur, and Daubentonia robusta. In such environments, these giant lemurs would likely have been highly vulnerable to increasing human pressure in southwestern Madagascar.     

The hands and feet of Archaeolemur: metrical affinities and their functional significance

Recent expeditions to Madagascar have recovered abundant skeletal remains of Archaeolemur, one of the so-called "monkey lemurs" known from Holocene deposits scattered across the island. These new skeletons are sufficiently complete to permit reassembly of entire hands and feet--postcranial elements crucial to drawing inferences about substrate preferences and positional behavior. Univariate and multivariate analysis of intrinsic hand and foot proportions, phalangeal indices, relative pollex and hallux lengths, phalangeal curvature, and distal phalangeal shape reveal a highly derived and unique morphology for an extinct strepsirrhine that diverges dramatically from that of living lemurs and converges in some respects on that of Old World monkeys (e.g., mandrills, but not baboons or geladas). The hands and feet of Archaeolemur are relatively short (extremely so relative to body size); the carpus and tarsus are both "long" relative to total hand and foot lengths, respectively; phalangeal indices of both the hands and feet are low; both pollex and hallux are reduced; the apical tufts of the distal phalanges are very broad; and the proximal phalanges are slightly curved (but more so than in baboons). Overall grasping capabilities may have been compromised to some extent, and dexterous handling of small objects seems improbable. Deliberate and noncursorial quadrupedalism was most likely practiced on both the ground and in the trees. A flexible locomotor repertoire in conjunction with a eurytopic trophic adaptation allowed Archaeolemur to inhabit much of Madagascar and may explain why it was one of the latest surviving subfossil lemurs.