sign in sign up
<<
Home , Aepyornis, Babakotia, Hadropithecus, Lemur, Megaladapis, Mesopropithecus

Evolutionary Anthropology 12:252–263 (2003)

ARTICLES

The Extinct of

LAURIE R. GODFREY AND WILLIAM L. JUNGERS

Paleontological expeditions to Madagascar over the past two decades have deed, Alfred Grandidier,5–7 the West- yielded large quantities of bones of extinct lemurs. These include abundant post- ern scientist credited with discovering cranial and cranial remains of new belonging to a group of giant extinct Ambolisatra, the first site, lemurs that we have called sloth lemurs due to their remarkable postcranial needed only to follow the led of a vil- convergence with arboreal . New have come from a variety of loca- lage headman to a marsh in south- tions in Madagascar, including caves in the Northwest (Anjohibe) and the Ankarana western Madagascar in which, he was Massif, located in the extreme north, as well as pits in the karstic plains near Toliara assured, the bones of the “Song’aomby” in southwestern Madagascar. The most spectacular of these is the extremely deep (literally, the “cow that isn’t a cow,” or pit (Ͼ100 m) called Ankilitelo, the “place of the three kily .” These new pygmy hippopotamus) could be found materials provide insights into the adaptive diversity and evolution of sloth lemurs. (Box 1). Among the bones that Grandi- New carpal and pedal bones, as well as vertebrae and other portions of the axial dier retrieved from that marsh in 1868 skeletons, allow better reconstruction of the positional behavior of these . was the distal of a sloth le- New analytical tools have begun to unlock the secrets of life-history of mur, —perhaps the the Palaeopropithecidae, making explicit exactly what they had in common with first specimen of a giant extinct their relatives, the . Paleoecological research has elucidated the contexts to be examined by a Western scientist. in which they lived and the likely causes of their disappearance. It was not described until decades lat- er,8 and its association with sloth le- mur remained obscure for de- The sloth lemurs, or Palaeopro- in body size of all families of Malagasy cades more. But no longer could there pithecidae, comprise four of the eight lemurs (from under 10 kg to over 200 be any doubt that fabulous mega- recognized genera of extinct lemurs kg) and the most extreme modifica- beasts once thrived in Madagascar. and more than a third of the extinct tion of the hind limb and axial skele- The nomen Palaeopropithecus in- species (Table 1; Figs. 1 and 2). Four ton. The elongation of the gens was allocated to a genera are currently recognized as be- and reduction of the hind limb are all found at another subfossil site in longing in this : Palaeopropithe- the more remarkable because their southwestern Madagascar just before cus (the type ), the truly gigantic closest relatives, the Indriidae, have the turn of the twentieth century.9 The Archaeoindris, the much smaller-bod- some of the longest and mandible was chimp-sized but had si- ied , and the mid- shortest in the Pri- faka-like teeth. Similar and sized, recently discovered . mates. A sister taxon relationship of associated skulls were recovered from This family exhibits the greatest range the Palaeopropithecidae to the - a marsh site, Ampasambazimba, in idae is supported by molecular data1 the interior of the island, and Palaeo- and a host of dental morphological propithecus maximus was named.10 and developmental specializations. Postcranial bones were assigned to Western scientists first learned of Palaeopropithecus, almost always in- Laurie R. Godfrey is Professor of Anthro- the existence of giant on the correctly. pology at the University of Massachusetts at Amherst. [email protected] island of Madagascar in the mid-sev- Other whole or partial crania with William L. Jungers is Professor of Anatom- enteenth century through the writings -like teeth were recovered at ical Sciences at Stony Brook University, New York. [email protected] of French colonial governor Etienne Ampasambazimba in the early 1900s. Both have been working on the evolution, de Flacourt. In addition to providing They ranged dramatically in size: ecomorphology, and of pri- his own descriptions of the biota of Some (Mesopropithecus pithecoides)10 mates in Madagascar for the last three 2 decades. Both have collaborated on pa- Madagascar, Flacourt recorded puta- were barely larger than the crania of leontological expeditions in Madagascar tive Malagasy eyewitness accounts of diademed , while others (Ar- with Elwyn L. Simons at huge and dangerous beasts roaming chaeoindris fontoynontii)11 rivaled the and David Burney at Fordham University. the Great Red Island. In some rural size of crania. The gorilla-sized regions of Madagascar, even today, as Archaeoindris was established on the © 2003 Wiley-Liss, Inc. during the past hundred , stories basis of a mandible and two fragmen- DOI 10.1002/evan.10123 Published online in Wiley InterScience of hornless “water cows” and other tary maxillae. A femur belonging to (www.interscience.wiley.com). large creatures can be heard.3,4 In- Archaeoindris was attributed to an- ARTICLES Sloth Lemurs of Madagascar 253

TABLE 1. of the Sloth Lemurs Palaeopropithecus as an aquatic crea- Family Palaeopropithecidae (Tattersall, 1973) ture, swimming at the water’s surface Genus Palaeopropithecus (G. Grandidier, 1899) with its eyes, ears, and nostrils barely Palaeopropithecus ingens (G. Grandidier, 1899) above water. Such behavior, Standing Palaeopropithecus maximus (Standing, 1903) believed, could explain not merely the [Palaeopropithecus sp. nov.] elevation of the nasals and the upward Genus Archaeoindris (Standing, 1909) Archaeoindris fontoynontii (Standing, 1909) orientation of the axes of the orbits, Genus Babakotia (Godfrey and coworkers, 1990) but also the alignment of the nasal Babakotia radofilai (Godfrey and coworkers, 1990) aperture, orbits, and external auditory Genus Mesopropithecus (Standing, 1905) meatus in a plane perpendicular to Mesopropithecus pithecoides (Standing, 1905) that of the occipital condyles, the Mesopropithecus globiceps (Lamberton, 1936) “elongation” and “flattening” of the Mesopropithecus dolichobrachion (Simons and coworkers, 1995) , the narrowing of the postorbital region, the flattening of the bullae, other lemur species, Lemuridother- nial and postcranial features. On the and the placement of the lacrimal ium.12 The only known cranium and basis of its cranium, paleontologist inside the orbital rim (Fig. 3). possibly associated mandible of Ar- Herbert F. Standing25 reconstructed Standing25 believed that the postcra- chaeoindris were discovered much later at Ampasambazimba.13 In the 1930s, Charles Lamberton launched a series of paleontological expeditions (mainly in the Southwest) that were to add to the list of recog- nized species of extinct lemurs. In 1936 he described, at first under an- other genus name, additional crania belonging to Mesopropithecus.14,15 In 1938, Decary16 recovered specimens belonging to a new species of Palaeo- propithecus at Anjohibe, but the uniqueness of these specimens was not recognized at the time. In 1965, Mahe´17 found additional specimens of the same species at Amparihingidro in the Northwest. Yet more species of sloth lemurs were discovered in the late twentieth century. Beginning in the early 1980s, Elwyn Simons18–20 launched a series of expeditions to central, northwestern, northern, and southwestern Madagascar. Among the more spectacular discoveries of Si- mons and his team were those of a nearly complete skeleton of the new species of Palaeopropithecus from the northwest21,22; a new genus and spe- cies of giant lemur, Babakotia rado- filai, from the north and northwest23; and a new species of Mesopropithecus (M. dolichobrachion) from the ex- treme north.24

BEHAVIORAL RECONSTRUCTION OF THE SLOTH LEMURS Early reconstructions of the life ways of Palaeopropithecus and other giant lemurs were confounded by postcranial misattributions as well as Figure 1. Map of Madagascar, showing the known geographic distributions of sloth lemur fanciful interpretations of both cra- species, and highlighting selected subfossil sites. 254 Godfrey and Jungers ARTICLES

imba for those of Mesopropithecus pithecoides and somehow took these to imply likenesses. Refer- ences to Archaeoindris as being simi- lar to in its locomotor be- havior were also based, at least in part, on attributional errors.31 Inter- pretations of the locomotion of Ar- chaeoindris were hampered as well by a dearth of specimens. Only six post- crania belonging to Archaeoindris have ever been found: a damaged hu- merus, the “Lemuridotherium” femur, and four shafts of the long bones of an immature individual. Postcrania of Mesopropithecus are better repre-

In addition to providing his own descriptions of the biota of Madagascar, Flacourt Figure 2. Working cladogram for the Indriidae and the Palaeopropithecidae. The Palaeo- propithecidae share a host of postcranial characteristics that bear testimony to their slow recorded putative climbing and suspensory habits (see text). They can also be distinguished craniodentally from the Indriidae, their closest relatives, by the increased lateral flare and greater robus- Malagasy eyewitness ticity of the zygoma, stronger postorbital constriction, more robust , more accounts of huge and convergent and often confluent temporal lines, with the frequent development of sagittal and nuchal crests, even in the smallest taxa. The orbits are relatively smaller than in the dangerous beasts Indriidae, but, as in all lemurs and , there is no postorbital closure. Palaeopropithecus and Archaeoindris share a suite of peculiar, derived traits craniodental specializations roaming the Great Red (described in the caption to Figure 3). Island. In some rural regions of Madagascar, nia of Palaeopropithecus provided inde- in 1935 with a confused assemblage even today, as during pendent evidence of swimming adapta- that included a humerus and of the past hundred years, tions. Unfortunately, the postcranial Megaladapis, a fibula of Megaladapis bones that he brought to bear on his misidentified as a clavicle, and the as- stories of hornless “water argument did not even belong to trago-navicular of a , Sera28 cows” and other large Palaeopropithecus.26 Actual postcranial reconstructed Palaeopropithecus as an bones of Palaeopropithecus had been as- arboreal-aquatic acrobat with a loco- creatures can be heard. cribed to other taxa, including the long- motor repertoire combining climbing, snouted Megaladapis and a presumed diving, and swimming. In 1938 he gigantic sloth that Alfred Grandidi- broadened his aquatic theory to en- 29 er’s son, Guillaume, called Bradythe- compass other extinct lemurs. Mega- sented in the record, but until 27 rium. In turn, a femur of Hadropithe- ladapis, for example, became a dorso- recently some critical elements, in- cus and forelimb bones of Megaladapis ventrally flattened skate- or ray-like cluding the radius, ulna, vertebrae, were attributed to Palaeopropithecus. swimmer, its underwater conceal- and foot bones, and the , The femur exhibited a ment while feeding on aquatic mol- were unknown. torsion that Standing25 believed might lusks and crustaceans facilitated by The paleontologist who did the facilitate swimming, while the short, the varus orientation of its knee and most to correct early problems of massive Megaladapis humerus seemed rotation of the iliac blade into the attribution and interpretation was an ideal paddle, with its prominent del- frontal plane! Charles Lamberton. Others had begun toid crest and limited capacity for el- Whereas Mesopropithecus and Ar- to tackle the problems of synonymy bow extension.11 chaeoindris were spared such gro- and association,12,30,32 but it was up to Italian paleontologist Guiseppe tesque misrepresentation, neither en- Lamberton33,34 to dispose once and Sera embraced Standing’s aquatic tirely escaped attributional errors. for all of Guillaume Grandidier’s fossil theory of giant sloth lemur locomo- Carleton30 mistook postcrania of Pro- sloth theory and Sera’s theory of tion and carried it further. Beginning pithecus diadema at Ampasambaz- aquatic lemur locomotion. In 1957, ARTICLES Sloth Lemurs of Madagascar 255

Box 1. Early Descriptions, Early Discoveries L.. Godfrey, W.L. Jungers, and E.L. Simons

The first of the extinct lemurs to be on the extinct of Mada- where I sensed a large object, and described by a Western scientist was gascar. Alfred was fascinated by Mal- lifted it. After washing it, I found to my the “tretretretre.” In the seventeenth agasy accounts of fantastic beasts, surprise and joy that it was a femur— century, French naturalist and ex- especially the “Song’aomby,” or the the thighbone of a . The bird must plorer E´ tienne de Flacourt2 described “cow that isn’t a cow,” which some have been enormous, like the famous this creature as living in southeast had interpreted as a ferocious, man- of 1001 Nights. Enthusiastically, I Madagascar. According to Flacourt’s eating donkey.3,4 When, in 1868, a returned to the water and, with some translation of Malagasy accounts, Malagasy village chief showed him a of my men, dug into the mud that this was a large, frightening, and sol- marsh where the bones of the carpeted the floor of the marsh. I re- itary beast with a short and curly coat, Song’aomby could be found, Grandi- trieved more bones of the colossal rounded ear pinnae, flat face, long dier understood that the Song’aomby bird, , known previously digits, and a short tail. While a num- was actually an extinct hippopota- only from its 8-liter eggs and a few ber of authors have suggested that mus. Grandidier’s own fascinating indeterminable pieces sent by Mr. this might describe a Megaladapis, account of the events of that day Abadi and described in 1850 by Isi- such an inference is strongly contra- was published more than 100 years dore Geoffroy Saint-Hilaire. Along- dicted by the extreme elongation of later in his “Souvenirs de voyages side these bird bones were numerous the facial skeleton of all species be- d’Alfred Grandidier.”7 This is a other bones belonging to an unknown longing to that genus. A better match translation from the original French species of hippopotamus that I is provided by the sloth lemur, (p. 13): named Hippopotamus Lemerlei in Palaeopropithecus. Sloth lemurs, like “I had stopped to cook my lunch at honor of our odd-job man at Tule´ ar, living indriids, had faces that were Ambohisatrana [that is, the place as well as bones of other new and considerably shorter than those of where satrana, or dwarf palm tree interesting animals.” Megaladapis. Also, we know from plants grow, later called Ambolisatra, Among the “bones of other new skeletal remains that Palaeopropithe- the satrana plantation] where I was and interesting animals” that Alfred cus had long, curved digits and a ves- visited by the chief of the region, with Grandidier had found was a distal hu- tigial tail (see Box 2). Rounded ear whom I discussed, as was usual for merus of a sloth lemur, Palaeopro- pinnae characterize all of the indriids my conversations with the native pithecus. That humerus was not for- and might well have characterized people, the local industry and animals mally described until 1895, when it their close relatives. (particularly the Song’aomby, a cow- was named Thaumastolemur grandi- Proof of the prior existence of giant like ). Because I asked for infor- dieri.8 Shortly thereafter, it was incor- lemurs and other megafauna in mation regarding the Song’aomby rectly synonymized with Megaladapis Madagascar came in the form of (previously known to me only through madagascariensis.69 It wasn’t until “subfossil” remains (so-called be- a very poor description that Flacourt nine decades later that Thaumastole- cause they are too fresh to be fossil- had provided under the name Man- mur’s taxonomic priority over Palaeo- ized), first reported in the scientific garsahoc), the chief of the region in- propithecus was recognized70 and literature of the Western world in the dicated the location of a nearby then quickly suppressed by the Inter- mid-1800s. Palaeopropithecus was marsh, and informed me that I could national Commission for Zoological quite possibly also the first of the ex- find this animal’s bones there. On that Nomenclature, for lack of use.71 tinct lemurs to be unearthed by a advice, I hurried to the location— “Thaumastolemur” is now judged to Western scientist. That scientist was barefooted and barelegged, with be an invalid generic name for Alfred Grandidier, French geogra- pants cut at the knees, as I am prone Palaeopropithecus (1993; Opinion pher, ethnologist, and father of natu- to do. I entered the marsh, and low- 1737, Bulletin of Zoological Nomen- ralist Guillaume Grandidier, who later ering myself, tapped the bottom clature 50(2):190–191). contributed volumes to the literature

Lamberton35 published a devastating rors for Archaeoindris, however. Asso- had been cleared. Carleton and Lam- rebuttal to Sera,28,29,36 correcting his ciations between postcrania and cra- berton had both forcefully demon- numerous misattributions point by nia of Archaeoindris were not really strated that Palaeopropithecus was sus- point and tactfully marveling at his established until 198831 (but see also pensory. What remained to be debated, unbridled imagination. Lamberton37 Walker38 and Jungers39). was the relative strength of alternative also corrected Carleton’s30 postcranial By the mid-twentieth century, most models of suspensory locomotion for attributions for Mesopropithecus. He of the major attributional problems Palaeopropithecus, largely on the basis failed to correct early attributional er- that had plagued early interpretations of the evidence of new elements of the 256 Godfrey and Jungers ARTICLES

are “vertical clingers and leapers” with elongated and feet, spe- cial adaptations for what has been called “thigh-powered” leaping,47–51 and intermembral indices much lower than those of the Palaeopro- pithecidae. They typically feed in ver- tical sitting or hanging positions. They sometimes use their hindlimbs (or hindlimbs and forelimbs) to support their weight in suspension. Occasion- ally, they use forelimb suspension in traveling.38,52 Thus, these animals ex- hibit the odd behavioral combination of being both specialized leapers and adept climbers and hangers.86 It is likely that the common ancestor of the Indriidae and Palaeopropithecidae was less specialized for leaping than are

Standing believed that the postcrania of Palaeopropithecus provided independent Figure 3. Lateral view of skulls of Palaeopropithecus maximus (top) and Archaeoindris fontoynontii (bottom), both from Ampasambazimba. Archaeoindris shares with Palaeo- evidence of swimming propithecus derived features of the auditory and nasal regions of the skull (e.g., the auditory bullae are deflated; the superior portion of the premaxillae and part of the nasals adaptations. contribute to a pair of protuberances over the nasal aperture) as well as the Unfortunately, the and postcrania. The teeth are very similar in morphology and proportions (e.g., stubby comprise a modified ; a diastema seperates the anterior and posterior postcranial bones that lower ; the third maxillary and mandibular molars are reduced in size, and the first and second molars are long and buccolingually compressed). The mandibular symphsyis he brought to bear on is long and fused early. These taxa form a distinct clade within the Palaeopropithecidae. his argument did not However, their facial profiles are different, and, in many features, Archaeoindris is less derived. For example, the orbits of Archaeoindris lack the distinctly thickened rimming that even belong to characterizes those of Palaeopropithecus, and they are less dorsally directed. The nasal protuberances are less developed. The cheek teeth are less wrinkled and slightly higher- Palaeopropithecus. crowned.

carpals and tarsals of previously known with hooklike hands and feet entirely modern indriids, and sometimes used species, as well as the anatomy of the unsuited for weight bearing in terres- suspension in feeding and traveling. Af- 30 new species of sloth lemurs. Carleton trial locomotion (Table 2). Numerous ter their split, the palaeopropithecid lin- had favored a sloth model, Lamber- postcranial adaptations suggest a com- eage would have sacrificed leaping en- 34 ton an orang model. Subfossil discov- mitment to slow, vertical climbing and tirely, while the indriid lineage eries in the late 1900s tipped the bal- suspensory modes of locomotion in the emphasized leaping. 19,24,26,41–45 ance in favor of the sloth model, sloth lemurs (Box 2). Lim- The dentitions of the indriids and convincing us that Mesopropithecus ited scansoriality has been postulated palaeopropithecids are strikingly was a member of the family Palaeopro- for the gorilla-sized Archaeoin- similar.26,53 All indriids and palaeo- pithecidae (and not an indriid, as previ- dris,26,31,46 which has been likened to a propithecids have a derived dental ously thought).24,40 The spectrum of .39 However, its very high formula (2.1.2.3/2.0.2.3), with no postcranial variation within the Palaeo- femoral neck-shaft angle and other mandibular canine, only two pairs of propithecidae, including Mesopropithe- highly derived postcranial features, premolars, and high shearing cus and the newly discovered Babako- which are shared only with Palaeopro- quotients. M1 and M2 have four main tia, is much like that observed in lorises pithecus, suggest more committed ar- cusps plus strong parastyles and weak and sloths. Mesopropithecus is the most boreality. metastyles. M3 is reduced. The lower quadrupedal and -like, while The nearest relatives to the Palaeo- molars have accentuated trigonid and Palaeopropithecus is the most sloth-like, propithecidae, the living Indriidae, talonid basins; there are five cusps on ARTICLES Sloth Lemurs of Madagascar 257

TABLE 2. Characteristics of the Palaeopropithecidae Body Mass Salient Characteristics; Inferred Taxon (kg)46 Diet54,55 Positional Behavior46 Mesopropithecus (3 species) 9–11 kg Leaves, fruit, and seeds Curved proximal phalanges; hindfoot somewhat reduced; intermembral indices ca. 97–113. Quadrupedal, loris-like slow climber; some fore- and suspension Babakotia (1 species) 15–18 kg Leaves, fruit, and seeds; Curved proximal phalanges; hindfoot some hard objects more reduced than in Mesopropithecus; ca. 118.5. Slow climber, apparently more suspensory than Mesopropithecus but less than Palaeopropithecus Archaeoindris (1 species) 190–210 kg Leaves, fruit, and seeds Humerus longer than femur; a high femoral neck-shaft angle and other features of the postcrania suggest scansoriality Palaeopropithecus (3 species) 25–55 kg Leaves, fruit, and seeds Long, hook-like hands and feet, very curved proximal phalanges, and very reduced hallux and hindfoot; intermembral indices ca. 138–144. Highly suspensory and convergent with Bradypus in many aspects of its skeletal anatomy

M1 (protoconid, paraconid, metac- scale. Some of the anatomical corre- THE DISAPPEARANCE OF THE onid, entoconid, and hypoconid) and lates of this developmental pattern in- SLOTH LEMURS there may be a hypoconulid on M3. clude a diminution of the deciduous The lower premolars are bilaterally teeth and an unusual pattern of perma- Madagascar was one of the last land compressed. There is a long and nent loss (apparently P2 in masses to be colonized by people, and oblique mandibular symphysis and and P in mandible). These the impacts of that colonization on 3 the giant lemurs and other megafauna deep genial fossa. The mandibular cor- characteristics may link all palaeopro- were immediately felt (Boxes 4 and 5). pus is deep, especially in the region of pithecids and indriids. Nevertheless, radiocarbon dates con- the gonial angle, but relatively thin, and Recent studies have begun to probe firm that several of the giant lemurs, the mandibular condyle is compressed possible life-history correlates of this including Palaeopropithecus, Archae- and rounded in coronal view. Palaeo- developmental pattern. Living indriids olemur, and Megaladapis, survived propithecids and indriids also have a grow slowly and tend to delay first re- into the past millennium, along with robust zygomatic with distinct cranial production; their weanlings also tend to gigantic flightless , hippos, and convexity in sagittal view. Their com- be relatively small in body.58–60 Yet other subfossil fauna.20,61–66 A few mon ancestor would have possessed a they all exhibit accelerated dental devel- may have succumbed only very re- conventional toothcomb (with procum- opment, attaining ecological adulthood cently. A specimen of Palaeopropithe- bent, elongated teeth) but with only long in advance of sexual maturation cus ingens from Ankilitelo in south- four elements. The toothcomb is and the cessation of somatic growth. As west Madagascar was recently present in Mesopropithecus and Baba- compared to sympatric lemurids, sifa- radiocarbon-dated at 510 Ϯ 80 BP.20 kotia, but lost in Palaeopropithecus and kas also tend to experience relatively Confidence limits on this date include 46 Archaeoindris. Analysis of molar mi- low adult mortality under moderate re- the historical period.4,66 The causes of 54,55 59,60 crowear suggests a mixed diet sim- source crunches. We have sug- the have been hotly de- ilar to the diets of extant indriids. gested that this pattern may reflect an bated (Box 5), but a major impact by It is also noteworthy that all palaeo- ability to survive on low-quality (that is, humans can no longer be contested. propithecid species for which imma- highly fibrous) staple or fallback foods Gabriel Ferrand67 was one of sev- ture individuals are known can be and a life-history “strategy” of low eral European folklorists who, in the shown to have had unusually acceler- maternal input and slow returns in last nineteenth century, recorded ated dental development, apparently an unpredictable and periodically Malagasy tales of fabulous hippo- for early processing of fibrous foods stressful environment.60 Evidence is like, elephant-bird-like, and lemur- (Box 3).56,57 Crown initiation and min- accumulating that palaeopropithec- like beasts. There was a ferocious, eralization is accelerated both relative ids followed similar developmental hornless, dim-sighted “not-cow-cow” to cranial growth and on an absolute trajectories.56,57 that sprayed , and charged and 258 Godfrey and Jungers ARTICLES

Box 2. Extreme Sport W. L. Jungers and L. R. Godfrey All of the sloth lemurs (Mesopro- pithecus, Babakotia, Palaeopropithe- cus, and Archaeoindris) exhibit post- cranial convergences with true sloths to some degree.46 However, the cul- mination of extreme suspensory ad- aptations in the palaeopropithecids can be seen in the skeleton of the family’s namesake, Palaeopropithe- cus—probably the most antiprono- grade arborealist ever to evolve in the order . All species of this ge- nus are characterized by extreme forelimb dominance, with a humero- femoral index hovering around 150 (by comparison, siamang and orang- utans top out in the 130 range). This remarkable proportionality is driven primarily by extreme reduction of the hind limb relative to estimated body mass. The hands and feet of Palaeopro- pithecus are long, hook-like append- The tarsal bones of Palaeopropithecus are unique among primates in their shape and ages with pronounced phalangeal articulation. The calcaneus is short and quite small, and the head of the talus articu- curvatures44; even the distal phalan- lates with the navicular and the cuboid. ges are “bent.” The proximal phalan- ges have pronounced flexor ridges for trum in a mortar-and-pestle arrange- bar vertebrae is the extreme reduc- deep osseofibrous tunnels through ment.45 The ankle of Palaeopropithe- tion of the spinous processes to mere which the digital flexor tendons ran. cus is simply bizarre, and epitomizes nubbins, another feature that harkens The metacarpophalangeal joints have mobility. Neither the tibia nor the fib- back to sloth-like anatomy. The a “-and-groove” geometry, ula has a real malleolus, and both transverse processes of the lumbar unique among primates, that guides articulate with a semi-spherical talar vertebrae have migrated dorsally and limits movement of the rays to trochlea in a mobile arrangement that onto the vertebral arches in hominoid stereotypical flexion and extension. recalls the hominoid shoulder joint. fashion, and the laminae are quite The hallux is very reduced in length; The calcaneus is extremely small, so broad. We speculate that the liga- we suspect that the pollex was too. reduced, in fact, that it was originally mentum flavum was especially well Although virtually every joint of the mistaken for a pisiform.21 It served as developed as a passive fibroelastic postcranium of Palaeopropithecus little more than a bony guide for the mechanism for resisting vertebral shows modifications for enhanced tendons of the pedal digital flexors. flexion in upside-down postures. The mobility or hanging, the wrist and an- The head of the talus is planar-flexed virtual lack of spinous processes con- kle joints are especially derived in this and projects distally far beyond the tinues down onto the sacrum. The respect. Further, the olecranon pro- tiny calcaneus; it articulates uniquely sacral hiatus is small, as is the artic- cess of the ulna is very reduced, as among primates with both the navic- ular facet for the first caudal . in hominoids, and the globular fem- ular and cuboid. The total foot has an We suspect that the tail was vestigial oral head sits atop a neck aligned inverted set, so that it is difficult to in Palaeopropithecus. Locomotion on almost vertically with the femoral imagine it functioning in pronograde the ground would have been un- shaft. weight support. gainly, perhaps comical, and proba- The carpus has an overall “flexed The vertebral column is equally bly quite rare, except to creep across set” relative to the forearm, and the specialized for suspensory postures the ground from one feeding tree to conical ulnar styloid process articu- and locomotion. One of the most re- the next when presented with gaps in lates exclusively with the trique- markable features of the thoracolum- the forest .

mauled people. There was a jealous body of an animal but the face of a it was unable to move on flat surfaces. and powerful ogre-bird that could not human that could be rendered help- It is tempting to think that this de- fly. There was another ogre with the less on smooth rock outcrops because scription might have been based on ARTICLES Sloth Lemurs of Madagascar 259

Box 3. Big Bodies, Fast Teeth G.T. Schwartz and L.R. Godfrey

Large-bodied extant primates gen- erally have slow dental crown forma- tion. This tends to be correlated with prolonged dental eruption, delayed maturation, and a generally slow pace of life history. In anthropoid pri- mates, M1 crowns initiate during the last third of the gestation period; in the case of the largest-bodied an- thropoids with the slowest life histo- ries, they initiate only just before . It is possible to reconstruct the tim- ing of molar crown formation in ex- tinct species because of one unique property of teeth: They preserve within them an indelible record of their growth. Teeth grow incremen- tally, like trees or shells, and the cells that produce the two main tissue components of tooth crowns (amelo- blasts in enamel and odontoblasts in dentine) do so in accordance with the Chronology of dental development in Palaeopropithecus, Propithecus, and Pongo. body’s circadian rhythm. As these Indicated above the bars are the days devoted to crown formation before and after cells secrete enamel and dentine, birth in each of these three taxa. they leave in their wake a trail of in- cremental markings, of which there are two types: short-period, or daily crown. These were used to recon- mates, but from that of other mam- lines (cross striations) and long-pe- struct individual molar crown forma- mals of comparable body size. It can riod lines (striae of Retzius). It is these tion times, the time of initiation and be achieved in an animal the size of incremental features that provide the completion of each molar crown, and Palaeopropithecus only through ex- “road map” for charting tooth-crown the sequence of molar crown develop- ceedingly high daily rates of enamel formation times, the timing of tooth ment. All of these data were then used secretion. initiation and completion, and the tim- to generate a timeline of molar devel- Remarkably, the same pattern of ing of birth and age at death. Ulti- opment relative to the time of birth. accelerated dental development is mately, these features allow paleontol- For a of its body and molar evident in extant indriids, such as the ogists to reconstruct the trajectory of size, Palaeopropithecus ingens has sifaka. A nearly identical timeline for dental development in extinct species. remarkably short crown formation first molar formation has been con- Given a likely body mass of ca. 45 times: M1 ϭ 221 days (0.61 years); firmed for Propithecus verreauxi.57 In kg (comparable to that of orang- M2 ϭ 247 days (0.68 years); and this species, as in its much larger rel- utans),46 Palaeopropithecus ingens M3 Ͼ 135 days (Ͼ0.37 years). The ative, M1 crown formation time is might be expected to exhibit slow den- degree of sequential molar develop- 0.61 years. The M1 crown initiates tal development. Recently, Schwartz mental overlap is great, with all three equally early (98 to 113 days prena- and others57 conducted a microstruc- molars initiating before birth, as is ev- tally). tural analysis of the molars of this ident from the presence in all three Our study of dental development in giant sloth lemur. Histological thin molars of a neonatal line. Taken to- giant lemurs is helping to elucidate sections of the molar series were pre- gether, these data point to a relatively the relationships among body mass, pared from a single juvenile P. ingens short overall period devoted to molar dental development and aspects of specimen from Ankazoabo Cave, in crown development. Indeed, the pro- the life histories of primates. Clearly, southwestern Madagascar. Both cess is completed several months af- a simple relationship between body short- and long-period lines were vis- ter birth. This pattern differs not size and the pace of dental develop- ible throughout the entire enamel merely from that of large-bodied pri- ment is not tenable. 260 Godfrey and Jungers ARTICLES

Box 4. Butchered Sloth Lemurs V.R. Perez, D.A. Burney, L.R. Godfrey, and M. Nowak-Kemp

Cut-mark analysis of specimens of Palaeopropithecus ingens belonging to the Oxford University of Natural History has provided the first definitive evidence of the hunting and consumption of giant lemurs in Madagascar. Specimens from Ta- olambiby, a subfossil site in south- western Madagascar, show classic signs of butchering, including sharp cuts near joints, spiral fractures, and percussion striae. These spec- imens were discovered by Hon. Paul Ayshford Methuen, who sailed to Madagascar in 1911 expressly to collect bones of the extinct lemurs for the Oxford Museum. Methuen spent a few years as a member of the staff at the Transvaal Museum before abandoning biology for life as an artist at his estate, Corsham Court, near Chippenham, England. Methuen’s subfossil lemur collec- tion remained in obscurity at the Ox- ford Museum until it was effectively rediscovered at the turn of the twenty- first century. We have found definitive cut marks on six of the seventeen specimens of Palaeopropithecus long bones in the Methuen collection that we have ex- amined. These six bones have a total This left humerus of Palaeopropithecus ingens in the Methuen collection (OXUM of forty-three cuts, all of which show 14342A) shows cut marks just above the medial epicondyle. The orientation and location of these cutmarks suggest that this animal was disarticulated and processed classic signs of having been pro- for consumption. duced by butchery. Some appear to have resulted from dismembering and skinning, whereas others appear acute angles to the long axis of the surprisingly early given that abundant to have resulted from filleting. The lo- bone. Filleting marks, which result evidence from introduced and ruderal cation and morphological character- from the removal of muscle, run along pollen types, dates on human-modi- istics of the marks provide clues to the long axis of the shaft and are fied hippo bones, and drastic in- their origins.72–75 Ninety-five percent found at or near points of muscle or- creases in particles from of the marks on these sloth lemur igin or insertion. These are present on sites all over Madagascar point to hu- bones are V-shaped; that is, the sides three bones: a right ulna and a left man arrival about two millennia ago, of the kerf walls meet at the base. and right tibia. give or take a couple of centuries This suggests the use of a sharp- The dating of these sloth lemur (summarized by Burney66). After cali- edged implement that compressed bones was largely unsuccessful. bration against the tree-ring record at the cortex to the sides as it was Most of the cut material from Taolam- 2␴, the Palaeopropithecus bone re- drawn across the surface of the biby contained too little collagen for sult is 417 to 257 BC. If this date is bone,76–78 as might be expected reliable 14C dating. However, the ex- correct, this sloth lemur may have when cadavers are skinned and dis- ception was a right proximal radius of been killed and eaten by some of the articulated.72,74,79 Disarticulation and Palaeopropithecus ingens that had first people to reach Taolambiby. skinning marks tend to be located conspicuous butchery marks. Colla- Whoever they were, these folks were near the joints and to be compara- gen extracted from this bone yielded perhaps among the island’s earliest tively deep, V-shaped, and aligned at an age of 2,325 Ϯ 43 years BP. This is human inhabitants. ARTICLES Sloth Lemurs of Madagascar 261

Box 5. Extinction in Madagascar: The Anatomy of a Catastrophe D.A. Burney

The last and most extreme of a long chain of extinction events took out diverse of mammals, birds, and reptiles from Australia, the Americas, and the world’s larger is- lands. Whereas most places lost three-quarters or four-fifths of their large genera, Madagascar lost all of its native mammals over ca. 10 kg, including pygmy hippos and giant lemurs, as well as the huge el- ephant birds and giant tortoises. De- spite a lot of scientific detective work, the cause or causes of these extinc- tions are still shrouded in mystery. Early botanists working in Mada- gascar, such as Henri Humbert,80 suggested that the early Malagasy precipitated these extinctions by in- troducing fire and transforming the animals’ habitat. Mahe´ and Sourdat61 cited evidence of desiccation in the dry southern region as a reason for A simple conceptual model for the author’s synergy hypothesis, proposed to explain the extinctions in Madagascar. The empirical evidence suggests that human overex- megafaunal decline there. Many sci- ploitation of the megafauna may have set in motion a series of environmental changes entists have invoked changes that led to collapse. of various sorts to try to explain late prehistoric extinctions elsewhere. disease theories, but it is not clear For instance, what if the vegeta- Paul Martin81 extended to Madagas- what that evidence would look like. tion of Madagascar’s wooded sa- car his “blitzkrieg” model for rapid ex- No known disease is equally and rap- vannas, semiarid bushlands, and tinction following overkill. Robert De- idly lethal for primates, other mam- forests had been closely cropped war62 wondered if the introduction of mals, birds, and reptiles. for millions of years by the presum- to Madagascar might have Whatever happened, the great ably abundant native grazers and had something to do with it, while number of new automated mass browsers, and these communities MacPhee and Marx82 suggested that spectroscopy 14C dates on collagen were suddenly disrupted by over- an unknown “hypervirulent disease” from a wide array of extinct creatures hunting? Long before extinction set could account for losses here and show that many of them survived until in, fires would have increased in fre- worldwide. a few centuries ago. Some, such as quency and severity in this accumu- All these hypotheses were spawned Hippopotamus and perhaps even Ar- lating plant biomass, changing in the absence of sufficient evidence to chaeolemur, may have held out in re- many areas to the depauperate mount a definitive test. Recently, many mote pockets until the nineteenth steppe and spiny bush- pertinent facts have come to light that century or even later.3,4,66 lands characteristic of so much of suggest that all of these explanations Perhaps extinction theorists would the island today. The opening of might be insufficiently complex. Recent do well to borrow some ideas from sys- these habitats would have made it data show that people arrived in Mada- tem modelers, especially those in an easier for hunters to find the survi- gascar around two millennia ago or area of mathematics known as com- vors and, with the introduction of possibly a few centuries earlier (see plexity theory.85 Humans arrived in livestock and exotic carnivores such Box 4). However, it took them over a Madagascar on the heels of the in- as and cats, new impacts millennium to colonize the more humid creasingly dry and uncertain would emerge. Every human and parts of the interior,66 perhaps due to documented for the Southern Hemi- natural challenge would have com- setbacks from tropical diseases that af- sphere during the late . It is pounded the impact of each of the flict humans in this region. not hard to imagine that the array of others, driving the to Evidence also has been found for impacts they exerted could have acted new states that were less favorable climate changes that immediately synergistically.66 Perhaps unexpect- to survival of the struggling mega- predated human arrival,84 hunting by edly strong interactions occurred that fauna. Such a combinatorial solution humans64 (see Box 4), and changes in moved the ecosystems of Madagascar fits the data better than any previous fire regime (although fires also pre- far from their normal equilibria into a hypothesis and equally well de- date humans in some areas83). No phase transition from which there was scribes the present crisis evidence has been found to support no return. in Madagascar. 262 Godfrey and Jungers ARTICLES

Palaeopropithecus; surely this giant Madagascar compose´e par le Sieur de Flacourt, 2 lemur (Palaeopropithecidae) from Northwest sloth lemur would not have been able vols. Paris: Chez G. de Lvyne. Madagascar. 3 Godfrey LR. 1986. The tale of the tsy-aomby- 23 Godfrey LR, Simons EL, Chatrath PS, Rako- to negotiate smooth, flat surfaces. We aomby. The Sciences 1986:49–51. tosamimanana B. A new fossil lemur (Babakotia, probably will never know whether or 4 Burney DA, Ramilisonina. 1998. The kilopilo- Primates) from northern Madagascar. C R Acad not Etienne de Flacourt’s2 “tretretre- pitsofy, kidoky, and bokyboky: accounts of Sci Paris 310 (Se´rie II):81–87. tre” or Gabriel Ferrand’s67,68 flat-faced strange animals from Belo-sur-mer, Madagascar, 24 Simons EL, Godfrey LR, Jungers WL, Cha- and the megafaunal “extinction window.” Am trath PS, Ravaoarisoa J. 1995. A new species of ogre do indeed describe Palaeopro- Anthropol 100:1–10. Mesopropithecus (Primates, Palaeopropitheci- pithecus. But there can be no question 5 Grandidier A. 1868. Lettre rectifiant la position dae) from Northern Madagascar. Int J Primatol that in the two thousand years since ge´ographique des principales rivie`res de la coˆte 16:653–682. sud-est et annonc¸ant la de´couverte d’ossements 25 Standing H-F. 1903. Rapport sur des ossements they first colonized Madagascar, the fossiles d’un nouvel Aepyornis et d’un Hippo- sub-fossiles provenant d’Ampasambazimba. Bull human inhabitants of Madagascar potame. Bull Soc Ge´ogr Paris, nov.–de´c. 1868: Acad Malgache 2:227–235. bore witness to some of the most re- 508–510. 26 Godfrey LR, Jungers WL. 2002. Quaternary markable primates ever to have 6 Grandidier A. 1868. Sur des de´couvertes fossil lemurs. In: Hartwig WC, editor. The pri- zoologiques faites re´cemment a` Madagascar (de- mate fossil record. New York: Cambridge Univer- evolved: Madagascar’s giant sloth le- scription d’un hippopotame nouveau, de tortues sity Press, p 97–122. murs. colossales et d’une espe`cede Chirogale). C R Acad 27 Grandidier G. 1901. Un nouvel e´dente´ subfos- Sci Paris. 63:1165–1167 and Annl Sci Nat (Zool) sile de Madagascar. Bull Mus Natl Hist Nat Paris 10:375–378. 7:54–56. ACKNOWLEDGMENTS 7 Grandidier A. 1971. Souvenirs de voyages 28 Sera GL. 1935. I caratteri morfologici di “Pa- d’Alfred Grandidier (1865–1870). Tananarive: As- leopropithecus” e l’adattamento acquatico primi- We thank John Fleagle for his en- sociation Malgache d’Arche´ologie (Se´rie Docu- tivo dei Mammiferi e dei Primati in particolare. ments anciens sur Madagascar VI). Contributo alla morphologia, all filogenesi e alla couragement and patience with re- 8 Filhol H. 1895. Observations concernant les paleobiologia dei Mammifera. Arch Ital di Anat e spect to this article. We are grateful mammife`res contemporains des Aepyornis a` Embriol 35:229–370. to many of our colleagues who con- Madagascar. Bull Mus Natl Hist Nat Paris 1:12– 29 Sera GL. 1938. Alcuni cratteri scheletrici di importanza ecologica e filletica nei Lemuri fossili tributed to the recovery of fossils, 14. 9 Grandidier G. 1899. Description d’ossements ed attuali. Studi sulla paleobiologia e sulla filo- data and ideas embodied in our re- de le´muriens disparus. Bull Mus Natl Hist Nat genesi dei Primati. Paleontog Ital Memorie Pale- view of sloth lemurs, including our Paris 5:344–348. ontol 38 (n.s. 8):1–113. Box contributors Elwyn Simons (Duke 10 Standing H-F. 1905. Rapport sur des ossements 30 Carleton A. 1936. The limb-bones and verte- brae of the extinct lemurs of Madagascar. Proc sub-fossiles provenant d’Ampasambazimba. Bull University), Gary Schwartz (Northern Zool Soc Lond 106:281–307. Acad Malgache 4:95–100. 31 Vuillaume-Randriamanantena M. 1988. The Illinois University), Ventura Perez (Uni- 11 Standing H-F. 1909. Subfossiles provenant taxonomic attributions of giant subfossil lemur versity of Massachusetts, Amherst), des fouilles d’Ampasambazimba. Bull Acad Mal- bones from Ampasambazimba: Archaeoindris gache 6:9–11. David Burney (Fordham University) and Lemuridotherium. J Hum Evol 17:379–391. 12 Standing H-F. 1910. Note sur les ossements and Malgosia Nowak-Kemp (Oxford 32 Standing H-F. 1913. Proce`s-verbal de la se´- subfossiles provenant des fouilles d’Ampasam- ance du 28 novembre 1912. (Reported by M. Fon- University Museum of Natural His- bazimba. Bull Acad Malgache 7:61–64. toynont). Bull Acad Malgache 10:41–44. tory). We also thank Prithijit Chatrath, 13 Lamberton C. 1934. Contribution a` la con- 33 Lamberton C. 1939. Contribution a` la con- Mark Hamrick, Karen Samonds, Gina naissance de la faune subfossile de Madagascar. naissance de la faune subfossile de Madagascar: Semprebon, Liza Shapiro, Ian Tatter- Le´muriens et . L’Archaeoindris fon- Le´muriens et cryptoproctes. Note VI. Des os du toynonti Stand. Me´m Acad Malgache 17:9–39. sall, Mark Teaford, Martine Vuillaume- pied de quelques le´muriens subfossiles mal- 14 Lamberton C. 1936. Nouveaux le´muriens fos- gaches. Me´m Acad Malgache 27:75–139. Randriamanantena, Alan Walker, and siles du groupe des Propithe`ques et l’inte´reˆt de 34 Lamberton C. 1947. Contribution a` la con- Roshna Wunderlich. We are indebted leur de´couverte. Bull Mus Natl Hist Nat Paris naissance de la faune subfossile de Madagascar. (2e`me Se´rie) 8:370–373. to our colleagues and friends in Mada- Note XVI. Bradytherium ou Palaeopropithe`que? 15 Tattersall I. 1971. Revision of the subfossil Bull Acad Malgache (nouv se´rie) 26:89–140. gascar for their trust and permission to Indriinae. Folia Primatol 15:257–269. 35 Lamberton C. 1957. Examen de quelques hy- work in their country on their fossils. 16 De Saint-Ours J. 1953. Etude des grottes potheses de Sera concernant les le´muriens fos- These include Gise`le Randria, Berthe d’Andranoboka. Travaux du Bureau Ge´ologique silles et actuels. Bull Acad Malgache (nouv se´rie) Rakotosamimanana, Armand Ra- Nume´ro 43. : Service Ge´ologique. 34:51–65. 17 Mahe´ J. 1965. Un gisement nouveau de sub- 36 Sera GL. 1950. Ulteriori osservazioni sui le- soamiaramanana, and Benjamin Andri- fossiles a` Madagascar. C R Sommaire des Se´- muri fossili ed attuali Significato di alcuni carat- amihaja. We greatly appreciate com- ances de la Socie´te´Ge´ologique de France 2:66. teri in rapporto con l’evoluzione dei Primati. Pa- ments on an earlier draft of this 18 Simons EL, Godfrey LR, Vuillaume-Randria- leontog Ital 47 (n.s. 17):1–97. manantena M, Chatrath PS, Gagnon M. 1990. 37 Lamberton C. 1948. Contribution a` la con- manuscript by Ian Tattersall and Alan Discovery of new giant subfossil lemurs in the naissance de la faune subfossile de Madagascar. Walker. Thanks, finally, to Luci Betti- Ankarana Mountains of Northern Madagascar. J Note 20. Membre posterieur des Neopro- Nash for help in preparing the figures. Hum Evol 19:311–319. pithe`ques et des Mesopropithe`ques. Bull Acad Malgache (nouv se´rie) 27:30–32. This work was supported in part by NSF 19 Simons EL, Godfrey LR, Jungers WL, Cha- trath PS, Rakotosamimanana B. 1992. A new 38 Walker AC. 1967. Locomotor in grants BCS-0237338, BCS-0129185, giant subfossil lemur, Babakotia, and the evolu- recent and fossil Madagascar lemurs. Doctoral SBR-0001429, and SBR-963350. tion of the sloth lemurs. Folia Primatol 58:197– dissertation, University of London. 203. 39 Jungers WL. 1980. Adaptive diversity in sub- 20 Simons EL. 1997. Lemurs: old and new. In: fossil Malagasy . Z Morphol An- REFERENCES Goodman SM, Patterson BD, editors. Natural thropol 71:177–186. change and human impact in Madagascar. 40 Godfrey LR. 1988. Adaptive diversification of 1 Yoder AD, Rakotosamimanana B, Parsons T. Washington, D.C.: Smithsonian Malagasy strepsirrhines. J Hum Evol 17:93–134. 1999. Ancient DNA in subfossil lemurs: method- Press, p 142–166. 41 Jungers WL, Godfrey LR, Simons EL, Cha- ological challenges and their solutions. In: Rako- 21 MacPhee RDE, Simons EL, Wells NA, Vuil- trath PS, Rakotosamimanana B. 1991. Phyloge- tosamimanana B, Rasamimanana H, Ganzhorn laume-Randriamanantena M. 1984. Team finds netic and functional affinities of Babakotia rado- JU, Goodman SM, editors. New directions in le- giant lemur skeleton. Geotimes 29:10–11. filai, a new fossil lemur from Madagascar. Proc mur studies. New York: Plenum Press. p 1–17. 22 Jungers WL, Simons EL, Godfrey LR, Cha- Nat Acad Sci USA 88:9082–9086. 2 de Flacourt E. 1658. Histoire de la grande Isle trath PS, Rakotosamimanana B. n.d. A new sloth 42 Demes B, Jungers WL. 1993. Long bone cross- ARTICLES Sloth Lemurs of Madagascar 263

sectional geometry of extant and subfossil indri- 57 Schwartz GT, Samonds KE, Godfrey LR, mates): proposed conservation of both generic oid primates. Am J Phys Anthropol 16(suppl):80– Jungers WL, Simons EL. 2002. Dental micro- and specific names. Bull Zool Nomenclature 49: 81. structure and life history in subfossil Malagasy 55–57. 43 Shapiro L, Jungers WL, Godfrey LR, Simons lemurs. Proc Natl Acad Sci 99:6124–6129. 72 Binford LR. 1981. Bones: ancient men and EL. 1994. Vertebral morphology of extinct le- 58 Wright PC. 1999. Lemur traits and Madagas- modern myths. New York: Academic Press. murs. Am J Phys Anthropol 18(suppl):179–180. car ecology: coping with an island environment. 73 Cruz-Uribe K, Klein RG. 1994. Chew marks 44 Jungers WL, Godfrey LR, Simons EL, Cha- Yearbook Phys Anthropol 42:31–72. and cut marks on animal bones from the Kasteel- trath PS. 1997. Phalangeal curvature and posi- 59 Richard AF, Dewar RE, Schwartz M, Ratsir- berg B and Dune Field Midden Later Stone Age tional behavior in extinct sloth lemurs (Primates, arson J. 2002. Life in the slow lane? Demography sites, Western Cape Province, South . J Ar- Palaeopropithecidae). Proc Natl Acad Sci USA and life histories of male and female sifaka (Pro- chaeol Sci 21:35–49. 94:11998–12001. pithecus verreauxi verreauxi). J Zool 256:421–436. 74 Lyman RL. 1987. Archaeofaunas and butch- 45 Hamrick MW, Simons EL, Jungers WL. 2000. 60 Godfrey LR, Samonds KE, Jungers WL, Suth- ery studies: a taphonomic perspective. Adv Ar- New wrist bones of the Malagasy giant subfossil erland MR, Irwin MT. n.d. Ontogenetic corre- chaeol Method Theory 10:249–337. lemurs. J Hum Evol 38:635–650. lates of diet in Malagasy lemurs. Am J Phys An- 75 Potts R, Shipman P. 1981. Cutmarks made by 46 Jungers WL, Godfrey LR, Simons EL, thropol. In press. stone tools on bones from Olduvai Gorge, Tan- Wunderlich RE, Richmond BG, Chatrath PS. 61 Mahe´ J, Sourdat M. 1972. Sur l’extinction sur zania. Nature 291:577–580. 2002. Ecomorphology and behavior of giant ex- les verte´bre´s subfossiles et l’aridification du cli- 76 Maples WR. 1986. Trauma analysis by the tinct lemurs from Madagascar. In: Plavcan JM, mat dans le Sud-ouest de Madagascar. Bull Soc forensic anthropologist. In: Reichs KJ, editor. Kay RF, Jungers WL, van Schaik CP, editors. Geol Fr 14:295–309. Forensic osteology: advances in the identification Reconstructing behavior in the primate fossil 62 Dewar RE. 1984. Recent extinctions in Mada- of human remains. Springfield: Charles C record. New York: Kluwer Academic/Plenum gascar: the loss of the subfossil fauna. In: Martin Thomas. p 218–228. Publishers, p 371–411. PS, Klein RG, editors. Quaternary extinctions: a 77 Reichs KJ. 1998. Postmortem dismember- 47 Napier JR, Walker AC. 1967. Vertical clinging prehistoric revolution. Tucson: University of Ar- ment: recovery, analysis and interpretation. In: and leaping: a newly recognized category of pri- izona Press, p 574–593. Reichs KJ, editor. Forensic osteology: advances mate locomotion. Folia Primatol 6:204–219. 63 Dewar RE. 1997. Were people responsible for in the identification of human remains, 2nd ed. 48 Walker AC. 1974. Locomotor adaptations in the extinction of Madagascar’s , and Springfield: Charles C Thomas. p 353–388. past and present primates. In: Jenkins how will we ever know? In: Goodman SM, Patter- FA Jr, editor. Primate locomotion. New York: son BD, editors. Natural change and human im- 78 Perez VR. 2002. La Quemada tool induced Academic Press. p 349–381. pact in Madagascar. Washington, DC: Smithso- bone alterations: cutmark differences between human and animal bones. Archaeol Southwest ´ nian Press. p 364–377. 49 Jouffroy F-K, Lessertisseur J. 1978. Etude 16:10. e´comorphologiqie des proportions des membres 64 MacPhee RDE, Burney DA. 1991. Dating of des Primates et specialement des Prosimiens. modified femoral of extinct dwarf Hippopotamus 79 Jelinek J. 1993. Dismembering, fileting and Ann Sci Natur Zool Biol Anim 20:99–128. from southern Madagascar: implications for con- evisceration of human bodies in a Bronze Age straining human colonization and ex- site in Moravia, Czech Republic. Anthropologie 50 Anemone RL. 1990. The VCL hypothesis re- 31:99–114. visited: patterns of femoral morphology among tinction events. J Archaeol Sci 18:695–706. quadrupedal and saltatorial prosimian primates. 65 Simons EL, Burney DA, Chatrath PS, Godfrey 80 Humbert H. 1927. De´struction d’une flore in- Am J Phys Anthropol 83:373–393. LR, Jungers WL, Rakotosamimanana B. 1995. sulaire par le feu. Me´m Acad Malgache 5:1–80. 14 51 Demes B, Jungers WL, Fleagle JG, Wunder- AMS dates on extinct lemurs from caves in the 81 Martin PS. 1984. Prehistoric overkill: the lich RE, Richmond BG, Lemelin P. 1996. Body Ankarana Massif of northern Madagascar. Quar- global model. In: Martin PS, Klein RG, editors. size and leaping kinematics in Malagasy vertical ternary Res 43:249–254. Quarternary extinctions: a prehistoric revolu- clingers and leapers. J Hum Evol 31:367–388. 66 Burney DA. 1999. Rates, patterns, and pro- tion. Tucson: University of Arizona Press. p 354– 403. 52 Gebo DL. 1987. Locomotor diversity in pros- cesses of landscape transformation and extinc- imian primates. Am J Primatol 13:271–281. tion in Madagascar. In: MacPhee RDE, editor. 82 MacPhee RDE, Marx PA. 1997. The 40,000- Extinctions in near time: causes, contexts, and plague: humans, hypervirulent diseases, and 53 Tattersall I, Schwartz JH. 1974. Craniodental consequences. New York: Plenum Press. p 145– first-contact extinctions. In: Goodman SM, morphology and the of the Malagasy 164. Patterson BD, editors. Natural change and hu- lemurs (Primates, Prosimii). Anthropol Pap Am Museum Nat Hist 52:137–192. 67 Ferrand G. 1893. Contes populaire mal- man impact in Madagascar. Washington, DC: gaches. Paris: Ernest Leroux. Smithsonian Press. p 169–217. 54 Rafferty K, Teaford MF, Jungers WL. 2002. Molar microwear of subfossil lemurs: improving 68 Ferrand G. 1905. Dictionnaire de la langue de 83 Burney DA. 1997. Theories and facts regard- the resolution of dietary inferences. J Hum Evol Madagascar d’apre`s l’e´dition de 1658 et l’histoire ing Holocene environmental change before and 43:645–657. de la grande isle Madagascar de 1661. Paris: E. after human colonization. In: Goodman SM, Leroux. p 35. Patterson BD, editors. Natural change and hu- 55 Godfrey LR, Semprebon GM, Jungers WL, 69 Grandidier G. 1902. Observations sur les le´- man impact in Madagascar. Washington DC: Sutherland MR, Simons EL, Solounias N. n.d. Smithsonian Press. p 75–89. Dental use wear in extinct lemurs: evidence of muriens disparus de Madagascar. Collections Al- diet and . J Hum Evol. Sub- luaud, Gaubert, Grandidier. Bull Mus Natl Hist 84 Burney DA. 1993. Late Holocene environmen- mitted. Nat Paris 8:497–505. tal changes in arid southwestern Madagascar. Quaternary Res 40:98–106. 56 Godfrey LR, Petto AJ, Sutherland MR. 2002. 70 Vuillaume-Randriamanantena M. 1990. Palaeo- Dental ontogeny and life-history strategies: the propithecus ingens Grandidier, 1899 synonyme 85 Prigogine I, Nicolis G. 1998. Exploring com- case of the giant extinct indroids of Madagascar. de Thaumastolemur grandidieri Filhol, 1895. C R plexity: an introduction. New York: W.H. Free- In: Plavcan JM, Kay RF, Jungers WL, van Schaik Acad Sci Paris, Se´rie II 310:1307–1313. man. CP, editors. Reconstructing behavior in the pri- 71 Tattersall I, Simons EL, Vuillaume-Randria- 86 Gebo D, Dagosto, M. 1988. Foot anatomy, mate fossil record. New York: Kluwer Academic/ manantena M. 1992. Case 2785. Palaeopropithe- climbing, and the origin of the Indriidae. J Hu- Plenum Publishers, p 113–157. cus ingens G. Grandidier, 1899 (Mammalia, Pri- man Evol 17:135–154.