The Extinct Sloth Lemurs of Madagascar
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Evolutionary Anthropology 12:252–263 (2003)
ARTICLES
The Extinct Sloth Lemurs of Madagascar
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 species belonging to a group of giant extinct Ambolisatra, the first subfossil 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 sloths. New fossils 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 (⬎100 m) called Ankilitelo, the “place of the three kily trees.” 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 animals. was the distal humerus of a sloth le-
New analytical tools have begun to unlock the secrets of life-history adaptations of mur, Palaeopropithecus—perhaps the
the Palaeopropithecidae, making explicit exactly what they had in common with first specimen of a giant extinct lemur
their relatives, the Indriidae. 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 skulls 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 forelimb gens was allocated to a mandible
genera are currently recognized as be- and reduction of the hind limb are all found at another subfossil site in
longing in this family: Palaeopropithe- the more remarkable because their southwestern Madagascar just before
cus (the type genus), 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 hindlimbs and mandible was chimp-sized but had si-
ied Mesopropithecus, and the mid- shortest forelimbs in the Order Pri- faka-like teeth. Similar mandibles and
sized, recently discovered Babakotia. mates. A sister taxon relationship of associated skulls were recovered from
This family exhibits the greatest range the Palaeopropithecidae to the Indri- 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 mammals on the correctly.
pology at the University of Massachusetts
at Amherst. lgodfrey@anthro.umass.edu 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 sifaka-like teeth were recovered at
ical Sciences at Stony Brook University,
New York. William.Jungers@sunysb.edu
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 extinction of pri- his own descriptions of the biota of Some (Mesopropithecus pithecoides)10
mates in Madagascar for the last three
decades. Both have collaborated on pa- Madagascar, Flacourt2 recorded puta- were barely larger than the crania of
leontological expeditions in Madagascar tive Malagasy eyewitness accounts of diademed sifakas, while others (Ar-
with Elwyn L. Simons at Duke University 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 gorilla crania. The gorilla-sized
regions of Madagascar, even today, as Archaeoindris was established on the
© 2003 Wiley-Liss, Inc. during the past hundred years, 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. Taxonomy 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)
skull, 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 fossa 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,
Mahé17 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 monkey likenesses. Refer-
ences to Archaeoindris as being simi-
lar to Megaladapis 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
Figure 2. Working cladogram for the Indriidae and the Palaeopropithecidae. The Palaeo-
Madagascar, Flacourt
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 postorbital bar, more
convergent and often confluent temporal lines, with the frequent development of sagittal
accounts of huge and
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 lorises, 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 radius of
tions. Unfortunately, the postcranial Megaladapis, a fibula of Megaladapis
the past hundred years,
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 crocodile, 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 tree sloth that Alfred Grandidi- broadened his aquatic theory to en-
er’s son, Guillaume, called Bradythe- compass other extinct lemurs.29 Mega- sented in the fossil record, but until
rium.27 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- hand and foot bones, and the pelvis,
The Hadropithecus 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 megafauna 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 bird. The bird must
plorer Étienne 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- Roc 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, Aepyornis, 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 Tuléar,
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 animal). 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 the256 Godfrey and Jungers ARTICLES
are “vertical clingers and leapers”
with elongated hands 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
Figure 3. Lateral view of skulls of Palaeopropithecus maximus (top) and Archaeoindris
provided independent
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 dentitions
and postcrania. The teeth are very similar in morphology and proportions (e.g., stubby
Unfortunately, the
incisors comprise a modified toothcomb; a diastema seperates the anterior and posterior postcranial bones that
lower premolars; 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.
However, their facial profiles are different, and, in many features, Archaeoindris is less
his argument did not
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-
new species of sloth lemurs. Carleton30 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-
ton34 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.
ance in favor of the sloth model, sloth lemurs (Box 2).19,24,26,41– 45 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 ground sloth.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 molar 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 loris-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 onARTICLES 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 hindlimb suspension
Babakotia (1 species) 15–18 kg Leaves, fruit, and seeds; Curved proximal phalanges; hindfoot
some hard objects more reduced than in
Mesopropithecus; intermembral
index 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 premolar loss (apparently P2 in masses to be colonized by people, and
oblique mandibular symphysis and maxilla and P3 in mandible). These the impacts of that colonization on
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 birds, 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 ⫾ 80 BP.20
kotia, but lost in Palaeopropithecus and kas also tend to experience relatively Confidence limits on this date include
Archaeoindris.46 Analysis of molar mi- low adult mortality under moderate re- the historical period.4,66 The causes of
crowear54,55 suggests a mixed diet sim- source crunches.59,60 We have sug- the extinctions 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 urine, and charged and258 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 Primates. 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 “tongue-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 vertebra.
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 canopy.
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 onARTICLES 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 birth.
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
birth in each of these three taxa.
cells secrete enamel and dentine,
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 primate 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 ⫽ 221 days (0.61 years); firmed for Propithecus verreauxi.57 In
kg (comparable to that of orang- M2 ⫽ 247 days (0.68 years); and this species, as in its much larger rel-
utans),46 Palaeopropithecus ingens M3 ⬎ 135 days (⬎0.37 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 Museum 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
14342A) shows cut marks just above the medial epicondyle. The orientation and
of forty-three cuts, all of which show
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 charcoal 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 ⫾ 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 megafaunas 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 mammal 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. Mahé 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 climate changes that led to ecosystem 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-
livestock 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 grasslands 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 dogs and cats, new impacts
millennium to colonize the more humid creasingly dry and uncertain climates 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 Holocene. 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 ecosystems 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 biodiversity crisis
evidence has been found to support no return. in Madagascar.262 Godfrey and Jungers ARTICLES
Palaeopropithecus; surely this giant Madagascar composée par le Sieur de Flacourt, 2 lemur (Palaeopropithecidae) from Northwest
vols. Paris: Chez G. de Lvyne. Madagascar.
sloth lemur would not have been able
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 (Série II):81–87.
strange animals from Belo-sur-mer, Madagascar, 24 Simons EL, Godfrey LR, Jungers WL, Cha-
tre” or Gabriel Ferrand’s67,68 flat-faced trath PS, Ravaoarisoa J. 1995. A new species of
and the megafaunal “extinction window.” Am
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
géographique des principales rivières de la côte 16:653–682.
that in the two thousand years since
sud-est et annonçant la découverte 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 Géogr Paris, nov.– déc. 1868: Acad Malgache 2:227–235.
bore witness to some of the most re- 508 –510. 26 Godfrey LR, Jungers WL. 2002. Quaternary
6 Grandidier A. 1868. Sur des découvertes fossil lemurs. In: Hartwig WC, editor. The pri-
markable primates ever to have mate fossil record. New York: Cambridge Univer-
zoologiques faites récemment à Madagascar (de-
evolved: Madagascar’s giant sloth le- scription d’un hippopotame nouveau, de tortues sity Press, p 97–122.
murs. colossales et d’une espèce de Chirogale). C R Acad 27 Grandidier G. 1901. Un nouvel édenté 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’Archéologie (Série 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 mammifères contemporains des Aepyornis à 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
14. importanza ecologica e filletica nei Lemuri fossili
tributed to the recovery of fossils, ed attuali. Studi sulla paleobiologia e sulla filo-
9 Grandidier G. 1899. Description d’ossements
data and ideas embodied in our re- de lémuriens 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.
30 Carleton A. 1936. The limb-bones and verte-
Box contributors Elwyn Simons (Duke 10 Standing H-F. 1905. Rapport sur des ossements
brae of the extinct lemurs of Madagascar. Proc
University), Gary Schwartz (Northern sub-fossiles provenant d’Ampasambazimba. Bull
Zool Soc Lond 106:281–307.
Acad Malgache 4:95–100.
Illinois University), Ventura Perez (Uni- 11 Standing H-F. 1909. Subfossiles provenant
31 Vuillaume-Randriamanantena M. 1988. The
versity of Massachusetts, Amherst), taxonomic attributions of giant subfossil lemur
des fouilles d’Ampasambazimba. Bull Acad Mal-
bones from Ampasambazimba: Archaeoindris
David Burney (Fordham University) gache 6:9 –11.
and Lemuridotherium. J Hum Evol 17:379 –391.
and Malgosia Nowak-Kemp (Oxford 12 Standing H-F. 1910. Note sur les ossements
32 Standing H-F. 1913. Procès-verbal de la sé-
subfossiles provenant des fouilles d’Ampasam-
University Museum of Natural His- ance du 28 novembre 1912. (Reported by M. Fon-
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 à la con-
33 Lamberton C. 1939. Contribution à la con-
Mark Hamrick, Karen Samonds, Gina naissance de la faune subfossile de Madagascar. naissance de la faune subfossile de Madagascar:
Lémuriens et Ratites. L’Archaeoindris fon-
Semprebon, Liza Shapiro, Ian Tatter- toynonti Stand. Mém Acad Malgache 17:9 –39.
Lémuriens et cryptoproctes. Note VI. Des os du
pied de quelques lémuriens subfossiles mal-
sall, Mark Teaford, Martine Vuillaume- 14 Lamberton C. 1936. Nouveaux lémuriens fos- gaches. Mém Acad Malgache 27:75–139.
Randriamanantena, Alan Walker, and siles du groupe des Propithèques et l’intérêt de 34 Lamberton C. 1947. Contribution à la con-
Roshna Wunderlich. We are indebted leur découverte. Bull Mus Natl Hist Nat Paris naissance de la faune subfossile de Madagascar.
(2ème Série) 8:370 –373. Note XVI. Bradytherium ou Palaeopropithèque?
to our colleagues and friends in Mada-
15 Tattersall I. 1971. Revision of the subfossil Bull Acad Malgache (nouv série) 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 lémuriens fos-
These include Gisèle Randria, Berthe d’Andranoboka. Travaux du Bureau Géologique silles et actuels. Bull Acad Malgache (nouv série)
Numéro 43. Antananarivo: Service Géologique. 34:51–65.
Rakotosamimanana, Armand Ra-
17 Mahé J. 1965. Un gisement nouveau de sub- 36 Sera GL. 1950. Ulteriori osservazioni sui le-
soamiaramanana, and Benjamin Andri- fossiles à Madagascar. C R Sommaire des Sé- muri fossili ed attuali Significato di alcuni carat-
amihaja. We greatly appreciate com- ances de la Société Géologique 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 à 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. pithèques et des Mesopropithèques. Bull Acad
19 Simons EL, Godfrey LR, Jungers WL, Cha- Malgache (nouv série) 27:30 –32.
This work was supported in part by NSF
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SBR-0001429, and SBR-963350. tion of the sloth lemurs. Folia Primatol 58:197– dissertation, University of London.
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