Subfossil lemur
Encyclopedia
Subfossil lemurs are lemur
s from Madagascar
that are represented by recent (subfossil
) remains dating from nearly 26,000 years ago (during the late Pleistocene
) to approximately 560 years ago. They include both living and extinct
species, although the term more frequently refers to the extinct giant lemurs. The diversity of subfossil lemur communities was greater than that of present-day lemur communities, ranging from as high as 20 or more species per location, compared with 10 to 12 species today. Extinct species are estimated to have ranged in size from slightly over 10 kg (22 lb) to roughly 200 kg (440.9 lb). Even the subfossil remains of living species are larger and more robust than the skeletal remains of modern specimens. The subfossil sites found around most of the island demonstrate that most giant lemurs had wide distributions and that ranges of living species have contracted significantly since the arrival of humans.
Despite their size, the giant lemurs shared many features with living lemurs, including rapid development, poor day vision, relatively small brains, and lack of male dominance. They also had many distinct traits among lemurs, including a tendency to rely on terrestrial locomotion, slow climbing, and suspension
instead of leaping, as well as a greater dependence on leaf-eating
and seed predation. The giant lemurs likely filled ecological niche
s now left vacant, particularly seed dispersal
for plants with large seeds. There were three distinct families of giant lemur, including the Palaeopropithecidae (sloth lemurs), Megaladapidae (koala lemurs), and Archaeolemuridae (monkey lemur
s). Two other types were more closely related and similar in appearance to living lemurs: the giant aye-aye
and Pachylemur
, a genus
of "giant ruffed lemur
s".
Subfossil remains were first discovered on Madagascar in the 1860s, but giant lemur species were not formally described until the 1890s. The paleontological
interest sparked by the initial discoveries resulted in an overabundance of new species names, the allocation of bones to the wrong species, and inaccurate reconstructions during the early 20th century. Discoveries waned during the mid-20th century, although paleontological work resumed in the 1980s and resulted in the discovery of new species and a new genus. Research has recently focused on diets, lifestyle, social behavior, and other aspects of biology. The remains of the subfossil lemurs are relatively recent, with all or most species dating within the last 2,000 years. Humans first arrived on Madagascar around that time and likely played a role in the demise of the lemurs and the other megafauna
that once existed on the large island. Although hunting and habitat change have been investigated as the primary cause of their extinction, a mosaic of complex interactions between multiple factors is now seen as the ultimate cause of their disappearance. Yet oral tradition
s and recent sightings by Malagasy villagers are still reported, suggesting either lingering populations or very recent extinctions.
(Indri indri) and diademed sifaka
(Propithecus diadema), which weigh up to 9.5 kg (20.9 lb). The estimated weights for the subfossil lemurs have varied. Techniques used for these weight estimations include the comparison of skull lengths, tooth size, the head diameter of the femur
, and more recently, the area of cortical bone
(hard bone) in long bone
s (such as the humerus
). Despite the variations in the size estimates for some species, all subfossil lemurs were larger than living species, weighing 10 kg (22 lb) or more, and one species may have weighed as much as 200 kg (440.9 lb).
All but one species, the giant aye-aye
, are thought to have been active during the day. Not only were they unlike the living lemurs in both size and appearance, they also filled ecological niche
s that no longer exist or are now left unoccupied. Their remains have been found in most parts of the island, except for the eastern rainforests and the Sambirano domain (seasonal moist forests in the northwest of the island), where no subfossil sites are known. Radiocarbon dates
for subfossil lemur remains range from approximately 26,000 years BP
(for Megaladapis
in northern Madagascar at the Ankarana Massif
) to around 500 years BP (for Palaeopropithecus in the southwest).
, Mesopropithecus
, and the giant aye-aye), were larger than the lemur species alive today. The largest species were among the largest primate
s ever to have evolved. Due to their larger size, the extinct subfossil lemurs have been compared to large-bodied anthropoids
(monkeys and apes), yet they more closely resemble the small-bodied lemurs. Like other lemurs, the subfossil lemurs did not exhibit appreciable differences in body or canine tooth
size between males and females (sexual dimorphism
). This suggests that they, too, either exhibited female social dominance or lacked male dominance, possibly exhibiting the same levels of agonism
(aggressive competition) seen in extant lemurs. Like other lemurs, they had smaller brains than comparably sized anthropoids. Most species also had a unique strepsirrhine dental trait, called a toothcomb
, which is used for grooming
. Even tooth development
and weaning
was rapid compared to similarly sized anthropoids, suggesting faster sexual maturity
of their offspring. Most subfossil lemurs also had high retinal summation
(sensitivity to low light), resulting in poor day vision (low visual acuity
) compared to anthropoids. This has been demonstrated by the ratio between their relatively small orbits
(eye sockets) and the relative size of their optic canal, which is comparable to that of other lemurs, not diurnal anthropoids.
Although these traits are shared among both living and extinct lemurs, they are uncommon among primates in general. Two prevailing hypotheses to explain these unique adaptations are the energy frugality hypothesis by Patricia Wright
(1999) and the evolutionary disequilibrium hypothesis by Carel van Schaik and Peter M. Kappeler (1996). The energy frugality hypothesis expanded on Alison Jolly
's energy conservation hypotheses by claiming that most lemur traits not only help conserve energy, but also maximize the use of highly limited resources, enabling them to live in severely seasonal environments with low productivity. The evolutionary disequilibrium hypothesis postulated that living lemurs are in the process of evolving to fill open ecological niches left by the recently extinct subfossil lemurs. For example, small nocturnal prosimians are typically nocturnal and monogamous, while the larger living lemurs are generally active both day and night (cathemeral
) and live in small groups (gregarious
). Cathemerality and increased gregariousness might indicate that the larger living lemurs are evolving to fill the role of the giant lemurs, which were thought to be diurnal (day-living) and more monkey-like in behavior. Since most giant subfossil lemurs have been shown to share many of the unique traits of their living counterparts, and not those of monkey
s, Godfrey et al. (2003) argued that the energy frugality hypothesis seems to best explain both living and extinct lemur adaptations.
Despite the similarities, subfossil lemurs had several distinct differences from their lemur relatives. In addition to being larger, the subfossil lemurs were more dependent on leaves and seeds in their diet, rather than fruit. They utilized slow climbing, hanging, and terrestrial quadrupedalism for locomotion, rather than vertical clinging and leaping
and arboreal
quadrupedalism. Also, all but one of them—the giant aye-aye—are assumed to have been diurnal (due to their body size and small orbits
), whereas many small lemurs are nocturnal and medium-sized are cathemeral.
Their skeletons suggest that most subfossil lemurs were tree-dwellers, adapted for living in forests and possibly limited to such habitats. Unlike some of the living species, the subfossil lemurs lacked adaptations for leaping. Instead, suspension
, used by some indriids
and ruffed lemur
s, was extensively used in some lineages. Although living lemurs are known to visit the ground to varying extents, only the extinct archaeolemurids exhibit adaptations for semiterrestrial locomotion. Due to the size of the extinct subfossil lemurs, all were likely to travel on the ground between trees. They had shorter, more robust limbs, heavily built axial skeleton
s (trunks), and large heads and are thought to have shared the common lemur trait of low basal metabolic rate
s, making them slow-moving. Studies of their semicircular canals confirm this assumption, showing that koala lemurs moved slower than orangutans, monkey lemurs were less agile than Old World monkey
s, and sloth lemurs exhibited slow movements like those of lorises and sloths.
The sloth lemurs (family
Palaeopropithecidae) were the most species-rich group of the subfossil lemurs, with four genera and eight species. The common name
is due to strong similarities in morphology
with arboreal sloths, or in the case of Archaeoindris
, with giant ground sloths. They ranged in size from some of the smallest of the subfossil lemurs, such as Mesopropithecus
, weighing as little as 10 kg (22 lb), to the largest, Archaeoindris
, weighing approximately 200 kg (440.9 lb). Their characteristic curved finger and toe bones (phalanges
) suggest slow suspensory movement, similar to that of an orangutan
or a loris
, making them some of the most specialized mammals for suspension
. Their day vision was very poor, and they had relatively small brains and short tails. Their diet consisted mostly of leaves, seeds, and fruit, although dental wear analysis suggests they were primarily folivorous seed-predators.
Koala lemurs
The koala lemurs of the family Megaladapidae most closely resemble marsupial
koalas from Australia. According to genetic evidence they were most closely related to the family Lemuridae
, although for many years they were paired with the sportive lemur
s of the family Lepilemuridae due to similarities in their skulls and molar teeth
. They were slow climbers and had long forelimbs and powerful grasping feet, possibly using them for suspension. Koala lemurs ranged in size from an estimated 45 to 85 kg (99.2 to 187.4 lb), making them as large as a male orangutan or a female gorilla. They had poor day vision, short tails, lacked permanent upper incisor
s, and had a reduced toothcomb. Their diet generally consisted of leaves, with some species being specialized folivore
s and others having a broader diet, possibly including tough seeds.
Monkey lemur
s
Monkey lemurs, or baboon lemurs, share similarities with macaque
s, although they have also been compared to baboon
s. Members of the family Archaeolemuridae, they were the most terrestrial of the lemurs, with short, robust forelimbs and relatively flat digits. Although they spent a lot of time on the ground, they were only semi-terrestrial, spending time in trees to feed and sleep. They were heavy-bodied and ranged in size from approximately 13 to 35 kg (28.7 to 77.2 lb). They had relatively good day vision and large brains compared with other lemurs. Their robust jaws and specialized teeth suggest a diet of hard objects, such as nuts and seeds, yet other evidence, including fecal pellets, suggests they may have had a more varied diet, including leaves, fruit, and animal matter (omnivory
). Dental wear analysis has shed some light on this dietary mystery, suggesting that monkey lemurs had a more eclectic diet, while using tough seeds as a fall-back food item. Within the family, the genus Archaeolemur was the most widespread in distribution, resulting in hundreds of subfossil specimens, and may have been one of the last subfossil lemurs to die out.
Giant aye-aye
An extinct, giant relative of the living aye-aye
, the giant aye-aye shared at least two of the aye-aye's bizarre traits: ever-growing central incisors and an elongated, skinny middle finger. These shared featured suggest a similar lifestyle and diet, focused on percussive foraging (tapping with the skinny digit and listening for reverberation from hollow spots) of defended resources, such as hard nuts and invertebrate larvae concealed inside decaying wood. Weighing as much as 14 kg (30.9 lb), it was between two-and-half and five times the size of living aye-aye. Alive when humans came to Madagascar, its teeth were collected and drilled to make necklaces.
Pachylemur
The only extinct member of the family Lemuridae, the genus Pachylemur contains two species that closely resembled living ruffed lemurs. Sometimes referred to as "giant ruffed lemurs", they were approximately three times larger than ruffed lemurs, weighing between 10 and 13 kg (22 and 28.7 lb). Despite their size, they were arboreal quadrupeds, possibly utilizing more suspensory behavior and cautious climbing than their sister taxon. Their skull and teeth were similar to those of ruffed lemurs, suggesting a diet high in fruit and possibly some leaves. The rest of its skeleton (postcrania
) was much more robust and their vertebrae had distinctly different features.
of subfossil lemurs has been problematic because studies of morphology
, developmental biology
, and molecular phylogenetics have sometimes yielded conflicting results. All studies agree that the family Daubentoniidae (including the giant aye-aye) diverged first from the other lemurs at least 60 million years ago. The relationship between the remaining families has been less clear. Morphological, developmental, and molecular studies have offered support for lumping the four sloth lemur genera of the family Palaeopropithecidae with the family Indriidae
(including the indri, sifakas, and woolly lemur
s). The placement of family Megaladapidae has been more controversial, with similarities in teeth and skull features suggesting a close relationship with family Lepilemuridae (sportive lemur
s). Molecular data, instead, indicate a closer relationship to family Lemuridae. Likewise, a relationship between family Archaeolemuridae and family Lemuridae has been suggested, based on morphological and developmental traits, yet molar morphology, the number of teeth in the specialized toothcomb, and molecular analysis support a closer relationship with the indriid–sloth lemur clade
. Other subfossil lemurs, including the giant aye-aye and Pachylemur, are more easily placed due to strong similarities with existing lemurs (the aye-aye and ruffed lemurs, respectively).
for the area in which their subfossil remains were found. Because subfossil sites are found across most of the island, with the most notable exception being the eastern rainforest, both paleocommunity composition and paleodistributions can be determined. Geographic range
s have contracted for numerous species, including the indri, greater bamboo lemur
, and ruffed lemurs. For instance, subfossil remains of the indri have been found in marsh deposits near Ampasambazimba in the Central Highlands
and in other deposits in both central and northern Madagascar, demonstrating a much larger range than the small region on the east coast that it currently occupies. Even the greater bamboo lemur, a critically endangered species restricted to a small portion of the south-central eastern rainforest, has undergone significant range contraction since the mid-Holocene
, with subfossil remains from Ankarana Massif
in the far north of Madagascar dating to 2565 BCE
± 70 years. Combined with finds from other subfossil sites, data suggests that it used to range across the northern, northwestern, central, and eastern parts of the island. It is unclear whether these locations were wetter
in the past or whether distinct subpopulations or subspecies
occupied the drier forests, much like modern diversity of sifaka
s.
In addition to previously having expanded geographic ranges, extant subfossil lemurs exhibited significant variation in size. Researchers have noted that subfossil bones of living species are more robust and generally larger than their present-day counterparts. The relative size of living species may be related to regional ecological factors, such as resource seasonality, a trend that is still observable today, where individuals from the spiny forests
are, on average, smaller than individuals from the southwestern succulent woodlands or the dry deciduous forests
.
over the past 40 to 60 million years to fill many ecological niche
s normally occupied by other primates. In the recent past, their diversity was significantly greater, with 17 extinct species sharing body proportions and specializations with loris
es and various non-primates, such as tree sloth
s, giant ground sloth
s, koala
s, and striped possums (genus Dactylopsila
). Although the diversity of lemur communities today can be as high as 10 to 12 species per region, communities of 20 or more lemur species existed as recently as 1,000 years ago in areas that now have no lemurs at all. Just like living species, many of the extinct species shared overlapping ranges with closely related species (sympatry
) through niche differentiation
(resource partitioning). Among all the late Quaternary
assemblages of megafauna
, only Madagascar was dominated by large primates.
Although anatomical evidence suggests that even the large, extinct species were adapted to tree-climbing, some habitats, including gallery forest
s and the spiny forests of southern Madagascar, in which they occurred would not have allowed them to be strictly arboreal. Even today, most lemur species will visit the ground to cross open areas, suggesting that the extinct species did the same. Monkey lemurs (family Archaeolemuridae), including Archaeolemur majori
and Hadropithecus stenognathus
, have been reconstructed as being primarily terrestrial
. In contrast, the sloth lemurs (family Palaeopropithecidae) were highly arboreal despite the large size of some species.
Species of both extinct and living (extant) lemur vary in size based on habitat conditions, despite their differences in niche preference. Within related groups, larger species tend to inhabit wetter, more productive habitat
s, while smaller sister taxa are found in drier, less productive habitats. This pattern suggests that populations of both living and extinct lemur species had become geographically isolated by differences in habitat and evolved in isolation
due to varying primary production
within different ecosystem
s. Thermoregulation
may also have played a role in the evolution of their increased body size. Yet despite this pressure to specialize and differentiate, some of the extinct subfossil lemurs, such as Archaeolemur, may have had island-wide distributions during the Holocene, unlike the living lemurs. If this is the case, it may suggest that some larger lemurs might have been more tolerant to regional differences in ecology than living lemurs.
s), seed predators, or both. Today, leaf-eating along with seed predation is only seen in mid-sized lemurs, and is far less common than it was in the past. Strict folivory is also less common, now found primarily in small lemurs. In certain cases, subfossil lemurs, such as the sloth lemurs and koala lemurs, may have used leaves as an important fallback food, whereas other species, such as the monkey lemurs and the giant aye-aye, specialized on structurally defended resources, such as hard seeds and wood-boring insect larvae. Last, Pachylemur was primarily a fruit eater (frugivorous
). Subfossil lemur diets have been reconstructed using analytical tools, including techniques to compare tooth anatomy, structure, and wear; biogeochemistry
(analysis of isotope
levels, like carbon-13
); and the dissection of fecal pellets
associated with subfossil remains.
The diets of most subfossil lemurs, most notably Palaeopropithecus and Megaladapis, consisted primarily of C3 plants
, which use a form of photosynthesis
that results in higher water loss through transpiration
. Other subfossil lemurs, such as Hadropithecus and Mesopropithecus, fed on CAM
and C4 plants
, which use more water-efficient forms of photosynthesis. Fruit
and animal matter was more common in the diets of subfossil lemurs including Pachylemur, Archaeolemur, and the giant aye-aye. In southern and southwestern Madagascar, the subfossil lemurs of the spiny forests generally favored the C3 plants over the more abundant CAM plants, although closely related sympatric species may have fed upon the two types of plants in different ratios, allowing each to divide resources and coexist. Since plants produce defenses against leaf-eating animals, the extensive use of spines by plants in the spiny forests suggest that they evolved to cope with leaf-eating lemurs, large and small.
, possibly targeting species that did not attract the seed dispersal services of the extinct elephant bird
s. Biogeochemistry studies have shown that they may have been the primary seed dispersers for the endemic and native C3 trees in the spiny forests. Terrestrial species may even have dispersed seeds for small bushes in addition to tall trees. Seed dispersal can involve passing seeds through the gut (endozoochory) or attaching the seeds to the animal's body (epizoochory), and both processes probably occurred with subfossil lemurs. Seeds from Uncarina
species embed themselves in lemur fur, and likely did the same with subfossil lemurs. Seed dispersal biology is known for very few species in the spiny forest, including genera
of plants suspected of depending on giant lemurs, such as Adansonia
, Cedrelopsis
, Commiphora
, Delonix
, Diospyros
, Grewia
, Pachypodium
, Salvadora, Strychnos
, and Tamarind
us. For example, Delonix has edible pods that are rich in protein, and Adansonia fruits have a nutritious pulp and large seeds that may have been dispersed by Archaeolemur majori or Pachylemur insignis.
Seed size may be a limiting factor for some plant species, since their seeds are too large for living (extant) lemurs. The common brown lemur (Eulemur fulvus) can swallow seeds 20 mm (0.78740157480315 in) in diameter, while the black-and-white ruffed lemur
(Varecia variegata) is capable of swallowing seeds up to 30 mm (1.2 in) in diameter. A large lemur, such as Pachylemur, which was more than twice the size of today's ruffed lemur
s, could probably swallow even larger seeds. Seed dispersal limitations tied to megafaunal extinction are exhibited by Commiphora guillaminii. At present, this tree species has a short dispersal distance, but its genetics
indicate higher levels of regional gene flow
in the past, based on comparisons with a closely related species in Africa that still has its seeds dispersed by large animals.
in the mid-17th century introduced the existence of giant Malagasy mammals to Western science with recorded eye-witness accounts from the local people of dangerous animals, hornless "water cows", and a large lemur-like creature referred to locally as the tretretretre or tratratratra. Today, the latter is thought to have been a species of Palaeopropithecus or possibly Megaladapis. Flacourt described it as:
Local tales of a song'aomby (Malagasy for "cow that is not a cow"), or pygmy hippopotamus, led French naturalist Alfred Grandidier
to follow a village headman to a marsh in southwestern Madagascar, a site called Ambolisatra, which became the first known subfossil site in Madagascar. In 1868, Grandidier uncovered the first subfossil remains of lemurs—a humerus
from Palaeopropithecus and a tibia
of a sifaka. The Palaeopropithecus remains were not described for several decades, and it took decades more for the remains to be correctly paired with other sloth lemur remains. It was not until 1893 that giant lemur species were formally described, when Charles Immanuel Forsyth Major
discovered and described a long, narrow skull of Megaladapis madagascariensis in a marsh. His discoveries in various marshes of central and southwestern Madagascar sparked paleontological
interest, resulting in an overabundance of taxonomic names
and confused assemblages of bones from numerous species, including non-primates. Specimens were distributed between European museums and Madagascar, often resulting in the loss of field data that went with the specimens, if the data had been recorded at all.
In 1905, Alfred Grandidier's son, Guillaume Grandidier
, reviewed subfossil lemur taxonomy and determined that too many names had been created. His review established most of the presently known family and genera names for the extinct lemurs. Despite the taxonomic clarification, subfossil postcrania from different genera, particularly Megaladapis, Palaeopropithecus and Hadropithecus, continued to be incorrectly paired and sometimes assigned to non-primates. Since subfossil remains were often dredged from marshes one by one, pairing skulls with other bones was often guesswork based on size-matching, and was not very accurate as a consequence. Even as late as the 1950s, bones of non-primates were attributed to subfossil lemurs. One reconstruction of the confounded subfossil remains by paleontologist Herbert F. Standing depicted Palaeopropithecus as an aquatic animal that swam near the surface, keeping its eyes, ears, and nostrils slightly above water. Postcranial remains of Palaeopropithecus had previously been paired with Megaladapis by Guillaume Grandidier, who viewed it as a giant tree sloth, which he named Bradytherium. Standing's aquatic theory was supported by Italian paleontologist Guiseppe Sera, who reconstructed Palaeopropithecus as an "arboreal-aquatic acrobat" that not only swam in water but climbed trees and dove from there into the water. Sera took the aquatic theory further in 1938 by including other extinct lemurs, including Megaladapis, which he viewed as a thin ray
-like swimmer that fed on mollusks and crustaceans while concealed underwater. It was primarily the paleontologist Charles Lamberton who correctly paired many of the confused subfossils, although others had also helped address problems of association and taxonomic synonyms
. Lamberton also refuted Guillaume Grandidier's sloth theory for Megaladapis, as well as the aquatic lemur theory of Standing and Sera.
Excavations during the early 20th century by researchers like Lamberton failed to unearth any new extinct lemur genera. Fourteen of the approximately seventeen known species had previously been identified from field work in southern, western, and central Madagascar. When paleontological field work resumed in the early 1980s, new finds provided associated skeletal remains, including rare bones such as carpal bones
(wrist bones), phalanges
(finger and toe bones), and bacula
(penile bone). In some cases, nearly complete hands and feet were found. Enough remains have been found for some groups to demonstrate the physical development
of juveniles. Standard long-bone indices have been calculated in order to determine the intermembral index (a ratio that compares limb proportions), and body mass estimates have been made based on long-bone circumference measurements. Even preserved fecal pellets
from Archaeolemur have been found, allowing researchers to learn about its diet. More recently, electron microscopy
has allowed researchers to study behavioral patterns, and DNA amplification
has helped with genetic tests that determine the phylogenetic relationships between the extinct and living lemurs.
A new genus of sloth lemur, Babakotia
, was discovered in 1986 by a team led by Elwyn Simons of Duke University
in karst
caves on the Ankarana Massif in northern Madagascar. Along with Babakotia, a new species of Mesopropithecus, M. dolichobrachion, was also discovered, but not formally described until 1995. The same team has also helped promote new ideas about sloth lemur adaptations and the relationships among the four genera. They have also provided evidence that living species, such as the indri and the greater gamboo lemur, have lost much of their original range. In 2009, a new species of large sloth lemur, called Palaeopropithecus kelyus, was described from northwestern Madagascar by a Franco-Madagascan team. The new species was found to be smaller than the two previously known species from the genus, and its diet reportedly consisted of more hard-textured food. The resurgence in subfossil lemur work has also sparked new interest in Madagascar's small mammals, which have also been found at the subfossil sites. This has led to new ideas about the origins, diversity, and distribution of these animals.
The number of Malagasy subfossil sites containing subfossil lemurs has increased significantly since the mid-20th century. At that time, subfossil lemurs had only been found in the center, south, and southwest of the island. Since then, only the eastern rainforests have not been represented, and paleodistributions are now known for both extinct and living species around most of the island. Large quantities of subfossil lemur remains have been found in caves, marshes, and streambank sites in drier regions. The subfossil sites are clustered together geographically and are recent in age, mostly dating between 2,500 and 1,000 years old, with a few spanning back into the last glaciation, which ended approximately 10,000 years ago.
included not only giant lemurs, but also elephant bird
s, giant tortoise
s, several species of Malagasy hippopotamus
es, Cryptoprocta spelea
(a "giant Fossa
"), large crocodiles (Voay robustus
), and Plesiorycteropus
, a unique digging mammal, all of which died out during the same period. Madagascar's megafaunal extinctions were among the most severe for any continent or large island, with all endemic wildlife over 10 kg (22 lb) disappearing, totaling approximately 25 species. The most severely impacted lemurs were generally large and diurnal, particularly the clade containing the living indriids and extinct sloth lemurs. Although only the indriids are alive today and represent only a small percentage of the living lemur species, this clade collectively contained the majority of the extinct giant lemur species.
By region, the Central Highlands lost the greatest number of lemur species. Although it has lost nearly all of its woodland habitat, some lemur species still survive in isolated forest patches. Lemur diversity is tightly linked with plant diversity, which in turn decreases with increased forest fragmentation
. In extreme cases, treeless sites such as the town of Ampasambazimba from the central region no longer support any of the lemur species represented in their subfossil record. However, other locations no longer have giant subfossil lemurs, yet they still maintain forested habitat that could support them. Even though the giant lemurs have disappeared from these locations, while the smaller species survive in the forest patches that remain, the subfossil remains indicate that the living species used to be more widespread and coexisted with the extinct species. Although the Central Highlands saw the greatest species loss, it was not the only region or habitat type to witness extinctions. However, the least-understood region is the eastern rainforests, which have not yielded subfossil lemur remains. Consequently, it is impossible to know what percentage of lemur taxa were recently lost there, although studies of Malagasy customs (ethnohistory
) along with archaeological evidence suggests the eastern rainforests were more ecologically disturbed in the past than they are today. Hunting and trapping by humans may have severely impacted large lemurs in this region as well.
Comparisons of species counts from subfossil deposits and remnant populations in neighboring Special Reserves has further demonstrated decreased diversity in lemur communities and contracted geographic ranges. At Ampasambazimba in central Madagascar, 20 species of subfossil lemur have been found. At nearby Ambohitantely Reserve
, only 20% of those species still survive. Only six of 13 species found at Ankilitelo and Ankomaka Caves in the southwest still survive at Beza Mahafaly Reserve
. In the extreme north, the caves of Ankarana have yielded 19 species, yet only nine remain in the surrounding forests. In the northwest, 10 or 11 subfossil species have been found at Anjohibe, whereas only six species remain at nearby Ankarafantsika National Park
.
As with the extinctions that occurred on other land masses during the late Pleistocene and Holocene (known as the Quaternary extinction event
), the disappearance of Madagascar's megafauna is tightly linked with the arrival of humans, with nearly all extinctions dating to around the same time of the earliest evidence of human activity on the island or significantly later. The exact date of human arrival is unknown, although a radius
(arm bone) of a Palaeopropithecus ingens with distinct cut marks from the removal of flesh with sharp objects dates to approximately 2325 ± 43 BP (2366–2315 cal yr BP). Based on this evidence from Taolambiby in the southwest interior, as well as other dates for human-modified dwarf hippo bones and introduced plant pollen from other parts of the island, the arrival of humans is conservatively estimated at approximately 350 cal yr BCE. Measurements of stratigraphic charcoal
and the appearance of exotic plant pollen dated from Holocene core sample
s confirm these approximated dates for human arrival in the southwestern corner of the island and further suggest that the central and northern parts of the island did not experience significant human impact until 700 to 1,500 years later. The humid forests of the lower interior of the island were the last to be settled (as shown by the presence of charcoal particles), possibly due to the prevalence of human diseases, such as plague, malaria
, and dysentery
. The entire island was not fully colonized by humans until the beginning of the second millennium CE.
The extinction of Madagascar's megafauna, including the giant lemurs, was one of the most recent in history, with large lemur species like Palaeopropithecus ingens surviving until approximately 500 years ago and one bone of the extinct Hippopotamus laloumena radiocarbon dated
to about 100 years BP An even wider extinction window for the subfossil lemurs, ranging up until the 20th century, may be possible if reports of unidentified animals are true. As recently as the early 17th century, dwindling populations of subfossil lemurs may have persisted in coastal regions where tree-cutting and uncontrolled fires had less of an impact. By that date, the Central Highlands' forests were mostly gone, with the exception of scattered forest fragments and strips. Along the northwest coast, forms such as Archaeolemur may have survived for more than a millennium after the arrival of humans. This is supported by radiocarbon dates for Archaeolemur from the Ankarana Massif dating to 975 ± 50 CE as well as archaeological data that show there was little human activity in the area until a few centuries ago, with low human population density along the northwest coast until nearly 1500 CE.
livestock outcompeted the endemic wildlife in a moderately fast series of multiple waves across the island. In 1997, MacPhee and Marx speculated that a rapid spread of hypervirulent
disease might explain the die-offs that occurred after the appearance of humans worldwide, including Madagascar. Finally, in 1999, David Burney proposed that the complete set of human impacts worked together, in some cases along with natural climate change, and very slowly brought about the demise of the giant subfossil lemurs and other recently extinct endemic wildlife.
Since all extinct lemurs were larger than the ones that currently survive, and the remaining large forests still support large populations of smaller lemurs, large size appears to have conveyed some distinct disadvantages. Large-bodied animals require larger habitats in order to maintain viable populations, and are most strongly impacted by habitat loss and fragmentation
. Large folivores typically have slower reproductive rates, live in smaller groups, and have low dispersal rates (vagility), making them especially vulnerable to habitat loss, hunting pressure, and possibly disease. Large, slow-moving animals are often easier to hunt and provide a larger amount of food than smaller prey. Furthermore, leaf-eating, large-bodied slow climbers, and semiterrestrial seed predators and omnivores disappeared completely, suggesting an extinction pattern based on habitat use.
Since the subfossil bones of extinct lemurs have been found alongside the remains of highly arboreal living lemur species, we know that much of Madagascar had been covered in forest prior to the arrival of humans; however, the forest coverage of the high plateau region has been debated. Humbert and other botanists suggested that the central plateau had once been blanketed in forest, later to be destroyed by fire for use by humans. However, recent paleoenvironmental studies by Burney have shown that the grasslands of that region have fluctuated over the course of millennia and were not entirely created by humans. Similarly, the role humans played in the aridification of the south and southwest has been questioned, since natural drying of the climate started before human arrival. The marshes of the region (in which subfossil remains have been found) have dried up, subfossil sites have yielded a host of arboreal lemurs, and site names, such as Ankilitelo ("place of three kily or tamarind trees
") suggest a recent wetter past. Pollen studies have shown that the aridification process began nearly 3,000 years ago, and peaked 1,000 years prior to the time of the extinctions. However, no extinctions occurred prior to the arrival of humans, and the recent climatic changes have not been as severe as those prior to human arrival, suggesting that humans and their effect on the vegetation did play a role in the extinctions. The central plateau lost more species than the dry south and southwest, suggesting that degraded habitats were more affected than arid habitats.
Over-hunting by humans has been one of the most widely accepted hypotheses for the ultimate demise of the subfossil lemurs. The extinctions and human hunting pressure are associated due to the synchronicity of human arrival and species decline, as well as the suspected naïveté of the Malagasy wildlife during the early encounters with human hunters. Despite the assumptions, evidence of butchery has been minimal until recently, although folk memories of rituals associated with the killing of megafauna have been reported. Archeological evidence for butchery of giant subfossil lemurs, including Palaeopropithecus ingens and Pachylemur insignis, was found on specimens from two sites in southwestern Madagascar, Taolambiby and Tsirave. Although the bones had been collected in the early 20th century and lacked stratigraphic records, one of the bones with tool marks had been dated to the time of the first arrival of humans. Tool-induced bone alterations, in the form of cuts and chop marks near joints and other characteristic cuts and fractures, indicated the early human settlers skinned, disarticulated, and filleted giant lemurs. Prior to these finds, only modified bones of dwarf hippos and elephant birds, as well as giant aye-aye teeth, had been found.
Although there is evidence that habitat loss, hunting, and other factors played a role in the demise of the subfossil lemurs, prior to the synergy hypothesis, each had its own discrepancies. Humans may have hunted the giant lemurs for food, but no signs of game-dependent butchery have been found. In fact, Madagascar was colonized by Iron-age pastoralists, horticulturalists, and fishermen, not big-game hunters. Additionally, the blitzkrieg hypothesis predicts extinction within 100 and 1,000 years as humans sweep across the island, yet humans lived alongside the giant lemurs for more than 1,500 years. Alternatively, habitat loss and deforestation have been argued against because many giant lemurs were thought to be terrestrial, they are missing from undisturbed forested habitats, and their environment was not fully forested prior to the arrival of humans. Anthropologist Laurie Godfrey defended the effects of habitat loss by pointing out that most of the extinct lemurs have been shown to have been at least partly arboreal and dependent upon leaves and seeds for food, and also that these large-bodied specialists would be most vulnerable to habitat disturbance and fragmentation due to their low reproductive resilience and their need for large, undisturbed habitats. Still, much of the island remained covered in forest, even into the 20th century.
Linking human colonization to a specific cause for extinction has been difficult since human activities have varied from region to region. Although no single human activity can account for the extinction of the giant subfossil lemurs, the humans are still regarded as being primarily responsible. Each of the contributing human-caused factors played a role (having a synergistic effect
) in varying degrees. Even the most widespread and adaptable species, such as Archaeolemur, were able to survive despite hunting pressure and human-caused habitat change until human population growth and other factors reached a tipping point, cumulatively resulting in their extinction.
s of the coprophilous fungus
, Sporormiella
, found in sediment cores experienced a dramatic decline shortly after the arrival of humans. Since this fungus
cannot complete its life cycle without dung from large animals, its decline also indicates a sharp decline in giant subfossil lemur populations, as well as other large herbivores, starting around 230–410 cal yr CE. Following the decline of megafauna, the presence of charcoal particles increased significantly, starting in the southwest corner of the island, gradually spreading to the other coasts and the island's interior over the next 1,000 years. The first evidence for the introduction of cattle to the island dates to 1,000 years after the initial decline of coprophilous fungal spores.
The loss of grazers and browsers might have resulted in the accumulation of excessive plant material and litter, promoting more frequent and destructive wildfires, which would explain the rise in charcoal particles following the decline in coprophilous fungus spores. This in turn resulted in ecological restructuring through the elimination of the wooded savannas and preferred arboreal habits on which the giant subfossil lemurs depended. This left their populations at unsustainably low levels, and factors such as their slow reproduction, continued habitat degradation, increased competition with introduced species, and continued hunting (although at lower levels, depending on the region) prevented them from recovering and gradually resulted in their extinction.
Hunting is thought to have caused the initial rapid decline, referred to as the primary trigger, although other explanations may be plausible. In theory, habitat loss should affect frugivores more than folivores, since leaves are more widely available. However, both large-bodied frugivores and large-bodied folivores disappeared simultaneously, while smaller species remained. Furthermore, other large non-primate grazers also disappeared around the same time. Consequently, large body size has been shown to have the strongest link to the extinctions—more so than activity patterns or diet. Since large animals are more attractive as prey, fungal spores associated with their dung declined rapidly with the arrival of humans, and butchery marks have been found on giant subfossil lemur remains, hunting appears to be a plausible explanation for the initial decline of the megafauna.
By region, studies have revealed specific details that have helped outline the series of events that led to the extinction of the local megafauna. In the Central Highlands, dense forests existed until 1600 CE, with lingering patches persisting until the 19th and 20th centuries. Today, small fragments stand isolated among vast expanses of human-created savanna, despite an average annual rainfall that is sufficient to sustain the evergreen forests once found there. Deliberately set fires were the cause of the deforestation, and forest regrowth is restricted by soil erosion
and the presence of fire-resistant, exotic grasses. In the southeast, an extended drought dating to 950 cal yr BP led to fires and transition of open grasslands. The drought may also have pushed humans populations to rely more heavily on bushmeat
. Had humans not been present, the subfossil lemur populations might have adjusted to the new conditions and recovered. Had the drought not reduced the population of the subfossil lemurs, the pressure from the small number of people living in the region at the time might not have been enough to cause the extinctions. As in the past, all of the factors that have played a role in past extinctions are still present and active today. As a result, the extinction event that claimed Madagascar's giant subfossil lemurs has not fully concluded.
14C dating, such as 630 ± 50 BP for Megaladapis remains and 510 ± 80 BP for Palaeopropithecus remains, indicate that the giant lemurs survived into modern times. Moreover, it is likely that memories of these creatures persist in the oral tradition
s of some Malagasy cultural groups. Some recent stories from around Belo sur Mer
in southwestern Madagascar might even suggest that some of the giant subfossil lemurs still survive in remote forests.
Flacourt's 1658 description of the tretretretre or tratratratra was the first mention of the now extinct giant lemurs in Western culture, although it is unclear whether he saw it. The creature Flacourt described has traditionally been interpreted as a species of Megaladapis. However, the size may have been exaggerated, and the "round head and a human face" would not match Megaladapis, which had an enlarged snout and eyes that did not face entirely forward. In fact, Megaladapis had the least forward-facing eyes of all primates. The facial description, along with the mention of a short tail, solitary habits, and other traits better match the most recent interpretation—Palaeopropithecus. Likewise, Malagasy tales recorded by the 19th-century folklorist Gabriel Ferrand describing a large animal with a flat, human-like face that was unable to negotiate smooth, rock outcrops best match Palaeopropithecus, which would also have had difficulty on flat, smooth surfaces.
In 1995, a research team led by David Burney and Ramilisonina
performed interviews in and around Belo sur Mer, including Ambararata and Antsira, in order to locate subfossil megafaunal sites used early in the century by other paleontologists. During carefully controlled interviews, the team recorded stories of recent sightings of dwarf hippos (called kilopilopitsofy) and of a large, lemur-like creature known as kidoky; a report of the interviews was published in 1998 with encouragement from primatologist Alison Jolly
and anthropologist Laurie Godfrey. In one interview, an 85-year-old man named Jean Noelson Pascou recounted seeing the rare kidoky up close in 1952. Pascou said that the animal looks similar to a sifaka, but had a human-like face, and was "the size of a seven-year-old girl." It had dark fur and a discernible white spot both on the forehead and below the mouth. According to Pascou, it was a shy animal that fled on the ground instead of in the trees. Burney interpreted the old man as saying that it moved in "a series of leaps", but Godfrey later claimed that "a series of bounds" was a better translation—a description that would closely match the foot anatomy of monkey lemurs, such as Hadropithecus and Archaeolemur. Pascou was also able to imitate its call, a long single "whoop", and said that kidoky would come closer and continue calling if he imitated the call correctly. The call Pascou imitated was comparable to that of a short call for an indri, from the other side of the island. When shown a picture of an indri, Pascou said kidoky did not look like that, and that it had a rounder face, more similar to a sifaka. Pascou also speculated that kidoky could stand on two legs and that it was a solitary animal.
Another interviewee, François, a middle-aged woodcutter who spent time in the forests inland (east) from the main road between Morondava
and Belo sur Mer, along with five of his friends, reported seeing kidoky recently. Their description of the animal and François's imitation of its long call were virtually identical to Pascou's. One of the young men insisted that its fur had a lot of white in it, but the other men could not confirm that. François and his friends reported that it had never climbed a tree in their presence, and that it flees on the ground in short leaps or bounds. When Burney imitated the sideways leaping of a sifaka moving on the ground, one of the men corrected him, pointing out that he was imitating a sifaka. The man's imitation of the gallop kidoky used was very baboon-like. The men also reported that imitating its call can draw the animal closer and cause it to continue calling.
Burney and Ramilisonina admitted that the most parsimonious explanation for the sightings was that kidoky was a misidentified sifaka or other larger living lemur species. However, the authors did not feel comfortable with such a dismissal because of their careful quizzing and use of unlabeled color plates during the interviews and because of the competence demonstrated by the interviewees in regards to local wildlife and lemur habits. The possibility of a wild, introduced baboon surviving in the forests could not be dismissed. However, the descriptions of kidoky, with its terrestrial, baboon-like gait, make Hadropithecus and Archaeolemur the most plausible candidates among the giant subfossil lemurs. At the very least, the stories support a wider extinction window for the giant subfossil lemurs, suggesting that their extinction was recent enough for such vivid stories to still survive in the oral traditions of the Malagasy people.
Lemur
Lemurs are a clade of strepsirrhine primates endemic to the island of Madagascar. They are named after the lemures of Roman mythology due to the ghostly vocalizations, reflective eyes, and the nocturnal habits of some species...
s from Madagascar
Madagascar
The Republic of Madagascar is an island country located in the Indian Ocean off the southeastern coast of Africa...
that are represented by recent (subfossil
Subfossil
Subfossil refers to remains whose fossilization process is not complete, either for lack of time or because the conditions in which they were buried were not optimal for fossilization....
) remains dating from nearly 26,000 years ago (during the late Pleistocene
Late Pleistocene
The Late Pleistocene is a stage of the Pleistocene Epoch. The beginning of the stage is defined by the base of the Eemian interglacial phase before the final glacial episode of the Pleistocene 126,000 ± 5,000 years ago. The end of the stage is defined exactly at 10,000 Carbon-14 years BP...
) to approximately 560 years ago. They include both living and extinct
Extinction
In biology and ecology, extinction is the end of an organism or of a group of organisms , normally a species. The moment of extinction is generally considered to be the death of the last individual of the species, although the capacity to breed and recover may have been lost before this point...
species, although the term more frequently refers to the extinct giant lemurs. The diversity of subfossil lemur communities was greater than that of present-day lemur communities, ranging from as high as 20 or more species per location, compared with 10 to 12 species today. Extinct species are estimated to have ranged in size from slightly over 10 kg (22 lb) to roughly 200 kg (440.9 lb). Even the subfossil remains of living species are larger and more robust than the skeletal remains of modern specimens. The subfossil sites found around most of the island demonstrate that most giant lemurs had wide distributions and that ranges of living species have contracted significantly since the arrival of humans.
Despite their size, the giant lemurs shared many features with living lemurs, including rapid development, poor day vision, relatively small brains, and lack of male dominance. They also had many distinct traits among lemurs, including a tendency to rely on terrestrial locomotion, slow climbing, and suspension
Suspensory behavior
Suspensory Behavior, exhibited by primates, is a form of arboreal locomotion or a feeding behavior which involves hanging or suspension of the body below or among the branches, rather than moving or sitting on top of the branches...
instead of leaping, as well as a greater dependence on leaf-eating
Folivore
In zoology, a folivore is a herbivore that specializes in eating leaves. Mature leaves contain a high proportion of hard-to-digest cellulose, less energy than other types of foods, and often toxic compounds. For this reason folivorous animals tend to have long digestive tracts and slow metabolisms....
and seed predation. The giant lemurs likely filled ecological niche
Ecological niche
In ecology, a niche is a term describing the relational position of a species or population in its ecosystem to each other; e.g. a dolphin could potentially be in another ecological niche from one that travels in a different pod if the members of these pods utilize significantly different food...
s now left vacant, particularly seed dispersal
Seed dispersal
Seed dispersal is the movement or transport of seeds away from the parent plant. Plants have limited mobility and consequently rely upon a variety of dispersal vectors to transport their propagules, including both abiotic and biotic vectors. Seeds can be dispersed away from the parent plant...
for plants with large seeds. There were three distinct families of giant lemur, including the Palaeopropithecidae (sloth lemurs), Megaladapidae (koala lemurs), and Archaeolemuridae (monkey lemur
Monkey lemur
The Monkey lemurs or Baboon lemurs are an extinct type of lemurs that includes one family, Archaeolemuridae, two genera and three species. Despite their common names, members of Archaeolemuridae were not as closely related to monkeys as they were to other lemurs....
s). Two other types were more closely related and similar in appearance to living lemurs: the giant aye-aye
Giant Aye-aye
The giant aye-aye is an extinct relative of the aye-aye, the only other species in the genus Daubentonia. It lived in Madagascar, appears to have disappeared less than 1,000 years ago, is entirely unknown in life, and is only known from subfossil remains.As of 2004, giant aye-aye remains consisted...
and Pachylemur
Pachylemur
Pachylemur is an extinct genus of lemur most closely related to the ruffed lemurs . Its two representative species, Pachylemur insignis and Pachylemur jullyi, are only known from subfossil remains found at sites in central and southwestern Madagascar...
, a genus
Genus
In biology, a genus is a low-level taxonomic rank used in the biological classification of living and fossil organisms, which is an example of definition by genus and differentia...
of "giant ruffed lemur
Ruffed lemur
The ruffed lemurs of the genus Varecia are strepsirrhine primates and the largest extant lemurs within the family Lemuridae. Like all living lemurs, they are found only on the island of Madagascar...
s".
Subfossil remains were first discovered on Madagascar in the 1860s, but giant lemur species were not formally described until the 1890s. The paleontological
Paleontology
Paleontology "old, ancient", ὄν, ὀντ- "being, creature", and λόγος "speech, thought") is the study of prehistoric life. It includes the study of fossils to determine organisms' evolution and interactions with each other and their environments...
interest sparked by the initial discoveries resulted in an overabundance of new species names, the allocation of bones to the wrong species, and inaccurate reconstructions during the early 20th century. Discoveries waned during the mid-20th century, although paleontological work resumed in the 1980s and resulted in the discovery of new species and a new genus. Research has recently focused on diets, lifestyle, social behavior, and other aspects of biology. The remains of the subfossil lemurs are relatively recent, with all or most species dating within the last 2,000 years. Humans first arrived on Madagascar around that time and likely played a role in the demise of the lemurs and the other megafauna
Megafauna
In terrestrial zoology, megafauna are "giant", "very large" or "large" animals. The most common thresholds used are or...
that once existed on the large island. Although hunting and habitat change have been investigated as the primary cause of their extinction, a mosaic of complex interactions between multiple factors is now seen as the ultimate cause of their disappearance. Yet oral tradition
Oral tradition
Oral tradition and oral lore is cultural material and traditions transmitted orally from one generation to another. The messages or testimony are verbally transmitted in speech or song and may take the form, for example, of folktales, sayings, ballads, songs, or chants...
s and recent sightings by Malagasy villagers are still reported, suggesting either lingering populations or very recent extinctions.
Extinct giant lemurs
Until recently, giant lemurs existed on Madagascar. Although they are only represented by subfossil remains, they were modern forms, having adaptations unlike those seen in lemurs today, and are counted as part of the rich lemur diversity that has evolved in isolation for up to 60 million years. All 17 extinct lemurs were larger than the extant forms, including the largest living lemurs, the indriIndri
The indri , also called the babakoto, is one of the largest living lemurs. It is a diurnal tree-dweller related to the sifakas and, like all lemuroids, it is native to Madagascar.- Etymology :...
(Indri indri) and diademed sifaka
Diademed Sifaka
The diademed sifaka , or diademed simpona, is an endangered species of sifaka, one of the lemurs endemic to certain rainforests in eastern Madagascar. This species is one of the world's largest living lemurs, with a total adult length of approximately 105 centimetres , half of which is tail...
(Propithecus diadema), which weigh up to 9.5 kg (20.9 lb). The estimated weights for the subfossil lemurs have varied. Techniques used for these weight estimations include the comparison of skull lengths, tooth size, the head diameter of the femur
Femur
The femur , or thigh bone, is the most proximal bone of the leg in tetrapod vertebrates capable of walking or jumping, such as most land mammals, birds, many reptiles such as lizards, and amphibians such as frogs. In vertebrates with four legs such as dogs and horses, the femur is found only in...
, and more recently, the area of cortical bone
Cortical bone
Cortical bone, synonymous with compact bone, is one of the two types of osseous tissue that form bones. Cortical bone facilitates bone's main functions: to support the whole body, protect organs, provide levers for movement, and store and release chemical elements, mainly calcium. As its name...
(hard bone) in long bone
Long bone
The long bones are those that are longer than they are wide. They are one of five types of bones: long, short, flat, irregular and sesamoid. Long bones, especially the femur and tibia, are subjected to most of the load during daily activities and they are crucial for skeletal mobility. They grow...
s (such as the humerus
Humerus
The humerus is a long bone in the arm or forelimb that runs from the shoulder to the elbow....
). Despite the variations in the size estimates for some species, all subfossil lemurs were larger than living species, weighing 10 kg (22 lb) or more, and one species may have weighed as much as 200 kg (440.9 lb).
All but one species, the giant aye-aye
Giant Aye-aye
The giant aye-aye is an extinct relative of the aye-aye, the only other species in the genus Daubentonia. It lived in Madagascar, appears to have disappeared less than 1,000 years ago, is entirely unknown in life, and is only known from subfossil remains.As of 2004, giant aye-aye remains consisted...
, are thought to have been active during the day. Not only were they unlike the living lemurs in both size and appearance, they also filled ecological niche
Ecological niche
In ecology, a niche is a term describing the relational position of a species or population in its ecosystem to each other; e.g. a dolphin could potentially be in another ecological niche from one that travels in a different pod if the members of these pods utilize significantly different food...
s that no longer exist or are now left unoccupied. Their remains have been found in most parts of the island, except for the eastern rainforests and the Sambirano domain (seasonal moist forests in the northwest of the island), where no subfossil sites are known. Radiocarbon dates
Radiocarbon dating
Radiocarbon dating is a radiometric dating method that uses the naturally occurring radioisotope carbon-14 to estimate the age of carbon-bearing materials up to about 58,000 to 62,000 years. Raw, i.e. uncalibrated, radiocarbon ages are usually reported in radiocarbon years "Before Present" ,...
for subfossil lemur remains range from approximately 26,000 years BP
Before Present
Before Present years is a time scale used in archaeology, geology, and other scientific disciplines to specify when events in the past occurred. Because the "present" time changes, standard practice is to use AD 1950 as the origin of the age scale, reflecting the fact that radiocarbon...
(for Megaladapis
Megaladapis
Koala lemurs, genus Megaladapis, belong to the family Megaladapidae, consisting of three extinct species of lemurs that once inhabited the island of Madagascar. The largest measured between in length.-Appearance and habits:...
in northern Madagascar at the Ankarana Massif
Ankarana Reserve
Ankarana Reserve is a small, partially vegetated plateau in northern Madagascar composed of 150-million-year-old middle Jurassic limestone. With an average annual rainfall of about , the underlying rocks are susceptible to erosion, thereby producing caves and underground rivers—a karst topography...
) to around 500 years BP (for Palaeopropithecus in the southwest).
Characteristics
All of the extinct subfossil lemurs, including the smallest species (PachylemurPachylemur
Pachylemur is an extinct genus of lemur most closely related to the ruffed lemurs . Its two representative species, Pachylemur insignis and Pachylemur jullyi, are only known from subfossil remains found at sites in central and southwestern Madagascar...
, Mesopropithecus
Mesopropithecus
Mesopropithecus is an extinct genus of small to medium-sized lemur, or strepsirrhine primate, from Madagascar that includes three species, M. dolichobrachion, M. globiceps, and M. pithecoides. Together with Palaeopropithecus, Archaeoindris, and Babakotia, it is part of the sloth...
, and the giant aye-aye), were larger than the lemur species alive today. The largest species were among the largest primate
Primate
A primate is a mammal of the order Primates , which contains prosimians and simians. Primates arose from ancestors that lived in the trees of tropical forests; many primate characteristics represent adaptations to life in this challenging three-dimensional environment...
s ever to have evolved. Due to their larger size, the extinct subfossil lemurs have been compared to large-bodied anthropoids
Simian
The simians are the "higher primates" familiar to most people: the Old World monkeys and apes, including humans, , and the New World monkeys or platyrrhines. Simians tend to be larger than the "lower primates" or prosimians.- Classification and evolution :The simians are split into three groups...
(monkeys and apes), yet they more closely resemble the small-bodied lemurs. Like other lemurs, the subfossil lemurs did not exhibit appreciable differences in body or canine tooth
Canine tooth
In mammalian oral anatomy, the canine teeth, also called cuspids, dogteeth, fangs, or eye teeth, are relatively long, pointed teeth...
size between males and females (sexual dimorphism
Sexual dimorphism
Sexual dimorphism is a phenotypic difference between males and females of the same species. Examples of such differences include differences in morphology, ornamentation, and behavior.-Examples:-Ornamentation / coloration:...
). This suggests that they, too, either exhibited female social dominance or lacked male dominance, possibly exhibiting the same levels of agonism
Agonistic behaviour
In ethology, agonistic behaviour is any social behaviour related to fighting. Thus it is broader than aggressive behaviour because it includes not only actual aggression but also threats, displays, retreats, placating aggressors, and conciliation. The term was coined by Scott and Fredericson in 1951...
(aggressive competition) seen in extant lemurs. Like other lemurs, they had smaller brains than comparably sized anthropoids. Most species also had a unique strepsirrhine dental trait, called a toothcomb
Toothcomb
A toothcomb is an anatomical structure found in strepsirrhine primates, which includes lemurs, lorises and galagos. A toothcomb consists of long, flat forward-angled teeth, and includes the lower incisors and the canine teeth...
, which is used for grooming
Personal grooming
Personal grooming is the art of cleaning, grooming, and maintaining parts of the body. It is a species-typical behavior that is controlled by neural circuits in the brain.- In humans :...
. Even tooth development
Tooth development
Tooth development or odontogenesis is the complex process by which teeth form from embryonic cells, grow, and erupt into the mouth. Although many diverse species have teeth, non-human tooth development is largely the same as in humans...
and weaning
Weaning
Weaning is the process of gradually introducing a mammal infant, either human or animal, to what will be its adult diet and withdrawing the supply of its mother's milk.The process takes place only in mammals, as only mammals produce milk...
was rapid compared to similarly sized anthropoids, suggesting faster sexual maturity
Sexual maturity
Sexual maturity is the age or stage when an organism can reproduce. It is sometimes considered synonymous with adulthood, though the two are distinct...
of their offspring. Most subfossil lemurs also had high retinal summation
Retinal summation
Retinal summation describes the relationship between different types of cells in the retina: cone photoreceptor cells, bipolar cells, and ganglion cells. With high retinal summation, a large number of photoreceptor cells converge on a smaller number of bipolar cells in transferring their signals...
(sensitivity to low light), resulting in poor day vision (low visual acuity
Visual acuity
Visual acuity is acuteness or clearness of vision, which is dependent on the sharpness of the retinal focus within the eye and the sensitivity of the interpretative faculty of the brain....
) compared to anthropoids. This has been demonstrated by the ratio between their relatively small orbits
Orbit (anatomy)
In anatomy, the orbit is the cavity or socket of the skull in which the eye and its appendages are situated. "Orbit" can refer to the bony socket, or it can also be used to imply the contents...
(eye sockets) and the relative size of their optic canal, which is comparable to that of other lemurs, not diurnal anthropoids.
Although these traits are shared among both living and extinct lemurs, they are uncommon among primates in general. Two prevailing hypotheses to explain these unique adaptations are the energy frugality hypothesis by Patricia Wright
Patricia Wright
Patricia C. Wright is the Executive Director of the Institute for the Conservation of Tropical Environments and Professor at Stony Brook University in New York. Dr. Wright, a MacArthur Fellow, has been active in research and conservation in Madagascar since 1985. In 1986, Dr...
(1999) and the evolutionary disequilibrium hypothesis by Carel van Schaik and Peter M. Kappeler (1996). The energy frugality hypothesis expanded on Alison Jolly
Alison Jolly
Alison Jolly is a primatologist, known for her studies of lemur biology. She has written several books for both popular and scientific audiences and conducted extensive fieldwork on Lemurs in Madagascar, primarily at the Berenty Reserve, a small private reserve of gallery forest set in the...
's energy conservation hypotheses by claiming that most lemur traits not only help conserve energy, but also maximize the use of highly limited resources, enabling them to live in severely seasonal environments with low productivity. The evolutionary disequilibrium hypothesis postulated that living lemurs are in the process of evolving to fill open ecological niches left by the recently extinct subfossil lemurs. For example, small nocturnal prosimians are typically nocturnal and monogamous, while the larger living lemurs are generally active both day and night (cathemeral
Cathemeral
A cathemeral organism is one that has sporadic and random intervals of activity during the day or night in which food is acquired, socializing with other organisms occurs, and any other activities necessary for livelihood are performed...
) and live in small groups (gregarious
Social
The term social refers to a characteristic of living organisms...
). Cathemerality and increased gregariousness might indicate that the larger living lemurs are evolving to fill the role of the giant lemurs, which were thought to be diurnal (day-living) and more monkey-like in behavior. Since most giant subfossil lemurs have been shown to share many of the unique traits of their living counterparts, and not those of monkey
Monkey
A monkey is a primate, either an Old World monkey or a New World monkey. There are about 260 known living species of monkey. Many are arboreal, although there are species that live primarily on the ground, such as baboons. Monkeys are generally considered to be intelligent. Unlike apes, monkeys...
s, Godfrey et al. (2003) argued that the energy frugality hypothesis seems to best explain both living and extinct lemur adaptations.
Despite the similarities, subfossil lemurs had several distinct differences from their lemur relatives. In addition to being larger, the subfossil lemurs were more dependent on leaves and seeds in their diet, rather than fruit. They utilized slow climbing, hanging, and terrestrial quadrupedalism for locomotion, rather than vertical clinging and leaping
Vertical clinging and leaping
"Vertical clinging and leaping" is a type of arboreal locomotion seen most commonly among the strepsirrhine primates, and particularly the members of the family Indriidae. At rest, the animal clings to a vertical support, such as the side of a tree or bamboo stalk...
and arboreal
Arboreal locomotion
Arboreal locomotion is the locomotion of animals in trees. In every habitat in which trees are present, animals have evolved to move in them. Some animals may only scale trees occasionally, while others are exclusively arboreal. These habitats pose numerous mechanical challenges to animals...
quadrupedalism. Also, all but one of them—the giant aye-aye—are assumed to have been diurnal (due to their body size and small orbits
Orbit (anatomy)
In anatomy, the orbit is the cavity or socket of the skull in which the eye and its appendages are situated. "Orbit" can refer to the bony socket, or it can also be used to imply the contents...
), whereas many small lemurs are nocturnal and medium-sized are cathemeral.
Their skeletons suggest that most subfossil lemurs were tree-dwellers, adapted for living in forests and possibly limited to such habitats. Unlike some of the living species, the subfossil lemurs lacked adaptations for leaping. Instead, suspension
Suspensory behavior
Suspensory Behavior, exhibited by primates, is a form of arboreal locomotion or a feeding behavior which involves hanging or suspension of the body below or among the branches, rather than moving or sitting on top of the branches...
, used by some indriids
Indriidae
The Indriidae are a family of strepsirrhine primates. They are medium to large sized lemurs with only four teeth in the toothcomb instead of the usual six...
and ruffed lemur
Ruffed lemur
The ruffed lemurs of the genus Varecia are strepsirrhine primates and the largest extant lemurs within the family Lemuridae. Like all living lemurs, they are found only on the island of Madagascar...
s, was extensively used in some lineages. Although living lemurs are known to visit the ground to varying extents, only the extinct archaeolemurids exhibit adaptations for semiterrestrial locomotion. Due to the size of the extinct subfossil lemurs, all were likely to travel on the ground between trees. They had shorter, more robust limbs, heavily built axial skeleton
Axial skeleton
The axial skeleton consists of the 80 bones along the central axis of the human body. It is composed of six parts; the human skull, the ossicles of the middle ear, the hyoid bone of the throat, the rib cage, sternum and the vertebral column...
s (trunks), and large heads and are thought to have shared the common lemur trait of low basal metabolic rate
Basal metabolic rate
Basal Metabolic Rate , and the closely related resting metabolic rate , is the amount of daily energy expended by humans and other animals at rest. Rest is defined as existing in a neutrally temperate environment while in the post-absorptive state...
s, making them slow-moving. Studies of their semicircular canals confirm this assumption, showing that koala lemurs moved slower than orangutans, monkey lemurs were less agile than Old World monkey
Old World monkey
The Old World monkeys or Cercopithecidae are a group of primates, falling in the superfamily Cercopithecoidea in the clade Catarrhini. The Old World monkeys are native to Africa and Asia today, inhabiting a range of environments from tropical rain forest to savanna, shrubland and mountainous...
s, and sloth lemurs exhibited slow movements like those of lorises and sloths.
Types
Sloth lemursThe sloth lemurs (family
Family (biology)
In biological classification, family is* a taxonomic rank. Other well-known ranks are life, domain, kingdom, phylum, class, order, genus, and species, with family fitting between order and genus. As for the other well-known ranks, there is the option of an immediately lower rank, indicated by the...
Palaeopropithecidae) were the most species-rich group of the subfossil lemurs, with four genera and eight species. The common name
Common name
A common name of a taxon or organism is a name in general use within a community; it is often contrasted with the scientific name for the same organism...
is due to strong similarities in morphology
Morphology (biology)
In biology, morphology is a branch of bioscience dealing with the study of the form and structure of organisms and their specific structural features....
with arboreal sloths, or in the case of Archaeoindris
Archaeoindris
Archaeoindris fontoynonti is an extinct species of Malagasy lemur that was the largest primate to evolve on Madagascar. It weighed about and measured around 1.5m in height, more than a silverback gorilla. Archaeoindris is one of eight known members of the Palaeopropithecinae subfamily...
, with giant ground sloths. They ranged in size from some of the smallest of the subfossil lemurs, such as Mesopropithecus
Mesopropithecus
Mesopropithecus is an extinct genus of small to medium-sized lemur, or strepsirrhine primate, from Madagascar that includes three species, M. dolichobrachion, M. globiceps, and M. pithecoides. Together with Palaeopropithecus, Archaeoindris, and Babakotia, it is part of the sloth...
, weighing as little as 10 kg (22 lb), to the largest, Archaeoindris
Archaeoindris
Archaeoindris fontoynonti is an extinct species of Malagasy lemur that was the largest primate to evolve on Madagascar. It weighed about and measured around 1.5m in height, more than a silverback gorilla. Archaeoindris is one of eight known members of the Palaeopropithecinae subfamily...
, weighing approximately 200 kg (440.9 lb). Their characteristic curved finger and toe bones (phalanges
Phalanx bones
In anatomy, phalanx bones are those that form the fingers and toes. In primates such as humans and monkeys, the thumb and big toe have two phalanges, while the other fingers and toes consist of three. Phalanges are classified as long bones.The phalanges do not have individual names...
) suggest slow suspensory movement, similar to that of an orangutan
Orangutan
Orangutans are the only exclusively Asian genus of extant great ape. The largest living arboreal animals, they have proportionally longer arms than the other, more terrestrial, great apes. They are among the most intelligent primates and use a variety of sophisticated tools, also making sleeping...
or a loris
Loris
Loris is the common name for the strepsirrhine primates of the subfamily Lorisinae in family Lorisidae. Loris is one genus in this subfamily and includes the slender lorises, while Nycticebus is the genus for the slow lorises....
, making them some of the most specialized mammals for suspension
Suspensory behavior
Suspensory Behavior, exhibited by primates, is a form of arboreal locomotion or a feeding behavior which involves hanging or suspension of the body below or among the branches, rather than moving or sitting on top of the branches...
. Their day vision was very poor, and they had relatively small brains and short tails. Their diet consisted mostly of leaves, seeds, and fruit, although dental wear analysis suggests they were primarily folivorous seed-predators.
Koala lemurs
The koala lemurs of the family Megaladapidae most closely resemble marsupial
Marsupial
Marsupials are an infraclass of mammals, characterized by giving birth to relatively undeveloped young. Close to 70% of the 334 extant species occur in Australia, New Guinea, and nearby islands, with the remaining 100 found in the Americas, primarily in South America, but with thirteen in Central...
koalas from Australia. According to genetic evidence they were most closely related to the family Lemuridae
Lemuridae
Lemuridae is a family of prosimian primates native to Madagascar, and one of five families commonly known as lemurs. These animals were thought to be the evolutionary predecessors of monkeys and apes, but this is no longer considered correct...
, although for many years they were paired with the sportive lemur
Sportive lemur
The sportive lemurs are the medium sized primates that make up the Lepilemuridae family. The family consists of only one extant genus, Lepilemur, as well as the extinct genus Megaladapis. They are closely related to the other lemurs and exclusively live on the island of Madagascar...
s of the family Lepilemuridae due to similarities in their skulls and molar teeth
Molar (tooth)
Molars are the rearmost and most complicated kind of tooth in most mammals. In many mammals they grind food; hence the Latin name mola, "millstone"....
. They were slow climbers and had long forelimbs and powerful grasping feet, possibly using them for suspension. Koala lemurs ranged in size from an estimated 45 to 85 kg (99.2 to 187.4 lb), making them as large as a male orangutan or a female gorilla. They had poor day vision, short tails, lacked permanent upper incisor
Incisor
Incisors are the first kind of tooth in heterodont mammals. They are located in the premaxilla above and mandible below.-Function:...
s, and had a reduced toothcomb. Their diet generally consisted of leaves, with some species being specialized folivore
Folivore
In zoology, a folivore is a herbivore that specializes in eating leaves. Mature leaves contain a high proportion of hard-to-digest cellulose, less energy than other types of foods, and often toxic compounds. For this reason folivorous animals tend to have long digestive tracts and slow metabolisms....
s and others having a broader diet, possibly including tough seeds.
Monkey lemur
Monkey lemur
The Monkey lemurs or Baboon lemurs are an extinct type of lemurs that includes one family, Archaeolemuridae, two genera and three species. Despite their common names, members of Archaeolemuridae were not as closely related to monkeys as they were to other lemurs....
s
Monkey lemurs, or baboon lemurs, share similarities with macaque
Macaque
The macaques constitute a genus of Old World monkeys of the subfamily Cercopithecinae. - Description :Aside from humans , the macaques are the most widespread primate genus, ranging from Japan to Afghanistan and, in the case of the barbary macaque, to North Africa...
s, although they have also been compared to baboon
Baboon
Baboons are African and Arabian Old World monkeys belonging to the genus Papio, part of the subfamily Cercopithecinae. There are five species, which are some of the largest non-hominoid members of the primate order; only the mandrill and the drill are larger...
s. Members of the family Archaeolemuridae, they were the most terrestrial of the lemurs, with short, robust forelimbs and relatively flat digits. Although they spent a lot of time on the ground, they were only semi-terrestrial, spending time in trees to feed and sleep. They were heavy-bodied and ranged in size from approximately 13 to 35 kg (28.7 to 77.2 lb). They had relatively good day vision and large brains compared with other lemurs. Their robust jaws and specialized teeth suggest a diet of hard objects, such as nuts and seeds, yet other evidence, including fecal pellets, suggests they may have had a more varied diet, including leaves, fruit, and animal matter (omnivory
Omnivore
Omnivores are species that eat both plants and animals as their primary food source...
). Dental wear analysis has shed some light on this dietary mystery, suggesting that monkey lemurs had a more eclectic diet, while using tough seeds as a fall-back food item. Within the family, the genus Archaeolemur was the most widespread in distribution, resulting in hundreds of subfossil specimens, and may have been one of the last subfossil lemurs to die out.
Giant aye-aye
Giant Aye-aye
The giant aye-aye is an extinct relative of the aye-aye, the only other species in the genus Daubentonia. It lived in Madagascar, appears to have disappeared less than 1,000 years ago, is entirely unknown in life, and is only known from subfossil remains.As of 2004, giant aye-aye remains consisted...
An extinct, giant relative of the living aye-aye
Aye-aye
The aye-aye is a lemur, a strepsirrhine primate native to Madagascar that combines rodent-like teeth and a special thin middle finger to fill the same ecological niche as a woodpecker...
, the giant aye-aye shared at least two of the aye-aye's bizarre traits: ever-growing central incisors and an elongated, skinny middle finger. These shared featured suggest a similar lifestyle and diet, focused on percussive foraging (tapping with the skinny digit and listening for reverberation from hollow spots) of defended resources, such as hard nuts and invertebrate larvae concealed inside decaying wood. Weighing as much as 14 kg (30.9 lb), it was between two-and-half and five times the size of living aye-aye. Alive when humans came to Madagascar, its teeth were collected and drilled to make necklaces.
Pachylemur
Pachylemur
Pachylemur is an extinct genus of lemur most closely related to the ruffed lemurs . Its two representative species, Pachylemur insignis and Pachylemur jullyi, are only known from subfossil remains found at sites in central and southwestern Madagascar...
The only extinct member of the family Lemuridae, the genus Pachylemur contains two species that closely resembled living ruffed lemurs. Sometimes referred to as "giant ruffed lemurs", they were approximately three times larger than ruffed lemurs, weighing between 10 and 13 kg (22 and 28.7 lb). Despite their size, they were arboreal quadrupeds, possibly utilizing more suspensory behavior and cautious climbing than their sister taxon. Their skull and teeth were similar to those of ruffed lemurs, suggesting a diet high in fruit and possibly some leaves. The rest of its skeleton (postcrania
Postcrania
Postcrania[p] in zoology and vertebrate paleontology refers to all or part of the skeleton apart from the skull. Frequently, fossil remains, e.g...
) was much more robust and their vertebrae had distinctly different features.
Phylogeny
Determining the phylogenyPhylogenetics
In biology, phylogenetics is the study of evolutionary relatedness among groups of organisms , which is discovered through molecular sequencing data and morphological data matrices...
of subfossil lemurs has been problematic because studies of morphology
Morphology (biology)
In biology, morphology is a branch of bioscience dealing with the study of the form and structure of organisms and their specific structural features....
, developmental biology
Developmental biology
Developmental biology is the study of the process by which organisms grow and develop. Modern developmental biology studies the genetic control of cell growth, differentiation and "morphogenesis", which is the process that gives rise to tissues, organs and anatomy.- Related fields of study...
, and molecular phylogenetics have sometimes yielded conflicting results. All studies agree that the family Daubentoniidae (including the giant aye-aye) diverged first from the other lemurs at least 60 million years ago. The relationship between the remaining families has been less clear. Morphological, developmental, and molecular studies have offered support for lumping the four sloth lemur genera of the family Palaeopropithecidae with the family Indriidae
Indriidae
The Indriidae are a family of strepsirrhine primates. They are medium to large sized lemurs with only four teeth in the toothcomb instead of the usual six...
(including the indri, sifakas, and woolly lemur
Woolly lemur
The woolly lemurs, also known as avahis or woolly indris, are nine species of strepsirrhine primates. Like all other lemurs, they live only on the island of Madagascar....
s). The placement of family Megaladapidae has been more controversial, with similarities in teeth and skull features suggesting a close relationship with family Lepilemuridae (sportive lemur
Sportive lemur
The sportive lemurs are the medium sized primates that make up the Lepilemuridae family. The family consists of only one extant genus, Lepilemur, as well as the extinct genus Megaladapis. They are closely related to the other lemurs and exclusively live on the island of Madagascar...
s). Molecular data, instead, indicate a closer relationship to family Lemuridae. Likewise, a relationship between family Archaeolemuridae and family Lemuridae has been suggested, based on morphological and developmental traits, yet molar morphology, the number of teeth in the specialized toothcomb, and molecular analysis support a closer relationship with the indriid–sloth lemur clade
Cladistics
Cladistics is a method of classifying species of organisms into groups called clades, which consist of an ancestor organism and all its descendants . For example, birds, dinosaurs, crocodiles, and all descendants of their most recent common ancestor form a clade...
. Other subfossil lemurs, including the giant aye-aye and Pachylemur, are more easily placed due to strong similarities with existing lemurs (the aye-aye and ruffed lemurs, respectively).
Living species
Subfossil sites in Madagascar have yielded the remains of more than just extinct lemurs. Extant lemur remains have also been found, and radiocarbon dating has demonstrated that both types of lemur lived at the same time. Furthermore, in some cases living species are locally extinctLocal extinction
Local extinction, also known as extirpation, is the condition of a species which ceases to exist in the chosen geographic area of study, though it still exists elsewhere...
for the area in which their subfossil remains were found. Because subfossil sites are found across most of the island, with the most notable exception being the eastern rainforest, both paleocommunity composition and paleodistributions can be determined. Geographic range
Range (biology)
In biology, the range or distribution of a species is the geographical area within which that species can be found. Within that range, dispersion is variation in local density.The term is often qualified:...
s have contracted for numerous species, including the indri, greater bamboo lemur
Greater Bamboo Lemur
The Greater Bamboo Lemur , also known as the Broad-nosed Bamboo Lemur and the Broad-nosed Gentle Lemur, is the largest bamboo lemur, at over five pounds or nearly 2.5 kilograms. It has greyish brown fur and white ear tufts, and has a head-body length of around one and a half feet, or forty to...
, and ruffed lemurs. For instance, subfossil remains of the indri have been found in marsh deposits near Ampasambazimba in the Central Highlands
Central Highlands (Madagascar)
The Central Highlands, Central High Plateau, or Hauts-Plateaux are a mountainous biogeographical region in central Madagascar. They include the contiguous part of the island's interior above 800 m altitude...
and in other deposits in both central and northern Madagascar, demonstrating a much larger range than the small region on the east coast that it currently occupies. Even the greater bamboo lemur, a critically endangered species restricted to a small portion of the south-central eastern rainforest, has undergone significant range contraction since the mid-Holocene
Holocene
The Holocene is a geological epoch which began at the end of the Pleistocene and continues to the present. The Holocene is part of the Quaternary period. Its name comes from the Greek words and , meaning "entirely recent"...
, with subfossil remains from Ankarana Massif
Ankarana Reserve
Ankarana Reserve is a small, partially vegetated plateau in northern Madagascar composed of 150-million-year-old middle Jurassic limestone. With an average annual rainfall of about , the underlying rocks are susceptible to erosion, thereby producing caves and underground rivers—a karst topography...
in the far north of Madagascar dating to 2565 BCE
Common Era
Common Era ,abbreviated as CE, is an alternative designation for the calendar era originally introduced by Dionysius Exiguus in the 6th century, traditionally identified with Anno Domini .Dates before the year 1 CE are indicated by the usage of BCE, short for Before the Common Era Common Era...
± 70 years. Combined with finds from other subfossil sites, data suggests that it used to range across the northern, northwestern, central, and eastern parts of the island. It is unclear whether these locations were wetter
Mesic habitat
In ecology, a mesic habitat is a type of habitat with a moderate or well-balanced supply of moisture, e.g., a mesic forest, a temperate hardwood forest, or dry-mesic prairie. Compared to a dry habitat, a mesic habitat is moister....
in the past or whether distinct subpopulations or subspecies
Subspecies
Subspecies in biological classification, is either a taxonomic rank subordinate to species, ora taxonomic unit in that rank . A subspecies cannot be recognized in isolation: a species will either be recognized as having no subspecies at all or two or more, never just one...
occupied the drier forests, much like modern diversity of sifaka
Sifaka
Sifakas are a genus of lemur from the family Indriidae within the order Primates. Their name of the family is an onomatopoeia of their characteristic "shi-fak" alarm call. Like all lemurs, they are found only on the island of Madagascar...
s.
In addition to previously having expanded geographic ranges, extant subfossil lemurs exhibited significant variation in size. Researchers have noted that subfossil bones of living species are more robust and generally larger than their present-day counterparts. The relative size of living species may be related to regional ecological factors, such as resource seasonality, a trend that is still observable today, where individuals from the spiny forests
Madagascar spiny thickets
The Madagascar spiny thickets is an ecoregion in Madagascar. The vegetation type is found on poor substrates with low, erratic winter rainfall. An estimated 14,000 to is covered with this habitat, all in the southwest of the country...
are, on average, smaller than individuals from the southwestern succulent woodlands or the dry deciduous forests
Madagascar dry deciduous forests
The Madagascar dry deciduous forests represent a tropical dry forest ecoregion generally situated in the western part of Madagascar. The area has high numbers of endemic plant and animal species but has suffered large-scale clearance for agriculture...
.
Ecology
As a group, the lemurs of Madagascar are extremely diverse, having evolved in isolation and radiatedAdaptive radiation
In evolutionary biology, adaptive radiation is the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage. Starting with a recent single ancestor, this process results in the speciation and phenotypic adaptation of an array of species exhibiting different...
over the past 40 to 60 million years to fill many ecological niche
Ecological niche
In ecology, a niche is a term describing the relational position of a species or population in its ecosystem to each other; e.g. a dolphin could potentially be in another ecological niche from one that travels in a different pod if the members of these pods utilize significantly different food...
s normally occupied by other primates. In the recent past, their diversity was significantly greater, with 17 extinct species sharing body proportions and specializations with loris
Loris
Loris is the common name for the strepsirrhine primates of the subfamily Lorisinae in family Lorisidae. Loris is one genus in this subfamily and includes the slender lorises, while Nycticebus is the genus for the slow lorises....
es and various non-primates, such as tree sloth
Sloth
Sloths are the six species of medium-sized mammals belonging to the families Megalonychidae and Bradypodidae , part of the order Pilosa and therefore related to armadillos and anteaters, which sport a similar set of specialized claws.They are arboreal residents of the jungles of Central and South...
s, giant ground sloth
Ground sloth
Ground sloths are a diverse group of extinct sloths, in the mammalian superorder Xenarthra. Their most recent survivors lived in the Antilles, where it has been proposed they may have survived until 1550 CE; however, the youngest AMS radiocarbon date reported is 4190 BP, calibrated to c. 4700 BP...
s, koala
Koala
The koala is an arboreal herbivorous marsupial native to Australia, and the only extant representative of the family Phascolarctidae....
s, and striped possums (genus Dactylopsila
Dactylopsila
Dactylopsila is a genus of marsupial in the Petauridae family.It contains the following species:*Great-tailed Triok, Dactylopsila megalura*Long-fingered Triok, Dactylopsila palpator*Tate's Triok, Dactylopsila tatei...
). Although the diversity of lemur communities today can be as high as 10 to 12 species per region, communities of 20 or more lemur species existed as recently as 1,000 years ago in areas that now have no lemurs at all. Just like living species, many of the extinct species shared overlapping ranges with closely related species (sympatry
Sympatry
In biology, two species or populations are considered sympatric when they exist in the same geographic area and thus regularly encounter one another. An initially-interbreeding population that splits into two or more distinct species sharing a common range exemplifies sympatric speciation...
) through niche differentiation
Niche differentiation
The term niche differentiation , as it applies to the field of ecology, refers to the process by which natural selection drives competing species into different patterns of resource use or different niches...
(resource partitioning). Among all the late Quaternary
Quaternary
The Quaternary Period is the most recent of the three periods of the Cenozoic Era in the geologic time scale of the ICS. It follows the Neogene Period, spanning 2.588 ± 0.005 million years ago to the present...
assemblages of megafauna
Megafauna
In terrestrial zoology, megafauna are "giant", "very large" or "large" animals. The most common thresholds used are or...
, only Madagascar was dominated by large primates.
Although anatomical evidence suggests that even the large, extinct species were adapted to tree-climbing, some habitats, including gallery forest
Gallery forest
Gallery forests are evergreen forests that form as corridors along rivers or wetlands and project into landscapes that are otherwise only sparsely treed such as savannas, grasslands or deserts....
s and the spiny forests of southern Madagascar, in which they occurred would not have allowed them to be strictly arboreal. Even today, most lemur species will visit the ground to cross open areas, suggesting that the extinct species did the same. Monkey lemurs (family Archaeolemuridae), including Archaeolemur majori
Archaeolemur
Archaeolemur is an extinct genus of lemurs that includes two species, Archaeolemur edwardsi and A. majori.The genus was widespread throughout Madagascar through much of the Holocene epoch, and its remains are often abundant at fossil sites across the island. The wide geographical and temporal range...
and Hadropithecus stenognathus
Hadropithecus
Hadropithecus is a medium-sized, extinct genus of lemur, or strepsirrhine primate, from Madagascar that includes a single species, Hadropithecus stenognathus. Due to its rarity and lack of sufficient skeletal remains, it is one of the least understood of the extinct lemurs...
, have been reconstructed as being primarily terrestrial
Terrestrial animal
Terrestrial animals are animals that live predominantly or entirely on land , as compared with aquatic animals, which live predominantly or entirely in the water , or amphibians, which rely on a combination of aquatic and terrestrial habitats...
. In contrast, the sloth lemurs (family Palaeopropithecidae) were highly arboreal despite the large size of some species.
Species of both extinct and living (extant) lemur vary in size based on habitat conditions, despite their differences in niche preference. Within related groups, larger species tend to inhabit wetter, more productive habitat
Habitat
* Habitat , a place where a species lives and grows*Human habitat, a place where humans live, work or play** Space habitat, a space station intended as a permanent settlement...
s, while smaller sister taxa are found in drier, less productive habitats. This pattern suggests that populations of both living and extinct lemur species had become geographically isolated by differences in habitat and evolved in isolation
Allopatric speciation
Allopatric speciation or geographic speciation is speciation that occurs when biological populations of the same species become isolated due to geographical changes such as mountain building or social changes such as emigration...
due to varying primary production
Primary production
400px|thumb|Global oceanic and terrestrial photoautotroph abundance, from September [[1997]] to August 2000. As an estimate of autotroph biomass, it is only a rough indicator of primary production potential, and not an actual estimate of it...
within different ecosystem
Ecosystem
An ecosystem is a biological environment consisting of all the organisms living in a particular area, as well as all the nonliving , physical components of the environment with which the organisms interact, such as air, soil, water and sunlight....
s. Thermoregulation
Thermoregulation
Thermoregulation is the ability of an organism to keep its body temperature within certain boundaries, even when the surrounding temperature is very different...
may also have played a role in the evolution of their increased body size. Yet despite this pressure to specialize and differentiate, some of the extinct subfossil lemurs, such as Archaeolemur, may have had island-wide distributions during the Holocene, unlike the living lemurs. If this is the case, it may suggest that some larger lemurs might have been more tolerant to regional differences in ecology than living lemurs.
Diet
Research on subfossil lemur diets, particularly in southern and southwestern Madagascar, has indicated that ecological communities have been significantly affected by their recent extinction. Many extinct subfossil lemurs were large-bodied leaf-eaters (folivoreFolivore
In zoology, a folivore is a herbivore that specializes in eating leaves. Mature leaves contain a high proportion of hard-to-digest cellulose, less energy than other types of foods, and often toxic compounds. For this reason folivorous animals tend to have long digestive tracts and slow metabolisms....
s), seed predators, or both. Today, leaf-eating along with seed predation is only seen in mid-sized lemurs, and is far less common than it was in the past. Strict folivory is also less common, now found primarily in small lemurs. In certain cases, subfossil lemurs, such as the sloth lemurs and koala lemurs, may have used leaves as an important fallback food, whereas other species, such as the monkey lemurs and the giant aye-aye, specialized on structurally defended resources, such as hard seeds and wood-boring insect larvae. Last, Pachylemur was primarily a fruit eater (frugivorous
Frugivore
A frugivore is a fruit eater. It can be any type of herbivore or omnivore where fruit is a preferred food type. Because approximately 20% of all mammalian herbivores also eat fruit, frugivory is considered to be common among mammals. Since frugivores eat a lot of fruit they are highly dependent...
). Subfossil lemur diets have been reconstructed using analytical tools, including techniques to compare tooth anatomy, structure, and wear; biogeochemistry
Biogeochemistry
Biogeochemistry is the scientific discipline that involves the study of the chemical, physical, geological, and biological processes and reactions that govern the composition of the natural environment...
(analysis of isotope
Isotope
Isotopes are variants of atoms of a particular chemical element, which have differing numbers of neutrons. Atoms of a particular element by definition must contain the same number of protons but may have a distinct number of neutrons which differs from atom to atom, without changing the designation...
levels, like carbon-13
Carbon-13
Carbon-13 is a natural, stable isotope of carbon and one of the environmental isotopes. It makes up about 1.1% of all natural carbon on Earth.- Detection by mass spectrometry :...
); and the dissection of fecal pellets
Feces
Feces, faeces, or fæces is a waste product from an animal's digestive tract expelled through the anus or cloaca during defecation.-Etymology:...
associated with subfossil remains.
The diets of most subfossil lemurs, most notably Palaeopropithecus and Megaladapis, consisted primarily of C3 plants
C3 carbon fixation
carbon fixation is a metabolic pathway for carbon fixation in photosynthesis. This process converts carbon dioxide and ribulose bisphosphate into 3-phosphoglycerate through the following reaction:...
, which use a form of photosynthesis
Photosynthesis
Photosynthesis is a chemical process that converts carbon dioxide into organic compounds, especially sugars, using the energy from sunlight. Photosynthesis occurs in plants, algae, and many species of bacteria, but not in archaea. Photosynthetic organisms are called photoautotrophs, since they can...
that results in higher water loss through transpiration
Transpiration
Transpiration is a process similar to evaporation. It is a part of the water cycle, and it is the loss of water vapor from parts of plants , especially in leaves but also in stems, flowers and roots. Leaf surfaces are dotted with openings which are collectively called stomata, and in most plants...
. Other subfossil lemurs, such as Hadropithecus and Mesopropithecus, fed on CAM
Crassulacean acid metabolism
Crassulacean acid metabolism, also known as CAM photosynthesis, is a carbon fixation pathway that evolved in some plants as an adaptation to arid conditions. The stomata in the leaves remain shut during the day to reduce evapotranspiration, but open at night to collect carbon dioxide...
and C4 plants
C4 carbon fixation
C4 carbon fixation is one of three biochemical mechanisms, along with and CAM photosynthesis, used in carbon fixation. It is named for the 4-carbon molecule present in the first product of carbon fixation in these plants, in contrast to the 3-carbon molecule products in plants. fixation is an...
, which use more water-efficient forms of photosynthesis. Fruit
Fruit
In broad terms, a fruit is a structure of a plant that contains its seeds.The term has different meanings dependent on context. In non-technical usage, such as food preparation, fruit normally means the fleshy seed-associated structures of certain plants that are sweet and edible in the raw state,...
and animal matter was more common in the diets of subfossil lemurs including Pachylemur, Archaeolemur, and the giant aye-aye. In southern and southwestern Madagascar, the subfossil lemurs of the spiny forests generally favored the C3 plants over the more abundant CAM plants, although closely related sympatric species may have fed upon the two types of plants in different ratios, allowing each to divide resources and coexist. Since plants produce defenses against leaf-eating animals, the extensive use of spines by plants in the spiny forests suggest that they evolved to cope with leaf-eating lemurs, large and small.
Seed dispersal
Giant subfossil lemurs are thought to have also played a significant role in seed dispersalSeed dispersal
Seed dispersal is the movement or transport of seeds away from the parent plant. Plants have limited mobility and consequently rely upon a variety of dispersal vectors to transport their propagules, including both abiotic and biotic vectors. Seeds can be dispersed away from the parent plant...
, possibly targeting species that did not attract the seed dispersal services of the extinct elephant bird
Elephant bird
Elephant birds are an extinct family of flightless birds found only on the island of Madagascar and comprising the genera Aepyornis and Mullerornis.-Description:...
s. Biogeochemistry studies have shown that they may have been the primary seed dispersers for the endemic and native C3 trees in the spiny forests. Terrestrial species may even have dispersed seeds for small bushes in addition to tall trees. Seed dispersal can involve passing seeds through the gut (endozoochory) or attaching the seeds to the animal's body (epizoochory), and both processes probably occurred with subfossil lemurs. Seeds from Uncarina
Uncarina
Uncarina is a genus of plant in family Pedaliaceae found in Madagascar. It contains the following species :* Uncarina decaryi, Humbert ex Ihlenf.* Uncarina didierii, Stapf...
species embed themselves in lemur fur, and likely did the same with subfossil lemurs. Seed dispersal biology is known for very few species in the spiny forest, including genera
Genus
In biology, a genus is a low-level taxonomic rank used in the biological classification of living and fossil organisms, which is an example of definition by genus and differentia...
of plants suspected of depending on giant lemurs, such as Adansonia
Adansonia
Adansonia is a genus of eight species of tree, six native to Madagascar, one native to mainland Africa and the Arabian Peninsula and one to Australia. The mainland African species also occurs on Madagascar, but it is not a native of that island....
, Cedrelopsis
Cedrelopsis
Cedrelopsis is a flowering plant genus in the family Meliaceae found in Madagascar.Species:-External links:*...
, Commiphora
Commiphora
Commiphora is a genus of flowering plants in the family Burseraceae. It includes about 185 species of trees and shrubs, often armed or thorny, native to Africa, Arabia, and the Indian subcontinent.-Uses:...
, Delonix
Delonix
Delonix is a genus of flowering plants in the pea family, Fabaceae, subfamily Caesalpinioideae. It contains trees that are native to Madagascar and east Africa. By far the best known species is the Royal Poinciana ....
, Diospyros
Diospyros
Diospyros is a genus of about 450–500 species of deciduous and evergreen trees. The majority are native to the tropics, with only a few species extending into temperate regions. They are commonly known as ebony or persimmon trees...
, Grewia
Grewia
The large flowering plant genus Grewia is today placed by most authors in the mallow family Malvaceae, in the expanded sense as proposed by in the APG. Formerly, it was placed in either the linden family or the Sparrmanniaceae...
, Pachypodium
Pachypodium
Pachypodium is a genus of succulent spine-bearing trees and shrubs, native to Africa. It belongs to the dogbane family, Apocynaceae. Pachypodium comes from a Latin form from Greek pachus and podion , hence meaning thick-footed.-Genus characteristics:All Pachypodium are succulent plants that...
, Salvadora, Strychnos
Strychnos
Strychnos is a genus of flowering plants, belonging to family Loganiaceae . The genus includes about 190 species of trees and lianas, distributed around the world's tropics....
, and Tamarind
Tamarind
Tamarind is a tree in the family Fabaceae. The genus Tamarindus is monotypic .-Origin:...
us. For example, Delonix has edible pods that are rich in protein, and Adansonia fruits have a nutritious pulp and large seeds that may have been dispersed by Archaeolemur majori or Pachylemur insignis.
Seed size may be a limiting factor for some plant species, since their seeds are too large for living (extant) lemurs. The common brown lemur (Eulemur fulvus) can swallow seeds 20 mm (0.78740157480315 in) in diameter, while the black-and-white ruffed lemur
Black-and-white ruffed lemur
The black-and-white ruffed lemur is the more endangered of the two species of ruffed lemurs, both of which are endemic to the island of Madagascar. Despite having a larger range than the red ruffed lemur, it has a much smaller population that is spread out, living in lower population densities...
(Varecia variegata) is capable of swallowing seeds up to 30 mm (1.2 in) in diameter. A large lemur, such as Pachylemur, which was more than twice the size of today's ruffed lemur
Ruffed lemur
The ruffed lemurs of the genus Varecia are strepsirrhine primates and the largest extant lemurs within the family Lemuridae. Like all living lemurs, they are found only on the island of Madagascar...
s, could probably swallow even larger seeds. Seed dispersal limitations tied to megafaunal extinction are exhibited by Commiphora guillaminii. At present, this tree species has a short dispersal distance, but its genetics
Genetics
Genetics , a discipline of biology, is the science of genes, heredity, and variation in living organisms....
indicate higher levels of regional gene flow
Gene flow
In population genetics, gene flow is the transfer of alleles of genes from one population to another.Migration into or out of a population may be responsible for a marked change in allele frequencies...
in the past, based on comparisons with a closely related species in Africa that still has its seeds dispersed by large animals.
Discovery and research
The writings of French colonial governor Étienne de FlacourtÉtienne de Flacourt
Étienne de Flacourt was a French governor of Madagascar, born at Orléans in 1607. He was named governor of Madagascar by the French East India Company in 1648....
in the mid-17th century introduced the existence of giant Malagasy mammals to Western science with recorded eye-witness accounts from the local people of dangerous animals, hornless "water cows", and a large lemur-like creature referred to locally as the tretretretre or tratratratra. Today, the latter is thought to have been a species of Palaeopropithecus or possibly Megaladapis. Flacourt described it as:
Local tales of a song'aomby (Malagasy for "cow that is not a cow"), or pygmy hippopotamus, led French naturalist Alfred Grandidier
Alfred Grandidier
Alfred Grandidier was a French naturalist and explorer.From a very wealthy family, he and his brother, Ernest Grandidier , undertook a voyage around the world...
to follow a village headman to a marsh in southwestern Madagascar, a site called Ambolisatra, which became the first known subfossil site in Madagascar. In 1868, Grandidier uncovered the first subfossil remains of lemurs—a humerus
Humerus
The humerus is a long bone in the arm or forelimb that runs from the shoulder to the elbow....
from Palaeopropithecus and a tibia
Tibia
The tibia , shinbone, or shankbone is the larger and stronger of the two bones in the leg below the knee in vertebrates , and connects the knee with the ankle bones....
of a sifaka. The Palaeopropithecus remains were not described for several decades, and it took decades more for the remains to be correctly paired with other sloth lemur remains. It was not until 1893 that giant lemur species were formally described, when Charles Immanuel Forsyth Major
Charles Immanuel Forsyth Major
Charles Immanuel Forsyth Major was a Swiss zoologist and vertebrate palaeontologist.Major was born in Glasgow and studied at Basel and Zurich Universities in Switzerland and later Göttingen in Germany...
discovered and described a long, narrow skull of Megaladapis madagascariensis in a marsh. His discoveries in various marshes of central and southwestern Madagascar sparked paleontological
Paleontology
Paleontology "old, ancient", ὄν, ὀντ- "being, creature", and λόγος "speech, thought") is the study of prehistoric life. It includes the study of fossils to determine organisms' evolution and interactions with each other and their environments...
interest, resulting in an overabundance of taxonomic names
Taxonomy
Taxonomy is the science of identifying and naming species, and arranging them into a classification. The field of taxonomy, sometimes referred to as "biological taxonomy", revolves around the description and use of taxonomic units, known as taxa...
and confused assemblages of bones from numerous species, including non-primates. Specimens were distributed between European museums and Madagascar, often resulting in the loss of field data that went with the specimens, if the data had been recorded at all.
In 1905, Alfred Grandidier's son, Guillaume Grandidier
Guillaume Grandidier
Guillaume Grandidier was a French geographer , ethnologist , zoologist who studied the island of Madagascar.He was the son of the wealthy industrialist Alfred Grandidier also a zoologist and expert on Madagascar...
, reviewed subfossil lemur taxonomy and determined that too many names had been created. His review established most of the presently known family and genera names for the extinct lemurs. Despite the taxonomic clarification, subfossil postcrania from different genera, particularly Megaladapis, Palaeopropithecus and Hadropithecus, continued to be incorrectly paired and sometimes assigned to non-primates. Since subfossil remains were often dredged from marshes one by one, pairing skulls with other bones was often guesswork based on size-matching, and was not very accurate as a consequence. Even as late as the 1950s, bones of non-primates were attributed to subfossil lemurs. One reconstruction of the confounded subfossil remains by paleontologist Herbert F. Standing depicted Palaeopropithecus as an aquatic animal that swam near the surface, keeping its eyes, ears, and nostrils slightly above water. Postcranial remains of Palaeopropithecus had previously been paired with Megaladapis by Guillaume Grandidier, who viewed it as a giant tree sloth, which he named Bradytherium. Standing's aquatic theory was supported by Italian paleontologist Guiseppe Sera, who reconstructed Palaeopropithecus as an "arboreal-aquatic acrobat" that not only swam in water but climbed trees and dove from there into the water. Sera took the aquatic theory further in 1938 by including other extinct lemurs, including Megaladapis, which he viewed as a thin ray
Batoidea
Batoidea is a superorder of cartilaginous fish commonly known as rays and skates, containing more than 500 described species in thirteen families...
-like swimmer that fed on mollusks and crustaceans while concealed underwater. It was primarily the paleontologist Charles Lamberton who correctly paired many of the confused subfossils, although others had also helped address problems of association and taxonomic synonyms
Synonym (taxonomy)
In scientific nomenclature, a synonym is a scientific name that is or was used for a taxon of organisms that also goes by a different scientific name. For example, Linnaeus was the first to give a scientific name to the Norway spruce, which he called Pinus abies...
. Lamberton also refuted Guillaume Grandidier's sloth theory for Megaladapis, as well as the aquatic lemur theory of Standing and Sera.
Excavations during the early 20th century by researchers like Lamberton failed to unearth any new extinct lemur genera. Fourteen of the approximately seventeen known species had previously been identified from field work in southern, western, and central Madagascar. When paleontological field work resumed in the early 1980s, new finds provided associated skeletal remains, including rare bones such as carpal bones
Carpus
In tetrapods, the carpus is the sole cluster of bones in the wrist between the radius and ulna and the metacarpus. The bones of the carpus do not belong to individual fingers , whereas those of the metacarpus do. The corresponding part of the foot is the tarsus...
(wrist bones), phalanges
Phalanx bones
In anatomy, phalanx bones are those that form the fingers and toes. In primates such as humans and monkeys, the thumb and big toe have two phalanges, while the other fingers and toes consist of three. Phalanges are classified as long bones.The phalanges do not have individual names...
(finger and toe bones), and bacula
Baculum
The baculum is a bone found in the penis of most mammals. It is absent in humans, but present in other primates, such as the gorilla and chimpanzee.The bone aids in sexual intercourse.-Purpose:...
(penile bone). In some cases, nearly complete hands and feet were found. Enough remains have been found for some groups to demonstrate the physical development
Ontogeny
Ontogeny is the origin and the development of an organism – for example: from the fertilized egg to mature form. It covers in essence, the study of an organism's lifespan...
of juveniles. Standard long-bone indices have been calculated in order to determine the intermembral index (a ratio that compares limb proportions), and body mass estimates have been made based on long-bone circumference measurements. Even preserved fecal pellets
Feces
Feces, faeces, or fæces is a waste product from an animal's digestive tract expelled through the anus or cloaca during defecation.-Etymology:...
from Archaeolemur have been found, allowing researchers to learn about its diet. More recently, electron microscopy
Electron microscope
An electron microscope is a type of microscope that uses a beam of electrons to illuminate the specimen and produce a magnified image. Electron microscopes have a greater resolving power than a light-powered optical microscope, because electrons have wavelengths about 100,000 times shorter than...
has allowed researchers to study behavioral patterns, and DNA amplification
DNA replication
DNA replication is a biological process that occurs in all living organisms and copies their DNA; it is the basis for biological inheritance. The process starts with one double-stranded DNA molecule and produces two identical copies of the molecule...
has helped with genetic tests that determine the phylogenetic relationships between the extinct and living lemurs.
A new genus of sloth lemur, Babakotia
Babakotia
Babakotia is a medium-sized, extinct genus of lemur, or strepsirrhine primate, from Madagascar that contains a single species, Babakotia radofilai. Together with Palaeopropithecus, Archaeoindris, and Mesopropithecus, it forms the family Palaeopropithecidae, commonly known as the sloth lemurs...
, was discovered in 1986 by a team led by Elwyn Simons of Duke University
Duke University
Duke University is a private research university located in Durham, North Carolina, United States. Founded by Methodists and Quakers in the present day town of Trinity in 1838, the school moved to Durham in 1892. In 1924, tobacco industrialist James B...
in karst
Karst topography
Karst topography is a geologic formation shaped by the dissolution of a layer or layers of soluble bedrock, usually carbonate rock such as limestone or dolomite, but has also been documented for weathering resistant rocks like quartzite given the right conditions.Due to subterranean drainage, there...
caves on the Ankarana Massif in northern Madagascar. Along with Babakotia, a new species of Mesopropithecus, M. dolichobrachion, was also discovered, but not formally described until 1995. The same team has also helped promote new ideas about sloth lemur adaptations and the relationships among the four genera. They have also provided evidence that living species, such as the indri and the greater gamboo lemur, have lost much of their original range. In 2009, a new species of large sloth lemur, called Palaeopropithecus kelyus, was described from northwestern Madagascar by a Franco-Madagascan team. The new species was found to be smaller than the two previously known species from the genus, and its diet reportedly consisted of more hard-textured food. The resurgence in subfossil lemur work has also sparked new interest in Madagascar's small mammals, which have also been found at the subfossil sites. This has led to new ideas about the origins, diversity, and distribution of these animals.
The number of Malagasy subfossil sites containing subfossil lemurs has increased significantly since the mid-20th century. At that time, subfossil lemurs had only been found in the center, south, and southwest of the island. Since then, only the eastern rainforests have not been represented, and paleodistributions are now known for both extinct and living species around most of the island. Large quantities of subfossil lemur remains have been found in caves, marshes, and streambank sites in drier regions. The subfossil sites are clustered together geographically and are recent in age, mostly dating between 2,500 and 1,000 years old, with a few spanning back into the last glaciation, which ended approximately 10,000 years ago.
Extinction
At least 17 species of giant subfossil lemur vanished during the Holocene, with all or most extinctions happening after the colonization of Madagascar by humans around 2,000 years ago. Madagascar's megafaunaMegafauna
In terrestrial zoology, megafauna are "giant", "very large" or "large" animals. The most common thresholds used are or...
included not only giant lemurs, but also elephant bird
Elephant bird
Elephant birds are an extinct family of flightless birds found only on the island of Madagascar and comprising the genera Aepyornis and Mullerornis.-Description:...
s, giant tortoise
Giant tortoise
Giant tortoises are characteristic reptiles of certain tropical islands. Often reaching enormous size—they can weigh as much as 300 kg and can grow to be 1.3 m long—they live, or lived , in the Seychelles, the Mascarenes and the Galapagos...
s, several species of Malagasy hippopotamus
Malagasy Hippopotamus
Several species of Malagasy Hippopotamus lived on the island of Madagascar but are now believed to be extinct. The animals were very similar to the extant Hippopotamus and Pygmy Hippopotamus...
es, Cryptoprocta spelea
Cryptoprocta spelea
Cryptoprocta spelea, also known as the giant fossa, is an extinct species of carnivore from Madagascar in the family Eupleridae, which is most closely related to the mongooses and includes all Malagasy carnivorans. It was first described in 1902, and in 1935 was recognized as a separate species...
(a "giant Fossa
Fossa (animal)
The fossa is a cat-like, carnivorous mammal that is endemic to Madagascar. It is a member of the Eupleridae, a family of carnivorans closely related to the mongoose family . Its classification has been controversial because its physical traits resemble those of cats, yet other traits suggest a...
"), large crocodiles (Voay robustus
Voay
Voay is an extinct genus of crocodylid crocodilian. Numerous subfossils have been found from Madagascar, including complete skulls as well as vertebrae and osteoderms from such places as Ambolisatra and Antsirabe. The genus is thought to have become extinct relatively recently during the Holocene...
), and Plesiorycteropus
Plesiorycteropus
Plesiorycteropus, also known as the bibymalagasy or Malagasy aardvark, is a recently extinct eutherian mammalian genus from Madagascar. Upon its description in 1895, it was classified with the aardvark, but recent studies have found little evidence to link it to aardvarks or any other order of...
, a unique digging mammal, all of which died out during the same period. Madagascar's megafaunal extinctions were among the most severe for any continent or large island, with all endemic wildlife over 10 kg (22 lb) disappearing, totaling approximately 25 species. The most severely impacted lemurs were generally large and diurnal, particularly the clade containing the living indriids and extinct sloth lemurs. Although only the indriids are alive today and represent only a small percentage of the living lemur species, this clade collectively contained the majority of the extinct giant lemur species.
By region, the Central Highlands lost the greatest number of lemur species. Although it has lost nearly all of its woodland habitat, some lemur species still survive in isolated forest patches. Lemur diversity is tightly linked with plant diversity, which in turn decreases with increased forest fragmentation
Forest fragmentation
Forest fragmentation is a form of habitat fragmentation, occurring when forests are cut down in a manner that leaves relatively small, isolated patches of forest known as forest fragments or forest remnants. The intervening matrix that separates the remaining woodland patches can be natural open...
. In extreme cases, treeless sites such as the town of Ampasambazimba from the central region no longer support any of the lemur species represented in their subfossil record. However, other locations no longer have giant subfossil lemurs, yet they still maintain forested habitat that could support them. Even though the giant lemurs have disappeared from these locations, while the smaller species survive in the forest patches that remain, the subfossil remains indicate that the living species used to be more widespread and coexisted with the extinct species. Although the Central Highlands saw the greatest species loss, it was not the only region or habitat type to witness extinctions. However, the least-understood region is the eastern rainforests, which have not yielded subfossil lemur remains. Consequently, it is impossible to know what percentage of lemur taxa were recently lost there, although studies of Malagasy customs (ethnohistory
Ethnohistory
Ethnohistory is the study of ethnographic cultures and indigenous customs by examining historical records. It is also the study of the history of various ethnic groups that may or may not exist today....
) along with archaeological evidence suggests the eastern rainforests were more ecologically disturbed in the past than they are today. Hunting and trapping by humans may have severely impacted large lemurs in this region as well.
Comparisons of species counts from subfossil deposits and remnant populations in neighboring Special Reserves has further demonstrated decreased diversity in lemur communities and contracted geographic ranges. At Ampasambazimba in central Madagascar, 20 species of subfossil lemur have been found. At nearby Ambohitantely Reserve
Ambohitantely Reserve
Ambohitantely Reserve is a wildlife reserve of Madagascar....
, only 20% of those species still survive. Only six of 13 species found at Ankilitelo and Ankomaka Caves in the southwest still survive at Beza Mahafaly Reserve
Beza Mahafaly Reserve
The Beza Mahafaly Reserve is a nature reserve in Madagascar located northeast of Betioky Sud. The Reserve also provides training and research opportunities. It consists of a fenced gallery forest, approximately , separated by from a gallery of arid spiny forest...
. In the extreme north, the caves of Ankarana have yielded 19 species, yet only nine remain in the surrounding forests. In the northwest, 10 or 11 subfossil species have been found at Anjohibe, whereas only six species remain at nearby Ankarafantsika National Park
Ankarafantsika National Park
Ankarafantsika National Park is a National Park in the Boeny Region of Madagascar. The closest city is Majunga 115 km north of the park. Ankarafantsika is mostly tropical in climate type. The Sakalava people are the predominate ethnic group in the park. The rodent Macrotarsomys ingens occurs only...
.
As with the extinctions that occurred on other land masses during the late Pleistocene and Holocene (known as the Quaternary extinction event
Quaternary extinction event
The Quaternary period saw the extinctions of numerous predominantly larger, especially megafaunal, species, many of which occurred during the transition from the Pleistocene to the Holocene epoch. However, the extinction wave did not stop at the end of the Pleistocene, but continued especially on...
), the disappearance of Madagascar's megafauna is tightly linked with the arrival of humans, with nearly all extinctions dating to around the same time of the earliest evidence of human activity on the island or significantly later. The exact date of human arrival is unknown, although a radius
Radius (bone)
The radius is one of the two large bones of the forearm, the other being the ulna. It extends from the lateral side of the elbow to the thumb side of the wrist and runs parallel to the ulna, which exceeds it in length and size. It is a long bone, prism-shaped and slightly curved longitudinally...
(arm bone) of a Palaeopropithecus ingens with distinct cut marks from the removal of flesh with sharp objects dates to approximately 2325 ± 43 BP (2366–2315 cal yr BP). Based on this evidence from Taolambiby in the southwest interior, as well as other dates for human-modified dwarf hippo bones and introduced plant pollen from other parts of the island, the arrival of humans is conservatively estimated at approximately 350 cal yr BCE. Measurements of stratigraphic charcoal
Stratigraphy
Stratigraphy, a branch of geology, studies rock layers and layering . It is primarily used in the study of sedimentary and layered volcanic rocks....
and the appearance of exotic plant pollen dated from Holocene core sample
Core sample
A core sample is a cylindrical section of a naturally occurring substance. Most core samples are obtained by drilling with special drills into the substance, for example sediment or rock, with a hollow steel tube called a core drill. The hole made for the core sample is called the "core hole". A...
s confirm these approximated dates for human arrival in the southwestern corner of the island and further suggest that the central and northern parts of the island did not experience significant human impact until 700 to 1,500 years later. The humid forests of the lower interior of the island were the last to be settled (as shown by the presence of charcoal particles), possibly due to the prevalence of human diseases, such as plague, malaria
Malaria
Malaria is a mosquito-borne infectious disease of humans and other animals caused by eukaryotic protists of the genus Plasmodium. The disease results from the multiplication of Plasmodium parasites within red blood cells, causing symptoms that typically include fever and headache, in severe cases...
, and dysentery
Dysentery
Dysentery is an inflammatory disorder of the intestine, especially of the colon, that results in severe diarrhea containing mucus and/or blood in the faeces with fever and abdominal pain. If left untreated, dysentery can be fatal.There are differences between dysentery and normal bloody diarrhoea...
. The entire island was not fully colonized by humans until the beginning of the second millennium CE.
The extinction of Madagascar's megafauna, including the giant lemurs, was one of the most recent in history, with large lemur species like Palaeopropithecus ingens surviving until approximately 500 years ago and one bone of the extinct Hippopotamus laloumena radiocarbon dated
Radiocarbon dating
Radiocarbon dating is a radiometric dating method that uses the naturally occurring radioisotope carbon-14 to estimate the age of carbon-bearing materials up to about 58,000 to 62,000 years. Raw, i.e. uncalibrated, radiocarbon ages are usually reported in radiocarbon years "Before Present" ,...
to about 100 years BP An even wider extinction window for the subfossil lemurs, ranging up until the 20th century, may be possible if reports of unidentified animals are true. As recently as the early 17th century, dwindling populations of subfossil lemurs may have persisted in coastal regions where tree-cutting and uncontrolled fires had less of an impact. By that date, the Central Highlands' forests were mostly gone, with the exception of scattered forest fragments and strips. Along the northwest coast, forms such as Archaeolemur may have survived for more than a millennium after the arrival of humans. This is supported by radiocarbon dates for Archaeolemur from the Ankarana Massif dating to 975 ± 50 CE as well as archaeological data that show there was little human activity in the area until a few centuries ago, with low human population density along the northwest coast until nearly 1500 CE.
Hypotheses
In the 20th century, six hypotheses for explaining the extinction of the giant subfossil lemurs have been proposed and tested. They are known as the "Great Fire", "Great Drought", "Blitzkrieg", "Biological Invasion", "Hypervirulent Disease", and "Synergy" hypotheses. The first was proposed in 1927 when Henri Humbert and other botanists working in Madagascar suspected that human-introduced fire and uncontrolled burning intended to create pasture and fields for crops transformed the habits quickly across the island. In 1972, Mahé and Sourdat proposed that the arid south had become progressively drier, slowly killing off lemur fauna as the climate changed. Paul S. Martin applied his overkill hypothesis or "blitzkrieg" model to explain the loss of the Malagasy megafauna in 1984, predicting a rapid die-off as humans spread in a wave across the island, hunting the large species to extinction. That same year, Robert Dewar speculated that introducedIntroduced species
An introduced species — or neozoon, alien, exotic, non-indigenous, or non-native species, or simply an introduction, is a species living outside its indigenous or native distributional range, and has arrived in an ecosystem or plant community by human activity, either deliberate or accidental...
livestock outcompeted the endemic wildlife in a moderately fast series of multiple waves across the island. In 1997, MacPhee and Marx speculated that a rapid spread of hypervirulent
Virulence
Virulence is by MeSH definition the degree of pathogenicity within a group or species of parasites as indicated by case fatality rates and/or the ability of the organism to invade the tissues of the host. The pathogenicity of an organism - its ability to cause disease - is determined by its...
disease might explain the die-offs that occurred after the appearance of humans worldwide, including Madagascar. Finally, in 1999, David Burney proposed that the complete set of human impacts worked together, in some cases along with natural climate change, and very slowly brought about the demise of the giant subfossil lemurs and other recently extinct endemic wildlife.
Since all extinct lemurs were larger than the ones that currently survive, and the remaining large forests still support large populations of smaller lemurs, large size appears to have conveyed some distinct disadvantages. Large-bodied animals require larger habitats in order to maintain viable populations, and are most strongly impacted by habitat loss and fragmentation
Habitat destruction
Habitat destruction is the process in which natural habitat is rendered functionally unable to support the species present. In this process, the organisms that previously used the site are displaced or destroyed, reducing biodiversity. Habitat destruction by human activity mainly for the purpose of...
. Large folivores typically have slower reproductive rates, live in smaller groups, and have low dispersal rates (vagility), making them especially vulnerable to habitat loss, hunting pressure, and possibly disease. Large, slow-moving animals are often easier to hunt and provide a larger amount of food than smaller prey. Furthermore, leaf-eating, large-bodied slow climbers, and semiterrestrial seed predators and omnivores disappeared completely, suggesting an extinction pattern based on habitat use.
Since the subfossil bones of extinct lemurs have been found alongside the remains of highly arboreal living lemur species, we know that much of Madagascar had been covered in forest prior to the arrival of humans; however, the forest coverage of the high plateau region has been debated. Humbert and other botanists suggested that the central plateau had once been blanketed in forest, later to be destroyed by fire for use by humans. However, recent paleoenvironmental studies by Burney have shown that the grasslands of that region have fluctuated over the course of millennia and were not entirely created by humans. Similarly, the role humans played in the aridification of the south and southwest has been questioned, since natural drying of the climate started before human arrival. The marshes of the region (in which subfossil remains have been found) have dried up, subfossil sites have yielded a host of arboreal lemurs, and site names, such as Ankilitelo ("place of three kily or tamarind trees
Tamarind
Tamarind is a tree in the family Fabaceae. The genus Tamarindus is monotypic .-Origin:...
") suggest a recent wetter past. Pollen studies have shown that the aridification process began nearly 3,000 years ago, and peaked 1,000 years prior to the time of the extinctions. However, no extinctions occurred prior to the arrival of humans, and the recent climatic changes have not been as severe as those prior to human arrival, suggesting that humans and their effect on the vegetation did play a role in the extinctions. The central plateau lost more species than the dry south and southwest, suggesting that degraded habitats were more affected than arid habitats.
Over-hunting by humans has been one of the most widely accepted hypotheses for the ultimate demise of the subfossil lemurs. The extinctions and human hunting pressure are associated due to the synchronicity of human arrival and species decline, as well as the suspected naïveté of the Malagasy wildlife during the early encounters with human hunters. Despite the assumptions, evidence of butchery has been minimal until recently, although folk memories of rituals associated with the killing of megafauna have been reported. Archeological evidence for butchery of giant subfossil lemurs, including Palaeopropithecus ingens and Pachylemur insignis, was found on specimens from two sites in southwestern Madagascar, Taolambiby and Tsirave. Although the bones had been collected in the early 20th century and lacked stratigraphic records, one of the bones with tool marks had been dated to the time of the first arrival of humans. Tool-induced bone alterations, in the form of cuts and chop marks near joints and other characteristic cuts and fractures, indicated the early human settlers skinned, disarticulated, and filleted giant lemurs. Prior to these finds, only modified bones of dwarf hippos and elephant birds, as well as giant aye-aye teeth, had been found.
Although there is evidence that habitat loss, hunting, and other factors played a role in the demise of the subfossil lemurs, prior to the synergy hypothesis, each had its own discrepancies. Humans may have hunted the giant lemurs for food, but no signs of game-dependent butchery have been found. In fact, Madagascar was colonized by Iron-age pastoralists, horticulturalists, and fishermen, not big-game hunters. Additionally, the blitzkrieg hypothesis predicts extinction within 100 and 1,000 years as humans sweep across the island, yet humans lived alongside the giant lemurs for more than 1,500 years. Alternatively, habitat loss and deforestation have been argued against because many giant lemurs were thought to be terrestrial, they are missing from undisturbed forested habitats, and their environment was not fully forested prior to the arrival of humans. Anthropologist Laurie Godfrey defended the effects of habitat loss by pointing out that most of the extinct lemurs have been shown to have been at least partly arboreal and dependent upon leaves and seeds for food, and also that these large-bodied specialists would be most vulnerable to habitat disturbance and fragmentation due to their low reproductive resilience and their need for large, undisturbed habitats. Still, much of the island remained covered in forest, even into the 20th century.
Linking human colonization to a specific cause for extinction has been difficult since human activities have varied from region to region. Although no single human activity can account for the extinction of the giant subfossil lemurs, the humans are still regarded as being primarily responsible. Each of the contributing human-caused factors played a role (having a synergistic effect
Synergy
Synergy may be defined as two or more things functioning together to produce a result not independently obtainable.The term synergy comes from the Greek word from , , meaning "working together".-Definitions and usages:...
) in varying degrees. Even the most widespread and adaptable species, such as Archaeolemur, were able to survive despite hunting pressure and human-caused habitat change until human population growth and other factors reached a tipping point, cumulatively resulting in their extinction.
Extinction timeline and the primary trigger
While it is generally agreed that both human and natural factors contributed to the subfossil lemur extinction, studies of sediment cores have helped to clarify the general timeline and initial sequence of events. SporeSpore
In biology, a spore is a reproductive structure that is adapted for dispersal and surviving for extended periods of time in unfavorable conditions. Spores form part of the life cycles of many bacteria, plants, algae, fungi and some protozoa. According to scientist Dr...
s of the coprophilous fungus
Coprophilous fungi
Coprophilous fungi are a type of saprobic fungi that grow on animal dung. The hardy spores of coprophilous species are unwittingly consumed by herbivores from vegetation, and are excreted along with the plant matter...
, Sporormiella
Sporormiella
Sporormiella is a genus of fungi in the Sporormiaceae family. Species of the genus are obligately coprophilous, occurring on the dung of domestic livestock as well as wild herbivores. The genus is distributed across boreal and temperate regions of the world, and contains about 80 species...
, found in sediment cores experienced a dramatic decline shortly after the arrival of humans. Since this fungus
Fungus
A fungus is a member of a large group of eukaryotic organisms that includes microorganisms such as yeasts and molds , as well as the more familiar mushrooms. These organisms are classified as a kingdom, Fungi, which is separate from plants, animals, and bacteria...
cannot complete its life cycle without dung from large animals, its decline also indicates a sharp decline in giant subfossil lemur populations, as well as other large herbivores, starting around 230–410 cal yr CE. Following the decline of megafauna, the presence of charcoal particles increased significantly, starting in the southwest corner of the island, gradually spreading to the other coasts and the island's interior over the next 1,000 years. The first evidence for the introduction of cattle to the island dates to 1,000 years after the initial decline of coprophilous fungal spores.
The loss of grazers and browsers might have resulted in the accumulation of excessive plant material and litter, promoting more frequent and destructive wildfires, which would explain the rise in charcoal particles following the decline in coprophilous fungus spores. This in turn resulted in ecological restructuring through the elimination of the wooded savannas and preferred arboreal habits on which the giant subfossil lemurs depended. This left their populations at unsustainably low levels, and factors such as their slow reproduction, continued habitat degradation, increased competition with introduced species, and continued hunting (although at lower levels, depending on the region) prevented them from recovering and gradually resulted in their extinction.
Hunting is thought to have caused the initial rapid decline, referred to as the primary trigger, although other explanations may be plausible. In theory, habitat loss should affect frugivores more than folivores, since leaves are more widely available. However, both large-bodied frugivores and large-bodied folivores disappeared simultaneously, while smaller species remained. Furthermore, other large non-primate grazers also disappeared around the same time. Consequently, large body size has been shown to have the strongest link to the extinctions—more so than activity patterns or diet. Since large animals are more attractive as prey, fungal spores associated with their dung declined rapidly with the arrival of humans, and butchery marks have been found on giant subfossil lemur remains, hunting appears to be a plausible explanation for the initial decline of the megafauna.
By region, studies have revealed specific details that have helped outline the series of events that led to the extinction of the local megafauna. In the Central Highlands, dense forests existed until 1600 CE, with lingering patches persisting until the 19th and 20th centuries. Today, small fragments stand isolated among vast expanses of human-created savanna, despite an average annual rainfall that is sufficient to sustain the evergreen forests once found there. Deliberately set fires were the cause of the deforestation, and forest regrowth is restricted by soil erosion
Erosion
Erosion is when materials are removed from the surface and changed into something else. It only works by hydraulic actions and transport of solids in the natural environment, and leads to the deposition of these materials elsewhere...
and the presence of fire-resistant, exotic grasses. In the southeast, an extended drought dating to 950 cal yr BP led to fires and transition of open grasslands. The drought may also have pushed humans populations to rely more heavily on bushmeat
Bushmeat
Bushmeat initially referred to the hunting of wild animals in West and Central Africa and is a calque from the French viande de brousse. Today the term is commonly used for meat of terrestrial wild animals, killed for subsistence or commercial purposes throughout the humid tropics of the Americas,...
. Had humans not been present, the subfossil lemur populations might have adjusted to the new conditions and recovered. Had the drought not reduced the population of the subfossil lemurs, the pressure from the small number of people living in the region at the time might not have been enough to cause the extinctions. As in the past, all of the factors that have played a role in past extinctions are still present and active today. As a result, the extinction event that claimed Madagascar's giant subfossil lemurs has not fully concluded.
Lingering populations and oral tradition
Recent radiocarbon dates from accelerator mass spectrometryAccelerator mass spectrometry
Accelerator mass spectrometry differs from other forms of mass spectrometry in that it accelerates ions to extraordinarily high kinetic energies before mass analysis. The special strength of AMS among the mass spectrometric methods is its power to separate a rare isotope from an abundant...
14C dating, such as 630 ± 50 BP for Megaladapis remains and 510 ± 80 BP for Palaeopropithecus remains, indicate that the giant lemurs survived into modern times. Moreover, it is likely that memories of these creatures persist in the oral tradition
Oral tradition
Oral tradition and oral lore is cultural material and traditions transmitted orally from one generation to another. The messages or testimony are verbally transmitted in speech or song and may take the form, for example, of folktales, sayings, ballads, songs, or chants...
s of some Malagasy cultural groups. Some recent stories from around Belo sur Mer
Belo sur Mer
Belo sur Mer is a town and commune in Madagascar. It belongs to the district of Morondava, which is a part of Menabe Region. The population of the commune was estimated to be approximately 8,000 in 2001 commune census....
in southwestern Madagascar might even suggest that some of the giant subfossil lemurs still survive in remote forests.
Flacourt's 1658 description of the tretretretre or tratratratra was the first mention of the now extinct giant lemurs in Western culture, although it is unclear whether he saw it. The creature Flacourt described has traditionally been interpreted as a species of Megaladapis. However, the size may have been exaggerated, and the "round head and a human face" would not match Megaladapis, which had an enlarged snout and eyes that did not face entirely forward. In fact, Megaladapis had the least forward-facing eyes of all primates. The facial description, along with the mention of a short tail, solitary habits, and other traits better match the most recent interpretation—Palaeopropithecus. Likewise, Malagasy tales recorded by the 19th-century folklorist Gabriel Ferrand describing a large animal with a flat, human-like face that was unable to negotiate smooth, rock outcrops best match Palaeopropithecus, which would also have had difficulty on flat, smooth surfaces.
In 1995, a research team led by David Burney and Ramilisonina
Ramilisonina
Ramilisonina is an archaeologist from Madagascar.His work has focused on the prehistory of Madagascar, especially the period between the fifteenth and nineteenth centuries...
performed interviews in and around Belo sur Mer, including Ambararata and Antsira, in order to locate subfossil megafaunal sites used early in the century by other paleontologists. During carefully controlled interviews, the team recorded stories of recent sightings of dwarf hippos (called kilopilopitsofy) and of a large, lemur-like creature known as kidoky; a report of the interviews was published in 1998 with encouragement from primatologist Alison Jolly
Alison Jolly
Alison Jolly is a primatologist, known for her studies of lemur biology. She has written several books for both popular and scientific audiences and conducted extensive fieldwork on Lemurs in Madagascar, primarily at the Berenty Reserve, a small private reserve of gallery forest set in the...
and anthropologist Laurie Godfrey. In one interview, an 85-year-old man named Jean Noelson Pascou recounted seeing the rare kidoky up close in 1952. Pascou said that the animal looks similar to a sifaka, but had a human-like face, and was "the size of a seven-year-old girl." It had dark fur and a discernible white spot both on the forehead and below the mouth. According to Pascou, it was a shy animal that fled on the ground instead of in the trees. Burney interpreted the old man as saying that it moved in "a series of leaps", but Godfrey later claimed that "a series of bounds" was a better translation—a description that would closely match the foot anatomy of monkey lemurs, such as Hadropithecus and Archaeolemur. Pascou was also able to imitate its call, a long single "whoop", and said that kidoky would come closer and continue calling if he imitated the call correctly. The call Pascou imitated was comparable to that of a short call for an indri, from the other side of the island. When shown a picture of an indri, Pascou said kidoky did not look like that, and that it had a rounder face, more similar to a sifaka. Pascou also speculated that kidoky could stand on two legs and that it was a solitary animal.
Another interviewee, François, a middle-aged woodcutter who spent time in the forests inland (east) from the main road between Morondava
Morondava
Morondava is a city located in Menabe Region, of which it is the capital, in Madagascar. It is located in the delta of the Morandava River at .-Communication:...
and Belo sur Mer, along with five of his friends, reported seeing kidoky recently. Their description of the animal and François's imitation of its long call were virtually identical to Pascou's. One of the young men insisted that its fur had a lot of white in it, but the other men could not confirm that. François and his friends reported that it had never climbed a tree in their presence, and that it flees on the ground in short leaps or bounds. When Burney imitated the sideways leaping of a sifaka moving on the ground, one of the men corrected him, pointing out that he was imitating a sifaka. The man's imitation of the gallop kidoky used was very baboon-like. The men also reported that imitating its call can draw the animal closer and cause it to continue calling.
Burney and Ramilisonina admitted that the most parsimonious explanation for the sightings was that kidoky was a misidentified sifaka or other larger living lemur species. However, the authors did not feel comfortable with such a dismissal because of their careful quizzing and use of unlabeled color plates during the interviews and because of the competence demonstrated by the interviewees in regards to local wildlife and lemur habits. The possibility of a wild, introduced baboon surviving in the forests could not be dismissed. However, the descriptions of kidoky, with its terrestrial, baboon-like gait, make Hadropithecus and Archaeolemur the most plausible candidates among the giant subfossil lemurs. At the very least, the stories support a wider extinction window for the giant subfossil lemurs, suggesting that their extinction was recent enough for such vivid stories to still survive in the oral traditions of the Malagasy people.