Subfossil lemur

A giant lemur with long arms, short legs, hangs vertically from a tree, with one arm held off to the side. Its hands show very long, curved fingers.
Palaeopropithecus ingens, an extinct species of sloth lemur

Subfossil lemurs are lemurs from Madagascar that are represented by recent (subfossil) remains dating from nearly 26,000 years ago to approximately 560 years ago (from the late Pleistocene until the Holocene). 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 160 kg (350 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 niches 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 lemurs). 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 lemurs".

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; 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 hunting likely played a role in the rapid decline of the lemurs and the other megafauna that once existed on the large island. Additional factors are thought to have contributed to their ultimate disappearance. Oral traditions and recent reports of sightings by Malagasy villagers have been interpreted by some as suggesting either lingering populations or very recent extinctions.

Diversity

Extinct giant lemurs

Until recently, giant lemurs existed in 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.[1] All 17 extinct lemurs were larger than the extant forms, including the largest living lemurs, the indri (Indri indri) and diademed sifaka (Propithecus diadema), which weigh up to 9.5 kg (21 lb).[2] 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 bones (such as the humerus).[3] 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 160 kg (350 lb).[4]

All but one species, the giant aye-aye, are thought to have been active during the day.[5] Not only were they unlike the living lemurs in both size and appearance, they also filled ecological niches that no longer exist or are now left unoccupied.[1] 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.[6] 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).[6][7]

Characteristics

All of the extinct subfossil lemurs, including the smallest species (Pachylemur, Mesopropithecus, and the giant aye-aye), were larger than the lemur species alive today. The largest species were among the largest primates 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.[8] Like other lemurs, the subfossil lemurs did not exhibit appreciable differences in body or canine tooth size between males and females (sexual dimorphism).[8] This suggests that they, too, exhibited female social dominance, possibly exhibiting the same levels of agonism (aggressive competition) seen in extant lemurs.[9] 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,[8][9] suggesting faster sexual maturity of their offspring.[8] Most subfossil lemurs also had high retinal summation (sensitivity to low light), resulting in poor day vision (low visual acuity) compared to anthropoids.[8][9] 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.[9]

These traits are shared among both living and extinct lemurs, but 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 monkeys, Godfrey et al. (2003) argued that the energy frugality hypothesis seems to best explain both living and extinct lemur adaptations.[9]

A lemur skull, seen from the right.
The skull and teeth of Pachylemur insignis suggest that it ate mostly fruit and some leaves.

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.[6][9]

Their skeletons suggest that most subfossil lemurs were tree-dwellers, adapted for living in forests and possibly limited to such habitats.[6][8][9] Unlike some of the living species, the subfossil lemurs lacked adaptations for leaping. Instead, suspension, used by some indriids and ruffed lemurs, was extensively used in some lineages. Living lemurs are known to visit the ground to varying extents, but 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.[8] They had shorter, more robust limbs, heavily built axial skeletons (trunks), and large heads[10] and are thought to have shared the common lemur trait of low basal metabolic rates, making them slow-moving.[9] Studies of their semicircular canals confirm this assumption, showing that koala lemurs moved slower than orangutans, monkey lemurs were less agile than Old World monkeys, and sloth lemurs exhibited slow movements like those of lorises and sloths.[11]

Types

Archaeoindris was the largest of the sloth lemurs, and the largest known lemur. It weighed approximately 160 kg (350 lb).
Sloth lemurs

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,[9] or in the case of Archaeoindris, with giant ground sloths.[12] They ranged in size from some of the smallest of the subfossil lemurs, such as Mesopropithecus, weighing as little as 10 kg (22 lb),[12] to the largest, Archaeoindris, weighing approximately 160 kg (350 lb).[4] 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.[9][13] Their day vision was very poor, and they had relatively small brains and short tails.[8] Their diet consisted mostly of leaves, seeds, and fruit;[8][9] dental wear analysis suggests they were primarily folivorous seed-predators.[14]

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 lemurs of the family Lepilemuridae due to similarities in their skulls and molar teeth.[12] They were slow climbers and had long forelimbs and powerful grasping feet, possibly using them for suspension.[8][12] Koala lemurs ranged in size from an estimated 45 to 85 kg (99 to 187 lb),[12] making them as large as a male orangutan or a female gorilla.[9] They had poor day vision, short tails, lacked permanent upper incisors, and had a reduced toothcomb.[8] Their diet generally consisted of leaves,[8][9] with some species being specialized folivores and others having a broader diet, possibly including tough seeds.[14]

A giant lemur walks on all four feet, with a dark tail held low. The head has a short snout (for a lemur).
A full-body, right side profile of giant lemur walking on all four feet, with a bushy tail head up in the air. The head has a long snout compared to a monkey, but on par with that of a lemur.
Monkey lemurs, such as Hadropithecus stenognathus (above) and Archaeolemur edwardsi (below), were the most terrestrial of the lemurs.
Monkey lemurs

Monkey lemurs, or baboon lemurs, share similarities with macaques; they have also been compared to baboons.[9][15] Members of the family Archaeolemuridae, they were the most terrestrial of the lemurs,[9][12] with short, robust forelimbs and relatively flat digits. They spent time on the ground, and were semi-terrestrial, spending time in trees to feed and sleep. They were heavy-bodied and ranged in size from approximately 13 to 35 kg (29 to 77 lb).[8][12] They had relatively good day vision and large brains compared with other lemurs.[8] 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).[8][9][12] 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.[14] 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.[16]

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.[8] These shared features 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 (31 lb), it was between two-and-half and five times the size of living aye-aye.[7][12] Alive when humans came to Madagascar, its teeth were collected and drilled to make necklaces.[9]

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,[9] weighing between 10 and 13 kg (22 and 29 lb).[12] Despite their size, they were arboreal quadrupeds, possibly utilizing more suspensory behavior and cautious climbing than their sister taxon.[7][12][15] 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.[8][9]

Phylogeny

Determining the phylogeny 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 lemurs).[17] The placement of family Megaladapidae has been more controversial, with similarities in teeth and skull features suggesting a close relationship with family Lepilemuridae (sportive lemurs).[17][8] Molecular data, instead, indicate a closer relationship to family Lemuridae.[17] 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.[17] 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).[8]

Subfossil lemur phylogeny[8][18][19]
 Lemuriformes 
 Daubentoniidae 

Daubentonia madagascariensis

Daubentonia robusta

 †Megaladapis 

Megaladapis edwardsi

Megaladapis grandidieri

Megaladapis madagascariensis

 Lemuridae 
 †Pachylemur 

Pachylemur insignis

Pachylemur jullyi

Varecia

Lemur, Hapalemur, & Prolemur

Eulemur

Cheirogaleidae (Allocebus, Phaner, Cheirogaleus, Mirza, & Microcebus)

Lepilemur

 †Archaeolemuridae 
 †Archaeolemur 

Archaeolemur majori

Archaeolemur edwardsi

Hadropithecus stenognathus

 †Palaeopropithecidae 
 †Mesopropithecus 

Mesopropithecus pithecoides

Mesopropithecus globiceps

Mesopropithecus dolichobrachion

Babakotia radofilai

 †Palaeopropithecus 

Palaeopropithecus maximus

Palaeopropithecus ingens

Palaeopropithecus kelyus

Archaeoindris fontoynontii

Indriidae (Propithecus, Avahi, & Indri)

Living species

A medium-sized lemur clings to a tree while looking over its shoulder. It has a very short tail and its face, hands, and upper back are black while the rest of it is white.
Subfossil remains of the indri (Indri indri) suggest a recent and significant reduction in its geographic range.

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. In some cases living species are locally extinct 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 ranges have contracted for numerous species, including the indri, greater bamboo lemur, and ruffed lemurs.[6] For instance, subfossil remains of the indri have been found in marsh deposits near Ampasambazimba in the Central Highlands[20] 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.[6] 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,[6][21] with subfossil remains from Ankarana Massif in the far north of Madagascar dating to 2565 BCE ± 70 years.[22] 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.[6][21] 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 sifakas.[6][20]

In addition to previously having expanded geographic ranges, extant subfossil lemurs exhibited significant variation in size.[23] Researchers have noted that subfossil bones of living species are more robust and generally larger than their present-day counterparts.[20] 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.[23]