Subfossil lemur

See also: Lemur

Babakotia radofilai, an extinct subfossil lemur and a type of sloth lemur.

Subfossil lemurs are lemurs from Madagascar that are represented by recent (subfossil) remains dating from the late Pleistocene to approximately 500 years ago (BP). They include both living and extinct species, although term more frequently refers to the extinct giant lemurs. The diversity of subfossil lemur communities was higher than that of present-day lemur communities, ranging as high as 20 or more species, compared to 10 to 12 species today. Extinct species ranged in size from slightly over 10 kg (22 lb) to roughly 200 kg (440 lb). Even the subfossil remains of living species are larger and more robust than modern specimens. The subfossil sites found around most of the island demonstrate that most giant lemurs had wide geographic ranges 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 poor day vision, small brains, a lack of male dominance, and rapid development. 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, including the Giant Aye-aye and Pachylemur, a genus of "giant ruffed lemurs." The sloth lemurs were most closely related to the living indriids (Indri, sifakas, and woolly lemurs), while the monkey lemurs were the next closest relatives of clade formed by the sloth lemurs and indriids. The koala lemurs were most closely related to family Lemuridae, which contains the Ring-tailed Lemur, ruffed lemurs, true lemurs, and bamboo lemurs.

Subfossil remains were first discovered on Madagascar in the 1860s, but giant lemur species were not formally described until the 1890s. Their remains are fresh, 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 their demise, along with the other megafauna that once existed on the large island.

Ecology

As a group, the lemurs of Madagascar are extremely diverse, having evolved in isolation and radiated over the past 40 to 60 million years to fill many ecological niches normally occupied by higher primates. In the recent past, their diversity was significantly greater, with 17 extinct species sharing body proportions and specializations with lorises and various non-primates, such as tree sloths, giant ground sloths, koalas, and striped possums. 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. The extinct lemurs filled a wide range of niches, including those outside of the gallery forests that surviving lemur species are most often studied in. Just like living species, many of the extinct species shared overlapping ranges with closely related species (sympatry) through 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, not all habitats in which they occurred would have allowed them to be strictly arboreal, including gallery forests and the spiny forests of southern Madagascar. Even today, most lemurs species will visit the ground the cross open areas, indicating 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 their differences in niche preference. Within related groups, larger species tend to inhabit wetter, more productive habitats, 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 ecosystems. Thermoregulation may also have played a role. Yet despite this pressure to specialize and differentiate, some of the extinct subfossil lemurs, such as Archaeolemur, had island-wide distributions during the Holocene, unlike the living lemurs. These wider distribution patterns among the extinct lemurs suggest that larger lemurs might have been more tolerant to ecological change 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 (folivores), 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-bodied lemurs. In certain cases, some subfossil lemurs, such as the sloth lemurs and koala lemurs, may have used leaves an important fallback food, whereas other species, such as the monkey lemurs and the Giant Aye-aye, specialized on structurally-defended resources. Yet others, such as Pachylemur was primarily a fruit eater (frugivorous). Subfossil lemur diets have been reconstructed using analytical tools, including dental gross morphology, shearing quotients, microwear, mesowear, dental microstructure, biogeochemistry, 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, a group of plants that 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, plant groups that use more recently evolved 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 in order to divide resources and coexist (niche differentiation). 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 dispersal, possibly targeting species that did not attract the seed dispersal services of the extinct elephant birds. 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 by attaching the seeds to the animals body (epizoochory), and both processes were likely facilitated by the subfossil lemurs. Seeds from Uncarina (family Pedaliaceae) 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, including Adansonia, Cedrelopsis (family Meliaceae), Commiphora, Delonix, Diospyros, Grewia, Pachypodium, Salvadora, Strychnos, and Tamarindus. For example, Delonix has edible pods that 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 (0.79 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 lemurs, could probably swallow even larger seeds. Seed dispersal limitations tied to megafaunal extinction is exhibited by Commiphora guillaminii. At present, the 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 is still has its seeds dispersed by large animals.

Diversity

Extinct giant lemurs

Until recently, giant lemurs existed on Madagascar. Although they are only represented by recent or 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, some weighing as much as 200 kg (440 lb), and are thought to have been active during the day. Not only were they were unlike the living lemurs in both size and appearance, they also filled ecological niches 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.

Characteristics

All of the extinct subfossil lemurs, including the smallest species (e.g. Pachylemur, Mesopropithecus, and the Giant Aye-aye), were larger than the lemur species alive today. The largest species were among the largest primates to ever evolve. Due to their larger size, the extinct subfossil lemurs have been compared to large-bodied anthropoids (monkeys and apes), yet in more ways 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 (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 compared to those of comparatively-sized anthropoids. Most species also had a unique strepsirrhine dental trait, called a toothcomb, which is used for grooming. Most subfossil lemurs also had high retinal summation (sensitivity to low light), resulting in poor day vision (low visual acuity) compared to anthropoids. Even tooth development and weaning was rapid compared to like-sized anthropoids, suggesting faster sexual maturity of their offspring.

Despite the similarities, subfossil lemurs had several distinct differences from their lemur relatives. In addition to being larger, the subfossil lemurs were more dependent upon leaves and seeds in their diet, rather than fruit; they utilized slow climbing, hanging, and terrestrial quadrupedalism for locomotion more-so than vertical clinging and leaping and arboreal quadrupedalism; and all but one of them—the Giant Aye-aye—were assumed to be diurnal (due to their body size and small orbits), whereas many small lemurs are nocturnal and medium-sized are cathemeral (active both day and night).

Locomotion of subfossil lemurs has been studied to help understand where they lived and their behavior. Their skeletons suggest that most were tree-dwellers, adapted for living in forests and possibly limited to such habitats. Unlike some of the living lemurs, the subfossil lemurs lacked adapatations for leaping. Instead, suspension, used by some indriids and ruffed lemurs, was extensively used in some lineages. Although living lemurs are known to visit the ground to varying extents, only the extinct archaeolemurids exhibit the 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 skeletons (trunks), and large heads and are thought to have share the common lemur trait of low basal metabolic rates, making them slower in movement. Studies of their semicircular canals confirm this assumption, showing that koala lemurs moved slower than oranguatans, monkey lemurs were less agile than Old World monkeys, and sloth lemurs exhibited slower movements of lorises and sloths.

Types

Sloth lemurs

Further information: [[:Sloth lemur]]

The sloth lemurs were the most speciose group of the subfossil lemurs. Belonging to family Palaeopropithecidae, they included four genera and eight species. The common name is due to strong similarities in morphology with arboreal sloths, or in the case of Archaeoindris, a giant ground sloth. 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 lb). Their characteristic curved finger and toe bones (phalanges) suggest slow suspensory movement, similar to that of an orangutan or a loris, making them one of the most specialized mammals for suspension to have evolved. Their day vision was very poor, and they had relatively small brains and short tails. Their diet consisted primarily of leaves, seeds, and fruit, although dental wear analysis suggests it was primarily a folivorous seed-predator.

Koala lemurs

Further information: [[:Koala lemur]]

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 lemurs of family Lemuridae, although for many years they were paired with the sportive lemurs of the family Lepilemur due to similarities in their skull and moral 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 to 187 lb), making them as large as a male orangutan or a female gorilla. They had poor day vision, short tails, lacked permanent upper incisors, and had a reduced toothcomb. Their diet generally consisted of leaves, with some species being specialized folivores and others having a broader diet, possibly including tough seeds.

Monkey lemurs

Further information: [[:Monkey lemur]]

Monkey lemurs, or baboon lemurs, share similarities with macaques, although they have also been compared to baboons. Members of the family Archaeolemuridae, they were the most terrestrial of the lemurs, with short, robust forelimbs and relatively flat digits. Although they spend 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 (29 to 77 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 also have had a more varied diet, including leaves, fruit, and animal matter (omnivory). Dental wear analysis has shed little 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 go extinct.

Giant Aye-aye

Further information: [[:Giant Aye-aye]]

An extinct, giant relative of the living Aye-aye, the Giant Aye-aye shared at least two of the Aye-ayes 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 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. Alive when humans came to Madagascar, its teeth were collected and drilled to make necklaces.

Pachylemur

Further information: [[: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", it was approximately three times larger than ruffed lemurs, weighing between 10 to 13 kg (22 to 29 lb). Despite its size, it was an arboreal quadruped, possibly utilizing more suspensory behavior and cautious climbing that its sister taxon. Its skull and teeth were similar to that of ruffed lemurs, suggesting a diet high in fruit and possibly some leaves. The rest of its skeleton (postcrania) was much more robust and its vertebrate had distinctly different features.

Phylogeny

Further information: [[:Lemur evolutionary history]]

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 lumping the four sloth lemur genera of the family Palaeopropithecidae with the family Indriidae (including the Indri, sifakas, and woolly lemurs). 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). Molecular data, instead, indicates a closer relationship to family Lemuridae (true lemurs, ruffed lemurs, bamboo lemurs, and the Ring-tailed Lemur). Likewise, a relationship between family Archaeolemuridae and family Lemuridae, 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).

Subfossil lemur phylogeny

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

Subfossil remains of the Indri (Indri indri) suggest a recent and significant reduction in its geographic range.

Subfossil sites in Madagsacar dating have yielded the remains of more than just extinct lemurs. Extant lemurs 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 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, ruffed lemurs, and others. For instance, subfossil remains of the Indri have been found in marsh deposits near Ampasambazimba in the central highlands. Other Indri subfossil remains have been found 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, used to range across the northern, northwestern, central, and eastern parts of the island. It is unclear whether these location had wetter in the past or whether distinct subpopulations or subspecies occupied the drier forests, much like modern diversity of sifakas.

In addition to 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.

Discovery and research

The first subfossil remains of lemurs—a humerus from Palaeopropithecus and a tibia of a sifaka—were uncovered by Alfred Grandidier in 1865 at Ambolisatra. However, Charles Immanuel Forsyth Major was the first to formally describe a giant lemur species in 1893 with the discovery of 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. However, a review from 1905 by Guillaume Grandidier established most of the presently-known family and genera names for the extinct lemurs.

Extinction

Similar to other continents, the decline of Madagascar's large mammals coincided with the arrival of humans.

See also: Quaternary extinction event

All known species of giant subfossil lemur went extinct during the Holocene, with all or most extinctions happening after the colonization of Madagascar by humans 2,000 years ago. Madagascar's megafauna included not only giant lemurs, but also included elephant birds, giant tortoises, a dwarf Malagasy Hippopotamus, the Giant Fossa, and Plesiorycteropus, a unique aardvark-like mammal, all of which died out during the same time period. Madagascar's megafaunal extinctions were one of the most severe for any continent or large islands, having lost all of its endemic wildlife over 10 kg (22 lb). This extinction event was one of the most recent in history, with large lemur species like Palaeopropithecus ingens surviving until approximately 500 years ago and the Malagasy Hippopotamus disappearing around 100 years ago.

References

Books cited

• MacPhee (Editor), R.D.E.; Sues, H.-D. (eds.). Extinction in Near Time. Springer. ISBN 978-0306460920. {{cite book}}: |editor1-last= has generic name (help)

• Burney, D.A. (1999). "Chapter 7: Rates, patterns, and processes of landscape transformation and extinction in Madagascar". pp. 145–164. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)

• Garbutt, N. (2007). Mammals of Madagascar, A Complete Guide. A&C Black Publishers. ISBN 978-0-300-12550-4. {{cite book}}: Invalid |ref=harv (help)

• Goodman, S.M.; Benstead, J.P., eds. (2003). The Natural History of Madagascar. University of Chicago Press. ISBN 0-226-30306-3.

Chapter 5 - Human Ecology

• Dewar, R. E. (2003). "Relationship between Human Ecological Pressure and the Vertebrate Extinctions". The Natural History of Madagascar. pp. 119–122. {{cite book}}: Invalid |ref=harv (help)

Chapter 13 - Mammals

• Goodman, S.M.; Ganzhorn, J.U.; Rakotondravony, D. (2003). "Introduction to the Mammals". pp. 1159–1186. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)
• Godfrey, L.R.; Jungers, W.L. (2003). "Subfossil Lemurs". pp. 1247–1252. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)

• Goodman, S.M.; Patterson, B.D., eds. (1997). Natural Change and Human Impact in Madagascar. Smithsonian Institution Press. ISBN 978-1560986829.

• Simons, E.L. (1997). "Chapter 6: Lemurs: Old and New". pp. 142–166. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)
• Godfrey, L.R.; Jungers, W.L.; Reed, K.E.; Simons, E.L.; Chatrath, P.S. (1997). "Chapter 8: Subfossil Lemurs". pp. 218–256. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)

• Gould, L.; Sauther, M.L., eds. (2006). Lemurs: Ecology and Adaptation. Springer. ISBN 978-0387-34585-7.

• Godfrey, L.R.; Jungers, W.L.; Schwartz, G.T. (2006). "Chapter 3: Ecology and Extinction of Madagascar's Subfossil Lemurs". pp. 41–64. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)

• Hartwig, W.C., ed. (2002). The Primate Fossil Record. ISBN 0-521-66315-6. {{cite book}}: Invalid |ref=harv (help)

• Godfrey, L.R.; Jungers, W.L. (2002). "Chapter 7: Quaternary fossil lemurs". pp. 97–121. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)

• Preston-Mafham, K. (1991). Madagascar: A Natural History. Facts on File. ISBN 978-0816024032. {{cite book}}: Invalid |ref=harv (help)

• Sussman, R.W. (2003). Primate Ecology and Social Structure. Pearson Custom Publishing. ISBN 978-0536743633. {{cite book}}: Invalid |ref=harv (help)

• Werdelin, L.; Sanders, W.J., eds. (2010). Cenozoic Mammals of Africa. ISBN 978-0520257214. {{cite book}}: Invalid |ref=harv (help)

• Godfrey, L.R.; Jungers, W.L.; Burney, D.A. (2010). "Chapter 21: Subfossil Lemurs of Madagascar". {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)