Taxonomy of lemurs
Encyclopedia
The taxonomic history
of lemur
s dates back to 1758 when Carl Linnaeus first classified
them, and the taxonomy remains controversial today, with approximately 70 to 100 species
and subspecies
recognized, depending on how the term "species" is defined
. Having undergone their own independent evolution on Madagascar, lemurs have diversified to fill many niches
normally filled by other types of mammals. They include the smallest primates in the world, and once included some of the largest. Since the arrival of humans approximately 2,000 years ago, lemurs have become restricted to 10% of the island, or approximately 60000 square kilometres (23,166.1 sq mi), and many face extinction
. Concerns over lemur conservation have affected lemur taxonomy, since distinct species receive increased conservation attention compared to subspecies.
The relationship between the aye-aye
and the rest of the lemurs has had the greatest impact on lemur taxonomy at the family
rank and above. Genetic analysis of this relationship has also clarified lemur phylogeny
and supports the hypothesis that lemurs rafted to Madagascar. Despite general agreement on phylogeny, the taxonomy is still under debate. At the genus
level, the taxonomy has been relatively stable since 1931, but a number of additional genera have been recognized since then.
Since the 1990s, there has been a steep increase in the number of recognized lemur species and subspecies through the discovery of new species, the elevation of existing subspecies to full species status, and the recognition of new species among previously known populations that were not even distinct subspecies. Currently living lemur species are divided into five families and 15 genera. If the extinct subfossil lemur
s are included, three families, eight genera, and 17 species would be added to the count. The recent rise in species numbers is due to both improved genetic analysis and a push in conservation to encourage the protection of isolated and distinct lemur populations. Not everyone in the scientific community supports these taxonomic changes, with some preferring instead an estimate of 50 living species.
isolated island with a unique mammalian fauna, lemurs have diversified both in behavior and morphology. Their diversity rivals that of the monkeys and apes found throughout the rest of the world, especially when the recently extinct subfossil lemur
s are considered. Ranging in size from the 30 g (1.1 oz) Madame Berthe's mouse lemur
, probably the world's smallest primate, to the extinct 160 – Archaeoindris fontoynonti, the largest known prosimian
, lemurs evolved diverse forms of locomotion, varying levels of social complexity, and unique adaptations to the local climate. They went on to fill many niches normally occupied by monkeys, squirrel
s, woodpecker
s, and large grazing ungulate
s. In addition to the incredible diversity between lemur families, there has also been great diversification among closely related lemurs.
The arrival of humans on the island 1,500 to 2,000 years ago has taken a significant toll, not only on the size of lemur populations, but also on their diversity. Due to habitat destruction
and hunting, at least 17 species and 8 genera have gone extinct and many others have become threatened. Historically, lemurs ranged across the entire island inhabiting a wide variety of habitats, including dry deciduous forests
, lowland forests
, spiny thickets
, subhumid forests
, montane forest
, and mangrove
. Today, their collective range is restricted to 10% of the island, or approximately 60000 square kilometre. Most of the remaining forests and lemurs are found along the periphery of the island. The center of the island, the Hauts-Plateaux
, was converted by early settlers to rice paddies
and grassland
through slash-and-burn agriculture
, known locally as tavy. As erosion
depleted the soil, the cyclical forest regrowth and burning ended as the forest gradually failed to return. In 2008, 41% of all lemur taxa were threatened with extinction while 42% were classified on the IUCN Red List
as "Data Deficient
".
(1758), Carl Linnaeus, the founder of modern binomial nomenclature
, created the genus Lemur to include three species: Lemur tardigradus (the red slender loris
, now known as Loris tardigradus), Lemur catta (the ring-tailed lemur
), and Lemur volans (the Philippine colugo
, now known as Cynocephalus volans). Although the term "lemur" was apparently at first intended for loris
es, it was soon applied to the endemic Malagasy primates, which have been known as "lemurs" ever since. The name derives from the Latin
term lemures, which refers to the "spirits of the dead" from Roman mythology
. Linnaeus was familiar with the nocturnal habits and ghost-like appearance of lemurs and lorises, as well as their noiseless movements at night, reflective eyes
, and ghostly cries. He may also have known about Malagasy legends that lemurs are the souls of their ancestors. Being familiar with the works of Virgil
and Ovid
and seeing an analogy that fit with his naming scheme, Linnaeus adapted the term "lemur" for these nocturnal primates.
Since the first taxonomic classification
of lemurs, many changes have been made to lemur taxonomy. Within the primate order, treeshrew
s (order Scandentia) were considered basal, prosimian primates—close relatives of lemurs—until the 1980s. Colugo
s, also incorrectly referred to as "flying lemurs", were once considered lemur-like primates, but were reclassified as close relatives of bats, and more recently as close relatives of primates within their own order, Dermoptera. Primates, together with their closest relatives, the treeshrews, colugos, and long-extinct plesiadapiform
s, form the taxonomically unranked Euarchonta
clade
within the Euarchontoglires
. Lorisids
, some of which were originally placed in the genus Lemur by Carl Linnaeus, have since been moved into either their own infraorder (Lorisiformes) or their own superfamily (Lorisoidea) within Lemuriformes.
For the Malagasy primate fauna, taxonomic nomenclature proliferated during the 1800s, with the aid of museum systematists
, such as Albert Günther and John Edward Gray
, as well as naturalists and explorers, such as Alfred Grandidier
. This nomenclature was not sorted out until decades later, when Ernst Schwarz
standardized it in 1931. It was not until the 1990s that this nomenclature started to see a new wave of taxonomic change.
by Johann Friedrich Blumenbach
in 1775. (He also placed humans in the order Bimana.) This view was upheld by other famous naturalists and zoologists
of the time, including Étienne Geoffroy Saint-Hilaire
(who first placed lemurs in Strepsirrhini in 1812), Georges Cuvier
, and (initially) John Edward Gray. By 1862, William Henry Flower
, a comparative anatomist
, was arguing against moving strepsirrhines out of Quadrumana into Insectivora
(a now-abandoned biological grouping), claiming that their brain had features transitional between other primates and "inferior" mammals. In 1863, Thomas Henry Huxley restored the order Primates to include humans, other apes, monkeys, lemurs, and even colugos. However, opposition continued with many specialists arguing that lemurs (or "Half-apes") should be placed in their own order. In 1873, English comparative anatomist St. George Jackson Mivart countered these arguments and proceeded to define the primates by a list of anatomical features.
Since the 19th century, the classification of lemurs above the genus level has seen many changes. Early taxonomists proposed a variety of classifications for lemurs, but generally separated indriids from other lemurs and placed the aye-aye in a major group of its own; some classified the dwarf and mouse lemurs with the galagos. In 1915, William King Gregory
published a classification that remained generally accepted over the next decades. He placed all the lemurs together in a "series" Lemuriformes and recognized three families: Daubentoniidae, Indriidae, and Lemuridae (including the current Cheirogaleidae and Lepilemuridae). George Gaylord Simpson
's influential 1945 classification of mammals placed the treeshrews and the fossil Anagale
(both now classified outside Primates) inside Lemuriformes and classified the fossil families Plesiadapidae
and Adapidae in a superfamily Lemuroidea with most of the lemurs.
Although treeshrews, plesiadapids, and the like are now no longer considered to be closely related to lemurs, disagreements persist over the classification of lemurs and related groups, resulting in two competing arrangements of the infraorders and superfamilies
within Strepsirrhini. Colin Groves, in the 2005 third edition of Mammal Species of the World
, classifies living strepsirrhines under three infraorders and two superfamilies. This places the aye-aye within its own infraorder, separate from both lemurs (divided into two superfamilies) and lorises. Since the publication of Mammal Species of the World, there has been little support in the academic literature for placing the aye-aye in its own infraorder, and more recently Mittermeier, Groves, and other editors have ignored this taxonomic level. An alternative classification draws the lines for infraorders and superfamilies differently, though using the same general phylogenetic tree
. It classifies all living strepsirrhines under one infraorder, with the lorises and lemurs in separate superfamilies.
The classification of several lemur taxa has elicited particular debate. Most significantly, the placement of the aye-aye has been controversial since its introduction to Western science in 1782, and it has been a topic of debate until very recently. Arguing against Darwin
's theory of natural selection
, Richard Owen
claimed in 1863 that the aye-aye's distinct characteristics, including its ever-growing incisor
s and unique, highly flexible middle finger, are so perfectly adapted for their uses in extractive foraging
that they could not have evolved gradually through natural selection. More recently, the aye-aye's placement has posed problems for the rafting hypothesis for the primate colonization of Madagascar. If this species does not form a monophyletic group
with the rest of the lemurs, then multiple colonization events would have had to occur to explain the occurrence of lemurs on Madagascar.
Until Owen published a definitive anatomical study in 1866, early naturalists were uncertain whether the aye-aye (genus Daubentonia) was a primate
, rodent
, or marsupial
. In the late eighteenth century, for example, the aye-aye was classified under the squirrel genus Sciurus
. By emphasizing its primate features, such as its postorbital bar
, stereoscopic vision
, and opposable hallux
, over its rodent-like teeth, Owen demonstrated its affinity with other primates. In 1996, Ankel-Simons demonstrated that the shape and arrangement of the aye-aye's diminutive deciduous incisors indicate that this genus has a shared ancestry with the toothcomb
ed primates. However, the placement of the aye-aye within the primates remained problematic until very recently. The karyotype
of the aye-aye is noticeably different from that of its closest relatives, the lorises and the rest of the lemurs, with a diploid chromosome
count of 2n=30. Based on its anatomy, researchers have found support for classifying the genus Daubentonia as a specialized indriid
, a sister group
to all strepsirrhines, and an indeterminate taxon within the primates. In 1931, Schwarz labeled the aye-aye as an offshoot of Indriidae, claiming that all lemurs were monophyletic, whereas Reginald Innes Pocock
had previously placed the aye-aye outside of the lemurs. In that same year, Anthony and Coupin classified the aye-aye under infraorder Chiromyiformes, a sister group to the other strepsirrhines. Colin Groves upheld this classification in 2005 because he was not entirely convinced the aye-aye formed a clade with the rest of the Malagasy lemurs, despite molecular tests that had shown Daubentoniidae was basal to all Lemuriformes.
Another interpretation of the aye-aye's origins has once again called into question the single origins of the lemurs. The aye-aye and a fossil strepsirrhine primate from Africa, Plesiopithecus, share similarities in the shape of the skull and the morphology of the lower jaw, which suggest that the latter could be a primitive relative of the aye-aye. However, the placement of an aye-aye ancestor in Africa would require multiple colonizations of Madagascar by strepsirrhine primates. Molecular tests may offer support, since they show that the aye-aye was the first to diverge in the lemur clade and that the other lemur families did not diverge until much later.
Often classified with the galagos by early students, the cheirogaleids (dwarf and mouse lemurs) were placed with the other lemurs from Gregory's 1915 classification until the early 1970s, when several anthropologists proposed that they were more closely related to lorisiforms, based on morphological data. However, relevant genetic studies unanimously place cheirogaleids within the lemuriform clade and Groves himself, who had promoted the cheirogaleid-lorisiform relationship in a 1974 paper, by 2001 regarded the idea as refuted.
Classifications in the first half of the 20th century divided lemurs into three families: Daubentoniidae, Indriidae, and Lemuridae, with the latter including the current Cheirogaleidae and Lepilemuridae. Because of concerns that Lemuridae might not be monophyletic, the family was later split; in 1982 Tattersall separated the Cheirogaleidae for the dwarf lemurs, mouse lemurs and relatives, and the Lepilemuridae for the sportive lemurs and bamboo lemurs (including the greater bamboo lemur
). This classification is still used, except that the bamboo lemurs were moved back to Lemuridae.
From the 1970s to the 1990s, there have been suggestions that the ruffed lemurs might be related to indriids or a sister group to Lemuridae and Indriidae and that the bamboo lemurs are related to the sportive lemurs, but neither view is supported by molecular phylogeny. The sportive lemurs and the extinct koala lemurs (Megaladapidae) both lack upper incisors in the permanent dentition, and in 1981, Groves placed both together in the family Megaladapidae, which he renamed Lepilemuridae in 2005 because that older name takes precedence
. Genetic research does not support a close relationship between the sportive and koala lemurs and instead places the koala lemurs as a sister group to Lemuridae; therefore, the two are now placed in separate families (Lepilemuridae for the sportive lemurs and Megaladapidae for the koala lemurs). The sloth lemurs (Palaeopropithecidae) and monkey lemur
s (Archaeolemuridae) were classified as subfamilies within Indriidae as late as 1982, but are now recognized as separate families.
The relationships among the families of lemurs have been problematic and have yet to be definitively resolved. Two competing phylogenies
exist based on genetic and molecular data. One approach (Horvath et al.) looks at a larger number of genes, but among fewer species. This results in Lemuridae being a sister group to Lepilemuridae, Cheirogaleidae, and Indriidae. The other approach (Orlando et al.) looks at fewer genes, but more lemur species. Using this analysis, Lepilemuridae becomes the sister group to Lemuridae, Cheirogaleidae, and Indriidae. Both phylogenies agree that the Malagasy primates are monophyletic and that Daubentoniidae (the aye-aye) is basal to the lemuriform clade, having split off significantly earlier than the other families. However, two problems create complications for both approaches. First, the four most closely related living lemur families diverged within a narrow window of approximately 10 million years, making it much harder to distinguish the splits with molecular evidence. In addition, these families diverged from their last common ancestor approximately 42 mya; such distant splits create a lot of noise
for molecular techniques.
split the Cheirogaleus medius species group of the dwarf lemurs into a separate genus Opolemur, but this was not accepted. Genus-level taxonomy was largely stabilized by Schwarz in 1931, but a number of later changes have become accepted:
, the president of Conservation International
(CI), taxonomist Colin Groves
, and others, there are currently 101 recognized species or subspecies of extant lemur, divided into five families and 15 genera. Conversely, other experts in the field label this as a possible example of taxonomic inflation
, and prefer instead an estimate of at least 50 species. All sides generally agree that the recently extinct subfossil lemurs should be classified in three families
, eight genera
, and 17 species.
Over the past two decades, the number of recognized lemur species has more than tripled according to some experts. In 1994, 32 distinct species were named in the first edition of Conservation International
's field guide, Lemurs of Madagascar
, and 68 were described in the 2nd edition, published in 2006. In December 2008, Russell Mittermeier, Colin Groves, and other experts co-wrote an article in the International Journal of Primatology classifying 99 species and subspecies. In late 2010, the 3rd edition of Lemurs of Madagascar listed 101 taxa. The number of lemur species is likely to continue growing in the coming years, as field studies, cytogenetic
and molecular genetic
research continues, particularly on cryptic species, such as mouse lemurs, which cannot be distinguished visually.
This threefold increase in less than two decades has not had universal support among taxonomists and lemur researchers. In many cases, classifications ultimately depends upon which species concept is used. Due to the critical condition that most Malagasy primate populations are in, taxonomists
and conservationists
sometimes favor splitting them into separate species to develop an effective strategy for the conservation of the full range of lemur diversity. Implicitly, this means that full species status will help grant genetically distinct populations added environmental protection.
The first large wave of new lemur species descriptions came in 2000, when Colin Groves split two species of dwarf lemur
(Cheirogaleus) into seven species while Rodin Rasoloarison and colleagues recognized seven species of mouse lemur in western Madagascar. Then in 2001, Colin Groves elevated the red ruffed lemur
(Varecia rubra), five subspecies of brown lemur (Eulemur albifrons, E. albocollaris, E. collaris, E. rufus and E. sanfordi), and four subspecies of sifaka
(Propithecus coquereli, P. deckenii, P. edwardsi, and P. perrieri) to full species status. Additional elevations of all remaining subspecies within the Eulemur and Propithecus genera were made in the years that followed. These and subsequent changes in taxonomy were largely due to a shift to the phylogenetic species concept, and are not universally endorsed.
By far the most explosive growth in species numbers (in absolute terms) has been in the genera Microcebus and Lepilemur. In 2006, 15 new species of Lepilemur were described, with three new species reported in February, one in June, and 11 in September. Since then, three additional species have been described, one of which turned out to be identical to a previously described species. Genetic and morphological differences seem to suggest that they are cryptic species, but there is still debate whether these merit full species status or should be regarded as subspecies of previously identified, "core" species.
Both brown lemurs and mouse lemurs were initially divided into a small number of species, either with no distinguishable subspecies
(in the case of mouse lemurs) or with several distinguishable subspecies (in the case of brown lemurs). With molecular research suggesting a more distant split in both genera, these subspecies or undistinguished populations have been promoted to species status.
In the case of mouse lemurs, the rise in species numbers has been only slightly less sudden and dramatic. Classified as one species by Ernst Schwarz
in 1931 (excluding one, Coquerel's giant mouse lemur, that is no longer classified in Microcebus), the genus was revised to contain two species, the gray mouse lemur
(Microcebus murinus) and the brown mouse lemur (M. rufus), after an extensive field study in 1972 showed both living in sympatry
in southeastern Madagascar. At the time, the gray mouse lemur was known in the drier parts of the north, west, and south, while the brown mouse lemur inhabited the humid rainforest regions of the east. However, we now know the species diversity
and distribution to be significantly more complex. Revisions throughout the 1990s and 2000s identified numerous new species through genetic testing using mitochondrial DNA
, demonstrating that the genus is represented by a multitude of cryptic species. Many, but not all of these defined species have been supported by nuclear DNA
tests.
However, there are still concerns that species are being identified prematurely. Ian Tattersall
, an anthropologist who recognized 42 species of lemur in 1982, has expressed concern that the geographically organized variety in lemur populations is being recognized with full species status while the number of subspecies in lemur genera has virtually disappeared. He has argued that taxonomists are confusing differentiation and speciation
, two processes that are often unrelated, while denying the role of microevolution
in evolutionary processes. Still other researchers who emphasize the framework of the "general lineage concept of species" contend that lineage divergence or differentiation demarcates the beginning of a new species.
New species have been identified due to differences in morphology
, karyotypes, cytochrome b sequences, and other genetic tests, as well as several combinations of these. When nuclear DNA (nDNA) was tested in conjunction with mitochondrial DNA (mtDNA) in mouse lemurs, a few species, such as Claire's mouse lemur
(Microcebus mamiratra) were demonstrated to be indistinguishable from other closely related species. In such cases, nDNA did not vary, but the mtDNA that had been used to define it as a species was still distinct. Differences in results between nDNA, which is inherited from both parents, and mtDNA, which is inherited from the mother, was attributed to female philopatry
, where females remain within or close to the home range
into which they were born while males disperse. Since the isolated population known as Claire's mouse lemur has distinct mtDNA, but not nDNA, it is likely to contain a population descended from a related group of females, but which still disperses and interbreeds with nearby populations.
Traditionally, karyology has been considered when determining species status. For example, in 2006, three new species of sportive lemur were named based partly on karyotypes. From the lemurs studied so far, the diploid number of chromosomes varies between 2n=20 and 2n=66. In the case of the brown lemurs, the diploid number ranges from 2n=44 to 2n=60 while the individual chromosome sizes vary considerably, despite strong similarities in morphology.
Sometimes distinctions are made due to very slight differences in pelage coloration. For instance, three distinctly colored types of mouse lemur were discovered in a multi-year study in Beza Mahafaly Reserve
in southern Madagascar, but rather than being separate species, DNA tests revealed that they all belonged to a single species, the reddish-gray mouse lemur
(Microcebus griseorufus). For this reason, further research is needed to confirm or deny the recent species splits. Only through detailed studies of morphology, ecology, behavior, and genetics can the true number of lemur species be determined.
}
}
}
}
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...
of lemur
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 dates back to 1758 when Carl Linnaeus first classified
Biological classification
Biological classification, or scientific classification in biology, is a method to group and categorize organisms by biological type, such as genus or species. Biological classification is part of scientific taxonomy....
them, and the taxonomy remains controversial today, with approximately 70 to 100 species
Species
In biology, a species is one of the basic units of biological classification and a taxonomic rank. A species is often defined as a group of organisms capable of interbreeding and producing fertile offspring. While in many cases this definition is adequate, more precise or differing measures are...
and 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...
recognized, depending on how the term "species" is defined
Species problem
The species problem or species concept is a mixture of difficult, related questions that often come up when biologists identify species and when they define the word "species"....
. Having undergone their own independent evolution on Madagascar, lemurs have diversified to fill many niches
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...
normally filled by other types of mammals. They include the smallest primates in the world, and once included some of the largest. Since the arrival of humans approximately 2,000 years ago, lemurs have become restricted to 10% of the island, or approximately 60000 square kilometres (23,166.1 sq mi), and many face extinction
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...
. Concerns over lemur conservation have affected lemur taxonomy, since distinct species receive increased conservation attention compared to subspecies.
The relationship between the 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...
and the rest of the lemurs has had the greatest impact on lemur taxonomy at the 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...
rank and above. Genetic analysis of this relationship has also clarified lemur phylogeny
Phylogenetics
In biology, phylogenetics is the study of evolutionary relatedness among groups of organisms , which is discovered through molecular sequencing data and morphological data matrices...
and supports the hypothesis that lemurs rafted to Madagascar. Despite general agreement on phylogeny, the taxonomy is still under debate. At the 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...
level, the taxonomy has been relatively stable since 1931, but a number of additional genera have been recognized since then.
Since the 1990s, there has been a steep increase in the number of recognized lemur species and subspecies through the discovery of new species, the elevation of existing subspecies to full species status, and the recognition of new species among previously known populations that were not even distinct subspecies. Currently living lemur species are divided into five families and 15 genera. If the extinct subfossil lemur
Subfossil lemur
Subfossil lemurs are lemurs from Madagascar that are represented by recent remains dating from nearly 26,000 years ago to approximately 560 years ago. They include both living and extinct species, although the term more frequently refers to the extinct giant lemurs...
s are included, three families, eight genera, and 17 species would be added to the count. The recent rise in species numbers is due to both improved genetic analysis and a push in conservation to encourage the protection of isolated and distinct lemur populations. Not everyone in the scientific community supports these taxonomic changes, with some preferring instead an estimate of 50 living species.
Background
Since their arrival on Madagascar, a biogeographicallyBiogeography
Biogeography is the study of the distribution of species , organisms, and ecosystems in space and through geological time. Organisms and biological communities vary in a highly regular fashion along geographic gradients of latitude, elevation, isolation and habitat area...
isolated island with a unique mammalian fauna, lemurs have diversified both in behavior and morphology. Their diversity rivals that of the monkeys and apes found throughout the rest of the world, especially when the recently extinct subfossil lemur
Subfossil lemur
Subfossil lemurs are lemurs from Madagascar that are represented by recent remains dating from nearly 26,000 years ago to approximately 560 years ago. They include both living and extinct species, although the term more frequently refers to the extinct giant lemurs...
s are considered. Ranging in size from the 30 g (1.1 oz) Madame Berthe's mouse lemur
Madame Berthe's Mouse Lemur
Madame Berthe's mouse lemur or Berthe's mouse lemur is the smallest of the mouse lemurs and the smallest primate in the world; the average body length is and seasonal weight is around...
, probably the world's smallest primate, to the extinct 160 – Archaeoindris fontoynonti, the largest known prosimian
Prosimian
Prosimians are a grouping of mammals defined as being primates, but not monkeys or apes. They include, among others, lemurs, bushbabies, and tarsiers. They are considered to have characteristics that are more primitive than those of monkeys and apes. Prosimians are the only primates native to...
, lemurs evolved diverse forms of locomotion, varying levels of social complexity, and unique adaptations to the local climate. They went on to fill many niches normally occupied by monkeys, squirrel
Squirrel
Squirrels belong to a large family of small or medium-sized rodents called the Sciuridae. The family includes tree squirrels, ground squirrels, chipmunks, marmots , flying squirrels, and prairie dogs. Squirrels are indigenous to the Americas, Eurasia, and Africa and have been introduced to Australia...
s, woodpecker
Woodpecker
Woodpeckers are near passerine birds of the order Piciformes. They are one subfamily in the family Picidae, which also includes the piculets and wrynecks. They are found worldwide and include about 180 species....
s, and large grazing ungulate
Ungulate
Ungulates are several groups of mammals, most of which use the tips of their toes, usually hoofed, to sustain their whole body weight while moving. They make up several orders of mammals, of which six to eight survive...
s. In addition to the incredible diversity between lemur families, there has also been great diversification among closely related lemurs.
The arrival of humans on the island 1,500 to 2,000 years ago has taken a significant toll, not only on the size of lemur populations, but also on their diversity. Due to habitat destruction
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...
and hunting, at least 17 species and 8 genera have gone extinct and many others have become threatened. Historically, lemurs ranged across the entire island inhabiting a wide variety of habitats, including 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...
, lowland forests
Madagascar lowland forests
The Madagascar lowland forests are a tropical moist broadleaf forest ecoregion, found on the eastern coast of the island of Madagascar.-Setting:...
, spiny thickets
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...
, subhumid forests
Madagascar subhumid forests
The Madagascar subhumid forests are a tropical moist broadleaf forest ecoregion which originally covered most of the Central Highlands of the island of Madagascar.-Setting:...
, montane forest
Cloud forest
A cloud forest, also called a fog forest, is a generally tropical or subtropical evergreen montane moist forest characterized by a persistent, frequent or seasonal low-level cloud cover, usually at the canopy level. Cloud forests often exhibit an abundance of mosses covering the ground and...
, and mangrove
Mangrove
Mangroves are various kinds of trees up to medium height and shrubs that grow in saline coastal sediment habitats in the tropics and subtropics – mainly between latitudes N and S...
. Today, their collective range is restricted to 10% of the island, or approximately 60000 square kilometre. Most of the remaining forests and lemurs are found along the periphery of the island. The center of the island, the Hauts-Plateaux
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...
, was converted by early settlers to rice paddies
Paddy field
A paddy field is a flooded parcel of arable land used for growing rice and other semiaquatic crops. Paddy fields are a typical feature of rice farming in east, south and southeast Asia. Paddies can be built into steep hillsides as terraces and adjacent to depressed or steeply sloped features such...
and grassland
Grassland
Grasslands are areas where the vegetation is dominated by grasses and other herbaceous plants . However, sedge and rush families can also be found. Grasslands occur naturally on all continents except Antarctica...
through slash-and-burn agriculture
Slash and burn
Slash-and-burn is an agricultural technique which involves cutting and burning of forests or woodlands to create fields. It is subsistence agriculture that typically uses little technology or other tools. It is typically part of shifting cultivation agriculture, and of transhumance livestock...
, known locally as tavy. As 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...
depleted the soil, the cyclical forest regrowth and burning ended as the forest gradually failed to return. In 2008, 41% of all lemur taxa were threatened with extinction while 42% were classified on the IUCN Red List
IUCN Red List
The IUCN Red List of Threatened Species , founded in 1963, is the world's most comprehensive inventory of the global conservation status of biological species. The International Union for Conservation of Nature is the world's main authority on the conservation status of species...
as "Data Deficient
Data Deficient
Data Deficient is a category applied by the IUCN, other agencies, and individuals to a species when the available information is not sufficient for a proper assessment of conservation status to be made...
".
Overview of taxonomic and phylogenetic classification
In the first volume of the 10th edition of Systema Naturae10th edition of Systema Naturae
The 10th edition of Systema Naturae was a book written by Carl Linnaeus and published in two volumes in 1758 and 1759, which marks the starting point of zoological nomenclature...
(1758), Carl Linnaeus, the founder of modern binomial nomenclature
Binomial nomenclature
Binomial nomenclature is a formal system of naming species of living things by giving each a name composed of two parts, both of which use Latin grammatical forms, although they can be based on words from other languages...
, created the genus Lemur to include three species: Lemur tardigradus (the red slender loris
Red Slender Loris
The red slender loris is a small, nocturnal prosimian native to the rainforests of Sri Lanka. This is #6 of the 10 focal species and #22 of the 100 EDGE mammal species worldwide considered the most Evolutionarily Distinct and Globally Endangered. Two subspecies have been identified, L. t....
, now known as Loris tardigradus), Lemur catta (the ring-tailed lemur
Ring-tailed Lemur
The ring-tailed lemur is a large strepsirrhine primate and the most recognized lemur due to its long, black and white ringed tail. It belongs to Lemuridae, one of five lemur families. It is the only member of the Lemur genus. Like all lemurs it is endemic to the island of Madagascar...
), and Lemur volans (the Philippine colugo
Philippine Flying Lemur
The Philippine Flying Lemur is one of two species of flying lemurs, the only two living species in the order Dermoptera. Additionally, it is the only member of the genus Cynocephalus.-Distribution:...
, now known as Cynocephalus volans). Although the term "lemur" was apparently at first intended for 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, it was soon applied to the endemic Malagasy primates, which have been known as "lemurs" ever since. The name derives from the Latin
Latin
Latin is an Italic language originally spoken in Latium and Ancient Rome. It, along with most European languages, is a descendant of the ancient Proto-Indo-European language. Although it is considered a dead language, a number of scholars and members of the Christian clergy speak it fluently, and...
term lemures, which refers to the "spirits of the dead" from Roman mythology
Roman mythology
Roman mythology is the body of traditional stories pertaining to ancient Rome's legendary origins and religious system, as represented in the literature and visual arts of the Romans...
. Linnaeus was familiar with the nocturnal habits and ghost-like appearance of lemurs and lorises, as well as their noiseless movements at night, reflective eyes
Tapetum lucidum
The tapetum lucidum is a layer of tissue in the eye of many vertebrate animals....
, and ghostly cries. He may also have known about Malagasy legends that lemurs are the souls of their ancestors. Being familiar with the works of Virgil
Virgil
Publius Vergilius Maro, usually called Virgil or Vergil in English , was an ancient Roman poet of the Augustan period. He is known for three major works of Latin literature, the Eclogues , the Georgics, and the epic Aeneid...
and Ovid
Ovid
Publius Ovidius Naso , known as Ovid in the English-speaking world, was a Roman poet who is best known as the author of the three major collections of erotic poetry: Heroides, Amores, and Ars Amatoria...
and seeing an analogy that fit with his naming scheme, Linnaeus adapted the term "lemur" for these nocturnal primates.
Since the first taxonomic classification
Biological classification
Biological classification, or scientific classification in biology, is a method to group and categorize organisms by biological type, such as genus or species. Biological classification is part of scientific taxonomy....
of lemurs, many changes have been made to lemur taxonomy. Within the primate order, treeshrew
Treeshrew
The treeshrews are small mammals native to the tropical forests of Southeast Asia. They make up the families Tupaiidae, the treeshrews, and Ptilocercidae, the pen-tailed treeshrews, and the entire order Scandentia. There are 20 species in 5 genera...
s (order Scandentia) were considered basal, prosimian primates—close relatives of lemurs—until the 1980s. Colugo
Colugo
Colugos are arboreal gliding mammals found in South-east Asia. There are just two extant species, which make up the entire family Cynocephalidae and order Dermoptera. They are the most capable of all gliding mammals, using flaps of extra skin between their legs to glide from higher to lower...
s, also incorrectly referred to as "flying lemurs", were once considered lemur-like primates, but were reclassified as close relatives of bats, and more recently as close relatives of primates within their own order, Dermoptera. Primates, together with their closest relatives, the treeshrews, colugos, and long-extinct plesiadapiform
Plesiadapiformes
Plesiadapiformes is an extinct order of mammals. It is either closely related to the primates or a precursor to them. Many are too derived to be ancestral to primates, but the earliest Plesiadapiformes have teeth that are strongly indicative of a common ancestor...
s, form the taxonomically unranked Euarchonta
Euarchonta
The Euarchonta are a grandorder of mammals containing four orders: the Dermoptera or colugos, the Scandentia or treeshrews, the extinct Plesiadapiformes, and the Primates....
clade
Clade
A clade is a group consisting of a species and all its descendants. In the terms of biological systematics, a clade is a single "branch" on the "tree of life". The idea that such a "natural group" of organisms should be grouped together and given a taxonomic name is central to biological...
within the Euarchontoglires
Euarchontoglires
Euarchontoglires is a clade of mammals, the living members of which are rodents, lagomorphs, treeshrews, colugos and primates .-Evolutionary relationships:...
. Lorisids
Lorisidae
Lorisidae is a family of strepsirrhine primates. The lorisids are all slim arboreal animals and include the lorises, pottos and angwantibos. Lorisids live in tropical, central Africa as well as in south and southeast Asia....
, some of which were originally placed in the genus Lemur by Carl Linnaeus, have since been moved into either their own infraorder (Lorisiformes) or their own superfamily (Lorisoidea) within Lemuriformes.
For the Malagasy primate fauna, taxonomic nomenclature proliferated during the 1800s, with the aid of museum systematists
Systematics
Biological systematics is the study of the diversification of terrestrial life, both past and present, and the relationships among living things through time. Relationships are visualized as evolutionary trees...
, such as Albert Günther and John Edward Gray
John Edward Gray
John Edward Gray, FRS was a British zoologist. He was the elder brother of George Robert Gray and son of the pharmacologist and botanist Samuel Frederick Gray ....
, as well as naturalists and explorers, such as 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...
. This nomenclature was not sorted out until decades later, when Ernst Schwarz
Ernst Schwarz
Ernst Schwarz was a German zoologist.Schwarz was born in Frankfurt and studied zoology in Munich. He worked at the Museum of Natural History in Frankfurt and the Zoological Museum in Berlin. In 1929 he became professor of Zoology at the University of Greifswald. He worked at the Natural History...
standardized it in 1931. It was not until the 1990s that this nomenclature started to see a new wave of taxonomic change.
Suprageneric classification
Although Carl Linnaeus originally grouped the first "lemurs" he classified under the order Primates, lemurs and other non-human primates were later separated from humans by being placed in the order QuadrumanaQuadrumana
Quadrumana and Bimana form an obsolete division of the primates: the Quadrumana are primates with four hands , and the Bimana being those with two hands and two feet...
by Johann Friedrich Blumenbach
Johann Friedrich Blumenbach
Johann Friedrich Blumenbach was a German physician, physiologist and anthropologist, one of the first to explore the study of mankind as an aspect of natural history, whose teachings in comparative anatomy were applied to classification of what he called human races, of which he determined...
in 1775. (He also placed humans in the order Bimana.) This view was upheld by other famous naturalists and zoologists
Zoology
Zoology |zoölogy]]), is the branch of biology that relates to the animal kingdom, including the structure, embryology, evolution, classification, habits, and distribution of all animals, both living and extinct...
of the time, including Étienne Geoffroy Saint-Hilaire
Étienne Geoffroy Saint-Hilaire
Étienne Geoffroy Saint-Hilaire was a French naturalist who established the principle of "unity of composition". He was a colleague of Jean-Baptiste Lamarck and expanded and defended Lamarck's evolutionary theories...
(who first placed lemurs in Strepsirrhini in 1812), Georges Cuvier
Georges Cuvier
Georges Chrétien Léopold Dagobert Cuvier or Jean Léopold Nicolas Frédéric Cuvier , known as Georges Cuvier, was a French naturalist and zoologist...
, and (initially) John Edward Gray. By 1862, William Henry Flower
William Henry Flower
Sir William Henry Flower KCB FRCS FRS was an English comparative anatomist and surgeon. Flower became a leading authority on mammals, and especially on the primate brain...
, a comparative anatomist
Comparative anatomy
Comparative anatomy is the study of similarities and differences in the anatomy of organisms. It is closely related to evolutionary biology and phylogeny .-Description:...
, was arguing against moving strepsirrhines out of Quadrumana into Insectivora
Insectivora
The order Insectivora is a now-abandoned biological grouping within the class of mammals...
(a now-abandoned biological grouping), claiming that their brain had features transitional between other primates and "inferior" mammals. In 1863, Thomas Henry Huxley restored the order Primates to include humans, other apes, monkeys, lemurs, and even colugos. However, opposition continued with many specialists arguing that lemurs (or "Half-apes") should be placed in their own order. In 1873, English comparative anatomist St. George Jackson Mivart countered these arguments and proceeded to define the primates by a list of anatomical features.
Since the 19th century, the classification of lemurs above the genus level has seen many changes. Early taxonomists proposed a variety of classifications for lemurs, but generally separated indriids from other lemurs and placed the aye-aye in a major group of its own; some classified the dwarf and mouse lemurs with the galagos. In 1915, William King Gregory
William King Gregory
William King Gregory was an American zoologist, renowned as a primatologist, paleontologist, and functional and comparative morphologist. He was an expert on mammalian dentition, and a leading contributor to theories of evolution...
published a classification that remained generally accepted over the next decades. He placed all the lemurs together in a "series" Lemuriformes and recognized three families: Daubentoniidae, Indriidae, and Lemuridae (including the current Cheirogaleidae and Lepilemuridae). George Gaylord Simpson
George Gaylord Simpson
George Gaylord Simpson was an American paleontologist. Simpson was perhaps the most influential paleontologist of the twentieth century, and a major participant in the modern evolutionary synthesis, contributing Tempo and mode in evolution , The meaning of evolution and The major features of...
's influential 1945 classification of mammals placed the treeshrews and the fossil Anagale
Anagale
Anagale is an extinct genus of mammal from the early Oligocene of Mongolia. Its closest living relatives are the rodents and lagomorphs.Anagale was 30 cm long and resembled a rabbit, but with a longer tail. Also, the build of its hind legs indicates that it walked, and did not hop...
(both now classified outside Primates) inside Lemuriformes and classified the fossil families Plesiadapidae
Plesiadapidae
Plesiadapidae is a family of plesiadapiform mammals related to primates known from the Paleocene and Eocene of North America, Europe, and Asia...
and Adapidae in a superfamily Lemuroidea with most of the lemurs.
Although treeshrews, plesiadapids, and the like are now no longer considered to be closely related to lemurs, disagreements persist over the classification of lemurs and related groups, resulting in two competing arrangements of the infraorders and superfamilies
Taxonomic rank
In biological classification, rank is the level in a taxonomic hierarchy. Examples of taxonomic ranks are species, genus, family, and class. Each rank subsumes under it a number of less general categories...
within Strepsirrhini. Colin Groves, in the 2005 third edition of Mammal Species of the World
Mammal Species of the World
Mammal Species of the World, now in its 3rd edition, is a standard reference work in zoology giving descriptions and bibliographic data for the known species of mammals.An updated Third Edition of Mammal Species of the World was published late in 2005:...
, classifies living strepsirrhines under three infraorders and two superfamilies. This places the aye-aye within its own infraorder, separate from both lemurs (divided into two superfamilies) and lorises. Since the publication of Mammal Species of the World, there has been little support in the academic literature for placing the aye-aye in its own infraorder, and more recently Mittermeier, Groves, and other editors have ignored this taxonomic level. An alternative classification draws the lines for infraorders and superfamilies differently, though using the same general phylogenetic tree
Phylogenetic tree
A phylogenetic tree or evolutionary tree is a branching diagram or "tree" showing the inferred evolutionary relationships among various biological species or other entities based upon similarities and differences in their physical and/or genetic characteristics...
. It classifies all living strepsirrhines under one infraorder, with the lorises and lemurs in separate superfamilies.
|
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
|
The classification of several lemur taxa has elicited particular debate. Most significantly, the placement of the aye-aye has been controversial since its introduction to Western science in 1782, and it has been a topic of debate until very recently. Arguing against Darwin
Charles Darwin
Charles Robert Darwin FRS was an English naturalist. He established that all species of life have descended over time from common ancestry, and proposed the scientific theory that this branching pattern of evolution resulted from a process that he called natural selection.He published his theory...
's theory of natural selection
Natural selection
Natural selection is the nonrandom process by which biologic traits become either more or less common in a population as a function of differential reproduction of their bearers. It is a key mechanism of evolution....
, Richard Owen
Richard Owen
Sir Richard Owen, FRS KCB was an English biologist, comparative anatomist and palaeontologist.Owen is probably best remembered today for coining the word Dinosauria and for his outspoken opposition to Charles Darwin's theory of evolution by natural selection...
claimed in 1863 that the aye-aye's distinct characteristics, including its ever-growing 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 unique, highly flexible middle finger, are so perfectly adapted for their uses in extractive foraging
Foraging
- Definitions and significance of foraging behavior :Foraging is the act of searching for and exploiting food resources. It affects an animal's fitness because it plays an important role in an animal's ability to survive and reproduce...
that they could not have evolved gradually through natural selection. More recently, the aye-aye's placement has posed problems for the rafting hypothesis for the primate colonization of Madagascar. If this species does not form a monophyletic group
Monophyly
In common cladistic usage, a monophyletic group is a taxon which forms a clade, meaning that it contains all the descendants of the possibly hypothetical closest common ancestor of the members of the group. The term is synonymous with the uncommon term holophyly...
with the rest of the lemurs, then multiple colonization events would have had to occur to explain the occurrence of lemurs on Madagascar.
Until Owen published a definitive anatomical study in 1866, early naturalists were uncertain whether the aye-aye (genus Daubentonia) was a 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...
, rodent
Rodent
Rodentia is an order of mammals also known as rodents, characterised by two continuously growing incisors in the upper and lower jaws which must be kept short by gnawing....
, or 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...
. In the late eighteenth century, for example, the aye-aye was classified under the squirrel genus Sciurus
Sciurus
The genus Sciurus contains most of the common, bushy-tailed squirrels in North America, Europe, temperate Asia, Central America and South America.-Species:There are 30 species.Genus Sciurus - Tree squirrels*Subgenus Sciurus...
. By emphasizing its primate features, such as its postorbital bar
Postorbital bar
The postorbital bar is a bone which runs around the eyesocket of strepsirrhine primates. This is in contrast to the higher primates, haplorrhine, which have evolved fully enclosed sockets to protect their eyes....
, stereoscopic vision
Stereopsis
Stereopsis refers to impression of depth that is perceived when a scene is viewed with both eyes by someone with normal binocular vision. Binocular viewing of a scene creates two slightly different images of the scene in the two eyes due the the eyes' different positions on the head...
, and opposable hallux
Thumb
The thumb is the first digit of the hand. When a person is standing in the medical anatomical position , the thumb is the lateral-most digit...
, over its rodent-like teeth, Owen demonstrated its affinity with other primates. In 1996, Ankel-Simons demonstrated that the shape and arrangement of the aye-aye's diminutive deciduous incisors indicate that this genus has a shared ancestry with the 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...
ed primates. However, the placement of the aye-aye within the primates remained problematic until very recently. The karyotype
Karyotype
A karyotype is the number and appearance of chromosomes in the nucleus of an eukaryotic cell. The term is also used for the complete set of chromosomes in a species, or an individual organism.p28...
of the aye-aye is noticeably different from that of its closest relatives, the lorises and the rest of the lemurs, with a diploid chromosome
Chromosome
A chromosome is an organized structure of DNA and protein found in cells. It is a single piece of coiled DNA containing many genes, regulatory elements and other nucleotide sequences. Chromosomes also contain DNA-bound proteins, which serve to package the DNA and control its functions.Chromosomes...
count of 2n=30. Based on its anatomy, researchers have found support for classifying the genus Daubentonia as a specialized indriid
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...
, a sister group
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...
to all strepsirrhines, and an indeterminate taxon within the primates. In 1931, Schwarz labeled the aye-aye as an offshoot of Indriidae, claiming that all lemurs were monophyletic, whereas Reginald Innes Pocock
Reginald Innes Pocock
Reginald Innes Pocock F.R.S. was a British zoologist.Pocock was born in Clifton, Bristol, the fourth son of Rev. Nicholas Pocock and Edith Prichard. He began showing interest in natural history at St. Edward's School, Oxford. He received tutoring in zoology from Sir Edward Poulton, and was allowed...
had previously placed the aye-aye outside of the lemurs. In that same year, Anthony and Coupin classified the aye-aye under infraorder Chiromyiformes, a sister group to the other strepsirrhines. Colin Groves upheld this classification in 2005 because he was not entirely convinced the aye-aye formed a clade with the rest of the Malagasy lemurs, despite molecular tests that had shown Daubentoniidae was basal to all Lemuriformes.
Another interpretation of the aye-aye's origins has once again called into question the single origins of the lemurs. The aye-aye and a fossil strepsirrhine primate from Africa, Plesiopithecus, share similarities in the shape of the skull and the morphology of the lower jaw, which suggest that the latter could be a primitive relative of the aye-aye. However, the placement of an aye-aye ancestor in Africa would require multiple colonizations of Madagascar by strepsirrhine primates. Molecular tests may offer support, since they show that the aye-aye was the first to diverge in the lemur clade and that the other lemur families did not diverge until much later.
Often classified with the galagos by early students, the cheirogaleids (dwarf and mouse lemurs) were placed with the other lemurs from Gregory's 1915 classification until the early 1970s, when several anthropologists proposed that they were more closely related to lorisiforms, based on morphological data. However, relevant genetic studies unanimously place cheirogaleids within the lemuriform clade and Groves himself, who had promoted the cheirogaleid-lorisiform relationship in a 1974 paper, by 2001 regarded the idea as refuted.
Classifications in the first half of the 20th century divided lemurs into three families: Daubentoniidae, Indriidae, and Lemuridae, with the latter including the current Cheirogaleidae and Lepilemuridae. Because of concerns that Lemuridae might not be monophyletic, the family was later split; in 1982 Tattersall separated the Cheirogaleidae for the dwarf lemurs, mouse lemurs and relatives, and the Lepilemuridae for the sportive lemurs and bamboo lemurs (including the 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...
). This classification is still used, except that the bamboo lemurs were moved back to Lemuridae.
From the 1970s to the 1990s, there have been suggestions that the ruffed lemurs might be related to indriids or a sister group to Lemuridae and Indriidae and that the bamboo lemurs are related to the sportive lemurs, but neither view is supported by molecular phylogeny. The sportive lemurs and the extinct koala lemurs (Megaladapidae) both lack upper incisors in the permanent dentition, and in 1981, Groves placed both together in the family Megaladapidae, which he renamed Lepilemuridae in 2005 because that older name takes precedence
Principle of Priority
thumb|270px|Boa manditraIn zoology, the scientific study of animals, the Principle of Priority is one of the guiding principles of the International Code of Zoological Nomenclature, defined by Article 23....
. Genetic research does not support a close relationship between the sportive and koala lemurs and instead places the koala lemurs as a sister group to Lemuridae; therefore, the two are now placed in separate families (Lepilemuridae for the sportive lemurs and Megaladapidae for the koala lemurs). The sloth lemurs (Palaeopropithecidae) and 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 (Archaeolemuridae) were classified as subfamilies within Indriidae as late as 1982, but are now recognized as separate families.
The relationships among the families of lemurs have been problematic and have yet to be definitively resolved. Two competing phylogenies
Phylogenetics
In biology, phylogenetics is the study of evolutionary relatedness among groups of organisms , which is discovered through molecular sequencing data and morphological data matrices...
exist based on genetic and molecular data. One approach (Horvath et al.) looks at a larger number of genes, but among fewer species. This results in Lemuridae being a sister group to Lepilemuridae, Cheirogaleidae, and Indriidae. The other approach (Orlando et al.) looks at fewer genes, but more lemur species. Using this analysis, Lepilemuridae becomes the sister group to Lemuridae, Cheirogaleidae, and Indriidae. Both phylogenies agree that the Malagasy primates are monophyletic and that Daubentoniidae (the aye-aye) is basal to the lemuriform clade, having split off significantly earlier than the other families. However, two problems create complications for both approaches. First, the four most closely related living lemur families diverged within a narrow window of approximately 10 million years, making it much harder to distinguish the splits with molecular evidence. In addition, these families diverged from their last common ancestor approximately 42 mya; such distant splits create a lot of noise
Statistical noise
Statistical noise is the colloquialism for recognized amounts of unexplained variation in a sample. See errors and residuals in statistics....
for molecular techniques.
Genus-level classification
Early distribution of lemur species among genera differed in a number of ways from current taxonomy. For example, the fork-marked lemurs were initially placed in Lemur and then in Microcebus with the mouse lemurs before being placed in their own genus Phaner, and Charles Immanuel Forsyth MajorCharles 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...
split the Cheirogaleus medius species group of the dwarf lemurs into a separate genus Opolemur, but this was not accepted. Genus-level taxonomy was largely stabilized by Schwarz in 1931, but a number of later changes have become accepted:
- The ring-tailed lemurRing-tailed LemurThe ring-tailed lemur is a large strepsirrhine primate and the most recognized lemur due to its long, black and white ringed tail. It belongs to Lemuridae, one of five lemur families. It is the only member of the Lemur genus. Like all lemurs it is endemic to the island of Madagascar...
, ruffed lemurRuffed lemurThe 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, and brown lemurs were once grouped together in the genus Lemur due to a host of morphological similarities. For instance, the skeletons of the ring-tailed lemur and the brown lemurs are nearly indistinguishable. However, ruffed lemurs were reassigned to the genus Varecia in 1962, and due to similarities between the ring-tailed lemur and the bamboo lemurs, particularly in regards to molecular evidence and scent gland similarities, the brown lemurs were moved to the genus Eulemur in 1988. The genus Lemur is now monotypicMonotypicIn biology, a monotypic taxon is a taxonomic group with only one biological type. The term's usage differs slightly between botany and zoology. The term monotypic has a separate use in conservation biology, monotypic habitat, regarding species habitat conversion eliminating biodiversity and...
, containing only the ring-tailed lemur. - In 2001, Colin Groves concluded that despite similarities, the greater bamboo lemur was sufficiently distinct from the bamboo lemurBamboo lemurThe bamboo or gentle lemurs are the lemurs in genus Hapalemur. They are medium sized primates that live exclusively on Madagascar...
s of the genus Hapalemur to merit its own monotypic genus, Prolemur, in contrast to Schwarz's 1931 disagreement with Pocock's decision to separate Prolemur from Hapalemur. - Originally placed in the genus Microcebus (mouse lemurMouse lemurThe mouse lemurs are nocturnal lemurs of the genus Microcebus. Like all lemurs, mouse lemurs are native to Madagascar.Mouse lemurs have a combined head, body and tail length of less than , making them the smallest primates ; however, their weight fluctuates in response to daylight duration.Mouse...
s), the giant mouse lemurGiant mouse lemurThe giant mouse lemurs are small lemur species in the genus Mirza. They are native to the western deciduous forests of Madagascar, usually located near the coast or other sources of water...
was moved to its own genus, Mirza, in 1985 due to its larger size, morphological differences, dental characteristics, and behavior. - The hairy-eared dwarf lemurHairy-eared Dwarf LemurThe hairy-eared dwarf lemur , or hairy-eared mouse lemur, is a nocturnal lemur endemic to Madagascar. It is the only member of the genus Allocebus. This species is critically endangered and the population is estimated at 100-1000 individuals. They all live a single location in the northeastern part...
was first placed in the genus Cheirogaleus (dwarf lemurDwarf lemurThe dwarf lemurs are the lemurs of the genus Cheirogaleus. All of the species in this genus, like all other lemurs, are native to Madagascar.- Description :...
s) in 1875 and was later found to have closer affinities with Microcebus. However, its dentition and cranium structure were held sufficiently distinct to merit elevation to its own genus, Allocebus. - In 1948, paleontologist Charles Lamberton proposed a new sub-genus for the giant ruffed lemurs, PachylemurPachylemurPachylemur 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...
, which had previously been placed in the genus Lemur. Since the 1960s, it has been considered its own separate genus, although the two extinct species of giant ruffed lemur have sometimes been grouped under Varecia with their closest relatives. - A new genus of sloth lemur, BabakotiaBabakotiaBabakotia 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 named in 1990.
Species-level classification
There is widespread disagreement on aspects of species-level lemur taxonomy, particularly concerning the recent increase in the number of recognized species. According to Russell MittermeierRussell Mittermeier
Russell Alan Mittermeier is a primatologist, herpetologist and biological anthropologist. He has written several books for both popular and scientist audiences, and has authored some 300 scientific papers.-Biography:...
, the president of Conservation International
Conservation International
Conservation International is a nonprofit organization headquartered in Arlington, Virginia, which seeks to ensure the health of humanity by protecting Earth's ecosystems and biodiversity. CI’s work focuses on six key initiatives that affect human well-being: climate, food security, freshwater...
(CI), taxonomist Colin Groves
Colin Groves
Colin Peter Groves is Professor of Biological Anthropology at the Australian National University in Canberra, Australia.Born in England on 24 June 1942, Colin Groves completed a Bachelor of Science at University College London in 1963, and a Doctor of Philosophy at the Royal Free Hospital School of...
, and others, there are currently 101 recognized species or subspecies of extant lemur, divided into five families and 15 genera. Conversely, other experts in the field label this as a possible example of taxonomic inflation
Taxonomic inflation
Taxonomic inflation is a pejorative term for what is perceived to be an excessive increase in the number of recognised taxa in a given context, due not to the discovery of new taxa but rather to putatively arbitrary changes to how taxa are delineated....
, and prefer instead an estimate of at least 50 species. All sides generally agree that the recently extinct subfossil lemurs should be classified in three families
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...
, eight 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...
, and 17 species.
Over the past two decades, the number of recognized lemur species has more than tripled according to some experts. In 1994, 32 distinct species were named in the first edition of Conservation International
Conservation International
Conservation International is a nonprofit organization headquartered in Arlington, Virginia, which seeks to ensure the health of humanity by protecting Earth's ecosystems and biodiversity. CI’s work focuses on six key initiatives that affect human well-being: climate, food security, freshwater...
's field guide, Lemurs of Madagascar
Lemurs of Madagascar (book)
Lemurs of Madagascar, currently in its third edition, is a reference work and field guide for the lemurs of Madagascar, giving descriptions and biogeographic data for the known species. The primary contributor is Russell Mittermeier, president of Conservation International, and the cover art and...
, and 68 were described in the 2nd edition, published in 2006. In December 2008, Russell Mittermeier, Colin Groves, and other experts co-wrote an article in the International Journal of Primatology classifying 99 species and subspecies. In late 2010, the 3rd edition of Lemurs of Madagascar listed 101 taxa. The number of lemur species is likely to continue growing in the coming years, as field studies, cytogenetic
Cytogenetics
Cytogenetics is a branch of genetics that is concerned with the study of the structure and function of the cell, especially the chromosomes. It includes routine analysis of G-Banded chromosomes, other cytogenetic banding techniques, as well as molecular cytogenetics such as fluorescent in situ...
and molecular genetic
Molecular genetics
Molecular genetics is the field of biology and genetics that studies the structure and function of genes at a molecular level. The field studies how the genes are transferred from generation to generation. Molecular genetics employs the methods of genetics and molecular biology...
research continues, particularly on cryptic species, such as mouse lemurs, which cannot be distinguished visually.
This threefold increase in less than two decades has not had universal support among taxonomists and lemur researchers. In many cases, classifications ultimately depends upon which species concept is used. Due to the critical condition that most Malagasy primate populations are in, taxonomists
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 conservationists
Conservation movement
The conservation movement, also known as nature conservation, is a political, environmental and a social movement that seeks to protect natural resources including animal, fungus and plant species as well as their habitat for the future....
sometimes favor splitting them into separate species to develop an effective strategy for the conservation of the full range of lemur diversity. Implicitly, this means that full species status will help grant genetically distinct populations added environmental protection.
The first large wave of new lemur species descriptions came in 2000, when Colin Groves split two species of dwarf lemur
Dwarf lemur
The dwarf lemurs are the lemurs of the genus Cheirogaleus. All of the species in this genus, like all other lemurs, are native to Madagascar.- Description :...
(Cheirogaleus) into seven species while Rodin Rasoloarison and colleagues recognized seven species of mouse lemur in western Madagascar. Then in 2001, Colin Groves elevated the red ruffed lemur
Red Ruffed Lemur
The red ruffed lemur is one of two species in the genus Varecia, the ruffed lemurs; the other is the black-and-white ruffed lemur . Like all lemurs, it is native to Madagascar and occurs only in the rainforests of Masoala, in the northeast of the island...
(Varecia rubra), five subspecies of brown lemur (Eulemur albifrons, E. albocollaris, E. collaris, E. rufus and E. sanfordi), and four subspecies 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...
(Propithecus coquereli, P. deckenii, P. edwardsi, and P. perrieri) to full species status. Additional elevations of all remaining subspecies within the Eulemur and Propithecus genera were made in the years that followed. These and subsequent changes in taxonomy were largely due to a shift to the phylogenetic species concept, and are not universally endorsed.
By far the most explosive growth in species numbers (in absolute terms) has been in the genera Microcebus and Lepilemur. In 2006, 15 new species of Lepilemur were described, with three new species reported in February, one in June, and 11 in September. Since then, three additional species have been described, one of which turned out to be identical to a previously described species. Genetic and morphological differences seem to suggest that they are cryptic species, but there is still debate whether these merit full species status or should be regarded as subspecies of previously identified, "core" species.
Both brown lemurs and mouse lemurs were initially divided into a small number of species, either with no distinguishable 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...
(in the case of mouse lemurs) or with several distinguishable subspecies (in the case of brown lemurs). With molecular research suggesting a more distant split in both genera, these subspecies or undistinguished populations have been promoted to species status.
In the case of mouse lemurs, the rise in species numbers has been only slightly less sudden and dramatic. Classified as one species by Ernst Schwarz
Ernst Schwarz
Ernst Schwarz was a German zoologist.Schwarz was born in Frankfurt and studied zoology in Munich. He worked at the Museum of Natural History in Frankfurt and the Zoological Museum in Berlin. In 1929 he became professor of Zoology at the University of Greifswald. He worked at the Natural History...
in 1931 (excluding one, Coquerel's giant mouse lemur, that is no longer classified in Microcebus), the genus was revised to contain two species, the gray mouse lemur
Gray Mouse Lemur
The gray mouse lemur , or lesser mouse lemur, is a small lemur, a type of strepsirrhine primate, found only on the island of Madagascar. Weighing , it is the largest of the mouse lemurs , a group which include the smallest primates in the world...
(Microcebus murinus) and the brown mouse lemur (M. rufus), after an extensive field study in 1972 showed both living in 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...
in southeastern Madagascar. At the time, the gray mouse lemur was known in the drier parts of the north, west, and south, while the brown mouse lemur inhabited the humid rainforest regions of the east. However, we now know the species diversity
Species diversity
Species diversity is an index that incorporates the number of species in an area and also their relative abundance. It is a more comprehensive value than species richness....
and distribution to be significantly more complex. Revisions throughout the 1990s and 2000s identified numerous new species through genetic testing using mitochondrial DNA
Mitochondrial DNA
Mitochondrial DNA is the DNA located in organelles called mitochondria, structures within eukaryotic cells that convert the chemical energy from food into a form that cells can use, adenosine triphosphate...
, demonstrating that the genus is represented by a multitude of cryptic species. Many, but not all of these defined species have been supported by nuclear DNA
Nuclear DNA
Nuclear DNA, nuclear deoxyribonucleic acid , is DNA contained within a nucleus of eukaryotic organisms. In mammals and vertebrates, nuclear DNA encodes more of the genome than the mitochondrial DNA and is composed of information inherited from two parents, one male, and one female, rather than...
tests.
However, there are still concerns that species are being identified prematurely. Ian Tattersall
Ian Tattersall
Ian Tattersall is a paleoanthropologist and a curator at the American Museum of Natural History. Tattersall received his PhD from Yale University in 1971. In addition to human evolution, he has worked extensively with lemurs. He is working with The Templeton Foundation.-Selected publications:* The...
, an anthropologist who recognized 42 species of lemur in 1982, has expressed concern that the geographically organized variety in lemur populations is being recognized with full species status while the number of subspecies in lemur genera has virtually disappeared. He has argued that taxonomists are confusing differentiation and speciation
Speciation
Speciation is the evolutionary process by which new biological species arise. The biologist Orator F. Cook seems to have been the first to coin the term 'speciation' for the splitting of lineages or 'cladogenesis,' as opposed to 'anagenesis' or 'phyletic evolution' occurring within lineages...
, two processes that are often unrelated, while denying the role of microevolution
Microevolution
Microevolution is the changes in allele frequencies that occur over time within a population. This change is due to four different processes: mutation, selection , gene flow, and genetic drift....
in evolutionary processes. Still other researchers who emphasize the framework of the "general lineage concept of species" contend that lineage divergence or differentiation demarcates the beginning of a new species.
New species have been identified due to differences in morphology
Comparative anatomy
Comparative anatomy is the study of similarities and differences in the anatomy of organisms. It is closely related to evolutionary biology and phylogeny .-Description:...
, karyotypes, cytochrome b sequences, and other genetic tests, as well as several combinations of these. When nuclear DNA (nDNA) was tested in conjunction with mitochondrial DNA (mtDNA) in mouse lemurs, a few species, such as Claire's mouse lemur
Claire's Mouse Lemur
Claire's mouse lemur , or Nosy Be mouse lemur, is a newly described species of lemur from the genus of the mouse lemurs . It lives on the island Nosy Bé in the Antsiranana province of Madagascar, and on the mainland near the village of Manehoka, including Lokobe Reserve...
(Microcebus mamiratra) were demonstrated to be indistinguishable from other closely related species. In such cases, nDNA did not vary, but the mtDNA that had been used to define it as a species was still distinct. Differences in results between nDNA, which is inherited from both parents, and mtDNA, which is inherited from the mother, was attributed to female philopatry
Philopatry
Broadly, philopatry is the behaviour of remaining in, or returning to, an individual's birthplace. More specifically, in ecology philopatry is the behaviour of elder offspring sharing the parental burden in the upbringing of their siblings, a classic example of kin selection...
, where females remain within or close to the home range
Home range
Home range is the area where an animal lives and travels in. It is closely related to, but not identical with, the concept of "territory".The concept that can be traced back to a publication in 1943 by W. H. Burt, who constructed maps delineating the spatial extent or outside boundary of an...
into which they were born while males disperse. Since the isolated population known as Claire's mouse lemur has distinct mtDNA, but not nDNA, it is likely to contain a population descended from a related group of females, but which still disperses and interbreeds with nearby populations.
Traditionally, karyology has been considered when determining species status. For example, in 2006, three new species of sportive lemur were named based partly on karyotypes. From the lemurs studied so far, the diploid number of chromosomes varies between 2n=20 and 2n=66. In the case of the brown lemurs, the diploid number ranges from 2n=44 to 2n=60 while the individual chromosome sizes vary considerably, despite strong similarities in morphology.
Sometimes distinctions are made due to very slight differences in pelage coloration. For instance, three distinctly colored types of mouse lemur were discovered in a multi-year study in 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 southern Madagascar, but rather than being separate species, DNA tests revealed that they all belonged to a single species, the reddish-gray mouse lemur
Reddish-gray Mouse Lemur
The reddish-gray mouse lemur also known as the gray-brown mouse lemur or rufous-gray mouse lemur, is found in Western Madagascar in the region around Beza Mahafaly Reserve, north to Lamboharana....
(Microcebus griseorufus). For this reason, further research is needed to confirm or deny the recent species splits. Only through detailed studies of morphology, ecology, behavior, and genetics can the true number of lemur species be determined.
| 1931 Schwarz |
1982 Tattersall |
1994 Mittermeier et al. |
2005 Groves |
2006 Mittermeier et al. |
2010 Mittermeier et al. |
|||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| genus | species | subspecies | species | subspecies | species | subspecies | species | subspecies | species | subspecies | species | subspecies |
| Allocebus | – | – | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 |
| Avahi | 1 | 2 | 1 | 2 | 2 | 0 | 3 | 0 | 4 | 0 | 9 | 0 |
| Cheirogaleus | 3 | 4 | 2 | 0 | 2 | 0 | 7 | 0 | 7 | 0 | 5 | 0 |
| Daubentonia | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 |
| Eulemur | – | – | – | – | 5 | 8 | 11 | 2 | 10 | 2 | 12 | 0 |
| Hapalemur | 2 | 2 | 2 | 3 | 3 | 3 | 4 | 2 | 5 | 0 | 5 | 3 |
| Indri | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 2 | 1 | 0 | 1 | 0 |
| Lemur | 6 | 7 | 4 | 7 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 |
| Lepilemur | 2 | 0 | 1 | 6 | 7 | 0 | 8 | 0 | 8 | 0 | 26 | 0 |
| Microcebus | 2 | 2 | 2 | 0 | 3 | 0 | 8 | 0 | 12 | 0 | 18 | 0 |
| Mirza | – | – | 1 | 0 | 1 | 0 | 1 | 0 | 2 | 0 | 2 | 0 |
| Phaner | 1 | 0 | 1 | 0 | 1 | 4 | 4 | 0 | 4 | 0 | 4 | 0 |
| Prolemur | – | – | – | – | – | – | 1 | 0 | 1 | 0 | 1 | 0 |
| Propithecus | 2 | 9 | 2 | 9 | 3 | 8 | 7 | 4 | 9 | 0 | 9 | 0 |
| Varecia | – | – | 1 | 2 | 1 | 2 | 1 | 4 | 2 | 3 | 2 | 3 |
| Totals | 21 | 26 | 20 | 29 | 32 | 25 | 59 | 14 | 68 | 5 | 97 | 6 |
| 38 | 42 | 50 | 67 | 71 | 101 | |||||||
Literature cited
}}
}
}
}