Taxonomy of lemurs

From Wikipedia, the free encyclopedia

This is an old revision of this page, as edited by Maky (talk | contribs) at 23:24, 27 March 2011 (Begin article split from Evolutionary history of lemurs). The present address (URL) is a permanent link to this revision, which may differ significantly from the current revision.

(diff) ← Previous revision | Latest revision (diff) | Newer revision → (diff)
Two ring-tailed lemur sit curled up together on a rock.
The ring-tailed lemur was one of the first lemurs to be classified by Carl Linnaeus in 1753.

The taxonomic history of lemurs spans back to 1753 when Carl Linnaeus first defined the genus and remains controversial today, with approximately 70 to 100 taxa (species and subspecies) recognized, depending on how the 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 are now restricted to 10% of the island, or approximately 60,000 square kilometres (23,000 sq mi), and many face extinction. For this reason, researchers have been trying to identify and assess every species. Over the last 10 to 20 years, there has been a steep increase in the number of recognized lemur species and subspecies both through the discovery of new species and the elevation of existing subspecies to full species status. Currently there are approximately 100 or more recognized species or subspecies of living lemur, which are divided into five families and 15 genera. If the extinct subfossil lemurs are included, an additional three families, eight genera, and 17 species would be included. 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.

Taxonomic and phylogenetic classification

Lemur taxonomy is controversial, and not all experts agree, particularly with the recent increase in the number of recognized species.[1][2][3] According to Russell Mittermeier, 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.[4] Conversely, other experts in the field label this as a possible example of taxonomic inflation,[3] and prefer instead an estimate of at least 50 species.[1] All sides generally agree that the recently extinct subfossil lemurs should be classified in three families, eight genera, and 17 species.[5][6]

Closest lemur relations[7]
Euarchonta 

Scandentia (treeshrews)

Dermoptera (colugos)

Since the first taxonomic classification of lemurs in 1758 by Carl Linnaeus,[8] many changes have been made to lemur taxonomy. Within the order Primates, treeshrews (order Scandentia) were considered basal, prosimian primates—close relatives of lemurs—until the 1980s.[9] Colugos, also incorrectly referred to as "flying lemurs", were once considered lemur-like primates, but were reclassified as close relatives of bats,[10] and more recently as close relatives of primates within their own order, Dermoptera.[7] Primates, together with their closest relatives, the treeshrews, colugos, and long-extinct plesiadapiforms, form the taxonomically unranked Euarchonta clade within the Euarchontoglires. Also, all lorisids 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.[11][12]

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 and Alphonse Milne-Edwards.[13][14] The taxonomic nomenclature of lemurs was not sorted out until decades later, when Ernst Schwarz standardized it in 1931.[13][14][15] It was not until the 1990s that this nomenclature started to see a new wave of taxonomic change.[3]

Suprageneric classification

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.[16] In 1915, William King Gregory published a classification[17] 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).[16] 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.[18]

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.[11] 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.[19] 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.[12]

Two alternative lemur classifications at the infraorder and superfamily levels
3 infraorders, 2 superfamilies[11] 1 infraorder, 2 superfamilies[12][20]

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 up until very recently.[21][22][16] Hinged upon morphological traits and molecular data, it has had profound implications on scientific theories.[22] Arguing against Darwin's theory of natural selection, Richard Owen claimed in 1863 that the aye-aye's distinct characteristics, including its ever-growing incisors 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.[22] More recently, the aye-aye's placement within the order Primates 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 present-day distribution of non-human primates on Madagascar.[21]

Aye-aye (a lemuriform primate with large head, ears, and eyes; black, wiry fur; long, bushy tail; and hands with one unusually thin and long middle finger) perched on a branch
The aye-aye has traditionally been difficult to classify due to its unique physical traits.

Until Richard Owen published a definitive anatomical study in 1866, early naturalists were uncertain whether the aye-aye (genus Daubentonia) was a primate, rodent, or marsupial.[22][23][24] In the late eighteenth century, for example, the aye-aye was classified under the squirrel genus Sciurus.[25] 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.[22][26] 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 toothcombed primates.[27] However, the placement of the aye-aye within the order 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.[28] Based on its anatomy, researchers have found support for classifying the genus Daubentonia as a specialized indriid, a monotypic sister group to all strepsirrhines, and an indeterminate taxon within the order Primates.[29] 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.[15] 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,[30] despite molecular tests that had shown Daubentoniidae was basal to all Lemuriformes.[29][31] In 2008, Russell Mittermeier, Colin Groves, and others ignored addressing higher-level taxonomy by defining lemurs as monophyletic and containing five living families, including Daubentoniidae.[19]

Another interpretation of the aye-aye's origins has once again called into question the single origins of the lemurs. Comparisons have been made between the aye-aye and a fossil strepsirrhine primate from Africa, Plesiopithecus. Similarities in the shape of the skull and the morphology of the lower jaw have raised the question of whether or not this could be an aye-aye ancestor. However, the placement of an aye-aye ancestor in Africa would require multiple colonizations 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.[12]

Often classified with the galagos by early students, the cheirogaleids were placed with the other lemurs from Gregory's 1915 classification until the early 1970s, when several anthropologists proposed that they are more closely related to lorisiforms, based on morphological data.[16][32] However, relevant genetic studies nearly unanimously place cheirogaleids within the lemuriform clade and Groves, who had promoted the cheirogaleid-lorisiform relationship in a 1974 paper, by 2001 himself regarded the idea as refuted.[29][31][32]

Lemur phylogeny[33][34][35]

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.[16] Because of concerns that Lemuridae might not be monophyletic, the family was later split; in 1982, for example, 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).[36] This classification is still used, except that the bamboo lemurs are placed in Lemuridae.[37][19]

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,[38] but neither view is supported by molecular phylogeny.[33] The sportive lemurs and the extinct koala lemurs (Megaladapidae) both lack upper incisors in the permanent dentition,[23] and in 1981, Groves placed both together in the family Megaladapidae, which he renamed Lepilemuridae in 2005 because that older name takes precedence.[39] 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).[40][41][35] The sloth lemurs (Palaeopropithecidae) and monkey lemurs (Archaeolemuridae) were classified as subfamilies within Indriidae as late as 1982,[36] but are now recognized as separate families.[35]

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.[33] 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.[35] 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.[29][33][35] However, two problems create complications for both approaches. First, the four most closely related lemur families diverged within a narrow window of approximately 10 million years, making it much harder to distinguish the splits with molecular evidence. Second, the divergence occurred approximately 42 mya;[42] such distant splits create a lot of noise for molecular techniques.

Genus-level classification

Early classifications of the genera of lemurs differed in a number of ways from current taxonomy. For example, the fork-marked lemurs were initially placed in the genus Lemur and then in Microcebus with the mouse lemurs before being placed in their own genus Phaner;[43][44][15][45] and Charles Immanuel Forsyth Major split the Cheirogaleus medius species group of the dwarf lemurs into a separate genus Opolemur, but this was not accepted.[45][15] Genus-level taxonomy was largely stabilized by Schwarz in 1931,[15] but a number of changes have become accepted:

  • The ring-tailed lemur, ruffed lemurs, and true 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 true lemurs are nearly indistinguishable.[46] However, ruffed lemurs were reassigned to the genus Varecia in 1962,[47] and due to similarities between the ring-tailed lemur and the bamboo lemurs, particularly in regards to molecular evidence and scent glands similarities, the true lemurs were moved to the genus Eulemur in 1988.[48][46][49] The genus Lemur is now monotypic, containing only the ring-tailed lemur.
  • In 2001, Colin Groves concluded that despite similarities, the greater bamboo lemur was sufficiently distinct from the bamboo lemurs of the genus Hapalemur to merit its own monotypic genus, Prolemur.[46][50] This follows Schwarz's 1931 opposition to Pocock's decision to separate Prolemur from Hapalemur.[15]
  • Originally placed in the genus Microcebus (mouse lemurs), the giant mouse lemur was moved to its own genus, Mirza, in 1985 due to its larger size, morphological differences, dental characteristics, and behavior.[43][51]
  • The hairy-eared dwarf lemur was first placed in the genus Cheirogaleus (dwarf lemurs) in 1875 and was later found to have closer affinities with Microcebus. However, its dentition and cranium structure were sufficiently distinct to merit elevation to its own genus, Allocebus.[43][52]

Species-level classification

Over the past two decades, the number of recognized lemur species has more than doubled 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.[1][53] 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.[19] In late 2010, the 3rd edition of Lemurs of Madagascar listed 101 taxa.[4] 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.[1]

A sportive lemur (small body, long legs, brown fur, large eyes, and thick, furry tail) clings to the side of a tree, with its head turned towards the camera.
The Sahamalaza sportive lemur (Lepilemur sahamalazensis) was identified as a distinct species as recently as 2006.

This threefold increase in nearly 15 years 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.[1][19] Implicitly, this means that full species status will help grant genetically distinct populations added environmental protection.[1]

The first large wave of new lemur species descriptions came in 2001 when Colin Groves elevated the red ruffed lemur (Varecia rubra),[46][54] five subspecies of brown lemur (Eulemur albifrons, E. albocollaris, E. collaris, E. rufus and E. sanfordi),[55] and four subspecies of sifaka (Propithecus coquereli, P. deckenii, P. edwardsi, and P. perrieri) to full species status.[56] Additional elevations of all remaining subspecies within the Eulemur and Propithecus genera were made in the years that followed.[48][46][57] These and subsequent changes in taxonomy were largely due to a shift to the phylogenetic species concept,[58] yet are not universally endorsed.[3]

By far the most explosive growth in species numbers has been in the genera Microcebus and Lepilemur. In 2006, 15 new species of Lepilemur were described, with three new species reported in February,[59] one species in June,[60] and 11 in September.[61] Since then, two additional species have been described.[19] 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.[3][40]

In true lemurs and mouse lemurs, both groups 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 true lemurs).[62][63] With molecular research suggesting a more distant split in both genera, these subspecies or undistinguished populations have been promoted to species status.[63]

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),[15] 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.[64] 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.[43] 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.[19][65][66][67] Many, but not all of these defined species have been supported by nuclear DNA tests.[68]

However, there are still concerns that species are being identified prematurely. Ian Tattersall, an anthropologist who recognized 42 species of lemur in 1982,[69] 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.[3] 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.[68]

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.[3] 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.[68]

Traditionally, karyology has been considered when determining species status. From the lemurs studied so far, the diploid number of chromosomes in lemurs varies between 2n=20 and 2n=66. In the case of the true lemurs, the diploid number ranges from 2n=48 to 2n=60 while the individual chromosome sizes vary considerably.[28]

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).[70] 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.[1]

Lemur species and subspecies count by year and genus
1931
Schwarz[15]
1982
Tattersall[69]
1994
Mittermeier et al.[71]
2005
Groves[37]
2006
Mittermeier et al.[53]
2010
Mittermeier et al.[4]
genus species subspecies species subspecies species subspecies species subspecies species subspecies species subspecies
Allocebus[N 1] 1 0 1 0 1 0 1 0 1 0
Avahi 1 2 1 2 2 0 3 0 4 0 9 0
Cheirogaleus[N 1] 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[N 2] 5 8 11 2 10 2 12 0
Hapalemur[N 3] 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[N 2][N 4] 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[N 5] 2 2 2 0 3 0 8 0 12 0 18 0
Mirza[N 5] 1 0 1 0 1 0 2 0 2 0
Phaner 1 0 1 0 1 4 4 0 4 0 4 0
Prolemur[N 3] 1 0 1 0 1 0
Propithecus 2 9 2 9 3 8 7 4 9 0 9 0
Varecia[N 4] 1 2 1 2 1 4 2 3 2 3
Totals[N 6] 21 26 20 29 32 25 59 14 68 5 97 6
38 42 50 67 71 101

Notes

  1. ^ a b In 1931, Allocebus was not recognized as a separate genus, but was lumped under the genus Cheirogaleus.
  2. ^ a b In 1931 and 1982, Eulemur was not recognized as a separate genus, but was lumped under the genus Lemur.
  3. ^ a b The genus Prolemur was not distinguished until 2001. Prior to this, the greater bamboo lemur was placed in the genus Hapalemur.
  4. ^ a b In 1931, Varecia was not recognized as a separate genus, but was lumped under the genus Lemur.
  5. ^ a b In 1931, Mirza was not recognized as a separate genus, but was lumped under Microcebus.
  6. ^ The grand total of species and subspecies for each year will not equal the sum of the species total and the subspecies total since each subspecies group already counts as one species. For example, in 2010 there were three subspecies for Varecia variegata recognized: V. v. variegata, V. v. editorum, and V. v. subcincta. Together, they count as one species, which is already included in the species total for that year. The same applies that year for Hapalemur. For this reason there are 101 species and subspecies (97 − 2 + 6 = 101), not 103. In 1994, there were seven species with subspecies listed, so the grand total is: 32 − 7 + 25 = 50

References

  1. ^ a b c d e f g Yoder, A.D. (2007). "Lemurs: a Quick Guide" (PDF). Current Biology. 17 (20): 866–868.
  2. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1186/1471-2148-9-30, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1186/1471-2148-9-30 instead.
  3. ^ a b c d e f g Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1002/evan.20126, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1002/evan.20126 instead.
  4. ^ a b c Mittermeier et al. 2010, pp. 100–103.
  5. ^ Mittermeier et al. 2006, pp. 37–51.
  6. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1016/j.crpv.2009.02.001, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1016/j.crpv.2009.02.001 instead.
  7. ^ a b Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1126/science.1147555, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1126/science.1147555 instead.
  8. ^ Linnaeus 1753, p. 30.
  9. ^ Rowe 1996, p. 13.
  10. ^ Rowe 1996, p. 27.
  11. ^ a b c Groves, C. P. (2005). "Strepsirrhini". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  12. ^ a b c d Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1159/000095391, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1159/000095391 instead.
  13. ^ a b Jolly & Sussman 2006, pp. 19–40.
  14. ^ a b Mittermeier et al. 2006, pp. 27–36.
  15. ^ a b c d e f g h Schwarz, E. (1931). "A revision of the genera and species of Madagascar Lemuridae". Proceedings of the Zoological Society of London. 1931: 399–428.
  16. ^ a b c d e Tattersall 1982, pp. 246–247.
  17. ^ Gregory, W.K. (1915). "1. On the relationships of the Eocene lemur Notharctus to the Adapidae and other primates. 2. On the classification and phylogeny of the Lemuroidea". Bulletin of the Geological Society of America. 26: 419–446.
  18. ^ Simpson, G.G. (1945). Tyler, R. (ed.). "The principles of classification and the classification of mammals" (PDF). Bulletin of the America Museum of Natural History. 85. New York: Order of the Trustees.
  19. ^ a b c d e f g Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1007/s10764-008-9317-y, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1007/s10764-008-9317-y instead.
  20. ^ Cartmill 2010, pp. 10–30.
  21. ^ a b Garbutt 2007, pp. 85–86.
  22. ^ a b c d e Sterling & McCreless 2006, pp. 159–184.
  23. ^ a b Ankel-Simons 2007, pp. 224–283.
  24. ^ Garbutt 2007, pp. 205–207.
  25. ^ Elliot 1907, p. 5527.
  26. ^ Owen, R. (1866). "On the Aye-aye (Chiromys, Cuvier; Chiromys Madagascariensis, Desm.; Sciurus Madagascariensis, Gmel., Sonnerat; Lemur Psilodactylus, Schreber, Shaw)" (PDF). Transactions of the Zoological Society of London. 5: 33–101. Retrieved 18 February 2011.
  27. ^ Simons 1997, pp. 142–166.
  28. ^ a b Ankel-Simons 2007, pp. 533–559.
  29. ^ a b c d Yoder 2003, pp. 1242–1247.
  30. ^ Groves, C. P. (2005). "Chiromyiformes". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  31. ^ a b Attention: This template ({{cite pmid}}) is deprecated. To cite the publication identified by PMID 8952078, please use {{cite journal}} with |pmid= 8952078 instead.
  32. ^ a b Groves 2001, p. 55.
  33. ^ a b c d Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1101/gr.7265208, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1101/gr.7265208 instead.
  34. ^ Godfrey & Jungers 2003, pp. 1247–1252.
  35. ^ a b c d e Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1186/1471-2148-8-121, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1186/1471-2148-8-121 instead.
  36. ^ a b Tattersall 1982, p. 263.
  37. ^ a b Groves, C. P. (2005). "Order Primates". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  38. ^ Groves 2001, pp. 54–55.
  39. ^ Groves, C. P. (2005). "Lepilemuridae". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  40. ^ a b Garbutt 2007, pp. 115–136.
  41. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1073/pnas.0408354102, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1073/pnas.0408354102 instead.
  42. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1046/j.1365-294X.2004.02106.x, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1046/j.1365-294X.2004.02106.x instead.
  43. ^ a b c d Garbutt 2007, pp. 86–114.
  44. ^ Groves, C. P. (2005). "Phaner". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  45. ^ a b Groves 2001, pp. 65–66.
  46. ^ a b c d e Garbutt 2007, pp. 137–175.
  47. ^ Groves, C. P. (2005). "Varecia". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  48. ^ a b Mittermeier et al. 2006, pp. 209–323.
  49. ^ Groves, C. P. (2005). "Eulemur". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  50. ^ Groves, C. P. (2005). "Prolemur". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  51. ^ Groves, C. P. (2005). "Mirza". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  52. ^ Groves, C. P. (2005). "Allocebus". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  53. ^ a b Mittermeier et al. 2006, pp. 85–88.
  54. ^ Groves, C. P. (2005). "Varecia rubra". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  55. ^ Groves, C. P. (2005). "Eulemur fulvus". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  56. ^ Groves, C. P. (2005). "Propithecus". In Wilson, D. E.; Reeder, D. M (eds.). Mammal Species of the World: A Taxonomic and Geographic Reference (3rd ed.). Johns Hopkins University Press. pp. 111–184. ISBN 978-0-8018-8221-0. OCLC 62265494.
  57. ^ Garbutt 2007, pp. 176–204.
  58. ^ Thalmann, U. (December 2006). "Lemurs – Ambassadors for Madagascar" (PDF). Madagascar Conservation & Development. 1: 4–8. ISSN 1662-2510.
  59. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1186/1471-2148-6-17, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1186/1471-2148-6-17 instead.
  60. ^ Rabarivola, C.; Zaramody, A.; Fausser, J.; Andriaholinirina, N.; Roos, C.; Zinner, D.; Marcel, H.; Rumpler, Y. (2006). "Cytogenetic and molecular characteristics of a new species of sportive lemur from Northern Madagascar" (PDF). Lemur News. 11: 45–49. ISSN 0343-3528.
  61. ^ Louis, Jr., E.E.; Engberg, S.E.; Lei, R.; Geng, H.; Sommer, J.A.; Randriamamapionona, R.; Randriamanana, J.C.; Zaonarivelo, J.R.; Andriantompohavana, R. (2006). "Molecular and morphological analyses of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) reveals 11 previously unrecognized species" (PDF). Texas Tech University Special Publications (49): 1–49. ISSN 0169-0237. {{cite journal}}: Check |issn= value (help)
  62. ^ Sussman 2003, pp. 149–229.
  63. ^ a b Johnson 2006, pp. 187–210.
  64. ^ Kappeler & Rasoloarison 2003, pp. 1310–1315.
  65. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1186/1741-7007-6-19, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1186/1741-7007-6-19 instead.
  66. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1016/j.ympev.2006.10.026, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1016/j.ympev.2006.10.026 instead.
  67. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1896/052.023.0103, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1896/052.023.0103 instead.
  68. ^ a b c Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1371/journal.pone.0009883, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1371/journal.pone.0009883 instead.
  69. ^ a b Tattersall 1982, pp. 40–43.
  70. ^ Attention: This template ({{cite doi}}) is deprecated. To cite the publication identified by doi: 10.1186/1471-2148-6-98, please use {{cite journal}} (if it was published in a bona fide academic journal, otherwise {{cite report}} with |doi= 10.1186/1471-2148-6-98 instead.
  71. ^ Mittermeier et al. 1994, pp. 80–82.

Literature cited

  • Yoder, A.D. (2003). "Phylogeny of the Lemurs". pp. 1242–1247. {{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)
  • Kappeler, P.M.; Rasoloarison, R.M. (2003). "Microcebus, Mouse Lemurs, Tsidy". pp. 1310–1315. {{cite book}}: Invalid |ref=harv (help); Missing or empty |title= (help)
  • Linnaeus, Carl (1753). Systema Naturae (in Latin). Vol. 1. Stockholm: Impensis Direct. Laurentii Salvii. {{cite book}}: Invalid |ref=harv (help)