"Lemurs of Madagascar" redirects here. For the book, see Lemurs of Madagascar (book). For other uses, see Lemur (disambiguation).
Lemurs ( ( listen)LEE-mər) are a clade of strepsirrhineprimatesendemic to the island of Madagascar. The word lemur derives from the word lemures (ghosts or spirits) from Roman mythology and was first used to describe a slender loris due to its nocturnal habits and slow pace, but was later applied to the primates on Madagascar. As with other strepsirrhine primates, such as lorises, pottos, and galagos (bush babies), lemurs share resemblance with basal primates. In this regard, lemurs are often confused with ancestral primates, when in actuality, lemurs did not give rise to monkeys and apes, but evolved independently.
Due to Madagascar's highly seasonal climate, lemur evolution has produced a level of species diversity rivaling that of any other primate group. Until shortly after humans arrived on the island around 2,000 years ago, there were lemurs as large as a male gorilla. Today, there are nearly 100 species of lemurs, and most of those species have been discovered or promoted to full species status since the 1990s; however, lemur taxonomic classification is controversial and depends on which species concept is used. Even the higher-level taxonomy is disputed, with some experts preferring to place most lemurs within the infraorderLemuriformes, while others prefer Lemuriformes to contain all living strepsirrhines, placing all lemurs in the superfamilyLemuroidea and all lorises and galagos in the superfamily Lorisoidea.[a]
Ranging in weight from the 30-gram (1.1 oz) mouse lemur to the 9-kilogram (20 lb) indri, lemurs share many common, basal primate traits, such as divergent digits on their hands and feet and nails instead of claws (in most species). However, their brain-to-body size ratio is smaller than that of anthropoid primates, and among many other traits they share with other strepsirrhine primates, they have a "wet nose" (rhinarium). Lemurs are generally the most social of the strepsirrhine primates and communicate more with scents and vocalizations than with visual signals. Many lemur adaptations are in response to Madagascar's highly seasonal environment. Lemurs have relatively low basal metabolic rates and may exhibit seasonal breeding, dormancy (such as hibernation or torpor), or female social dominance. Most eat a wide variety of fruits and leaves, while some are specialists. Although many share similar diets, different species of lemur share the same forests by differentiating niches.
Lemur research during the 18th and 19th centuries focused on taxonomy and specimen collection. Although field observations trickled in from early explorers, modern studies of lemur ecology and behavior did not begin in earnest until the 1950s and 1960s. Initially hindered by political instability and turmoil on Madagascar during the mid-1970s, field studies resumed in the 1980s and have greatly increased the understanding of these primates. Research facilities like the Duke Lemur Center have provided research opportunities under more controlled settings. Lemurs are important for research because their mix of ancestral characteristics and traits shared with anthropoid primates can yield insights on primate and human evolution. However, many lemur species are threatened with extinction due to habitat loss and hunting. Although local traditions generally help protect lemurs and their forests, illegal logging, widespread poverty, and political instability hinder and undermine conservation efforts. Because of these threats and their declining numbers, the International Union for Conservation of Nature (IUCN) considers lemurs to be the world's most endangered mammals, noting that—as of 2013—up to 90% of all lemur species face extinction within the next 20 to 25 years.
Carl Linnaeus, the founder of modern binomial nomenclature, gave lemurs their name as early as 1758, when he used it in the 10th edition of Systema Naturae. He included three species under the genus Lemur: 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).
Lemures dixi hos, quod noctu imprimis obambulant, hominibus quodanmodo similes, & lento passu vagantur.
[I call them lemurs, because they go around mainly by night, in a certain way similar to humans, and roam with a slow pace.]
in reference to the red slender loris
Although the term "lemur" was first intended for slender lorises, it was soon limited to the endemic Malagasy primates, which have been known as "lemurs" ever since. The name derives from the Latin term lemures, which refers to specters or ghosts that were exorcised during the Lemuria festival of ancient Rome. According to Linnaeus' own explanation, the name was selected because of the nocturnal activity and slow movements of the slender loris. 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. However, Dunkel et al. noted in 2012 that it has been commonly and falsely assumed that Linnaeus was referring to the ghost-like appearance, reflective eyes, and ghostly cries of lemurs. It has also been speculated that Linnaeus may also have known that some Malagasy people have held legends that lemurs are the souls of their ancestors, but this is unlikely given that the name was selected for slender lorises from India, according to Dunkel et al.
Main article: Evolution of lemurs
Lemurs are primates belonging to the suborder Strepsirrhini. Like other strepsirrhine primates, such as lorises, pottos, and galagos, they share ancestral (or plesiomorphic) traits with early primates. In this regard, lemurs are popularly confused with ancestral primates; however, lemurs did not give rise to monkeys and apes (simians). Instead, they evolved independently in isolation on Madagascar. All modern strepsirrhines including lemurs are traditionally thought to have evolved from early primates known as adapiforms during the Eocene (56 to 34 mya) or Paleocene (66 to 56 mya). Adapiforms, however, lack a specialized arrangement of teeth, known as a toothcomb, which nearly all living strepsirrhines possess. A more recent hypothesis is that lemurs descended from lorisoids (loris-like) primates. This is supported by comparative studies of the cytochrome b gene and the presence of the strepsirrhine toothcomb in both groups. Instead of being the direct ancestors of lemurs, the adapiforms may have given rise to both the lemurs and lorisoids, a split that would be supported by molecular phylogenetic studies. The later split between lemurs and lorises is thought to have occurred approximately 62 to 65 mya according to molecular studies, although other genetic tests and the fossil record in Africa suggest more conservative estimates of 50 to 55 mya for this divergence. However, the oldest lemur fossils on Madagascar are actually subfossils dating to the Late Pleistocene.
Once part of the supercontinent Gondwana, the island of Madagascar has been isolated since it broke away from eastern Africa (~160 mya), Antarctica (~80–130 mya), and India (~80–90 mya). Since ancestral lemurs are thought to have originated in Africa around 62 to 65 mya, they must have crossed the Mozambique Channel, a deep channel between Africa and Madagascar with a minimum width of about 560 km (350 mi). In 1915, paleontologistWilliam Diller Matthew noted that the mammalian biodiversity on Madagascar (including lemurs) can only be accounted for by random rafting events, where very small populations rafted from nearby Africa on tangled mats of vegetation, which get flushed out to sea from major rivers. This form of biological dispersal can occur randomly over millions of years. In the 1940s, American paleontologist George Gaylord Simpson coined the term "sweepstakes hypothesis" for such random events. Rafting has since been the most accepted explanation for the lemur colonization of Madagascar, but until recently this trip was thought to be very unlikely because strong ocean currents flow away from the island. In January 2010, a report demonstrated that around 60 mya both Madagascar and Africa were 1,650 km (1,030 mi) south of their present-day positions, placing them in a different ocean gyre, producing currents that ran counter to what they are today. The ocean currents were shown to be even stronger than today, which would have pushed a raft along faster, shortening the trip to 30 days or less—short enough for a small mammal to survive easily. As the continental plates drifted northward, the currents gradually changed, and by 20 mya the window for oceanic dispersal had closed, effectively isolating the lemurs and the rest of the terrestrial Malagasy fauna from mainland Africa. Isolated on Madagascar with only a limited number of mammalian competitors, the lemurs did not have to compete with other evolving arboreal mammalian groups, such as squirrels. They were also spared from having to compete with monkeys, which evolved later. The intelligence, aggression, and deceptiveness of monkeys gave them an advantage over other primates in exploiting the environment.
Distribution and diversity
See also: Subfossil lemur
Lemurs have adapted to fill many open ecological niches since making their way to Madagascar. Their diversity in both behavior and morphology (outward appearance) rivals that of the monkeys and apes found elsewhere in the world. Ranging in size from the 30 g (1.1 oz) Madame Berthe's mouse lemur, the world's smallest primate, to the recently extinct 160–200 kg (350–440 lb) Archaeoindris fontoynonti, lemurs evolved diverse forms of locomotion, varying levels of social complexity, and unique adaptations to the local climate.
Lemurs lack any shared traits that make them stand out from all other primates. Different types of lemurs have evolved unique combinations of unusual traits to cope with Madagascar's harsh, seasonal climate. These traits can include seasonal fat storage, hypometabolism (including torpor and hibernation), small group sizes, low encephalization (relative brain size), cathemerality (activity both day and night), and strict breeding seasons. Extreme resource limitations and seasonal breeding are also thought to have given rise to three other relatively common lemur traits: female social dominance, sexual monomorphism, and male–male competition for mates involving low levels of agonism, such as sperm competition.
Before the arrival of humans roughly 1500 to 2000 years ago, lemurs were found all across the island. However, early settlers quickly converted the forests to rice paddies and grassland through slash-and-burn agriculture (known locally as tavy), restricting lemurs to approximately 10% of the island's area, ~60,000 km2 (23,000 sq mi). Today, the diversity and complexity of lemur communities increases with floral diversity and precipitation and is highest in the rainforests of the east coast, where precipitation and floral diversity are also at their highest. Despite their adaptations for weathering extreme adversity, habitat destruction and hunting have resulted in lemur populations declining sharply, and their diversity has diminished, with the recent extinction of at least 17 species in eight genera, known collectively as the subfossil lemurs. Most of the approximately 100 species and subspecies of lemur are either threatened or endangered. Unless trends change, extinctions are likely to continue.
Until recently, giant lemurs existed on Madagascar. Now represented only by recent or subfossil remains, they were modern forms that were once part of the rich lemur diversity that has evolved in isolation. Some of their adaptations were unlike those seen in their living relatives. All 17 extinct lemurs were larger than the extant (living) forms, some weighing as much as 200 kg (440 lb), and are thought to have been active during the day. Not only were they unlike the living lemurs in both size and appearance, they also filled ecological niches that either no longer exist or are now left unoccupied. Large parts of Madagascar, which are now devoid of forests and lemurs, once hosted diverse primate communities that included more than 20 lemur species covering the full range of lemur sizes.
Taxonomic classification and phylogeny
Main article: Taxonomy of lemurs
For a more comprehensive list, see List of lemur species.
From a taxonomic standpoint, the term "lemur" originally referred to the genus Lemur, which currently contains only the ring-tailed lemur. The term is now used in the colloquial sense in reference to all Malagasy primates.
Lemur taxonomy is controversial, and not all experts agree, particularly with the recent increase in the number of recognized species. According to Russell Mittermeier, the president of Conservation International (CI), taxonomist Colin Groves, and others, there are nearly 100 recognized species or subspecies of extant (or living) lemur, divided into five families and 15 genera. Because genetic data indicates that the recently extinct subfossil lemurs were closely related to living lemurs, an additional three families, eight genera, and 17 species can be included in the total. In contrast, other experts have labeled this as taxonomic inflation, instead preferring a total closer to 50 species.
The classification of lemurs within the suborder Strepsirrhini is equally controversial, although most experts agree on the same phylogenetic tree. In one taxonomy, the infraorder Lemuriformes contains all living strepsirrhines in two superfamilies, Lemuroidea for all lemurs and Lorisoidea for the lorisoids (lorisids and galagos). Alternatively, the lorisoids are sometimes placed in their own infraorder, Lorisiformes, separate from the lemurs. In another taxonomy published by Colin Groves, the aye-aye was placed in its own infraorder, Chiromyiformes, while the rest of the lemurs were placed in Lemuriformes and the lorisoids in Lorisiformes.
Although it is generally agreed that the aye-aye is the most basal member of the lemur clade, the relationship between the other four families is less clear since they diverged during a narrow 10 to 12 million-year window between the Late Eocene (42 mya) and into the Oligocene (30 mya). The two main competing hypotheses are shown in the adjacent image.
|2 infraorders||3 infraorders||4 infraorders|
Lemur taxonomy has changed significantly since the first taxonomic classification of lemurs by Carl Linnaeus in 1758. One of the greatest challenges has been the classification of the aye-aye, which has been a topic of debate up until very recently. 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. However, the placement of the aye-aye within the order Primates remained problematic until very recently. Based on its anatomy, researchers have found support for classifying the genus Daubentonia as a specialized indriid, a sister group to all strepsirrhines, and as an indeterminate taxon within the order Primates. Molecular tests have now shown Daubentoniidae is basal to all Lemuriformes, and 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.
Relationships among lemur families have also proven to be problematic and have yet to be definitively resolved. To further complicate the issue, several Paleogene fossil primates from outside Madagascar, such as Bugtilemur, have been classified as lemurs. However, scientific consensus does not accept these assignments based on genetic evidence, and therefore it is generally accepted that the Malagasy primates are monophyletic. Another area of contention is the relationship between the sportive lemurs and the extinct koala lemurs (Megaladapidae). Formerly grouped in the same family due to similarities in dentition, they are no longer considered to be closely related due to genetic studies.
More taxonomic changes have occurred at the genus level, although these revisions have proven more conclusive, often supported by genetic and molecular analysis. The most noticeable revisions included the gradual split of a broadly defined genus Lemur into separate genera for the ring-tailed lemur, ruffed lemurs, and brown lemurs due to a host of morphological differences.
Due to several taxonomic revisions by Russell Mittermeier, Colin Groves, and others, the number of recognized lemur species has grown from 33 species and subspecies in 1994 to approximately 100 in 2008. With continuing cytogenetic and molecular genetic research, as well as ongoing field studies, particularly with cryptic species such as mouse lemurs, the number of recognized lemur species is likely to keep growing. However, the rapid increase in the number of recognized species has had its critics among taxonomists and lemur researchers. Since classifications ultimately depend on the species concept used, conservationists often favor definitions that result in the splitting of genetically distinct populations into separate species to gain added environmental protection. Others favor a more thorough analysis.
Anatomy and physiology
Lemurs vary greatly in size. They include the smallest primates in the world and, until recently, also included some of the largest. They currently range in size from about 30 g (1.1 oz) for Madame Berthe's mouse lemur (Microcebus berthae) up to 7–9 kg (15–20 lb) for the indri (Indri indri) and diademed sifaka (Propithecus diadema). When recently extinct species are considered, the size range extended up to that of a gorilla at 160–200 kg (350–440 lb) for Archaeoindris fontoynonti.
Like all primates, lemurs have five divergent digits with nails (in most cases) on their hands and feet. Most lemurs possess a laterally compressed, elongated nail, called a toilet-claw, on the second toe and use it for scratching and grooming. In addition to the toilet-claw, lemurs share a variety of other traits with other strepsirrhine primates, which include a rhinarium (or "wet nose"); a fully functional vomeronasal organ, which detects pheromones; a postorbital bar and the lack of postorbital closure (a wall of thin bone behind the eye); orbits (bony sockets that enclose the eye) that are not fully facing forward; left and right mandible (lower jaw) bones that are not fully fused; and a small brain-to-body mass ratio.
Additional traits shared with other prosimian primates (strepsirrhine primates and tarsiers) include a bicornuate (two-horned) uterus and epitheliochorial placentation. Because their thumbs are only pseudo-opposable, making their movement less independent of the other fingers, their hands are less than perfect at grasping and manipulating objects. On their feet, they have a widely abducted hallux (first toe) which facilitates the grasping of tree limbs. A common misconception is that lemurs have a prehensile tail, a trait found only in New World monkeys, particularly atelids, among primates. Lemurs also rely heavily on their sense of smell, a trait shared with most other mammals and early primates, but not with the visually oriented higher primates. This sense of smell is important in terms of marking territory as well as provide an indication of whether or not another lemur is a viable breeding partner.
Lemurs are a diverse group of primates in terms of morphology and physiology. Some lemurs, such as the sportive lemurs and indriids, have longer hind limbs than forelimbs, making them excellent leapers. Indriids also have a specialized digestive system for folivory, exhibiting enlarged salivary glands, a spacious stomach, and an elongated caecum (lower gut) that facilitates fermentation. The hairy-eared dwarf lemur (Allocebus trichotis) reportedly has a very long tongue, allowing it to feed on nectar. Likewise, the red-bellied lemur (Eulemur rubriventer) has a feathery brush-shaped tongue, also uniquely adapted to feed on nectar and pollen. The aye-aye has evolved some traits that are unique among primates, making it stand out among the lemurs. Such traits include continuously growing, rodent-like front teeth for gnawing through wood and hard seeds; a highly mobile, filiform (filament-shaped) middle finger for extracting food from tiny holes; large, bat-like ears for detecting hollow spaces within trees; and use of self-generated acoustical cues to forage.
Lemurs are unusual since they have great variability in their social structure, yet generally lack sexual dimorphism in size and canine tooth morphology. However, some species tend towards having larger females, and two species of true lemur (genus Eulemur), the gray-headed lemur (E. albocollaris) and the red lemur (E. rufus), exhibit size differences in canine teeth. True lemurs show sexual dichromatism (sexual differences in fur coloration), but the difference between the genders varies from strikingly obvious, as in the blue-eyed black lemur (E. macaco), to nearly imperceptible in the case of the common brown lemur (E. fulvus).
Crypsis, or the inability of humans to visually distinguish between two or more distinct species, has recently been discovered among lemurs, particularly within the sportive lemurs (Lepilemur) and mouse lemurs (Microcebus). With sportive lemurs, subspecies were traditionally defined based on slight morphological differences, but new genetic evidence has supported giving full species status to these regional populations. In the case of mouse lemurs, the gray mouse lemur (M. murinus), golden-brown mouse lemur (M. ravelobensis), and Goodman's mouse lemur (M. lehilahytsara) were considered the same species until recently, when genetic tests identified them as cryptic species.
The lemur dentition is heterodont (having multiple tooth morphologies) and derives from an ancestral primate permanent dentition of 188.8.131.52.1.3.3. Indriids, sportive lemurs, the aye-aye, and the extinct sloth lemurs, monkey lemurs, and koala lemurs have reduced dentitions, having lost incisors, canines, or premolars. The ancestral deciduous dentition is 184.108.40.206.3, but young indriids, aye-ayes, koala lemurs, sloth lemurs, and probably monkey lemurs have fewer deciduous teeth.
There are also noticeable differences in dental morphology and tooth topography between lemurs. Indri, for instance, have teeth that are perfectly adapted for shearing leaves and crushing seeds. In the toothcomb of most lemurs, the bottom incisors and canine teeth are procumbent (face forward rather than up) and finely spaced, thus providing a tool for either grooming or feeding. For instance, indri use their toothcomb not only for grooming, but also to pry out the large seeds from the tough epicarp of Beilschmiedia fruits, while fork-marked lemurs use their relatively long toothcomb to cut through tree bark to induce the flow of tree sap. The toothcomb is kept clean by the sublingua or "under-tongue", a specialized structure that acts like a toothbrush to remove hair and other debris. The sublingua extends below the tip of the tongue and is tipped with keratinized, serrated points that rake between the front teeth.
The island of Madagascar harbors a unique biodiversity that evolved due to its long-lasting isolation from other land masses. Numerous plant and animal species are found solely on Madagascar. Lemurs, a subgroup of primates, are among the most prominent representatives of the island's unique fauna. They are found almost exclusively on Madagascar. The only exceptions are two species of the genus Eulemur that also live on the Comoros Islands, where they probably have been introduced by humans.
Thanks to extensive field research over the past decades, numerous previously unknown lemur species have been discovered. Dwarf lemurs in turn received relatively little attention to date and the diversity within this genus is still not well known. Researchers of the universities of Mainz and Antananarivo have investigated lemur populations in southern Madagascar. Based on fieldwork and laboratory analyses, they now identified a previously unknown species of dwarf lemur. The findings of the research project have recently been published in the journal Molecular Phylogenetics and Evolution.
"Together with Malagasy scientists, we have been studying the diversity of lemurs for several years now," said Dr. Andreas Hapke of the Institute of Anthropology at Johannes Gutenberg University Mainz (JGU). "It is only now that we were able to determine that some of the animals examined represent a previously unknown species." The newly described Lavasoa Dwarf Lemur (Cheirogaleus lavasoensis) inhabits three isolated forest fragments in the extreme south of Madagascar. According to current knowledge, it does not occur outside this area. The exact population size is unknown. Preliminary estimates indicate that there are less than 50 individuals remaining. The Lavasoa Dwarf Lemur is thus rare and extremely endangered.
The lifestyle of dwarf lemurs makes them extremely difficult to study as these nocturnal forest dwellers often remain in the upper parts of the forest canopy. Moreover, they hibernate for several months during the austral winter. Their main period of activity is the rainy season, when many of the forests they inhabit are virtually inaccessible to scientists. Nevertheless, the researchers were able to carefully capture a total of 51 dwarf lemurs in live traps at nine locations for this study and to take minute tissue samples before releasing the animals back into their natural habitat.
The tissue samples were subjected to molecular-genetic analyses at the Institute of Anthropology at Mainz University. The data generated through the process were then compared with data already published by other research groups. "The new data from southern Madagascar enabled us to significantly enlarge existing datasets," explained Dana Thiele of the JGU Institute of Anthropology. "We then used extensive data analyses to examine the genetic diversity in two closely related lemur genera, the mouse lemurs (Microcebus) and the dwarf lemurs (Cheirogaleus). The comparison showed that the species diversity of dwarf lemurs is greater than previously thought."
Andreas Hapke and Refaly Ernest, working as a local field assistant for the project, had discovered the first individuals of the Lavasoa Dwarf Lemur during a field study in Madagascar in 2001. Few genetic data from other parts of the island were available for comparison at that time. The animals were thus initially assigned to an already known species, Cheirogaleus crossleyi. Only now it was possible to ascertain that the Lavasoa Dwarf Lemur is a distinct species.
Materials provided by Universität Mainz. Note: Content may be edited for style and length.
- Dana Thiele, Emilienne Razafimahatratra, Andreas Hapke. Discrepant partitioning of genetic diversity in mouse lemurs and dwarf lemurs – biological reality or taxonomic bias?Molecular Phylogenetics and Evolution, 2013; DOI: 10.1016/j.ympev.2013.07.019
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Universität Mainz. "New primate species native of Madagascar, Lavasoa Dwarf Lemur, discovered." ScienceDaily. ScienceDaily, 29 July 2013. <www.sciencedaily.com/releases/2013/07/130729111701.htm>.
Universität Mainz. (2013, July 29). New primate species native of Madagascar, Lavasoa Dwarf Lemur, discovered. ScienceDaily. Retrieved March 9, 2018 from www.sciencedaily.com/releases/2013/07/130729111701.htm
Universität Mainz. "New primate species native of Madagascar, Lavasoa Dwarf Lemur, discovered." ScienceDaily. www.sciencedaily.com/releases/2013/07/130729111701.htm (accessed March 9, 2018).