Lemur

• 1. Introduction

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  Madame Berthe's mouse lemur weighs about 30 grams, which makes it the smallest primate in the world. Lemurs also once included Archaeoindris, an extinct giant that rivaled a gorilla in size. Both belong to one group of wet-nosed primates found naturally only on the island of Madagascar. Today that group numbers around 100 species in 15 genera. Most are small, with pointed snouts, large eyes, and long tails.

  Lemurs are popularly confused with the ancestors of monkeys and apes. They are not. They evolved on their own, cut off from the rest of the primate world, and the diversity they produced on one island rivals that of any other primate group.

  Several puzzles run through their story. How did small mammals cross open ocean to reach Madagascar? Why does a name borrowed from Roman ghosts belong to them? How does a primate survive months of hibernation, or a diet that would poison most mammals? Why do females so often hold the upper hand? How many species are there, really? And what is happening to them today?

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• 2. A Ghostly Name

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  In 1758, Carl Linnaeus, the founder of modern binomial nomenclature, declared the genus Lemur in the 10th edition of his Systema Naturae. He placed three species in it. One was the red slender loris. One was the ring-tailed lemur, Lemur catta. The third was the Philippine colugo, Lemur volans. Only the ring-tailed lemur remains in the genus today. The word was first meant for slender lorises, but it soon narrowed to the primates of Madagascar and has stayed with them ever since.

  Linnaeus knew the works of Virgil and Ovid, and both of them mention lemures. These were the specters or ghosts driven out during the Lemuria festival of ancient Rome. He saw an analogy that suited his naming scheme and adapted the word for these nocturnal primates.

  For generations, writers assumed he was thinking of the ghostly look of Madagascar's lemurs, their reflective eyes, and their eerie cries. Some also guessed that he knew of a belief among some Malagasy people that lemurs were the souls of their ancestors. A note published in 2012 discredited both ideas. Linnaeus explained his own reasoning: "I call them lemurs, because they go around mainly by night, in a certain way similar to humans, and roam with a slow pace."

  The animal he had in mind was the red slender loris, which is not a Malagasy primate at all. The true home of the name's eventual owners was an island that had been waiting a very long time for its first mammal passengers.

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• 3. Rafting to Madagascar

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  In 1915, the paleontologist William Diller Matthew pointed out that Madagascar's mammals, lemurs included, could only be explained by chance. Small populations from Africa would have drifted out to sea on tangled mats of vegetation flushed from major rivers. In the 1940s, the American paleontologist George Gaylord Simpson named such random events the sweepstakes hypothesis. Rafting has been the favored explanation ever since.

  The odds looked poor. Ancestral lemurs are thought to have originated in Africa around 62 to 65 million years ago. The Mozambique Channel they had to cross is at least 560 km wide, or about 350 miles. Madagascar has been isolated since it broke away from eastern Africa roughly 160 million years ago. Worse, strong ocean currents today flow away from the island, so the trip long seemed very unlikely.

  A report in January 2010 reversed that view. Around 60 million years ago, both Madagascar and Africa lay 1,650 km south of their present positions, inside a different ocean gyre. The currents then ran against today's pattern, and they were even stronger. A raft could make the crossing in 30 days or less, short enough for a small mammal to survive easily. As the plates drifted north, the currents gradually changed, and by 20 million years ago the window for crossing had closed.

  What the arrivals found was a quiet island with few mammalian competitors. They did not have to contend with squirrels or other tree-dwelling mammal groups. Monkeys, whose intelligence, aggression, and deceptiveness gave them an edge over other primates, evolved later.

  Where lemurs sit in the primate family tree is still argued. All modern strepsirrhines, the group that includes lemurs, lorises, pottos, and galagos, were traditionally traced to early primates called adapiforms. These lived in the Eocene or Paleocene. Adapiforms lacked a specialized arrangement of teeth that nearly all living strepsirrhines possess. A newer hypothesis says lemurs descended from loris-like primates, with adapiforms as the common ancestor of both. Molecular studies place the split between lemurs and lorises at 62 to 65 million years ago, while African fossils suggest 50 to 55 million. The oldest lemur fossils on Madagascar itself are subfossils from the Late Pleistocene.

  That specialized arrangement of teeth is called a toothcomb, and it turns out to be one of the lemur's most versatile tools.

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• 4. Surviving Seasonal Extremes

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  Madagascar swings from extended drought to floods driven by cyclones, and its eastern rainforests and dry western regions are radically different worlds. Lemurs survive by enduring the extremes rather than the yearly averages. One tool is a low basal metabolic rate, as much as 20% below the values predicted for mammals of similar body mass. The red-tailed sportive lemur reportedly has one of the lowest rates among all mammals. Many species add behavior to the equation, including sunning, hunched sitting, group huddling, and nest sharing.

  Dwarf lemurs and mouse lemurs go further. Before the dry season they store fat in tissue at the base of the tail and the hind legs, doubling their weight. By the season's end, their body mass may fall to half. Mouse lemurs have been seen in torpor lasting several days. Dwarf lemurs hibernate for six to eight months each year, particularly on the west coast. They are the only primates known to hibernate for extended periods.

  Their hibernation is unusual. Dwarf lemurs spend five months in continuous deep hibernation, from May through September, with April and October as transition months of limited foraging. Hibernating mammals from temperate regions must wake every few days. Dwarf lemurs do not, and their body temperature rises and falls with the surrounding air instead of staying low and stable.

  Birth timing follows the same logic. Lemurs schedule mating and births so that weaning coincides with the greatest food supply. In their native Southern Hemisphere habitat, mouse lemurs give birth in September and October. In captive settings in the Northern Hemisphere, they give birth from May through June.

  Diet is flexible, and some of it is startling. The golden bamboo lemur eats giant bamboo that contains high levels of cyanide. It can take in twelve times the dose that would normally kill most mammals, every day. How it avoids poisoning is unknown. At the Duke Lemur Center in the United States, lemurs roaming outdoor enclosures have eaten poison ivy with no ill effects. Research also overturned an assumption about the tiniest species. Mouse lemurs eat more fruit than insects, contradicting the idea that small primates must live on protein-rich prey. Overall, lemurs use members of at least 109 plant families, or 55% of the plant families known in Madagascar.

  Different diets also let neighbors coexist. In the dry western forests, up to five nocturnal species share a patch during the wet season. When the dry season bites, fork-marked lemurs turn to tree gum, sportive lemurs to leaves, and giant mouse lemurs sometimes to insect secretions. The gray mouse lemur uses torpor, and the fat-tailed dwarf lemur hibernates completely. On the east coast, three bamboo lemur species share small stretches of forest by using different bamboo species, different parts of the plant, or different layers of the forest.

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• 5. Scent, Sight, and Teeth

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  The lemur's wet nose, called the rhinarium, is popularly said to sharpen its sense of smell. In fact it is a touch organ. A lemur presses it against a scent-marked object, and pheromone molecules travel down the midline cleft of the nose to a detector called the vomeronasal organ.

  Scent marking works well at night. Lemurs mark with urine and with glands on the wrists, the inside of the elbow, the genital region, or the neck. Male ring-tailed lemurs have glands on their forearms beside a thornlike spur, which they use to gouge and scent-mark branches at the same time. They also wipe their tails between their forearms and wave them at rivals in what researchers call stink fights. The indri is the exception, since it lacks most lemur scent glands and has a greatly reduced olfactory region in the brain.

  Sight matters less. Lemurs have no fovea, the retinal patch that gives sharp vision, because they have only a bony bar behind the eye rather than a wall of bone. Their visual acuity is low whether they are active by night, by day, or both. Their eyes sit at a slightly different angle from those of anthropoid primates, which gives them a combined visual field of 250 to 280 degrees against 180 to 190. Nocturnal mouse lemurs and dwarf lemurs have retinas made entirely of rod cells. The ring-tailed lemur sees blue and yellow but cannot tell red from green. The reflective layer behind their retinas is made of crystalline riboflavin, which is unique among mammals and scatters light.

  Most lemurs carry a toothcomb of six teeth, four incisors and two canines, on the lower jaw. A structure called the sublingua, or under-tongue, keeps it clean. It works like a toothbrush, with serrated keratinized points that rake between the front teeth. Indri use the comb to pry large seeds out of the tough covering of Beilschmiedia fruits. Fork-marked lemurs use theirs to cut through bark and make tree sap flow.

  The aye-aye breaks every pattern. It lacks a functional toothcomb, although the milk incisors it loses shortly after birth show that its ancestors had one. Its replacement incisors grow continuously, like a rodent's, for gnawing through wood and hard seeds. It has a thin, filament-shaped middle finger for extracting food from tiny holes, and large bat-like ears for detecting hollow spaces inside trees. It even forages using sounds it generates itself. This odd mix of features is a large part of why its place in the primate family tree took so long to settle.

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• 6. Female Rule, Forest Song

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  Among ring-tailed lemurs, males act submissively whether or not females show aggression. Male crowned lemurs are subtler. They submit only when females act aggressively toward them. Female social dominance sets lemurs apart from most primates and mammals, where males normally dominate unless females form coalitions. The greater bamboo lemur is one species that does not share the trait.

  Why lemurs behave this way remains open after decades of research. The dominant view says dominance helps females cope with the high costs of reproduction and scarce resources. Yet other primates facing similar or harsher conditions stay male-dominated. In 2008, a hypothesis built on simple game theory argued that when two animals are equally matched, the one with more to lose wins the fight. Females need more for pregnancy, lactation, and maternal care. That idea assumed the sexes are similar in size, so a hypothesis the following year tried to explain why. Most female lemurs are receptive for only a day or two each year, so males can guard mates passively with copulatory plugs that block the female reproductive tract. That reduces the need for aggression and for large male bodies.

  Lemur groups usually contain fewer than 15 individuals. Nocturnal lemurs are mostly described as solitary but social, foraging alone at night yet often nesting together by day. True lemurs often live in multi-male groups of ten or fewer. Ruffed lemurs form fission-fusion societies, and the indri forms pair bonds.

  Voices fill the gaps between groups. Ruffed lemurs have loud calls that carry up to 1 km on a clear, calm day. The indri is louder still, with calls that reach 2 km or more across a home range of 34 to 40 hectares. Its song lasts from 45 seconds to more than 3 minutes and settles into a duet comparable to that of gibbons. Yet the indri is often heard and rarely seen, because dappled light hides it, which has earned it a reputation as a ghost of the forest.

  Sifakas settle territory disputes with ritual. They stare, growl, scent-mark, and leap to claim sections of a tree. Indriids can leap up to 10 m from trunk to trunk. When trees stand too far apart, sifakas descend and cross more than 100 m on the ground, standing upright and hopping sideways with their arms waving. This is sometimes called a dance-hop. Verreaux's sifaka leaps through the spiny forests of southern Madagascar, and no one knows how it avoids impaling its palms on the thorn-covered trunks of Alluaudia plants.

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• 7. Counting Species

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  Until Richard Owen published a definitive anatomical study in 1866, early naturalists could not say whether the aye-aye was a primate, a rodent, or a marsupial. Even afterward its place in the primate order stayed contested. Molecular tests now show that its family, Daubentoniidae, is basal to all the other lemurs. In 2008, Russell Mittermeier, Colin Groves, and others defined lemurs as one lineage of five living families, the aye-aye's included.

  The tally of species has moved even faster. After revisions led by Mittermeier, Groves, and others, the number of recognized lemur species and subspecies rose from 33 in 1994 to approximately 100 in 2008. Genetic tests drove many of the changes. The gray mouse lemur, the golden-brown mouse lemur, and Goodman's mouse lemur were treated as one species until recently. Genetic work then showed them to be cryptic species, which humans cannot tell apart by sight. Sportive lemur populations have been given full species status on similar evidence.

  Critics call this taxonomic inflation and prefer a total closer to 50 species. Classification ultimately depends on which species concept is used. Conservationists often favor splitting genetically distinct populations into separate species, because that earns added environmental protection. Others call for a more thorough analysis first.

  Other lines have been redrawn too. The broadly defined genus Lemur was gradually split into separate genera for the ring-tailed lemur, the ruffed lemurs, and the brown lemurs. Sportive lemurs and the extinct koala lemurs were once placed in one family because of similar teeth, but genetic studies ended that pairing. Some Paleogene fossil primates from outside Madagascar, such as Bugtilemur, have been called lemurs. Scientific consensus rejects those assignments on genetic evidence. With ongoing research on cryptic groups such as mouse lemurs, the count is likely to keep growing.

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• 8. Vanishing Forests

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  Roughly 1500 to 2000 years ago, humans arrived on Madagascar, and lemurs began losing their island. Before then they lived across all of it. Early settlers converted forest into rice paddies and grassland by slash-and-burn farming, known locally as tavy. That confined lemurs to approximately 10% of the island, around 60,000 square km, or 23,000 square miles.

  At least 17 species in eight genera, known collectively as the subfossil lemurs, have since gone extinct. Every one was larger than any living lemur, and they are thought to have been active by day. They filled ecological niches that no longer exist or now sit empty. Large areas that are bare of forests and lemurs today once held communities of more than 20 lemur species, spanning the full range of sizes.

  The losses are not over. Most of the approximately 100 species and subspecies are threatened or endangered, and habitat loss and hunting continue. Local traditions such as fady generally help protect lemurs and their forests. Yet illegal logging, economic privation, and political instability undermine conservation. The International Union for Conservation of Nature considers lemurs the most endangered mammals in the world. It warns that up to 90% of lemur species could face extinction in the wild within 20 to 25 years.

  The ring-tailed lemur has become an iconic flagship species, and lemurs as a whole have helped eco-tourism emerge on Madagascar. Conservation organizations increasingly turn to community-based approaches that protect lemurs while promoting sustainability.

  Scientific attention came late. Lemur research in the 18th and 19th centuries focused on taxonomy and specimen collection. Studies of ecology and behavior began in earnest in the 1950s and 1960s. They were hindered by political problems on Madagascar in the mid-1970s and resumed in the 1980s. Researchers value lemurs because they combine ancestral primate traits with traits shared with anthropoid primates, which can shed light on primate and human evolution. Most species have been discovered or promoted to full species status only since the 1990s, so the portrait of this group is still being drawn even as its forests shrink.

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