Tuesday, June 19, 2012

The Mysterious Brain of the Fat-Tailed Dwarf Lemur, the World's Only Hibernating Primate

fat-tailed dwarf lemur

A fat-tailed dwarf lemur (Image courtesy of Kathrin Dausmann)

In the 18th century Carl Linnaeus named them lemurs, after the Latin lemures?spirits of the dead, wandering ghosts. He knew the primates roamed Madagascar?s forests at night, their large eyes brimming with moonlight, their shrill cries crashing through the treetops. One of the smallest lemurs on the island, the fat-tailed dwarf lemur, resembled a phantom in another way: it completely vanished for seven months each year.

For a long time, no one understood where the fat-tailed dwarf lemur went?a remote part of the island? the spirit world??or what it was doing all that time, but scientists had a hunch. Perhaps the lemur was hibernating. If so, it would be the only primate in the world?and one of the only tropical mammals?to do so. Given Madagascar?s climate, however, it made sense that a lemur might hibernate to survive annual periods of drought.

In general, Madagascar has two seasons: the hot, wet season from November to April, and the cooler, dry season from April through October. The deciduous forests on the west coast, where many fat-tailed dwarf lemurs live, offer no open sources of water during the dry season and only fibrous fruits bereft of sugar. Perhaps, scientists reasoned, the fat-tailed dwarf lemur hunkered down and waited for the rains to return, slowing its metabolism and dropping its body temperature. It could survive off of nutrients stored in its tail, which always grew plumper as the dry season drew closer.

In 1993 Kathrin Dausmann of the University of Hamburg and her colleagues finally put the hibernation hypothesis to the test. Between 1993 and 2003, the researchers regularly traveled to the forest of Kirindy on the west coast of Madagascar, where they captured 53 fat-tailed dwarf lemurs (Cheirogaleus medius). They tagged all the lemurs with radio transmitters to track their location and implanted six of the primates with small temperature sensors.

Around April, the lemurs disappeared as usual, but they were not really gone?just out of sight. The radio transmitters revealed their hiding spots?nests within tree hollows?and the temperature sensors confirmed that the primates were in fact hibernating during the dry season. The lemurs? approach to hibernation, however, was unusual.

fat-tailed dwarf lemur

A fat-tailed dwarf lemur on the west coast of Madagascar (Credit: Frank Vassen, via Wikimedia Commons)

Many small hibernating mammals?including arctic ground squirrels and European hedgehogs?regularly emerge from deep hibernation every few weeks and enter brief periods of biological activity during which their body temperatures rise, their metabolism speeds up and their brain activity increases. The animals do not necessarily get up and move around, but they might urinate and defecate. When they emerge from hibernation, they also sleep. That may seem paradoxical at first; isn?t hibernation a form of deep sleep? No, it?s not. During hibernation the mammalian brain is too cold and too idle to generate the electrical activity that regulates the kind of sleep we look forward to each night. Some scientists think that the need for sleep entirely explains why mammals periodically wake up from hibernation, while others think it is just one reason. What scientists know for certain is that any mammal deprived of sleep for too long will die.

In Dausmann?s study, lemurs hibernating in well-insulated hollows maintained a constant body temperature of about 25 degrees Celsius (77 degrees Fahrenheit), rousing themselves once every 10 to 14 days, somewhat like ground squirrels and hedgehogs. But the body temperatures of lemurs inside poorly insulated hollows fluctuated by 20 degrees Celsius or more every day with the ambient temperature, which increased from 10 degrees Celsius (50 degrees Fahrenheit) or colder at night to 30 degrees Celsius (86 degrees Fahrenheit) or warmer during the day. No one had ever observed such passive hibernation in a mammal. Dausmann thinks the primates essentially return to a reptilian form of temperature regulation, relinquishing control of their body?s thermostat to the environment and sparing themselves the energetic cost of waking up periodically during hibernation. The sun does most of the work for them.

In recent years, Peter Klopfer of Duke University and his colleagues have been visiting the forest of Kirindy on Madagascar to learn more about fat-tailed dwarf lemurs. Klopfer is particularly interested in studying how the dwarf lemur?s brain copes with hibernation. As a primate brain, the lemur?s brain is larger relative to body size, more complex and more demanding of energy than a squirrel?s brain. Klopfer and his teammates observe lemurs at the Duke Lemur Center and set up nesting boxes on Madagascar. They measure how much oxygen the lemurs use while inside their boxes as a proxy for changes in body temperature, as well as implanting temperature sensors just below the skin. The researchers also slip small, slender electrode needles below the lemurs? scalps to measure electrical activity in their brains.

fat-tailed dwarf lemur

A fat-tailed dwarf lemur with a plump tail (Image courtesy of Kathrin Dausmann)

So far, their data suggests that the hibernating fat-tailed dwarf lemur brain is unique among all hibernators, orchestrating sleep patterns that look nothing like those of ground squirrels or other hibernating mammals.

In people and most other mammals, rapid eye movement (REM) sleep?the phase most strongly associated with dreams?occupies about 25 percent of a night?s sleep. This is true for fat-tailed dwarf lemurs that are not hibernating. Klopfer and his team discovered that when hibernating dwarf lemurs sleep, however, they exclusively enter REM-sleep and they stay in REM sleep for an unusually long time. Arctic ground squirrels, in contrast, rarely or never enter REM sleep during hibernation. It?s almost as though the primate brain builds up a desperate need for REM-sleep during hibernation, Klopfer speculates, and satisfies the need with long REM sessions. As part of a recent study, scientists discovered that hibernating black bears maintain typical cycling between REM and non-REM sleep, but unlike many smaller hibernators their body temperatures do not drop all that much.

To Klopfer, the discrepancy between the sleeping patterns of hibernating ground squirrels and dwarf lemurs suggests that hibernation is not a conserved trait passed down from one evolutionary generation to the next. Rather, hibernation might be a convergent trait that evolved independently several times in different groups of animals. But studies on how fat-tailed dwarf lemurs hibernate are preliminary, Klopfer stresses, and?as with much hibernation research?there are still more questions than definitive answers.

Klopfer also thinks that, as a primate, the fat-tailed dwarf lemur is a better animal model than the arctic ground squirrel, hamster or hedgehog for studies on inducing hibernation in people. Some scientists have framed the possibility of deliberately reducing a person?s body temperature and metabolism in a controlled manner as a medical breakthrough that could permit otherwise impossible surgeries, as well as deep space travel. Although researchers have made some progress in artificially inducing hibernation in rodents, we are nowhere near ready to send human popsicles to Mars.

In about a week, Klopfer is returning to Madagascar to continue studying the fat-tailed dwarf lemur and to begin investigating the brain activity of the tenrec, which looks somewhat like a shrew and is the only other tropical mammal that hibernates. If the tenrec also enters REM sleep during hibernation, then this style of hibernation might be explained by a tropical environment, rather than a behavior unique to hibernating primates. Perhaps, Dausmann proposes, only the brains of tropical hibernators have the opportunity to get warm enough for REM sleep in an energetically efficient manner. An arctic ground squirrel hibernating in a burrow deep underground is not exposed to much fluctuation in ambient temperature, so it has to actively warm its brain in order to sleep, which requires a lot of energy?perhaps too much energy to fully enter REM sleep. A tropical hibernator, in contrast, could rely in part on high ambient temperatures to warm its brain enough for REM sleep.

Regardless of the exact details, the fact remains: fat-tailed dwarf lemurs are remarkable.? These tiny lemurs show that is is possible for a primate and its brain to survive off of nothing but a tail?s worth of fat for seven months?enduring large fluctuations in body temperature every day during that period?and to emerge from the whole experience, a little groggy perhaps, but as healthy as ever. Scientists now know where dwarf lemurs go when they disappear and what they are doing. Now they just have to figure out how they do it.

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