The Lemurs of Kirindy

by Peter M. Kappeler, Alexandra Dill

Near the west-central coast of Madagascar, and a mere hour's drive from the town of Morondava, is the 25,000-acre Kirindy Forest. Dominated by majestic baobab trees, it is home to the world's smallest known primate as well as to dozens of amphibian and reptile species and more than sixty species of birds. Every rainy season, Kirindy transforms itself from a tangle of dry branches on which not a single green leaf can be found to an impenetrable emerald wall. Its changeable beauty and the diversity of its inhabitants are enough to captivate any visitor. But the forest's pull on us lies not so much in its considerable visual charm as in the actions of its eight resident species of lemurs.

Some of Kirindy's lemurs are strictly nocturnal, others are active only in the daytime, and some are up and about day and night. Different species also exhibit different patterns of activity over the course of a year. In some, both sexes hibernate, while in others, only the female takes time out. For almost a decade, we and other members of the German Primate Center have been working to find out more about this unusual web of daily and yearly activity cycles.

Kirindy is indeed a place of pronounced seasonal changes. A short, hot rainy season between December and February is followed by nine months with virtually no rain. At the height of the dry season, nightly temperatures regularly drop below 50 [degrees] F and sometimes stay just above freezing; during the day, temperatures may rise above 86 [degrees] E During the rainy season, temperatures fluctuate between 68 [degrees] and 104 [degrees] in the course of twenty-four hours. Most of the forest's trees respond to the extended dry season by dropping all their leaves to conserve water. Some, such as the three species of baobabs, also store water in their huge trunks. Kirindy's trees tend to grow extremely slowly and (unlike many tropical trees) have pronounced seasonal cycles of flowering, leafing, and fruiting.

The response of most amphibians and reptiles to the area's dramatic seasonality is to do much of their hard living--finding a mate, producing eggs, growing, and preparing for the next dry season--during the rainy weeks and to be much less active the rest of the year. For example, five-foot-long Leioheterodon snakes pass the dry months several feet below ground, curled up in a nest of ants, and emerge only after the rains begin. Similarly, many of Kirindy's birds spend the harsh months in other parts of Madagascar or in Africa or Europe. None of these patterns are surprising. Many birds migrate, and many of the world's frogs, lizards, and snakes lie low during cooler periods of the year. Some of the lemurs and other mammals of Kirindy, however, are quite another story, a striking exception to the rule that tropical mammals generally do not exhibit strong seasonal variations in activity. Most puzzling among them are several species that hibernate even when the weather is warm.

Verreaux's sifakas (Propithecus verreauxi verreauxi) are the most prominent inhabitants of Kirindy. These long-legged, seven-pound lemurs, white with dark patches, leap among tree trunks high in the canopy, propelled by their powerful hind legs but continually maintaining an upright posture. Like the vast majority of primates elsewhere in the world, they live in small, cohesive groups of two to eight members and are active exclusively during the day. Sifakas have teeth and guts that are specialized for feeding on leaves, but they adapt their menu opportunistically as different flowers and fruits come into season. These lemurs cope with the long dry season primarily by expending less energy, sometimes halving the distance they travel each day and the time they devote to foraging and other activities. Sifakas' body temperature falls a few degrees at night, another calorie-saving adaptation; when morning comes, they take extended sunbaths high in the trees to bring their temperature back up to normal. Remarkably, the females give birth at this time of year; nursing sifaka mothers produce very dilute milk and thus lose significant amounts of water during lactation. Nevertheless, these animals never descend to the ground to drink, seemingly able to balance their water budget by choosing plants high in liquid content and by occasionally licking dew from leaves and tree trunks in the early morning hours.

Early morning is a time when members of the other group-living lemur species in Kirindy may take a breather from their efforts for a few hours. Red-fronted lemurs (Eulemur fulvus rufus), like other members of the genus Eulemur and the closely related bamboo, or gentle, lemurs (genus Hapalemur), have an unusual circadian rhythm, consisting of several bursts of activity irregularly distributed over the twenty-four-hour cycle. This type of activity pattern, which is termed cathemeral, has been reported outside Madagascar in only one other primate: Azara's night monkey (Aotus azari) in South America. (More generally, among the tropical arboreal mammals of Africa, Asia, and South America, only sloths have such an on-again, off-again lifestyle.) Perhaps the cathemeral cycle of these lemurs represents an evolutionary midpoint in the transition from a nocturnal to a diurnal pattern; night vision requires increased sensitivity to light and generally comes at the expense of color vision and acuity. The transition to cathemeral activity may have been triggered by ecological changes associated with the extinction of large raptors and giant, probably diurnal, lemurs after the onset of human settlement in Madagascar about 2,000 years ago and the resultant hunting and deforestation.

Kirindy's six other lemur species have strictly nocturnal habits but adapt to the changing seasons in a variety of ways. Coquerel's dwarf lemur (Mirza coquereli) and the fork-marked dwarf lemur (Phaner furcifer) are active year-round. The leaf-eating red-tailed sportive lemur (Lepilemur ruficaudatus)--like the sifaka--saves energy during the dry season by reducing its already low activity level and metabolic rate (and presumably its body temperature as well, although we have yet to measure this precisely).

Fat-tailed dwarf lemurs (Cheirogaleus medius) take energy savings to an extreme. These five-ounce animals squeeze an entire reproductive cycle into the rainy season and, during this time of plenty, accumulate enough fat reserves to fuel up to eight months of hibernation. Feeding on high-energy fruits and insects, the lemurs convert most of their food into fat, which is primarily stored in the tail, nearly doubling their body mass. At the beginning of the dry season, small groups of males and females retire into hollow trees, their body temperature and metabolic rate drop, and the animals begin hibernation.

The gray mouse lemur (Microcebus murinus) can also hibernate for months, but in this species, only adult females do it. Like their fat-tailed cousins, female gray mouse lemurs go through their complete reproductive cycle between late December and early February, acquiring impressive amounts of fat and increasing body mass by more than 40 percent. As the nights begin to get cool, these two-ounce lemurs resort to another remarkable strategy to reduce energy expenditure: night-time torpor. When the temperature falls below a certain point, they enter a tree hole and reduce metabolism, thus lowering body temperature close to the level of the air around them. (Some of our colleagues have recorded body temperatures as low as 48 [degrees] F in torpid animals.) Huddling together in well-insulated holes further enhances their energy savings. When the ambient temperature rises during the morning, body temperature follows passively up to about 82 [degrees] F, at which point the metabolism kicks in again and heats the lemurs up to a normal level of about 100 [degrees] F.

As the dry season progresses, adult females stop leaving the tree hole altogether, remaining inactive for the next four months or more. Males, however, continue venturing out to forage (mainly on gum and the few remaining insects) for at least a few hours almost every night. Why they forgo the substantial energy savings enjoyed by females and expose themselves to owls and other predators every night is something of a mystery to us. However, the mating season begins soon after the females emerge, and we think the males may be taking advantage of these months to establish dominance hierarchies.