Ian Tattersall is a paleontologist and primatologist who has worked extensively on the living and subfossil le-murs of Madagascar as well as on a range of problems in early primate and human evolution. Curator and chairman in the department of anthropology of the Amer-ican Museum of Natural History, Tattersall is especially interested in the integration of evolutionary theory with the fossil record. He has also served as curator for several major exhibitions at the museum, the most recent of these being the Hall of Human Biology and Evolution, scheduled to open in early 1993.

Reprinted with permission from Scientific American, January 1993

From dense rain forests to broad coastal plains, from deciduous thickets to desert, Madagascar offers an extraordinary range of environments. These habitats harbor an equally extraordinary primate fauna that shows more clearly than any other what our own primate ancestors were like early in the Age of Mammals, approximately 50 million years ago.

These animals are the lemurs, Madagascar's dominant mammals. Why they are there is not entirely clear. The story used to be that the 1,000-mile-long Madagascan minicontinent had simply preserved (in somewhat impoverished fashion) an archaic fauna that was marooned on it when Madagascar separated from the African mainland and drifted out to sea. In many ways the island's living "lower" primates more closely resemble the primates of the Eocene epoch (about 57 to 35 million years ago) than they do the "higher" primates dominating the tropical continents today. That fact was taken to imply that the separation had occurred in the Eocene or thereabouts.

But we now know that Madagascar began its journey away from Africa as much as 165 million years ago, when the dinosaurs ruled and the only mammals were tiny and vaguely shrewlike. Moreover, the island appears to have reached its present separation of roughly 250 miles from Africa some tens of millions of years before the great diversification of the mammals and thus well before today's familiar groups such as the primates, bats and rodents came into existence.

For land-bound latecomers such as primates, then, the only possible means of access to Madagascar was by "rafting": floating across the Mozambique Channel from Africa on matted tangles of vegetation. Arriving thus, the ancestral lemurs would have found an incredible wealth of ecological opportunities on an island that is only slightly smaller than Texas and topographically, climatically and ecologically much more diverse.

The island of Madagascar looks rather like a giant left footprint in the sea, its long axis oriented more or less north-south. It extends from within 12 degrees of the equator all the way to the southern subtropical zone. Its eastern side presents a steep escarpment to the prevailing easterly winds; here heavy rainfall year-round supports a dense growth of rain forest. To the west, a rugged central plateau slopes more gently to broad coastal plains that become drier toward the south. Moist forests in the northwest give way to deciduous forests and thickets. These in turn yield in the far south to an extraordinary desert-adapted flora in which as many as 98 percent of the species are unique. Add to these major regions a host of local microclimates and secondary physiographic features, and you have an unparalleled assortment of environments for forest-living mammals to exploit.

No one knows what the range of habitats was in Madagascar at the remote time when primates first arrived or what lived in those habitats; the fossil record is simply lacking. What is certain, though, is that the primates flourished and that by the time human beings arrived under 2,000 years ago the island was home to at least 45 lemur species. These primates ranged in body size from the two-ounce mouse lemur, Microcebus, to the 400-pound Archaeoindris, a match for a large gorilla.

Each of the lemur species was a lower primate, belonging (with the bush babies, pottos and lorises) to the primate suborder Strepsirhini. We, on the other hand, are higher primates, belonging (with the monkeys and apes) to the suborder Anthropoidea. (There is no consensus about which group the tiny and enigmatic tarsier of Southeast Asia belongs to.) The distinction between lower and higher primates is in fact a rather archaic concept that is now going out of fashion, but it is a convenient one to use here.

The higher primates appeared on the evolutionary scene much later than did the lower primates, from one of which they presumably evolved toward the end of the Eocene. Madagascar's lemurs and their continental cousins have much in common with Eocene forms, retaining a suite of physical characteristics that have been lost among higher primates. But only in Madagascar do we still find lower primates that are diurnal, or active during the day. Virtually all modern higher primates are diurnal, and if anything in paleontology is certain, it is that all anthropoids are descended from a diurnal common ancestor. So if we wish to find analogies to our remote Eocene ancestors, we must turn to the primates of Madagascar.

Modern lower and higher primates are distinguished from one another by a number of structural features, most significantly in their nervous systems and sense organs. The lower primates have much smaller brains relative to body size than do higher primates. They also differ in the development of the association areas, which govern the transfer of information between the various brain centers.

The balance between the senses of vision and smell also differs. Although the eyes of lower primates are quite forward-facing, the left and right visual fields do not overlap as much as they do in higher primates. This arrangement limits depth perception to the central part of the field of view. And whereas it is natural that the nocturnal lower primates lack color-sensitive cone cells in their retinas, what little is known about visual discrimination in the diurnal lemurs suggests that their color vision is at best limited.

As for the sense of smell, the lower primates have roomier nasal cavities than do higher primates, with more complex internal structures. Living lower primates retain the primitive mammalian rhinarium, or "wet nose." It is part of a system for the transfer of particles to the nasal cavity, where they are analyzed by an organ that is, at most, vestigial in most higher primates.

Many lower primates (but only a few South American monkeys among the higher primates) have scent glands that exude substances used to "mark" the environment. This process is important in communication between individuals. Visual cues are less important; the faces of lower primates lack the musculature needed to produce the complex expressions through which higher primates convey their states of mind.

Living primates in general have lost the primitive claws that enabled the first pre-Eocene primates to scale trees without the ability to grasp. In their stead is a thumb, shifted away from the other digits, that is at least to some extent opposable to them, and sensitive tactile pads on the fingertips, which are backed by flat nails. This fundamental change has consequences that extend far beyond locomotion as well as into manipulative abilities. But whereas higher primates generally manipulate objects using the thumb in opposition to the other digits, lemurs tend to pick things up with the whole hand. An item held in this way is then more likely to be sniffed rather than inspected visually and turned in the fingers for further examination.

Both the lower and the higher primates are, of course, extremely diverse groups, whose members represent myriad variations on the themes outlined above. Nevertheless, the lower primates are obviously more primitive than the higher primates (with respect to the body systems discussed) in the sense that they more closely resemble the ancestor from which both modern groups emerged. Although fossils are limited to bones and teeth, they reveal clearly that in the Eocene primate brains were even smaller in relation to body size than are those typical of modern lemurs and that the visual sense had not achieved the total domination over olfaction we see in today's higher primates. Eocene primate hands and feet were certainly capable of grasping but could probably manipulate objects no more precisely than lemurs do at present. In other words, as functioning organisms, Eocene primates were probably not too different from today's lemurs. They were certainly close enough so that by studying the lives of lemurs we can glimpse something of the Eocene behavioral potential from which our vaunted human capacities ultimately arose.

Not until the 1960s did information about the behavior of lemurs begin to be available from field studies in Madagascar. The results of those studies have been increasingly at odds with earlier anticipations. For example, as long as it was possible to think of "the lemur" as a general ancestral model, the expectation, if any, was simple: lemurs would show a set of relatively stereotypical behavior patterns, similar to those exhibited by early primates and from which the higher primates had managed to emancipate themselves. Yet perhaps the most remarkable revelation of the field studies is how diverse the lemurs are in their ways of life.

Of course, certain predictions from anatomy were indeed borne out. Olfactory marking, using urine and feces as well as the secretions of specialized glands, has been shown to be a significant component of lemur behavior. To judge by its wide occurrence among mammals, such marking is an ancient behavior, and few would question its importance in communication among Eocene primates.

Lemurs also turn out, as expected, to have a tendency to explore their environments with their noses-to choose ripe fruit, for example, by smell rather than by appearance. Undoubtedly, then, olfaction is of the greatest importance to members of all five living families of lemurs, as it was to their Eocene precursors, and much more so than it is to most higher primates. But does the reverse apply to vision? Anyone who has watched a sifaka lemur hurtle through the forest would conclude that the animal is hardly handicapped by its lack of a higher primate's visual system.

Lemurs, in fact, turn out to be as diverse as or even more so than the higher primates in most aspects of their behavior and ecology. Their diets, for instance, consist of much the same items as those consumed by the higher primates: fruit, flowers, leaves, buds and insects. But feeding on nectar, which is unusual in higher primates, is being increasingly noted. As a whole, lemurs tend to be dietary generalists, but some at least are highly specialized-for example, the bamboo lemurs. Many of them concentrate not just on bamboo but on particular parts of bamboo plants. Indeed, individuals of the species Hapalemur aureus, weighing only a couple of pounds each, daily eat shoots containing enough cyanide to kill half a dozen humans.

Similarly, lemurs occupy nearly all of the vegetational habitats exploited by higher primates, from rain forest to arid brush. Again, whereas almost all higher primates are diurnal, some lemurs are nocturnal, others diurnal and yet others "cathemeral," spreading their activity fairly evenly between daylight and darkness.

The range of types of social organization among lemurs is enormous. Some lead more or less solitary lives, in which small female ranges are overlapped by larger male ones. In certain species, adult pairs rear immature off-spring, whereas in others, small groups consist of just a few adults of each sex. And still other species live in fluid groups or in more stable larger units that contain a couple of dozen individuals or more.

Within these broad categories, there are still further variations. What is perhaps most surprising is that even within the same species, substantial variation in social organization may be found from place to place. What seems to be most significant is that even though lemur brains tend to be smaller than those of higher primates, at least some lemurs display the complex sociality we usually associate with the higher primates.

The picture that is therefore beginning to emerge of the behavioral variety of the lemurs has important implications for the understanding of our own Eocene ancestors. Despite the retention of such primitive behavioral traits as olfactory marking, the wide variety suggests that from the beginning, well before the increase in brain size that we associate with the higher primates today, primates showed a behavioral flexibility and adaptability that belie the inference most people would draw from the description of these early forms as "primitive." It seems to me that this is the essential evolutionary heritage of our order, something far more important than any of the anatomic characteristics to which we are wont to draw attention. As higher primates ourselves, we tend to look at the lemurs and ask why they did not evolve further in our direction. But in doing this, we are missing the critical point that, as a whole, the lemurs have actually inherited from their Eocene ancestors, as we have from ours, the most significant primate characteristic of all.

Looking at this picture from another perspective, it is certainly clear that the lemurs had no need of higher primate physical characteristics to make full use of the varied ecological opportunities that Madagascar offered them. Perhaps this point is emphasized most dramatically by considering the full range of lemur species that existed on Madagascar when humans first arrived there. The present range is impressive enough: at the small end is the tiny two-ounce mouse lemur and at the large end, the 15-pound babakoto. But in its pristine state, the island was home to a spectrum of primate types that equals, if it does not surpass, the entire variety achieved by anthropoids in the rest of the world.

Late in the 19th century, excavations at sites in the central plateau of Madagascar began bringing to light the subfossil, or partially fossilized, remains of large-bodied extinct lemurs that were clearly not of great age. We know of at least 15 species of subfossil lemurs, belonging to eight or possibly more different genera. All of them are larger than any surviving lemurs. The same pattern of large body size is found among the nonprimate members of the subfossil fauna, including the "elephant bird," Aepyornis maximus (the largest bird that ever lived, possibly weighing almost half a ton), the pygmy hippopotamus and a giant tortoise.

A long series of studies has revealed an astonishing array of locomotor and positional behaviors among the subfossil lemurs. Even by themselves, the living lemurs show a great variety of such behaviors, ranging from the rapid, scurrying quadrupedal motion of the tiny Microcebus to the spectacular leaping of the long-legged indrid lemurs (sifakas, babakotos and the like). It cannot really be said that any of the living lemurs is excluded from any part of the forest environment by its anatomic locomotor specializations, but it is generally true that most species avoid spending much time on the ground. The only notable exception is the ringtailed lemur, Lemur catta.

Among the extinct lemurs, on the other hand, was a group that was clearly adapted for life on the ground. This is the family Archaeolemuridae, containing the two medium-sized genera Archaeolemur and Hadropithecus. Laurie R. Godfrey of the University of Massachusetts at Amherst (the source for all the estimates of subfossil body weight presented here) has estimated that the various archaeolemurid species weighed between 35 and 55 pounds.

These lemurs were rather powerfully built, short-legged relatives of the indrids, with highly specialized teeth. Clifford J. Jolly of New York University has compared them, respectively, with two African higher primates, the common and gelada baboons. The common baboon is an extremely adaptable form, at home in woodlands and deciduous forests as well as in the savanna habitats in which it is so familiar. The gelada baboon is specifically adapted to the treeless Ethiopian highlands, and virtually all its food is derived from terrestrial sources. Both the dentition and what is known of the body skeleton of Hadropithecus suggest strongly that this lemur had similar dietary and habitat preferences.

Another extinct indrid relative showed a totally different set of adaptations. For analogues, one must look well beyond the primates. Palaeopropithecus comprised at least two species with a weight range of perhaps 90 to 130 pounds. Ross MacPhee, my colleague at the American Museum of Natural History, has analyzed a substantially complete skeleton recovered in northern Madagascar a few years ago and concluded it was a generally slow-moving and somewhat slothlike arboreal hanger, built for flexibility rather than strength. Its even larger relative Archaeoindris (probably more than 400 pounds) is poorly known, but Martine Vuillaume-Randriamanantena of the University of Madagascar believes it was probably a terrestrial quadruped somewhat like the extinct ground sloths of the New World. Both of these forms had specializations of the skull, particularly of the nose area, that are unmatched among living primates.

We also have to look outside our own order to find an analogue to the best-known subfossil lemur, Megaladapis. The three species, ranging in weight from about 90 to 170 pounds, have been described by Alan C. Walker of the Johns Hopkins School of Medicine as closest in locomotion to the marsupial koala of Australia. Like the koala, these lemurs would have climbed slowly, presumably preferring vertical supports, and they had limited leaping capabilities. A number of specializations of the skull may have compensated for such locomotor limitations. They would have allowed the animal to feed in a large radius from a single sitting position.

The best known of the sites that have yielded extinct lemurs is Ampasambazimba in Madagascar's central highlands. The 14 primate species (including both extinct and surviving lemurs) whose bones have been recovered there compare favorably in abundance with the species at any other place in the world where primates are found. Yet Ampasambazimba is in the middle of what is now an essentially treeless plateau. How does it boast this rich and heterogeneous forest-living fauna?

Studies dating from early in this century seemed to have the answer. Before the advent of humans, the argument goes, Madagascar was essentially fully forested. The fact that forest had survived only in patches was attributed to the propensity of the early settlers to burn off vast areas of forest to provide grazing for cattle and land for agriculture. Indeed, the process is still only too evident.

Following this argument, loss of habitat must have been at least a major influence in the disappearance of Madagascar's large birds and mammals. There was also a selective aspect of this extinction: the lemurs known to have become extinct were large bodied and thus of the greatest interest and vulnerability to hunters. Presumably, they also reproduced more slowly than the smaller forms that have survived. The case for a combination of direct and indirect human activity as the agent of extinction seems compelling.

Climatic change has also been promoted as an agent of extinction, initially because many subfossil sites consist of dried-up lakes or marshes. As a total explanation of the extinctions, drying was never completely convincing. Still, interest in a possible climatic effect has been revived recently by the demonstration that some of the grasslands of Madagascar's center are of long (and certainly prehuman) standing.

Analyses of lake cores by David A. Burney of Fordham University have underscored the fact that, like every other region of the earth, Madagascar has undergone climatic fluctuations over the past few thousand years. At the end of the last ice age some 10,000 years ago, Madagascar's forests were apparently just beginning to recover from a period of contraction. It is therefore hardly surprising that the central highlands were not fully forested by the time Madagascar's first people arrived.

Climatic stress and the consequent reduction and redistribution of forests thus constitute one potential factor in the disappearance of the subfossil fauna of Madagascar. But it is clear that in that land as elsewhere, periodic disturbances of this kind have occurred throughout time. The ancestral lineages of the extinct lemurs obviously survived these earlier vicissitudes, and there is no reason to believe that on their own the most recent (rather mild) round of climate changes should have had a fatal effect on several lineages simultaneously. This is especially true when we consider that most subfossil lemurs were probably ecological generalists. Megaladapis, Palaeopropithecus and Archaeolemur, among others, lived in environments ranging from humid to arid and were clearly highly adaptable in terms of choice of habitat. Hence, something other than simply another cycle of disturbance of natural habitat must be invoked to explain the disappearance of the giant lemurs. Only one truly novel factor presents itself: Homo sapiens.

To talk of the "extinction event" of the large-bodied lemurs implies a process that has ended. That is not so. The extinct and living lemurs form part of a single process that is continuing. The smaller, fleeter lemurs have survived so far, but they are themselves under increasing pressure from an expanding human population. The toll of hunting increases as human numbers and the use of more sophisticated weapons do. Another important consideration is the population movements that tend to erode the local beliefs that, in certain places, have traditionally protected various lemur species.

More worrying yet is destruction of habitat, principally by slash-and-burn agriculture but also by the cutting of trees for fuel and by commercial logging. The largest continuous forest tract in Madagascar lies along the island's humid eastern escarpment. By analyzing historical documents and satellite images, Glen M. Green and Robert W. Sussman of Washington University have shown that 66 percent of the area covered by this forest at the turn of the century had been denuded by 1985. They estimate that within another 35 years only the steepest slopes of the escarpment will still bear trees. In the flatter western and southern regions of the island, the rate of disappearance of forest is probably faster.

Such pressures have existed for many decades. In the 1920s the colonial authorities in Madagascar set up one of the world's first systems of natural reserves. But as one of the world's poorest countries, Madagascar, despite its government's genuine concern, cannot afford to police these reserves adequately or, in some cases, at all. Fortunately, in recent years the island has attracted the attention of the international conservation community. The country figured recently in one of the first "debt for nature" swaps, in which foreign debt is reduced in exchange for the protection of natural areas.

It is, of course, the real and immediate needs of desperately poor local communities that are being met by most of the forest destruction. In many cases, large-scale agreements on conservation have yet to devolve from the higher governmental sphere to actual projects on the ground. But as they do, one can hope for the stabilization and perhaps even for the long-term improvement of Madagascar's environmental situation.

Meanwhile the lemur populations continue to dwindle. It is tragic to see any part of the world's biodiversity disappear, but the tragedy is particularly acute in the case of Madagascar's lemurs, which still have so much to teach us about our own past.

Climatic stress and the consequent reduction and redistribution of forests thus constitute one potential factor in the disappearance of the subfossil fauna of Madagascar. But it is clear that in that land as elsewhere, periodic disturbances of this kind have occurred throughout time. The ancestral lineages of the extinct lemurs obviously survived these earlier vicissitudes, and there is no reason to believe that on their own the most recent (rather mild) round of climate changes should have had a fatal effect on several lineages simultaneously. This is especially true when we consider that most subfossil lemurs were probably ecological generalists. Megaladapis, Palaeopropithecus and Archaeolemur, among others, lived in environments ranging from humid to arid and were clearly highly adaptable in terms of choice of habitat. Hence, something other than simply another cycle of disturbance of natural habitat must be invoked to explain the disappearance of the giant lemurs. Only one truly novel factor presents itself: Homo sapiens.

To talk of the "extinction event" of the large-bodied lemurs implies a process that has ended. That is not so. The extinct and living lemurs form part of a single process that is continuing. The smaller, fleeter lemurs have survived so far, but they are themselves under increasing pressure from an expanding human population. The toll of hunting increases as human numbers and the use of more sophisticated weapons do. Another important consideration is the population movements that tend to erode the local beliefs that, in certain places, have traditionally protected various lemur species.

More worrying yet is destruction of habitat, principally by slash-and-burn agriculture but also by the cutting of trees for fuel and by commercial logging. The largest continuous forest tract in Madagascar lies along the island's humid eastern escarpment. By analyzing historical documents and satellite images, Glen M. Green and Robert W. Sussman of Washington University have shown that 66 percent of the area covered by this forest at the turn of the century had been denuded by 1985. They estimate that within another 35 years only the steepest slopes of the escarpment will still bear trees. In the flatter western and southern regions of the island, the rate of disappearance of forest is probably faster.

Such pressures have existed for many decades. In the 1920s the colonial authorities in Madagascar set up one of the world's first systems of natural reserves. But as one of the world's poorest countries, Madagascar, despite its government's genuine concern, cannot afford to police these reserves adequately or, in some cases, at all. Fortunately, in recent years the island has attracted the attention of the international conservation community. The country figured recently in one of the first "debt for nature" swaps, in which foreign debt is reduced in exchange for the protection of natural areas.

It is, of course, the real and immediate needs of desperately poor local communities that are being met by most of the forest destruction. In many cases, large-scale agreements on conservation have yet to devolve from the higher governmental sphere to actual projects on the ground. But as they do, one can hope for the stabilization and perhaps even for the long-term improvement of Madagascar's environmental situation.

Meanwhile the lemur populations continue to dwindle. It is tragic to see any part of the world's biodiversity disappear, but the tragedy is particularly acute in the case of Madagascar's lemurs, which still have so much to teach us about our own past.