Pruning the Primate Family Tree

Frustrated by the failure of gorillas to thrive in captivity, in 1914 the Bronx Zoo's director William Hornaday lamented "There is not the slightest reason to hope that an adult gorilla, either male or female, ever will be seen living in a zoological park or garden." Whereas wild adult gorillas were "savage" and "implacable" beasts which could not be captured (a photo of a sculpture included in Hornaday's article depicts a gorilla strangling one man, brandishing another about with its other arm, and standing on the body of a third), young gorillas were fragile animals that did not last long in the concrete and steel enclosures made for them. One gorilla in Germany had survived for seven years, but the average lifespan of a captive juvenile gorilla was about nine months, and often considerably less than that. This was not to say that zoological parks would stop trying to capture and import young gorillas - Hornaday gave no indication that he wished to stop procuring young gorillas for his zoo - but only that visitors to the Bronx Zoo and other menageries would probably never see an adult gorilla.

Zoos had been failing miserably at keeping apes in captivity for centuries. Most of the animals captured were young individuals which had been snatched from their families or had just been orphaned by specimen collectors. They regularly died on the journey out of Africa or shortly after they arrived at their public confines. Many refused to eat, and most would become sick before passing away, but why this should be so puzzled zoologists. Perhaps, they speculated, it was a matter of climate. The cooler climates of Europe and North America were poor proxies for equatorial Africa, so it was hardly surprising that mortality was so high.

Looking back at the practices of zoos during the early 20th century, however, it is apparent that the different climates of Europe and North America cannot solely be blamed for the deaths of these apes. The traditional methods of catching and collecting wild animals which had worked for many other species caused a great deal of stress for captured apes, and the concrete and steel enclosures in which they were placed were cruel by today's standards. (Though, even under today's improved conditions, it can still be questions whether zoos are capable of keeping apes happy and healthy.) Still, in reference to climate, what is curious about the modern disparity between Africa and the places to which the young apes were shipped is that, not so very long ago, much of the northern hemisphere was inhabited by a variety of apes species. North American never had apes, but Europe and much of Asia did, making today's ape species the tattered branches of what once was a richer family tree.

Between 23 and 5.3 million years ago, during the slice of geologic time known as the Miocene, at least ten genera of hominoids (the clade representing all apes) existed at different times across Europe and Asia, and this diversity was bolstered by the presence of the closely-related pliopithecoids in the same areas. Together these types of large primates flourished in the warm, wet forests of the northern hemisphere, but by about 8.7 million years ago the hominoids and pliopithecoids were extirpated from Europe, with apes surviving only in Africa and Asia and the pliopithecoids eventually becoming entirely extinct. Several millions years before the origin of our own lineage (the hominins) in Africa, there was a major crash in Europe's primate diversity, but the key to what happened there is not found among the apes. Instead it is to be found among the herbivorous, hoofed mammals which lived on the ground below them.

The changeover among primates, and other animal groups, during the Late Miocene has been recognized for a long time. It appears that towards the close of the period seasons were becoming more intense and there was a drying trend, leading to the establishment of grasslands where there once were forests. The proliferation of grazing species during this time is in accord with this hypothesis, but the specific reactions of the fauna to these changes remains blurry. For example, high-crowned cheek teeth are characteristic of grazing animals and so it would be expected that an increased number of herbivores with high cheek teeth would indicate the spread of grasslands, but some of the animals taken as indicative of this trend only had high cheek teeth because they inherited them from their ancestors. They could have just as easily browsed on softer foods or had a more mixed diet.

Indeed, teeth can be a tricky thing. On a superficial level the overall shape of a tooth can help indicate whether an animal grazed on the plains or browsed for soft plants in forests, but extinct herbivores cannot so easily be shunted into just one category or another. Among fossil horses, especially, it has been found that some species once given the "grazer" label had more mixed diets or did not restrict their feeding to grasslands, and this enhanced resolution has often been achieved by looking at the microscopic scratch and wear patterns on teeth. Unlike bone, teeth do not heal when damaged, and so the wear caused by feeding is permanently recorded on teeth. By looking at these wear patterns paleontologists can test what was supposed on gross tooth morphology and gain a clearer indication of what an animal's ecology was like.

The scratches on the teeth of fossil herbivores from Europe provided paleontologists Gildas Merceron, Thomas Kaiser, Dimitri Kostopoulos, and Ellen Schulz with the evidence they needed to figure out the tempo of ape extinction in Europe. In a study just published in the Proceedings of the Royal Society B, the scientists looked at the short- and long-term patterns of wear on the teeth of 552 specimens of deer, bovids, "mouse deer", and "musk deer" from sites in Germany, Hungary, and Greece spanning about eleven to seven million years ago from which fossil primates had also been found. These sites record the drastic drop in primate diversity, and if changes in the diets of herbivores were recorded on their teeth, then it could signal quick alterations in habitat which drove the hominoids and pliopithecoids into extinction.

The scientists divided up their samples according to the times and places they represented and calculated the average mesowear (a measure of tooth wear over the long term judged by the height and sharpness of the cusps along the cheek-side of the upper second molar) and microwear (indicators of dietary preferences close to the organism's death based upon scratches and pits on the tooth) statistics for each. What the researchers found was that, taken together, each community of herbivores represented different habitat types in each location. The wear on the herbivore teeth differed from species to species as would be expected due to herbivores carving out their own niches while living alongside one another, and the average values calculated for each place/time period combination also represented different aspects along the scale between open grasslands and closed-in forests.

The researchers broke down the results by time period. During the Vallesian, about 11.6 to 9 million years ago, the primate Ouranopithecus occupied more open habitats shared by grazers than the other primates of Hungary and Germany, and among the latter two countries there were significantly more browsers in Germany than Hungary. These patterns changed by beginning of the next age, the Turolian, in which the similarity between the three places increased. There were more grazers in Germany and Hungary, and, oddly enough, a few more browsers in Greece, reducing the amount of disparity between the places. Grasslands spread in Germany and Hungary, while there was probably an increase in bushy shrubs in Greece.

The overall picture that emerged from the pool of data is that the sites in Germany, Hungary, and Greece were quickly changing in response to both global and local changes. During the span of time considered in the study, the Alps were being uplifted, there was a succession of glaciations in Antarctica, and other large-scale changes altered the global climate. These changes caused the forests of Europe to become more open and for semi-tropical type plants to become replaced by those seen at high altitudes or cooler conditions. The forests did not disappear all at once, but rather opened up and allowed the establishment of low, scrubby vegetation in the grass-dominated gaps.

Different kinds of mammals responded to these changes in different ways. While herbivorous hoofed mammals diversified as a result of the changes in low-to-the-ground vegetation, the primates lost the multi-level distribution of niches once available in the trees. This pattern is more marked in central Europe than in Greece - the authors of the paper note that the primates there did not live in a place with close tree cover, and instead their decline may be related to the increase in bushy shrubs - although the overall development of a cooler, drier climate appears to have done in primates elsewhere (such as Sivapithecus in what is now central Asia), as well.

By using the shifting diets of herbivores for proxies of climate change, the researchers were able to demonstrate that the decline in primate diversity coincided with the opening up of forests towards the end of the Miocene. The details of why these primates did not survive, especially since those in Greece lived in a more open habitat already, are not yet clear, but there appears to be a strong relationship between fluctuations in primate diversity and climate. We can see the similar changes occurring today, but among a very different group of primates being adversely affected by the activities of our species.

Lemurs are strepsirrhine primates, living members of a diverse group which split from our side of the family tree (the haplorrhines) over 55 million years ago. While their close relatives - such as lorises and galagos - range across Africa and Asia, lemurs only exist on the island of Madagascar, a place where environmental destruction has put nearly all living lemur species at risk of extinction. The chaotic nature of local politics has done nothing to help this, especially as many government officials have allowed destruction of forests to get as much money as they can before being booted from office, but the activities of people all over the world are also putting pressure on the lemurs. Much like mountain uplift and glaciations changed the climate of the Miocene, the amount of greenhouse gases our species has dumped into the atmosphere since the Industrial Revolution is also changing the climate, and according to a new paper in Global Change Biology this may have dire consequences for Madagascar's unique primates.

When the issue of human-driven climate change comes up, dwindling polar bear populations and melting glaciers most immediately come to mind. They are dramatic examples of change happening on a timescale we can see and comprehend. Despite the phrases "global warming" and "global climate change", however, it is often forgotten that fluctuations in climate affect organisms in the tropics as well as at the poles, and scientists Amy Dunham, Elizabeth Erhart, and Patricia Wright have found that for at least one species of lemur - Milne Edward's sifaka (Propithecus edwardsi) - fluctuations in climate greatly influence the survival of infant individuals past their first year.

Lemur mothers give birth to and raise their offspring according to a schedule attuned to their surroundings. The distinct divide between the wet and dry seasons means that important resources are only available during particular times of the year, and it appears that weaning schedules for lemur babies are roughly scheduled according to when fruit and soft young leaves will be the most abundant. If baby lemurs are to reach their first birthday (and beyond), timing is everything, but natural phenomena such as the El Nino Southern Oscillations may alter patterns in rainfall and other factors which are important to young lemur survival.

To figure out how climate relates to fecundity in Milne Edward's sifaka populations clustered in the southeastern part of the islands, the scientists looked at half a century's worth of climate data and two decades worth of lemur demographics to see if fluctuations in the local climate influenced lemur populations. The results confirmed what had previously been suspected on anecdotal evidence. Variations in rainfall, the regular landfall of cyclones, and alterations to local climate triggered by El Nino all influenced the mortality of infant lemurs, but each in different ways. While a drought would obviously have adverse consequences for lemurs, extreme amounts of rainfall caused by El Nino appear to be even worse as it causes the death of trees and vegetation essential to the survival of young lemurs. Cyclones are even more dramatic in their effect. A cyclone can entirely wipe out the available fruit on large trees, robbing lactating mothers of the resources they need to provide energy-rich milk for their young. The number of young which survive to their first year dip and rally according to these events, confirming that the population dynamics of this species of lemur is heavily affected by fluctuations in climate and extreme weather events.

What the results of the study suggests is that continued anthropogenic climate change may bring lemurs such as Milne Edward's sifaka closer to extinction. Natural fluctuations in climate, from the effects of El Nino to cyclones, already adversely effect the number of lemurs that are able to survive past their first year, but human-caused climate change has the potential to make the shifts in climate more extreme. Deforestation remains a significant threat to the lemurs and other parts of Madagascar's native fauna, but the development of drier dry seasons and wetter wet seasons (as has been predicted by climate models over the next century based upon the influence of human-driven climate change) may tip the scales. Even if we save Madagascar's forests, the shifts in climate may be enough to put some lemurs over the edge.

The lemurs of southern Madagascar are not the only primates in such a predicament. Habitat loss and climate change will no doubt continue to put pressure on other species all around the world, many of which are already endangered. Apes, especially, are under serious threats from our species, and should they disappear it will wipe away the vestiges of global ape diversity which existed during the Miocene. Then we would be the last ape, a lonely species left to wonder when we, too, will slip into extinction.

Merceron, G., Kaiser, T., Kostopoulos, D., & Schulz, E. (2010). Ruminant diets and the Miocene extinction of European great apes Proceedings of the Royal Society B: Biological Sciences DOI: 10.1098/rspb.2010.0523

DUNHAM, A., ERHART, E., & WRIGHT, P. (2010). Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar Global Change Biology DOI: 10.1111/j.1365-2486.2010.02205.x