The genetic history of six large herbivores - the woolly rhinoceros, woolly mammoth, wild horse, reindeer, bison, and musk ox - has shown that both climate change and humans were responsible for the extinction or near extinction of large mammal populations within the last 10,000 years. The study, which is the first to use genetic, archeological, and climatic data together to infer the population history of large-bodied Ice-Age mammals, will be published in the journal Nature.

The study was led by Professor Eske Willerslev of the Centre for GeoGenetics at the University of Copenhagen and includes an international team of paleontologists, geologists, geneticists and climate modelers including Beth Shapiro, the Shaffer Associate Professor of Biology at Penn State University.

The study's findings are expected to shed light on the possible fates of living species of mammals as our planet continues its current warming cycle.

"Our findings put a final end to the single-cause theories of these extinctions," said Willerslev. "Our data suggest care should be taken in making generalizations regarding past and present species extinctions; the relative impacts of climate change and human encroachment on species extinctions really depends on which species we're looking at."

Shapiro explained that all six of the species the team studied flourished during the Pleistocene Epoch - the period of geological time that lasted from about 2 million to 12,000 years ago.

"During this time, there were lots of climatic ups and downs - oscillations between long, warm intervals called interglacial periods, during which the climate was similar to what we have today, followed by long, cold intervals called glacial periods, or ice ages," Shapiro said.

"Although these cold-adapted animals certainly fared better during the colder, glacial periods, they still managed to find places where the climate was just right - refugia - so that they could survive during the warmer, interglacial periods.

Then, after the peak of the last ice age around 20,000 years ago, their luck started to run out. The question is, what changed? Why were these mammals no longer able to find safe refugia where they could survive in a warm climate?"

To answer these questions, the team collected many different types of data to test hypotheses about how, when, and why the woolly rhinoceros, woolly mammoth, and wild horse all went extinct after the last ice age, and why the reindeer, bison, and musk ox were able to survive - albeit in much more restricted ranges than they could inhabit during the ice ages. "One source of information we used was DNA from the animals themselves," Shapiro explained.

"With genetic data, it's possible to estimate when and how much populations were able to grow and shrink as the climate changed and their habitat started to disappear." The team also collected climatic data - temperature and precipitation patterns - from both glacial and interglacial periods, as well as archeological data, which they used to study the extent to which early humans may have influenced the survival of these six mammal species.

"For example, in locations where animal bones had been cooked or converted into spears, we know that humans lived there and were using them as a resource," Shapiro said.

"Even where we don't find evidence that humans were using the animals, if humans and the animals lived in the same place and at the same time, humans could have had some influence on whether the animals survived or not."

In the case of the now-extinct woolly rhinoceros, the scientists found that, in Europe, the ranges of humans and woolly rhinoceros never overlapped. "These data suggest that climate change, and not humans, was the main reason why this particular species went extinct in present-day Europe," Shapiro said.

"Still, we expect humans might have played a role in other regions of the world where they did overlap with woolly rhinos, and so further studies will be necessary to test this hypothesis." Much clearer was the evidence that humans did influence, and not always negatively, the population sizes of the five other species - the woolly mammoth, wild horse, reindeer, bison, and musk ox.

Shapiro explained that population fluctuations for all six species continued until the end of the last ice age - around 14,000 years ago - when many of the species simply disappeared.

"The take-home message is that during the most recent warming event, when the last ice age faded into the warm interval we have today, something kept these animals from doing what they had always done, from finding alternative refugia - less-than-ideal, but good-enough chunks of land on which to keep their populations at a critical mass," Shapiro said. "That 'something' was probably us - humans."

During the period when these animals were declining, the human population was beginning its boom, and was spreading out across not only the large-bodied mammals' cold-climate habitats, but also across their warm-climate refuges, changing the landscape with agriculture and other activities.

Many large-bodied, cold-adapted mammals, including the horse - which is considered extinct in the wild and now survives only as a domesticated animal - suddenly had no alternative living spaces, and, as such, no means to maintain their populations.

"The results of our study suggest that although past warm periods caused these animal species to go through periodic bottlenecks - evolutionary events during which the size of a population diminishes substantially and stays small for a long time - they always seemed to bounce back, and to return to their previous habitats as soon as the Earth became cooler again. Then, during the most-recent warming cycle, that trend changed," Shapiro said.

As the climate became warmer after the last ice age, the woolly rhinoceros, woolly mammoth, and wild horse became extinct, and the reindeer, bison, and musk ox may have just been fortunate in avoiding extinction, according to Shapiro.

"We couldn't pinpoint what patterns characterize extinct species, despite the large and varying amount of data analyzed," said Eline Lorenzen, from the University of Copenhagen and the first author of the study.

"This suggests that it will be challenging for experts to predict how existing mammals will respond to future global climate change - to predict which species will go extinct and which will survive."

Reindeer managed to find safe habitat in high arctic regions and, today, have few predators or competitors for limited resources. Bison are extinct in Asia, where their populations were extensive during the ice ages, and today they are found only in North America, although a related species survives in small numbers in Europe.

Cold-adapted muskoxen now live only in the arctic regions of North America and Greenland, with small introduced populations in Norway, Siberia, and Sweden.

Interestingly, if humans had any impact on musk-ox populations, it may have been to help sustain them. Musk-ox populations first became established in Greenland around 5,000 years ago, after which they expanded rapidly, despite having been a major resource for the Paleo-Eskimo population. Today, the animal species survives in large numbers.

Shapiro also said that the findings could help to predict the fate of populations threatened by the climate change and habitat alteration that is happening today.

"Our results provide direct evidence that something changed between the most-recent glacial cycle, when many of these species went extinct, and previous glacial cycles, through which they all managed to survive.

"Although it is clear that climate change drives the dynamics of these species, we, as humans, have to take some of the blame for what happened during this most-recent cycle. It seems that our ancestors were able to change the landscape so dramatically that these animals were effectively cut off from what they needed to survive, even when the human population was small," Shapiro said.

"There are many more humans today, and we have changed and are continuing to change the planet in even more important ways."

In addition to Shapiro, Willerslev and Lorenzen, many other scientists contributed to this study. In the United States, contributing authors are from institutions in Utah, California, Texas, Missouri, Maryland, Colorado, Massachusetts, Oregon, and Kansas. The study's international contributors are from institutions in Denmark, Australia, Sweden, Spain, the United Kingdom, the Netherlands, Germany, Norway, Russia, China, and Canada.