Published online 23 May 2010 | Nature | doi:10.1038/news.2010.258

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Past climate change led to lower diversity in the small and furry.

The adaptable deer mouse spread through northern California at the end of the Pleistocene era. Gerry Ellis/Minden Pictures/FLPA

The period of global warming linked to the extinction of animal giants such as the woolly mammoth also made its mark on smaller mammals who survived the event.

Adaptable deer mice came to dominate the small furry communities of northern California as the climate warmed at the end of the last ice age, around 11,700 years ago, an excavation of one ancient woodrat nest shows. Overall, the number of small mammalian species in the area declined by about one-third, say Jessica Blois, currently at the University of Wisconsin, Madison, and her colleagues.

The study, published today in Nature1, emphasizes that concentrating solely on eye-catching species extinctions fails to capture the full impact of climate change on biodiversity. "If we focus only on extinction, we're not getting the whole story," says Blois. The work also suggests that rapidly reproducing, adaptable species — such as the deer mice — could benefit further from future warming.

Tales from rodent nests

The end of the Pleistocene era is famous for its megafauna extinctions, and researchers have been searching for megafaunal remains for at least a century. One of many sites at which such remains have been found is the Samwell Cave along a drainage basin in Shasta County, California — the site of the current study.

Blois's team, however, looked for evidence of diversity in smaller creatures. "We were mainly interested in small mammals, the guys that survived the extinction event," she says. The researchers picked through fossilized woodrat nests, called middens, which have been well preserved in caves. Woodrats collect scat and pellets containing, among other things, small mammalian bones, which carnivores such as eagles, owls and foxes have defecated or regurgitated. "You just have to find the midden, and animals have already done all the work for us," says Blois. "The carnivores sample and the woodrats collect the dead and digested animals."

Sifting through the biological debris, the authors found ample evidence of changes in species diversity that occurred thousands of years ago. They measured this diversity in two ways: by 'richness', the number of different species present; and 'evenness', the relative dominance of certain species over others.

Some of the larger specimens from the Samwell Cave Popcorn Dome deposits. Rodent teeth are shown as the upper teeth in Level IVb. Jessica Blois

Pleistocene communities had fewer species considered rare, so were significantly more even than today's. But Blois's team found that in northern California, richness locally declined by 32%. This was partly due to the disappearance from the area of two species: the Mazama pocket gopher and the mountain beaver, both of which left for cooler climes elsewhere. From genetic data and tooth morphology, Blois surmised that the Mazama pocket gopher had been the dominant gopher species in the past. But there was a large gopher turnover around the end of the Pleistocene, and by about 6,000 years ago Botta's pocket gopher was the only gopher species in the region. It remains so today.

Meanwhile, the number of native deer mice (Peromyscus) in the fossil deposits nearly doubled between 16,000 and 13,000 years ago, contributing to a 26% drop in evenness. Because Peromyscus mice are habitat generalists with high reproduction rates and broad climate tolerances, Blois speculates that these mice were better able to deal with disturbances.

Climate and diversity

To connect these changes in diversity with climate, the authors compared their small-mammal data with global oxygen-isotope numbers. They found that declines in both evenness and richness correlated strongly with climate warming — providing "the unequivocal link between climatic changes and decreases in biodiversity", according to David Nogués-Bravo of the Center for Macroecology, Evolution and Climate at the University of Copenhagen.

Last month, Nogués-Bravo and his co-workers reported on climate predictors of extinctions2, showing that, in general, continents that experienced greater magnitudes of climate change witnessed more extinctions. Blois's study is regional and looks at changes in surviving species, but Nogués-Bravo says that both papers point to climate change during the late Pleistocene as the primary driver of diversity changes.

Previous work on plants and microbes has shown that richer and more even communities recover more rapidly from perturbations. "Past diversity declines mean that the mammal communities we see around us today may already be at a disadvantage in terms of their resilience to climate change and other human impacts," Blois says.

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Future climate projections show a warmer and possibly drier California, which may mean a further boost for mouse numbers. But some habitats will be lost, likely taking with them other small mammals and the ecosystem functions that they serve. Gophers, for example, act as ecosystem engineers, mixing and aerating soil and cycling nutrients between the surface and below ground as they dig their burrows; whereas northern flying squirrels spread fungal spores when they dig for truffles.

"The mice aren't able to fulfil all those roles," Blois says. "There's no one super animal in the community who can perform all those functions."