Demonstrations of coupled phenotypic and demographic responses to climate change are rare. But they are much needed in formulating predictions of the effects of climate change on natural populations.

Climate change is affecting natural systems, as is clear from the ample data on shifts in the seasonal timing — the phenology — of reproduction and migration, and in body size and species' distribution ranges1. Evidence that climate change is affecting population numbers is less abundant; variations in population size can have many causes. On page 482 of this issue, however, Ozgul and colleagues2 describe just such a connection.

Ozgul et al. have studied the impact of climate change on the demographic processes affecting population numbers of yellow-bellied marmots (Marmota flaviventris, pictured on the cover). These rodents live in a subalpine habitat in the United States and spend the winter hibernating. Climate change has led to a shift in the marmots' phenology of hibernation and reproduction: they now emerge earlier in spring and also wean their young earlier. As a consequence, their growing season has become longer, and they are heavier before they begin hibernation. Such shifts in phenology have been shown many times, but Ozgul et al. take matters further by assessing the effect that the increase in mass has had on various demographic rates, such as winter survival and probability of reproduction. These demographic effects are then used to explain the sharp, threefold increase in marmot numbers from the year 2000 onwards.

The authors show that the marmots' demographic rates are affected in two ways by climate change. The first is a straightforward effect of the increased mass preceding hibernation. This mass directly affects winter survival, so more animals are surviving. But the second is more subtle: climate change also affects the relationship between mass and demographic processes. For instance, adult winter survival has been more strongly dependent on mass in more recent, warmer years, but, on top of that, animals have also survived better over the entire range of hibernation masses during this period than in the past. Both factors have influenced the overall increased survival. The authors use the combined effects to explain the population increase. It is fascinating that these links between phenotype and demographic processes are altering owing to climate change.

The pre-hibernation increase in mass over the study period (1976–2008) was largely due to phenotypic plasticity, as has often been found3, rather than to genetic change. This means that the marmots are not changing genetically, but that they have higher masses owing to altered environmental conditions. It remains unclear why they are now heavier. In a mechanistic approach, there is always another underlying causal level to be explored. For instance, Ruf and Arnold4 showed that hibernating alpine marmots (Marmota marmota) that had pre-hibernation dietary access to specific plant compounds (polyunsaturated fatty acids) were able to drop their temperature at hibernation to a lower level, and hence needed less fat at the start of hibernation.

It is thus possible that, in the yellow-bellied marmot, changes in flower phenology or seed production also play a part. Interestingly, Ozgul and colleagues observed a marked decline in the number of flowers of tall bluebells (Mertensia ciliata), a plant included in the marmots' diet5, in the study after the year 2000. This may mean that the marmots have lacked some specific plant compounds, and so have needed to be fatter to survive hibernation. This would indicate a strategic change in hibernation mass, whereas Ozgul et al. assume that change is attributable simply to the prolonged growing season, and the extension of the time available for marmots to become heavier. Further insight into the complex ecological and physiological mechanisms involving energy expenditure during hibernation, winter temperature and diet during pre-hibernation fattening is needed to fully understand the observed abrupt increase in the marmot population after 2000.

The major challenge in climate-change ecology is to predict the impact of future climate change on populations6. The study on marmots2 emphasizes again that this challenge needs to be tackled with mechanistic population models that incorporate ecological and evolutionary processes7,8. In the case of the marmots, the altered ecological processes change the way in which the demographic rates are affected by hibernation mass. The evolutionary processes select for phenotypic plasticity — that is, how the environment influences hibernation mass. The task ahead is to model these processes simultaneously2,8, as well as to integrate physiology and molecular genetics into these mechanistic population models. It is only by this route that biologists will be able to forecast the implications of various climate scenarios for population viability and, ultimately, for biodiversity.

References 1 Parmesan, C. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006). 2 Ozgul, A. et al. Nature 466, 482–485 (2010). 3 Gienapp, P., Teplitsky, C., Alho, J. S., Mills, J. A. & Merilä, J. Mol. Ecol. 17, 167–178 (2008). 4 Ruf, T. & Arnold, W. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1044–R1052 (2008). 5 Frase, B. A. & Armitage, K. B. Ethol. Ecol. Evol. 1, 353–366 (1989). 6 Jenouvrier, S. et al. Proc. Natl Acad. Sci. USA 106, 1844–1847 (2009). 7 Visser, M. E. Proc. R. Soc. B 275, 649–659 (2008). 8 Chevin, L.-M., Lande, R. & Mace, G. M. PLoS Biol. 8, e1000357 (2010). Download references

Author information Affiliations Marcel E. Visser is at the Netherlands Institute of Ecology (NIOO-KNAW), PO Box 40, 6666 ZG Heteren, the Netherlands. m.visser@nioo.knaw.nl Marcel E. Visser Authors Marcel E. Visser View author publications You can also search for this author in PubMed Google Scholar

Rights and permissions Reprints and Permissions