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Winter and spring warming result in delayed spring phenology on the Tibetan Plateau
Edited by F. Stuart Chapin, University of Alaska, Fairbanks, AK, and approved October 25, 2010 (received for review August 23, 2010)

Abstract
Climate change has caused advances in spring phases of many plant species. Theoretically, however, strong warming in winter could slow the fulfillment of chilling requirements, which may delay spring phenology. This phenomenon should be particularly pronounced in regions that are experiencing rapid temperature increases and are characterized by highly temperature-responsive vegetation. To test this hypothesis, we used the Normalized Difference Vegetation Index ratio method to determine the beginning, end, and length of the growing season of meadow and steppe vegetation of the Tibetan Plateau in Western China between 1982 and 2006. We then correlated observed phenological dates with monthly temperatures for the entire period on record. For both vegetation types, spring phenology initially advanced, but started retreating in the mid-1990s in spite of continued warming. Together with an advancing end of the growing season for steppe vegetation, this led to a shortening of the growing period. Partial least-squares regression indicated that temperatures in both winter and spring had strong effects on spring phenology. Although warm springs led to an advance of the growing season, warm conditions in winter caused a delay of the spring phases. This delay appeared to be related to later fulfillment of chilling requirements. Because most plants from temperate and cold climates experience a period of dormancy in winter, it seems likely that similar effects occur in other environments. Continued warming may strengthen this effect and attenuate or even reverse the advancing trend in spring phenology that has dominated climate-change responses of plants thus far.
Footnotes
- 1To whom correspondence should be addressed. E-mail: J.C.Xu{at}cgiar.org.
Author contributions: H.Y. and J.X. designed research; H.Y., E.L., and J.X. performed research; H.Y. and E.L. contributed new reagents/analytic tools; H.Y. and E.L. analyzed data; and H.Y. and E.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1012490107/-/DCSupplemental.
Freely available online through the PNAS open access option.
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