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Herbarium specimens show contrasting phenological responses to Himalayan climate

  1. Jianchu Xuc,d
  1. aDepartment of Biology, University of Missouri–St. Louis, St. Louis, MO 63121;
  2. bWilliam L. Brown Center, Missouri Botanical Garden, St. Louis, MO 63166;
  3. cKey Laboratory of Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, China; and
  4. dWorld Agroforestry Centre, East and Central Asia, Kunming 650204, China

  1. Edited* by Peter H. Raven, Missouri Botanical Garden, St. Louis, Missouri, and approved June 5, 2014 (received for review March 7, 2014)

Significance

Natural events in temperate ecosystems are triggered by seasonal temperature changes. Climate change may shift the timing of these events. We use a century of herbarium collections of Himalayan rhododendrons to investigate climate-driven change in flowering time. Although increased annual temperatures are associated with earlier flowering, increased fall temperatures are associated with delayed flowering. Annual warming may advance flowering through positive effects on overwintering bud formation, whereas fall warming may delay flowering through an impact on chilling requirements. These contrasting effects have resulted in opposing changes in flowering time, even as temperatures have warmed rapidly in the past 45 y. This study demonstrates the value of natural history collections to inform ecological questions, especially regarding climate change.

Abstract

Responses by flowering plants to climate change are complex and only beginning to be understood. Through analyses of 10,295 herbarium specimens of Himalayan Rhododendron collected by plant hunters and botanists since 1884, we were able to separate these responses into significant components. We found a lack of directional change in mean flowering time over the past 45 y of rapid warming. However, over the full 125 y of collections, mean flowering time shows a significant response to year-to-year changes in temperature, and this response varies with season of warming. Mean flowering advances with annual warming (2.27 d earlier per 1 °C warming), and also is delayed with fall warming (2.54 d later per 1 °C warming). Annual warming may advance flowering through positive effects on overwintering bud formation, whereas fall warming may delay flowering through an impact on chilling requirements. The lack of a directional response suggests that contrasting phenological responses to temperature changes may obscure temperature sensitivity in plants. By drawing on large collections from multiple herbaria, made over more than a century, we show how these data may inform studies even of remote localities, and we highlight the increasing value of these and other natural history collections in understanding long-term change.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: robbie.hart{at}mobot.org.

  • Author contributions: R.H., J.S., S.R., and J.X. designed research; R.H. and J.S. performed research; R.H., J.S., and S.R. analyzed data; and R.H., J.S., S.R., and J.X. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1403376111/-/DCSupplemental.

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