Herbarium specimens show contrasting phenological responses to Himalayan climate

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 longterm change.phenology | global warming I n an era of ongoing climate change (1), shifts in seasonal timing of life history events (phenology) are among the first and the most important responses seen in biological systems (2-5). Changes in phenology potentially impact organism reproduction, population survival, species boundaries, and ecosystem service (6-8). However, despite the importance of phenological changes (9, 10), data sources are limited (11). Satellite imagery (12), experimental studies (13), and modern observational records of phenology (11,14) are temporally restricted to the last few decades. Although historical phenological records kept by scientists, amateur naturalists, or for cultural reasons (15-17) may extend much further, these are often limited in geographic range, and tend to focus on North America and Europe (but see ref. 18).Such records have not been found for the Himalayan region, an area of particular concern when considering climate change. Rapid temperature increases and changes in precipitation, in combination with the importance of Himalayan snowpack and glaciers to water supply and monsoon cycles, make the region one of the most threatened nonpolar areas of the world (1,19). Recent climate change is impacting Himalayan biological systems, including those upon which humans rely (20-23).Despite its remoteness, the botanical richness of Yulong Mountain (27°N, 100.2°E), at the eastern limit of the Himalayan region, has made it a center of botanical collection since the late 19th century. Yulong Mountain was home to the prolific plant hunters George Forrest (collecting 1904-1930) and Joseph Rock (collecting 1918-1948). Other early collectors in the area included Jean Marie Delavayi, Heinrich ...

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