In recent decades, the final frost dates of winter have advanced throughout North America, and many angiosperm taxa have simultaneously advanced their flowering times as the climate has warmed. Phenological advancement may reduce plant fitness, as flowering prior to the final frost date of the winter/spring transition may damage flower buds or open flowers, limiting fruit and seed production. The risk of floral exposure to frost in the recent past and in the future, however, also depends on whether the last day of winter frost is advancing more rapidly, or less rapidly, than the date of onset of flowering in response to climate warming. This study presents the first continental-scale assessment of recent changes in frost risk to floral tissues, using digital records of 475,694 herbarium specimens representing 1,653 angiosperm species collected across North America from 1920 to 2015. For most species, among sites from which they have been collected, dates of last frost have advanced much more rapidly than flowering dates. As a result, frost risk has declined in 66% of sampled species. Moreover, exotic species consistently exhibit lower frost risk than native species, primarily because the former occupy warmer habitats where the annual frost-free period begins earlier. While reducing the probability of exposure to frost has clear benefits for the survival of flower buds and flowers, such phenological advancement may disrupt other ecological processes across North America, including pollination, herbivory, and disease transmission.

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Understanding the effects of climate change on the phenological structure of plant communities will require measuring variation in sensitivity among thousands of cooccurring species across regions. Herbarium collections provide vast resources with which to do this, but may also exhibit biases as sources of phenological data. Despite general recognition of these caveats, validation of herbarium-based estimates of phenological sensitivity against estimates obtained using field observations remains rare and limited in scope. Here, we leveraged extensive datasets of herbarium specimens and of field observations from the USA National Phenology Network for 21 species in the United States and, for each species, compared herbarium-and field-based estimates of peak flowering dates expected under standardized temperature conditions, and of sensitivity of peak flowering time to geographic and interannual variation in mean minimum temperatures (TMIN). We found strong agreement between herbariumand field-based estimates for standardized peak flowering time (r = 0.91, p < 0.001) and for the direction and magnitude of sensitivity to both geographic TMIN variation (r = 0.88, p < 0.001) and interannual TMIN variation (r = 0.82, p < 0.001). This agreement was robust to substantial differences between datasets in 1) the long-term TMIN conditions observed among collection and phenological monitoring sites and 2) the interannual TMIN conditions observed in the time periods encompassed by both datasets for most species. Our results show that herbarium-based sensitivity estimates are reliable among species spanning a wide diversity of life histories and biomes, demonstrating their utility in a broad range of ecological contexts, and underscoring the potential of herbarium collections to enable phenoclimatic analysis at taxonomic and spatiotemporal scales not yet captured by observational data.

BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

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