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Phenology varies widely over space and time because of its sensitivity to climate. However, whether phenological variation is primarily generated by rapid organismal responses (plasticity) or local adaptation remains unresolved. Here we used 1,038,027 herbarium specimens representing 1,605 species from the continental United States to measure flowering-time sensitivity to temperature over time (Stime) and space (Sspace). By comparing these estimates, we inferred how adaptation and plasticity historically influenced phenology along temperature gradients and how their contributions vary among species with different phenology and native climates and among ecoregions differing in species composition. Parameters Sspace and Stime were positively correlated (r = 0.87), of similar magnitude and more frequently consistent with plasticity than adaptation. Apparent plasticity and adaptation generated earlier flowering in spring, limited responsiveness in late summer and delayed flowering in autumn in response to temperature increases. Nonetheless, ecoregions differed in the relative contributions of adaptation and plasticity, from consistently greater importance of plasticity (for example, southeastern United States plains) to their nearly equal importance throughout the season (for example, Western Sierra Madre Piedmont). Our results support the hypothesis that plasticity is the primary driver of flowering-time variation along temperature gradients, with local adaptation having a widespread but comparatively limited role.

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.

Abstract: Aim: Climate affects the flowering time of many species. Little is known, however, about how climate influences the properties of regional floras, including the rate at which taxa flower sequentially throughout the flowering season. This study is the first to detect geographical variation in this rate across North America. In addition, we tested for the independent effects of intraspecific variation in flowering time and taxonomic composition on the rate of sequential flowering among regional floras distributed across a temperature gradient. Location: North America. Time period: This study examined >59,000 herbarium specimens that were collected in flower from 1901 to 2013. Major taxa studied: 2,803 angiosperm taxa. Methods: We identified 51 climatically homogeneous regions across the continental, mostly western states of the USA, in each of which ≥100 species were represented by herbarium specimens. We then examined the effects of mean annual temperature (MAT) on the rate of sequential flowering among species in each region. We also evaluated whether geographical variation in the rate of sequential flowering was attributable to intraspecific variation in the flowering time and/or the taxonomic composition of regional floras. Results: As MAT increased over space, the rate of sequential flowering (standardized by the absolute length of the flowering season in each region) increased among relatively early‐flowering taxa but decreased among the latest‐flowering taxa. Both intraspecific variation and shifts in taxonomic composition among floras contributed to this pattern. Main conclusions: Among floras throughout North America, the rate of sequential flowering among co‐occurring taxa changes with MAT. Intraspecific phenological variation primarily affects the rate of sequential flowering during the first half of the growing season, consistent with the inference that future warming will most strongly affect flowering synchrony among early‐flowering taxa.

PremiseHerbarium specimens have been used to detect climate-induced shifts in flowering time by using the day of year of collection (DOY) as a proxy for first or peak flowering date. Variation among herbarium sheets in their phenological status, however, undermines the assumption that DOY accurately represents any particular phenophase. Ignoring this variation can reduce the explanatory power of pheno-climatic models (PCMs) designed to predict the effects of climate on flowering date.MethodsHere we present a protocol for the phenological scoring of imaged herbarium specimens using an ImageJ plugin, and we introduce a quantitative metric of a specimen's phenological status, the phenological index (PI), which we use in PCMs to control for phenological variation among specimens of Streptanthus tortuosus (Brassicaceeae) when testing for the effects of climate on DOY. We demonstrate that including PI as an independent variable improves model fit.ResultsIncluding PI in PCMs increased the model R 2 relative to PCMs that excluded PI; regression coefficients for climatic parameters, however, remained constant.DiscussionOur protocol provides a simple, quantitative phenological metric for any observed plant. Including PI in PCMs increases R 2 and enables predictions of the DOY of any phenophase under any specified climatic conditions.