skip to main content

Title: Advancing frost dates have reduced frost risk among most North American angiosperms since 1980

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.

more » « less
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Global Change Biology
Page Range / eLocation ID:
p. 165-176
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Despite a global footprint of shifts in flowering phenology in response to climate change, the reproductive consequences of these shifts are poorly understood. Furthermore, it is unknown whether altered flowering times affect plant population viability.

    We examine whether climate change‐induced earlier flowering has consequences for population persistence by incorporating reproductive losses from frost damage (a risk of early flowering) into population models of a subalpine sunflower (Helianthella quinquenervis). Using long‐term demographic data for three populations that span the species’ elevation range (8–15 years, depending on the population), we first examine how snowmelt date affects plant vital rates. To verify vital rate responses to snowmelt date experimentally, we manipulate snowmelt date with a snow removal experiment at one population. Finally, we construct stochastic population projection models and Life Table Response Experiments for each population.

    We find that populations decline (λs < 1) as snowmelt dates become earlier. Frost damage to flower buds, a consequence of climate change‐induced earlier flowering, does not contribute strongly to population declines. Instead, we find evidence that negative effects on survival, likely due to increased drought risk during longer growing seasons, drive projected population declines under earlier snowmelt dates.

    Synthesis.Shifts in flowering phenology are a conspicuous and important aspect of biological responses to climate change, but here we show that the phenology of reproductive events can be unreliable measures of threats to population persistence, even when earlier flowering is associated with substantial reproductive losses. Evidence for shifts in reproductive phenology, along with scarcer evidence that these shifts actually influence reproductive success, are valuable but can paint an incomplete and even misleading picture of plant population responses to climate change.

    more » « less
  2. Abstract

    Changes from historic weather patterns have affected the phenology of many organisms world‐wide. Altered phenology can introduce organisms to novel abiotic conditions during growth and modify species interactions, both of which could drive changes in reproduction.

    We explored how climate change can alter plant reproduction using an experiment in which we manipulated the individual and combined effects of snowmelt timing and frost exposure, and measured subsequent effects on flowering phenology, peak flower density, frost damage, pollinator visitation and reproduction of four subalpine wildflowers. Additionally, we conducted a pollen‐supplementation experiment to test whether the plants in our snowmelt and frost treatments were pollen limited for reproduction. The four plants included species flowering in early spring to mid‐summer.

    The phenology of all four species was significantly advanced, and the bloom duration was longer in the plots from which we removed snow, but with species‐specific responses to snow removal and frost exposure in terms of frost damage, flower production, pollinator visitation and reproduction. The two early blooming species showed significant signs of frost damage in both early snowmelt and frost treatments, which negatively impacted reproduction for one of the species. Further, we recorded fewer pollinators during flowering for the earliest‐blooming species in the snow removal plots. We also found lower fruit and seed set for the early blooming species in the snow removal treatment, which could be attributed to the plants growing under unfavourable abiotic conditions. However, the later‐blooming species escaped frost damage even in the plots where snow was removed, and experienced increased pollinator visitation and reproduction.

    Synthesis.This study provides insight into how plant communities could become altered due to changes in abiotic conditions, and some of the mechanisms involved. While early blooming species may be at a disadvantage under climate change, species that bloom later in the season may benefit from early snowmelt, suggesting that climate change has the potential to reshape flowering communities.

    more » « less
  3. Summary

    Phenological studies often focus on relationships between flowering date and temperature or other environmental variables. Yet in species that preform flowers, anthesis is one stage of a lengthy developmental process, and effects of temperature on flower development in the year(s) before flowering are largely unknown.

    We investigated the effects of temperature during preformation on flower development inVaccinium vitis‐idaea. Using scanning electron microscopy, we established scores for developing primordia and examined effects of air temperature, depth of soil thaw, time of year and previous stage on development.

    Onset of flower initiation depends on soil thaw, and developmental change is greatest at early stages and during the warmest months. Regardless of temperature and time during the season, all basal floral primordia pause development at the same stage before whole‐plant dormancy.

    Once primordia are initiated, development does not appear to be influenced by air temperature differences within the range of variation among our sites. There may be strong endogenous flower‐level controls over development, particularly the stage at which morphogenesis ceases before dormancy. However, the strength of such internal controls in the face of continuing temperature extremes under a changing climate is unclear.

    more » « less
  4. Phenology––the timing of life-history events––is a key trait for understanding responses of organisms to climate. The digitization and online mobilization of herbarium specimens is rapidly advancing our understanding of plant phenological response to climate and climatic change. The current common practice of manually harvesting data from individual specimens greatly restricts our ability to scale data collection to entire collections. Recent investigations have demonstrated that machine-learning models can facilitate data collection from herbarium specimens. However, present attempts have focused largely on simplistic binary coding of reproductive phenology (e.g., flowering or not). Here, we use crowd-sourced phenological data of numbers of buds, flowers, and fruits of more than 3000 specimens of six common wildflower species of the eastern United States (Anemone canadensis, A. hepatica, A. quinquefolia, Trillium erectum, T. grandiflorum, and T. undulatum} to train a model using Mask R-CNN to segment and count phenological features. A single global model was able to automate the binary coding of reproductive stage with greater than 90% accuracy. Segmenting and counting features were also successful, but accuracy varied with phenological stage and taxon. Counting buds was significantly more accurate than flowers or fruits. Moreover, botanical experts provided more reliable data than either crowd-sourcers or our Mask R-CNN model, highlighting the importance of high-quality human training data. Finally, we also demonstrated the transferability of our model to automated phenophase detection and counting of the three Trillium species, which have large and conspicuously-shaped reproductive organs. These results highlight the promise of our two-phase crowd-sourcing and machine-learning pipeline to segment and count reproductive features of herbarium specimens, providing high-quality data with which to study responses of plants to ongoing climatic change. 
    more » « less
  5. Premise of the Study

    New growth in the spring requires resource mobilization in the vascular system at a time when xylem and phloem function are often reduced in seasonally cold climates. As a result, the timing of leaf out and/or flowering could depend on when the vascular system resumes normal function in the spring. This study investigated whether flowering time is influenced by vascular phenology in plants that flower precociously before they have leaves.


    Flower, leaf, and vascular phenology were monitored in pairs of precocious and non‐precocious congeners. Differences in resource allocation were quantified by measuring bud dry mass and water content throughout the year, floral hydration was modelled, and a girdling treatment completed on branches in the field.

    Key Results

    Precocious flowering species invested more in floral buds the year before flowering than did their non‐precocious congeners, thus mobilizing less water in the spring, which allowed flowering before new vessel maturation.


    A shift in the timing of resource allocation in precocious flowering plants allowed them to flower before the production of mature vessels and minimized the significance of seasonal changes in vascular function to their flowering phenology. The low investment required to complete floral development in the spring when the plant vascular system is often compromised could explain why flowers can emerge before leaf out.

    more » « less