Divergent responses to spring and winter warming drive community level flowering trends

Abstract

Analyses of datasets throughout the temperate midlatitude regions show a widespread tendency for species to advance their springtime phenology, consistent with warming trends over the past 20-50 y. Within these general trends toward earlier spring, however, are species that either have insignificant trends or have delayed their timing. Various explanations have been offered to explain this apparent nonresponsiveness to warming, including the influence of other abiotic cues (e.g., photoperiod) or reductions in fall/winter chilling (vernalization). Few studies, however, have explicitly attributed the historical trends of nonresponding species to any specific factor. Here, we analyzed long-term data on phenology and seasonal temperatures from 490 species on two continents and demonstrate that (i) apparent nonresponders are indeed responding to warming, but their responses to fall/winter and spring warming are opposite in sign and of similar magnitude; (ii) observed trends in first flowering date depend strongly on the magnitude of a given species' response to fall/winter vs. spring warming; and (iii) inclusion of fall/winter temperature cues strongly improves hindcast model predictions of long-term flowering trends compared with models with spring warming only. With a few notable exceptions, climate change research has focused on the overall mean trend toward phenological advance, minimizing discussion of apparently nonresponding species. Our results illuminate an understudied source of complexity in wild species responses and support the need for models incorporating diverse environmental cues to improve predictability of community level responses to anthropogenic climate change.

Fig. 1.

Change (temporal trend) in FFD within four response categories at Chinnor. Plant species at Chinnor fall into four categories of observed seasonal temperature responses that covary with the species’ long-term trends in FFD over time: species that respond to spring warming only (spring-only responders, n = 275 species), species with both significant spring warming and fall/winter vernalization sensitivities (divergent responders, n = 70 species), species with fall/winter vernalization sensitivity only (vern-only, n = 14 species), and species with no significant climate sensitivity (non-resp, n = 25 species). Observed changes in FFD over time (x axis, trend in d⋅y⁻¹) are negative for species that have advanced their spring FFD and positive for species that have delayed their spring FFD. (A) Normalized histogram for each response category. (B) Empirical cumulative distribution function for each response category.

Fig. 2.

Spring warming sensitivities for spring-only (green) and divergent (blue) responders. Normalized histograms compare the magnitude of spring warming sensitivities between the spring-only (green line) and divergent (blue line) responders. Because the climate predictors are standardized to zero mean and unit SD (Z-score), sensitivity units are in days per Z-score deviation. Mean spring warming sensitivities are not significantly different (P = 0.51; Table S2) between the spring-only and divergent species: −6.4 d⋅Z⁻¹ for spring-only responders and −6.7 d⋅Z⁻¹ for divergent responders. Results indicate that spring-only and divergent responders are equally sensitive and responsive to spring warmth.

Fig. 3.

Vernalization vs. spring warming sensitivities for divergent responders (n = 70 species categorized as divergent responders based on P value criteria in the Chinnor dataset). (A) Each species from the divergent responders group is represented by two dots: one blue dot for the magnitude of its vernalization sensitivity and one green dot for the magnitude of its spring warming sensitivity. Negative values indicate that warming advances FFD, and positive values indicate that warming delays FFD (y axis). Mean FFD for each species (day of year) is shown (x axis). The absolute magnitudes of the spring and vernalization (fall/winter) temperature sensitivities tend to decrease with later mean FFD, suggesting earlier flowering species are more sensitive to external climate forcing. (B) Estimated vernalization (x axis) and spring warming (y axis) sensitivities for each of the 70 divergent species. The dashed line indicates the 1:1 line, and the y axis is reversed. The preponderance of circles above the dashed line indicates that spring warming sensitivities generally are stronger (have greater absolute magnitude) than fall/winter vernalization sensitivities.

Fig. 4.

Observed and modeled FFD trends (d⋅y⁻¹) for the 70 divergent responders at Chinnor. Observed trends in FFD are colored gray, modeled FFD trends using only spring warming sensitivities are colored green, and modeled FFD trends using spring warming and vernalization sensitivities are colored blue (n = 70 species). The observed trends are centered on zero, and trends for the models incorporating vernalization sensitivity are similarly centered. If only the spring warming predictors are considered for these species, modeled trends are biased negative, predicting a general advance in the timing of FFD that is at odds with the observations. Including vernalization sensitivity as well as spring warming sensitivity improves the ability of the model to reproduce the observed temporal FFD trends.