Wildflower phenological escape differs by continent and spring temperature

We used a hierarchical Bayesian modeling approach to evaluate the relationship between the spring phenology of tree and wildflower species and various climate drivers (see Methods). Following model selection, our final model structure included fixed effects of average spring (March–April) temperature and elevation, as well as species-level random effects. We show continental distributions of spring temperature values in Fig. 1b (means and standard deviations are listed in Table S2). We report estimates for spring temperature sensitivities from the final model structure in the main text. Parameter estimates for elevation sensitivities as well as the model performance of other potential drivers and combinations of drivers are reported in Tables S3 and S4. An extended discussion of model assumptions and limitations is included in the Supplementary Information.

Sensitivity differences by strata

Tree leaf out phenology (LOD) was substantially more sensitive to average spring temperature in North America (mean = −3.62 days °C⁻¹; 95% credible interval (CI) = [−3.76, −3.49]) than in Europe (mean = −2.79; CI = [−3.27, −2.30]) and Asia (mean = −2.62; CI = [−2.97, −2.26]; Fig. 2). These values are consistent with previously reported phenological sensitivities in North America⁷ (−5.5 to −3.3 days °C⁻¹) and Europe⁸ (−4.1 to −3.0 days °C⁻¹), as the credible intervals from our results overlap with the reported credible intervals of prior studies. However, the Asian LOD sensitivity was less sensitive than previously reported²⁷ (−3.50 to −3.03 days °C⁻¹), potentially owing to differences in species selection²⁸ or model structure. Previously reported sensitivities were determined in separate studies using either observational data^7,8 or long-term observation-based weather station data²⁷. The general consistency between our findings suggests that phenology data from herbarium collections are good indicators of patterns in natural systems^29,30,31, a point supported by a recent study of phenological sensitivity derived from herbaria and from observed citizen science data³². These herbarium-based results provide evidence that phenological sensitivity differs across the temperate forest biome (but see ref. 33 for evidence of differences in response to warming and chilling accumulation). To our knowledge, our study is the first to contrast overstory and understory phenology across multiple continents and, therefore, to find differences in phenological sensitivity between trees and forest wildflowers across continents. We recommend future studies explore these differences using alternative approaches and methodologies that focus on the physiological basis for and mechanisms that underlie these patterns.

In contrast to trees, wildflower sensitivity to spring temperature was similar across all three continents and exhibited no strong differences (i.e., overlap in 95% Bayesian credible intervals) among continents (means and 95% credible intervals in brackets: North America = −3.14, [−3.28, −3.00]; Europe = −3.02, [−3.48, −2.56]; Asia = −3.12, [−3.36, −2.86]; Fig. 2). These values are also generally consistent with those reported elsewhere in the literature (i.e., 95% credible intervals overlap with those reported in other studies; −2.2, [−3.7, −0.76] days °C⁻¹ in North America⁷ and −3.6, [−4.04, −3.18] days °C⁻¹ in Europe⁹), although we are unaware of any studies that have estimated phenological sensitivity for Asian forest wildflowers in days °C⁻¹. Ge et al.³ report herbaceous plant sensitivity of −5.71 days per decade in Asia (±7.90 standard deviation; based primarily on long-term observational data), which appears to be roughly consistent with our model results, but the difference in units makes this more speculative than the other comparisons. Discrepancies in mean responses between this study and others may be due in part to different types of data (herbarium specimens versus field observations) and to choice in focal taxa, as temperature sensitivity has been shown to vary widely across taxa²⁸.

Particularly noticeable in our results was that r² coefficients of predicted versus observed phenology were much higher in North America (0.70 and 0.76 for wildflower and tree models, respectively) compared to Asian (0.40 and 0.44, respectively) and European models (0.41 and 0.25, respectively). This difference in model performance could be due to the higher interannual variability of spring temperatures in North America³³, leading to greater selective pressure for strong sensitivity to spring temperatures in North American plants. This difference could explain why North American species exhibit higher correlation of phenology with average spring temperatures (Table S4). Alternatively, European and Asian species may have stronger phenological responses to alternative spring forcing windows, winter chilling temperatures, or photoperiod, relative to the March–April temperature period used in this study (see Methods). We think the latter explanation is unlikely, given the strong correlations of phenology with spring temperature across all continents (see Supplementary Information – Justification for March–April Temperature Window).

Herbarium-based phenological models may be improved by accounting for spatial autocorrelation within the dataset. For example, Willems et al.⁹ found that including spatial autocorrelation significantly improved predictability of European herbaceous flowering phenology, even when accounting for multiple drivers of spring phenology. We followed a similar approach as their study and found similar improvements in model performance with the addition of spatial autocorrelation (Tables S3–S4) that had substantial positive effects on r² values of Asian and European models. However, spatial distributions of specimens differed substantially among continents (see Figs. S2–S4), and these differences could lead to artifacts that make results unreliable to interpret (see Supplementary Information). Therefore, we focus here on results for models without spatial autocorrelation while acknowledging that spatial aggregation of herbarium specimens in Europe and Asia may be partially responsible for the relatively lower r² values. We encourage other researchers to explore this question further both with our data set and other datasets.

Climate change and spring light windows

The relative difference between wildflower and tree sensitivity varied substantially among continents, with wildflowers being approximately equally as sensitive to spring temperature as trees in Asia and Europe but substantially less sensitive (i.e., 95% BCI do not overlap) than trees in North America (Fig. 2). Importantly, these differences were driven by changes in tree phenological sensitivities among continents and resulted in different expectations for spring light window duration (i.e., the difference in time between estimated wildflower flowering date and canopy tree leaf out date) on different continents under current climate conditions (Fig. 3), based on modeled leaf out and flowering under a climate scenario derived from average climate conditions from 2009–2018 (Fig. S5).

Interestingly, the time between leaf out and flowering in North America is greater in the north than in the south (Fig. 3c), indicating a greater spring light window duration at higher latitudes. In addition, although there was regional variation in spring light window duration on each continent, there was broad overlap in duration among continents estimated under current environmental conditions (North America light window duration averages 11.7 ± 4.1 s.d. days; European duration averages 14.7 ± 3.0 s.d. days; and Asian duration averages 8.0 ± 4.6 s.d. days). This suggests that, under current climate conditions, wildflowers across all continents experience similar length of spring light windows, but the impact of warming on shrinking or expanding window size will differ among continents with uncertain impacts on wildflower populations.

Still, differences among continents resulted in different projections for how spring light window duration will respond to climate change over the coming century (Fig. 4), which will likely have implications for understory plant demography^7,12,13,16. We used climate change projections for 2081–2100 (assuming an extreme climate change scenario; Institut Pierre‐Simon Laplace CM6A-LR climate model – shared socioeconomic pathway 585; see Methods for more details) to forecast wildflower flowering date and canopy tree leaf-out date for the end of the current century (Fig. S6) and then calculated the difference between forecasted wildflower flowering and tree leaf out phenology for the period of 2081–2100 (future spring light window duration; Fig. S7). To estimate the change in spring light window duration between now and the end of the century (Fig. 4), we subtracted the forecasted future light window duration from the modeled light window duration under current climate conditions.

Dramatic differences in the projected change in spring light window duration emerged, ranging from increasing spring light window durations for wildflowers in Asia, to minimal change in spring light window length in Europe, to decreasing spring light window length in North America. Importantly, these differences in phenological escape trajectories are primarily attributable to differences in phenological sensitivities between overstory and understory species and not to differences in projected spring temperature changes among continents. Projected changes in March–April temperature broadly overlapped across continents (mean ± s.d. of projected change in spring temperature is 5.41 ± 1.87 °C, 6.36 ± 2.36 °C, and 5.04 ± 2.92 °C in Asia, Europe, and North America, respectively; Fig. S8). Intracontinental differences, however, such as the more extreme projected changes in phenological escape in the northern regions of each continent, are due to gradients of projected spring temperature change across latitudes, with higher latitude regions expected to experience greater spring warming relative to lower latitudes^34,35.

The North American results are consistent with findings from a previous study that similarly predicted reduction in access to spring light at a single site in the U.S. Northeast⁷. Although no previous studies have specifically addressed phenological escape in Asia, our results are consistent with previous research that found higher sensitivity to spring temperature for Asian herbaceous plants compared to Asian woody trees and shrubs³. Similarly, we are not aware of European studies that have directly compared phenological sensitivity between wildflowers and trees nor that have quantified phenological escape, but our estimates of sensitivity are consistent with previously reported values^8,9. Together, this supports our conclusion that the duration of spring light windows will be differently affected by climate change on different continents.

Importantly, it is impossible to fully measure the ecological and demographic implications of these results using herbarium specimens. Linking changing access to light to changes in photosynthetic carbon assimilation, growth, and survival necessitates the use of experimental studies of living specimens such as those previously conducted in eastern North America^7,12,13,16. Previous studies that have done so have linked access to spring light before canopy closure with the growth^{10,12,17,18,19}, survival^12,18,19,20, flowering^17,20, and reproductive output^10,17,21,22 of understory plant species. This large body of research suggests that reductions in access to spring light can have negative ramifications for the demographic success of understory species.

For example, projected reductions of several days in phenological escape may not intuitively seem like much, but the spring ephemeral wildflowers in this study have growing seasons that last only 3–5 weeks. A decrease in one day of phenological escape can therefore be as much as a 4% loss of total growing season length. In a study of phenological escape in sugar maple seedlings, Kwit et al.¹⁴ found that increasing access to spring light by three days could increase photosynthetic carbon assimilation by more than 50%, an amount that other studies suggest would substantially increase annual growth and probability of survival^12,13. For spring ephemeral herbaceous plants, Heberling et al.¹⁶ showed that a similar three-day loss in access to spring light resulted in up to a 30% loss in spring carbon assimilation. It is important to note, however, that the exact impacts of change in phenological escape on plant performance in Asia and Europe remains to be directly measured.

Thus, although our results suggest strong differences in change in performance when assuming the minimal differences in photosynthetic rates among species on different continents, it is possible that systematic intercontinental differences could lead to different outcomes. For example, if spring wildflowers were to be shown to have much lower spring photosynthetic rates, differences in projected access to light could have much less impact on overall carbon assimilation and demographic performance. Still, others have found relatively strong relationships between spring light availability and understory plant performance on other continents²¹, suggesting that photosynthetic rates are similar enough to be comparable in this study. Therefore, we conclude that the relatively small changes in spring light availability projected here are likely to have substantial ecological consequences for the performance and demography of understory plant species.

The future for spring ephemerals

The herbaceous layer accounts for more than 80% of plant species in temperate forests worldwide³⁶ and provides a critical role in the functioning of these ecosystems³⁷. Understory wildflower species face many threats that include deer herbivory^38,39,40, habitat loss⁴¹, pollinator declines⁴² and mismatch^43,44, presence of nonnative, invasive plants^45,46, and nutrient pollution^47,48. Furthermore, there is substantial evidence that many of these species are limited in their dispersal ability^41,49 and populations are likely unable to shift their distributions as rapidly as regional climates are predicted to warm. Our results show that mismatch between understory and overstory phenology, specifically in North America, is another concern for this already threatened group^36,50. Reductions in spring light windows will likely lead to reduced carbon gains each year for spring forest wildflowers^7,16, which may ultimately lead to population decline as plant fitness declines. Therefore, we highlight the need for future conservation efforts to consider the impact of loss of spring light in restoration planning, with simultaneous studies of overstory and understory responses together³⁷. Furthermore, this information may assist conservation practitioners in their decisions of where to focus management or conservation efforts based on projected changes to future forest ecosystems.

The patterns examined in this study point to distinctions in plant phenological responses among continents, but they cannot provide a mechanistic explanation for why these differences exist. Wildflowers and trees advance their phenology with warming spring temperatures, for example, but why are North American trees more responsive than co-occurring wildflower species to warming? Some speculate it is because perennial wildflowers overwinter underground whereas tree buds overwinter aboveground; trees may therefore be more affected by air temperature relative to wildflowers^10,11. Although global soil and near-surface temperature data are recently becoming available⁵¹, there are as yet no historical estimates of soil temperatures for use in herbarium studies. Thus, future empirical studies will be needed to directly test this theory. Similarly, what are the mechanisms that allow North American trees to be more sensitive to spring temperature than trees in Europe and Asia? Studies using dormant twigs, potted seedlings, and trees growing in botanical gardens are possible methods for investigating this. Common garden experiments with manipulated treatments may provide a more mechanistic understanding of our observations, including to rule out potentially confounding variables such as intercontinental differences in soil properties, precipitation, and photoperiod.

Other recent research highlights the growing need to assess the potential for nonlinear phenological responses to spring warming. As reviewed by Wolkovich et al.⁵², future phenological responses to spring warming may be nonlinear owing to a number of reasons (including threshold responses to extreme environmental conditions and interactions among drivers besides spring forcing). Accounting for factors that might drive nonlinearities in plant phenological response to warming will necessitate controlled experiments^52,53, which was not possible with the observational herbarium dataset used in our study. We did not find evidence for nonlinear responses to spring temperature, but we acknowledge that experimental studies that can experimentally manipulate and test for the impacts of spring forcing, winter chilling, and photoperiodic effects on plant phenology could further illuminate how nonlinearity affects phenological escape. Also, nonlinear responses may become more evident in the future if extreme weather conditions occur more frequently.

Our study represents an early attempt to address phenological questions using herbarium specimens at the intercontinental level. Digitization of herbarium specimens and other historical data and citizen science programs like iNaturalist and iSpot are making data increasingly available and enabling new research⁵⁴. Additional research that utilizes international herbaria and collaborations to synthesize these data at a global scale will aid in addressing pressing ecological and climate change questions.

In sum, our results indicate that spring ephemeral wildflowers are similarly sensitive to spring warming across temperate forests in Asia, Europe, and North America, but that deciduous canopy trees in North America are more sensitive to spring warming compared to trees on the other two continents. Furthermore, differences in tree leaf-out sensitivity mean that North American wildflowers are projected to experience decreasing access to spring light under climate change conditions, whereas those in Asia and Europe are unlikely to experience substantial gains or losses in spring light availability. These intercontinental differences suggest that climate change may adversely affect spring ephemerals in North America more than on the other two continents, and thus that North American wildflowers may be especially threatened by warming springs.

Source: Ecology - nature.com