Ecological drivers of flower-leaf sequences: aridity and proxies for pollinator attraction select for flowering-first in the American plums.

Across temperate forests, many tree species produce flowers before their leaves emerge. This flower-leaf phenological sequence, known as hysteranthy, is generally described as an adaptation for wind pollination. However, this explanation does not address why hysteranthy is also common in biotically pollinated taxa. We quantified flower-leaf sequence variation in the American plums (Prunus, subg. Prunus sect. Prunocerasus), a clade of insect-pollinated trees, using herbaria specimens and Bayesian hierarchical modeling. We tested two common, but rarely interrogated hypotheses - that hysteranthy confers aridity tolerance and/or pollinator visibility - by modeling the associations between hysteranthy and related traits. To understand how these phenology-trait associations were sensitive to taxonomic scale and flower-leaf sequence classification, we then extended these analyses to all Prunus species in North America. Our findings across two taxonomic levels support the hypotheses that hysteranthy may help temporally partition hydraulic demand to reduce water stress and increase pollinator visibility - thereby reducing selective pressure on inflorescence size. Our results provide foundational insights into the evolution of flower-leaf sequences in the genus Prunus, with implications for understanding these patterns in biotically pollinated plants in general. Our approach suggests a path to advance these hypotheses to other clades, but teasing out drivers fully will require new experiments.

Climate change: Shifts in time between flowering and leaf-out are complex and consequential.

A new study investigated how time intervals between flowering and leaf-out in woody plants are impacted by climate change. Climate change has shifted the timing of both stages, but its impact on the interval between them is complex and variable.

Integrating experiments to predict interactive cue effects on spring phenology with warming.

Climate change has advanced plant phenology globally 4-6 d °C-1 on average. Such shifts are some of the most reported and predictable biological impacts of rising temperatures. Yet as climate change has marched on, phenological shifts have appeared muted over recent decades - failing to match simple predictions of an advancing spring with continued warming. The main hypothesis for these changing trends is that interactions between spring phenological cues - long-documented in laboratory environments - are playing a greater role in natural environments due to climate change. Here, we argue that accurately linking shifts observed in long-term data to underlying phenological cues is slowed by biases in observational studies and limited integration of insights from laboratory studies. We synthesize seven decades of laboratory experiments to quantify how phenological cue-space has been studied and how treatments compare with shifts caused by climate change. Most studies focus on one cue, limiting our ability to make accurate predictions, but some well-studied forest species offer opportunities to advance forecasting. We outline how greater integration of controlled-environment studies with long-term data could drive a new generation of laboratory experiments, built on physiological insights, that would transform our fundamental understanding of phenology and improve predictions.

A simple explanation for declining temperature sensitivity with warming.

Recently, multiple studies have reported declining phenological sensitivities (∆ days per ℃) with higher temperatures. Such observations have been used to suggest climate change is reshaping biological processes, with major implications for forecasts of future change. Here, we show that these results may simply be the outcome of using linear models to estimate nonlinear temperature responses, specifically for events that occur after a cumulative thermal threshold is met-a common model for many biological events. Corrections for the nonlinearity of temperature responses consistently remove the apparent decline. Our results show that rising temperatures combined with linear estimates based on calendar time produce the observations of declining sensitivity-without any shift in the underlying biology. Current methods may thus undermine efforts to identify when and how warming will reshape biological processes.

Spatial and temporal shifts in photoperiod with climate change.

Climate change causes both temporal (e.g. advancing spring phenology) and geographic (e.g. range expansion poleward) species shifts, which affect the photoperiod experienced at critical developmental stages ('experienced photoperiod'). As photoperiod is a common trigger of seasonal biological responses - affecting woody plant spring phenology in 87% of reviewed studies that manipulated photoperiod - shifts in experienced photoperiod may have important implications for future plant distributions and fitness. However, photoperiod has not been a focus of climate change forecasting to date, especially for early-season ('spring') events, often assumed to be driven by temperature. Synthesizing published studies, we find that impacts on experienced photoperiod from temporal shifts could be orders of magnitude larger than from spatial shifts (1.6 h of change for expected temporal vs 1 min for latitudinal shifts). Incorporating these effects into forecasts is possible by leveraging existing experimental data; we show that results from growth chamber experiments on woody plants often have data relevant for climate change impacts, and suggest that shifts in experienced photoperiod may increasingly constrain responses to additional warming. Further, combining modeling approaches and empirical work on when, where and how much photoperiod affects phenology could rapidly advance our understanding and predictions of future spatio-temporal shifts from climate change.

Reconciling competing hypotheses regarding flower-leaf sequences in temperate forests for fundamental and global change biology.

Phenology is a major component of an organism's fitness. While individual phenological events affect fitness, there is growing evidence to suggest that the relationship between events could be equally or more important. This could explain why temperate deciduous woody plants exhibit considerable variation in the order of reproductive and vegetative events, or flower-leaf sequences (FLSs). There is evidence to suggest that FLSs may be adaptive, with several competing hypotheses to explain their function. Here, we advance existing hypotheses with a new framework that accounts for quantitative FLS variation at multiple taxonomic scales using case studies from temperate forests. Our inquiry provides several major insights towards a better understanding of FLS variation. First, we show that support for FLS hypotheses is sensitive to how FLSs are defined, with quantitative definitions being the most useful for robust hypothesis testing. Second, we demonstrate that concurrent support for multiple hypotheses should be the starting point for future FLS analyses. Finally, we highlight how adopting a quantitative, intraspecific approach generates new avenues for evaluating fitness consequences of FLS variation and provides cascading benefits to improving predictions of how climate change will alter FLSs and thereby reshape plant communities and ecosystems.