Introduction

Forests can seem like static natural cathedrals, but these ecosystems are constantly changing—year to year and season to season. Seasonal change is perhaps best exemplified in temperate deciduous forests, which are governed so much by differences in environmental conditions that we use terms associated with plant life cycles such as “growing season” and “[leaf] fall” interchangeably with “summer” and “autumn.” Importantly, the timing of these seasonal life history events, which is generally referred to as phenology (see “Glossary”), varies over years in response to interannual variation in the environmental conditions that cue it.

This variation in phenology has many important effects on individual-, population-, and community-level plant performances, largely through overlap in resource availability and activity periods with other plants and animals (here and throughout, we define activity period as the duration of all aboveground activity, particularly photosynthesis in green tissues, but including flowering, fruiting, and activity of nonplants, such as flower visitation by pollinators). For the former, plants are often adapted such that their activity overlaps strongly with the availability of critical resources while often avoiding activity during particularly stressful periods. Deciduous species, for example, are primarily active in spring and summer, when they can minimize frost damage and optimize access to soil nutrient pools, liquid water, and temperatures suitable for maintaining active photosynthesis. Initiating activity too early can lead to damage from frost that stunts growth and reduces reproductive success (Vitasse et al. 2014; Augspurger and Salk 2017), whereas waiting too long in spring to initiate the growing season can lead to suboptimal carbon assimilation as a result of a competitive disadvantage for limiting resources (Kwit et al. 2010; Lee and Ibáñez 2021b). Mismatch between plants and critical resources can thus play a large role in governing ecological processes ranging from intraspecific demography to interspecific coexistence (Visser and Gienapp 2019).

Phenological mismatch (see “Glossary”) specifically describes asynchrony in the timing of biotic interactions and implies a deviation from average or evolved interactions. This typically (but not always) implies a negative fitness consequence for at least one of the interacting organisms. As reviewed by Renner and Zohner (2018), David Cushing (1990) initially used this term to describe a lack of synchrony in activity between Arctic cod larvae and their planktonic food source. Since then, it has been used to describe phenological asynchrony between predator and prey (Damien and Tougeron 2019), between producer and consumer (Kharouba and Wolkovich 2020), between plants and pollinators (Kudo and Ida 2013; Gérard et al. 2020), and between competitors (Nakazawa and Doi 2012; Stenseth et al. 2015; Visser and Gienapp 2019; Labonté et al. 2023). However, studies of plant phenological mismatch have focused predominantly on plant interactions with animals as either consumers or pollinators. Plant-plant mismatch is often studied only in the context of indirect competition for pollinators (e.g., Anderson and Schelfhout 1980; Labonté et al. 2023).

Over the past decade, several studies have begun to highlight the ways in which direct plant-plant interactions (primarily reproduction and competition) are affected by phenological asynchrony. For example, a mismatch between male and female individuals of dioecious species could affect reproductive success under increased asynchrony (Forrest 2014; Yang et al. 2022). Furthermore, high variability in phenology within populations of wind-pollinated plants has been directly linked to reduced reproductive success (Koenig et al. 2012), suggesting that flowering phenology in such species is subject to strong stabilizing selection. These case studies provide initial evidence that seed set and fruit production can be directly affected by asynchrony between plants, irrespective of plant-pollinator interactions.

Several reviews have previously described in great detail various types of phenological mismatch and how they affect plant communities (Wolkovich and Cleland 2011; Visser and Gienapp 2019). In this primer, we focus on evidence for a specific type of niche partitioning that is absent from previous reviews on phenological mismatch but that has been recently implicated as likely to be negatively affected by future climate change. This ecological strategy, called phenological escape (see “Glossary”; Jacques et al. 2015; Heberling et al. 2019b; Lee and Ibáñez 2021a, 2021b), refers to understory plants avoiding shade to gain access to light by emerging earlier than canopy trees in temperate deciduous forests. That is, by occupying a different temporal niche than canopy trees, understory plants escape summer shady periods to improve their photosynthetic performance. Understory plants emerge and/or leaf out up to several weeks before nearby canopy trees so as to assimilate 50%–100% of their annual carbon budgets in early spring prior to being shaded out (Kwit et al. 2010; Heberling et al. 2019a; Lee and Ibáñez 2021b), and access to this ephemeral resource is strongly implicated as affecting various metrics of plant performance, such as growth, survival, and reproductive success (Kudo et al. 2008; Kwit et al. 2010; Heberling et al. 2019b; Lee and Ibáñez 2021a, 2021b). Access to spring light is projected to change because of differences in phenological sensitivity (see “Glossary”) to various environmental forcing cues between understory plants and co-occurring canopy trees (Heberling et al. 2019b; Lee and Ibáñez 2021a; Lee et al. 2022), suggesting that it is a prime candidate for current and future phenological mismatches. Here, we describe (i) the physiological importance of access to early spring light for understory plant species, (ii) the causes of shifts in canopy and understory phenology and the consequences to access to light, and (iii) the ecological implications for changing phenological escape as a case study in phenological mismatch, particularly within the context of projected climate change.

Physiological Importance of Access to Spring Light Availability

Ecosystems are often defined by the resource limitations that shape plant communities, with mean temperature, temperature variability, and water availability being the predominant drivers. In that sense, temperate deciduous forests are defined by their seasonality and the broad range of environmental conditions that they are exposed to over the course of a given year. Different types of deciduous forests exist (e.g., the dry-season deciduous forests in Central and South America), but deciduous species in temperate forests are most often cold deciduous, meaning that they senesce their leaves at the end of summer and remain dormant through a cold, wet winter.

Understory herbaceous plant species are extremely biodiverse in temperate forests, with one recent paper estimating that they comprise around 80% of the total plant biodiversity in North American temperate forests (Spicer et al. 2020). To this point, some temperate North American forests have been shown to have up to 10 times more species in the herbaceous understory layer than in the canopy (Gilliam 2007). Understory plants vary widely in their phenological strategies. These diverse strategies provide an important aspect of niche differences across species that presumably promote coexistence and high diversity of herbaceous species on the forest floor (Gilliam 2007). A striking feature of the herbaceous layer in many deciduous forests is that one encounters different species from month to month, making a single midseason survey far from a complete inventory of all species present. Ranging from plants active for only a few weeks to evergreen plants that maintain green aboveground tissue year round, understory plants are often categorized into phenological syndromes (see “Glossary”) that include groups such as spring ephemeral (leaves die back before tree canopy leaves flush), summer green (maintain green leaves through summer), wintergreen (leaves produced in fall or winter), and evergreen (leaves last longer than 1 yr; Uemura 1994; Neufeld and Young 2014). It is important to note that while these discrete groupings are useful, there is considerable diversity within phenological syndromes across a complex continuum of leaf strategies and phenological traits, including, for example, some species that produce overwintering rosettes or multiple leaf flushes. Of particular importance to phenological escape are winter-deciduous species that leaf out in early spring, when access to direct sunlight is high and risk of damage from frost is reduced. This group includes species that are active aboveground only specifically during this period (spring ephemerals; sensu Yancy et al. 2024) as well as species that maintain their aboveground activity later into the growing season (including spring-active wildflowers and seedlings and saplings of many temperate deciduous tree species). Most spring ephemerals are perennial and store carbon in belowground rooting structures during dormancy (Lubbers and Lechowicz 1989; Lapointe and Lerat 2006). However, there is at least one exception to this, which is the annual spring ephemeral Floerkea proserpinacoides (McKenna and Houle 2000).

For temperate deciduous plants, especially trees, budburst and leaf expansion are primarily cued by three environmental drivers (Richardson et al. 2006; Ettinger et al. 2020; Buonaiuto and Wolkovich 2021): spring temperature forcing (the accumulation of warm temperature exposure above some critical threshold), winter chilling (sometimes referred to as vernalization effects; the accumulation of cold temperature below a critical threshold while in dormancy), and photoperiod (daylength). Additionally, many spring-active and spring ephemeral wildflower species have shallow roots and rhizomes that are sensitive to soil moisture and temperature, which is less variable than air temperature. In high-latitude or high-elevation montane systems, understory emergence and flowering phenology may instead be correlated primarily with the timing of snowmelt and the associated increase in temperatures that normally accompany it (e.g., Anderson et al. 2012). Importantly, however, deciduous forest canopies are rare in these systems, so there may be less ephemeral light available for understory wildflowers to utilize. The role of soil moisture on plant phenology is not well established for temperate deciduous forests, especially in the mesic forests that harbor much of the herbaceous diversity in temperate forests.

Spring temperature forcing is an important signal for two primary reasons. First, accumulation of warm temperatures signals a reduction in risk from late-winter and early-spring frost events, which can greatly reduce the survival and reproductive performance of deciduous plant species active during this period (Inouye 2008; Augspurger 2009; Vitasse et al. 2014; Gezon et al. 2016; Park et al. 2021). Second, photosynthetic rates scale nonlinearly with temperature (Caemmerer 2000), and accumulation of spring forcing temperatures signals to plants that conditions are sufficient to photosynthesize at or near peak efficiency: too cold and photosynthesis is inhibited by lack of energy and inaccessible soil water (Ensminger et al. 2008), but too warm and net carbon gain becomes inhibited by disproportionately elevated respiration rates relative to concurrent increases in photosynthetic rates (Caemmerer 2000; Lee and Ibáñez 2021b).

In addition to temperature, photosynthetic carbon assimilation in temperate deciduous forests is often also inhibited by insufficient access to light. Understory light levels can decrease by up to three orders of magnitude once canopy trees expand their leaves (fig. 1; Augspurger et al. 2005; Jacques et al. 2015; Lee and Ibáñez 2021b). In contrast to understory conditions, however, canopy trees are rarely light limited throughout the growing season and can therefore afford to be relatively conservative with their foliar phenology, prioritizing avoidance of frost damage (Seiwa 1999). Their conservative strategy means that they delay their leaf expansion several weeks after environmental conditions are initially suitable, providing a window of opportunity for understory plant species to exploit elevated understory light levels (Neufeld and Young 2014; Augspurger and Salk 2017).

By leafing out before the canopy closes, spring-active understory plant species are able to assimilate between 50% and 100% of their annual aboveground carbon budget in as little as 3–4 wk (Kwit et al. 2010; Heberling et al. 2019a; Lee and Ibáñez 2021b). This is especially true for spring ephemeral wildflowers (Heberling et al. 2019a), which are characterized by completion of aboveground activity prior to canopy leaf out (Yancy et al. 2024). This group always assimilates 100% of its aboveground carbon budget in early spring and is therefore expected to be highly sensitive to interannual variation in the duration of spring light windows (fig. 2; Neufeld and Young 2014; Heberling et al. 2019b; Lee et al. 2022). Still, spring-active understory plants have been shown to strongly rely on this period of time regardless of their growing season length. For example, temperate tree seedlings that have 7–8-mo-long growing seasons still assimilate 50%–80% of their annual carbon budgets within an early light availability window that is only 2–3 wk long (Kwit et al. 2010; Lee and Ibáñez 2021b). Additionally, even understory herbaceous species that retain leaves well into summer (summer greens; fig. 2) rely on this early-spring high light window for photosynthesis (e.g., Arisaema triphyllum [Jack-in-the-pulpit] assimilates >40% of annual carbon through spring photosynthesis; Heberling et al. 2019a).

Spring-active deciduous plants are often adapted to maintain extremely high photosynthetic rates during this early period of high light availability (Sparling 1967; Taylor and Pearcy 1976; Lapointe 2001). For example, Kudo et al. (2008) used high photosynthetic rates to define a spring-blooming phenological syndrome, further noting that access to spring light was directly and positively correlated with fruiting success in understory wildflower species. Elevated photosynthetic efficiency was also recorded for the spring ephemeral Claytonia virginica (Virginia spring beauty; Heberling et al. 2019a), with maximum photosynthetic rates that were substantially higher than observed rates for spring-active (but not ephemeral) wildflower species. Importantly, spring ephemeral wildflowers tend to be shade avoiders as opposed to shade tolerators (sensu Rothstein and Zak 2001) and thus show limited ability to acclimate to shady conditions (Eickmeier and Schussler 1993). Instead, these species senesce their leaves as the canopy closes above them.

In contrast, species that employ phenological escape while also maintaining leaves later into the growing season often demonstrate the capacity to maintain high photosynthetic rates in early spring before downregulating their photosynthetic machinery in the shady part of the growing season. This has been demonstrated broadly in nonephemeral herbaceous wildflower species (Ida and Kudo 2008; Heberling et al. 2019a) but more commonly studied in spring-active woody plant species. For example, Lee and Ibáñez (2021a) recorded a pronounced shift to more shade-tolerant photosynthetic rates (e.g., lower maxima coupled with lower light compensation points to better efficiency in low light conditions) for temperate deciduous tree seedlings, with reductions in overall capacity associated with corresponding reductions in respiration demand. Similar acclimation has been demonstrated in other tree seedlings (Augspurger et al. 2005; Kwit et al. 2010; Peltier and Ibáñez 2015), saplings and understory trees (Gill et al. 1998; Augspurger et al. 2005), and shrubs (Gill et al. 1998; Xu et al. 2007; Martinez and Fridley 2018), suggesting that seasonal regulation of photosynthesis is an important adaptation for deciduous understory species in general and woody understory species in particular (Valladares and Niinemets 2008).

So far in this primer, we have focused on evidence for how access to spring light affects photosynthetic carbon assimilation, but it is important to also address how changes in spring carbon assimilation translate to individual plant performance and population-level demography. Although this is a growing area of research with a limited number of studies, there are studies that both directly and indirectly relate phenological escape to individual metrics of plant performance. The main direct evidence comes from Lee and Ibáñez (2021a), who directly related tree seedling phenology and access to spring light to photosynthetic carbon assimilation and individual-based metrics of growth and survival. Specifically, they found that earlier seedling leaf expansion (and thus greater access to spring light) was significantly positively correlated with both spring and annual carbon accumulation. Carbon accumulation was, in turn, then positively correlated with annual growth and probability of survival.

To our knowledge, only one study has mechanistically linked wildflower performance to spring carbon assimilation. Lapointe (1998) demonstrated that spring-active Trillium erectum was able to successfully reproduce solely from carbohydrates assimilated during spring photosynthesis without relying on carbon stored in belowground tissue. Although this study did not include variation in spring light availability as an experimental treatment, other studies have directly linked phenological escape to wildflower carbon assimilation in spring (Heberling et al. 2019a). Another study related leaf-level gas exchange to wildflower phenology and reproductive performance (Jacques et al. 2015) but did not compute individual aboveground carbon budgets as part of the analysis. Other studies found important relationships between spring shade avoidance and wildflower reproductive success (Kudo et al. 2008) even within species (albeit without direct measurement or estimation of carbon gain; Routhier and Lapointe 2002), thereby supporting the hypothesis that phenological escape is important for maintaining natural populations of spring wildflowers. Furthermore, Routhier and Lapointe (2002) hypothesized that a latitudinal difference in the duration between understory emergence and tree leaf out, where the window duration increased with latitude, may explain the relative geographic distribution of species with the spring ephemeral strategy. That is, the authors predicted that longer spring light windows in the north could be at least partially responsible for spring wildflower southern range limits.

Most recently, Yancy et al. (2024) found important biogeographic and environmental drivers of spring ephemeral wildflower distributions across eastern North America. Results from their work suggest that phenological escape dynamics can also affect species distributions and long-term population persistence across the landscape. Specifically, “true” spring ephemeral wildflowers (those that completed 100% of their aboveground activity prior to canopy closure) were found to be most abundant at central latitudes in eastern North American forests. This pattern of reduced ephemeral abundance in the northern and southern regions of the temperate forest biome is likely indicative of a combination of drivers. More frequent and severe frost events could reduce spring wildflower success in the north and at higher elevations, while earlier canopy closure and longer tree growing seasons in the south could restrict the ability for understory plants to avoid canopy shade (Yancy et al. 2024). Furthermore, northern distributions of many species are likely to be affected by the history of glaciation in North America and by species-level dispersal rates following glacier recession (Vellend et al. 2003). Still, the results from Yancy et al. (2024) suggest that up to one in every five understory wildflower species in eastern North America is categorized as spring ephemeral (and therefore as strongly reliant on phenological escape) in at least part of its range.

In sum, phenological escape provides a mechanism by which a wide variety of spring-active deciduous plant species obtain enough energy to grow, survive, and reproduce. Species ranging from deciduous tree seedlings to spring ephemeral wildflowers rely on elevated access to light in early spring to assimilate 50%–100% of their annual carbon budgets. There is both direct and indirect evidence that their capacity to do so determines individual performance metrics such as growth, probability of survival, and reproductive success. Recent evidence further suggests that a wide diversity of understory wildflowers in North America relies on phenological escape, especially at central latitudes. In the next section, we discuss how access to spring light is expected to change as a direct result of climate change.

Climate Change Effects on Phenological Escape

Shifts in plant phenology are some of the most common and intuitive signals of climate change, with some phenology datasets dating back several centuries (e.g., Aono 2015). We now have decades of research showing that the start of season phenology of Northern Hemisphere temperate tree species is shifting earlier (Menzel and Fabian 1999; Parmesan and Yohe 2003; Menzel et al. 2006; Piao et al. 2019) and that these shifts correlate strongly with warmer spring temperatures (Menzel et al. 2006; Ettinger et al. 2020). Climate change is therefore altering the initiation (and sometimes the duration) of growing seasons for temperate tree species (Linderholm 2006; Song et al. 2009), at least as recorded for mature canopy trees. Until recently, however, the responsiveness of understory plant phenology to environmental variation was largely unstudied. That is, as illustrated in figure 3, temperate forest canopies were closing earlier in the year, but it was unknown whether deciduous understory species were shifting at the same rate.

Recently, several studies have sought to address this gap in the literature using different types of data and for different groups of understory species. The first of these studies was conducted by Heberling et al. (2019b) using historical observations dating back ∼170 yr. The authors of this paper compared the phenological sensitivity of a suite of spring-blooming wildflower species to that of co-occurring canopy tree species in the state of Massachusetts. By using comparisons to more recent datasets, the authors found that wildflower species were less sensitive to changes in temperature than tree species, resulting in a 7-d reduction in access to spring light for wildflower species from 1852 to 2018. Furthermore, using an extreme climate change projection for the year 2080, they predicted that wildflower access to spring light will decrease by a further 8 d over the next ∼60 yr.

These initial findings have received mixed support from subsequent studies. Lee et al. (2022) used herbarium specimens instead of observational data while also expanding the spatial extent of study to include data from across all of eastern North America (as opposed to just one location in Massachusetts) as well as temperate deciduous forests in Europe and Asia. While these authors found support for diminishing spring light windows for wildflowers in North America, they instead found neutral to positive change in spring light window length for wildflowers on the other two continents, suggesting that climate change will not be as dire for spring ephemeral wildflowers outside of North America. A second study using the North American subset of the Lee et al. (2022) herbarium data (Miller et al. 2022) binned observations to look for differences in phenological sensitivity in wildflowers and canopy trees associated with latitudinal and environmental gradients. They found that past and future changes in phenological escape depended on whether they were considering warm, cool, or intermediate parts of species’ ranges; wildflowers experienced the previously described reductions in access to early spring light in the northern, cooler parts of their range but fared better in the warm and intermediate regions.

Likewise, Alecrim et al. (2023) conducted an analysis highly similar to the Miller et al. (2022) analysis but using community science observational data instead of data sourced from herbarium collections. These authors used tree and wildflower phenology data sourced from the National Phenology Network (https://www.usanpn.org/) spanning the eastern United States and separated the data into latitudinal bins while looking for biogeographic gradients in phenological sensitivity. Contrary to the results from the other three papers, Alecrim et al. (2023) found that wildflower species were overall more sensitive to spring temperature than co-occurring tree species, resulting in projected increased access to spring light under warmer temperatures (a result also echoed by research done in the Appalachian Trail corridor; Tourville et al. 2023). Interestingly, although the authors found more extreme differences in phenological sensitivity between wildflowers and trees in northern regions (somewhat echoing the results of Miller et al. 2022), they instead found that wildflowers were more sensitive than co-occurring canopy trees, suggesting that the understory plants will gain access to light under climate change conditions.

Last, authors from some of these studies came together to conduct an in-depth comparison of the Miller et al. (2022) and Alecrim et al. (2023) papers to determine whether the dramatically different results could be reconciled in a comparative analysis. Although Lee et al. (2024) were unable to fully reconcile the differences between the two reports, they concluded that differences in species selection and spatiotemporal study extents were at least partially responsible for the differences between these two studies. Lee et al. (2024) found strong similarities in phenological sensitivity of individual species—species that were present in both the herbarium and the community science datasets had similar sensitivities across both datasets. However, while this echoes a recent study suggesting strong similarities in phenological sensitivity when comparing herbarium and community science datasets (Ramirez-Parada et al. 2022), Lee et al. (2024) found that the inferred changes in mismatch (i.e., whether understory plants were predicted to gain or lose access to spring light) differed consistently across the two datasets. This finding suggests that the inferences we make about biological interactions depend strongly on the type and scope of data used and that researchers in this area should consider this issue as they design and implement their experiments and models.

Climate change implications for phenological escape of other groups of understory plant species (other than spring ephemeral wildflowers) are less studied, but existing evidence suggests that woody plant species may fare relatively better under warming springs. In addition to the wildflowers discussed previously, Miller et al. (2022) also examined phenological sensitivity of various native and invasive shrub species using herbarium data. Shrubs were found to be relatively more sensitive than wildflowers and approximately as sensitive as trees to variation in spring temperatures, suggesting that they may be able to maintain access to light moving forward. Furthermore, another study found spring leaf-out phenology of temperate tree seedlings to be more sensitive to spring temperature than conspecific co-occurring canopy trees. Lee and Ibáñez (2021a), building on other work showing the importance of phenological escape for seedling carbon budgets (Lee and Ibáñez 2021b), found that climate change is projected to lead to increased spring light windows for juvenile trees in the North American Great Lakes region. This, too, suggests that woody understory plant species may be better situated to maintain (or even increase) access to spring light than herbaceous wildflowers.

An important caveat to the results discussed in the previous paragraph is that much of the work investigating phenological escape has been observational, relying on herbarium collections (Lee et al. 2022; Miller et al. 2022), historical observations (Heberling et al. 2019b), or community science datasets (Alecrim et al. 2023; Tourville et al. 2023). While some experimental studies do exist (Lee and Ibáñez 2021a, 2021b), they have been limited in scope to only a few species studied at the site level. More experimental studies are likely needed to better evaluate and predict how phenological escape might change over time.

Ecological Implications of Reduced Phenological Escape

In the previous sections, we presented evidence in the literature showing (i) the importance of access to spring light for the carbon budgets of spring-active understory plant species and (ii) how climate change could alter access to spring light because of differences in phenological sensitivity to spring temperatures. However, so far these dynamics have all been described in terms of individual-level performance metrics. For example, access to spring light determines survival and reproductive success of spring wildflowers (Lapointe 1998; Routhier and Lapointe 2002; Ida and Kudo 2008; Kudo et al. 2008; Neufeld and Young 2014). In woody plants, such as deciduous tree seedlings, access to spring light is directly tied to annual growth and probability of survival (Lee and Ibáñez 2021a, 2021b). The question remains: how do changes in phenological escape and individual plant performance scale up to affect population- and community-level ecological dynamics?

This is a question that in large part remains unanswered. A recent meta-analysis that investigated how phenological shifts affect demography found very few studies that directly and mechanistically linked the two topics, at least for plants (Iler et al. 2021). The authors found many studies that linked phenology shifts to individual metrics of performance (reproductive success, growth, survival, etc.; see “Climate Change Effects on Phenological Escape” above for examples), but only a few studies then went the extra step of determining how changes in individual performance affect population-level dynamics. For example, one study that did specifically investigate this relationship in montane wildflowers found that earlier phenology linked to warmer springs reduced survival because of increased risk of drought (and, to a lesser extent, increased frost damage; Iler et al. 2019). This reduction in survival was then mechanistically linked to reductions in population growth rates (finite rate of increase [λ]; Caswell 2008), meaning that reduced survival directly and negatively influenced the population’s ability to persist in the study location.

Overall, though, studies that directly link plant phenology shifts with changes in demographic rates remain rare despite the commonly held assumption that changes in individual performance associated with the former will translate directly into changes in the latter (Iler et al. 2021). This assumption should be questioned and explicitly tested, however, because the extent to which individual performance affects population-level dynamics depends on the species and the system. For example, although seed set has been shown to be negatively affected by shifts in phenology (Ida and Kudo 2008; Kudo et al. 2008) and posited as a potential consequence of reductions in spring light availability for spring ephemeral wildflowers (Heberling et al. 2019a; Lee et al. 2022), reductions in fruit production and seed set will have only negative consequences for population-level performance if a species is seed limited at a given location (e.g., Lundgren et al. 2015). Similarly, it is theorized that growth and survival limitations will play larger roles in shaping long-lived plant demography (such as for woody or perennial species) while fluctuation in reproductive success and germination will more strongly shape short-lived plant species (Franco and Silvertown 2004). It is therefore important that future studies of phenological escape (and shifts in phenology more broadly) work to apply their results to trends in demography and to explore how and whether changes in access to light manifest in changes to population persistence.

Beyond plant demography, changes in phenological escape may also indirectly affect other organisms that interact with understory plant species. One example of this is the potential disruption of plant-pollinator interactions. Previous research provides evidence for disruption in general plant-pollinator interactions due to shifting activity periods (Kudo et al. 2008; Kudo and Ida 2013). That is, flowering phenology and pollinator phenology can have different (or even opposite) sensitivities to environmental variation, leading to decreased overlap in activity with climate change.

It is also possible for phenological escape to further disrupt these interactions by increasing the amount of time that wildflowers spend in shade, even if plants and pollinators would otherwise overlap in activity periods. For example, bumble bees (genus Bombus) are often some of the earliest pollinators to emerge in spring and rely heavily on spring ephemeral wildflowers and other early-flowering plants for nectar resources (Timberlake et al. 2019). This can be especially true for queens of some species because they are first to emerge in order to initiate their hive before the rest of the colony becomes active later in spring (Timberlake et al. 2019; Mola et al. 2021). Bee activity has also been shown to decrease with increasing canopy closure within a growing season (Proctor et al. 2012; Williams and Winfree 2013; Hanula et al. 2015) and to be generally lower in mature closed-canopy forests (Hilmers et al. 2018). Thus, diminishing spring light window duration could disrupt wildflower-pollinator interactions regardless of the level of phenological overlap that already exists between the two groups. That is, even if flowering phenology and pollinator activity are shifting earlier in spring at the same rate, earlier understory shading may reduce pollinator activity in the forest interior, thereby leading to reduced reproductive success (Kudo et al. 2008).

Potential Avenues for Future Research

Climate change–driven shifts in phenological escape and plant-plant interactions more broadly are relatively new ideas that deserve further exploration. In addition to a need for more evidence as to how changes in individual performance translate to population-level demographic performance (see “Ecological Implications of Reduced Phenological Escape”), there are several areas that we want to highlight here that represent persisting knowledge gaps related to phenological escape and could prove to be fruitful avenues of future research (table 1).

Conclusions

Phenological escape, although not well defined until recently, is an important ecological driver of understory plant performance in systems where understory light availability is seasonal and ephemeral. Access to elevated understory light levels in spring (and, to a lesser extent, fall) has been consistently found to account for between 50% and 100% of the annual aboveground carbon budgets for a wide range of species ranging from spring ephemeral wildflowers to woody tree seedlings and shrubs. Spring carbon assimilation has been directly and indirectly linked to individual-level performance metrics such as growth, survival, and reproductive success, meaning that access to spring light is likely to have a strong role in demographic processes (although this largely remains untested in practice). Climate change is expected to alter access to spring light for many species and thus has the capacity to dramatically affect temperate plant species through changes in phenological escape. Still, unanswered questions remain, particularly concerning whether and how phenological escape affects understory plant performance for species that do not rely on spring light (such as those in drought- or mixed-deciduous forests and those that instead rely on access to fall light). Filling these knowledge gaps is an important next step toward understanding how climate change shapes plant performance and plant communities.

Guest Editor: Susana Wadgymar