Phenological shifts are among the most visible ecological effects of global climate change. Research on individual species (e.g., CaraDonna et al., 2014), meta-analyses (Root et al., 2003; Munguía-Rosas et al., 2011), and community-wide taxonomic surveys (Ovaskainen et al., 2013) demonstrate that phenological, or the timing of life history, events in most species and stages are advancing in response to warmer temperatures. Well-studied life history stages include migration (Mayor et al., 2017) and breeding (Burger et al., 2012) in birds, hibernation in mammals (Sheriff et al., 2011), adult emergence in insects (Bartomeus et al., 2011; Renner and Zohner, 2018), and green-up and flowering in plants (Calinger et al., 2013; Rafferty and Nabity, 2017; Ettinger et al., 2018). In contrast, other life history stages, such as fruiting, have received relatively little attention (Chuine and Régnière, 2017; Mendoza et al., 2017; Ettinger et al., 2018). An important gap in our understanding concerns whether the latter of successive events in the life histories of an organism (e.g., fruiting which follows flowering) are shifting independently of, or are functionally constrained by, earlier stages.

It is reasonable to predict that climate-induced shifts in the timing of early life history stages result in parallel shifts in subsequent life-history stages of the same organism. The timing of life history stages is driven by a combination of external (climate) and internal (physiological or endogenous) factors. It is largely unknown, however, to what extent each factor drives the timing of one life history stage relative to earlier ones (McDermott and DeGroote, 2017; Ettinger et al., 2018; Gougherty and Gougherty, 2018; Augspurger and Zaya, 2020; Buonaiuto et al., 2021). With the exception of a few pioneering studies (e.g., Menzel et al., 2001; Post et al., 2008a,b; Haggerty and Galloway, 2011; Jiang et al., 2016; Segrestin et al., 2018), little research has yet explored whether successive life history stages predictably shift in concert with each other in response to climate change, nor, when they do, what drivers underlie this relationship (Chuine and Régnière, 2017; Ettinger et al., 2018). Parallel shifts might occur either if the interval between successive life-history events is constant or nearly so (likely a product of internal factors such as physiology or development), or if the external, proximate climatic cues for the two events are the same or tightly associated. Parallel shifts in successive life history stages could be related to reproductive strategy and traits (Forrest and Miller-Rushing, 2010; Ettinger et al., 2018; reviewed in Gougherty and Gougherty, 2018; Buonaiuto et al., 2021), genetics and selective processes (Crozier et al., 2008; Wilczek et al., 2010), and temporal boundaries on the growing or breeding season (Morales et al., 2005). Alternatively, successive life history stages could respond to different climatic conditions (Kingsolver et al., 2011), resulting in a changing interval between them as the climate changes (Lany et al., 2016). Determining which internal or external mechanisms are acting on the timing of life history events should offer critical predictive insights into whether and how climate change will affect the persistence not only of individual taxa, but also of the interactions among them.

Perhaps the most thoroughly documented phenological shift in response to climate change involves flowering. Advances in flowering time (conventionally noted by opening of flowers on an earlier date) have been found both across communities and within them, and contrasting responses across regions and taxa have been explored in some depth (e.g., Fitter and Fitter, 2002; Root et al., 2003; Miller-Rushing and Primack, 2008; CaraDonna et al., 2014; Rafferty and Nabity, 2017). Here, we use this wealth of knowledge on flowering phenology to explore whether subsequent life stages are linked, and if so, how they are linked. Although several investigators have speculated about whether advances in flowering time are accompanied by parallel shifts in fruiting time (Primack, 1987; Eriksson and Ehrlén, 1991; Forrest and Miller-Rushing, 2010), there are as yet few tests of these ideas (Chmielewski et al., 2004; Sherry et al., 2007; Segrestin et al., 2018). As a consequence, the response of fruiting phenologies to a changing climate remains poorly understood (Chuine and Régnière, 2017).

Experimental warming studies have shown that with higher temperatures, most species fruit earlier in the season (Sherry et al., 2007; Post et al., 2008a,b). However, observational studies of fruiting phenology, particularly those using datasets that span decades, vastly lag behind the number published for flowering. One possible reason for the focus on flowering phenology over fruiting is that assigning a date to fruiting is less straightforward because fruit morphology is more diverse across taxa than flower morphology, and stages of fruit development are less easily identified through observation. We follow convention of previous studies and, unless otherwise noted, use “fruiting” or “fruiting time” to denote the first date on which the presence of mature fruits or seeds is observed (e.g., Gordo and Sanz, 2009; Haggerty and Galloway, 2011; Ettinger et al., 2018), and, in our discussions of published studies and within the case study we present, we compare across taxa with different fruiting structures (e.g., fleshy, dry, indehiscent, dehiscent, animal-dispersed, and wind-dispersed; Menzel et al., 2006, 2020; Ge et al., 2015).

Here, we explore promising pathways for advancing understanding of which and how fruiting times are linked to flowering times. In animal-dispersed plants, shifts in fruiting phenology have the potential to affect or even disrupt seed-dispersal interactions (Forrest, 2014; Rafferty et al., 2015). Thus, an understanding of shifting fruiting phenologies is important to our ability to predict the effects of global change on plant-animal communities (Rogers et al., 2021). We incorporate plants that are animal-dispersed as well as those that employ abiotic seed dispersal, but we focus on the interaction and community repercussions for animal-dispersed plants. First, we synthesize current understanding of the linkages between flowering and fruiting stages across angiosperms. Second, to ground our discussion of life history stage linkages in a real-world framework, we report on a case study designed to determine how the flowering and fruiting times of individuals tracked over multiple decades at the same location are linked. Third, we leverage our extensive knowledge of climate-mediated shifts in flowering phenology to develop a conceptual model for how successive life history stages are linked and how climate change could affect these linkages. We then return to our case study results to demonstrate how to distinguish and eliminate proposed mechanisms for these linkages. Finally, we suggest directions for future research to test these mechanisms, and discuss the implications of climate change-driven shifts in fruiting phenology for ecological communities.

Few studies have determined the extent to which flowering and fruiting phenology are linked or physiologically constrained. We argue here that examining the flowering-to-fruiting interval can provide insight. We define the flowering-to-fruiting interval (hereafter, FTFI) as the period from flower opening to the first date on which the presence of mature fruits or seeds is observed. The FTFI is “constrained” if it remains fixed in length, including within warming experiments or in a changing climate. The FTFI is a trait defined at the level of the reproductive structure; i.e., it is the length of time from flowering to fruiting measured on a single flower developing into a fruit on an individual plant. In order to make use of historical datasets in which observations were not collected at this level, most previous studies have largely used population- or species-level measurements, with a few examples of individual-level measurements (Table 1). If flowering and fruiting are linked, internal drivers will dictate that fruiting times are related to flowering times as well as to the FTFI. If external factors are instead driving phenology, the FTFI could lengthen or shorten as flowering and fruiting respond to these external factors independently. If flowering and fruiting are responding independently to the same external factors, or if by chance these two life stages are responding in similar ways to different independent factors, the FTFI will stay the same.

The few previous studies of how flowering and fruiting are linked provide evidence for internal drivers, but also evidence for independent responses of flowering and fruiting to external factors (Post et al., 2008a,b; Ettinger et al., 2018; Segrestin et al., 2018; Table 1). Studies that present evidence for external factors independently driving fruiting and flowering times often show some evidence for internal drivers as well (Lechowicz, 1995; Menzel et al., 2006, 2020; Haggerty and Galloway, 2011; Jiang et al., 2016; Sethi et al., 2020; Table 1). Table 1 synthesizes the results of these previous studies and the mixed evidence for internal and external drivers of flowering and fruiting. An early study of the FTFI based on a nearly 30-year dataset found no evidence for a linear relationship between flowering and fruiting dates across many temperate species, even when grouped by time of season in which fruiting occurs (Lechowicz, 1995). In contrast, a more recent single-year study did find evidence for this linear relationship in 25 U.S. species (Ettinger et al., 2018), as did a 12-year study of 100 European species (Segrestin et al., 2018). Even concurrent studies on the same species have produced mixed evidence for internal and external drivers of the FTFI. A 1-year warming experiment revealed that higher temperatures shortened the entire reproductive cycle of Betula nana by 27 days on average, from flower bud set to fruit set (Post et al., 2008b), thereby also shortening the FTFI. However, a concurrent 2-year warming experiment showed that higher temperatures did not decrease the FTFI in B. nana (Post et al., 2008a), even though flowering and fruiting were advanced.

Other experimental studies have yielded evidence for both internal and external drivers of the FTFI. Alpine plants transplanted to warmer and cooler altitudes for 3 years flowered earlier and later, respectively, but fruiting times remained the same (Jiang et al., 2016). These results support external drivers of the FTFI, but a different elevation transplant study (Haggerty and Galloway, 2011) showed evidence for both external and internal drivers: in a single-year common garden experiment, Campanulastrum americanum populations planted at lower elevations had a shortened FTFI relative to those planted at higher elevations. However, populations from low elevations planted at either elevation had a longer reproductive cycle overall than those from high elevations (Haggerty and Galloway, 2011).

Observational studies have similarly yielded mixed evidence. A recent observational study on 28 species of U.S. alpine plants showed mostly shortened FTFI with climate change, comparing observations taken in 2015 to those taken in 2011–2014 (Sethi et al., 2020). Shorter FTFI were shorter by 3–15 days, but two species showed an FTFI change of a day or less, and the FTFI of three species increased by 3–5 days (Sethi et al., 2020). Menzel et al. (2006) used phenological records to determine (1) how timing of life history stages was changing in 14 European countries over 30 years and (2) how these phenological changes correlated with temperature across 9 European countries over 15 years. While flowering time was largely negatively correlated with temperature, fruiting time was more variable: the correlation with temperature was negative for most species, but positive for a few others. A recent update of this study incorporating data on the same European species from 1951 to 2018 showed the same pattern (Menzel et al., 2020). As temperature increases and flowering times advance, Menzel et al.’s (2006, 2020) findings imply that the FTFI will shorten for some species, remain the same for some, and lengthen for others, depending on how internal and external factors interact to determine fruiting times.

Nearly all of the few studies that directly analyze the FTFI do so on the scale of a year or a few years, and in the case of multi-year analyses, only for a single species (Table 1). Publicly available fruiting data at time scales longer than 20 years are particularly sparse (Chuine and Régnière, 2017; see Supplementary Appendix 1 for descriptions of publicly available phenology databases). Yet, time series > 30 years are needed to estimate robust trends (Dose and Menzel, 2004; Menzel et al., 2020). Here, we use a three-and-a-half-decade dataset (from the PEP725 database; Templ et al., 2018) to assess how the FTFI is changing in individual plants. Our case study both illustrates the challenges of analyzing the phenology of certain life history stages on a decadal scale using publicly available data. At the same time, it provides compelling evidence that such data, when available, can be used to analyze changes to the length of time between phenophases with climate change. We do not present here a comprehensive treatment of FTFI across species. Although more long-term data are needed to assess changes in the FTFI across diverse taxa and regions (Mendoza et al., 2017; Supplementary Appendix 1), we use this case study to illustrate the potential power of analyzing relationships between the timing of different life history stages.

If the timing between flowering and fruiting is physiologically constrained, a shift in timing in flowering should have a direct effect on the timing of fruiting. This could result in flowering and fruiting times advancing in parallel, as in three of the six species in our case study. However, we cannot rule out the possibility that separate, possibly correlated external factors are acting on each of the life history stages. Furthermore, external factors could act on flowering and fruiting separately or jointly, such that the FTFI lengthens or shortens, as seen in the other three species in our case study. Below we propose four general mechanisms for how flowering and fruiting times may jointly or independently shift with climate change. While the specifics of these mechanisms can relate more strongly to one seed dispersal type than another, as noted below, all four mechanisms apply to plants with either biotic or abiotic seed dispersal. We additionally recognize that multiple mechanisms could be operating at once.

Several of the mechanisms proposed above for how fruiting and flowering phenology respond jointly or independently to climate change could produce identical results in the FTFI over time (Table 2 and Figure 2). Here we return to our case study to demonstrate how we could use the FTFI in combination with additional research to tease apart the mechanisms behind changes, or lack thereof, to the FTFI (Figure 3). For example, an absence of change in the FTFI, such as we found in three of our six species (Figure 1), indicates that the mechanism driving the FTFI for these species could be internal. Stabilizing selection is expected to produce a change in the FTFI, so that mechanism can be discarded. Constancy in the FTFI is consistent with Mechanisms 3, directional selection, and 4, environmental controls. The mechanism of environmental controls is difficult to rule out because, for example, an incremental increase in temperature across many years could have an equally strong correlation with fruiting as flowering has with fruiting. If, over many years and across yearly temperature and/or precipitation fluctuations, fruiting time is more strongly correlated with flowering time than with environmental cues, we could rule out environmental controls. The other processes affecting environmental controls are either difficult to track or require vastly more data. If length of flowering time, specifically from flower opening to pollination, does not affect fruiting time and thus FTFI, environmental controls via flower longevity could be ruled out. If any of the processes related to the acquisition of resources, like frost or herbivore damage to leaves, are not correlated with FTFI, we can rule out environmental controls. However, collecting data to discriminate multiple processes related to environmental controls is a massive undertaking. This will make discerning the importance of environmental controls via resource acquisition difficult. If we find no genetic evidence for directional selection on fruiting times (e.g., see Giménez-Benavides et al., 2011; Munguía-Rosas et al., 2011; Anderson et al., 2012; Yeoh et al., 2017, for studies on flowering), or if we find no fitness benefits for those individuals for which the FTFI remains constant, we can rule out directional selection.

Ruling out stabilizing selection, directional selection, and environmental controls leaves only physiological and developmental constraints as mechanisms producing a constant FTFI over time and in the face of climate change. Comparing the FTFI among species within the same genus and to species of genera with similar fruit or seed sizes could point to whether phylogenetic or developmental constraints are operating. Accounting for phylogenetic signal in the analysis of changes in FTFI across multiple years, species, and continents (i.e., Davis et al., 2010 for flowering) could point to the relative influence of evolutionary history on phenological responses to changing climate. However, none of these approaches permits elimination of either pathway through which the internal mechanism could be operating.

One of the six species in our case study, Aesculus hippocastanum, experienced an increase in FTFI over time (Figure 1). We expect physiological and developmental constraints to result in a constant FTFI over time, suggesting that the other three mechanisms we have proposed—stabilizing selection, directional selection, or environmental controls—could be responsible. Stabilizing selection could be acting if the time of first ripe fruits remains constant. However, for A. hippocastanum the timing of fruiting shifted earlier (Figure 1). Another indication of stabilizing selection might be fruit ripening that remains constant in reference to an abiotic or biotic event. If we found no correlation between fruiting times and abiotic or biotic events, or no genetic evidence for stabilizing selection on fruiting times, we could rule out this mechanism. Furthermore, if we found no genetic evidence of directional selection on fruiting times, or if we found no fitness benefits for those individuals for which the FTFI increases, we could rule out directional selection. If flower longevity was driving the lengthening of the FTFI by an increased amount of time between flower opening (the beginning of the FTFI, as defined above) and flower closing, we would expect to observe a lengthening of the first flowering to flower senescence interval over multiple years. We would also potentially expect to see a strong correlation between date of pollination and first ripe fruit dates. If neither this correlation nor a correlation between pollination and first ripe fruits were found, environmental controls via flower longevity could be rejected. If both flowering and fruiting were correlated with the same or independent environmental conditions, with no evidence for selection on either, environmental controls might be driving the increased FTFI. However, correlations with environmental conditions may be direct (e.g., temperature and/or precipitation acting directly on flowering and fruiting) or indirect, via resource acquisition. A number of pathways that affect photosynthesis could be involved in this indirect relationship, and teasing them apart would require extensive data collection in, for example, leaf damage and cloudless days.

Two of the six species represented in this case study experienced a decreased FTFI (Figure 1), again suggesting that stabilizing selection, directional selection, or environmental controls could be responsible. As with A. hippocastanum, in Ribes rubrum, and R. grossularia fruiting occurred earlier (Figure 1), indicating that stabilizing selection could only be acting if fruit ripening time remained constant in reference to an unknown abiotic or biotic event. The same process of eliminating mechanisms just described for A. hippocastanum could be applied to these Ribes species.

Throughout this paper, we have stressed that additional research is needed to further distinguish which mechanisms are driving the FTFI, and through what pathways. Here we discuss research directions for internal drivers of the FTFI, how genetics and selection influence the FTFI and will determine future fruiting responses to climate change, and the interactions among different environmental controls and how these affect fruiting both now and with climate change. Although different species may be driven by different mechanisms, and all of the mechanisms discussed here may be operational in nature, simultaneous, standardized studies of multiple species could provide evidence for or eliminate possible mechanisms on a broad scale. We additionally emphasize that long-term studies of phenology are essential because short-term interannual variation could reflect phenological plasticity rather than evolutionary change.

Further research could elucidate how physiological mechanisms determine the FTFI, and to what extent different mechanisms co-occur and can interact. Taking a trait-based approach to determine differences in seed and fruit development time across the range of seed and fruit traits could advance our understanding of the extent to which the time of fruit development is constrained, or varies, along trait axes (e.g., Singh and Kushwaha, 2006). Determining which families or clades have long fruit or seed development times closely linked to the number of growing degree days within a season could shed light on the extent to which phylogenetic constraints work in concert with environmental controls to determine the length of the fruit development period. Similarly, studies that compare the relative influence of evolutionary history and environmental controls could tease apart the extent to which internal vs. external process are driving phenology (e.g., Staggemeier et al., 2015), particularly with the incorporation of phenological shifts due to climate change (Davis et al., 2010). We suggest incorporating standardized FTFI measures into existing phenological data collection protocols so as to more accurately compare across datasets, as Buonaiuto et al. (2021) have suggested for the interval between flowering and leaf-out.

If fruit or seed dispersal mode does not predict the strength of selection on fruit ripening times (e.g., Schluter, 1988; Kingsolver et al., 2001; Palacio et al., 2021), it is less likely that stabilizing selection is acting on fruit ripening times across many species. Additionally, if peak activity of seed dispersers and fruit ripening times are shifting and becoming out of phase with climate change, instead of shifting in parallel, biotic interactions driving stabilizing selection in animal-dispersed fruits can be discarded as a general pattern. To determine how peak activity of dispersers and fruit ripening times are responding to each other and climate change, more long-term studies that track disperser phenology along with fruiting phenology, particularly in the tropics where biotic interactions are assumed to play a greater role than climatic factors, are sorely needed (Mendoza et al., 2017).

Mechanistic research that addresses the molecular and regulatory basis of fruit ripening in wild species would further disentangle selection for particular genes associated with ripening from changing environmental cues and altered physiological processes (Chen et al., 2020). Additionally, determining how selection is acting on the reaction norm for fruit ripening times (Inouye et al., 2019) as climate changes, and how genetic variation in wild species of genes associated with fruiting responds to changes in temperature, precipitation, and other climatic factors, would help further our understanding of how a changing environment is interacting with selective pressures. Agricultural scientists are exploring the genetic underpinnings of plant phenology (e.g., Satake et al., 2013; Marrano et al., 2019; Chen et al., 2020) and phenological responses to climate change of cultivated species (e.g., Chmielewski et al., 2004; Darbyshire et al., 2014); future research that draws on this body of literature could inform our understanding of wild plants in natural systems. Additionally, studies that correlate climatic cues with gene expression in genes associated with fruiting in wild plants (e.g., see Kudoh, 2016; Yeoh et al., 2017 for this type of research with genes associated with flowering) would increase our ability to tease apart the pathways and extent to which different climatic variables impact the genetic component of fruiting. Lastly, in animal-dispersed species, disperser activity could directionally select for fruiting phenology, and further studies are needed to explore to what extent and in which species dispersers drive phenotypic selection, particularly with reference to the FTFI and population-level traits like crop size and fruiting duration (Palacio et al., 2021).

We have emphasized that different types of environmental controls can interact with each other. Further studies are needed to understand and differentiate among these effects. For example, in an analysis of the midpoint of listed fruiting dates of 11,605 Chinese species within a compiled flora, Du et al. (2020) found that mean annual precipitation, precipitation seasonality, temperature seasonality, and temperature of the coldest quarter were included in the best supported models of the variation in fruiting times across species. Reduced soil moisture was a climate-related variable that was correlated with shortened FTFI in some alpine plant species, as was increased temperature in most species, although the interaction between them was not specifically tested (Sethi et al., 2020). Further, interactions between temperature and precipitation (e.g., Misson et al., 2010; Butt et al., 2015; Mazer et al., 2015) with climate change could be additive and cause fruiting times to advance more than changes to temperature or precipitation alone. Further research is also needed on how precipitation affects fruiting phenology, including the effect of higher or lower precipitation on the FTFI and how timing of precipitation affects fruiting (e.g., Molau, 1997; Fitter and Fitter, 2002; Parmesan and Yohe, 2003; Du et al., 2020). Additionally, seasonality of precipitation and how it relates to fruiting phenology in tropical wet forests needs to be further investigated, as current studies show contradictory patterns (Mendoza et al., 2017). Finally, environmental controls could interact with other factors influencing a species’ phenology and our other proposed mechanisms. For example, higher temperatures due to climate change could interact with biogeography (e.g., Loarie et al., 2009; Butt et al., 2015; Ge et al., 2015, reviewed in Du et al., 2020), phylogeny (Davis et al., 2010), and life form (Du et al., 2020; Ganjurjav et al., 2021) to produce patterns in the FTFI across many species.

Lastly, we recommend that future research precisely define the beginning and end of the FTFI and that these definitions are incorporated into study design. Because FTFI is defined at the level of a single reproductive structure on an individual plant, the start and end of the FTFI can be defined in terms of flower opening, closing, or pollen deposition, and the end of the FTFI can be defined as when the individual fruit is ripe, with the recognition that “ripeness” will need to be precisely delineated for each species. While our case study was limited by available phenological data, future studies can tease apart flower longevity by defining the beginning of the FTFI at the time of pollen deposition or flower closing and can investigate intraspecific, and even intraindividual, variation in FTFI. Long-term studies using these definitions on the boundaries of the FTFI, which are currently lacking, can then be used to determine interannual variation.

The mechanisms we propose that could drive the FTFI in the context of a changing climate are relevant to all plants with biotic and abiotic seed dispersal. However, FTFI and fruiting phenology changes in animal-dispersed plants are particularly important to study since they have larger repercussions for the communities of which these plants are a part. For example, changes in fruiting phenology and animal abundance or activity could result in a temporal mismatch between partners, especially if plants and animals are responding to different environmental cues or responding in different ways (Forrest, 2014; Rafferty et al., 2015; Palacio et al., 2021). If the timing of peak disperser activity is shifting in response to environmental changes in a similar direction to fruiting times, with fruiting times responding via either genotypic variation or environmental controls in plants, no phenological mismatch will result. However, if the FTFI is internally driven, fruiting times will shift earlier in the season in conjunction with earlier flower times. If the FTFI is externally driven, changing environmental conditions could result in fruiting times that are out of step with peak disperser activity, resulting in a similar phenological mismatch outcome as if FTFI were internally driven. The same is true if the FTFI is a result of stabilizing selection, unless other selective pressures act to re-align fruiting times with peak disperser activity. Phenological mismatch could result in dispersal failure via fruiting occurring before dispersers are active (Warren and Bradford, 2013), lower plant fitness via reduced disperser activity (McConkey and Drake, 2006; Traveset et al., 2012; Rogers et al., 2017), animal population declines via reduced fecundity or increased mortality (van Schaik et al., 1993; Wright et al., 1999; Saino et al., 2011), or changes in community composition (Moegenburg and Levey, 2003; Peralta et al., 2020).

Phenological mismatch is not the only way in which plant and animal populations, communities, and ecosystems could be affected by climate change impacts on the FTFI. Plant and seed-disperser populations could be affected by reduced fruit production resulting from higher than average temperatures, increases or decreases in precipitation, or a combination (Young et al., 2004; Augspurger, 2009; CaraDonna and Bain, 2016; Babweteera et al., 2018; Benlloch-González et al., 2018; Chapman et al., 2018; Lee et al., 2018; Mendoza et al., 2018; Pardee et al., 2018; Nussbaumer et al., 2020; Rogers et al., 2021) if internal or external drivers of the FTFI pull fruiting times into less than ideal climatic conditions. Additionally, fruiting phenology could shift earlier at different magnitudes across elevation or space (e.g., Rafferty et al., 2020), leading to shifting spatial activity of seed dispersers in response to changed resource levels across the landscape (Curran and Leighton, 2000). Lastly, major shifts in frugivorous animal activity could lead to a cascade of effects that impact ecosystem function (Rogers et al., 2021), even if seed dispersal is not directly affected. For example, red elderberry fruiting early in Alaska caused bears to leave salmon runs to gorge on fruits, disrupting a strong predator-prey interaction (Deacy et al., 2017) and likely causing a reduction in nitrogen influx to the forest (Helfield and Naiman, 2006).

We have leveraged here the extensive data on flowering phenology to explore how flowering and fruiting phenologies are linked. We found strong evidence in some species but not in others for a link between flowering and fruiting times. These results suggest that we should rapidly expand our understanding of the FTFI and shifts in fruiting phenology to enable better predictions for future climate change-influenced conditions. For those plant species demonstrating climate-driven phenological shifts in either direction, we need to explore when and to what extent those shifts will affect the ecological functioning and conservation concerns of plant and/or animal populations and/or mutualisms (e.g., Saino et al., 2011; Rafferty et al., 2015; Renner and Zohner, 2018). A better understanding of the magnitude of the effects on plant and animal populations and communities, as well as the factors that produce those effects, could enable parameterization of fitness models, and increase our ability to predict population trajectories and community composition in a changing climate.

Publicly available datasets were analyzed in this study. Data were provided by the members of the PEP725 project: http://www.pep725.eu (PEP725).

MES performed case study analyses. MES, CEA, LP, and JLB jointly wrote the first draft of the manuscript. All authors contributed substantially to revisions.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.