A Mechanistic Framework for Understanding the Effects of Climate Change on the Link Between Flowering and Fruiting Phenology

Abstract

Phenological shifts are a widely studied consequence of climate change. Little is known, however, about certain critical phenological events, nor about mechanistic links between shifts in different life-history stages of the same organism. Among angiosperms, flowering times have been observed to advance with climate change, but, whether fruiting times shift as a direct consequence of shifting flowering times, or respond differently or not at all to climate change, is poorly understood. Yet, shifts in fruiting could alter species interactions, including by disrupting seed dispersal mutualisms. In the absence of long-term data on fruiting phenology, but given extensive data on flowering, we argue that an understanding of whether flowering and fruiting are tightly linked or respond independently to environmental change can significantly advance our understanding of how fruiting phenologies will respond to warming climates. Through a case study of biotically and abiotically dispersed plants, we present evidence for a potential functional link between the timing of flowering and fruiting. We then propose general mechanisms for how flowering and fruiting life history stages could be functionally linked or independently driven by external factors, and we use our case study species and phenological responses to distinguish among proposed mechanisms in a real-world framework. Finally, we identify research directions that could elucidate which of these mechanisms drive the timing between subsequent life stages. Understanding how fruiting phenology is altered by climate change is essential for all plant species but is particularly critical to sustaining the large numbers of plant species that rely on animal-mediated dispersal, as well as the animals that rely on fruit for sustenance.

Current and lagged climate affects phenology across diverse taxonomic groups

“…While warmer temperatures are well-known to advance phenological events for many taxa, the magnitude of change, or the number of days advanced per unit time, can differ among phenological events [31]. For example, plant flowering and fruiting may both advance in response to higher temperatures, but flowering may advance more rapidly [32,33]. Phenological responses to climate can vary greatly among species; species can respond to different climate cues, different aspects of a given cue, or to the same cue in different ways [34,35] (figure 1a).…”

“…While warmer temperatures are well-known to advance phenological events for many taxa, the magnitude of change, or the number of days advanced per unit time, can differ among phenological events [31]. For example, plant flowering and fruiting may both advance in response to higher temperatures, but flowering may advance more rapidly [32,33].…”

Fruiting phenology matters

“…Furthermore, most of these studies do not follow the phenology of a sizeable fraction of the local flora, usually including only a few species and very rarely more than 100 species (e.g., Chuine et al, 2004;Gordo & Sanz, 2010;Lechowicz, 1995;Mendoza et al, 2017Mendoza et al, , 2018Miller et al, 2021;Rosbakh et al, 2021). The conclusion is that despite relevant seminal work, current knowledge of fruiting phenology is still embarrassingly poor, if compared, for example, with that of flowering phenology (to which it might or might not be directly correlated; Sandor et al, 2021). A clear sign of the historical primacy given to flowering phenology is that most published Floras contain information on the main flowering months for the plant species in a particular area (e.g., Tutin et al, 1964).…”

Leaf gene expression trajectories during the growing season are consistent between sites and years in American beech

“…These deviations can exceed the reaction norms of trees [3][4][5][6][7][8]. For temperate trees, shifts in the spring arrival, and changing precipitation regimes can affect the phenological scheduling of vital biological events such as vessel activation [9], the acquisition of soil nutrients [10], flowering [3,[11][12][13], leaf flushing [14][15][16][17][18], xylogenesis [19], seeding and fruiting [20][21][22], and senescence-induced nutrient re-uptake from leaves [16,[23][24][25][26]. Ultimately, the resulting evolutionary dynamics will redefine competition and reshape species ranges [18,27,28].…”