Phenology-the timing of biological events-is highly sensitive to climate change. However, our general understanding of how phenology responds to climate change is based almost solely on incomplete assessments of phenology (such as first date of flowering) rather than on entire phenological distributions. Using a uniquely comprehensive 39-y flowering phenology dataset from the Colorado Rocky Mountains that contains more than 2 million flower counts, we reveal a diversity of species-level phenological shifts that bring into question the accuracy of previous estimates of long-term phenological change. For 60 species, we show that first, peak, and last flowering rarely shift uniformly and instead usually shift independently of one another, resulting in a diversity of phenological changes through time. Shifts in the timing of first flowering on average overestimate the magnitude of shifts in the timing of peak flowering, fail to predict shifts in the timing of last flowering, and underrepresent the number of species changing phenology in this plant community. Ultimately, this diversity of species-level phenological shifts contributes to altered coflowering patterns within the community, a redistribution of floral abundance across the season, and an expansion of the flowering season by more than I mo during the course of our study period. These results demonstrate the substantial reshaping of ecological communities that can be attributed to shifts in phenology.growing season | no-analogue community | phenological mismatch | phenology curve | species interactions P henology, the timing of biological events, is intimately tied to the reproduction and survival of organisms (1). Phenological events generally are occurring earlier in temperate environments in accordance with climate change, although several recent studies have emphasized species-specificity in the direction and magnitude of change (2-5). The great majority of these longterm datasets contain a single measure of phenology for individual species, most often the first day on which a biological event is observed (i.e., "phenological firsts" such as first flowering) (Fig. 1A). In addition to phenological firsts, basic components of an entire phenological response include the timing of the ending of a biological event and details of intermediate stages, such as the timing and magnitude of peak abundance or activity (Fig. 1A). Given that phenological firsts represent the early tail of a population-level response, most assessments of phenological change to date may provide an incomplete view of the magnitude of change, the number of responsive species, and how species-level shifts contribute to change at higher levels of biological organization.We have amassed a unique long-term record of flowering phenology that allows us to investigate complete phenological responses for a plant community. Over a 39-y period , we have sampled a montane site (2,900 m elevation) in Colorado, USA, counting the total number of flowers of 121 plant species across a series of permanent...
Over the past decade, the Arctic has warmed by 0.75°C, far outpacing the global average, while Antarctic temperatures have remained comparatively stable. As Earth approaches 2°C warming, the Arctic and Antarctic may reach 4°C and 2°C mean annual warming, and 7°C and 3°C winter warming, respectively. Expected consequences of increased Arctic warming include ongoing loss of land and sea ice, threats to wildlife and traditional human livelihoods, increased methane emissions, and extreme weather at lower latitudes. With low biodiversity, Antarctic ecosystems may be vulnerable to state shifts and species invasions. Land ice loss in both regions will contribute substantially to global sea level rise, with up to 3 m rise possible if certain thresholds are crossed. Mitigation efforts can slow or reduce warming, but without them northern high latitude warming may accelerate in the next two to four decades. International cooperation will be crucial to foreseeing and adapting to expected changes.
Many alpine and subalpine plant species exhibit phenological advancements in association with earlier snowmelt. While the phenology of some plant species does not advance beyond a threshold snowmelt date, the prevalence of such threshold phenological responses within plant communities is largely unknown. We therefore examined the shape of flowering phenology responses (linear versus nonlinear) to climate using two long-term datasets from plant communities in snow-dominated environments: Gothic, CO, USA (1974–2011) and Zackenberg, Greenland (1996–2011). For a total of 64 species, we determined whether a linear or nonlinear regression model best explained interannual variation in flowering phenology in response to increasing temperatures and advancing snowmelt dates. The most common nonlinear trend was for species to flower earlier as snowmelt advanced, with either no change or a slower rate of change when snowmelt was early (average 20% of cases). By contrast, some species advanced their flowering at a faster rate over the warmest temperatures relative to cooler temperatures (average 5% of cases). Thus, some species seem to be approaching their limits of phenological change in response to snowmelt but not temperature. Such phenological thresholds could either be a result of minimum springtime photoperiod cues for flowering or a slower rate of adaptive change in flowering time relative to changing climatic conditions.
Variation in species' responses to abiotic phenological cues under climate change may cause changes in temporal overlap among interacting taxa, with potential demographic consequences. Here, we examine associations between the abiotic environment and plant-pollinator phenological synchrony using a long-term syrphid fly-flowering phenology dataset (1992-2011). Degree-days above freezing, precipitation, and timing of snow melt were investigated as predictors of phenology. Syrphids generally emerge after flowering onset and end their activity before the end of flowering. Neither flowering nor syrphid phenology has changed significantly over our 20-year record, consistent with a lack of directional change in climate variables over the same time frame. Instead we document interannual variability in the abiotic environment and phenology. Timing of snow melt was the best predictor of flowering onset and syrphid emergence. Snow melt and degree-days were the best predictors of the end of flowering, whereas degree-days and precipitation best predicted the end of the syrphid period. Flowering advanced at a faster rate than syrphids in response to both advancing snow melt and increasing temperature. Different rates of phenological advancements resulted in more days of temporal overlap between the flower-syrphid community in years of early snow melt because of extended activity periods. Phenological synchrony at the community level is therefore likely to be maintained for some time, even under advancing snow melt conditions that are evident over longer term records at our site. These results show that interacting taxa may respond to different phenological cues and to the same cues at different rates but still maintain phenological synchrony over a range of abiotic conditions. However, our results also indicate that some individual plant species may overlap with the syrphid community for fewer days under continued climate change. This highlights the role of interannual variation in these flower-syrphid interactions and shows that species-level responses can differ from community-level responses in nonintuitive ways.
Organisms' life cycles consist of hierarchical stages, from a single phenological stage (for example, flowering within a season), to vegetative and reproductive phases, to the total lifespan of the individual. Yet phenological events are typically studied in isolation, limiting our understanding of life history responses to climate change. Here, we reciprocally transfer plant communities along an elevation gradient to investigate plastic changes in the duration of sequential phenological events for six alpine species. We show that prolonged flowering leads to longer reproductive phases and activity periods when plants are moved to warmer locations. In contrast, shorter post-fruiting leaf and flowering stages led to shorter vegetative and reproductive phases, respectively, which resulted in shorter activity periods when plants were moved to cooler conditions. Therefore, phenological responses to warming and cooling do not simply mirror one another in the opposite direction, and low temperature may limit reproductive allocation in the alpine region.
When a phenological shift affects a demographic vital rate such as survival or reproduction, the altered vital rate may or may not have population-level consequences. We review the evidence that climate change affects populations by shifting species’ phenologies, emphasizing the importance of demographic life-history theory. We find many examples of phenological shifts having both positive and negative consequences for vital rates. Yet, few studies link phenological shifts to changes in vital rates known to drive population dynamics, especially in plants. When this link is made, results are largely consistent with life-history theory: Phenological shifts have population-level consequences when they affect survival in longer-lived organisms and reproduction in shorter-lived organisms. However, there are just as many cases in which demographic mechanisms buffer population growth from phenologically induced changes in vital rates. We provide recommendations for future research aiming to understand the complex relationships among climate, phenology, and demography, which will help to elucidate the extent to which phenological shifts actually alter population persistence.
Despite a global footprint of shifts in flowering phenology in response to climate change, the reproductive consequences of these shifts are poorly understood. Furthermore, it is unknown whether altered flowering times affect plant population viability. We examine whether climate change‐induced earlier flowering has consequences for population persistence by incorporating reproductive losses from frost damage (a risk of early flowering) into population models of a subalpine sunflower (Helianthella quinquenervis). Using long‐term demographic data for three populations that span the species’ elevation range (8–15 years, depending on the population), we first examine how snowmelt date affects plant vital rates. To verify vital rate responses to snowmelt date experimentally, we manipulate snowmelt date with a snow removal experiment at one population. Finally, we construct stochastic population projection models and Life Table Response Experiments for each population. We find that populations decline (λs < 1) as snowmelt dates become earlier. Frost damage to flower buds, a consequence of climate change‐induced earlier flowering, does not contribute strongly to population declines. Instead, we find evidence that negative effects on survival, likely due to increased drought risk during longer growing seasons, drive projected population declines under earlier snowmelt dates. Synthesis. Shifts in flowering phenology are a conspicuous and important aspect of biological responses to climate change, but here we show that the phenology of reproductive events can be unreliable measures of threats to population persistence, even when earlier flowering is associated with substantial reproductive losses. Evidence for shifts in reproductive phenology, along with scarcer evidence that these shifts actually influence reproductive success, are valuable but can paint an incomplete and even misleading picture of plant population responses to climate change.
Males and females are ecologically distinct in many species, but whether responses to climate change are sex-specific is unknown. We document sex-specific responses to climate change in the plant Valeriana edulis (valerian) over four decades and across its 1800-meter elevation range. Increased elevation was associated with increased water availability and female frequency, likely owing to sex-specific water use efficiency and survival. Recent aridification caused male frequency to move upslope at 175 meters per decade, a rate of trait shift outpacing reported species' range shifts by an order of magnitude. This increase in male frequency reduced pollen limitation and increased seedset. Coupled with previous studies reporting sex-specific arthropod communities, these results underscore the importance of ecological differences between the sexes in mediating biological responses to climate change.
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