Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment (original) (raw)

Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change

Proceedings. Biological sciences / The Royal Society, 2012

Anthropogenic climate change has already altered the timing of major life-history transitions, such as the initiation of reproduction. Both phenotypic plasticity and adaptive evolution can underlie rapid phenological shifts in response to climate change, but their relative contributions are poorly understood. Here, we combine a continuous 38 year field survey with quantitative genetic field experiments to assess adaptation in the context of climate change. We focused on Boechera stricta (Brassicaeae), a mustard native to the US Rocky Mountains. Flowering phenology advanced significantly from 1973 to 2011, and was strongly associated with warmer temperatures and earlier snowmelt dates. Strong directional selection favoured earlier flowering in contemporary environments (2010 -2011). Climate change could drive this directional selection, and promote even earlier flowering as temperatures continue to increase. Our quantitative genetic analyses predict a response to selection of 0.2 to 0.5 days acceleration in flowering per generation, which could account for more than 20 per cent of the phenological change observed in the long-term dataset. However, the strength of directional selection and the predicted evolutionary response are likely much greater now than even 30 years ago because of rapidly changing climatic conditions. We predict that adaptation will likely be necessary for long-term in situ persistence in the context of climate change.

Region‐specific phenological sensitivities and rates of climate warming generate divergent temporal shifts in flowering date across a species' range

American Journal of Botany, 2021

Forecasting how species will respond phenologically to future changes in climate is a major challenge. Many studies have focused on estimating species-and community-wide phenological sensitivities to climate to make such predictions, but sensitivities may vary within species, which could result in divergent phenological responses to climate change. Methods: We used 743 herbarium specimens of the mountain jewelflower (Streptanthus tortuosus, Brassicaceae) collected over 112 years to investigate whether individuals sampled from relatively warm vs. cool regions differ in their sensitivity to climate and whether this difference has resulted in divergent phenological shifts in response to climate warming. Results: During the past century, individuals sampled from warm regions exhibited a 20-day advancement in flowering date; individuals in cool regions showed no evidence of a shift. We evaluated two potential drivers of these divergent responses: differences between regions in (1) the degree of phenological sensitivity to climate and (2) the magnitude of climate change experienced by plants, or (3) both. Plants sampled from warm regions were more sensitive to temperature-related variables and were subjected to a greater degree of climate warming than those from cool regions; thus our results suggest that the greater temporal shift in flowering date in warm regions is driven by both of these factors. Conclusions: Our results are among the first to demonstrate that species exhibited intraspecific variation in sensitivity to climate and that this variation can contribute to divergent responses to climate change. Future studies attempting to forecast temporal shifts in phenology should consider intraspecific variation.

SUBALPINE MEADOW FLOWERING PHENOLOGY RESPONSES TO CLIMATE CHANGE: INTEGRATING EXPERIMENTAL AND GRADIENT METHODS

Ecological Monographs, 2003

We integrated experimental and natural gradient field methods to investigate effects of climate change and variability on flowering phenology of 11 subalpine meadow shrub, forb, and graminoid species in Gunnison County, Colorado (USA). At a subalpine meadow site, overhead electric radiant heaters advanced snowmelt date by 16 d and warmed and dried soil during the growing season. At three additional sites, a snow removal manipulation advanced snowmelt date by 7 d without altering growing season soil microclimate. We compared phenological responses to experimental climate change with responses to natural microclimate variability across spatial gradients at small and landscape scales, as well as across a temporal gradient from a separate study.

Will phenotypic plasticity affecting flowering phenology keep pace with climate change?

Global Change Biology, 2016

Rising temperatures have begun to shift flowering time, but it is unclear whether phenotypic plasticity can accommodate projected temperature change for this century. Evaluating clines in phenological traits and the extent and variation in plasticity can provide key information on assessing risk of maladaptation and developing strategies to mitigate climate change. In this study, flower phenology was examined in 52 populations of big sagebrush (Artemisia tridentata) growing in three common gardens. Flowering date (anthesis) varied 91 days from late July to late November among gardens. Mixed‐effects modeling explained 79% of variation in flowering date, of which 46% could be assigned to plasticity and genetic variation in plasticity and 33% to genetics (conditional R2 = 0.79, marginal R2 = 0.33). Two environmental variables that explained the genetic variation were photoperiod and the onset of spring, the Julian date of accumulating degree‐days >5 °C reaching 100. The genetic vari...

Variation in the impact of climate change on flowering phenology and abundance: An examination of two pairs of closely related wildflower species

American journal of botany, 2009

Variability in plant phenological responses to climate change is likely to lead to changes in many ecological relationships as the climate continues to change. We used a 34-yr record of fl owering times and fl ower abundance for four species (two Delphinium [Ranunculaceae] species and two Mertensia [Boraginaceae] species) from a subalpine plant community near the Rocky Mountain Biological Laboratory to test the hypothesis that the phenologies of early-fl owering species change more rapidly in response to climatological and other abiotic cues than do late-fl owering species, a pattern previously found in plant communities in North America and Europe. We also explored a related hypothesis, that fl ower abundance of late-fl owering species is more responsive to changes in climate than that of early-fl owering species. The Delphinium species did not support these hypotheses, but the Mertensia species did. The difference between the peak fl owering times of the early and late Mertensia species is expanding, leading to a period of diminished resources for pollinators that specialize on this genus. Mertensia ciliata populations are already severely declining in our study area, possibly as a result of earlier snowmelt. Together, these results show that the reported differences between early-and late-fl owering species may be widespread, but they are not ubiquitous.

Divergent responses to spring and winter warming drive community level flowering trends

Proceedings of the National Academy of Sciences of the United States of America, 2012

Analyses of datasets throughout the temperate midlatitude regions show a widespread tendency for species to advance their springtime phenology, consistent with warming trends over the past 20-50 y. Within these general trends toward earlier spring, however, are species that either have insignificant trends or have delayed their timing. Various explanations have been offered to explain this apparent nonresponsiveness to warming, including the influence of other abiotic cues (e.g., photoperiod) or reductions in fall/winter chilling (vernalization). Few studies, however, have explicitly attributed the historical trends of nonresponding species to any specific factor. Here, we analyzed long-term data on phenology and seasonal temperatures from 490 species on two continents and demonstrate that (i) apparent nonresponders are indeed responding to warming, but their responses to fall/winter and spring warming are opposite in sign and of similar magnitude; (ii) observed trends in first flow...

Reproductive losses due to climate change‐induced earlier flowering are not the primary threat to plant population viability in a perennial herb

Journal of Ecology, 2019

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 popul...

Diverse Developmental Responses to Warming Temperatures Underlie Changes in Flowering Phenologies

Integrative and Comparative Biology, 2019

Climate change has resulted in increased temperature means across the globe. Many angiosperms flower earlier in response to rising temperature and the phenologies of these species are reasonably well predicted by models that account for spring (early growing season) and winter temperatures. Surprisingly, however, exceptions to the general pattern of precocious flowering are common. Many species either do not appear to respond or even delay flowering in, or following, warm growing seasons. Existing phenological models have not fully addressed such exceptions to the common association of advancing phenologies with warming temperatures. The phenological events that are typically recorded (e.g., onset of flowering) are but one phase in a complex developmental process that often begins one or more years previously, and flowering time may be strongly influenced by temperature over the entire multi-year course of flower development. We propose a series of models that explore effects of growing-season temperature increase on the multiple processes of flower development and how changes in development may impact the timing of anthesis. We focus on temperate forest trees, which are characterized by preformation, the initiation of flower primordia one or more years prior to anthesis. We then synthesize the literature on flower development to evaluate the models. Although fragmentary, the existing data suggest the potential for temperature to affect all aspects of flower development in woody perennials. But, even for relatively well studied taxa, the critical developmental responses that underlie phenological patterns are difficult to identify. Our proposed models explain the seemingly counter-intuitive observations that warmer growingseason temperatures delay flowering in many species. Future research might concentrate on taxa that do not appear to respond to temperature, or delay flowering in response to warm temperatures, to understand what processes contribute to this pattern.