Effects of plant size and weather on the flowering phenology of the organ pipe cactus (Stenocereus thurberi)

Background and Aims

Flowering phenology is a critical life-history trait that influences reproductive success. It has been shown that genetic, climatic and other factors such as plant size affect the timing of flowering and its duration. The spatial and temporal variation in the reproductive phenology of the columnar cactus Stenocereus thurberi and its association with plant size and environmental cues was studied.

Methods

Flowering was monitored during 3 years in three populations of S. thurberi along a latitudinal gradient. Plant size was related to phenological parameters. The actual and past weather were used for each site and year to investigate the environmental correlates of flowering.

Key Results

There was significant variation in the timing of flowering within and among populations. Flowering lasted 4 months in the southern population and only 2 months in the northern population. A single flowering peak was evident in each population, but ocurred at different times. Large plants produced more flowers, and bloomed earlier and for a longer period than small plants. Population synchrony increased as the mean duration of flowering per individual decreased. The onset of flowering is primarily related to the variance in winter minimum temperatures and the duration to the autumn–winter mean maximum temperature, whereas spring mean maximum temperature is best correlated with synchrony.

Conclusions

Plant size affects individual plant fecundity as well as flowering time. Thus the population structure strongly affects flowering phenology. Indications of clinal variation in the timing of flowering and reproductive effort suggest selection pressures related to the arrival of migrating pollinators, climate and resource economy in a desert environment. These pressures are likely to be relaxed in populations where individual plants can attain large sizes.Key words: Flowering phenology, optimal timing, plant size, Sonoran Desert, Stenocereus thurberi, temperature     

Genetic and physiological bases for phenological responses to current and predicted climates

We are now reaching the stage at which specific genetic factors with known physiological effects can be tied directly and quantitatively to variation in phenology. With such a mechanistic understanding, scientists can better predict phenological responses to novel seasonal climates. Using the widespread model species Arabidopsis thaliana, we explore how variation in different genetic pathways can be linked to phenology and life-history variation across geographical regions and seasons. We show that the expression of phenological traits including flowering depends critically on the growth season, and we outline an integrated life-history approach to phenology in which the timing of later life-history events can be contingent on the environmental cues regulating earlier life stages. As flowering time in many plants is determined by the integration of multiple environmentally sensitive gene pathways, the novel combinations of important seasonal cues in projected future climates will alter how phenology responds to variation in the flowering time gene network with important consequences for plant life history. We discuss how phenology models in other systems—both natural and agricultural—could employ a similar framework to explore the potential contribution of genetic variation to the physiological integration of cues determining phenology.     

Earlier Migration Timing,Decreasing Phenotypic Variation,and Biocomplexity in Multiple Salmonid Species

Climate-induced phenological shifts can influence population, evolutionary, and ecological dynamics, but our understanding of these phenomena is hampered by a lack of long-term demographic data. We use a multi-decade census of 5 salmonid species representing 14 life histories in a warming Alaskan stream to address the following key questions about climate change and phenology: How consistent are temporal patterns and drivers of phenology for similar species and alternative life histories? Are shifts in phenology associated with changes in phenotypic variation? How do phenological changes influence the availability of resource subsidies? For most salmonid species, life stages, and life histories, freshwater temperature influences migration timing – migration events are occurring earlier in time (mean = 1.7 days earlier per decade over the 3–5 decades), and the number of days over which migration events occur is decreasing (mean = 1.5 days per decade). Temporal trends in migration timing were not correlated with changes in intra-annual phenotypic variation, suggesting that these components of the phenotypic distribution have responded to environmental change independently. Despite commonalities across species and life histories, there was important biocomplexity in the form of disparate shifts in migration timing and variation in the environmental factors influencing migration timing for alternative life history strategies in the same population. Overall, adult populations have been stable during these phenotypic and environmental changes (λ ≈1.0), but the temporal availability of salmon as a resource in freshwater has decreased by nearly 30 days since 1971 due to changes in the median date of migration timing and decreases in intra-annual variation in migration timing. These novel observations advance our understanding of phenological change in response to climate warming, and indicate that climate change has influenced the ecology of salmon populations, which will have important consequences for the numerous species that depend on this resource.     

Climate change and the risks associated with delayed breeding in a tropical wild bird population

There is growing evidence of changes in the timing of important ecological events, such as flowering in plants and reproduction in animals, in response to climate change, with implications for population decline and biodiversity loss. Recent work has shown that the timing of breeding in wild birds is changing in response to climate change partly because individuals are remarkably flexible in their timing of breeding. Despite this work, our understanding of these processes in wild populations remains very limited and biased towards species from temperate regions. Here, we report the response to changing climate in a tropical wild bird population using a long-term dataset on a formerly critically endangered island endemic, the Mauritius kestrel. We show that the frequency of spring rainfall affects the timing of breeding, with birds breeding later in wetter springs. Delays in breeding have consequences in terms of reduced reproductive success as birds get exposed to risks associated with adverse climatic conditions later on in the breeding season, which reduce nesting success. These results, combined with the fact that frequency of spring rainfall has increased by about 60 per cent in our study area since 1962, imply that climate change is exposing birds to the stochastic risks of late reproduction by causing them to start breeding relatively late in the season.     

Reproductive limits of a late-flowering high-mountain Mediterranean plant along an elevational climate gradient

Mountain plants are particularly sensitive to climate warming because snowmelt timing exerts a direct control on their reproduction. Current warming is leading to earlier snowmelt dates and longer snow-free periods. Our hypothesis is that high-mountain Mediterranean plants are not able to take advantage of a lengthened snow-free period because this leads to longer drought that truncates the growing season. However, reproductive timing may somewhat mitigate these negative effects through temporal shifts. We assessed the effects of flowering phenology on the reproductive success of Silene ciliata, a Mediterranean high-mountain plant, across an altitudinal gradient during two climatically contrasting years. The species showed a late-flowering pattern hampering the use of snowmelt water. Plant fitness was largely explained by the elapsed time from snowmelt to onset of flowering, suggesting a selective pressure towards early flowering caused by soil moisture depletion. The proportion of flowering plants decreased at the lowest population, especially in the drier year. Plants produced more flowers, fruits and seeds at the highest population and in the mild year. Our results indicate that water deficit in dry years could threaten the lowland populations of this mountainous species, while high-altitude environments are more stable over time.     

Evolution in stressful environments. I. Phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses

Considerable debate has accompanied efforts to integrate the selective impacts of environmental stresses into models of life-history evolution. This study was designed to determine if different environmental stresses have consistent phenotypic effects on life-history characters and whether selection under different stresses leads to consistent evolutionary responses. We created lineages of a wild mustard (Sinapis arvensis) that were selected for three generations under five stress regimes (high boron, high salt, low light, low water, or low nutrients) or under near-optimal conditions (control). Full-sibling families from the six selection histories were divided among the same six experimental treatments. In that test generation, lifetime plant fecundity and six phenotypic traits were measured for each plant. Throughout this greenhouse study, plants were grown individually and stresses were applied from the early seedling stage through senescence. Although all stresses consistently reduced lifetime fecundity and most size- and growth-related traits, different stresses had contrasting effects on flowering time. On average, stress delayed flowering compared to favorable conditions, although plants experiencing low nutrient stress flowered earliest and those experiencing low light flowered latest. Contrary to expectations of Grime's triangle model of life-history evolution, this ruderal species does not respond phenotypically to poor environments by flowering earlier. Most stresses enhanced the evolutionary potential of the study population. Compared with near-optimal conditions, stresses tended to increase the opportunity for selection as well as phenotypic variance, although both of these quantities were reduced in some stresses. Rather than favoring traits characteristic of stress tolerance, such as slow growth and delayed reproduction, phenotypic selection favored stress-avoidance traits: earlier flowering in all five stress regimes and faster seedling height growth in three stresses. Phenotypic correlations reinforced direct selection on these traits under stress, leading to predicted phenotypic change under stress, but no significant selection in the control environment. As a result of these factors, selection under stress resulted in an evolutionary shift toward earlier flowering. Environmental stresses may drive populations of ruderal plant species like S. arvensis toward a stress-avoidance strategy, rather than toward stress tolerance. Further studies will be needed to determine when selection in stressful environments leads to these alternative life-history strategies.     

A change in climate causes rapid evolution of multiple life-history traits and their interactions in an annual plant

Climate change is likely to spur rapid evolution, potentially altering integrated suites of life-history traits. We examined evolutionary change in multiple life-history traits of the annual plant Brassica rapa collected before and after a recent 5-year drought in southern California. We used a direct approach to examining evolutionary change by comparing ancestors and descendants. Collections were made from two populations varying in average soil moisture levels, and lines propagated from the collected seeds were grown in a greenhouse and experimentally subjected to conditions simulating either drought (short growing season) or high precipitation (long growing season) years. Comparing ancestors and descendants, we found that the drought caused many changes in life-history traits, including a shift to earlier flowering, longer duration of flowering, reduced peak flowering and greater skew of the flowering schedule. Descendants had thinner stems and fewer leaf nodes at the time of flowering than ancestors, indicating that the drought selected for plants that flowered at a smaller size and earlier ontogenetic stage rather than selecting for plants to develop more rapidly. Thus, there was not evidence for absolute developmental constraints to flowering time evolution. Common principal component analyses showed substantial differences in the matrix of trait covariances both between short and long growing season treatments and between populations. Although the covariances matrices were generally similar between ancestors and descendants, there was evidence for complex evolutionary changes in the relationships among the traits, and these changes depended on the population and treatment. These results show that a full appreciation of the impacts of global change on phenotypic evolution will entail an understanding of how changes in climatic conditions affect trait values and the structure of relationships among traits.     

Evolution under changing climates: climatic niche stasis despite rapid evolution in a non-native plant

A topic of great current interest is the capacity of populations to adapt genetically to rapidly changing climates, for example by evolving the timing of life-history events, but this is challenging to address experimentally. I use a plant invasion as a model system to tackle this question by combining molecular markers, a common garden experiment and climatic niche modelling. This approach reveals that non-native Lactuca serriola originates primarily from Europe, a climatic subset of its native range, with low rates of admixture from Asia. It has rapidly refilled its climatic niche in the new range, associated with the evolution of flowering phenology to produce clines along climate gradients that mirror those across the native range. Consequently, some non-native plants have evolved development times and grow under climates more extreme than those found in Europe, but not among populations from the native range as a whole. This suggests that many plant populations can adapt rapidly to changed climatic conditions that are already within the climatic niche space occupied by the species elsewhere in its range, but that evolution to conditions outside of this range is more difficult. These findings can also help to explain the prevalence of niche conservatism among non-native species.     

Network robustness and structure depend on the phenological characteristics of plants and pollinators

Many structural patterns have been found to be important for the stability and robustness of mutualistic plant–pollinator networks. These structural patterns are impacted by a suite of variables, including species traits, species abundances, their spatial configuration, and their phylogenetic history. Here, we consider a specific trait: phenology, or the timing of life history events. We expect that timing and duration of activity of pollinators, or of flowering in plants, could greatly affect the species'' roles within networks in which they are embedded. Using plant–pollinator networks from 33 sites in southern British Columbia, Canada, we asked (a) how phenological species traits, specifically timing of first appearance in the network and duration of activity in a network, were related to species'' roles within a network, and (b) how those traits affected network robustness to phenologically biased species loss. We found that long duration of activity increased connection within modules for both pollinators and plants and among modules for plants. We also found that date of first appearance was positively related to interaction strength asymmetry in plants but negatively related to pollinators. Networks were generally more robust to the loss of pollinators than plants, and robustness increased if the models allow new interactions to form when old ones are lost, constrained by overlapping phenology of plants and pollinators. Robustness declined with the loss of late‐flowering plants, which tended to have higher interaction strength asymmetry. In addition, robustness declined with loss of early‐flying or long‐duration pollinators. These pollinators tended to be among‐module connectors. Our results point to networks being limited by early‐flying pollinators. If plants flower earlier due to climate change, plant fitness may decline as they will depend on early emerging pollinators, unless pollinators also emerge earlier.     

What have two decades of laboratory life-history evolution studies onDrosophila melanogaster taught us?

A series of laboratory selection experiments onDrosophila melanogaster over the past two decades has provided insights into the specifics of life-history tradeoffs in the species and greatly refined our understanding of how ecology and genetics interact in life-history evolution. Much of what has been learnt from these studies about the subtlety of the microevolutionary process also has significant implications for experimental design and inference in organismal biology beyond life-history evolution, as well as for studies of evolution in the wild. Here we review work on the ecology and evolution of life-histories in laboratory populations ofD. melanogaster, emphasizing how environmental effects on life-history-related traits can influence evolutionary change. We discuss life-history tradeoffs—many unexpected—revealed by selection experiments, and also highlight recent work that underscores the importance to life-history evolution of cross-generation and cross-life-stage effects and interactions, sexual antagonism and sexual dimorphism, population dynamics, and the possible role of biological clocks in timing life-history events. Finally, we discuss some of the limitations of typical selection experiments, and how these limitations might be transcended in the future by a combination of more elaborate and realistic selection experiments, developmental evolutionary biology, and the emerging discipline of phenomics.     

Herbarium records identify sensitivity of flowering phenology of eucalypts to climate: Implications for species response to climate change

Flowering phenology is very sensitive to climate and with increasing global warming the flowering time of plants is shifting to earlier or later dates. Changes in flowering times may affect species reproductive success, associated phenological events, species synchrony, and community composition. Long‐term data on phenological events can provide key insights into the impacts of climate on phenology. For Australia, however, limited data availability restricts our ability to assess the impacts of climate change on plant phenology. To address this limitation other data sources must be explored such as the use of herbarium specimens to conduct studies on flowering phenology. This study uses herbarium specimens for investigating the flowering phenology of five dominant and commercially important Eucalyptus species of south‐eastern Australia and the consequences of climate variability and change on flowering phenology. Relative to precipitation and air humidity, mean temperature of the preceding 3 months was the most influential factor on the flowering time for all species. In response to a temperature increment of 1°C, a shift in the timing of flowering of 14.1–14.9 days was predicted for E. microcarpa and E. tricarpa while delays in flowering of 11.3–15.5 days were found for E. obliqua, E. radiata and E. polyanthemos. Eucalyptus polyanthemos exhibited the greatest sensitivity to climatic variables. The study demonstrates that herbarium data can be used to detect climatic signals on flowering phenology for species with a long flowering duration, such as eucalypts. The robust relationship identified between temperature and flowering phenology indicates that shifts in flowering times will occur under predicted climate change which may affect reproductive success, fitness, plant communities and ecosystems.     

Integrating candidate gene and quantitative genetic approaches to understand variation in timing of breeding in wild tit populations

Two commonly used techniques for estimating the effect of genes on traits in wild populations are the candidate gene approach and quantitative genetic analyses. However, whether these two approaches measure the same underlying processes remains unresolved. Here, we use these two methods to test whether they are alternative or complementary approaches to understanding genetic variation in the timing of reproduction - a key trait involved in adaptation to climate change - in wild tit populations. Our analyses of the candidate gene Clock show weak correlates with timing variables in blue tits, but no association in great tits, confirming earlier results. Quantitative genetic analyses revealed very low levels of both direct (female) and indirect (male) additive genetic variation in timing traits for both species, in contrast to previous studies on these traits, and much lower than generally assumed. Hence, neither method suggests strong genetic effects on the timing of breeding in birds, and further work should seek to assess the generality of these conclusions. We discuss how differences in the genetic control of traits, species life-history and confounding environmental variables may determine how useful integrating these two techniques is to understand the phenotypic variation in wild populations.     

Photographs and herbarium specimens as tools to document phenological changes in response to global warming

Global warming is affecting natural systems across the world. Of the biological responses to warming, changes in the timing of phenological events such as flowering are among the most sensitive. Despite the recognized importance of phenological changes, the limited number of long-term records of phenological events has restricted research on the topic in most areas of the world. In a previous study in Boston (American Journal of Botany 91: 1260-1264), we used herbarium specimens and one season of field observations to show that plants flowered earlier as the climate warmed over the past 100 yr. In our new study, we found that two extra years of data did not strengthen the explanatory power of the analysis. Analysis of herbarium specimens without any field data yielded results similar to analyses that included field observations. In addition, we found that photographs of cultivated and wild plants in Massachusetts, data similar to that contained in herbarium specimens, show changes in flowering times that closely match independent data on the same species in the same locations. Dated photographs of plants in flower represent a new resource to extend the range of species and localities addressed in global-warming research.     

Disparity in Onset Timing and Frequency of Flowering and Fruiting Events in Two Bornean Peat‐Swamp Forests

The timing and frequency of flowering and fruiting events are key tropical forest characteristics that have substantial influence on fauna. Although our understanding of geographic variation in habitat‐wide timing and frequency of flowering and fruiting is advancing, corresponding information for individual tree species is limited. Thus, we compared climate and reproductive phenology of 16 tree species over 70 mo at two Bornean tropical peat‐swamp forest sites. We found significant inter‐site correlations in rainfall and temperature, and only small absolute temperature differences. In both sites, most species exhibited within‐site synchrony in flowering and fruiting onset. Broad‐scale flowering and fruiting onset frequency classifications showed high congruence between sites. Significant correlations in flowering and fruiting onset timing between sites were found for only 19 and 17 percent of the species, respectively. This remained the case when applying 1‐ and 2‐month lag periods for both sites, with neither site consistently lagging behind. Significant differences in the exact frequency of new flowering and fruiting events were detected for 44 and 58 percent of species, respectively, and no significant relationships between the onset timing synchrony and exact frequency of new reproductive events were found for either flowers or fruit. We conclude that inter‐site climatic and ecological similarities do not necessarily lead to high inter‐site synchrony in either onset timing or exact frequency of tree reproductive events. Potential reasons for this are discussed, as are the implications for understanding tropical forest ecology and improving forest restoration project seed collections.     

A Range-Expanding Shrub Species Alters Plant Phenological Response to Experimental Warming

Shifts in plant species phenology (the timing of life-history events such as flowering) have been observed worldwide in concert with rising global temperatures. While most species display earlier phenology with warming, there is large variation among, and even within, species in phenological sensitivity to rising temperatures. Other indirect effects of climate change, such as shifting species composition and altered species interactions, may also be contributing to shifting plant phenology. Here, we describe how experimental warming and the presence of a range-expanding species, sagebrush (Artemisia rothrockii), interact to influence the flowering phenology (day of first and peak flowering) and production (number of flowers) of an alpine cushion plant, Trifolium andersonii, in California’s White Mountains. Both first flowering and peak flowering were strongly accelerated by warming, but not when sagebrush was present. Warming significantly increased flower production of T. andersonii, but less so in the presence of sagebrush. A shading treatment delayed phenology and lowered flower production, suggesting that shading may be the mechanism by which sagebrush presence delayed flowering of the understory species. This study demonstrates that species interactions can modify phenological responses to climate change, and suggests that indirect effects of rising temperatures arising from shifting species ranges and altered species interactions may even exceed the direct effects of rising temperatures on phenology.     

Life-history traits of lake plankton species may govern their phenological response to climate warming

A prominent response of temperate aquatic ecosystems to climate warming is changes in phenology – advancements or delays in annually reoccurring events in an organism's life cycle. The exact seasonal timing of warming, in conjunction with species-specific life-history events such as emergence from resting stages, timing of spawning, generation times, or stage-specific prey requirements, may determine the nature of a species' response. We demonstrate that recent climate-induced shifts in the phenology of lake phytoplankton and zooplankton species in a temperate eutrophic lake (Müggelsee, Germany) differed according to differences in their characteristic life cycles. Fast-growing plankton in spring (diatoms, Daphnia ) showed significant and synchronous forward movements by about 1 month, induced by concurrent earlier ice break-up dates (diatoms) and higher spring water temperature ( Daphnia ). No such synchrony was observed for slow-growing summer zooplankton species with longer and more complex life cycles (copepods, larvae of the mussel Dreissena polymorpha ). Although coexisting, the summer plankton responded species specifically to seasonal warming trends, depending on whether the timing of warming matched their individual thermal requirements at decisive developmental stages such as emergence from diapause (copepods), or spawning ( Dreissena ). Others did not change their phenology significantly, but nevertheless, increased in abundances. We show that the detailed seasonal pattern of warming influences the response of phyto- and zooplankton species to climate change, and point to the diverse nature of responses for species exhibiting complex life-history traits.     

Climatic Variability Leads to Later Seasonal Flowering of Floridian Plants

Understanding species responses to global change will help predict shifts in species distributions as well as aid in conservation. Changes in the timing of seasonal activities of organisms over time may be the most responsive and easily observable indicator of environmental changes associated with global climate change. It is unknown how global climate change will affect species distributions and developmental events in subtropical ecosystems or if climate change will differentially favor nonnative species. Contrary to previously observed trends for earlier flowering onset of plant species with increasing spring temperatures from mid and higher latitudes, we document a trend for delayed seasonal flowering among plants in Florida. Additionally, there were few differences in reproductive responses by native and nonnative species to climatic changes. We argue that plants in Florida have different reproductive cues than those from more northern climates. With global change, minimum temperatures have become more variable within the temperate-subtropical zone that occurs across the peninsula and this variation is strongly associated with delayed flowering among Florida plants. Our data suggest that climate change varies by region and season and is not a simple case of species responding to consistently increasing temperatures across the region. Research on climate change impacts need to be extended outside of the heavily studied higher latitudes to include subtropical and tropical systems in order to properly understand the complexity of regional and seasonal differences of climate change on species responses.     

Stochastic flowering phenology in Dactylis glomerata populations described by Markov chain modelling

Understanding the relationship between flowering patterns and pollen dispersal is important in climate change modelling, pollen forecasting, forestry and agriculture. Enhanced understanding of this connection can be gained through detailed spatial and temporal flowering observations on a population level, combined with modelling simulating the dynamics. Species with large distribution ranges, long flowering seasons, high pollen production and naturally large populations can be used to illustrate these dynamics. Revealing and simulating species-specific demographic and stochastic elements in the flowering process will likely be important in determining when pollen release is likely to happen in flowering plants. Spatial and temporal dynamics of eight populations of Dactylis glomerata were collected over the course of two years to determine high-resolution demographic elements. Stochastic elements were accounted for using Markov chain approaches in order to evaluate tiller-specific contribution to overall population dynamics. Tiller-specific developmental dynamics were evaluated using three different RV matrix correlation coefficients. We found that the demographic patterns in population development were the same for all populations with key phenological events differing only by a few days over the course of the seasons. Many tillers transitioned very quickly from non-flowering to full flowering, a process that can be replicated with Markov chain modelling. Our novel approach demonstrates the identification and quantification of stochastic elements in the flowering process of D. glomerata, an element likely to be found in many flowering plants. The stochastic modelling approach can be used to develop detailed pollen release models for Dactylis, other grass species and probably other flowering plants.

     

The phenology of growth and reproduction in plants

The study of phenological aspects of plants involves the observation, recording and interpretation of the timing of their life history events. This review considers the phenology of leafing, flowering and fruit production in a range of species and communities. The selective forces (both abiotic and biotic) that influence the timing of these events are discussed. Within the limits imposed by phylogenetic constraints, the phenological patterns (timing, frequency, duration, degree of synchrony, etc.) of each phase are probably the result of a compromise between a variety of selective pressures, such as seasonal climatic changes, resource availability, and the presence of pollinators, predators and seed dispersers. Many studies on flowering times stress the role of interactions between plant species which share pollinators or predators. The timing of fruiting plays a key role in controlling the abundance and variety of obligate frugivores in many tropical communities. The importance of long-term recording is stressed, particularly in species which fruit irregularly. An understanding of the phenology of plants is crucial to the understanding of community function and diversity.     

Selection on flowering time in Mediterranean high-mountain plants under global warming

Under climate warming, plants will undergo novel selective pressures to adjust reproductive timing. Adjustment between reproductive phenology and environment is expected to be higher in arctic and alpine habitats because the growing season is considerably short. As early- and late-flowering species reproduce under very different environmental conditions, selective pressures on flowering phenology and potential effects of climate change are likely to differ between them. However, there is no agreement on the magnitude of the benefits and costs of early- vs. late-flowering species under a global warming scenario. In spite of its relevance, phenotypic selection on flowering phenology has rarely been explored in alpine plants and never in Mediterranean high mountain species, where selective pressures are very different due to the summer drought imposed over the short growth season. We hypothesized that late-flowering plants in Mediterranean mountains should present stronger selective pressures towards early onset of reproduction than early-flowering species, because less water is available in the soil as growing season progresses. We performed selection analyses on flowering onset and duration in two high mountain species of contrasting phenology. Since phenotypic selection can be highly context-dependent, we studied several populations of each species for 2 years, covering their local altitudinal ranges and their different microhabitats. Surrogates of biotic selective agents, like fruitset for pollinators and flower and fruit loss for flower and seed predators, were included in the analysis. Differences between the early- and the late-flowering species were less than expected. A consistent negative correlational selection of flowering onset and duration was found affecting plant fitness, i.e., plants that bloomed earlier flowered for longer periods improving plant fitness. Nevertheless, the late-flowering species may experience higher risks under climate warming because in extremely warm and dry years the earlier season does not bring about a longer flowering duration due to summer drought.