Amy M. Iler

Shifts in flowering phenology reshape a subalpine plant community

Significance Seasonal timing of biological events, phenology, is one of the strongest bioindicators of climate change. Our general understanding of phenological responses to climate change is based almost solely on the first day on which an event is observed, limiting our understanding of how ecological communities may be responding as a whole. Using a unique long-term record of flowering phenology from Colorado, we find that the number of species changing their flowering times likely has been underestimated and the magnitude of phenological change overestimated. In addition to earlier first flowering, we document a diverse assortment of other changes, such as delayed last flowering, as temperatures warm. This variety of species-level phenological shifts has ultimately reshaped various temporal components of the plant community. 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.

Nonlinear flowering responses to climate: are species approaching their limits of phenological change?

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.

Phenological overlap of interacting species in a changing climate: an assessment of available approaches.

Concern regarding the biological effects of climate change has led to a recent surge in research to understand the consequences of phenological change for species interactions. This rapidly expanding research program is centered on three lines of inquiry: (1) how the phenological overlap of interacting species is changing, (2) why the phenological overlap of interacting species is changing, and (3) how the phenological overlap of interacting species will change under future climate scenarios. We synthesize the widely disparate approaches currently being used to investigate these questions: (1) interpretation of long-term phenological data, (2) field observations, (3) experimental manipulations, (4) simulations and nonmechanistic models, and (5) mechanistic models. We present a conceptual framework for selecting approaches that are best matched to the question of interest. We weigh the merits and limitations of each approach, survey the recent literature from diverse systems to quantify their use, and characterize the types of interactions being studied by each of them. We highlight the value of combining approaches and the importance of long-term data for establishing a baseline of phenological synchrony. Future work that scales up from pairwise species interactions to communities and ecosystems, emphasizing the use of predictive approaches, will be particularly valuable for reaching a broader understanding of the complex effects of climate change on the phenological overlap of interacting species. It will also be important to study a broader range of interactions: to date, most of the research on climate-induced phenological shifts has focused on terrestrial pairwise resource–consumer interactions, especially those between plants and insects.

Long-term trends mask variation in the direction and magnitude of short-term phenological shifts

PREMISE OF THE STUDY Plants are flowering earlier in response to climate change. However, substantial interannual variation in phenology may make it difficult to discern and compare long-term trends. In addition to providing insight on data requirements for discerning such trends, phenological shifts within subsets of long-term records will provide insight into the mechanisms driving changes in flowering over longer time scales. METHODS To examine variation in flowering shifts among temporal subsets of long-term records, we used two data sets of flowering phenology from snow-dominated habitats: subalpine meadow in Gothic, Colorado, USA (38 yr), and arctic tundra in Zackenberg, Greenland (16 yr). Shifts in flowering time were calculated as 10-yr moving averages for onset, peak, and end of flowering. KEY RESULTS Flowering advanced over the course of the entire time series at both sites. Flowering shifts at Gothic were variable, with some 10-yr time frames showing significant delays and others significant advancements. Early-flowering species were more responsive than later-flowering species, while the opposite was true at Zackenberg. Flowering shifts at Zackenberg were less variable, with advanced flowering across all 10-yr time frames. At both sites, long-term advancement seemed to be primarily driven by strong advancements in flowering in the 1990s and early 2000s. CONCLUSIONS Analysis of long-term trends can mask substantial variation in phenological shifts through time. This variation in the direction and magnitude of phenological shifts has implications for the evolution of flowering time and for interspecific interactions with flowering plants and can provide more detailed insights into the dynamics of phenological responses to climate change.

Sex-specific responses to climate change in plants alter population sex ratio and performance

Changing sex ratios Climate-warming temperatures might be expected to affect the sex ratio of species if sex determination is temperature-dependent. Petry et al. show that indirect climate effects could also alter sex ratios in species in which sex is genetically determined and damage reproductive fitness (see the Perspective by Etterson and Mazer). Over four decades, sex ratios in populations of a dioecious alpine plant have shifted toward females as a result of the different water needs of the male and female plants. The lack of males has reduced the reproductive success and fitness of the females. Similar subtle differences between sexes in environmental sensitivities could eventually lead to population declines. Science, this issue p. 69; see also p. 32 Over the past 40 years, differences in responses of male and female alpine valerian plants to changing climate have changed their relative numbers. 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.

Effects of climate change on mast-flowering cues in a clonal montane herb, Veratrum tenuipetalum (Melanthiaceae)

UNLABELLED PREMISE OF THE STUDY Climate change threatens to alter the timing and magnitude of abiotic cues that synchronize mast flowering, such as temperature and precipitation. Climate change may therefore alter the frequency of masting, in turn affecting species in the community that use pulsed resources. • METHODS We used 29-yr (1984-2012) records of climate and flowering to investigate proximate flowering cues for the clonal, mast-flowering herb Veratrum tenuipetalum. Because clonal reproduction is tied to flowering in Veratrum, we used a parallel record of ramet abundance to examine the effects of masting on long-term ramet abundance. • KEY RESULTS Cool summer temperatures 2 years before flowering were associated with a higher percentage of flowering in Veratrum populations, consistent with its life history. Ramet abundance increased by 9.5% ± 5.6% on average following mast years compared to an average loss of 0.73% ± 1.1% in nonmast years, and ramet abundance increased over the time frame of our records. • CONCLUSIONS Ramet abundance has increased over the time frame of our records mainly because of clonal reproduction in masting years. If summer temperatures continue to increase at our site and Veratrum does not alter its climate thresholds, we predict that masting will become less frequent in this species, with consequent reduction in opportunities for both sexual and clonal reproduction.

Detrending phenological time series improves climate–phenology analyses and reveals evidence of plasticity

Time series have played a critical role in documenting how phenology responds to climate change. However, regressing phenological responses against climatic predictors involves the risk of finding potentially spurious climate-phenology relationships simply because both variables also change across years. Detrending by year is a way to address this issue. Additionally, detrending isolates interannual variation in phenology and climate, so that detrended climate-phenology relationships can represent statistical evidence of phenotypic plasticity. Using two flowering phenology time series from Colorado, USA and Greenland, we detrend flowering date and two climate predictors known to be important in these ecosystems: temperature and snowmelt date. In Colorado, all climate-phenology relationships persist after detrending. In Greenland, 75% of the temperature-phenology relationships disappear after detrending (three of four species). At both sites, the relationships that persist after detrending suggest that plasticity is a major component of sensitivity of flowering phenology to climate. Finally, simulations that created different strengths of correlations among year, climate, and phenology provide broader support for our two empirical case studies. This study highlights the utility of detrending to determine whether phenology is related to a climate variable in observational data sets. Applying this as a best practice will increase our understanding of phenological responses to climatic variation and change.