Does pollination interact with the abiotic environment to affect plant reproduction?

BACKGROUND AND AIMS: Abiotic and biotic components of the environment both limit plant reproduction, but how they interact with one another in combination is less understood. Understanding these interactions is especially relevant because abiotic and biotic environmental components respond differently to various global change drivers. Here we aim to understand whether the effects of pollination (biotic component) on plant reproduction depend on soil moisture (abiotic component), two factors known to affect plant reproduction and that are changing with global change. METHODS: We conducted pollen supplementation experiments for two plant species, Delphinium nuttallianum and Hydrophyllum fendleri, in subalpine meadows in the Western USA across four years that varied in soil moisture. In a separate one-year field experiment, we factorially crossed water addition with pollen supplementation. We measured proportion fruit set, seeds per fruit, and seeds per plant, in addition to stomatal conductance, to determine whether plant physiology responded to watering. KEY RESULTS: In the four-year study, only H. fendleri reproduction was pollen limited, and this occurred independently of soil moisture. Experimental water addition significantly increased soil moisture and stomatal conductance for both species. The effect of pollen addition on reproduction depended on the watering treatment only for H. fendleri fruit production. Reproduction in D. nuttallianum was not significantly affected by pollen addition or water addition, but it did respond to interannual variation in soil moisture. CONCLUSIONS: Although we find some evidence for the effect of a biotic interaction depending on abiotic conditions, it was only for one aspect of reproduction in one species, and it was in an unexpected direction. Our work highlights interactions between the abiotic and biotic components of the environment as an area of further research for improving our understanding of how plant reproduction responds to global change.

Genotype accounts for intraspecific variation in the timing and duration of multiple, sequential life-cycle events in a willow species.

PREMISE: Phenological variation among individuals within populations is common and has a variety of ecological and evolutionary consequences, including forming the basis for population-level responses to environmental change. Although the timing of life-cycle events has genetic underpinnings, whether intraspecific variation in the duration of life-cycle events reflects genetic differences among individuals is poorly understood. METHODS: We used a common garden experiment with 10 genotypes of Salix hookeriana (coastal willow) from northern California, United States to investigate the extent to which genetic variation explains intraspecific variation in the timing and duration of multiple, sequential life-cycle events: flowering, leaf budbreak, leaf expansion, fruiting, and fall leaf coloration. We used seven clones of each genotype, for a total of 70 individual trees. RESULTS: Genotype affected each sequential life-cycle event independently and explained on average 62% of the variation in the timing and duration of vegetative and reproductive life-cycle events. All events were significantly heritable. A single genotype tended to be "early" or "late" across life-cycle events, but for event durations, there was no consistent response within genotypes. CONCLUSIONS: This research demonstrates that genetic variation can be a major component underlying intraspecific variation in the timing and duration of life-cycle events. It is often assumed that the environment affects durations, but we show that genetic factors also play a role. Because the timing and duration of events are independent of one another, our results suggest that the effects of environmental change on one event will not necessarily cascade to subsequent events.

Effects of drought on grassland phenology depend on functional types.

Shifts in flowering phenology are important indicators of climate change. However, the role of precipitation in driving phenology is far less understood compared with other environmental cues, such as temperature. We use a precipitation reduction gradient to test the direction and magnitude of effects on reproductive phenology and reproduction across 11 plant species in a temperate grassland, a moisture-limited ecosystem. Our experiment was conducted in a single, relatively wet year. We examine the effects of precipitation for species, functional types, and the community. Our results provide evidence that reduced precipitation shifts phenology, alters flower and fruit production, and that the magnitude and direction of the responses depend on functional type and species. For example, early-blooming species shift toward earlier flowering, whereas later-blooming species shift toward later flowering. Because of opposing species-level shifts, there is no overall shift in community-level phenology. This study provides experimental evidence that changes in rainfall can drive phenological shifts. Our results additionally highlight the importance of understanding how plant functional types govern responses to changing climate conditions, which is relevant for forecasting phenology and community-level changes. Specifically, the implications of divergent phenological shifts between early- and late-flowering species include resource scarcity for pollinators and seed dispersers and new temporal windows for invasion.

Plant-pollinator interaction niche broadens in response to severe drought perturbations.

The composition of plant-pollinator interactions-i.e., who interacts with whom in diverse communities-is highly dynamic, and we have a very limited understanding of how interaction identities change in response to perturbations in nature. One prediction from niche and diet theory is that resource niches will broaden to compensate for resource reductions driven by perturbations, yet this has not been empirically tested in plant-pollinator systems in response to real-world perturbations in the field. Here, we use a long-term dataset of floral visitation to Ipomopsis aggregata, a montane perennial herb, to test whether the breadth of its floral visitation niche (i.e., flower visitor richness) changed in response to naturally occurring drought perturbations. Fewer floral resources are available in drought years, which could drive pollinators to expand their foraging niches, thereby expanding plants' floral visitation niches. We compared two drought years to three non-drought years to analyze changes in niche breadth and community composition of floral visitors to I. aggregata, predicting broadened niche breadth and distinct visitor community composition in drought years compared to non-drought years. We found statistically significant increases in niche breadth in drought years as compared to non-drought conditions, but no statistically distinguishable changes in community composition of flower visitors. Our findings suggest that plants' floral visitation niches may exhibit considerable plasticity in response to disturbance. This may have widespread consequences for community-level stability as well as functional consequences if increased niche overlap affects pollination services.

Snow melt timing acts independently and in conjunction with temperature accumulation to drive subalpine plant phenology.

Organisms use environmental cues to align their phenology-the timing of life events-with sets of abiotic and biotic conditions that favor the successful completion of their life cycle. Climate change has altered the environmental cues organisms use to track climate, leading to shifts in phenology with the potential to affect a variety of ecological processes. Understanding the drivers of phenological shifts is critical to predicting future responses, but disentangling the effects of temperature from precipitation on phenology is often challenging because they tend to covary. We addressed this knowledge gap in a high-elevation environment where phenological shifts are associated with both the timing of spring snow melt and temperature. We factorially crossed early snow melt and passive warming treatments to (1) disentangle the effects of snow melt timing and warming on the phenology of flowering and fruiting and reproductive success in three subalpine plant species (Delphinium nuttallianum, Valeriana edulis, and Potentilla pulcherrima); and (2) assess whether snow melt acts via temperature accumulation or some other aspect of the environment (e.g., soil moisture) to affect phenological events. Both the timing and duration of flowering and fruiting responded to the climate treatments, but the effect of snow melt timing and warming varied among species and phenological stages. The combined effects of the treatments on phenology were always additive, and the snow melt treatment often affected phenology even when the warming treatment did not. Despite marked responses of phenology to climate manipulations, the species showed little change in reproductive success, with only one species producing fewer seeds in response to warming (Delphinium, -56%). We also found that snow melt timing can act both through temperature accumulation and as a distinct cue for phenology, and these effects are not mutually exclusive. Our results show that one environmental cue, here snow melt timing, may act through multiple mechanisms to shift phenology.

Can flowers affect land surface albedo and soil microclimates?

The phenology of vegetation, namely leaf-out and senescence, can influence the Earth's climate over regional spatial scales and long time periods (e.g., over 30 years or more), in addition to microclimates over local spatial scales and shorter time periods (weeks to months). However, the effects of flowers on climate and microclimate are unknown. We investigate whether flowers can influence light reflected by the land surface and soil microclimate in a subalpine meadow. We conducted a flower removal experiment with a common sunflower species, Helianthella quinquenervis, for 3 years (2015, 2017, and 2019). The flower removal treatment simulates the appearance of the meadow when Helianthella flowers earlier under climate change and loses its flowers to frost (other plant structures are not damaged by frost). We test the hypotheses that a reduction in cover of yellow flowers leads to a greener land surface, lower reflectance, warmer and drier soils, and increased plant water stress. Flower removal plots are greener, reflect less light, exhibit up to 1.2 °C warmer soil temperatures during the warmest daylight hours, and contain ca. 1% less soil moisture compared to controls. However, soils were warmer in only 2 of the 3 years, when flower abundance was high. Helianthella water use efficiency did not differ between removal and control plots. Our study provides evidence for a previously undocumented effect of flowers on soil microclimate, an effect that is likely mediated by climate change and flowering phenology. Many anthropogenic environmental changes alter landscape albedo, all of which could be mediated by flowers: climate change, plant invasions, and agriculture. This study highlights how further consideration of the effects of flowers on land surface albedo could improve our understanding of the effects of vegetation on microclimate.

Lagged and dormant season climate better predict plant vital rates than climate during the growing season.

Understanding the effects of climate on the vital rates (e.g., survival, development, reproduction) and dynamics of natural populations is a long-standing quest in ecology, with ever-increasing relevance in the face of climate change. However, linking climate drivers to demographic processes requires identifying the appropriate time windows during which climate influences vital rates. Researchers often do not have access to the long-term data required to test a large number of windows, and are thus forced to make a priori choices. In this study, we first synthesize the literature to assess current a priori choices employed in studies performed on 104 plant species that link climate drivers with demographic responses. Second, we use a sliding-window approach to investigate which combination of climate drivers and temporal window have the best predictive ability for vital rates of four perennial plant species that each have over a decade of demographic data (Helianthella quinquenervis, Frasera speciosa, Cylindriopuntia imbricata, and Cryptantha flava). Our literature review shows that most studies consider time windows in only the year preceding the measurement of the vital rate(s) of interest, and focus on annual or growing season temporal scales. In contrast, our sliding-window analysis shows that in only four out of 13 vital rates the selected climate drivers have time windows that align with, or are similar to, the growing season. For many vital rates, the best window lagged more than 1 year and up to 4 years before the measurement of the vital rate. Our results demonstrate that for the vital rates of these four species, climate drivers that are lagged or outside of the growing season are the norm. Our study suggests that considering climatic predictors that fall outside of the most recent growing season will improve our understanding of how climate affects population dynamics.

The polar regions in a 2°C warmer world.

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.

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.

Responses of sequential and hierarchical phenological events to warming and cooling in alpine meadows.

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.

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

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.

Shifts in flowering phenology reshape a subalpine 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.

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.

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.

Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate.

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.

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.

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

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.