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

Abstract 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 longterm 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 longterm 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 climateinduced phenological shifts has focused on terrestrial pairwise resourceconsumer interactions, especially those between plants and insects

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

Data from: Experimental warming in the field delays phenology and reduces body mass and survival: implications for the persistence of a pollinator under climate change

1. Climate change is rapidly altering thermal environments across the globe. The effects of increased temperatures in already warm environments may be particularly strong because organisms are likely to be near their thermal safety margins, with limited tolerance to additional heat stress. 2. We conduct an in situ field experiment over two years to investigate the direct effects of temperature on an early-season solitary bee in a warm, arid region of the Southwestern USA. Our field experiment manipulates the thermal environment of Osmia ribifloris (Megachilidae) from larval development through adult emergence, simulating both previous cooler (ca. 1950; nest boxes painted white), and future warmer (2040–2099; nest boxes painted black) climate conditions. In each year we measure adult emergence phenology, linear body size, body mass, fat content, and survival. 3. Bees in the warming treatment exhibit delayed emergence and a substantial increase in phenological variance. Increases in temperature also lead to reductions in body mass and fat content. Whereas bees in the cooling and control treatments experience negligible amounts of mortality, bees in the warming treatment experience 30–75% mortality. 4. Our findings indicate that temperature changes that have occurred since ca. 1950 have likely had relatively weak and non-negative effects, but predicted warmer temperatures create a high stress thermal environment for O. ribifloris. Later and more variable emergence dates under warming likely compromise phenological synchrony with floral resources and the ability of individuals to find mates. The consequences of phenological asynchrony, combined with reductions in body mass and fat content, will likely impose fitness reductions in surviving bees. Combined with high rates of mortality, our results suggest that O. ribifloris may face local extirpation in the warmer parts of its range within the century. 5. Temperature increases in already warm ecosystems can have substantial consequences for key components of life history, physiology, and survival. Our study suggests that the response of ectothermic insects to temperature increases in already warm environments may be insufficient to mitigate the negative consequences of future warming

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

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

1. 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. 2. 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) in 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. 3. 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. 4. 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

Data from: 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 1800m elevation range. Increased elevation was associated with increased water availability and female frequency, likely due to sex-specific water use efficiency and survival. Recent aridification caused male frequency to move up-slope at 175 m/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

Species range shifts in response to climate change

Data for meta-analysis of montane plant species range shifts in response to climate change

Integrated water use efficiency by sex in four population of Valeriana edulis

Carbon isotope ratios of Valeriana edulis leaf samples used to test for sex differences in integrated water use efficiency. See README.txt for column descriptions