Diversity buffers winegrowing regions from climate change losses.

Agrobiodiversity-the variation within agricultural plants, animals, and practices-is often suggested as a way to mitigate the negative impacts of climate change on crops [S. A. Wood et al., Trends Ecol. Evol. 30, 531-539 (2015)]. Recently, increasing research and attention has focused on exploiting the intraspecific genetic variation within a crop [Hajjar et al., Agric. Ecosyst. Environ. 123, 261-270 (2008)], despite few relevant tests of how this diversity modifies agricultural forecasts. Here, we quantify how intraspecific diversity, via cultivars, changes global projections of growing areas. We focus on a crop that spans diverse climates, has the necessary records, and is clearly impacted by climate change: winegrapes (predominantly Vitis vinifera subspecies vinifera). We draw on long-term French records to extrapolate globally for 11 cultivars (varieties) with high diversity in a key trait for climate change adaptation-phenology. We compared scenarios where growers shift to more climatically suitable cultivars as the climate warms or do not change cultivars. We find that cultivar diversity more than halved projected losses of current winegrowing areas under a 2 °C warming scenario, decreasing areas lost from 56 to 24%. These benefits are more muted at higher warming scenarios, reducing areas lost by a third at 4 °C (85% versus 58%). Our results support the potential of in situ shifting of cultivars to adapt agriculture to climate change-including in major winegrowing regions-as long as efforts to avoid higher warming scenarios are successful.

Rethinking false spring risk.

Temperate plants are at risk of being exposed to late spring freezes. These freeze events-often called false springs-are one of the strongest factors determining temperate plants species range limits and can impose high ecological and economic damage. As climate change may alter the prevalence and severity of false springs, our ability to forecast such events has become more critical, and it has led to a growing body of research. Many false spring studies largely simplify the myriad complexities involved in assessing false spring risks and damage. While these studies have helped advance the field and may provide useful estimates at large scales, studies at the individual to community levels must integrate more complexity for accurate predictions of plant damage from late spring freezes. Here, we review current metrics of false spring, and how, when, and where plants are most at risk of freeze damage. We highlight how life stage, functional group, species differences in morphology and phenology, and regional climatic differences contribute to the damage potential of false springs. More studies aimed at understanding relationships among species tolerance and avoidance strategies, climatic regimes, and the environmental cues that underlie spring phenology would improve predictions at all biological levels. An integrated approach to assessing past and future spring freeze damage would provide novel insights into fundamental plant biology and offer more robust predictions as climate change progresses, which are essential for mitigating the adverse ecological and economic effects of false springs.

Global shifts in the phenological synchrony of species interactions over recent decades.

Phenological responses to climate change (e.g., earlier leaf-out or egg hatch date) are now well documented and clearly linked to rising temperatures in recent decades. Such shifts in the phenologies of interacting species may lead to shifts in their synchrony, with cascading community and ecosystem consequences. To date, single-system studies have provided no clear picture, either finding synchrony shifts may be extremely prevalent [Mayor SJ, et al. (2017) Sci Rep 7:1902] or relatively uncommon [Iler AM, et al. (2013) Glob Chang Biol 19:2348-2359], suggesting that shifts toward asynchrony may be infrequent. A meta-analytic approach would provide insights into global trends and how they are linked to climate change. We compared phenological shifts among pairwise species interactions (e.g., predator-prey) using published long-term time-series data of phenological events from aquatic and terrestrial ecosystems across four continents since 1951 to determine whether recent climate change has led to overall shifts in synchrony. We show that the relative timing of key life cycle events of interacting species has changed significantly over the past 35 years. Further, by comparing the period before major climate change (pre-1980s) and after, we show that estimated changes in phenology and synchrony are greater in recent decades. However, there has been no consistent trend in the direction of these changes. Our findings show that there have been shifts in the timing of interacting species in recent decades; the next challenges are to improve our ability to predict the direction of change and understand the full consequences for communities and ecosystems.

Shifting regimes and changing interactions in the Lake Washington, U.S.A., plankton community from 1962-1994.

Understanding how changing climate, nutrient regimes, and invasive species shift food web structure is critically important in ecology. Most analytical approaches, however, assume static species interactions and environmental effects across time. Therefore, we applied multivariate autoregressive (MAR) models in a moving window context to test for shifting plankton community interactions and effects of environmental variables on plankton abundance in Lake Washington, U.S.A. from 1962-1994, following reduced nutrient loading in the 1960s and the rise of Daphnia in the 1970s. The moving-window MAR (mwMAR) approach showed shifts in the strengths of interactions between Daphnia, a dominant grazer, and other plankton taxa between a high nutrient, Oscillatoria-dominated regime and a low nutrient, Daphnia-dominated regime. The approach also highlighted the inhibiting influence of the cyanobacterium Oscillatoria on other plankton taxa in the community. Overall community stability was lowest during the period of elevated nutrient loading and Oscillatoria dominance. Despite recent warming of the lake, we found no evidence that anomalous temperatures impacted plankton abundance. Our results suggest mwMAR modeling is a useful approach that can be applied across diverse ecosystems, when questions involve shifting relationships within food webs, and among species and abiotic drivers.

Phenological niches and the future of invaded ecosystems with climate change.

In recent years, research in invasion biology has focused increasing attention on understanding the role of phenology in shaping plant invasions. Multiple studies have found non-native species that tend to flower distinctly early or late in the growing season, advance more with warming or have shifted earlier with climate change compared with native species. This growing body of literature has focused on patterns of phenological differences, but there is a need now for mechanistic studies of how phenology contributes to invasions. To do this, however, requires understanding how phenology fits within complex functional trait relationships. Towards this goal, we review recent literature linking phenology with other functional traits, and discuss the role of phenology in mediating how plants experience disturbance and stress-via climate, herbivory and competition-across the growing season. Because climate change may alter the timing and severity of stress and disturbance in many systems, it could provide novel opportunities for invasion-depending upon the dominant climate controller of the system, the projected climate change, and the traits of native and non-native species. Based on our current understanding of plant phenological and growth strategies-especially rapid growing, early-flowering species versus later-flowering species that make slower-return investments in growth-we project optimal periods for invasions across three distinct systems under current climate change scenarios. Research on plant invasions and phenology within this predictive framework would provide a more rigorous test of what drives invader success, while at the same time testing basic plant ecological theory. Additionally, extensions could provide the basis to model how ecosystem processes may shift in the future with continued climate change.

Progress towards an interdisciplinary science of plant phenology: building predictions across space, time and species diversity.

Climate change has brought renewed interest in the study of plant phenology - the timing of life history events. Data on shifting phenologies with warming have accumulated rapidly, yet research has been comparatively slow to explain the diversity of phenological responses observed across latitudes, growing seasons and species. Here, we outline recent efforts to synthesize perspectives on plant phenology across the fields of ecology, climate science and evolution. We highlight three major axes that vary among these disciplines: relative focus on abiotic versus biotic drivers of phenology, on plastic versus genetic drivers of intraspecific variation, and on cross-species versus autecological approaches. Recent interdisciplinary efforts, building on data covering diverse species and climate space, have found a greater role of temperature in controlling phenology at higher latitudes and for early-flowering species in temperate systems. These efforts have also made progress in understanding the tremendous diversity of responses across species by incorporating evolutionary relatedness, and linking phenological flexibility to invasions and plant performance. Future research with a focus on data collection in areas outside the temperate mid-latitudes and across species' ranges, alongside better integration of how risk and investment shape plant phenology, offers promise for further progress.

Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change.

PREMISE OF THE STUDY: The study of how phenology may contribute to the assembly of plant communities has a long history in ecology. Climate change has brought renewed interest in this area, with many studies examining how phenology may contribute to the success of exotic species. In particular, there is increasing evidence that exotic species occupy unique phenological niches and track climate change more closely than native species. METHODS: Here, we use long-term records of species' first flowering dates from fi ve northern hemisphere temperate sites (Chinnor, UK and in the United States, Concord, Massachusetts; Fargo, North Dakota; Konza Prairie, Kansas; and Washington,D.C.) to examine whether invaders have distinct phenologies. Using a broad phylogenetic framework, we tested for differences between exotic and native species in mean annual flowering time, phenological changes in response to temperature and precipitation,and longer-term shifts in first flowering dates during recent pronounced climate change ("flowering time shifts"). KEY RESULTS: Across North American sites, exotic species have shifted flowering with climate change while native species, on average, have not. In the three mesic systems, exotic species exhibited higher tracking of interannual variation in temperature,such that flowering advances more with warming, than native species. Across the two grassland systems, however, exotic species differed from native species primarily in responses to precipitation and soil moisture, not temperature. CONCLUSIONS: Our findings provide cross-site support for the role of phenology and climate change in explaining species' invasions.Further, they support recent evidence that exotic species may be important drivers of extended growing seasons observed with climate change in North America.

Phenological tracking enables positive species responses to climate change.

Earlier spring phenology observed in many plant species in recent decades provides compelling evidence that species are already responding to the rising global temperatures associated with anthropogenic climate change. There is great variability among species, however, in their phenological sensitivity to temperature. Species that do not phenologically "track" climate change may be at a disadvantage if their growth becomes limited by missed interactions with mutualists, or a shorter growing season relative to earlier-active competitors. Here, we set out to test the hypothesis that phenological sensitivity could be used to predict species performance in a warming climate, by synthesizing results across terrestrial warming experiments. We assembled data for 57 species across 24 studies where flowering or vegetative phenology was matched with a measure of species performance. Performance metrics included biomass, percent cover, number of flowers, or individual growth. We found that species that advanced their phenology with warming also increased their performance, whereas those that did not advance tended to decline in performance with warming. This indicates that species that cannot phenologically "track" climate may be at increased risk with future climate change, and it suggests that phenological monitoring may provide an important tool for setting future conservation priorities.

Incompletely resolved phylogenetic trees inflate estimates of phylogenetic conservatism.

The tendency for more closely related species to share similar traits and ecological strategies can be explained by their longer shared evolutionary histories and represents phylogenetic conservatism. How strongly species traits co-vary with phylogeny can significantly impact how we analyze cross-species data and can influence our interpretation of assembly rules in the rapidly expanding field of community phylogenetics. Phylogenetic conservatism is typically quantified by analyzing the distribution of species values on the phylogenetic tree that connects them. Many phylogenetic approaches, however, assume a completely sampled phylogeny: while we have good estimates of deeper phylogenetic relationships for many species-rich groups, such as birds and flowering plants, we often lack information on more recent interspecific relationships (i.e., within a genus). A common solution has been to represent these relationships as polytomies on trees using taxonomy as a guide. Here we show that such trees can dramatically inflate estimates of phylogenetic conservatism quantified using S. P. Blomberg et al.'s K statistic. Using simulations, we show that even randomly generated traits can appear to be phylogenetically conserved on poorly resolved trees. We provide a simple rarefaction-based solution that can reliably retrieve unbiased estimates of K, and we illustrate our method using data on first flowering times from Thoreau's woods (Concord, Massachusetts, USA).