Warming experiments are increasingly relied on to estimate plant responses to global climate change. For experiments to provide meaningful predictions of future responses, they should reflect the empirical record of responses to temperature variability and recent warming, including advances in the timing of flowering and leafing. We compared phenology (the timing of recurring life history events) in observational studies and warming experiments spanning four continents and 1,634 plant species using a common measure of temperature sensitivity (change in days per degree Celsius). We show that warming experiments underpredict advances in the timing of flowering and leafing by 8.5-fold and 4.0-fold, respectively, compared with long-term observations. For species that were common to both study types, the experimental results did not match the observational data in sign or magnitude. The observational data also showed that species that flower earliest in the spring have the highest temperature sensitivities, but this trend was not reflected in the experimental data. These significant mismatches seem to be unrelated to the study length or to the degree of manipulated warming in experiments. The discrepancy between experiments and observations, however, could arise from complex interactions among multiple drivers in the observational data, or it could arise from remediable artefacts in the experiments that result in lower irradiance and drier soils, thus dampening the phenological responses to manipulated warming. Our results introduce uncertainty into ecosystem models that are informed solely by experiments and suggest that responses to climate change that are predicted using such models should be re-evaluated.
Forecasting how species and ecosystems will respond to climate change has been a major aim of ecology in recent years. Much of this research has focused on phenology -the timing of life-history events. Phenology has well-demonstrated links to climate, from genetic to landscape scales; yet our ability to explain and predict variation in phenology across species, habitats and time remains poor. Here, we outline how merging approaches from ecology, climate science and evolutionary biology can advance research on phenological responses to climate variability. Using insight into seasonal and interannual climate variability combined with niche theory and community phylogenetics, we develop a predictive approach for species' reponses to changing climate. Our approach predicts that species occupying higher latitudes or the early growing season should be most sensitive to climate and have the most phylogenetically conserved phenologies. We further predict that temperate species will respond to climate change by shifting in time, while tropical species will respond by shifting space, or by evolving. Although we focus here on plant phenology, our approach is broadly applicable to ecological research of plant responses to climate variability.
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) 7:1902] or relatively uncommon [Iler AM, et al. (2013) 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.
Summary1. Phenological events -defined points in the life cycle of a plant or animal -have been regarded as highly plastic traits, reflecting flexible responses to various environmental cues. 2. The ability of a species to track, via shifts in phenological events, the abiotic environment through time might dictate its vulnerability to future climate change. Understanding the predictors and drivers of phenological change is therefore critical. 3. Here, we evaluated evidence for phylogenetic conservatism -the tendency for closely related species to share similar ecological and biological attributes -in phenological traits across flowering plants. We aggregated published and unpublished data on timing of first flower and first leaf, encompassing 4000 species at 23 sites across the Northern Hemisphere. We reconstructed the phylogeny for the set of included species, first, using the software program Phylomatic, and second, from DNA data. We then quantified phylogenetic conservatism in plant phenology within and across sites. 4. We show that more closely related species tend to flower and leaf at similar times. By contrasting mean flowering times within and across sites, however, we illustrate that it is not the time of year that is conserved, but rather the phenological responses to a common set of abiotic cues. 5. Our findings suggest that species cannot be treated as statistically independent when modelling phenological responses. 6. Synthesis. Closely related species tend to resemble each other in the timing of their life-history events, a likely product of evolutionarily conserved responses to environmental cues. The search for the underlying drivers of phenology must therefore account for species' shared evolutionary histories.
Parents face a timing problem as to when they should begin devoting resources from their own growth and survival to mating and offspring development. Seed mass and number, as well as maternal survival via plant size, are dependent on time for development. The time available in the favorable season will also affect the size of the developing juveniles and their survival through the unfavorable season. Flowering time may thus represent the outcome of such a time partitioning problem. We analyzed correlations between flowering onset time, seed mass, and plant height in a north‐temperate flora, using both cross‐species comparisons and phylogenetic comparative methods. Among perennial herbs, flowering onset time was negatively correlated with seed mass (i.e. plants with larger seeds started flowering earlier) while flowering onset time was positively correlated with plant height. Neither of these correlations was found among woody plants. Among annual plants, flowering onset time was positively correlated with seed mass. Cross‐species and phylogenetically informed analyses largely agreed, except that flowering onset time was also positively correlated with plant height among annuals in the cross‐species analysis. The different signs of the correlations between flowering onset time and seed mass (compar. gee regression coefficient=−7.8) and flowering onset time and plant height (compar. gee regression coefficient=+30.5) for perennial herbs, indicate that the duration of the growth season may underlie a tradeoff between maternal size and offspring size in perennial herbs, and we discuss how the partitioning of the season between parents and offspring may explain the association between early flowering and larger seed mass among these plants.
Disparate ecological datasets are often organized into databases post hoc and then analyzed and interpreted in ways that may diverge from the purposes of the original data collections. Few studies, however, have attempted to quantify how biases inherent in these data (for example, species richness, replication, climate) affect their suitability for addressing broad scientific questions, especially in under-represented systems (for example, deserts, tropical forests) and wild communities. Here, we quantitatively compare the sensitivity of species first flowering and leafing dates to spring warmth in two phenological databases from the Northern Hemisphere. One-PEP725-has high replication within and across sites, but has low species diver- Author Contributions: All authors contributed to the study design and offered comments on this manuscript as part of the ''Forecasting Phenology'' working group funded by the National Center for Ecological Analysis and Synthesis. Author Cook conceived of and designed the study, analyzed the data, and wrote the paper. Wolkovich and Davies contributed significantly to the refinement of the ideas and analyses and assisted with the writing. Ault contributed significantly to the analyses, including processing of the GHCN climate data. Betancourt contributed significantly to the writing and study design. The first five authors are listed in order of their contributions; all other authors are listed alphabetically.*Corresponding author; e-mail: benjamin.i.cook@nasa.gov Ecosystems DOI: 10.1007/s10021-012-9584-5 Ó 2012 Springer Science+Business Media, LLC (outside the USA) sity and spans a limited climate gradient. The other-NECTAR-includes many more species and a wider range of climates, but has fewer sites and low replication of species across sites. PEP725, despite low species diversity and relatively low seasonality, accurately captures the magnitude and seasonality of warming responses at climatically similar NECTAR sites, with most species showing earlier phenological events in response to warming. In NECTAR, the prevalence of temperature responders significantly declines with increasing mean annual temperature, a pattern that cannot be detected across the limited climate gradient spanned by the PEP725 flowering and leafing data. Our results showcase broad areas of agreement between the two databases, despite significant differences in species richness and geographic coverage, while also noting areas where including data across broader climate gradients may provide added value. Such comparisons help to identify gaps in our observations and knowledge base that can be addressed by ongoing monitoring and research efforts. Resolving these issues will be critical for improving predictions in understudied and undersampled systems outside of the temperature seasonal mid-latitudes.
The Pan European Phenology (PEP) project is a European infrastructure to promote and facilitate phenological research, education, and environmental monitoring. The main objective is to maintain and develop a Pan European Phenological database (PEP725) with an open, unrestricted data access for science and education. PEP725 is the successor of the database developed through the COST action 725 "Establishing a European phenological data platform for climatological applications" working as a single access point for European-wide plant phenological data. So far, 32 European meteorological services and project partners from across Europe have joined and supplied data collected by volunteers from 1868 to the present for the PEP725 database. Most of the partners actively provide data on a regular basis. The database presently holds almost 12 million records, about 46 growing stages and 265 plant species (including cultivars), and can be accessed via http://www.pep725.eu/ . Users of the PEP725 database have studied a diversity of topics ranging from climate change impact, plant physiological question, phenological modeling, and remote sensing of vegetation to ecosystem productivity.
O. 2005. Fleshy fruits Á/ origins, niche shifts, and diversification. Á/ Oikos 109: 255 Á/272.We examined shifts in fruit type, fleshy vs non-fleshy, in relation to habitat-related niche shifts, species richness, and historical distribution, in 50 phylogenetically independent plant lineages. Each lineage consisted of a sister-group pair of fleshy vs non-fleshy taxa and their outgroup. Niche shifts were assessed based on plant community characteristics. Two niche dimensions assumed to reflect community dynamics were derived: spatial predictability of disturbances and canopy closure. Phylogenetically independent origins of fleshy fruit types (1) were correlated with changes to habitats characterized by more shaded and spatially more unpredictable disturbances, (2) had an opposite effect on species richness in woody and herbaceous clades, enhancing species richness in woody clades, and (3) were continuously distributed over a period covering the last 70 million years. These results support the hypothesis that fleshy fruit evolution is driven by vegetation dynamics, and suggest that the strength of frugivore mediated selection on fleshy fruits increases when recruitment sites are spatially unpredictable and/or characterized by low light conditions.
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