Theresa M. Crimmins

Warming experiments underpredict plant phenological responses to climate change

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.

Monitoring Plant Phenology Using Digital Repeat Photography

Repeated observations of plant phenology have been shown to be important indicators of global change. However, capturing the exact date of key events requires daily observations during the growing season, making phenologic observations relatively labor intensive and costly to collect. One alternative to daily observations for capturing the dates of key phenologic events is repeat photography. In this study, we explored the utility of repeat digital photography for monitoring phenologic events in plants. We provide an illustration of this approach and its utility by placing observations made using repeat digital imagery in context with local meteorologic and edaphic variables. We found that repeat photography provides a reliable, consistent measurement of phenophase. In addition, digital photography offers advantages in that it can be mathematically manipulated to detect and enhance patterns; it can classify objects; and digital photographs can be archived for future analysis. In this study, an estimate of greenness and counts of individual flowers were extracted by way of mathematic algorithms from the photo time series. These metrics were interpreted using meteorologic measurements collected at the study site. We conclude that repeat photography, coupled with site-specific meteorologic measurements, could greatly enhance our understanding environmental triggers of phenologic events. In addition, the methods described could easily be adopted by citizen scientists and the general public as well as professionals in the field.

Phylogenetic conservatism in plant phenology

Summary 1. 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.

Standardized phenology monitoring methods to track plant and animal activity for science and resource management applications

Phenology offers critical insights into the responses of species to climate change; shifts in species’ phenologies can result in disruptions to the ecosystem processes and services upon which human livelihood depends. To better detect such shifts, scientists need long-term phenological records covering many taxa and across a broad geographic distribution. To date, phenological observation efforts across the USA have been geographically limited and have used different methods, making comparisons across sites and species difficult. To facilitate coordinated cross-site, cross-species, and geographically extensive phenological monitoring across the nation, the USA National Phenology Network has developed in situ monitoring protocols standardized across taxonomic groups and ecosystem types for terrestrial, freshwater, and marine plant and animal taxa. The protocols include elements that allow enhanced detection and description of phenological responses, including assessment of phenological “status”, or the ability to track presence–absence of a particular phenophase, as well as standards for documenting the degree to which phenological activity is expressed in terms of intensity or abundance. Data collected by this method can be integrated with historical phenology data sets, enabling the development of databases for spatial and temporal assessment of changes in status and trends of disparate organisms. To build a common, spatially, and temporally extensive multi-taxa phenological data set available for a variety of research and science applications, we encourage scientists, resources managers, and others conducting ecological monitoring or research to consider utilization of these standardized protocols for tracking the seasonal activity of plants and animals.

Sensitivity of Spring Phenology to Warming Across Temporal and Spatial Climate Gradients in Two Independent Databases

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 diversity 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 under-sampled systems outside of the temperature seasonal mid-latitudes.

Spring and summer patterns in flowering onset, duration, and constancy across a water-limited gradient.

UNLABELLED PREMISE OF THE STUDY Community-level flowering patterns can be characterized by onset, duration, and end as well as constancy, the degree to which species commence, cease, and reinitiate flowering within a season. In the mountainous Sky Islands region of the southwestern United States, flowering onset is clearly influenced by elevation in the spring, but much less so in the summer season. We evaluated whether these flowering metrics reflect these dissimilar patterns between distinct spring and summer seasons regarding the influence of the elevation and moisture gradient. • METHODS We characterized flowering onset, end, duration, and constancy by plant functional type and their relationships to climate variables in spring and summer. We also evaluated the influence of climate on seasonal flowering patterns. • KEY RESULTS Gaps in seasonal flowering occur frequently in this system in both seasons and among all plant functional types. In both seasons, annual plants exhibit the shortest flowering durations and highest constancies, and plants at low elevations, inhabiting environments with variable moisture conditions, show a greater tendency for longer flowering durations and lower constancy than high-elevation plants. Spring flowering characteristics are most influenced by the total amount of October-March precipitation as well as temperatures in these months, whereas summer flowering characteristics are influenced by the timing of summer-season precipitation, and next by the total amount of summer precipitation. • CONCLUSIONS Flowering metrics, especially constancy and duration, show similar patterns in spring and summer and vary across elevation and moisture gradients. These patterns have substantial implications for plant and animal communities.

USA National Phenology Network’s volunteer-contributed observations yield predictive models of phenological transitions

Purpose In support of science and society, the USA National Phenology Network (USA-NPN) maintains a rapidly growing, continental-scale, species-rich dataset of plant and animal phenology observations that with over 10 million records is the largest such database in the United States. The aim of this study was to explore the potential that exists in the broad and rich volunteer-collected dataset maintained by the USA-NPN for constructing models predicting the timing of phenological transition across species’ ranges within the continental United States. Contributed voluntarily by professional and citizen scientists, these opportunistically collected observations are characterized by spatial clustering, inconsistent spatial and temporal sampling, and short temporal depth (2009-present). Whether data exhibiting such limitations can be used to develop predictive models appropriate for use across large geographic regions has not yet been explored. Methods We constructed predictive models for phenophases that are the most abundant in the database and also relevant to management applications for all species with available data, regardless of plant growth habit, location, geographic extent, or temporal depth of the observations. We implemented a very basic model formulation—thermal time models with a fixed start date. Results Sufficient data were available to construct 107 individual species × phenophase models. Remarkably, given the limited temporal depth of this dataset and the simple modeling approach used, fifteen of these models (14%) met our criteria for model fit and error. The majority of these models represented the “breaking leaf buds” and “leaves” phenophases and represented shrub or tree growth forms. Accumulated growing degree day (GDD) thresholds that emerged ranged from 454 GDDs (Amelanchier canadensis-breaking leaf buds) to 1,300 GDDs (Prunus serotina-open flowers). Such candidate thermal time thresholds can be used to produce real-time and short-term forecast maps of the timing of these phenophase transition. In addition, many of the candidate models that emerged were suitable for use across the majority of the species’ geographic ranges. Real-time and forecast maps of phenophase transitions could support a wide range of natural resource management applications, including invasive plant management, issuing asthma and allergy alerts, and anticipating frost damage for crops in vulnerable states. Implications Our finding that several viable thermal time threshold models that work across the majority of the species ranges could be constructed from the USA-NPN database provides clear evidence that great potential exists this dataset to develop more enhanced predictive models for additional species and phenophases. Further, the candidate models that emerged have immediate utility for supporting a wide range of management applications.

Differential changes in the onset of spring across US National Wildlife Refuges and North American migratory bird flyways

Warming temperatures associated with climate change can have indirect effects on migratory birds that rely on seasonally available food resources and habitats that vary across spatial and temporal scales. We used two heat-based indices of spring onset, the First Leaf Index (FLI) and the First Bloom Index (FBI), as proxies of habitat change for the period 1901 to 2012 at three spatial scales: the US National Wildlife Refuge System; the four major bird migratory flyways in North America; and the seasonal ranges (i.e., breeding and non-breeding grounds) of two migratory bird species, Blue-winged Warbler (Vermivora cyanoptera) and Whooping Crane (Grus americana). Our results show that relative to the historical range of variability, the onset of spring is now earlier in 76% of all wildlife refuges and extremely early (i.e., exceeding 95% of historical conditions) in 49% of refuges. In all flyways but the Pacific, the rate of spring advance is generally greater at higher latitudes than at lower latitudes. This differential rate of advance in spring onset is most pronounced in the Atlantic flyway, presumably because of a “warming hole” in the southeastern US. Both FLI and FBI have advanced markedly in the breeding ranges–but not the non-breeding ranges–of the two selected bird species, albeit with considerable intra-range variation. Differences among species in terms of migratory patterns and the location and extent of seasonal habitats, as well as shifts in habitat conditions over time, may complicate predictions of the vulnerability of migratory birds to climate change effects. This study provides insight into how differential shifts in the phenology of disparate but linked habitats could inform local- to landscape-scale management strategies for the conservation of migratory bird populations.

Development and release of phenological data products—A case study in compliance with federal open data policy

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