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"Primack, Richard B"
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Leaf-out phenology of temperate woody plants: from trees to ecosystems
CONTENTS: Summary 926 I. Introduction 927 II. What triggers a plant to leaf-out? 928 III. Variation in leaf-out among species 929 IV. Leaf-out and climate change 932 V. Conclusions 937 Acknowledgements 937 References 937 SUMMARY: Leafing-out of woody plants begins the growing season in temperate forests and is one of the most important drivers of ecosystem processes. There is substantial variation in the timing of leaf-out, both within and among species, but the leaf development of almost all temperate tree and shrub species is highly sensitive to temperature. As a result, leaf-out times of temperate forests are valuable for observing the effects of climate change. Analysis of phenology data from around the world indicates that leaf-out is generally earlier in warmer years than in cooler years and that the onset of leaf-out has advanced in many locations. Changes in the timing of leaf-out will affect carbon sequestration, plant-animal interactions, and other essential ecosystem processes. The development of remote sensing methods has expanded the scope of leaf-out monitoring from the level of an individual plant or forest to an entire region. Meanwhile, historical data have informed modeling and experimental studies addressing questions about leaf-out timing. For most species, onset of leaf-out will continue to advance, although advancement may be slowed for some species because of unmet chilling requirements. More information is needed to reduce the uncertainty in predicting the timing of future spring onset.
Journal Article
Drivers of leaf‐out phenology and their implications for species invasions: insights from Thoreau's Concord
To elucidate climate‐driven changes in leaf‐out phenology and their implications for species invasions, we observed and experimentally manipulated leaf out of invasive and native woody plants in Concord, MA, USA. Using observations collected by Henry David Thoreau (1852–1860) and our own observations (2009–2013), we analyzed changes in leaf‐out timing and sensitivity to temperature for 43 woody plant species. We experimentally tested winter chilling requirements of 50 species by exposing cut branches to warm indoor temperatures (22°C) during the winter and spring of 2013. Woody species are now leafing out an average of 18 d earlier than they did in the 1850s, and are advancing at a rate of 5 ± 1 d °C⁻¹. Functional groups differ significantly in the duration of chilling they require to leaf out: invasive shrubs generally have weaker chilling requirements than native shrubs and leaf out faster in the laboratory and earlier in the field; native trees have the strongest chilling requirements. Our results suggest that invasive shrub species will continue to have a competitive advantage as the climate warms, because native plants are slower to respond to warming spring temperatures and, in the future, may not meet their chilling requirements.
Journal Article
Citizen scientists and university students monitor noise pollution in cities and protected areas with smartphones
Noise pollution can cause increased stress, cognitive impairment and illness in humans and decreased fitness and altered behavior in wildlife. Maps of noise pollution are used to visualize the distribution of noise across a landscape. These maps are typically created by taking a relatively small number of sound measurements or simulated on the basis of theoretical models. However, smartphones with inexpensive sound measuring apps can be used to monitor noise and create dense maps of real-world noise measurements. Public concern with noise can make monitoring noise pollution with smartphones an engaging and educational citizen science activity. We demonstrate a method utilizing single-day citizen science noise mapping events and a university lab to collect noise data in urban environments and protected areas. Using this approach, we collected hundreds of noise measurements with participants that we used to create noise maps. We found this method was successful in engaging volunteers and students and producing usable noise data. The described methodology has potential applications for biological research, citizen science engagement, and teaching.
Journal Article
Widespread sampling biases in herbaria revealed from large-scale digitization
Nonrandom collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras online offer a timely opportunity to assess commonalities and differences in herbarium sampling biases.
We determined spatial, temporal, trait, phylogenetic, and collector biases in c. 5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England, USA (NE).
We identified numerous shared and unique biases among these regions. Shared biases included specimens collected close to roads and herbaria; specimens collected more frequently during biological spring and summer; specimens of threatened species collected less frequently; and specimens of close relatives collected in similar numbers. Regional differences included overrepresentation of graminoids in SA and AU and of annuals in AU; and peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by very few individuals. We hypothesize that these mega-collectors, with their associated preferences and idiosyncrasies, shaped patterns of collection bias via ‘founder effects’.
Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.
Journal Article
Wildflower phenological escape differs by continent and spring temperature
Temperate understory plant species are at risk from climate change and anthropogenic threats that include increased deer herbivory, habitat loss, pollinator declines and mismatch, and nutrient pollution. Recent work suggests that spring ephemeral wildflowers may be at additional risk due to phenological mismatch with deciduous canopy trees. The study of this dynamic, commonly referred to as “phenological escape”, and its sensitivity to spring temperature is limited to eastern North America. Here, we use herbarium specimens to show that phenological sensitivity to spring temperature is remarkably conserved for understory wildflowers across North America, Europe, and Asia, but that canopy trees in North America are significantly more sensitive to spring temperature compared to in Asia and Europe. We predict that advancing tree phenology will lead to decreasing spring light windows in North America while spring light windows will be maintained or even increase in Asia and Europe in response to projected climate warming.
Climate change may be inducing phenological mismatches between trees and understory plants. Here, phenological models based on long-term data from herbarium specimens indicate that spring ephemeral wildflowers are more vulnerable to such mismatches in North America than in Eurasia.
Journal Article
Record-Breaking Early Flowering in the Eastern United States
Flowering times are well-documented indicators of the ecological effects of climate change and are linked to numerous ecosystem processes and trophic interactions. Dozens of studies have shown that flowering times for many spring-flowering plants have become earlier as a result of recent climate change, but it is uncertain if flowering times will continue to advance as temperatures rise. Here, we used long-term flowering records initiated by Henry David Thoreau in 1852 and Aldo Leopold in 1935 to investigate this question. Our analyses demonstrate that record-breaking spring temperatures in 2010 and 2012 in Massachusetts, USA, and 2012 in Wisconsin, USA, resulted in the earliest flowering times in recorded history for dozens of spring-flowering plants of the eastern United States. These dramatic advances in spring flowering were successfully predicted by historical relationships between flowering and spring temperature spanning up to 161 years of ecological change. These results demonstrate that numerous temperate plant species have yet to show obvious signs of physiological constraints on phenological advancement in the face of climate change.
Journal Article
From observations to experiments in phenology research
Climate change is advancing the leaf-out times of many plant species and mostly extending the growing season in temperate ecosystems. Laboratory experiments using twig cuttings from woody plant species present an affordable, easily replicated approach to investigate the relative importance of factors such as winter chilling, photoperiod, spring warming and frost tolerance on the leafing-out times of plant communities. This Viewpoint article demonstrates how the results of these experiments deepen our understanding beyond what is possible via analyses of remote sensing and field observation data, and can be used to improve climate change forecasts of shifts in phenology, ecosystem processes and ecological interactions.
The twig method involves cutting dormant twigs from trees, shrubs and vines on a single date or at intervals over the course of the winter and early spring, placing them in containers of water in controlled environments, and regularly recording leaf-out, flowering or other phenomena. Prior to or following leaf-out or flowering, twigs may be assigned to treatment groups for experiments involving temperature, photoperiod, frost, humidity and more. Recent studies using these methods have shown that winter chilling requirements and spring warming strongly affect leaf-out and flowering times of temperate trees and shrubs, whereas photoperiod requirements are less important than previously thought for most species. Invasive plant species have weaker winter chilling requirements than native species in temperate ecosystems, and species that leaf-out early in the season have greater frost tolerance than later leafing species.
This methodology could be extended to investigate additional drivers of leaf-out phenology, leaf senescence in the autumn, and other phenomena, and could be a useful tool for education and outreach. Additional ecosystems, such as boreal, southern hemisphere and sub-tropical forests, could also be investigated using dormant twigs to determine the drivers of leaf-out times and how these ecosystems will be affected by climate change.
Journal Article
Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change
Climate change has led to major changes in the phenology (the timing of seasonal activities, such as flowering) of some species but not others. The extent to which flowering-time response to temperature is shared among closely related species might have important consequences for community-wide patterns of species loss under rapid climate change. Henry David Thoreau initiated a dataset of the Concord, Massachusetts, flora that spans [almost equal to]150 years and provides information on changes in species abundance and flowering time. When these data are analyzed in a phylogenetic context, they indicate that change in abundance is strongly correlated with flowering-time response. Species that do not respond to temperature have decreased greatly in abundance, and include among others anemones and buttercups [Ranunculaceae pro parte (p.p.)], asters and campanulas (Asterales), bluets (Rubiaceae p.p.), bladderworts (Lentibulariaceae), dogwoods (Cornaceae), lilies (Liliales), mints (Lamiaceae p.p.), orchids (Orchidaceae), roses (Rosaceae p.p.), saxifrages (Saxifragales), and violets (Malpighiales). Because flowering-time response traits are shared among closely related species, our findings suggest that climate change has affected and will likely continue to shape the phylogenetically biased pattern of species loss in Thoreau's woods.
Journal Article
Forecasting phenology under global warming
As a consequence of warming temperatures around the world, spring and autumn phenologies have been shifting, with corresponding changes in the length of the growing season. Our understanding of the spatial and interspecific variation of these changes, however, is limited. Not all species are responding similarly, and there is significant spatial variation in responses even within species. This spatial and interspecific variation complicates efforts to predict phenological responses to ongoing climate change, but must be incorporated in order to build reliable forecasts. Here, we use a long-term dataset (1953–2005) of plant phenological events in spring (flowering and leaf out) and autumn (leaf colouring and leaf fall) throughout Japan and South Korea to build forecasts that account for these sources of variability. Specifically, we used hierarchical models to incorporate the spatial variability in phenological responses to temperature to then forecast species' overall and site-specific responses to global warming. We found that for most species, spring phenology is advancing and autumn phenology is getting later, with the timing of events changing more quickly in autumn compared with the spring. Temporal trends and phenological responses to temperature in East Asia contrasted with results from comparable studies in Europe, where spring events are changing more rapidly than are autumn events. Our results emphasize the need to study multiple species at many sites to understand and forecast regional changes in phenology.
Journal Article