Experimental warming differentially affects vegetative and reproductive phenology of tundra plants.

Rapid climate warming is altering Arctic and alpine tundra ecosystem structure and function, including shifts in plant phenology. While the advancement of green up and flowering are well-documented, it remains unclear whether all phenophases, particularly those later in the season, will shift in unison or respond divergently to warming. Here, we present the largest synthesis to our knowledge of experimental warming effects on tundra plant phenology from the International Tundra Experiment. We examine the effect of warming on a suite of season-wide plant phenophases. Results challenge the expectation that all phenophases will advance in unison to warming. Instead, we find that experimental warming caused: (1) larger phenological shifts in reproductive versus vegetative phenophases and (2) advanced reproductive phenophases and green up but delayed leaf senescence which translated to a lengthening of the growing season by approximately 3%. Patterns were consistent across sites, plant species and over time. The advancement of reproductive seasons and lengthening of growing seasons may have significant consequences for trophic interactions and ecosystem function across the tundra.

Leaf longevity in temperate evergreen species is related to phylogeny and leaf size.

Leaf longevity (LL), the amount of time a photosynthetically active leaf remains on a plant, is an important trait of evergreen species, affecting physiological ecology and ecosystem processes. A long LL gives leaves more time to fix carbon but carries higher construction costs, while a short LL allows plants to respond more rapidly to changing environmental conditions. For many evergreen taxa, LL data are not readily available, and it is not known if LL is phylogenetically conserved. To address this gap, we measured LL for 169 temperate and boreal evergreen woody species at the Arnold Arboretum, a botanical garden in Boston, Massachusetts, along with metrics of leaf size and number known to be related to LL. We hypothesized that LL is phylogenetically conserved, and that longer LL is associated with a greater numbers of leaves, smaller leaves, and a colder hardiness zone of the species' native range. We found that average LL ranged from 1.4 years in Rhododendron tomentosum to 10.5 years in Abies cilicia. LL was phylogenetically conserved, with some genera, such as Abies and Picea, exhibiting long LL (> 3 years) and others, such as Ilex and Rhododendron, exhibiting short LL (< 3 years). Leaf length was negatively correlated with LL in conifers, due to differences between Pinus and other genera; however, there was no correlation between LL and number of leaves. This study highlights the considerable variation and phylogenetic pattern in LL among temperate evergreen species, which has implications for carbon budgets and ecosystem models.

Patterns and biases in an Arctic herbarium specimen collection: Implications for phenological research.

PREMISE OF THE STUDY: Herbarium specimens are increasingly used in phenological studies. However, natural history collections can have biases that influence the analysis of phenological events. Arctic environments, where remoteness and cold climate govern collection logistics, may give rise to unique or pronounced biases. METHODS: We assessed the presence of biases in time, space, phenological events, collectors, taxonomy, and plant traits across Nunavut using herbarium specimens accessioned at the National Herbarium of Canada (CAN). RESULTS: We found periods of high and low collection that corresponded to societal and institutional events; greater collection density close to common points of air and sea access; and preferences to collect plants at the flowering phase and in peak flower, and to collect particular taxa, flower colours, growth forms, and plant heights. One-quarter of collectors contributed 90% of the collection. DISCUSSION: Collections influenced by temporal and spatial biases have the potential to misrepresent phenology across space and time, whereas those shaped by the interests of collectors or the tendency to favour particular phenological stages, taxa, and plant traits could give rise to imbalanced phenological comparisons. Underlying collection patterns may vary among regions and institutions. To guide phenological analyses, we recommend routine assessment of any herbarium data set prior to its use.

Author Correction: Warming shortens flowering seasons of tundra plant communities.

In the version of this Article originally published, the following sentence was missing from the Acknowledgements: "This work was supported by the Norwegian Research Council SnoEco project, grant number 230970". This text has now been added.

Warming shortens flowering seasons of tundra plant communities.

Advancing phenology is one of the most visible effects of climate change on plant communities, and has been especially pronounced in temperature-limited tundra ecosystems. However, phenological responses have been shown to differ greatly between species, with some species shifting phenology more than others. We analysed a database of 42,689 tundra plant phenological observations to show that warmer temperatures are leading to a contraction of community-level flowering seasons in tundra ecosystems due to a greater advancement in the flowering times of late-flowering species than early-flowering species. Shorter flowering seasons with a changing climate have the potential to alter trophic interactions in tundra ecosystems. Interestingly, these findings differ from those of warmer ecosystems, where early-flowering species have been found to be more sensitive to temperature change, suggesting that community-level phenological responses to warming can vary greatly between biomes.

Patterns and predictors of fleshy fruit phenology at five international botanical gardens.

PREMISE OF THE STUDY: To improve our understanding of the patterns and drivers of fleshy fruit phenology, we examined the sequence, patterns across years and locations, and drivers of fruiting times at five botanical gardens on three continents. METHODS: We monitored four stages of fruit phenology for 406 temperate, fleshy-fruited, woody plant species in 2014 and 2015. KEY RESULTS: Across all gardens, ripe fruits were present from May to March of the following year, with peak fruiting durations ranging from under 1 week to over 150 days. Species-level first fruiting and onset of peak fruiting dates were strongly associated with one another within sites and were more consistent between years and sites than the end of peak fruiting and last fruiting date. The order of fruiting among species between years and gardens was moderately consistent, and both peak fruiting times and fruiting durations were found to be phylogenetically conserved. CONCLUSIONS: The consistent order of fruiting among species between years and locations indicates species-specific phenological responses to environmental conditions. Wide variation in fruiting times across species and in the duration of peak fruiting reinforces the importance of understanding how plant phenology impacts dispersers and monitoring the health and consistency of these interactions.

Shifts in pollen release envelope differ between genera with non-uniform climate change.

PREMISE OF THE STUDY: Plant phenological responses to climate change now constitute one of the best studied areas of the ecological impacts of climate change. Flowering time responses to climate change of wind-pollinated species have, however, been less well studied. A novel source of flowering time data for wind-pollinated species is allergen monitoring records. METHODS: We studied the male flowering time response to climatic variables of two wind-pollinated genera, Betula (Betulaceae) and Populus (Salicaceae), using pollen count records over a 17-year period. KEY RESULTS: We found that changes in the pollen release envelope differed between the two genera. Over the study period, the only month with a significant rise in temperature was April, resulting in the duration of pollen release of the April-flowering Populus to shorten and the start and peak of the May-flowering Betula to advance. The quantity of pollen released by Betula has increased and was related to increases in the previous year's August precipitation, while the quantity of pollen released by Populus has not changed and was related to the previous year's summer and autumn temperatures. CONCLUSIONS: Our findings suggest that taxa differ in the reproductive consequences of environmental change. Differing shifts in phenology among species may be related to different rates of change in climatic variables in different months of the year. While our study only considers two genera, the results underscore the importance of understanding non-uniform intra-annual variation in climate when studying the ecological implications of climate change.

Prediction of Arctic plant phenological sensitivity to climate change from historical records.

The pace of climate change in the Arctic is dramatic, with temperatures rising at a rate double the global average. The timing of flowering and fruiting (phenology) is often temperature dependent and tends to advance as the climate warms. Herbarium specimens, photographs, and field observations can provide historical phenology records and have been used, on a localised scale, to predict species' phenological sensitivity to climate change. Conducting similar localised studies in the Canadian Arctic, however, poses a challenge where the collection of herbarium specimens, photographs, and field observations have been temporally and spatially sporadic. We used flowering and seed dispersal times of 23 Arctic species from herbarium specimens, photographs, and field observations collected from across the 2.1 million km2 area of Nunavut, Canada, to determine (1) which monthly temperatures influence flowering and seed dispersal times; (2) species' phenological sensitivity to temperature; and (3) whether flowering or seed dispersal times have advanced over the past 120 years. We tested this at different spatial scales and compared the sensitivity in different regions of Nunavut. Broadly speaking, this research serves as a proof of concept to assess whether phenology-climate change studies using historic data can be conducted at large spatial scales. Flowering times and seed dispersal time were most strongly correlated with June and July temperatures, respectively. Seed dispersal times have advanced at double the rate of flowering times over the past 120 years, reflecting greater late-summer temperature rises in Nunavut. There is great diversity in the flowering time sensitivity to temperature of Arctic plant species, suggesting climate change implications for Arctic ecological communities, including altered community composition, competition, and pollinator interactions. Intraspecific temperature sensitivity and warming trends varied markedly across Nunavut and could result in greater changes in some parts of Nunavut than in others.

Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes.

Warmer temperatures are accelerating the phenology of organisms around the world. Temperature sensitivity of phenology might be greater in colder, higher latitude sites than in warmer regions, in part because small changes in temperature constitute greater relative changes in thermal balance at colder sites. To test this hypothesis, we examined up to 20 years of phenology data for 47 tundra plant species at 18 high-latitude sites along a climatic gradient. Across all species, the timing of leaf emergence and flowering was more sensitive to a given increase in summer temperature at colder than warmer high-latitude locations. A similar pattern was seen over time for the flowering phenology of a widespread species, Cassiope tetragona. These are among the first results highlighting differential phenological responses of plants across a climatic gradient and suggest the possibility of convergence in flowering times and therefore an increase in gene flow across latitudes as the climate warms.

Substantial variation in leaf senescence times among 1360 temperate woody plant species: implications for phenology and ecosystem processes.

BACKGROUND AND AIMS: Autumn leaf senescence marks the end of the growing season in temperate ecosystems. Its timing influences a number of ecosystem processes, including carbon, water and nutrient cycling. Climate change is altering leaf senescence phenology and, as those changes continue, it will affect individual woody plants, species and ecosystems. In contrast to spring leaf out times, however, leaf senescence times remain relatively understudied. Variation in the phenology of leaf senescence among species and locations is still poorly understood. METHODS: Leaf senescence phenology of 1360 deciduous plant species at six temperate botanical gardens in Asia, North America and Europe was recorded in 2012 and 2013. This large data set was used to explore ecological and phylogenetic factors associated with variation in leaf senescence. KEY RESULTS: Leaf senescence dates among species varied by 3 months on average across the six locations. Plant species tended to undergo leaf senescence in the same order in the autumns of both years at each location, but the order of senescence was only weakly correlated across sites. Leaf senescence times were not related to spring leaf out times, were not evolutionarily conserved and were only minimally influenced by growth habit, wood anatomy and percentage colour change or leaf drop. These weak patterns of leaf senescence timing contrast with much stronger leaf out patterns from a previous study. CONCLUSIONS: The results suggest that, in contrast to the broader temperature effects that determine leaf out times, leaf senescence times are probably determined by a larger or different suite of local environmental effects, including temperature, soil moisture, frost and wind. Determining the importance of these factors for a wide range of species represents the next challenge for understanding how climate change is affecting the end of the growing season and associated ecosystem processes.

Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy.

Leaf out phenology affects a wide variety of ecosystem processes and ecological interactions and will take on added significance as leaf out times increasingly shift in response to warming temperatures associated with climate change. There is, however, relatively little information available on the factors affecting species differences in leaf out phenology. An international team of researchers from eight Northern Hemisphere temperate botanical gardens recorded leaf out dates of c. 1600 woody species in 2011 and 2012. Leaf out dates in woody species differed by as much as 3 months at a single site and exhibited strong phylogenetic and anatomical relationships. On average, angiosperms leafed out earlier than gymnosperms, deciduous species earlier than evergreen species, shrubs earlier than trees, diffuse and semi-ring porous species earlier than ring porous species, and species with smaller diameter xylem vessels earlier than species with larger diameter vessels. The order of species leaf out was generally consistent between years and among sites. As species distribution and abundance shift due to climate change, interspecific differences in leaf out phenology may affect ecosystem processes such as carbon, water, and nutrient cycling. Our open access leaf out data provide a critical framework for monitoring and modelling such changes going forward.

Herbarium specimens, photographs, and field observations show Philadelphia area plants are responding to climate change.

PREMISE OF THE STUDY: The global climate is changing rapidly and is expected to continue changing in coming decades. Studying changes in plant flowering times during a historical period of warming temperatures gives us a way to examine the impacts of climate change and allows us to predict further changes in coming decades. The Greater Philadelphia region has a long and rich history of botanical study and documentation, with abundant herbarium specimens, field observations, and botanical photographs from the mid-1800s onward. These extensive records also provide an opportunity to validate methodologies employed by other climate change researchers at a different biogeographical area and with a different group of species. METHODS: Data for 2539 flowering records from 1840 to 2010 were assessed to examine changes in flowering response over time and in relation to monthly minimum temperatures of 28 Piedmont species native to the Greater Philadelphia region. KEY RESULTS: Regression analysis of the date of flowering with year or with temperature showed that, on average, the Greater Philadelphia species studied are flowering 16 d earlier over the 170-yr period and 2.7 d earlier per 1°C rise in monthly minimum temperature. CONCLUSIONS: Of the species studied, woody plants with short flowering duration are the best indicators of a warming climate. For monthly minimum temperatures, temperatures 1 or 2 mo prior to flowering are most significantly correlated with flowering time. Studies combining herbarium specimens, photographs, and field observations are an effective method for detecting the effects of climate change on flowering times.