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1. Floral freezing tolerance is tied to flowering time in North American woody plant species

   https://doi.org/10.1093/aob/mcae117  

   Savage, Jessica_A ; Fakhreddine, Qadry ; Vandenheuvel, Britton ( July 2024 , Annals of Botany)

   As winter and spring temperatures continue to increase, the timing of flowering and leaf-out is advancing in many seasonally cold regions. This advancement could put plants that flower early in the spring at risk of decreased reproduction in years when there are late freeze events. Unfortunately, relatively little is known about floral freezing tolerance in forest communities. In this study, we examined the impact of freezing temperatures on the flowers of woody plants in a region where there is rapid winter warming in North America.

   We subjected the flowers of 25 woody species to a hard (−5 °C) and a light freeze (0 °C). We assessed tissue damage using electrolyte leakage. In a subset of species, we also examined the impact of a hard freeze on pollen tube growth. To determine if the vulnerability of flowers to freezing damage relates to flowering time and to examine the responsiveness of flowering time to spring temperature, we recorded the date of first flower for our study species for 3 years.

   Across species, we found that floral freezing tolerance was strongly tied to flowering time, with the highest freezing tolerance occurring in plants that bloomed earlier in the year. We hypothesize that these early blooming species are unlikely to be impacted by a false spring. Instead, the most vulnerable species to a false spring should be those that bloom later in the season. The flowering time in these species is also more sensitive to temperature, putting them at a great risk of experiencing a false spring. Ultimately, floral damage in one year will not have a large impact on species fitness, but if false springs become more frequent, there could be long-term impacts on reproduction of vulnerable species.

    

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2. Coordination of spring vascular and organ phenology in deciduous angiosperms growing in seasonally cold climates

   https://doi.org/10.1111/nph.17289  

   Savage, Jessica A. ; Chuine, Isabelle ( March 2021 , New Phytologist)

   In seasonally cold climates, many woody plants tolerate chilling and freezing temperatures by ceasing growth, shedding leaves and entering dormancy. At the same time, transport within these plants often decreases as the vascular system exhibits reduced functionality. As spring growth requires water and nutrients, we ask the question: how much does bud, leaf and flower development depend on the vasculature in spring? In this review, we present what is known about leaf, flower and vascular phenology to sort out this question. In early stages of bud development, buds rely on internal resources and do not appear to require vascular support. The situation changes during organ expansion, after leaves and flowers reconnect to the stem vascular system. However, there are major gaps in our understanding of the timing of vascular development, especially regarding the phloem, as well as the synchronization among leaves, flowers, stem and root vasculature. We believe these gaps are mainly the outcome of research completed in silo and urge future work to take a more integrative approach. We highlight current challenges and propose future directions to make rapid progress on this important topic in upcoming years.

    

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3. Temperature controls phenology in continuously flowering Protea species of subtropical Africa

   https://doi.org/10.1002/aps3.1232  

   Daru, Barnabas H. ; Kling, Matthew M. ; Meineke, Emily K. ; van Wyk, Abraham E. ( March 2019 , Applications in Plant Sciences)

   Herbarium specimens are increasingly used as records of plant flowering phenology. However, most herbarium‐based studies on plant phenology focus on taxa from temperate regions. Here, we explore flowering phenologic responses to climate in the subtropical plant genusProtea(Proteaceae), an iconic group of plants that flower year‐round and are endemic to subtropical Africa.

   We present a novel, circular sliding window approach to investigate phenological patterns developed for species with year‐round flowering. We employ our method to evaluate the extent to which site‐to‐site and year‐to‐year variation in temperature and precipitation affect flowering dates using a database of 1727 herbarium records of 25Proteaspecies. We also explore phylogenetic conservatism in flowering phenology.

   We show that herbarium data combined with our sliding window approach successfully captured independently reported flowering phenology patterns (r= 0.93). Both warmer sites and warmer years were associated with earlier flowering of 3–5 days/°C, whereas precipitation variation had no significant effect on flowering phenology. Although species vary widely in phenological responsiveness, responses are phylogenetically conserved, with closely related species tending to shift flowering similarly with increasing temperature.

   Our results point to climate‐responsive phenology for this important plant genus and indicate that the subtropical, aseasonally flowering genusProteahas temperature‐driven flowering responses that are remarkably similar to those of better‐studied northern temperate plant species, suggesting a generality across biomes that has not been described elsewhere.

    

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4. Seasonal patterns of increases in stem girth, vessel development, and hydraulic function in deciduous tree species

   https://doi.org/10.1093/aob/mcac032  

   Valdovinos-Ayala, Jessica ; Robles, Catherine ; Fickle, Jaycie C. ; Pérez-de-Lis, Gonzalo ; Pratt, R. Brandon ; Jacobsen, Anna L. ( March 2022 , Annals of Botany)

   The onset of spring growth and vessel formation were examined within three deciduous woody plant species, Acer rubrum, Populus balsamifera ssp. trichocarpa and Quercus rubra. We were broadly interested in the lag between the onset of girth expansion and the formation of mature and hydraulically conductive vessels within the new xylem.

   Dendrometers were installed on 20 trees (6–7 per species), and expansion of both bole and distal stems was monitored throughout the growing season in a common garden. For each species, four to six distal stems were harvested every other week for anatomical examination of vessel formation. Additionally, for Populus and Quercus, hydraulic conductivity measurements and active xylem staining were completed on all stem samples.

   For all three species, the timing of girth expansion was similar. Expansion of distal branches occurred 12–37 d earlier than that of the bole. Vessel formation initiated several weeks prior to leaf-out, but no new earlywood vessels were mature at the time of bud break for Acer and Populus and only a few were present in Quercus. Initial stem girth expansion occurred 2 to >6 weeks before the maturation of the first current-year vessels, and there was an additional delay of up to 4 weeks before mature vessels became hydraulically functional. Hydraulic conductivity was strongly correlated with the number and diameter of stained vessels.

   Bud break and leaf expansion relied predominantly on water supplied by vessels formed during prior seasons. Early-season activity is likely affected by the function of older xylem vessels and the environmental factors that influence their structure and function. Understanding the functional lifespan of vessels and the varying contributions of new and older vessels to conductivity are critical to understanding of the phenology and vascular function of long-lived woody plants in response to changing climates.

    

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5. Flowering time responses to warming drive reproductive fitness in a changing Arctic

   https://doi.org/10.1093/aob/mcae007  

   Collins, Courtney G. ; Angert, Amy L. ; Clark, Karin ; Elmendorf, Sarah C. ; Elphinstone, Cassandra ; Henry, Greg H. R. ( January 2024 , Annals of Botany)

   The Arctic is warming at an alarming rate, leading to earlier spring conditions and plant phenology. It is often unclear to what degree changes in reproductive fitness (flower, fruit and seed production) are a direct response to warming versus an indirect response through shifting phenology. The aim of this study was to quantify the relative importance of these direct and indirect pathways and project the net effects of warming on plant phenology and reproductive fitness under current and future climate scenarios.

   We used two long-term datasets on 12 tundra species in the Canadian Arctic as part of the International Tundra Experiment (ITEX). Phenology and reproductive fitness were recorded annually on tagged individual plants at both Daring Lake, Northwest Territories (64° 52' N, - 111° 35' W) and Alexandra Fiord, Nunavut (78° 49' N, - 75° 48' W). The plant species encompassed a wide taxonomic diversity across a range of plant functional types with circumpolar/boreal distributions. We used hierarchical Bayesian structural equation models to compare the direct and indirect effects of climate warming on phenology and reproductive fitness across species, sites and years.

   We found that warming, both experimental and ambient, drove earlier flowering across species, which led to higher numbers of flowers and fruits produced, reflecting directional phenotypic selection for earlier flowering phenology. Furthermore, this indirect effect of climate warming mediated through phenology was generally about two to three times stronger than the direct effect of climate on reproductive fitness. Under future climate predictions, individual plants showed a ~2- to 4.5-fold increase in their reproductive fitness (flower counts) with advanced flowering phenology.

   Our results suggest that, on average, the benefits of early flowering, such as increased development time and subsequent enhanced reproductive fitness, might outweigh its risks. Overall, this work provides important insights into population-level consequences of phenological shifts in a warming Arctic over multi-decadal time scales.

    

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