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      Probability of Spring Frosts, Not Growing Degree-Days, Drives Onset of Spruce Bud Burst in Plantations at the Boreal-Temperate Forest Ecotone

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          Abstract

          Climate warming-driven early leaf-out is expected to increase forest productivity but concurrently increases leaf exposure to spring frosts, which could reduce forests' net productivity. We hypothesized that due to their damaging effect on buds, spring frosts exert a stronger control on bud phenology than do growing degree-days. We monitored bud flush phenology of three white spruce seed sources (one local seed source from the boreal mixedwood forest and two seed sources from the temperate forest), one black spruce seed source originating from the boreal mixedwood forest and four nonlocal Norway spruce seed sources in 2016 and 2017 in two plantations located on both sides of the temperate-boreal mixedwood forest ecotone in eastern Canada (Quebec). We aimed to determine inter- and intraspecies variations in bud break timing and sensitivity to air temperature and photoperiod. We expected that bud break timing for boreal species and seed sources would be better synchronized with the decrease in frost probability than for nonlocal species and seed sources. We used mixed binomial regressions and AICc model selection to determine the best environmental variables predicting each transition from one stage of bud phenology to the next. At both plantation sites, white spruce bud flush began and ended earlier compared to black and Norway spruce. Buds of all spruce species were sensitive to frost probability for early phenological stages, whereas growing degree-days controlled the remaining stages. Photoperiod sensitivity was higher for white spruce compared to black and Norway spruce and reached its maximum in the temperate forest. At intraspecies level, the two southern white spruce seed sources opened their buds earlier than the local source and were more sensitive to photoperiod, which increased their exposure to spring frosts. Onset of spruce bud flush is driven by spring frosts and photoperiod, but once started, bud phenology responds to temperature. The high photoperiod sensitivity in white spruces could counterbalance climate warming and limit future premature leaf-out, whereas the low photoperiod sensitivity in black spruce should not restrain leaf-out advancement with climate warming. Our results call for adapting the temperature-driven hypotheses of ecophysiological models predicting leaf-out to include spring frost probability.

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          Most cited references78

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          Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers.

          The timing of life history traits is central to lifetime fitness and nowhere is this more evident or well studied as in the phenology of flowering in governing plant reproductive success. Recent changes in the timing of environmental events attributable to climate change, such as the date of snowmelt at high altitudes, which initiates the growing season, have had important repercussions for some common perennial herbaceous wildflower species. The phenology of flowering at the Rocky Mountain Biological Laboratory (Colorado, USA) is strongly influenced by date of snowmelt, which makes this site ideal for examining phenological responses to climate change. Flower buds of Delphinium barbeyi, Erigeron speciosus, and Helianthella quinquenervis are sensitive to frost, and the earlier beginning of the growing season in recent years has exposed them to more frequent mid-June frost kills. From 1992 to 1998, on average 36.1% of Helianthella buds were frosted, but for 1999-2006 the mean is 73.9%; in only one year since 1998 have plants escaped all frost damage. For all three of these perennial species, there is a significant relationship between the date of snowmelt and the abundance of flowering that summer. Greater snowpack results in later snowmelt, later beginning of the growing season, and less frost mortality of buds. Microhabitat differences in snow accumulation, snowmelt patterns, and cold air drainage during frost events can be significant; an elevation difference of only 12 m between two plots resulted in a temperature difference of almost 2 degrees C in 2006 and a difference of 37% in frost damage to buds. The loss of flowers and therefore seeds can reduce recruitment in these plant populations, and affect pollinators, herbivores, and seed predators that previously relied on them. Other plant species in this environment are similarly susceptible to frost damage so the negative effects for recruitment and for consumers dependent on flowers and seeds could be widespread. These findings point out the paradox of increased frost damage in the face of global warming, provide important insights into the adaptive significance of phenology, and have general implications for flowering plants throughout the region and anywhere climate change is having similar impacts.
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            Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982-2008

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              The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms.

              In tree species native to temperate and boreal regions, the activity-dormancy cycle is an important adaptive trait both for survival and growth. We discuss recent research on mechanisms controlling the overlapping developmental processes that define the activity-dormancy cycle, including cessation of apical growth, bud development, induction, maintenance and release of dormancy, and bud burst. The cycle involves an extensive reconfiguration of metabolism. Environmental control of the activity-dormancy cycle is based on perception of photoperiodic and temperature signals, reflecting adaptation to prevailing climatic conditions. Several molecular actors for control of growth cessation have been identified, with the CO/FT regulatory network and circadian clock having important coordinating roles in control of growth and dormancy. Other candidate regulators of bud set, dormancy and bud burst have been identified, such as dormancy-associated MADS-box factors, but their exact roles remain to be discovered. Epigenetic mechanisms also appear to factor in control of the activity-dormancy cycle. Despite evidence for gibberellins as negative regulators in growth cessation, and ABA and ethylene in bud formation, understanding of the roles that plant growth regulators play in controlling the activity-dormancy cycle is still very fragmentary. Finally, some of the challenges for further research in bud dormancy are discussed. © 2012 Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                22 July 2020
                2020
                : 11
                : 1031
                Affiliations
                [1] 1 Institut de Recherche sur les Forêts, Université du Québec en Abitibi Témiscamingue , Rouyn-Noranda, QC, Canada
                [2] 2 Département de Sciences Biologiques, Université du Québec à Montréal , Montréal, QC, Canada
                [3] 3 Department of Geography, Centre for Forest Research, and Centre for Northern Studies, Laval University , Québec, QC, Canada
                Author notes

                Edited by: Jian-Guo Huang, Chinese Academy of Sciences, China

                Reviewed by: Hanxue Liang, Chinese Academy of Sciences, China; Marcin Klisz, Forest Research Institute (IBL), Poland

                *Correspondence: Benjamin Marquis, benjamin.marquis@ 123456uqat.ca

                This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.01031
                7396537
                32849673
                62f29540-7b72-4e99-9598-c1de4b89fafb
                Copyright © 2020 Marquis, Bergeron, Simard and Tremblay

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 19 March 2020
                : 23 June 2020
                Page count
                Figures: 8, Tables: 6, Equations: 0, References: 95, Pages: 19, Words: 10323
                Funding
                Funded by: Natural Sciences and Engineering Research Council of Canada 10.13039/501100000038
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                bud phenology,growing degree-days,leaf-out,photoperiod,picea,spring frost,temperature,thermal acclimation

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