Biomass, carbohydrate, and leakage conductance in buds of six ornamental tree species subjected to a “false spring” in Northeast China


  • Xiaopei Wang 1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China; 2. University of Chinese Academy of Sciences, Beijing 100049, China
  • Lingquan Meng 1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China;
  • Hongxu Wei 1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China; 2. University of Chinese Academy of Sciences, Beijing 100049, China



Global warming, Late-spring frost, Post-winter chill, Budburst, Tree physiology


Information is highly scarce about the possible effect of a late spring frost on physiological response of buds in ornamental trees. In this study, spring temperature of Changchun at Northeast China was recorded to identify the characteristics of a false spring by detecting extraordinary warming and sudden freeze in early April of 2017. Buds of six local ornamental tree species were investigated for their dynamics in biomass, non-structural carbohydrates, frost resistance on days of 7, 14, 21, and 28 April 2017. According to a comparison with spring temperature records historically from 2007 to 2016, a false spring was determined. Black pine (Pinus tabuliformis var. mukdensis) had greater bud biomass than apricot (Prunus sibirica L.). Peach (Prunus persica L. var. persica f. rubro-plena Schneid.) reserved greater non-structural carbohydrate content in post-chilling buds than black pine, and apricot and willow (Salix babylonica L.) had greater soluble sugars and starch contents in buds, respectively. Cumulative number of days with temperature below 12°C had a negative relationship with relative conductance in sorbus (Sorbus pohuashanensis [Hance] Hedl.). Chokecherry (Padus virginiana ‘Canada Red’) had greatest bud starch content on 21 April. Overall, a late spring frost imposed interruption on carbohydrate metabolism rather than direct damage on buds of ornamental trees before late April. Advanced warming induced more pronounced negative impact of a false spring than the sudden decline of minimum temperature.

Author Biographies

Xiaopei Wang, 1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China; 2. University of Chinese Academy of Sciences, Beijing 100049, China

Master student in research group of Urban Forest and Wetland at Key Laboratory of Wetland Ecology and Enviornment of Chinese Academy of Sciences

Lingquan Meng, 1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China;

research assistant in research group of Urban Forest and Wetland at Key Laboratory of Wetland Ecology and Enviornment of Chinese Academy of Sciences

Hongxu Wei, 1. Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China; 2. University of Chinese Academy of Sciences, Beijing 100049, China

Associate researcher in research group of Urban Forest and Wetland at Key Laboratory of Wetland Ecology and Enviornment of Chinese Academy of Sciences


"Times New Roman",serif;mso-fareast-font-family:宋体'>

field-begin'> ADDIN EN.REFLIST

style='mso-element:field-separator'>Augspurger C.K., 2009. Spring 2007 warmth and frost: phenology, damage and refoliation in a temperate deciduous forest. Funct Ecol 23:1031-1039. DOI: 10.1111/j.1365-2435.2009.01587.xAugspurger C.K., 2013. Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing. Ecology 94:41-50. DOI: 10.1890/12-0200.1Awaya Y., Tanaka K., Kodani E., Nishizono T., 2009. Responses of a beech (Fagus crenata Blume) stand to late spring frost damage in Morioka, Japan. For Ecol Manage 257:2359-2369. DOI: 10.1016/j.foreco.2009.03.028Bascietto M., Bajocco S., Mazzenga F., Matteucci G., 2018. Assessing spring frost effects on beech forests in Central Apennines from remotely-sensed data. Agric For Meteorol 248:240-250. DOI: 10.1016/j.agrformet.2017.10.007Bennie J., Kubin E., Wiltshire A., Huntley B., Baxter R., 2010. Predicting spatial and temporal patterns of bud-burst and spring frost risk in north-west Europe: the implications of local adaptation to climate. Glob Change Biol 16:1503-1514. DOI: 10.1111/j.1365-2486.2009.02095.xBureau of Forestry and Landscaping of Changchun (2018) Series flowering news from Landscape and Greening Bureau of Changchun City: flowering news delivered again when canopies of willow trees are closing (adapted from Chinese) Accessed 20 October 2020Cannell M.G.R., Smith R.I., 1986. Climatic warming, spring budburst and forest damage on trees. Journal of Applied Ecology 23:177-191. DOI: 10.2307/2403090Chamberlain C.J., Cook B.I., Morales-Castilla I., Wolkovich E.M., 2020. Climate change reshapes the drivers of false spring risk across European trees. New Phytol:12. DOI: 10.1111/nph.16851Changchun City Meteorological Service (2020) Realtime Monitoring of Daily Temperature in Changchun City. Accessed 22 October 2020Charrier G., Lacointe A., Ameglio T., 2018. Dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut trees Juglans regia L. Frontiers in Plant Science 9:14. DOI: 10.3389/fpls.2018.01746Chmielewski F.M., Gotz K.P., Weber K.C., Moryson S., 2018. Climate change and spring frost damages for sweet cherries in Germany. Int J Biometeorol 62:217-228. DOI: 10.1007/s00484-017-1443-9Chung U., Seo H.H., Hwang K.H., Hwang B.S., Choi J., Lee J.T., Yun J.I., 2006. Minimum temperature mapping over complex terrain by estimating cold air accumulation potential. Agric For Meteorol 137:15-24. DOI: population (2020) China: Jilin. Accessed 22 October 2020D'Andrea E. et al., 2019. Winter's bite: beech trees survive complete defoliation due to spring late-frost damage by mobilizing old C reserves. New Phytol 224:625-631. DOI: 10.1111/nph.16047Dai J.H., Wang H.J., Ge Q.S., 2013. The decreasing spring frost risks during the flowering period for woody plants in temperate area of eastern China over past 50 years. J Geogr Sci 23:641-652. DOI: 10.1007/s11442-013-1034-6Gu L. et al., 2008. The 2007 Eastern US spring freeze: Increased cold damage in a warming world? BioScience 58:253-262. DOI: 10.1641/B580311 %J BioScienceHeide O.M., 1993. Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531-540. DOI: 10.1111/j.1399-3054.1993.tb01368.xHeide O.M., Prestrud A.K., 2005. Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiology 25:109-114. DOI: 10.1093/treephys/25.1.109 %J Tree PhysiologyHubalek Z., 2016. The North Atlantic Oscillation system and plant phenology. Int J Biometeorol 60:749-756. DOI: 10.1007/s00484-015-1070-2Hufkens K., Friedl M.A., Keenan T.F., Sonnentag O., Bailey A., O'Keefe J., Richardson A.D., 2012. Ecological impacts of a widespread frost event following early spring leaf-out. Glob Change Biol 18:2365-2377. DOI: 10.1111/j.1365-2486.2012.02712.xJochner S., Hofler J., Beck I., Gottlein A., Ankerst D.P., Traidl-Hoffmann C., Menzel A., 2013. Nutrient status: a missing factor in phenological and pollen research? J Exp Bot 64:2081-2092. DOI: 10.1093/jxb/ert061Kim Y., Kimball J.S., Didan K., Henebry G.M., 2014. Response of vegetation growth and productivity to spring climate indicators in the conterminous United States derived from satellite remote sensing data fusion. Agric For Meteorol 194:132-143. DOI: 10.1016/j.agrformet.2014.04.001Kreyling J., Thiel D., Nagy L., Jentsch A., Huber G., Konnert M., Beierkuhnlein C., 2012. Late frost sensitivity of juvenile Fagus sylvatica L. differs between southern Germany and Bulgaria and depends on preceding air temperature. Eur J For Res 131:717-725. DOI: 10.1007/s10342-011-0544-yL’Hirondelle S.J., Simpson D.G., Binder W.D., 2006. Overwinter storability of conifer planting stock: Operational testing of fall frost hardiness. New Forests 32:307. DOI: 10.1007/s11056-006-9005-8Lenz A., Hoch G., Korner C., Vitasse Y., 2016. Convergence of leaf-out towards minimum risk of freezing damage in temperate trees. Funct Ecol 30:1480-1490. DOI: 10.1111/1365-2435.12623Malmqvist C., Wallin E., Lindstrom A., Sall H., 2017. Differences in bud burst timing and bud freezing tolerance among interior and coastal seed sources of Douglas fir. Trees-Struct Funct 31:1987-1998. DOI: 10.1007/s00468-017-1603-xMan R.Z., Lu P.X., Dang Q.L., 2017. Insufficient chilling effects vary among boreal tree species and chilling duration. Frontiers in Plant Science 8:9. DOI: 10.3389/fpls.2017.01354Man R.Z., Lu P.X., Dang Q.L., 2020. Effects of insufficient chilling on budburst and growth of six temperate forest tree species in Ontario. New Forests:13. DOI: 10.1007/s11056-020-09795-1Marino G.P., Kaiser D.P., Gu L.H., Ricciuto D.M., 2011. Reconstruction of false spring occurrences over the southeastern United States, 1901-2007: an increasing risk of spring freeze damage? Environ Res Lett 6:8. DOI: 10.1088/1748-9326/6/2/024015Marquis B., Bergeron Y., Simard M., Tremblay F., 2020. Probability of spring frosts, Not growing degree-days, drives onset of spruce bud burst in plantations at the boreal-temperate forest ecotone. Frontiers in Plant Science 11. DOI: 10.3389/fpls.2020.01031Menzel A., Helm R., Zang C., 2015. Patterns of late spring frost leaf damage and recovery in a European beech (Fagus sylvatica L.) stand in south-eastern Germany based on repeated digital photographs. Frontiers in Plant Science 6:110. DOI: 10.3389/fpls.2015.00110Meyers T. (2020) US-WBW: Walker Branch Watershed. Accessed 22 October 2020Muffler L., Beierkuhnlein C., Aas G., Jentsch A., Schweiger A.H., Zohner C., Kreyling J., 2016. Distribution ranges and spring phenology explain late frost sensitivity in 170 woody plants from the Northern Hemisphere. Glob Ecol Biogeogr 25:1061-1071. DOI: 10.1111/geb.12466Muilu-Makela R., Vuosku J., Saarinen M., Hamberg L., Ruotsalainen S., Haggman H., Sarjala T., 2017. Coping with spring frost-effects on polyamine metabolism of Scots pine seedlings. iForest 10:227-236. DOI: 10.3832/ifor2003-009National Meteorological Information Centre (2020) China Meteorological Data Service Center. Accessed 22 October 2020Ögren E., Nilsson T., Sundblad L.-G., 1997. Relationship between respiratory depletion of sugars and loss of cold hardiness in coniferous seedlings over-wintering at raised temperatures: indications of different sensitivities of spruce and pine. Plant, Cell & Environment 20:247-253. DOI: 10.1046/j.1365-3040.1997.d01-56.xOlsson C., Olin S., Lindstrom J., Jonsson A.M., 2017. Trends and uncertainties in budburst projections of Norway spruce in Northern Europe. Ecol Evol 7:9954-9969. DOI: 10.1002/ece3.3476Pagter M., Arora R., 2013. Winter survival and deacclimation of perennials under warming climate: physiological perspectives. Physiol Plant 147:75-87. DOI: 10.1111/j.1399-3054.2012.01650.xPark I.W., 2016. Timing the bloom season: a novel approach to evaluating reproductive phenology across distinct regional flora. Landsc Ecol 31:1567-1579. DOI: 10.1007/s10980-016-0339-0Perry L.G., Shafroth P.B., Hay L.E., Markstrom S.L., Bock A.R., 2020. Projected warming disrupts the synchrony of riparian seed release and snowmelt streamflow. New Phytol 225:693-712. DOI: 10.1111/nph.16191Polgar C.A., Primack R.B., 2011. Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol 191:926-941. DOI: 10.1111/j.1469-8137.2011.03803.xPrincipe A., van der Maaten E., van der Maaten-Theunissen M., Struwe T., Wilmking M., Kreyling J., 2017. Low resistance but high resilience in growth of a major deciduous forest tree (Fagus sylvatica L.) in response to late spring frost in southern Germany. Trees-Struct Funct 31:743-751. DOI: 10.1007/s00468-016-1505-3Puchalka R., Koprowski M., Przybylak J., Przybylak R., Dabrowski H.P., 2016. Did the late spring frost in 2007 and 2011 affect tree-ring width and earlywood vessel size in Pedunculate oak (Quercus robur) in northern Poland? Int J Biometeorol 60:1143-1150. DOI: 10.1007/s00484-015-1107-6Rodrigo J., 2000. Spring frosts in deciduous fruit trees - morphological damage and flower hardiness. Sci Hortic 85:155-173. DOI: 10.1016/s0304-4238(99)00150-8Scheifinger H., Menzel A., Koch E., Peter C., 2003. Trends of spring time frost events and phenological dates in Central Europe. Theor Appl Climatol 74:41-51. DOI: 10.1007/s00704-002-0704-6Schieber B., Kubov M., Janik R., 2017. Effects of climate warming on vegetative phenology of the common beech Fagus sylvatica in a submontane forest of the Western Carpathians: two-decade analysis. Pol J Ecol 65:339-351. DOI: 10.3161/15052249pje2017.65.3.003Strimbeck G.R., DeHayes D.H., 2000. Rapid freezing injury in red spruce: seasonal changes in sensitivity and effects of temperature range. Tree Physiology 20:187-194Thomas F.M., Sporns K., 2009. Frost sensitivity of Fagus sylvatica and co-occurring deciduous tree species at exposed sites. Flora 204:74-81. DOI: 10.1016/j.flora.2008.01.006Thum T., Aalto T., Laurila T., Aurela M., Hatakka J., Lindroth A., Vesala T., 2009. Spring initiation and autumn cessation of boreal coniferous forest CO2 exchange assessed by meteorological and biological variables. Tellus Ser B-Chem Phys Meteorol 61:701-717. DOI: 10.1111/j.1600-0889.2009.00441.xVitasse Y. et al., 2019. Contrasting resistance and resilience to extreme drought and late spring frost in five major European tree species. Glob Change Biol 25:3781-3792. DOI: 10.1111/gcb.14803Vitasse Y., Schneider L., Rixen C., Christen D., Rebetez M., 2018. Increase in the risk of exposure of forest and fruit trees to spring frosts at higher elevations in Switzerland over the last four decades. Agric For Meteorol 248:60-69. DOI: 10.1016/j.agrformet.2017.09.005Wang L., Wu Z.F., He H.S., Wang F.X., Du H.B., Zong S.W., 2017. Changes in start, end, and length of frost-free season across Northeast China. Int J Climatol 37:271-283. DOI: 10.1002/joc.5002Weather of China (2020) Introduction of Changchun City. Accessed 22 October 2020Wei H.X., Guo P., 2017. Carbohydrate metabolism during new root growth in transplanted Larix olgensis seedlings: post-transplant response to nursery-applied inorganic fertilizer and organic amendment. iForest 10:15-22. DOI: 10.3832/ifor1988-009Wei H.X., Xu C.Y., Ma L.Y., Duan J., Jiang L.N., Ren J., 2014. Effect of Late-season fertilizatoin on nutrient reserves and carbohydrate accumulation in bareroot Larix olgensis seedlings. J Plant Nutr 37:279-293. DOI: 10.1080/01904167.2013.859697Wood J., Gu L.H. (2020) US-MOz: Missouri Ozark Site. Accessed 22 October 2020Zhang D. et al., 2016. Effects of forest type and urbanization on species composition and diversity of urban forest in Changchun, Northeast China. Urban Ecosyst 19:455-473. DOI: 10.1007/s11252-015-0473-5Zohner C.M. et al., 2020. Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia. Proc Natl Acad Sci U S A 117:12192-12200. DOI: 10.1073/pnas.1920816117

0pt;font-family:"Times New Roman",serif;mso-fareast-font-family:宋体;








Research article