Advertisement

International Journal of Biometeorology

, Volume 63, Issue 12, pp 1631–1640 | Cite as

Responses of bud-break phenology to daily-asymmetric warming: daytime warming intensifies the advancement of bud break

  • Shaokang Zhang
  • Nathalie Isabel
  • Jian-Guo HuangEmail author
  • Hai Ren
  • Sergio Rossi
Original Paper

Abstract

There is evidence that the ongoing climate change is happening through nighttime rather than daytime warming. How such a daily-asymmetric warming modifies plant phenology is still unclear. We investigated the effects of asymmetric warming on bud break by daily monitoring seedlings belonging to 26 black spruce [Picea mariana (Mill.) BSP.] and 15 balsam fir [Abies balsamea (L.) Mill.] provenances from the native range in Canada. Seedlings were subjected to either daytime or nighttime warming in three growth chambers at temperatures ranging between 10 and 24 °C. On average, a warming of 4 °C advanced the timings of bud break in both species by 2.4 days, with the later phases being more sensitive to the treatment. Bud break of both species responded more strongly to daytime warming, with the bud break occurred 1.2 and 3.2 days earlier under daytime than nighttime warming in black spruce and balsam fir, respectively. A marked ecotypic differentiation was only observed in black spruce that originated from provenances distributed broadly across Canada, with seedlings from the warmest provenance completing bud break 8.3 days later than those from the coldest one. However, no significant effect of provenance was observed for balsam fir, the narrowly distributed species. Overall, the above results suggest that a higher temporal resolution such as temperatures during daytime and nighttime, and higher spatial resolution should be taken into account to improve the accuracy of phenological model predictions under global change scenarios. Phenological models based on daily average temperature should take into account the diverging impacts of asymmetric warming on plant phenology. Our findings may indicate that the influence of warming on plant phenology may be less dramatic than expected.

Keywords

Bud burst Climate change Phenotype Ecotype Black spruce Balsam fir 

Notes

Acknowledgments

The authors thank C.-D. Bouchard Ouellet, I. Froment, J. Gravel-Grenier, M.-J. Tremblay, and S. Carles for technical support and A. Garside for checking the English text.

Authors’ contributions

S. Rossi designed the experiment. S. Zhang performed the experiment. S. Zhang and S. Rossi wrote the article with contributions from N. Isabel, J-G. Huang, and H Ren.

Funding information

This work was funded by China Postdoctoral Science Foundation funded project, Natural Resources Canada, Consortium de Recherche sur la Foret Boreale Commerciale, Canada Foundation for Innovation, the China Scholarship Council, the National Natural Science Foundation of China (31570584, 41661144007, 41861124001), and the International Collaborative Key Project of the Chinese Academy of Sciences (CAS) (GJHZ1752).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

484_2019_1776_MOESM1_ESM.docx (329 kb)
ESM 1 (DOCX 329 kb)

References

  1. Antonucci S, Rossi S, Deslauriers A, Lombardi F, Marchetti M, Tognetti R (2015) Synchronisms and correlations of spring phenology between apical and lateral meristems in two boreal conifers. Tree Physiol 35:1086–1094Google Scholar
  2. Balducci L, Deslauriers A, Giovannelli A, Beaulieu M, Delzon S, Rossi S, Rathgeber CB (2015) How do drought and warming influence survival and wood traits of Picea mariana saplings? J Exp Bot 66:377–389Google Scholar
  3. Beaulieu J, Bousquet J (2010) Facteurs génétiques affectant la variabilité des cernes annuels chez les espèces arborescentes nordiquesGoogle Scholar
  4. Bennie 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 Chang Biol 16:1503–1514Google Scholar
  5. Boulouf Lugo J, Deslauriers A, Rossi S (2012) Duration of xylogenesis in black spruce lengthened between 1950 and 2010. Ann Bot 110:1099–1108Google Scholar
  6. Caffarra A, Donnelly A (2011) The ecological significance of phenology in four different tree species: effects of light and temperature on bud burst. Int J Biometeorol 55:711–721Google Scholar
  7. CaraDonna PJ, Iler AM, Inouye DW (2014) Shifts in flowering phenology reshape a subalpine plant community. P Natl Acad Sci USA 111:4916–4921Google Scholar
  8. Chuine I (2010) Why does phenology drive species distribution? Philos Trans R Soc Lond Ser B Biol Sci 365:3149–3160Google Scholar
  9. Cinget B, Gerardi S, Beaulieu J, Bousquet J (2015) Less pollen-mediated gene flow for more signatures of glacial lineages: congruent evidence from balsam fir cpDNA and mtDNA for multiple refugia in eastern and central North America. PLoS One 10:e0122815Google Scholar
  10. Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–252Google Scholar
  11. De Barba D, Rossi S, Deslauriers A, Morin H (2016) Effects of soil warming and nitrogen foliar applications on bud burst of black spruce. Trees-Structure and Function 30:87–97Google Scholar
  12. Dhont C, Sylvestre P, Gros-Louis M-C, Isabel N (2010) Field guide for identifying apical bud break and bud formation stages in white spruce. Nature Resources Canada, Quebec:1–48Google Scholar
  13. Donat MG, Alexander LV (2012) The shifting probability distribution of global daytime and night-time temperatures. Geophys Res Lett 39:L14707Google Scholar
  14. Ellwood ER, Temple SA, Primack RB, Bradley NL, Davis CC (2013) Record-breaking early flowering in the eastern United States. PLoS One 8:e53788Google Scholar
  15. Fu YH, Campioli M, Deckmyn G, Janssens IA (2013) Sensitivity of leaf unfolding to experimental warming in three temperate tree species. Agric For Meteorol 181:125–132Google Scholar
  16. Fu YH, Liu Y, De Boeck HJ, Menzel A, Nijs I, Peaucelle M, Penuelas J et al (2016) Three times greater weight of daytime than of night-time temperature on leaf unfolding phenology in temperate trees. New Phytol 212:590–597Google Scholar
  17. Fu YH, Piao S, Zhao H, Jeong SJ, Wang X, Vitasse Y, Ciais P, Janssens IA (2014) Unexpected role of winter precipitation in determining heat requirement for spring vegetation green-up at northern middle and high latitudes. Glob Chang Biol 20:3743–3755Google Scholar
  18. Fu YH, Zhao H, Piao S, Peaucelle M, Peng S, Zhou G, Ciais P, Huang M, Menzel A, Peñuelas J, Song Y, Vitasse Y, Zeng Z, Janssens IA (2015) Declining global warming effects on the phenology of spring leaf unfolding. Nature 526:104–107Google Scholar
  19. Grindal G, Junttila O, Reid JB, Moe R (1998) The response to gibberellin in Pisum sativum grown under alternating day and night temperature. J Plant Growth Regul 17:161–167Google Scholar
  20. Hansen E, Olsen JE, Junttila O (1999) Gibberellins and subapical cell divisions in relation to bud set and bud break in Salix pentandra. J Plant Growth Regul 18:167–170Google Scholar
  21. Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292Google Scholar
  22. Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems; with 47 tables. Springer Science & Business MediaGoogle Scholar
  23. Korner C, Basler D (2010) Phenology under global warming. Science 327:1461–1462Google Scholar
  24. Laube J, Sparks TH, Estrella N, Hofler J, Ankerst DP, Menzel A (2014) Chilling outweighs photoperiod in preventing precocious spring development. Glob Chang Biol 20:170–182Google Scholar
  25. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659–659Google Scholar
  26. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-KÜBler K et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976Google Scholar
  27. Nealis VG, Régnière J (2004) Insect–host relationships influencing disturbance by the spruce budworm in a boreal mixedwood forest. Can J For Res 34:1870–1882Google Scholar
  28. Pallardy SG (2010) Physiology of woody plants. Academic Press, New YorkGoogle Scholar
  29. Park H, Jeong S-J, Ho C-H, Kim J, Brown ME, Schaepman ME (2015) Nonlinear response of vegetation green-up to local temperature variations in temperate and boreal forests in the Northern Hemisphere. Remote Sens Environ 165:100–108Google Scholar
  30. Peng S, Piao S, Ciais P, Myneni RB, Chen A, Chevallier F, Dolman AJ, Janssens IA, Peñuelas J, Zhang G, Vicca S, Wan S, Wang S, Zeng H (2013) Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation. Nature 501:88–92Google Scholar
  31. Piao S, Tan J, Chen A, Fu YH, Ciais P, Liu Q, Janssens IA, Vicca S, Zeng Z, Jeong SJ, Li Y, Myneni RB, Peng S, Shen M, Peñuelas J (2015) Leaf onset in the northern hemisphere triggered by daytime temperature. Nat Commun 6:6911Google Scholar
  32. Piao SL, Friedlingstein P, Ciais P, Viovy N, Demarty J (2007) Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Glob Biogeochem Cycles 21Google Scholar
  33. Picard G, Quegan S, Delbart N, Lomas MR, Toan T, Woodward FI (2005) Bud-burst modelling in Siberia and its impact on quantifying the carbon budget. Glob Chang Biol 11:2164–2176Google Scholar
  34. Plummer DA, Caya D, Frigon A, Cote H, Giguere M, Paquin D, Biner S et al (2006) Climate and climate change over North America as simulated by the Canadian RCM. J Clim 19:3112–3132Google Scholar
  35. Prunier J, Laroche J, Beaulieu J, Bousquet J (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Mol Ecol 20:1702–1716Google Scholar
  36. Régnière J, St-Amant R (2007) Stochastic simulation of daily air temperature and precipitation from monthly normals in North America north of Mexico. Int J Biometeorol 51:415–430Google Scholar
  37. Richardson AD, Anderson RS, Arain MA, Barr AG, Bohrer G, Chen G, Chen JM, Ciais P, Davis KJ, Desai AR, Dietze MC, Dragoni D, Garrity SR, Gough CM, Grant R, Hollinger DY, Margolis HA, McCaughey H, Migliavacca M, Monson RK, Munger JW, Poulter B, Raczka BM, Ricciuto DM, Sahoo AK, Schaefer K, Tian H, Vargas R, Verbeeck H, Xiao J, Xue Y (2012) Terrestrial biosphere models need better representation of vegetation phenology: results from the North American Carbon Program Site Synthesis. Glob Chang Biol 18:566–584Google Scholar
  38. Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173Google Scholar
  39. Rossi S (2015) Local adaptations and climate change: converging sensitivity of bud break in black spruce provenances. Int J Biometeorol 59:827–835Google Scholar
  40. Rossi S, Bousquet J (2014) The bud break process and its variation among local populations of boreal black spruce. Front Plant Sci 5:574Google Scholar
  41. Rossi S, Isabel N (2017) Bud break responds more strongly to daytime than night-time temperature under asymmetric experimental warming. Glob Chang Biol 23:446–454Google Scholar
  42. Santner A, Calderon-Villalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307Google Scholar
  43. Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the Northern Hemisphere. Glob Chang Biol 12:343–351Google Scholar
  44. Silvestro R, Rossi S, Zhang S, Froment I, Huang JG, Saracino A (2019) From phenology to forest management: ecotypes selection can avoid early or late frosts, but not both. For Ecol Manag 436:21–26Google Scholar
  45. Stocker T (2014) Climate change 2013: the physical science basis: Working Group I contribution to the Fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University PressGoogle Scholar
  46. Tan J, Piao S, Chen A, Zeng Z, Ciais P, Janssens IA, Mao J, Myneni RB, Peng S, Peñuelas J, Shi X, Vicca S (2015) Seasonally different response of photosynthetic activity to daytime and night-time warming in the Northern Hemisphere. Glob Chang Biol 21:377–387Google Scholar
  47. Thingnaes E, Torre S, Ernstsen A, Moe R (2003) Day and night temperature responses in Arabidopsis: effects on gibberellin and auxin content, cell size, morphology and flowering time. Ann Bot 92:601–612Google Scholar
  48. Thomson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early-flowering geophyte. Philos Trans R Soc Lond Ser B Biol Sci 365:3187–3199Google Scholar
  49. Toomey M, Friedl MA, Frolking S, Hufkens K, Klosterman S, Sonnentag O, Baldocchi DD, Bernacchi CJ, Biraud SC, Bohrer G, Brzostek E, Burns SP, Coursolle C, Hollinger DY, Margolis HA, Mccaughey H, Monson RK, Munger JW, Pallardy S, Phillips RP, Torn MS, Wharton S, Zeri M, And AD, Richardson AD (2015) Greenness indices from digital cameras predict the timing and seasonal dynamics of canopy-scale photosynthesis. Ecol Appl 25:99–115Google Scholar
  50. Turnbull MH, Murthy R, Griffin KL (2002) The relative impacts of daytime and night-time warming on photosynthetic capacity in Populus deltoides. Plant Cell Environ 25:1729–1737Google Scholar
  51. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363Google Scholar
  52. Wan SQ, Xia JY, Liu WX, Niu SL (2009) Photosynthetic overcompensation under nocturnal warming enhances grassland carbon sequestration. Ecology 90:2700–2710Google Scholar
  53. Wang Y, Li X, Dawadi B, Eckstein D, Liang E (2012) Phenological variation in height growth and needle unfolding of Smith fir along an altitudinal gradient on the southeastern Tibetan Plateau. Trees 27:401–407Google Scholar
  54. Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, Davies TJ, Kraft NJB, Ault TR, Bolmgren K, Mazer SJ, McCabe GJ, McGill BJ, Parmesan C, Salamin N, Schwartz MD, Cleland EE (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497Google Scholar
  55. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10Google Scholar
  56. Zhang X, Vincent LA, Hogg WD, Niitsoo A (2000) Temperature and precipitation trends in Canada during the 20th century. Atmosphere-Ocean 38:395–429Google Scholar

Copyright information

© ISB 2019

Authors and Affiliations

  • Shaokang Zhang
    • 1
    • 2
    • 3
    • 4
  • Nathalie Isabel
    • 5
  • Jian-Guo Huang
    • 1
    • 2
    • 3
    Email author
  • Hai Ren
    • 1
    • 2
    • 3
  • Sergio Rossi
    • 1
    • 6
  1. 1.Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  2. 2.Center of Plant Ecology, Core Botanical GardensChinese Academy of SciencesGuangzhouChina
  3. 3.Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  4. 4.University of the Chinese Academy of SciencesBeijingChina
  5. 5.Natural Resources Canada, Canadian Forest Service, Laurentian Forestry CentreQuébecCanada
  6. 6.Département des Sciences FondamentalesUniversité du Québec à ChicoutimiChicoutimiCanada

Personalised recommendations