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


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.


Bud burst Climate change Phenotype Ecotype Black spruce Balsam fir 



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)


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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

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