Abstract

Wood is the main terrestrial biotic reservoir for long-term carbon sequestration1, and its formation in trees consumes around 15% of anthropogenic carbon dioxide emissions each year2. However, the seasonal dynamics of woody biomass production cannot be quantified from eddy covariance or satellite observations. As such, our understanding of this key carbon cycle component, and its sensitivity to climate, remains limited. Here, we present high-resolution cellular based measurements of wood formation dynamics in three coniferous forest sites in northeastern France, performed over a period of 3 years. We show that stem woody biomass production lags behind stem-girth increase by over 1 month. We also analyse more general phenological observations of xylem tissue formation in Northern Hemisphere forests and find similar time lags in boreal, temperate, subalpine and Mediterranean forests. These time lags question the extension of the equivalence between stem size increase and woody biomass production to intra-annual time scales3, 4, 5, 6. They also suggest that these two growth processes exhibit differential sensitivities to local environmental conditions. Indeed, in the well-watered French sites the seasonal dynamics of stem-girth increase matched the photoperiod cycle, whereas those of woody biomass production closely followed the seasonal course of temperature. We suggest that forecasted changes in the annual cycle of climatic factors7 may shift the phase timing of stem size increase and woody biomass production in the future.

  • Subscribe to Nature Plants for full access:

    $62

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    Sequestration of atmospheric CO2 in global carbon pools. Energy Environ. Sci. 1, 86–100 (2008).

  2. 2.

    et al. A large and persistent carbon sink in the world's forests. Science 333, 988–993 (2011).

  3. 3.

    et al. Factors controlling long-and short-term sequestration of atmospheric CO2 in a mid-latitude forest. Science 294, 1688–1691 (2001).

  4. 4.

    et al. The carbon balance of two contrasting mountain forest ecosystems in Switzerland: similar annual trends, but seasonal differences. Ecosystems 14, 1289–1309 (2011).

  5. 5.

    , , , & Multi-year convergence of biometric and meteorological estimates of forest carbon storage. Agr. Forest Meteorol. 148, 158–170 (2008).

  6. 6.

    et al. Drought impact on forest carbon dynamics and fluxes in Amazonia. Nature 519, 78–82 (2015).

  7. 7.

    , & Changes in the phase of the annual cycle of surface temperature. Nature 457, 435–440 (2009).

  8. 8.

    et al. Enhanced seasonal exchange of CO2 by northern ecosystems since 1960. Science 341, 1085–1089 (2013).

  9. 9.

    et al. The next generation of scenarios for climate change research and assessment. Nature 463, 747–756 (2010).

  10. 10.

    Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future. Global Change Biol. 9, 479–492 (2003).

  11. 11.

    et al. Belowground carbon allocation in forests estimated from litterfall and IRGA-based soil respiration measurements. Agr. Forest Meteorol. 113, 39–51 (2002).

  12. 12.

    , , , & Near-surface remote sensing of spatial and temporal variation in canopy phenology. Ecol. Appl. 19, 1417–1428 (2009).

  13. 13.

    et al. Remote sensing estimates of boreal and temperate forest woody biomass: carbon pools, sources, and sinks. Remote Sens. Environ. 84, 393–410 (2003).

  14. 14.

    , , , & Ten years of fluxes and stand growth in a young beech forest at Hesse, North-eastern France. Ann. For. Sci. 65, 704–716 (2008).

  15. 15.

    et al. Link between continuous stem radius changes and net ecosystem productivity of a subalpine Norway spruce forest in the Swiss Alps. New Phytol. 187, 819–830 (2010).

  16. 16.

    , , , & Climatic drivers of hourly to yearly tree radius variations along a 6 °C natural warming gradient. Agr. Forest. Meteorol. 168, 36–46 (2013).

  17. 17.

    , , , & Kinetics of tracheid development explain conifer tree-ring structure. New Phytol. 203, 1231–1241 (2014).

  18. 18.

    , & Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol. 185, 471–480 (2010).

  19. 19.

    Plant responses to photoperiod. New Phytol. 181, 517–531 (2009).

  20. 20.

    et al. Critical temperatures for xylogenesis in conifers of cold climates. Global Ecol. Biogeogr. 17, 696–707 (2008).

  21. 21.

    , , & Cambial reactivation in locally heated stems of the evergreen conifer Abies sachalinensis (Schmidt) Masters. Planta 212, 684–691 (2001).

  22. 22.

    et al. Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol. 170, 301–310 (2006).

  23. 23.

    et al. Intra-annual dynamics of non-structural carbohydrates in the cambium of mature conifer trees reflects radial growth demands. Tree Physiol. 33, 913–923 (2013).

  24. 24.

    Carbon limitation in trees. J. Ecol. 91, 4–17 (2003).

  25. 25.

    Lignification and lignin topochemistry—an ultrastructural view. Phytochemistry 57, 859–873 (2001).

  26. 26.

    et al. Temperature-induced responses of xylem structure of Larix sibirica (Pinaceae) from the Russian Altay. Am. J. Bot. 100, 1332–1343 (2013).

  27. 27.

    et al. Tree-ring width and density data around the Northern Hemisphere: Part 1, local and regional climate signals. Holocene 12, 737 (2002).

  28. 28.

    et al. Above-ground woody carbon sequestration measured from tree rings is coherent with net ecosystem productivity at five eddy-covariance sites. New Phytol. 201, 1289–1303 (2014).

  29. 29.

    & Traits, properties, and performance: how woody plants combine hydraulic and mechanical functions in a cell, tissue, or whole plant. New Phytol. 204, 747–764 (2014).

  30. 30.

    , , , & Mechanistic scaling of ecosystem function and dynamics in space and time: Ecosystem Demography model version 2. J. Geophys. Res. 114, G01002 (2009).

Download references

Acknowledgements

H.E.C. and C.B.K.R. thank E. Cornu, E. Farré, C. Freyburger, P. Gelhaye and A. Mercanti for fieldwork at the French sites; M. Harroué for sample preparation in the laboratory; B. Longdoz of the forest ecology and ecophysiology (EEF) team of the French national institute for agronomy research (INRA), and the association for the study and monitoring of air pollution in Alsace (ASPA), for the meteorological data. M. Nicolas of the French permanent plot network for the monitoring of forest ecosystems (RENECOFOR) for the meteorological data and the description of the soil profiles. L. Kulmala and J. Guiot for comments on an early version of this manuscript. H.M., T.J. and P.N. thank T. Kalliokoski for the Solböle data. J.G.H. thanks L.H. Zhai for laboratory work and Y. Bergeron for project supervision. H.V. and V.G. thank J. Hacurová and G. Vichrová for laboratory work. H.E.C. was supported by a grant overseen by the French National Research Agency (ANR) as part of the ‘Investissements d'Avenir’ programme (ANR-11-LABX-0002-01, Lab of Excellence ARBRE). D.F. and P.F. acknowledge the SNF (INTEGRAL-121859 and LOTFOR-150205), and the WSL SwissTree project. J.G.H. was funded by 100 Talents Program of the Chinese Academy of Sciences (Y421081001). I.S. and A.G. were funded by the Austrian Science Fund (FWF P19563-B16 and P22280-B16). H.M., T.J. and P.N. were supported by grants from the Academy of Finland (Nos. 250299, 257641 and 265504). P.P., J.G. and K.C. were supported by the Slovenian Research Agency, young researchers' programme and programmes P4-0015 and P4-0107. H.V. and V.G. were supported by the European Social Fund and the state budget of the Czech Republic, Project Indicators of trees vitality Reg. No. CZ.1.07/2.3.00/20.0265. M.V.B. and A.V.K. were supported by Russian Science Foundation project 14-14-00295. The Canadian boreal forest dataset collected by H.M, C.K, A.D. and S.R. were supported by the CRSNG, the FRQNT, the FCI and the Consortium de Recherche sur la Forêt Boréale Commerciale. S.R. was also supported by the CAS President's International Fellowship Initiative (GRANT No. 2015VBB032). The dataset on xylem phenology was generated by the GLOBOXYLO initiative (http://www6.nancy.inra.fr/foret-bois-lerfob_eng/Projects/Current/GLOBOXYLO), which was developed in the framework of the FPS COST Action STReESS (FP1106).

Author information

Affiliations

  1. INRA, UMR 1092 LERFOB, Champenoux F-54280, France

    • Henri E. Cuny
    • , Cyrille B. K. Rathgeber
    •  & Meriem Fournier
  2. AgroParisTech, UMR 1092 LERFOB, Nancy F-54000, France

    • Henri E. Cuny
    • , Cyrille B. K. Rathgeber
    •  & Meriem Fournier
  3. Swiss Federal Research Institute WSL, Birmensdorf CH-8903, Switzerland

    • Henri E. Cuny
    • , David Frank
    •  & Patrick Fonti
  4. Oeschger Centre for Climate Change Research, Bern CH-3012, Switzerland

    • David Frank
  5. Natural Resources Institute Finland, PO Box 18, Vantaa 01301, Finland

    • Harri Mäkinen
    • , Tuula Jyske
    •  & Pekka Nöjd
  6. Slovenian Forestry Institute, Vecna pot 2, Ljubljana 1000, Slovenia

    • Peter Prislan
    •  & Jožica Gričar
  7. Université du Québec à Chicoutimi, Chicoutimi, QC G7H 2B1, Canada

    • Sergio Rossi
    • , Annie Deslauriers
    • , Hubert Morin
    •  & Cornelia Krause
  8. Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, Provincial Key Laboratory of Applied Botany South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China

    • Sergio Rossi
    •  & Jian-Guo Huang
  9. Department of Geography and Regional Planning, Environmental Science Institute (IUCA), University of Zaragoza, C/Pedro Cerbuna 12, Zaragoza 50009, Spain

    • Edurne Martinez del Castillo
    •  & Martin De Luis
  10. Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, Coimbra 3000–456, Portugal

    • Filipe Campelo
    • , Joana Vieira
    •  & Cristina Nabais
  11. Faculty of Forestry and Wood Technology, Department of Wood Science, Mendel University in Brno, Zemědělská 3, Brno 613 00, Czech Republic

    • Hanuš Vavrčík
    •  & Vladimír Gryc
  12. Instituto Pirenaico de Ecología (IPE-CSIC), Avda. Montañana 1005, Zaragoza 50192, Spain

    • Jesus Julio Camarero
  13. V.N. Sukachev Institute of Forest, SB RAS, Krasnoyarsk 660036, Russia

    • Marina V. Bryukhanova
    •  & Alexander V. Kirdyanov
  14. Siberian Federal University, 660041 Krasnoyarsk, Russia

    • Marina V. Bryukhanova
    •  & Alexander V. Kirdyanov
  15. Biotechnical Faculty, University of Ljubljana, Jamnikarjeva 101, Ljubljana 1000, Slovenia

    • Katarina Čufar
  16. University of Innsbruck, Institute of Botany, Sternwartestrasse 15, Innsbruck 6020, Austria

    • Walter Oberhuber
    • , Irene Swidrak
    •  & Andreas Gruber
  17. Faculty of Science, Charles University in Prague, Prague CZ-12843, Czech Republic

    • Vaclav Treml
  18. Key Laboratory of Tibetan Environment Changes and Land Surface Processes and Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, Beijing 100101, China

    • Xiaoxia Li
    •  & Eryuan Liang
  19. Department of Geography, Queen's University, Kingston, Canada

    • Gregory King

Authors

  1. Search for Henri E. Cuny in:

  2. Search for Cyrille B. K. Rathgeber in:

  3. Search for David Frank in:

  4. Search for Patrick Fonti in:

  5. Search for Harri Mäkinen in:

  6. Search for Peter Prislan in:

  7. Search for Sergio Rossi in:

  8. Search for Edurne Martinez del Castillo in:

  9. Search for Filipe Campelo in:

  10. Search for Hanuš Vavrčík in:

  11. Search for Jesus Julio Camarero in:

  12. Search for Marina V. Bryukhanova in:

  13. Search for Tuula Jyske in:

  14. Search for Jožica Gričar in:

  15. Search for Vladimír Gryc in:

  16. Search for Martin De Luis in:

  17. Search for Joana Vieira in:

  18. Search for Katarina Čufar in:

  19. Search for Alexander V. Kirdyanov in:

  20. Search for Walter Oberhuber in:

  21. Search for Vaclav Treml in:

  22. Search for Jian-Guo Huang in:

  23. Search for Xiaoxia Li in:

  24. Search for Irene Swidrak in:

  25. Search for Annie Deslauriers in:

  26. Search for Eryuan Liang in:

  27. Search for Pekka Nöjd in:

  28. Search for Andreas Gruber in:

  29. Search for Cristina Nabais in:

  30. Search for Hubert Morin in:

  31. Search for Cornelia Krause in:

  32. Search for Gregory King in:

  33. Search for Meriem Fournier in:

Contributions

C.B.K.R. conceived the French experimental device and compiled the Northern Hemisphere dataset on xylem phenology. H.E.C. created the data for the French sites, performed the research and analysed the data with the help of C.B.K.R. H.E.C. wrote the manuscript and prepared the figures, with the assistance of C.B.K.R., D.F., P.F. and M.F. All the authors contributed with xylem phenology data and discussed the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Henri E. Cuny.

Supplementary information