Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Woody biomass production lags stem-girth increase by over one month in coniferous forests

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Purchase on Springer Link

Instant access to full article PDF

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Seasonal dynamics of stem-girth increase, xylem size increase and woody biomass production.
Figure 2: Asynchrony of xylem size increase and woody biomass production, along with xylem phenology.
Figure 3: Delay between xylem size increase and woody biomass production for the major coniferous forest biomes of the Northern Hemisphere.
Figure 4: Coordination of xylem size increase and woody biomass production with environmental factors.

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Gough, C., Vogel, C., Schmid, H., Su, H.-B. & Curtis, P. Multi-year convergence of biometric and meteorological estimates of forest carbon storage. Agr. Forest Meteorol. 148, 158–170 (2008).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Stine, A. R., Huybers, P. & Fung, I. Y. Changes in the phase of the annual cycle of surface temperature. Nature 457, 435–440 (2009).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Richardson, A. D., Braswell, B. H., Hollinger, D. Y., Jenkins, J. P. & Ollinger, S. V. Near-surface remote sensing of spatial and temporal variation in canopy phenology. Ecol. Appl. 19, 1417–1428 (2009).

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Granier, A., Bréda, N., Longdoz, B., Gross, P. & Ngao, J. Ten years of fluxes and stand growth in a young beech forest at Hesse, North-eastern France. Ann. For. Sci. 65, 704–716 (2008).

    Article  Google Scholar 

  15. Zweifel, R. 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).

    Article  CAS  Google Scholar 

  16. King, G., Fonti, P., Nievergelt, D., Büntgen, U. & Frank, D. Climatic drivers of hourly to yearly tree radius variations along a 6 °C natural warming gradient. Agr. Forest. Meteorol. 168, 36–46 (2013).

    Article  Google Scholar 

  17. Cuny, H. E., Rathgeber, C. B. K., Frank, D., Fonti, P. & Fournier, M. Kinetics of tracheid development explain conifer tree-ring structure. New Phytol. 203, 1231–1241 (2014).

    Article  Google Scholar 

  18. Camarero, J. J., Olano, J. M. & Parras, A. Plastic bimodal xylogenesis in conifers from continental Mediterranean climates. New Phytol. 185, 471–480 (2010).

    Article  Google Scholar 

  19. Jackson, S. D. Plant responses to photoperiod. New Phytol. 181, 517–531 (2009).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  21. Oribe, Y., Funada, R., Shibagaki, M. & Kubo, T. Cambial reactivation in locally heated stems of the evergreen conifer Abies sachalinensis (Schmidt) Masters. Planta 212, 684–691 (2001).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  23. Simard, S. 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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  28. Babst, F. 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).

    Article  CAS  Google Scholar 

  29. Lachenbruch, B. & McCulloh, K. A. 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).

    Article  Google Scholar 

  30. Medvigy, D., Wofsy, S., Munger, J., Hollinger, D. & Moorcroft, P. Mechanistic scaling of ecosystem function and dynamics in space and time: Ecosystem Demography model version 2. J. Geophys. Res. 114, G01002 (2009).

    Article  Google Scholar 

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

Authors and Affiliations

Authors

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.

Corresponding author

Correspondence to Henri E. Cuny.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cuny, H., Rathgeber, C., Frank, D. et al. Woody biomass production lags stem-girth increase by over one month in coniferous forests. Nature Plants 1, 15160 (2015). https://doi.org/10.1038/nplants.2015.160

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.160

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing