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The persistence of carbon in the African forest understory

Nature Plantsvolume 5pages133140 (2019) | Download Citation


Quantifying carbon dynamics in forests is critical for understanding their role in long-term climate regulation1,2,3,4. Yet little is known about tree longevity in tropical forests3,5,6,7,8, a factor that is vital for estimating carbon persistence3,4. Here we calculate mean carbon age (the period that carbon is fixed in trees7) in different strata of African tropical forests using (1) growth-ring records with a unique timestamp accurately demarcating 66 years of growth in one site and (2) measurements of diameter increments from the African Tropical Rainforest Observation Network (23 sites). We find that in spite of their much smaller size, in understory trees mean carbon age (74 years) is greater than in sub-canopy (54 years) and canopy (57 years) trees and similar to carbon age in emergent trees (66 years). The remarkable carbon longevity in the understory results from slow and aperiodic growth as an adaptation to limited resource availability9,10,11. Our analysis also reveals that while the understory represents a small share (11%) of the carbon stock12,13, it contributes disproportionally to the forest carbon sink (20%). We conclude that accounting for the diversity of carbon age and carbon sequestration among different forest strata is critical for effective conservation management14,15,16 and for accurate modelling of carbon cycling4.

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Data availability

The input data and R-scripts to generate the figures and tables are available for download using the following private link: https://figshare.com/s/06c793575d3b52ef5574. Images of wood cores are available using the following link: https://figshare.com/s/e6101fe7d330f8ea140a. This folder also contains all annotation documents needed to visualize growth ring boundaries on the wood samples (please consult the README document for guidelines). Wood samples used to conduct this analysis are stored in the Tervuren xylarium (http://www.africamuseum.be/collections/browsecollections/naturalsciences/earth/xylarium). These samples may be studied, within the Tervuren xylarium, on request addressed to the curator H.B. (hans.beeckman@africamuseum.be) or the corresponding author W.H. (whubau@gmail.com).

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Nkulapark: W.H. and T.D.M. were both funded by the Brain programme of the Belgian Federal Government (BR/132/A1/AFRIFORD and BR/143/A3/HERBAXYLAREDD). The PhD project of T.D.M and the tenure track of J.V.d.B. were supported by Ghent University Special Research Fund (BOF). Fieldwork was sponsored by the King Leopold III fund for nature exploration and conservation. B.A.I. is supported by the Institut National pour l’Étude et la Recherche Agronomiques en R.D.Congo (INERA- RDC- Luki) and the École Régionale Postuniversitaire d’Aménagement et de Gestion intégrés des Forêts et Territoires tropicaux (ERAIFT Kinshasa). We thank WWF-RDC (G. Lejeune), INERA and ERAIFT for facilitating fieldwork in the Luki Reserve. We thank the INERA employees (J.-B. Ndunga, J.-M., F. Mbungu Phaka, L. Ngoma, P. Noble), the WWF ecoguards and the students of the Universities of Kinshasa (UNIKIN) and Boma for assistance in the field. For assistance with datasets we thank M. De Groot, K. Lievens, P. Dekeyser, S. Willen and J. Kempenaers. The 23 permanent inventory plots: This paper is also a product of the AfriTRON network, for which we are indebted to hundreds of institutions, field assistants and local communities for establishing and maintaining the plots. This network has been supported by the European Research Council (291585, ‘T-FORCES’ – Tropical Forests in the Changing Earth System, Advanced Grant to O.L.P. and S.L.L.), the Gordon and Betty Moore Foundation, the David and Lucile Packard Foundation, the European Union’s Seventh Framework Programme (no. 283080, ‘GEOCARBON’) and Natural Environment Research Council (NERC) Consortium Grant ‘TROBIT’ (no. NE/D005590/1), ‘BIO-RED’ (no. NE/N012542/1) and a NERC New Investigators Grant, the Royal Society, the Centre for International Forestry (CIFOR) and Gabon’s National Parks Agency (ANPN). We are indebted to the University of Yaounde I, the National Herbarium of Yaounde, Rougier-Gabon, the Marien Ngouabi University of Brazzaville, WCS-Congo, Salonga National Park, WCS-D.R.Congo and the University of Kisangani for logistical support in Africa.

Author information

Author notes

  1. These authors contributed equally: W. Hubau, T. De Mil.


  1. Service of Wood Biology, Royal Museum for Central Africa, Tervuren, Belgium

    • Wannes Hubau
    • , Tom De Mil
    • , Bhély Angoboy Ilondea
    • , Laurent Nsenga
    • , Benjamin Toirambe
    • , Camille Couralet
    • , Nils Bourland
    • , Sofie Dierickx
    • , Emmanuel Kasongo Yakusu
    • , Mélissa Rousseau
    • , John Tshibamba Mukendi
    •  & Hans Beeckman
  2. UGent-Woodlab, Laboratory of Wood Technology, Department of Environment, Ghent University, Ghent, Belgium

    • Wannes Hubau
    • , Tom De Mil
    • , Jan Van den Bulcke
    • , Joris Van Acker
    • , Victor Deklerck
    •  & Emmanuel Kasongo Yakusu
  3. School of Geography, University of Leeds, Leeds, UK

    • Wannes Hubau
    • , Oliver L. Phillips
    • , Martin J. P. Sullivan
    • , Serge K. Begne
    • , Timothy R. Baker
    • , Martin Gilpin
    • , Gabriela Lopez-Gonzalez
    • , Georgia Pickavance
    • , Joey Talbot
    •  & Simon L. Lewis
  4. Centre for X-ray Tomography , Ghent University, Ghent, Belgium

    • Jan Van den Bulcke
    • , Joris Van Acker
    •  & Victor Deklerck
  5. Institut National pour l’Étude et la Recherche Agronomique, Kinshasa, Democratic Republic of the Congo

    • Bhély Angoboy Ilondea
  6. École Régionale Postuniversitaire d’Aménagement et de Gestion intégrés des Forêts et Territoires tropicaux , Kinshasa, Democratic Republic of the Congo

    • Bhély Angoboy Ilondea
  7. Centre for Ecology and Hydrology, Penicuik, UK

    • Lindsay F. Banin
  8. Plant Systematic and Ecology Laboratory, Higher Teachers’ Training College, University of Yaounde, Yaounde, Cameroon

    • Serge K. Begne
    • , Marie-Noel D. Kamdem
    • , Bonaventure Sonké
    • , Hermann Taedoumg
    •  & Lise Zemagho
  9. CIFOR, Bogor, Indonesia

    • Nils Bourland
    •  & Terry Sunderland
  10. Forest Resources Management, Gembloux Agro-Bio Tech, University of Liège, Liège, Belgium

    • Nils Bourland
    •  & Jean-Louis Doucet
  11. Resources and Synergies Development, Singapore, Singapore

    • Nils Bourland
    •  & Mélissa Rousseau
  12. Rougier-Gabon, Libreville, Gabon

    • Eric Chezeaux
  13. Nicholas School of the Environment, Duke University, Durham, NC, USA

    • Connie J. Clark
    •  & John R. Poulsen
  14. Grantham Research Institute on Climate Change and the Environment, London, UK

    • Murray Collins
  15. Inventory and Monitoring Program, National Park Service, Fredericksburg, VA, USA

    • James A. Comiskey
  16. Smithsonian Institution, Washington, DC, USA

    • James A. Comiskey
  17. Department of Geography, University College London, London, UK

    • Aida Cuni-Sanchez
    •  & Simon L. Lewis
  18. Department of Geography and Environment, University of York, York, UK

    • Aida Cuni-Sanchez
  19. Wildlife Conservation Society-DR Congo, Kinshasa I, Democratic Republic of the Congo

    • Corneille E. N. Ewango
    • , Jean-Remy Makana
    •  & Jacques Mukinzi
  20. Centre de Formation et de Recherche en Conservation Forestière , Epulu, Democratic Republic of the Congo

    • Corneille E. N. Ewango
  21. Faculté de Gestion de Ressources Naturelles Renouvelables, Université de Kisangani, Kisangani, Democratic Republic of the Congo

    • Corneille E. N. Ewango
    • , Emmanuel Kasongo Yakusu
    • , Faustin M. Mbayu
    •  & John Tshibamba Mukendi
  22. Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK

    • Ted R. Feldpausch
  23. National Herbarium, Yaounde, Cameroon

    • Christelle Gonmadje
  24. ForestGEO, Smithsonian Tropical Research Institute, Panamá, Republic of Panama

    • Jefferson S. Hall
  25. Royal Botanic Garden Edinburgh, Edinburgh, UK

    • David J. Harris
  26. Service d’Évolution Biologique et écologie, Faculté des Sciences, Université Libre de Bruxelles, Brussels, Belgium

    • Olivier J. Hardy
    •  & Jason Vleminckx
  27. Faculty of Science, Department of Botany and Plant Physiology, University of Buea, Buea, Cameroon

    • Marie-Noel D. Kamdem
  28. Environmental Change Institute, School of Geography and the Environment, University of Oxford, Oxford, UK

    • Yadvinder Malhi
    •  & Sam Moore
  29. Salonga National Park, Kinshasa I, Democratic Republic of the Congo

    • Jacques Mukinzi
  30. Bureau Waardenburg, Culemborg, the Netherlands

    • Jan Reitsma
  31. Faculty of Forestry, University of British Columbia, Vancouver, Canada

    • Terry Sunderland
  32. Faculté des Sciences Appliquées, Université de Mbujimayi, Mbujimayi, Democratic Republic of the Congo

    • John Tshibamba Mukendi
  33. Yale School of Forestry and Environmental Studies, New Haven, CT, USA

    • Peter M. Umunay
  34. Department of Biological Sciences, Florida International University, Miami, FL, USA

    • Jason Vleminckx
  35. Agence Nationale des Parcs Nationaux, Libreville, Gabon

    • Lee J. T. White
  36. Institut de Recherche en Écologie Tropicale, Libreville, Gabon

    • Lee J. T. White
  37. School of Natural Sciences, University of Stirling, Stirling, UK

    • Lee J. T. White


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W.H., T.D.M., J.V.d.B., J.V.A. and H.B. conceived and designed the Nkulapark study and S.L.L. conceived the AfriTRON plot network. T.D.M. and B.A.I. coordinated collection of Nkulapark data and wood cores. T.D.M. and J.V.d.B. measured growth ring series. W.H. carried out the data analysis and wrote the paper. S.L.L., O.L.P., T.R.B. and Y.M. conceived the ForestPlots.net database, and most co-authors helped collecting AfriTRON forest census data. S.L.L., B.S., S.K.B., A.C.S., W.H., T.S., T.R.F., T.S., C.E.N.E. and L.W.W. coordinated forest plots data collection. M.J.P.S., G.L.G., S.L.L., O.L.P., T.R.B. and G.P. contributed tools to analyse and curate data. All co-authors commented on or approved the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Wannes Hubau.

Supplementary information

  1. Supplementary Information

    Supplementary Figures 1–4

  2. Reporting Summary

  3. Supplementary Table 1

    Number of growth rings, growth-ring formation rate, tree age and mean carbon age of all 55 Nkulapark trees with 1,948 nail traces used for this analysis

  4. Supplementary Table 2

    List of all 23 plots included in this analysis, with geographic coordinates, plot size, dates of first and last census, and the main researchers for each plot

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