Annals of Forest Science

, Volume 71, Issue 8, pp 831–842 | Cite as

Elevated atmospheric CO2 and humidity delay leaf fall in Betula pendula, but not in Alnus glutinosa or Populus tremula × tremuloides

  • Douglas GodboldEmail author
  • Arvo Tullus
  • Priit Kupper
  • Jaak Sõber
  • Ivika Ostonen
  • Jasmin A. Godbold
  • Martin Lukac
  • Iftekhar U. Ahmed
  • Andrew R. Smith
Original Paper



Anthropogenic activity has increased the level of atmospheric CO2, which is driving an increase of global temperatures and associated changes in precipitation patterns. At Northern latitudes, one of the likely consequences of global warming is increased precipitation and air humidity.


In this work, the effects of both elevated atmospheric CO2 and increased air humidity on trees commonly growing in northern European forests were assessed.


The work was carried out under field conditions by using Free Air Carbon dioxide Enrichment (FACE) and Free Air Humidity Manipulation (FAHM) systems. Leaf litter fall was measured over 4 years (FACE) or 5 years (FAHM) to determine the effects of FACE and FAHM on leaf phenology.


Increasing air humidity delayed leaf litter fall in Betula pendula, but not in Populus tremula × tremuloides. Similarly, under elevated atmospheric CO2, leaf litter fall was delayed in B. pendula, but not in Alnus glutinosa. Increased CO2 appeared to interact with periods of low precipitation in summer and high ozone levels during these periods to effect leaf fall.


This work shows that increased CO2 and humidity delay leaf fall, but this effect is species-specific.


Climate change Free air CO2 enrichment (FACE) Free air humidity manipulation Leaf fall Ozone 



The FAHM study was supported by the Ministry of Education and Science of Estonia (grant SF SF0180025s12) and by the EU through the European Social Fund (Mobilitas postdoctoral grant MJD 257) and the European Regional Development Fund (Centre of Excellence ENVIRON) and Project no. 3.2.0802.11-0043 (BioAtmos). The development of BangorFACE site infrastructure was funded by SRIF. We thank the Aberystwyth and Bangor Universities Partnership Centre for Integrated Research in the Rural Environment and the Forestry Commission Wales for financially supporting the running costs of the experiment. Andrew Smith was supported by the Sir Williams Roberts PhD Scholarship match funded by the Drapers’ Company.

Supplementary material

13595_2014_382_MOESM1_ESM.pdf (169 kb)
Online Resource 1 (PDF 169 kb)


  1. Ahmed IUMT (2006) Leaf decomposition of birch (Betula pendula), alder (Alnus glutinosa) and beech (Fagus sylvatica) grown under elevated atmospheric CO2. Dissertation, Bangor UniversityGoogle Scholar
  2. Ainsworth EA, Long SP (2005) What have we learned from 15 years of free air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–371PubMedCrossRefGoogle Scholar
  3. Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199CrossRefGoogle Scholar
  4. Chang H, Jones ML, Banowetz GM, Clark DG (2003) Overproduction of cytokinins in petunia flowers transformed with PSAG12-IPT delays corolla senescence and decreases sensitivity to ethylene. Plant Physiol 132:1–10CrossRefGoogle Scholar
  5. Dong H, Niu Y, Li W, Zhang D (2008) Effects of cotton rootstock on endogenous cytokinins and abscisic acid in xylem sap and leaves in relation to leaf senescence. J Exp Bot 59:1295–1304PubMedCrossRefGoogle Scholar
  6. Eamus D, Jarvis PG (1989) The direct effects of increases in the global atmospheric CO2 concentration on natural and commercial temperate trees and forests. Adv Ecol Res 19:1–55CrossRefGoogle Scholar
  7. Ferreira V, Gonçalves AL, Godbold DL, Canhoto C (2010) Effect of increased atmospheric CO2 on the performance of an aquatic detritivore through changes in water temperature and litter quality. Glob Chang Biol 16:3284–3296CrossRefGoogle Scholar
  8. Hansen R, Mander Ü, Soosaar K, Maddison M, Lõhmus K, Kupper P, Kanal A, Sõber J (2013) Greenhouse gas fluxes in an open air humidity manipulation experiment. Landsc Ecol 28:637–649CrossRefGoogle Scholar
  9. Herrick JD, Thomas RB (2003) Leaf senescence and late-season net photosynthesis of sun and shade leaves of overstory sweetgum (Liquidambar styraciflua) grown in elevated and ambient carbon dioxide concentrations. Tree Physiol 23:109–118PubMedCrossRefGoogle Scholar
  10. Houpis JLJ, Surano KA, Cowles S, Shinn JH (1988) Chlorophyll and carotenoid concentrations in two varieties of pine ponderosa seedlings subjected to long-term elevated carbon dioxide. Tree Physiol, 4:187–193Google Scholar
  11. IPCC (2013) Climate change 2013: the physical science basis. Cambridge University Press, CambridgeGoogle Scholar
  12. Iverson CM (2010) Digging deeper: fine-root response to rising atmospheric CO2 concentration in forested ecosystems. New Phytol 186:346–357CrossRefGoogle Scholar
  13. Kont A, Jaagus J, Aunap R (2003) Climate change scenarios and the effect of sea-level rise for Estonia. Glob Planet Change 36:1–15CrossRefGoogle Scholar
  14. Kupper P, Sõber J, Sellin A, Lõhmus K, Tullus A, Räim O, Lubenets K, Tulva I, Uri V, Zobel M, Kull O, Sõber A (2011) An experimental facility for Free Air Humidity Manipulation (FAHM) can alter water flux through deciduous tree canopy. Environ Exp Bot 72:432–438CrossRefGoogle Scholar
  15. Leutzinger S, Hätenschwiler S (2013) Beyond global change: lessons from 25 years of CO2 research. Oecologia 171:639–651CrossRefGoogle Scholar
  16. Li JH, Dijkstra P, Hymus GJ, Wheeler RM, Piastuch WC, Hinkle CR, Drake BR (2000) Leaf senescence of Quercus myrtifolia as affected by long-term CO2 enrichment in its native environment. Glob Chang Biol 6:727–733CrossRefGoogle Scholar
  17. Lim PO, Kim HJ, Name HG (2007) Leaf senescence. Ann Rev Plant Biol 58:115–136CrossRefGoogle Scholar
  18. Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kubler K, Bissolli P, Brasklavska O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatczak K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, van Vliet AJH, Wielgolaski F-M, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1–8CrossRefGoogle Scholar
  19. Morris K, A-H-Mackerness S, Page T, John F, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23:677–685PubMedCrossRefGoogle Scholar
  20. Murakami PF, Schaberg PG, Shane JB (2008) Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiol 28:1467–1473PubMedCrossRefGoogle Scholar
  21. Parts K, Tedersoo L, Lõhmus K, Kupper P, Rosenvald K, Sõber A, Ostonen I (2013) Increased air humidity and understory composition shape short root traits and the colonizing ectomycorrhizal fungal community in silver birch stand. For Ecol Manag 310:720–728CrossRefGoogle Scholar
  22. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 19 Mar 2014
  23. Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Plant Sci 5:278–282CrossRefGoogle Scholar
  24. Schaberg PG, Murakami PF, Turner MR, Heitz HK, Hawley GJ (2008) Association of red coloration with senescence of sugar maple leaves in autumn. Trees 22:573–578CrossRefGoogle Scholar
  25. Sellin A, Tullus A, Niglas A, Õunapuu E, Karusion A, Lõhmus K (2013) Humidity-driven changes in growth rate, photosynthetic capacity, hydraulic properties and other functional traits in silver birch (Betula pendula). Ecol Res 28:523–535CrossRefGoogle Scholar
  26. Sigurdsson BD (2001) Elevated [CO2] and nutrient status modified leaf phenology and growth rhythm of young Populus trichocarpa trees in a 3-year field study. Trees 15:403–413CrossRefGoogle Scholar
  27. Smith AR, Lukac M, Hood R, Healey JR, Miglietta F, Godbold D (2013a) Elevated CO2 enrichment induces a differential biomass response in a mixed species temperate forest plantation. New Phytol 198:156–168PubMedCrossRefGoogle Scholar
  28. Smith AR, Lukac M, Bambrick M, Miglietta F, Godbold DL (2013b) Tree species diversity interacts with elevated CO2 to induce a greater root system response. Glob Chang Biol 19:217–228PubMedCrossRefGoogle Scholar
  29. Swartzberg D, Hanael R, Granot D (2010) Relationship between hexokinase and cytokinin in the regulation of leaf senescence and seed germination. Plant Biol 13:439–444CrossRefGoogle Scholar
  30. Tallis MJ, Lin Y, Rogers A, Zhang J, Street NR, Miglietta F, Karnosky DF, De Angelis P, Calfapietra C, Taylor G (2010) The transcriptome of Populus in elevated CO2 reveals increased anthocyanin biosynthesis during delayed autumnal senescence. New Phytol 186:415–428PubMedCrossRefGoogle Scholar
  31. Taylor G, Tallis MJ, Giardina CP, Percy KE, Miglietta F, Gupta PS, Gioli B, Calfapietra C, Gielen B, Kubiske MEM, Scarascia-mugnozza GE, Kets K, Long SP, Karnosky DF (2008) Future atmospheric CO2 leads to delayed autumnal senescence. Glob Chang Biol 14:264–275CrossRefGoogle Scholar
  32. Tullus A, Kupper P, Sellin A, Parts L, Sõber J, Tullus T, Lõhmus K, Sõber A, Tullus H (2012) Climate change at Northern latitudes: rising atmospheric humidity decreases transpiration, N-uptake and growth rate of hybrid aspen. PLoS One 7:e42648PubMedCentralPubMedCrossRefGoogle Scholar
  33. Winger A, Purdy S, MacLean JA, Poutau N (2006) The role of sugars in integrating environmental signals during leaf senescence. J Exp Bot 57:391–399CrossRefGoogle Scholar
  34. Wood S (2014) The mgcv Package v. 1.3-28, Mixed GAM Computation Vehicle with GCV/AIC/REML smoothness estimation. Accessed 19 Mar 2014
  35. Yendrik CR, Leisner CP, Ainsworth EA (2013) Chronic ozone exacerbates the reduction in photosynthesis and acceleration of senescence caused by limited N availability in Nicotiana sylvestris. Glob Chang Biol 19:3155–3166CrossRefGoogle Scholar
  36. Yong JWH, Wong SC, Letham DS, Hocart CH, Farquhar GD (2000) Effects of elevated [CO2] and nitrogen nutrition on cytokinins in the xylem sap and leaves of cotton. Plant Physiol 124:767–779PubMedCentralPubMedCrossRefGoogle Scholar
  37. Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14:1220–1226PubMedCrossRefGoogle Scholar
  38. Zhou L, Tucker CJ, Kaufmann RK, Slayback D, Shabanov NV, Myneni RB (2001) Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J Geophys Res 106:20069–20083CrossRefGoogle Scholar
  39. Zuur AF, Leno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer Verlag, New York, LLC, p 574Google Scholar
  40. Zuur AF, Leno EN, Smith, GM (2007) Analysing Ecological Data. Springer, New York, p 680Google Scholar

Copyright information

© INRA and Springer-Verlag France 2014

Authors and Affiliations

  • Douglas Godbold
    • 1
    Email author
  • Arvo Tullus
    • 2
  • Priit Kupper
    • 2
  • Jaak Sõber
    • 2
  • Ivika Ostonen
    • 3
  • Jasmin A. Godbold
    • 4
  • Martin Lukac
    • 5
  • Iftekhar U. Ahmed
    • 1
  • Andrew R. Smith
    • 6
  1. 1.Institute of Forest Ecology, Universität für Bodenkultur (BOKU)ViennaAustria
  2. 2.Department of Botany, Institute of Ecology and Earth SciencesUniversity of TartuTartuEstonia
  3. 3.Department of Geography, Institute of Ecology and Earth SciencesUniversity of TartuTartuEstonia
  4. 4.School of Ocean and Earth Science, National Oceanography Centre, SouthamptonUniversity of SouthamptonSouthamptonUK
  5. 5.School of Agriculture, Policy and DevelopmentUniversity of ReadingReadingUK
  6. 6.School of Environment, Natural Resources and GeographyBangor UniversityGwyneddUK

Personalised recommendations