, Volume 21, Issue 7, pp 1445–1458 | Cite as

Spatial Variation of Soil CO2, CH4 and N2O Fluxes Across Topographical Positions in Tropical Forests of the Guiana Shield

  • Elodie A. CourtoisEmail author
  • Clément Stahl
  • Joke Van den Berge
  • Laëtitia Bréchet
  • Leandro Van Langenhove
  • Andreas Richter
  • Ifigenia Urbina
  • Jennifer L. Soong
  • Josep Peñuelas
  • Ivan A. Janssens


The spatial variation of soil greenhouse gas fluxes (GHG; carbon dioxide—CO2, methane—CH4 and nitrous oxide—N2O) remains poorly understood in highly complex ecosystems such as tropical forests. We used 240 individual flux measurements of these three GHGs from different soil types, at three topographical positions and in two extreme hydric conditions in the tropical forests of the Guiana Shield (French Guiana, South America) to (1) test the effect of topographical positions on GHG fluxes and (2) identify the soil characteristics driving flux variation in these nutrient-poor tropical soils. Surprisingly, none of the three GHG flux rates differed with topographical position. CO2 effluxes covaried with soil pH, soil water content (SWC), available nitrogen and total phosphorus. The CH4 fluxes were best explained by variation in SWC, with soils acting as a sink under drier conditions and as a source under wetter conditions. Unexpectedly, our study areas were generally sinks for N2O and N2O fluxes were partly explained by total phosphorus and available nitrogen concentrations. This first study describing the spatial variation of soil fluxes of the three main GHGs measured simultaneously in forests of the Guiana Shield lays the foundation for specific studies of the processes underlying the observed patterns.


tropical forest GHG soil fluxes Guiana Shield soil characteristics spatial variation French Guiana 



This research was supported by the European Research Council Synergy grant ERC-2013-SyG 610028-IMBALANCE-P. We thank the staff of the Nouragues station, managed by USR mixte LEEISA (CNRS; Cayenne), and the Paracou station, managed by UMR Ecofog (CIRAD, INRA; Kourou). Both research stations received support from “Investissement d’Avenir” grants managed by Agence Nationale de la Recherche (CEBA: ANR-10-LABX-25-01, ANAEE-France: ANR-11-INBS-0001). We thank the subject-matter editor Dr Butterbach-Bahl, Dr Teh and one anonymous reviewer for their comments on previous versions of this manuscript. We thank Nicola Arriga, Jan Segers and Fred Kockelbergh for building the chambers and for advice on the field measurements. We are grateful to Stanislas Talaga, Jérôme Levy-Valensky and Jean-Pierre Robert for their help in the field, to Oriol Grau and Vincent Freycon for the identification and characterization of each topographical position and to Margarethe Watzka for the gas analyses.

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  1. Allié E, Pélissier R, Engel J, Petronelli P, Freycon V, Deblauwe V, Soucémarianadin L, Weigel J, Baraloto C. 2015. Pervasive local-scale tree-soil habitat association in a tropical forest community. PLoS ONE 10:e0141488.CrossRefGoogle Scholar
  2. Arias-Navarro C, Díaz-Pinés E, Klatt S, Brandt P, Rufino MC, Butterbach-Bahl K, Verchot L. 2017. Spatial variability of soil N2O and CO2 fluxes in different topographic positions in a tropical montane forest in Kenya. J Geophys Res Biogeosci 122:514–27.CrossRefGoogle Scholar
  3. Bai Z, Yang G, Chen H, Zhu Q, Chen D, Li Y, Wang X, Wu Z, Zhou G, Peng C. 2014. Nitrous oxide fluxes from three forest types of the tropical mountain rainforests on Hainan Island, China. Atmos Environ 92:469–77.CrossRefGoogle Scholar
  4. Baraloto C, Morneau F, Bonal D, Blanc L, Ferry B. 2007. Seasonal water stress tolerance and habitat associations within four neotropical tree genera. Ecology 88:478–89.CrossRefGoogle Scholar
  5. Bartlett KB, Harriss RC. 1993. Review and assessment of methane emissions from wetlands. Chemosphere 26:261–320.CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S. 2014. lme4: linear mixed-effects models using Eigen and S4. R Package Version 1(7):1–23.Google Scholar
  7. Bonal D, Bosc A, Ponton S, Goret J, Burban B, Gross P, Bonnefond J, Elbers J, Longdoz B, Epron D. 2008. Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana. Glob Change Biol 14:1917–33.CrossRefGoogle Scholar
  8. Bongers F. 2001. Nouragues: dynamics and plant-animal interactions in a Neotropical rainforest. Berlin: Springer.CrossRefGoogle Scholar
  9. Bonhomme V, Picq S, Gaucherel C, Claude J. 2014. Momocs: outline analysis using R. J Stat Softw 56(13):1–24.CrossRefGoogle Scholar
  10. Bray RH, Kurtz LT. 1945. Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46.CrossRefGoogle Scholar
  11. Bréchet L, Ponton S, Alméras T, Bonal D, Epron D. 2011. Does spatial distribution of tree size account for spatial variation in soil respiration in a tropical forest? Plant Soil 347:293–303.CrossRefGoogle Scholar
  12. Bremner JM. 1997. Sources of nitrous oxide in soils. Nutrient Cycl Agroecosyst 49:7–16.CrossRefGoogle Scholar
  13. Breuer L, Papen H, Butterbach-Bahl K. 2000. N2O emission from tropical forest soils of Australia. J Geophys Res Atmos 105:26353–67.CrossRefGoogle Scholar
  14. Brito LDF, Marques Júnior J, Pereira GT, Souza ZM, La Scala Júnior N. 2009. Soil CO2 emission of sugarcane fields as affected by topography. Sci Agric 66:77–83.CrossRefGoogle Scholar
  15. Brumme R, Borken W, Finke S. 1999. Hierarchical control on nitrous oxide emission in forest ecosystems. Glob Biogeochem Cycles 13:1137–48.CrossRefGoogle Scholar
  16. Butterbach-Bahl K, Kock M, Willibald G, Hewett B, Buhagiar S, Papen H, Kiese R. 2004. Temporal variations of fluxes of NO, NO2, N2O, CO2, and CH4 in a tropical rain forest ecosystem. Glob Biogeochem Cycles 18(3):GB3012.CrossRefGoogle Scholar
  17. Butterbach-Bahl K, Baggs E, Dannenmann M, Kiese R, Zechmeister-Boltenstern S. 2013. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Philos Trans R Soc Lond Ser B 368(1621):20130122.CrossRefGoogle Scholar
  18. Chapuis-Lardy L, Wrage N, Metay A, Chotte J, Bernoux M. 2007. Soils, a sink for N2O? A review. Glob Change Biol 13:1–17.CrossRefGoogle Scholar
  19. Chen D, Li J, Lan Z, Hu S, Bai Y. 2015. Soil acidification exerts a greater control on soil respiration than soil nitrogen availability in grasslands subjected to long-term nitrogen enrichment. Funct Ecol 30(4):658–69.CrossRefGoogle Scholar
  20. Corre M, Van Kessel C, Pennock D. 1996. Landscape and seasonal patterns of nitrous oxide emissions in a semiarid region. Soil Sci Soc Am J 60:1806–15.CrossRefGoogle Scholar
  21. Davidson EA, Verchot LV. 2000. Testing the hole-in-the-pipe model of nitric and nitrous oxide emissions from soils using the TRAGNET database. Glob Biogeochem Cycles 14:1035–43.CrossRefGoogle Scholar
  22. Davidson EA, Verchot LV, Cattanio JH, Ackerman IL, Carvalho J. 2000. Effects of soil water content on soil respiration in forests and cattle pastures of eastern Amazonia. Biogeochemistry 48:53–69.CrossRefGoogle Scholar
  23. Davidson EA, Ishida FY, Nepstad DC. 2004. Effects of an experimental drought on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob Change Biol 10:718–30.CrossRefGoogle Scholar
  24. Davidson EA, Nepstad DC, Ishida FY, Brando PM. 2008. Effects of an experimental drought and recovery on soil emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical forest. Glob Change Biol 14:2582–90.CrossRefGoogle Scholar
  25. Dray S, Dufour AB. 2007. The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20.CrossRefGoogle Scholar
  26. Dutaur L, Verchot LV. 2007. A global inventory of the soil CH4 sink. Glob Biogeochem Cycles 21:GB4013. Scholar
  27. Epron D, Bosc A, Bonal D, Freycon V. 2006. Spatial variation of soil respiration across a topographic gradient in a tropical rain forest in French Guiana. J Trop Ecol 22:565–74.CrossRefGoogle Scholar
  28. Fang Y, Gundersen P, Zhang W, Zhou G, Christiansen JR, Mo J, Dong S, Zhang T. 2009. Soil–atmosphere exchange of N2O, CO2 and CH4 along a slope of an evergreen broad-leaved forest in southern China. Plant Soil 319:37–48.CrossRefGoogle Scholar
  29. Ferry B, Morneau F, Bontemps J, Blanc L, Freycon V. 2010. Higher treefall rates on slopes and waterlogged soils result in lower stand biomass and productivity in a tropical rain forest. J Ecol 98:106–16.CrossRefGoogle Scholar
  30. Fewster RM, Buckland ST, Siriwardena GM, Baillie SR, Wilson JD. 2000. Analysis of population trends for farmland birds using generalized additive models. Ecology 81:1970–84.CrossRefGoogle Scholar
  31. Geng S, Chen Z, Han S, Wang F, Zhang J. 2017. Rainfall reduction amplifies the stimulatory effect of nitrogen addition on N2O emissions from a temperate forest soil. Sci Rep 7:43329.CrossRefGoogle Scholar
  32. Gibbs AK, Barron CN. 1993. The geology of the Guiana Shield. Oxford: Oxford University Press.Google Scholar
  33. Gourlet-Fleury S, Guehl J-M, Laroussinie O. 2004. Ecology and management of a neotropical rainforest. Lessons drawn from Paracou, a long-term experimental research site in French Guiana: Elsevier.Google Scholar
  34. Grau O, Peñuelas J, Ferry B, Freycon V, Blanc L, Desprez M, Baraloto C, Chave J, Descroix L, Dourdain A. 2017. Nutrient-cycling mechanisms other than the direct absorption from soil may control forest structure and dynamics in poor Amazonian soils. Sci Rep 7:45017.CrossRefGoogle Scholar
  35. Hall SJ, Asner GP, Kitayama K. 2004. Substrate, climate, and land use controls over soil N dynamics and N-oxide emissions in Borneo. Biogeochemistry 70:27–58.CrossRefGoogle Scholar
  36. Hammond DS. 2005. Tropical forests of the Guiana shield: ancient forests in a modern world. Wallingford: CABI.CrossRefGoogle Scholar
  37. Hanson P, Edwards N, Garten C, Andrews J. 2000. Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–46.CrossRefGoogle Scholar
  38. Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova S, Tyukavina A, Thau D, Stehman S, Goetz S, Loveland T. 2013. High-resolution global maps of 21st-century forest cover change. Science 342:850–3.CrossRefGoogle Scholar
  39. Hättenschwiler S, Aeschlimann B, Coûteaux M, Roy J, Bonal D. 2008. High variation in foliage and leaf litter chemistry among 45 tree species of a neotropical rainforest community. New Phytol 179:165–75.CrossRefGoogle Scholar
  40. Hink L, Nicol GW, Prosser JI. 2017. Archaea produce lower yields of N2O than bacteria during aerobic ammonia oxidation in soil. Environ Microbiol 19:4829–37.CrossRefGoogle Scholar
  41. Hörtnagl L, Wohlfahrt G. 2014. Methane and nitrous oxide exchange over a managed hay meadow. Biogeosci Online 11:7219.CrossRefGoogle Scholar
  42. Janssens IA, Barigah ST, Ceulemans R. 1998. Soil CO2 efflux rates in different tropical vegetation types in French Guiana. In: EDP sciences, Vol. 55, pp 671–80.CrossRefGoogle Scholar
  43. Janssens I, Lankreijer H, Matteucci G, Kowalski A, Buchmann N, Epron D, Pilegaard K, Kutsch W, Longdoz B, Grünwald T. 2001. Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Glob Change Biol 7:269–78.CrossRefGoogle Scholar
  44. Jones CM, Spor A, Brennan FP, Breuil M-C, Bru D, Lemanceau P, Griffiths B, Hallin S, Philippot L. 2014. Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Change 4:801–5.CrossRefGoogle Scholar
  45. Keller M, Reiners WA. 1994. Soil-atmosphere exchange of nitrous oxide, nitric oxide, and methane under secondary succession of pasture to forest in the Atlantic lowlands of Costa Rica. Glob Biogeochem Cycles 8:399–409.CrossRefGoogle Scholar
  46. Keller M, Varner R, Dias JD, Silva H, Crill P, de Oliveira Jr RC, Asner GP. 2005. Soil–atmosphere exchange of nitrous oxide, nitric oxide, methane, and carbon dioxide in logged and undisturbed forest in the Tapajos National Forest, Brazil. Earth Interact 9:1–28.CrossRefGoogle Scholar
  47. Kuhn M. 2008. Caret package. J Stat Softw 28:1–26.CrossRefGoogle Scholar
  48. Liptzin D, Silver WL, Detto M. 2011. Temporal dynamics in soil oxygen and greenhouse gases in two humid tropical forests. Ecosystems 14:171–82.CrossRefGoogle Scholar
  49. Luizao RC, Luizao FJ, Paiva RQ, Monteiro TF, Sousa LS, Kruijt B. 2004. Variation of carbon and nitrogen cycling processes along a topographic gradient in a central Amazonian forest. Glob Change Biol 10:592–600.CrossRefGoogle Scholar
  50. Luo G, Kiese R, Wolf B, Butterbach-Bahl K. 2013. Effects of soil temperature and moisture on methane uptake and nitrous oxide emissions across three different ecosystem types. Biogeosciences 10:3205–19.CrossRefGoogle Scholar
  51. Martin JG, Bolstad PV. 2009. Variation of soil respiration at three spatial scales: components within measurements, intra-site variation and patterns on the landscape. Soil Biol Biochem 41:530–43.CrossRefGoogle Scholar
  52. Meir P, Wood TE, Galbraith DR, Brando PM, Da Costa AC, Rowland L, Ferreira LV. 2015. Threshold responses to soil moisture deficit by trees and soil in tropical rain forests: insights from field experiments. BioScience 65:882–92.CrossRefGoogle Scholar
  53. Merbold L, Steinlin C, Hagedorn F. 2013. Winter greenhouse gas fluxes (CO2, CH4 and N2O) from a subalpine grassland. Biogeosciences 10:3185–203.CrossRefGoogle Scholar
  54. Merbold L, Wohlfahrt G, Butterbach-Bahl K, Pilegaard K, DelSontro T, Stoy P, Zona D. 2015. Preface: towards a full greenhouse gas balance of the biosphere. Biogeosciences 12:453–6.CrossRefGoogle Scholar
  55. Morley N, Baggs EM. 2010. Carbon and oxygen controls on N2O and N2 production during nitrate reduction. Soil Biol Biochem 42:1864–71.CrossRefGoogle Scholar
  56. Morley N, Baggs EM, Dörsch P, Bakken L. 2008. Production of NO, N2O and N2 by extracted soil bacteria, regulation by NO2 − and O2 concentrations. FEMS Microbiol Ecol 65:102–12.CrossRefGoogle Scholar
  57. Nachtergaele FO, Spaargaren O, Deckers JA, Ahrens B. 2000. New developments in soil classification: world reference base for soil resources. Geoderma 96:345–57.CrossRefGoogle Scholar
  58. Nobre A, Keller M, Crill P, Harriss R. 2001. Short-term nitrous oxide profile dynamics and emissions response to water, nitrogen and carbon additions in two tropical soils. Biol Fertil Soils 34:363–73.CrossRefGoogle Scholar
  59. Parkin TB, Venterea RT, Hargreaves SK. 2012. Calculating the detection limits of chamber-based soil greenhouse gas flux measurements. J Environ Qual 41:705–15.CrossRefGoogle Scholar
  60. Pedersen AR, Petersen SO, Schelde K. 2010. A comprehensive approach to soil-atmosphere trace-gas flux estimation with static chambers. Eur J Soil Sci 61(6):888–902.CrossRefGoogle Scholar
  61. Peichl M, Arain A, Moore T, Brodeur J, Khomik M, Ullah S, Restrepo-Coupé N, McLaren J, Pejam M. 2014. Carbon and greenhouse gas balances in an age sequence of temperate pine plantations. Biogeosciences 11:5399–410.CrossRefGoogle Scholar
  62. Pennock D, Van Kessel C, Farrell R, Sutherland R. 1992. Landscape-scale variations in denitrification. Soil Sci Soc Am J 56:770–6.CrossRefGoogle Scholar
  63. Penuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J. 2013. Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934.CrossRefGoogle Scholar
  64. Petitjean C, Hénault C, Perrin A-S, Pontet C, Metay A, Bernoux M, Jehanno T, Viard A, Roggy J-C. 2015. Soil N2O emissions in French Guiana after the conversion of tropical forest to agriculture with the chop-and-mulch method. Agric Ecosyst Environ 208:64–74.CrossRefGoogle Scholar
  65. Prosser JI, Nicol GW. 2008. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10:2931–41.CrossRefGoogle Scholar
  66. Reiners WA, Keller M, Gerow KG. 1998. Estimating rainy season nitrous oxide and methane fluxes across forest and pasture landscapes in Costa Rica. Water Air Soil Pollut 105:117–30.CrossRefGoogle Scholar
  67. Rees RM, Wuta M, Furley PA, Li C. 2006. Nitrous oxide fluxes from savanna(miombo) woodlands in Zimbabwe. J Biogeogr 33:424–37.CrossRefGoogle Scholar
  68. Reth S, Reichstein M, Falge E. 2005. The effect of soil water content, soil temperature, soil pH-value and the root mass on soil CO2 efflux—a modified model. Plant Soil 268:21–33.CrossRefGoogle Scholar
  69. Riveros-Iregui DA, McGlynn BL. 2009. Landscape structure control on soil CO2 efflux variability in complex terrain: Scaling from point observations to watershed scale fluxes. J Geophys Res Biogeosci 114:G2.CrossRefGoogle Scholar
  70. Rowland L, Hill TC, Stahl C, Siebicke L, Burban B, Zaragoza-Castells J, Ponton S, Bonal D, Meir P, Williams M. 2014. Evidence for strong seasonality in the carbon storage and carbon use efficiency of an Amazonian forest. Glob Change Biol 20:979–91.CrossRefGoogle Scholar
  71. Rowlings D, Grace P, Kiese R, Weier K. 2012. Environmental factors controlling temporal and spatial variability in the soil-atmosphere exchange of CO2, CH4 and N2O from an Australian subtropical rainforest. Glob Change Biol 18:726–38.CrossRefGoogle Scholar
  72. Sabatier D, Grimaldi M, Prévost M-F, Guillaume J, Godron M, Dosso M, Curmi P. 1997. The influence of soil cover organization on the floristic and structural heterogeneity of a Guianan rain forest. Plant Ecol 131:81–108.CrossRefGoogle Scholar
  73. Schlesinger WH. 2013. An estimate of the global sink for nitrous oxide in soils. Glob Change Biol 19:2929–31.CrossRefGoogle Scholar
  74. Schmidt I, van Spanning RJM, Jetten MSM. 2004. Denitrification and ammonia oxidation by Nitrosomonas europaea wild-type, and NirK- and NorB-deficient mutants. Microbiology 150:4107–14.CrossRefGoogle Scholar
  75. Silver WL, Lugo A, Keller M. 1999. Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–28.Google Scholar
  76. Smith K, Ball T, Conen F, Dobbie K, Massheder J, Rey A. 2003. Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 54:779–91.CrossRefGoogle Scholar
  77. Stahl C, Burban B, Goret J-Y, Bonal D. 2011. Seasonal variations in stem CO2 efflux in the Neotropical rainforest of French Guiana. Ann For Sci 68:771–82.CrossRefGoogle Scholar
  78. Tang X, Liu S, Zhou G, Zhang D, Zhou C. 2006. Soil-atmospheric exchange of CO2, CH4, and N2O in three subtropical forest ecosystems in southern China. Glob Change Biol 12:546–60.CrossRefGoogle Scholar
  79. Teh YA, Silver WL. 2006. Effects of soil structure destruction on methane production and carbon partitioning between methanogenic pathways in tropical rain forest soils. J Geophys Res Biogeosci 111:G1.Google Scholar
  80. Teh YA, Silver WL, Conrad ME. 2005. Oxygen effects on methane production and oxidation in humid tropical forest soils. Glob Change Biol 11:1283–97.CrossRefGoogle Scholar
  81. Teh YA, Dubinsky EA, Silver WL, Carlson CM. 2008. Suppression of methanogenesis by dissimilatory Fe(III)-reducing bacteria in tropical rain forest soils: implications for ecosystem methane flux. Glob Change Biol 14:413–22.CrossRefGoogle Scholar
  82. Teh Y, Diem T, Jones S, Huaraca Quispe L, Baggs E, Morley N, Richards M, Smith P, Meir P. 2013. Methane and nitrous oxide fluxes from the tropical Andes. Biogeosci Discuss 10:17397–438.CrossRefGoogle Scholar
  83. Teh Y, Diem T, Jones S, Huaraca Quispe LP, Baggs E, Morley N, Richards M, Smith P, Meir P. 2014. Methane and nitrous oxide fluxes across an elevation gradient in the tropical Peruvian Andes. Biogeosciences 11:2325–39.CrossRefGoogle Scholar
  84. Tian D, Niu S. 2015. A global analysis of soil acidification caused by nitrogen addition. Environ Res Lett 10:024019.CrossRefGoogle Scholar
  85. Townsend AR, Asner GP, Cleveland CC. 2008. The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 23:424–31.CrossRefGoogle Scholar
  86. van der Meer PJ, Bongers F. 1996. Patterns of tree-fall and branch-fall in a tropical rain forest in French Guiana. J Ecol 84(1):19–29.CrossRefGoogle Scholar
  87. van Lent J, Hergoualc’h K, Verchot L. 2015. Reviews and syntheses: soil N2O and NO emissions from land use and land use change in the tropics and subtropics: a meta-analysis. Biogeosciences 12:7299–313.CrossRefGoogle Scholar
  88. Veldkamp E, Koehler B, Corre M. 2013. Indications of nitrogen-limited methane uptake in tropical forest soils. Biogeosciences 10:5367–79.CrossRefGoogle Scholar
  89. Von Fischer JC, Hedin LO. 2002. Separating methane production and consumption with a field-based isotope pool dilution technique. Glob Biogeochem Cycles 16(3):8-1–8-13. Scholar
  90. Von Fischer JC, Hedin LO. 2007. Controls on soil methane fluxes: tests of biophysical mechanisms using stable isotope tracers. Glob Biogeochem Cycles. Scholar
  91. Werner C, Zheng X, Tang J, Xie B, Liu C, Kiese R, Butterbach-Bahl K. 2006. N2O, CH4 and CO2 emissions from seasonal tropical rainforests and a rubber plantation in Southwest China. Plant Soil 289:335–53.CrossRefGoogle Scholar
  92. Weslien P, Kasimir Klemedtsson Å, Börjesson G, Klemedtsson L. 2009. Strong pH influence on N2O and CH4 fluxes from forested organic soils. Eur J Soil Sci 60:311–20.CrossRefGoogle Scholar
  93. Wolf K, Flessa H, Veldkamp E. 2012. Atmospheric methane uptake by tropical montane forest soils and the contribution of organic layers. Biogeochemistry 111:469–83.CrossRefGoogle Scholar
  94. Wood S, Wood MS. 2007. The mgcv package. www R-Proj Org.Google Scholar
  95. Yan J, Zhang W, Wang K, Qin F, Wang W, Dai H, Li P. 2014. Responses of CO2, N2O and CH4 fluxes between atmosphere and forest soil to changes in multiple environmental conditions. Glob Change Biol 20(1):300–12.CrossRefGoogle Scholar
  96. Yang H, Detto M, Liu S, Yuan W, Hsieh C-I, Wang X, Chen R, Chen H, Peng C, Jiang X, Li Y, Xu H, Liu W, Yang Q. 2017. Effects of canopy gaps on N2O fluxes in a tropical montane rainforest in Hainan of China. Ecol Eng 105:325–34.CrossRefGoogle Scholar
  97. Zona D, Janssens IA, Aubinet M, Gioli B, Vicca S, Fichot R, Ceulemans R. 2013. Fluxes of the greenhouse gases (CO2, CH4 and N2O) above a short-rotation poplar plantation after conversion from agricultural land. Agric For Meteorol 169:100–10.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018
Corrected publication August/2018

Authors and Affiliations

  • Elodie A. Courtois
    • 1
    • 2
    Email author
  • Clément Stahl
    • 1
    • 3
  • Joke Van den Berge
    • 1
  • Laëtitia Bréchet
    • 1
    • 3
  • Leandro Van Langenhove
    • 1
    • 3
  • Andreas Richter
    • 4
    • 5
  • Ifigenia Urbina
    • 6
    • 7
  • Jennifer L. Soong
    • 1
  • Josep Peñuelas
    • 6
    • 7
  • Ivan A. Janssens
    • 1
  1. 1.Department of Biology, Centre of Excellence PLECO (Plant and Vegetation Ecology)University of AntwerpWilrijkBelgium
  2. 2.Laboratoire Ecologie, évolution, interactions des systèmes amazoniens (LEEISA)Université de Guyane, CNRS, IFREMERCayenneFrench Guiana
  3. 3.INRA, UMR Ecology of Guiana Forests (Ecofog), AgroParisTech, Cirad, CNRS, Université des AntillesUniversité de GuyaneKourouFrench Guiana
  4. 4.Department of Microbiology and Ecosystem ScienceUniversity of ViennaViennaAustria
  5. 5.International Institute of Applied Systems Analysis (IIASA)LaxenburgAustria
  6. 6.CSIC, Global Ecology Unit CREAF-CSIC-UABBellaterra, CataloniaSpain
  7. 7.CREAFCataloniaSpain

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