Disaggregation of canopy photosynthesis among tree species in a mixed broadleaf forest

. 2024 Jul 02 ; 44 (7) : .

Jazyk angličtina Země Kanada Médium print

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Perzistentní odkaz   https://www.medvik.cz/link/pmid38864558

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Carbon dioxide sequestration from the atmosphere is commonly assessed using the eddy covariance method. Its net flux signal can be decomposed into gross primary production and ecosystem respiration components, but these have seldom been tested against independent methods. In addition, eddy covariance lacks the ability to partition carbon sequestration among individual trees or species within mixed forests. Therefore, we compared gross primary production from eddy covariance versus an independent method based on sap flow and water-use efficiency, as measured by the tissue heat balance method and δ13C of phloem contents, respectively. The latter measurements were conducted on individual trees throughout a growing season in a mixed broadleaf forest dominated by three tree species, namely English oak, narrow-leaved ash and common hornbeam (Quercus robur L., Fraxinus angustifolia Vahl, and Carpinus betulus L., respectively). In this context, we applied an alternative ecophysiological method aimed at verifying the accuracy of a state-of-the-art eddy covariance system while also offering a solution to the partitioning problem. We observed strong agreement in the ecosystem gross primary production estimates (R2 = 0.56; P < 0.0001), with correlation being especially high and nearly on the 1:1 line in the period before the end of July (R2 = 0.85; P < 0.0001). After this period, the estimates of gross primary production began to diverge. Possible reasons for the divergence are discussed, focusing especially on phenology and the limitation of the isotopic data. English oak showed the highest per-tree daily photosynthetic rates among tree species, but the smaller, more abundant common hornbeam contributed most to the stand-level summation, especially early in the spring. These findings provide a rigorous test of the methods and the species-level photosynthesis offers avenues for enhancing forest management aimed at carbon sequestration.

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Acosta  M, Darenova  E, Dušek  J, Pavelka  M. 2017. Soil carbon dioxide fluxes in a mixed floodplain forest in the Czech Republic. Eur J Soil Biol  82:35–42. 10.1016/j.ejsobi.2017.08.006. DOI

Ameray  A, Bergeron  Y, Valeria  O, Montoro Girona  M, Cavard  X. 2021. Forest carbon management: a review of silvicultural practices and management strategies across boreal, temperate and tropical forests. Curr For Rep. 7(4):245–266. 10.1007/s40725-021-00151-w. DOI

Aubinet  M, Vesala  T, Papale  D. (eds), 2012. Eddy covariance: a practical guide to measurement and data analysis. Springer, Dordrecht.

Augspurger  CK, Cheeseman  JM, Salk  CF. 2005. Light gains and physiological capacity of understorey woody plants during phenological avoidance of canopy shade. Funct Ecol. 19(4):537–546. 10.1111/j.1365-2435.2005.01027.x. DOI

Baldocchi  D. 2008. ‘Breathing’ of the terrestrial biosphere: lessons learned from a global network of carbon dioxide flux measurement systems. Aust J Bot. 56(1):1–26. 10.1071/BT07151. DOI

Baldocchi  DD. 2003. Assessing the eddy covariance technique for evaluating carbon dioxide exchange rates of ecosystems: past, present and future: carbon balance and eddy covariance. Glob Chang Biol. 9(4):479–492. 10.1046/j.1365-2486.2003.00629.x. DOI

Bassow  SL, Bazzaz  FA. 1997. Intra- and inter-specific variation in canopy photosynthesis in a mixed deciduous forest. Oecologia. 109(4):507–515. 10.1007/s004420050111. PubMed DOI

Bögelein  R, Lehmann  MM, Thomas  FM. 2019. Differences in carbon isotope leaf-to-phloem fractionation and mixing patterns along a vertical gradient in mature European beech and Douglas fir. New Phytol. 222(4):1803–1815. 10.1111/nph.15735. PubMed DOI

Campioli  M, Malhi  Y, Vicca  S, Luyssaert  S, Papale  D, Peñuelas  J, Reichstein  M, Migliavacca  M, Arain  MA, Janssens  IA. 2016. Evaluating the convergence between eddy-covariance and biometric methods for assessing carbon budgets of forests. Nat Commun. 7(1):13717. 10.1038/ncomms13717. PubMed DOI PMC

Campioli  M, Vicca  S, Luyssaert  S, Bilcke  J, Ceschia  E, Chapin Iii  FS, Ciais  P, Fernández-Martínez  M, Malhi  Y, Obersteiner  M, et al.  2015. Biomass production efficiency controlled by management in temperate and boreal ecosystems. Nat Geosci. 8(11):843–846. 10.1038/ngeo2553. DOI

Čermák  J, Deml  M, Penka  M. 1973. A new method of sap flow rate determination in trees. Biol Plant. 15(3):171–178. 10.1007/BF02922390. DOI

Čermák  J, Kučera  J, Nadezhdina  N. 2004. Sap flow measurements with some thermodynamic methods, flow integration within trees and scaling up from sample trees to entire forest stands. Trees. 18(5):529–546. 10.1007/s00468-004-0339-6. DOI

Cernusak  LA, Ubierna  N, Winter  K, Holtum  JAM, Marshall  JD, Farquhar  GD. 2013. Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytol. 200(4):950–965. 10.1111/nph.12423. PubMed DOI

Delpierre  N, Berveiller  D, Granda  E, Dufrêne  E. 2016. Wood phenology, not carbon input, controls the interannual variability of wood growth in a temperate oak forest. New Phytol. 210(2):459–470. 10.1111/nph.13771. PubMed DOI

Etzold  S, Buchmann  N, Eugster  W. 2010. Contribution of advection to the carbon budget measured by eddy covariance at a steep mountain slope forest in Switzerland. Biogeosciences. 7(8):2461–2475. 10.5194/bg-7-2461-2010. DOI

Farquhar  GD, O’Leary  MH, Berry  JA. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct Plant Biol. 9(2):121–137. 10.1071/PP9820121. DOI

Flo  V, Martinez-Vilalta  J, Steppe  K, Schuldt  B, Poyatos  R. 2019. A synthesis of bias and uncertainty in sap flow methods. Agric For Meteorol  271:362–374. 10.1016/j.agrformet.2019.03.012. DOI

Foken  T, Göockede  M, Mauder  M, Mahrt  L, Amiro  B, Munger  W. 2005. Post-field data quality control. In: Lee  X, Massman  W, Law  B (eds) Handbook of micrometeorology. Kluwer Academic Publishers, Dordrecht, pp 181–208  10.1007/1-4020-2265-4_9 [accessed 2023 May 23]. DOI

Fratini  G, Mauder  M. 2014. Towards a consistent eddy-covariance processing: an intercomparison of EddyPro and TK3. Atmos Meas Tech. 7(7):2273–2281. 10.5194/amt-7-2273-2014. DOI

Gessler  A, Rennenberg  H, Keitel  C. 2004. Stable isotope composition of organic compounds transported in the phloem of European beech--evaluation of different methods of phloem sap collection and assessment of gradients in carbon isotope composition during leaf-to-stem transport. Plant Biol (Stuttg). 6(6):721–729. 10.1055/s-2004-830350. PubMed DOI

Gimeno  TE, Campany  CE, Drake  JE, Barton  CVM, Tjoelker  MG, Ubierna  N, Marshall  JD. 2021. Whole-tree mesophyll conductance reconciles isotopic and gas-exchange estimates of water-use efficiency. New Phytol. 229(5):2535–2547. 10.1111/nph.17088. PubMed DOI

Granier  A. 1985. Une nouvelle méthode pour la mesure du flux de sève brute dans le tronc des arbres. Ann For Sci. 42(2):193–200. 10.1051/forest:19850204. DOI

Hu  J, Moore  DJP, Riveros-Iregui  DA, Burns  SP, Monson  RK. 2010. Modeling whole-tree carbon assimilation rate using observed transpiration rates and needle sugar carbon isotope ratios. New Phytol. 185(4):1000–1015. 10.1111/j.1469-8137.2009.03154.x. PubMed DOI

Ibrom  A, Dellwik  E, Flyvbjerg  H, Jensen  NO, Pilegaard  K. 2007. Strong low-pass filtering effects on water vapour flux measurements with closed-path eddy correlation systems. Agric For Meteorol. 147(3–4):140–156. 10.1016/j.agrformet.2007.07.007. DOI

Jarosz  N, Brunet  Y, Lamaud  E, Irvine  M, Bonnefond  J-M, Loustau  D. 2008. Carbon dioxide and energy flux partitioning between the understorey and the overstorey of a maritime pine forest during a year with reduced soil water availability. Agric For Meteorol. 148(10):1508–1523. 10.1016/j.agrformet.2008.05.001. DOI

Jocher  G, Ottosson Löfvenius  M, De Simon  G, et al.  2017. Apparent winter CO2 uptake by a boreal forest due to decoupling. Agric For Meteorol  232:23–34. 10.1016/j.agrformet.2016.08.002. DOI

Jocher  G, Fischer  M, Šigut  L, Pavelka  M, Sedlák  P, Katul  G. 2020. Assessing decoupling of above and below canopy air masses at a Norway spruce stand in complex terrain. Agric For Meteorol  294:108149. 10.1016/j.agrformet.2020.108149. DOI

Jones  HG. 2013. Plants and microclimate: a quantitative approach to environmental plant physiology, 3rd edn. Cambridge University Press, Cambridge.

Klein  T, Rotenberg  E, Cohen-Hilaleh  E, Raz-Yaseef  N, Tatarinov  F, Preisler  Y, Ogée  J, Cohen  S, Yakir  D. 2014. Quantifying transpirable soil water and its relations to tree water use dynamics in a water-limited pine forest. Ecohydrology. 7(2):409–419. 10.1002/eco.1360. DOI

Klein  T, Rotenberg  E, Tatarinov  F, Yakir  D. 2016. Association between sap flow-derived and eddy covariance-derived measurements of forest canopy CO2 uptake. New Phytol. 209(1):436–446. 10.1111/nph.13597. PubMed DOI

Kowalska  N, Šigut  L, Stojanović  M, Fischer  M, Kyselova  I, Pavelka  M. 2020. Analysis of floodplain forest sensitivity to drought. Philos Trans R Soc B Biol Sci. 375(1810):20190518. 10.1098/rstb.2019.0518. PubMed DOI PMC

Kowalska  N, Jocher  G, Šigut  L, Pavelka  M. 2022. Does below-above canopy air mass decoupling impact temperate floodplain forest CO2 exchange?  Atmos phere. 13(3):437. 10.3390/atmos13030437. DOI

Krejza  J, Haeni  M, Darenova  E, et al.  2022. Disentangling carbon uptake and allocation in the stems of a spruce forest. Environ Exp Bot  196:104787. 10.1016/j.envexpbot.2022.104787. DOI

Kučera  J, Čermák  J, Penka  M. 1977. Improved thermal method of continual recording the transpiration flow rate dynamics. Biol Plant. 19(6):413–420. 10.1007/BF02922976. DOI

Kučera  J, Vaníček  R, Urban  J. 2020. Automated exponential feedback weighting method for subtraction of heat losses from sap flow measured by the trunk heat balance method. Acta Hortic. (1300):81–88. 10.17660/ActaHortic.2020.1300.11. DOI

Lasslop  G, Reichstein  M, Papale  D, Richardson  AD, Arneth  A, Barr  A, Stoy  P, Wohlfahrt  G. 2010. Separation of net ecosystem exchange into assimilation and respiration using a light response curve approach: critical issues and global evaluation. Glob Chang Biol. 16(1):187–208. 10.1111/j.1365-2486.2009.02041.x. DOI

Lee  X, Massman  W, Law  B. 2005. Handbook of micrometeorology. Springer, Netherlands, Dordrecht, 10.1007/1-4020-2265-4 [accessed 2023 Jun 7, ]. DOI

Lundblad  M, Lagergren  F, Lindroth  A. 2001. Evaluation of heat balance and heat dissipation methods for sapflow measurements in pine and spruce. Ann For Sci. 58(6):625–638. 10.1051/forest:2001150. DOI

Luyssaert  S, Marie  G, Valade  A, Chen  Y-Y, Njakou Djomo  S, Ryder  J, Otto  J, Naudts  K, Lansø  AS, Ghattas  J, et al.  2018. Tradeoffs in using European forests to meet climate objectives. Nature. 562(7726):259–262. 10.1038/s41586-018-0577-1. PubMed DOI PMC

Marshall  JD, Tarvainen  L, Zhao  P, Lim  H, Wallin  G, Näsholm  T, Lundmark  T, Linder  S, Peichl  M. 2023. Components explain, but do eddy fluxes constrain? Carbon budget of a nitrogen-fertilized boreal scots pine forest. New Phytol. 239(6):2166–2179. 10.1111/nph.18939. PubMed DOI

Nezval  O, Krejza  J, Světlík  J, Šigut  L, Horáček  P. 2020. Comparison of traditional ground-based observations and digital remote sensing of phenological transitions in a floodplain forest. Agric For Meteorol  291:108079. 10.1016/j.agrformet.2020.108079. DOI

Offermann  C, Ferrio  JP, Holst  J, Grote  R, Siegwolf  R, Kayler  Z, Gessler  A. 2011. The long way down—are carbon and oxygen isotope signals in the tree ring uncoupled from canopy physiological processes?  Tree Physiol. 31(10):1088–1102. 10.1093/treephys/tpr093. PubMed DOI

Oulehle  F, Urban  O, Tahovská  K, Kolář  T, Rybníček  M, Büntgen  U, Hruška  J, Čáslavský  J, Trnka  M. 2023. Calcium availability affects the intrinsic water-use efficiency of temperate forest trees. Commun Earth Environ. 4(1):1–99.. 10.1038/s43247-023-00822-5. PubMed DOI

Pan  Y, Birdsey  RA, Fang  J, Houghton  R, Kauppi  PE, Kurz  WA, Phillips  OL, Shvidenko  A, Lewis  SL, Canadell  JG, et al.  2011. A large and persistent carbon sink in the world’s forests. Science. 333(6045):988–993. 10.1126/science.1201609. PubMed DOI

Paul-Limoges  E, Wolf  S, Eugster  W, Hörtnagl  L, Buchmann  N. 2017. Below-canopy contributions to ecosystem CO2 fluxes in a temperate mixed forest in Switzerland. Agric For Meteorol  247:582–596. 10.1016/j.agrformet.2017.08.011. DOI

Peters  RL, Fonti  P, Frank  DC, Poyatos  R, Pappas  C, Kahmen  A, Carraro  V, Prendin  AL, Schneider  L, Baltzer  JL, et al.  2018. Quantification of uncertainties in conifer sap flow measured with the thermal dissipation method. New Phytol. 219(4):1283–1299. 10.1111/nph.15241. PubMed DOI

Poyatos  R, Granda  V, Flo  V, Adams  MA, Adorján  B, Aguadé  D, Aidar  MPM, Allen  S, Alvarado-Barrientos  MS, Anderson-Teixeira  KJ, et al.  2021. Global transpiration data from sap flow measurements: the SAPFLUXNET database. Earth Syst Sci Data. 13(6):2607–2649. 10.5194/essd-13-2607-2021. DOI

Puchi  PF, Khomik  M, Frigo  D, Arain  MA, Fonti  P, von  Arx  G, Castagneri  D. 2023. Revealing how intra- and inter-annual variability of carbon uptake (GPP) affects wood cell biomass in an eastern white pine forest. Environ Res Lett. 18(2):024027. 10.1088/1748-9326/acb2df. DOI

Reichstein  M, Falge  E, Baldocchi  D, Papale  D, Aubinet  M, Berbigier  P, Bernhofer  C, Buchmann  N, Gilmanov  T, Granier  A, et al.  2005. On the separation of net ecosystem exchange into assimilation and ecosystem respiration: review and improved algorithm. Glob Chang Biol. 11(9):1424–1439. 10.1111/j.1365-2486.2005.001002.x. DOI

Ryan  MG. 2023. The enduring mystery of differences between eddy covariance and biometric measurements for ecosystem respiration and net carbon storage in forests. New Phytol. 239(6):2060–2063. 10.1111/nph.19105. PubMed DOI

Sakuratani  T. 1981. A heat balance method for measuring water flux in the stem of intact plants. J Agric Meteorol. 37(1):9–17. 10.2480/agrmet.37.9. DOI

Schiestl-Aalto  P, Stangl  ZR, Tarvainen  L, Wallin  G, Marshall  J, Mäkelä  A. 2021. Linking canopy-scale mesophyll conductance and phloem sugar δ13C using empirical and modelling approaches. New Phytol. 229(6):3141–3155. 10.1111/nph.17094. PubMed DOI PMC

Schulze  E-D, Čermák  J, Matyssek  M, Penka  M, Zimmermann  R, Vasícek  F, Gries  W, Kučera  J. 1985. Canopy transpiration and water fluxes in the xylem of the trunk of Larix and Picea trees — a comparison of xylem flow, porometer and cuvette measurements. Oecologia. 66(4):475–483. 10.1007/BF00379337. PubMed DOI

Stangl  ZR, Tarvainen  L, Wallin  G, Marshall  JD. 2022. Limits to photosynthesis: seasonal shifts in supply and demand for CO2 in scots pine. New Phytol. 233(3):1108–1120. 10.1111/nph.17856. PubMed DOI

Steppe  K, De Pauw  DJW, Doody  TM, Teskey  RO. 2010. A comparison of sap flux density using thermal dissipation, heat pulse velocity and heat field deformation methods. Agric For Meteorol. 150(7–8):1046–1056. 10.1016/j.agrformet.2010.04.004. DOI

Szatniewska  J, Zavadilova  I, Nezval  O, Krejza  J, Petrik  P, Čater  M, Stojanović  M. 2022. Species-specific growth and transpiration response to changing environmental conditions in floodplain forest. For Ecol Manage  516:120248. 10.1016/j.foreco.2022.120248. DOI

Tatarinov  FA, Kučera  J, Cienciala  E. 2005. The analysis of physical background of tree sap flow measurement based on thermal methods. Meas Sci Technol. 16(5):1157–1169. 10.1088/0957-0233/16/5/016. DOI

Thomas  CK, Martin  JG, Law  BE, Davis  K. 2013. Toward biologically meaningful net carbon exchange estimates for tall, dense canopies: multi-level eddy covariance observations and canopy coupling regimes in a mature Douglas-fir forest in Oregon. Agric For Meteorol  173:14–27. 10.1016/j.agrformet.2013.01.001. DOI

Thompson  RL, Manning  AC, Gloor  E, Schultz  U, Seifert  T, Hänsel  F, Jordan  A, Heimann  M. 2009. In-situ measurements of oxygen, carbon monoxide and greenhouse gases from Ochsenkopf tall tower in Germany. Atmos Meas Tech. 2(2):573–591. 10.5194/amt-2-573-2009. DOI

Tian  X, Minunno  F, Schiestl-Aalto  P, et al.  2021. Disaggregating the effects of nitrogen addition on gross primary production in a boreal scots pine forest. Agric For Meteorol  301-302:108337. 10.1016/j.agrformet.2021.108337. DOI

Ubierna  N, Marshall  JD. 2011. Estimation of canopy average mesophyll conductance using δ13C of phloem contents. Plant Cell Environ. 34(9):1521–1535. 10.1111/j.1365-3040.2011.02350.x. PubMed DOI

Urban  J, Krofta  K, Kučera  J. 2012. Calibration of stem heat balance sensors upon a study of water balance of the hop plantation. Acta Hortic. (951):79–86. 10.17660/ActaHortic.2012.951.8. DOI

Vernay  A, Tian  X, Chi  J, Linder  S, Mäkelä  A, Oren  R, Peichl  M, Stangl  ZR, Tor-Ngern  P, Marshall  JD. 2020. Estimating canopy gross primary production by combining phloem stable isotopes with canopy and mesophyll conductances. Plant Cell Environ. 43(9):2124–2142. 10.1111/pce.13835. PubMed DOI

Vernay  A, Hasselquist  N, Leppä  K, Klosterhalfen  A, Gutierrez Lopez  J, Stangl  ZR, Chi  J, Kozii  N, Marshall  JD. 2024. Partitioning gross primary production of a boreal forest among species and strata: a multi-method approach. Agric For Meteorol  345:109857. 10.1016/j.agrformet.2023.109857. DOI

Wehr  R, Munger  JW, McManus  JB, Nelson  DD, Zahniser  MS, Davidson  EA, Wofsy  SC, Saleska  SR. 2016. Seasonality of temperate forest photosynthesis and daytime respiration. Nature. 534(7609):680–683. 10.1038/nature17966. PubMed DOI

Wilczak  JM, Oncley  SP, Stage  SA. 2001. Sonic anemometer tilt correction algorithms. Bound Layer Meteorol. 99(1):127–150. 10.1023/A:1018966204465. DOI

Wohlfahrt  G, Galvagno  M. 2017. Revisiting the choice of the driving temperature for eddy covariance CO2 flux partitioning. Agric For Meteorol  237-238:135–142. 10.1016/j.agrformet.2017.02.012. PubMed DOI PMC

Wutzler  T, Lucas-Moffat  A, Migliavacca  M, Knauer  J, Sickel  K, Šigut  L, Menzer  O, Reichstein  M. 2018. Basic and extensible post-processing of eddy covariance flux data with REddyProc. Biogeosciences. 15(16):5015–5030. 10.5194/bg-15-5015-2018. DOI

Yi  R, Xu  X. 2023. Species with larger vessel area have higher bias for the original Granier equation in calculating sap flux density. J Hydrol  622(B):129762. 10.1016/j.jhydrol.2023.129762. DOI

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