Abstract
Within limited growth age in some regions, forest production, including gross primary production (GPP) and net primary production (NPP), was linearly correlated with leaf area index (LAI). However, over wide range of growth age in the global scale, LAI patterns of forest production are unclear. Here, we compiled a subset from the Global Soil Respiration Database (SRDB) for global temperate forest ecosystems. The subset database mainly included forest production, soil respiration, and LAI data in 493 study sites over wide range of forest growth age (0–500 years). The results showed that LAI initially increased rapidly, reached a peak at juvenility, decreased slowly until maturity, and again increased possibly with further forest aging (R2 = 0.21, P < 0.001). We found that the dynamics of both GPP and NPP across global temperate forest ecosystems were driven by LAI. GPP initially increased and subsequently stabilized with increasing LAI. NPP peaked at LAI of about 5.6 m2 m−2, and subsequently decreased. The decrease in NPP resulted from the asymptotic increase in GPP and the continuing decrease in the NPP/GPP ratio with increasing LAI. The decline in the NPP/GPP ratio resulted from the significant increase in autotrophic respiration (Ra), and especially after canopy closure, Ra increased more quickly with increasing LAI than GPP. These results will improve our understanding of the control of LAI on ecosystem production.
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References
Allen HL, Dougherty PM, Campbell RG (1990) Manipulation of water and nutrients — practice and opportunity in southern U.S. pine forests. For Ecol Manag 30:437–453
Allen RB, Clinton PW, Davis MR (1997) Cation storage and availability along a Nothofagus forest development sequence in New Zealand. Can J For Res 27:323–330
Asner GP, Scurlock JMO, Hicke JA (2003) Global synthesis of leaf area index observations: implications for ecological and remote sensing studies. Glob Ecol Biogeogr 12:191–205
Bolstad PV, Vose JM, McNulty SG (2000) Forest productivity, leaf area, and terrain in southern appalachian deciduous forests. For Sci 47:419–427
Bondeau A, Kicklighter DW, Kaduk J, Intercomparison T, Participants, OF., ThE., Potsdam, NpP., Model (1999) Comparing global models of terrestrial net primary productivity (NPP): importance of vegetation structure on seasonal NPP estimates. Glob Chang Biol 5:35–45
Bond-Lamberty BP, Thomson AM (2018) A global database of soil respiration data, Version 4.0, in, ORNL Distributed Active Archive Center
Boone RD, Nadelhoffer KJ, Canary JD, Kaye JP (1998) Roots exert a strong influence on the temperature sensitivity of soil respiration. Nature 396:570–572
Clinton PW, Allen RB, Davis MR (2002) Nitrogen storage and availability during stand development in a New Zealand Nothofagus forest. Can J For Res 32:344–352
Cook RD (1977) Detection of influential observation in linear regression. Technometrics 19:15–18
Cook RD, Weisberg S (1982) Residuals and influence in regression. Chapman & Hall, New York
da Silva DA, Pfeifer M, Pattison Z, Vibrans AC (2020) Drivers of leaf area index variation in Brazilian Subtropical Atlantic Forests. For Ecol Manag 476:118477
de Almeida CL, de Carvalho TRA, de Araújo JC (2019) Leaf area index of Caatinga biome and its relationship with hydrological and spectral variables. Agric For Meteorol 279:107705
Drake JE, Davis SC, Raetz LM, DeLucia EH (2011) Mechanisms of age-related changes in forest production: the influence of physiological and successional changes. Glob Chang Biol 17:1522–1535
Fotis AT, Morin TH, Fahey RT, Hardiman BS, Bohrer G, Curtis PS (2018) Forest structure in space and time: biotic and abiotic determinants of canopy complexity and their effects on net primary productivity. Agric For Meteorol 250-251:181–191
Galmés J, Flexas J, Savé R, Medrano H (2007) Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. Plant Soil 290:139–155
Gholz HL (1982) Environmental limits on aboveground net primary production, leaf area, and biomass in vegetation zones of the Pacific northwest. Ecology 63:469–481
Giuliani R, Koteyeva N, Voznesenskaya E, Evans MA, Cousins AB, Edwards GE (2013) Coordination of leaf photosynthesis, transpiration, and structural traits in rice and wild relatives (genus Oryza). Plant Physiol 162:1632–1651
Goulden ML, McMillan AMS, Winston GC, Rocha AV, Manies KL, Harden JW, Bond-Lamberty BP (2011) Patterns of NPP, GPP, respiration, and NEP during boreal forest succession. Glob Chang Biol 17:855–871
Gower ST, Vogt KA, Grier CC (1992) Carbon dynamics of rocky mountain douglas-fir: influence of water and nutrient availability. Ecol Monogr 62:43–65
Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: potential causes. Trends Ecol Evol 11:378–382
Han T, Ren H, Wang J, Lu H, Song G, Chazdon RL (2020) Variations of leaf eco-physiological traits in relation to environmental factors during forest succession. Ecol Indic 117:106511
He L, Chen JM, Pan Y, Birdsey R, Kattge J (2012) Relationships between net primary productivity and forest stand age in U.S. forests. Glob. Biogeochem Cycles 26:GB3009
Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792
Holdaway RJ, Allen RB, Clinton PW, Davis MR, Coomes DA (2008) Intraspecific changes in forest canopy allometries during self-thinning. Funct Ecol 22:460–469
Jenkins JC, Chojnacky DC, Heath LS, Birdsey RA (2003) National-scale biomass estimators for United States tree species. For Sci 49:12–35
Joggi D, Hofer U, Nösberger J (1983) Leaf area index, canopy structure and photosynthesis of red clover (Trifolium pratense L.). Plant, Cell Environ 6:611–616
Jung M, Le Maire G, Zaehle S, Luyssaert S, Vetter M, Churkina G, Ciais P, Viovy N, Reichstein M (2007) Assessing the ability of three land ecosystem models to simulate gross carbon uptake of forests from boreal to Mediterranean climate in Europe. Biogeosciences 4:647–656
Kashian DM, Romme WH, Tinker DB, Turner MG, Ryan MG (2013) Postfire changes in forest carbon storage over a 300-year chronosequence of Pinus contorta-dominated forests. Ecol Monogr 83:49–66
Kassnacht KS, Gower ST (1997) Interrelationships among the edaphic and stand characteristics, leaf area index, and aboveground net primary production of upland forest ecosystems in north Central Wisconsin. Can J For Res 27:1058–1067
Kira T, Shidei T (1967) Primary production and turnover of organic matter in different forest ecosystems of the western pacific. Jpn J Ecol 17:70–87
Kitajima K, Mulkey SS, Wright SJ (2005) Variation in crown light utilization characteristics among tropical canopy trees. Ann Bot 95:535–547
Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334
Kulmala L, Pumpanen J, Kolari P, Dengel S, Berninger F, Köster K, Matkala L, Vanhatalo A, Vesala T, Bäck J (2019) Inter- and intra-annual dynamics of photosynthesis differ between forest floor vegetation and tree canopy in a subarctic Scots pine stand. Agric For Meteorol 271:1–11
Kushida K, Isaev AP, Maximov TC, Takao G, Fukuda M (2007) Remote sensing of upper canopy leaf area index and forest floor vegetation cover as indicators of net primary productivity in a Siberian larch forest. Journal of Geophysical Research: Biogeosciences 112:G02003
Lee H, Park J, Cho S, Lee M, Kim HS (2019) Impact of leaf area index from various sources on estimating gross primary production in temperate forests using the JULES land surface model. Agric For Meteorol 276-277:107614
Levenberg K (1944) A method for the solution of certain non-linear problems in least squares. Q Appl Math 2:164–168
Li L, Chen S, Yang C, Meng F, Sigrimis N (2020) Prediction of plant transpiration from environmental parameters and relative leaf area index using the random forest regression algorithm. J Clean Prod 261:121136
Lourakis M (2005) A brief description of the Levenberg-Marquardt algorithm implemened by levmar. Foundation of Research and Technology 4:1–6
Luyssaert S, Inglima I, Jung M, Richardson AD, Reichstein M, Papale D, Piao SL, Schulze E-D, Wingate L, Matteucci G, Aragao L, Aubinet M, Beer C, Bernhofer C, Black KG, Bonal D, Bonnefond J-M, Chambers J, Ciais P, Cook B, Davis KJ, Dolman AJ, Gielen B, Goulden M, Grace J, Granier A, Grelle A, Griffis T, Gr Nwald T, Guidolotti G, Hanson P, Harding R, Hollinger DY, Hutyra LR, Kolari P, Kruijt B, Kutsch W, Lagergren F, Laurila T, Law B, Le Maire G, Lindroth A, Loustau D, Malhi Y, Mateus J, Migliavacca M, Misson L, Montagnani L, Moncrieff J, Moors E, Munger JW, Nikinmaa E, Ollinger S, Pita G, Rebmann C, Roupsard O, Saigusa N, Sanz M, Seufert G, Sierra C, Smith M-L, Tang J, Valentini R, Vesala T, Janssens IA (2007) CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob Chang Biol 13:2509–2537
Luyssaert S, Schulze ED, Börner A, Knohl A, Hessenmöller D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455:213–215
Maass J, Vose JM, Swank WT, Martínez-Yrízar A (1995) Seasonal changes of leaf area index (LAI) in a tropical deciduous forest in west Mexico. For Ecol Manag 74:171–180
Marquardt DW (1963) An algorithm for least-squares estimation of nonlinear parameters. J Soc Ind Appl Math 11:431–441
Metcalfe DB, Meir P, Aragão LEOC, da Costa ACL, Braga AP, Gonçalves PHL, de Athaydes Silva Junior J, de Almeida SS, Dawson LA, Malhi Y, Williams M (2008) The effects of water availability on root growth and morphology in an Amazon rainforest. Plant Soil 311:189–199
Migliavacca M, Sonnentag O, Keenan TF, Cescatti A, O'Keefe J, Richardson AD (2012) On the uncertainty of phenological responses to climate change, and implications for a terrestrial biosphere model. Biogeosciences 9:2063–2083
Parker GG (2020) Tamm review: leaf area index (LAI) is both a determinant and a consequence of important processes in vegetation canopies. For Ecol Manag 477:118496
Pregitzer KS, Euskirchen ES (2004) Carbon cycling and storage in world forests: biome patterns related to forest age. Glob Chang Biol 10:2052–2077
Propastin P, Ibrom A, Knohl A, Erasmi S (2012) Effects of canopy photosynthesis saturation on the estimation of gross primary productivity from MODIS data in a tropical forest. Remote Sens Environ 121:252–260
Running SW, Coughlan JC (1988) A general model of forest ecosystem processes for regional applications I. Hydrologic balance, canopy gas exchange and primary production processes. Ecol Model 42:125–154
Ryan MG, Binkley D, Fownes JH (1997) Age-related decline in forest productivity: pattern and process. In: Begon M, Fitter AH (eds) . Academic Press, Adv Ecol Res, pp 213–262
Ryan MG, Binkley D, Fownes JH, Giardina CP, Senock RS (2004) An experimental test of the causes of forest growth decline with stand age. Ecol Monogr 74:393–414
Sellers PJ, Hall FG, Asrar G, Strebel DE, Murphy RE (1988) The first ISLSCP field experiment (FIFE). Bull Am Meteorol Soc 69:22–27
Sellers PJ, Hall FG, Kelly RD, Black A, Baldocchi D, Berry J, Ryan M, Ranson KJ, Crill PM, Lettenmaier DP, Margolis H, Cihlar J, Newcomer J, Fitzjarrald D, Jarvis PG, Gower ST, Halliwell D, Williams D, Goodison B, Wickland DE, Guertin FE (1997) BOREAS in 1997: experiment overview, scientific results, and future directions. Journal of Geophysical Research: Atmospheres 102:28731–28769
Tanaka K, Hashimoto S (2006) Plant canopy effects on soil thermal and hydrological properties and soil respiration. Ecol Model 196:32–44
Tang J, Luyssaert S, Richardson AD, Kutsch W, Janssens IA (2014) Steeper declines in forest photosynthesis than respiration explain age-driven decreases in forest growth. Proc Natl Acad Sci U S A 111:8856–8860
Tyrrell ML, Ross J, Kelty M (2012) Carbon dynamics in the temperate forest. In: Ashton MS, Tyrrell ML, Spalding D, Gentry B (eds) Managing forest carbon in a changing climate. Springer Netherlands, Dordrecht, pp 77–107
Wales SB, Kreider MR, Atkins J, Hulshof CM, Fahey RT, Nave LE, Nadelhoffer KJ, Gough CM (2020) Stand age, disturbance history and the temporal stability of forest production. For Ecol Manag 460:117865
Wang C, Yang J (2007) Rhizospheric and heterotrophic components of soil respiration in six Chinese temperate forests. Glob Chang Biol 13:123–131
Waring RH, Running SW (2007) CHAPTER 10 - advances in Eddy-flux analyses, remote sensing, and evidence of climate change. In: Waring RH, Running SW (eds) Forest ecosystems (Third Edition). Academic Press, San Diego, pp 317–344
Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325
Xu F, Guo W, Xu W, Wei Y, Wang R (2009) Leaf morphology correlates with water and light availability: what consequences for simple and compound leaves? Prog Nat Sci 19:1789–1798
Yang X, Mustard JF, Tang J, Xu H (2012) Regional-scale phenology modeling based on meteorological records and remote sensing observations Journal of Geophysical Research: Biogeosciences 117
Zha TS, Barr AG, Bernier PY, Lavigne MB, Trofymow JA, Amiro BD, Arain MA, Bhatti JS, Black TA, Margolis HA, McCaughey JH, Xing ZS, Van Rees KCJ, Coursolle C (2013) Gross and aboveground net primary production at Canadian forest carbon flux sites. Agric For Meteorol 174-175:54–64
Acknowledgments
This work was funded jointly by the National Natural Science Foundation of China (Nos. 41877037, 41425006, and 41101218), and the Western Light Project of Chinese Academy of Sciences (No. K318001103). The authors thank B. Bond-Lamberty for making available the comprehensive soil respiration database including plant primary production data.
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The National Natural Science Foundation of China (Nos. 41877037, 41425006, and 41101218), the Western Light Project of Chinese Academy of Sciences (No. K318001103).
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W.Z. analyzed the data. W.Z., W.F.T., and S.Q.L. contributed to the discussion of the results and wrote the paper.
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Zhao, W., Tan, W. & Li, S. High leaf area index inhibits net primary production in global temperate forest ecosystems. Environ Sci Pollut Res 28, 22602–22611 (2021). https://doi.org/10.1007/s11356-020-11928-0
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DOI: https://doi.org/10.1007/s11356-020-11928-0