Changes in plant community traits and relationship to productivity during temperate forest restoration

Abstract

The restoration of severely fragmented forests requires urgent guidance from succession theory. New theories and methods in plant functional ecology offer novel perspectives on the mechanisms that drive forest succession and productivity. Here, we established a restoration gradient of seven forest logging periods in temperate forests in China, and conducted systematic surveys on the leaf functional traits of all observed plant species, plant community structure, and soil properties. Inspired by the new concept of two-dimensional plant community traits (i.e., efficiency and quantity traits) and plant trait networks (PTNs), we explored the adaptation mechanisms of forest communities along a restoration succession and their relationship to productivity. Efficiency and quantity traits initially increased and then stabilized, whereas multi-trait relationships (MR) exhibited fluctuations, with community resource utilization efficiency increasing initially before stabilization. As expected, productivity is poorly explained by either efficiency or quantity traits alone but is substantially better explained by their joint consideration as two-dimensional community traits. Among these, the efficiency and quantity traits of leaf area and leaf dry weight can explain up to 43% of productivity. Furthermore, MR exhibit a time-lag effect on productivity. A structural equation model (SEM) with time-lag analysis showed that efficiency traits, quantity traits, MR, and soil properties explained 64% of the spatial variation in productivity during forest succession. Efficiency and quantity traits directly regulated productivity, whereas soil properties and MR indirectly regulated productivity. Our findings are the first to demonstrate the regulation mechanisms between forest succession and productivity from the framework of efficiency traits–quantity traits-MR, providing theoretical guidance and a reference for ecological restoration, and predicting the spatial variation of forest productivity, especially at small scale.

Keywords

Forest / Succession / Productivity / Traits / Plant trait network

References

[1] An H, Yang XG, Liu BR, Li XB, He XZ, Song NP. Changes of plant community biomass and soil nutrients during the vegetation succession on abandoned cultivated land in desert steppe region. J Appl Ecol, 2011, 22(12): 3145-3149

[2] Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK. The contribution of species richness and composition to bacterial services. Nature, 2005, 436(7054): 1157-1160

[3] Bloom AJ, Chapin FS, Mooney HA. Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst, 1985, 16: 363-392

[4] Cardinale BJ, Ives AR, Inchausti P. Effects of species diversity on the primary productivity of ecosystems: extending our spatial and temporal scales of inference. Oikos, 2004, 104(3): 437-450

[5] Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. Towards a worldwide wood economics spectrum. Ecol Lett, 2009, 12(4): 351-366

[6] Chen SP, Wang WT, Xu WT, Wang Y, Wan HW, Chen DM, Tang ZY, Tang XL, Zhou GY, Xie ZQ, Zhou DW, Shangguan Z, Huang JH, He JS, Wang YF, Sheng JD, Tang LS, Li XR, Dong M, Wu Y, Wang QF, Wang ZH, Wu JG, Chapin FSIII, Bai YF. Plant diversity enhances productivity and soil carbon storage. Proc Natl Acad Sci U S A, 2018, 115(16): 4027-4032

[7] Cortez J, Garnier E, Pérez-Harguindeguy N, Debussche M, Gillon D. Plant traits, litter quality and decomposition in a Mediterranean old-field succession. Plant Soil, 2007, 296(1): 19-34

[8] Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Colin Prentice I, Garnier E, Bönisch G, Westoby M, Poorter H, Reich PB, Moles AT, Dickie J, Gillison AN, Zanne AE, Chave J, Joseph Wright S, Sheremet’ev SN, Jactel H, Baraloto C, Cerabolini B, Pierce S, Shipley B, Kirkup D, Casanoves F, Joswig JS, Günther A, Falczuk V, Rüger N, Mahecha MD, Gorné LD (2016) The global spectrum of plant form and function. Nature 529(7585):167–171. https://doi.org/10.1038/nature16489

[9] Ehrlich PR. Conservation in temperate forests: what do we need to know and do?. For Ecol Manag, 1996, 85(1–3): 9-19

[10] Franks PJ, Beerling DJ. CO₂-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology, 2009, 7(2): 227-236

[11] Garnier E, Cortez J, Billès G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint JP. Plant functional markers capture ecosystem properties during secondary succession. Ecology, 2004, 85(9): 2630-2637

[12] He NP, Li Y, Liu CC, Xu L, Li MX, Zhang JH, He JS, Tang ZY, Han XG, Ye Q, Xiao CW, Yu Q, Liu SR, Sun W, Niu SL, Li SG, Sack L, Yu GR. Plant trait networks: improved resolution of the dimensionality of adaptation. Trends Ecol Evol, 2020, 35(10): 908-918

[13] He NP, Liu CC, Piao SL, Sack L, Xu L, Luo YQ, He JS, Han XG, Zhou GS, Zhou XH, Lin Y, Yu Q, Liu SR, Sun W, Niu SL, Li SG, Zhang JH, Yu GR. Ecosystem traits linking functional traits to macroecology. Trends Ecol Evol, 2019, 34(3): 200-210

[14] He NP, Yan P, Liu CC, Xu L, Li MX, Van Meerbeek K, Zhou GS, Zhou GY, Liu SR, Zhou XH, Li SG, Niu SL, Han XG, Buckley TN, Sack L, Yu GR. Predicting ecosystem productivity based on plant community traits. Trends Plant Sci, 2023, 28(1): 43-53

[15] Isbell F, Cowles J, Dee LE, Loreau M, Reich PB, Gonzalez A, Hector A, Schmid B. Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecol Lett, 2018, 21(6): 763-778

[16] Kazakou E, Garnier E, Navas ML, Roumet C, Collin C, Laurent G. Components of nutrient residence time and the leaf economics spectrum in species from Mediterranean old-fields differing in successional status. Funct Ecol, 2007, 21(2): 235-245

[17] Li L, Luke McCormack M, Ma CG, Kong DL, Zhang Q, Chen XY, Zeng H, Niinemets Ü, Guo DL. Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett, 2015, 18(9): 899-906

[18] Li Y, Li Q, Xu L, Li MX, Chen Z, Song ZP, Hou JH, He NP. Plant community traits can explain variation in productivity of selective logging forests after different restoration times. Ecol Indic, 2021, 131 108181

[19] Li Y, Liu CC, Sack L, Xu L, Li MX, Zhang JH, He NP. Leaf trait network architecture shifts with species-richness and climate across forests at continental scale. Ecol Lett, 2022, 25(6): 1442-1457

[20] Li Y, Liu CC, Zhang JH, Yang H, Xu L, Wang QF, Sack L, Wu XQ, Hou JH, He NP. Variation in leaf chlorophyll concentration from tropical to cold-temperate forests: association with gross primary productivity. Ecol Indic, 2018, 85: 383-389

[21] Liu CC, He NP, Zhang JH, Li Y, Wang QF, Sack L, Yu GR. Variation of stomatal traits from cold temperate to tropical forests and association with water use efficiency. Funct Ecol, 2018, 32(1): 20-28

[22] Liu CC, Li Y, Yan P, He NP. How to improve the predictions of plant functional traits on ecosystem functioning?. Front Plant Sci, 2021, 12 622260

[23] Loreau M, Hector A. Not even wrong: comment by loreau and hector. Ecology, 2019, 100(10 e02794

[24] Mensens C, De Laender F, Janssen CR, Sabbe K, De Troch M. Different response-effect trait relationships underlie contrasting responses to two chemical stressors. J Ecol, 2017, 105(6): 1598-1609

[25] Milla R, Reich PB. The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proc Biol Sci, 2007, 274(1622): 2109-2114

[26] Noble IR, Dirzo R. Forests as human-dominated ecosystems. Science, 1997, 277(5325): 522-525

[27] Odum EP. The strategy of ecosystem development. Science, 1969, 164(3877): 262-270

[28] Paquette A, Messier C. The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob Ecol Biogeogr, 2011, 20(1): 170-180

[29] Reich PB. The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol, 2014, 102(2): 275-301

[30] Sack L, Cowan PD, Jaikumar N, Holbrook NM. The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ, 2003, 26(8): 1343-1356

[31] Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E. The influence of functional diversity and composition on ecosystem processes. Science, 1997, 277(5330): 1300-1302

[32] Vile D, Shipley B, Garnier E. A structural equation model to integrate changes in functional strategies during old-field succession. Ecology, 2006, 87(2): 504-517

[33] Wang B, Huang JY, Yang XS, Zhang B, Liu MC. Estimation of biomass, net primary production and net ecosystem production of China’s forests based on the 1999–2003 National Forest Inventory. Scand J for Res, 2010, 25(6): 544-553

[34] Wang RM, He NP, Li SG, Xu L, Li MX. Variation and adaptation of leaf water content among species, communities, and biomes. Environ Res Lett, 2021, 16(12 124038

[35] Wang RL, Yu GR, He NP, Wang QF, Zhao N, Xu ZW, Ge JP. Latitudinal variation of leaf stomatal traits from species to community level in forests: linkage with ecosystem productivity. Sci Rep, 2015, 5: 14454

[36] Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee TL, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R. The worldwide leaf economics spectrum. Nature, 2004, 428(6985): 821-827

[37] Wright JP, Sutton-Grier A. Does the leaf economic spectrum hold within local species pools across varying environmental conditions?. Funct Ecol, 2012, 26(61390-1398

[38] Wu X, Wang XP, Tang ZY, Shen ZH, Zheng CY, Xia XL, Fang JY. The relationship between species richness and biomass changes from boreal to subtropical forests in China. Ecography, 2015, 38(6): 602-613

[39] Yan P, He NP, Yu KL, Xu L, Van Meerbeek K. Integrating multiple plant functional traits to predict ecosystem productivity. Commun Biol, 2023, 6(1): 239

[40] Yan P, Li MX, Yu GR, Qi Y, He NP. Plant community traits associated with nitrogen can predict spatial variability in productivity. Ecol Indic, 2022, 140 109001

[41] Zhang JH, Ren TT, Yang JJ, Xu L, Li MX, Zhang YH, Han XG, He NP. Leaf multi-element network reveals the change of species dominance under nitrogen deposition. Front Plant Sci, 2021, 12 580340

[42] Zhang JH, Zhao N, Liu CC, Yang H, Li ML, Yu GR, Wilcox K, Yu Q, He NP. C: N: P stoichiometry in China’s forests: from organs to ecosystems. Funct Ecol, 2018, 32(150-60

[43] Zhang Y, He NP, Li MX, Yan P, Yu GR. Community chlorophyll quantity determines the spatial variation of grassland productivity. Sci Total Environ, 2021, 801 149567

[44] Zhou G, Yin G, Tang X, Wen D, Liu C, Kuang Y, Wang W. Forest ecosystem carbon stocks in China: Biomass equation, 2018, Beijing, Science Press(in Chinese)

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Northeast Forestry University