Differential responses of photosynthetic parameters in saplings and adult trees to nitrogen and phosphorus addition in an evergreen broad-leaved forest

doi:10.17520/biods.2024435

Abstract

Abstract:

Aims:Assessing the impact of nitrogen-phosphorus imbalance inputs on the carbon sink capacity of subtropical forests is currently a hot topic. Maximum carboxylation rate (V_cmax) and maximum electron transport rate (J_max) are crucial parameters in the C₃ plant photosynthetic model (FvCB model), exploring the mechanisms underlying photosynthetic biochemical limitations in response to N and P deposition, which will help to improve the understanding of biodiversity conservation and management in the context of global change.

Methods:A six-year N and P addition experiment was conducted in an evergreen broad-leaved forest of Jiulianshan, Jiangxi Province. Six dominant tree species were selected to quantify V_cmax, J_max, leaf mass per area, leaf N and P content, and analyze correlations between photosynthetic parameters and leaf traits of saplings and adult trees under N and P addition.

Results:We found that addition of either N or P significantly altered photosynthetic parameters of saplings. Specifically, N addition significantly increased the J_max of saplings, while P addition significantly increased the V_cmax. However, combined N and P addition had no significant effects on V_cmax, J_max, and J_max/V_cmax, showing an antagonistic effect. In contrast, none of N and P treatments significantly affected V_cmax, J_max, and J_max/V_cmax in adult trees. During the transition from saplings to adult trees, V_cmax and J_max increased more than threefold. Furthermore, saplings exhibited species-specific responses to N and P addition. Schima superba and Castanopsis fargesii were more sensitive to N addition, Castanopsis carlesii was more sensitive to P addition, and Machilus breviflorawas more sensitive to combined N and P addition. Combined N and P addition significantly decreased the leaf mass per area (LMA) of saplings while increasing leaf nitrogen concent, whereas P addition significantly increased leaf nitrogen content in adult trees. However, leaf traits did not explain the variation in photosynthetic parameters.

Conclusions: These findings confirm the theoretical prediction that saplings were more responsive to nutrient inputs than adult trees, which may allocate more nutrient resources to reproduction and defense systems rather than altering photosynthetic biochemical limitations in response to N and P addition. The antagonistic effect of combined N and P addition on sapling photosynthetic parameters suggests that excessive nutrient supply led to nutrient allocation toward non-photosynthetic components, reducing the efficiency of the photosynthetic system. Clearly, N and P availability significantly alter the FvCB model parameters in an evergreen broad-leaved forest, with size-dependent and species-specific effects on photosynthetic biochemical limitations.

Key words: long-term nutrient additions, in-situ experiment, photosynthetic biochemical limitation, saplings, adult trees

Li Hongru, Yang Hua, Chen Fusheng, Sun Rongxi, Ye Xuemin. Differential responses of photosynthetic parameters in saplings and adult trees to nitrogen and phosphorus addition in an evergreen broad-leaved forest[J]. Biodiv Sci, 2025, 33(4): 24435.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2024435

https://www.biodiversity-science.net/EN/Y2025/V33/I4/24435

Figures/Tables 7

Table 1 Number of individuals of different species measured by photosynthetic gas exchange

物种 Species	合计 Total	CO₂响应曲线数量 Number of CO₂ response curves
物种 Species	合计 Total	对照 Control	氮添加 N addition (+N)	磷添加 P addition (+P)	氮磷同添 Combined N + P addition (N + P)
幼树 Saplings	115	34	25	22	34
木荷 Schima superba	22	7	6	3	6
绒毛润楠 Machilus velutina	18	5	5	3	5
短序润楠 Machilus breviflora	14	4	4	2	4
丝栗栲 Castanopsis fargesii	20	6	1	5	8
米槠 Castanopsis carlesii	25	7	6	5	7
甜槠 Castanopsis eyrei	16	5	3	4	4
成树 Adult trees	45	11	12	12	10
木荷 Schima superba	12	3	3	3	3
短序润楠 Machilus breviflora	11	3	3	3	2
丝栗栲 Castanopsis fargesii	12	3	3	3	3
米槠 Castanopsis carlesii	10	2	3	3	2
所有个体 All trees	160	45	37	34	44

Fig. 1 Response of physicochemical properties of surface soil (0-10 cm) and canopy direct radiation to N and P addition. +N, N addition; +P, P addition; N + P, Combined N + P addition. Lowercase letters indicate significant differences (P < 0.05) among the four treatments.

Fig. 2 Effects of N and P addition on maximum carboxylation rate (Vcmax), maximum electron transport rate (Jmax), and Jmax/Vcmax in saplings of six dominant tree species in an evergreen broad-leaved forest. The line within the boxplot depicts the median, while the upper and lower bounds of the box signify the 25th and 75th percentiles, respectively. The whiskers extend to 1.5 times the interquartile range, the range between the 25th and 75th percentiles, with points beyond them considered outliers. S, N and P represent the effects of species, nitrogen addition and phosphorus addition, respectively. * P < 0.05; ** P < 0.01; *** P < 0.001. +N, N addition; +P, P addition; N + P, Combined N + P addition. Lowercase letters indicate significant differences (P < 0.05) among the four treatments.

Fig. 3 Effects of N and P addition on maximum carboxylation rate (Vcmax), maximum electron transport rate (Jmax), and Jmax/Vcmax in adult trees of four dominant tree species in an evergreen broad-leaved forest. The line within the boxplot depicts the median, while the upper and lower bounds of the box signify the 25th and 75th percentiles, respectively. The whiskers extend to 1.5 times the interquartile range, the range between the 25th and 75th percentiles, with points beyond them considered outliers. +N, N addition; +P, P addition; N + P, Combined N + P addition.

Fig. 4 Correlation between maximum carboxylation rate (Vcmax) and maximum electron transport rate (Jmax) of saplings and adult trees in an evergreen broad-leaved forest.

Fig. 5 Effects of N and P addition on leaf mass per area (LMA), leaf N content (LNC), and leaf P content (LPC) of saplings and adult trees in an evergreen broad-leaved forest. The line within the boxplot depicts the median, while the upper and lower bounds of the box signify the 25th and 75th percentiles, respectively. The whiskers extend to 1.5 times the interquartile range, the range between the 25th and 75th percentiles, with points beyond them considered outliers. S, N and P represent the effects of species, nitrogen addition and phosphorus addition, respectively. * P < 0.05; ** P < 0.01; *** P < 0.001. +N, N addition; +P, P addition; N + P, Combined N + P addition. Lowercase letters indicate significant differences (P < 0.05) among the four treatments.

Table 2 Correlation between leaf traits and photosynthetic parameters of dominant tree species (both saplings and adult trees) in an evergreen broad-leaved forest treated with N and P addition. ns P > 0.05.

叶片性状 Leaf traits		最大羧化速率 Maximum carboxylation rate (V_cmax)	最大电子传递速率 Maximum electron transport rate (J_max)	J_max/V_cmax
比叶质量 Leaf mass per area (LMA)	P	0.157^ns	0.730^ns	0.827^ns
比叶质量 Leaf mass per area (LMA)	R²	0.09	-0.07	-0.08
叶片氮含量 Leaf N content (LNC)	P	0.248^ns	0.23^ns	0.167^ns
叶片氮含量 Leaf N content (LNC)	R²	0.047	0.09	0.08
叶片磷含量 Leaf P content (LPC)	P	0.94^ns	0.28^ns	0.45^ns
叶片磷含量 Leaf P content (LPC)	R²	-0.08	0.021	-0.03

References 56

[1]	Alvarez-Clare S, Mack MC, Brooks M (2013) A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. Ecology, 94, 1540-1551. PMID
[2]	Aoyagi R, Kitayama K, Turner BL (2022) How do tropical tree species maintain high growth rates on low-phosphorus soils? Plant and Soil, 480, 31-56.
[3]	Bartholomew DC, Bittencourt PR, da Costa AC, Banin LF, de Britto Costa P, Coughlin SI, Domingues TF, Ferreira LV, Giles A, Mencuccini M, Mercado L, Miatto RC, Oliveira A, Oliveira R, Meir P, Rowland L (2020) Small tropical forest trees have a greater capacity to adjust carbon metabolism to long-term drought than large canopy trees. Plant, Cell & Environment, 43, 2380-2393.
[4]	Bauer GA, Berntson GM, Bazzaz FA (2001) Regenerating temperate forests under elevated CO₂ and nitrogen deposition: Comparing biochemical and stomatal limitation of photosynthesis. New Phytologist, 152, 249-266.
[5]	Bown HE, Watt MS, Clinton PW, Mason EG, Richardson B (2007) Partititioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiata. Tree Physiology, 27, 335-344.
[6]	Bubier JL, Smith R, Juutinen S, Moore TR, Minocha R, Long S, Minocha S (2011) Effects of nutrient addition on leaf chemistry, morphology, and photosynthetic capacity of three bog shrubs. Oecologia, 167, 355-368. DOI PMID
[7]	Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Campanello PI, Villalobos-Vega R, Bustamante M, Miralles-Wilhelm F (2006) Nutrient availability constrains the hydraulic architecture and water relations of savannah trees. Plant, Cell & Environment, 29, 2153-2167.
[8]	Chen FS, Niklas KJ, Liu Y, Fang XM, Wan SZ, Wang HM (2015) Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Chinese fir leaves and twigs differing in age. Tree Physiology, 35, 1106-1117.
[9]	Collalti A, Prentice I (2019) Is NPP proportional to GPP? Waring’s hypothesis 20 years on. Tree Physiology, 39, 1473-1483. DOI PMID
[10]	Chu CJ, Wang YS, Liu Y, Jiang L, He FL (2017) Advances in species coexistence theory. Biodiversity Science, 25, 345-354. (in Chinese with English abstract) DOI
	[储诚进, 王酉石, 刘宇, 蒋林, 何芳良 (2017) 物种共存理论研究进展. 生物多样性, 25, 345-354.] DOI
[11]	Damián X, Fornoni J, Domínguez CA, Boege K (2018) Ontogenetic changes in the phenotypic integration and modularity of leaf functional traits. Functional Ecology, 32, 234-246.
[12]	DeForest JL, Snell RS (2020) Tree growth response to shifting soil nutrient economy depends on mycorrhizal associations. New Phytologist, 225, 2557-2566. DOI PMID
[13]	Domingues TF, Meir P, Feldpausch TR, Saiz G, Veenendaal EM, Schrodt F, Bird M, Djagbletey G, Hien F, Compaore H, Diallo A, Grace J, Lloyd J (2010) Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment, 33, 959-980.
[14]	Farquhar GD, von Caemmerer SV, Berry JA (1980) A biochemical model of photosynthetic CO₂ assimilation in leaves of C₃ species. Planta, 149, 78-90. DOI PMID
[15]	Fownes JH, Harrington RA (2004) Seedling response to gaps: Separating effects of light and nitrogen. Forest Ecology and Management, 203, 297-310.
[16]	Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: Past, present, and future. Biogeochemistry, 70, 153-226.
[17]	Gough C, Seiler J, Maier C (2004) Short-term effects of fertilization on loblolly pine (Pinus taeda L.)physiology. Plant, Cell & Environement, 27, 876-886.
[18]	Hidaka A, Kitayama K (2013) Relationship between photosynthetic phosphorus-use efficiency and foliar phosphorus fractions in tropical tree species. Ecology and Evolution, 3, 4872-4880. DOI PMID
[19]	Hu Y, Schäfer KV, Zhu L, Zhao P, Zhao X, Ni G, Zhang Y, Ye H, Zhao W, Shen W, Fu SL (2021) Impacts of canopy and understory nitrogen additions on stomatal conductance and carbon assimilation of dominant tree species in a temperate broadleaved deciduous forest. Ecosystems, 24, 1468-1484.
[20]	Jiang J, Wang Y, Liu F, Du Y, Zhuang W, Chang Z, Yu M, Yan J (2021) Antagonistic and additive interactions dominate the responses of belowground carbon-cycling processes to nitrogen and phosphorus additions. Soil Biology and Biochemistry, 156, 108216.
[21]	Jiang L, Tian D, Ma SH, Zhou XL, Xu LC, Zhu JX, Jing X, Zheng CY, Shen HH, Zhou Z, Li YD, Zhu B, Fang JY (2018) The response of tree growth to nitrogen and phosphorus additions in a tropical montane rainforest. Science of the Total Environment, 618, 1064-1070.
[22]	Kellomäki S, Wang KY (1997) Photosynthetic responses of Scots pine to elevated CO₂ and nitrogen supply: Results of a branch-in-bag experiment. Tree Physiology, 17, 231-240. PMID
[23]	Kuusk V, Niinemets Ü, Valladares F (2018) Structural controls on photosynthetic capacity through juvenile-to-adult transition and needle ageing in Mediterranean pines. Functional Ecology, 32, 1479-1491.
[24]	LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology, 89, 371-379. DOI PMID
[25]	Leuning R (1997) Scaling to a common temperature improves the correlation between the photosynthesis parameters J_max and V_cmax. Journal of Experimental Botany, 48, 345-347.
[26]	Liang X, Zhang T, Lu X, Ellsworth DS, BassiriRad H, You C, Wang D, He P, Deng Q, Liu H, Mo J, Ye Q (2020) Global response patterns of plant photosynthesis to nitrogen addition: A meta-analysis. Global Change Biology, 26, 3585-3600. DOI PMID
[27]	Liu L, Zhang T, Gilliam FS, Gundersen P, Zhang W, Chen H, Mo J (2013) Interactive effects of nitrogen and phosphorus on soil microbial communities in a tropical forest. PLoS ONE, 8, e61188.
[28]	Lu D, Zhu J, Wang X, Hao G, Wang GG (2021) A systematic evaluation of gap size and within-gap position effects on seedling regeneration in a temperate secondary forest, Northeast China. Forest Ecology and Management, 490, 119140.
[29]	Luo X, Keenan TF, Chen JM, Croft H, Colin Prentice I, Smith NG, Walker AP, Wang H, Wang R, Xu CG, Zhang Y (2021) Global variation in the fraction of leaf nitrogen allocated to photosynthesis. Nature Communications, 12, 4866. DOI PMID
[30]	Manu R, Corre MD, Aleeje A, Mwanjalolo MJG, Babweteera F, Veldkamp E, van Straaten O (2022) Responses of tree growth and biomass production to nutrient addition in a semi-deciduous tropical forest in Africa. Ecology, 103, e3659.
[31]	Mo Q, Li Z, Sayer EJ, Lambers H, Li Y, Zou B, Tang J, Heskel M, Ding Y, Wang F, Ostertag R (2019) Foliar phosphorus fractions reveal how tropical plants maintain photosynthetic rates despite low soil phosphorus availability. Functional Ecology, 33, 503-513.
[32]	Niinemets Ü, Tenhunen J, Canta N, Chaves M, Faria T, Pereira JS, Reynolds JF (1999) Interactive effects of nitrogen and phosphorus on the acclimation potential of foliage photosynthetic properties of cork oak, Quercus suber, to elevated atmospheric CO₂ concentrations. Global Change Biology, 5, 455-470.
[33]	Pasquini SC, Santiago LS (2012) Nutrients limit photosynthesis in seedlings of a lowland tropical forest tree species. Oecologia, 168, 311-319. DOI PMID
[34]	Peng Y, Peng Z, Zeng X, Houx JH (2019) Effects of nitrogen-phosphorus imbalance on plant biomass production: A global perspective. Plant and Soil, 436, 245-252.
[35]	Poorter L, Wright SJ, Paz H, Ackerly DD, Condit R, Ibarra-Manríquez G, Harms KE, Licona JC, Martínez-Ramos M, Mazer SJ, Muller-Landau HC, Peña-Claros M, Webb CO, Wright IJ (2008) Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology, 89, 1908-1920. DOI PMID
[36]	Shigeo K, Li CH, Hideyuki K, Yasuhide N (2001) Nutrients return of litterfall of a natural evergreen broad-leaved forest in Southern China. Resources Science, 23(S1), 58-67. (in Chinese with English abstract)
	[片桐成夫, 李昌华, 川口英之, 长山泰秀 (2001) 中国南部天然常绿阔叶林的凋落物养分归还. 资源科学, 23(S1), 58-67.]
[37]	Stefanski A, Bermudez R, Sendall KM, Montgomery RA, Reich PB (2020) Surprising lack of sensitivity of biochemical limitation of photosynthesis of nine tree species to open-air experimental warming and reduced rainfall in a southern boreal forest. Global Change Biology, 26, 746-759. DOI PMID
[38]	Sturchio MA, Chieppa J, Simpson LT, Feller IC, Chapman SK, Aspinwall MJ (2023) Contrasting effects of nitrogen addition on leaf photosynthesis and respiration in black mangrove in North Florida. Estuaries and Coasts, 46, 182-197.
[39]	Tang XL, Cao YH, Gu LH, Zhou BZ (2017) Advances in photo-physiological responses of leaves to environmental factors based on the FvCB model. Acta Ecologica Sinica, 37, 6633-6645. (in Chinese with English abstract)
	[唐星林, 曹永慧, 顾连宏, 周本智 (2017) 基于FvCB模型的叶片光合生理对环境因子的响应研究进展. 生态学报, 37, 6633-6645.]
[40]	Tian DS, Niu SL (2015) A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters, 10, 024019.
[41]	Tsujii Y, Onoda Y, Kitayama K (2017) Phosphorus and nitrogen resorption from different chemical fractions in senescing leaves of tropical tree species on Mount Kinabalu, Borneo. Oecologia, 185, 171-180. DOI PMID
[42]	Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature, 555, 367-370.
[43]	Walker AP, Beckerman AP, Gu LH, Kattge J, Cernusak LA, Domingues TF, Scales JC, Wohlfahrt G, Wullschleger SD, Woodward FI (2014) The relationship of leaf photosynthetic traits—V_cmax and J_max—to leaf nitrogen, leaf phosphorus, and specific leaf area: A meta-analysis and modeling study. Ecology and Evolution, 4, 3218-3235.
[44]	Wallace ZP, Lovett GM, Hart JE, Machona B (2007) Effects of nitrogen saturation on tree growth and death in a mixed-oak forest. Forest Ecology and Management, 243, 210-218.
[45]	Wang D, Ling T, Wang P, Jing P, Fan J, Wang H, Zhang Y (2018) Effects of 8-year nitrogen and phosphorus treatments on the ecophysiological traits of two key species on Tibetan Plateau. Frontiers in Plant Science, 9, 1290. DOI PMID
[46]	Wang H, Prentice IC, Davis TW, Keenan TF, Wright IJ, Peng C (2017) Photosynthetic responses to altitude: An explanation based on optimality principles. New Phytologist, 213, 976-982. DOI PMID
[47]	Warren CR, McGrath JF, Adams MA (2005) Differential effects of N, P and K on photosynthesis and partitioning of N in Pinus pinaster needles. Annals of Forest Science, 62, 1-8.
[48]	Wright SJ, Turner BL, Yavitt JB, Harms KE, Kaspari M, Tanner EVJ, Bujan J, Griffin EA, Mayor JR, Pasquini SC, Sheldrake M, Garcia MN (2018) Plant responses to fertilization experiments in lowland, species-rich, tropical forests. Ecology, 99, 1129-1138. DOI PMID
[49]	Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EV, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology, 92, 1616-1625. PMID
[50]	Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C₃ plants—A retrospective analysis of the A-C_i curves from 109 species. Journal of Experimental Botany, 44, 907-920.
[51]	Yavitt JB, Harms KE, Garcia MN, Mirabello MJ, Wright SJ (2011) Soil fertility and fine root dynamics in response to 4 years of nutrient (N, P, K) fertilization in a lowland tropical moist forest, Panama. Austral Ecology, 36, 433-445.
[52]	Ye XM, Bu W, Hu X, Liu B, Liang K, Chen F (2023a) Species divergence in seedling leaf traits and tree growth response to nitrogen and phosphorus additions in an evergreen broadleaved forest of subtropical China. Journal of Forestry Research, 34, 137-150.
[53]	Ye XM, Bu W, Hu X, Wang F, Sun R, He P, Liang X, Chen F (2023b) Are small trees more responsive to nutrient addition than large trees in an evergreen broadleaved forest? Forest Ecology and Management, 543, 121129.
[54]	Yu Q, Ni X, Cheng X, Ma S, Tian D, Zhu B, Zhu J, Ji C, Tang Z, Fang J (2022) Foliar phosphorus allocation and photosynthesis reveal plants' adaptative strategies to phosphorus limitation in tropical forests at different successional stages. Science of the Total Environment, 846, 157456.
[55]	Zhai ZW, Gong JR, Luo QP, Pan Y, Baoyin T, Xu S, Liu M, Yang LL (2017) Effects of nitrogen addition on photosynthetic characteristics of Leymus chinensis in the temperate grassland of Nei Mongol, China. Chinese Journal of Plant Ecology, 41, 196-208. (in Chinese with English abstract)
	[翟占伟, 龚吉蕊, 罗亲普, 潘琰, 宝音陶格涛, 徐沙, 刘敏, 杨丽丽 (2017) 氮添加对内蒙古温带草原羊草光合特性的影响. 植物生态学报, 41, 196-208.] DOI
[56]	Zhu F, Lu X, Mo J (2014) Phosphorus limitation on photosynthesis of two dominant understory species in a lowland tropical forest. Journal of Plant Ecology, 7, 526-534. DOI