Effects of nitrogen addition on phytolith-occluded carbon of understory plant-soil system in a subtropical evergreen broadleaf forest in south China

doi:10.17521/cjpe.2023.0184

Abstract

Abstract:

Aims As plants take up silicon (Si) from soil solutions and then form phytoliths, a little organic carbon (C) can be occluded, which is called phytolith-occluded C (PhytOC). Recently, PhytOC storage is recognized as one mechanism influencing C storage in terrestrial ecosystems. Elevated atmospheric nitrogen (N) deposition over the past few decades has profoundly affected C dynamics in forest ecosystems. However, limited study focused on increased exogenous N inputs effects on phytolith C sequestration in forests.

Methods Here, we designed an experiment with canopy N addition of 25 and 50 kg·hm⁻²·a⁻¹ (simplified as CN25 and CN50), respectively, and understory N addition of 25 and 50 kg·hm⁻²·a⁻¹ (simplified as UN25 and UN50), respectively, in a subtropical evergreen broadleaf forest, to explore the effects of atmospheric N deposition on PhytOC sequestration of dominant shrub, herb and soil in subtropical forest.

Important findings Our results showed that UN50 significantly increased PhytOC concentration in both plant leaves and litter. Exogenous N input can stimulate plant Si uptake, and thus promotes the phytolith C sequestration. However, only CN50 significantly increased PhytOC concentration in the soil, while as UN50 had a minor effect. This would be attributed to the inhibition of litter decomposition caused by UN50, thereby impeding phytolith release. Structural equation model showed that increased phosphorus (P) limitation, soil acidification, and alterations in litter decomposition rates caused by N addition affected PhytOC accumulation in leaves and soil. In summary, our results suggest that N deposition can promote the potential for PhytOC sequestration of understory plants and soil in subtropical forests.

Key words: nitrogen deposition, phytolith-occluded carbon, carbon storage, subtropical forest, understory plants

LU Xiao-Fei, QIN Zhang-Fen, WANG Bin, KUANG Yuan-Wen. Effects of nitrogen addition on phytolith-occluded carbon of understory plant-soil system in a subtropical evergreen broadleaf forest in south China[J]. Chin J Plant Ecol, 2024, 48(10): 1302-1311.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2023.0184

https://www.plant-ecology.com/EN/Y2024/V48/I10/1302

Figures/Tables 7

Fig. 1 Effects of nitrogen (N) addition on the contents of phytolith-occluded carbon (PhytOC) in the leaves of understory species in a subtropical evergreen broadleaf forest in south China (mean ± SD). Different lowercase letters indicate significant differences among treatments (p < 0.05). M, mode of N addition; R, level of N addition. CK, control; CN, canopy N addition; UN, understory N addition; 25 and 50 represent the N addition amount of 25 and 50 kg·hm-2·a-1, respectively.

Table 1 Effects of different nitrogen (N) addition on the leaves of understory plants in a subtropical evergreen broadleaf forest in south China (mean ± SD)

处理 Treatment	碳含量 Carbon (C) content (mg·g^-1)	氮含量 Nitrogen (N) content (mg·g^-1)	磷含量 Phosphorus (P) content (mg·g^-1)	碳氮比 C:N	氮磷比 N:P
CK	447.08 ± 20.95^a	19.96 ± 0.50^b	1.04 ± 0.04^a	22.76 ± 0.65^a	19.72 ± 0.91^b
CN25	448.93 ± 20.92^a	22.95 ± 1.27^a	1.02 ± 0.03^a	20.48 ± 1.02^b	22.98 ± 1.49^a
CN50	446.13 ± 30.45^a	21.31 ± 0.49^a	0.95 ± 0.04^a	21.20 ± 0.54^b	23.30 ± 1.23^a
UN25	449.41 ± 30.53^a	20.71 ± 0.74^b	1.01 ± 0.04^a	22.19 ± 0.88^a	20.98 ± 1.09^ab
UN50	450.02 ± 40.67^a	21.07 ± 0.52^ab	0.99 ± 0.04^a	21.64 ± 0.56^ab	21.87 ± 0.82^ab

Fig. 2 Effects of nitrogen (N) addition on the contents of phytolith-occluded carbon (PhytOC) in the litter in a subtropical evergreen broadleaf forest in south China (mean ± SD). Different lowercase letters indicate significant differences among treatments (p < 0.05). M, mode of N addition; R, level of N addition. CK, control; CN, canopy N addition; UN, understory N addition; 25 and 50 represent the N addition amount as 25 and 50 kg·hm-2·a-1, respectively.

Table 2 Effects of different nitrogen (N) addition on the chemical elements content of litter (mean ± SD)

处理 Treatment	碳含量 Carbon (C) content (mg·g^-1)	氮含量 N content (mg·g^-1)	磷含量 Phosphorus (P) content (mg·g^-1)	碳氮比 C:N	氮磷比 N:P
CK	481.5 ± 16.3^a	15.0 ± 0.81^b	0.95 ± 0.05^ab	32.2 ± 1.92^a	15.79 ± 0.61^b
CN25	463.0 ± 10.4^a	16.1 ± 0.42^b	0.99 ± 0.04^ab	28.7 ± 0.93^ab	16.27 ± 0.71^ab
CN50	469.8 ± 13.6^a	17.6 ± 1.01^a	1.07 ± 0.03^a	26.9 ± 2.21^b	16.44 ± 0.43^ab
UN25	466.9 ± 17.3^a	15.6 ± 0.63^b	1.01 ± 0.05^ab	30.6 ± 1.41^a	15.44 ± 0.49^b
UN50	480.0 ± 11.2^a	15.7 ± 1.02^b	0.94 ± 0.06^b	29.7 ± 2.54^a	16.70 ± 0.50^a

Fig. 3 Effects of nitrogen (N) addition on the contents of phytolith-occluded carbon (PhytOC) in the soil in a subtropical evergreen broadleaf forest in south China (mean ± SD). Different lowercase letters indicate significant differences among treatments (p < 0.05). M, mode of N addition; R, level of N addition. CK, control; CN, canopy N addition; UN, understory N addition; 25 and 50 represent N addition amount as 25 and 50 kg·hm-2·a-1, respectively.

Table 3 Effects of different nitrogen (N) addition on the soil properties (mean ± SD)

处理 Treatment	有机碳含量 SOC content (mg·g^-1)	植硅体碳/总有机碳 PhytOC/SOC (mg·g^-1)	总氮含量 N content (mg·g^-1)	可利用性氮含量 AN content (mg·kg^-1)	pH
CK	41.52 ± 1.13^ab	2.11 ± 0.21^b	2.65 ± 0.21^a	12.69 ± 0.81^b	3.81 ± 0.06^a
CN25	38.03 ± 3.14^b	2.20 ± 0.18^ab	2.44 ± 0.35^a	14.01 ± 1.65^ab	3.76 ± 0.07^ab
CN50	39.24 ± 0.88^b	2.84 ± 0.34^a	2.80 ± 0.32^a	15.59 ± 2.27^ab	3.64 ± 0.04^ab
UN25	43.31 ± 2.01^ab	1.92 ± 0.32^b	2.67 ± 0.30^a	16.04 ± 2.87^ab	3.56 ± 0.04^b
UN50	44.13 ± 1.52^a	2.51 ± 0.27^a	2.91 ± 0.28^a	17.19 ± 2.40^a	3.54 ± 0.05^b

Fig. 4 Structural equation model (SEM) for biological silicon feedback to nitrogen addition (N) and standardized total effects on foliar (A, B) and soil phytolith-occluded carbon (C, D) contents. Goodness-of-fit statistics for SEM are shown below (CFI, comparative fit index; df, degrees of freedom; RMSEA, root mean squared error of approximation). Blue and red arrows indicate significantly positive and negative relationships (p < 0.05), respectively. The numbers adjacent to arrows are standardized path coefficients. Arrow thickness is proportional to parameter size. P, phosphorus; PhytOC, phytolith-occluded carbon.

References 44

[1]	Alexandre A, Meunier JD, Colin F, Koud JM (1997). Plant impact on the biogeochemical cycle of silicon and related weathering processes. Geochimica et Cosmochimica Acta, 61, 677-682.
[2]	Bonan GB (2008). Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science, 320, 1444-1449.
[3]	Cama J, Ganor J (2006). The effects of organic acids on the dissolution of silicate minerals: a case study of oxalate catalysis of kaolinite dissolution. Geochimica et Cosmochimica Acta, 70, 2191-2209.
[4]	Carey JC, Fulweiler RW (2013). Nitrogen enrichment increases net silica accumulation in a temperate salt marsh. Limnology and Oceanography, 58, 99-111.
[5]	Carey JC, Fulweiler RW (2016). Human appropriation of biogenic silicon—The increasing role of agriculture. Functional Ecology, 30, 1331-1339.
[6]	Cornelis JT, Delvaux B (2016). Soil processes drive the biological silicon feedback loop. Functional Ecology, 30, 1298-1310.
[7]	de Tombeur F, Laliberté E, Lambers H, Faucon MP, Zemunik G, Turner BL, Cornelis JT, Mahy G (2021). A shift from phenol to silica-based leaf defences during long-term soil and ecosystem development. Ecology Letters, 24, 984-995. DOI PMID
[8]	de Tombeur F, Turner BL, Laliberté E, Lambers H, Mahy G, Faucon MP, Zemunik G, Cornelis JT (2020). Plants sustain the terrestrial silicon cycle during ecosystem retrogression. Science, 369, 1245-1248. DOI PMID
[9]	Farmer VC, Delbos E, Miller JD (2005). The role of phytolith formation and dissolution in controlling concentrations of silica in soil solutions and streams. Geoderma, 127, 71-79.
[10]	Feng H, Guo J, Peng C, Kneeshaw D, Roberge G, Pan C, Ma X, Zhou D, Wang W (2023). Nitrogen addition promotes terrestrial plants to allocate more biomass to aboveground organs: a global meta-analysis. Global Change Biology, 29, 3970-3989. DOI PMID
[11]	Fraysse F, Pokrovsky OS, Schott J, Meunier JD (2009). Surface chemistry and reactivity of plant phytoliths in aqueous solutions. Chemical Geology, 258, 197-206.
[12]	Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008). Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science, 320, 889-892. DOI PMID
[13]	Gao XP, Zou CQ, Wang LJ, Zhang FS (2005). Silicon improves water use efficiency in maize plants. Journal of Plant Nutrition, 27, 1457-1470.
[14]	Gewirtzman J, Tang J, Melillo JM, Werner WJ, Kurtz AC, Fulweiler RW, Carey JC (2019). Soil warming accelerates biogeochemical silica cycling in a temperate forest. Frontiers in Plant Science, 10, 1097. DOI: 10.3389/fpls.2019.01097. PMID
[15]	Gong HJ, Chen KM, Chen GC, Wang SM, Zhang CL (2003). Effects of silicon on growth of wheat under drought. Journal of Plant Nutrition, 26, 1055-1063.
[16]	Haynes RJ (2014). A contemporary overview of silicon availability in agricultural soils. Journal of Plant Nutrition and Soil Science, 177, 831-844.
[17]	He SQ, Huang ZT, Wu JS, Yang J, Jiang PK (2016). Evolution pattern of phytolith-occluded carbon in typical forest-soil ecosystems in tropics and subtropics, China. Chinese Journal of Applied Ecology, 27, 697-704.
	[ 何珊琼, 黄张婷, 吴家森, 杨杰, 姜培坤 (2016). 热带、亚热带典型森林-土壤系统植硅体碳演变规律. 应用生态学报, 27, 697-704.] DOI
[18]	Kostic L, Nikolic N, Bosnic D, Samardzic J, Nikolic M (2017). Silicon increases phosphorus (P) uptake by wheat under low P acid soil conditions. Plant and Soil, 419, 447-455.
[19]	Li Z, Song Z, Li B (2013). The production and accumulation of phytolith-occluded carbon in Baiyangdian reed wetland of China. Applied Geochemistry, 37, 117-124.
[20]	Liu GS (1996). Soil Physical and Chemical Analysis & Description of Soil Profiles. Standards Press of China, Beijing.
	[ 刘光崧 (1996). 土壤理化分析与剖面描述. 中国标准出版社, 北京.]
[21]	Liu SJ, Behm JE, Wan SQ, Yan JH, Ye Q, Zhang W, Yang XD, Fu SL (2021). Effects of canopy nitrogen addition on soil fauna and litter decomposition rate in a temperate forest and a subtropical forest. Geoderma, 382, 114703. DOI: 10.1016/j.geoderma.2020.114703.
[22]	Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013). Enhanced nitrogen deposition over China. Nature, 494, 459-462.
[23]	Lu X, Qin Z, Lambers H, Tang S, Kaal J, Hou E, Kuang Y (2022). Nitrogen addition increases aboveground silicon and phytolith concentrations in understory plants of a tropical forest. Plant and Soil, 477, 25-39.
[24]	Lü HY, Jia JW, Wang WM, W YJ, Liu KB (2002). On the meaning of phytolith and its classification in Gramineae. Acta Micropalaeontologica Sinica, 19, 389-396.
	[ 吕厚远, 贾继伟, 王伟铭, 王永吉, 廖淦标 (2002). “植硅体”含义和禾本科植硅体的分类. 微体古生物学报, 19, 389-396.]
[25]	Mao Q, Lu X, Mo H, Gundersen P, Mo J (2018). Effects of simulated N deposition on foliar nutrient status, N metabolism and photosynthetic capacity of three dominant understory plant species in a mature tropical forest. Science of the Total Environment, 610-611, 555-562.
[26]	Meunier JD, Sandhya K, Prakash NB, Borschneck D, Dussouillez P (2018). pH as a proxy for estimating plant-available Si? A case study in rice fields in Karnataka (South India). Plant and Soil, 432, 143-155.
[27]	Parr J, Sullivan L, Chen B, Ye G, Zheng W (2010). Carbon bio-sequestration within the phytoliths of economic bamboo species. Global Change Biology, 16, 2661-2667.
[28]	Parr JF, Sullivan LA (2005). Soil carbon sequestration in phytoliths. Soil Biology & Biochemistry, 37, 117-124.
[29]	Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y, Hinsinger P, Llusia J, Nardin E, Vicca S, Obersteiner M, Janssens IA (2013). Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications, 4, 2934. DOI: 10.1038/ncomms3934. PMID
[30]	Quigley KM, Griffith DM, Donati GL, Anderson TM (2020). Soil nutrients and precipitation are major drivers of global patterns of grass leaf silicification. Ecology, 101, e03006. DOI: 10.1002/ecy.3006.
[31]	Reyerson PE, Alexandre A, Harutyunyan A, Corbineau R, Martinez de la Torre HA, Badeck F, Cattivelli L, Santos GM (2016). Unambiguous evidence of old soil carbon in grass biosilica particles. Biogeosciences, 13, 1269-1286.
[32]	Song ZL, Liu HY, Si Y, Yin Y (2012). The production of phytoliths in China’s grasslands: implications to the biogeochemical sequestration of atmospheric CO₂. Global Change Biology, 18, 3647-3653.
[33]	Song Z, Liu H, Strömberg CAE, Yang X, Zhang X (2017). Phytolith carbon sequestration in global terrestrial biomes. Science of the Total Environment, 603-604, 502-509.
[34]	Sun Y, Wang CT, Chen HYH, Ruan HH (2020). Responses of C:N stoichiometry in plants, soil, and microorganisms to nitrogen addition. Plant and Soil, 456, 277-287.
[35]	Tian D, Li P, Fang WJ, Xu J, Luo YK, Yan ZB, Zhu BA, Wang JA, Xu XN, Fang JY (2017). Growth responses of trees and understory plants to nitrogen fertilization in a subtropical forest in China. Biogeosciences, 14, 3461-3469.
[36]	Tian DS, Niu SL (2015). A global analysis of soil acidification caused by nitrogen addition. Environmental Research Letters, 10, 024019. DOI: 10.1088/1748-9326/10/2/024019.
[37]	Tian Q, Lu P, Ma P, Zhou H, Yang M, Zhai X, Chen M, Wang H, Li W, Bai W, Lambers H, Zhang W (2020). Processes at the soil-root interface determine the different responses of nutrient limitation and metal toxicity in forbs and grasses to nitrogen enrichment. Journal of Ecology, 109, 927-938.
[38]	Tian Y, Lu H, Wang J, Lin Y, Campbell DE, Jian S (2019). Effects of canopy and understory nitrogen addition on the structure and ec-oexergy of a subtropical forest community. Ecological Indicators, 106, 105459. DOI: 10.1016/j.ecolind.2019.105459.
[39]	Yan ZB, Tian D, Han WX, Tang ZY, Fang JY (2017). An assessment on the uncertainty of the nitrogen to phosphorus ratio as a threshold for nutrient limitation in plants. Annals of Botany, 120, 937-942. DOI PMID
[40]	Yang X, Song Z, Liu H, Bolan NS, Wang H, Li Z (2015). Plant silicon content in forests of north China and its implications for phytolith carbon sequestration. Ecological Research, 30, 347-355.
[41]	Ying YQ, Xiang TT, Li YF, Wu JS, Jiang PK (2015). Estimation of sequestration potential via phytolith carbon by important forest species in subtropical China. Journal of Natural Resources, 30, 133-140. DOI
	[ 应雨骐, 项婷婷, 李永夫, 吴家森, 姜培坤 (2015). 中国亚热带重要树种植硅体碳封存潜力估测. 自然资源学报, 30, 133-140.]
[42]	Zhang W, Shen WJ, Zhu SD, Wan SQ, Luo YQ, Yan JH, Wang KY, Liu L, Dai HT, Li PX, Dai KY, Zhang WX, Liu ZF, Wang FM, Kuang YW, et al. (2015). Can canopy addition of nitrogen better illustrate the effect of atmospheric nitrogen deposition on forest ecosystem? Scientific Reports, 5, 11245. DOI: 10.1038/srep11245. PMID
[43]	Zhang XD, Song ZL, Hao Q, Wang YD, Ding F, Song AL (2019). Phytolith-occluded carbon storages in forest litter layers in Southern China: implications for evaluation of long-term forest carbon budget. Frontiers in Plant Science, 10, 581. DOI: 10.3389/fpls.2019.00581. PMID
[44]	Zhao YY, Song ZL, Xu XT, Liu HY, Wu XC, Li ZM, Guo FS, Pan WJ (2016). Nitrogen application increases phytolith carbon sequestration in degraded grasslands of North China. Ecological Research, 31, 117-123.