Research Articles

Effects of previous nitrogen addition on aboveground and belowground carbon and nitrogen allocation dynamics in drought-exposed sessile oak seedlings

  • FENG Mei ,
  • OUYANG Sheng-Nan ,
  • Matthias SAURER ,
  • LI Mai-He ,
  • ZHOU Xiao-Qian ,
  • TIE Lie-Hua ,
  • SHEN Wei-Jun ,
  • DUAN Hong-Lang ,
  • Arthur GESSLER
Expand
  • 1Institute for Forest Resources and Environment of Guizhou, Guizhou Key Laboratory of Forest Cultivation in Plateau Mountain, College of Forestry,Guizhou University, Guiyang 550025, China
    2Swiss Federal Institute for Forest, Snow and Landscape Research, Birmensdorf 8903, Switzerland
    3School of Life Science, Hebei University, Baoding, Hebei 071000, China
    4College of Forestry, Guangxi University, Nanning 530004, China
    5Institute of Terrestrial Ecosystems, Swiss Federal Institute of Technology, Zurich 8902, Switzerland

Received date: 2024-07-04

  Accepted date: 2025-01-20

  Online published: 2025-01-20

Supported by

National Natural Science Foundation of China(32360259);National Natural Science Foundation of China(32460379);Guizhou Provincial Science and Technology Projects(ZK[2023]YIBAN110);Guizhou Provincial Science and Technology Projects(ZK[2022]YIBAN101)

Abstract

Aims Drought effects on the carbon (C) balance are considered the major factor of tree mortality and are assumed to be regulated by soil nutrient (e.g., nitrogen (N)) availability. However, the effects of nitrogen addition on trees’ carbon and nitrogen distribution between aboveground and belowground and the coupling between carbon and nitrogen relations in various organs in response to drought are still unclear in trees.
Methods A two-year full factorial microcosm experiment was set up with sessile oak (Quercus petraea). Nitrogen addition was performed in the first year, and a drought treatment was conducted in the second year. Isotope 15N and 13C labelling were carried out before drought and during drought, respectively. Three consecutive samplings were conducted after the dual labelling with 13C and 15N in the second year, and the effects of nitrogen addition on carbon and nitrogen allocation dynamics during progressive drought were tested.
Important findings Our results showed that previous nitrogen addition promoted photosynthetic carbon fixation and nitrogen allocation, increased root nitrogen uptake, reduced the non-structural carbohydrates (NSC) contents in all organs and changed the relationships of carbon and nitrogen in aboveground and belowground organs. In contrast, drought had minor effects on nitrogen and carbon allocation between aboveground and belowground and the relationship of carbon with nitrogen in all organs (represented by the ratio of 13C to 15N in all organs). Drought only significantly reduced the content of NSC. During drought (from day 40 to 73), previous nitrogen addition led sessile oak to prioritise belowground carbon and nitrogen allocation. Our results indicate that sessile oak can change its carbon and nitrogen allocation strategies to adapt to drought, while previous nitrogen addition may increase its drought sensitivity.

Cite this article

FENG Mei , OUYANG Sheng-Nan , Matthias SAURER , LI Mai-He , ZHOU Xiao-Qian , TIE Lie-Hua , SHEN Wei-Jun , DUAN Hong-Lang , Arthur GESSLER . Effects of previous nitrogen addition on aboveground and belowground carbon and nitrogen allocation dynamics in drought-exposed sessile oak seedlings[J]. Chinese Journal of Plant Ecology, 2025 , 49(9) : 1527 -1542 . DOI: 10.17521/cjpe.2024.0218

References

[1] Anderegg WRL, Klein T, Bartlett M, Sack L, Pellegrini AFA, Choat B, Jansen S (2016). Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proceedings of the National Academy of Sciences of the United States of America, 113, 5024-5029.
[2] Anderegg WRL, Trugman AT, Badgley G, Anderson CM, Bartuska A, Ciais P, Cullenward D, Field CB, Freeman J, Goetz SJ, Hicke JA, Huntzinger D, Jackson RB, Nickerson J, Pacala S, Randerson JT (2020). Climate-driven risks to the climate mitigation potential of forests. Science, 368, eaaz7005. DOI: 10.1126/science.aaz700.
[3] Bloom AJ, Chapin III FS, Mooney HA (1985). Resource limitation in plants-an economic analogy. Annual Review of Ecology and Systematics, 16, 363-392.
[4] Cary KL, Ranieri GM, Pittermann J (2020). Xylem form and function under extreme nutrient limitation: an example from California’s pygmy forest. New Phytologist, 226, 760-769.
[5] Chen LT, Gao RM, Shi XD (2017). Drought stress on chlorophyll content and root activity in seedlings of Larix principis-rupprechtii and Pinus tabuliformis. Journal of Agriculture, 7(3), 67.
  [陈龙涛, 高润梅, 石晓东 (2017). 干旱胁迫对华北落叶松和油松幼苗叶绿素含量与根系活力的影响. 农学学报, 7(3), 67.]
[6] Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018). Triggers of tree mortality under drought. Nature, 558, 531-539.
[7] Cochard H, Cruiziat P, Tyree MT (1992). Use of positive pressures to establish vulnerability curves: further support for the air-seeding hypothesis and implications for pressure-volume analysis. Plant Physiology, 100, 205-209.
[8] Dietze MC, Sala AN, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014). Nonstructural carbon in woody plants. Annual Review of Plant Biology, 65, 667-687.
[9] Duan HL, Wu JP, Liu WF, Liao YC, Zhang HN, Fan HB (2015). Water relations and carbon dynamics under drought stress and the mechanisms of drought-induced tree mortality. Scientia Silvae Sinicae, 51(11), 113-120.
  [段洪浪, 吴建平, 刘文飞, 廖迎春, 张海娜, 樊后保 (2015). 干旱胁迫下树木的碳水过程以及干旱死亡机理. 林业科学, 51(11), 113-120.]
[10] Dziedek C, H?rdtle W, von Oheimb G, Fichtner A (2016). Nitrogen addition enhances drought sensitivity of young deciduous tree species. Frontiers in Plant Science, 7, 1100. DOI: 10.3389/fpls.2016.01100.
[11] Ellenberg H, Leuschner C (2010). Vegetation Mitteleuropas mit den Alpen: in ?kologischer, Dynamischer und Historischer Sicht. Springer Spektrum, Germany.
[12] Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, et al. (2013). The global nitrogen cycle in the twenty-first century. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 368, 20130164. DOI: 10.1098/rstb.2013.0164.
[13] Galiano L, Timofeeva G, Saurer M, Siegwolf R, Martínez-Vilalta J, Hommel R, Gessler A (2017). The fate of recently fixed carbon after drought release: towards unravelling C storage regulation in Tilia platyphyllos and Pinus sylvestris. Plant, Cell & Environment, 40, 1711-1724.
[14] Gessler A, Jung K, Gasche R, Papen H, Heidenfelder A, B?rner E, Metzler B, Augustin S, Hildebrand E, Rennenberg H (2005). Climate and forest management influence nitrogen balance of European beech forests: microbial N transformations and inorganic N net uptake capacity of mycorrhizal roots. European Journal of Forest Research, 124, 95-111.
[15] Gessler A, Keitel C, Kreuzwieser J, Matyssek R, Seiler W, Rennenberg H (2007). Potential risks for European beech (Fagus sylvatica L.) in a changing climate. Trees, 21, 1-11.
[16] Gessler A, Keitel C, Nahm M, Rennenberg H (2004). Water shortage affects the water and nitrogen balance in Central European beech forests. Plant Biology, 6, 289-298.
[17] Gessler A, Schaub M, McDowell NG (2017). The role of nutrients in drought-induced tree mortality and recovery. New Phytologist, 214, 513-520.
[18] Hagedorn F, Joseph J, Peter M, Luster J, Pritsch K, Geppert U, Kerner R, Molinier V, Egli S, Schaub M, Liu JF, Li MH, Sever K, Weiler M, Siegwolf RTW, Gessler A, Arend M (2016). Recovery of trees from drought depends on belowground sink control. Nature Plants, 2, 16111. DOI: 10.1038/nplants.2016.111.
[19] Hartmann H, Trumbore S (2016). Understanding the roles of nonstructural carbohydrates in forest trees—From what we can measure to what we want to know. New Phytologist, 211, 386-403.
[20] Hartmann H, Ziegler W, Kolle O, Trumbore S (2013a). Thirst beats hunger-declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytologist, 200, 340-349.
[21] Hartmann H, Ziegler W, Trumbore S (2013b). Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Functional Ecology, 27, 413-427.
[22] Haynes BE, Gower ST (1995). Belowground carbon allocation in unfertilized and fertilized red pine plantations in northern Wisconsin. Tree Physiology, 15, 317-325.
[23] Hertenberger G, Wanek W (2004). Evaluation of methods to measure differential 15N labeling of soil and root N pools for studies of root exudation. Rapid Communications in Mass Spectrometry, 18, 2415-2425.
[24] Hikino K, Danzberger J, Riedel VP, Hesse BD, Hafner BD, Gebhardt T, Rehschuh R, Ruehr NK, Brunn M, Bauerle TL, Landh?usser SM, Lehmann MM, R?tzer T, Pretzsch H, Buegger F, et al. (2022). Dynamics of initial carbon allocation after drought release in mature Norway spruce—Increased belowground allocation of current photoassimilates covers only half of the carbon used for fine-root growth. Global Change Biology, 28, 6889-6905.
[25] Hoch G, Richter A, K?rner C (2003). Non-structural carbon compounds in temperate forest trees. Plant, Cell & Environment, 26, 1067-1081.
[26] Joseph J, Luster J, Bottero A, Buser N, Baechli L, Sever K, Gessler A (2021). Effects of drought on nitrogen uptake and carbon dynamics in trees. Tree Physiology, 41, 927-943.
[27] Kleczewski NM, Herms DA, Bonello P (2010). Effects of soil type, fertilization and drought on carbon allocation to root growth and partitioning between secondary metabolism and ectomycorrhizae of Betula papyrifera. Tree Physiology, 30, 807-817.
[28] Kreuzwieser J, Gessler A (2010). Global climate change and tree nutrition: influence of water availability. Tree Physiology, 30, 1221-1234.
[29] Li WB, Zhang HX, Huang GZ, Liu RX, Wu HJ, Zhao CY, McDowell NG (2020). Effects of nitrogen enrichment on tree carbon allocation: a global synthesis. Global Ecology and Biogeography, 29, 573-589.
[30] Lu JY, Yang JF, Keitel C, Yin LM, Wang P, Cheng WX, Dijkstra FA (2022). Belowground carbon efficiency for nitrogen and phosphorus acquisition varies between Lolium perenne and Trifolium repens and depends on phosphorus fertilization. Frontiers in Plant Science, 13, 927435. DOI: 10.3389/fpls.2022.927435.
[31] Ma Y, Su BL, Han YG, Wu XH, Zhou WM, Wang QW, Zhou L, Yu DP (2021). Response of photosynthetic characteristics and non-structural carbohydrate accumulation of Betula ermanii seedlings to drought stress. Chinese Journal of Applied Ecology, 32, 513-520.
  [马玥, 苏宝玲, 韩艳刚, 吴星慧, 周旺明, 王庆伟, 周莉, 于大炮 (2021). 岳桦幼苗光合特性和非结构性碳水化合物积累对干旱胁迫的响应. 应用生态学报, 32, 513-520.]
[32] Malagoli P, Laine P, Rossato L, Ourry A (2005). Dynamics of nitrogen uptake and mobilization in field-grown winter oilseed rape (Brassica napus) from stem extension to harvest. II. An 15N-labelling-based simulation model of N partitioning between vegetative and reproductive tissues. Annals of Botany, 95, 1187-1198.
[33] Maru?i? M, Seletkovi? I, Ognjenovi? M, Jonard M, Sever K, Schaub M, Gessler A, ?ango M, Sirovica I, Zegnal I, Bogdani? R, Poto?i? N (2023). Nutrient and growth response of Fagus sylvatica L. saplings to drought is modified by fertilisation. Forests, 14, 2445. DOI: 10.3390/f14122445.
[34] McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008). Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytologist, 178, 719-739.
[35] McDowell NG (2011). Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology, 155, 1051-1059.
[36] McDowell NG, Sevanto S (2010). The mechanisms of carbon starvation: How, when, or does it even occur at all? New Phytologist, 186, 264-266.
[37] McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002). Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature, 415, 68-71.
[38] Millard P, Sommerkorn M, Grelet GA (2007). Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytologist, 175, 11-28.
[39] O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A (2014). Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nature Climate Change, 4, 710-714.
[40] Ouyang SN, Gessler A, Saurer M, Hagedorn F, Gao DC, Wang XY, Schaub M, Li MH, Shen WJ, Sch?nbeck L (2021). Root carbon and nutrient homeostasis determines downy oak sapling survival and recovery from drought. Tree Physiology, 41, 1400-1412.
[41] Ouyang SN, Tie LH, Saurer M, Bose AK, Duan HL, Li MH, Xu XL, Shen WJ, Gessler A (2024). Divergent role of nutrient availability in determining drought responses of sessile oak and Scots pine seedlings: evidence from 13C and 15N dual labeling. Tree Physiology, 44, tpad105. DOI: 10.1093/treephys/tpad105.
[42] Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012). Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist, 193, 30-50.
[43] Rehschuh R, Rehschuh S, Gast A, Jakab AL, Lehmann MM, Saurer M, Gessler A, Ruehr NK (2022). Tree allocation dynamics beyond heat and hot drought stress reveal changes in carbon storage, belowground translocation and growth. New Phytologist, 233, 687-704.
[44] Rehschuh R, Ruehr NK (2024). What is the role of soil nutrients in drought responses of trees? Tree Physiology, 44, tpad152. DOI: 10.1093/treephys/tpad152.
[45] Rennenberg H, Dannenmann M, Gessler A, Kreuzwieser J, Simon J, Papen H (2009). Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biology, 11, 4-23.
[46] Rissanen K, H?ltt? T, B?ck J, Rigling A, Wermelinger B, Gessler A (2021). Drought effects on carbon allocation to resin defences and on resin dynamics in old-grown scots pine. Environmental and Experimental Botany, 185, 104410. DOI: 10.1016/j.envexpbot.2021.104410.
[47] Rouphael Y, Cardarelli M, Schwarz D, Franken P, Colla G (2012). Effects of drought on nutrient uptake and assimilation in vegetable crops//Aroca R. Plant Responses to Drought Stress. Springer, Berlin. 171-195.
[48] Ruehr NK, Offermann CA, Gessler A, Winkler JB, Ferrio JP, Buchmann N, Barnard RL (2009). Drought effects on allocation of recent carbon: from beech leaves to soil CO2 efflux. New Phytologist, 184, 950-961.
[49] Sala AN, Piper F, Hoch G (2010). Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytologist, 186, 274-281.
[50] Sala A, Woodruff DR, Meinzer FC (2012). Carbon dynamics in trees: feast or famine? Tree Physiology, 32, 764-775.
[51] Salmon Y, Torres-Ruiz JM, Poyatos R, Martinez-Vilalta J, Meir P, Cochard H, Mencuccini M (2015). Balancing the risks of hydraulic failure and carbon starvation: a twig scale analysis in declining Scots pine. Plant, Cell & Environment, 38, 2575-2588.
[52] Santos M, Barros V, Lima L, Frosi G, Santos MG (2021). Whole plant water status and non-structural carbohydrates under progressive drought in a Caatinga deciduous woody species. Trees, 35, 1257-1266.
[53] Sardans J, Pe?uelas J (2012). The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiology, 160, 1741-1761.
[54] Sch?nbeck L, Gessler A, Schaub M, Rigling A, Hoch G, Kahmen A, Li MH (2020). Soil nutrients and lowered source: sink ratio mitigate effects of mild but not of extreme drought in trees. Environmental and Experimental Botany, 169, 103905. DOI: 10.1016/j.envexpbot.2019.103905.
[55] Sch?nbeck L, Li MH, Lehmann MM, Rigling A, Schaub M, Hoch G, Kahmen A, Gessler A (2021). Soil nutrient availability alters tree carbon allocation dynamics during drought. Tree Physiology, 41, 697-707.
[56] Sevanto S, Dickman LT (2015). Where does the carbon go? —Plant carbon allocation under climate change. Tree Physiology, 35, 581-584.
[57] Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014). How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment, 37, 153-161.
[58] Shang JZ, Gao TH, Wang WF, Zhou XJ, Zong YZ (2022). Effect of nitrogen addition for two consecutive years on photosynthetic characteristics, carbon and nitrogen distribution of Populus × euramericana ‘Zhongjin7’ seedlings. Scientia Silvae Sinicae, 58(6), 23-32.
  [尚佳州, 高钿惠, 王卫锋, 周新军, 宗毓铮 (2022). 连续2年氮添加对中金杨幼苗叶光合特性与碳氮分配的影响. 林业科学, 58(6), 23-32.]
[59] Wang J, Bian YY, Zhu YL, Yang QP, Fang X (2024). Effects of nitrogen addition and drought on sapling growth of four subtropical tree species. Journal of Tropical and Subtropical Botany, 32, 475-482.
  [王涓, 边妍妍, 朱玉璘, 杨清培, 方熊 (2024). 氮添加和干旱对亚热带4种幼树生长的影响. 热带亚热带植物学报, 32, 475-482.]
[60] Wang JX, Villar-Salvador P, Li GL, Liu Y (2019). Moderate water stress does not inhibit nitrogen remobilization, allowing fast growth in high nitrogen content Quercus variabilis seedlings under dry conditions. Tree Physiology, 39, 650-660.
[61] Wang J, Zheng FL, Zhao MM, Wei HM, Jiao JY, Wang XS (2022). Effects of CO2 doubling, warming, and light drought stress on root growth and nitrogen uptake of winter wheat. Journal of Plant Nutrition and Fertilizers, 28, 1977-1989.
  [王婧, 郑粉莉, 赵苗苗, 魏晗梅, 焦健宇, 王雪松 (2022). CO2浓度倍增、增温和轻度干旱对冬小麦根系生长和氮素吸收的影响. 植物营养与肥料学报, 28, 1977-1989.]
[62] Wang K, Wang X, Zhang RS, Liu C (2024). Seasonal dynamics of non structural carbohydrates in Populus alba and Ulmus pumila in Horqin Sandy Land. Journal of Ecology, 43, 3624-3631.
  [王凯, 王欣, 张日升, 刘畅 (2024). 科尔沁沙地银中杨与白榆非结构性碳水化合物的季节动态比较. 生态学杂志, 43, 3624-3631.]
[63] Wu M, Zhang WH, Zhou JY, Ma C, Han WJ (2014). Effects of drought stress on growth, physiological and biochemical parameters in fine roots of Quercus variabilis B1. seedlings. Acta Ecologica Sinica, 34, 4223-4233.
  [吴敏, 张文辉, 周建云, 马闯, 韩文娟 (2014). 干旱胁迫对栓皮栎幼苗细根的生长与生理生化指标的影响. 生态学报, 34, 4223-4233.]
[64] Yang Y, Ouyang SN, Gessler A, Wang XY, Na RS, He HS, Wu ZF, Li MH (2022). Root carbon resources determine survival and growth of young trees under long drought in combination with fertilization. Frontiers in Plant Science, 13, 929855. DOI: 10.3389/fpls.2022.929855.
[65] You R, Deng XW, Hu YT, Ouyang S, Chen L, Xiang WH (2023). Progress on physiological and ecological responses of trees to drought stress and rewatering. Scientia Silvae Sinicae, 59(11), 124-136.
  [游韧, 邓湘雯, 胡彦婷, 欧阳帅, 陈亮, 项文化 (2023). 树木对干旱胁迫及复水的生理生态响应研究进展. 林业科学, 59(11), 124-136.]
[66] Zhang HX, Li XR, Guan DX, Wang AZ, Yuan FH, Wu JB (2021). Nitrogen nutrition addition mitigated drought stress by improving carbon exchange and reserves among two temperate trees. Agricultural and Forest Meteorology, 311, 108693. DOI: 10.1016/j.agrformet.2021.108693.
[67] Zhang PP (2020). Response of Tree Non-structural Carbohydrates to Drought and Its Regulation Mechanism. PhD dissertation, East China Normal University, Shanghai.
  [张佩佩 (2020). 树木非结构性碳水化合物对干旱的响应及其调控机制. 博士学位论文, 华东师范大学, 上海.]
[68] Zhang QZ, Zhang JY, Shi ZL, Kang BY, Tu HK, Zhu JY, Li HY (2023). Nitrogen addition and drought affect nitrogen uptake patterns and biomass production of four urban greening tree species in North China. Science of the Total Environment, 893, 164893. DOI: 10.1016/j.scitotenv.2023.164893.
[69] Zhang T (2018). Effects of Drought Stress on Unstructured Carbohydrate of Robinia pseudoacacia and Pinus tabulaeformis seedlings. PhD dissertation, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing.
  [张婷 (2018). 干旱胁迫对刺槐和油松幼苗非结构性碳水化合物的影响. 博士学位论文, 中国科学院大学中国科学院教育部水土保持与生态环境研究中心, 北京.]
[70] Zhao N, Liao YC, Huang GM, Liu WF, Shen FF, Duan HL (2021). The effects of lethal drought on non-structural carbohydrates in seedlings of 8 tree species. Journal of Tropical Biology, 12, 289-295.
  [赵楠, 廖迎春, 黄国敏, 刘文飞, 沈芳芳, 段洪浪 (2021). 致死性干旱对8种树种幼苗非结构性碳水化合物的影响. 热带生物学报, 12, 289-295.]
[71] Zhao YJ, Ouyang SN, Tie LH, Cui Y, Duan HL (2022). Visual analysis of effects of nutrients on plant drought responses based on bibliometrics. Subtropical Plant Science, 51, 405-416.
  [赵永菊, 欧阳胜男, 铁烈华, 崔雍, 段洪浪 (2022). 基于文献计量学的养分添加影响植物干旱响应的可视化分析. 亚热带植物科学, 51, 405-416.]
[72] Zhou GY, Zhou LY, Shao JJ, Zhou XH (2020). Effects of extreme drought on terrestrial ecosystems: review and prospects. Chinese Journal of Plant Ecology, 44, 515-525.
  [周贵尧, 周灵燕, 邵钧炯, 周旭辉 (2020). 极端干旱对陆地生态系统的影响: 进展与展望. 植物生态学报, 44, 515-525.]
[73] Zhou XQ, Ouyang SN, Saurer M, Feng M, Bose AK, Duan HL, Gessler A (2024). Species-specific responses of C and N allocation to N addition: evidence from dual 13C and 15N labeling in three tree species. Science of the Total Environment, 927, 172164. DOI: 10.1016/j.scitotenv.2024.172164.
Outlines

/