Response of mangrove fine root functional traits to sediment nutrient changes at different tide levels in Dongzhaigang, Hainan, China

doi:10.17521/cjpe.2024.0307

Abstract

Abstract:

Aims Different levels of tidal flooding significantly affect mangrove sediment nutrients and stoichiometric characteristics, and plant fine root functional traits are keys strategies to cope with nutrient changes. However, there is a lack of in-depth understanding of the correlation between mangrove sediment nutrient changes and fine root functional traits at different tide levels, and relatively few studies have been conducted to explore the nutrient dynamics in exotic and native mangrove plants from the scale of fine root functional traits.

Methods The present study used native species Bruguiera sexangular and exotic species Sonneratia apetala to sample fine root and rhizosphere sediments at different tide levels. The relationship between fine root functional traits of two mangrove species and the content of nutrients and enzyme activities in rhizosphere sediments was analyzed.

Important findings The results showed that: 1) The exotic species displayed higher nutrient acquisition requirements and more substantial metabolic capacity than the native species, and both species were subjected to a certain degree of nitrogen restriction. 2) Within a certain range, the conversion rates of nitrogen and phosphorus in sediments accelerate significantly with the increase of waterlogging degree, and the contents of ammonium nitrogen, nitrate nitrogen, and available phosphorus in sediments increase with the increase of waterlogging time. 3) The specific root length of fine roots of the two species was significantly positively correlated with the nitrate nitrogen content in the sediment, indicating that the increase of sediment nutrient availability played an important role in promoting the root elongation of mangrove plants. This study can provide basic data and scientific reference for the environmental protection of the mangrove ecosystem and the development and utilization of biological resources.

Key words: mangrove, fine root, functional traits, intertidal elevation, sediment nutrients, nutritional restriction

LI Meng-Qi, MIAO Ling-Feng, LI Da-Dong, LONG Yi-Fan, YE Bing-Bing, YANG Fan. Response of mangrove fine root functional traits to sediment nutrient changes at different tide levels in Dongzhaigang, Hainan, China[J]. Chin J Plant Ecol, 2025, 49(4): 552-561.

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URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2024.0307

https://www.plant-ecology.com/EN/Y2025/V49/I4/552

Figures/Tables 6

Table 1 Root functional traits and ecological stoichiometry of two mangrove plants under different tide levels (mean±SE)

Table 2 Nutrients and moisture contents in rhizosphere sediments of two mangrove species at different tide levels (mean ± SE)

物种/潮位 Species/intertidal elevation	SWC (%)	NH₄⁺-N (mg·kg^-1)	NO₃^--N (mg·kg^-1)	AP (mg·kg⁻¹)
海莲/低 Bruguiera sexangular/L	0.56 ± 0.01^a	0.95 ± 0.01^c	1.10 ± 0.19^b	27.68 ± 2.68^a
海莲/中 Bruguiera sexangular/M	0.48 ± 0.03^b	1.05 ± 0.01^b	0.62 ± 0.03^c	17.74 ± 5.51^a
海莲/高 Bruguiera sexangular/H	0.37 ± 0.00^c	0.76 ± 0.02^e	0.45 ± 0.11^d	26.71 ± 12.06^a
无瓣海桑/低 Sonneratia apetala/L	0.56 ± 0.01^a	0.85 ± 0.02^d	1.61 ± 0.13^a	33.21 ± 8.71^a
无瓣海桑/中 Sonneratia apetala/M	0.48 ± 0.03^b	1.23 ± 0.01^a	0.33 ± 0.05^d	24.82 ± 5.75^a
无瓣海桑/高 Sonneratia apetala/H	0.37 ± 0.00^c	0.67 ± 0.01^f	0.29 ± 0.10^d	16.65 ± 5.11^a

Fig. 1 Activities of root peroxidase, sediment urease and acid phosphatase of 2 mangrove plants under different tide levels (mean ± SE). A, Root peroxidase activity. B, Urease activity of sediments. C, Sediment acid phosphatase activity. HL, Bruguiera sexangular; HS, Sonneratia apetala. H, high intertidal elevation; M, middle intertidal elevation; L, low intertidal elevation. Different lowercase letters indicate that the activities of root peroxidase, rhizosphere sediment urease, and acid phosphatase are significantly different at various tide levels and between the two species (p < 0.05).

Fig. 2 Relationship of fine root length, specific root surface area, root tissue density of two mangrove species with ammonium and nitrate nitrogen, and available phosphorus contents in sediments under different tide levels in mangrove ecosystem of Dongzhaigang. HL, Bruguiera sexangular; HS, Sonneratia apetala. H, high intertidal elevation; M, middle intertidal elevation; L, low intertidal elevation.

Fig. 3 Relationship between specific root length, specific root surface area, root tissue density, and root nitrogen content of two mangrove species under different tide levels in Dongzhaigang mangrove ecosystem. HL, Bruguiera sexangular; HS, Sonneratia apetala. H, high intertidal elevation; M, middle intertidal elevation; L, low intertidal elevation.

Fig. 4 Relationship between carbon (C), nitrogen (N), and phosphorus (P) contents of fine roots of two mangrove species at different tide levels in the mangrove ecosystem of Dongzhaigang. HL, Bruguiera sexangular; HS, Sonneratia apetala. H, high intertidal elevation; M, middle intertidal elevation; L, low intertidal elevation.

References 41

[1]	A’Bear AD, Jones TH, Kandeler E, Boddy L (2014). Interactive effects of temperature and soil moisture on fungal-mediated wood decomposition and extracellular enzyme activity. Soil Biology & Biochemistry, 70, 151-158.
[2]	Bao SD (2000). Soil Agro-Chemistrical Analysis. 3rd ed. China Agriculture Press, Beijing.
	[鲍士旦 (2000). 土壤农化分析. 3版. 中国农业出版社, 北京.]
[3]	Blokhina OB, Chirkova TV, Fagerstedt KV (2001). Anoxic stress leads to hydrogen peroxide formation in plant cells. Journal of Experimental Botany, 52, 1179-1190. PMID
[4]	Chai M, Li R, Tam NFY, Zan Q (2019). Effects of mangrove plant species on accumulation of heavy metals in sediment in a heavily polluted mangrove swamp in Pearl River Estuary, China. Environmental Geochemistry and Health, 41, 175-189. DOI PMID
[5]	Chen L, Hong WJ, Huang YP, Mai ZT, Zeng DH (2019). Growth, leaf element content and stoichiometric characteristics of six common mangrove species. Forestry and Environmental Science, 35(1), 83-88.
	[陈亮, 洪文君, 黄永平, 麦志通, 曾德华 (2019). 6种红树树种生长与叶片元素含量及化学计量特征. 林业与环境科学, 35(1), 83-88.]
[6]	Chen R, Wang WW, Cao LR, Chen M, Chen GS, Yao XD, Wang XH (2023). Variation of carbon, nitrogen and phosphorus stoichiometric characteristics of fine roots in masson pine and Chinese fir plantations with soil depth. Acta Ecologica Sinica, 43, 3709-3718.
	[陈蓉, 王韦韦, 曹丽荣, 陈铭, 陈光水, 姚晓东, 王小红 (2023). 马尾松和杉木人工林细根碳氮磷化学计量特征随土层深度的变化. 生态学报, 43, 3709-3718.]
[7]	Chen XH, Chen ZZ, Lei JR, Wu TT, Li YL (2022). Distribution characteristics of active organic carbon components in sediments of typical community types of mangrove wetland in Qinglan Port. Acta Ecologica Sinica, 42, 4572-4581.
	[陈小花, 陈宗铸, 雷金睿, 吴庭天, 李苑菱 (2022). 清澜港红树林湿地典型群落类型沉积物活性有机碳组分分布特征. 生态学报, 42, 4572-4581.]
[8]	Chen XP, Guo BQ, Zhong QL, Wang MT, Li M, Yang FC, Cheng DL (2018). Response of fine root carbon, nitrogen, and phosphorus stoichiometry to soil nutrients in Pinus taiwanensis along an elevation gradient in the Wuyi Mountains. Acta Ecologica Sinica, 38, 273-281.
	[陈晓萍, 郭炳桥, 钟全林, 王满堂, 李曼, 杨福春, 程栋梁 (2018). 武夷山不同海拔黄山松细根碳、氮、磷化学计量特征对土壤养分的适应. 生态学报, 38, 273-281.]
[9]	Dai J (2018). Adaptational Mechanism of Mangrove Seedlings of Kandelia obovata to Tidal Waterlogging. Master degree dissertation, East China Normal University, Shanghai.
	[代捷 (2018). 秋茄幼苗对潮汐水淹的适应机制. 硕士学位论文, 华东师范大学, 上海.]
[10]	Fazlioglu F, Chen L (2020). Introduced non-native mangroves express better growth performance than co-occurring native mangroves. Scientific Reports, 10, 3854. DOI: 10.1038/s41598-020-60454-z. PMID
[11]	Freschet GT, Valverde-Barrantes OJ, Tucker CM, Craine JM, McCormack ML, Violle C, Fort F, Blackwood CB, Urban-Mead KR, Iversen CM, Bonis A, Comas LH, Cornelissen JHC, Dong M, Guo DL, et al. (2017). Climate, soil and plant functional types as drivers of global fine-root trait variation. Journal of Ecology, 105, 1182-1196.
[12]	Gao JF (2006). Experimental Supervision of Plant Physiology. Higher Education Press, Beijing.
	[高俊凤 (2006). 植物生理学实验指导. 高等教育出版社, 北京.]
[13]	Gargallo-Garriga A, Sardans J, Pérez-Trujillo M, Oravec M, Urban O, Jentsch A, Kreyling J, Beierkuhnlein C, Parella T, Peñuelas J (2015). Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots. New Phytologist, 207, 591-603. DOI PMID
[14]	Grassein F, Lemauviel-Lavenant S, Lavorel S, Bahn M, Bardgett RD, Desclos-Theveniau M, Laîné P (2015). Relationships between functional traits and inorganic nitrogen acquisition among eight contrasting european grass species. Annals of Botany, 115, 107-115. DOI PMID
[15]	Hartzell JL, Jordan TE, Cornwell JC (2017). Phosphorus sequestration in sediments along the salinity gradients of chesapeake bay subestuaries. Estuaries and Coasts, 40, 607-1625.
[16]	Huang AM, Fang Y, Sun J, Li JL, Hu DD, Zhong QL, Cheng DL (2023). Fine root traits of Phyllostachys edulis at different altitudes in Wuyi Mountain. Acta Ecologica Sinica, 43, 398-407.
	[黄爱梅, 方毅, 孙俊, 李锦隆, 胡丹丹, 钟全林, 程栋梁 (2023). 武夷山不同海拔毛竹细根功能性状. 生态学报, 43, 398-407.]
[17]	Koerselman, Willem, Meuleman, Arthur FM, (1996). The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology, 33, 1441-1450.
[18]	Long YF, Tian MJ, Ye BB, Li MQ, Li DD, Yang F (2024). Comparative study on the community characteristics and population dynamics of Bruguiera sexangula at different tidal elevations in Dongzhaigang Nature Reserve. Plant Science Journal, 43, 72-81.
	[龙奕帆, 田梦洁, 叶冰冰, 李梦琦, 李大东, 杨帆 (2024). 东寨港自然保护区不同潮位下海莲群落特征及种群动态的比较研究. 植物科学学报, 43, 72-81.]
[19]	Lovelock CE, Feller IC, Adame MF, Reef R, Penrose HM, Wei Ll, Ball MC (2011). Intense storms and the delivery of materials that relieve nutrient limitations in mangroves of an arid zone estuary. Functional Plant Biology, 38, 514-522. DOI PMID
[20]	Magara F, Boury-Jamot B (2024). About statistical significance, and the lack thereof. Laboratory Animals, 58, 448-452.
[21]	Mueller P, Granse D, Nolte S, Weingartner M, Hoth S, Jensen K (2020). Unrecognized controls on microbial functioning in blue carbon ecosystems: the role of mineral enzyme stabilization and allochthonous substrate supply. Ecology and Evolution, 10, 998-1011. DOI PMID
[22]	Ortega-Morales BO, Chan-Bacab MJ, de la Rosa SDC, Camacho-Chab JC (2010). Valuable processes and products from marine intertidal microbial communities. Current Opinion in Biotechnology, 21, 346-352. DOI PMID
[23]	Pan F, Liang Y, Wang K, Zhang W (2018). Responses of fine root functional traits to soil nutrient limitations in a karst ecosystem of southwest China. Forests, 9, 743. DOI: 10.3390/f9120743.
[24]	Qi X, Chen L, Zhu J, Li Z, Lei H, Shen Q, Wu H, Ouyang S, Zeng Y, Hu Y, Xiang W (2022). Increase of soil phosphorus bioavailability with ectomycorrhizal tree dominance in subtropical secondary forests. Forest Ecology and Management, 521, 120435. DOI: 10.1016/j.foreco.2022.120435.
[25]	Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011). Phosphorus dynamics: from soil to plant. Plant Physiology, 156, 997-1005. DOI PMID
[26]	Song X, Wang Y, Lv X (2016). Responses of plant biomass, photosynthesis and lipid peroxidation to warming and precipitation change in two dominant species (Stipa grandis and Leymus chinensis) from north China grasslands. Ecology & Evolution, 6, 1871-1882.
[27]	Sun Y, Gu J, Zhuang H, Wang Z (2010). Effects of ectomycorrhizal colonization and nitrogen fertilization on morphology of root tips in a Larix gmelinii plantation in northeastern China. Ecological Research, 25, 95-302.
[28]	Tian CM, Liu JJ, Liang YM, Liu YH (1999). Rhizosphere microorganisms and soil bio-chemical properties at Huoditang forest region of the Qinling Mountains. Bulletin of Soil and Water Conservation, 19(2), 19-22.
	[田呈明, 刘建军, 梁英梅, 刘永华 (1999). 秦岭火地塘林区森林根际微生物及其土壤生化特性研究. 水土保持通报, 19(2), 19-22.]
[29]	Trumbore SE, Gaudinski JB (2003). The secret lives of roots. Science, 302, 1344-1345. PMID
[30]	Tully K, Gedan K, Epanchin-Niell R, Strong A, Bernhardt ES, Bendor T, Mitchell M, Kominoski J, Jordan TE, Neubauer SC (2019). The invisible flood: the chemistry, ecology, and social implications of coastal saltwater intrusion. Bioscience, 69, 368-378. DOI
[31]	Valverde Barrantes OJ, Smemo KA, Blackwood CB (2015). Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees. Functional Ecology, 29, 796-807.
[32]	Voesenek L, Colmer TD, Pierik R, Millenaar FF, Peeters A (2006). How plants cope with complete submergence. New Phytologist, 170, 213-226. PMID
[33]	Wahl S, Ryser P (2000). Root tissue structure is linked to ecological strategies of grasses. New Phytologist, 148, 459-471. DOI PMID
[34]	Wurzburger N, Wright SJ (2015). Fine-root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology, 96, 2137-2146. PMID
[35]	Ye Y, Tam NF, Wong YS, Lu CY (2003). Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environmental and Experimental Botany, 49, 209-221.
[36]	Yu M, Su W, Huang L, Parikh SJ, Tang C, Dahlgren RA, Xu J (2021). Bacterial community structure and putative nitrogen-cycling functional traits along a charosphere gradient under waterlogged conditions. Soil Biology & Biochemistry, 162, 08420. DOI: 10.1016/j.soilbio.2021.108420.
[37]	Zhou Y, Guan F, Li Z, Zheng Y, Zhou X, Zhang X (2022). Effects of tree species on moso bamboo (Phyllostachys edulis (Carriere) J. Houzeau) fine root morphology, biomass, and soil properties in bamboo-broadleaf mixed forests. Forests, 13, 1834. DOI: 10.3390/f13111834.
[38]	Zhou YH, Zhang ZH, Li J, Liu X, Hu G (2020). Ecological stoichiometric characteristics of carbon, nitrogen and phosphorus in leaves and soils of mangroves in Beilun estuary, Guangxi. Earth and Environment, 48, 58-65.
	[周元慧, 张忠华, 黎洁, 刘熊, 胡刚 (2020). 广西北仑河口红树植物叶片和土壤的碳氮磷生态化学计量特征. 地球与环境, 48, 58-65.]
[39]	Zhu D, Hui D, Huang Z, Qiao X, Tong S, Wang M, Yang Q, Yu S (2021). Comparative impact of light and neighbor effect on the growth of introduced species Sonneratia apetala and native mangrove species in China: implications for restoration. Restoration Ecology, 30, e13522. DOI: 10.1111/rec.13522.
[40]	Zhu ZL, Xing GX (2002). Nitrogen Cycle—A Natural Process that Sustains Life on Earth. Tsinghua University Press, Beijing.
	[朱兆良, 邢光熹 (2002). 氮循环: 维系地球生命生生不息的一个自然过程. 清华大学出版社, 北京.]
[41]	Zornoza R, Guerrero C, Mataix-Solera J, Arcenegui V, García-Orenes F, Mataix-Beneyto J (2006). Assessing air-drying and rewetting pre-treatment effect on some soil enzyme activities under mediterranean conditions. Soil Biology & Biochemistry, 38, 2125-2134.