Absorptive root anatomical traits of 26 tropical and subtropical fern species

doi:10.17521/cjpe.2021.0328

Abstract

Abstract:

Aims The plant absorptive roots function to absorb water and nutrients. Investigations of anatomical traits of the roots are to understanding environmental adaptations of plant species. Ferns in tropical and subtropical regions are abundant and of important ecological and economic values. However, the anatomical traits of the absorptive roots of ferns are not fully comprehended.

Methods We investigated anatomical traits of absorptive roots for 26 fern species from four typical tropical/ subtropical forests by analyzing inter-specific differences in the traits across the species to explain the influence of phylogeny and climate. In addition, we compiled relevant root traits of subtropical angiosperm tree species and temperate fern species from literature to explore the trait differences among the groups.

Important findings (1) We found significant differences in eight root anatomical traits among the 26 fern species, with coefficient of variation ranging from 20.61% to 41.75%. (2) Root traits showed no significant phylogeny signal except in cortex thickness (CT), indicating little affection from phylogeny. However, climate might exert significant impacts on root traits, i.e., root diameter (RD) and CT significantly increased with decreasing precipitation of the driest month (quarter). (3) As RD decreases, the subtropical angiosperm woody plants showed a significant decrease in the ratio of CT to stele diameter (SD), but fern had an opposite pattern. Compared to temperate ferns, the tropical and subtropical ferns had higher RD, CT, and tracheid diameter (TD).

Key words: absorptive root, climate, phylogeny, root diameter, cortex thickness, stele diameter

XIANG Wei, HUANG Dong-Liu, ZHU Shi-Dan. Absorptive root anatomical traits of 26 tropical and subtropical fern species[J]. Chin J Plant Ecol, 2022, 46(5): 593-601.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2021.0328

https://www.plant-ecology.com/EN/Y2022/V46/I5/593

Figures/Tables 5

References 42

[1]	Brundrett MC, Tedersoo L (2018). Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist, 220, 1108-1115. DOI PMID
[2]	Carlquist S, Schneider EL (2001). Vessels in ferns: structural, ecological, and evolutionary significance. American Journal of Botany, 88, 1-13. PMID
[3]	Chang WJ, Guo DL (2008). Variation in root diameter among 45 common tree species in temperate, subtropical and tropical forests in China. Journal of Plant Ecology (Chinese Version), 32, 1248-1257.
	[ 常文静, 郭大立 (2008). 中国温带、亚热带和热带森林45个常见树种细根直径变异. 植物生态学报, 32, 1248-1257.] DOI
[4]	Chen WL, Zeng H, Eissenstat DM, Guo DL (2013). Variation of first-order root traits across climatic gradients and evolutionary trends in geological time. Global Ecology and Biogeography, 22, 846-856. DOI URL
[5]	Chen X, Chen DQ, Liu HK, Zhao CZ, Zhao WT, Dong Z, Zhang YT, Wang YP (2021). Responses of fine root anatomical traits of eleven tree species to the soil conditions in coastal saline-alkali stand sites of the Yellow River delta. Acta Ecologica Sinica, 41, 4150-4159.
	[ 陈旭, 陈冬倩, 刘洪凯, 赵春周, 赵文太, 董智, 张永涛, 王延平 (2021). 黄河三角洲滨海盐碱地11个造林树种细根解剖性状对土壤条件的响应. 生态学报, 41, 4150-4159.]
[6]	Comas LH, Mueller KE, Taylor LL, Midford PE, Callahan HS, Beerling DJ (2012). Evolutionary patterns and biogeochemical significance of angiosperm root traits. International Journal of Plant Sciences, 173, 584-595. DOI URL
[7]	Ding DJ, Liao BW, Guan W, Xiong YM, Li M, Chen YJ (2016). Evaluation on service value of coastal wetland ecosystem in Dongzhai harbor mangrove nature reserve. Ecological Science, 35, 182-190.
	[ 丁冬静, 廖宝文, 管伟, 熊燕梅, 李玫, 陈玉军 (2016). 东寨港红树林自然保护区滨海湿地生态系统服务价值评估. 生态科学, 35, 182-190.]
[8]	Ding JX, Kong DL, Zhang ZL, Cai Q, Xiao J, Liu Q, Yin HJ (2020). Climate and soil nutrients differentially drive multidimensional fine root traits in ectomycorrhizal- dominated alpine coniferous forests. Journal of Ecology, 108, 2544-2556. DOI URL
[9]	Dong XY, Wang HF, Gu JC, Wang Y, Wang ZQ (2015). Root morphology, histology and chemistry of nine fern species (Pteridophyta) in a temperate forest. Plant and Soil, 393, 215-227. DOI URL
[10]	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. DOI URL
[11]	Gao J, Zhou MY, Shao JJ, Zhou GY, Liu RQ, Zhou LY, Liu HY, He YH, Chen Y, Zhou XH (2021). Fine root trait-function relationships affected by mycorrhizal type and climate. Geoderma, 394, 115011. DOI: 10.1016/j.geoderma.2021.115011. DOI URL
[12]	Gu JC, Xu Y, Dong XY, Wang HF, Wang ZQ (2014). Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species. Tree Physiology, 34, 415-425. DOI URL
[13]	Guo DL, Xia MX, Wei X, Chang WJ, Liu Y, Wang ZQ (2008). Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytologist, 180, 673-683. DOI URL
[14]	He TP, Tan WF, Wen YG, Zhao ZH, Wen XF, Huang ZH, Men YY (2007). Diversity of rare and endangered plants in Shiwandashan Mountain National Natural Reserve. Journal of Guangxi Agricultural and Biological Science, 26, 125-131.
	[ 和太平, 谭伟福, 温远光, 赵泽红, 文祥凤, 黄志辉, 门媛媛 (2007). 十万大山国家级自然保护区珍稀濒危植物的多样性. 广西农业生物科学, 26, 125-131.]
[15]	Huang BR, Eissenstat DM (2000). Linking hydraulic conductivity to anatomy in plants that vary in specific root length. Journal of the American Society for Horticultural Science, 125, 260-264. DOI URL
[16]	Huang Y, Wang B, Yan LM, Wei XM, Lin L, Wei JW, Li HJ (2020). Observations on the spatial and temporal patterns of amphibian diversity in Damingshan, Guangxi. Journal of Ecology and Rural Environment, 36, 968-974.
	[ 黄勇, 王波, 颜琳妙, 韦筱媚, 林莉, 韦建威, 李华坚 (2020). 广西大明山两栖动物多样性时空格局观测. 生态与农村环境学报, 36, 968-974.]
[17]	Jin Y, Qian H (2019). V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography, 42, 1353-1359. DOI
[18]	Kong DL, Ma CG, Zhang Q, Li L, Chen XY, Zeng H, Guo DL (2014). Leading dimensions in absorptive root trait variation across 96 subtropical forest species. New Phytologist, 203, 863-872. DOI URL
[19]	Kong DL, Wang JJ, Valverde-Barrantes OJ, Kardol P (2021). A framework to assess the carbon supply-consumption balance in plant roots. New Phytologist, 229, 659-664. DOI URL
[20]	Kong DL, Wang JJ, Wu HF, Valverde-Barrantes OJ, Wang RL, Zeng H, Kardol P, Zhang HY, Feng YL (2019). Nonlinearity of root trait relationships and the root economics spectrum. Nature Communications, 10, 2203. DOI URL
[21]	Kong DL, Wang JJ, Zeng H, Liu MZ, Miao Y, Wu HF, Kardol P (2017). The nutrient absorption-transportation hypothesis: optimizing structural traits in absorptive roots. New Phytologist, 213, 1569-1572. DOI URL
[22]	Li HB, Liu BT, McCormack ML, Ma ZQ, Guo DL (2017). Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient. New Phytologist, 216, 1140-1150. DOI URL
[23]	Ma ZQ, Guo DL, Xu XL, Lu MZ, Bardgett RD, Eissenstat DM, McCormack ML, Hedin LO (2018). Evolutionary history resolves global organization of root functional traits. Nature, 555, 94-97. DOI URL
[24]	McAdam SAM, Brodribb TJ (2012). Stomatal innovation and the rise of seed plants. Ecology Letters, 15, 1-8. DOI PMID
[25]	McCormack ML, Kaproth MA, Cavender-Bares J, Carlson E, Hipp AL, Han Y, Kennedy PG (2020). Climate and phylogenetic history structure morphological and architectural trait variation among fine-root orders. New Phytologist, 228, 1824-1834. DOI URL
[26]	Page CN (2002). Ecological strategies in fern evolution: a neopteridological overview. Review of Palaeobotany and Palynology, 119, 1-33.
[27]	Paradis E, Claude J, Strimmer K (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289-290. DOI URL
[28]	Pregitzer KS (2002). Fine roots of trees—A new perspective. New Phytologist, 154, 267-270. DOI PMID
[29]	Rueden CT, Hiner MC, Eliceiri KW (2016). ImageJ: image analysis interoperability for the next generation of biological image data. Microscopy and Microanalysis, 22, 2066-2067. DOI URL
[30]	Tyree MT, Zimmermann MH (2002). Xylem Structure and the Ascent of Sap. 2nd ed. Springer, Berlin.
[31]	Valverde-Barrantes OJ, Freschet GT, Roumet C, Blackwood CB (2017). A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine-root tissues in seed plants. New Phytologist, 215, 1562-1573. DOI PMID
[32]	Valverde-Barrantes OJ, Maherali H, Baraloto C, Blackwood CB (2020). Independent evolutionary changes in fine-root traits among main clades during the diversification of seed plants. New Phytologist, 228, 541-553. DOI URL
[33]	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. DOI URL
[34]	Wang HF, Wang ZQ, Dong XY (2019). Anatomical structures of fine roots of 91 vascular plant species from four groups in a temperate forest in Northeast China. PLOS ONE, 14, e0215126. DOI: 10.1371/journal.pone.0215126. DOI URL
[35]	Wu WX (2019). Plant Diversity, Soil Microbial Diversity and Ecosystem Multifunction in Pure and Mixed Plantations. PhD dissertation, Guangxi University, Nanning.
	[ 巫文香 (2019). 人工纯林和混交林植物、土壤微生物多样性与生态系统多功能性. 博士学位论文, 广西大学, 南宁.]
[36]	Yang L, Huang YH, Lima LV, Sun ZY, Liu MJ, Wang J, Liu N, Ren H (2021). Rethinking the ecosystem functions of Dicranopteris, a widespread genus of ferns. Frontiers in Plant Science, 11, 581513. DOI: 10.3389/fpls.2020.581513. DOI URL
[37]	You YM, Xu JY, Cai DX, Liu SR, Zhu HG, Wen YG (2016). Environmental factors affecting plant species diversity of understory plant communities in a Castanopsis hystrix plantation chronosequence in Pingxiang, Guangxi, China. Acta Ecologica Sinica, 36, 164-172.
	[ 尤业明, 徐佳玉, 蔡道雄, 刘世荣, 朱宏光, 温远光 (2016). 广西凭祥不同年龄红椎林林下植物物种多样性及其环境解释. 生态学报, 36, 164-172.]
[38]	Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB, Royer DL, Soltis DE, Stevens PF, Westoby M, Wright IJ, et al. (2014). Three keys to the radiation of angiosperms into freezing environments. Nature, 506, 89-92. DOI URL
[39]	Zhang KM, Shen Y, Zhou XL, Fang YM (2019). Analysis of fern research article trends across the Web of Science in the 21st century. Biodiversity Science, 27, 1245-1250. DOI URL
	[ 张开梅, 沈羽, 周晓丽, 方炎明 (2019). 21世纪以来蕨类植物研究论文的发表情况: 基于Web of Science的数据统计. 生物多样性, 27, 1245-1250.] DOI
[40]	Zhang XC (2012). Lycophytes and Ferns of China. Peking University Press, Beijing. 711.
	[ 张宪春 (2012). 中国石松类和蕨类植物. 北京大学出版社, 北京. 711.]
[41]	Zhou M, Bai WM, Li QM, Guo YM, Zhang WH (2021). Root anatomical traits determined leaf-level physiology and responses to precipitation change of herbaceous species in a temperate steppe. New Phytologist, 229, 1481-1491. DOI URL
[42]	Zhu SD, Li RH, Song J, He PC, Liu H, Berninger F, Ye Q (2016). Different leaf cost-benefit strategies of ferns distributed in contrasting light habitats of sub-tropical forests. Annals of Botany, 117, 497-506. DOI URL

物种 Species	缩写 Abbreviation	科 Family	地点 Site	海拔¹⁾ Altitude¹⁾ (m)
无腺毛蕨 Cyclosorus procurrens	Cp	金星蕨科 Thelypteridaceae	大明山 Damingshan	200-1 900
披针贯众 Cyrtomium devexiscapulae	Cd	鳞毛蕨科 Dryopteridaceae	大明山 Damingshan	380-700
薄叶双盖蕨 Diplazium pinfaense	Dp	蹄盖蕨科 Athyriaceae	大明山 Damingshan	400-1 800
双扇蕨 Dipteris conjugata	Dc	双扇蕨科 Dipteridaceae	大明山 Damingshan	1 400-2 100
栗蕨 Histiopteris incisa	Hi	碗蕨科 Dennstaedtiaceae	大明山 Damingshan	500-1 900
华南鳞盖蕨 Microlepia hancei	Mh	碗蕨科 Dennstaedtiaceae	大明山 Damingshan	300-800
斜方鳞盖蕨 Microlepia rhomboidea	Mr	碗蕨科 Dennstaedtiaceae	大明山 Damingshan	<1 000
乌蕨 Odontosoria chinensis	Oc	鳞始蕨科 Lindsaeaceae	大明山 Damingshan	200-1 900
紫萁 Osmunda japonica	Oj	紫萁科 Osmundaceae	大明山 Damingshan	<2 300
钝角金星蕨 Parathelypteris angulariloba	Pa	金星蕨科 Thelypteridaceae	大明山 Damingshan	500-800
瘤足蕨 Plagiogyria adnata	Pla	瘤足蕨科 Plagiogyriaceae	大明山 Damingshan	500-2 000
华中瘤足蕨 Plagiogyria euphlebia	Ple	瘤足蕨科 Plagiogyriaceae	大明山 Damingshan	500-1 200
井栏边草 Pteris multifida	Pm	凤尾蕨科 Pteridaceae	大明山 Damingshan	<1 000
半边旗 Pteris semipinnata	Ps	凤尾蕨科 Pteridaceae	大明山 Damingshan	<850
蜈蚣凤尾蕨 Pteris vittata	Pv	凤尾蕨科 Pteridaceae	大明山 Damingshan	<2 000
卤蕨 Acrostichum aureum	Aa	凤尾蕨科 Pteridaceae	东寨港 Dongzhaigang	-
桫椤 Alsophila spinulosa	As	桫椤科 Cyatheaceae	伏波 Fubo	260-1 600
乌毛蕨 Blechnum orientale	Bo	乌毛蕨科 Blechnaceae	伏波 Fubo	300-800
金毛狗 Cibotium barometz	Cb	金毛狗科 Cibotiaceae	伏波 Fubo	150-1 800
长叶实蕨 Bolbitis heteroclita	Bh	鳞毛蕨科 Dryopteridaceae	十万大山 Shiwandashan	50-1 500
芒萁 Dicranopteris pedata	Dip	里白科 Gleicheniaceae	十万大山 Shiwandashan	1 880
中华里白 Diplopterygium chinense	Dic	里白科 Gleicheniaceae	十万大山 Shiwandashan	800-1 650
肾蕨 Nephrolepis cordifolia	Nc	肾蕨科 Nephrolepidaceae	十万大山 Shiwandashan	30-1 500
华南紫萁 Osmunda vachellii	Ov	紫萁科 Osmundaceae	十万大山 Shiwandashan	<700
红色新月蕨 Pronephrium lakhimpurense	Pl	金星蕨科 Thelypteridaceae	十万大山 Shiwandashan	300-1 550
条裂叉蕨 Tectaria phaeocaulis	Tp	叉蕨科 Tectariaceae	十万大山 Shiwandashan	400-500

物种 Species	缩写 Abbreviation	科 Family	地点 Site	海拔¹⁾ Altitude¹⁾ (m)
无腺毛蕨 Cyclosorus procurrens	Cp	金星蕨科 Thelypteridaceae	大明山 Damingshan	200-1 900
披针贯众 Cyrtomium devexiscapulae	Cd	鳞毛蕨科 Dryopteridaceae	大明山 Damingshan	380-700
薄叶双盖蕨 Diplazium pinfaense	Dp	蹄盖蕨科 Athyriaceae	大明山 Damingshan	400-1 800
双扇蕨 Dipteris conjugata	Dc	双扇蕨科 Dipteridaceae	大明山 Damingshan	1 400-2 100
栗蕨 Histiopteris incisa	Hi	碗蕨科 Dennstaedtiaceae	大明山 Damingshan	500-1 900
华南鳞盖蕨 Microlepia hancei	Mh	碗蕨科 Dennstaedtiaceae	大明山 Damingshan	300-800
斜方鳞盖蕨 Microlepia rhomboidea	Mr	碗蕨科 Dennstaedtiaceae	大明山 Damingshan	<1 000
乌蕨 Odontosoria chinensis	Oc	鳞始蕨科 Lindsaeaceae	大明山 Damingshan	200-1 900
紫萁 Osmunda japonica	Oj	紫萁科 Osmundaceae	大明山 Damingshan	<2 300
钝角金星蕨 Parathelypteris angulariloba	Pa	金星蕨科 Thelypteridaceae	大明山 Damingshan	500-800
瘤足蕨 Plagiogyria adnata	Pla	瘤足蕨科 Plagiogyriaceae	大明山 Damingshan	500-2 000
华中瘤足蕨 Plagiogyria euphlebia	Ple	瘤足蕨科 Plagiogyriaceae	大明山 Damingshan	500-1 200
井栏边草 Pteris multifida	Pm	凤尾蕨科 Pteridaceae	大明山 Damingshan	<1 000
半边旗 Pteris semipinnata	Ps	凤尾蕨科 Pteridaceae	大明山 Damingshan	<850
蜈蚣凤尾蕨 Pteris vittata	Pv	凤尾蕨科 Pteridaceae	大明山 Damingshan	<2 000
卤蕨 Acrostichum aureum	Aa	凤尾蕨科 Pteridaceae	东寨港 Dongzhaigang	-
桫椤 Alsophila spinulosa	As	桫椤科 Cyatheaceae	伏波 Fubo	260-1 600
乌毛蕨 Blechnum orientale	Bo	乌毛蕨科 Blechnaceae	伏波 Fubo	300-800
金毛狗 Cibotium barometz	Cb	金毛狗科 Cibotiaceae	伏波 Fubo	150-1 800
长叶实蕨 Bolbitis heteroclita	Bh	鳞毛蕨科 Dryopteridaceae	十万大山 Shiwandashan	50-1 500
芒萁 Dicranopteris pedata	Dip	里白科 Gleicheniaceae	十万大山 Shiwandashan	1 880
中华里白 Diplopterygium chinense	Dic	里白科 Gleicheniaceae	十万大山 Shiwandashan	800-1 650
肾蕨 Nephrolepis cordifolia	Nc	肾蕨科 Nephrolepidaceae	十万大山 Shiwandashan	30-1 500
华南紫萁 Osmunda vachellii	Ov	紫萁科 Osmundaceae	十万大山 Shiwandashan	<700
红色新月蕨 Pronephrium lakhimpurense	Pl	金星蕨科 Thelypteridaceae	十万大山 Shiwandashan	300-1 550
条裂叉蕨 Tectaria phaeocaulis	Tp	叉蕨科 Tectariaceae	十万大山 Shiwandashan	400-500

根解剖特征 Root anatomical trait	Blomberg’s K	p
根直径 Root diameter	0.44	0.18
中柱直径 Stele diameter	0.32	0.62
皮层厚度 Cortex thickness	0.60	0.03
中柱直径/根直径 Stele diameter/root diameter	0.43	0.22
皮层厚度/中柱直径 Cortex thickness/stele diameter	0.38	0.41
木质部面积比 Xylem area ratio	0.28	0.82
管胞数量 Tracheid number	0.42	0.25
管胞直径 Tracheid diameter	0.34	0.52

根解剖特征 Root anatomical trait	Blomberg’s K	p
根直径 Root diameter	0.44	0.18
中柱直径 Stele diameter	0.32	0.62
皮层厚度 Cortex thickness	0.60	0.03
中柱直径/根直径 Stele diameter/root diameter	0.43	0.22
皮层厚度/中柱直径 Cortex thickness/stele diameter	0.38	0.41
木质部面积比 Xylem area ratio	0.28	0.82
管胞数量 Tracheid number	0.42	0.25
管胞直径 Tracheid diameter	0.34	0.52