Coordination and differences in root-leaf functional traits between tree species and understory shrub species in a subtropical natural evergreen broadleaf forest

doi:10.17521/cjpe.2024.0140

Abstract

Abstract:

Aims Studying the coordination and differences in the functional traits of leaves and fine roots can help better understand the ecological strategies of plants from a whole-plant perspective.

Methods In this study, we measured and analyzed the leaf and root traits of 20 woody species (10 trees and 10 shrubs) from the natural evergreen broadleaf forest in Wanmulin Nature Reserve, Fujian Province. We explored the coordination of root and leaf functional traits and differences in survival strategies between tree and understory shrub species in this subtropical natural evergreen broadleaf forest.

Important findings We found a strong correlation between the leaf nitrogen concentration and root nitrogen concentration, but this was observed only for similar traits of leaf and first-order root, irrespective of phylogeny. In the studied forest, there was a leaf economics spectrum and a leaf tissue density-leaf thickness variance axis, shaped by the measured leaf traits. For first-order root, we observed a cooperative axis (represented by the negative correlation between root diameter and specific root length) and a root economics spectrum (represented by the negative correlation between root nitrogen concentration and root tissue density). There was no significant correlation between root and leaf economic spectra. Significant differences were found between tree and shrub species only along the root collaboration axis, with trees having larger root diameters and shrubs having higher specific root lengths. In addition, the specific leaf area of shrub species was significantly larger than that of tree species. The results indicated that leaf and root traits are integrated into a complex relationship, with tree and shrub species adopting different aboveground and belowground strategies to adapt to the habitat heterogeneity in the studied area. Our results expand the understanding of the coordination between root and leaf traits at a local scale, and provide deeper insights into the ecological processes and species coexistence mechanisms within the community.

Key words: plant functional trait, leaf economics spectrum, root economics space, aboveground-belowground linkages, functional trade-offs, first-order root, leaf

DU Ying-Jie, FAN Ai-Lian, WANG Xue, YAN Xiao-Jun, CHEN Ting-Ting, JIA Lin-Qiao, JIANG Qi, CHEN Guang-Shui. Coordination and differences in root-leaf functional traits between tree species and understory shrub species in a subtropical natural evergreen broadleaf forest[J]. Chin J Plant Ecol, 2025, 49(4): 585-595.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.plant-ecology.com/EN/10.17521/cjpe.2024.0140

https://www.plant-ecology.com/EN/Y2025/V49/I4/585

Figures/Tables 7

References 53

[1]	Ackerly D, Knight C, Weiss S, Barton K, Starmer K (2002). Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia, 130, 449-457. DOI PMID
[2]	Bardgett RD, Mommer L, de Vries FT (2014). Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 692-699.
[3]	Bergmann J, Weigelt A, van Der Plas F, Laughlin DC, Kuyper TW, Guerrero-Ramirez NR, Valverde-Barrantes OJ, Bruelheide H, Freschet GT, Iversen CM, Kattge J, McCormack ML, Meier IC, Rillig MC, Roumet C, et al. (2020). The fungal collaboration gradient dominates the root economics space in plants. Science Advances, 6, eaba3756. DOI: 10.1126/sciadv.aba3756.
[4]	Blomberg SP, Garland Jr T, Ives AR (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution, 57, 717-745. DOI PMID
[5]	Chen WL, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM (2016). Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proceedings of the National Academy of Sciences of the United States of America, 113, 8741-8746. DOI PMID
[6]	Chen YT, Xu ZZ (2014). Review on research of leaf economics spectrum. Chinese Journal of Plant Ecology, 38, 1135-1153.
	[陈莹婷, 许振柱 (2014). 植物叶经济谱的研究进展. 植物生态学报, 38, 1135-1153.] DOI
[7]	Cheng JH, Chu PF, Chen DM, Bai YF (2016). Functional correlations between specific leaf area and specific root length along a regional environmental gradient in Inner Mongolia grasslands. Functional Ecology, 30, 985-997.
[8]	Craine JM, Lee WG, Bond WJ, Williams RJ, Johnson LC (2005). Environmental constraints on a global relationship among leaf and root traits of grasses. Ecology, 86, 12-19.
[9]	Erktan A, Roumet C, Munoz F (2023). Dissecting fine root diameter distribution at the community level captures root morphological diversity. Oikos, 2023, e08907. DOI: 10.1111/oik.08907.
[10]	Evans JR, Poorter H (2001). Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment, 24, 755-767.
[11]	Freschet GT, Cornelissen JHC, Aerts R (2010). Evidence of the ‘plant economics spectrum’ in a subarctic flora. Journal of Ecology, 98, 362-373.
[12]	Freschet GT, Violle C, Bourget MY, Scherer-Lorenzen M, Fort F (2018). Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress. New Phytologist, 219, 1338-1352. DOI PMID
[13]	Geng Y, Wang L, Jin DM, Liu HY, He JS (2014). Alpine climate alters the relationships between leaf and root morphological traits but not chemical traits. Oecologia, 175, 445-455. DOI PMID
[14]	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 PMID
[15]	Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011). Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. Journal of Ecology, 99, 954-963.
[16]	Hu YK, Pan X, Yang XJ, Liu GF, Liu XY, Song YB, Zhang MY, Cui LJ, Dong M (2019). Is there coordination of leaf and fine root traits at local scales? A test in temperate forest swamps. Ecology and Evolution, 9, 8714-8723.
[17]	Jin N, Yu XC, Dong JL, Duan MC, Mo YX, Feng LY, Bai R, Zhao JL, Song J, Dossa GGO, Lu HZ (2024). Vertical variation in leaf functional traits of Parashorea chinensis with different canopy layers. Frontiers in Plant Science, 15, 1335524. DOI: 10.3389/fpls.2024.1335524.
[18]	Joswig JS, Wirth C, Schuman MC, Kattge J, Reu B, Wright IJ, Sippel SD, Rüger N, Richter R, Schaepman ME, van Bodegom PM, Cornelissen JHC, Díaz S, Hattingh WN, Kramer K, et al. (2022). Climatic and soil factors explain the two-dimensional spectrum of global plant trait variation. Nature Ecology & Evolution, 6, 36-50.
[19]	Kandlikar GS, Kleinhesselink AR, Kraft NJB (2022). Functional traits predict species responses to environmental variation in a California grassland annual plant community. Journal of Ecology, 110, 833-844.
[20]	Kitajima K, Poorter L (2010). Tissue-level leaf toughness, but not Lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist, 186, 708-721. DOI PMID
[21]	Kleyer M, Trinogga J, Cebrián-Piqueras MA, Trenkamp A, Fløjgaard C, Ejrnæs R, Bouma TJ, Minden V, Maier M, Mantilla-Contreras J, Albach DC, Blasius B (2019). Trait correlation network analysis identifies biomass allocation traits and stem specific length as hub traits in herbaceous perennial plants. Journal of Ecology, 107, 829-842.
[22]	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 PMID
[23]	Kong DL, Wang JJ, Kardol P, Wu HF, Zeng H, Deng XB, Deng Y (2016). Economic strategies of plant absorptive roots vary with root diameter. Biogeosciences, 13, 415-424.
[24]	Kramer-Walter KR, Bellingham PJ, Millar TR, Smissen RD, Richardson SJ, Laughlin DC (2016). Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. Journal of Ecology, 104, 1299-1310.
[25]	Li YP, Ni YL, Xu H, Lian JY, Ye WH (2021). Relationship between variation of plant functional traits and individual growth at different vertical layers in a subtropical evergreen broad-leaved forest of Dinghushan. Biodiversity Science, 29, 1186-1197.
	[李艳朋, 倪云龙, 许涵, 练琚愉, 叶万辉 (2021). 鼎湖山南亚热带常绿阔叶林植物功能性状变异与不同垂直层次个体生长的关联. 生物多样性, 29, 1186-1197.] DOI
[26]	Liu GF, Freschet GT, Pan X, Cornelissen JHC, Li Y, Dong M (2010). Coordinated variation in leaf and root traits across multiple spatial scales in Chinese semi-arid and arid ecosystems. New Phytologist, 188, 543-553. DOI PMID
[27]	Luo XZ, Keenan TF, Chen JM, Croft H, Colin Prentice I, Smith NG, Walker AP, Wang H, Wang R, Xu C, Zhang Y (2021). Global variation in the fraction of leaf nitrogen allocated to photosynthesis. Nature Communications, 12, 4866. DOI: 10.1038/s41467-021-25163-9.
[28]	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.
[29]	Makita N, Hirano Y, Yamanaka T, Yoshimura K, Kosugi Y (2012). Ectomycorrhizal-fungal colonization induces physio-morphological changes in Quercus serrata leaves and roots. Journal of Plant Nutrition and Soil Science, 175, 900-906.
[30]	McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, et al. (2015). Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytologist, 207, 505-518. DOI PMID
[31]	Niinemets Ü (2001). Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology, 82, 453-469.
[32]	Niinemets Ü, Ellsworth DS, Lukjanova A, Tobias M (2001). Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. Tree Physiology, 21, 1231-1244. PMID
[33]	Ntawuhiganayo EB, Uwizeye FK, Zibera E, Dusenge ME, Ziegler C, Ntirugulirwa B, Nsabimana D, Wallin G, Uddling J (2020). Traits controlling shade tolerance in tropical montane trees. Tree Physiology, 40, 183-197.
[34]	Pagel M (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877-884.
[35]	Poorter H, Lambers H, Evans JR (2014). Trait correlation networks: a whole-plant perspective on the recently criticized leaf economic spectrum. New Phytologist, 201, 378-382. DOI PMID
[36]	Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009). Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist, 182, 565-588.
[37]	Silva JLA, Souza AF, Caliman A, Voigt EL, Lichston JE (2018). Weak whole-plant trait coordination in a seasonally dry South American stressful environment. Ecology and Evolution, 8, 4-12. DOI PMID
[38]	Silvertown J (2004). Plant coexistence and the niche. Trends in Ecology & Evolution, 19, 605-611.
[39]	Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005). Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytologist, 167, 493-508. PMID
[40]	Valladares F, Martinez-ferri E, Balaguer L, Perez-corona E, Manrique E (2000). Low leaf-level response to light and nutrients in Mediterranean evergreen oaks: a conservative resource-use strategy? New Phytologist, 148, 79-91. DOI PMID
[41]	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
[42]	Valverde-Barrantes OJ, Horning AL, Smemo KA, Blackwood CB (2016). Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. Plant and Soil, 404, 1-12.
[43]	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.
[44]	Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J (2012). The return of the variance: intraspecific variability in community ecology. Trends in Ecology & Evolution, 27, 244-252.
[45]	Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007). Let the concept of trait be functional! Oikos, 116, 882-892.
[46]	Wang RL, Wang QF, Zhao N, Yu GR, He NP (2017). Complex trait relationships between leaves and absorptive roots: coordination in tissue N concentration but divergence in morphology. Ecology and Evolution, 7, 2697-2705. DOI PMID
[47]	Wang ZY, Chen XP, Cheng Y, Wang MT, Zhong QL, Li M, Cheng DL (2021). Leaf and fine root economics spectrum across 49 woody plant species in Wuyi Mountains. Chinese Journal of Plant Ecology, 45, 242-252.
	[王钊颖, 陈晓萍, 程英, 王满堂, 钟全林, 李曼, 程栋梁 (2021). 武夷山49种木本植物叶片与细根经济谱. 植物生态学报, 45, 242-252.]
[48]	Weemstra M, Freschet GT, Stokes A, Roumet C (2020). Patterns in intraspecific variation in root traits are species-specific along an elevation gradient. Functional Ecology, 35, 342-356.
[49]	Weemstra M, Mommer L, Visser EJW, van Ruijven J, Kuyper TW, Mohren GMJ, Sterck FJ (2016). Towards a multidimensional root trait framework: a tree root review. New Phytologist, 211, 1159-1169. DOI PMID
[50]	Weigelt A, Mommer L, Andraczek K, Iversen CM, Bergmann J, Bruelheide H, Fan Y, Freschet GT, Guerrero-Ramírez NR, Kattge J, Kuyper TW, Laughlin DC, Meier IC, van der Plas F, Poorter H, et al. (2021). An integrated framework of plant form and function: the belowground perspective. New Phytologist, 232, 42-59. DOI PMID
[51]	Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, et al. (2004). The worldwide leaf economics spectrum. Nature, 428, 821-827.
[52]	Yang YY, Xiao CC, Wu XM, Long WX, Feng G, Liu GY (2021). Differing trade-off patterns of tree vegetative organs in a tropical cloud forest. Frontiers in Plant Science, 12, 680379. DOI: 10.3389/fpls.2021.680379.
[53]	Zhou T, Cui YC, Ye YY, Zhao WJ, Hou YJ, Wu P, Ding FJ (2022). Leaf functional traits of typical karst forest plants under different niches. Journal of Central South University of Forestry & Technology, 42(10), 129-140.
	[周汀, 崔迎春, 叶雨艳, 赵文君, 侯贻菊, 吴鹏, 丁访军 (2022). 不同小生境下典型喀斯特森林植物叶片功能性状特征. 中南林业科技大学学报, 42(10), 129-140.]

物种 Species	科 Family	生长型 Growth form
米槠 Castanopsis carlesii	壳斗科 Fagaceae	乔木 Tree
青冈 Cyclobalanopsis glauca	壳斗科 Fagaceae	乔木 Tree
罗浮锥 Castanopsis faberi	壳斗科 Fagaceae	乔木 Tree
苦槠 Castanopsis sclerophylla	壳斗科 Fagaceae	乔木 Tree
观光木 Michelia odora	木兰科 Magnoliaceae	乔木 Tree
沉水樟 Cinnamomum micranthum	樟科 Lauraceae	乔木 Tree
刨花润楠 Machilus pauhoi	樟科 Lauraceae	乔木 Tree
天竺桂 Cinnamomum japonicum	樟科 Lauraceae	乔木 Tree
细柄蕈树 Altingia gracilipes	蕈树科 Altingiaceae	乔木 Tree
木荷 Schima superba	山茶科 Theaceae	乔木 Tree
杜茎山 Maesa japonica	报春花科 Primulaceae	灌木 Shrub
罗浮冬青 Ilex tutcheri	冬青科 Aquifoliaceae	灌木 Shrub
三花冬青 Ilex triflora	冬青科 Aquifoliaceae	灌木 Shrub
檵木 Loropetalum chinense	金缕梅科 Hamamelidaceae	灌木 Shrub
尖叶假蚊母树 Distyliopsis dunnii	金缕梅科 Hamamelidaceae	灌木 Shrub
狗骨柴 Diplospora dubia	茜草科 Rubiaceae	灌木 Shrub
娥眉鼠刺 Itea omeiensis	鼠刺科 Iteaceae	灌木 Shrub
华幌伞枫 Heteropanax chinensis	五加科 Araliaceae	灌木 Shrub
细枝柃 Eurya loquaiana	五列木科 Pentaphylacaceae	灌木 Shrub
杨桐 Adinandra milletii	五列木科 Pentaphylacaceae	灌木 Shrub

物种 Species	科 Family	生长型 Growth form
米槠 Castanopsis carlesii	壳斗科 Fagaceae	乔木 Tree
青冈 Cyclobalanopsis glauca	壳斗科 Fagaceae	乔木 Tree
罗浮锥 Castanopsis faberi	壳斗科 Fagaceae	乔木 Tree
苦槠 Castanopsis sclerophylla	壳斗科 Fagaceae	乔木 Tree
观光木 Michelia odora	木兰科 Magnoliaceae	乔木 Tree
沉水樟 Cinnamomum micranthum	樟科 Lauraceae	乔木 Tree
刨花润楠 Machilus pauhoi	樟科 Lauraceae	乔木 Tree
天竺桂 Cinnamomum japonicum	樟科 Lauraceae	乔木 Tree
细柄蕈树 Altingia gracilipes	蕈树科 Altingiaceae	乔木 Tree
木荷 Schima superba	山茶科 Theaceae	乔木 Tree
杜茎山 Maesa japonica	报春花科 Primulaceae	灌木 Shrub
罗浮冬青 Ilex tutcheri	冬青科 Aquifoliaceae	灌木 Shrub
三花冬青 Ilex triflora	冬青科 Aquifoliaceae	灌木 Shrub
檵木 Loropetalum chinense	金缕梅科 Hamamelidaceae	灌木 Shrub
尖叶假蚊母树 Distyliopsis dunnii	金缕梅科 Hamamelidaceae	灌木 Shrub
狗骨柴 Diplospora dubia	茜草科 Rubiaceae	灌木 Shrub
娥眉鼠刺 Itea omeiensis	鼠刺科 Iteaceae	灌木 Shrub
华幌伞枫 Heteropanax chinensis	五加科 Araliaceae	灌木 Shrub
细枝柃 Eurya loquaiana	五列木科 Pentaphylacaceae	灌木 Shrub
杨桐 Adinandra milletii	五列木科 Pentaphylacaceae	灌木 Shrub

叶性状 Leaf trait	K	λ	根性状 Root trait	K	λ
叶厚度 Leaf thickness	0.11	0.00	根直径 Root diameter	0.69	0.93
比叶面积 Specific leaf area	0.14	0.00	比根长 Specific root length	0.39	0.79
叶组织密度 Leaf tissue density	0.14	0.00	根组织密度 Root tissue density	0.39	0.20
叶碳浓度 Leaf carbon concentration	0.19	0.33	根碳浓度 Root carbon concentration	0.13	0.00
叶氮浓度 Leaf nitrogen concentration	0.36	0.00	根氮浓度 Root nitrogen concentration	0.83	0.92

叶性状 Leaf trait	K	λ	根性状 Root trait	K	λ
叶厚度 Leaf thickness	0.11	0.00	根直径 Root diameter	0.69	0.93
比叶面积 Specific leaf area	0.14	0.00	比根长 Specific root length	0.39	0.79
叶组织密度 Leaf tissue density	0.14	0.00	根组织密度 Root tissue density	0.39	0.20
叶碳浓度 Leaf carbon concentration	0.19	0.33	根碳浓度 Root carbon concentration	0.13	0.00
叶氮浓度 Leaf nitrogen concentration	0.36	0.00	根氮浓度 Root nitrogen concentration	0.83	0.92

	叶PC1 Leaf PC1	叶PC2 Leaf PC2	叶pPC1 Leaf pPC1	叶pPC2 Leaf pPC2
根PC1 Root PC1	-0.342 (0.14)	-0.136 (0.57)
根PC2 Root PC2	0.002 (0.99)	0.437 (0.11)
根pPC1 Root pPC1			0.342 (0.14)	0.134 (0.57)
根pPC2 Root pPC2			0.004 (0.99)	0.438 (0.11)