{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,6]],"date-time":"2026-03-06T02:38:44Z","timestamp":1772764724754,"version":"3.50.1"},"reference-count":56,"publisher":"MDPI AG","issue":"24","license":[{"start":{"date-parts":[[2021,12,13]],"date-time":"2021-12-13T00:00:00Z","timestamp":1639353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["41901060, 41671430"],"award-info":[{"award-number":["41901060, 41671430"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>Little attention has been paid to the impact of vertical canopy position on the leaf spectral properties of tall trees, and few studies have explored the ability of leaf spectra to characterize the variation of leaf traits across different canopy positions. Using a tower crane, we collected leaf samples from three canopy layers (lower, middle, and upper) and measured eight leaf traits (equivalent water thickness, specific leaf area, leaf carbon content, leaf nitrogen content, leaf phosphorus content, leaf chlorophyll content, flavonoid, and nitrogen balance index) in a subtropical evergreen broadleaved forest. We evaluated the variability of leaf traits and leaf spectral properties, as well as the ability of leaf spectra to track the variation of leaf traits among three canopy layers for six species within the entire reflectance spectrum. The results showed that the eight leaf traits that were moderately or highly correlated with each other showed significant differences along the vertical canopy profile. The three canopy layers of leaf spectra showed contrasting patterns for light-demanding (Castanopsis chinensis, Castanopsis fissa, Schima superba, and Machilus chinensis) and shade-tolerant species (Cryptocarya chinensis and Cryptocarya concinna) along the vertical canopy profile. The spectra at the lower and upper canopy layers were more sensitive than the middle layer for tracking the variation of leaf chlorophyll and flavonoid content. Our results revealed that it is important to choose an appropriate canopy layer for the field sampling of tall trees, and we suggest that flavonoid is an important leaf trait that can be used for mapping and monitoring plant growth with hyperspectral remote sensing.<\/jats:p>","DOI":"10.3390\/rs13245057","type":"journal-article","created":{"date-parts":[[2021,12,14]],"date-time":"2021-12-14T01:22:05Z","timestamp":1639444925000},"page":"5057","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Understanding the Impact of Vertical Canopy Position on Leaf Spectra and Traits in an Evergreen Broadleaved Forest"],"prefix":"10.3390","volume":"13","author":[{"given":"Fangyuan","family":"Yu","sequence":"first","affiliation":[{"name":"School of Geographical Sciences and Remote Sensing, Guangzhou University, Guangzhou 510006, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8134-4849","authenticated-orcid":false,"given":"Tawanda W.","family":"Gara","sequence":"additional","affiliation":[{"name":"School of Forest Resources, College of Natural Sciences, Forestry, and Agriculture, University of Maine, Orono, ME 04469, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Juyu","family":"Lian","sequence":"additional","affiliation":[{"name":"Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China"},{"name":"Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou 510650, China"},{"name":"Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 510650, China"},{"name":"Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wanhui","family":"Ye","sequence":"additional","affiliation":[{"name":"Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China"},{"name":"Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou 510650, China"},{"name":"Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 510650, China"},{"name":"Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jian","family":"Shen","sequence":"additional","affiliation":[{"name":"Institute of Agricultural Resources and Environment, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1138-8464","authenticated-orcid":false,"given":"Tiejun","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Natural Resources, Faculty of Geo-Information Science and Earth Observation, University of Twente, P.O. Box 217, 7500 AE Enschede, The Netherlands"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhifeng","family":"Wu","sequence":"additional","affiliation":[{"name":"School of Geographical Sciences and Remote Sensing, Guangzhou University, Guangzhou 510006, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4839-7724","authenticated-orcid":false,"given":"Junjie","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Sciences and Oceanography, Shenzhen University, Shenzhen 518060, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.rse.2016.08.013","article-title":"Review of studies on tree species classification from remotely sensed data","volume":"186","author":"Fassnacht","year":"2016","journal-title":"Remote Sens. Environ."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1111\/gcb.12385","article-title":"Substantial reorganization of China\u2019s tropical and subtropical forests: Based on the permanent plots","volume":"20","author":"Zhou","year":"2014","journal-title":"Global Chang. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1007\/s13595-011-0102-2","article-title":"The use of terrestrial LiDAR technology in forest science: Application fields, benefits and challenges","volume":"68","author":"Dassot","year":"2011","journal-title":"Ann. Forest Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.rse.2018.09.006","article-title":"A methodology to derive global maps of leaf traits using remote sensing and climate data","volume":"218","author":"Kattge","year":"2018","journal-title":"Remote Sens. Environ."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1111\/brv.12359","article-title":"Building essential biodiversity variables (EBVs) of species distribution and abundance at a global scale","volume":"93","author":"Kissling","year":"2018","journal-title":"Biol. Rev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.rse.2014.11.011","article-title":"Quantifying forest canopy traits: Imaging spectroscopy versus field survey","volume":"158","author":"Asner","year":"2015","journal-title":"Remote Sens. Environ."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.rse.2012.07.010","article-title":"Mapping tree species composition in South African savannas using an integrated airborne spectral and LiDAR system","volume":"125","author":"Cho","year":"2012","journal-title":"Remote Sens. Environ."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1017\/S0376892914000307","article-title":"Choosing and using multiple traits in functional diversity research","volume":"42","author":"Lefcheck","year":"2014","journal-title":"Environ. Conserv."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1086\/519400","article-title":"Trait Evolution, Community Assembly, and the Phylogenetic Structure of Ecological Communities","volume":"170","author":"Kraft","year":"2007","journal-title":"Am. Nat."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1111\/j.0030-1299.2007.15559.x","article-title":"Let the concept of trait be functional!","volume":"116","author":"Violle","year":"2007","journal-title":"Oikos"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1111\/1365-2435.12934","article-title":"Variation in leaf anatomical traits from tropical to cold-temperate forests and linkage to ecosystem functions","volume":"32","author":"He","year":"2017","journal-title":"Funct. Ecol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1111\/j.1365-2435.2010.01727.x","article-title":"A multi-trait approach reveals the structure and the relative importance of intra- vs. interspecific variability in plant traits","volume":"24","author":"Albert","year":"2010","journal-title":"Funct. Ecol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1038\/nature02403","article-title":"The worldwide leaf economics spectrum","volume":"428","author":"Wright","year":"2004","journal-title":"Nature"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.tree.2018.11.004","article-title":"Ecosystem Traits Linking Functional Traits to Macroecology","volume":"34","author":"He","year":"2019","journal-title":"Trends Ecol. Evol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Gara, T., Darvishzadeh, R., Skidmore, A., and Wang, T. (2018). Impact of Vertical Canopy Position on Leaf Spectral Properties and Traits across Multiple Species. Remote Sens., 10.","DOI":"10.3390\/rs10020346"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1080\/01431160701281023","article-title":"Canopy chlorophyll concentration estimation using hyperspectral and lidar data for a boreal mixedwood forest in northern Ontario, Canada","volume":"29","author":"Thomas","year":"2008","journal-title":"Int. J. Remote Sens."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.agrformet.2012.10.004","article-title":"Canopy vertical heterogeneity plays a critical role in reflectance simulation","volume":"169","author":"Wang","year":"2013","journal-title":"Agr. Forest Meteorol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1111\/1365-2435.12490","article-title":"Functional leaf traits of vascular epiphytes: Vertical trends within the forest, intra- and interspecific trait variability, and taxonomic signals","volume":"30","author":"Petter","year":"2015","journal-title":"Funct. Ecol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1093\/treephys\/tpu016","article-title":"Canopy position affects the relationships between leaf respiration and associated traits in a tropical rainforest in Far North Queensland","volume":"34","author":"Weerasinghe","year":"2014","journal-title":"Tree Physiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"D09111","DOI":"10.1029\/2006JD007821","article-title":"Third Radiation Transfer Model Intercomparison (RAMI) exercise: Documenting progress in canopy reflectance models","volume":"112","author":"Widlowski","year":"2007","journal-title":"J. Geophys. Res. Atmos."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1093\/treephys\/21.12-13.951","article-title":"Leaf morphology and photosynthetic adjustments among deciduous broad-leaved trees within the vertical canopy profile","volume":"21","author":"Koike","year":"2001","journal-title":"Tree Physiol."},{"key":"ref_22","first-page":"185","article-title":"A field study on solar-induced chlorophyll fluorescence and pigment parameters along a vertical canopy gradient of four tree species in an urban environment","volume":"466","author":"Alonso","year":"2014","journal-title":"Sci. Total Environ."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.fcr.2012.11.017","article-title":"Non-uniform vertical nitrogen distribution within plant canopy and its estimation by remote sensing: A review","volume":"142","author":"Li","year":"2013","journal-title":"Field Crop. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1093\/aob\/mci051","article-title":"Variation in crown light utilization characteristics among tropical canopy trees","volume":"95","author":"Kitajima","year":"2005","journal-title":"Ann. Bot."},{"key":"ref_25","first-page":"3172","article-title":"Leaf Nitrogen Content Indirectly Estimated by Leaf Traits Derived From the PROSPECT Model","volume":"8","author":"Wang","year":"2015","journal-title":"IEEE J.-Stars"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1111\/j.1469-8137.2012.04076.x","article-title":"Plant science in forest canopies\u2014The first 30 years of advances and challenges (1980\u20132010)","volume":"194","author":"Lowman","year":"2012","journal-title":"New Phytol."},{"key":"ref_27","unstructured":"Schmit-Neuerburg, V. (2002). Dynamics of Vascular Epiphyte Vegetation in the Venezuelan Lowland Rain Forest of the Surumoni Crane Project. [Ph.D. Thesis, Rheinische Friedrich-Wilhelms-Universit\u00e4t]."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"664","DOI":"10.2307\/1312172","article-title":"Access to the Upper Forest Canopy with a Large Tower Crane","volume":"42","author":"Parker","year":"1992","journal-title":"Bioscience"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1314","DOI":"10.1126\/science.309.5739.1314","article-title":"Forest research\u2014Sky-high experiments","volume":"309","author":"Pennisi","year":"2005","journal-title":"Science"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"119433","DOI":"10.1016\/j.foreco.2021.119433","article-title":"An old-growth subtropical evergreen broadleaved forest suffered more damage from Typhoon Mangkhut than an adjacent secondary forest","volume":"496","author":"Ni","year":"2021","journal-title":"For. Ecol. Manag."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Condit, R. (1998). Tropical Forest Census Plots\u2014Methods and Results From Barro Colorado Island, Panama and a Comparison With Other Plots, Springer.","DOI":"10.1007\/978-3-662-03664-8"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"619","DOI":"10.17520\/biods.2019107","article-title":"Vertical structure and its biodiversity in a subtropical evergreen broad- leaved forest at Dinghushan in Guangdong Province, China","volume":"27","author":"Gui","year":"2019","journal-title":"Biodivers. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1071\/BT02124","article-title":"A handbook of protocols for standardised and easy measurement of plant functional traits worldwide","volume":"51","author":"Cornelissen","year":"2003","journal-title":"Aust. J. Bot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1007\/BF00032301","article-title":"Calibration of the Minolta SPAD-502 leaf chlorophyll meter","volume":"46","author":"Markwell","year":"1995","journal-title":"Photosynth. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1007\/s00442-016-3545-1","article-title":"Phenological variation of leaf functional traits within species","volume":"180","author":"Fajardo","year":"2016","journal-title":"Oecologia"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1093\/forestry\/cpv021","article-title":"Comparison of regeneration and recruitment of shade-tolerant and light-demanding tree species in mixed uneven-aged forests: Experiences from the Dinaric region","volume":"88","year":"2015","journal-title":"Forestry"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1046\/j.1365-2435.1998.00214.x","article-title":"Distribution of leaf photosynthetic properties in tree canopies: Comparison of species with different shade tolerance","volume":"12","author":"Kull","year":"1998","journal-title":"Funct. Ecol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/s00442-014-3126-0","article-title":"Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees","volume":"177","author":"Kenzo","year":"2015","journal-title":"Oecologia"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1890\/0012-9658(1999)080[0187:LGPATT]2.0.CO;2","article-title":"Light gradient partitioning among tropical tree species through differential seedling mortality and growth","volume":"80","author":"Kobe","year":"1999","journal-title":"Ecology"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.foreco.2018.12.008","article-title":"Coordination of intra and inter-species leaf traits according to leaf phenology and plant age for three temperate broadleaf species with different shade tolerances","volume":"434","author":"Liu","year":"2019","journal-title":"For. Ecol. Manag."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1052","DOI":"10.1111\/j.1365-3040.2007.01683.x","article-title":"Photosynthesis and resource distribution through plant canopies","volume":"30","author":"Niinemets","year":"2007","journal-title":"Plant Cell Environ."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/s00442-010-1650-0","article-title":"Genotypic and environmental variation in specific leaf area in a widespread Alpine plant after transplantation to different altitudes","volume":"164","author":"Scheepens","year":"2010","journal-title":"Oecologia"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1016\/j.agrformet.2008.10.023","article-title":"Responses of leaf traits of European beech (Fagus sylvatica L.) saplings to supplemental UV-B radiation and UV-B exclusion","volume":"149","author":"Veres","year":"2009","journal-title":"Agr. Forest Meteorol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1007\/BF00013762","article-title":"Protection from UV-B-induced DNA damage by flavonoids","volume":"26","author":"Kootstra","year":"1994","journal-title":"Plant Mol. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1405","DOI":"10.1104\/pp.115.4.1405","article-title":"Flavonoid-Peroxidase Reaction as a Detoxification Mechanism of Plant Cells against H2O2","volume":"115","author":"Yamasaki","year":"1997","journal-title":"Plant Physiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.plaphy.2015.03.001","article-title":"Interactive effects of supplemental UV-B and temperature in European aspen seedlings: Implications for growth, leaf traits, phenolic defense and associated organisms","volume":"93","author":"Randriamanana","year":"2015","journal-title":"Plant Physiol. Biochem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1923","DOI":"10.1111\/1365-2745.13384","article-title":"Testing trait plasticity over the range of spectral composition of sunlight in forb species differing in shade tolerance","volume":"108","author":"Wang","year":"2020","journal-title":"J. Ecol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1820","DOI":"10.3390\/rs4061820","article-title":"Species-Level Differences in Hyperspectral Metrics among Tropical Rainforest Trees as Determined by a Tree-Based Classifier","volume":"4","author":"Clark","year":"2012","journal-title":"Remote Sens."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/S0034-4257(98)00014-5","article-title":"Biophysical and Biochemical Sources of Variability in Canopy Reflectance","volume":"64","author":"Asner","year":"1998","journal-title":"Remote Sens. Environ."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"S78","DOI":"10.1016\/j.rse.2008.10.018","article-title":"Characterizing canopy biochemistry from imaging spectroscopy and its application to ecosystem studies","volume":"113","author":"Kokaly","year":"2009","journal-title":"Remote Sens. Environ."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3958","DOI":"10.1016\/j.rse.2008.07.003","article-title":"Spectral and chemical analysis of tropical forests: Scaling from leaf to canopy levels","volume":"112","author":"Asner","year":"2008","journal-title":"Remote Sens. Environ."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"S67","DOI":"10.1016\/j.rse.2008.10.019","article-title":"Retrieval of foliar information about plant pigment systems from high resolution spectroscopy","volume":"113","author":"Ustin","year":"2009","journal-title":"Remote Sens. Environ."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/S0034-4257(01)00191-2","article-title":"Detecting vegetation leaf water content using reflectance in the optical domain","volume":"77","author":"Ceccato","year":"2001","journal-title":"Remote Sens. Environ."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/0034-4257(89)90046-1","article-title":"Detection of changes in leaf water content using Near- and Middle-Infrared reflectances","volume":"30","author":"Hunt","year":"1989","journal-title":"Remote Sens. Environ."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3955","DOI":"10.1080\/01431161.2021.1887541","article-title":"Predicting medicinal phytochemicals of Moringa oleifera using hyperspectral reflectance of tree canopies","volume":"42","author":"Tshabalala","year":"2021","journal-title":"Int. J. Remote Sens."},{"key":"ref_56","first-page":"101919","article-title":"Evaluating the performance of PROSPECT in the retrieval of leaf traits across canopy throughout the growing season","volume":"83","author":"Gara","year":"2019","journal-title":"Int. J. Appl. Earth Obs. Geoinf."}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/13\/24\/5057\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:46:50Z","timestamp":1760168810000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/13\/24\/5057"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,13]]},"references-count":56,"journal-issue":{"issue":"24","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["rs13245057"],"URL":"https:\/\/doi.org\/10.3390\/rs13245057","relation":{},"ISSN":["2072-4292"],"issn-type":[{"value":"2072-4292","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,13]]}}}