{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T20:09:14Z","timestamp":1772136554758,"version":"3.50.1"},"reference-count":60,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2015,12,15]],"date-time":"2015-12-15T00:00:00Z","timestamp":1450137600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>Epidermal structures (ES) of leaves are known to affect the functional properties and spectral responses. Spectral studies focused mostly on the effect of hairs or wax layers only. We studied a wider range of different ES and their impact on spectral properties. Additionally, we identified spectral regions that allow distinguishing different ES. We used a field spectrometer to measure ex situ leaf spectral responses from 350 nm\u20132500 nm. A spectral library for 25 species of the succulent family Aizoaceae was assembled. Five functional types were defined based on ES: flat epidermal cell surface, convex to papillary epidermal cell surface, bladder cells, hairs and wax cover. We tested the separability of ES using partial least squares discriminant analysis (PLS-DA) based on the spectral data. Subsequently, variable importance (VIP) was calculated to identify spectral regions relevant for discriminating our functional types (classes). Classification performance was high, with a kappa value of 0.9 indicating well-separable spectral classes. VIP calculations identified six spectral regions of increased importance for the classification. We confirmed and extended previous findings regarding the visible-near-infrared spectral region. Our experiments also confirmed that epidermal leaf traits can be classified due to clearly distinguishable spectral signatures across species and genera within the Aizoaceae.<\/jats:p>","DOI":"10.3390\/rs71215862","type":"journal-article","created":{"date-parts":[[2015,12,15]],"date-time":"2015-12-15T10:09:11Z","timestamp":1450174151000},"page":"16901-16914","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["The Effect of Epidermal Structures on Leaf Spectral Signatures of Ice Plants (Aizoaceae)"],"prefix":"10.3390","volume":"7","author":[{"given":"Ren\u00e9","family":"Heim","sequence":"first","affiliation":[{"name":"Biodiversity Ecology and Evolution of Plants, Biocenter Klein Flottbek and Botanical Garden, University of Hamburg, Ohnhorststra\u00dfe 18, 22609 Hamburg, Germany"}]},{"given":"Norbert","family":"J\u00fcrgens","sequence":"additional","affiliation":[{"name":"Biodiversity Ecology and Evolution of Plants, Biocenter Klein Flottbek and Botanical Garden, University of Hamburg, Ohnhorststra\u00dfe 18, 22609 Hamburg, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6075-5497","authenticated-orcid":false,"given":"Andr\u00e9","family":"Gro\u00dfe-Stoltenberg","sequence":"additional","affiliation":[{"name":"Institute of Landscape Ecology, Heisenbergstra\u00dfe 2, 48149 M\u00fcnster, Germany"}]},{"given":"Jens","family":"Oldeland","sequence":"additional","affiliation":[{"name":"Biodiversity Ecology and Evolution of Plants, Biocenter Klein Flottbek and Botanical Garden, University of Hamburg, Ohnhorststra\u00dfe 18, 22609 Hamburg, Germany"}]}],"member":"1968","published-online":{"date-parts":[[2015,12,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/S0034-4257(02)00010-X","article-title":"Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages","volume":"81","author":"Sims","year":"2002","journal-title":"Remote Sens. Environ."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1093\/jxb\/erl123","article-title":"Hyperspectral remote sensing of plant pigments","volume":"58","author":"Blackburn","year":"2007","journal-title":"J. Exp. Bot."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"307","DOI":"10.3389\/fpls.2015.00307","article-title":"Retrieving nitrogen isotopic signatures from fresh leaf reflectance spectra: Disentangling delta \u03b415N from biochemical and structural leaf properties","volume":"6","author":"Hellmann","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5604","DOI":"10.1073\/pnas.1401181111","article-title":"Amazonian functional diversity from forest canopy chemical assembly","volume":"111","author":"Asner","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.3390\/rs70201225","article-title":"Field spectroscopy in the vnir-swir region to discriminate between mediterranean native plants and exotic-invasive shrubs based on leaf tannin content","volume":"7","author":"Lehmann","year":"2015","journal-title":"Remote Sens."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1016\/j.rse.2007.01.012","article-title":"Hyperspectral discrimination of tropical dry forest lianas and trees: Comparative data reduction approaches at the leaf and canopy levels","volume":"109","author":"Kalacska","year":"2007","journal-title":"Remote Sens. Environ."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1016\/S0034-4257(02)00151-7","article-title":"Estimation of vegetation water content and photosynthetic tissue area from spectral reflectance: A comparison of indices based on liquid water and chlorophyll absorption features","volume":"84","author":"Sims","year":"2003","journal-title":"Remote Sens. Environ."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1111\/j.1469-8137.2006.01823.x","article-title":"Attenuated total reflectance spectroscopy of plant leaves: A tool for ecological and botanical studies","volume":"172","year":"2006","journal-title":"New Phytol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/BF00349805","article-title":"Pubescence and leaf spectral characteristics in a desert shrub, encelia farinosa","volume":"36","author":"Ehleringer","year":"1978","journal-title":"Oecologia"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1111\/j.1438-8677.1985.tb02936.x","article-title":"Epidermis and the spectral properties of plant-surfaces","volume":"98","author":"Eller","year":"1985","journal-title":"Ber. Deut. Bot. Ges."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/BF00345796","article-title":"The significance of leaf pubescence for the absorption of global radiation by tussilago farfara l.","volume":"29","author":"Eller","year":"1977","journal-title":"Oecologia"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/BF00344990","article-title":"Leaf hairs: Effects on physiological activity and adaptive value to a desert shrub","volume":"37","author":"Ehleringer","year":"1978","journal-title":"Oecologia"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1007\/BF00345193","article-title":"Spectral properties of heavily glaucous and non-glaucous leaves of a succulent rosette-plant","volume":"38","author":"Mulroy","year":"1979","journal-title":"Oecologia"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/S0176-1617(86)80151-1","article-title":"Epidermis structure and its significance for the optical-properties of leaves of the mesembryanthemaceae","volume":"125","author":"Tanner","year":"1986","journal-title":"J. Plant Physiol."},{"key":"ref_15","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":"Huntjr","year":"1989","journal-title":"Remote Sens. Environ."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1890\/1051-0761(1997)007[0431:HSRRSO]2.0.CO;2","article-title":"High spectral resolution remote sensing of forest canopy lignin, nitrogen, and ecosystem processes","volume":"7","author":"Martin","year":"1997","journal-title":"Ecol. Appl."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/S0034-4257(98)00035-2","article-title":"Determining forest species composition using high spectral resolution remote sensing data","volume":"65","author":"Martin","year":"1998","journal-title":"Remote Sens. Environ."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"677","DOI":"10.2307\/2657068","article-title":"Leaf optical properties in higher plants: Linking spectral characteristics to stress and chlorophyll concentration","volume":"88","author":"Carter","year":"2001","journal-title":"Am. J. Bot."},{"key":"ref_19","unstructured":"Von Willert, D.J. (1992). Life Strategies of Succulents in Deserts: With Special Reference to the Namib Desert, CUP Archive."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1038\/35002501","article-title":"Biodiversity hotspots for conservation priorities","volume":"403","author":"Myers","year":"2000","journal-title":"Nature"},{"key":"ref_21","unstructured":"Cutler, D.F., Alvin, K.L., and Price, C.E. (1982). The Plant Cuticle, Academic Press."},{"key":"ref_22","unstructured":"List, T.P. The Plant List (2013). Version 1.1. Available online: http:\/\/www.theplantlist.org\/."},{"key":"ref_23","first-page":"139","article-title":"Untersuchungen zur \u00d6kologie sukkulenter Pflanzen des s\u00fcdlichen Afrika","volume":"21","year":"1986","journal-title":"Mitt. Inst. Allg. Bot. Hamburg"},{"key":"ref_24","unstructured":"Niesler, I.M. (1998). Untersuchungen zur Ontogenie und zum Bau der Bl\u00e4tter bei Mesembryanthemaceae Fenzl unter besonderer Ber\u00fccksichtigung der Epidermis. [Ph.D. Thesis, Universit\u00e4t Hamburg]."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.rse.2005.03.009","article-title":"Hyperspectral discrimination of tropical rain forest tree species at leaf to crown scales","volume":"96","author":"Clark","year":"2005","journal-title":"Remote Sens. Environ."},{"key":"ref_26","first-page":"177","article-title":"Hyperspectral discrimination of tree species with different classifications using single- and multiple-endmember","volume":"23","author":"Ghiyamat","year":"2013","journal-title":"Int. J. Appl. Earth Observ. Geoinf."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"8494","DOI":"10.3390\/rs6098494","article-title":"Plant species discrimination in a tropical wetland using in situ hyperspectral data","volume":"6","author":"Prospere","year":"2014","journal-title":"Remote Sens."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1238","DOI":"10.1016\/j.jfoodeng.2006.04.042","article-title":"Discrimination of varieties of tea using near infrared spectroscopy by principal component analysis and bp model","volume":"79","author":"He","year":"2007","journal-title":"J. Food Eng."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1021\/jf001196p","article-title":"Rapid method for the discrimination of red wine cultivars based on mid-infrared spectroscopy of phenolic wine extracts","volume":"49","author":"Edelmann","year":"2001","journal-title":"J. Agric. Food Chem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1007\/s11119-007-9037-x","article-title":"Development of an agricultural crops spectral library and classification of crops at cultivar level using hyperspectral data","volume":"8","author":"Rao","year":"2007","journal-title":"Precis. Agric."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1111\/j.1469-8137.2010.03284.x","article-title":"Remote sensing of plant functional types","volume":"186","author":"Ustin","year":"2010","journal-title":"New Phytol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1177\/030913330002400403","article-title":"Plant functional types: An alternative to taxonomic plant community description in biogeography?","volume":"24","author":"Duckworth","year":"2000","journal-title":"Prog. Phys. Geogr."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ecocom.2013.06.003","article-title":"Review of optical-based remote sensing for plant trait mapping","volume":"15","author":"Homolova","year":"2013","journal-title":"Ecol. Complex."},{"key":"ref_34","first-page":"1","article-title":"Advances in remote sensing of vegetation function and traits","volume":"43","author":"Houborg","year":"2015","journal-title":"Int. J. Appl. Earth Observ. Geoinf."},{"key":"ref_35","unstructured":"Dorigo, W., Bachmann, M., and Heldens, W. (2006). AS Toolbox & Processing of Field Spectra-user\u2019s manual, German Aerospace Center, DLR-DFD. Imaging Spectroscopy Group."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.chemolab.2008.11.006","article-title":"On the geometry of snv and msc","volume":"96","author":"Fearn","year":"2009","journal-title":"Chemom. Intell. Lab. Syst."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1366\/0003702894202201","article-title":"Standard normal variate transformation and de-trending of near-infrared diffuse reflectance spectra","volume":"43","author":"Barnes","year":"1989","journal-title":"Appl. Spectrosc."},{"key":"ref_38","unstructured":"Sanchez, G., Determan, C., and Sanchez, M.G. R Package DiscriMiner (Version 0.1\u201329). Available online: https:\/\/cran.r-project.org\/web\/packages\/DiscriMiner\/."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Kuhn, M., and Johnson, K. (2013). Applied Predictive Modeling, Springer.","DOI":"10.1007\/978-1-4614-6849-3"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Thenkabail, P.S., Lyon, J.G., and Huete, A. (2011). Hyperspectral Remote Sensing of Vegetation, CRC Press.","DOI":"10.1201\/b11222-41"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.chemolab.2004.12.011","article-title":"Performance of some variable selection methods when multicollinearity is present","volume":"78","author":"Chong","year":"2005","journal-title":"Chemom. Intell. Lab. Syst."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1002\/(SICI)1099-128X(199609)10:5\/6<463::AID-CEM445>3.0.CO;2-L","article-title":"Hierarchical multiblock pls and pc models for easier model interpretation and as an alternative to variable selection","volume":"10","author":"Wold","year":"1996","journal-title":"J. Chemom."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"K\u00e5gstr\u00f6m, B., and Ruhe, A. (1983). Matrix Pencils, Springer.","DOI":"10.1007\/BFb0062089"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1002\/cem.785","article-title":"Partial least squares for discrimination","volume":"17","author":"Barker","year":"2003","journal-title":"J. Chemom."},{"key":"ref_45","first-page":"581","article-title":"Prediction of clinical outcome with microarray data: A partial least squares discriminant analysis (PLS-DA) approach","volume":"112","author":"Tenenhaus","year":"2003","journal-title":"Hum. Genet"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1111\/j.1469-1809.1936.tb02137.x","article-title":"The use of multiple measurements in taxonomic problems","volume":"7","author":"Fisher","year":"1936","journal-title":"Ann. Eugen."},{"key":"ref_47","unstructured":"Leung, K., Cheong, F., Cheong, C., O\u2019Farrell, S., Tissington, R., and Ou, C.M. (2008, January 4). A Comparison of Variable Selection Techniques for Credit Scoring. Proceedings of the 7th International Conference on Computational Intelligence in Economics and Finance, Taiwan."},{"key":"ref_48","first-page":"548","article-title":"Improvements on cross-validation: The 632+ bootstrap method","volume":"92","author":"Efron","year":"1997","journal-title":"J. Am. Stat. Assoc."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1177\/001316446002000104","article-title":"A coefficient of agreement for nominal scales","volume":"20","author":"Cohen","year":"1960","journal-title":"Educ. Psychol. Meas."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"159","DOI":"10.2307\/2529310","article-title":"The measurement of observer agreement for categorical data","volume":"33","author":"Landis","year":"1977","journal-title":"Biometrics"},{"key":"ref_51","first-page":"397","article-title":"Accuracy assessment\u2014A users perspective","volume":"52","author":"Story","year":"1986","journal-title":"Photogramm Eng. Remote Sens."},{"key":"ref_52","unstructured":"Jones, H.G., and Vaughan, R.A. (2010). Remote Sensing of Vegetation: Principles, Techniques, and Applications, Oxford University Press."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"27","DOI":"10.2985\/1070-0048(2005)11[27:LAOCNE]2.0.CO;2","article-title":"Leaf anatomy of conophytum n.E.Br. (aizoaceae)","volume":"11","author":"Opel","year":"2005","journal-title":"Haseltonia"},{"key":"ref_54","unstructured":"Opel, M.R., and Hammer, S.A. (2002). SA Hammer, Dumpling and His Wife: New Views of the Genus Conophytum, EAE Creative Color Ltd."},{"key":"ref_55","first-page":"671","article-title":"Physiologische pflanzenanatomie, Leipzig 1909, IV","volume":"557","author":"Haberland","year":"1909","journal-title":"Aufl. S"},{"key":"ref_56","first-page":"67","article-title":"Zur Feinstruktur, Chemie und taxonomischen Signifikanz epicuticularer Wachse und \u00e4hnlicher Sekrete","volume":"32","author":"Barthlott","year":"1981","journal-title":"Trop. Subtrop. Pflanzenwelt."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1002\/wnan.1330","article-title":"Hyperspectral microscopy as an analytical tool for nanomaterials","volume":"7","author":"Roth","year":"2015","journal-title":"Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1007\/s10021-004-0144-5","article-title":"Spectral and structural measures of northwest forest vegetation at leaf to landscape scales","volume":"7","author":"Roberts","year":"2004","journal-title":"Ecosystems"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Hartmann, H.E.K. (2002). Illustrated Handbook of Succulent Plants: Aizoaceae A\u2013E, Springer Science & Business Media.","DOI":"10.1007\/978-3-642-56265-5"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Hartmann, H.E.K. (2002). Illustrated Handbook of Succulent Plants: Aizoaceae F\u2013Z, Springer Science & Business Media.","DOI":"10.1007\/978-3-642-56265-5"}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/7\/12\/15862\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T20:54:06Z","timestamp":1760216046000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/7\/12\/15862"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,12,15]]},"references-count":60,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2015,12]]}},"alternative-id":["rs71215862"],"URL":"https:\/\/doi.org\/10.3390\/rs71215862","relation":{},"ISSN":["2072-4292"],"issn-type":[{"value":"2072-4292","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,12,15]]}}}