Abstract
Forest productivity is closely linked to seasonal variations and vertical differentiation in leaf traits. However, leaf structural and chemical traits variation among co-existing species, and plant functional types within the canopy are poorly quantified. In this study, the seasonality of leaf chlorophyll, nitrogen (N), and phosphorus (P) were quantified vertically along the canopy of four major tree species and two types of herbs in a temperate deciduous forest. The role of shade tolerance in shaping the seasonal variation and vertical differentiation was examined. During the entire season, chlorophyll content showed a distinct asymmetric unimodal pattern for all species, with greater chlorophyll levels in autumn than in spring, and the timing of peak chlorophyll per leaf area gradually decreased as shade tolerance increased. Chlorophyll a:b ratios gradually decreased with increasing shade tolerance. Leaf N and P contents sharply declined during leaf expansion, remained steady in the mature stage and decreased again during leaf senescence. Over the seasons, the lower canopy layer had significantly higher chlorophyll per leaf mass but not chlorophyll per leaf area than the upper canopy layer regardless of degree of shade tolerance. However, N and P per leaf area of intermediate shade-tolerant and fully shade-tolerant tree species were significantly higher in the upper canopy than in the lower. Seasonal variations in N:P ratios suggest changes in N or P limitation. These findings indicate that shade tolerance is a key feature shaping inter-specific differences in leaf chlorophyll, N, and P contents as well as their seasonality in temperate deciduous forests, which have significant implications for modeling leaf photosynthesis and ecosystem production.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- N:
-
Nitrogen
- P:
-
Phosphorus
- Chl:
-
Chlorophyll
- Chl a:
-
Chlorophyll a content
- Chl b:
-
Chlorophyll b content
- N leaf :
-
Leaf nitrogen
- N mass :
-
Nitrogen/leaf mass
- N area :
-
Nitrogen/leaf area
- P leaf :
-
Leaf phosphorus
- P mass :
-
Phosphorus/leaf mass
- P area :
-
Phosphorus/leaf area
- Chlleaf :
-
Leaf chlorophyll
- Chlmass :
-
Chlorophyll/leaf mass
- Chlarea :
-
Chlorophyll/leaf area
References
Bachofen C, D’Odorico P, Buchmann N (2020) Light and VPD gradients drive foliar nitrogen partitioning and photosynthesis in the canopy of European beech and silver fir. Oecologia 192(2):323–339. https://doi.org/10.1007/s00442-019-04583-x
Chapin FS, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64(2):376–391. https://doi.org/10.2307/1937083
Chen JM, Wang R, Liu YH, He LM, Croft H, Luo XZ, Wang H, Smith NG, Keenan TF, Prentice IC, Zhang YG, Ju WM, Dong N (2022a) Global datasets of leaf photosynthetic capacity for ecological and earth system research. Earth Syst Sci Data 14(9):4077–4093. https://doi.org/10.5194/essd-14-4077-2022
Chen LT, Zhang Y, Nunes MH, Stoddart J, Khoury S, Chan AHY, Coomes DA (2022b) Predicting leaf traits of temperate broadleaf deciduous trees from hyperspectral reflectance: Can a general model be applied across a growing season? Remote Sens Environ 269:112767. https://doi.org/10.1016/j.rse.2021.112767
Coble AP, Cavaleri MA (2015) Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment. Oecologia 177(4):1131–1143. https://doi.org/10.1007/s00442-015-3219-4
Croft H, Chen JM, Froelich NJ, Chen B, Staebler RM (2015) Seasonal controls of canopy chlorophyll content on forest carbon uptake: implications for GPP modeling. J Geophys Res: Biogeo 120(8):1576–1586. https://doi.org/10.1002/2015JG002980
Croft H, Chen JM, Luo X, Bartlett P, Chen B, Staebler RM (2017) Leaf chlorophyll content as a proxy for leaf photosynthetic capacity. Global Change Biol 23(9):3513–3524. https://doi.org/10.1111/gcb.13599
Croft H, Chen JM, Wang R, Mo G, Luo S, Luo X, He L, Gonsamo A, Arabian J, Zhang Y, Simic-Milas A, Noland T, He Y, Homolová L, Malenovský Z, Yi Q, Beringer J, Amiri R, Hutley L, Arellano P, Stahl C, Bonal D (2020) The global distribution of leaf chlorophyll content. Remote Sens Environ 236:111479. https://doi.org/10.1016/j.rse.2019.111479
De Las Heras J, Hernández-Tecles EJ, Moya D (2017) Seasonal nutrient retranslocation in reforested Pinus halepensis Mill. stands in Southeast Spain. New for 48:397–413. https://doi.org/10.1007/s11056-016-9564-2
Du E, Terrer C, Pellegrini AF, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu X, Jackson RB (2020) Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci 13(3):221–226. https://doi.org/10.1038/s41561-019-0530-4
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 Environ 24(8):755–761. https://doi.org/10.1046/j.1365-3040.2001.00724.x
Finer L (1994) Variation in needle nutrient concentrations in the crown of Scots pine on peatland. Silva Fenn 28(1):41–51. https://doi.org/10.14214/sf.a9161
Granata MU, Bracco F, Nola P, Catoni R (2020) Photosynthetic characteristic and leaf traits variations along a natural light gradient in Acer campestre and Crataegus monogyna. Flora 268:151626. https://doi.org/10.1016/j.flora.2020.151626
Hallik L, Kull O, Niinemets Ü, Aan A (2009a) Contrasting correlation networks between leaf structure, nitrogen and chlorophyll in herbaceous and woody canopies. Basic Appl Ecol 10(4):309–318. https://doi.org/10.1016/j.baae.2008.08.001
Hallik L, Niinemets U, Wright IJ (2009b) Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora? New Phytol 184(1):257–274. https://doi.org/10.1111/j.1469-8137.2009.02918.x
He NP, Liu CC, Piao SL, Sack L, Xu L, Luo YQ, He JS, Han XG, Zhou GS, Zhou XH, Lin Y, Yu Q, Liu SR, Sun W, Niu SL, Li SG, Zhang JH, Yu GR (2019) Ecosystem traits linking functional traits to macroecology. Trends Ecol Evol 34(3):200–210. https://doi.org/10.1016/j.tree.2018.11.004
Heaton EA, Dohleman FG, Long SP (2009) Seasonal nitrogen dynamics of Miscanthus × giganteus and Panicum virgatum. GCB Bioenergy 1(4):297–307. https://doi.org/10.1111/j.1757-1707.2009.01022.x
Hikosaka K (2016) Optimality of nitrogen distribution among leaves in plant canopies. J Plant Res 129(3):299–311. https://doi.org/10.1007/s10265-016-0824-1
Hirose T (2005) Development of the Monsi-Saeki theory on canopy structure and function. Ann Bot-London 95(3):483–494. https://doi.org/10.1093/aob/mci047
Hollinger DY (1996) Optimality and nitrogen allocation in a tree canopy. Tree Physiol 16(7):627–634. https://doi.org/10.1093/treephys/16.7.627
Katahata SI, Naramoto M, Kakubari Y, Mukai Y (2007) Photosynthetic capacity and nitrogen partitioning in foliage of the evergreen shrub Daphniphyllum humile along a natural light gradient. Tree Physiol 27(2):199–208. https://doi.org/10.1093/treephys/27.2.199
Keenan TF, Darby B, Felts E, Sonnentag O, Friedl MA, Hufkens K, O’Keefe J, Klosterman S, Munger JW, Toomey M, Richardson AD (2014) Tracking forest phenology and seasonal physiology using digital repeat photography: a critical assessment. Ecol Appl 24(6):1478–1489. https://doi.org/10.1890/13-0652.1
Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T (2006) Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiol 26(7):865–873. https://doi.org/10.1093/treephys/26.7.865
Kikuzawa K (2003) Phenological and morphological adaptations to the light environment in two woody and two herbaceous plant species. Funct Ecol 17(1):29–38. https://doi.org/10.1046/j.1365-2435.2003.00707.x
Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26(6):857–865. https://doi.org/10.1046/j.1365-3040.2003.01017.x
Kitaoka S, Koike T (2004) Invasion of broad-leaf tree species into a larch plantation: seasonal light environment, photosynthesis and nitrogen allocation. Physiol Plantarum 121(4):604–611. https://doi.org/10.1111/j.1399-3054.2004.00359.x
Kobayashi H, Inoue S, Gyokusen K (2010) Spatial and temporal variations in the photosynthesis-nitrogen relationship in a Japanese cedar (Cryptomeria japonica D. Don) canopy. Photosynthetica 48(2):249–256. https://doi.org/10.1007/s11099-010-0031-6
Koerselman W, Meuleman AFM (1996) The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33(6):1441–1450. https://doi.org/10.2307/2404783
Legner N, Fleck S, Leuschner C (2014) Within-canopy variation in photosynthetic capacity, SLA and foliar N in temperate broad-leaved trees with contrasting shade tolerance. Trees 28(1):263–280. https://doi.org/10.1007/s00468-013-0947-0
Li Y, He NP, Hou JH, Xu L, Liu CC, Zhang JH, Wang QF, Zhang X, Wu XQ (2018) Factors influencing leaf chlorophyll content in natural forests at the biome scale. Fron Ecol Evol 6:10. https://doi.org/10.3389/fevo.2018.00064
Li YJ, Ma QM, Chen JM, Croft H, Luo XZ, Zheng T, Rogers C, Liu J (2021) Fine-scale leaf chlorophyll distribution across a deciduous forest through two-step model inversion from sentinel-2 data. Remote Sens Environ 264:112618. https://doi.org/10.1016/j.rse.2021.112618
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomenbranes. Method Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Lichtenthaler HK, Babani F (2022) Contents of photosynthetic pigments and ratios of chlorophyll a/b and chlorophylls to carotenoids (a+b)/(x+c) in C4 plants as compared to C3 plants. Photosynthetica 60:3–9. https://doi.org/10.32615/ps.2021.041
Liu JX, Zhang DQ, Zhou GY, Duan HL (2012) Changes in leaf nutrient traits and photosynthesis of four tree species: effects of elevated [CO2], N fertilization and canopy positions. J Plant Ecol 5(4):376–390. https://doi.org/10.1093/jpe/rts006
Liu ZL, Wang CK, Chen JM, Wang XC, Jin GZ (2015) Empirical models for tracing seasonal changes in leaf area index in deciduous broadleaf forests by digital hemispherical photography. Forest Ecol Manag 351:67–77. https://doi.org/10.1016/j.foreco.2015.05.005
Liu F, Wang XC, Wang CK (2019) Measuring vegetation phenology with near-surface remote sensing in a temperate deciduous forest: effects of sensor type and deployment. Remote Sensing 11(9):1063. https://doi.org/10.3390/rs11091063
Liu F, Wang XC, Wang CK, Zhang QZ (2021) Environmental and biotic controls on the interannual variations in CO2 fluxes of a continental monsoon temperate forest. Agric for Meteorol 296:108232. https://doi.org/10.1016/j.agrformet.2020.108232
Mandre M (2009) Vertical gradients of mineral elements in Pinus sylvestris crown in alkalised soil. Environ Monit Assess 159(1–4):111–124. https://doi.org/10.1007/s10661-008-0616-8
Muller O, Hikosaka K, Hirose T (2005) Seasonal changes in light and temperature affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understory shrub. Oecologia 143(4):501–508. https://doi.org/10.1007/s00442-005-0024-5
Muller O, Hirose T, Werger MJ, Hikosaka K (2011) Optimal use of leaf nitrogen explains seasonal changes in leaf nitrogen content of an understorey evergreen shrub. Ann Bot-London 108(3):529–536. https://doi.org/10.1093/aob/mcr167
Niinemets Ü (2007) Photosynthesis and resource distribution through plant canopies. Plant Cell Environ 30(9):1052–1071. https://doi.org/10.1111/j.1365-3040.2007.01683.x
Niinemets Ü (2010) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25(4):693–714. https://doi.org/10.1007/s11284-010-0712-4
Niinemets Ü (2023) Variation in leaf photosynthetic capacity within plant canopies: optimization, structural, and physiological constraints and inefficiencies. Photosynth Res 158:131–149. https://doi.org/10.1007/s11120-023-01043-9
Niinemets Ü, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant Cell Environ 20(7):845–866. https://doi.org/10.1046/j.1365-3040.1997.d01-133.x
Niinemets Ü, Keenan TF, Hallik L (2015) A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol 205(3):973–993. https://doi.org/10.1111/nph.13096
Nilsen P, Abrahamsen G (2003) Scots pine and Norway spruce stands responses to annual N, P and Mg fertilization. Forest Ecol Manag 174(1):221–232. https://doi.org/10.1016/S0378-1127(02)00024-5
Noda HM, Muraoka H, Nasahara KN, Saigusa N, Murayama S, Koizumi H (2015) Phenology of leaf morphological, photosynthetic, and nitrogen use characteristics of canopy trees in a cool-temperate deciduous broadleaf forest at Takayama, central Japan. Ecol Res 30(2):247–266. https://doi.org/10.1007/s11284-014-1222-6
Ollinger SV, Richardson AD, Martin ME, Hollinger DY, Frolking SE, Reich PB, Plourde LC, Katul GG, Munger JW, Oren R, Smith ML, Paw UKT, Bolstad PV, Cook BD, Day MC, Martin TA, Monson RK, Schmid HP (2008) Canopy nitrogen, carbon assimilation, and albedo in temperate and boreal forests: functional relations and potential climate feedbacks. P Natl Acad Sci USA 105(49):19336–19341. https://doi.org/10.1073/pnas.0810021105
Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340(6133):741–744. https://doi.org/10.1126/science.1231574
Ots K, Mandre M, Pärn H, Kask R, Pikk J (2009) Changes in the allocation of nutrients and biomass in scots pine (Pinus sylvestris L.) canopy in an area of cement industry in Northeast Estonia. Balt for 15(2):237–247
Palma RM, Defrieri RL, Tortarolo MF, Prause J, Gallardo JF (2000) Seasonal changes of bioelements in the litter and their potential return to green leaves in four species of the argentine subtropical forest. Ann Bot-London 85(2):181–186. https://doi.org/10.1006/anbo.1999.1005
Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quetier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61(3):167–234. https://doi.org/10.1071/BT12225
Sabate S, Sala A, Gracia CA (1995) Nutrient content in Quercus ilex canopies: seasonal and spatial variation within a catchment. Plant Soil 169(1):297–304. https://doi.org/10.1007/BF00029341
Seidel F, Lopez CML, Bonifacio E, Kurokawa H, Yamanaka T, Celi L (2022) Seasonal phosphorus and nitrogen cycling in four Japanese cool-temperate forest species. Plant Soil 472(1–2):391–406. https://doi.org/10.1007/s11104-021-05251-x
Simic A, Chen JM, Noland TL (2011) Retrieval of forest chlorophyll content using canopy structure parameters derived from multi-angle data: the measurement concept of combining nadir hyperspectral and off-nadir multispectral data. Int J Remote Sens 32(20):5621–5644. https://doi.org/10.1080/01431161.2010.507257
Sun XF, Liu F, Zhang QZ, Li YC, Zhang LF, Wang J, Zhang HY, Wang CK, Wang XC (2021) Biotic and climatic controls on the interannual variation in canopy litterfall of a deciduous broad-leaved forest. Agric for Meteorol 307:108483. https://doi.org/10.1016/j.agrformet.2021.108483
Sun X, Wang XC, Wang CK, Zhang QZ, Guo QX (2023) Filling the “vertical gap” between canopy tree species and understory shrub species: biomass allometric equations for subcanopy tree species. J Forestry Res 34(4):903–913. https://doi.org/10.1007/s11676-022-01568-0
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol S 39(1):237–257. https://doi.org/10.1146/annurev.ecolsys.39.110707.173506
Wang L, Ibrom A, Korhonen JFJ, Arnoud Frumau KF, Wu J, Pihlatie M, Schjoerring JK (2013) Interactions between leaf nitrogen status and longevity in relation to N cycling in three contrasting European forest canopies. Biogeosciences 10(2):999–1011. https://doi.org/10.5194/bg-10-999-2013
Wang SQ, Li Y, Ju WM, Chen B, Chen JH, Croft H, Mickler RA, Yang FT (2020) Estimation of leaf photosynthetic capacity from leaf chlorophyll content and leaf age in a subtropical evergreen coniferous plantation. J Geophys Res Biogeo 125(2):14. https://doi.org/10.1029/2019jg005020
Wang CS, Guo JJ, Zhao ZG, Wang H, Zeng J (2021) Spatial patterns and seasonal dynamics of foliar nutrients in 5-year-old Betula alnoides plantations. Forest Ecol Manag 480:118683. https://doi.org/10.1016/j.foreco.2020.118683
Wang XC, Song HM, Liu F, Quan XK, Wang CK (2022) Timing of leaf fall and changes in litter nutrient concentration compromise estimates of nutrient fluxes and nutrient resorption efficiency. Forest Ecol Manag 513:120188. https://doi.org/10.1016/j.foreco.2022.120188
Yang X, Tang JW, Mustard JF, Wu J, Zhao KG, Serbin S, Lee JE (2016) Seasonal variability of multiple leaf traits captured by leaf spectroscopy at two temperate deciduous forests. Remote Sens Environ 179:1–12. https://doi.org/10.1016/j.rse.2016.03.026
Yang HL, Yang X, Heskel M, Sun SC, Tang JW (2017) Seasonal variations of leaf and canopy properties tracked by ground-based NDVI imagery in a temperate forest. Sci Rep 7(1):1267. https://doi.org/10.1038/s41598-017-01260-y
Yoshimura K (2010) Irradiance heterogeneity within crown affects photosynthetic capacity and nitrogen distribution of leaves in Cedrela sinensis. Plant Cell Environ 33(5):750–758. https://doi.org/10.1111/j.1365-3040.2009.02100.x
Zhang YQ, Chen JM, Thomas SC (2007) Retrieving seasonal variation in chlorophyll content of overstory and understory sugar maple leaves from leaf-level hyperspectral data. Can J Remote Sens 33(5):406–415. https://doi.org/10.5589/m07-037
Zhuang J, Zhou L, Wang YL, Chi YG (2021) Nitrogen allocation regulates the relationship between maximum carboxylation rate and chlorophyll content along the vertical gradient of subtropical forest canopy. Agric for Meteorol 307:108512. https://doi.org/10.1016/j.agrformet.2021.108512
Acknowledgements
We thank Guangdong Cao and Daosheng Liang for their help in collecting samples, and the Maoershan Forest Ecosystem Research Station for logistic support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Project funding: This work was supported by the National Natural Science Foundation of China (32171765).
The online version is available at http://www.springerlink.com.
Corresponding editor: Yanbo Hu.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zeng, J., Liu, F., Zhu, Y. et al. Degree of shade tolerance shapes seasonality of chlorophyll, nitrogen and phosphorus levels of trees and herbs in a temperate deciduous forest. J. For. Res. 35, 72 (2024). https://doi.org/10.1007/s11676-024-01703-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11676-024-01703-z