Abstract
While foliar photosynthetic relationships with light, nitrogen, and water availability have been well described, environmental factors driving vertical gradients of foliar traits within forest canopies are still not well understood. We, therefore, examined how light availability and vapour pressure deficit (VPD) co-determine vertical gradients (between 12 and 42 m and in the understorey) of foliar photosynthetic capacity (Amax), 13C fractionation (∆), specific leaf area (SLA), chlorophyll (Chl), and nitrogen (N) concentrations in canopies of Fagus sylvatica and Abies alba growing in a mixed forest in Switzerland in spring and summer 2017. Both species showed lower Chl/N and lower SLA with higher light availability and VPD at the top canopy. Despite these biochemical and morphological acclimations, Amax during summer remained relatively constant and the photosynthetic N-use efficiency (PNUE) decreased with higher light availability for both species, suggesting suboptimal N allocation within the canopy. ∆ of both species were lower at the canopy top compared to the bottom, indicating high water-use efficiency (WUE). VPD gradients strongly co-determined the vertical distribution of Chl, N, and PNUE in F. sylvatica, suggesting stomatal limitation of photosynthesis in the top canopy, whereas these traits were only related to light availability in A. alba. Lower PNUE in F. sylvatica with higher WUE clearly indicated a trade-off in water vs. N use, limiting foliar acclimation to high light and VPD at the top canopy. Species-specific trade-offs in foliar acclimation to environmental canopy gradients may thus be considered for scaling photosynthesis from leaf to canopy to landscape levels.
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References
Ambrose AR, Baxter WL, Wong CS et al (2016) Hydraulic constraints modify optimal photosynthetic profiles in giant sequoia trees. Oecologia 182:713–730
Arend M, Brem A, Kuster TM, Günthardt-Goerg MS (2013) Seasonal photosynthetic responses of European oaks to drought and elevated daytime temperature. Plant Biol 15:169–176
Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525
Bachofen C, Wohlgemuth T, Moser B (2019) Biomass partitioning in a future dry and CO2 enriched climate: shading aggravates drought effects in Scots pine but not European black pine seedlings. J Appl Ecol 56:866–879
Bloom AJ, Chapin FS, Mooney HA (1985) Plants—an economic analogy. Annu Rev Ecol Syst 16:363–392
Buchmann N, Ehleringer JR (1998) CO2 concentration profiles, and carbon and oxygen isotopes in C3 and C4 crop canopies. Agric For Meteorol 89:45–58
Buchmann N, Kao WY, Ehleringer JR (1996) Carbon dioxide concentrations within forest canopies—variation with time, stand structure, and vegetation type. Glob Chang Biol 2:421–432
Buchmann N, Guehl JM, Barigah TS, Ehleringer JR (1997a) Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110:120–131
Buchmann N, Kao WY, Ehleringer J (1997b) Influence of stand structure on carbon-13 of vegetation, soils, and canopy air within deciduous and evergreen forests in Utah, United States. Oecologia 110:109–119
Buckley TN, Cescatti A, Farquhar GD (2013) What does optimization theory actually predict about crown profiles of photosynthetic capacity when models incorporate greater realism? Plant Cell Environ 36:1547–1563
Catoni R, Gratani L, Sartori F et al (2015) Carbon gain optimization in five broadleaf deciduous trees in response to light variation within the crown: correlations among morphological, anatomical and physiological leaf traits. Acta Bot Croat 74:71–94
Chapin FS, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57
Coble AP, Cavaleri MA (2015) Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment. Oecologia 177:1131–1143
Coble AP, Cavaleri MA, Niinemets Ü (2014) Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest. Tree Physiol 34:146–158
Delucia EH, Schlesinger WH (1991) Resource-use efficiency and drought tolerance in adjacent Great Basin and Sierran plants. Ecology 72:51–58
Dewar RC, Tarvainen L, Parker K et al (2012) Why does leaf nitrogen decline within tree canopies less rapidly than light? An explanation from optimization subject to a lower bound on leaf mass per area. Tree Physiol 32:520–534
Duursma RA, Marshall JD (2006) Vertical canopy gradients in δ13C correspond with leaf nitrogen content in a mixed-species conifer forest. Trees Struct Funct 20:496–506
Ellsworth DS, Reich PB (1992) Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seedlings in contrasting forest light environments. Funct Ecol 6:423–435
Ellsworth DS, Reich PB (1993) Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96:169–178
Etzold S, Buchmann N, Eugster W (2010) Contribution of advection to the carbon budget measured by eddy covariance at a steep mountain slope forest in Switzerland. Biogeosciences 7:2461–2475
Etzold S, Ruehr NK, Zweifel R et al (2011) The carbon balance of two contrasting mountain forest ecosystems in Switzerland: similar annual trends, but seasonal differences. Ecosystems 14:1289–1309
Evans JR (1989) Photosynthesis and nitrogen relationship in leaves of C3 plants. Oecologia 78:9–19
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 24:755–767
Evans JR, Seemann JR (1989) The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. In: Briggs W (ed) Photosynthesis. Alan R. Liss Inc., New York, pp 183–205
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40:503–537
Field C, Merino J, Mooney HA (1983) Compromises between water-use efficiency and nitrogen-use efficiency in five species of California evergreens. Oecologia 60:384–389
Guehl JM, Aussenac G, Bouachrine J et al (1991) Sensitivity of leaf gas exchange to atmospheric drought, soil drought, and water-use efficiency in some Mediterranean Abies species. Can J For Res 21:1507–1515
Hanba YT, Mori S, Lei TT et al (1997) Variations in leaf δ13C along a vertical profile of irradiance in a temperate Japanese forest. Oecologia 110:253–261
Hartmann H, Adams HD, Hammond WM et al (2018) Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environ Exp Bot 152:7–18
Hikosaka K, Niinemets Ü, Anten NPR (2016) Canopy photosynthesis: from basics to applications. Springer, Berlin, Heidelberg
Jones HG (1992) Plants and microclimate: a quantitative approach to environmental plant physiology. Cambridge University Press, Cambridge
Jones HG (1998) Stomatal control of photosynthesis and transpiration. J Exp Bot 49:387–398
Kuznetsova A, Bruun BP, Christensen RHB (2017) lmerTest: tests for random and fixed effects for linear mixed effect models. J Stat Softw 82:1–26
Lange OL, Führer G, Gebel J (1986) Rapid field determination of photosynthetic capacity of cut spruce twigs (Picea abies) at saturating ambient CO2. Trees 1:70–77
Maire V, Martre P, Kattge J et al (2012) The coordination of leaf photosynthesis links C and N fluxes in C3 plant species. PLoS One 7:1–15
Meir P, Kruijt B, Broadmeadow M et al (2002) Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant Cell Environ 25:343–357
Meng F, Arp PA (1992) Net photosynthesis and stomatal conductance of red spruce twigs before and after twig detachment. Can J For Res 23:716–721
Nabeshima E, Hiura T (2004) Size dependency of photosynthetic water- and nitrogen-use efficiency and hydraulic limitation in Acer mono. Tree Physiol 24:745–752
Niinemets Ü (2016) Leaf age dependent changes in within-canopy variation in leaf functional traits: a meta-analysis. J Plant Res 129:313–338
Niinemets Ü, Anten NPR (2009) Packing the photosynthetic machinery: from leaf to canopy. Photosynthesis in silico. Springer, Berlin, Heidelberg, pp 363–399
Niinemets U, Kull O, Tenhunen JD (1998) An analysis of light effects on foliar morphology, physiology, and light interception in temperate deciduous woody species of contrasting shade tolerance. Tree Physiol 18:681–696
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 205:973–993
Norman JM (1993) Scaling processes between leaf and canopy levels. In: Ehleringer Field (ed) Scaling physiological processes: leaf to globe. Academic Press, San Diego, pp 41–76
Oldham AR, Sillett SC, Tomescu AMF, Koch GW (2010) The hydrostatic gradient, not light availability, drives height-related variation in Sequoia sempervirens (Cupressaceae) leaf anatomy. Am J Bot 97:1087–1097
Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2014) Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340:741–745
Panek JA, Waring RH (1995) Carbon isotope variation in Douglas-fir foliage: improving the δ13C-climate relationship. Tree Physiol 15:657–663
Pao Y-C, Chen T-W, Moualeu-Ngangue DP, Stützel H (2018) Environmental triggers for photosynthetic protein turnover determine the optimal nitrogen distribution and partitioning in the canopy. J Exp Bot 70:2419–2434
Paul-Limoges E, Wolf S, Eugster W et al (2017) Below-canopy contributions to ecosystem CO2 fluxes in a temperate mixed forest in Switzerland. Agric For Meteorol 247:582–596
Paul-Limoges E, Damm A, Hueni A et al (2018) Effect of environmental conditions on sun-induced fluorescence in a mixed forest and a cropland. Remote Sens Environ 219:310–323
Paul-Limoges E, Wolf S, Schneider FD et al (2020) Partitioning evapotranspiration with concurrent eddy covariance measurements in a mixed forest. Agric For Meteorol 280:107786
Peltoniemi MS, Duursma RA, Medlyn BE (2012) Co-optimal distribution of leaf nitrogen and hydraulic conductance in plant canopies. Tree Physiol 32:510–519
Pflug EE, Buchmann N, Siegwolf RTW et al (2018) Resilient leaf physiological response of European beech (Fagus sylvatica L.) to Summer drought and drought release. Front Plant Sci 9:1–11
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
Renninger HJ, Carlo NJ, Clark KL, Schäfer KVR (2015) Resource use and efficiency, and stomatal responses to environmental drivers of oak and pine species in an Atlantic Coastal Plain forest. Front Plant Sci 6:1–16
Robakowski P, Antczak P (2008) Ability of silver fir and European beech saplings to acclimate photochemical processes to the light environment under different canopies of trees. Polish J Ecol 56:3–16
Robakowski P, Montpied P, Dreyer E (2003) Plasticity of morphological and physiological traits in response to different levels of irradiance in seedlings of silver fir (Abies alba Mill). Trees Struct Funct 17:431–441
Seiwa K (1999) Changes in leaf phenology are dependent on tree height in Acer mono, a deciduous broad-leaved tree. Ann Bot 83:355–361
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432
Terashima I, Hikosaka K (1995) Comparative ecophysilogy of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257
Valladares F, Chico JM, Aranda I et al (2002) The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees Struct Funct 16:395–403
Vitasse Y (2013) Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol 198:149–155
Walker AP, Beckerman AP, Gu L et al (2014) The relationship of leaf photosynthetic traits—Vcmax and Jmax—to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecol Evol 4:3218–3235
Waring RH, Silvester WB (1994) Variation in foliar carbon-13 values within the crowns of Pinus radiata trees. Tree Physiol 14:1203–1213
Werner RA, Bruch BA, Brand WA (1999) ConFlo III—an interface for high precision δ13C and δ15N analysis with an extended dynamic range. Rapid Commun Mass Spectrom 13:1237–1241
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Zeeman MJ, Werner RA, Eugster W et al (2008) Optimization of automated gas sample collection and isotope ratio mass spectrometric analysis of δ13C of CO2 in air. Rapid Commun Mass Spectrom 22:3883–3892
Zhou Y, Wu X, Ju W et al (2016) Global parameterization and validation of a two-leaf light use efficiency model for predicting gross primary production across FLUXNET sites. J Geophys Res Biogeosci 121:1045–1072
Acknowledgements
We are grateful to E. Merz, A. Marchetti, Y. Liu, and A. Ackermann for their assistance with field and laboratory work, and T. Baur for maintenance of the equipment at the research site. We also thank M. Gysin and A. Erni for providing samples and measurements from the tree canopy. This project was funded by the State Secretariat for Education, Research and Innovation (SERI) in the frame of COST Action ES1309 (C15.0053).
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N.B., P.D., and C.B. conceived and planned the study; field work and data analyses were carried out by C.B., supported by P.D. and N.B.; C.B., P.D., and N.B. wrote the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Bachofen, C., D’Odorico, P. & Buchmann, N. Light and VPD gradients drive foliar nitrogen partitioning and photosynthesis in the canopy of European beech and silver fir. Oecologia 192, 323–339 (2020). https://doi.org/10.1007/s00442-019-04583-x
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DOI: https://doi.org/10.1007/s00442-019-04583-x