Abstract
Rising temperatures pose a threat to the stability of climate regulation by carbon metabolism in subtropical forests. Although the effects of temperature on leaf carbon metabolism traits in sun-exposed leaves are well understood, there is limited knowledge about its impacts on shade leaves and the implications for ecosystem–climate feedbacks. In this study, we measured temperature response curves of photosynthesis and respiration for 62 woody species in summer (including both evergreen and deciduous species) and 20 evergreen species in winter. The aim was to uncover the temperature dependence of carbon metabolism in both sun and shade leaves in subtropical forests. Our findings reveal that shade had no significant effects on the mean optimum photosynthetic temperatures (TOpt) or temperature range (T90). However, there were decreases observed in mean stomatal conductance, mean area-based photosynthetic rates at TOpt and 25 °C, as well as mean area-based dark respiration rates at 25 °C in both evergreen and deciduous species. Moreover, the respiration–temperature sensitivity (Q10) of sun leaves was higher than that of shade leaves in winter, with the reverse being true in summer. Leaf economics spectrum traits, such as leaf mass per area, and leaf concentration of nitrogen and phosphorus across species, proved to be good predictors of TOpt, T90, mass-based photosynthetic rate at TOpt, and mass-based photosynthetic and respiration rate at 25 °C. However, Q10 was poorly predicted by these leaf economics spectrum traits except for shade leaves in winter. Our results suggest that model estimates of carbon metabolism in multilayered subtropical forest canopies do not necessitate independent parameterization of T90 and TOpt temperature responses in sun and shade leaves. Nevertheless, a deeper understanding and quantification of canopy variations in Q10 responses to temperature are necessary to confirm the generality of temperature–carbon metabolism trait responses and enhance ecosystem model estimates of carbon dynamics under future climate warming.
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References
Anderegg LD, Berner LT, Badgley G, Sethi ML, Law BE, HilleRisLambers J (2018) Within-species patterns challenge our understanding of the leaf economics spectrum. Ecol Lett 21:734–744
Arora VK, Boer GJ, Friedlingstein P et al (2013) Carbon-concentration and carbon-climate feedbacks in CMIP5 earth system models. J Clim 26:5289–5314
Aspinwall MJ, Vårhammar A, Blackman CJ et al (2017) Adaptation and acclimation both influence photosynthetic and respiratory temperature response in Corymbia calophylla. Tree Physiol 37:1095–1112
Atkin O, Tjoelker M (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351
Atkin OK, Holly C, Ball MC (2000) Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant Cell Environ 23:15–26
Atkin OK, Bruhn D, Hurry VM et al (2005) The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct Plant Biol 32:87–105
Battaglia M, Beadle C, Loughhead S (1996) Photosynthetic temperature responses of Eucalyptus globulus and Eucalyptus nitens. Tree Physiol 16:81–89
Bernacchi CJ, Singsaas EL, Pimentel C et al (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24:253–259
Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543
Blomberg SP, Garland JT, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449
Bryla DR, Bouma TJ, Eissenstat DM (1997) Root respiration in citrus acclimates to temperature and slows during drought. Plant Cell Environ 20:1411–1420
Bryla DR, Bouma TJ, Hartmond U, Eissenstat DM (2001) Influence of temperature and soil drying on respiration of individual roots in citrus: Integrating greenhouse observations into a predictivemodel for the field. Plant Cell Environ 24:781–790
Cheesman AW, Winter K (2013) Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings. J Exp Bot 64:3817–3828
Chen XP, Sun J, Wang MT, Lyu M, Niklas KJ, Michaletz ST, Zhong QL, Cheng DL (2020) The leaf economics spectrum constrains phenotypic plasticity across a light gradient. Front Plant Sci 11:735
Chi Y, Xu M, Shen R et al (2013) Acclimation of foliar respiration and photosynthesis in response to experimental warming in a temperate steppe in northern China. PLoS ONE 8:e56482
Coley PD (1988) Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74:531–536
Crous KY, Quentin AG, Lin YS et al (2013) Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Glob Chang Biol 19:3790–3807
Crous KY, Uddling J, De Kauwe M (2022) Temperature responses of photosynthesis and respiration in evergreen trees from boreal to tropical latitudes. New Phytol 234:353–374
Diffenbaugh NS, Scherer M (2011) Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries. Clim Change 107:615–624
Dillaway DN, Kruger EL (2010) Thermal acclimation of photosynthesis: a comparison of boreal and temperate tree species along a latitudinal transect. Plant Cell Environ 33:888–899
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930
Doughty CE, Goulden ML (2008) Are tropical forests near a high temperature threshold? J Geophys Res Biogeosci 113:G00B07
Dufresne JL, Foujols MA, Denvil S et al (2013) Climate change projections using the IPSL-CM5 Earth System Model: from CMIP3 to CMIP5. Clim Dyn 40:2123–2165
Erratum (1985) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 166:437–437
Fauset S, Freitas HC, Galbraith DR et al (2018) Differences in leaf thermoregulation and water-use strategies between three co-occurring Atlantic Forest tree species. Plant Cell Environ 41:1618–1631
Griffin KL, Turnbull MH, Murthy R et al (2002) Canopy position affects the temperature response of leaf respiration in Populus deltoids. New Phytol 154:609–619
Gunderson CA, Norby RJ, Wullschleger SD (2000) Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence. Tree Physiol 20:87–96
Gunderson CA, O’Hara KH, Campion CM et al (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Change Biol 16:2272–2286
Harley PC, Baldocchi DD (1995) Scaling carbon dioxide and water vapour exchange from leaf to canopy in a deciduous forest. I. Leaf model parametrization. Plant Cell Environ 18:1146–1156
He L, Chen JM, Gonsamo A, Luo X, Wang R, Liu Y, Liu R (2018) Changes in the shadow: the shifting role of shaded leaves in global carbon and water cycles under climate change. Geophys Res Lett 45:5052–5061
Hernández GG, Winter K, Slot M (2020) Similar temperature dependence of photosynthetic parameters in sun and shade leaves of three tropical tree species. Tree Physiol 40:637–651
Heskel MA, O’Sullivan OS, Reich PB et al (2016) Convergence in the temperature response of leaf respiration across biomes and plant functional types. Proc Natl Acad Sci USA 113:3832–3837
Hikosaka K, Ishikawa K, Borjigidai A et al (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J Exp Bot 57:291–302
Huntingford C, Atkin OK, Martinez-de la Torre A et al (2017) Implications of improved representation of plant respiration in a changing climate. Nat Commun 8:1–11
Koike T, Kitao M, Maruyama Y, Mori S, Lei TT (2001) Leaf morphology and photosynthetic adjustments among deciduous broad-leaved trees within the vertical canopy profile. Tree Physiol 21:951–958
Kositsup B, Montpied P, Kasemsap P et al (2009) Photosynthetic capacity and temperature responses of photosynthesis of rubber trees (Hevea brasiliensis Müll. Arg.) acclimate to changes in ambient temperatures. Trees 23:357–365
Krause GH, Cheesman AW, Winter K et al (2013) Thermal tolerance, net CO2 exchange and growth of a tropical tree species, Ficus insipida, cultivated at elevated daytime and nighttime temperatures. J Plant Physiol 170:822–827
Kumarathunge DP, Medlyn BE, Drake JE et al (2018) Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale. New Phytol 222:768–784
Lachapelle PP, Shipley B (2012) Interspecific prediction of photosynthetic light response curves using specific leaf mass and leaf nitrogen content: effects of differences in soil fertility and growth irradiance. Ann Bot 109:1149–1157
Lin H, Chen Y, Zhang H et al (2017) Stronger cooling effects of transpiration and morphology of the plants from a hot dry habitat than from a hot wet habitat. Funct Ecol 31:2202–2211
Loveys BR, Scheurwater I, Pons TL et al (2002) Growth temperature influences the underlying components of relative growth rate: an investigation using inherently fast- and slow-growing plant species. Plant Cell Environ 25:975–987
Malhi Y, Aragão LEOC, Metcalfe DB et al (2009) Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Glob Change Biol 15:1255–1274
Malhi Y, Girardin CAJ, Goldsmith GR et al (2017) The variation of productivity and its allocation along a tropical elevation gradient: a whole carbon budget perspective. New Phytol 21:1019–1032
Marino G, Aqil M, Shipley B (2010) The leaf economics spectrum and the prediction of photosynthetic light-response curves. Funct Ecol 24:263–272
Michaletz ST, Weiser MD, Mcdowell NG et al (2016) The energetic and carbon economic origins of leaf thermoregulation. Nat Plants 2:16129
Mori S, Yamaji K, Ishida A, Prokushkin SG, Masyagina OV, Hagihara A et al (2010) Mixed-power scaling of whole-plant respiration from seedlings to giant trees. Proc Natl Acad Sci U S A 107:1447–1451
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
Niklas KJ, Cobb ED (2010) Ontogenetic changes in the numbers of short- vs. long-shoots account for decreasing specific leaf area in acer rubrum aceraceae. as trees increase in size. Am J Bot 97:27–37
Niu S, Li Z, Xia J et al (2008) Climatic warming changes plant photosynthesis and its temperature dependence in a temperate steppe of northern China. Environ Exp Bot 63:91–101
Noguchi K, Terashima I (1997) Different regulation of leaf respiration between Spinacia oleracea, a sun species, and Alocasia odora, a shade species. Physiol Plant 101:1–7
Norby RJ, Gu L, Haworth IC et al (2017) Informing models through empirical relationships between foliar phosphorus, nitrogen and photosynthesis across diverse woody species in tropical forests of Panama. New Phytol 215:1425–1437
O’Sullivan OS, Weerasinghe KWLK, Evans JR et al (2013) High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function. Plant Cell Environ 36:1268–1284
O’sullivan OS, Heskel MA, Reich PB et al (2016) Thermal limits of leaf metabolism across biomes. Glob Change Biol 23:209–223
Padfield D, Yvon-Durocher G, Buckling A et al (2016) Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecol Lett 19:133–142
Pan Y, Birdsey RA, Phillips OL et al (2013) The structure, distribution, and biomass of the world’s forests. Annu Rev Ecol Evol Syst 44:593–622
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Reich PB, Walters MB, Ellsworth DS et al (1998) Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114:471–482
Reich PB, Sendall KM, Stefanski A et al (2016) Boreal and temperate trees show strong acclimation of respiration to warming. Nature 531:633–636
Salvucci ME, Crafts-Brner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plantarum 120:179–186
Scafaro AP, Xiang S, Long BM et al (2017) Strong thermal acclimation of photosynthesis in tropical and temperate wet-forest tree species: the importance of altered Rubisco content. Glob Change Biol 23:2783–2800
Scott D (1970) Relative growth rates under controlled temperatures of some New Zealand indigenous and introduced grasses. N Z J Bot 8:76–81
Sendall KM, Reich PB, Zhao C et al (2015) Acclimation of photosynthetic temperature optima of temperate and boreal tree species in response to experimental forest warming. Glob Chang Biol 21:1342–1357
Shaver GR (1981) Mineral nutrition and leaf longevity in an Evergreen Shrub, Ledum palustre ssp. decumbens. Oecologia 49:362–365
Slot M, Kitajima K (2015) General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types. Oecologia 177:885–900
Slot M, Winter K (2017) In situ temperature response of photosynthesis of 42 tree and liana species in the canopy of two Panamanian lowland tropical forests with contrasting rainfall regimes. New Phytol 214:1103–1117
Slot M, Rey-Sánchez C, Winter K et al (2015) Trait-based scaling of temperature-dependent foliar respiration in a species-rich tropical forest canopy. Funct Ecol 28:1074–1086
Slot M, Garcia MN, Winter K (2016) Temperature response of CO2 exchange in three tropical tree species. Funct Plant Biol 43:468–478
Slot M, Winter K (2016) The effects of rising temperature on the ecophysiology of tropical forest trees. In: Tropical Tree Physiol. Springer, Cham, pp 385–412
Stinziano JR, Way DA, Bauerle WL (2018) Improving models of photosynthetic thermal acclimation: which parameters are most important and how many should be modified? Glob Chang Biol 24:1580–1598
Tan ZH, Zeng J, Zhang YJ et al (2017) Optimum air temperature for tropical forest photosynthesis: mechanisms involved and implications for climate warming. Environ Res Lett 12:054022
Tarelkin Y, Hufkens K, Hahn S et al (2019) Wood anatomy variability under contrasted environmental conditions of common deciduous and evergreen species from central African forests. Trees 33:893–909
Tenkanen A, Suprun S, Oksanen E et al (2021) Strategy by latitude? Higher photosynthetic capacity and root mass fraction in northern than southern silver birch (Betula pendula Roth) in uniform growing conditions. Tree Physiol 41:974–991
Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351
Tjoelker MG, Reich PB, Oleksyn J (1999) Changes in leaf nitrogen and carbohydrates underlie temperature and CO2, acclimation of dark respiration in five boreal tree species. Plant Cell Environ 22:767–778
Tjoelker MG, Oleksyn J, Reich PB (2001) Modelling respiration of vegetation: evidence for a general temperature-dependent Q10. Glob Change Biol 7:223–230
Tjoelker MG, Oleksyn J, Reich PB et al (2008) Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations. Glob Change Biol 14:782–797
Tjoelker MG, Oleksyn J, Lorencplucinska G et al (2009) Acclimation of respiratory temperature responses in northern and southern populations of Pinus banksiana. New Phytol 181:218–229
Varhammar A, Wallin G, McLean CM et al (2015) Photosynthetic temperature responses of tree species in Rwanda: evidence of pronounced negative effects of high temperature in montane rainforest climax species. New Phytol 206:1000–1012
Vinod N, Slot M, McGrego IR et al (2023) Thermal sensitivity across forest vertical profiles: patterns, mechanisms, and ecological implications. New Phytol 237:22–47
Way DA, Yamori W (2014) Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynth Res 119:89–100
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Wright IJ, Leishman MR, Read C et al (2006) Gradients of light availability and leaf traits with leaf age and canopy position in 28 Australian shrubs and trees. Funct Plant Biol 33:407–419
Wyka TP, Karolewski P, Żytkowiak R, Chmielarz P, Oleksyn J (2016) Whole-plant allocation to storage and defense in juveniles of related evergreen and deciduous shrub species. Tree Physiol 5:536–547
Yamaguchi DP, Nakaji T, Hiura T, Hikosaka K (2016) Effects of seasonal change and experimental warming on the temperature dependence of photosynthesis in the canopy leaves of Quercus serrata. Tree Physiol 36:1283–1295
Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117
Yoder BJ, Ryan MG, Waring RH, Kaufmann MR (1994) Evidence of reduced photosynthetic rates in old trees. Forest Sci 40:513–527
Zanne AE, Tank DC, Cornwell WK et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92
Zhou X, Liu X, Wallace LL, Luo WY (2007) Photosynthetic and respiratory acclimation to experimental warming for four species in a tallgrass prairie ecosystem. J Integr Plant Biol 49:270–281
Acknowledgements
We would like to thank L.Q. Zhu and X.G. Le for facilitating this study at the Yangjifeng National Nature Reserve.
Funding
This work was financially supported by the National Natural Science Foundation of China (32071555, 31971643, and 32001094); the Major S&T Project of Fujian Province (2019N5009); Fujian Provincial Department of Education Grant (JAT190084). JP was supported by the Spanish Government Grant PID2020115770RB-I, TED2021-132627 B-I00, funded by MCIN, AEI/10.13039/501100011033 European Union Next Generation EU/PRTR, and the Fundación Ramón Areces grant CIVP20A6621.
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XPC, DLC, QLZ, and DDH planned and designed the research. XPC, JLL and XQL performed experiments, conducted fieldwork, analyzed data, etc. XPC, MTW, DLC, and PJ wrote the manuscript.
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Communicated by Ülo Niinemets.
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Chen, X., Li, J., Peñuelas, J. et al. Temperature dependence of carbon metabolism in the leaves in sun and shade in a subtropical forest. Oecologia 204, 59–69 (2024). https://doi.org/10.1007/s00442-023-05487-7
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DOI: https://doi.org/10.1007/s00442-023-05487-7