ACKNOWLEDGEMENTS
This research was supported by the Smithsonian Tropical Research Institute (STRI). The authors thank Milton Garcia for installing and maintaining the temperature and CO2 control and monitoring system and Jorge Aranda for establishing and watering the plants. MS was supported by the Earl S. Tupper–STRI postdoctoral fellowship. SWR was supported by The Oxford Martin School Climate Partnership with the Nature Conservancy. We are grateful for the feedback provided by N.G. Smith and one anonymous reviewer on a previous version of the paper.
REFERENCESAinsworth, E.A. & Rogers, A. (2007). The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant, Cell & Environment, 30(3), 258–270. Arp, W.J. (1991). Effects of source‐sink relations on photosynthetic acclimation to elevated CO2. Plant, Cell & Environment, 14(8), 869–875. Atkin, O.K. & Tjoelker, M.G. (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science, 8(7), 343-351. Atkin, O.K., Bruhn, D. & Tjoelker, M.G. (2005) Response of plant respiration to changes in temperature: mechanisms and consequences of variations in Q10 values and acclimation. In: Plant respiration (pp. 95–135). Springer, Dordrecht. Bernacchi, C.J., Singsaas E.L., Pimentel C., Portis Jr A.R. & Long S.P. (2001). Improved temperature response functions for models of Rubisco‐limited photosynthesis. Plant, Cell & Environment, 24(2), 253–259. Berry, J. & Björkman, O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31(1), 491–543. Berryman, C.A., Eamus, D. & Duff, G.A. (1994) Stomatal responses to a range of variables in two tropical tree species grown with CO2 enrichment. Journal of Experimental Botany, 45(5), 539–546. Booth, B.B., Jones, C.D., Collins, M., Totterdell, I.J., Cox, P.M., Sitch, S., Huntingford, C., Betts, R.A., Harris, G.R. & Lloyd, J. (2012) High sensitivity of future global warming to land carbon cycle processes. Environmental Research Letters, 7(2), p.024002. Brooks, A. & Farquhar, G.D. (1985). Effect of temperature on the CO2/O2 specificity of ribulose-1, 5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta, 165(3), 397–406. Bürkner, P.-C. (2018). Advanced Bayesian Multilevel Modeling with the R Package brms. The R Journal, 10(1), 395−411. von Caemmerer, S., & Farquhar G.D. (1981). Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Planta, 153(4), 376–387. Cernusak, L.A., Winter, K., Martínez, C., Correa, E., Aranda, J., Garcia, M., Jaramillo, C. & Turner, B.L., 2011. Responses of legume versus nonlegume tropical tree seedlings to elevated CO2concentration. Plant Physiology, 157(1), 372–385. Cheesman, A.W. & Winter, K. (2013). Elevated night‐time temperatures increase growth in seedlings of two tropical pioneer tree species.New Phytologist, 197(4), 1185–1192. Condit, R., Pérez, R. & Daguerre, N. (2010). Trees of Panama and Costa Rica. Princeton University Press. Corlett, R.T. (2011) Impacts of warming on tropical lowland rainforests.Trends in Ecology &. Evolution, 26(11), 145–150. Crous, K.Y., Drake, J.E., Aspinwall, M.J., Sharwood, R.E., Tjoelker, M.G. & Ghannoum, O. (2018) Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species. Global Change Biology, 24(10), 4626–4644
Doughty, C.E. (2011). An in situ leaf and branch warming experiment in the Amazon. Biotropica , 43(6), 658–665.
Dusenge, M.E., Madhavji, S. & Way, D.A. (2020). Contrasting acclimation responses to elevated CO2 and warming between an evergreen and a deciduous boreal conifer. Global Change Biology, 26(6), 3639−3657. Duursma, R.A. (2015). Plantecophys-an R Package for analysing and modelling leaf gas exchange data. PloS one 10(11), e0143346. Farquhar, G.D., von Caemmerer S. & Berry J.A. (1980). A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149(1), 78–90. Farquhar G.D. & Sharkey T.D. (1982). Stomatal conductance and photosynthesis. Annual Review of Plant Physiology, 33(1), 317–345. Fauset, S., Oliveira, L., Buckeridge, M.S., Foyer, C.H., Galbraith, D., Tiwari, R. & Gloor, M. (2019) Contrasting responses of stomatal conductance and photosynthetic capacity to warming and elevated CO2 in the tropical tree species Alchornea glandulosa under heatwave conditions. Environmental and Experimental Botany, 158, 28–39. Gunderson, C.A., O’Hara, K.H., Campion, C.M., Walker, A.V. & Edwards, N.T. (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Global Change Biology, 16(8), 2272−2286. Hernández, G.G., Winter K, & Slot M. (2020) Similar temperature dependence of photosynthetic parameters in sun and shade leaves of three tropical tree species. Tree Physiology, 40(5), 637−651. Hikosaka, K., Ishikawa, K., Borjigidai, A., Muller, O. & Onoda, Y. (2006) Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate.Journal of Experimental Botany, 57(2), 291–302. Kattge, J. & Knorr W. (2007). Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species.Plant, Cell & Environment, 30(9), 1176–1190. Klein, T. & Ramon, U. (2019) Stomatal sensitivity to CO2 diverges between angiosperm and gymnosperm tree species. Functional Ecology, 33(8), 1411–1424. Körner, C. & Würth, M. (1996). A simple method for testing leaf responses of tall tropical forest trees to elevated CO2.Oecologia, 107(4), 421–425. Kositsup, B., Montpied, P., Kasemsap, P., Thaler, P., Améglio, T. & Dreyer, E. (2009) Photosynthetic capacity and temperature responses of photosynthesis of rubber trees (Hevea brasiliensis Müll. Arg.) acclimate to changes in ambient temperatures. Trees, 23(2), 357−365. Kumarathunge, D.P., Medlyn, B.E., Drake, J.E., Tjoelker, M.G., Aspinwall, M.J., Battaglia, M., Cano, F.J., Carter, K.R., Cavaleri, M.A., Cernusak, L.A. et al. (2019) Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale. New Phytologist, 222(2), 768–784. Leakey, A.D.B., Xu, F., Gillespie, K.M., McGrath, J.M., Ainsworth, E.A. & Ort, D.R. (2009) Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide. Proceedings of the National Academy of Sciences, 106(9), 3597–3602. Leakey, A.D., Bishop, K.A. & Ainsworth, E.A. (2012) A multi-biome gap in understanding of crop and ecosystem responses to elevated CO2. Current Opinion in Plant Biology, 15(3), 228–236. Lin, Y.S., Medlyn B.E., & Ellsworth D.S. (2012) Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiology, 32(2), 219–231. Lombardozzi, D.L., Bonan, G.B., Smith, N.G., Dukes, J.S., & Fisher, R.A. (2015). Temperature acclimation of photosynthesis and respiration: A key uncertainty in the carbon cycle‐climate feedback.Geophysical Research Letters, 42(20), 8624–8631. Long, S.P. (1991). Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2concentrations: has its importance been underestimated? Plant, Cell & Environment, 14(8), 729–739. Long, S.P., Ainsworth, E.A., Rogers, A. & Ort, D.R. (2004) Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology, 55, 591–628. Lovelock, C.E., Winter, K., Mersits, R. & Popp, M. (1998). Responses of communities of tropical tree species to elevated CO2 in a forest clearing.Oecologia, 116(1-2), 207–218. Lovelock, C.E., Virgo, A., Popp, M., & Winter, K. (1999) Effects of elevated CO2 concentrations on photosynthesis, growth and reproduction of branches of the tropical canopy tree species,Luehea seemannii Tr. & Planch. Plan,t Cell & Environment, 22(1), 49–59. Luo, Y., Field, C.B., & Mooney, H.A. (1994). Predicting responses of photosynthesis and root fraction to elevated [CO2] a: interactions among carbon, nitrogen, and growth. Plant, Cell & Environment, 17(11), 1195–1204. Luo, Y., Su, B.O., Currie, W.S., Dukes, J.S., Finzi, A., Hartwig, U., et al. (2004). Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. AIBS Bulletin, 54(8), 731–739. Marchin, R.M., Broadhead, A.A., Bostic, L.E., Dunn, R.R., & Hoffmann, W.A. (2016). Stomatal acclimation to vapour pressure deficit doubles transpiration of small tree seedlings with warming. Plant, Cell & Environment, 39(10), 2221–2234. Mediavilla, S. & Escudero, A. (2004). Stomatal responses to drought of mature trees and seedlings of two co-occurring Mediterranean oaks.Forest Ecology and Management, 187(2-3), 281−294. Medlyn, B.E., Badeck, F.W., De Pury, D.G.G., Barton, C.V.M., Broadmeadow, M., Ceulemans, R., et al. (1999). Effects of elevated [CO2] on photosynthesis in European forest species: a meta‐analysis of model parameters. Plant, Cell & Environment, 22(12), 1475–1495. Medlyn, B.E., Barton, C.V.M., Broadmeadow, M.S.J., Ceulemans, R., De Angelis, P., Forstreuter, M., Freeman, M., Jackson, S.B., Kellomäki, S., Laitat, E. et al. (2001). Stomatal conductance of forest species after long‐term exposure to elevated CO2 concentration: a synthesis. New Phytologist, 149(2), 247−264. Medlyn, B.E., Dreyer E., Ellsworth D., Forstreuter M., Harley P.C., Kirschbaum M.U.F., et al. (2002). Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment, 25(9), 1167–1179. Mercado, L.M., Medlyn, B.E., Huntingford, C., Oliver, R.J., Clark, D.B., Sitch, S., Zelazowski, P., Kattge, J., Harper, A.B. & Cox, P.M. (2018) Large sensitivity in land carbon storage due to geographical and temporal variation in the thermal response of photosynthetic capacity.New Phytologist, 218(4), 1462–1477. Moore, B.D., Cheng, S.-H., Sims, D. & Seemann J.R. (1999) The biochemical and molecular basis for photosynthetic acclimation to elevated CO2. Plant, Cell & Environment, 22(6), 567–582. Neales, T., & Incoll, L.D. (1968). The control of leaf photosynthesis rate by the level of assimilate concentration in the leaf: A review of the hypothesis. Botanical Review, 34(2), 107–125. R Development Core Team. (2018) R: a language and environment for statistical computing. R v.3.5.2. R Foundation for Statistical Computing, Vienna, Austria. Rifai, S.W., Li, S. & Malhi, Y. (2019) Coupling of El Niño events and long-term warming leads to pervasive climate extremes in the terrestrial tropics. Environmental Research Letters, 14(10), 105002. Sage, R.F. (1994) Acclimation of photosynthesis to increasing atmospheric CO2: the gas exchange perspective.Photosynthesis Research, 39(3), 351–368. Sage, R.F., & Kubien D.S. (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell Environment, 30(9), 1086–1106. Sage, R.F., Way D.A., & Kubien D.S. (2008) Rubisco, Rubisco activase, and global climate change. Journal of Experimental Botany, 59(7), 1581–1595. Saxe, H., Ellsworth, D.S. & Heath, J. (1998) Tree and forest functioning in an enriched CO2 atmosphere. New Phytologist, 139(3), 395–436. Scafaro, A.P., Xiang S., Long B.M., Bahar N.H., Weerasinghe L.K., Creek D., et al. (2017). Strong thermal acclimation of photosynthesis in tropical and temperate wet‐forest tree species: the importance of altered Rubisco content. Global Change Biology, 23(7), 2783–2800. Slot, M., Rey-Sánchez, C., Gerber, S., Lichstein, J.W., Winter, K., & Kitajima, K. (2014) Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical forest carbon balance. Global Change Biology, 20(9), 2915–2926. Slot, M., & Kitajima, K. (2015) General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types.Oecologia, 177(3), 885–900. Slot, M., Garcia, M.N., & Winter, K. (2016) Temperature response of CO2 exchange in three tropical tree species.Functional Plant Biology, 43(5), 468–478. Slot, M., & Winter, K. (2017a). Photosynthetic acclimation to warming in tropical forest tree seedlings. Journal of Experimental Botany, 68(9), 2275–2284. Slot, M., & Winter, K. (2017b). In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species. Plant, Cell & Environment, 40(12), 3055–3068. Slot, M., & Winter, K. (2017c) 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 Phytologist, 214(3), 1103–1117. Slot, M. & Winter, K. (2018) High tolerance of tropical sapling growth and gas exchange to moderate warming. Functional Ecology, 32(3), 599–611. Smith, M.N., Taylor, T.C., van Haren, J., Rosolem, R., Restrepo-Coupe, N., Adams, J., Wu, J., de Oliveira, R.C., da Silva, R., de Araujo, A.C. et al. (2020) Empirical evidence for resilience of tropical forest photosynthesis in a warmer world. Nature Plants, 6(10), 1225−1230. Smith, N.G., & Dukes, J.S. (2013). Plant respiration and photosynthesis in global‐scale models: incorporating acclimation to temperature and CO2. Global Change Biology, 19(1), 45–63. Smith, N.G., Malyshev, S.L., Shevliakova, E., Kattge, J., & Dukes, J.S. (2016). Foliar temperature acclimation reduces simulated carbon sensitivity to climate. Nature Climate Change, 6(4), 407. Smith, N.G., & Dukes, J.S. (2018). Drivers of leaf carbon exchange capacity across biomes at the continental scale. Ecology, 99(7), 1610–1620. Stan Development Team (2018) Stan Modeling Language User’s Guide and Reference Manual, Version 2.18.0 (2018). http://mc-stan.org/ Stinziano, J.R., Way, D.A., & Bauerle, W.L. (2018). Improving models of photosynthetic thermal acclimation: Which parameters are most important and how many should be modified? Global Change Biology, 24(4), 1580–1598. Tan, Z.H., Zeng, J., Zhang, Y.J., Slot, M., Gamo, M., Hirano, T., Kosugi, Y., Da Rocha, H.R., Saleska, S.R., Goulden, M.L. et al. (2017). Optimum air temperature for tropical forest photosynthesis: Mechanisms involved and implications for climate warming. Environmental Research Letters, 12, p.054022. Vårhammar, A., Wallin, G., McLean, C.M., Dusenge, M.E., Medlyn, B.E., Hasper, T.B., … Uddling, J. (2015). Photosynthetic temperature responses of tree species in Rwanda: evidence of pronounced negative effects of high temperature in montane rainforest climax species.New Phytologist, 206(3), 1000–1012. Warren, J.M., Jensen, A.M., Medlyn, B.E., Norby, R.J. & Tissue, D.T. (2015). Carbon dioxide stimulation of photosynthesis inLiquidambar styraciflua is not sustained during a 12-year field experiment. AoB Plants, 7. Way, D.A., Oren R., & Kroner, Y. (2015). The space‐time continuum: the effects of elevated CO2 and temperature on trees and the importance of scaling. Plant, Cell & Environment, 38(6), 991–1007. Way, D.A., & Yamori, W. (2014). Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynthesis Research,119(1), 89–100.
Way, D.A., Aspinwall, M.J., Drake, J.E., Crous, K.Y., Campany, C.E., Ghannoum, O., Tissue, D.T., &Tjoelker, M.G. (2019). Responses of respiration in the light to warming in field‐grown trees: a comparison of the thermal sensitivity of the Kok and Laisk methods. New Phytologist , 222(1), 132–143.
Winter, K, & Virgo, A. (1998). Elevated CO2 enhances growth in the rain forest understory plant, Piper cordulatum , at extremely low light intensities. Flora , 193(3), 323–326.
Winter, K., Garcia, M., Gottsberger, R. & Popp, M. (2001). Marked growth response of communities of two tropical tree species to elevated CO2 when soil nutrient limitation is removed.Flora , 196(1), 47–58.
Wood, S.N. (2017) Generalized Additive Models: An Introduction with R (2nd edition). Chapman and Hall/CRC.
Wright, S.J., Muller-Landau, H.C. & Schipper, J. (2009). The future of tropical species on a warmer planet. Conservation Biology , 23(6), 1418–1426.
Wu, G., Liu, H., Hua, L., Luo, Q., Lin, Y., He, P., Feng, S., Liu, J. & Ye, Q. (2018). Differential responses of stomata and photosynthesis to elevated temperature in two co-occurring subtropical forest tree species. Frontiers in Plant Science , 9, 467.
Yamori, W., Hikosaka, K. & Way, D.A. (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis Research , 119(1), 101–117.