title: Photosynthetic temperature responses of tree species in Rwanda: evidence of pronounced negative effects of high temperature in montane rainforest climax species.
abstract: The sensitivity of photosynthetic metabolism to temperature has been identified as a key uncertainty for projecting the magnitude of the terrestrial feedback on future climate change. While temperature responses of photosynthetic capacities have been comparatively well investigated in temperate species, the responses of tropical tree species remain unexplored. We compared the responses of seedlings of native cold-adapted tropical montane rainforest tree species with those of exotic warm-adapted plantation species, all growing in an intermediate temperature common garden in Rwanda. Leaf gas exchange responses to carbon dioxide (CO2 ) at different temperatures (20-40°C) were used to assess the temperature responses of biochemical photosynthetic capacities. Analyses revealed a lower optimum temperature for photosynthetic electron transport rates than for Rubisco carboxylation rates, along with lower electron transport optima in the native cold-adapted than in the exotic warm-adapted species. The photosynthetic optimum temperatures were generally exceeded by daytime peak leaf temperatures, in particular in the native montane rainforest climax species. This study thus provides evidence of pronounced negative effects of high temperature in tropical trees and indicates high susceptibility of montane rainforest climax species to future global warming.
authors: Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
authors: Angelica
authors: A
authors: Vårhammar
authors: Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
authors: Göran
authors: G
authors: Wallin
authors: Department of Biological Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia.
authors: Christopher M
authors: CM
authors: McLean
authors: Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.|Department of Biology, University of Rwanda, Huye, Rwanda.
authors: Mirindi Eric
authors: ME
authors: Dusenge
authors: Department of Biological Sciences, Macquarie University, North Ryde, NSW, 2109, Australia.
authors: Belinda E
authors: BE
authors: Medlyn
authors: Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
authors: Thomas B
authors: TB
authors: Hasper
authors: Department of Biology, University of Rwanda, Huye, Rwanda.
authors: Donat
authors: D
authors: Nsabimana
authors: Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.
authors: Johan
authors: J
authors: Uddling
mesh_terms: D002245:Carbon Dioxide / Q000378:metabolism; D004579:Electron Transport; D057232:Global Warming; D008954:Models, Biological; D010788:Photosynthesis; D018515:Plant Leaves / Q000378:metabolism / Q000502:physiology; D065947:Rainforest; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism; D012432:Rwanda; D013696:Temperature; D014197:Trees / Q000378:metabolism / Q000502:physiology*; D014329:Tropical Climate
chemical_list: D002245:Carbon Dioxide; D012273:Ribulose-Bisphosphate Carboxylase
keywords: Africa; leaf energy balance; maximum rate of electron transport (Jmax); optimum temperature (Topt); stomatal conductance (gs); the maximum carboxylation rate of oxygenase (Vcmax); tropical montane rainforest
references: Ainsworth EA, Long SP. 2005. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist 165: 351-372.
references: ALA. 2014. Atlas of living Australia. Climate data: Temperature - ‘mean diurnal range’, ‘month hottest maximum’, ‘month mean absolute max’ and ‘max absolute mean max.’ Species records; ‘Eucalyptus microcorys - Tallow-wood’ and ‘Eucalyptus globulus subsp. maidenii’. [Online database] [WWW document] URL ala.spatial.org.au. [accessed 26 June 2014].
references: Ames BN. 1966. Assay of inorganic phosphate, total phosphate and phosphatases. In: Neufild E, Ginsberg V, eds. Methods in enzymology complex vol. VIII Complex carbohydrates. New York, NY, USA: Academic Press, 115-118.
references: Battaglia M, Beadle C, Loughhead S. 1996. Photosynthetic temperature responses of Eucalyptus globulus and Eucalyptus nitens. Tree Physiology 16: 81-89.
references: Beer C, Reichstein M, Tomelleri E, Ciais P, Jung M, Carvalhais N, Rödenbeck C, Arain MA, Baldocchi D, Bonan GB et al. 2010. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329: 834-838.
references: Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR Jr, Long SP. 2001. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24: 253-259.
references: Berry J, Björkman O. 1980. Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31: 491-543.
references: Bloesch U, Troupin G, Derungs N. 2009. Les plantes ligneuses du Rwanda Flore, ecologie et usages. Aachen, Germany: Shaker Verlag.
references: Bonan GB. 2008. Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 203: 1444-1449.
references: Booth BBB, Jones CD, Collins M, Totterdell IJ, Cox PM, Sitch S, Huntingford C, Betts RA, Harris GH, Lloyd A. 2012. High sensitivity of future global warming to land carbon cycle processes. Environmental Research Letters 7: 024002.
references: Brooker MI, Klenig DA. 2006. Field guide to Eucalypts, vol. 1: South-eastern Australia. Melbourne, VIC, Australia: Bloomings Books.
references: Burrows MT, Schoeman DS, Richardson AJ, Molinos JG, Hoffman A, Buckley LB, Moore PJ, Brown CJ, Bruno JF, Duarte CM et al. 2014. Geographical limits to species-range shifts are suggested by climate velocity. Nature 507: 492-495.
references: Campbell GS, Norman JM. 1998. An introduction to environmental biophysics, 2nd edn. New York, NY, USA: Springer-Verlag.
references: Cao M, Zhang Q, Shugart HH. 2001. Dynamic responses of African ecosystem carbon cycling to climate change. Climate Research 17: 183-193.
references: Carswell FE, Meir P, Wandelli EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace J, Jarvis PG. 2000. Photosynthetic capacity in a central Amazonian rain forest. Tree Physiology 20: 179-186.
references: Cavieres LA, Rada F, Azócar A, García-Núñez C, Cabrera HM. 2000. Gas exchange and low temperature resistance in two tropical high mountain tree species from the Venezuelan Andes. Acta Oecologica 21: 203-211.
references: Cheesman AW, Winter K. 2013. Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings. Journal of Experimental Botany 64: 3817-3828.
references: Clark DA. 2004. Sources or sinks? The responses of tropical forests to current and future climate and atmospheric composition. Philosophical Transactions of the Royal Society B. Biological Sciences 359: 477-491.
references: Clark DA, Piper SC, Keeling CD, Clark DB. 2003. Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984-2000. Proceedings of the National Academy of Sciences, USA 100: 5852-5857.
references: Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ. 2000. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408: 184-187.
references: Crous KY, Quentin AG, Lin YS, Medlyn BE, Williams DG, Barton CVM, Ellsworth DS. 2013. Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Global Change Biology 19: 3790-3807.
references: Cunningham SC, Read J. 2002. Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature. Oecologica 133: 112-119.
references: Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM, Dickinson RE, Hauglustaine D, Heinze C, Holland E, Jacob D et al. 2007. Couplings between changes in the climate system and biogeochemistry. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds. Climate Change 2007: The physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK & New York, NY, USA: Cambridge University Press.
references: Domingues TF, Meir P, Feldpausch TR, Saiz G, Veenendaal EM, Schrodt F, Bird M, Djagbletey G, Hien F, Compaore H et al. 2010. Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment 33: 959-980.
references: Doughty CE, Goulden ML. 2008. Are tropical forests near a high temperature threshold? Journal of Geophysical Research-Biogeosciences 113: G00B07.
references: Dreyer E, Le Roux X, Montpied P, Daudet FA, Masson F. 2001. Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiology 21: 223-232.
references: Farquhar GD, Sharkey TD. 1982. Stomatal conductance and photosynthesis. Annual Reviews in Plant Physiology 33: 317-345.
references: Farquhar GD, von Cammerer S, Berry JA. 1980. A biochemical model of photosynthetic CO2 in leaves of C3 species. Planta 149: 78-90.
references: Feeley KJ, Wright SJ, Supardi MNN, Kassim AR, Davies SJ. 2007. Decelerating growth in tropical forest trees. Ecology Letters 10: 461-469.
references: Fischer E, Killmann D. 2008. Illustrated field guide to the plants of Nyungwe National Park Rwanda. Koblenz, Germany: Geographical Colloquia Series Biogeographical Monographs 1.
references: GBIF. 2014. Global Biodiversity Information Facility - free and open access to biodiversity data. Records: ‘Dickoré B. The Himalayan uplands plant database (HUP Version 1). Global mountain biodiversity assessment GMBA’ and ‘Royal Botanic Garden Edinburgh. (2014) preserved collections database (E)’. [Online database] [WWW document] URL http://www.gbif.org/[accessed 26 June 2014].
references: Gunderson C, O'Hara KH, Campion CM, Walker AV, Edwards NT. 2010. Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Global Change Biology 16: 2272-2286.
references: 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 Physiology 20: 87-96.
references: Hartmann DL, Klein TankAMG, Rusticucci M, Alexander LV, Brönnimann S, Charabi Y, Dentener FJ, Dlugokencky EJ, Easterling DR, Kaplan A et al. 2013. Observations: atmosphere and surface. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, eds. Climate Change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK & New York, NY, USA: Cambridge University Press.
references: Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø. 2009. How does climate warming affect plant-pollinator interactions? Ecology Letters 12: 184-195.
references: Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978.
references: 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: 291-302.
references: Hill K. 1991. Eucalyptus In: Harden GJ, ed. Flora of New South Wales, vol. 2. Kensington, University of NSW Press, 76-142.
references: Hill RS, Read J, Busby JR. 1988. The temperature-dependence of photosynthesis of some Australian temperate rainforest trees and its biogeographical significance. Journal of Biogeography 15: 431-449.
references: Hughes L. 2000. Biological consequences of global warming: is the signal already apparent? Trends in Ecology and Evolution 15: 56-61.
references: IPCC. 2013. Summary for policymakers. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, eds. Climate Change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK & New York, NY, USA: Cambridge University Press.
references: IPCC. 2014. Africa. In: Dube P, Leary N, eds. Volume II: regional aspects, Ch. 22: Africa, Climate Change 2014: impacts, adaptation, and vulnerability. Contribution of the Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK & New York, NY, USA: Cambridge University Press.
references: ISAR. 2011. Rwanda agricultural research institute. [WWW document] URL http://www.isar.rw/spip.php?article52. [accessed 7 June 2011].
references: Ishida A, Toma T, Marjenah. 1999. Limitation of leaf carbon gain by stomatal and photochemical processes in the top canopy of Macaranga conifera, a tropical pioneer tree. Tree Physiology 19: 467-473.
references: Kattge J, Knorr W. 2007. Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant, Cell & Environment 30: 1176-1190.
references: Kattge J, Knorr W, Raddatz T, Wirth C. 2009. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 15: 976-991.
references: Kenfack D. 2011. Resurrection in Carapa (Meliaceae): a reassessment of morphological variation and species boundaries using multivariate methods in a phylogenetic context. Botanical Journal of the Linnean Society 165: 186-221.
references: Kenzo T, Ichie T, Watanabe Y, Oneda YR, Ninomiya I, Koike T. 2006. Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiology 26: 865-873.
references: Kirschbaum MUF. 2004. Direct and indirect climate change effects on photosynthesis and transpiration. Plant Biology 6: 242-253.
references: Larcher W. 2003. Physiological plant ecology. Berlin: Springer.
references: Lemmens RHMJ. 2008. Entandrophragma excelsum (Dawe & Sprague) Sprague. In: Louppe D, Oteng-Amoako AA, Brink M, eds. Prota 7(1): Timbers/Bois d’œuvre 1. [CD-Rom]. Wageningen, the Netherlands: PROTA. URL http://database.prota.org/PROTAhtml/Entandrophragma%20excelsum_En.htm [accessed 1 September 2014].
references: Lewis SL. 2006. Tropical forests and the changing of earth system. Philosophical Transactions of the Royal Society B. Biological Sciences 361: 195-210.
references: Lloyd J, Farquhar GD. 2008. Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philosophical Transactions of the Royal Society B. Biological Sciences 363: 1811-1817.
references: Long SP. 1991. Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant, Cell & Environment 14: 729-739.
references: Medjibe VP, Poulsen JR, Clark CJ, Mbani OA. 2014. Natural regeneration of selected timber species in the Republic of Congo. African Journal of Ecology 52: 552-563.
references: Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A et al. 2002a. Temperature response of parameters of biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25: 1167-1179.
references: Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CVM, Crous KY, De Angelis P, Freeman M, Wingate L. 2011. Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology 17: 2134-2144.
references: Medlyn BE, Loustau D, Delzon S. 2002b. Temperature response of parameters of a biochemically-based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). Plant, Cell & Environment 25: 1155-1165.
references: Mercado LM, Patiño S, Domingues TF, Fyllas NM, Weedon GP, Sitch S, Quesada CA, Phillips OL, Aragão LEOC, Malhi Y et al. 2011. Variations in Amazon forest productivity correlated with foliar nutrients and modelled rates of photosynthetic carbon supply. Philosophical Transactions of the Royal Society B: Biological Sciences 366: 3316-3329.
references: Mori T, Nakashizuka T, Sumizono T, Yap SK. 1990. Growth and photosynthetic responses to temperature in several Malaysian tree species. Journal of Tropical Forest Science 3: 44-57.
references: Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K. 2000. Trienoic fatty acids and plant tolerance of high temperature. Science 287: 476-479.
references: Nsabimana D. 2009. Carbon stock and fluxes in Nyungwe forest and Ruhande Arboretum in Rwanda. PhD thesis, University of Gothenburg, Gothenburg, Sweden.
references: Nsabimana D, Klemedtson L, Kaplin BA, Wallin G. 2009. Soil CO2 flux in six monospecific forest plantations in Southern Rwanda. Soil Biology and Biochemistry 41: 369-402.
references: Orwa C, Mutua A, Kindt R, Jamnadass R, Anthony S. 2009. Agroforestree Database: a tree reference and selection guide version 4.0. [WWW document] URL http://www.worldagroforestry.org/sites/treedbs/treedatabases.asp [accessed 25 June 2014].
references: Pearcy RW. 1987. Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understory micro-environments. Functional Ecology 1: 169-178.
references: Pitman AJ. 2003. The evolution of, and revolution in, land surface schemes designed for climate models. International Journal of Climatology 23: 479-510.
references: Poethig RS. 2003. Phase change and the regulation of developmental timings in plants. Science 301: 334-336.
references: Poulsen JR, Clark CJ, Bolker BM. 2011. Decoupling the effects of logging and hunting on an Afrotropical animal community. Ecological Applications 21: 1819-1836.
references: Prentice C, Bondeau A, Cramer W, Harrison SP, Hickler T, Lucht W, Sitch S, Smith B, Sykes MT. 2007. Dynamic global vegetation modelling: quantifying terrestrial ecosystem responses to large-scale environmental change. In: Canadell JG, Pataki D, Pitelka LF, eds. Terrestrial ecosystems in a changing world. Berlin, Germany: Springer, 175-192.
references: Rada F, Azócar A, Briceño B, González J, García-Núñez C. 1996. Carbon and water balance in Polylepis sericea, a tropical treeline species. Trees 10: 218-222.
references: Read J. 1990. Some effects of acclimation temperature on net photosynthesis in some tropical and extra-tropical Australasian Nothophagus species. Journal of Ecology 78: 100-112.
references: Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA. 2003. Fingerprints of global warming on wild animals and plants. Nature 421: 57-60.
references: Sage RF. 2002. Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. Journal of Experimental Botany 369: 609-620.
references: Sage RF, Kubien DS. 2007. The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30: 1086-1106.
references: Säll T, Pettersson P. 1994. A model of photosynthetic acclimation as a special case of reaction norms. Journal of Theoretical Biology 166: 1-8.
references: Sellers PJ, Dickinson RE, Randall DA, Betts AK, Hall FG, Berry JA, Collatz GJ, Denning AS, Mooney HA, Nobre CA et al. 1997. Modelling the exchanges of energy, water, and carbon between continents and the atmosphere. Science 275: 502-509.
references: Thoning KW, Kitzis DR, Crotwell A. 2014. Atmospheric carbon dioxide dry air mole fractions from quasi-continuous measurements at Barrow, Alaska; Mauna Loa, Hawaii; American Samoa; and South Pole, 1973-2013, version: 2014-06-27. [WWW document] URL ftp://aftp.cmdl.noaa.gov/data/trace_gases/co2/in-situ/surface/. [accessed 18 August 2014].
references: Valderrama JC. 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry 10: 109-122.
references: Walcroft AS, Whitehead D, Silvester WB, Kelliher EM. 1997. The response of photosynthetic model parameters to temperature and nitrogen concentration in Pinus radiata D. Don. Plant, Cell & Environment 20: 1338-1348.
references: Way DA, Oren R. 2010. Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiology 30: 669-688.
references: White F. 1983. The vegetation of Africa - a descriptive memoir to accompany the Unesco/AETFAT/UNSO vegetation map of Africa. Paris, France: UNESCO.
references: Wittich B, Horna V, Homeier J, Leuschner C. 2012. Altitudinal change in the photosynthetic capacity of tropical trees: a case study from Ecuador and a pantropical literature analysis. Ecosystems 15: 958-973.
references: Zhang SB, Zhou ZK, Hu H, Xu K. 2007. Gas exchange and resource utilization in two alpine oaks at different altitudes in the Hengduan Mountains. Canadian Journal of Forest Research 37: 1184-1193.
references: Zhou X, Fu Y, Zhou L, Li B, Luo Y. 2013. An imperative need for global change research in tropical forests. Tree Physiology 33: 903-912.
references: Zhu K, Woodall CW, Ghosh S, Gelfand AE, Clark JS. 2014. Dual impacts of climate change: forest migration and turnover through life history. Global Change Biology 20: 251-264.