Temperature response of CO2 exchange in three tropical tree species
Martijn Slot A B , Milton N. Garcia A and Klaus Winter AA Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Republic of Panama.
B Corresponding author. Email: martijnslot78@gmail.com
Functional Plant Biology 43(5) 468-478 https://doi.org/10.1071/FP15320
Submitted: 12 October 2015 Accepted: 21 January 2016 Published: 2 March 2016
Abstract
Tropical forests play a critical role in the global carbon cycle, but our limited understanding of the physiological sensitivity of tropical forest trees to environmental factors complicates predictions of tropical carbon fluxes in a changing climate. We determined the short-term temperature response of leaf photosynthesis and respiration of seedlings of three tropical tree species from Panama. For one of the species net CO2 exchange was also measured in situ. Dark respiration of all species increased linearly – not exponentially – over a ~30°C temperature range. The early-successional species Ficus insipida Willd. and Ochroma pyramidale (Cav. ex Lam.) Urb. had higher temperature optima for photosynthesis (Topt) and higher photosynthesis rates at Topt than the late-successional species Calophyllum longifolium Willd. The decrease in photosynthesis above Topt could be assigned, in part, to observed temperature-stimulated photorespiration and decreasing stomatal conductance (gS), with unmeasured processes such as respiration in the light, Rubisco deactivation, and changing membrane properties probably playing important additional roles, particularly at very high temperatures. As temperature increased above Topt, gS of laboratory-measured leaves first decreased, followed by an increase at temperatures >40−45°C. In contrast, gS of canopy leaves of F. insipida in the field continued to decrease with increasing temperature, causing complete suppression of photosynthesis at ~45°C, whereas photosynthesis in the laboratory did not reach zero until leaf temperature was ~50°C. Models parameterised with laboratory-derived data should be validated against field observations when they are used to predict tropical forest carbon fluxes.
Additional keywords: carbon balance, gas exchange, global warming, photosynthetic temperature response, stomatal conductance, tropical forest.
References
Amthor JS (1984) The role of maintenance respiration in plant growth. Plant, Cell & Environment 7, 561–569.Atkin OK, Bloomfield KJ, Reich PB, Tjoelker MG, Asner GP, Bonal D, Bönisch G, Bradford M, Cernusak LA, Cosio EG, et al (2015) Global variability in leaf respiration among plant functional types in relation to climate and leaf traits. New Phytologist 206, 614–636.
| Global variability in leaf respiration among plant functional types in relation to climate and leaf traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvFCksb8%3D&md5=7190bb8158d4dc1caa512b97bc07caa8CAS | 25581061PubMed |
Baber O, Slot M, Celis G, Kitajima K (2014) Diel patterns of leaf carbohydrate concentrations differ between seedlings and mature trees of two sympatric oak species. Botany 92, 535–540.
| Diel patterns of leaf carbohydrate concentrations differ between seedlings and mature trees of two sympatric oak species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvVegsrs%3D&md5=c98a8ec070969cdce0005a653849a7f9CAS |
Bazzaz FA, Pickett STA (1980) Physiological ecology of tropical succession: a comparative review. Annual Review of Ecology and Systematics 11, 287–310.
| Physiological ecology of tropical succession: a comparative review.Crossref | GoogleScholarGoogle Scholar |
Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP (2001) Improved temperature response functions for models of Rubisco‐limited photosynthesis. Plant, Cell & Environment 24, 253–259.
| Improved temperature response functions for models of Rubisco‐limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFGrt7k%3D&md5=9b68d3f71e781eaf3f6b448168168491CAS |
Bernacchi CJ, Pimentel C, Long SP (2003) In vivo temperature response functions of parameters required to model RuBP‐limited photosynthesis. Plant, Cell & Environment 26, 1419–1430.
| In vivo temperature response functions of parameters required to model RuBP‐limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFyru7o%3D&md5=bb2512db05be085b366683c41c454d5eCAS |
Booth BBB, Jones CD, Collins M, Totterdell IJ, Cox PM, Sitch S, Huntingford C, Betts RA, Harris GR, Lloyd J (2012) High sensitivity of future global warming to land carbon cycle processes. Environmental Research Letters 7, 024002
| High sensitivity of future global warming to land carbon cycle processes.Crossref | GoogleScholarGoogle Scholar |
Cavaleri MA, Oberbauer SF, Ryan MG (2008) Foliar and ecosystem respiration in an old‐growth tropical rain forest. Plant, Cell & Environment 31, 473–483.
| Foliar and ecosystem respiration in an old‐growth tropical rain forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1CksrY%3D&md5=0e28ac569235f30053bea7fbb0ccb747CAS |
Cernusak LA, Winter K, Dalling JW, Holtum JA, Jaramillo C, Körner C, Leakey ADB, Norby RJ, Poulter B, Turner BL, Wright SJ (2013) Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research. Functional Plant Biology 40, 531–551.
| Tropical forest responses to increasing atmospheric CO2: current knowledge and opportunities for future research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsVOksrs%3D&md5=55c3bae1db01c6313cd979594689379cCAS |
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.
| Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yrsr3E&md5=c462e3b95412ff8a098ff305eddc6a7dCAS | 23873999PubMed |
Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proceedings of the National Academy of Sciences of the United States of America 97, 13430–13435.
| Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVOjsLk%3D&md5=4e9027d8e7cfd61a56b2f92f9a24000fCAS | 11069297PubMed |
Cunningham SC, Read J (2002) Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature. Oecologia 133, 112–119.
| Comparison of temperate and tropical rainforest tree species: photosynthetic responses to growth temperature.Crossref | GoogleScholarGoogle Scholar |
Doughty CE (2011) An in situ leaf and branch warming experiment in the Amazon. Biotropica 43, 658–665.
| An in situ leaf and branch warming experiment in the Amazon.Crossref | GoogleScholarGoogle Scholar |
Doughty CE, Goulden ML (2008) Are tropical forests near a high temperature threshold? Journal of Geophysical Research. Biogeosciences 113, G00B07
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXksVWrt7w%3D&md5=14e11031293958031aaa70cd1cf0fa5aCAS | 24306196PubMed |
Huntingford C, Zelazowski P, Galbraith D, Mercado LM, Sitch S, Fisher R, Lomas M, Walker AP, Jones CD, Booth BBB, et al (2013) Simulated resilience of tropical rainforests to CO2-induced climate change. Nature Geoscience 6, 268–273.
| Simulated resilience of tropical rainforests to CO2-induced climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjs1Chsrk%3D&md5=01415ff3c82b48373aefcbe75b67cbabCAS |
Hüve K, Bichele I, Ivanova H, Keerberg O, Pärnik T, Rasulov B, Tobias M, Niinemets Ü (2012) Temperature responses of dark respiration in relation to leaf sugar concentration. Physiologia Plantarum 144, 320–334.
| Temperature responses of dark respiration in relation to leaf sugar concentration.Crossref | GoogleScholarGoogle Scholar | 22188403PubMed |
Ionenko IF, Anisimov AV, Dautova NR (2010) Effect of temperature on water transport through aquaporins. Biologia Plantarum 54, 488–494.
| Effect of temperature on water transport through aquaporins.Crossref | GoogleScholarGoogle Scholar |
Kitajima K (1994) Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98, 419–428.
| Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees.Crossref | GoogleScholarGoogle Scholar |
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, 357–365.
| Photosynthetic capacity and temperature responses of photosynthesis of rubber trees (Hevea brasiliensis Müll. Arg.) acclimate to changes in ambient temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSms70%3D&md5=11f7381db1e509f21136557b1f9ee512CAS |
Krause GH, Winter K, Krause B, Jahns P, García M, Aranda J, Virgo A (2010) High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations. Functional Plant Biology 37, 890–900.
| High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations.Crossref | GoogleScholarGoogle Scholar |
Krause GH, Winter K, Krause B, Virgo A (2015) Light-stimulated heat tolerance in leaves of two neotropical tree species, Ficus insipida and Calophyllum longifolium. Functional Plant Biology 42, 42–51.
| Light-stimulated heat tolerance in leaves of two neotropical tree species, Ficus insipida and Calophyllum longifolium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFSns7jP&md5=b435e4cef65287ef25ca0a9924838c71CAS |
Lin YS, Medlyn BE, Ellsworth DS (2012) Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiology 32, 219–231.
| Temperature responses of leaf net photosynthesis: the role of component processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmslGjsb8%3D&md5=200969f42ccb56aff95c24cb882dfec1CAS | 22278379PubMed |
Markesteijn L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought‐and shade‐tolerance. Journal of Ecology 97, 311–325.
| Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought‐and shade‐tolerance.Crossref | GoogleScholarGoogle Scholar |
Markesteijn L, Poorter L, Bongers F, Paz H, Sack L (2011) Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance. New Phytologist 191, 480–495.
| Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance.Crossref | GoogleScholarGoogle Scholar | 21477008PubMed |
Meir P, Grace J, Miranda AC (2001) Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature. Functional Ecology 15, 378–387.
| Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature.Crossref | GoogleScholarGoogle Scholar |
Mott KA, Peak D (2011) Alternative perspective on the control of transpiration by radiation. Proceedings of the National Academy of Sciences of the United States of America 108, 19820–19823.
| Alternative perspective on the control of transpiration by radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1CmsbbE&md5=cc3e0e8d145d4df707073d7cb07bfafbCAS | 22106306PubMed |
O’Sullivan OS, Weerasinghe KK, Evans JR, Egerton JJ, Tjoelker MG, Atkin OK (2013) High‐resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high‐temperature limits to respiratory function. Plant, Cell & Environment 36, 1268–1284.
| High‐resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high‐temperature limits to respiratory function.Crossref | GoogleScholarGoogle Scholar |
Pan Y, Birdsey RA, Phillips OL, Jackson RB (2013) The structure, distribution, and biomass of the world’s forests. Annual Review of Ecology Evolution and Systematics 44, 593–622.
| The structure, distribution, and biomass of the world’s forests.Crossref | GoogleScholarGoogle Scholar |
Peraudeau S, Lafarge T, Roques S, Quiñones CO, Clement-Vidal A, Ouwerkerk PB, van Rie J, Fabre D, Jagadish KSV, Dingkuhn M (2015) Effect of carbohydrates and night temperature on night respiration in rice. Journal of Experimental Botany 66, 3931–3944.
| Effect of carbohydrates and night temperature on night respiration in rice.Crossref | GoogleScholarGoogle Scholar | 25954047PubMed |
Piao S, Sitch S, Ciais P, Friedlingstein P, Peylin P, Wang X, Ahlström A, Anav A, Canadell JG, Cong N, et al (2013) Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO2 trends. Global Change Biology 19, 2117–2132.
| Evaluation of terrestrial carbon cycle models for their response to climate variability and to CO2 trends.Crossref | GoogleScholarGoogle Scholar | 23504870PubMed |
Pons TL, Welschen RA (2003) Midday depression of net photosynthesis in the tropical rainforest tree Eperua grandiflora: contributions of stomatal and internal conductances, respiration and Rubisco functioning. Tree Physiology 23, 937–947.
| Midday depression of net photosynthesis in the tropical rainforest tree Eperua grandiflora: contributions of stomatal and internal conductances, respiration and Rubisco functioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVCmurY%3D&md5=6aaba506e743d9e75ec1907ee2bd7085CAS | 12952780PubMed |
Ryan MG (1991) Effects of climate change on plant respiration. Ecological Applications 1, 157–167.
| Effects of climate change on plant respiration.Crossref | GoogleScholarGoogle Scholar |
Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30, 1086–1106.
| The temperature response of C3 and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrP&md5=52a0c02ec3de4bee82f1b20c5ed3dc31CAS |
Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. Journal of Experimental Botany 59, 1581–1595.
| Rubisco, Rubisco activase, and global climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtleltLc%3D&md5=e11633be4a335429a3e498d9b11aa0b5CAS | 18436544PubMed |
Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiology 134, 1460–1470.
| Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKms7s%3D&md5=31662c95cd77364ffeb36f9901f7805aCAS | 15084731PubMed |
Saugier B, Roy J, Mooney HA (2001) Estimations of global terrestrial productivity: converging toward a single number? In ‘Terrestrial global productivity’. (Eds J Roy, B Saugier, HA Mooney) pp. 543–557. (Academic Press: New York)
Slot M, Winter K (2016) The effects of rising temperature on the ecophysiology of tropical forest trees. In ‘Tropical tree physiology: adaptations and responses in a changing environment’. (Eds LS Santiago, G Goldstein). (Springer International Publishing: Cham, Switzerland) In press.
Slot M, Wright SJ, Kitajima K (2013) Foliar respiration and its temperature sensitivity in trees and lianas: in situ measurements in the upper canopy of a tropical forest. Tree Physiology 33, 505–515.
| Foliar respiration and its temperature sensitivity in trees and lianas: in situ measurements in the upper canopy of a tropical forest.Crossref | GoogleScholarGoogle Scholar | 23592296PubMed |
Slot M, Rey‐Sánchez C, Winter K, Kitajima K (2014) Trait‐based scaling of temperature‐dependent foliar respiration in a species‐rich tropical forest canopy. Functional Ecology 28, 1074–1086.
| Trait‐based scaling of temperature‐dependent foliar respiration in a species‐rich tropical forest canopy.Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Nardini A, Salleo S, Sack L, El Omari B (2005) The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response? Journal of Experimental Botany 56, 737–744.
| The dependence of leaf hydraulic conductance on irradiance during HPFM measurements: any role for stomatal response?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2ruro%3D&md5=66601fcf23089cbc88f5835503c8a884CAS | 15582928PubMed |
Vanderwel MC, Slot M, Lichstein JW, Reich PB, Kattge J, Atkin OK, Bloomfield K, Tjoelker M, Kitajima K (2015) Global convergence in projected leaf respiration from estimates of thermal acclimation across time and space. New Phytologist 207, 1026–1037.
| Global convergence in projected leaf respiration from estimates of thermal acclimation across time and space.Crossref | GoogleScholarGoogle Scholar | 25898850PubMed |
Vargas G, Cordero SR (2013) Photosynthetic responses to temperature of two tropical rainforest tree species from Costa Rica. Trees 27, 1261–1270.
| Photosynthetic responses to temperature of two tropical rainforest tree species from Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Vårhammar A, Wallin G, McLean CM, Dusenge ME, Medlyn BE, Hasper TB, Nsabimana D, 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, 1000–1012.
| Photosynthetic temperature responses of tree species in Rwanda: evidence of pronounced negative effects of high temperature in montane rainforest climax species.Crossref | GoogleScholarGoogle Scholar | 25656943PubMed |
von Caemmerer S, Evans JR (2015) Temperature responses of mesophyll conductance differ greatly between species. Plant, Cell & Environment 38, 629–637.
| Temperature responses of mesophyll conductance differ greatly between species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvVKjtLw%3D&md5=51d522056b86a6ee37bf0bee9af01518CAS |
von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
| Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjtFyjug%3D%3D&md5=594706df358e95aa5af132f56bfba10eCAS | 24276943PubMed |
von Caemmerer S, Quick WP (2000) Rubisco: physiology in vivo. In ‘Photosynthesis’. (Eds RC Leegood, TD Sharkey, S von Caemmerer) pp. 85–113. (Springer: Dordrecht, The Netherlands)
Way DA, Holly C, Bruhn D, Ball MC, Atkin OK (2015) Diurnal and seasonal variation in light and dark respiration in field-grown Eucalyptus pauciflora. Tree Physiology 35, 840–849.
| Diurnal and seasonal variation in light and dark respiration in field-grown Eucalyptus pauciflora.Crossref | GoogleScholarGoogle Scholar | 26253839PubMed |
Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field‐grown pima cotton plants at high temperature. Plant, Cell & Environment 27, 717–724.
| Electron transport is the functional limitation of photosynthesis in field‐grown pima cotton plants at high temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVGgtLk%3D&md5=8994d0d1eaf7e2707205d02ac392990fCAS |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M, et al (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=d60b0f91594517529da250089e292021CAS | 15103368PubMed |
Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Díaz S, Engelbrecht BM (2010) Functional traits and the growth–mortality trade-off in tropical trees. Ecology 91, 3664–3674.
| Functional traits and the growth–mortality trade-off in tropical trees.Crossref | GoogleScholarGoogle Scholar | 21302837PubMed |
Zotz G, Harris G, Königer M, Winter K (1995) High rates of photosynthesis in a tropical pioneer tree, Ficus insipida. Flora 190, 265–272.