Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Light inhibition of foliar respiration in response to soil water availability and seasonal changes in temperature in Mediterranean holm oak (Quercus ilex) forest

Matthew H. Turnbull A K , Romà Ogaya B C , Adrià Barbeta B C J , Josep Peñuelas B C , Joana Zaragoza-Castells D , Owen K. Atkin E , Fernando Valladares F , Teresa E. Gimeno G J , Beatriz Pías H and Kevin L. Griffin I
+ Author Affiliations
- Author Affiliations

A Centre for Integrative Ecology, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand.

B CREAF, Cerdanyola del Vallès, 08193, Catalonia, Spain.

C CSIC, Global Ecology Unit CREAF-CSIC-UAB, Cerdanyola del Vallès, 08193, Catalonia, Spain.

D Geography, College of Life and Environmental Sciences, University of Exeter, Amory Building, Rennes Drive, Exeter EX4 4RJ, UK.

E ARC Centre of Excellence in Plant Energy Biology, Division of Plant Sciences, Research School of Biology, Building 134, The Australian National University, Canberra, ACT 2601, Australia.

F Museo Nacional de Ciencias Naturales, CSIC, Serrano 115, E-28006 Madrid, Spain.

G Hawkesbury Institute for the Environment, University of Western Sydney, Locked bag 1797, Penrith, NSW 2751, Australia.

H Departamento de Botánica, Universidad Complutense de Madrid, José Antonio Novais 2, 28040, Madrid, Spain.

I Lamont-Doherty Earth Observatory of Columbia University, 61 Route 9W, 6 Biology, Palisades, NY 10964, USA.

J ISPA, Bordeaux Science Agro, INRA, 33140 Villenave d’Ornon, France.

K Corresponding author. Email: matthew.turnbull@canterbury.ac.nz

Functional Plant Biology 44(12) 1178-1193 https://doi.org/10.1071/FP17032
Submitted: 27 January 2017  Accepted: 23 July 2017   Published: 17 August 2017

Abstract

In the present study we investigated variations in leaf respiration in darkness (RD) and light (RL), and associated traits in response to season, and along a gradient of soil moisture, in Mediterranean woodland dominated by holm oak (Quercus ilex L.) in central and north-eastern Spain respectively. On seven occasions during the year in the central Spain site, and along the soil moisture gradient in north-eastern Spain, we measured rates of leaf RD, RL (using the Kok method), light-saturated photosynthesis (A) and related light response characteristics, leaf mass per unit area (MA) and leaf nitrogen (N) content. At the central Spain site, significant seasonal changes in soil water content and ambient temperature (T) were associated with changes in MA, foliar N, A and stomatal conductance. RD measured at the prevailing daily T and in instantaneous RT responses, displayed signs of partial acclimation and was not significantly affected by time of year. RL was always less than, and strongly related to, RD, and RL/RD did not vary significantly or systematically with seasonal changes in T or soil water content. Averaged over the year, RL/RD was 0.66 ± 0.05 s.e. (n = 14) at the central Spain site. At the north-eastern Spain site, the soil moisture gradient was characterised by increasing MA and RD, and reduced foliar N, A, and stomatal conductance as soil water availability decreased. Light inhibition of R occurred across all sites (mean RL/RD = 0.69 ± 0.01 s.e. (n = 18)), resulting in ratios of RL/A being lower than for RD/A. Importantly, the degree of light inhibition was largely insensitive to changes in soil water content. Our findings provide evidence for a relatively constrained degree of light inhibition of R (RL/RD ~ 0.7, or inhibition of ~30%) across gradients of water availability, although the combined impacts of seasonal changes in both T and soil water content increase the range of values expressed. The findings thus have implications in terms of the assumptions made by predictive models that seek to account for light inhibition of R, and for our understanding of how environmental gradients impact on leaf trait relationships in Mediterranean plant communities.

Additional keywords: Kok effect, leaf functional traits, leaf dark respiration, leaf light respiration, leaf mass per unit area, nitrogen, photosynthesis, plasticity, season, soil moisture, temperature.


References

Alt C, Stutzel H, Kage H (2000) Optimal nitrogen content and photosynthesis in cauliflower (Brassica oleracea L. botrytis). Scaling up from a leaf to the whole plant. Annals of Botany 85, 779–787.
Optimal nitrogen content and photosynthesis in cauliflower (Brassica oleracea L. botrytis). Scaling up from a leaf to the whole plant.CrossRef | 1:CAS:528:DC%2BD3cXjs12hu7k%3D&md5=49376a8d2181f6274369003bb3689cddCAS |

Amthor JS (1989) ‘Respiration and crop productivity.’ (Springer-Verlag: New York).

Atkin OK, Day DA (1990) A comparison of the respiratory processes and growth rates of selected Australian alpine and related lowland plant species. Australian Journal of Plant Physiology 17, 517–526.
A comparison of the respiratory processes and growth rates of selected Australian alpine and related lowland plant species.CrossRef |

Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Annals of Botany 103, 581–597.
The crucial role of plant mitochondria in orchestrating drought tolerance.CrossRef | 1:CAS:528:DC%2BD1MXktVGnu7k%3D&md5=b2203770bcef2bc6a135ea72a9b662c0CAS |

Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends in Plant Science 8, 343–351.
Thermal acclimation and the dynamic response of plant respiration to temperature.CrossRef | 1:CAS:528:DC%2BD3sXls1CjtLk%3D&md5=bfcd6e18c93ebde62eeae8604bbe253cCAS |

Atkin OK, Westbeek MHM, Cambridge ML, Lambers H, Pons TL (1997) Leaf respiration in light and darkness. A comparison of slow- and fast-growing Poa species. Plant Physiology 113, 961–965.
Leaf respiration in light and darkness. A comparison of slow- and fast-growing Poa species.CrossRef | 1:CAS:528:DyaK2sXhvFSmtr4%3D&md5=c50a07bc208cb246621fe07635bccd84CAS |

Atkin OK, Edwards EJ, Loveys BR (2000a) Response of root respiration to changes in temperature and its relevance to global warming. New Phytologist 147, 141–154.
Response of root respiration to changes in temperature and its relevance to global warming.CrossRef | 1:CAS:528:DC%2BD3cXms1yltL4%3D&md5=85c6f5688c4771442b23b404384b2cddCAS |

Atkin OK, Holly C, Ball MC (2000b) 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 & Environment 23, 15–26.
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.CrossRef |

Atkin OK, Bruhn D, Tjoelker MG (2005) Response of plant respiration to changes in temperature: mechanisms and consequences of variations in the Q 10 and acclimation. In ‘Plant respiration: from cell to ecosystem’. (Eds H Lambers, M Ribas-Carbo) pp. 95–136. (Springer: Dordrecht, The Netherlands).

Atkin OK, Scheurwater I, Pons TL (2006) High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric. Global Change Biology 12, 500–515.
High thermal acclimation potential of both photosynthesis and respiration in two lowland Plantago species in contrast to an alpine congeneric.CrossRef |

Atkin OK, Scheurwater I, Pons TL (2007) Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures. New Phytologist 174, 367–380.
Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures.CrossRef | 1:CAS:528:DC%2BD2sXls12ltbY%3D&md5=8fb5a0f6ece6f6fb40b0ecb972b0b14aCAS |

Atkin OK, Atkinson LJ, Fisher RA, Campbell CD, Zaragoza-Castells J, Pitchford J, Woodward FI, Hurry V (2008) Using temperature-dependent changes in leaf scaling relationships to quantitatively account for thermal acclimation of respiration in a coupled global climate-vegetation model. Global Change Biology 14, 2709–2726.

Atkin OK, Turnbull MH, Zaragoza-Castell J, Fyllas NM, Lloyd J, Meir P, Griffin KL (2013) Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method. Plant and Soil 367, 163–182.
Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method.CrossRef | 1:CAS:528:DC%2BC3sXlsVKitrs%3D&md5=bc7d577dc42572091e83cd1ad687c47dCAS |

Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytologist 190, 1003–1018.
Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature.CrossRef |

Ayub G, Zaragoza-Castells J, Griffin KL, Atkin OK (2014) Leaf respiration in darkness and in the light under pre-industrial, current and elevated atmospheric CO2 concentrations. Plant Science 226, 120–130.
Leaf respiration in darkness and in the light under pre-industrial, current and elevated atmospheric CO2 concentrations.CrossRef | 1:CAS:528:DC%2BC2cXpslKmtLo%3D&md5=cebac81f282c096309929d1bfa868b70CAS |

Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-biphosphate carboxylase/oxygenase and the rate of respiration in the light. Estimates from gas exchange measurements on spinach. Planta 165, 397–406.
Effect of temperature on the CO2/O2 specificity of ribulose-1,5-biphosphate carboxylase/oxygenase and the rate of respiration in the light. Estimates from gas exchange measurements on spinach.CrossRef | 1:CAS:528:DyaL2MXltlyrsLc%3D&md5=aa2f7b476b7b08e0d672bc305eddc526CAS |

Buckley TN, Adams MA (2011) An analytical model of non-photorespiratory CO2 release in the light and dark in leaves of C3 species based on stoichiometric flux balance. Plant, Cell & Environment 34, 89–112.
An analytical model of non-photorespiratory CO2 release in the light and dark in leaves of C3 species based on stoichiometric flux balance.CrossRef | 1:CAS:528:DC%2BC3MXht1Gnurc%3D&md5=d54c2a3ba9154009d993aefe14a28fe7CAS |

Budde RJA, Randall DD (1990) Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 87, 673–676.
Pea leaf mitochondrial pyruvate dehydrogenase complex is inactivated in vivo in a light-dependent manner.CrossRef | 1:CAS:528:DyaK3cXhtFGrtLY%3D&md5=d1f8d6330dcda5f4c891ea81cab1eab2CAS |

Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML (2002) How plants cope with water stress in the field: photosynthesis and growth. Annals of Botany 89, 907–916.
How plants cope with water stress in the field: photosynthesis and growth.CrossRef | 1:CAS:528:DC%2BD38XlsVeitb4%3D&md5=d9e10b40b950e7009011d31320164d1aCAS |

Crous KY, Zaragoza-Castells J, Low M, Ellsworth DS, Tissue DT, Tjoelker MG, Barton CVM, Gimeno TE, Atkin OK (2011) Seasonal acclimation of leaf respiration in Eucalyptus saligna trees: impacts of elevated atmospheric CO2 and summer drought. Global Change Biology 17, 1560–1576.
Seasonal acclimation of leaf respiration in Eucalyptus saligna trees: impacts of elevated atmospheric CO2 and summer drought.CrossRef |

Crous KY, Zaragoza-Castells J, Ellsworth DS, Duursma RA, Low M, Tissue DT, Atkin OK (2012) Light inhibition of leaf respiration in field-grown Eucalyptus saligna in whole-tree chambers under elevated atmospheric CO2 and summer drought. Plant, Cell & Environment 35, 966–981.
Light inhibition of leaf respiration in field-grown Eucalyptus saligna in whole-tree chambers under elevated atmospheric CO2 and summer drought.CrossRef | 1:CAS:528:DC%2BC38XosFSqsb4%3D&md5=01a2c51cb4497fb001441c83b332be64CAS |

Farquhar GD, Busch FA (2017) Changes in the chloroplastic CO2 concentration explain much of the observed Kok effect: a model. New Phytologist 214, 570–584.
Changes in the chloroplastic CO2 concentration explain much of the observed Kok effect: a model.CrossRef | 1:CAS:528:DC%2BC2sXksFaksrg%3D&md5=3ba54ac6e33611a25bd6c35bedd53339CAS |

Farquhar GD, von Caemmerer S (1982) Modelling of photosynthetic response to environmental conditions. In ‘Encyclopedia of plant physiology. Vol. 12B. Physiological plant ecology II. Water relations and carbon assimilation’. (Eds OL Lange, PS Nobel, CB Osmond, H Ziegler) pp. 551–587. (Springer Verlag: Berlin).

Flexas J, Galmes J, Ribas-Carbo M, Medrano H (2005) The effects of water stress on plant respiration. In ‘Plant respiration: from cell to ecosystem. Vol. 18’. (Eds H Lambers, M Ribas-Carbo) pp. 85–94. (Springer: Dordrecht, The Netherlands).

Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiologia Plantarum 127, 343–352.
Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress.CrossRef | 1:CAS:528:DC%2BD28XosVKhu7o%3D&md5=f33d3d5a29c9759f29ee6c21e6c322f7CAS |

Gemel J, Randall DD (1992) Light regulation of leaf mitochondrial pyruvate dehydrogenase complex. Role of photorespiratory carbon metabolism. Plant Physiology 100, 908–914.
Light regulation of leaf mitochondrial pyruvate dehydrogenase complex. Role of photorespiratory carbon metabolism.CrossRef | 1:CAS:528:DyaK38XmsVyltr8%3D&md5=c44a85d9c86a33bb9a7a44fdab3b6990CAS |

Ghashghaie J, Duranceau M, Badeck FW, Cornic G, Adeline MT, Deleens E (2001) δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant, Cell & Environment 24, 505–515.
δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought.CrossRef | 1:CAS:528:DC%2BD3MXkt1Oit7k%3D&md5=1f0e863f192d79674640a113dd293598CAS |

Gifford RM (1995) Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature – long-term vs short-term distinctions for modelling. Global Change Biology 1, 385–396.
Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature – long-term vs short-term distinctions for modelling.CrossRef |

Grassi G, Meir P, Cromer R, Tompkins D, Jarvis PG (2002) Photosynthetic parameters in seedlings of Eucalyptus grandis as affected by rate of nitrogen supply. Plant, Cell & Environment 25, 1677–1688.
Photosynthetic parameters in seedlings of Eucalyptus grandis as affected by rate of nitrogen supply.CrossRef |

Griffin KL, Turnbull MH (2013) Light saturated RuBP oxygenation by Rubisco is a robust predictor of light inhibition of respiration in Triticum aestivum L. Plant Biology 15, 769–775.
Light saturated RuBP oxygenation by Rubisco is a robust predictor of light inhibition of respiration in Triticum aestivum L.CrossRef | 1:CAS:528:DC%2BC3sXhtFOgsLjK&md5=8a0586ced8e2a55520f5fc918422bae8CAS |

Griffin KL, Turnbull M, Murthy R (2002a) Canopy position affects the temperature response of leaf respiration in Populus deltoides. New Phytologist 154, 609–619.
Canopy position affects the temperature response of leaf respiration in Populus deltoides.CrossRef |

Griffin KL, Turnbull M, Murthy R, Lin GH, Adams J, Farnsworth B, Mahato T, Bazin G, Potasnak M, Berry JA (2002b) Leaf respiration is differentially affected by leaf vs stand-level night-time warming. Global Change Biology 8, 479–485.
Leaf respiration is differentially affected by leaf vs stand-level night-time warming.CrossRef |

Griffin KL, Anderson OR, Tissue DT, Turnbull MH, Whitehead D (2004) Variations in dark respiration and mitochondrial numbers within needles of Pinus radiata grown in ambient or elevated CO2 partial pressure. Tree Physiology 24, 347–353.
Variations in dark respiration and mitochondrial numbers within needles of Pinus radiata grown in ambient or elevated CO2 partial pressure.CrossRef |

Gulias J, Flexas J, Abadia A, Madrano H (2002) Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species. Tree Physiology 22, 687–697.
Photosynthetic responses to water deficit in six Mediterranean sclerophyll species: possible factors explaining the declining distribution of Rhamnus ludovici-salvatoris, an endemic Balearic species.CrossRef | 1:CAS:528:DC%2BD38Xlsl2murg%3D&md5=1dba8fbf0037c73bd5bbf29500e91c63CAS |

Heskel M, Anderson OR, Atkin OK, Turnbull MH, Griffin KL (2012) Leaf- and cell-level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species. American Journal of Botany 99, 1702–1714.
Leaf- and cell-level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species.CrossRef | 1:CAS:528:DC%2BC38XhvVSnt7nJ&md5=5bcacf84c6ac3c846e1a6137ac026d8cCAS |

Heskel M, Greaves H, Kornfeld A, Gough L, Atkin O, Turnbull M, Shaver G, Griffin KL (2013) Differential physiological responses to environmental change promote woody shrub expansion. Ecology and Evolution 3, 1149–1162.
Differential physiological responses to environmental change promote woody shrub expansion.CrossRef |

Heskel M, Bitterman DS, Atkin O, Turnbull MH, Griffin KL (2014) Seasonality of foliar respiration in two dominant plant species from the Arctic tundra: response to long-term warming and short-term temperature variability. Functional Plant Biology 41, 287–300.
Seasonality of foliar respiration in two dominant plant species from the Arctic tundra: response to long-term warming and short-term temperature variability.CrossRef |

Hoefnagel MHN, Atkin OK, Wiskich JT (1998) Interdependence between chloroplasts and mitochondria in the light and the dark. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1366, 235–255.
Interdependence between chloroplasts and mitochondria in the light and the dark.CrossRef | 1:CAS:528:DyaK1cXmtlSit7g%3D&md5=0b3ca5c1e7ecc39d2817b60ddc715e04CAS |

Hurry VM, Tobiaeson M, Kromer S, Gardestrom P, Oquist G (1995) Mitochondria contribute to increased photosynthetic capacity of leaves of winter rye (Secale cereale L.) following cold-hardening. Plant, Cell & Environment 18, 69–76.
Mitochondria contribute to increased photosynthetic capacity of leaves of winter rye (Secale cereale L.) following cold-hardening.CrossRef |

Hurry V, Igamberdiev AU, Keerberg O, Pärnik TR, Atkin OK, Zaragoza-Castells J, Gardeström P (2005) Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light. In ‘Advances in photosynthesis and respiration: respiration and the environment’. (Eds H Lambers and M Ribas-Carbo) pp. 43–61. (Springer: Dordrecht, The Netherlands).

Igamberdiev AU, Romanowska E, Gardestrom P (2001) Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions. Journal of Plant Physiology 158, 1325–1332.
Photorespiratory flux and mitochondrial contribution to energy and redox balance of barley leaf protoplasts in the light and during light-dark transitions.CrossRef | 1:CAS:528:DC%2BD3MXosl2mu7Y%3D&md5=3da1bcbbdfe67c18166a55ddef937b16CAS |

IPCC (2007) ‘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 University Press: Cambridge, UK).

Kirschbaum MUF, Farquhar GD (1987) Investigation of the CO2 dependence of quantum yield and respiration in Eucalyptus pauciflora. Plant Physiology 83, 1032–1036.
Investigation of the CO2 dependence of quantum yield and respiration in Eucalyptus pauciflora.CrossRef | 1:CAS:528:DyaL2sXktVCmtLg%3D&md5=912b6d2fc4c8a1cf5be127ba447fb237CAS |

Koide RT, Robichaux RH, Morse SR, Smith CM (1989) Plant water status, hydraulic resistance and capacitance. In ‘Plant physiological ecology’. (Eds RW Pearcy, J Ehleringer, HA Mooney, PW Rundel) pp. 161–184. (Chapman & Hall: London).

Kok B (1948) A critical consideration of the quantum yield of Chlorella-photosynthesis. Enzymologia 13, 1–56.

Krömer S (1995) Respiration during photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 46, 45–70.
Respiration during photosynthesis.CrossRef |

Larigauderie A, Körner C (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Annals of Botany 76, 245–252.
Acclimation of leaf dark respiration to temperature in alpine and lowland plant species.CrossRef |

Lloyd J, Shibistova O, Zolotoukhine D, Kolle O, Arneth A, Wirth C, Styles JM, Tchebakova NM, Schulze ED (2002) Seasonal and annual variations in the photosynthetic productivity and carbon balance of a central Siberian pine forest. Tellus. Series B, Chemical and Physical Meteorology 54, 590–610.
Seasonal and annual variations in the photosynthetic productivity and carbon balance of a central Siberian pine forest.CrossRef |

Loomis RS, Amthor JS (1999) Yield potential, plant assimilatory capacity, and metabolic efficiencies. Crop Science 39, 1584–1596.
Yield potential, plant assimilatory capacity, and metabolic efficiencies.CrossRef | 1:CAS:528:DC%2BD3cXpt1Gktw%3D%3D&md5=7036b9613fa53835624a31195145694eCAS |

Loveys BR, Atkinson LJ, Sherlock DJ, Roberts RL, Fitter AH, Atkin OK (2003) Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species. Global Change Biology 9, 895–910.
Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species.CrossRef |

McLaughlin BC, Xu C-Y, Rastetter EB, Griffin KL (2014) Predicting ecosystem carbon balance in a warming Arctic: the importance of long-term thermal acclimation potential and inhibitory effects of light on respiration. Global Change Biology 20, 1901–1912.
Predicting ecosystem carbon balance in a warming Arctic: the importance of long-term thermal acclimation potential and inhibitory effects of light on respiration.CrossRef |

Mercado LM, Huntingford C, Gash JHC, Cox PM, Jogireddy V (2007) Improving the representation of radiation interception and photosynthesis for climate model applications. Tellus. Series B, Chemical and Physical Meteorology 59, 553–565.
Improving the representation of radiation interception and photosynthesis for climate model applications.CrossRef |

Mitchell KA, Bolstad PV, Vose JM (1999) Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species. Tree Physiology 19, 861–870.
Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species.CrossRef | 1:STN:280:DC%2BC2sbhtFWlsw%3D%3D&md5=f5aaf1d92079829eaaa31f07ed159b5bCAS |

Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8, 87–99.
Interaction between photosynthesis and respiration in illuminated leaves.CrossRef | 1:CAS:528:DC%2BD2sXhsVOlt77F&md5=63281d7a4beccdd7581884d380d0345dCAS |

Ogaya R, Peñuelas J (2007) Tree growth, mortality and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecology 189, 291–299.
Tree growth, mortality and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought.CrossRef |

Ogaya R, Peñuelas J (2008) Changes in leaf δ13C and δ15N for three Mediterranean tree species in relation to soil water availability. Acta Oecologica 34, 331–338.
Changes in leaf δ13C and δ15N for three Mediterranean tree species in relation to soil water availability.CrossRef |

Ow LF, Griffin KL, Whitehead D, Walcroft AS, Turnbull MH (2008a) Thermal acclimation of leaf respiration but not photosynthesis in Populus deltoids × nigra. New Phytologist 178, 123–134.
Thermal acclimation of leaf respiration but not photosynthesis in Populus deltoids × nigra.CrossRef |

Ow LF, Whitehead D, Walcroft AS, Turnbull MH (2008b) Thermal acclimation of respiration but not photosynthesis in Pinus radiata. Functional Plant Biology 35, 448–461.
Thermal acclimation of respiration but not photosynthesis in Pinus radiata.CrossRef |

Pärnik T, Ivanova H, Keerberg O (2007) Photorespiratory and respiratory decarboxylations in leaves of C3 plants under different CO2 concentrations and irradiances. Plant, Cell & Environment 30, 1535–1544.
Photorespiratory and respiratory decarboxylations in leaves of C3 plants under different CO2 concentrations and irradiances.CrossRef |

Peñuelas J, Boada M (2003) A global change-induced biome shift in the Montseny mountains (NE Spain). Global Change Biology 9, 131–140.
A global change-induced biome shift in the Montseny mountains (NE Spain).CrossRef |

Peñuelas J, Sardans J, Estiarte M, Ogaya R, Carnicer J, Coll M, Barbeta A, Rivas-Ubach A, Llusià J, Garbulsky M, Filella I, Jump AS (2013) Evidence of current impact of climate change on life: a walk from genes to the biosphere. Global Change Biology 19, 2303–2338.
Evidence of current impact of climate change on life: a walk from genes to the biosphere.CrossRef |

Pons TL, Welschen RAM (2002) Overestimation of respiration rates in commercially available clamp-on leaf chambers. Complications with measurement of net photosynthesis. Plant, Cell & Environment 25, 1367–1372.
Overestimation of respiration rates in commercially available clamp-on leaf chambers. Complications with measurement of net photosynthesis.CrossRef |

Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiology 94, 621–627.
Carbon and nitrogen economy of 24 wild species differing in relative growth rate.CrossRef | 1:CAS:528:DyaK3MXjsFOi&md5=0909639c3add1a1dbd3bbe05b5260ba3CAS |

R Development Core Team (2008) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna) Available at http://www.R-project.org/ [Verified 6 May 2017].

Rodríguez-Calcerrada J, Jaeger C, Limousin JM, Ourcival JM, Joffre R, Rambal S (2011) Leaf CO2 efflux is attenuated by acclimation of respiration to heat and drought in a Mediterranean tree. Functional Ecology 25, 983–995.
Leaf CO2 efflux is attenuated by acclimation of respiration to heat and drought in a Mediterranean tree.CrossRef |

Ryan MG (1995) Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content. Plant, Cell & Environment 18, 765–772.
Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content.CrossRef | 1:CAS:528:DyaK2MXnsFKmurg%3D&md5=a65e0963ed104fd622d38c4cbe2bc64bCAS |

Sabaté S, Gracia CA, Sánchez A (2002) Likely effects of climate change on growth of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in the Mediterranean region. Forest Ecology and Management 162, 23–37.
Likely effects of climate change on growth of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in the Mediterranean region.CrossRef |

Searle SY, Bitterman DS, Thomas S, Griffin KL, Atkin OK, Turnbull MH (2011) Respiratory alternative oxidase responds to both low- and high-temperature stress in Quercus rubra leaves along an urban–rural gradient in New York. Functional Ecology 25, 1007–1017.
Respiratory alternative oxidase responds to both low- and high-temperature stress in Quercus rubra leaves along an urban–rural gradient in New York.CrossRef |

Shapiro JB, Griffin KL, Lewis JD, Tissue DT (2004) Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature. New Phytologist 162, 377–386.
Response of Xanthium strumarium leaf respiration in the light to elevated CO2 concentration, nitrogen availability and temperature.CrossRef | 1:CAS:528:DC%2BD2cXksVWjur0%3D&md5=d7a224d8f5c5beac36405b3b5545b0e5CAS |

Tcherkez G, Cornic G, Bligny R, Gout E, Ghashghaie J (2005) In vivo respiratory metabolism of illuminated leaves. Plant Physiology 138, 1596–1606.
In vivo respiratory metabolism of illuminated leaves.CrossRef | 1:CAS:528:DC%2BD2MXmvV2ks70%3D&md5=7a810ed2aaa4ffe481f7ccd148cb35f4CAS |

Tcherkez G, Bligny R, Gout E, Mahe A, Hodges M, Cornic G (2008) Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions. Proceedings of the National Academy of Sciences of the United States of America 105, 797–802.
Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions.CrossRef | 1:CAS:528:DC%2BD1cXhtVSjtLw%3D&md5=f7721eb18c3f264bd039bc22edd11706CAS |

Tcherkez G, Mahe A, Gauthier P, Mauve C, Gout E, Bligny R, Cornic G, Hodges M (2009) In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D Isotope effects highlight the noncyclic nature of the tricarboxylic acid ‘cycle’ in illuminated leaves. Plant Physiology 151, 620–630.
In folio respiratory fluxomics revealed by 13C isotopic labeling and H/D Isotope effects highlight the noncyclic nature of the tricarboxylic acid ‘cycle’ in illuminated leaves.CrossRef | 1:CAS:528:DC%2BD1MXht12qu7fK&md5=f11fa5999e412a1e32790f5e8cc253a3CAS |

Tcherkez G, Boex-Fontvieille E, Mahé A, Hodges M (2012) Respiratory carbon fluxes in leaves. Current Opinion in Plant Biology 15, 308–314.
Respiratory carbon fluxes in leaves.CrossRef | 1:CAS:528:DC%2BC38Xnsl2qsb0%3D&md5=86d394a23771c158855e830fc873737cCAS |

Tcherkez G, Gauthier P, Buckley TN, Busch FA, Barbour MM, Bruhn D, Heskel MA, Gong XY, Crous K, Griffin KL, Way DA, Turnbull MH, Adams MA, Atkin OK, Bender M, Farquhar GD, Cornic G (2017) Tracking the origins of the Kok effect, 70 years after its discovery. New Phytologist 214, 506–510.
Tracking the origins of the Kok effect, 70 years after its discovery.CrossRef |

Tissue DT, Lewis JD, Wullschleger SD, Amthor JS, Griffin KL, Anderson R (2002) Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field. Tree Physiology 22, 1157–1166.
Leaf respiration at different canopy positions in sweetgum (Liquidambar styraciflua) grown in ambient and elevated concentrations of carbon dioxide in the field.CrossRef |

Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytologist 167, 493–508.
Linking leaf and root trait syndromes among 39 grassland and savannah species.CrossRef | 1:CAS:528:DC%2BD2MXpt1ersbg%3D&md5=007024a432df89c59854b538761b85aeCAS |

Tjoelker MG, Oleksyn J, Lorenc-Plucinska G, Reich PB (2009) Acclimation of respiratory temperature responses in northern and southern populations of Pinus banksiana. New Phytologist 181, 218–229.
Acclimation of respiratory temperature responses in northern and southern populations of Pinus banksiana.CrossRef | 1:CAS:528:DC%2BD1MXhtlaktL0%3D&md5=3a013c40f44f75e39cd016c02dcff474CAS |

Turnbull MH, Whitehead D, Tissue DT, Schuster WSF, Brown KJ, Griffin KL (2003) Scaling foliar respiration in two contrasting forest canopies. Functional Ecology 17, 101–114.
Scaling foliar respiration in two contrasting forest canopies.CrossRef |

Turnbull MH, Tissue DT, Griffin KL, Richardson SJ, Peltzer DA, Whitehead D (2005) Respiration characteristics in temperate rainforest tree species differ along a long-term soil-development chronosequence. Oecologia 143, 271–279.
Respiration characteristics in temperate rainforest tree species differ along a long-term soil-development chronosequence.CrossRef |

Valladares F, Zaragoza-Castells J, Sanchez-Gomez D, Matesanz S, Alonso B, Portsmuth A, Delgado A, Atkin OK (2008) Is shade beneficial for Mediterranean shrubs experiencing periods of extreme drought and late-winter frosts? Annals of Botany 102, 923–933.
Is shade beneficial for Mediterranean shrubs experiencing periods of extreme drought and late-winter frosts?CrossRef |

Villar R, Held AA, Merino J (1994) Comparison of methods to estimate dark respiration in the light in leaves of two woody species. Plant Physiology 105, 167–172.
Comparison of methods to estimate dark respiration in the light in leaves of two woody species.CrossRef | 1:CAS:528:DyaK2cXjtFyrs74%3D&md5=bf692cb6d50f3b3991f562377dd4bbfaCAS |

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 | 1:CAS:528:DyaL38XjtFyjug%3D%3D&md5=31bf351b27c18f0eb8ba097d189b9e2fCAS |

Wang XZ, Lewis JD, Tissue DT, Seemann JR, Griffin KL (2001) Effects of elevated atmospheric CO2 concentration on leaf dark respiration of Xanthium strumarium in light and in darkness. Proceedings of the National Academy of Sciences of the United States of America 98, 2479–2484.
Effects of elevated atmospheric CO2 concentration on leaf dark respiration of Xanthium strumarium in light and in darkness.CrossRef | 1:CAS:528:DC%2BD3MXhslKmsrg%3D&md5=e06147171de019e44f9251a8d9b4c167CAS |

Wang XZ, Anderson OR, Griffin KL (2004) Chloroplast numbers, mitochondrion numbers and carbon assimilation physiology of Nicotinana sylvestris as affected by CO2 concentration. Environmental and Experimental Botany 51, 21–31.
Chloroplast numbers, mitochondrion numbers and carbon assimilation physiology of Nicotinana sylvestris as affected by CO2 concentration.CrossRef | 1:CAS:528:DC%2BD2cXosVyj&md5=7a1a11ea83ab1874e731c78bcdd8646aCAS |

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.
Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data.CrossRef |

Whitehead D, Boelman N, Turnbull M, Griffin K, Tissue D, Barbour M, Hunt J, Richardson S, Peltzer D (2005) Photosynthesis and reflectance indices for rainforest species in ecosystems undergoing progression and retrogression along a soil fertility chronosequence in New Zealand. Oecologia 144, 233–244.
Photosynthesis and reflectance indices for rainforest species in ecosystems undergoing progression and retrogression along a soil fertility chronosequence in New Zealand.CrossRef |

Wingate L, Seibt U, Moncrieff JB, Jarvis PG, Lloyd J (2007) Variations in 13C discrimination during CO2 exchange by Picea sitchensis branches in the field. Plant, Cell & Environment 30, 600–616.
Variations in 13C discrimination during CO2 exchange by Picea sitchensis branches in the field.CrossRef | 1:CAS:528:DC%2BD2sXlt1Ggsr8%3D&md5=49af8b2e614380d6188535df04ae0654CAS |

Wohlfahrt G, Bahn M, Haslwanter A, Newesely C, Cernusca A (2005) Estimation of daytime ecosystem respiration to determine gross primary production of a mountain meadow. Agricultural and Forest Meteorology 130, 13–25.
Estimation of daytime ecosystem respiration to determine gross primary production of a mountain meadow.CrossRef |

Wright IJ, Reich PB, Atkin OK, Lusk CH, Tjoelker MG, Westoby M (2006) Irradiance, temperature and rainfall influence leaf dark respiration in woody plants: evidence from comparisons across 20 sites. New Phytologist 169, 309–319.
Irradiance, temperature and rainfall influence leaf dark respiration in woody plants: evidence from comparisons across 20 sites.CrossRef | 1:CAS:528:DC%2BD28XhtlKntLo%3D&md5=9fdc558045b085137fffc0b6a7ad3a35CAS |

Wythers KR, Reich PB, Tjoelker MG, Bolstad PB (2005) Foliar respiration acclimation to temperature and temperature variable Q 10 alter ecosystem carbon balance. Global Change Biology 11, 435–449.
Foliar respiration acclimation to temperature and temperature variable Q 10 alter ecosystem carbon balance.CrossRef |

Xu CY, Griffin KL (2006) Seasonal variation in the temperature response of leaf respiration in Quercus rubra: foliage respiration and leaf properties. Functional Ecology 20, 778–789.
Seasonal variation in the temperature response of leaf respiration in Quercus rubra: foliage respiration and leaf properties.CrossRef |

Xu M, Debiase TA, Qi Y, Goldstein A, Liu Z (2001) Ecosystem respiration in a young ponderosa pine plantation in the Sierra Nevada Mountains, California. Tree Physiology 21, 309–318.
Ecosystem respiration in a young ponderosa pine plantation in the Sierra Nevada Mountains, California.CrossRef | 1:STN:280:DC%2BD3M7mtlOmtg%3D%3D&md5=a74959b9040544453d229163c6195a92CAS |

Zaragoza-Castells J, Sanchez-Gomez D, Valladares F, Hurry V, Atkin OK (2007) Does growth irradiance affect temperature dependence and thermal acclimation of leaf respiration? Insights from a Mediterranean tree with long-lived leaves. Plant, Cell & Environment 30, 820–833.
Does growth irradiance affect temperature dependence and thermal acclimation of leaf respiration? Insights from a Mediterranean tree with long-lived leaves.CrossRef | 1:CAS:528:DC%2BD2sXnvFGitbY%3D&md5=0885755c8c85b15b0638090ef943e466CAS |

Zaragoza-Castells J, Sanchez-Gomez D, Hartley IP, Matesanz S, Valladares F, Lloyd J, Atkin OK (2008) Climate-dependent variations in leaf respiration in a dry-land, low productivity Mediterranean forest: the importance of acclimation in both high-light and shaded habitats. Functional Ecology 22, 172–184.



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