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Boreal and temperate trees show strong acclimation of respiration to warming

Abstract

Plant respiration results in an annual flux of carbon dioxide (CO2) to the atmosphere that is six times as large as that due to the emissions from fossil fuel burning, so changes in either will impact future climate. As plant respiration responds positively to temperature, a warming world may result in additional respiratory CO2 release, and hence further atmospheric warming1,2. Plant respiration can acclimate to altered temperatures, however, weakening the positive feedback of plant respiration to rising global air temperature3,4,5,6,7, but a lack of evidence on long-term (weeks to years) acclimation to climate warming in field settings currently hinders realistic predictions of respiratory release of CO2 under future climatic conditions. Here we demonstrate strong acclimation of leaf respiration to both experimental warming and seasonal temperature variation for juveniles of ten North American tree species growing for several years in forest conditions. Plants grown and measured at 3.4 °C above ambient temperature increased leaf respiration by an average of 5% compared to plants grown and measured at ambient temperature; without acclimation, these increases would have been 23%. Thus, acclimation eliminated 80% of the expected increase in leaf respiration of non-acclimated plants. Acclimation of leaf respiration per degree temperature change was similar for experimental warming and seasonal temperature variation. Moreover, the observed increase in leaf respiration per degree increase in temperature was less than half as large as the average reported for previous studies4,7, which were conducted largely over shorter time scales in laboratory settings. If such dampening effects of leaf thermal acclimation occur generally, the increase in respiration rates of terrestrial plants in response to climate warming may be less than predicted, and thus may not raise atmospheric CO2 concentrations as much as anticipated.

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Figure 1: Leaf dark respiration rate of ambient and experimentally warmed plants.
Figure 2: Increase in leaf dark respiration (Rleaf) with +3.4 °C warming for acclimated and non-acclimated plants, among species, by biome of the species.
Figure 3: Relationship between leaf dark respiration measured at 20 °C and the prior 5-night mean temperature, across seasons and years.

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References

  1. Cox, P. M., Betts, R. A., Jones, C. D., Spall, S. A. & Totterdell, I. J. Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408, 184–187 (2000)

    Article  ADS  CAS  Google Scholar 

  2. Heimann, M. & Reichstein, M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451, 289–292 (2008)

    Article  ADS  CAS  Google Scholar 

  3. Atkin, O. K. & Tjoelker, M. G. Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci. 8, 343–351 (2003)

    Article  CAS  Google Scholar 

  4. Campbell, C. et al. Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional type. New Phytol. 176, 375–389 (2007)

    Article  CAS  Google Scholar 

  5. Arneth, A. et al. Terrestrial biogeochemical feedbacks in the climate system. Nature Geosci. 3, 525–532 (2010)

    Article  ADS  CAS  Google Scholar 

  6. Intergovernmental Panel on Climate Change.Climate Change 2013: The Physical Science Basis (Cambridge Univ. Press, 2013)

  7. Slot, M. & Kitajima, K. General patterns of acclimation of leaf respiration to warmer temperatures across biomes and plant types. Oecologia 177, 885–900 (2015)

    Article  ADS  Google Scholar 

  8. Luo, Y. Terrestrial carbon-cycle feedback to climate warming. Annu. Rev. Ecol. Evol. Syst. 38, 683–712 (2007)

    Article  Google Scholar 

  9. Gunderson, C. A., Norby, R. J. & Wullschleger, S. D. Acclimation of photosynthesis and respiration to simulated climatic warming in northern and southern populations of Acer saccharum: laboratory and field evidence. Tree Physiol. 20, 87–96 (2000)

    Article  Google Scholar 

  10. Lee, T. D., Reich, P. B. & Bolstad, P. V. Acclimation of leaf respiration to temperature is rapid and related to specific leaf area, soluble sugars and leaf nitrogen across three temperate deciduous tree species. Funct. Ecol. 19, 640–647 (2005)

    Article  Google Scholar 

  11. Loveys, B. R. et al. Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species. Glob. Change Biol. 9, 895–910 (2003)

    Article  ADS  Google Scholar 

  12. Slot, M. et al. Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming, and consequences for tropical forest carbon balance. Glob. Chang. Biol. 20, 2915–2926 (2014)

    Article  ADS  Google Scholar 

  13. Tjoelker, M. G., Oleksyn, J., Reich, P. B. & Zytkowiak, R. Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations. Glob. Change Biol. 14, 782–797 (2008)

    Article  ADS  Google Scholar 

  14. Smith, N. G. & Dukes, J. S. Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2 . Glob. Chang. Biol. 19, 45–63 (2013)

    Article  ADS  Google Scholar 

  15. Atkin, O. K., Meir, P. & Turnbull, M. H. Improving representation of leaf respiration in large-scale predictive climate–vegetation models. New Phytol. 202, 743–748 (2014)

    Article  Google Scholar 

  16. Smith, N. G. et al. Foliar temperature acclimation reduces simulated carbon sensitivity to climate. Nature Clim. Change http://dx.doi.org/10.1038/nclimate2878 (2016)

  17. Lombardozzi, D. L. et al. Temperature acclimation of photosynthesis and respiration: A key uncertainty in the carbon cycle-climate feedback. Geophys. Res. Lett. 42, 8624–8631 (2015)

    Article  ADS  CAS  Google Scholar 

  18. Reich, P. B. et al. Geographic range predicts photosynthetic and growth response to warming in co-occurring tree species. Nature Clim. Change 5, 148–152 (2015)

    Article  ADS  CAS  Google Scholar 

  19. Rich, R. L. et al. Design and performance of combined infrared canopy and belowground warming in the B4WarmED (Boreal Forest Warming at an Ecotone in Danger) experiment. Glob. Chang. Biol. 21, 2334–2348 (2015)

    Article  ADS  Google Scholar 

  20. O'Sullivan, O. S. et al. High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function. Plant Cell Environ. 36, 1268–1284 (2013)

    Article  Google Scholar 

  21. Kruse, J., Rennenberg, H. & Adams, M. A. Steps towards a mechanistic understanding of respiratory temperature responses. New Phytol. 189, 659–677 (2011)

    Article  CAS  Google Scholar 

  22. Tjoelker, M. G., Oleksyn, J. & Reich, P. B. Modelling respiration of vegetation: evidence for a general temperature-dependent Q10 . Glob. Change Biol. 7, 223–230 (2001)

    Article  ADS  Google Scholar 

  23. Atkin, O. K., Holly, C. & Ball, M. C. Acclimation of snow gum (Eucalyptus pauciflora) leaf respiration to seasonal and diurnal variations in temperature: the importance of changes in the capacity and temperature sensitivity of respiration. Plant Cell Environ. 23, 15–26 (2000)

    Article  Google Scholar 

  24. Bolstad, P. V., Reich, P. B. & Lee, T. D. Rapid temperature acclimation of leaf respiration rates in Quercus alba and Quercus rubra. Tree Physiol. 23, 969–976 (2003)

    Article  Google Scholar 

  25. Reich, P. B. et al. Scaling of respiration to nitrogen in leaves, stems, and roots of higher land plants. Ecol. Lett. 11, 793–801 (2008)

    Article  Google Scholar 

  26. Sendall, K. M. et al. Acclimation of photosynthetic temperature optima of temperate and boreal tree species in response to experimental warming. Glob. Chang. Biol. 21, 1342–1357 (2015)

    Google Scholar 

  27. Katja, H. et al. Temperature responses of dark respiration in relation to leaf sugar concentration. Physiol. Plant. 144, 320–334 (2012)

    Article  Google Scholar 

  28. Ow, L. F., Griffin, K. L., Whitehead, D., Walcroft, A. S. & Turnbull, M. H. Thermal acclimation of leaf respiration but not photosynthesis in Populus deltoides × nigra. New Phytol. 178, 123–134 (2008)

    Article  Google Scholar 

  29. Mitchell, K. A., Bolstad, P. V. & Vose, J. M. Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species. Tree Physiol. 19, 861–870 (1999)

    Article  CAS  Google Scholar 

  30. Heskel, M. A. et al. Convergence in the temperature response of leaf respiration across biomes and plant functional types. Proc. Natl Acad. Sci. (in press)

  31. Atkin, O. K. Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytol. 206, 614–636 (2015)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the US Department of Energy, Office of Science, Office of Biological and Environmental Research award DE-FG02-07ER64456; Minnesota Agricultural Experiment Station MIN-42-030 and MIN-42-060; the Minnesota Department of Natural Resources; and the College of Food, Agricultural, and Natural Resources Sciences and Wilderness Research Foundation, University of Minnesota. Assistance with experimental operation and data collection was provided by K. Rice, C. Buschena, C. Zhao, H. Jihua and numerous summer interns.

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Authors and Affiliations

Authors

Contributions

P.B.R., R.A.M. and R.L.R. designed the study. R.L.R. designed the warming system. R.L.R. and A.S. implemented the warming system and A.S., K.M.S. and X.W. the day-to-day field measurements. P.B.R. analysed the data. P.B.R. wrote the first draft and along with the other co-authors jointly wrote the manuscript.

Corresponding author

Correspondence to Peter B. Reich.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Illustration of complete and partial acclimation.

a, If a plant increased respiration by 40% when placed under conditions 5 °C warmer for 30 min (solid line), but had no increase after 3 weeks at the same +5 °C conditions (dotted line), it would have completely acclimated. b, If the increase over 3 weeks was 30%, it would have partially acclimated by 25% (dotted lined), and so on.

Extended Data Figure 2 Q10 in ambient and experimentally warmed treatments.

ad, Q10 (exponent of the short-term temperature response function, equation (1)) of ambient and experimentally warmed plants of all 10 species, shown for each site (grouped by biome affiliation of the species). Sample size by biome type, site, and warming treatment: boreal, Cloquet (a), ambient = 194, warmed = 206; temperate, Cloquet (b), ambient = 244, warmed = 247; boreal, Ely (c), ambient = 169, warmed = 174; temperate, Ely (d), ambient = 190; warmed = 196. Data are mean and s.e.m.

Extended Data Figure 3 Leaf dark respiration rate using Q10 approach, at a standardized measurement temperature, for ambient and experimentally warmed plants.

ad, Mean (and s.e.m.) leaf respiration at 20 °C (R20) of ambient and experimentally warmed plants of all 10 species. Data derived from equation (1) (Q10 approach) shown for each site (grouped by biome affiliation of the species). Sample size by biome type, site, and warming treatment: boreal, Cloquet (a), ambient = 194, warmed = 206; temperate, Cloquet (b), ambient = 244, warmed = 247; boreal, Ely (c), ambient = 169, warmed = 174; temperate, Ely (d), ambient = 190; warmed = 196.

Extended Data Figure 4 Leaf dark respiration rate using Michaelis–Menton approach, at a standardized measurement temperature, for ambient and experimentally warmed plants.

ad, Mean (and s.e.m.) leaf respiration at 20 °C (R20) of ambient and experimentally warmed plants of all 10 species. Data derived from equation (6) shown for each site (grouped by biome affiliation of the species). Sample size by biome type, site, and warming treatment: boreal, Cloquet (a), ambient = 194, warmed = 206; temperate, Cloquet (b), ambient = 244, warmed = 247; boreal, Ely (c), ambient = 169, warmed = 174; temperate, Ely (d), ambient = 190; warmed = 196.

Extended Data Figure 5 Leaf dark respiration rate of ambient and experimentally warmed plants.

a, b, Data are from five boreal (a) and five temperate (b) tree species. Figure is identical to Fig. 1 except fits were made using equation (6) (Michaelis–Menton model approach) instead of equation (1) (Q10 approach). Respiration is shown at measurement temperatures of 20 °C and 23.4 °C for ambient-grown plants; respiration for plants grown at +3.4 °C conditions is shown at measurement temperature of 23.4 °C. The two values for ambient plants show the increase in respiration with a +3.4 °C temperature increase for non-acclimated plants; comparison of ambient plants measured at 20 °C with warmed plants measured at 23.4 °C represents the increase in respiration with a +3.4 °C temperature increase for acclimated plants. Data are mean and s.e.m. (s.e.m. are from the full model). Sample sizes as in Fig. 2.

Extended Data Figure 6 Percentage acclimation by biome, in response to both experimental warming and seasonal temperature variation.

a, Experimental warming. b, Seasonal temperature variation. Data are mean and s.e.m. Sample sizes as in Fig. 2. Percentage acclimation is calculated according to equation (2).

Extended Data Figure 7 Relationship between Q10 and activation energy of respiration (Ea).

Graph shows relationship between the exponent of the short-term temperature response function (Q10; from equation (1)), and the activation energy of respiration (Ea) from the Arrhenius model (equation (3)). n = 1,620.

Extended Data Figure 8 Frequency distribution of parameter c from the log polynomial model (equation 5) for the respiration–temperature response curve.

Among the 1,620 curves, 894 curves had c < 0, 726 curves had c > 0. Negative c values support the idea of a decelerating function (with a decreasing temperature-sensitive Q10); positive values support an accelerating function. The inconsistency of c being negative indicates a lack of support for a decelerating function, and thus a lack of support for the decelerating log polynomial model as useful for the data in this paper.

Extended Data Table 1 Mean and median R2 and r.m.s.e. of four models
Extended Data Table 2 Species-specific equations relating log(R20) to the prior 5-night temperature

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Reich, P., Sendall, K., Stefanski, A. et al. Boreal and temperate trees show strong acclimation of respiration to warming. Nature 531, 633–636 (2016). https://doi.org/10.1038/nature17142

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