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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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.

Author information

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.

Correspondence to Peter B. Reich.

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Competing interests

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) doi:10.1038/nature17142

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