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Effects of climate warming on photosynthesis in boreal tree species depend on soil moisture

Naturevolume 562pages263267 (2018) | Download Citation

Abstract

Climate warming will influence photosynthesis via thermal effects and by altering soil moisture1,2,3,4,5,6,7,8,9,10,11. Both effects may be important for the vast areas of global forests that fluctuate between periods when cool temperatures limit photosynthesis and periods when soil moisture may be limiting to carbon gain4,5,6,9,10,11. Here we show that the effects of climate warming flip from positive to negative as southern boreal forests transition from rainy to modestly dry periods during the growing season. In a three-year open-air warming experiment with juveniles of 11 temperate and boreal tree species, an increase of 3.4 °C in temperature increased light-saturated net photosynthesis and leaf diffusive conductance on average on the one-third of days with the wettest soils. In all 11 species, leaf diffusive conductance and, as a result, light-saturated net photosynthesis decreased during dry spells, and did so more sharply in warmed plants than in plants at ambient temperatures. Consequently, across the 11 species, warming reduced light-saturated net photosynthesis on the two-thirds of days with driest soils. Thus, low soil moisture may reduce, or even reverse, the potential benefits of climate warming on photosynthesis in mesic, seasonally cold environments, both during drought and in regularly occurring, modestly dry periods during the growing season.

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Data availability

The data reported in this paper are available from the Environmental Data Initiative (EDI) at https://doi.org/10.6073/pasta/258239f68244c959de0f97c922ac313f.

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References

  1. 1.

    Kao, S. C. & Ganguly, A. R. Intensity, duration, and frequency of precipitation extremes under 21st-century warming scenarios. J. Geophys. Res. 116, D16119 (2011).

  2. 2.

    Novick, K. A. et al. The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nat. Clim. Change 6, 1023–1027 (2016).

  3. 3.

    Seager, R. et al. Dynamical and thermodynamical causes of large-scale changes in the hydrological cycle over North America in response to global warming. J. Clim. 27, 7921–7948 (2014).

  4. 4.

    Moyes, A. B., Castanha, C., Germino, M. J. & Kueppers, L. M. Warming and the dependence of limber pine (Pinus flexilis) establishment on summer soil moisture within and above its current elevation range. Oecologia 171, 271–282 (2013).

  5. 5.

    Price, D. T. et al. Anticipating the consequences of climate change for Canada’s boreal forest ecosystems. Environ. Rev. 21, 322–365 (2013).

  6. 6.

    Hogg, E. H., Michaelian, M., Hook, T. I. & Undershultz, M. E. Recent climatic drying leads to age-independent growth reductions of white spruce stands in western Canada. Glob. Change Biol. 23, 5297–5308 (2017).

  7. 7.

    IPCC. Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) (Cambridge Univ. Press, 2013).

  8. 8.

    Sherwood, S. & Fu, Q. A drier future? Science 343, 737–739 (2014).

  9. 9.

    Wang, Y., Hogg, E. H., Price, D. T., Edward, J. & Williamson, T. Past and projected future changes in moisture conditions in the Canadian boreal forest. Forest. Chron. 90, 678–691 (2014).

  10. 10.

    Girardin, M. P. et al. No growth stimulation of Canada’s boreal forest under half-century of combined warming and CO2 fertilization. Proc. Natl Acad. Sci. USA 113, E8406–E8414 (2016).

  11. 11.

    D’Orangeville, L. et al. Northeastern North America as a potential refugium for boreal forests in a warming climate. Science 352, 1452–1455 (2016).

  12. 12.

    Wong, S. C., Cowan, I. R. & Farquhar, G. D. Stomatal conductance correlates with photosynthetic capacity. Nature 282, 424–426 (1979).

  13. 13.

    Bloom, A. J., Chapin, I. F. S. & Mooney, H. A. Resource limitation in plants—an economic analogy. Annu. Rev. Ecol. Syst. 16, 363–392 (1985).

  14. 14.

    Rastetter, E. B. & Shaver, G. R. A model of multiple element limitation for acclimating vegetation. Ecology 73, 1157–1174 (1992).

  15. 15.

    Buermann, W., Bikash, P. R., Jung, M., Burn, D. H. & Reichstein, M. Earlier springs decrease peak summer productivity in North American boreal forests. Environ. Res. Lett. 8, 024027 (2013).

  16. 16.

    Ma, Z. et al. Regional drought-induced reduction in the biomass carbon sink of Canada’s boreal forests. Proc. Natl Acad. Sci. USA 109, 2423–2427 (2012).

  17. 17.

    Moyes, A. B., Germino, M. J. & Kueppers, L. M. Moisture rivals temperature in limiting photosynthesis by trees establishing beyond their cold-edge range limit under ambient and warmed conditions. New Phytol. 207, 1005–1014 (2015).

  18. 18.

    Peng, C. et al. A drought-induced pervasive increase in tree mortality across Canada’s boreal forests. Nat. Clim. Change 1, 467–471 (2011).

  19. 19.

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

  20. 20.

    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. Change Biol. 21, 2334–2348 (2015).

  21. 21.

    Sendall, K. M. et al. Effects of experimental forest warming on photosynthetic temperature optima of temperate and boreal tree species. Glob. Change Biol. 21, 1342–1357 (2015).

  22. 22.

    Reich, P. B. et al. Boreal and temperate trees show strong acclimation of respiration to warming. Nature 531, 633–636 (2016).

  23. 23.

    Rawls, W. J., Brakensiek, D. L. & Sexton, K. E. Estimation of soil water properties. Trans. ASAE 25, 1316–1320 (1982).

  24. 24.

    Campbell, G. S. & Norman, J. M. An Introduction to Environmental Biophysics (Springer-Verlag, New York, 1998).

  25. 25.

    Sharkey, T. D. Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot. Rev. 51, 53–105 (1985).

  26. 26.

    Jones, H. G. Partitioning stomatal and non-stomatal limitations to photosynthesis. Plant Cell Environ. 8, 95–104 (1985).

  27. 27.

    Sage, R. F. & Kubien, D. S. The temperature response of C3 and C4 photosynthesis. Plant Cell Environ. 30, 1086–1106 (2007).

  28. 28.

    Körner, C. Paradigm shift in plant growth control. Curr. Opin. Plant Biol. 25, 107–114 (2015).

  29. 29.

    FOA. State of the World’s Forests http://www.fao.org/docrep/013/i2000e/i2000e00.htm (FOA, 2011).

  30. 30.

    De Kauwe, M. G. et al. A test of the ‘one-point method’ for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis. New Phytol. 210, 1130–1144 (2016).

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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. We thank D. Ellsworth, Ch. Messier, J. Drake and B. Medlyn for helpful comments on the manuscript.

Reviewer information

Nature thanks M. Mencuccini, M. Ryan and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

  1. Department of Forest Resources, University of Minnesota, St. Paul, MN, USA

    • Peter B. Reich
    • , Kerrie M. Sendall
    • , Artur Stefanski
    • , Roy L. Rich
    •  & Rebecca A. Montgomery
  2. Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia

    • Peter B. Reich
  3. Department of Biology, Georgia Southern University, Statesboro, GA, USA

    • Kerrie M. Sendall
  4. Smithsonian Environmental Research Center, Edgewater, MD, USA

    • Roy L. Rich
  5. Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN, USA

    • Sarah E. Hobbie

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Contributions

P.B.R., R.A.M., R.L.R. and S.E.H. designed the overall experiment. P.B.R., R.A.M. and A.S. designed the specific study reported herein. R.L.R. designed the warming system, R.L.R. and A.S. implemented the warming system, and A.S. and K.M.S. coordinated the day-to-day field measurements. P.B.R. coordinated the overall experiment and this specific study and analysed the data. P.B.R. wrote the first draft and jointly wrote subsequent drafts of the manuscript with the other co-authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Peter B. Reich.

Extended data figures and tables

  1. Extended Data Fig. 1 Soil water (VWC) in relation to day of year.

    af, VWC (m3 m−3; 0–20 cm depth) was averaged by day, variation shown daily across the season among treatments, sites and years. Daily values represent means among all plots within a treatment at each site. Measurements were logged continuously, recorded hourly, thus a total of approximately 3,600 measurements for each of the 24 plots in each year for the time period are shown. Vertical dashed lines show the range of dates during which photosynthetic measurements were made.

  2. Extended Data Fig. 2 Range of temperature, evaporative demand (VPG) and soil moisture across the three growing seasons during gas exchange measurements.

    Top, average leaf temperature and VPG for all gas exchange measurements across the three years in relation to soil water (VWC). There was no significant correlation between VPG and VWC over the three-year period (P > 0.30); there was a significant correlation (R2 = 0.03, P < 0.001) between leaf temperature and VWC across warming treatments. Bottom, net photosynthetic rate in relation to leaf temperature (polynomial fit all data pooled, R2 = 0.02, P < 0.001). Blue, ambient; red, +3.4 °C. Sample sizes, approximately 1,989–2,050, around half in each warming treatment. A few data points are out of the y-axis range and therefore not visible.

  3. Extended Data Fig. 3 Maximum biochemical photosynthetic capacity in moist soils.

    Mean (±s.e.m.) maximum carboxylation capacity (Vcmax-25, μmol m−2 s−1) at 25 °C of 11 gymnosperm and angiosperm trees species in ambient (grey) and +3.4 °C experimentally warmed (black) treatments for days with moist soils (data are shown for the highest half of VWC observations, those with VWC > 0.148). Species within groups are arranged from left to right from most temperate to most boreal distribution (as in Fig. 1). Data are from multiple days across three years and otherwise averaged across the spectrum of moist soil water availability. Individual measurements are shown as small grey dots. Sample sizes by species for ambient, +3.4 °C: A. rubrum, 78, 55; Q. rubra, 75, 47; Q macrocarpa, 43, 28; R. cathartica, 69, 48; A. saccharum, 44, 29; P. tremuloides, 92, 50; B. papyrifera, 91, 56; P. strobus, 36, 22; P banksiana, 36, 24; A. balsamea, 10, 6; P glauca, 11, 6. A few data points are out of the y-axis range and are therefore not visible.

  4. Extended Data Fig. 4 Percentage of stomatal limitation of net photosynthesis in relation to soil moisture (VWC) by species for ambient and experimentally warmed plants.

    The percentage of stomatal limitation was calculated according to previous studies25,26. Data are from multiple days across three years (n = 1,991 across species). In a full model analogous to those used in Table 1, the slope of the percentage of stomatal limitation versus VWC was significantly steeper in warmed (red) than ambient (blue) plants (interaction of VWC × warming treatment, F1,593 = 38.1, P < 0.0001). The arrows show the median VWC across all measurements for the ambient and warmed plants of each species. Species are arranged from top to bottom by their geographical ranges (temperate species in top two rows, boreal in bottom two rows).

  5. Extended Data Fig. 5 Relationships of net photosynthesis and leaf conductance to soil water content for different VPG classes and leaf temperatures.

    Relationships are shown for two temperature treatments, for three VPG classes (left four panels) and three leaf temperature classes (right four panels). Data are pooled across all species and show the regression line for Anet and gs in relation to VWC in three VPG classes (0.4–1.6, 1.6–2.8, 2.8–4.0 kPa; red, green and blue lines, respectively) and for ambient and warmed (+3.4 °C) treatment plants; and in relation to VWC in three Tleaf classes (8–20, 20–32, 32–38 °C; dashed, dotted, and solid black lines, respectively) for ambient and warmed (+3.4 °C) treatment plants. Sample sizes in each panel, around 950–995. A few data points are out of the y-axis range and therefore not visible.

  6. Extended Data Fig. 6 Conceptual illustration of mechanisms that influence the effect of climate warming on the response of realized Anet and soil water content (VWC).

    Schematics are shown for angiosperms (left) and gymnosperms (right). Red lines indicate warmed treatment plants, blue lines ambient plants. The regression lines are pooled for all seven angiosperms and all four gymnosperms, at each warming treatment. The arrows show the direction of the effect of warming treatment on specific factors and the size of the letters indicates the relative magnitude of those effects on Anet. Bold fonts in black indicate changes that increase Anet in warmed plants relative to ambient plants, italic fonts in grey indicate changes that decrease Anet in warmed plants relative to ambient plants. For angiosperms in moist soils, warmed plants exhibit large increases in Vcmax and in carbon demand (from 23% higher growth19) that far outweigh the likely modest increases in dark respiration in the light (Rlight)22 and in photorespiration (Rphoto)27, to result in large increases in Anet. For angiosperms in dry soils, however, experimental warming results in lower water availability that slows growth, reducing carbon demand in warmed (compared to ambient) plants. In dry soils, warming also increases stomatal limitation of photosynthesis (perhaps due in part to slightly higher VPG in warmed plots), and constrains the magnitude of positive effects of Vcmax on Anet. The combination of increased Rlight and Rphoto and reduced carbon demand, slightly outweigh increased Vcmax and result in slightly reduced Anet in warmed compared to ambient angiosperms. The responses of gymnosperms are similar, except that changes in Vcmax with warming are less positive (than in angiosperms) in moist soils and negative in dry soils; additionally, the negative overall growth response (−26% growth response on average19) to warming suggests at most a small warming-induced increase in carbon sink strength when soils are wet and a larger decline when soils are dry. Collectively these factors make the Anet response of gymnosperms to warming more negative than that of angiosperms at every VWC level. Additionally (not shown in this conceptual figure, see Fig. 1), climate warming leads to higher evapotranspiration and thus more pronounced soil drying, therefore warmed plants operate at lower levels of VWC on average (Fig. 1) and at the vast majority of points in time (Extended Data Fig. 1), promoting the tendency of warmed plants to have lower Anet on average than ambient plants (Fig. 3).

  7. Extended Data Table 1 Annual climate means for the two sites before and during the experiment
  8. Extended Data Table 2 VWC percentiles for measurement dates and all dates
  9. Extended Data Table 3 Species-specific models of photosynthesis in relation to warming treatment and soil moisture
  10. Extended Data Table 4 Summaries of mixed model analyses for species examined across two or three years

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https://doi.org/10.1038/s41586-018-0582-4

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