, Volume 183, Issue 1, pp 303–313 | Cite as

Photosynthetic responses of a dominant C4 grass to an experimental heat wave are mediated by soil moisture

  • D. L. HooverEmail author
  • A. K. Knapp
  • M. D. Smith
Global change ecology – original research


Extreme heat waves and drought are predicted to increase in frequency and magnitude with climate change. These extreme events often co-occur, making it difficult to separate their direct and indirect effects on important ecophysiological and carbon cycling processes such as photosynthesis. Here, we assessed the independent and interactive effects of experimental heat waves and drought on photosynthesis in Andropogon gerardii, a dominant C4 grass in a native mesic grassland. We experimentally imposed a two-week heat wave at four intensity levels under two contrasting soil moisture regimes: a well-watered control and an extreme drought. There were three main findings from this study. First, the soil moisture regimes had large effects on canopy temperature, leading to extremely high temperatures under drought and low temperatures under well-watered conditions. Second, soil moisture mediated the photosynthetic response to heat; heat reduced photosynthesis under the well-watered control, but not under the extreme drought treatment. Third, the effects of heat on photosynthesis appeared to be driven by a direct thermal effect, not indirectly through other environmental or ecophysiological variables. These results suggest that while photosynthesis in this dominant C4 grass is sensitive to heat stress, this sensitivity can be overwhelmed by extreme drought stress.


Canopy temperature Climate extremes Drought Ecophysiology Tallgrass prairie 



We thank Patrick O’ Neal, Jeff Taylor, Kelsey Duffy, Mellissa Steen, Peter Bridgwater, Qee Qee Gao, and Katie Earixson for help with field and lab work. We would also like to acknowledge the Konza Prairie Biological Station, the Konza Prairie Long-Term Ecological Research program, Kansas State University Division of Biology and Colorado State University for institutional support. This project was funded by the Department of Energy Terrestrial Ecosystems Science Program (DE-FG02-04ER63892).

Author contribution statement

DLH, AKK, and MDS designed the study, analyzed the data, and wrote the manuscript. DLH established the experiment and collected the field data. MDS acquired financial support.

Supplementary material

442_2016_3755_MOESM1_ESM.docx (27 kb)
Supplementary material 1 (DOCX 26 kb)


  1. Arnone JA, Verburg PSJ, Johnson DW et al (2008) Prolonged suppression of ecosystem carbon dioxide uptake after an anomalously warm year. Nature 455:383–386. doi: 10.1038/nature07296 CrossRefPubMedGoogle Scholar
  2. Blecker SW (2005) Silica biogeochemistry across a grassland climosequence, PhD Disser. Colorado State University, Fort Collins, CO, USAGoogle Scholar
  3. Burnette DJ, Stahle DW (2012) Historical perspective on the dust bowl drought in the central United States. Clim Change 116:479–494. doi: 10.1007/s10584-012-0525-2 CrossRefGoogle Scholar
  4. Burnette DJ, Stahle DW, Mock CJ (2010) Daily-mean temperature reconstructed for kansas from early instrumental and modern observations. J Clim 23:1308–1333. doi: 10.1175/2009JCLI2445.1 CrossRefGoogle Scholar
  5. De Boeck HJ, Dreesen FE, Janssens IA, Nijs I (2010) Climatic characteristics of heat waves and their simulation in plant experiments. Glob Chang Biol 16:1992–2000. doi: 10.1111/j.1365-2486.2009.02049.x CrossRefGoogle Scholar
  6. De Boeck HJ, Dreesen FE, Janssens IA, Nijs I (2011) Whole-system responses of experimental plant communities to climate extremes imposed in different seasons. New Phytol 189:806–817. doi: 10.1111/j.1469-8137.2010.03515.x CrossRefPubMedGoogle Scholar
  7. De Boeck HJ, Bassin S, Verlinden M et al (2016) Simulated heat waves affected alpine grassland only in combination with drought. New Phytol 209:531–541. doi: 10.1111/nph.13601 CrossRefPubMedGoogle Scholar
  8. Déry SJ, Wood EF (2005) Observed twentieth century land surface air temperature and precipitation covariability. Geophys Res Lett 32:L21414–L21418. doi: 10.1029/2005GL024234 CrossRefGoogle Scholar
  9. Dwyer SA, Ghannoum O, Nicotra A, Von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant Cell Environ 30:53–66. doi: 10.1111/j.1365-3040.2006.01605.x CrossRefPubMedGoogle Scholar
  10. Gates DM (1965) Energy, Plants, and Ecology. Ecology 46:1–13. doi: 10.2307/1935252 CrossRefGoogle Scholar
  11. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  12. Hoover DL, Knapp AK, Smith MD (2014a) Contrasting sensitivities of two dominant C4 grasses to heat waves and drought. Plant Ecol 215:721–731. doi: 10.1007/s11258-014-0345-8 CrossRefGoogle Scholar
  13. Hoover DL, Knapp AK, Smith MD (2014b) Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95:2646–2656. doi: 10.1890/13-2186.1 CrossRefGoogle Scholar
  14. Houghton RA (2007) Balancing the Global Carbon Budget. Annu Rev Earth Planet Sci 35:313–347. doi: 10.1146/ CrossRefGoogle Scholar
  15. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the Fifth assessment report of the intergovernmental panel on climate change. Cambdridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  16. Jentsch A, Kreyling J, Beierkuhnlein C (2007) A new generation of climate-change experiments: events, not trends. Front Ecol Environ 5:365–374CrossRefGoogle Scholar
  17. Knapp AK, Briggs JM, Hartnett DC, Collins SL (1998) Grassland dynamics: long-term ecological reserach in tallgrass prairie. Oxford University Press Inc, New YorkGoogle Scholar
  18. Knapp A, Briggs J, Koelliker J (2001) Frequency and extent of water limitation to primary production in a mesic temperate grassland. Ecosystems 4:19–28. doi: 10.1007/s100210000057 CrossRefGoogle Scholar
  19. Marchand FL, Verlinden M, Kockelbergh F, Graae BJ (2006) Disentangling effects of an experimentally imposed extreme temperature event and naturally associated. Funct Ecol 20:917–928. doi: 10.1111/j.1365-2435.2006.01203.x CrossRefGoogle Scholar
  20. Milbau A, Scheerlinck L, Reheul D et al (2005) Ecophysiological and morphological parameters related to survival in grass species exposed to an extreme climatic event. Physiol Plant 125:500–512. doi: 10.1111/j.1399-3054.2005.00586.x CrossRefGoogle Scholar
  21. Mildrexler DJ, Zhao M, Running SW (2011) A global comparison between station air temperatures and MODIS land surface temperatures reveals the cooling role of forests. J Geophys Res 116:G03025. doi: 10.1029/2010JG001486 CrossRefGoogle Scholar
  22. Nippert JB, Fay PA, Carlisle JD et al (2009) Ecophysiological responses of two dominant grasses to altered temperature and precipitation regimes. Acta Oecol 35:400–408. doi: 10.1016/j.actao.2009.01.010 CrossRefGoogle Scholar
  23. Noy-Meir I (1973) Desert Ecosystems; environment and producers. Annu Reveue Ecol Syst 4:25–51CrossRefGoogle Scholar
  24. Oki T, Kanae S (2006) Global hydrological cycles and world water resources. Science 313:1068–1072. doi: 10.1126/science.1128845 CrossRefPubMedGoogle Scholar
  25. Rodriguez-Itrube I, Poropato A (2004) Ecohydrology of water-controlled ecosystems: Soil moisture and plant dynamics. Cambridge University Press, Cambridge, EnglandGoogle Scholar
  26. Sala O, Parton W, Joyce L, Lauenroth W (1988) Primary production of the central grassland region of the United States. Ecology 69:40–45CrossRefGoogle Scholar
  27. Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186CrossRefPubMedGoogle Scholar
  28. Seneviratne SI, Corti T, Davin EL et al (2010) Investigating soil moisture-climate interactions in a changing climate: a review. Earth Sci Rev 99:125–161. doi: 10.1016/j.earscirev.2010.02.004 CrossRefGoogle Scholar
  29. Smith MD (2011) An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J Ecol 99:656–663. doi: 10.1111/j.1365-2745.2011.01798.x CrossRefGoogle Scholar
  30. Smith M, Knapp A (2003) Dominant species maintain ecosystem function function with non-random species loss. Ecol Lett 6:509–517CrossRefGoogle Scholar
  31. Swemmer A, Knapp A, Smith M (2006) Growth responses of two dominant C4 grass species to altered water availability. Int J Plant Sci 167:1001–1010CrossRefGoogle Scholar
  32. Trenberth KE, Shea DJ (2005) Relationships between precipitation and surface temperature. Geophys Res Lett 32:1–4. doi: 10.1029/2005GL022760 CrossRefGoogle Scholar
  33. Trenberth KE, Fasullo JT, Kiehl J (2009) Earth’s global energy budget. Bull Am Meteorol Soc 90:311–323. doi: 10.1175/2008BAMS2634.1 CrossRefGoogle Scholar
  34. Wahid A, Gelani S, Ashraf M, Foolad M (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223. doi: 10.1016/j.envexpbot.2007.05.011 CrossRefGoogle Scholar
  35. Weaver J (1954) North American Prairie. Johnsen, Lincoln, NebraskaGoogle Scholar
  36. Whan K, Zscheischler J, Orth R et al (2015) Impact of soil moisture on extreme maximum temperatures in Europe. Weather Clim Extrem 9:57–67. doi: 10.1016/j.wace.2015.05.001 CrossRefGoogle Scholar
  37. Woodhouse C, Overpeck J (1998) 2000 years of drought variability in the central United States. Bull Am Meteorol Soc 79:2693–2714CrossRefGoogle Scholar
  38. Yahdjian L, Sala O (2002) A rainout shelter design for intercepting different amounts of rainfall. Oecologia 133:95–101. doi: 10.1007/s00442-002-1024-3 CrossRefGoogle Scholar
  39. Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117. doi: 10.1007/s11120-013-9874-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Graduate Degree Program in Ecology and Department of BiologyColorado State UniversityFort CollinsUSA

Personalised recommendations