Identification of suites of traits that explains drought resistance and phenological patterns of plants in a semi-arid grassland community

Abstract

Grassland ecosystems are comprised of plants that occupy a wide array of phenological niches and vary considerably in their ability to resist the stress of seasonal soil–water deficits. Yet, the link between plant drought resistance and phenology remains unclear in perennial grassland ecosystems. To evaluate the role of soil water availability and plant drought tolerance in driving phenology, we measured leaf hydraulic conductance (Ksat), resistance to hydraulic failure (P50), leaf gas exchange, plant and soil water stable isotope ratios (δ18O), and several phenology metrics on ten perennial herbaceous species in mixed-grass prairie. The interaction between P50 and δ18O of xylem water explained 67% of differences in phenology, with lower P50 values associated with later season activity, but only among shallow-rooted species. In addition, stomatal control and high water-use efficiency also contributed to the late flowering and late senescence strategies of plants that had low P50 values and relied upon shallow soil water. Alternatively, plants with deeper roots did not possess drought-tolerant leaves, but had high hydraulic efficiency, contributing to their ability to efficiently move water longer distances while maintaining leaf water potential at relatively high values. The suites of traits that characterize these contrasting strategies provide a mechanistic link between phenology and plant–water relations; thus, these traits could help predict grassland community responses to changes in water availability, both temporally and vertically within the soil profile.

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References

  1. Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405

    PubMed  Google Scholar 

  2. Blumenthal DM, Mueller KE, Kray JA, LeCain DR, Pendall E, Duke S, Zelikova TJ, Dijkstra FA, Williams DG, Morgan JA (2018) Warming and elevated CO2 interact to alter seasonality and reduce variability of soil water in a semiarid grassland. Ecosystems 21:1533–1544

    CAS  Google Scholar 

  3. Borghetti M, Leonarditi S, Raschit A, Snyderman D, Tognetti R (1993) Ecotypic variation of xylem embolism, phenological traits, growth parameters and allozyme characteristics in Fagus sylvatica. Funct Ecol 7:713–720

    Google Scholar 

  4. Bragg WK, Knapp AK, Briggs JM (1993) Comparative water relations of seedling and adult Quercus species during gallery forest expansion in tallgrass prairie. For Ecol Manage 56:29–41

    Google Scholar 

  5. Brodribb T, Holbrook N (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Bucher SF, König P, Menzel A, Migliavacca M, Ewald J, Römermann C (2018) Traits and climate are associated with first flowering day in herbaceous species along elevational gradients. Ecol Evol 8:1147–1158

    PubMed  Google Scholar 

  7. Chen JW, Zhang Q, Li XS, Cao KF (2009) Independence of stem and leaf hydraulic traits in six Euphorbiaceae tree species with contrasting leaf phenology. Planta 230:459–468

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006) Diverse responses of phenology to global changes in a grassland ecosystem. Proc Natl Acad Sci 103:13740–13744

    CAS  PubMed  Google Scholar 

  9. Craine JM, Wolkovich EM, Gene Towne E, Kembel SW (2012) Flowering phenology as a functional trait in a tallgrass prairie. New Phytol 193:673–682

    PubMed  Google Scholar 

  10. Delzon S (2015) New insight into leaf drought tolerance. Funct Ecol 29:1247–1249

    Google Scholar 

  11. Denny EG, Gerst KL, Miller-Rushing AJ, Tierney GL, Crimmins TM, Enquist CAF, Guertin P, Rosemartin AH, Schwartz MD, Thomas KA et al (2014) Standardized phenology monitoring methods to track plant and animal activity for science and resource management applications. Int J Biometeorol 58:591–601

    PubMed  PubMed Central  Google Scholar 

  12. Dickinson CE, Dodd JL (1976) Phenological patterns in the shortgrass prairie. Am Midl Nat 96:367–378

    Google Scholar 

  13. Dorji T, Totland Ø, Moe SR, Hopping KA, Pan J, Klein JA (2013) Plant functional traits mediate reproductive phenology and success in response to experimental warming and snow addition in Tibet. Glob Change Biol 19:459–472

    Google Scholar 

  14. Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24:411–439

    Google Scholar 

  15. Fowler N (1986) The role of competition in plant communities in arid and semiarid regions. Annu Rev Ecol Syst 17:89–110

    Google Scholar 

  16. Fu PL, Jiang YJ, Wang AY, Brodribb TJ, Zhang JL, Zhu SD, Cao KF (2012) Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest. Ann Bot 110:189–199

    PubMed  PubMed Central  Google Scholar 

  17. Gleason SM, Stephens AEA, Tozer WC, Blackman CJ, Butler DW, Chang Y, Cook AM, Cooke J, Laws CA, Rosell JA et al (2018) Shoot growth of woody trees and shrubs is predicted by maximum plant height and associated traits. Funct Ecol 32:247–259

    Google Scholar 

  18. Golluscio RA, Sala OE (1993) Plant functional types and ecological strategies in Patagonian forbs. J Veg Sci 4:839–846

    Google Scholar 

  19. Griffin-Nolan RJ, Ocheltree TW, Mueller KE, Blumenthal DM, Kray JA, Knapp AK (2019a) Extending the osmometer method for assessing drought tolerance in herbaceous species. Oecologia 189:353–363

    PubMed  Google Scholar 

  20. Griffin-Nolan RJ, Blumenthal DM, Collins SL, Farkas TE, Hoffman AM, Mueller KE, Ocheltree TW, Smith MD, Whitney KD, Knapp AK (2019b) Shifts in plant functional composition following long-term drought in grasslands. J Ecol 107:2133–2148

    CAS  Google Scholar 

  21. Hacke U, Sperry J, Pittermann J (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 41:31–41

    Google Scholar 

  22. Hovenden MJ, Wills KE, Vander Schoor JK, Williams AL, Newton PCD (2008) Flowering phenology in a species-rich temperate grassland is sensitive to warming but not elevated CO2. New Phytol 178:815–822

    CAS  PubMed  Google Scholar 

  23. Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268

    PubMed  Google Scholar 

  24. Keefe KO, Nippert JB (2017) An assessment of diurnal water uptake in a mesic prairie: evidence for hydraulic lift? Oecologia 183:963–975

    Google Scholar 

  25. Kirkham MB (2005) Principles of soil and plant water relations. Elsevier Academic Press, Burlington

    Google Scholar 

  26. Kulmatiski A, Beard KH (2013) Woody plant encroachment facilitated by increased precipitation intensity. Nat Clim Change 3:833–837

    CAS  Google Scholar 

  27. Kunkel K, Stevens L, Stevens S, Sun L, Janssen E, Wuebbles D, Kruk M, Thomas D, Shulski S, Umphlett N et al (2013) Regional climate trends and scenarios for the U.S. National Climate Assessment. Part 4. Climate of the U.S. Great Plains. NOAA, Washington D.C

  28. Lane DR, Coffin DP, Lauenroth WK (2000) Changes in grassland canopy structure across a precipitation gradient. J Veg Sci 11:359–368

    Google Scholar 

  29. Lauenroth W, Sala O (1992) Long-term forage production of North-American shortgrass steppe. Ecol Appl 2:397–403

    CAS  PubMed  Google Scholar 

  30. Levitt J (1980) Responses of plants to environmental stresses. Volume II. Water, radiation, salt, and other stresses. Academic Press, New York

    Google Scholar 

  31. Lopez OR, Kursar TA, Cochard H, Tyree MT (2005) Interspecific variation in xylem vulnerability to cavitation among tropical tree and shrub species. Tree Physiol 25:1553–1562

    PubMed  Google Scholar 

  32. Moore LM, Lauenroth WK (2017) Differential effects of temperature and precipitation on early- vs. Late-flowering species. Ecosphere 8

  33. Moore LM, Lauenroth WK, Bell DM, Schlaepfer DR (2015) Soil water and temperature explain canopy phenology and onset of spring in a semiarid steppe. Great Plains Res 25:121–138

    Google Scholar 

  34. Mueller KE, Blumenthal DM, Pendall E, Carrillo Y, Dijkstra FA, Williams DG, Follett RF, Morgan JA (2016) Impacts of warming and elevated CO2 on a semi-arid grassland are non-additive, shift with precipitation, and reverse over time. Ecol Lett 19:956–966

    CAS  PubMed  Google Scholar 

  35. Nobel PS, De La Barrera E (2002) Stem water relations and net CO2 uptake for a hemiepiphytic cactus during short-term drought. Environ Exp Bot 48:129–137

    Google Scholar 

  36. Ocheltree TW, Nippert JB, Prasad PVV (2016) A safety vs efficiency trade-off identified in the hydraulic pathway of grass leaves is decoupled from photosynthesis, stomatal conductance and precipitation. New Phytol 210:97–107

    CAS  PubMed  Google Scholar 

  37. Panchen ZA, Primack RB, Nordt B, Ellwood ER, Stevens AD, Renner SS, Willis CG, Fahey R, Whittemore A, Du Y et al (2014) Leaf out times of temperate woody plants are related to phylogeny, deciduousness, growth habit and wood anatomy. New Phytol 203:1208–1219

    CAS  PubMed  Google Scholar 

  38. Poorter L, McDonald I, Alarcon A, Fichtler E, Licona JC, Peña-Carlos M, Sterck F, Villegas Z, Sass-klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species—Poorter—2009—New Phytologist—Wiley Online Library. New Phytol 481–492

    PubMed  Google Scholar 

  39. Reich PB, Buschena C, Tjoelker MG, Wrage K, Knops J, Tilman D, Machado JL (2003) Variation in growth rate and ecophysiology among 34 grassland and savanna species under contrasting N supply: a test of functional group differences. New Phytol 157:617–631

    Google Scholar 

  40. Schindelin J, Arganda-Carreras I, Frise E, Al E (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    CAS  Google Scholar 

  41. Schuman G, Reeder JD, Manley JT, Hart RH, Manley WA (1999) Impact of grazing management on the carbon and nitrogen balance of a mixed-grass rangeland. Ecol Appl 9:65–71

    Google Scholar 

  42. Schwinning S, Davis K, Richardson L, Ehleringer J (2002) Deuterium enriched irrigation indicates different forms of rain use in shrub/grass species of the Colorado Plateau. Oecologia 130:345–355

    PubMed  Google Scholar 

  43. Scoffoni C, McKown AD, Rawls M, Sack L (2012) Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state. J Exp Bot 63:643–658

    CAS  PubMed  Google Scholar 

  44. Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiol 164:1772–1788

    CAS  PubMed  Google Scholar 

  45. Smedley MP, Dawson TE, Comstock JP, Donovan LA, Sherrill DE, Cook CS, Ehleringer JR (1991) Seasonal carbon isotope discrimination in a grassland community. Oecologia 85:314–320

    PubMed  Google Scholar 

  46. Sun S, Frelich LE (2011) Flowering phenology and height growth pattern are associated with maximum plant height, relative growth rate and stem tissue mass density in herbaceous grassland species. J Ecol 99:991–1000

    Google Scholar 

  47. Tucker SS, Craine JM, Nippert JB (2011) Physiological drought tolerance and the structuring of tallgrass prairie assemblages. Ecosphere 2:art48

    Google Scholar 

  48. Tyree MT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot 23:267–282

    Google Scholar 

  49. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer-Verlag, Berlin

    Google Scholar 

  50. Volaire F (2018) A unified framework of plant adaptive strategies to drought: crossing scales and disciplines. Glob Change Biol 24:2929–2938

    Google Scholar 

  51. Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Funct Ecol 6:469–475

    Google Scholar 

  52. Wolkovich EM, Cleland EE (2014) Phenological niches and the future of invaded ecosystems with climate change. AoB PLANTS 6:1–16

    Google Scholar 

  53. Yin J, Fridley JD, Smith MS, Bauerle TL (2016) Xylem vessel traits predict the leaf phenology of native and non-native understorey species of temperate deciduous forests. Funct Ecol 30:206–214

    Google Scholar 

  54. Yu K, Goldsmith GR, Wang Y, Anderegg WRL (2019) Phylogenetic and biogeographic controls of plant nighttime stomatal conductance. New Phytol 222:1778–1788

    CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to acknowledge the ARS Rangeland Resources and Systems Research unit for access to facilities at the High Plains Grassland Research Station in Cheyenne, WY. We also want to thank Julie Bushey and Mary Carlson for their energetic assistance and good humor during field work, and the thoughtful comments from the anonymous reviewers of our manuscript.

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TO developed the idea and hypotheses of the project; TO, KM, and DB designed the experiment; TO, KM, DB, DL, JK, and KC collected and analyzed the data. TO led the writing of the manuscript with editing and intellectual contributions from KM, DB, JK, and KC.

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Correspondence to T. W. Ocheltree.

Additional information

Communicated by David R. Bowling.

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Ocheltree, T.W., Mueller, K.M., Chesus, K. et al. Identification of suites of traits that explains drought resistance and phenological patterns of plants in a semi-arid grassland community. Oecologia 192, 55–66 (2020). https://doi.org/10.1007/s00442-019-04567-x

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Keywords

  • Drought tolerance
  • Leaf hydraulic conductance
  • Phenology
  • P50
  • Rooting depth
  • Semi-arid grassland
  • Water isotopes
  • Water-use strategies