Skip to main content
Log in

Leaf functional trait responses to changes in water status differ among three oak (Quercus) species

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

We monitored differences in rates of foliar carbon-compound increases with progressive drought as an indicator of sink limitation status and subsequent drought tolerance. We postulate that species which increase foliar carbohydrates and protein-precipitable phenolics (PPP) more quickly than related species over the same time period and drought conditions have stronger sink limitations and are therefore less drought tolerant. Quercus macrocarpa, Q. shumardii, and Q. virginiana saplings were subjected to two treatments for approximately 3.5 months: (1) watered, which received the equivalent of average weekly precipitation for College Station, TX, USA, and (2) droughted, in which precipitation was reduced by 100%. Q. virginiana’s photosynthesis (A) and stomatal conductance (gs) were 44 and 54% greater, respectively, than the other species in the drought treatment. Q. virginiana’s gs also increased more dramatically with watering and subsequent increases in predawn leaf water potential. This plasticity suggests Q. virginiana is best equipped to deal with sporadic rainfall events and soil moisture changes, at least in the short term. Results indicate that the three species allocate carbon from photosynthate in different ways. Q. shumardii had the most soluble sugar in its foliage but had the least PPP, while Q. virginiana and macrocarpa had more PPP and less sugar than Q. shumardii. Diameter:height growth rate was greatest in Q. shumardii. Foliar protein-precipitable phenolic content appears to be more affected by factors other than drought. Differences in species’ physiological responses to drought may result in stand composition shifts with future climate alterations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abdala-Díaz RT, Cabello-Pasini A, Pérez-Rodríguez E, Conde Álvarez RM, Figueroa FL (2006) Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Marine Biol 148:459–465

    Article  Google Scholar 

  • Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238

    Article  Google Scholar 

  • Acero A, Muir JP, Wolfe RM (2010) Nutritional composition and condensed tannin concentration changes as browse leaves become litter. J Sci Food Agric 90:2582–2585

    Article  CAS  Google Scholar 

  • Adams HD, Guardiola-Claramonte M, Barron-Gafford GA, Villegas JC, Breshears DD, Zou CB, Troch PA, Huxman TE (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc Natl Acad Sci 106:7063–7066

    Article  CAS  Google Scholar 

  • Adams HD, Germino MJ, Breshears DD, Barron-Gafford GA, Guardiola-Claramonte M, Zou CB, Huxman TE (2013) Nonstructural leaf carbohydrate dynamics of Pinus edulis during drought-induced tree mortality reveal role for carbon metabolism in mortality mechanism. New Phytol 197:1142–1151

    Article  CAS  Google Scholar 

  • Adams HD, Zeppel MJ, Anderegg WRL et al (2017) A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol 1:1285

    Article  Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684

    Article  Google Scholar 

  • Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:129

    Article  Google Scholar 

  • Anderegg WRL, Martinez-Vilalta J, Cailleret M, Camarero JJ, Ewers BE, Galbraith D, Gessler A, Grote R, Huang C, Levick SR, Powell TL, Rowland L, Sanchez-Salguero R, Trotsiuk V (2016) When a tree dies in the forest: scaling climate-driven tree mortality to ecosystem water and carbon fluxes. Ecosystems 19:1133–1147

    Article  Google Scholar 

  • Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    Article  CAS  Google Scholar 

  • Balok CA, St. Hilaire H (2002) Drought responses among seven southwestern landscape tree taxa. J Am Soc Hort Sci 127:211–218

    Google Scholar 

  • Bendevis MA, Owens MK, Heilman JL, McInnes KJ (2010) Carbon exchange and water loss from two evergreen trees in a semiarid woodland. Ecohydrol 3:107–115

    CAS  Google Scholar 

  • Blackman CJ, Brodribb TJ, Jordan GJ (2012) Leaf hydraulic vulnerability influences species’ bioclimatic limits in a diverse group of woody angiosperms. Oecologia 168:1–10

    Article  Google Scholar 

  • Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT (2009) Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Front Ecol Environ 7:185–189

    Article  Google Scholar 

  • Breshears DD, Adams HD, Eamus D, McDowell N, Law DJ, Will R, Williams AP, Zou CB (2013) The critical amplifying role of increasing atmospheric moisture demand on tree mortality and associated regional die-off. Front Plant Sci 4:266

    Article  Google Scholar 

  • Cavender-Bares J, Holbrook NM (2001) Hydraulic properties and freezing-induced cavitation in sympatric evergreen and deciduous oaks with contrasting habitats. Plant Cell Environ 24:1243–1256

    Article  Google Scholar 

  • Cavender-Bares J, Sack L, Savage J (2007) Atmospheric and soil drought reduce nocturnal conductance in live oaks. Tree Physiol 27:611–620

    Article  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Chervenka WG (2003) Soil survey of Brazos County, Texas. [Washington, DC]: U.S. Department of Agriculture, Natural Resources Conservation Service

  • Clark JS, Iverson L, Woodall CW, Allen CD, Bell DM, Bragg DC, D’amato AW, Davis FW, Hersh MH, Ibanez I, Jackson ST, Matthews S, Pederson N, Peters M, Schwartz MW, Waring KM, Zimmermann NE (2016) The impacts of increasing drought on forest dyanamics, structure, and biodiversity in the United States. Global Change Biol 22:2329–2352

    Article  Google Scholar 

  • Close DC, McArthur C (2002) Rethinking the role of many plant phenolics- protection from photodamage not herbivores? Oikos 99:166–172

    Article  CAS  Google Scholar 

  • Del Tredici P (2001) Sprouting in temperate trees: a morphological and ecological review. Bot Rev 67:121–140

    Article  Google Scholar 

  • Dickson RE, Tomlinson PT (1996) Oak growth, development and carbon metabolism in response to water stress. Ann Sci For 53:181–196

    Article  Google Scholar 

  • Domec J-C, Johnson DM (2012) Does homeostasis or disturbance of homeostasis in minimum leaf water potential explain the isohydric versus anisohydric behavior of Vitis vinifera L. cultivars? Tree Physiol 32:245–248

    Article  Google Scholar 

  • Galiano L, Martínez-Vilalta J, Sabaté S, Lloret F (2012) Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean holm oak forest. Tree Physiol 32:478–489

    Article  Google Scholar 

  • Galle A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytol 174:799–810

    Article  CAS  Google Scholar 

  • Galvez DA, Landhäusser SM, Tyree MT (2011) Root carbon reserve dynamics in aspen seedlings: does simulated drought induce reserve limitation? Tree Physiol 31:250–257

    Article  Google Scholar 

  • Gazal RM, Kubiske ME (2004) Influence of initial root length on physiological responses of cherrybark oak and Shumard oak seedlings to field drought conditions. For Ecol Manag 189:295–305

    Article  Google Scholar 

  • Gilman EF, Watson DG (1994) Quercus virginiana: Southern live oak. ENH-722, IFAS Extension, University of Florida, Gainesville

  • Hagerman AE, Butler LG (1978) Protein precipitation method for the quantitative determination of tannins. J Agric Food Chem 26:809–812

    Article  CAS  Google Scholar 

  • Hamerlynck E, Knapp AK (1996) Photosynthetic and stomatal responses to high temperature and light in two oaks at the western limit of their range. Tree Physiol 16:557–565

    Article  CAS  Google Scholar 

  • Heilman JL, McInnes KJ, Kjelgaard JF, Owens MK, Schwinning S (2009) Energy balance and water use in a subtropical karst woodland on the Edwards Plateau, Texas. J. Hydrol. 373:426–435

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quart Rev Biol 67:283–335

    Article  Google Scholar 

  • Hirota M, Holmgren M, Van Nes EH, Scheffer M (2011) Global resilience of tropical forest and savanna to critical transitions. Science 334:232–235

    Article  CAS  Google Scholar 

  • Hrazdina G (1992) Biosynthesis of flavonoids. In: Hemingway RW, Laks PE (eds) Plant polyphenols: synthesis, properties, significance. Springer Science + Business Media, New York, pp 61–72

    Chapter  Google Scholar 

  • Jactel H, Petit J, Desprez-Loustau M-L, Delzon S, Piou D, Battisti A, Koricheva J (2011) Drought effects on damage by forest insects and pathogens: a meta-analysis. Global Change Biol 18:267–276

    Article  Google Scholar 

  • Johnson DM, Woodruff DR, McCulloh KA, Meinzer FC (2009) Leaf hydraulic conductance, measured in situ, declines and recovers daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species. Tree Physiol 29:879–887

    Article  CAS  Google Scholar 

  • Johnson DM, Berry ZC, Baker KV, Smith DD, McCulloh KA, Domec JC (2018) Leaf hydraulic parameters are more plastic in species that experience a wider range of leaf water potentials. Funct Ecol 32:894–903

    Article  Google Scholar 

  • Kandil FE, Grace MH, Seigler DS, Cheeseman JM (2004) Polyphenolics in Rhizophora mangle L. leaves and their changes during leaf development and senescence. Trees 18:518–528

    Article  CAS  Google Scholar 

  • Keskitalo J, Bergquist G, Gardeström P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139:1635–1648

    Article  CAS  Google Scholar 

  • Kleczewski NM, Herms DA, Bonello P (2010) Effects of soil type, fertilization, and drought on carbon allocation to root growth and partitioning between secondary metabolism and ectomycorrhizae of Betula papyrifera. Tree Physiol 30:807–817

    Article  CAS  Google Scholar 

  • Korner C (2003) Carbon limitation in trees. J Ecol 91:4–17

    Article  Google Scholar 

  • Kozlowski TT, Pallardy SG (2002) Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334

    Article  Google Scholar 

  • Kukowski KR, Schwinning S, Schwartz BF (2013) Hydraulic responses to extreme drought conditions in three co-dominant tree species in shallow soil over bedrock. Oecologia 171:819–830

    Article  Google Scholar 

  • Leuschner C, Moser G, Bertsch C, Röderstein M, Hertel D (2007) Large altitudinal increase in tree root/shoot ratio in tropical forests of Ecuador. Basic Appl Ecol 8:219–230

    Article  Google Scholar 

  • Libby RA (1970) Direct starch analysis using DMSO solubilization and glucoamylase. Cereal Chem 47:273–281

    CAS  Google Scholar 

  • Litvak ME, Schwinning S, Heilman JL (2011) Woody plant rooting depth and ecosystem function of savannas: a case study from the Edwards Plateau Karst, Texas. In: Hill MJ, Hanan NP (eds) Ecosystem function in savannas: measurement and modeling at landscape to global scales. CRC Press, Boca Raton, pp 117–135

    Google Scholar 

  • Mayer AL, Khalyani AH (2011) Grass trumps trees with fire. Science 334:188–189

    Article  CAS  Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    Article  Google Scholar 

  • McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol 26:523–532

    Article  Google Scholar 

  • Meinzer FC, Woodruff DR, Eissenstat DM, Lin HS, Adams TS, McCulloh KA (2013) Above- and belowground controls on water use by trees of different wood types in an eastern US deciduous forest. Tree Physiol 33:345–356

    Article  Google Scholar 

  • Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes an R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941

    Article  CAS  Google Scholar 

  • Moore GW, Edgar CB, Vogel JG, Washington-Allen RA, March RG, Zehnder R (2016) Tree mortality from an exceptional drought spanning mesic to semiarid ecoregions. Ecol Appl 26:602–611

    Article  Google Scholar 

  • Moya D, de las Heras J, López-Serrano FR, Ferrandis P (2015) Post-fire seedling recruitment and morpho-ecophysiological responses to induced drought and salvage logging in Pinus halepensis Mill. stands. Forests 6:1858–1877

    Article  Google Scholar 

  • Myster RW (2009) Controls on Shumard oak (Quercus shumardii) establishment into the Cross Timbers Ecotone of Oklahoma: implications for restoration. Restor Ecol 17:893–899

    Article  Google Scholar 

  • National Weather Service (NWS) (2014) College Station Climate Data. Issued by NWS Houston/Galveston, TX. http://www.weather.gov/hgx/climate_cll. Accessed 7 Feb 2017

  • Naumann HD, Hagerman AE, Lambert BD, Muir JP, Tedeschi LO, Kothmann MM (2014) Molecular weight and protein-precipitating ability of condensed tannins from warm-season perennial legumes. J Plant Interact 9:212–219

    Article  CAS  Google Scholar 

  • Nowacki GJ, Abrams MD (2008) The demise of fire and “mesophication” of forests in the Eastern United States. BioScience 58:123–138

    Article  Google Scholar 

  • Olano JM, Menges ES, Martínez E (2006) Carbohydrate storage in five resprouting Florida scrub plants across a fire chronosequence. New Phytol 170:99–106

    Article  CAS  Google Scholar 

  • Owens MK, Schreiber MC (1992) Seasonal gas exchange characteristics of two evergreen trees in a semiarid environment. Photosynthetica 26:389–398

    Google Scholar 

  • Peterson DW, Reich PB (2001) Prescribed fire in oak savanna: fire frequency effects on stand structure and dynamics. Ecol Appl 11:914–927

    Article  Google Scholar 

  • Picon C, Ferhi A, Guehl JM (1997) Concentration and σ13C of leaf carbohydrates in relation to gas exchange in Quercus robur under elevated CO2 and drought. J Exp Bot 48:1547–1556

    CAS  Google Scholar 

  • Pockman WT, Sperry JS (2000) Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. Am J Bot 87:1287–1299

    Article  CAS  Google Scholar 

  • Porensky LM, Wittman SE, Riginos C, Young TP (2013) Herbivory and drought interact to enhance spatial patterning and diversity in a savanna understory. Oecologia 173:591–602

    Article  Google Scholar 

  • Poyatos R, Llorens P, Pinol J, Rubio C (2008) Response of Scots pine (Pinus sylvestris L.) and pubescent oak (Quercus pubescens Willd.) to soil and atmospheric water deficits under Mediterranean mountain climate. Ann For Sci 65:306

    Article  Google Scholar 

  • Renninger HJ, Carlo NJ, Clark KL, Schäfer KVR (2015) Resource use and efficiency, and stomatal responses to environmental drivers of oak and pine species in an Atlantic Coastal Plain forest. Front Plant Sci 6:1–16

    Article  Google Scholar 

  • Rodriguez-Calcerrada J, Buatois B, Chiche E, Shahin O, Staudt M (2013) Leaf isoprene emission declines in Quercus pubescens seedlings experiencing drought: any implication of soluble sugars and mitochondrial respiration? Environ Exp Bot 85:36–42

    Article  CAS  Google Scholar 

  • Rose R, Rose CL, Omi SK, Forry KR, Durall DM, Bigg WL (1991) Starch determination by perchloric acid vs enzymes: evaluating the accuracy and precision of six colorimetric methods. J Agric Food Chem 39:2–11

    Article  CAS  Google Scholar 

  • Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281

    Article  Google Scholar 

  • Sevanto S, McDowell NG, Dickman LT, Pangle R, Pockman WT (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ 37:153–161

    Article  CAS  Google Scholar 

  • Staver AC, Archibald S, Levin S (2011) Tree cover in sub-Saharan Africa: rainfall and fire contstrain forest and savanna as alternative stable states. Ecology 92:1063–1072

    Article  Google Scholar 

  • Turtola S, Rousi M, Pusenius J, Yamaji K, Heiska S, Tirkkonen V, Meier B, Julkunen-Tiitto R (2005) Clone-specific responses in leaf phenolics of willows exposed to enhanced UVB radiation and drought stress. Global Change Biol 11:1655–1663

    Article  Google Scholar 

  • Villar-Salvador P, Planelles R, Oliet J, Penuelas-Rubira JL, Jacobs DF, Gonzalez M (2004) Drought tolerance and transplanting performance of holm oak (Quercus ilex) seedlings after drought hardening in the nursery. Tree Physiol 24:1147–1155

    Article  Google Scholar 

  • Voelker SL, Meinzer FC, Lachenbruch B, Brooks JR, Guyete RP (2013) Drivers of radial growth and carbon isotope discrimination of bur oak (Quercus macrocarpa Michx.) across continental gradients in precipitation, vapour pressure deficit, and irradiance. Plant Cell Environ 37:766–779

    Article  Google Scholar 

  • Volder A, Tjoelker MG, Briske DD (2010) Contrasting physiological responsiveness of establishing trees and a C4 grass to rainfall events, intensified summer drought, and warming in oak savanna. Global Change Biol 16:3349–3362

    Article  Google Scholar 

  • Volder A, Briske DD, Tjoelker MG (2013) Climate warming and precipitation redistribution modify tree-grass interactions and tree species establishment in a warm-temperate savanna. Global Change Biol 19:843–857

    Article  Google Scholar 

  • Wang Z, Stutte GW (1992) The role of carbohydrates in active osmotic adjustment in apple under water stress. J Am Soc Hort Sci 117:816–823

    CAS  Google Scholar 

  • Will RE, Wilson SM, Zou CB, Hennessey TC (2013) Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone. New Phytol 200:366–374

    Article  Google Scholar 

  • Wolfe RM, Terrill TH, Muir JP (2008) Drying method and origin of standard affect condensed tannin (CT) concentrations in perennial herbaceous legumes using simplified butanol-HCl CT analysis. J Sci Food Ag 88:1060–1067

    Article  CAS  Google Scholar 

  • Wu M, Zhang WH, Ma C, Zhou JY (2013) Changes in morphological, physiological, and biochemical responses to different levels of drought stress in Chinese cork oak (Quercus variabilis Bl.) seedlings. Rus J Plant Physiol 60:681–692

    Article  CAS  Google Scholar 

  • Wurth MKR, Pelaez-Riedl S, Wright S, Korner C (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia 143:11–24

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Eboni Hall for assistance with designing the experiment, planting seedlings, and refurbishing the rainout shelters. Dr. Tom Byram and the Texas A&M Forest Service provided the seedlings. We thank Luiza Aparecido, Qihua He, Marco Minor, Ingrid Karklins, and the Aggie Research Scholars for assistance with field measurements. Nichole Cherry assisted with laboratory analyses. This research was supported in part by an Ann Miller Gonzalez Graduate Research Grant from the Native Plant Society of Texas.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Caitlyn E. Cooper.

Additional information

Communicated by Marjan Jongen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 53 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cooper, C.E., Vogel, J.G., Muir, J.P. et al. Leaf functional trait responses to changes in water status differ among three oak (Quercus) species. Plant Ecol 219, 1463–1479 (2018). https://doi.org/10.1007/s11258-018-0894-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-018-0894-3

Keywords

Navigation