Skip to main content
Log in

Homeostasis in leaf water potentials on leeward and windward sides of desert shrub crowns: water loss control vs. high hydraulic efficiency

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Phenotypic plasticity in morphophysiological leaf traits in response to wind was studied in two dominant shrub species of the Patagonian steppe, used as model systems for understanding effects of high wind speed on leaf water relations and hydraulic properties of small woody plants. Morpho-anatomical traits, hydraulic conductance and conductivity and water relations in leaves of wind-exposed and protected crown sides were examined during the summer with nearly continuous high winds. Although exposed sides of the crowns were subjected to higher wind speeds and air saturation deficits than the protected sides, leaves throughout the crown had similar minimum leaf water potential (ΨL). The two species were able to maintain homeostasis in minimum ΨL using different physiological mechanisms. Berberis microphylla avoided a decrease in the minimum ΨL in the exposed side of the crown by reducing water loss by stomatal control, loss of cell turgor and low epidermal conductance. Colliguaja integerrima increased leaf water transport efficiency to maintain transpiration rates without increasing the driving force for water loss in the wind-exposed crown side. Leaf physiological changes within the crown help to prevent the decrease of minimum ΨL and thus contribute to the maintenance of homeostasis, assuring the hydraulic integrity of the plant under unfavorable conditions. The responses of leaf traits that contribute to mechanical resistance (leaf mass per area and thickness) differed from those of large physiological traits by exhibiting low phenotypic plasticity. The results of this study help us to understand the unique properties of shrubs which have different hydraulic architecture compared to trees.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aasamaa K, Sober A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Aust J Plant Physiol 28:765–774

    Google Scholar 

  • Anten NP, Casado-Garcia R, Pierik R, Pons TL (2006) Ethylene sensitivity affects changes in growth patterns, but not stem properties, in response to mechanical stress in tobacco. Physiol Plant 128:274–282

    Article  CAS  Google Scholar 

  • Anten NPR, Alcala-Herrera R, Schieving F, Onoda Y (2010) Wind and mechanical stimuli differentially affect leaf traits in Plantago major. New Phytol 188:554–564

    Article  PubMed  Google Scholar 

  • Bauerle WL, Hinckley TM, Cermak J, Kucera J, Bible K (1999) The canopy water relations of old-growth Douglas-fir trees. Trees 13:211–217

    Article  Google Scholar 

  • Beeskow AM, Del Valle HF, Rostagno CM (1987) Los sistemas fisiográficos de la región árida y semiárida de la provincia del Chubut. S. C de Bariloche SECYT Delegacion Regional Patagonica

  • Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123

    Article  PubMed  Google Scholar 

  • Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P, Scholz FG (2005) Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water in Neotropical savanna trees. Trees 19:296–304

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Franco AC, Campanello PI, Villalobos-Vega R, Bustamante M, Miralles-Wilhelm F (2006) Nutrient availability constrains the hydraulic architecture and water relations of savannah trees. Plant Cell Environ 29:2153–2167

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Hoffmann WA, Meinzer FC, Franco AC, Giambelluca T, Miralles-Wilhelm F (2008) Controls and stand transpiration and soil water utilization along a tree density gradient in a Neotropical savanna. Agric For Meteorol 148:839–849

    Article  Google Scholar 

  • Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Arce ME (2009) Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species. Oecologia 160:631–641

    Article  PubMed  Google Scholar 

  • Campbell GS, Norman JM (1998) An introduction to environmental biophysics. Springer, New York

    Book  Google Scholar 

  • Cochard H, Lemoine D, Dreyer E (1999) The effects of acclimatation to sunlight on the xylem vulnerability to embolism in Fagus sylvatica L. Plant Cell Environ 22:101–108

    Article  Google Scholar 

  • Cordero RA (1999) Ecophysiology of Cecropia schreberiana saplings in two wind regimes in an elfin cloud forest: growth, gas exchange, architecture and stem biomechanics. Tree Physiol 19:153–163

    Google Scholar 

  • De Kroon H, Huber H, Stuefer JF, van Groenendael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82

    Article  PubMed  Google Scholar 

  • De la Barrera E, Walter HS (2006) Wind effects on leaf morphology for the mangrove Conocarpus erecta at an oceanic island from the Mexican Pacific Ocean. Rev Chil Hist Nat 79:451–463

    Google Scholar 

  • Ellsworth DS, Reich PB (1993) Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96:169–178

    Article  Google Scholar 

  • Evans RD, Black RA, Link SO (1990) Rehydration-induced changes in pressure–volume relationships of Artemisia tridentate Nutt. ssp. tridentata. Plant Cell Environ 13:455–461

  • Fluckiger W, Oertli JJ, Fluckiger-Keller H (1978) The effect of wind gusts on leaf growth and foliar water relations of aspen. Oecologia 34:101–106

    Article  Google Scholar 

  • Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30:19–30

    Article  PubMed  Google Scholar 

  • Garcia-Verdugo C (2011) Intracanopy plasticity under strong wind conditions in the wild olive tree (Olea europaea L.): a conserved response between closely related taxa? Trees 25:509–518

    Article  Google Scholar 

  • Garcia-Verdugo C, Granado-Yela C, Manrique E, Rubio de Casas R, Balaguer L (2009) Phenotypic plasticity and integration across the canopy of Olea europaea subsp. guanchica (oleaceae) in populations with different wind exposures. Am J Bot 96:1454–1461

    Article  PubMed  Google Scholar 

  • Gebauer R, Volarik D, Urban J, Borja I, Nagy NE, Drablos Eldhuset T, Krokene P (2012) Effects of different light conditions on the xylem structure of Norway spruce needles. Trees 26(4):1079–1089

    Google Scholar 

  • Givnish TJ, Montgomery RA, Goldstein G (2004) Adaptive radiation of photosynthetic physiology in the Hawaiian lobelias: light regimes, static light responses, and whole-plant compensation points. Am J Bot 9:228–246

    Article  Google Scholar 

  • Grace J (1974) The effect of wind on grasses. 1. Cuticular and stomatal transpiration. J Exp Bot 25:542–551

    Article  Google Scholar 

  • Grace J (1988) Plant response to wind. Agric Ecosyst Environ 22(23):71–88

    Article  Google Scholar 

  • Gratani L, Covone F, Larcher W (2006) Leaf plasticity in response to light of three evergreen species of the Mediterranean maquis. Trees 20:549–558

    Article  Google Scholar 

  • Hejnowicz Z, Barthlott W (2005) Structural and mechanical peculiarities of the petioles of giant leaves of Amorphophallus (Araceae). Am J Bot 92:391–403

    Article  PubMed  Google Scholar 

  • Hoad SP, Grace J, Jeffree EC (1996) A leaf disc method for measuring cuticular conductance. J Exp Bot 47:431–437

    Article  CAS  Google Scholar 

  • Hoad SP, Marzoli A, Grace J, Jeffree CE (1998) Response of leaf surfaces and gas exchange to wind stress and acid mist in birch (Betula pubescens). Trees 13:1–12

    Google Scholar 

  • Howard AR, Donovan LA (2007) Helianthus nighttime conductance and transpiration respond to soil water but not nutrient availability. Plant Physiol 143:145–155

    Article  PubMed  CAS  Google Scholar 

  • Iogna PA, Bucci SJ, Scholz FG, Goldstein G (2011) Water relations and hydraulic architecture of two Patagonian steppe shrubs: effect of slope orientation and microclimate. J Arid Environ 75:763–772

    Article  Google Scholar 

  • Jaffe MJ (1973) Thigmomorphogenesis: the response of plant growth and development to mechanical stimulation. Planta 114:143–157

    Article  Google Scholar 

  • Jarvis PG, McNaughton KJ (1986) Stomatal control of transpiration: scaling up from leaf to region. Adv Ecol Res 15:1–49

    Article  Google Scholar 

  • Kerstiens G (2006) Water transport in plant cuticles: an update. J Exp Bot 57:2493–2499

    Article  PubMed  CAS  Google Scholar 

  • Kolb KJ, Sperry JS, Lamont BB (1996) A method for measuring xylem hydraulic conductance and embolism in entire root and shoot systems. J Exp Bot 47:1805–1810

    Article  CAS  Google Scholar 

  • Lemoide DH, Cochard H, Granier A (2002) Within crown variation in hydraulic architecture in beech (Fagus sylvatica L.): evidence for a stomatal control of xylem embolism. Ann For Sci 59:19–27

    Article  Google Scholar 

  • Maherali H, DeLucia EH (2000) Interactive effects of elevated CO2 and temperature on water transport in ponderosa pine. Am J Bot 87:243–249

    Article  PubMed  CAS  Google Scholar 

  • Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199

    Article  Google Scholar 

  • Meinzer FC, Rundel PW, Sharifi MR, Nilsen ET (1986) Turgor and osmotic relation of the desert shrub Larrea tridentata. Plant Cell Environ 9:467–475

    Article  Google Scholar 

  • Meinzer FC, Goldstein G, Jackson P, Holbrook MN, Gutierrez MV, Cavelier J (1995) Environmental and physiological regulation of transpiration in tropical forest gap species: the influence of boundary layer and hydraulic properties. Oecologia 101:514–522

    Article  Google Scholar 

  • Nardini A, Salleo S (2005) Water stress-induced modifications of leaf hydraulic architecture in sunflower: co-ordination with gas exchange. J Exp Bot 56:3093–3101

    Article  PubMed  CAS  Google Scholar 

  • Nardini A, Tyree MT, Salleo S (2001) Xylem cavitation in the leaf of Prunus laurocerasus and its impact on leaf hydraulics. Plant Physiol 125:1700–1709

    Article  PubMed  CAS  Google Scholar 

  • Niklas KJ (1988) Dependency of the tensile modulus of transverse dimensions, water potential, and cell number of pith parenchyma. Am J Bot 75:1286–1292

    Article  Google Scholar 

  • Niklas KJ (1992) Plant biomechanics: an engineering approach to plant form and function. University of Chicago Press, Chicago

    Google Scholar 

  • Niklas KJ (1996) Differences between Acer saccharum leaves from open and wind-protected sites. Ann Bot 78:61–66

    Article  Google Scholar 

  • Niklas KJ, Molina-Freaner F, Tinoco-Ojanguren C, Paolillo DJ (2000) Wood biomechanics and anatomy of Pachycereus pringlei. Am J Bot 87:469–481

    Article  PubMed  CAS  Google Scholar 

  • Onoda Y, Anten NPR (2011) Challenges to understand plant responses to wind. Plant Signal Behav 6:1057–1059

    Article  PubMed  CAS  Google Scholar 

  • Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Dıaz S, Dominy NJ, Elgart A, Enrico L, Fine PVA, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Perez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE Jr, Van Bael SA, Warton DI, Wright IJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312

    Article  PubMed  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

    Article  PubMed  Google Scholar 

  • Pruyn ML, Ewers BJ, Telewski FW (2000) Thigmomorphogenesis: changes in the morphology and mechanical properties of two Populus hybrids in response to mechanical perturbation. Tree Physiol 20:535–540

    Article  PubMed  Google Scholar 

  • Read J, Sanson GD (2003) Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types. New Phytol 160:81–99

    Article  Google Scholar 

  • Read J, Sanson GD, Lamont BB (2005) Leaf mechanical properties in sclerophyll woodland and shrubland on contrasting soils. Plant Soil 276:95–113

    Google Scholar 

  • Richardson AD, Ashton PMS, Berlyn GP, McGroddy ME, Cameron IR (2001) Within-crown foliar plasticity of western hemlock, Tsuga heterophylla, in relation to stand age. Ann Bot 88:1007–1015

    Article  Google Scholar 

  • Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    Article  PubMed  CAS  Google Scholar 

  • Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. J Exp Bot 53:2177–2184

    Article  PubMed  CAS  Google Scholar 

  • Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell Environ 26:1343–1356

    Article  Google Scholar 

  • Sack L, Melcher PJ, Liu WH, Middleton E, Pardee T (2006) How strong is intracanopy leaf plasticity in temperate deciduous trees? Am J Bot 93:829–839

    Article  PubMed  Google Scholar 

  • Scholz FG, Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Miralles-Wilhelm F (2007) Removal of nutrient limitations by long-term fertilization decreases nocturnal water loss in savanna trees. Tree Physiol 27:551–559

    Article  PubMed  Google Scholar 

  • Scholz FG, Bucci SJ, Arias NS, Meinzer FC, Goldstein G (2012) Osmotic and elastic adjustments in cold desert shrubs differing in rooting depth: coping with drought and subzero temperatures. Oecologia 170:885–897

    Article  PubMed  Google Scholar 

  • Sellin A, Kupper P (2004) Within-crown variation in leaf conductance of Norway spruce: effects of irradiance, vapor pressure deficit, leaf water status and plant hydraulic constraints. Ann For Sci 61:419–429

    Article  Google Scholar 

  • Smith VC, Ennos R (2003) The effects of air flow and stem flexure on the mechanical and hydraulic properties of the stems of sunflowers Helianthus annuus L. J Exp Bot 54:845–849

    Article  PubMed  CAS  Google Scholar 

  • Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modeling isohydric and anisohydric behaviors. J Exp Bot 49:419–432

    Google Scholar 

  • Telewski W (2006) A unified hypothesis of mechanoperception in plants. Amer J Bot 93:1466–1476

    Article  Google Scholar 

  • Telewski FW, Jaffe MJ (1986) Thigmomorphogenesis: field and laboratory studies of Abies fraseri in response to wind or mechanical perturbation. Physiol Plant 66:211–218

    Article  PubMed  CAS  Google Scholar 

  • Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Answer from a model. Plant Physiol 88:574–580

    Article  PubMed  CAS  Google Scholar 

  • Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Plant Mol Biol 40:19–48

    Article  Google Scholar 

  • Tyree MT, Cheung YNS, McGregor ME, Talbot AJB (1978) The characteristic of seasonal and ontogenic changes in the tissue-water relations of Acer, Populus, Tsuga and Picea. Can J Bot 56:635–647

    Article  Google Scholar 

  • Valladares F, Chico JM, Aranda I, Balaguer L, Dizengremel P, Manrique E, Dreyer E (2002) The greater seedling high-light tolerance of Quercus robur over Fagus sylvatica is linked to a greater physiological plasticity. Trees 16:395–403

    CAS  Google Scholar 

  • Van Gardingen PR, Grace J, Jeffree CE (1991) Abrasive damage by wind to the needle surfaces of Picea sitchensis (Bong.) Carr. and Pinus sylvestris L. Plant Cell Environ 14:185–193

    Article  Google Scholar 

  • White DO, Turner NC, Galbraith JH (2000) Leaf water relations and stomatal behavior of four allopatric Eucalyptus species planted in Mediterranean southwestern Australia. Tree Physiol 20:1157–1165

    Article  PubMed  Google Scholar 

  • Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Environ 27:229–236

    Article  Google Scholar 

  • Wyka TP, Oleksyn J, Ytkowiak RZ, Karolewski P, Jagodzinski AM, Reich PB (2012) Responses of leaf structure and photosynthetic properties to intra-canopy light gradients: a common garden test with four broadleaf deciduous angiosperm and seven evergreen conifer tree species. Oecologia 170:11–24

    Article  PubMed  Google Scholar 

  • Zhang Y, Oren R, Kang S (2012) Spatiotemporal variation of crown-scale stomatal conductance in an arid Vitis vinifera L. cv. Merlot vineyard: direct effects of hydraulic properties and indirect effects of canopy leaf area. Tree Physiol 32:262–279

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported in part by CONICET (PIP112-200801-01703) and FONCyT (PICT2010-960) grants. This work complies with Argentinian Law.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabián G. Scholz.

Additional information

Communicated by Kouki Hikosaka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iogna, P.A., Bucci, S.J., Scholz, F.G. et al. Homeostasis in leaf water potentials on leeward and windward sides of desert shrub crowns: water loss control vs. high hydraulic efficiency. Oecologia 173, 675–687 (2013). https://doi.org/10.1007/s00442-013-2666-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2666-z

Keywords

Navigation