Skip to main content

Advertisement

SpringerLink
Log in

Loss of whole-tree hydraulic conductance during severe drought and multi-year forest die-off

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

Abstract

Understanding the pathways through which drought stress kills woody vegetation can improve projections of the impacts of climate change on ecosystems and carbon-cycle feedbacks. Continuous in situ measurements of whole trees during drought and as trees die hold promise to illuminate physiological pathways but are relatively rare. We monitored leaf characteristics, water use efficiency, water potentials, branch hydraulic conductivity, soil moisture, meteorological variables, and sap flux on mature healthy and sudden aspen decline-affected (SAD) trembling aspen (Populus tremuloides) ramets over two growing seasons, including a severe summer drought. We calculated daily estimates of whole-ramet hydraulic conductance and modeled whole-ramet assimilation. Healthy ramets experienced rapid declines of whole-ramet conductance during the severe drought, providing an analog for what likely occurred during the previous drought that induced SAD. Even in wetter periods, SAD-affected ramets exhibited fivefold lower whole-ramet hydraulic conductance and sevenfold lower assimilation than counterpart healthy ramets, mediated by changes in leaf area, water use efficiency, and embolism. Extant differences between healthy and SAD ramets reveal that ongoing multi-year forest die-off is primarily driven by loss of whole-ramet hydraulic capability, which in turn limits assimilation capacity. Branch-level measurements largely captured whole-plant hydraulic limitations during drought and mortality, but whole-plant measurements revealed a potential role of other losses in the hydraulic continuum. Our results highlight the importance of a whole-tree perspective in assessing physiological pathways to tree mortality and indicate that the effects of mortality on these forests’ assimilation and productivity are larger than expected based on canopy leaf area differences.

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

Access this article

Log in via an institution

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
Fig. 7

Similar content being viewed by others

References

  • Adams HD et al (2009) Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global-change-type drought. Proc Natl Acad Sci USA 106:7063–7066

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Allen CD et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. doi:10.1016/j.foreco.2009.09.001

    Article  Google Scholar 

  • Anderegg W (2012) Complex aspen forest carbon and root dynamics during drought. Clim Change 111:983–991

    Article  Google Scholar 

  • Anderegg WRL, Berry JA, Field CB (2012a) Linking definitions, mechanisms, and modeling of drought-induced tree death. Trends Plant Sci 17:693–700

    Article  CAS  PubMed  Google Scholar 

  • Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB (2012b) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. Proc Natl Acad Sci USA 109:233–237

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anderegg WRL, Kane JM, Anderegg LDL (2012c) Consequences of widespread tree mortality triggered by drought and temperature stress. Nat Clim. 3:30–36

    Article  Google Scholar 

  • Anderegg LDL, Anderegg WRL, Abatzoglou J, Hausladen AM, Berry JA (2013a) Drought characteristics’ role in widespread aspen forest mortality across Colorado, USA. Glob Change Biol 19:1526–1537. doi:10.1111/gcb.12146

    Article  Google Scholar 

  • Anderegg WRL, Plavcová L, Anderegg LDL, Hacke UG, Berry JA, Field CB (2013b) Drought’s legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Glob Change Biol 19:1188–1196

    Article  Google Scholar 

  • Barr AG et al (2007) Climatic controls on the carbon and water balances of a boreal aspen forest, 1994–2003. Glob Change Biol 13:561–576

    Article  Google Scholar 

  • Becker P, Tyree MT, Tsuda M (1999) Hydraulic conductances of angiosperms versus conifers: similar transport sufficiency at the whole-plant level. Tree Physiol 19:445–452

    Article  PubMed  Google Scholar 

  • Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449. doi:10.1126/science.1155121

    Article  CAS  PubMed  Google Scholar 

  • Bowling DR, Burns SP, Conway TJ, Monson RK, White JWC (2005) Extensive observations of CO2 carbon isotope content in and above a high-elevation subalpine forest. Glob Biogeochem. Cycles 19:GB3023. doi: 10.1029/2004GB002394

  • Brodribb TJ (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Sci 177:245–251. doi:10.1016/j.plantsci.2009.06.001

    Article  CAS  Google Scholar 

  • Brodribb TJ, Feild TS (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant Cell Environ 23:1381–1388. doi:10.1046/j.1365-3040.2000.00647.x

    Article  Google Scholar 

  • Brugnoli E, Hubick KT, von Caemmerer S, Wong SC, Farquhar GD (1988) Correlation between the carbon isotope discrimination in leaf starch and sugars of C3 plants and the ratio of intercellular and atmospheric partial pressures of carbon dioxide. Plant Physiol 88:1418–1424. doi:10.1104/pp.88.4.1418

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choat B et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755

    CAS  PubMed  Google Scholar 

  • Clearwater MJ, Meinzer FC, Andrade JL, Goldstein G, Holbrook NM (1999) Potential errors in measurement of nonuniform sap flow using heat dissipation probes. Tree Physiol 19:681–687. doi:10.1093/treephys/19.10.681

    Article  PubMed  Google Scholar 

  • Easterling DR, Evans JL, Groisman PY, Karl TR, Kunkel KE, Ambenje P (2000) Observed variability and trends in extreme climate events: a brief review. Bull Am Meteorol Soc 81:417–425

    Article  Google Scholar 

  • Ewers BE, Oren R, Sperry JS (2000) Influence of nutrient versus water supply on hydraulic architecture and water balance in Pinus taeda. Plant Cell Environ 23:1055–1066

    Article  Google Scholar 

  • Ewers BE, Gower ST, Bond-Lamberty B, Wang CK (2005) Effects of stand age and tree species on canopy transpiration and average stomatal conductance of boreal forests. Plant Cell Environ 28:660–678. doi:10.1111/j.1365-3040.2005.01312.x

    Article  Google Scholar 

  • Farquhar G, O’Leary M, Berry J (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137

    Article  CAS  Google Scholar 

  • Fisher R et al (2010) Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations. New Phytol 187:666–681

    Article  PubMed  Google Scholar 

  • Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyzer (GLA), Version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true- colour fisheye photographs, users manual and program documentation. Simon Fraser University, Burnaby

  • Galiano L, Martínez-Vilalta J, Lloret F (2011) Carbon reserves and canopy defoliation determine the recovery of Scots pine 4 yr after a drought episode. New Phytol 190:750–759

    Article  CAS  PubMed  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. doi:10.1093/treephys/tpr012

    Article  PubMed  Google Scholar 

  • Granier A, Loustau D (1994) Measring and modeling the transpiration of a maritime pine canopu from sap-flow data. Agric For Meteorol 71:61–81

    Article  Google Scholar 

  • Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh KA (2001) Cavitation fatigue. Embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol 125:779–786

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hartmann H, Ziegler W, Trumbore S (2013) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427. doi:10.1111/1365-2435.12046

    Article  Google Scholar 

  • Hogg EH et al (1997) A comparison of sap flow and eddy fluxes of water vapor from a boreal deciduous forest. J Geophys Res Atmos 102:28929–28937

    Article  CAS  Google Scholar 

  • Hölttä T, Mencuccini M, Nikinmaa E (2009) Linking phloem function to structure: analysis with a coupled xylem–phloem transport model. J Theor Biol 259:325–337. doi:10.1016/j.jtbi.2009.03.039

    Article  PubMed  Google Scholar 

  • Hu J, Moore DJP, Riveros-Iregui DA, Burns SP, Monson RK (2010) Modeling whole-tree carbon assimilation rate using observed transpiration rates and needle sugar carbon isotope ratios. New Phytol 185:1000–1015. doi:10.1111/j.1469-8137.2009.03154.x

    Article  CAS  PubMed  Google Scholar 

  • Huang C-Y, Anderegg WRL (2012) Large drought-induced aboveground live biomass losses in southern Rocky Mountain aspen forests. Glob Change Biol 18:1016–1027

    Article  Google Scholar 

  • IPCC (2007) Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva

  • Kane J, Kolb T (2010) Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164:601–609. doi:10.1007/s00442-010-1683-4

    Article  PubMed  Google Scholar 

  • Katul GG, Palmroth S, Oren RAM (2009) Leaf stomatal responses to vapour pressure deficit under current and CO2-enriched atmosphere explained by the economics of gas exchange. Plant Cell Environ 32:968–979

    Article  CAS  PubMed  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. doi:10.1016/j.tree.2011.06.003

    Article  PubMed  Google Scholar 

  • Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182. doi:10.1046/j.1365-3040.2003.00991.x

    Article  Google Scholar 

  • Michaelian M, Hogg EH, Hall RJ, Arsenault E (2011) Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Glob Change Biol 17:2084–2094. doi:10.1111/j.1365-2486.2010.02357.x

    Article  Google Scholar 

  • Nikinmaa E et al (2013) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant Cell Environ 36:655–669. doi:10.1111/pce.12004

    Article  CAS  PubMed  Google Scholar 

  • Oishi AC, Oren R, Stoy PC (2008) Estimating components of forest evapotranspiration: a footprint approach for scaling sap flux measurements. Agric For Meteorol 148:1719–1732

    Article  Google Scholar 

  • Oren R et al (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526

    Article  Google Scholar 

  • Pan Y et al (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993. doi:10.1126/science.1201609

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Perala DA (1990) Populus tremuloides Michx. Quaking aspen. In: Burns RM, Honkala BH (eds). Silvics of North America, vol 2: Hardwoods. USDA Forest Service Agricultural Handbook 654. US Forest Service, Washington, DC, pp 555–569

  • Phillips OL et al (2010) Drought-mortality relationships for tropical forests. New Phytol 187:631–646. doi:10.1111/j.1469-8137.2010.03359.x

    Article  PubMed  Google Scholar 

  • Plaut JA et al (2012) Hydraulic limits preceding mortality in a piñon–juniper woodland under experimental drought. Plant Cell Environ 35:1601–1617

    Article  PubMed  Google Scholar 

  • Richter A et al (2009) Preparation of starch and soluble sugars of plant material for the analysis of carbon isotope composition: a comparison of methods. Rapid Commun Mass Spectrom 23:2476–2488. doi:10.1002/rcm.4088

    Article  CAS  PubMed  Google Scholar 

  • Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol. doi: 10.1093/treephys/tpr143

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675

    Article  CAS  Google Scholar 

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia (Berlin) 155:441–454. doi:10.1007/s00442-007-0932-7

    Article  Google Scholar 

  • Sperry JS (2011) Hydraulics of vascular water transport mechanical integration of plant cells and plants, vol 9. In: Wojtaszek P (ed) Signalling and communication in plants: mechanical integration of plant cells and plants. Springer, Heidelberg, pp 303–327

  • Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ 11:35–40. doi:10.1111/j.1365-3040.1988.tb01774.x

    Article  Google Scholar 

  • Sperry JS, Adler FR, Campbell GS, Comstock JP (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ 21:347–359. doi:10.1046/j.1365-3040.1998.00287.x

    Article  Google Scholar 

  • van Mantgem PJ et al (2009) Widespread increase of tree mortality rates in the western United States. Science 323:521–524. doi:10.1126/science.1165000

    Article  PubMed  Google Scholar 

  • West AG, Hultine KR, Sperry JS, Bush SE, Ehleringer JR (2008) Transpiration and hydraulic strategies in a piñon-juniper woodland. Ecol Appl 18:911–927

    Article  CAS  PubMed  Google Scholar 

  • Worrall JJ et al (2008) Rapid mortality of Populus tremuloides in southwestern Colorado, USA. For Ecol Manag 255:686–696. doi:10.1016/j.foreco.2007.09.071

    Article  Google Scholar 

  • Worrall JJ, Marchetti SB, Egeland L, Mask RA, Eager T, Howell B (2010) Effects and etiology of sudden aspen decline in southwestern Colorado, USA. For Ecol Manag 260:638–648. doi::10.1016/j.foreco.2010.05.020

    Article  Google Scholar 

  • Wullschleger SD, Meinzer FC, Vertessy RA (1998) A review of whole-plant water use studies in tree. Tree Physiol 18:499–512. doi:10.1093/treephys/18.8-9.499

    Article  PubMed  Google Scholar 

  • Monteith JL, Unsworth M (1990) Principles of environmental physics. Butterworth-Heinemann, Woburn

    Google Scholar 

Download references

Acknowledgments

We thank K. Pham, G. Griffin, M. Anderegg, E. Callaway, C. Kucharczyk, L. Giles and M. Dini for assistance in field and laboratory work, and an anonymous reviewer for helpful comments. Funding for study: NSF DDIG Program. W.R.L.A. was supported in part by an award from the Department of Energy (DOE) Office of Science Graduate Fellowship Program (DOE SCGF) and a NOAA Climate and Global Change Postdoctoral Fellowship.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, 106A Guyot Hall, Princeton, NJ, 08544-2016, USA

    William R. L. Anderegg

  2. Department of Biology, University of Washington, Seattle, WA, USA

    Leander D. L. Anderegg

  3. Department of Global Ecology, Carnegie Institution for Science, Stanford, CA, 94305, USA

    Joseph A. Berry & Christopher B. Field

Authors
  1. William R. L. Anderegg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leander D. L. Anderegg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph A. Berry
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher B. Field
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to William R. L. Anderegg.

Additional information

Communicated by Ram Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 157 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anderegg, W.R.L., Anderegg, L.D.L., Berry, J.A. et al. Loss of whole-tree hydraulic conductance during severe drought and multi-year forest die-off. Oecologia 175, 11–23 (2014). https://doi.org/10.1007/s00442-013-2875-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2875-5

Keywords

Search

Navigation