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Defoliation increases risk of carbon starvation in root systems of mature aspen

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Abstract

Large trees are noted to decline and die over several years after defoliation or extended periods of drought. The underlying mechanisms of this decline are thought to be driven by moisture limitations to photosynthesis, but alternative considerations also suggest carbon storage limitations as a driver. This research assesses the non-structural carbohydrate reserves in crowns and roots tissues during and after defoliation by insects in trembling aspen. We monitored the non-structural carbon reserves of nine tall mature aspen forest stands over 8 years, including two defoliation events. We report on the carbohydrate dynamics in root and crown tissues during and after defoliation. Following defoliation, branch reserves recovered to levels of undefoliated control trees within the same season, while roots took up to 2 years to recover. We argue that in large trees, tissues closest to the foliage are the first sinks to access C in the phloem stream, while roots, which are more distal and separated by a long bole, will only receive adequate supplies of C when the other more proximate sinks are sated. These results support the hypothesis that in times of limited carbon assimilation, root tissues in mature trees experience the longest reduction in carbon reserves, which likely plays a critical role in tree decline and mortality.

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References

  • 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: implications for regional die-off under global-change-type drought. Proc Nat Acad Sci 106:7063–7066

    Article  PubMed  CAS  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 JH, 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 Manage 259:660–684

    Article  Google Scholar 

  • Bartos DL, Campbell RB Jr (1998) Decline of quaking aspen in the Interior West—examples from Utah. Range 20:17–24

    Google Scholar 

  • Battaglia M, Cherry ML, Deadle CL, Sands PJ, Hingston A (1998) Prediction of leaf area index in eucalypt plantations: effect of water stress and temperature. Tree Physiol 18:521–528

    PubMed  Google Scholar 

  • Batzer HO, Hodson AC, Schneider AE (1954) Preliminary results of an inquiry into effects of defoliation of aspen trees by the forest tent caterpillar. School of Forestry, University of Minnesota, St. Paul Forestry Notes 31

    Google Scholar 

  • Bigler C, Gavin DG, Gunning C, Veblen TT (2007) Drought induces lagged tree mortality in a subalpine forest in the Rocky Mountains. Oikos 116:1983–1994

    Article  Google Scholar 

  • Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644

    Article  Google Scholar 

  • Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J (2010) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc Nat Acad Sci. http://www.pnas.org/cgi/doi/10.1073/pnas.1010070108

  • Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Ann Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • Chow PS, Landhäusser SM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24:1129–1136

    Article  PubMed  CAS  Google Scholar 

  • Dang Q-L, Margolis HA, Coyea M, Sy M, Collatz GJ (1997) Regulation of branch-level gas exchange of boreal treess: roles of shoot water potential and vapor pressure difference. Tree Physiol 17:521–535

    PubMed  CAS  Google Scholar 

  • De Schepper V, Steppe K (2010) Development and verification of a water and sugar transport model using measured stem diameter variations. J Exp Bot 61:2083–2099

    Article  PubMed  Google Scholar 

  • Di Orio AP, Callas R, Schaefer RJ (2005) Forty-eight year decline and fragmentation of aspen (Populus tremuloides) in the South Warner Mountains of California. For Ecol Manage 206:307–313

    Article  Google Scholar 

  • Dickmann DI, Nguyen PV, Pregitzer KS (1996) Effects of irrigation and coppicing on above-ground growth, physiology, and fine-root dynamics of two field-grown hybrid poplar clones. For Ecol Manage 80:163–174

    Article  Google Scholar 

  • Environment Canada (2010) www.climate.weatheroffice.gc.ca/climateData (Accessed 20 March 2010)

  • Frey BR, Lieffers VJ, Hogg EH, Landhäusser SM (2004) Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps. Can J For Res 34:1379–1390

    Article  Google Scholar 

  • Galiano L, Martinez-Villalta 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  PubMed  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  PubMed  Google Scholar 

  • Goodsman DW, Lieffers VJ, Landhäusser SM, Erbilgin N (2010) Fertilization of lodgepole pine trees increased diameter growth but reduced root carbohydrate concentrations. For Ecol Manage 260:1914–1920

    Article  Google Scholar 

  • Hildahl V, Reeks WA (1960) Outbreaks of the forest tent caterpillar, Malacosoma disstria Hbn., and their effects on stands of trembling aspen in Manitoba and Saskatchewan. Can Entomol 92:199–209

    Article  Google Scholar 

  • Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659

    Article  CAS  Google Scholar 

  • Hogg EH (1999) Simulation of interannual responses of trembling aspen stands to climatic variation and insect defoliation in western Canada. Ecol Model 114:175–193

    Article  CAS  Google Scholar 

  • Hogg EH, Saugier B, Pontailler J-Y, Black TA, Chen W, Hurdle PA, Wu A (2000) Response of trembling aspen and hazelnut to vapor pressure deficit in a boreal deciduous forest. Tree Physiol 20:725–734

    PubMed  Google Scholar 

  • Hogg EH, Brandt JP, Kochtubajda B (2002) Growth and dieback of Aspen forests in northwestern Alberta, Canada, in relation to climate and insects. Can J For Res 32:823–832

    Article  Google Scholar 

  • Hogg EH, Brandt JP, Michaelin M (2008) Impacts of a regional drought on the productivity, dieback, and biomass of Canadian aspen forests. Can J For Res 38:1373–1384

    Article  Google Scholar 

  • Hölttä T, Vesala T, Sevanto S, Perämäki M, Nikinmaa E (2006) Modeling xylem and phloem water flows in trees according to cohesion theory and Münch hypothesis. Trees 20:67–78

    Article  Google Scholar 

  • Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Peláez-Riedl S, Pepin S, Siegwolf RTW, Zotzl G (2005) Carbon flux and growth in mature deciduous forest trees exposed to elevated CO2. Science 309:1360–1362

    Article  PubMed  Google Scholar 

  • Kosola KR, Dickmann DI, Paul EA, Parry D (2001) Repeated insect defoliation effects on growth, nitrogen acquisition, carbohydrates, and root demography of poplars. Oecolologia 129:65–74

    Article  Google Scholar 

  • Kosola KR, Dickmann DI, Parry D (2002) Carbohydrates in individual poplar fine roots: effects of root age and defoliation. Tree Physiol 22:741–746

    Article  PubMed  CAS  Google Scholar 

  • Landhäusser SM (2011) Aspen shoots are carbon autonomous during bud break. Trees 25:531–536

    Article  Google Scholar 

  • Landhäusser SM, Lieffers VJ (1998) Growth of Populus tremuloides in association with Calamagrostis canadensis. Can J For Res 28:396–401

    Article  Google Scholar 

  • Landhäusser SM, Lieffers VJ (2002) Leaf area renewal, root retention and carbohydrate reserves in a clonal tree species following aboveground disturbance. J Ecol 90:658–665

    Article  Google Scholar 

  • Landhäusser SM, Lieffers VJ (2003) Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones. Trees 17:471–476

    Google Scholar 

  • Le Dantec V, Dufrêne E, Saugier B (2000) Interannual and spatial variation in maximum leaf area index of temperate deciduous stands. For Ecol Manage 134:71–81

    Article  Google Scholar 

  • Leuzinger S, Bigler C, Wolf A, Körner C (2009) Poor methodology for predicting large-scale tree die-off. Proc Natl Acad Sci USA 106:E106 (author reply E107)

    Article  PubMed  CAS  Google Scholar 

  • Li MH, Hoch G, Körner C (2002) Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees 16:331–337

    Article  CAS  Google Scholar 

  • Ludovici KH, Allen HL, Albaugh TJ, Dougherty PM (2002) The influence of nutrient and water availability on carbohydrate storage in loblolly pine. For Ecol Manage 159:261–270

    Article  Google Scholar 

  • Man R, Kayahara GJ, Rice JA, MacDonald GB (2008) Response of trembling aspen to partial cutting and subsequent forest tent caterpillar defoliation in a boreal mixedwood stand in northeastern Ontario, Canada. Can J For Res 38:1349–1356

    Article  Google Scholar 

  • Martens L, Landhäusser SM, Lieffers VJ (2007) First-year growth response of cold-stored, nursery-grown aspen planting stock. New For 33:281–295

    Article  Google Scholar 

  • Martinez-Vilalta J, Pinol J, Beven K (2002) A hydraulic model to predict drought-induced mortality in woody plants: an application to climate change in the Mediterranean. Ecol Model 155:127–147

    Article  Google Scholar 

  • McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059

    Article  PubMed  CAS  Google Scholar 

  • McDowell NG, Sevanto S (2010) The mechanisms of carbon starvation: how, when. Or does it even occur at all? New Phytol 186:264–266

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Meier IC, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Glob Change Biol 14:2081–2095

    Article  Google Scholar 

  • Michaelia M, Hogg EH, Hall RJ, Aersenault E (2010) Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Glob Change Biol. doi: 10.1111/j.1365-2486.2010.02357.x

  • Minchin PEH (2007) Mechanistic modelling of carbon partitioning. In: Vos J, Marcelis LFM, de Visser PHB, Struik PC, Evers JB (eds) Functional-structural plant modelling in crop production. Springer, The Netherlands, pp 113–122

    Chapter  Google Scholar 

  • Minchin PEH, Lacointe A (2005) New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytol 166:771–779

    Article  PubMed  CAS  Google Scholar 

  • Minchin PEH, Thorpe MR (1993) Sink strength: a misnomer, and best forgotten. Plant Cell Environ 16:1039–1040

    Article  Google Scholar 

  • Newell EA, Mulkey SS, Wright SJ (2002) Seasonal patterns of carbohydrate storage in four tropical tree species. Oecologia 131:333–342

    Article  Google Scholar 

  • Perala DA (1990) Populus tremuloides Michx.: quaking aspen. In: Burns RM, Honkala BH (eds) Silvics of North America, Vol. 2 Hardwoods Agriculture handbook. 654, United States Department of Agriculture, pp 555–569

  • Peterson EB, Peterson NM (1992) Ecology, management, and use of aspen and balsam poplar in the Prairie Provinces, Canada. Forestry Canada, Northern Forestry Centre, Edmonton (Special report 1)

    Google Scholar 

  • Piispanen R, Saranpää P (2004) Seasonal and within-stem variations of neutral lipids in silver birch (Betula pendula) wood. Tree Physiol 24:991–999

    Article  PubMed  CAS  Google Scholar 

  • Pruyn ML, Gartner BL, Harmon ME (2005) Storage versus substrate limitation to bole respiratory potential in two coniferous tree species of contrasting sapwood width. J Exp Bot 56:2637–2649

    Article  PubMed  CAS  Google Scholar 

  • Sala A, Hoch G (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ 32:22–30

    Article  PubMed  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  PubMed  Google Scholar 

  • Sanz-Pérez V, Castro-Diez P, Joffre R (2009) Seasonal carbon storage and growth in Mediterranean tree seedlings under different water conditions. Tree Physiol 29:1105–1116

    Article  PubMed  Google Scholar 

  • Sauter JJ, VanCleve B (1991) Biochemical, immunochemical, and ultrastructural studies of protein storage in poplar (Populus x canadensis robusta) wood. Planta 183:92–100

    Article  CAS  Google Scholar 

  • Sauter JJ, VanCleve B (1994) Storage, mobilization and interrelations of starch sugars, proteins and fat in the ray storage tissue of poplar. Trees 8:297–304

    Article  Google Scholar 

  • Schädel C, Blöchl A, Richter A (2009) Short-term dynamics of nonstructural carbohydrates and hemicelluloses in young branches of temperate forest trees during bud break. Tree Physiol 29:901–911

    Article  PubMed  Google Scholar 

  • Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263

    Article  PubMed  Google Scholar 

  • Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Ann Rev Ecol Syst 22:309–334

    Article  Google Scholar 

  • Strand EK, Vierling LA, Bunting SC, Gessler PE (2009) Quantifying successional rates in western aspen woodlands: current conditions, future predictions. For Ecol Manage 257:1705–1715

    Article  Google Scholar 

  • Tardieu F (1993) Will increases in our understanding of soil-root relations and root signalling substantially alter water flux models? Phil Trans Royal Soc Biol Sci 341:57–66

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Thompson MV (2006) Phloem: the long and the short of it. Trends Plant Sci 11:26–32

    Article  PubMed  CAS  Google Scholar 

  • Tyree MT, Sperry JS (1988) Do woody-plants operate near the point of catastrophic xylem dysfunction caused by dynamic water-stress? Answers 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. Ann Rev Plant Physiol Molec Biol 40:19–36

    Article  Google Scholar 

  • van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149

    Article  Google Scholar 

  • Wan X, Zwiazek JJ, Lieffers VJ, Landhäusser SM (2001) Hydraulic conductance in aspen (Populus tremuloides) seedlings exposed to low root temperatures. Tree Physiol 21:691–696

    Article  PubMed  CAS  Google Scholar 

  • Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381

    Article  CAS  Google Scholar 

  • Worrall JJ, Egeland L, Eager T, Mask RA, Johnson EW, Kemp PA, Shepperd WD (2008) Rapid mortality of Populus tremuloides in southwestern Colorado, USA. For Ecol Manage 255:686–696

    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 Manage 260:638–648

    Article  Google Scholar 

  • Wright CJ (1989) Interactions between vegetative and reproductive growth. In: Wright CJ (ed) Manipulation of Fruiting. Butterworths, London

    Google Scholar 

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Acknowledgments

The authors thank Pak Chow for his assistance in the carbohydrate analyses and Devin Goodsman, Amanda Schoonmaker and David Galvez for the discussion of these ideas. This study has been supported by the Natural Sciences and Engineering Research Council of Canada (NSERC).

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Correspondence to Simon M. Landhäusser.

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Communicated by J. Carlson.

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Landhäusser, S.M., Lieffers, V.J. Defoliation increases risk of carbon starvation in root systems of mature aspen. Trees 26, 653–661 (2012). https://doi.org/10.1007/s00468-011-0633-z

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