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.
Similar content being viewed by others
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
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
Bartos DL, Campbell RB Jr (1998) Decline of quaking aspen in the Interior West—examples from Utah. Range 20:17–24
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659
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
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
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
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
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
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
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
Kosola KR, Dickmann DI, Parry D (2002) Carbohydrates in individual poplar fine roots: effects of root age and defoliation. Tree Physiol 22:741–746
Landhäusser SM (2011) Aspen shoots are carbon autonomous during bud break. Trees 25:531–536
Landhäusser SM, Lieffers VJ (1998) Growth of Populus tremuloides in association with Calamagrostis canadensis. Can J For Res 28:396–401
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
Landhäusser SM, Lieffers VJ (2003) Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones. Trees 17:471–476
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
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)
Li MH, Hoch G, Körner C (2002) Source/sink removal affects mobile carbohydrates in Pinus cembra at the Swiss treeline. Trees 16:331–337
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
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
Martens L, Landhäusser SM, Lieffers VJ (2007) First-year growth response of cold-stored, nursery-grown aspen planting stock. New For 33:281–295
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
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059
McDowell NG, Sevanto S (2010) The mechanisms of carbon starvation: how, when. Or does it even occur at all? New Phytol 186:264–266
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
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
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
Minchin PEH, Lacointe A (2005) New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. New Phytol 166:771–779
Minchin PEH, Thorpe MR (1993) Sink strength: a misnomer, and best forgotten. Plant Cell Environ 16:1039–1040
Newell EA, Mulkey SS, Wright SJ (2002) Seasonal patterns of carbohydrate storage in four tropical tree species. Oecologia 131:333–342
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)
Piispanen R, Saranpää P (2004) Seasonal and within-stem variations of neutral lipids in silver birch (Betula pendula) wood. Tree Physiol 24:991–999
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
Sala A, Hoch G (2009) Height-related growth declines in ponderosa pine are not due to carbon limitation. Plant Cell Environ 32:22–30
Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281
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
Sauter JJ, VanCleve B (1991) Biochemical, immunochemical, and ultrastructural studies of protein storage in poplar (Populus x canadensis robusta) wood. Planta 183:92–100
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
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
Sperry JS, Hacke UG, Oren R, Comstock JP (2002) Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ 25:251–263
Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Ann Rev Ecol Syst 22:309–334
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
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
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
Thompson MV (2006) Phloem: the long and the short of it. Trends Plant Sci 11:26–32
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
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Ann Rev Plant Physiol Molec Biol 40:19–36
van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant Cell Environ 26:125–149
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
Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381
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
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
Wright CJ (1989) Interactions between vegetative and reproductive growth. In: Wright CJ (ed) Manipulation of Fruiting. Butterworths, London
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Carlson.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-011-0633-z