Skip to main content
SpringerLink
Log in

Do Carbon Reserves Increase Tree Survival during Stress and Following Disturbance?

  • Climate Change and Carbon Sequestration (L Pinkard, Section Editor)
  • Published:
Current Forestry Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Carbon (C) storage provides trees with a pool of C that can be remobilized and used to sustain vital physiological processes when photosynthesis and/or C transport cannot meet a plant’s current demands. As such, it may be an important determinant of tree survival in many cases. However, we do not yet know how often tree mortality occurs as the result of carbon limitation, and therefore it remains unclear whether C storage is important for preventing tree death. The purpose of this review is therefore to summarize and assess recent research regarding the role of C storage in tree survival under different stressors and disturbances.

Recent Findings

Both recent and older work have identified many potential mechanisms by which C storage may influence tree survival, and there is evidence that higher tissue non-structural carbohydrate concentrations or total content can be associated with survival and recovery following defoliation and aboveground tissue destruction and under deep shade, drought, flooding, biotic attack, and freezing temperatures. However, in most cases, there is also evidence suggesting that C storage does not always or even often influence survival. Both drought and flooding may lead to inhibition of C transport, particularly to the roots, suggesting that increased root storage specifically might play a critical role in survival; however, this remains to be tested. In some cases, the ability to maintain C assimilation and transport might be more critical than increasing storage.

Summary

Though C storage can affect survival, we are far from knowing how common or uncommon this pattern is. Future work exploring the relationship between survival and storage needs to focus on measuring C storage in all organs and tissues, considering the importance of total storage content, not just concentrations, identifying the relevant compounds in different species that constitute the actual storage pool, and carefully separating out the effects of storage from other factors that also tend to change when storage concentrations are altered.

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

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. • Adams HD, Zeppel MJB, Anderegg WRL, et al. A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol. 2017;1:1285–91 This study provides a meta-analysis of the physiological mechanisms involved in drought mortality studies across taxa. Evidence of hydraulic failure was ubiquitous while starvation—supported by reduced NSC concentrations was not. Reduced NSC at death was most common in root tissues, suggestive of phloem failure during drought.

    Google Scholar 

  2. Aguadé D, Poyatos R, Gómez M, Oliva J, Martínez-Vilalta J. The role of defoliation and root rot pathogen infection in driving the mode of drought-related physiological decline in Scots pine (Pinus sylvestris L.). Tree Physiol. 2015;35:229–242.

    CAS  Google Scholar 

  3. Améglio T, Decourteix M, Alves G, Valentin V, Sakr S, Julien J-L, et al. Temperature effects on xylem sap osmolarity in walnut trees: evidence for a vitalistic model of winter embolism repair. Tree Physiol. 2004;24:785–93.

    Google Scholar 

  4. Anderegg WRL, Berry JA, Smith DD, Sperry JS, Anderegg LDL, Field CB. The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off. PNAS. 2012;109:233–7.

    CAS  Google Scholar 

  5. Anderegg WRL, Callaway ES. Infestation and hydraulic consequences of induced carbon starvation1. Plant Physiol. 2012;159:1866–74.

    CAS  Google Scholar 

  6. Angelov MN, Sung S-JS, Doong RL, Harms WR, Kormanik PP, Black CC. Long- and short-term flooding effects on survival and sink–source relationships of swamp-adapted tree species. Tree Physiol. 1996;16:477–84.

    CAS  Google Scholar 

  7. • Baerdemaeker NJFD, Salomón RL, Roo LD, Steppe K. Sugars from woody tissue photosynthesis reduce xylem vulnerability to cavitation. New Phytol. 2017;216:720–7 The authors found that limiting branch photosynthesis increased their vulnerability to cavitation. Because the contribution of new vessels to hydraulic conductivity was considered minor, anatomical explanations for increased vulnerability were ruled out and the effect of reduced sugar supply for production of xylem surfactants was hypothesized.

    Google Scholar 

  8. Baier P. Defence reactions of Norway spruce (Picea abies karst.) to controlled attacks of Ips typographus (L.) (Col., Scolytidae) in relation to tree parameters. J Applied Entomol. 1996;120:587–93.

    Google Scholar 

  9. Blackman CJ, Creek D, Maier C, Aspinwall MJ, Drake JE, Pfautsch S, et al. Drought response strategies and hydraulic traits contribute to mechanistic understanding of plant dry-down to hydraulic failure. Tree Physiol. 2019;39:910–24.

    Google Scholar 

  10. Bréda N, Huc R, Granier A, Dreyer E. Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci. 2006;63:625–44.

    Google Scholar 

  11. Brodribb TJ, Bowman DJMS, Nichols S, Delzon S, Burlett R. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytol. 2010;188:533–42.

    Google Scholar 

  12. Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDSL. Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ. 2003;26:1633–45.

    Google Scholar 

  13. Canham CD, Kobe RK, Latty EF, Chazdon RL. Interspecific and intraspecific variation in tree seedling survival: effects of allocation to roots versus carbohydrate reserves. Oecologia. 1999;121:1–11.

    Google Scholar 

  14. Carpenter LT, Pezeshki SR, Shields FD. Responses of nonstructural carbohydrates to shoot removal and soil moisture treatments in Salix nigra. Trees. 2008;22:737–48.

    CAS  Google Scholar 

  15. Chapin FS, Schulze E, Mooney HA. The ecology and economics of storage in plants. Annu Rev Ecol Syst. 1990;21:423–447.

    Google Scholar 

  16. Charrier G, Cochard H, Améglio T. Evaluation of the impact of frost resistances on potential altitudinal limit of trees. Tree Physiol. 2013;33:891–902.

    Google Scholar 

  17. Chen Z, Wang L, Dai Y, Wan X, Liu S. Phenology-dependent variation in the non-structural carbohydrates of broadleaf evergreen species plays an important role in determining tolerance to defoliation (or herbivory). Sci Rep. 2017;7:10125.

    Google Scholar 

  18. Christiansen E, Ericsson A. Starch reserves in Picea abies in relation to defence reaction against a bark beetle transmitted blue-stain fungus, Ceratocystis polonica. Can J For Res. 1986;16:78–83.

    Google Scholar 

  19. Clarke PJ, Lawes MJ, Midgley JJ, Lamont BB, Ojeda F, Burrows GE, et al. Resprouting as a key functional trait: how buds, protection and resources drive persistence after fire. New Phytol. 2013;197:19–35.

    CAS  Google Scholar 

  20. Cochard H, Lemoine D, Améglio T, Granier A. Mechanisms of xylem recovery from winter embolism in Fagus sylvatica. Tree Physiol. 2001;21:27–33.

    CAS  Google Scholar 

  21. Cox SE, Stushnoff C. Temperature-related shifts in soluble carbohydrate content during dormancy and cold acclimation in Populus tremuloides. Can J For Res. 2001;31:730–7.

    CAS  Google Scholar 

  22. Cruz A, Pérez B, Moreno JM. Plant stored reserves do not drive resprouting of the lignotuberous shrub Erica australis. New Phytol. 2003;157:251–61.

    Google Scholar 

  23. Dai Y, Wang L, Wan X. Relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality caused by drought. AoB Plants. 2018;10: plx069.

  24. Delgado M, Zúñiga-Feest A, Piper FI. Does carbon storage confer waterlogging tolerance? Evidence from four evergreen species of a temperate rainforest. Aust J Bot. 2018;66:74–84.

    Google Scholar 

  25. Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R. Nonstructural carbon in woody plants. Annu Rev Plant Biol. 2014;65:667–687.

    CAS  Google Scholar 

  26. • Dickman LT, Mcdowell NG, Sevanto S, Pangle RE, Pockman WT. Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios. Plant, Cell Environ. 2015;38:729–39 One of the first drought studies on mature trees in a field setting that demonstrates a reduction in NSC, and that this reduction is predictive of survival time in two species with contrasting strategies of stomatal regulation.

    CAS  Google Scholar 

  27. Dietrich L, Hoch G, Kahmen A, Körner C. Losing half the conductive area hardly impacts the water status of mature trees. Sci Rep. 2018;8:1–9.

    CAS  Google Scholar 

  28. Ding X, Luo J, Li Y, Ren B, Bian H, Yao X, et al. Survival of completely submerged Salix triandroides cuttings is associated with non-structural carbohydrate metabolism. J Freshw Ecol. 2019;34:395–404.

    CAS  Google Scholar 

  29. Duan H, Chaszar B, Lewis JD, Smith RA, Huxman TE, Tissue DT. CO2 and temperature effects on morphological and physiological traits affecting risk of drought-induced mortality. Tree Physiol. 2018;38:1138–51.

    CAS  Google Scholar 

  30. Dunn JP, Kimmerer TW, Potter DA. Winter starch reserves of white oak as a predictor of attack by the twolined chestnut borer, Agrilus bilineatus (weber) (Coleoptera: Buprestidae). Oecologia. 1987;74:352–5.

    CAS  Google Scholar 

  31. Eyles A, Bonello P, Ganley R, Mohammed C. Induced resistance to pests and pathogens in trees. New Phytol. 2010;185:893–908.

    Google Scholar 

  32. Ferner E, Rennenberg H, Kreuzwieser J. Effect of flooding on C metabolism of flood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species. Tree Physiol. 2012;32:135–45.

    CAS  Google Scholar 

  33. Ferreira SC, Piedade MT, Tiné MA, Rossatto DR, Parolin P, Buckeridge MS. The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions. Ann Bot. 2009;104:1111–9.

    CAS  Google Scholar 

  34. Galiano L, Martínez-Vilalta J, Lloret F. Carbon reserves and canopy defoliation determine the recovery of scots pine 4 yr after a drought episode. New Phytol. 2011;190:750–9.

    CAS  Google Scholar 

  35. Galiano L, Martínez-Vilalta J, Sabaté S, Lloret F. Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean holm oak forest. Tree Physiol. 2012;32:478–89.

    Google Scholar 

  36. Garcia-Forner N, Biel C, Savé R, Martínez-Vilalta J. Isohydric species are not necessarily more carbon limited than anisohydric species during drought. Tree Physiol. 2017;37:441–55.

    CAS  Google Scholar 

  37. Garcia-Forner N, Sala A, Biel C, Savé R, Martínez-Vilalta J. Individual traits as determinants of time to death under extreme drought in Pinus sylvestris L. Tree Physiol. 2016;36:1196–209.

    CAS  Google Scholar 

  38. Gaucher C, Gougeon S, Mauffette Y, Messier C. Seasonal variation in biomass and carbohydrate partitioning of understory sugar maple (Acer saccharum) and yellow birch (Betula alleghaniensis) seedlings. Tree Physiol. 2005;25:93–100.

    Google Scholar 

  39. Gaylord ML, Kolb TE, Pockman WT, Plaut JA, Yepez EA, Macalady AK, et al. Drought predisposes piñon–juniper woodlands to insect attacks and mortality. New Phytol. 2013;198:567–78.

    CAS  Google Scholar 

  40. Gleason SM, Ares A. Photosynthesis, carbohydrate storage and survival of a native and an introduced tree species in relation to light and defoliation. Tree Physiol. 2004;24:1087–97.

    CAS  Google Scholar 

  41. Goodsman DW, Lusebrink I, Landhäusser SM, Erbilgin N, Lieffers VJ. Variation in carbon availability, defense chemistry and susceptibility to fungal invasion along the stems of mature trees. New Phytol. 2013;197:586–94.

    CAS  Google Scholar 

  42. Gravatt DA, Kirby CJ. Patterns of photosynthesis and starch allocation in seedlings of four bottomland hardwood tree species subjected to flooding. Tree Physiol. 1998;18:411–7.

    Google Scholar 

  43. Guérard N, Maillard P, Bréchet C, Lieutier F, Dreyer E. Do trees use reserve or newly assimilated carbon for their defense reactions? A 13C labeling approach with young scots pines inoculated with a bark-beetle-associated fungus (Ophiostoma brunneo ciliatum). Ann For Sci. 2007;64:601–8.

    Google Scholar 

  44. Guy CL. Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol. 1990;41:187–223.

    CAS  Google Scholar 

  45. Hacke U, Sauter JJ. Xylem dysfunction during winter and recovery of hydraulic conductivity in diffuse-porous and ring-porous trees. Oecologia. 1996;105:435–9.

    CAS  Google Scholar 

  46. Hartmann H, Adams HD, Hammond WM, Hoch G, Landhäusser SM, Wiley E, et al. Identifying differences in carbohydrate dynamics of seedlings and mature trees to improve carbon allocation in models for trees and forests. Environ Exp Bot. 2018;152:7–18.

    CAS  Google Scholar 

  47. Hartmann H, Ziegler W, Kolle O, Trumbore S. Thirst beats hunger - declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol. 2013;200:340–9.

    CAS  Google Scholar 

  48. Hartmann H, Ziegler W, Trumbore S. Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol. 2013;27:413–27.

    Google Scholar 

  49. Herschbach C, Mult S, Kreuzwieser J, Kopriva S. Influence of anoxia on whole plant sulphur nutrition of flooding-tolerant poplar (Populus tremula × P. alba). Plant Cell Environ. 2005;28:167–75.

    CAS  Google Scholar 

  50. Hoch G, Richter A, Körner C. Non-structural carbon compounds in temperate forest trees. Plant Cell Environ. 2003;26:1067–81.

    CAS  Google Scholar 

  51. Hoch G, Körner C. The carbon charging of pines at the climatic treeline: a global comparison. Oecologia. 2003;135:10–21.

    Google Scholar 

  52. Hoekstra FA, Golovina EA, Buitink J. Mechanisms of plant desiccation tolerance. Trends Plant Sci. 2001;6:431–438.

    CAS  Google Scholar 

  53. Hood SM, Smith SL, Cluck DR. Predicting mortality for five California conifers following wildfire. Forest Ecol Manage. 2010;260:750-762 260:750–762.

    Google Scholar 

  54. Horntvedt R. Resistance of Picea Abies to Ips Typographus: tree response to monthly inoculations with Ophiostoma polonicum, a beetle transmitted blue-stain fungus. Scand J For Res. 1988;3:107–14.

    Google Scholar 

  55. Jaeger C, Gessler A, Biller S, Rennenberg H, Kreuzwieser J. Differences in C metabolism of ash species and provenances as a consequence of root oxygen deprivation by waterlogging. J Exp Bot. 2009;60:4335–45.

    CAS  Google Scholar 

  56. Kabeya D, Sakai S. The relative importance of carbohydrate and nitrogen for the resprouting ability of Quercus crispula seedlings. Ann Bot. 2005;96:479–88.

    CAS  Google Scholar 

  57. Kasuga J, Arakawa K, Fujikawa S. High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytol. 2007;174:569–79.

    CAS  Google Scholar 

  58. Kasuga J, Hashidoko Y, Nishioka A, Yoshiba M, Arakawa K, Fujikawa S. Deep supercooling xylem parenchyma cells of katsura tree (Cercidiphyllum japonicum) contain flavonol glycosides exhibiting high anti-ice nucleation activity. Plant Cell Environ. 2008;31:1335–48.

    CAS  Google Scholar 

  59. Kays JS, Canham CD. Effects of time and frequency of cutting on hardwood root reserves and sprout growth. For Sci. 1991;37:524–539.

  60. Kitajima K. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia. 1994;98:419–28.

    Google Scholar 

  61. Knox KJE, Clarke PJ. Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs. Funct Ecol. 2005;19:690–698.

    Google Scholar 

  62. Kobe RK. Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos. 1997;80:226–33.

    Google Scholar 

  63. • Kogawara S, Yamanoshita T, Norisada M, Kojima K. Steady sucrose degradation is a prerequisite for tolerance to root hypoxia. Tree Physiol. 2014;34:229–40 The authors experimentally manipulated root sugar content via exogenous glucose application to seedlings experiencing root hypoxia. They demonstrated that reduced ATP production in tree roots under hypoxia is caused by an insufficient supply of glucose, but suggest that hypoxia may also limit invertase activity and the breakdown of sucrose to support metabolism.

    CAS  Google Scholar 

  64. Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, et al. Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol. 2009;149:461–73.

    CAS  Google Scholar 

  65. • Kreuzwieser J, Rennenberg H. Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ. 2014;37:2245–59 A good review of the effects of flooding/waterlogging on tree physiology, which identifies carbohydrate supply for root metabolism as a key feature of flooding tolerance.

    CAS  Google Scholar 

  66. Lacointe A, Deleens E, Ameglio T, Saint-Joanis B, Lelarge C, Vandame M, et al. Testing the branch autonomy theory: a 13C/14C double-labelling experiment on differentially shaded branches. Plant Cell Environ. 2004;27:1159–68.

    CAS  Google Scholar 

  67. Lahr EC, Krokene P. Conifer stored resources and resistance to a fungus associated with the spruce bark beetle Ips typographus. PLoS One. 2013. https://doi.org/10.1371/journal.pone.0072405.

    CAS  Google Scholar 

  68. •• Landhäusser SM, Chow PS, Dickman LT, et al. Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates. Tree Physiol. 2018;38:1764–78 Demonstrates that three commonly used procedures for measuring NSC can produce very similar results that are in agreement with known sample NSC content. Very detailed, protocols for extractions and sugar and starch determination are included in the appendix.

    Google Scholar 

  69. Landhäusser SM, Lieffers VJ. Leaf area renewal, root retention and carbohydrate reserves in a clonal tree species following above-ground disturbance. J Ecol. 2002;90:658–65.

    Google Scholar 

  70. Lee JH, Yu DJ, Kim SJ, Choi D, Lee HJ. Intraspecies differences in cold hardiness, carbohydrate content and β-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiol. 2012;32:1533–40.

    CAS  Google Scholar 

  71. Li N, He N, Yu G, Wang Q, Sun J. Leaf non-structural carbohydrates regulated by plant functional groups and climate: evidences from a tropical to cold-temperate forest transect. Ecol Indic. 2016;62:22–31.

    Google Scholar 

  72. Liu J-F, Deng Y-P, Wang X-F, Ni Y-Y, Wang Q, Xiao W-F, et al. The concentration of non-structural carbohydrates, N, and P in Quercus variabilis does not decline toward its northernmost distribution range along a 1500 km transect in China. Front Plant Sci. 2018. https://doi.org/10.3389/fpls.2018.01444.

  73. Liu Z, Cheng R, Xiao W, Guo Q, Wang N. Effect of off-season flooding on growth, photosynthesis, carbohydrate partitioning, and nutrient uptake in Distylium chinense. PLoS One. 2014;9:e107636.

    Google Scholar 

  74. Luostarinen K, Kauppi A. Effects of coppicing on the root and stump carbohydrate dynamics in birches. New Forest. 2005;29:289–303.

    Google Scholar 

  75. Lusk CH, Piper FI. Seedling size influences relationships of shade tolerance with carbohydrate-storage patterns in a temperate rainforest. Funct Ecol. 2007;21:78–86.

    Google Scholar 

  76. Maguire AJ, Kobe RK. Drought and shade deplete nonstructural carbohydrate reserves in seedlings of five temperate tree species. Ecol Evol. 2015;5:5711–21.

    Google Scholar 

  77. Maringer J, Ascoli D, Küffer N, Schmidtlein S, Conedera M. What drives European beech (Fagus sylvatica L.) mortality after forest fires of varying severity? For Ecol Manag. 2016;368:81–93.

    Google Scholar 

  78. Martínez-Alcántara B, Jover S, Quiñones A, Forner-Giner MÁ, Rodríguez-Gamir J, Legaz F, et al. Flooding affects uptake and distribution of carbon and nitrogen in citrus seedlings. J Plant Physiol. 2012;169:1150–7.

    Google Scholar 

  79. • Martínez-Vilalta J, Sala A, Asensio D, Galiano L, Hoch G, Palacio S, et al. Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecological Monographs. 2016;86:495–516 This paper provides a meta-analysis of seasonal dynamics of perennial plants across functional types and biomes. Seasonal starch depletion was found to be common in cold-seasonal environments but sugar depletion did not occur; the authors argue this is indicative of the non-storage functions of sugars that are necessary for survival.

    Google Scholar 

  80. McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, et al. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol. 2008;178:719–39.

    Google Scholar 

  81. McDowell NG. Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol. 2011;155:1051–9.

    CAS  Google Scholar 

  82. Millard P, Sommerkorn M, Grelet G-A. Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol. 2007;175:11–28.

    CAS  Google Scholar 

  83. Mitchell PJ, O’Grady AP, Tissue DT, White DA, Ottenschlaeger ML, Pinkard EA. Drought response strategies define the relative contributions of hydraulic dysfunction and carbohydrate depletion during tree mortality. New Phytol. 2013;197:862–72.

    CAS  Google Scholar 

  84. Moing A (2000) Sugar alcohols as carbohydrate reserves in some higher plants. In: Gupta AK, Kaur N (eds) Developments in Crop Science. Elsevier, Amsterdam pp 337–358.

    Google Scholar 

  85. Moreira B, Tormo J, Pausas JG. To resprout or not to resprout: factors driving intraspecific variability in resprouting. Oikos. 2012;121:1577–84.

    Google Scholar 

  86. Morin X, Améglio T, Ahas R, Kurz-Besson C, Lanta V, Lebourgeois F, et al. Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol. 2007;27:817–25.

    CAS  Google Scholar 

  87. Myers JA, Kitajima K. Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J Ecol. 2007;95:383–95.

    CAS  Google Scholar 

  88. Nagy NE, Franceschi VR, Solheim H, Krekling T, Christiansen E. Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Am J Bot. 2000;87:302–13.

    CAS  Google Scholar 

  89. •• O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A. Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nature Climate Change. 2014;4:710–4 This paper provides the strongest evidence that NSC concentrations can affect drought survival, to date. Pre-drought NSC concentrations were correlated with differences in survival time under drought both between species and as the result of experimental manipulation of NSC, which did not change plant size.

    Google Scholar 

  90. Ogren E. Relationship between temperature, respiratory loss of sugar and premature dehardening in dormant scots pine seedlings. Tree Physiol. 1997;17:47–51.

    CAS  Google Scholar 

  91. Oliva J, Stenlid J, Martínez-Vilalta J. The effect of fungal pathogens on the water and carbon economy of trees: implications for drought-induced mortality. New Phytol. 2014;203:1028–35.

    CAS  Google Scholar 

  92. Palacio S, Maestro M, Montserrat-Martí G. Relationship between shoot-rooting and root-sprouting abilities and the carbohydrate and nitrogen reserves of Mediterranean dwarf shrubs. Ann Bot. 2007;100:865–74.

    CAS  Google Scholar 

  93. Palonen P, Buszard D, Donnelly D. Changes in carbohydrates and freezing tolerance during cold acclimation of red raspberry cultivars grown in vitro and in vivo. Physiol Plant. 2000;110:393–401.

    CAS  Google Scholar 

  94. Pate JS, Froend RH, Bowen BJ, Hansen A, Kuo J. Seedling growth and storage characteristics of seeder and resprouter species of Mediterranean-type ecosystems of S. W Australia Annals of Botany. 1990;65:585–601.

    Google Scholar 

  95. Piper FI. Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance. Ann For Sci. 2011;68:415–24.

    Google Scholar 

  96. Piper FI. Patterns of carbon storage in relation to shade tolerance in southern south American species. Am J Bot. 2015;102:1442–52.

    CAS  Google Scholar 

  97. Piper FI, Fajardo A. Foliar habit, tolerance to defoliation and their link to carbon and nitrogen storage. J Ecol. 2014;102:1101–11.

    CAS  Google Scholar 

  98. Piper FI, Fajardo A. Carbon dynamics of Acer pseudoplatanus seedlings under drought and complete darkness. Tree Physiol. 2016;36:1400–1408.

  99. Poirier M, Lacointe A, Améglio T. A semi-physiological model of cold hardening and dehardening in walnut stem. Tree Physiol. 2010;30:1555–69.

    Google Scholar 

  100. Poorter L, Kitajima K. Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology. 2007;88:1000–11.

    Google Scholar 

  101. • Quentin AG, Pinkard EA, Ryan MG, et al. Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol. 2015;35:1146–65 This paper demonstrated that there can be substantial variation between labs in estimates of sugar and starch concentrations of the same samples. Such variation is problematic for NSC comparisons between labs or for interpreting absolute values, such as relates to thresholds for starvation.

    CAS  Google Scholar 

  102. Ramel F, Sulmon C, Bogard M, Couée I, Gouesbet G. Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol. 2009;9:28.

    Google Scholar 

  103. Regier N, Streb S, Cocozza C, Schaub M, Cherubini P, Zeeman SC, et al. Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell Environ. 2009;32:1724–36.

    CAS  Google Scholar 

  104. Reinhardt K, Germino MJ, Kueppers LM, Domec J-C, Mitton J. Linking carbon and water relations to drought-induced mortality in Pinus flexilis seedlings. Tree Physiol. 2015;35:771–82.

    CAS  Google Scholar 

  105. Rodríguez-Calcerrada J, Li M, López R, Cano FJ, Oleksyn J, Atkin OK, et al. Drought-induced shoot dieback starts with massive root xylem embolism and variable depletion of nonstructural carbohydrates in seedlings of two tree species. New Phytol. 2017;213:597–610.

    Google Scholar 

  106. Sala A, Piper F, Hoch G. Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol. 2010;186:274–81.

    Google Scholar 

  107. Sala A, Woodruff DR, Meinzer FC. Carbon dynamics in trees: feast or famine? Tree Physiol. 2012;32:764–75.

    CAS  Google Scholar 

  108. Scarano FR, Cattânio JH, Crawford RMM. Root carbohydrate storage in young saplings of an Amazonian tidal várzea forest before the onset of the wet season. Acta Botanica Brasilica. 1994;8:129–39.

    Google Scholar 

  109. Schädel C, Blöchl A, Richter A, Hoch G. Short-term dynamics of nonstructural carbohydrates and hemicelluloses in young branches of temperate forest trees during bud break. Tree Physiol. 2009;29:901–11.

    Google Scholar 

  110. • Schenk HJ, Espino S, Romo DM, et al. Xylem Surfactants Introduce a New Element to the Cohesion-Tension Theory. Plant Physiol. 2017;173:1177–96 Paper demonstrates that angiosperm xylem contains lipid surfactants, found near hydrophobic surfaces and coating gas nanobubbles, which the authors argue will limit the formation of embolism and allow for water transport under tension.

    CAS  Google Scholar 

  111. Schoonmaker AL, Lieffers VJ, Landhäusser SM. Uniform versus asymmetric shading mediates crown recession in conifers. PLoS One. 2014;9:e104187.

    Google Scholar 

  112. Schwilk DW, Ackerly DD. Is there a cost to resprouting? Seedling growth rate and drought tolerance in sprouting and nonsprouting Ceanothus (Rhamnaceae). Am J Bot. 2005;92:404–10.

    Google Scholar 

  113. Secchi F, Pagliarani C, Zwieniecki MA. The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant Cell Environ. 2017;40:858–71.

    CAS  Google Scholar 

  114. Sevanto S. Phloem transport and drought. J Exp Bot. 2014;65:1751–9.

    CAS  Google Scholar 

  115. • Sevanto S, Mcdowell NG, Dickman LT, Pangle R, Pockman WT. How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant Cell Environ. 2014;37:153–61 Under experimental drought, the authors demonstrated that drought caused a loss of turgor in the phloem. This paper also provides a good discussion of the potential interactions between hydraulic failure and C starvation during drought.

    CAS  Google Scholar 

  116. Sloan JL, Islam MA, Jacobs DF. Reduced translocation of current photosynthate precedes changes in gas exchange for Quercus rubra seedlings under flooding stress. Tree Physiol. 2016;36:54–62.

    CAS  Google Scholar 

  117. Smith MG, Arndt SK, Miller RE, Kasel S, Bennett LT. Trees use more non-structural carbohydrate reserves during epicormic than basal resprouting. Tree Physiol. 2018;38:1779–91.

    CAS  Google Scholar 

  118. Sparks SR, Oechel WC. Factors influencing postfire sprouting vigor in the chaparral shrub ADENOSTOMA FASCICULATUM. Madroño. 1993;40:224–35.

    Google Scholar 

  119. Sperling O, Earles JM, Secchi F, Godfrey J, Zwieniecki MA. Frost induces respiration and accelerates carbon depletion in trees. PLoS One. 2015;10:e0144124.

    Google Scholar 

  120. Sperry JS, Sullivan JE. Xylem embolism in response to freeze-thaw cycles and water stress in ring-porous, diffuse-porous, and conifer species. Plant Physiol. 1992;100:605–13.

    CAS  Google Scholar 

  121. Spicer R. Symplasmic networks in secondary vascular tissues: parenchyma distribution and activity supporting long-distance transport. J Exp Bot. 2014;65:1829–48.

    CAS  Google Scholar 

  122. Strimbeck GR, Kjellsen TD, Schaberg PG, Murakami PF. Dynamics of low-temperature acclimation in temperate and boreal conifer foliage in a mild winter climate. Tree physiology. 2008;28:1365-1374. 28.

    Google Scholar 

  123. Tarkowski ŁP, Van den Ende W. Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Sci. 2015;6:203.

    Google Scholar 

  124. Valladares F, Niinemets Ü. Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst. 2008;39:237–57.

    Google Scholar 

  125. Verdaguer D, Ojeda F. Root starch storage and allocation patterns in seeder and resprouter seedlings of two cape Erica (Ericaceae) species. Am J Bot. 2002;89:1189–96.

    Google Scholar 

  126. Vitasse Y, Lenz A, Körner C. The interaction between freezing tolerance and phenology in temperate deciduous trees. Front Plant Sci. 2014. https://doi.org/10.3389/fpls.2014.00541.

  127. Voltas J, Camarero JJ, Carulla D, Aguilera M, Ortiz A, Ferrio JP. A retrospective, dual-isotope approach reveals individual predispositions to winter-drought induced tree dieback in the southernmost distribution limit of scots pine. Plant Cell Environ. 2013;36:1435–48.

    CAS  Google Scholar 

  128. Wachowski J, Landhäusser SM, Lieffers VJ. Depth of root placement, root size and carbon reserves determine reproduction success of aspen root fragments. For Ecol Manag. 2014;313:83–90.

    Google Scholar 

  129. Watson MA, Casper BB. Morphogenetic constraints on patterns of carbon distribution in plants. Ann Rev Ecol Syst. 1984;15:233–258.

    Google Scholar 

  130. • Weber R, Schwendener A, Schmid S, Lambert S, Wiley E, Landhäusser SM, et al. Living on next to nothing: tree seedlings can survive weeks with very low carbohydrate concentrations. New Phytol. 2018;218:107–18 This paper demonstrated that almost all ( >90%) starch, glucose, fructose, and sucrose is generally available for remobilization, at least under non-water limiting conditions. Thresholds below which trees starve were identified as 0.2–1.6% w/w for starch and 0.2–2.4% for sugar, depending on the tissue and the species.

    CAS  Google Scholar 

  131. Wiley E, Helliker B. A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol. 2012;195:285–9.

    CAS  Google Scholar 

  132. Wiley E, Hoch G, Landhäusser SM. Dying piece by piece: carbohydrate dynamics in aspen (Populus tremuloides) seedlings under severe carbon stress. J Exp Bot. 2017;68:5221–32.

    CAS  Google Scholar 

  133. • Wiley E, King C, Landhäusser SM. Identifying the relevant carbohydrate storage pools available for remobilization in aspen roots. Tree Physiol. 2019;39:1109–20 In contrast to Weber et al. 2018, this paper demonstrates that under starvation, substantial amounts of sugars—mostly excluding glucose, fructose, and sucrose—are never remobilized from root bark and xylem, providing evidence that a large portion of sugar pool may be either sequestered or not functioning as storage in older tree tissues.

    Google Scholar 

  134. Wiley E, Rogers BJ, Hodgkinson R, Landhäusser SM. Nonstructural carbohydrate dynamics of lodgepole pine dying from mountain pine beetle attack. New Phytol. 2016;209:550–62.

    CAS  Google Scholar 

  135. Wong BL, Baggett KL, Rye AH. Seasonal patterns of reserve and soluble carbohydrates in mature sugar maple (Acer saccharum). Canadian J Bot. 2003;81:780–8.

    CAS  Google Scholar 

  136. Yang B, Peng C, Zhu Q, Zhou X, Liu W, Duan M, et al. The effects of persistent drought and waterlogging on the dynamics of nonstructural carbohydrates of Robinia pseudoacacia L. seedlings in Northwest China. Forest. Ecosystems. 2019;6:23.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Central Arkansas, 201 Donaghey Ave, Conway, AR, 72035, USA

    Erin Wiley

Authors
  1. Erin Wiley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erin Wiley.

Ethics declarations

Conflict of Interest

The author declares that she has no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Climate Change and Carbon Sequestration

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wiley, E. Do Carbon Reserves Increase Tree Survival during Stress and Following Disturbance?. Curr Forestry Rep 6, 14–25 (2020). https://doi.org/10.1007/s40725-019-00106-2

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40725-019-00106-2

Keywords

Search

Navigation