Abstract
Key message
A ratio of storage to growth of at least 8.4 and a balanced storage-growth relationship might be essential for subalpine larch trees to persist at the treeline.
Abstract
Cold-adapted trees display acclimation in trade-off of carbon storage and growth under cold stress at their upper elevational range limits. However, two prevailing hypotheses (growth/sink limitation hypothesis and carbon/source limitation hypothesis) based on carbon supply-demand balance are highly controversial and cannot yet provide a broad explanation for the formation of alpine treeline. Here, to probe into the physiological mechanism of treeline formation from carbon allocation, we examined the spatial dynamics of whole-tree mobile carbon pools and structural growth of the deciduous treeline tree species Larix chinensis along an elevational gradient in the Qinling Mountains of north-central China. Our results showed that the whole-tree non-structural carbohydrates stock increased significantly while the structural growth decreased with the increase in elevation. The ratio of carbon storage to structural growth increased with the increase in elevation, showing that it was highest at a ratio of 8.4 at the treeline site at the end of growing season. Such variations of storage-growth ratio might be attributable to the trade-off of carbon allocation and tree survival, which changed along elevation due to different intensity of cold stress. Thus, we concluded that a ratio of storage to growth of at least 8.4 might be essential for subalpine larch trees to persist at their low-temperature edge. Therefore, a sufficient carbon storage-growth ratio and a balanced storage-growth relationship might be required for subalpine larch trees to survive and develop in the altitudinal treeline ecotone.
Similar content being viewed by others
Data availability
We confirm that, should the manuscript be accepted, the data supporting the results will be archived in a permanent public repository such as Dryad or figshare, and the data DOI will be provided at the end of the article.
References
Abeli T, Gentili R, Mondoni A, Orsenigo S, Rossi G (2014) Effects of marginality on plant population performance. J Biogeogr 41:239–249
Bansal S, Germino MJ (2008) Carbon balance of conifer seedlings at timberline: relative changes in uptake, storage, and utilization. Oecologia 158:217–227
Cong Y, Li MH, Liu K, Dang YC, Han HD, He HS (2019) Decreased temperature with increasing elevation decreases the end-season leaf-to-wood reallocation of resources in deciduous Betula ermanii cham. trees. Forests 10:166
Dang H, Zhang K, Zhang Q, Xu Y (2015) Temporal variations of mobile carbohydrates in Abies fargesii at the upper tree limits. Plant Biol 17:106–113
Dawes MA, S Hättenschwiler, P Bebi, F Hagedorn, IT Handa, C Körner, C Rixen (2011) Species-specific tree growth responses to 9 years of CO2 enrichment at the alpine treeline. J Ecol 99:383–394
Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687
Dolezal J, Kopecky M, Dvorsky M, Macek M, Rehakova K, Capkova K, Borovec J, Schweingruber F, Liancourt P, Altman J (2019) Sink limitation of plant growth determines tree line in the arid Himalayas. Funct Ecol 33:553–565
Ericsson T, Rytter L, Vapaavuori E (1996) Physiology of carbon allocation in trees. Biomass Bioenerg 11:115–127
Fajardo A, Piper FI, Cavieres LA (2011) Distinguishing local from global climate influences in the variation of carbon status with altitude in a tree line species. Glob Ecol Biogeogr 20:307–318
Fu ZJ (1994) Study on ecological features and biomass of Larix chinensis forest in the Taibai Mountain. J Hanzhong Normal Univ (nat Sci) 2:69–72
Furze ME, Huggett BA, Aubrecht DM, Stolz CD, Carbone MS, Richardson AD (2019) Whole-tree nonstructural carbohydrate storage and seasonal dynamics in five temperate species. New Phytol 221:1466–1477
Granda E, Camarero JJ (2017) Drought reduces growth and stimulates sugar accumulation: new evidence of environmentally driven non-structural carbohydrate use. Tree Physiol 37:997–1000
Gruber A, Pirkebner D, Oberhuber W, Wieser G (2011) Spatial and seasonal variations in mobile carbohydrates in Pinus cembra in the timberline ecotone of the Central Austrian Alps. Eur J for Res 130:173–179
Handa IT, Körner C, Hättenschwiler S (2005) A test of the treeline carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86:1288–1300
Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees - from what we can measure to what we want to know. New Phytol 211:386–403
Hartmann H, McDowell NG, Trumbore S (2015) Allocation to carbon storage pools in Norway spruce saplings under drought and low CO2. Tree Physiol 35:243–252
Hoch G, Korner C (2003) The carbon charging of pines at the climatic treeline: a global comparison. Oecologia 135:10–21
Hoch G, Körner C (2012) Global patterns of mobile carbon stores in trees at the high-elevation tree line. Glob Ecol Biogeogr 21:861–871
Hoch G, Popp M, Körner C (2002) Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos 98:361–374
Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081
Hoch G (2015) Carbon reserves as indicators for carbon limitation in trees. Progress in Botany 76:321–346
Huang J, Forkelová L, Unsicker SB, Forkel M, Griffith DWT, Trumbore S, Hartmann H (2019) Isotope labeling reveals contribution of newly fixed carbon to carbon storage and monoterpenes production under water deficit and carbon limitation. Environ Exp Bot 162:333–344
Körner C (1999) Alpine plant life. Springer, Berlin Heidelberg
Körner C (2003) Carbon limitation in trees. J Ecol 91:4–17
Körner C (2016) When it gets cold, plant size matters—a comment on treeline. J Veg Sci 27:6–7
Körner C, Paulsen J (2004) A world-wide study of high altitude treeline temperatures. J Biogeogr 31:713–732
Kozlowski TT (1992) Carbohydrate sources and sinks in woody-plants. Bot Rev 58:107–222
Li MH, Xiao WF, Shi P, Wang SG, Zhong YD, Liu XL, Wang XD, Cai XH, Shi ZM (2008a) Nitrogen and carbon source-sink relationships in trees at the Himalayan treelines compared with lower elevations. Plant Cell Environ 31:1377–1387
Li MH, Xiao WF, Wang SG, Cheng GW, Cherubini P, Cai XH, Liu XL, Wang XD, Zhu WZ (2008b) Mobile carbohydrates in Himalayan treeline trees I. Evidence for carbon gain limitation but not for growth limitation. Tree Physiol 28:1287–1296
Liancourt P, Spence LA, Song DS, Lkhagva A, Sharkhuu A, Boldgiv B, Helliker BR, Petraitis PS, Casper BB (2013) Plant response to climate change varies with topography, interactions with neighbors, and ecotype. Ecology 94:444–453
Liu YU, Linderholm HW, Song H, Cai Q, Tian Q, Sun J, Chen D, Simelton E, Seftigen K, Tian HUA, Wang R, Bao G, An Z (2009) Temperature variations recorded in Pinus tabulae form is tree rings from the southern and northern slopes of the central Qinling Mountains, central China. Boreas 38:285–291
Liu R, Li Q, Liu Y, Li X, Ren M, Ma Y, Sun C, Song H, Cai Q (2021) Relative humidity variation derived from tree-ring δ18O and possible large-scale atmospheric circulations linkage over the Guanzhong Plain, central northern China, since 1760 CE. Int J Climatol 41:3044–3057
Massad TJ, Trumbore SE, Ganbat G, Reichelt M, Unsicker S, Boeckler A, Gleixner G, Gershenzon J, Ruehlow S (2014) An optimal defense strategy for phenolic glycoside production in Populus trichocarpa–isotope labeling demonstrates secondary metabolite production in growing leaves. New Phytol 203:607–619
Monson RK, Rosenstiel TN, Forbis TA, Lipson DA, Jaeger CH 3rd (2006) Nitrogen and carbon storage in alpine plants. Integr Comp Biol 46:35–48
Morin X, Ameglio T, Ahas R, Kurz-Besson C, Lanta V, Lebourgeois F, Miglietta F, Chuine I (2007) Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol 27:817–825
Muffler L, Beierkuhnlein C, Aas G, Jentsch A, Schweiger AH, Zohner C, Kreyling J (2016) Distribution ranges and spring phenology explain late frost sensitivity in 170 woody plants from the Northern Hemisphere. Glob Ecol Biogeogr 25:1061–1071
Mund M, Herbst M, Knohl A, Matthaus B, Schumacher J, Schall P, Siebicke L, Tamrakar R, Ammer C (2020) It is not just a “trade-off”: indications for sink- and source-limitation to vegetative and regenerative growth in an old-growth beech forest. New Phytol 226:111–125
Myers JA, Kitajima K (2007) Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J Ecol 95:383–395
Osaki M, Shinano T, Tadano T (1991) Redistribution of carbon and nitrogen-compounds from the shoot to the harvesting organs during maturation in field crops. Soil Sci Plant Nutr 37:117–128
Palacio S, Hoch G, Sala A, Körner C, Millard P (2014) Does carbon storage limit tree growth? New Phytol 201:1096–1100
Peters RL, Miranda JC, Schonbeck L, Nievergelt D, Fonti MV, Saurer M, Stritih A, Fonti P, Wermelinger B, von Arx G, Lehmann MM (2020) Tree physiological monitoring of the 2018 larch budmoth outbreak: preference for leaf recovery and carbon storage over stem wood formation in Larix decidua. Tree Physiol 40:1697–1711
Piper FI, Cavieres LA, Reyes-Díaz M, Corcuera LJ (2005) Carbon sink limitation and frost tolerance control performance of the tree Kageneckia angustifolia D. Don (Rosaceae) at the treeline in central Chile. Plant Ecol 185:29–39
Poorter L, Kitajima K (2007) Carbohydrate storage and light requirements of tropical moist and dry forest tree species. Ecology 88:1000–1011
Reyes-Bahamonde C, Piper FI, Cavieres LA (2021) Carbon allocation to growth and storage depends on elevation provenance in an herbaceous alpine plant of Mediterranean climate. Oecologia 195:299–312
Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775
Savage JA, Cavender-Bares J (2013) Phenological cues drive an apparent trade-off between freezing tolerance and growth in the family Salicaceae. Ecology 94:1708–1717
Schwinning S, Weiner J (1998) Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113:447–455
Sheen J, Zhou L, Jang J-C (1999) Sugars as signaling molecules. Plant Biol 2:410–418
Shi PL, Körner C, Hoch G (2006) End of season carbon supply status of woody species near the treeline in western China. Basic Appl Ecol 7:370–377
Shi P, Körner C, Hoch G (2008) A test of the growth-limitation theory for alpine tree line formation in evergreen and deciduous taxa of the eastern Himalayas. Funct Ecol 22:213–220
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–1149
Susiluoto S, Hilasvuori E, Berninger F (2010) Testing the growth limitation hypothesis for subarctic Scots pine. J Ecol 98:1186–1195
Sveinbjörnsson B, Smith M, Traustason T, Ruess RW, Sullivan PF (2010) Variation in carbohydrate source–sink relations of forest and treeline white spruce in southern, interior and northern Alaska. Oecologia 163:833–843
Tang ZY, Fang JY (2006) Temperature variation along the northern and southern slopes of Mt. Taibai, China. Agric Forest Meteorol 139:200–207
Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861
Weber R, Gessler A, Hoch G (2019) High carbon storage in carbon-limited trees. New Phytol 222:171–182
Wiley E, Helliker B (2012) A re-evaluation of carbon storage in trees lends greater support for carbon limitation to growth. New Phytol 195:285–289
Wiley E, Huepenbecker S, Casper BB, Helliker BR (2013) The effects of defoliation on carbon allocation: can carbon limitation reduce growth in favour of storage? Tree Physiol 33:1216–1228
Wiley E, Casper BB, Helliker BR (2017) Recovery following defoliation involves shifts in allocation that favour storage and reproduction over radial growth in black oak. J Ecol 105:412–424
Wyka TP, Karolewski P, Zytkowiak R, Chmielarz P, Oleksyn J (2016) Whole-plant allocation to storage and defense in juveniles of related evergreen and deciduous shrub species. Tree Physiol 36:536–547
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514
Yu D, Wang Q, Liu J, Zhou W, Qi L, Wang X, Zhou L, Dai L (2014) Formation mechanisms of the alpine Erman’s birch (Betula ermanii) treeline on Changbai Mountain in Northeast China. Trees 28:935–947
Zhang WH, Wang YP, Kang YX, Liu XJ (2004) Study on the relationship between Larix chinensis population’s structure and environment factors. Acta Ecol Sin 24:41–47
Zhou Q, Shi H, He R, Liu H, Zhu W, Yu D, Zhang Q, Dang H (2021) Prioritized carbon allocation to storage of different functional types of species at the upper range limits is driven by different environmental drivers. Sci Total Environ 773:145581
Zhu W-Z, Cao M, Wang S-G, Xiao W-F, Li M-H (2012) Seasonal dynamics of mobile carbon supply in Quercus aquifolioides at the upper elevational limit. PLoS ONE 7:e34213
Funding
This work was supported by the National Natural Science Foundation of China (31971491, 31770517), the Biodiversity Survey and Assessment Project of the Ministry of Ecology and Environment of China (2019HJ2096001006).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.
Additional information
Communicated by B. Fernandez-Marin.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
He, R., Zhou, Q., Shi, H. et al. Variations in trade-off of carbon storage and growth in subalpine larch across an elevational gradient. Trees 36, 1895–1907 (2022). https://doi.org/10.1007/s00468-022-02336-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-022-02336-7