Skip to main content
SpringerLink
Log in

Mobile carbon supply in trees and shrubs at the alpine treeline ecotone

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Although the growth limitation hypothesis (GLH) is the most accepted physiological explanation for alpine treeline formation, the debate about its formation mechanisms still remains controversial due to contradictory findings from different studies. The functional difference between trees and alpine low-stature shrubs may hold answers, as shrubs grow well at higher elevations. We investigated carbon (C) storage in deciduous treeline species Betula ermanii (Erman’s birch) and two dominant shrubs (deciduous Vaccinium uliginosum and evergreen Rhododendron aureum), which naturally grow next to each other at the treeline ecotone on Changbai Mountain, Northeast China. We determined growth and non-structural carbohydrate (NSC) concentrations in organs with increasing elevation at the mid-growing season. Results showed that in the treeline ecotone soil temperature was lower than tree canopy air temperature due to unobvious aerodynamic decoupling near the ground. Species growth consistently decreased with increasing elevation, while NSC concentrations responded differently to elevation between trees and shrubs. An elevational increase and decrease in NSC were observed in leaves and woody organs, respectively, of B. ermanii. NSC concentrations in each organ significantly increased with increasing elevation for R. aureum but decreased for V. uliginosum. At the treeline, shrubs had higher values than B. ermanii in NSC, ratios of soluble sugars to starch in leaves, and leaf mass per area. Organ dependence of NSC with increasing elevation in Betula trees provided partial support for the GLH, while R. aureum and V. uliginosum provided strong support for the GLH and carbon limitation hypothesis, respectively. These imply that alpine shrubs may have evolved to maintain more advantageous C balance and functional features than did trees as an adaptation to higher-elevation climates.

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

Similar content being viewed by others

References

  • Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218

    Article  Google Scholar 

  • Dang HS, Zhang KR, Zhang QF, Xu YM (2015) Temporal variations of mobile carbohydrates in Abies fargesii at the upper tree limits. Plant Biol 17:106–113

    Article  CAS  PubMed  Google Scholar 

  • Dawes MA, Hattenschwiler S, Bebi P, Hagedorn F, Handa IT, Körner C, Rixen C (2011) Species-specific tree growth responses to 9 years of CO2 enrichment at the alpine treeline. J Ecol 99:383–394

    Google Scholar 

  • Fajardo A (2016) Wood density is a poor predictor of competitive ability among individuals of the same species. For Ecol Manag 372:217–225

    Article  Google Scholar 

  • Fajardo A, Piper FI (2014) An experimental approach to explain the southern Andes elevational treeline. Am J Bot 101:788–795

    Article  PubMed  Google Scholar 

  • Fajardo A, Piper FI (2017) An assessment of carbon and nutrient limitations in the formation of the southern Andes tree line. J Ecol 105:517–527

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fajardo A, Piper FI, Pfund L, Körner C, Hoch G (2012) Variation of mobile carbon reserves in trees at the alpine treeline ecotone is under environmental control. New Phytol 195:794–802

    Article  CAS  PubMed  Google Scholar 

  • Fajardo A, Piper FI, Hoch G (2013) Similar variation in carbon storage between deciduous and evergreen treeline species across elevational gradients. Ann Bot 112:623–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Genet M, Li MC, Luo TX, Fourcaud T, Clement-Vidal A, Stokes A (2011) Linking carbon supply to root cell-wall chemistry and mechanics at high altitudes in Abies georgei. Ann Bot 107:311–320

    Article  CAS  PubMed  Google Scholar 

  • Handa IT, Körner C, Hattenschwiler S (2005) A test of the tree-line carbon limitation hypothesis by in situ CO2 enrichment and defoliation. Ecology 86:1288–1300

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hoch G, Körner C (2009) Growth and carbon relations of tree line forming conifers at constant vs. variable low temperatures. J Ecol 97:57–66

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hultine KR, Marshall JD (2000) Altitude trends in conifer leaf morphology and stable carbon isotope composition. Oecologia 123:32–40

    Article  CAS  PubMed  Google Scholar 

  • James J, Grace J, Hoad S (1994) Growth and photosynthesis of Pinus sylvestris at its altitudinal limit in Scotland. J Ecol 82:297–306

    Article  Google Scholar 

  • Jobbágy E, Jackson R (2000) Global controls of forest line elevation in the northern and southern hemispheres. Glob Ecol Biogeogr 9:253–268

    Article  Google Scholar 

  • Körner C (1998) A re-assessment of high elevation treeline positions and their explanation. Oecologia 115:445–459

    Article  PubMed  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Berlin Heidelberg, New York

    Book  Google Scholar 

  • Körner C (2007) Climatic treelines: conventions, global patterns, causes. Erdkunde 61:316–324

    Article  Google Scholar 

  • Körner C (2008) Winter crop growth at low temperature may hold the answer for alpine treeline formation. Plant Ecol Divers 1:3–11

    Article  Google Scholar 

  • Körner C (2012a) Alpine treelines: functional ecology of the global high elevation tree limits. Springer Science & Business Media, New York

    Book  Google Scholar 

  • Körner C (2012b) Treelines will be understood once the functional difference between a tree and a shrub is. Ambio 41:197–206

    Article  PubMed  PubMed Central  Google Scholar 

  • Körner C, Paulsen J (2004) A world-wide study of high altitude treeline temperatures. J Biogeogr 31:713–732

    Article  Google Scholar 

  • Kozlowski TT (1992) Carbohydrate sources and sinks in woody-plants. Bot Rev 58:107–222

    Article  Google Scholar 

  • Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain J-L, Laloi M, Coutos-Thévenot P, Maurousset L (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272

    Article  PubMed  PubMed Central  Google Scholar 

  • Lenz A, Vitasse Y, Hoch G, Korner C (2014) Growth and carbon relations of temperate deciduous tree species at their upper elevation range limit. J Ecol 102:1537–1548

    Article  Google Scholar 

  • Li MH, Yang J (2004) Effects of microsite on growth of Pinus cembra in the subalpine zone of the Austrian Alps. Ann For Sci 61:319–325

    Article  Google Scholar 

  • Li MH, Hoch G, Korner C (2001) Spatial variability of mobile carbohydrates within Pinus cembra trees at the alpine treeline. Phyton-Ann Rei Botanicae 41:203–213

    CAS  Google Scholar 

  • Li MH, Xiao WF, Shi PL, 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Liu Q-J, Xu Q-Q, Zhang G-C (2009) Impact of alpine snowpacks on primary productivity in Rhododendron aureum community in Changbai Mountain, China. Acta Ecol Sinica 29:4035–4044

    Google Scholar 

  • Martínez-Vilalta J, Sala A, Asensio D, Galiano LA, Hoch GN, Palacio S, Piper FI, Lloret F (2016) Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol Monogr 86:495–516

    Article  Google Scholar 

  • McIntire EJB, Piper FI, Fajardo A (2016) Wind exposure and light exposure, more than elevation-related temperature, limit treeline seedling abundance on three continents. J Ecol 104:1379–1390

    Article  Google Scholar 

  • Piper FI, Vinegla B, Linares JC, Camarero JJ, Cavieres LA, Fajardo A (2016) Mediterranean and temperate treelines are controlled by different environmental drivers. J Ecol 104:691–702

    Article  Google Scholar 

  • Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

    Article  PubMed  Google Scholar 

  • Rossi S, Deslauriers A, Anfodillo T, Carraro V (2007) Evidence of threshold temperatures for xylogenesis in conifers at high altitudes. Oecologia 152:1–12

    Article  PubMed  Google Scholar 

  • Sakai A., Larcher W. 1987. Frost survival of plants: responses and adaptation to freezing stress. Berlin, etc.[Ecological Studies, vol. 62.] Springer-Verlag 321 pp. Chaps. incl.: freezing process in plants

  • Sala A, Woodruff DR, Meinzer FC (2012) Carbon dynamics in trees: feast or famine? Tree Physiol 32:764–775

    Article  CAS  PubMed  Google Scholar 

  • Shi P, Koerner 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Solfjeld I, Johnsen O (2006) The influence of root-zone temperature on growth of Betula pendula Roth. Trees-Struct Funct 20:320–328

    Article  Google Scholar 

  • Stevens GC, Fox JF (1991) The causes of treeline. Ann Rev Ecol System 22:177–191

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Tranquillini W (1979) Physiological ecology of the alpine timberline: tree existence at high altitude with special reference to the European Alps. Springer, Berlin

    Book  Google Scholar 

  • Wang Q-W, Qi L, Zhou W, Liu C-G, Yu D, Dai L (2018) Carbon dynamics in the deciduous broadleaf tree Erman’s birch (Betula ermanii) at the subalpine treeline on Changbai Mountain, Northeast China. Am J Bot. https://doi.org/10.1002/ajb2.1006

    Google Scholar 

  • Wardle P (1993) Causes of alpine timberline: a review of the hypotheses. In: Alden J.N., Mastrantonio J.L., Ødum S. (eds) Forest development in cold climates. NATO ASI Series (Series A: Life Sciences), vol 244. Springer, Boston, MA

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Xu WD, Lin CQ (1981) Preliminary study of relations between vertical distribution of vegetation and thermal climate in Changbai Mountain. Res For Ecosyst 2:88–95

    Google Scholar 

  • Yu DP, Wang GG, Dai LM, Wang QL (2007) Dendroclimatic analysis of Betula ermanii forests at their upper limit of distribution in Changbai Mountain, Northeast China. For Ecol Manag 240:105–113

    Article  Google Scholar 

  • 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 - Struct Funct 28:935–947

    Article  CAS  Google Scholar 

  • Zhu WZ, Cao M, Wang SG, Xiao WF, Li MH (2012) Seasonal dynamics of mobile carbon supply in Quercus aquifolioides at the upper elevational limit. PLoS ONE 7:e34213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Ms. Jie Tian, Juan Jia, Hong Ding, Jiaqing Liu, Yuewei Tong, and Guanhua Dai for technical assistance in the field, Ms. Xiaoyu Wang for valuable comments, and the Office of the Changbai Mountain Natural Reserve for field investigation permission. This work was supported by the National Natural Science Foundation of China [Grant Numbers 41701052, 41571197]; Open Fund of Changbai Mountain Academy of Science; Special Research Project of Institute of Applied Ecology, CAS [Grant Number Y5YZX151YD]; and Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, CAS [Grant Number LFEM2016–05]. We thank two anonymous reviewers for valuable comments that improved earlier versions of the manuscript.

Author information

Authors and Affiliations

  1. Key Laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, 72 Wenhua Road, Shenyang, 110164, China

    Qing-Wei Wang, Wangming Zhou, Lin Qi, Li Zhou, Dapao Yu & Limin Dai

  2. Key Laboratory of Tropical Plant Resources and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, 666303, China

    Cheng-Gang Liu

  3. Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan

    Qing-Wei Wang

Authors
  1. Qing-Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng-Gang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wangming Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lin Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Li Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dapao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Limin Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qing-Wei Wang or Dapao Yu.

Additional information

Communicated by Enright.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 152 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, QW., Liu, CG., Zhou, W. et al. Mobile carbon supply in trees and shrubs at the alpine treeline ecotone. Plant Ecol 219, 467–479 (2018). https://doi.org/10.1007/s11258-018-0809-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-018-0809-3

Keywords

Search

Navigation