Skip to main content
Log in

Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees

  • Physiological ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Despite extensive research on the seasonal dynamics of non-structural carbohydrate (NSC) and nitrogen (N) concentrations, the size and relative contributions of NSC and N pools across different tree organs are not well understood. We have measured the changes in NSC and N concentrations in leaves, branches, stems and all root branch orders at monthly intervals in control and girdled trees of larch (Larix gmelinii) and ash (Fraxinus mandshurica). The biomass of each plant compartment was also determined to calculate the size of the NSC and N pools. In both species, 13–37 % of the NSC and N pools were mobilized at the beginning of the growing season. Among the mobilized pools, stems and non-absorptive roots (branch orders 4–9) acted as the largest NSC sources in larch and ash, respectively, while branches served as the largest N source in both species. After stem girdling, 22  and 50 % of the root NSC stores in larch and ash, respectively, were mobilized to maintain root activities during the growing season. Tree mortality was observed 1 year after girdling, at which time there was still an abundant NSC pool in the roots. We conclude that (1) different storage organs differ in their contribution to new tissue growth at the beginning of the growing season and that those storage organs holding higher fractions of the NSC or N pool are not necessarily those which mobilize more NSC or N; (2) tree growth may not be limited by carbon (C) availability; (3) C storage in non-absorptive roots plays an important role in maintaining tree survival after the termination of photosynthate flow from aboveground sources.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Atkinson LJ, Hellicar MA, Fitter AH, Atkin OK (2007) Impact of temperature on the relationship between respiration and nitrogen concentration in roots: an analysis of scaling relationships, Q 10 values and thermal acclimation ratios. New Phytol 173:110–120

    Article  CAS  PubMed  Google Scholar 

  • Binkley D, Stape JL, Takahashi EN, Ryan MG (2006) Tree-girdling to separate root and heterotrophic respiration in two Eucalyptus stands in Brazil. Oecologia 148:447–454

    Article  PubMed  Google Scholar 

  • Burton AJ, Jarvey JC, Jarvi MP, Zak DR, Pregitzer KS (2012) Chronic N deposition alters root respiration-tissue N relationship in northern hardwood forests. Global Change Biol 18:258–266

    Article  Google Scholar 

  • Buysse J, Merckx R (1993) An improved colorimetric method to quantify sugar content of plant tissue. J Exp Bot 44:1627–1629

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chen D, Zhang Y, Lin Y, Fu S (2010) Changes in belowground carbon in Acacia crassicarpa and Eucalyptus urophylla plantations after tree girdling. Plant Soil 326:123–135

    Article  CAS  Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source sink manipulations in a longleaf pine forest. Oecologia 140:450–457

    Article  PubMed  Google Scholar 

  • Guo DL, Li H, Mitchell RJ, Han WX, Hendricks JJ, Fahey TJ, Hendrick RL (2008) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol 177:443–456

    PubMed  Google Scholar 

  • Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081

    Article  CAS  Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    Article  PubMed  Google Scholar 

  • Jia S, Wang Z, Li X, Sun Y, Zhang X, Liang A (2010) N fertilization affects on soil respiration, microbial biomass and root respiration in Larix gmelinii and Fraxinus mandshurica plantations in China. Plant Soil 333:325–336

    Article  CAS  Google Scholar 

  • Jia S, Wang Z, Li X, Zhang X, Mclaughlin NB (2011) Effect of nitrogen fertilizer, root branch order and temperature on respiration and tissue N concentration of fine roots in Larix gmelinii and Fraxinus mandshurica. Tree Physiol 31:718–726

    Article  PubMed  Google Scholar 

  • Kobe RK (1997) Carbohydrate allocation to storage as a basis of interspecific variation in sapling survivorship and growth. Oikos 80:226–233

    Article  Google Scholar 

  • Kobe RK, Iyer M, Walters MB (2010) Optimal partitioning theory revisited: nonstructural carbohydrates dominate root mass responses to nitrogen. Ecology 91:166–179

    Article  PubMed  Google Scholar 

  • Körner C (2003) Carbon limitation in trees. J Ecol 91:4–14

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Langley JA, Drake BG, Hungate BA (2002) Extensive belowground carbon storage supports roots and mycorrhizae in regenerating scrub oaks. Oecologia 131:542–548

    Article  Google Scholar 

  • Latt CR, Nair PKR, Kang BT (2001) Reserve carbohydrate levels in the boles and structural roots of five multipurpose tree species in a seasonally dry tropical climate. For Ecol Manag 146:145–158

    Article  Google Scholar 

  • Lynch DJ, Matamala R, Iversen CM, Norby RJ, Gonzalez-Meler MA (2013) Stored carbon partly fuels fine-root respiration but is not used for production of new fine roots. New Phytol 199:420–430

    Article  CAS  PubMed  Google Scholar 

  • Magel E, Jay-Allemand C, Ziegler H (1994) Formation of heart-wood substances in the stemwood of Robinia pseudoacacia L. II. Distribution of nonstructural carbohydrates and wood extrac-tives across the trunk. Trees 8:165–171

    Article  Google Scholar 

  • Magel E, Einig W, Hampp R (2000) Carbohydrates in trees. Develop. Crop Sci 26:317–336

    Google Scholar 

  • Matamala R, Gonzalez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302:1385–1387

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1089

    Article  CAS  PubMed  Google Scholar 

  • Palacio S, Millard P, Maestro M, Montserrat-Marti G (2007) Non-structural carbohydrates and nitrogen dynamics in Mediterranean sub-shrubs: an analysis of the functional role of over wintering leaves. Plant Biol 9:49–58

    Article  CAS  PubMed  Google Scholar 

  • Piispanen R, Saranpää P (2001) Variation of non-structural carbohydrates in silver birch (Betula pendula Roth) wood. Trees Struct Funct 15:444–451

    Article  CAS  Google Scholar 

  • Poorter H, Niklas KJ, Reich PB, Oleksyn J, Poot P, Mommer L (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50

    Article  CAS  PubMed  Google Scholar 

  • Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309

    Article  Google Scholar 

  • Prislan P, Gričar J, de Luis M, Smith KT, Čufar K (2013) Phenological variation in xylem and phloem formation in Fagus sylvatica from two contrasting sites. Agric For Meteorol 180:142–151

    Article  Google Scholar 

  • Regier N, Streb S, Zeeman SC, Frey B (2010) Seasonal changes in starch and sugar content of poplar (Populus deltoides × nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiol 30:979–987

    Article  CAS  PubMed  Google Scholar 

  • Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL (2008) Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol Lett 11:793–801

    Article  PubMed  Google Scholar 

  • Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY, Murakami P, Schaberg PG, Xu X (2013) Seasonal dynamics and age of stemwood nonstructural carbohydrates in temperate forest trees. New Phytol 197:850–861

    Google Scholar 

  • Sakai A, Sakai S (1998) A test for the resource remobilization hypothesis: tree sprouting using carbohydrates from above-ground parts. Ann Bot 82:213–216

    Article  CAS  Google Scholar 

  • Silpi U, Lacointe A, Kasempsap P, Thanysawanyangkura S, Chantuma P, Gohet E, Musigamart N, Clement A, Ameglio T, Thaler P (2007) Carbohydrate reserves as a competing sink: evidence from tapping rubber trees. Tree Physiol 27:881–889

    Article  CAS  PubMed  Google Scholar 

  • Spann TM, Beede RH, Dejong TM (2008) Seasonal carbohydrate storage and mobilization in bearing and non-bearing pistachio (Pistacia vera) trees. Tree Physiol 28:207–213

    Article  CAS  PubMed  Google Scholar 

  • Teixeira EI, Mott DJ, Mickelbart MV (2007) Seasonal patterns of root C and N reserves of lucerne crops (Medicago sativa L.) grown in a temperate climate were affected by defoliation regime. Eur J Agron 26:10–20

    Article  CAS  Google Scholar 

  • Vargas R, Trumbore SE, Allen MF (2009) Evidence of old carbon used to grow new fine roots in a tropical forest. New Phytol 182(3):710–718

    Article  PubMed  Google Scholar 

  • Venugopal N, Liangkuwang MG (2007) Cambial activity and annual rhythm of xylem production of elephant apple tree (Dillenia indica Linn.) in relation to phenology and climatic factor growing in sub-tropical wet forest of northeast India. Trees 21:101–110

    Article  Google Scholar 

  • Wang ZQ, Guo DL, Wang XR, Gu JC, Mei L (2006) Fine root architecture, morphology and biomass of different branch orders of two Chinese temperate tree species. Plant Soil 288:155–171

    Article  CAS  Google Scholar 

  • Würth MKR, Peláez-Riedl S, Wright SJ, Körner C (2005) Non-structural carbohydrate pools in a tropical forest. Oecologia 143:11–24

    Article  PubMed  Google Scholar 

  • Xia MX, Guo DL, Pregitzer KS (2010) Ephemeral root modules in Fraxinus mandshurica. New Phytol 188:1065–1074

    Article  PubMed  Google Scholar 

  • Zhang KM, Li Z, Li Y, Li YH, Kong DZ, Wu RH (2013) Carbohydrate accumulation may be the proximate trigger of anthocyanin biosynthesis under autumn conditions in Begonia semperflorens. Plant Biol 15:991–1000

    Article  CAS  PubMed  Google Scholar 

  • Zheng Z, Feng Z, Cao M, Li Z, Zhang J (2006) Forest structure and biomass of a tropical seasonal rain forest in Xishuangbanna, Southwest China. Biotropica 38:318–327

    Article  Google Scholar 

Download references

Acknowledgments

We thank Drs. Shuxia Jia, Jianwei Shi and Shuiqiang Yu for assistance in the field and laboratory. Our sincere thanks are extended to Dr. Sean Bloszies for the editing that greatly improved the manuscript. This study was supported by Grants from the National Basic Research Program of China (973 Program, 2012CB416903), One-Hundred Talent Project of Chinese Academy of Sciences (no. KZZD-EW-TZ-11), and National Science Foundation of China (31021001, 31370627).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Yanmei Xiong or Dali Guo.

Additional information

Communicated by Hermann Heilmeier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mei, L., Xiong, Y., Gu, J. et al. Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees. Oecologia 177, 333–344 (2015). https://doi.org/10.1007/s00442-014-3186-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3186-1

Keywords

Navigation