Skip to main content
SpringerLink
Log in

Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests

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

Abstract

The relative advantages of being deciduous or evergreen in subtropical forests and the relationship between leaf phenology and nutrient resorption efficiency are not well understood. The most successful deciduous species (Lyonia ovalifolia) in an evergreen-dominated subtropical montane cloud forest in southwest (SW) China maintains red senescing leaves throughout much of the winter. The aim of this study was to investigate whether red senescing leaves of this species were able to assimilate carbon in winter, to infer the importance of maintaining a positive winter carbon balance in subtropical forests, and to test whether an extended leaf life span is associated with enhanced nutrient resorption and yearly carbon gain. The red senescing leaves of L. ovalifolia assimilated considerable carbon during part of the winter, resulting in a higher yearly carbon gain than co-occurring deciduous species. Its leaf N and P resorption efficiency was higher than for co-occurring non-anthocyanic deciduous species that dropped leaves in autumn, supporting the hypothesis that anthocyanin accumulation and/or extended leaf senescence help in nutrient resorption. Substantial winter carbon gain and efficient nutrient resorption may partially explain the success of L. ovalifolia versus that of the other deciduous species in this subtropical forest. The importance of maintaining a positive carbon balance for ecological success in this forest also provides indirect evidence for the dominance of evergreen species in the subtropical forests of SW China.

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
Fig. 5

Similar content being viewed by others

References

  • Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10:402–407

    Article  PubMed  CAS  Google Scholar 

  • Archetti M, Doring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PG, Thomas H (2009) Adaptive explanations for autumn colours: an interdisciplinary approach. Trends Ecol Evol 24:166–173

    Article  PubMed  Google Scholar 

  • Axelrod DI (1966) Origin of deciduous and evergreen habit in temperate forests. Evolution 20:1–15

    Article  Google Scholar 

  • Barnes PW, Searles PS, Ballare CL, Ryel RJ, Caldwell MM (2000) Non-invasive measurements of leaf epidermal transmittance of UV radiation using chlorophyll fluorescence: field and laboratory studies. Physiol Plant 109:274–283

    Article  CAS  Google Scholar 

  • Bassman J, Zwier JC (1991) Gas exchange characteristics of Populus trichocarpa, Populus deltoides and a Populus trichocarpa × P. deltoides clone. Tree Physiol 8:145–149

    Article  PubMed  Google Scholar 

  • Bogard M, Jourdan M, Allard V, Martre P, Perretant MR, Ravel C, Heumez E, Orford S, Snape J, Griffiths S, Gaju O, Foulkes J, Le Gouis J (2011) Anthesis date mainly explained correlations between post-anthesis leaf senescence, grain yield, and grain protein concentration in a winter wheat population segregating for flowering time QTLs. J Exp Bot 62:3621–3636

    Article  PubMed  CAS  Google Scholar 

  • Boorse GC, Gartman TL, Meyer AC, Ewers FW, Davis SD (1998) Comparative methods of estimating freezing temperatures and freezing injury in leaves of chaparral shrubs. Int J Plant Sci 159:513–521

    Article  Google Scholar 

  • Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9

    Article  CAS  Google Scholar 

  • Chalker-Scott L (2002) Do anthocyanins function as osmoregulators in leaf tissues? In: Gould KS, Lee DW (eds) Anthocyanins in leaves. Advances in botanical research, vol 37. Academic, New York, pp 104–127

  • Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol 43:599–626

    CAS  Google Scholar 

  • Engel N, Jenny TA, Mooser V, Gossauer A (1991) Chlorophyll catabolism in Chlorella protothecoides. Isolation and structural elucidation of a red bilin derivative. FEBS Lett 293:131–133

    Article  PubMed  CAS  Google Scholar 

  • Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum). Plant Physiol 72:297–302

    Article  PubMed  CAS  Google Scholar 

  • Evans JR (1989) Photosynthesis—the dependence on nitrogen partitioning. In: Lambers H, Cambridge ML, Konings H, Pons TL (eds) Causes and consequences of variation in growth rate and productivity of higher plants. SPB, The Hague, pp 159–174

    Google Scholar 

  • Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127:566–574

    Article  PubMed  CAS  Google Scholar 

  • Gamon JA, Surfus JS (1999) Assessing leaf content and activity with a reflectometer. New Phytol 143:105–117

    Article  CAS  Google Scholar 

  • Gamon JA, Filella I, Penuelas J (1993) The dynamic 531-nanometer delta reflectance signal: a survey of twenty angiosperm species. In: Yamamoto HY, Smith CM (eds) Photosynthetic responses to the environment. American Society of Plant Physiologists, Rockville, pp 172–177

  • Gamon JA, Serrano L, Surfus JS (1997) The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. Oecologia 112:492–501

    Article  Google Scholar 

  • Germino MJ, Smith WK (1999) Sky exposure, crown architecture, and low-temperature photoinhibition in conifer seedlings at alpine treeline. Plant Cell Environ 22:407–415

    Article  Google Scholar 

  • Germino MJ, Smith WK (2000) Differences in microsite, plant form, and low-temperature photosynthesis in alpine plants. Arct Antarct Alp Res 32:388–396

    Article  Google Scholar 

  • Gitelson AA, Merzlyak MN, Chivkunova OB (2001) Optical properties and nondestructive estimation of anthocyanin content in plant leaves. Photochem Photobiol 74:38–45

    Article  PubMed  CAS  Google Scholar 

  • Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743

    Google Scholar 

  • Goldstein G, Nobel PS (1994) Water relations and low-temperature acclimation for cactus species varying in freezing tolerance. Plant Physiol 104:675–681

    PubMed  CAS  Google Scholar 

  • Gould KS (2004) Nature’s swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 5:314–320

    Article  Google Scholar 

  • Gould KS, Vogelmann TC, Han T, Clearwater MJ (2002) Profiles of photosynthesis within red and green leaves of Quintinia serrata. Physiol Plant 116:127–133

    Google Scholar 

  • Harborne JR (1988) The flavonoids: recent advances. In: Goodwin TW (ed) Plant pigments. Academic, London, pp 299–343

    Google Scholar 

  • Hoch WA, Zeldin EL, Mcgown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21:1–8

    Article  PubMed  CAS  Google Scholar 

  • Hoch WA, Singsaas EL, McCown BH (2003) Resorption protection. Anthocyanins facilitate nutrient recovery in autumn by shielding leaves from potentially damaging light levels. Plant Physiol 133:1296–1305

    Article  PubMed  CAS  Google Scholar 

  • Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol 98:1105–1114

    Article  PubMed  CAS  Google Scholar 

  • Hughes NM, Smith WK (2007) Attenuation of incident light in Galax urceolata (Diapensiaceae): concerted influence of adaxial and abaxial anthocyanic layers on photoprotection. Am J Bot 94:784–790

    Article  PubMed  CAS  Google Scholar 

  • Hughes NM, Burkey KO, Neufeld HS (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb, Galax urceolata. New Phytol 168:575–587

    Article  PubMed  CAS  Google Scholar 

  • Hughes NM, Carpenter KL, Cannon JG (2013) Estimating contribution of anthocyanin pigments to osmotic adjustment during winter leaf reddening. J Plant Physiol 170:230–233

    Article  PubMed  CAS  Google Scholar 

  • Iturraspe J, Engel N, Gossauer A (1994) Chlorophyll catabolism. Isolation and structure elucidation of chlorophyll b catabolites in Chlorella protothecoides. Phytochemistry 35:1387–1390

    Article  CAS  Google Scholar 

  • Kikuzawa K, Lechowicz MJ (2011) Ecology of leaf longevity. Springer, Berlin

    Book  Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • Kytridis V-P, Manetas Y (2006) Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of the oxy-radical source. J Exp Bot 57:2203–2210

    Article  PubMed  CAS  Google Scholar 

  • Lee DW, O’Keefe J, Holbrook NM, Feild TS (2003) Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecol Res 18:677–694

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • Lipp CC, Goldstein G, Meinzer FC, Neimczura W (1994) Freezing tolerance and avoidance in high-elevation Hawaiian plants. Plant Cell Environ 17:1035–1044

    Article  Google Scholar 

  • Malhi Y, Baldocchi DD, Jarvis PG (1999) The carbon balance of tropical temperate and boreal forests. Plant Cell Environ 22:715–740

    Article  CAS  Google Scholar 

  • Matile P (2000) Biochemistry of Indian summer: physiology of autumn leaf coloration. Exp Gerontol 35:145–158

    Article  PubMed  CAS  Google Scholar 

  • Matile R, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95

    Article  PubMed  CAS  Google Scholar 

  • Miyazawa Y, Kikuzawa K, Otsuki K (2007) Decrease in the capacity for RuBP carboxylation and regeneration with the progression of cold-induced photoinhibition during winter in evergreen broadleaf tree species in a temperate forest. Funct Plant Biol 34:393–401

    Article  CAS  Google Scholar 

  • Mur LAJ, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, James C, Papp I, Hortensteiner S, Thomas H, Ougham H (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188:161–174

    Article  PubMed  CAS  Google Scholar 

  • Murakami PF, Schaberg PG, Shane JB (2008) Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiol 28:1467–1473

    Article  PubMed  CAS  Google Scholar 

  • Neill SO, Gould KS (2003) Anthocyanins in leaves: light attenuators or antioxidants? Funct Plant Biol 30:865–873

    Article  CAS  Google Scholar 

  • Neill SO, Gould KS, Kilmartin PA, Mitchell KA, Markham KR (2002) Antioxidant activities of red versus green leaves in Elatostema rugosum. Plant Cell Environ 25:539–548

    Article  CAS  Google Scholar 

  • Oberbauer SF, Starr G (2002) The role of anthocyanins for photosynthesis of Alaskan Arctic evergreens during snowmelt. In: Gould KS, Lee DW (eds) Anthocyanins in leaves. Advances in botanical research, vol 37. Academic, New York, pp 129–145

  • Oliveira G, Penuelas J (2004) Effects of winter cold stress on photosynthesis and photochemical efficiency of PSII of the Mediterranean Cistus albidus L. and Quercus ilex L. Plant Ecol 175:179–191

    Article  Google Scholar 

  • Qiu X-Z, Xie S-C (1998) Studies on the forest ecosystem in Ailao Mountains, Yunnan. Yunnan Science and Technology, Kunming

    Google Scholar 

  • Schaberg PG, Murakami PF, Turner MR, Heitz HK, Hawley GJ (2008) Association of red coloration with senescence of sugar maple leaves in autumn. Trees 22:573–578

    Article  CAS  Google Scholar 

  • Sierra-Almeida A, Cavieres LA (2010) Summer freezing resistance in high-elevation plants exposed to experimental warming in the central Chilean Andes. Oecologia 163:267–276

    Article  PubMed  Google Scholar 

  • Smillie RM, Hetherington SE (1999) Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica 36:451–463

    Article  CAS  Google Scholar 

  • Song Y-C, Chen X-Y, Wang X-H (2005) Studies of evergreen broad-leaved forests of China: a retrospect and prospect. J East China Normal Univ 1:1–8 (in Chinese with English Abstract)

    Google Scholar 

  • Taneda H, Tateno M (2005) Hydraulic conductivity, photosynthesis and leaf water balance in six evergreen woody species from fall to winter. Tree Physiol 25:299–306

    Article  PubMed  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  • Wolfe JA (1987) Late Cretaceous–Cenozoic history of deciduousness and the terminal Cretaceous event. Paleobiology 13:215–226

    Google Scholar 

  • Wu Z-Y (1980) The vegetation of China. Science Press, Beijing

    Google Scholar 

  • Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank the staff of the Ailaoshan Station for Subtropical Ecosystem Studies who provided the climate data and logistic support. We thank the staff of the Biogeochemistry Laboratory of the Xishuangbanna Tropical Botanical Garden for the determination of nutrient concentrations. We also would like to thank Mr. Fu Xuwei, Mr. Zeng Xiaodong, Mr. Qi Jinhua, Mr. Luo Xin, Mr. Ai Ke, Mr. Li Xinde, and Mr. Liu Yuhong for their assistance in the field work. Y-J Zhang is currently supported by a Giorgio Ruffolo Fellowship in the Sustainability Science Program at the J.F. Kennedy School of Government, Harvard University. This study was supported by a grant from the National Natural Science Foundation of China (30670320).

Author information

Authors and Affiliations

  1. Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 666303, Mengla, Yunnan, China

    Yong-Jiang Zhang, Qiu-Yun Yang & Kun-Fang Cao

  2. Department of Biology, University of Miami, PO Box 249118, Coral Gables, FL, 33124, USA

    Yong-Jiang Zhang & Guillermo Goldstein

  3. Ailaoshan Station for Subtropical Forest Ecosystem Studies, Chinese Academy of Sciences, 676200, Jingdong, Yunnan, China

    Yong-Jiang Zhang & Qiu-Yun Yang

  4. Graduate University of Chinese Academy of Sciences, 100039, Beijing, China

    Yong-Jiang Zhang

  5. Department of Biological Sciences, Florida International University, Miami, FL, 33199, USA

    David W. Lee

  6. Departamento de Ecologia, Genetica y Evolucion, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Nuñez, Buenos Aires, Argentina

    Guillermo Goldstein

  7. State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, The Key Laboratory of Ministry of Education for Microbial and Plant Genetic Engineering, and College of Forestry, Guangxi University, 530004, Nanning, Guangxi, China

    Kun-Fang Cao

Authors
  1. Yong-Jiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiu-Yun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David W. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guillermo Goldstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kun-Fang Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guillermo Goldstein or Kun-Fang Cao.

Additional information

Communicated by Andrea Polle.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, YJ., Yang, QY., Lee, D.W. et al. Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests. Oecologia 173, 721–730 (2013). https://doi.org/10.1007/s00442-013-2672-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2672-1

Keywords

Search

Navigation