, Volume 173, Issue 3, pp 721–730 | Cite as

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

  • Yong-Jiang Zhang
  • Qiu-Yun Yang
  • David W. Lee
  • Guillermo GoldsteinEmail author
  • Kun-Fang CaoEmail author
Physiological ecology - Original research


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.


Deciduousness Leaf phenology Carbon balance Anthocyanin Cloud forest 



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).


  1. Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10:402–407PubMedCrossRefGoogle Scholar
  2. 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 24:166–173PubMedCrossRefGoogle Scholar
  3. Axelrod DI (1966) Origin of deciduous and evergreen habit in temperate forests. Evolution 20:1–15CrossRefGoogle Scholar
  4. 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 109:274–283CrossRefGoogle Scholar
  5. Bassman J, Zwier JC (1991) Gas exchange characteristics of Populus trichocarpa, Populus deltoides and a Populus trichocarpa × P. deltoides clone. Tree Physiol 8:145–149PubMedCrossRefGoogle Scholar
  6. 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 62:3621–3636PubMedCrossRefGoogle Scholar
  7. 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 159:513–521CrossRefGoogle Scholar
  8. Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70:1–9CrossRefGoogle Scholar
  9. 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 104–127Google Scholar
  10. Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol 43:599–626Google Scholar
  11. 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 293:131–133PubMedCrossRefGoogle Scholar
  12. Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum). Plant Physiol 72:297–302PubMedCrossRefGoogle Scholar
  13. 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 159–174Google Scholar
  14. 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 127:566–574PubMedCrossRefGoogle Scholar
  15. Gamon JA, Surfus JS (1999) Assessing leaf content and activity with a reflectometer. New Phytol 143:105–117CrossRefGoogle Scholar
  16. 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 172–177Google Scholar
  17. 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 112:492–501CrossRefGoogle Scholar
  18. Germino MJ, Smith WK (1999) Sky exposure, crown architecture, and low-temperature photoinhibition in conifer seedlings at alpine treeline. Plant Cell Environ 22:407–415CrossRefGoogle Scholar
  19. Germino MJ, Smith WK (2000) Differences in microsite, plant form, and low-temperature photosynthesis in alpine plants. Arct Antarct Alp Res 32:388–396CrossRefGoogle Scholar
  20. Gitelson AA, Merzlyak MN, Chivkunova OB (2001) Optical properties and nondestructive estimation of anthocyanin content in plant leaves. Photochem Photobiol 74:38–45PubMedCrossRefGoogle Scholar
  21. Givnish TJ (2002) Adaptive significance of evergreen vs. deciduous leaves: solving the triple paradox. Silva Fenn 36:703–743Google Scholar
  22. Goldstein G, Nobel PS (1994) Water relations and low-temperature acclimation for cactus species varying in freezing tolerance. Plant Physiol 104:675–681PubMedGoogle Scholar
  23. Gould KS (2004) Nature’s swiss army knife: the diverse protective roles of anthocyanins in leaves. J Biomed Biotechnol 5:314–320CrossRefGoogle Scholar
  24. Gould KS, Vogelmann TC, Han T, Clearwater MJ (2002) Profiles of photosynthesis within red and green leaves of Quintinia serrata. Physiol Plant 116:127–133Google Scholar
  25. Harborne JR (1988) The flavonoids: recent advances. In: Goodwin TW (ed) Plant pigments. Academic, London, pp 299–343Google Scholar
  26. Hoch WA, Zeldin EL, Mcgown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21:1–8PubMedCrossRefGoogle Scholar
  27. 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 133:1296–1305PubMedCrossRefGoogle Scholar
  28. 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 98:1105–1114PubMedCrossRefGoogle Scholar
  29. 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 94:784–790PubMedCrossRefGoogle Scholar
  30. Hughes NM, Burkey KO, Neufeld HS (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb, Galax urceolata. New Phytol 168:575–587PubMedCrossRefGoogle Scholar
  31. Hughes NM, Carpenter KL, Cannon JG (2013) Estimating contribution of anthocyanin pigments to osmotic adjustment during winter leaf reddening. J Plant Physiol 170:230–233PubMedCrossRefGoogle Scholar
  32. Iturraspe J, Engel N, Gossauer A (1994) Chlorophyll catabolism. Isolation and structure elucidation of chlorophyll b catabolites in Chlorella protothecoides. Phytochemistry 35:1387–1390CrossRefGoogle Scholar
  33. Kikuzawa K, Lechowicz MJ (2011) Ecology of leaf longevity. Springer, BerlinCrossRefGoogle Scholar
  34. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727CrossRefGoogle Scholar
  35. 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 57:2203–2210PubMedCrossRefGoogle Scholar
  36. 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 18:677–694CrossRefGoogle Scholar
  37. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592Google Scholar
  38. Lipp CC, Goldstein G, Meinzer FC, Neimczura W (1994) Freezing tolerance and avoidance in high-elevation Hawaiian plants. Plant Cell Environ 17:1035–1044CrossRefGoogle Scholar
  39. Malhi Y, Baldocchi DD, Jarvis PG (1999) The carbon balance of tropical temperate and boreal forests. Plant Cell Environ 22:715–740CrossRefGoogle Scholar
  40. Matile P (2000) Biochemistry of Indian summer: physiology of autumn leaf coloration. Exp Gerontol 35:145–158PubMedCrossRefGoogle Scholar
  41. Matile R, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95PubMedCrossRefGoogle Scholar
  42. 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 34:393–401CrossRefGoogle Scholar
  43. 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 188:161–174PubMedCrossRefGoogle Scholar
  44. Murakami PF, Schaberg PG, Shane JB (2008) Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiol 28:1467–1473PubMedCrossRefGoogle Scholar
  45. Neill SO, Gould KS (2003) Anthocyanins in leaves: light attenuators or antioxidants? Funct Plant Biol 30:865–873CrossRefGoogle Scholar
  46. Neill SO, Gould KS, Kilmartin PA, Mitchell KA, Markham KR (2002) Antioxidant activities of red versus green leaves in Elatostema rugosum. Plant Cell Environ 25:539–548CrossRefGoogle Scholar
  47. 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 129–145Google Scholar
  48. 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 175:179–191CrossRefGoogle Scholar
  49. Qiu X-Z, Xie S-C (1998) Studies on the forest ecosystem in Ailao Mountains, Yunnan. Yunnan Science and Technology, KunmingGoogle Scholar
  50. Schaberg PG, Murakami PF, Turner MR, Heitz HK, Hawley GJ (2008) Association of red coloration with senescence of sugar maple leaves in autumn. Trees 22:573–578CrossRefGoogle Scholar
  51. Sierra-Almeida A, Cavieres LA (2010) Summer freezing resistance in high-elevation plants exposed to experimental warming in the central Chilean Andes. Oecologia 163:267–276PubMedCrossRefGoogle Scholar
  52. Smillie RM, Hetherington SE (1999) Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica 36:451–463CrossRefGoogle Scholar
  53. 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
  54. Taneda H, Tateno M (2005) Hydraulic conductivity, photosynthesis and leaf water balance in six evergreen woody species from fall to winter. Tree Physiol 25:299–306PubMedCrossRefGoogle Scholar
  55. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599PubMedCrossRefGoogle Scholar
  56. Wolfe JA (1987) Late Cretaceous–Cenozoic history of deciduousness and the terminal Cretaceous event. Paleobiology 13:215–226Google Scholar
  57. Wu Z-Y (1980) The vegetation of China. Science Press, BeijingGoogle Scholar
  58. Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglaChina
  2. 2.Department of BiologyUniversity of MiamiCoral GablesUSA
  3. 3.Ailaoshan Station for Subtropical Forest Ecosystem StudiesChinese Academy of SciencesJingdongChina
  4. 4.Graduate University of Chinese Academy of SciencesBeijingChina
  5. 5.Department of Biological SciencesFlorida International UniversityMiamiUSA
  6. 6.Departamento de Ecologia, Genetica y Evolucion, Facultad de Ciencias Exactas y NaturalesUniversidad de Buenos Aires, Ciudad UniversitariaBuenos AiresArgentina
  7. 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 ForestryGuangxi UniversityNanningChina

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