Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

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

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 to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

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

  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 24:166–173

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

  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 109:274–283

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

  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 62:3621–3636

  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 159:513–521

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

  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 104–127

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

  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 293:131–133

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

  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 159–174

  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 127:566–574

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

  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 172–177

  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 112:492–501

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

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

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

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

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

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

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

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

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

  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 133:1296–1305

  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 98:1105–1114

  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 94:784–790

  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 168:575–587

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

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

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

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

  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 57:2203–2210

  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 18:677–694

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

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

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

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

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

  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 34:393–401

  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 188:161–174

  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 28:1467–1473

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

  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 25:539–548

  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 129–145

  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 175:179–191

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

  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 22:573–578

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

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

  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)

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

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

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

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

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

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

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, Y., Yang, Q., 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

Keywords

  • Deciduousness
  • Leaf phenology
  • Carbon balance
  • Anthocyanin
  • Cloud forest