Changes in foliar nitrogen resorption of Phyllostachys edulis with culm development

  • Changshun Zhang
  • Chunlan Liu
  • Wenyuan Zhang
  • Gaodi Xie
  • Shaohui Fan
  • Na Li
Original Paper


Leaf nitrogen resorption is very important to Phyllostachys edulis development because the withdrawn nitrogen can help newly emerging and growing culms. However, few studies have focused on the ontogenetic changes in leaf nitrogen resorption of P. edulis. Here, we examined the variability in mature leaf nitrogen concentrations (Nm), nitrogen resorption efficiency (NRE) and proficiency (NRP or Ns) and leaf-level nitrogen use efficiency (NUE) of the current-, 3rd- and 5th-year culms in P. edulis stands under extensive management. Analyses of variance and correlation indicated that patterns of Nm, NRP, NRE and NUE were markedly affected by culm age and leaf nitrogen status. Nm, Ns and NRE were significant higher in younger (current-year) culms with 1-year lifespan leaves, while NUE was markedly higher in older (3rd- or 5th-year) culms with 2-year lifespan leaves. Significant linear correlations between Nm and NRP, NRE and NUE, Nm and NUE, Ns and NRE were found for each culm age, and Nm was significantly positively correlated to NRE for all culms pooled. Higher proficiency in older culms led to higher NUE and lower NRE, these relationships can be modulated by Nm, which in turn, is restrained by leaf N availability and acquisition. Our results revealed that at the intraspecific level, P. edulis can adjust its leaf NRE, NRP, and leaf-level NUE in concert with culm development. Understanding nitrogen resorption characteristics and NUE of P. edulis can help decision-makers design appropriate deforestation strategies and achieve precise N fertilization for sustainable bamboo forest management.


Phyllostachys edulis Nitrogen resorption efficiency Nitrogen resorption proficiency Nitrogen-use efficiency Extensive management Culm development Precision fertilization 



Leaf nitrogen resorption efficiency


Leaf nitrogen resorption proficiency


Leaf-level nitrogen-use efficiency


Nitrogen concentrations in mature leaves


Nitrogen concentrations in senescent leaves


One-year lifespan leaves


Two-year lifespan leaves



We are grateful to Linhai Li, Yitai Xie and Shun Liu for assistance with fieldwork, Hongzhi Zhang and Yue Hu for assistance with plant analyses and two anonymous reviewers for feedback on the research and manuscript.


  1. Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608CrossRefGoogle Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67Google Scholar
  3. Birk EM, Vitousek PM (1986) Nitrogen availability and nitrogen use efficiency in loblolly pine stands. Ecology 67:69–79CrossRefGoogle Scholar
  4. Cai ZQ, Bongers F (2007) Contrasting nitrogen and phosphorus resorption efficiencies in trees and lianas from a tropical montane rain forest in Xishuangbanna, south-west China. J Trop Ecol 23:115–118CrossRefGoogle Scholar
  5. Carrera AL, Bertiller MB, Sain CL, Mazzarino MJ (2003) Relationship between plant nitrogen conservation strategies and the dynamics of soil nitrogen in the arid Patagonian Monte, Argentina. Plant Soil 255:595–604CrossRefGoogle Scholar
  6. Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annu Rev Ecol Syst 13:229–259CrossRefGoogle Scholar
  7. Chapin I (1991) Integrated responses of plants to stress: a centralized system of physiological responses. Bioscience 41:29–36CrossRefGoogle Scholar
  8. Chen GS, Zeng DH, Chen FS (2004) Concentrations of foliar and surface soil in nutrients Pinus spp. Plantations in relation to species and stand age in Zhanggutai sandy land, northeast China. J For Res 15:11–18CrossRefGoogle Scholar
  9. Cordell S, Goldstein G, Meinzer F, Vitousek P (2001) Regulation of leaf life-span and nutrient-use efficiency of Metrosideros polymorpha trees at two extremes of a long chronosequence in Hawaii. Oecologia 127:198–206CrossRefPubMedGoogle Scholar
  10. Cui K, He CY, Zhang JG, Duan AG, Zeng YF (2012) Temporal and spatial profiling of internode elongation-associated protein expression in rapidly growing culms of bamboo. J Proteome Res 11:2492–2507CrossRefPubMedGoogle Scholar
  11. Di B, Wang ZP (1996) Flora of China (vol 9, section 1). Science Press, BeijingGoogle Scholar
  12. Eckstein R, Karlsson P, Weih M (1999) Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic regions. New Phytol 143:177–189CrossRefGoogle Scholar
  13. England JR, Attiwill PM (2006) Changes in leaf morphology and anatomy with tree age and height in the broadleaved evergreen species Eucalyptus regnans F. Muell Trees 20:79–90CrossRefGoogle Scholar
  14. Escudero A, Mediavilla S (2003) Decline in photosynthetic nitrogen use efficiency with leaf age and nitrogen resorption as determinants of leaf life span. J Ecol 91:880–889CrossRefGoogle Scholar
  15. Escudero A, Arco J, Sanz I, Ayala J (1992) Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90:80–87CrossRefPubMedGoogle Scholar
  16. Fisher JB, Sitch S, Malhi Y, Fisher RA, Huntingford C, Tan SY (2010) Carbon cost of plant nitrogen acquisition: a mechanistic, globally applicable model of plant nitrogen uptake, retranslocation, and fixation. Glob Biogeochem Cycles 24:GB1014. CrossRefGoogle Scholar
  17. Freschet GT, Cornelissen JH, van Logtestijn RS, Aerts R (2010) Substantial nutrient resorption from leaves, stems and roots in a subarctic flora: what is the link with other resource economics traits? New Phytol 186:879–889CrossRefPubMedGoogle Scholar
  18. Hemminga MA, Marbà N, Stapel J (1999) Leaf nutrient resorption, leaf lifespan and the retention of nutrients in seagrass systems. Aquat Bot 65:141–158CrossRefGoogle Scholar
  19. Henderson DE, Jose S (2012) Nutrient use efficiency of three fast growing hardwood species across a resource gradient. Open J For 2:187–199Google Scholar
  20. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24CrossRefGoogle Scholar
  21. Huang JJ, Wang XH, Yan ER (2007) Leaf nutrient concentration, nutrient resorption and litter decomposition in an evergreen broad-leaved forest in eastern China. For Ecol Manag 239:150–158CrossRefGoogle Scholar
  22. Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727CrossRefGoogle Scholar
  23. Kobe RK, Lepczyk CA, Iyer M (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86:2780–2792CrossRefGoogle Scholar
  24. Kozovits A, Bustamante M, Garofalo C, Bucci S, Franco A, Goldstein G, Meinzer F (2007) Nutrient resorption and patterns of litter production and decomposition in a neotropical savanna. Funct Ecol 21:1034–1043CrossRefGoogle Scholar
  25. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379CrossRefPubMedGoogle Scholar
  26. Li R, Werger MJA, During HJ, Zhong ZC (1998) Carbon and nutrient dynamics in relation to growth rhythm in the giant bamboo Phyllostachys pubescens. Plant Soil 201:113–123CrossRefGoogle Scholar
  27. Li ZH, Zhao BY, Zhu ZQ (2003) Species and distribution of mountain bamboos in Shennongjia, central China. J For Res 14:35–38CrossRefGoogle Scholar
  28. Li XF, Zheng XB, Han SJ, Zheng JQ, Li TG (2010) Effects of nitrogen additions on nitrogen resorption and use efficiencies and foliar litterfall of six tree species in a mixed birch and poplar forest, northeastern China. Can J For Res 40:2256–2261CrossRefGoogle Scholar
  29. Li YL, Chen J, Cui JY, Zhao XY, Zhang TH (2013) Nutrient resorption in Caragana microphylla along a chronosequence of plantations: implications for desertified land restoration in North China. Ecol Eng 53:299–305CrossRefGoogle Scholar
  30. Lin YM, Peng ZQ, Lin P (2004) Dynamics of leaf mass, leaf area and element retranslocation efficiency during leaf senescence in Phyllostachys pubescens. Acta Bot Sin 46:1316–1323Google Scholar
  31. Lin YM, Zou XH, Liu JB, Guo ZJ, Lin P, Sonali S (2005) Nutrient, chlorophyll and caloric dynamics of Phyllostachys pubescens leaves in Yongchun County, Fujian, China. J Bamboo Rattan 4:369–385CrossRefGoogle Scholar
  32. Loveless AR (1961) A nutritional interpretation of sclerophylly based on differences in the chemical composition of sclerophyllous and mesophytic leaves. Ann Bot 25:168–184CrossRefGoogle Scholar
  33. Magnani F, Mencuccini M, Borghetti M, Berbigier P, Berninger F, Delzon S, Grelle A, Hari P, Jarvis PG, Kolari P, Kowalski AS, Lankreijer H, Law BE, Lindroth A, Loustau D, Manca G, Moncrieff JB, Rayment M, Tedeschi V, Valentini R, Grace J (2007) The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:849–851CrossRefGoogle Scholar
  34. Makowski D, Wallach D, Meynard JM (2001) Statistical methods for predicting responses to applied nitrogen and calculating optimal nitrogen rates. Agron J 93:531–539CrossRefGoogle Scholar
  35. McConnaughay KDM, Coleman JS (1999) Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80:2581–2593CrossRefGoogle Scholar
  36. Mediavilla S, Herranz M, González-Zurdo P, Escudero A (2013) Ontogenetic transition in leaf traits: a new cost associated with the increase in leaf longevity. J Plant Ecol 7:567–575CrossRefGoogle Scholar
  37. Mediavilla S, García-Iglesias J, González-Zurdo P, Escudero A (2014) Nitrogen resorption efficiency in mature trees and seedlings of four tree species co-occurring in a Mediterranean environment. Plant Soil 385:205–215CrossRefGoogle Scholar
  38. Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29CrossRefGoogle Scholar
  39. Niinemets Ü (2004) Adaptive adjustments to light in foliage and whole-plant characteristics depend on relative age in the perennial herb Leontodon hispidus. New Phytol 162:683–696CrossRefGoogle Scholar
  40. Norby RJ, Long TM, Hartz-Rubin JS, O’Neill EG (2000) Nitrogen resorption in senescing tree leaves in a warmer, CO2-enriched atmosephere. Plant Soil 224:15–29CrossRefGoogle Scholar
  41. Pastor-Pastor A, González-Paleo L, Vilela A, Ravetta D (2015) Age-related changes in nitrogen resorption and use efficiency in the perennial new crop Physaria mendocina (Brassicaceae). Ind Crop Prod 65:227–232CrossRefGoogle Scholar
  42. Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588CrossRefPubMedGoogle Scholar
  43. Pugnaire FI, Chapin FS (1992) Environmental and physiological factors governing nutrient resorption efficiency in barley. Oecologia 90:120–126CrossRefPubMedGoogle Scholar
  44. Quested HM, Cornelissen JHC, Press MC, Callaghan TV, Aerts R, Trosien F, Riemann P, Gwynn-Jones D, Kondratchuk A, Jonasson SE (2003) Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecology 84:3209–3221CrossRefGoogle Scholar
  45. Rejmánková E (2005) Nutrient resorption in wetland macrophytes: comparison across several regions of different nutrient status. New Phytol 167:471–482CrossRefPubMedGoogle Scholar
  46. Shen H, Cao ZH, Xu ZH (2000) Effects of fertilization on different carbon fractions and carbon management index in soils. Acta Pedol Sin 37:166–173Google Scholar
  47. Small E (1972) Photosynthetic rates in relation to nitrogen recycling as an adaptation to nutrient deficiency in peat bog plants. Can J Bot 50:2227–2233CrossRefGoogle Scholar
  48. Soil Survey Staff (1999) United States Department of Agriculture. Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys, 2nd edn. Agriculture Handbook, 436. USDA, Washington, p 869Google Scholar
  49. Stackpoole SM, Workmaster BAA, Jackson RD, Kosola KR (2008) Nitrogen conservation strategies of cranberry plants and ericoid mycorrhizal fungi in an agroecosystem. Soil Biol Biochem 40:2736–2742CrossRefGoogle Scholar
  50. Su WH (2012) Fertilization theory and practice for Phyllostachys pubescens stand based on growth and nutrient accumulation rules. Ph. D. paper, Chinese Academy of ForestryGoogle Scholar
  51. Ueda K (1960) Studies on the physiology of bamboo, with reference to practical application. Bull Kyoto Univ For 30:1–169Google Scholar
  52. Van Heerwaarden L, Toet S, Aerts R (2003) Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4 years of nitrogen fertilization. J Ecol 91:1060–1070CrossRefGoogle Scholar
  53. Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220CrossRefGoogle Scholar
  54. Vitousek P (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572CrossRefGoogle Scholar
  55. Wang ZN, Lu JY, Yang HM, Zhang X, Luo CL, Zhao YX (2014) Resorption of nitrogen, phosphorus and potassium from leaves of lucerne stands of different ages. Plant Soil 383:301–312CrossRefGoogle Scholar
  56. Wang CY, Zhou JW, Xiao HG, Liu J, Wang L (2015) Variations in leaf functional traits among plant species grouped by growth and leaf types in Zhenjiang, China. J For Res 28:241–248CrossRefGoogle Scholar
  57. Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19CrossRefGoogle Scholar
  58. Wu JS, Zhou GM, Xiu QF, Yang F (2005) Spatial distribution of nutrition element and its relationship with sojl nutrients in diferent years of Phyllostachys pubescens. Sci Silvae Sin 41:171–173Google Scholar
  59. Yasumura Y, Hikosaka K, Matsui K, Hirose T (2002) Leaf-level nitrogen-use efficiency of canopy and understorey species in a beech forest. Funct Ecol 16:826–834CrossRefGoogle Scholar
  60. Yen T-M, Lee J-S (2011) Comparing aboveground carbon sequestration between moso bamboo (Phyllostachys heterocycla) and China fir (Cunninghamia lanceolata) forests based on the allometric model. For Ecol Manag 261:995–1002CrossRefGoogle Scholar
  61. Yoshida S, Forno DA, Cock J (1971) Laboratory manual for physiological studies of rice. The International Rice Research Institute, PhiliphinesGoogle Scholar
  62. Yuan ZY, Chen HYH (2009) Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Glob Ecol Biogeogr 18:11–18CrossRefGoogle Scholar
  63. Yuan ZY, Chen HYH (2010) Changes in nitrogen resorption of trembling aspen (Populus tremuloides) with stand development. Plant Soil 327:121–129CrossRefGoogle Scholar
  64. Yuan ZY, Li LH, Han XG, Huang JH, Jiang GM, Wan SQ, Zhang WH, Chen QS (2005) Nitrogen resorption from senescing leaves in 28 plant species in a semi-arid region of northern China. J Arid Environ 63:191–202CrossRefGoogle Scholar
  65. Yuan ZY, Li LH, Han XG, Chen SP, Wang ZW, Chen QS, Bai WM (2006) Nitrogen response efficiency increased monotonically with decreasing soil resource availability: a case study from a semiarid grassland in northern China. Oecologia 148:564–572CrossRefPubMedGoogle Scholar
  66. Zhang CS, Xie GD, Fan SH, Zhen L (2010) Variation in vegetation structure and soil properties, and the relation between understory plants and environmental variables under different phyllostachys pubescens forests in southeastern china. Environ Manag 45:779–792CrossRefGoogle Scholar
  67. Zhou FC (1989) Harvest of bamboo groves. J Bamboo Res 1:156–161Google Scholar

Copyright information

© Northeast Forestry University and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Changshun Zhang
    • 1
  • Chunlan Liu
    • 2
  • Wenyuan Zhang
    • 3
  • Gaodi Xie
    • 1
  • Shaohui Fan
    • 4
  • Na Li
    • 5
  1. 1.Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingPeople’s Republic of China
  2. 2.Beijing Municipal Research Institute of Environmental ProtectionBeijingPeople’s Republic of China
  3. 3.College of Landscape and ArtJiangxi Agricultural UniversityNanchangPeople’s Republic of China
  4. 4.International Centre for Bamboo and RattanBeijingPeople’s Republic of China
  5. 5.University of Chinese Academy of SciencesBeijingPeople’s Republic of China

Personalised recommendations