Leaf nitrogen and phosphorus resorption of woody species in response to climatic conditions and soil nutrients: a meta-analysis

Abstract

Nutrient resorption before abscission is an important nutrient conservation mechanism regulated by climatic conditions and soil nutrients. However, our current understanding of leaf nutrient resorption is primarily derived from site-specific studies or from the use of green-leaf nutrient concentrations to represent those in soils. It remains unknown how nutrient resorption responds to natural soil-nutrient concentrations at a global scale. The effects of plant functional groups, climatic conditions, and soil nutrients and their interactions on leaf nutrient resorption are also unknown. In this study, we established a global database derived from 85 published papers, including 547 reports of nitrogen and phosphorus resorption efficiency (NRE and PRE), climatic factors (LAT, latitude; MAT, mean annual temperature; MAP, mean annual precipitation) and soil-nutrient data (STN, soil total nitrogen; STP, soil total phosphorus) across 111 research sites. The results demonstrated that mean NRE and PRE were 48.4 and 53.3%, respectively. NRE of trees was lower than those of shrubs. NRE and PRE of coniferous species were both higher than those of broad-leaved species. Evergreen species had higher PRE than did deciduous species. NRE was negatively related to STN, but PRE and STP were not related. Both NRE and PRE decreased with increasing MAT and MAP but increased with increasing LAT. Plant functional groups, climate and soil nutrients jointly explained 22 and 32% of the variations in NRE and PRE, respectively. It is important to note that climate (especially MAT) explained 12 and 29% of the variations in NRE and PRE, respectively, implying that continuing global warming will exert an increasingly profound influence on plant nutrient cycles.

Keywords

Global / Climate change / Nutrient resorption efficiency / Tree / Shrub

References

[1] Aerts R. Nutrient resorption from senescing leaves of perennials: are there general patterns?. J Ecol, 1996, 84: 597-608.

[2] Aerts R. Nitrogen partitioning between resorption and decomposition pathways: a trade-off between nitrogen use efficiency and litter decomposability?. Oikos, 1997, 80: 603-606.

[3] Aerts R, Chapin FS. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res, 2000, 30: 1-67.

[4] Brant AN, Chen HYH. Patterns and mechanisms of nutrient resorption in plants. Crit Rev Plant Sci, 2015, 34: 471-486.

[5] Chapin FS, Oechel WC. Photosynthesis, respiration, and phosphate absorption by Carex aquatilis ecotypes along latitudinal and local environmental gradients. Ecology, 1983, 64: 743-751.

[6] Chen YH, Han WX, Tang LY, Tang ZL, Fang JY. Leaf nitrogen and phosphorus concentrations of woody plants differ in responses to climate, soil and plant growth form. Ecography, 2013, 36: 178-184.

[7] Cramer MD, Hawkins HJ, Verboom GA. The importance of nutritional regulation of plant water flux. Oecologia, 2009, 161: 15-24.

[8] Escudero A, del Arco JM, Sanz IC, Ayala J. Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia, 1991, 90: 80-87.

[9] Freschet GT, Aerts R, Cornelissen JHC. A plant economics spectrum of litter decomposability. Funct Ecol, 2012, 26: 56-65.

[10] Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, Hillier SH, Hodkinson DJ, Jalili A, Liu Z, Mackey JML, Matthews N, Mowforth MA, Neal AM, Reader RJ, Reiling K, Ross-Fraser W, Spencer RE, Sutton F, Tasker DE, Thorpe PC, Whitehouse J. Integrated screening validates primary axes of specialisation in plants. Oikos, 1997, 79: 259-281.

[11] Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH. Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett, 2011, 14: 788-796.

[12] Han WX, Chen YH, Zhao FJ, Tang LY, Jiang RF, Zhang FS. Floral, climatic and soil pH controls on leaf ash content in China’s terrestrial plants. Glob Ecol Biogeogr, 2012, 21: 376-382.

[13] Han WX, Tang LY, Chen YH, Fang JY. Relationship between the relative limitation and resorption efficiency of nitrogen vs phosphorus in woody plants. PLoS ONE, 2013, 8: e83366.

[14] Hayes P, Turner BL, Lambers H, Laliberté E. Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol, 2014, 102: 396-410.

[15] Heikkinen R, Luoto M, Kuussaari M, Pöyry J. New insights into butterfly-environment relationships using partitioning methods. Proc Biol Sci, 2005, 272: 2203-2210.

[16] Hidaka A, Kitayama K. Allocation of foliar phosphorus fractions and leaf traits of tropical tree species in response to decreased soil phosphorus availability on Mount Kinabalu, Borneo. J Ecol, 2011, 99: 849-857.

[17] Huang JJ, Boerner REJ. Effects of fire alone or combined with thinning on tissue nutrient concentrations and nutrient resorption in Desmodium nudiflorum. Oecologia, 2007, 153: 233-243.

[18] Killingbeck KT. Nutrients in senesced leaves keys to the search for potential resorption and resorption proficiency. Ecology, 1996, 77: 1716-1727.

[19] Kobe RK, Lepczyk CA, Iyer M. Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology, 2005, 86: 2780-2792.

[20] Körner C. Alpine plant life: functional plant ecology of high mountain ecosystems, 1999, Berlin: Springer 1 338

[21] Lambers H, Chapin FS, Pons TL. Plant physiological ecology, 2008 2 New York: Springer 212 546

[22] Lü XT, Freschet GT, Flynn DFB, Han XG. Plasticity in leaf and stem nutrient resorption proficiency potentially reinforces plant–soil feedbacks and microscale heterogeneity in a semi-arid grassland. J Ecol, 2012, 100: 144-150.

[23] Maire V, Wright IJ, Prentice C, Batjes NH, Bhaskar R, van Bodegom PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A, Reich PB, Santiago LS. Global effects of soil and climate on leaf photosynthetic traits and rates. Glob Ecol Biogeogr, 2015, 24: 706-717.

[24] Oleksyn J, Reich PB, Zytkowiak R, Karolewski P, Tjoelker MG. Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations. Oecologia, 2003, 136: 220-235.

[25] Ordoñez JC, van Bodegom PM, Witte JPM, Wright IJ, Reich PB, Aerts R. A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Glob Ecol Biogeogr, 2009, 18: 137-149.

[26] Pan RC, Wang XJ, Li NH. Plant physiology, 2010, Beijing: Higher Education Press 14 24

[27] R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/

[28] Reed SC, Townsend AR, Davidson EA, Cleveland CC. Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol, 2012, 196: 173-180.

[29] Reich PB, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA, 2004, 101: 11001-11006.

[30] Robinson CH. Controls on decomposition and soil nitrogen availability at high latitudes. Plant Soil, 2002, 242: 65-81.

[31] Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE. Persistence of soil organic matter as an ecosystem property. Nature, 2011, 478: 48-56.

[32] Sun X, Kang H, Chen HYH, Björn B, Samuel BF, Liu C. Biogeographic patterns of nutrient resorption from Quercus variabilis Blume leaves across China. Plant Biol, 2016, 18: 505-513.

[33] Tang LY, Han WX, Chen YH, Fang JY. Resorption proficiency and efficiency of leaf nutrients in woody plants in eastern China. J Plant Ecol, 2013, 6: 408-417.

[34] Tully KL, Wood TE, Schwantes AM, Lawrence D. Soil nutrient availability and reproductive effort drive patterns in nutrient resorption in Pentaclethra macroloba. Ecology, 2013, 94: 930-940.

[35] van Heerwaarden LM, Toet S, Aerts R. Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos, 2003, 101: 664-669.

[36] Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr, 2012, 82: 205-220.

[37] Viers J, Prokushkin AS, Pokrovsky OS, Auda Y, Kirdyanov AV, Beaulieu E, Zouiten C, Oliva P, Dupré B. Seasonal and spatial variability of elemental concentrations in boreal forest larch foliage of Central Siberia on continuous permafrost. Biogeochemistry, 2013, 113: 435-449.

[38] Wright IJ, Westoby M. Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol, 2003, 17: 10-19.

[39] Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R. The worldwide leaf economics spectrum. Nature, 2004, 428: 821-827.

[40] Yan T, Lü XT, Yang K, Zhu JJ. Leaf nutrient dynamics and nutrient resorption: a comparison between larch plantations and adjacent secondary forests in Northeast China. J Plant Ecol, 2016, 9: 165-173.

[41] Yuan ZY, Chen YH. Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Global Ecol Biogeogr, 2009, 18: 11-18.

[42] Yuan ZY, Chen YH. Negative effects of fertilization on plant nutrient resorption. Ecology, 2015, 96: 373-380.

[43] Yuan ZY, Li LH, Han XG, Huang JH, Wan SQ. Foliar nitrogen dynamics and nitrogen resorption of a sandy shrub Salix gordejevii in northern China. Plant Soil, 2005, 278: 183-193.

[44] Zhang SB, Zhang JL, Slik JWF, Cao KF. Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Glob Ecol Biogeogr, 2012, 21: 809-818.

[45] Zhang JH, Tang ZY, Luo YK, Chi XL, Chen YH, Fang JY, Shen HH. Resorption efficiency of leaf nutrients in woody plants on Mt. Dongling of Beijing, North China. J Plant Ecol, 2015, 8: 530-538.