Stoichiometric patterns in foliar nutrient resorption across multiple scales

New Phytologist

Volumn 196, Issue 1, 2012, Pages 173-180

  Reed, Sasha C ^a   Townsend, Alan R ^b   Davidson, Eric A ^c   Cleveland, Cory C ^d  

^a U S GEOLOGICAL SURVEY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c WOODS HOLE RESEARCH CENTER   (United States)

^d UNIVERSITY OF MONTANA   (United States)

Author keywords

Forest succession; Net primary production; Nitrogen; Nutrient limitation; Phosphorus; Resorption; Stoichiometry; Tropical rain forest

Indexed keywords

NITROGEN; PHOSPHORUS; RAIN;

ABSCISSION; GLOBAL CHANGE; LEAF; NET PRIMARY PRODUCTION; NITROGEN; NUTRIENT LIMITATION; PHOSPHORUS; RAINFOREST; REGENERATION; RESORPTION; STOICHIOMETRY; SUCCESSION; TERRESTRIAL ECOSYSTEM; TROPICAL FOREST;

ARTICLE; BRAZIL; ECOSYSTEM; METABOLISM; PLANT LEAF; SOIL; SPECIES DIFFERENCE; TEMPERATURE; TREE; TROPIC CLIMATE;

BRAZIL; ECOSYSTEM; NITROGEN; PHOSPHORUS; PLANT LEAVES; RAIN; SOIL; SPECIES SPECIFICITY; TEMPERATURE; TREES; TROPICAL CLIMATE;

COSTA RICA;

EID: 84865547637     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04249.x     Document Type: Article

References (88)

1. Aerts R. 1990. Nutrient use efficiency in evergreen and deciduous species from heathlands. Oecologia 84: 391-397.
2. Aerts R. 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84: 597-608.
3. Aerts R. 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79: 439-449.
4. Aerts R, Chapin FS III. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30: 1-67.
5. Aerts R, Cornelissen JHC, van Logtestijin RSP, Callaghan TV. 2007. Climate change has only a minor impact on nutrient resorption parameters in a high-latitude peatland. Oecologia 151: 132-139.
6. Berendse F, Aerts R. 1987. Nitrogen-use-efficiency: a biologically meaningful definition? Functional Ecology 1: 293-296.
7. Bern CR, Townsend AR, Farmer GL. 2005. Unexpected dominance of parent material strontium in a tropical forest on highly weathered soils. Ecology 86: 626-632.
8. Berrange JP, Thorpe RS. 1988. The geology, geochemistry and emplacement of the Cretaceous Tertiary ophiolitic Nicoya complex of the Osa Peninsula, southern Costa Rica. Tectonophysics 147: 193-199.
9. Bowman WD. 1994. Accumulation and use of nitrogen and phosphorus following fertilization in two alpine tundra communities. Oikos 70: 261-270.
10. Chapin FS III. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11: 233-260.
11. Chapin FS III, Shaver GR. 1989. Differences in growth and nutrient use among arctic plant growth forms. Functional Ecology 3: 73-80.
12. 15nitrogen in shortgrass prairie. Ecology 58: 1322-1333.
13. Cleveland CC, Townsend AR. 2006. Nutrient additions to a tropical rain forest drive substantial carbon dioxide losses to the atmosphere. Proceedings of the National Academy of Sciences, USA 104: 10316-10321.
14. Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante MMC, Chuyong G, Dobrowski SZ, Grierson P, Harms KE, Houlton BZ et al. 2011. Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecology Letters 14: 1313-1317.
15. Currie WS. 2003. Relationships between carbon turnover and bioavailable energy fluxes in two temperate forest soils. Global Change Biology 9: 919-929.
16. Davidson EA, de Araújo AC, Artaxo P, Balch JK, Brown IF, Bustamante MMC, Coe MT, DeFries RS, Keller M, Longo M et al. 2012. The Amazon basin in transition. Nature 481: 321-328.
17. Davidson EA, de Carvalho CJR, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Sabá RT, Hayashi NS, Leal EC, Vieria IC et al. 2007. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447: 995-998.
18. 2O in a seasonally dry tropical forest. Ecology 74: 130-139.
19. Elser JJ, Bracken MES, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10: 1135-1142.
20. Enoki T, Kawaguchi H. 1999. Nitrogen resorption from needles of Pinus thunbergii Parl. growing along a topographic gradient of soil nutrient availability. Ecological Research 14: 1-8.
21. Franklin O, Ågren GI. 2002. Leaf senescence and resorption as mechanisms of maximizing photosynthetic production during canopy development at N limitation. Functional Ecology 16: 727-733.
22. Gosz JR, Likens GE, Bormann FH. 1976. Organic matter and nutrient dynamics of the forest and the forest floor in the Hubbard Brook Forest. Oecologia 22: 305-320.
23. Grime JP. 1979. Plant strategies and vegetation processes. Chichester, UK: Wiley.
24. Güsewell S. 2004. N:P ratios in terrestrial plants: variation and functional significance. New Phytologist 164: 243-266.
25. Güsewell S, Koerselman W. 2003. Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology, Evolution and Systematics 5: 37-61.
26. Güsewell S, Koerselman W, Verhoeven JTA. 2002. Time-dependent effects of fertilization in Dutch floating fens. Journal of Vegetation Science 13: 705-718.
27. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB et al. 2011. Nutrient co-limitation of primary producer communities. Ecology Letters 14: 852-862.
28. He H, Bleby TM, Veneklaas EJ, Lambers H. 2011. Dinitrogen-fixing Acacia species from phosphorus-impoverished soils resorb leaf phosphorus efficiently. Plant, Cell & Environment 34: 2060-2070.
29. Hedin LO, Brookshire ENJ, Menge DNL, Barron AR. 2009. The nitrogen paradox in tropical forest ecosystems. Annual Review of Ecology, Evolution and Systematics 40: 613-635.
30. Hedin LO, Vitousek PM, Matson PA. 2003. Nutrient losses over four million years of tropical forest development. Ecology 84: 2231-2255.
31. Holdridge LR, Grenke WC, Hatheway WH, Lian T, Tosi JA. 1971. Forest environments in tropical life zones: a pilot study. Oxford, UK: Oxford Pergamon Press.
32. 2 elicits long-term decline in nitrogen fixation. Science 304: 1291.
33. Jackson RB, Mooney HA, Schulze ED. 1997. A global budget for fine root biomass, surface area, and nutrient concentrations. Proceedings of the National Academy of Sciences, USA 94: 7362-7366.
34. John RJ, Dalling W, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M et al. 2007. Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences, USA 104: 864-869.
35. Kappelle M, Castro M, Acevedo H, Gonzalez L, Monge H. 2002. Ecosystems of the Osa Conservation Area (ACOSA). Santo Domingo de Heredia, Costa Rica: Instituto Nacional Biodiversidad (INBio).
36. Killingbeck KT. 1984. Nitrogen and phosphorus resorption dynamics of five tree species in a Kansas gallery forest. American Midland Naturalist 111: 155-164.
37. Killingbeck KT. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77: 1716-1727.
38. Killingbeck KT, May JD, Nyman S. 1990. Foliar senescence in an aspen (Populus tremuloides) clone: the response of element resorption to interramet variation and timing of abscission. Canadian Journal of Forest Research 20: 1156-1164.
39. Kitayama K, Aiba SI, Takyu M, Majalap N, Wagai R. 2004. Soil phosphorus fractionation and phosphorus-use efficiency of a Bornean tropical montane rain forest during soil aging with podzolization. Ecosystems 2004: 259-274.
40. Kobe RK, Lepczyk CA, Iyer M. 2005. Resorption efficiency decreases with increasing green leaf nutrients in a global dataset. Ecology 86: 2780-2792.
41. Koerselman W, Meuleman AFM. 1996. The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology 33: 1441-1450.
42. Kuo S. 1996. Phosphorus. Sparks DL, ed. Methods of soil analysis. Part 3: chemical methods. Madison, WI, USA: Soil Society of America, 3.
43. Lajtha K, Klein M. 1988. The effect of varying nitrogen and phosphorus availability on nutrient use by Larrea tridentata, a desert evergreen shrub. Oecologia 75: 348-353.
44. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklass EJ. 2006. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98: 693-713.
45. LeBauer DS, Treseder KK. 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89: 371-379.
46. Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K. 1999. Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46: 45-65.
47. May JD, Killingbeck KT. 1992. Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology 73: 1868-1878.
48. McGroddy ME, Daufresne T, Hedin LO. 2004. Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology 85: 2390-2401.
49. Melillo JM, Aber JD, Muratore JF. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63: 621-626.
50. Miller HG. 1995. The influence of stand development on nutrient demand, growth and allocation. Plant and Soil 168-169: 225-232.
51. Moore B, Braswell BH. 1994. Planetary metabolism: understanding the carbon-cycle. Ambio 23: 4-12.
52. 2-enriched sweetgum forest. Ecology 87: 5-14.
53. 2-enriched atmosphere. Plant and Soil 224: 15-29.
54. Nye PH. 1961. Organic matter and nutrient cycles under moist tropical forest. Plant and Soil 13: 333-345.
55. Oleksyn J, Reich PB, Zytkowaik R, Karolewski P, Tjoelker MG. 2003. Nutrient conservation increases with latitude of origin in European Pinus sylvestris populations. Oecologia 136: 220-235.
56. Ordoñez J, Van Bodegom PM, Witte J-PM, Wright IJ, Reich PB, Aerts R. 2008. A global study of relationships between leaf traits, climate and soil measurements of nutrient fertility. Global Ecology and Biogeography 18: 137-149.
57. Ostertag R. 2010. Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant and Soil 334: 85-98.
58. Oyarzabal M, Paruelo JM, Del Pino F, Oesterheld M, Lauenroth WK. 2008. Trait differences between grass species along a climatic gradient in South and North America. Journal of Vegetation Science 19: 183-192.
59. Pugnaire FI, Chapin FS. 1993. Controls over nutrient resorption from leaves of evergreen Mediterranean species. Ecology 74: 124-129.
60. Reed SC, Cleveland CC, Townsend AR. 2007. Controls over leaf litter and soil nitrogen fixation in two lowland tropical rain forests. Biotropica 39: 585-592.
61. Reed SC, Cleveland CC, Townsend AR. 2008. Tree species control rates of free-living nitrogen fixation in a tropical rain forest. Ecology 89: 2924-2934.
62. Reed SC, Cleveland CC, Townsend AR. 2011a. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annual Review of Ecology, Evolution, and Systematics 42: 489-512.
63. Reed SC, Vitousek PM, Cleveland CC. 2011b. Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106: 323-336.
64. Reich PB. 2011. Taking stock of forest carbon. Nature Climate Change 1: 346-347.
65. Reich PB, Oleksyn J. 2004. Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences, USA 101: 11001-11006.
66. Richardson SJ, Allen RB, Doherty JE. 2008. Shifts in leaf N:P ratio during resorption reflect soil P in temperate rainforest. Functional Ecology 22: 738-745.
67. Richardson SJ, Peltzer DA, Allen RB, McGlone MS, Parfitt RL. 2004. Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139: 267-276.
68. Robertson GP, Wedin D, Groffman PM, Blair JM, Holland EM, Nadelhoffer KJ, Harris D. 1999. Soil carbon and nitrogen availability: nitrogen mineralization and soil respiration potentials. Robertson GP, Coleman DC, Bledsoe CS, Sollins P, eds. Standard methods of long-term ecological research. New York, NY, USA: Oxford University Press, 258-271.
69. Sollins P. 1998. Factors influencing species composition in tropical lowland rain forest: does soil matter? Ecology 79: 23-30.
70. Stachurski A, Zimka JR. 1975. Methods of studying forest ecosystems: leaf area, leaf production, and withdrawal of nutrients from leaves of trees. Ekologia Polska 23: 637-648.
71. Tessier JT, Raynal DJ. 2003. Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. Journal of Applied Ecology 40: 523-534.
72. Thornton PE, Doney SC, Lindsay K, Moore JK, Mahowald NM, Randerson JT, Fung IY, Lamarque JF, Feddema JJ, Lee YH. 2009. Carbon-nitrogen interactions regulate climate-carbon cycle feedbacks: results from an atmosphere-ocean general circulation model. Biogeosciences 6: 2099-2120.
73. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC. 2007. Controls over foliar N:P ratios in tropical rain forests. Ecology 88: 107-118.
74. Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC. 2011. Multi-element regulation of the tropical forest carbon cycle. Frontiers in Ecology and Environment 9: 9-17.
75. Turner J. 1977. Effects of nitrogen availability on nitrogen cycling in a Douglas fir stand. Forest Science 23: 307-316.
76. Van Heerwaarden LM, Toet S, Aerts R. 2003a. Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101: 664-669.
77. Van Heerwaarden LM, Toet S, Aerts R. 2003b. Nitrogen and phosphorus resorption efficiency and proficiency in six sub-arctic bog species after 4years of nitrogen fertilization. Journal of Ecology 91: 1060-1070.
78. Vergutz L, Manzoni S, Porporato A, Novai RF, Jackson RB. 2012. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecological Monographs 82: 205-220.
79. Vitousek P. 1982. Nutrient cycling and nutrient use efficiency. American Naturalist 119: 553-572.
80. Vitousek P, Hobbie S. 2000. Heterotrophic nitrogen fixation in decomposing litter: patterns, mechanisms, and models. Ecology 75: 418-429.
81. Vitousek PM. 1984. Litterfall, nutrient cycling, and nutrient limitations in tropical forests. Ecology 65: 285-298.
82. Vitousek PM. 1998. Foliar and litter nutrients, nutrient resorption, and decomposition in the Hawaiian Metrosideros polymorpha. Ecosystems 1: 401-407.
83. Vitousek PM, Farrington H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37: 63-75.
84. Vitousek PM, Porder S, Houlton BZ, Chadwick OA. 2010. Terrestrial phosphorus limitation: mechanisms, implications and nitrogen-phosphorus interactions. Ecological Applications 20: 5-15.
85. Vitousek PM, Sanford RL Jr. 1986. Nutrient cycling in moist tropical forests. Annual Review of Ecology and Systematics 17: 137-167.
86. Wieder WR, Cleveland CC, Townsend AR. 2009. Controls over leaf litter decomposition in wet tropical forests. Ecology 90: 3333-3341.
87. Wood TE, Cavaleri MA, Reed SC. 2012. Tropical forest carbon balance in a warmer world: a critical review spanning microbial-to-ecosystem-scale processes. Biological Reviews. doi: 10.1111/j.1469-185X.2012.00232.x
88. Yuan ZY, Chen HYH. 2009. Global-scale patterns of nutrient resorption associated with latitude, temperature and precipitation. Global Ecology and Biogeography 18: 11-18.