Tropical Andean Forests Are Highly Susceptible to Nutrient Inputs-Rapid Effects of Experimental N and P Addition to an Ecuadorian Montane Forest

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Homeier, Jürgen ^a   Hertel, Dietrich ^a   Camenzind, Tessa ^b   Cumbicus, Nixon L ^c   Maraun, Mark ^d   Martinson, Guntars O ^d,e   Poma, L Nohemy ^f   Rillig, Matthias C ^b   Sandmann, Dorothee ^d   Scheu, Stefan ^d   Veldkamp, Edzo ^d   Wilcke, Wolfgang ^g   Wullaert, Hans ^h   Leuschner, Christoph ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSIDAD TÉCNICA PARTICULAR DE LOJA   (Ecuador)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^f Universidad National de Loja   (Ecuador)

^g UNIVERSITY OF BERN   (Switzerland)

^h JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; PHOSPHORUS;

ARTICLE; BIOMASS; ECOSYSTEM; ECUADOR; ECUADORIAN MONTANE RAIN FOREST; FINE ROOT BIOMASS; LITTER FALL; MICROBIAL BIOMASS; NONHUMAN; NUTRIENT CYCLING; NUTRIENT DYNAMICS; NUTRIENT LOADING; PLANT GROWTH; PLANT LEAF; PRODUCTIVITY; SOIL FERTILITY; SPECIES COMPOSITION; SPECIES DIVERSITY; STEM GROWTH; TROPICAL ANDEAN FOREST; TROPICAL RAIN FOREST;

BIOMASS; ECOSYSTEM; ECUADOR; FERTILIZERS; NITROGEN; PHOSPHORUS; PLANT LEAVES; PLANT ROOTS; SOIL; TREES; TROPICAL CLIMATE;

EID: 84867363686     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047128     Document Type: Article

References (82)

1. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, et al. (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320: 889-892.
2. Gruber N, Galloway N, (2008) An earth-system perspective of the global nitrogen cycle. Nature 451: 293-296.
3. Janssens IA, Dieleman W, Luyssaert S, Subke J-A, Reichstein M, et al. (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3: 315-322.
4. Mahowald NM, Artaxo P, Baker AR, Jickells TD, Okin GS, et al. (2005) Impacts of biomass burning emissions and land use change on Amazonian atmospheric phosphorus cycling and deposition. Global Biogeochem Cycles 19: GB4030.
5. Schlesinger WH, (2009) On the fate of anthropogenic nitrogen. Proc Natl Acad Sci U S A 106: 203-208.
6. Tilman D, Fargione J, Wolff B, D'Antonio C, Dobson A, et al. (2001) Forecasting agriculturally driven global environmental change. Science 292: 281-284.
7. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, et al. (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20: 30-59.
8. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, et al. (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10: 1135-1142.
9. Reay DS, Dentener F, Smith P, Grace J, Feely RA, (2008) Global nitrogen deposition and carbon sinks. Nat Geosci 1: 430-437.
10. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, et al. (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14: 852-862.
11. Hedin LO, Brookshire ENJ, Menge DNL, Barron A, (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol Syst 40: 613-635.
12. LeBauer DS, Treseder KK, (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89: 371-379.
13. Vitousek PM, Porder S, Houlton BZ, Chadwick OA, (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20: 5-15.
14. Xia J, Wan S, (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179: 428-439.
15. Bedison JE, McNeill BE, (2009) Is the growth of temperate forest trees enhanced along an ambient nitrogen deposition gradient? Ecology 90: 1736-1742.
16. Wright RF, Rasmussen L, (1998) Introduction to the NITREX and EXMAN projects. For Ecol Manage 101: 1-7.
17. Stevens CJ, Dise NB, Mountford JO, Gowing DJ, (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303: 1876-1879.
18. Högberg P, Fan H, Quist M, Binkley D, Tamm CO, (2006) Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob Chang Biol 12: 489-499.
19. Bouwman L, Goldewijka KK, Van Der Hoek KW, Beusena AHW, Van Vuurena DP, et al. (in press) Exploring global changes in nitrogen and phosphorus cycles in agriculture induced by livestock production over the 1900-2050 period. Proc Natl Acad Sci U S A doi: 10.1073/pnas.1012878108.
20. Phoenix G, Hicks WK, Cinderby S, Kuylenstierna JCI, Stocks WD, et al. (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12: 470-476.
21. Tamatamah RA, Hecky RE, Duthie HD, (2005) The atmospheric deposition of phosphorus in Lake Victoria (East Africa). Biogeochemistry 73: 325-344.
22. Okin GS, Mahowald N, Chadwick OA, Artaxo P, (2004) Impact of desert dust on the biogeochemistry of phosphorus in terrestrial ecosystems. Global Biogeochem Cycles 18: 1-14.
23. Pett-Ridge JC, (2009) Contributions of dust to phosphorus cycling in tropical forests of the Luquillo Mountains, Puerto Rico. Biogeochemistry 94: 63-80.
24. Fabian P, Kohlpaintner M, Rollenbeck R, (2005) Biomass burning in the Amazon - fertilizer for the mountaineous rain forest in Ecuador. Environ Sci Pollut Res Int 12: 290-296.
25. Boy J, Rollenbeck R, Valarezo C, Wilcke W, (2008) Amazonian biomass burning-derived acid and nutrient deposition in the north Andean montane forest of Ecuador. Global Biogeochem Cycles 22: GB4011.
26. Matson PA, McDowell WH, Townsend AR, Vitousek PM, (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46: 67-83.
27. Corre MD, Veldkamp E, Arnold J, Wright SJ, (2010) Impact of elevated N input on N cycling and retention of soils under old-growth lowland and montane forests in Panama. Ecology 91: 1715-1729.
28. Hall SJ, Matson PA, (2003) Nutrient status of tropical rain forests influences soil N dynamics after N addition. Ecol Monogr 73: 107-129.
29. Lewis SL, Malhi Y, Phillips OL, (2004) Fingerprinting the impacts of global change on tropical forests. Phil Trans R Soc Lond B Biol Sci 359: 437-462.
30. Li Y, Xu M, Zou X, (2006) Effects of nutrient additions on ecosystem carbon cycle in a Puerto Rican tropical wet forest. Glob Chang Biol 12: 284-293.
31. Wright SJ, (2005) Tropical forests in a changing environment. Trends Ecol Evol 20: 553-560.
32. Adamek M, Corre MD, Hölscher D, (2009) Early effect of elevated nitrogen input on above-ground net primary production of a lower montane rain forest, Panama. J Trop Ecol 25: 637-647.
33. Cavelier J, Tanner E, Santamaria J, (2000) Effect of water, temperature and fertilizers on soil nitrogen net transformations and tree growth in an elfin cloud forest of Colombia. J Trop Ecol pp. 83-99.
34. Tanner EVJ, Kapos V, Freskos S, Healey JR, Theobald AM, (1990) Nitrogen and phosphorus fertilization of Jamaican montane forest trees. J Trop Ecol 6: 231-238.
35. Tanner EVJ, Kapos V, Franco W, (1992) Nitrogen and phosphorus fertilization effects on Venezuelan montane forest trunk growth and litterfall. Ecology 73: 78-86.
36. Mirmanto E, Proctor J, Green J, Nagy L, (1999) Suriantata (1999) Effects of nitrogen and phosphorus fertilization in a lowland evergreen rainforest. Phil Trans R Soc Lond B Biol Sci 354: 1825-1829.
37. Nomura N, Kikuzawa K, (2003) Productive phenology of tropical montane forests: Fertilization experiments along a moisture gradient. Ecol Res 18: 573-586.
38. Ostertag R, (2010) Foliar nitrogen and phosphorus accumulation responses after fertilization: an example from nutrient-limited Hawaiian forests. Plant Soil 334: 85-98.
39. Vitousek PM, Farrington H, (1997) Nutrient limitation and soil development: Experimental test of a biogeochemical theory. Biogeochemistry 37: 63-75.
40. Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, et al. (2011) Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92: 1616-1625.
41. Wilcke W, Yasin S, Abramowski U, Valarezo C, Zech W, (2002) Nutrient storage and turnover in organic layers under tropical montane rain forest in Ecuador. Europ J Soil Sci 53: 15-27.
42. Treseder KK, (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11: 1111-1120.
43. Fog K, (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63: 433-462.
44. Lu M, Yang Y, Luo Y, Fang C, Zhou X, et al. (2011) Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phytol 189: 1040-1050.
45. Lohse KA, Matson P, (2005) Consequences of nitrogen additions for soil losses from wet tropical forests. Ecol Appl 15 (5) (): 1629-1648.
46. Matzner E, Zuber T, Lischeid G (2004) Response of soil solution chemistry and solute fluxes to changing deposition rates. In: Matzner E, editor. Biogeochemstry of forested catchments in a changing environment- A German case study. Ecological Studies Vol 172. Berlin: Springer. pp. 339-360.
47. Goller R, Wilcke W, Fleischbein K, Valarezo C, Zech W, (2006) Dissolved nitrogen, phosphorus, and sulfur forms in the ecosystem fluxes of a montane forest in Ecuador. Biogeochemistry 77: 57-89.
48. Wullaert H, Homeier J, Valarezo C, Wilcke W, (2010) Response of the N and P cycles of an old-growth montane forest in Ecuador to experimental low-level N and P amendments. For Ecol Manage 260: 1434-1445.
49. Wieder WR, Cleveland CC, Townsend AR, (2009) Controls over leaf litter decomposition in wet tropical forests. Ecology 90: 3333-3341.
50. Cleveland CC, Townsend AR, (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci U S A 103: 10316-10321.
51. Treseder KK, Vitousek PM, (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82: 946-954.
52. Gress SE, Nichols TD, Northcraft CC, Peterjohn W, (2007) Nutrient limitation in soils exhibiting differing nitrogen availabilities: what lies beyond nitrogen saturation? Ecology 88: 119-130.
53. Olander LP, Vitousek PM, (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49: 175-190.
54. Poorter L, Bongers F, (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87: 1733-1743.
55. Vitousek PM, Walker LR, Whiteaker LD, Matson PA, (1993) Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23: 197-215.
56. Güsewell S, Gessner MO, (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23: 211-219.
57. Cusack DF, Silver WL, Torn MS, McDowell WH, (2011) Effects of nitrogen additions on above- and belowground carbon dynamics in two tropical forests. Biogeochemistry 104: 203-225.
58. Gower ST, Vitousek PM, (1989) Effects of nutrient amendments on fine root biomass in a primary successional forest in Hawai'i. Oecologia 81: 566-568.
59. Nadelhoffer KJ, (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147: 131-139.
60. Yuan ZY, Chen HYH, (2012) A global analysis of fine root production as affected by soil nitrogen and phosphorus. Proc R Soc Lond B Biol Sci 279: 3796-3802.
61. Johnson NC, Rowland DL, Corkidi L, Allen EB, (2008) Plant winners and losers during grassland N-eutrophication differ in biomass allocation and mycorrhizas. Ecology 89: 2868-2878.
62. Treseder KK, (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164: 347-355.
63. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, et al. (2009) Phylogenetic trait conservatism and the evolution of functional tradeoffs in arbuscular mycorrhizal fungi. Proc R Soc Lond B Biol Sci 276: 4237-4245.
64. Vitousek PM, (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65: 285-298.
65. Kobe RK, Lepczyk CA, Iyer M, (2005) Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86: 2780-2792.
66. Güsewell S, (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164: 243-266.
67. Lu X, Mo J, Gilliam FS, Zhou G, Fang Y, (2010) Effects of experimental nitrogen additions on plant diversity in old-growth tropical forest. Glob Chang Biol 16: 2688-2700.
68. Townsend AR, Cleveland CC, Asner GP, Bustamente MMC, (2007) Controls over foliar N:P rations in tropical rain forests. Ecology 88: 107-118.
69. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, et al. (2004) The worldwide leaf economics spectrum. Nature 428: 821-827.
70. Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R, editors (2008) Gradients in a tropical mountain ecosystem of Ecuador. Ecological Studies Vol. 198. Berlin: Springer. 525 p.
71. Homeier J, Breckle S-W Günter S, Rollenbeck RT, Leuschner C, (2010) Tree diversity, forest structure and productivity along altitudinal and topographical gradients in a species-rich Ecuadorian montane rainforest. Biotropica 42: 140-148.
72. Scheu S, (1992) Automated measurement of the respiratory response of soil microcompartments: Active microbial biomass in earthworm faeces. Soil Biol Biochem 24: 1113-1118.
73. Anderson JJPE, Domsch KH, (1978) A physiological method for the quantitative measurement of microbial biomass in soil. Soil Biol Biochem 10: 215-221.
74. Beck T, Joergensen RG, Kandeler E, Makeschin F, Nuss E, et al. (1997) An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol Biochem 29: 1023-1032.
75. Hart SC, Stark JM, Davidson EA & Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Methods of Analysis Part 2. Microbiological and Biochemical Properties. Madison: Soil Science Society of America Book Series. pp 985-1018.
76. Koehler B, Corre MD, Veldkamp E, Wullaert H, Wright SJ, (2009) Immediate and long-term nitrogen oxide emissions from tropical forest soils exposed to elevated nitrogen input. Glob Chang Biol 15: 2049-2066.
77. Loftfield N, Flessa H, Augustin J, Beese F, (1997) Automated gas chromatographic system for rapid analysis of the atmospheric trace gases methane, carbon dioxide, and nitrous oxide. J Environ Qual 26: 560-564.
78. Persson H, (1978) Root dynamics in a young Scots pine stand in Central Sweden. Oikos 30: 508-519.
79. Leuschner C, Hertel D, Coners H, Büttner V, (2001) Root competition between beech and oak: a hypothesis. Oecologia 126: 276-284.
80. Rillig MC, Allen MF, Klironomos JN, Chiariello NR, Field CB, (1998) Plant species-specific changes in root-inhabiting fungi in a California annual grassland: responses to elevated CO2 and nutrients. Oecologia 113: 252-259.
81. Beck A, Haug I, Oberwinkler F, Kottke I, (2007) Structural characterization and molecular identification of arbuscular mycorrhiza morphotypes of Alzatea verticillata (Alzateaceae), a prominent tree in the tropical mountain rain forest of South Ecuador. Mycorrhiza 17: 607-625.
82. R Development Core Team (2011) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.