Distinct Microbial Limitations in Litter and Underlying Soil Revealed by Carbon and Nutrient Fertilization in a Tropical Rainforest

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Fanin, Nicolas ^a,b   Barantal, Sandra ^a   Fromin, Nathalie ^a   Schimann, Heidy ^c   Schevin, Patrick ^a   Hättenschwiler, Stephan ^a  

^a CNRS   (France)

^b UNIV MONTPELLIER   (France)

^c Campus Agronomique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE; HEMICELLULOSE; LIGNIN; ORGANIC CARBON; PHENOL DERIVATIVE; PHOSPHATE; TANNIN; UREA;

ARTICLE; CARBON MINERALIZATION; CONTROLLED STUDY; DECOMPOSITION; ENRICHMENT CULTURE; HETEROTROPHY; LEAF LITTER; MICROBIAL ACTIVITY; MICROBIAL COLONIZATION; NONHUMAN; NUTRIENT; NUTRIENT SUPPLY; PLANT LITTER; SOIL; SOIL FAUNA; SOIL FERTILIZATION; SPECIES DIFFERENCE; STOICHIOMETRY; SUBSTRATE INDUCED RESPIRATION; TROPICAL RAIN FOREST;

CARBON; CELLULOSE; ECOSYSTEM; FRENCH GUIANA; LINEAR MODELS; NITROGEN; PHOSPHATES; PHOSPHORUS; PLANTS; SOIL; SOIL MICROBIOLOGY; SOLID WASTE; TREES; TROPICAL CLIMATE; UREA;

EID: 84871276869     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049990     Document Type: Article

References (82)

1. Coûteaux M-M, Bottner P, Berg B, (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 10: 63-66.
2. Berg B, Matzner E, (1997) Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ Rev 5: 1-25.
3. Henry HAL, Cleland EE, Field CB, Vitousek PM, (2005) Interactive effects of elevated CO2, N deposition and climate change on plant litter quality in a California annual grassland. Oecologia 142: 465-473.
4. Davidson EA, Janssens IA, (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440: 165-173.
5. Janssens IA, Lankreijer H, Matteucci G, Kowalski AS, Buchmann N, et al. (2001) Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biol 7: 269-278.
6. Chambers JQ, Tribuzy ES, Toledo LC, Crispim BF, Higuchi N, et al. (2004) Respiration from a tropical forest ecosystem: Partitioning of sources and low carbon use efficiency. Ecol Appl 14: S72-S88.
7. Epron D, Nouvellon Y, Roupsard O, Mouvondy W, Mabiala A, et al. (2004) Spatial and temporal variations of soil respiration in a Eucalyptus plantation in Congo. Forest Ecol Manag 202: 149-160.
8. Yuste JC, Nagy M, Janssens IA, Carrara A, Ceulemans R, (2005) Soil respiration in a mixed temperate forest and its contribution to total ecosystem respiration. Tree Physiol 25: 609-619.
9. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, et al. (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70: 153-226.
10. Vitousek PM, Porder S, Houlton BZ, Chadwick OA, (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20: 5-15.
11. Phillips OL, Malhi Y, Higuchi N, Laurance WF, Nunez PV, et al. (1998) Changes in the carbon balance of tropical forests: Evidence from long-term plots. Science 282: 439-442.
12. Malhi Y, Grace J, (2000) Tropical forests and atmospheric carbon dioxide. Trends Ecol Evol 15: 332-337.
13. Grace J, Malhi Y, Higuchi N (2001) Productivity and carbon fluxes of tropical rain forests. In: Mooney HA, Roy J., Saugier B, editors. Terrestrial Global Productivity: Past, Present, and Future. San Diego: Academic Press. pp. 401-428.
14. Luyssaert S, Schulze ED, Borner A, Knohl A, Hessenmoller D, et al. (2008) Old-growth forests as global carbon sinks. Nature 455: 213-215.
15. Sayer EJ, Tanner EVJ, (2010) A new approach to trenching experiments for measuring root-rhizosphere respiration in a lowland tropical forest. Soil Biol Biochem 42: 347-352.
16. Silver WL, Thompson AW, McGroddy ME, Varner RK, Dias JD, et al. (2005) Fine root dynamics and trace gas fluxes in two lowland tropical forest soils. Global Change Biol 11: 290-306.
17. Gallardo A, Schelsinger WH, (1994) Factors limiting microbial biomass in the mineral soil and forest floor of a warm-temperate forest. Soil Biol Biochem 26: 1409-1415.
18. Joergensen RG, Scheu S, (1999) Response of soil microorganisms to the addition of carbon, nitrogen and phosphorus in a forest Rendzina. Soil Biol Biochem 31: 859-866.
19. Ilstedt U, Singh S, (2005) Nitrogen and phosphorus limitations of microbial respiration in a tropical phosphorus-fixing acrisol (ultisol) compared with organic compost. Soil Biol Biochem 37: 1407-1410.
20. Gnankambary Z, Stedt U, Nyberg G, Hien V, Malmer A, (2008) Nitrogen and phosphorus limitation of soil microbial respiration in two tropical agroforestry parklands in the south-Sudanese zone of Burkina Faso: The effects of tree canopy and fertilization. Soil Biol Biochem 40: 350-359.
21. Sterner RW, Elser JJ (2002) Ecological stoichiometry: The biology of elements from molecules of the biosphere. Princeton: Princeton University Press. 439 p.
22. Cherif M, Loreau M, (2009) When microbes and consumers determine the limiting nutrient of autotrophs: a theoretical analysis. Proc Roy Soc B-Biol Sci 276: 487-497.
23. Enriquez S, Duarte CM, Sand-Jensen K, (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C:N:P content. Oecologia 94: 457-471.
24. Manzoni S, Trofymow JA, Jackson RB, Porporato A, (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Mono 80: 89-106.
25. De Angelis P, Chigwerewe KS, Mugnozza GES, (2000) Litter quality and decomposition in a CO2-enriched Mediterranean forest ecosystem. Plant Soil 224: 31-41.
26. Körner C, Miglietta F, (1994) Long-term effects of naturally elevated CO2 on Mediterranean grassland and forest trees. Oecologia 99: 343-351.
27. Hättenschwiler S, Schafellner C, (2004) Gypsy moth feeding in the canopy of a CO2-enriched mature forest. Global Change Biol 10: 1899-1908.
28. Hättenschwiler S, Coq S, Barantal S, Handa IT, (2011) Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. New Phytol 189: 950-965.
29. Cleveland CC, Townsend AR, Taylor P, Alvarez-Clare S, Bustamante MMC, et al. (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14: 939-947.
30. Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC, (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9: 9-17.
31. Townsend AR, Asner GP, Cleveland CC, (2008) The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 8: 424-431.
32. Quesada CA, Lloyd J, Schwarz M, Patiño S, Baker TR, et al. (2010) Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7: 1515-1541.
33. Cleveland CC, Townsend AR, Schmidt SK, (2002) Phosphorus limitation of microbial processes in moist tropical forests: Evidence from short-term laboratory incubations and field studies. Ecosystems 5: 680-691.
34. Cleveland CC, Reed SC, Townsend AR, (2006) Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology 87: 492-503.
35. Cleveland CC, Townsend AR, (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. P Natl Acad Sci USA 103: 10316-10321.
36. Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, et al. (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11: 35-43.
37. Mo J, Zhang W, Zhu W, Gundersen P, Fang Y, et al. (2008) Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Global Change Biol 14: 403-412.
38. Cusack DF, Torn MS, McDowell WH, Silver WL, (2010) The response of heterotrophic activity and carbon cycling to nitrogen additions and warming in two tropical soils. Global Change Biol 16: 2555-2572.
39. 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.
40. Vitousek PM, Farrington H, (1997) Nutrient limitation and soil development: Experimental test of a biogeochemical theory. Biogeochemistry 37: 63-75.
41. Hobbie SE, Vitousek PM, (2000) Nutrient limitation of decomposition in Hawaiian forests. Ecology 81: 1867-1877.
42. Reed S, Vitousek P, Cleveland C, (2011) Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106: 323-336.
43. Barantal S, Schimann H, Fromin N, Hättenschwiler S, (2012) Nutrient and carbon limitation on decomposition in an Amazonian rainforest. Ecosystems 15: 1039-1052.
44. Krashevska V, Maraun M, Ruess L, Scheu S, (2010) Carbon and nutrient limitation of soil microorganisms and microbial grazers in a tropical montane rain forest. Oikos 119: 1020-1028.
45. Milcu A, Heim A, Ellis RJ, Scheu S, Manning P, (2011) Identification of general patterns of nutrient and labile carbon control on soil carbon dynamics across a successional gradient. Ecosystems 14: 710-719.
46. Priess JA, Fölster H, (2001) Microbial properties and soil respiration in submontane forests of Venezuelian Guyana: characteristics and response to fertilizer treatments. Soil Biol Biochem 33: 503-509.
47. Brown ALP, Garland JL, Day FP, (2009) Physiological profiling of soil microbial communities in a Florida scrub-oak ecosystem: spatial distribution and nutrient limitations. Micro Ecol 57: 14-24.
48. Hättenschwiler S, Aeschlimann B, Coûteaux MM, Roy J, Bonal D, (2008) High variation in foliage and leaf litter chemistry among 45 tree species of a neotropical rainforest community. New Phytol 179: 165-175.
49. Schreeg L, Mack M, Turner B, (2012) Nutrient-specific patterns in leaf litter solubility across 41 lowland tropical woody species. Ecology in press.
50. Wieder RW, Cleveland CC, Townsend AR, (2009) Controls over leaf litter decomposition in wet tropical forests. Ecology 90: 3333-3341.
51. Coq S, Souquet JM, Meudec E, Cheynier V, Hättenschwiler S, (2010) Interspecific variation in leaf litter tannins drives decomposition in a tropical rain forest of French Guiana. Ecology 91: 2080-2091.
52. Ushio M, Wagai R, Balser TC, Kitayama K, (2008) Variations in the soil microbial community composition of a tropical montane forest ecosystem: Does tree species matter? Soil Biol Biochem 40: 2699-2702.
53. Fanin N, Hättenschwiler S, Barantal S, Schimann H, Fromin N, (2011) Does variability in litter quality determine soil microbial respiration in an Amazonian rainforest? Soil Biol Biochem 43: 1014-1022.
54. Gonzalez G, Seastedt TR, (2001) Soil fauna and plant litter decomposition in tropical and subalpine forests. Ecology 82: 955:: 964.
55. Wall DH, Bradford MA, St John MG, Tofymow JA, Behan Pelletier VM, et al. (2008) Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Global Change Biol 14: 2661-2677.
56. Yang X, Chen J, (2009) Plant litter quality influences the contribution of soil fauna to litter decomposition in humid tropical forests, southwestern China. Soil Biol Biochem 41: 910-918.
57. Makkonen M, Berg MP, Handa T, Hättenschwiler S, van Ruijven J, et al. (2012) Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecol Lett 15: 1033-1041.
58. McGlynn TP, Salinas DJ, Dunn RR, Wood TE, Lawrence D, et al. (2007) Phosphorus limits tropical rain forest litter fauna. Biotropica 39: 50-53.
59. Bonal D, Bosc A, Ponton S, Goret JY, Burban B, et al. (2008) Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana. Global Change Biol 14: 1917-1933.
60. Gourlet-Fleury S, Houllier F, (2000) Modelling diameter increment in a lowland evergreen rain forest in French Guiana. Forest Ecol Manag 131: 269-289.
61. Roy J, Hättenschwiler S, Domenach AM (2005) Tree diversity and soil biology: a new research program in French Guiana. In: Binkley D, Menyailo O, editors. Tree species effects on soils: implications for global change. Kluwer Academic, Dordrecht. pp. 337-348.
62. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, et al. (2003) Microbial diversity and soil functions. Eur J Soil Sci 54: 655-670.
63. Beare MH, Neely CL, Coleman DC, Hargrove WL, (1990) A substrate-induced respiration (SIR) method for measurement of fungal and bacterial biomass on plant residues. Soil Biol Biochem 22: 585-594.
64. Pinheiro JC, Bates D, DebRoy S, Deepayan S, (2007) nlme: Linear and nonlinear mixed effects models. R Package Version 31 pp. 339.
65. Bates D, (2010) Linear mixed model implementation in lme4. R Package Version 3 pp. 32.
66. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP, (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75: 1182-1189.
67. Fontaine S, Barot S, Barre P, Bdioui N, Mary B, et al. (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450: 277-U210.
68. Talbot JM, Treseder KK, (2012) Interactions among lignin, cellulose, and nitrogen drive litter chemistry-decay relationships. Ecology 93: 345-354.
69. 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.
70. Schimel JP, Bennett J, (2004) Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85: 591-602.
71. Craine JM, Morrow C, Fierer N, (2007) Microbial nitrogen limitation increases decomposition. Ecology 88: 2105-2113.
72. Hättenschwiler S, Bracht-Jørgensen HB, (2010) Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest. J Ecol 98: 754-763.
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. Orwin KH, Wardle DA, Greenfield LG, (2006) Ecological consequences of carbon substrate identity and diversity in a laboratory study. Ecology 87: 580-593.
75. Feeley KJ, Davies SJ, Perez R, Hubbell SP, Foster RB, (2011) Directional changes in the species composition of a tropical forest. Ecology 92: 871-882.
76. Feeley KJ, Malhi Y, Zelazowski P, Silman MR, (2012) The relative importance of deforestation, precipitation change, and temperature sensitivity in determining the future distributions and diversity of Amazonian plant species. Global Change Biol 18: 2636-2647.
77. Okin GS, Mahowald N, Chadwick OA, Artaxo P, (2004) Impact of desert dust on the biogeochemistry of phosphorus in terrestrial ecosystems. Global Biogeochem Cy DOI:10.1029/2003GB002145.
78. Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, et al. (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419: 915-917.
79. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF, (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81: 2359-2365.
80. DeForest JL, Zak DR, Pregitzer KS, Burton AJ, (2004) Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68: 132-138.
81. Treseder KK, (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11: 1111-1120.
82. Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK, (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92: 621-632.