Nitrogen Isotope Patterns in Alaskan Black Spruce Reflect Organic Nitrogen Sources and the Activity of Ectomycorrhizal Fungi

Ecosystems

Volumn 15, Issue 5, 2012, Pages 819-831

  Mayor, Jordan R ^a,b   Schuur, Edward A G ^a   Mack, Michelle C ^a   Hollingsworth, Terresa N ^c   Bååth, Erland ^d  

^a UNIVERSITY OF FLORIDA   (United States)

^b SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^c UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^d LUND UNIVERSITY   (Sweden)

Author keywords

15N; black spruce; denitrifier method; dissolved organic nitrogen; ectomycorrhiza; isotope fractionation; mixing models

Indexed keywords

BIOGEOCHEMISTRY; BOREAL FOREST; CONCENTRATION (COMPOSITION); CONIFEROUS FOREST; DENITRIFICATION; ECTOMYCORRHIZA; FUNGUS; ISOTOPIC FRACTIONATION; NITROGEN CYCLE; NITROGEN ISOTOPE; ORGANIC NITROGEN; SOIL ORGANIC MATTER; STABLE ISOTOPE;

ALASKA; UNITED STATES;

FUNGI; PICEA MARIANA;

EID: 84864754599     PISSN: 14329840     EISSN: 14350629     Source Type: Journal    
DOI: 10.1007/s10021-012-9548-9     Document Type: Article

References (112)

1. Abuzinadah RA, Read DJ. 1986. The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. III. Protein utilisation by Betula, Picea and Pinus in mycorrhizal association with Hebeloma crustuliniforme. New Phyt 130: 507-14.
2. Abuzinadah RA, Read DJ. 1988. Amino acids as nitrogen sources for ectomycorrhizal fungi: utilisation of individual amino acids. Trans Br Mycol Soc 91: 473-9.
3. Allison SD, Hanson CA, Treseder KK. 2007. Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol Biochem 39: 1878-87.
4. Amundson R, Austin AT, Schuur EAG, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT. 2003. Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycles 17: 31.
5. Andersen DR. 2008. Model based inference in the life sciences: a primer on evidence. New York, NY: Springer.
6. 15N. Ecology 92: 883-91.
7. Bååth E, Nilsson LO, Goransson H, Wallander H. 2004. Can the extent of degradation of soil fungal mycelium during soil incubations be used to estimate ectomycorrhizal biomass in soil? Soil Biol Biochem 36: 2105-9.
8. Binkley D, Son Y, Valentine DW. 2000. Do forests receive occult inputs of nitrogen? Ecosystems 3: 321-31.
9. Bödeker ITM, Nygren CMR, Taylor AFS, Olson A, Lindahl BD. 2009. ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J 3: 1387-95.
10. 15N patterns in old-growth forests of southern Chile as integrator for N-cycling. Isot Environ Health Stud 41: 249-59.
11. 15N in long-term bare fallow soils: influence of annual N fertilizer and manure applications. Eur J Soil Sci 59: 617-29.
12. Bowman WD. 1994. Accumulation and use of nitrogen and phosphorus following fertilization in two alpine tundra communities. Oikos 70: 261-70.
13. Burnham KP, Anderson DR. 2004. Multimodel inference. Soc Meth Res 33: 261-304.
14. Cabrera ML, Beare MH. 1993. Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57: 1007-12.
15. Cambui CA, Svennerstam H, Gruffman L, Nordin A, Ganeteg U, Näsholm T. 2011. Patterns of plant biomass partitioning depend on nitrogen source. PLOS One 6: ee19211.
16. Chalot M, Javelle A, Blaudez D, Lambilliote R, Cooke R, Sentenac H, Wipf D, Botton B. 2002. An update on nutrient transport processes in ectomycorrhizas. Plant Soil 244: 165-75.
17. Chapin FS, Kedrowski RA. 1983. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64: 376-91.
18. Chapin FS, Hollingsworth TN, Murray DF, Viereck LA, Walker MD. 2006. Floristic diversity and vegetation distribution in the Alaskan boreal forest. In: Chapin FS, Oswood MW, van Cleve K, Viereck LA, Verbyla DL, Eds. Alaska's changing boreal forest. New York, NY: Oxford University Press.
19. Clemmensen KE, Michelsen A, Jonasson S, Shaver G. 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phyt 171: 391-404.
20. Clemmensen KE, Sorensen PL, Michelsen A, Jonasson S, Strom L. 2008. Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizla fungi. Oecologia 155: 771-83.
21. 15N during a century of forest regrowth after agricultural abandonment. Ecosystems 10: 1197-208.
22. Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ. 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phyt 183: 980-92.
23. Davidson EA, Reis de Carvalho CJ, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Saba RT, Hayashi SN, Leal EC, Vieira ICG, Martinelli LA. 2007. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447: 995-998.
24. Dijkstra P, Williamson C, Menyailo O, Doucett R, Koch G, Hungate BA. 2003. Nitrogen stable isotope composition of leaves and roots of plants growing in a forest and a meadow. Isot Environ Health Stud 39: 29-39.
25. Doyle A, Weintraub MN, Schimel JP. 2004. Persulfate digestion and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci Soc Am J 68: 669-76.
26. Elser JJ, Bracken MES, Cleland EE, 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. Ecol Lett 10: 1135-42.
27. Evans RD. 2001. Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6: 121-6.
28. Frostegård Å, Bååth E. 1996. The use of phospolipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fert Soil 22: 59-65.
29. Frostegård Å, Tunlid A, Bååth E. 1991. Microbial biomass measured as total lipid phosphate in soils of different organic content. J Microbiol Meth 14: 151-63.
30. Frostegård Å, Bååth E, Tunlid A. 1993. Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25: 723-30.
31. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vororsmarth CJ. 2004. Nitrogen cycles: past, present, and future. Biogeochemistry 70: 153-226.
32. Gebauer G, Schulze ED. 1991. Carbon and nitrogen isotope ratios in different compartments of a healthy and a declining Picea abies forest in the Fichtelgebirge, NE Bavaria. Oecologia 87: 1432-939.
33. Giblin AE, Laundre JA, Nadelhoffer KJ, Shaver GR. 1994. Measuring nutrient availability in arctic soils using ion exchange resins: a field test. Soil Sci Soc Am J 58: 1154-62.
34. Güsewell S. 2004. N: P ratios in terrestrial plants: variation and functional significance. New Phyt 164: 243-66.
35. Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD, Sims SE. 2006. Measuring external mycelia production of ectomycorrhizal fungi in the field: the soil matrix matters. New Phyt 171: 179-86.
36. Hobbie EA, Agerer R. 2009. Nitrogen isotopes in ectomycorrhizal sporocarps correspond to belowground exploration types. Plant Soil 327: 71-83.
37. Hobbie EA, Colpaert JV. 2003. Nitrogen availability and colonization by mycorrhizal fungi correlate with nitrogen isotope patterns in plants. New Phyt 157: 115-26.
38. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87: 816-22.
39. 15N in nitrogen-limited forests and tundra can estimate nitrogen cycling through mycorrhizal fungi: a review. Ecosystems 11: 815-30.
40. Hobbie EA, Ouimette AP. 2009. Controls of nitrogen isotope patterns in soil profiles. Biogeochem 95: 355-71.
41. 14N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models. Oecologia 146: 258-68.
42. 15N is the key signal. Can J Microbiol 55: 84-94.
43. 15N natural abundance in soil-plant systems. New Phyt 139: 595.
44. Högberg MN, Högberg P. 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phyt 154: 791-5.
45. 15N abundance of surface soils, roots and mycorrhizas in profiles of European forest soils. Oecologia 108: 207-14.
46. Högberg P, Högberg MN, Quist ME, Ekblad A, Näsholm T. 1999. Nitrogen isotope fractionation during nitrogen uptake by ectomycorrhizal and non-mycorrhizal Pinus sylvestris. New Phyt 142: 569-76.
47. Högberg MN, Bååth E, Nordgren A, Arnebrant K, Högberg P. 2003. Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs-a hypothesis based on field observations in boreal forest. New Phyt 160: 225-38.
48. Högberg MN, Briones MJI, Keel SG, Metcalfe DB, Campbell C, Midwood AJ, Thornton B, Hurry V, Linder S, Näsholm T, Högberg P. 2010. Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest. New Phyt 187: 485-93.
49. Högberg P, Johannison C, Yarwood S, Callesen I, Näsholm T, Myrold DD, Högberg MN. 2011. Recovery of ectomycorrhiza after 'nitrogen saturation' of a conifer forest. New Phyt 189: 515-25.
50. Hollingsworth TN, Walker MD, Chapin FSIII, Parsons AL. 2006. Scale-dependent environmental controls over species composition in Alaskan black spruce communities. Can J For Res 36: 1781-96.
51. Hollingsworth TN, Schuur EAG, Chapin FSIII, Walker MD. 2008. Plant community composition as a predictor of regional soil carbon storage in Alaskan boreal black spruce ecosystems. Ecosystems 11: 629-42.
52. Houlton BZ, Sigman DM, Hedin LO. 2006. Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci USA 103: 8745-50.
53. Houlton BZ, Sigman DM, Schuur EAG, Hedin LO. 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104: 8902-6.
54. Howarth RW, Marino R. 2006. Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limn Ocean 51: 364-76.
55. Jones DL, Kielland K. 2002. Soil amino acid turnover dominates the nitrogen flux in permafrost-dominated taiga forest soils. Soil Biol Biochem 34: 209-19.
56. Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A. 2005. Dissolved organic nitrogen uptake by plants-an important N uptake pathway? Soil Biol Biochem 37: 413-23.
57. 15N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient. Oecologia 156: 861-70.
58. 15N signature of taiga trees and shrubs. Can J For Res 28: 485-8.
59. Kielland K, McFarland JW, Olson K. 2007. Rapid cycling of organic nitrogen in taiga forest ecosystems. Ecosystems 10: 360-8.
60. Knapp AN, Sigman DM, Lipschultz F. 2005. N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic Time-series Study site. Glob Biogeochem Cycles 19: GB1018.
61. 15N abundance of plants and soil N in a temperate coniferous forest. Ecosystems 6: 457-69.
62. Koide RT, Xu B, Sharda J. 2005. Contrasting below-ground views of an ectomycorrhizal fungal community. New Phyt 166: 251-62.
63. Kolb KJ, Evans RD. 2002. Implications of leaf nitrogen recycling on the nitrogen isotope composition of deciduous plant tissues. New Phyt 156: 57-64.
64. 15N along productivity gradients of a boreal forest. Ecosystems 13: 108-17.
65. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM. 2002. Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83: 104-15.
66. Lilleskov EA, Hobbie EA, Horton TR. 2011. Conservation of ectomycorrhizal fungi: exploring the linkages between functional and taxonomic responses to anthropogenic N deposition. Fung Ecol 2: 174-83.
67. Lindahl BD, Taylor AFS. 2004. Occurrence of N-acetylhexosaminidase-encoding genes in ectomycorrhizal basidiomycetes. New Phyt 164: 193-9.
68. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD. 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phyt 173: 611-20.
69. Mack MC, Schuur EAG, Bret-Hart MS, Shaver GR, Chapin FSIII. 2004. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431: 440-3.
70. Mayor JR, Schuur EAG, Henkel TW. 2009. Elucidating the nutritional status of fungi. Ecol Lett 12: 171-83.
71. McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Landre JA, Murray G. 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415: 68-71.
72. Melillo JM, Aber JD, Linkins AE, Ricca A, Fry B, Nadelhoffer KJ. 1989. Carbon and nitrogen dynamics along the decay continuum: plant litter to soil organic matter. Plant Soil 115: 189-98.
73. Mellilo JM, Cowling EB. 2002. Reactive nitrogen and public policies for environmental protection. Ambio 31: 150-8.
74. 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105: 53-63.
75. 15N natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115: 406-18.
76. Nadelhoffer K, Fry B. 1994. Nitrogen isotope studies in forest ecosystems, Chap 2. In: Lajtha K, Michener R, Eds. Stable isotopes in ecology. Oxford, UK: Blackwell Scientific. p 22-44.
77. Näsholm T, Kielland K, Ganeteg U. 2009. Uptake of organic nitrogen by plants. New Phytologist 182: 31-48.
78. Nilsson LO, Wallander H. 2003. Production of external mycelium by ectomycorrhizal fungi in a norway spruce forest was reduced in response to nitrogen fertilization. New Phyt 158: 409-16.
79. Nilsson LO, Giesler R, Bååth E, Wallander H. 2005. Growth and biomass of mycorrhizal mycelia in coniferous forests along short natural nutrient gradients. New Phyt 165: 613-22.
80. Nygren CMR, Edqvist J, Elfstrand M, Heller G, Taylor AFS. 2007. Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi. Mycorrhiza 17: 241-8.
81. Orwin KH, Kirschbaum MUF, St John MG, Dickie IA. 2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14: 493-502.
82. 15N values: amino acids in grassland and arable soils. Soil Biol Biochem 31: 1751-5.
83. Pardo LH, Nadelhoffer KJ. 2010. Using nitrogen isotope ratios to assess terrestrial ecosystems at regional and global scales. In: West J, Bowen GJ, Dawson TE, Tu KP, Eds. Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. New York, NY: Springer.
84. 15N. Biogeochemistry 80: 143-71.
85. Piccolo MC, Neill C, Cerri CC. 1994. Net nitrogen mineralization and net nitrification along a tropical forest-to-pasture chronosequence. Plant Soil 162: 61-70.
86. 2O reflect the nitrogen dynamics of forest soils. Plant Soil 295: 79-94.
87. Read DJ, Leake JR, Perez-Moreno J. 2004. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82: 1243-63.
88. 15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16: 153-62.
89. Ruess R, Henkdrick RL, Burton AJ, Pregitzer KS, Sveinbjornsson B, Allen MF, Maurer GE. 2003. Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska. Ecol Monogr 73: 643-62.
90. Schulze ED, Chapin FS, Gebauer G. 1994. Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska. Oecologia 100: 406-12.
91. Schuur EAG, Matson PA. 2001. Aboveground net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128: 431-42.
92. 15N abundance. Aust J Plant Physiol 13: 699-757.
93. Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Bohlke JK. 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73: 4145-53.
94. Silfer JA, Engel MH, Macko SA. 1992. Kinetic fractionation of stable carbon and nitrogen isotopes during peptide bond hydrolysis: experimental evidence and geochemical implications. Chem Geo: Iso Geosci sec 101: 211-21.
95. Smith SE, Read DJ. 2008. Nitrogen mobilization and nutrition in ectomycorrhizal plants. New York: Academic Press.
96. + along the N leaching gradient. Rapid Commun Mass Spectrom 24: 1001-8.
97. Talbot JM, Allison SD, Treseder KK. 2008. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22: 955-63.
98. Taylor DL, Herriott IC, Stone KE, McFarland JW, Booth MG, Leigh MB. 2010. Structure and resilience of fungal communities in Alaskan boreal forest soils. Can J For Res 40: 1288-301.
99. Tedersoo L, May TW, Smith ME. 2010. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217-63.
100. Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS. 2006. Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phyt 170: 873-84.
101. Treseder K, Turner KM, Mack MC. 2007. Mycorrhizal responses to nitrogen fertilization in boreal ecosystems: potential consequences for soil carbon storage. Glob Change Biol 13: 78-88.
102. van Wijk MT, Williams M, Gough L, Hobbie SE, Shaver GR. 2003. Luxury consumption of soil nutrients: a possible competitive strategy in above-ground and below-ground biomass allocation and root morphology for slow-growing arctic vegetation? J Ecol 91: 664-76.
103. Viereck LA, Johnston WF. 1990. Picea mariana (Mill.) B. S. P. black spruce. In: Burns RM, Honkala BH, Eds. Silvics of North America. Washington D. C: Forest Service, US Department of Agriculture. p 227-37.
104. Vitousek PM. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol App 7: 737-50.
105. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13: 87-115.
106. 15N natural abundance in Hawaiian rainforest-patterns and possible mechanisms. Oecologia 78: 383-8.
107. Wallander H, Nilsson LO, Hagerberg D, Bååth E. 2001. Estimation of the biomass and production of external mycelium of ectomycorrhizal fungi in the field. New Phyt 151: 751-60.
108. 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139: 89-97.
109. 15N enrichment in soil profiles along a chronosequence undergoing isostatic rebound in northern Sweden. Oecologia 160: 87-96.
110. 15N in hydrolysable-N of arctic soils and its implication for mycorrhizal fungi-plant interaction. Biogeochemistry 97: 183-94.
111. Yarie J, Kane E, Mack M. 2007. Aboveground biomass equations for the trees of interior Alaska Bulletin of the Agricultural and Forestry Experiment Station at the University of Alaska Fairbanks 115.
112. 15N: progress over the last 30 years. Phytochem Rev 2: 121-32.