, Volume 95, Issue 2–3, pp 215–229 | Cite as

N2 fixing alder (Alnus viridis spp. fruticosa) effects on soil properties across a secondary successional chronosequence in interior Alaska

  • Jennifer S. Mitchell
  • Roger W. RuessEmail author


Green alder (Alnus viridis ssp. fruticosa) is a dominant understory shrub during secondary successional development of upland forests throughout interior Alaska, where it contributes substantially to the nitrogen (N) economy through atmospheric N2 fixation. Across a replicated 200+ year old vegetation chronosequence, we tested the hypotheses that green alder has strong effects on soil chemical properties, and that ecosystem-level N inputs via N2 fixation decrease with secondary successional stand development. Across early-, mid-, and late-successional stands, alder created islands of elevated soil N and carbon (C), depleted soil phosphorus (P), and more acidic soils. These effects translated to the stand-level in response to alder stem density. Although neither N2 fixation nor nodule biomass differed among stand types, increases in alder densities with successional time translated to increasing N inputs. Estimates of annual N inputs by A. viridis averaged across the upland chronosequence (6.6 ± 1.2 kg N ha−1 year−1) are substantially less than inputs during early succession by Alnus tenuifolia growing along Alaskan floodplains. However, late-succession upland forests, where densities of A. viridis are highest, may persist for centuries, depending on fire return interval. This pattern of prolonged N inputs to late successional forests contradicts established theory predicting declines in N2-fixation rates and N2-fixer abundance as stands age.


Alder Boreal Nitrogen cycling Nitrogen fixation Secondary succession 



We would like to thank the staff at the Institute of Arctic Biology at the University of Alaska Fairbanks (UAF) for providing logistical support to this project, as well as the staff at the UAF Forest Soils Lab and the UAF Experimental Greenhouse for their assistance. We greatly appreciate the comments and suggestions by Reviewers and the Associate Editor (Karsten Kalbitz), which substantially improved the aricle. Funding for the research was provided by the Bonanza Creek Long-Term Ecological Research program (funded jointly by NSF grant DEB-0423442 and USDA Forest Service, Pacific Northwest Research Station grant PNW01-JV11261952-231). We also thank those who aided in collection of field data for this study, especially J.J. Frost and the various peers, friends and family who helped along the way.


  1. Anderson MD, Ruess RW, Uliassi DD, Mitchell JS (2004) Estimating N2 fixation in two species of Alnus in interior Alaska using acetylene reduction and 15N2 uptake. Ecoscience 11:102–112Google Scholar
  2. Binkley D (2003) Seven decades of stand development in mixed and pure stands of conifers and nitrogen-fixing red alder. Can J For Res 33:2274–2279 CrossRefGoogle Scholar
  3. Binkley D, Sollins P (1990) Factors determining differences in soil pH in adjacent conifer and alder-conifer sands. Soil Sci Soc Am J 54:1427–1433Google Scholar
  4. Binkley D, Sollins P, Bell R, Sachs D, Myrold D (1992) Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73(6):2022–2033. doi: 10.2307/1941452 CrossRefGoogle Scholar
  5. Binkley D, Cromack JR, Baker D (1994) Nitrogen fixation by red alder: biology, rates, and controls. In: Hibbs DE, Debell DS, Tarrant RF (eds) The biology and management of red alder. Oregon State University Press, CorvallisGoogle Scholar
  6. Binkley D, Stape JL, Ryan MG, Barnard HR, Fownes J (2002) Age-related decline in forest ecosystem growth: an individual-tree, stand-structure hypothesis. Ecosystems (N Y, Print) 5(1):58–67. doi: 10.1007/s10021-001-0055-7 CrossRefGoogle Scholar
  7. Binkley D, Senock R, Cromack K (2003) Phosphorus limitation on nitrogen fixation by Facaltaria seedlings. For Ecol Man 186(1/3):171–176CrossRefGoogle Scholar
  8. Bormann BT, Cromack K, Russell WO (1994) Influences of red alder on soils and long-term ecosystem productivity. In: Hibbs DE, Debell DS, Tarrant RF (eds) The biology and management of red alder. Oregon State University Press, CorvallisGoogle Scholar
  9. Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64(2):149–175. doi: 10.2307/2937039 CrossRefGoogle Scholar
  10. Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Mueller-Dombois DA, Vitousek PM (1995) Changes in soil-phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76(5):1407–1424. doi: 10.2307/1938144 CrossRefGoogle Scholar
  11. Cross AF, Schlesinger WH (1999) Plant regulation of soil nutrient distribution in the northern Chihuahuan Desert. Plant Ecol 145(1):11–25. doi: 10.1023/A:1009865020145 CrossRefGoogle Scholar
  12. Cumming SG, Schmiegelow FKA, Burton PJ (2000) Gap dynamics in boreal aspen stands: Is the forest older than we think? Ecol Appl 10(3):744–759Google Scholar
  13. DeLuca TH, Zackrisson O, Nilsson MC, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419(6910):917–920. doi: 10.1038/nature01051 CrossRefGoogle Scholar
  14. DeLuca TH, Zackrisson O, Gundale MJ, Nilsson MC (2008) Ecosystem feedbacks and nitrogen fixation in boreal forests. Science 320:1181. doi: 10.1126/science.1154836 CrossRefGoogle Scholar
  15. Gallardo A, Schlesinger WH (1995) Factors determining soil microbial biomass and nutrient immobilization in desert soils. Biogeochemistry 28(1):55–68. doi: 10.1007/BF02178061 CrossRefGoogle Scholar
  16. Giardina CP, Huffman S, Binkley D, Caldwell BA (1995) Alders increase soil-phosphorus availability in a Douglas-fir plantation. Can J Res 25(10):1652–1657. doi: 10.1139/x95-179 CrossRefGoogle Scholar
  17. Hart SC, Binkley D, Perry DA (1997) Influence of red alder on soil nitrogen transformations in two conifer forests of contrasting productivity. Soil Biol Biochem 29(7):1111–1123. doi: 10.1016/S0038-0717(97)00004-7 CrossRefGoogle Scholar
  18. Helfield JM, Naiman RJ (2002) Salmon and alder as nitrogen sources to riparian forests in a boreal Alaskan watershed. Oecologia 133(4):573–582. doi: 10.1007/s00442-002-1070-x CrossRefGoogle Scholar
  19. Hogg EH, Hurdle PA (1995) The aspen parkland in western Canada: a dry-climate analog for the future boreal forest. Water Air Soil Pollut 82(1–2):391–400. doi: 10.1007/BF01182849 CrossRefGoogle Scholar
  20. Hu FS, Finney BP, Brubaker LB (2001) Effects of Holocene Alnus expansion on aquatic productivity, nitrogen cycling and soil development in southwestern Alaska. Ecosystems (N Y, Print) 4(4):358–368. doi: 10.1007/s10021-001-0017-0 CrossRefGoogle Scholar
  21. Huss-Danell K, Gentili F, Valverde C, Wall LG, Wiklund A (2002) Phosphorus is important in nodulation of actinorhizal plants and legumes. In: Finan TM, O’Brian MR, Layzell DB, Vessey JK, Newton W (eds) Nitrogen fixation: global perspectives. CAB International, WallingfordGoogle Scholar
  22. Johnson DW (1992) Effects of forest management on soil carbon storage. Water Air Soil Pollut 64(1–2):83–120. doi: 10.1007/BF00477097 CrossRefGoogle Scholar
  23. Johnstone JF (2005) Effects of aspen (Populus tremuloides) sucker removal on postfire conifer regeneration in central Alaska. Can J Res 35(2):483–486. doi: 10.1139/x04-171 CrossRefGoogle Scholar
  24. Kielland K, Olson K, Ruess RW, Boone RD (2006) Contribution of winter processes to soil nitrogen flux in taiga forest ecosystems. Biogeochemistry 81(3):349–360. doi: 10.1007/s10533-006-9045-3 CrossRefGoogle Scholar
  25. Kurkowski TA, Mann DH, Rupp TS, Verbyla DL (2008) Relative importance of different secondary successional pathways in an Alaskan boreal forest. Can J Res 38(7):1911–1923. doi: 10.1139/X08-039 CrossRefGoogle Scholar
  26. Mack MC, D’Antonio CM, Ley RE (2001) Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C-4 grasses in Hawaii. Ecol Appl 11(5):1323–1335Google Scholar
  27. Marion GM, Van Cleve K, Dyrness CT, Black CH (1993) The soil chemical environment along a forest primary successional sequence on the Tanana River floodplain, interior Alaska. Can J Res 23(5):914–922. doi: 10.1139/x93-119 CrossRefGoogle Scholar
  28. Matzek V, Vitousek PM (2003) Nitrogen fixation in bryophytes, lichens, and decaying wood along a soil-age gradient in Hawaiian montane rain forests. Biotropica 35(1):12–19Google Scholar
  29. Mitchell JS (2006) Patterns of and controls over N inputs by green alder (Alnus viridis ssp. fruticosa) to a secondary successional chronosequence in interior Alaska. M.S. Thesis, University of Alaska FairbanksGoogle Scholar
  30. Mitchell JS, Ruess RW (2009) Seasonal patterns of climate controls over nitrogen fixation by Alnus viridis spp. fruticosa in a secondary successional chronosequence in interior Alaska. Ecoscience (in press)Google Scholar
  31. Moro MJ, Pugnaire FI, Haase P, Puigdefabregas J (1997) Mechanisms of interaction between a leguminous shrub and its understory in a semi-arid environment. Ecography 20(2):175–184. doi: 10.1111/j.1600-0587.1997.tb00360.x CrossRefGoogle Scholar
  32. Mulligan D (2006) Soil survey of the Fairbanks and North Star Borough areas. US Department of Agriculture Natural Resources Conservation Service, PalmerGoogle Scholar
  33. Munsell Color Company (1992) Munsell soil color charts. Munsell Color, BaltimoreGoogle Scholar
  34. Pastor J, Binkley D (1998) Nitrogen fixation and the mass balances of carbon and nitrogen in ecosystems. Biogeochemistry 43(1):63–78. doi: 10.1023/A:1006057428096 CrossRefGoogle Scholar
  35. Rastetter EB, Vitousek P, Field CB, Shaver GR, Herbert D, Agren GI (2001) Resource optimization and symbiotic nitrogen fixation. Ecosystems (N Y, Print) 4(4):369–388. doi: 10.1007/s10021-001-0018-z CrossRefGoogle Scholar
  36. Resh SC, Binkley D, Parrotta JA (2002) Greater soil carbon sequestration under nitrogen-fixing trees compared with Eucalyptus species. Ecosystems (N Y, Print) 5(3):217–231. doi: 10.1007/s10021-001-0067-3 CrossRefGoogle Scholar
  37. Rhoades C, Eckert GE, Coleman DC (1998) Effect of pasture trees on soil nitrogen and organic matter: implications for tropical montane forest restoration. Restor Ecol 6(3):262–270. doi: 10.1046/j.1526-100X.1998.00639.x CrossRefGoogle Scholar
  38. Rhoades C, Oskarsson H, Binkley D, Stottlemyer B (2001) Alder (Alnus crispa) effects on soils in ecosystems of the Agashashok River valley, northwest Alaska. Ecoscience 8(1):89–95Google Scholar
  39. Ruess R, McFarland J, Trummer LM, Rohrs-Richey JK (2009) Disease-mediated declines in N-fixation inputs by Alnus tenuifolia to early-successional floodplains in interior and south-central Alaska. Ecosystems (N Y, Print). doi: 10.1007/s10021-009-9237-5
  40. SAS Institute (2001) The SAS System for Windows, Version 8.2. SAS Institute, Inc., CaryGoogle Scholar
  41. Schlesinger WH, Raikes JA, Hartley AE, Cross AF (1996) On the spatial pattern of soil nutrients in desert ecosystems. Ecology 77(4):1270. doi: 10.2307/2265595 CrossRefGoogle Scholar
  42. Seastedt TR, Adams GA (2001) Effects of mobile tree islands on alpine tundra soils. Ecology 82(1):8–17CrossRefGoogle Scholar
  43. Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, Liston LE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert Arctic tundra to shrubland. Bioscience 55(1):17–26. doi: 10.1641/0006-3568(2005)055[0017:WBPCHC]2.0.CO;2 CrossRefGoogle Scholar
  44. Uliassi DD, Ruess RW (2002) Limitations to symbiotic nitrogen fixation in primary succession on the Tanana River floodplain. Ecology 83(1):88–103Google Scholar
  45. Valentine D (1990) Influence of topography on soil acidity and hydrogen ion budgets in an Arctic landscape. Dissertation, Duke UniversityGoogle Scholar
  46. Valentine DW, Kielland K, Chapin FS, McGuire AD, Van Cleve K (2006) Patterns of biogeochemistry in Alaskan boreal forests. In: Chapin FS, Oswood MW, van Cleve K, Viereck LA, Verbyla DL (eds) Alaska’s changing boreal forest. Oxford University Press, New YorkGoogle Scholar
  47. Van Cleve K, Heal OW, Roberts D (1986) Bioassay of forest floor nitrogen supply for plant growth. Can J Res 16(6):1320–1326. doi: 10.1139/x86-233 CrossRefGoogle Scholar
  48. van Miegroet H, Cole DW (1984) The impact of nitrification on soil acidification and cation leaching in a red alder ecosystem. J Environ Qual 13(4):586–590Google Scholar
  49. Viereck LA, Van Cleve K, Adams PC, Schlentner RE (1993) Climate of the Tanana River floodplain near Fairbanks, Alaska. Can J Res 23(5):899–913. doi: 10.1139/x93-118 CrossRefGoogle Scholar
  50. Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46(1/3):179–202. doi: 10.1023/A:1006185020121 CrossRefGoogle Scholar
  51. Vitousek PM, Hobbie S (2000) Heterotrophic nitrogen fixation in decomposing litter: patterns and regulation. Ecology 81(9):2366–2376CrossRefGoogle Scholar
  52. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the seas: how can it occur? Biogeochemistry 13(2):87–115. doi: 10.1007/BF00002772 CrossRefGoogle Scholar
  53. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(1):1–45. doi: 10.1023/A:1015798428743 CrossRefGoogle Scholar
  54. Wall LG, Hellsten A, Huss-Danell K (2000) Nitrogen, phosphorus, and the ratio between them affect nodulation in Alnus incana and Trifolium pratense. Symbiosis 29(2):91–105Google Scholar
  55. Wardle DA, Lawrence R, Walker LR, Bardgett BD (2004) Ecosystem properties and forest decline in contrasting long-term chronosequences. Science 305(5683):509–513. doi: 10.1126/science.1098778 CrossRefGoogle Scholar
  56. Whitledge TE, Mallow SC, Patton CJ, Wirick CD (1981) Automated nutrient analysis in seawater. Ocean Science Division Brookhaven National Laboratory Technical ReportGoogle Scholar
  57. Wurtz TL (1995) Understory alder in 3 boreal forests of Alaska: local distribution and effects on soil fertility. Can J Res 25(6):987–996. doi: 10.1139/x95-107 CrossRefGoogle Scholar
  58. Wurtz TL (2000) Interactions between white spruce and shrubby alders at three boreal forest sites in Alaska. USDA Forest Service General Technical Report PNW-GTR-481Google Scholar
  59. Zackrisson O, DeLuca TH, Nilsson MC, Sellstedt A, Berglund LM (2004) Nitrogen fixation increases with successional age in boreal forests. Ecology 85(12):3327–3334. doi: 10.1890/04-0461 CrossRefGoogle Scholar
  60. Zar JH (1998) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood CliffsGoogle Scholar
  61. Zou XM, Binkley D, Caldwell BA (1995) Effects of dinitrogen-fixing trees on phosphorus biogeochemical cycling in contrasting forests. Soil Sci Soc Am J 59(5):1452–1458Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Institute of Arctic BiologyUniversity of Alaska, FairbanksFairbanksUSA

Personalised recommendations