, Volume 30, Issue 2, pp 523–537 | Cite as

Responses of symbiotic N2 fixation in Alnus species to the projected elevated CO2 environment

  • Hiroyuki Tobita
  • Kenichi Yazaki
  • Hisanori Harayama
  • Mitsutoshi Kitao


Key message

Nitrogen fixation inAlnusspecies in response to elevated CO2may depend on the presence of non-N2-fixing tree species in addition to soil conditions.


Alnus is a major genus of actinorhizal plants. Symbiosis with Frankia allows the Alnus species to fix nitrogen (N) at the rate of several to 320 kg N ha−1 year−1 with a nodule biomass of 16–480 kg ha−1. Alnus species ensures an effective supply of N to soils because of the high N content of leaf litter, rapid decomposition rate, and the influx of herbivorous insects. In addition, the association between regenerated endozoochorous species and Alnus hirsuta suggests that N2 fixation in Alnus species influences the distribution patterns of regenerated plants as well as improve soil fertility. N2 fixation by the AlnusFrankia symbiotic relationship may be positively associated with elevated carbon dioxide (CO2) levels. Nodule biomass increased under elevated CO2 due to enhanced plant growth, rather than changes in biomass allocation. The inhibitory effect of high soil N on nodulation was retained under elevated CO2, and the effects of elevated CO2 on N2 fixation depended on soil P availability, drought, and many other abiotic and biotic factors. Recent free-air CO2 enrichment experiments have demonstrated increased N2 fixation in A.glutinosa exposed to elevated CO2 in mixed-species stands containing non-N2-fixers but not in monocultures, suggesting that N2 fixation depends on an association with non-N2-fixing tree species. Because elevated CO2 can alter the N and P contents and stoichiometry of plants, it will be necessary to evaluate N allocation and accumulation of biomass when investigating the response of Alnus species to future global climate change.


Actinorhizal plants Frankia Nodule biomass Soil nutrients Stoichiometry 


  1. Agari T, Matsuki S, Tobita H et al (2007) The effects of elevated CO2 and soil fertility on the defense capacity against herbivore in two species of alder seedlings. Trans Mtg Hokkaido Br For Soc 55:56–58 (in Japanese) Google Scholar
  2. Ainsworth EA, Long SP (2004) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372CrossRefGoogle Scholar
  3. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270PubMedCrossRefGoogle Scholar
  4. Akkermans ADL, van Dijk C (1976) The formation and nitrogen-fixing activity of the root nodules of Alnus glutinosa under field conditions. In: Nutman PS (ed) Symbiotic nitrogen fixation in plants. Cambridge University Press, London, pp 511–520Google Scholar
  5. Anderson MD, Ruess RW, Myrold DD, Taylor DL (2009) Host species and habitat affect nodulation by specific Frankia genotypes in two species of Alnus in interior Alaska. Oecologia 160:619–630PubMedCrossRefGoogle Scholar
  6. Anderson MD, Taylor DL, Ruess RW (2013) Phylogeny and assemblage composition of Frankia in Alnus tenuifolia nodules across a primary successional sere in interior Alaska. Molecular Ecol 22:3864–3877CrossRefGoogle Scholar
  7. Aosaar J, Varik M, Lõhmus K et al (2013) Long-term study of above-and below-ground biomass production in relation to nitrogen and carbon accumulation dynamics in a grey alder (Alnus incana (L.) Moench) plantation on former agricultural land. Europ J For Res 132(5–6):737–749CrossRefGoogle Scholar
  8. Aranjuelo I, Molero G, Erice G et al (2011) Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). J Exp Bot 62:111–123PubMedPubMedCentralCrossRefGoogle Scholar
  9. Arnone JA III, Gordon JC (1990) Effect of nodulation, nitrogen fixation and CO2 enrichment on the physiology, growth and dry mass allocation of seedlings of Alnus rubra Bong. New Phytol 116:55–66CrossRefGoogle Scholar
  10. Avendano-Yanez MD, Sanchez-Velasquez LR, Meave JA, Pineda-Lopez MD (2014) Is facilitation a promising strategy for cloud forest restoration? For Ecol Manage 329:328–333CrossRefGoogle Scholar
  11. Awmack CS, Mondor EB, Lindroth RL (2007) Forest understory clover populations in enriched CO2 and O3 atmosphere: interspecific, intraspecific, and indirect effects. Environ Exp Bot 59:340–346CrossRefGoogle Scholar
  12. Bassin S, Volk M, Fuhrer J (2013) Species composition of subalpine grassland is sensitive to nitrogen deposition, but not to ozone, after seven years of treatment. Ecosystems 16:1105–1117CrossRefGoogle Scholar
  13. Benson D, Dawson JO (2007) Recent advances in biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330CrossRefGoogle Scholar
  14. Binkley D (1981) Nodule biomass and acetylene reduction rates of red alder and Sitka alder on Vancouver Island, B.C. Can J For Res 11:181–286Google Scholar
  15. Binkley D (1982) Nitrogen fixation and net primary production in a young Sitka alder stand. Can J Bot 60:281–284CrossRefGoogle Scholar
  16. Binkley D, Sollins P, Bell R et al (1992) Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73:2022–2033CrossRefGoogle Scholar
  17. Bormann BT, DeBell DS (1981) Nitrogen content and other soil properties related to age of red alder stands. Soil Sci Soc Am 45:428–432CrossRefGoogle Scholar
  18. Bormann BT, Gordon JC (1984) Stand density effects in young red alder plantations: productivity, photosynthate partitioning, and nitrogen fixation. Ecology 65:394–402CrossRefGoogle Scholar
  19. Bormann BT, Sidle RC (1990) Changes in productivity and distribution of nutrients in a chronosequence at Glacier Bay national park, Alaska. J Ecol 78:561–578CrossRefGoogle Scholar
  20. Brockley RP, Sanborn P (2003) Effects of Sitka alder on the growth and foliar nutrition of young lodgepole pine in the central interior of British Columbia. Can J For Res 33:1761–1771CrossRefGoogle Scholar
  21. Brown KR, Courtin PJ, Negrave RW (2011) Growth, foliar nutrition and δ13C responses of red alder (Alnus rubra) to phosphorus additions soon after planting on moist sites. For Ecol Manage 262:791–802CrossRefGoogle Scholar
  22. Bucher JB, Tarjan DP, Siegwolf RTW et al (1998) Growth of a deciduous tree seedlings community in response to elevated CO2 and nutrient supply. Chemosphere 36:777–782CrossRefGoogle Scholar
  23. Calfapietra C, Ainsworth EA, Beier C et al (2010) Challenges in elevated CO2 experiments on forests. Trends Plant Sci 15:5–10PubMedCrossRefGoogle Scholar
  24. Chaia EE, Myrold DD (2010) Variation of 15N natural abundance in leaves and nodules of actinorhizal shrubs in Northwest Patagonia. Symbiosis 50:97–105CrossRefGoogle Scholar
  25. Chapin FSIII, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier bay. Alaska. Ecol Monog 64(2):149–175CrossRefGoogle Scholar
  26. Chapin FSIII, Matson PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  27. Claessens H, Oosterbaan A, Savill P, Rondeux J (2010) A review of the characteristics of black alder (Alnus glutinosa (L.) Gaertn.) and their implications for silvicultural practices. Forestry 83:164–175CrossRefGoogle Scholar
  28. Cleveland CC, Townsend AR, Schimel DS et al (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biochem Cycle 13:623–645CrossRefGoogle Scholar
  29. Cole DW, Gessel SP, Turner J (1978) Comparative mineral cycling in red alder and Douglas-fir. In: Briggs DG, DeBell DS, Atkinson WA (eds) Utilization and management of alder. USFS Pacific Northwest Forest and Range Experiment Station, Portland, OR, pp 327–336Google Scholar
  30. Compton JE, Church MR, Larned ST, Hogsett WE (2002) Nitrogen export from forested watersheds in the Oregon coast range: the role of N2-fixing red alder. Ecosystems 6:773–785CrossRefGoogle Scholar
  31. Daly GT (1966) Nitrogen fixation by nodulated Alnus rugosa. Can J Bot 44:1607–1621CrossRefGoogle Scholar
  32. Dawson JO (2008) Ecology of actinorhizal plants. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 119–234Google Scholar
  33. Dawson JO, Gordon JC (1979) Nitrogen fixation in relation to photosynthesis in Alnus glutinosa. Bot Gaz 140:S70–S75CrossRefGoogle Scholar
  34. DeBell DS, Radwan MA (1979) Growth and nitrogen relations of coppiced black cottonwood and red alder in pure and mixed plantings. Bot Gaz 140:S97–S101CrossRefGoogle Scholar
  35. Dray MW, Crowther TW, Thomas SM et al (2014) Effects of elevated CO2 on litter chemistry and subsequent invertebrate detritivores feeding responses. PLoS One 9(1):e86246PubMedPubMedCentralCrossRefGoogle Scholar
  36. Eguchi N, Karatsu K, Ueda T et al (2008a) Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan. Trees 22:437–447CrossRefGoogle Scholar
  37. Eguchi N, Morii N, Ueda T et al (2008b) Changes in petiole hydraulic properties and leaf water flow in birch and oak saplings in a CO2-enriched atmosphere. Tree Physiol 28:287–295PubMedCrossRefGoogle Scholar
  38. Ekblad A, Huss-Danell K (1995) Nitrogen fixation by Alnus incana and nitrogen transfer from A. incana to Pinus sylvestris influenced by macronutrients and ectomycorrhiza. New Phytol 131:453–459CrossRefGoogle Scholar
  39. Eriksson E, Johansson T (2006) Effects of rotation period on biomass production and atmospheric CO2 emissions from broadleaved stands growing on abandoned farmland. Silva Fennica 40:603–613Google Scholar
  40. Feng GQ, Li Y, Cheng ZM (2014) Plant molecular and genomic responses to stresses in projected future CO2 environment. Crit Rev Plant Sci 33:238–249CrossRefGoogle Scholar
  41. Finzi AC, Norby RJ, Calfapietra C et al (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Nat Acad Sci USA 104:14014–14019PubMedPubMedCentralCrossRefGoogle Scholar
  42. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal ad non-stomatal limitations revisited. Ann Bot 89:183–189PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fowler D, Amann M, Anderson R et al (2008) Ground-level ozone in the 21st century: future trends, impacts and policy implications. R Soc Polic Doc, LondonGoogle Scholar
  44. Gentili F, Huss-Danell K (2003) Local and systemic effects of phosphorus and nitrogen on nodulation and nodule function in Alnus incana. J Exp Bot 54:2757–2767PubMedCrossRefGoogle Scholar
  45. Gentili F, Wall LG, Huss-Danell K (2006) Effects of phosphorus and nitrogen on nodulation are seen already at the stage of early cell divisions in Alnus incana. Ann Bot 98:309–315PubMedPubMedCentralCrossRefGoogle Scholar
  46. Gillespie KM, Xu F, Richter KT et al (2012) Greater antioxidant and respiratory metabolism in field-grown soybean exposed to elevated O3 under both ambient and elevated CO2. Plant Cell Environ 35:169–184PubMedCrossRefGoogle Scholar
  47. Godbold D, Tullus A, Kupper P et al (2014) Elevated atmospheric CO2 and humidity delay leaf fall in Betula pendula, but not in Alnus glutinosa or Populus tremula x tremuloides. Ann For Sci 71:831–842CrossRefGoogle Scholar
  48. Gordon JC, Wheeler CT (1978) Whole plant studies on photosynthesis and acetylene reduction in Alnus glutinosa. New Phytol 80:179–186CrossRefGoogle Scholar
  49. Gtari M, Tisa LS, Normand P (2013) Diversity of Frankia Strains, actinobacterial symbionts of actinorhizal plants. In: Ricardo A (ed) Symbiotic Endophytes. Springer, Berlin Heidelberg, pp 123–148CrossRefGoogle Scholar
  50. Hanley TA, Deal RL, Orlikowska EH (2006) Relationships between red alder composition and understory vegetation in young mixed forests of southeast Alaska. Can J For Res 36:738–748CrossRefGoogle Scholar
  51. Hewitt DKL, Mills G, Hayes F et al (2014) Highlighting the threat from current and near-future ozone pollution to clover in pasture. Environ Pollut 189:111–117PubMedCrossRefGoogle Scholar
  52. Hibbs DE, Cromack CJR (1990) Actinorhizal plants in Pacific Northwest forests. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic Press Inc, San Diego, pp 343–363Google Scholar
  53. Hibbs DE, Chan SS, Castellano M, Niu C-H (1995) Response of red alder seedlings to CO2 enrichment and water stress. New Phytol 129:569–577CrossRefGoogle Scholar
  54. Hiltbrunner E, Aerts R, Bühlmann T et al (2014) Ecological consequences of the expansion of N2-fixing plants in cold biomes. Oecologia 176:11–24PubMedCrossRefGoogle Scholar
  55. Hoosbeek MR, Lukae M, Velthorst E et al (2011) Free atmospheric CO2 enrichment increased above ground biomass but did not affect symbiotic N2-fixation and soil carbon dynamics in a mixed deciduous stand in Wales. Biogeoscience 8:353–364CrossRefGoogle Scholar
  56. Hungate BA, Dukes JT, Shaw MR et al (2003) Nitrogen and climate change. Science 302:1512–1513PubMedCrossRefGoogle Scholar
  57. Hungate BA, Stiling PD, Dijkstra P et al (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291PubMedCrossRefGoogle Scholar
  58. Hurd TM, Raynal DJ, Schwintzer CR (2001) Symbiotic N2 fixation of Alnus incana ssp. rugosa in shrub wetlands of the Adirondack Mountains, New York. USA. Oecologia 126:94–103CrossRefGoogle Scholar
  59. Huss-Danell K (1990) The physiology of actinorhizal nodules. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic Press Inc, Tokyo, pp 129–156Google Scholar
  60. Huss-Danell K (1997) Actinorhizal symbioses and their N2 fixation. New Phytol 136:375–405CrossRefGoogle Scholar
  61. Huss-Danell K, Ohlsson H (1992) Distribution of biomass and nitrogen among plant parts and soil nitrogen in a young Alnus incana stand. Can J Bot 70:1545–1549CrossRefGoogle Scholar
  62. Huss-Danell K, Sellstedt A (1983) Nitrogenase activity in response to restricted shoot growth in Alnus incana. Can J Bot 61:2949–2955CrossRefGoogle Scholar
  63. Huss-Danell K, Lundquist PO, Ohlsson H (1992) N2 fixation in a young Alnus incana stand, based on seasonal and diurnal variation in whole plant nitrogenase activity. Can J Bot 70:1537–1544CrossRefGoogle Scholar
  64. Hytönen J, Saarsalmi A (2015) Biomass production of coppiced grey alder and the effects of fertilization. Silva Fennica 49 no. 1 article id 1260.
  65. Hyvönen R, Ågren GI, Linder S et al (2007) The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review. New Phytol 173:463–480PubMedCrossRefGoogle Scholar
  66. Ingestad T (1981) Nutrition and growth of birch and grey alder seedlings in low conductivity solutions and at varied relative rates of nutrient addition. Physiol Plant 52:454–466CrossRefGoogle Scholar
  67. IPCC (2007) Climate change 2007: impacts, adaptation and vulnerability. contribution of working group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Cambridge University Press, Cambridge, UKGoogle Scholar
  68. IPCC (2013) Climate Change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex B, Midgley PM (eds) Cambridge University Press, Cambridge, UKGoogle Scholar
  69. Johnson DW (2006) Progressive N limitation in forest: review and implications for long-term responses to elevated CO2. Ecology 87(1):64–75PubMedCrossRefGoogle Scholar
  70. Johnsrud SC (1978) Nitrogen fixation by root nodules of Alnus incana in a Norwegian forest ecosystem. Oikos 30:475–479CrossRefGoogle Scholar
  71. Kaelke CM, Dawson JO (2005) The accretion of nonstructural carbohydrates changes seasonally in Alnus incana ssp. rugosa in accord with tissue type, growth, N allocation, and root hypoxia. Symbiosis 39:61–66Google Scholar
  72. Kallarackal J, Roby TJ (2012) Responses of trees to elevated carbon dioxide and climate change. Biodivers Conserv 21:1327–1342CrossRefGoogle Scholar
  73. Kawaguchi K, Hoshika Y, Watanabe M, Koike T (2012) Ecophysiological responses of northern birch forests to the changing atmospheric CO2 and O3 concentration. J Atmospheric Environ 6:192–205CrossRefGoogle Scholar
  74. Kikuzawa K, Asai T, Higashiura Y (1979) Leaf production and the effect of defoliation by the larval population of the winter moth, Operophtera brumata L. in an alder (Alnus inokumae MURAI et KUSAKA) stand. J J Ecol 29:111–120Google Scholar
  75. Kim DY (1987) Seasonal estimates of nitrogen fixation by Alnus rubra and Ceanothus species in western Oregon forest ecosystems. Dissertation, Oregon State UniversityGoogle Scholar
  76. Kitao M, Lei TT, Koike T et al (2007) Interaction of drought and elevated CO2 on photosynthetic down-regulation and susceptibility to photoinhibition in Japanese white birch (Betula platyphylla var. japonica) seedlings grown under limited N availability. Tree Physiol 27(5):727–735PubMedCrossRefGoogle Scholar
  77. Kogawara S, Norisada M, Tange T et al (2006) Elevated atmospheric CO2 concentration alters the effects of phosphate supply on growth of Japanese red pine (Pinus densiflora) seedlings. Tree Physiol 26:25–33PubMedCrossRefGoogle Scholar
  78. Koike T, Izuta T, Lei TT et al (1997) Effects of high CO2 on nodule formation in roots of Japanese mountain alder seedlings grown under two nutrient levels. In: Ando T, Fujita K, Mae T, Matsumoto H, Mori S, Sekiya J (eds) Plant nutrition—for sustainable food production and environment. Kluwer Academic Publishers, Japan, pp 887–888CrossRefGoogle Scholar
  79. Koike T, Tobita H, Shibata T et al (2006) Defense characteristics of deciduous broad-leaved tree seedlings grown under factorial combination of two levels of CO2 and nutrients. Popul Ecol 48:23–29CrossRefGoogle Scholar
  80. Körner C, Asshoff R, Bignucolo O et al (2005) Carbon flux and growth in mature deciduous forest tree exposed to elevated CO2. Science 309:1360–1362PubMedCrossRefGoogle Scholar
  81. Kostiainen K, Saranpaa P, Lundqvist SO et al (2014) Wood properties of Populus and Betula in long-term exposure to elevated CO2 and O3. Plant Cell Environ 37:1452–1463PubMedCrossRefGoogle Scholar
  82. Kucho K, Hay AE, Normand P (2010) The determinants of the actinorhizal symbiosis. Microbes Environ 25:241–252DPubMedCrossRefGoogle Scholar
  83. Lambers H, Chapin III FS, Pons T (2008) Plant physiological ecology, 2nd edn. Springer, BerlinCrossRefGoogle Scholar
  84. Lee YY, Son Y (2005) Diurnal and seasonal patterns of nitrogen fixation in an Alnus hirsuta plantation of central Korea. J Plant Biol 48(3):332–337CrossRefGoogle Scholar
  85. Lee TD, Reich PB, Tjoelker MG (2003) Legume presence increases photosynthesis and N concentrations of co-occurring non-fixers but does not modulate their responsiveness to carbon dioxide enrichment. Oecologia 137:22–31PubMedCrossRefGoogle Scholar
  86. Leisner CP, Ainsworth EA (2012) Quantifying the effects of ozone on plant reproductive growth and development. Global Change Biol 18:606–616CrossRefGoogle Scholar
  87. Leisner CP, Ming R, Ainsworth EA (2014) Distinct transcriptional profiles of ozone stress in soybean (Glycine max) flowers and pods. BMC Plant Biol 14:335–347PubMedPubMedCentralGoogle Scholar
  88. Leuzinger S, Hättenschwiler S (2013) Beyond global change: lessons from 25 years of CO2 research. Oecologia 171:639–651PubMedCrossRefGoogle Scholar
  89. Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36:2–21PubMedCrossRefGoogle Scholar
  90. Lindroth RL (2012) Atmospheric change, plant secondary metabolites, and ecological interactions. In: Iason GR, Dicke M, Hartley S (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, Cambridge, pp 120–153CrossRefGoogle Scholar
  91. Lõhmus K, Kuusemets V, Ivask M et al (2002) Budgets of nitrogen fluxes in riparian gray alder forests. Archiv fur Hydrobiol 13:321–332Google Scholar
  92. Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Riding atmospheric carbon dioxide: plants FACE the future. Annu Rev Plant Biol 55:591–628PubMedCrossRefGoogle Scholar
  93. Long SP, Ainsworth EA, Leakey ADB, Morgan PB (2005) Global food insecurity. Treatment of major food crops with elevated carbon dioxide or ozone under large-scale fully open-air conditions suggests recent models may have overestimated future yields. Phil Trans R Soc B 360:2011–2022PubMedPubMedCentralCrossRefGoogle Scholar
  94. Luo Y, Su B, Currie WS et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54(8):731–739CrossRefGoogle Scholar
  95. Mander Ü, Lõhmus K, Teiter S et al (2008) Gaseous nitrogen and carbon fluxes in riparian alder stands. Boreal Env Res 13:231–241Google Scholar
  96. Mander Ü, Maddison M, Soosaar K et al (2015) The impact of a pulsing groundwater table on greenhouse gas emissions in riparian grey alder stands. Environ Sci Pollut Res 22:2360–2371CrossRefGoogle Scholar
  97. Manning WJ, Godzik B (2004) Bioindicator plants for ambient ozone in central and Eastern Europe. Environ Pollut 130:33–39PubMedCrossRefGoogle Scholar
  98. Manning WJ, Godzik B, Musselman RM (2002) Potential bioindicator plant species for ambient ozone in forested mountain areas of central Europe. Environ Pollut 119:283–290PubMedCrossRefGoogle Scholar
  99. Markham JH, Chanway CP (1999) Does past contact reduce the degree of mutualism in the Alnus rubra-Frankia symbiosis? Can J Bot 77:434–441Google Scholar
  100. Matyssek R, Bytnerowicz A, Karlsson P-E et al (2007) Promoting the O3 flux concept for European forest trees. Environ Pollut 146:587–607PubMedCrossRefGoogle Scholar
  101. Meehan TD, Lindroth RL (2007) Modeling nitrogen flux by larval insect herbivores from a temperate hardwood forest. Oecologia 153:833–843PubMedCrossRefGoogle Scholar
  102. Millett J, Godbold D, Smith AR, Grant H (2012) N2 fixation and cycling in Alnus glutinosa, Betula pendula and Fagus sylvatica woodland exposed to free air CO2 enrichment. Oecologia 169:541–552PubMedCrossRefGoogle Scholar
  103. Mills G, Buse A, Gimeno B et al (2007) A synthesis of AOT40-based response functions and critical level of ozone for agricultural and horticultural crops. Atmos Environ 41:2630–2643CrossRefGoogle Scholar
  104. Moiroud A, Capellano A (1979) Etude de la dynamique de l’azote à haute altitude. I. Fixation d’azote (réductuion de l’acétylène) par Alnus viridis. Can J Bot 57:1979–1985Google Scholar
  105. Morgan PB, Ainsworth EA, Long SP (2003) How does elevated ozone impact soybean? A meta-analysis of photosynthesis, growth and yield. Plant Cell Environ 26:1317–1328CrossRefGoogle Scholar
  106. Mortensen LM, Skre O (1990) Effects of low ozone concentrations on growth of Betula pubescens Ehrh., Betula verrucosa Ehrh. and Alnus incana (L.) Moench. New Phytol 115:165–170CrossRefGoogle Scholar
  107. Myrold DD, Huss-Danell K (2003) Alder and lupine enhance nitrogen cycling in a degraded forest soil in Northern Sweden. Plant Soil 254:47–56CrossRefGoogle Scholar
  108. Newton M, Hassen BAE, Zavitkovski J (1968) Role of red alder in western forest succession. In: Trappe JM, Franklin JF, Tarrant RF, Hansen GH (eds) Biology of alder. USFS Pacific Northwest Forest and Range Experiment Station, Portland, OR, pp 73–83Google Scholar
  109. Noh NJ, Son Y, Koo JW et al (2010) Comparison of nitrogen fixation for north- and south-facing Robinia pseudoacacia stands in central Korea. J Plant Biol 53:61–69CrossRefGoogle Scholar
  110. Norby RJ (1987) Nodulation and nitrogenase activity in nitrogen-fixing woody plants stimulated by CO2 enrichment of the atmosphere. Physiol Plant 71:77–82CrossRefGoogle Scholar
  111. Norby R, Zak DR (2011) Ecological lessons from free-air CO2 Enrichment (FACE) experiments. Annu Rev Ecol Evol Syst 42:181–203CrossRefGoogle Scholar
  112. Norby RJ, Warren JM, Iversen CM et al (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. PNAS 107(45):19368–19373PubMedPubMedCentralCrossRefGoogle Scholar
  113. Nord EA, Lynch JP (2009) Plant phenology: a critical controller of soil resource acquisition. J Experiment Bot 60(7):1927–1937CrossRefGoogle Scholar
  114. Normand P (2013) A brief history of Frankia and actinorhizal plants meetings. J Bioscience 38:677–684CrossRefGoogle Scholar
  115. Pandey R, Zinta G, AbdElgawad H et al (2015) Physiological and molecular alterations in plants exposed to high [CO2] under phosphorus stress. Biotech Advances 33:303–316CrossRefGoogle Scholar
  116. Pawlowski N, Newton WE (2008) Nitrogen-fixing actinorhizal symbioses. Springer, DordrechtCrossRefGoogle Scholar
  117. Pawlowski N, Sprent JI (2008) Comparison between actinorhizal and legume symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 261–288CrossRefGoogle Scholar
  118. Pezeshki SR, Hinckley TM (1988) The water relations characteristics of Alnus rubra and Populus trichocarpa: responses to field drought. Can J For Res 18:1159–1166CrossRefGoogle Scholar
  119. Pokharel A, Mirza BS, Dawson JO, Hahn D (2011) Frankia populations in soil and root nodules of sympatrically grown Alnus taxa. Microb Ecol 61:92–100PubMedCrossRefGoogle Scholar
  120. Põlme S, Bahram M, Kõljalg U, Tedersoo L (2014) Global biogeography of Alnus-associated Frankia actinobacterial. New Phytol 204:979–988PubMedCrossRefGoogle Scholar
  121. Poorter H, Navas ML (2003) Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol 157:175–198CrossRefGoogle Scholar
  122. Pourhassan N, Wichard T, Roy S, Bellenger JP (2015) Impact of elevated CO2 on metal homeostasis and the actinorhizal symbiosis in early successional alder shrubs. Environ Exp Bot 109:168–176CrossRefGoogle Scholar
  123. Reverchon F, Xu Z, Blumfield TJ et al (2012) Impact of global change and fire on the occurrence and function of understory legumes in forest ecosystems. J Soil Sediments 12:150–160CrossRefGoogle Scholar
  124. 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 8:89–95Google Scholar
  125. Rogers A, Ainsworth EA, Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiol 131:1009–1016CrossRefGoogle Scholar
  126. Roggy JC, Moiroud A, Lensi R, Domenach AM (2004) Estimating N transfers between N2-fixing actinorhizal species and the non-N2-fixing Prunus avinm under partially controlled conditions. Biol Fertil Soils 39:312–319CrossRefGoogle Scholar
  127. Ruess RW, Anderson MD, Mitchell JS, McFarland JW (2006) Effects of defoliation on growth and N fixation in Alnus tenuifolia: consequences for changing disturbance regimes at high latitudes. Ecoscience 13:404–412CrossRefGoogle Scholar
  128. Ruess RW, Anderson MD, McFarland JM et al (2013) Ecosystem-level consequences of symbionts partnerships in an N-fixing shrub from interior Alaskan floodplains. Ecol Monog 83:177–194CrossRefGoogle Scholar
  129. Rytter L (1989) Distribution of roots and root nodules and biomass allocation in young intensively managed gray alder stands on a peat bog. Plant Soil 119:71–79CrossRefGoogle Scholar
  130. Rytter L, Arveby AS, Granhall U (1991) Dinitrogen (C2H2) fixation in relation to nitrogen fertilization of grey alder [Alnus incana (L.) Moench.] plantations in a peat bog. Biol Fertil Soils 10:233–240CrossRefGoogle Scholar
  131. Sanborn P, Preston C, Brockley R (2002) N2-fixation by Sitka alder in a young lodgepole pine stand in central interior British Columbia, Canada. For Ecol Manage 167: 223–231CrossRefGoogle Scholar
  132. Sardans J, Peñuelas J (2012) The role of plants in the effects of global change on nutrient availability and stoichiometry in the plant-soil system. Plant Physiol 160:1741–1761PubMedPubMedCentralCrossRefGoogle Scholar
  133. Schleppi P, Bucher-Wallin I, Hagedorn F, Körner C (2012) Increased nitrate availability in the soil of mixed mature temperate forest subjected to elevated CO2 concentration (canopy FACE). Global Change Biol 18:757–768CrossRefGoogle Scholar
  134. Schwintzer CR, Tjepkema JD (1997) Field nodules of Alnus incana ssp. rugosa and Myrica gale exhibit pronounced acetylene-induced declines in nitrogenase activity. Can J Bot 75:1415–1423CrossRefGoogle Scholar
  135. Scullion J, Smith AR, Gwynn-Jones D et al (2014) Deciduous woodland exposed to elevated atmospheric CO2 has species-specific impact on anecic earthworms. Appl Soil Ecol 80:84–92CrossRefGoogle Scholar
  136. Seeds JD, Bishop JG (2009) Low Frankia inoculation potentials in primary successional sites at Mount St. Helens, Washington, USA. Plant Soil 323:225–233CrossRefGoogle Scholar
  137. Seiler JR, Johnson JD (1984) Growth and acetylene reduction of black alder seedlings in response to water stress. Can J For Res 14:477–480CrossRefGoogle Scholar
  138. Sharma E, Ambasht RS (1984) Seasonal variation in nitrogen fixation by different ages of root nodules of Alnus nepalensis plantation, in the eastern Himalayas. J Appl Ecol 21:265–270CrossRefGoogle Scholar
  139. Sharma E, Ambasht RS (1986) Root nodule age-class transition, production and decomposition in an age sequence of Alnus nepalensis plantation stands in the eastern Himalayas. J Appl Ecol 23:689–701CrossRefGoogle Scholar
  140. Sharma E, Ambasht RS (1988) Nitrogen accretion and its energetics in the Himalayan alder. Funct Ecol 2:229–235CrossRefGoogle Scholar
  141. Sharma G, Sharma R, Sharma E, Singh KK (2002) Performance of age series of Alnus-cardamom plantation in the Sikkim Himalaya: nutrient dynamics. Ann Bot 89:273–282PubMedPubMedCentralCrossRefGoogle Scholar
  142. Sharma G, Sharma R, Sharma E (2008) Influence of stand age on nutrient and energy release through decomposition in alder-cardamom agroforestry systems of the Eastern Himalayas. Ecol Res 23:99–106CrossRefGoogle Scholar
  143. Sharma G, Sharma R, Sharma E (2010) Impact of altitudinal gradients on energetics and efficiencies of N2-fixation in alder-cardamom agroforestry systems of the eastern Himalayas. Ecol Res 25:1–12CrossRefGoogle Scholar
  144. Sicher RC, Barnaby JY (2012) Impact of carbon dioxide enrichment on the responses of maize leaf transcripts and metabolites to water stress. Physiol Plant 144:238–253PubMedCrossRefGoogle Scholar
  145. Sigurdsson BD, Medhurst JL, Wallin G et al (2013) Growth of mature boreal Norway spruce was not affected by elevated [CO2] and/or air temperature unless nutrient availability was improved. Tree Physiol 33:1192–1205PubMedCrossRefGoogle Scholar
  146. Silvester WB, Winship LJ (1990) Transient responses of nitrogenase to acetylene and oxygen by actinorhizal nodules and cultured Frankia. Plant Physiol 91:480–486CrossRefGoogle Scholar
  147. Silvester WB, Berg RH, Schwintzer CR, Tjepkema JD (2008) Oxygen responses, hemoglobin, and the structure and function of vesicles. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing Actinorhizal symbioses. Springer, Dordrecht, pp 105–146CrossRefGoogle Scholar
  148. Simard SW, Radosevich SR, Sachs DL, Hagerman SM (2006) Evidence for competition and facilitation trade-offs: effects of Sitka alder density on pine regeneration and soil productivity. Can J For Res 36:1286–1298CrossRefGoogle Scholar
  149. Smith AR, Lukac M, Bambrick M et al (2013a) Tree species diversity interacts with elevated CO2 to induce a greater root system response. Global Change Biol 19:217–228CrossRefGoogle Scholar
  150. Smith AR, Lukac M, Hood R et al (2013b) Elevated CO2 enrichment induces a differential biomass response in a mixed species temperate forest plantation. New Phytol 198:156–168PubMedCrossRefGoogle Scholar
  151. Son Y, Lee YY, Lee CY, Yi MJ (2007) Nitrogen fixation, soil nitrogen availability, and biomass in pure and mixed plantations of alder and pine in central Korea. J Plant Nutri 30:1841–1853CrossRefGoogle Scholar
  152. Stöcklin J, Körner CH (1999) Interactive effects of elevated CO2, P availability and legume presence on calcareous grassland: results of a glasshouse experiment. Funct Ecol 13:200–209CrossRefGoogle Scholar
  153. Tadaki Y, Mori H, Mori S (1987) Studies on the production structure of forests (XX) Primary productivity of a young alder stand. J J For Soc 69:207–214 (in Japanese) Google Scholar
  154. Takeda H (1998) Decomposition processes of litter along a latitudinal gradient. In: Sassa K (ed) Environmental forest science. Kuluwer, Dordrecht, pp 197–206CrossRefGoogle Scholar
  155. Tateno M (2003) Benefit to N2-fixing alder of extending growth period at the cost of leaf nitrogen loss without resorption. Oecologia 137:338–343PubMedCrossRefGoogle Scholar
  156. Tateno R, Tokuchi N, Yamanaka N et al (2007) Comparison of litterfall production and leaf litter decomposition between an exotic black locust plantation and an indigenous oak forest near Yan’an on the Loess Plateau, China. For Ecol Manage 241:84–90CrossRefGoogle Scholar
  157. Temperton VM, Grayston SJ, Jackson G et al (2003a) Effects of elevated carbon dioxide concentration on growth and nitrogen fixation in Alnus glutinosa in a long-term field experiment. Tree Physiol 23:1051–1059PubMedCrossRefGoogle Scholar
  158. Temperton VM, Millard P, Jarvis PG (2003b) Does elevated atmospheric carbon dioxide affect internal nitrogen allocation in the temperate trees Alnus glutinosa and Pinus sylvestris. Global Change Biol 9:286–294CrossRefGoogle Scholar
  159. Thomas RB, Bashkin MA, Richter DD (2000) Nitrogen inhibition of nodulation and N2 fixation of a tropical N2-fixing tree (Gliricidia sepium) grown in elevated atmospheric CO2. New Phytol 145:233–243CrossRefGoogle Scholar
  160. Tissue DT, Megonigal JP, Thomas RB (1997) Nitrogenase activities and N2 fixation are stimulated by elevated CO2 in a tropical N2-fixing tree. Oecologia 109:28–33CrossRefGoogle Scholar
  161. Tjepkema JD, Schwintzer CR, Monz CA (1988) Time course of acetylene reduction in nodules of five actinorhizal genera. Plant Physiol 86:581–583PubMedPubMedCentralCrossRefGoogle Scholar
  162. Tobita H, Kitao M, Koike T, Maruyama Y (2005) Effects of elevated CO2 and nitrogen availability on nodulation of Alnus hirsuta Turcz. Phyton 45:125–131Google Scholar
  163. Tobita H, Uemura A, Kitao M et al (2008) The effects of elevated CO2, low phosphorus supply, and drought on photosynthetic activity of Alnus hirsuta (Turcz.). Trans Mtg Hokkaido Br Jpn For Soc 56:43–45 (in Japanese) Google Scholar
  164. Tobita H, Hasegawa SF, Tian X et al (2010a) Spatial distribution and biomass of root nodules in a naturally regenerated stand of Alnus hirsuta (Turcz,) var. sibirica. Symbiosis 50:77–86CrossRefGoogle Scholar
  165. Tobita H, Uemura A, Kitao M et al (2010b) Interactive effects of elevated CO2, phosphorus deficiency, and soil drought on nodulation and nitrogenase activity in Alnus hirsuta and Alnus maximowiczii. Symbiosis 50:59–69CrossRefGoogle Scholar
  166. Tobita H, Uemura A, Kitao M et al (2011) Effects of elevated [CO2] and soil nutrients and water conditions on photosynthetic and growth responses of Alnus hirsuta. Funct Plant Biol 38:702–710CrossRefGoogle Scholar
  167. Tobita H, Hasegawa SF, Yazaki K et al (2013a) Growth and N2 fixation in an Alnus hirsuta (Turcz.) var. sibirica stand in Japan. J Biosci 38(4):761–776PubMedCrossRefGoogle Scholar
  168. Tobita H, Kucho K, Yamanaka T (2013b) Abiotic factors influencing nitrogen-fixing actinorhizal symbioses. In: Ricardo A (ed) Symbiotic endophytes. Springer, Berlin Heidelberg, pp 103–122CrossRefGoogle Scholar
  169. Tobita H, Nanami S, Hasegawa SF et al (2015) Spatial distribution of regenerated woody plants in Alnus hirsuta (Turcz.) var. sibirica stand in Japan. Open J For 5:210–220Google Scholar
  170. Tripp LN, Bezdicek DF, Heilman PE (1979) Seasonal and diurnal patterns and rates of nitrogen fixation by young red alder. Forest Sci 25: 371–380Google Scholar
  171. Tromas A, Diagne N, Diedhiou I et al (2013) Establishment of actinorhizal symbioses. In: Ricardo A (ed) Symbiotic Endophytes. Springer, Berlin Heidelberg, pp 89–101CrossRefGoogle Scholar
  172. Tsutsumi H, Nakatsubo T, Ino Y (1993) Field measurements of nitrogen-fixing activity of intact saplings of Alnus maximowiczii in the subalpine zone of Mt Fuji. Ecol Res 8:85–92CrossRefGoogle Scholar
  173. Uemura S, Sato T (1975) Non-leguminous root nodules in Japan (a supplementary report). In: Takahashi H (ed) Nitrogen fixation and nitrogen cycle. JIBP Synthesis. Univ of Tokyo Press, Tokyo, pp 17–24Google Scholar
  174. Uemura A, Tobita H, Kitaoka S, Utsugi H (2009) Effects of high CO2 concentration on water relations of two Alnus species. Trans Mtg Hokkaido Br Jpn For Soc 57:195–197 (in Japanese) Google Scholar
  175. Uliassi DD, Ruess RW (2002) Limitation to symbiotic nitrogen fixation in primary succession on the Tanana river floodplain. Ecology 83:88–103CrossRefGoogle Scholar
  176. Uliassi DD, Huss-Danell K, Ruess RW, Doran K (2000) Biomass allocation and nitrogenase activity in Alnus tenuifolia: responses to successional soil type and phosphorus availability. Ecoscience 7:73–79Google Scholar
  177. Urgiles N, Strauss A, Lojan P, Schussler A (2014) Cultured arbuscular mycorrhizal fungi and native soil inocula improve seedling development of two pioneer trees in the Andean region. New For 45:859–874CrossRefGoogle Scholar
  178. Uri V, Lõhmus K, Tullus H (2004) The budget of demand for nitrogen in grey alder (Alnus incana (L.) Moench) plantation on abandoned agricultural land in Estonia. Balt For 10:12–18Google Scholar
  179. Uri V, Lõhmus K, Mander Ü et al (2011) Long-term effects on the nitrogen budget of a short-rotation grey alder (Alnus incana (L.) Moench) forest on abandoned agricultural land. Ecol Eng 37:920–930CrossRefGoogle Scholar
  180. Uri V, Aosaar J, Varik M et al (2014) The dynamics of biomass production, carbon and nitrogen accumulation in grey alder (Alnus incana (L.) Moench) chronosequence stands in Estonia. For Ecol Manage 327:106–117CrossRefGoogle Scholar
  181. Valdés M (2008) Frankia ecology. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 49–72CrossRefGoogle Scholar
  182. Valverde C, Ferrari A, Wall LG (2002) Phosphorous and the regulation of nodulation in the actinorhizal symbiosis between Discaria trinervis (Rhamnaceae) and Frankia BCU110501. New Phytol 153:43–52CrossRefGoogle Scholar
  183. VanderHeyden D, Skelly J, Innes J et al (2001) Ozone exposure thresholds and foliar injury on forest plants in Switzerland. Environ Pollut 111:321–331PubMedCrossRefGoogle Scholar
  184. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  185. Vitousek PM, Walker LR (1987) Colonization, succession and resource availability: ecosystem-level interactions. In: Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell Scientific, Oxford, pp 207–223Google Scholar
  186. Vitousek PM, Cassman K, Cleveland C et al (2002) Towards and ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45CrossRefGoogle Scholar
  187. Vogel CS, Curtis PS (1995) Leaf gas exchange and nitrogen dynamics of N2-fixing, field-grown Alnus glutinosa under elevated atmospheric CO2. Global Change Biol 1:55–61CrossRefGoogle Scholar
  188. Vogel JG, Gower ST (1998) Carbon and nitrogen dynamics of boreal jack pine stands with and without a green alder understory. Ecosystems 1:386–400CrossRefGoogle Scholar
  189. Vogel CS, Curtis PS, Thomas RB (1997) Growth and nitrogen accretion of dinitrogen-fixing Alnus glutinosa (L.) Gaertn. under elevated carbon dioxide. Plant Ecol 130:63–70CrossRefGoogle Scholar
  190. Voigt GK, Steucek GL (1969) Nitrogen distribution and accretion in an alder ecosystem. Soil Sci Soc Am 33:946–949CrossRefGoogle Scholar
  191. Wall LG, Berry AM (2008) Early interactions, infection and nodulation in actinorhizal symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 147–166CrossRefGoogle Scholar
  192. Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeoscience 7:2261–2282CrossRefGoogle Scholar
  193. Watanabe Y, Satomura T, Sasa K et al (2010) Differential anatomical responses to elevated CO2 in saplings of four hardwood species. Plant Cell Environ 33:1101–1111PubMedGoogle Scholar
  194. Winship LJ, Tjepkema JD (1990) Techniques for measuring nitrogenase activity in Frankia and actinorhizal plants. In: Schwintzer CR, Tjepkema JD (eds) The biology of Frankia and actinorhizal plants. Academic Press Inc, Tokyo, pp 264–280Google Scholar
  195. Wittig VE, Ainsworth EA, Naidu SL et al (2009) Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta-analysis. Global Change Biol 15:396–424CrossRefGoogle Scholar
  196. Wurtz TL (1995) Understory alder in three boreal forests of Alaska: local distribution and effects on soil fertility. Can J For Res 25:987–996CrossRefGoogle Scholar
  197. Xu Z, Shimizu H, Yagasaki Y et al (2013) Interactive effects of elevated CO2, drought, and warming on plants. J Plant Growth Regul 32:692–707CrossRefGoogle Scholar
  198. Yamanaka T, Li CY, Bormann BT, Okabe H (2003) Tripartite associations in an alder: effects of Frankia and Alpova diplophloeus on the growth, nitrogen fixation and mineral acquisition of Alnus tenuifolia. Plant Soil 254:179–186CrossRefGoogle Scholar
  199. Yoon TK, Noh NJ, Han S et al. (2014) Soil moisture effects on leaf litter decomposition and soil carbon dioxide efflux in wetland and upland forests. Soil Sci Soc Am J 78:1804–1816CrossRefGoogle Scholar
  200. Younger PD, Kapustka LA (1983) N2 (C2H2) ase activity by Alnus incana ssp. rugosa (Betulaceae) in the northern hardwood forest. Am J Bot 70:30–39CrossRefGoogle Scholar
  201. Zak DR, Pregitzer KS, Kubiske ME, Burton AJ (2011) Forest productivity under elevated CO2 and O3: positive feedbacks to soil N cycling sustain decade-long net primary productivity enhancement by CO2. Ecol Lett 14:1220–1226PubMedCrossRefGoogle Scholar
  202. Zavitkovski J, Newton M (1968) Effect of organic matter and combined nitrogen on nodulation and nitrogen fixation in red alder. In: Trappe JM, Franklin JF, Tarrant RF, Hansen GH (eds) Biology of alder. USFS Pacific Northwest Forest and Range Experiment Station, Portland, OR, pp 209–223Google Scholar
  203. Zhang X, Sigman DM, Morel FMM, Kraepiel AML (2014) Nitrogen isotope fractionation by alternative nitrogenases and past ocean anoxia. PNAS 111:4782–4787PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Hiroyuki Tobita
    • 1
  • Kenichi Yazaki
    • 1
  • Hisanori Harayama
    • 2
  • Mitsutoshi Kitao
    • 1
  1. 1.Department of Plant EcologyForestry and Forest Products Research Institute (FFPRI)TsukubaJapan
  2. 2.Hokkaido Research CenterForestry and Forest Products Research Institute (FFPRI)SapporoJapan

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