Long-term fertilization of a boreal Norway spruce forest increases the temperature sensitivity of soil organic carbon mineralization

Ecology and Evolution

Volumn 3, Issue 16, 2013, Pages 5177-5188

  Coucheney, Elsa ^a   Strömgren, Monika ^a   Lerch, Thomas Z ^a,b   Herrmann, Anke M ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Boreal soils; Microbial community; Nutrient fertilization; Soil organic carbon; Temperature sensitivity; Warming

Indexed keywords

EID: 84890882360     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.895     Document Type: Article

References (66)

1. Agren, G. I., and E. Bosatta. 2002. Reconciling differences in predictions of temperature response of SOM. Soil Biol. Biochem. 34:129-132.
2. Allison, S. D., C. A. Hanson, and K. K. Treseder. 2007. N fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol. Biochem. 39:1878-1887.
3. Bergh, J., and S. Linder. 1999. Effects of soil warming during spring on photosynthetic recovery in boreal Norway spruce stands. Glob. Change Biol. 5:245-253.
4. Biasi, C., O. Rusalimova, H. Meyer, C. Kaiser, W. Wanek, P. Barsukov, et al. 2005. Temperature-dependent shift from labile to recalcitrant C sources of arctic heterotrophs. Rapid Commun. Mass Spectrom. 19:1401-1408.
5. Bjerke, J. W., S. Bokhorst, M. Zielke, T. V. Callaghan, F. W. Bowles, and G. K. Phoenix. 2011. Contrasting sensitivity to extreme winter warming events of dominant sub-Arctic heathland bryophyte and lichen species. J. Ecol. 99:1481-1488.
6. Bradford, M. A., C. A. Davies, S. D. Frey, T. R. Maddox, J. M. Melillo, J. E. Mohan, et al. 2008. Thermal adaptation of soil microbial respiration to elevated temperature. Ecol. Lett. 11:1316-1327.
7. Campbell, B. J., S. W. Polson, T. E. Hanson, M. C. Mack, and E. A. G. Schuur. 2010. The effect of nutrient deposition on bacterial communities in Arctic tundra soil. Environ. Microbiol. 12:1842-1854.
8. Cannell, M. G. R., and R. C. Dewar. 1994. C allocation in trees - a review of concepts for modelling. Adv. Ecol. Res. 25:59-104.
9. Conant, R. T., M. G. Ryan, G. I. Ågren, H. E. Birge, E. A. Davidson, P. E. Eliasson, et al. 2011. Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward. Glob. Change Biol. 17:3392-3404.
10. Contosta, A. R., S. D. Frey, and A. B. Cooper. 2011. Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils. Ecosphere 2:art36.
11. Cusack, D. F., M. S. Torn, W. H. McDowell, and W. L. Silver. 2010. The response of heterotrophic activity and C cycling to N additions and warming in two tropical soils. Glob. Change Biol. 16:2555-2572.
12. Demoling, F., L. O. Nilsson, and E. Bååth. 2008. Bacterial and fungal response to N fertilization in three coniferous forest soils. Soil Biol. Biochem. 40:370-379.
13. Eliasson, P. E., and G. I. Ågren. 2011. Feedback from soil inorganic nitrogen on soil organic matter mineralisation and growth in a boreal forest ecosystem. Plant Soil 338:193-203.
14. Fog, K. 1988. The effect of added N on the rate of decomposition of organic-matter. Biol. Rev. Camb. Philos. Soc. 63:433-462.
15. Franklin, O., P. Högberg, A. Ekblad, and G. I. Ågren. 2003. Pine forest floor C accumulation in response to N and PK additions: bomb C-14 modelling and respiration studies. Ecosystems 6:644-658.
16. Frey, S. D., M. Knorr, J. L. Parrent, and R. T. Simpson. 2004. Chronic N enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For. Ecol. Manage. 196:159-171.
17. Frey, S. D., R. Drijber, H. Smith, and J. Melillo. 2008. Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol. Biochem. 40:2904-2907.
18. Fritze, H., J. Pietikäinen, and T. Pennanen. 2000. Distribution of microbial biomass and phospholipid fatty acids in Podzol profiles under coniferous forest. Eur. J. Soil Sci. 51:565-573.
19. Fröberg, M., H. Grip, E. Tipping, M. Svensson, M. Strömgren, and D. B. Kleja. 2013. Long-term effects of experimental fertilization and soil warming on dissolved organic matter leaching from a spruce forest in Northern Sweden. Geoderma 200-201:172-179.
20. Frostegard, A., A. Tunlid, and E. Baath. 1993. Phospholipids fatty-acid composition, biomass, and activity of microbial communities from 2 soil types experimentally exposed to different heavy-metals. Appl. Environ. Microbiol. 59:3605-3617.
21. Gärdenäs, A. I., G. I. Ågren, J. A. Bird, M. Clarholm, S. Hallin, P. Ineson, et al. 2010. Knowledge gaps in soil C and N interactions - From molecular to global scale. Soil Biol. Biochem. 43:702-717.
22. Gillabel, J., B. Cebrian-Lopez, J. Six, and R. Merckx. 2010. Experimental evidence for the attenuating effect of SOM protection on temperature sensitivity of SOM decomposition. Glob. Change Biol. 16:2789-2798.
23. Hartley, I. P., A. Heinemeyer, and P. Ineson. 2007. Effects of three years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob. Change Biol. 13:1761-1770.
24. 2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Glob. Change Biol. 13:1786-1797.
25. Heinemeyer, A., M. Wilkinson, R. Vargas, J. A. Subke, E. Casella, J. I. L. Morison, et al. 2011. Exploring the "overflow tap" theory: linking forest soil CO2 fluxes and individual mycorrhizosphere components to photosynthesis. Biogeosciences 8:3155-3201.
26. Herrmann, A. M., and E. Witter. 2002. Sources of C and N contributing to the flush in mineralization upon freeze-thaw cycles in soils. Soil Biol. Biochem. 34:1495-1505.
27. Högberg, M. N., E. Baath, A. Nordgren, K. Arnebrant, and P. Högberg. 2003. Contrasting effects of N availability on plant C supply to mycorrhizal fungi and saprotrophs - a hypothesis based on field observations in boreal forest. New Phytol. 160:225-238.
28. Högberg, M. N., P. Högberg, and D. D. Myrold. 2007. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590-601.
29. Hyvönen, R., G. I. Ågren, S. Linder, T. Persson, M. S. Cotrufo, A. Ekblad, 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. 173:463-480.
30. Jandl, R., M. Lindner, L. Vesterdal, B. Bauwens, R. Baritz, F. Hagedorn, et al. 2007. How strongly can forest management influence soil C sequestration? Geoderma 137:253-268.
31. Janssens, I. A., W. Dieleman, S. Luyssaert, J. A. Subke, M. Reichstein, R. Ceulemans, et al. 2010. Reduction of forest soil respiration in response to N deposition. Nat. Geosci. 3:315-322.
32. Jin, X. B., J. H. Bai, and Y. K. Zhou. 2010. Temperature sensitivity of soil respiration is affected by N fertilization and land use. Acta Agr. Scand. B-S P. 60:427-436.
33. Leppälammi-Kujansuu, J., I. Ostonen, M. Strömgren, L. O. Nilsson, D. B. Kleja, S. P. Sah, et al. 2013. Effects of long-term temperature and nutrient manipulation on Norway spruce fine roots and mycelia production. Plant Soil 366:287-303.
34. Linder, S. 1995. Foliar analysis for detecting and correcting nutrient imbalances in Norway spruce. Pp. 178-190. Effects of acid deposition and tropospheric ozone on forest ecosystems in Sweden. Ecological Bulletins.
35. Long, X., C. Chen, Z. Xu, S. Linder, and J. He. 2012. Abundance and community structure of ammonia oxidizing bacteria and archaea in a Sweden boreal forest soil under 19-year fertilization and 12-year warming. J. Soils Sediments 12:1124-1133.
36. Lu, M., Y. H. Yang, Y. Q. Luo, C. M. Fang, X. H. Zhou, J. K. Chen, et al. 2011. Responses of ecosystem N cycle to N addition: a meta-analysis. New Phytol. 189:1040-1050.
37. von Lutzow, M., and I. Kogel-Knabner. 2009. Temperature sensitivity of SOM decomposition-what do we know? Biol. Fertil. Soils 46:1-15.
38. Magill, A. H., and J. D. Aber. 1998. Long-term effects of experimental N additions on foliar litter decay and humus formation in forest ecosystems. Plant Soil 203:301-311.
39. Magnani, F., M. Mencuccini, M. Borghetti, P. Berbigier, F. Berninger, S. Delzon, et al. 2007. The human footprint in the carbon cycle of temperate and boreal forests. Nature 447:848-850.
40. Moni, C., A. Chabbi, N. Nunan, C. Rumpel, and C. Chenu. 2010. Spatial dependance of organic carbon-metal relationships. Geoderma 158:120-127.
41. Moyano, F., W. L. Kutsch, and C. Rebmann. 2008. Soil respiration fluxes in relation to photosynthetic activity in broad-leaf and needle-leaf forest stands. Agric. For. Meteorol. 148:135-143.
42. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, R. B. O' Hara, G. L. Simpson, et al. 2011. Vegan: community ecology package. R package version 1.17-6. Available at http.//vegan.r-forge.r-project.org/.
43. O'Leary, W. M., and S. G. Wilkinson. 1988. Gram-positive bacteria. Vol. 1, Pp. Xviii+963. in C. Ratledge, S. G. Wilkinson, eds. Microbial lipids. Academic Press, London, UK; San Diego, CA, USA. Illus 117-202.
44. Olsson, P., S. Linder, R. Giesler, and P. Högberg. 2005. Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Glob. Change Biol. 11:1745-1753.
45. Phillips, R. P., and T. J. Fahey. 2007. Fertilization effects on fineroot biomass, rhizosphere microbes and respiratory fluxes in hardwood forest soils. New Phytol. 176:655-664.
46. R Development Core Team. 2008. R: a language and environment for statistical computing. Available at http://www.R- project.org.
47. Rinnan, R., A. Michelsen, E. Bååth, and S. Jonasson. 2007. Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob. Change Biol. 13:28-39.
48. Rustad, L. E., J. L. Campbell, G. M. Marion, R. J. Norby, M. J. Mitchell, A. E. Hartley, et al. 2001. A meta-analysis of the response of soil respiration, net N mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543-562.
49. Salome, C., N. Nunan, V. Pouteau, T. Z. Lerch, and C. Chenu. 2010. C dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob. Change Biol. 16:416-426.
50. Schindlbacher, A., S. Zechmeister-Boltenstern, and R. Jandl. 2009. Carbon losses due to soil warming: do autotrophic and heterotrophic soil respiration respond equally? Glob. Change Biol. 15:901-913.
51. Schindler, D. W., and P. G. Lee. 2010. Comprehensive conservation planning to protect biodiversity and ecosystem services in Canadian boreal regions under a warming climate and increasing exploitation. Biol. Conserv. 143:1571-1586.
52. Schmidt, M. W. I., M. S. Torn, S. Abiven, T. Dittmar, G. Guggenberger, I. A. Janssens, et al. 2011. Persistence of soil organic matter as an ecosystem property. Nature 478:49-56.
53. Sjöberg, G., H. Knicker, S. I. Nilsson, and D. Berggren. 2004. Impact of long-term N fertilization on the structural composition of spruce litter and mor humus. Soil Biol. Biochem. 36:609-618.
54. Sokolov, A. P., D. W. Kicklighter, J. M. Melillo, B. S. Felzer, C. A. Schlosser, and T. W. Cronin. 2008. Consequences of considering C-N interactions on the feedbacks between climate and the terrestrial C cycle. J. Clim. 21:3776-3796.
55. Strömgren, M. 2001. Soil-surface CO2 Flux and growth in a Boreal Norway Spruce stand: effects of soil warming and nutrition. Doctoral Thesis, Swedish University of Agricultural Sciences, Uppsala.
56. Strömgren, M., and S. Linder. 2002. Effects of nutrition and soil warming on stemwood production in a boreal Norway spruce stand. Glob. Change Biol. 8:1195-1204.
57. Swanston, C., P. S. Homann, B. A. Caldwell, D. D. Myrold, L. Ganio, and P. Sollins. 2004. Long-term effects of elevated N on forest SOM stability. Biogeochemistry 70:227-250.
58. Tilman, D. 1987. Secondary succession and the pattern of plant dominance along experimental N gradients. Ecol. Monogr. 57:189-214.
59. Treseder, K. K. 2004. A meta-analysis of mycorrhizal responses to N, phosphorus, and atmospheric CO2 in field studies. New Phytol. 164:347-355.
60. Treseder, K. K. 2008. N additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol. Lett. 11:1111-1120.
61. Vallack, H. W., V. Leronni, D. B. Metcalfe, P. Högberg, I. Ineson, and J. A. Subke. 2012. Application of nitrogen fertilizer to a boreal pine forest has a negative impact on the respiration of ectomycorrhizal hyphae. Plant Soil 352:405-417.
62. Vanhala, P., K. Karhu, M. Tuomi, K. Bjorklof, H. Fritze, and J. Liski. 2008. Temperature sensitivity of SOM decomposition in southern and northern areas of the boreal forest zone. Soil Biol. Biochem. 40:1758-1764.
63. Vitousek, P. M., J. D. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, et al. 1997. Human alteration of the global N cycle: sources and consequences. Ecol. Appl. 7:737-750.
64. Xu, C. G., C. Liang, S. Wullschleger, C. Wilson, and N. McDowell. 2011. Importance of feedback loops between soil inorganic N and microbial communities in the heterotrophic soil respiration response to global warming. Nat. Rev. Microbiol. 9:222.
65. Zelles, L. 1997. Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275-294.
66. Zelles, L. 1999. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol. Fertil. Soils 29:111-129.