Ecological Research

, Volume 29, Issue 5, pp 789–799

Controlling factors of temporal variation of soil respiration in a natural beech forest as revealed by natural incubation experiments

  • Shuang Lu
  • Shinitirou Katahata
  • Masaaki Naramoto
  • Hiromi Mizunaga
  • Quan Wang
Original Article


Microorganisms decompose organic substrates to obtain energy. This process releases carbon dioxide (CO2) and is the main cause of soil carbon release in terrestrial ecosystems. Fluctuations in microbial composition significantly affect net CO2 emissions in forests. Because factors are cross-correlated, addressing how they affect soil respiration (Rs), both directly and indirectly, is challenging. In this study, Rs-impacting soil properties, including soil organic carbon (SOC), soil organic nitrogen (SON), microbial diversity (Dsim, indicated by Simpson’s diversity index), and total microbial DNA concentration in natural beech forests were examined by structure equation modeling (SEM), which can explicitly evaluate the causal relationships among interacting variables. The results showed that decreasing Dsim, soil temperature, SOC, and SON clearly had direct and indirect effects on Rs under natural conditions. Increasing temperature was a primary factor and promoted a decrease in Rs during the growth season. Dsim was the only parameter with a direct positive effect on Rs, indicating that microbial diversity could accurately predict Rs. Soil nutrient factors indirectly affected Rs through Dsim, which was also affected by soil physical and chemical properties. Significant covariance between SON and Rs (0.42, p < 0.001) indicated multiple interacting variables affecting soil activity. Although the current study suggests that SEM can clarify complex functional processes related to Rs, future studies should consider additional impacting variables such as vegetation properties and enzyme dynamics.


Soil respiration Abiotic Biotic Microbial biodiversity SEM 


  1. Abe M, Izaki J, Miguchi H, Masaki T, Makita A, Nakashizuka T (2002) The effects of Sasa and canopy gap formation on tree regeneration in an old beech forest, Nakashizuka. J Veg Sci 13:565–574Google Scholar
  2. Allison SD, Wallenstein MD, Bradford MA (2010) Soil–carbon response to warming dependent on microbial physiology. Nature Geosci 3:336–340CrossRefGoogle Scholar
  3. Arctic Climate Impact Assessment Team (2004) Impacts of a warming arctic: arctic climate impact assessment. Cambridge University Press, Cambridge, pp 26–32Google Scholar
  4. Bahn M, Rodeghiero M, Anderson-Dunn M, Dore S, Gimeno C, Drösler M, Williams M, Ammann C, Berninger F, Flechard C, Jones S, Balzarolo M, Kumar S, Newesely C, Priwitzer T, Raschi A, Siegwolf R, Susiluoto S, Tenhunen Wohlfahrt JG, Cernusca A (2008) Soil respiration in European grasslands in relation to climate and assimilate supply. Ecosystems 11:1352–1367PubMedCrossRefPubMedCentralGoogle Scholar
  5. Baldrian P, Šnajdr J, Merhautová V, Dobiášová P, Cajthaml T, Valášková V (2013) Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem 56:60–68CrossRefGoogle Scholar
  6. Balser TC, Wixon DL (2009) Investigating biological control over soil carbon temperature sensitivity. Global Change Biol 15:2935–2949CrossRefGoogle Scholar
  7. Bell TH, Klironmos JN, Henry AL (2010) Seasonal responses of extracellular enzyme activity and microbial biomass to warming and nitrogen addition. Soil Sci Soc Am J 74:820–828CrossRefGoogle Scholar
  8. Biasi C, Meyer H, Rusolimova O, Hämmerle R, Kaiser C, Baranyi C, Daims H, Lashchinsky N, Barsukov P, Richter A (2008) Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of lichen-rich dwarf shrub tundra in Siberia. Plant Soil 307:191–205CrossRefGoogle Scholar
  9. Brahim N, Blavet D, Gallali T, Bernoux M (2011) Application of structural equation modeling for assessing relationships between organic carbon and soil properties in semiarid Mediterranean region. Environ Sci Technol 8:305–320Google Scholar
  10. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  11. De Angelis KM, Lindow SE, Firestone MK (2008) Bacterial quorum sensing and nitrogen cycling in rhizosphere soil. FEMS Microbiol Ecol 66:197–207CrossRefGoogle Scholar
  12. Fang C, Moncrieff JB (2001) The dependence of soil CO2 efflux on temperature. Soil Biol Biochem 33:155–165CrossRefGoogle Scholar
  13. Fierer N, Ladau J (2012) Predicting microbial distributions in space and time. Nat Methods 9:549–551PubMedCrossRefGoogle Scholar
  14. Frank H, David H, Kathrin S, Alf E, Björn L, Anja M, Beat FI, Tanya H, Stephan H (2013) Nine years of CO2 enrichment at the alpine tree line stimulates soil respiration but does not alter soil microbial communities. Soil Biol Biochem 57:390–400CrossRefGoogle Scholar
  15. Frey SD, Drijber R, Smith H, Meliio J (2008) Microbial biomass, functional capacity, and community structure after 12 years of soil warming. Soil Biol Biochem 40:2094–2907CrossRefGoogle Scholar
  16. Gärdenäs AI, Ågren GI, Bird JA, Clarholm M, Hallin S, Ineson P, Kätterer T, Knicker H, Nilsson SI, Näsholm T, Ogle S, Paustian K, Persson T, Stendahl J (2011) Knowledge gaps in soil carbon and nitrogen interactions—from molecular to global scale. Soil Biol Biochem 43:702–717CrossRefGoogle Scholar
  17. Geng Y, Wang YH, Yang K, Wang SP, Zeng H, Frank B, Kuehn P, Scholten T, He J (2012) Soil respiration in Tibetan alpine grasslands: belowground biomass and soil moisture, but not soil temperature, best explain the large-scale patterns. PLoS ONE 7:e34968PubMedCrossRefPubMedCentralGoogle Scholar
  18. Gershenson A, Bader NE, Cheng WX (2009) Effects of substrate availability on the temperature sensitivity of soil organic matter decomposition. Global Change Biol 15:176–183CrossRefGoogle Scholar
  19. Giardina CP, Ryan MG (2000) Evidence that decomposition rates of organic carbon in mineral soil do not vary with temperature. Nature 404:858–861PubMedCrossRefGoogle Scholar
  20. Grace JB, Anderson TM, Smith MD, Seabloom E, Andelman SJ, Meche G, Weiher E, Allain LK, Jutila H, Sankaran M, Knops J, Ritchie M, Willig MR (2007) Does species diversity limit productivity in natural grassland communities? Ecol Lett 10:680–689PubMedCrossRefGoogle Scholar
  21. Grace JB, Anderson TM, Olff H, Scheiner SM (2010) On the specification of structural equation models for ecological systems. Ecol Monogr 80:67–87CrossRefGoogle Scholar
  22. Hakkenberg R, Churkina G, Rodeghiero M, Börner A, Steinhof A, Cescatti A (2008) Temperature sensitivity of the turnover times of soil organic matter in forests. Ecol Appl 18:119–131PubMedCrossRefGoogle Scholar
  23. Hamdi S, Moyano F, Sall S, Bernoux M, Chevallier T (2013) Synthesis analysis of the temperature sensitivity of soil respiration from laboratory studies in relation to incubation methods and soil conditions. Soil Biol Biochem 58:115–126CrossRefGoogle Scholar
  24. Hart SC (2006) Potential impacts of climate change on nitrogen transformations and greenhouse gas fluxes in forests: a soil transfer study. Global Change Biol 12:1032–1046CrossRefGoogle Scholar
  25. Hart SC, Perry DA (1999) Transferring soils from high- to low-elevation forests increases nitrogen cycling rates: climate change implications. Global Change Biol 5:23–32CrossRefGoogle Scholar
  26. Högberg P, Nordgren A, Buchmann N, Taylor AF, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792PubMedCrossRefGoogle Scholar
  27. Ineson P, Cotrufo MF, Bol R, Harkness DD, Blum H (1996) Quantification of soil carbon inputs under elevated CO2: C3 plants in a C4 soil. Plant Soil 187:345–350CrossRefGoogle Scholar
  28. Joo SJ, Park SU, Park MS, Lee CS (2012) Estimation of soil respiration using automated chamber systems in an oak (Quercus mongolica) forest at the Nam-San site in Seoul, Korea. Sci Total Environ 416:400–409PubMedCrossRefGoogle Scholar
  29. Jussy JH, Colin-Belgrand M, Dambrine É, Ranger J, Zeller B, Bienaimé S (2004) N deposition, N transformation and N leaching in acid forest soils. Biol Chem 69:241–262Google Scholar
  30. Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A (2010) Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol 187:843–858PubMedCrossRefPubMedCentralGoogle Scholar
  31. Kakubari Y (1977) Distribution of primary productivity along the altitudinal gradient. JIBP Synth 16:201–212Google Scholar
  32. Kanea ES, Valentinea DW, Michaelsonb GJ, Foxa JD, Ping CL (2006) Controls over pathways of carbon efflux from soils along climate and black spruce productivity gradients in interior Alaska. Soil Biol Biochem 38:1438–1450CrossRefGoogle Scholar
  33. Kasuya MCM, Masaka K, Igarashi T (1995) Mycorrhizae of Monotropastrum giobosum growing in a Fagus crenata forest. Mycoscience 36:461–464CrossRefGoogle Scholar
  34. Kimball BA, Conley MM (2009) Infrared heater arrays for warming field plots scaled up to 5-m diameter. Agric Forest Meteorol 149:721–724CrossRefGoogle Scholar
  35. Kitzler B, Zechmeister SB, Holtermann C, Skiba U, Butterbach BK (2006) Nitrogen oxides emission from two beech forests subjected to different nitrogen loads. Biogeosciences 3:293–310CrossRefGoogle Scholar
  36. Koranda M, Kaiser C, Fuchslueger L, Kitzler B, Sessitsch A, Zechmeister- Boltenstern S, Richter A (2013) Seasonal variation in functional properties of microbial communities in beech forest soil. Soil Biol Biochem 60:95–104PubMedCrossRefPubMedCentralGoogle Scholar
  37. Krivtson V, Griffiths BS, Liddell K, Garside A, Salmond R, Bezginova T, Thompson J (2011) Soil nitrogen availability is reflected in the bacterial pathway. Pedosphere 21:26–30CrossRefGoogle Scholar
  38. Lam TY, Maguire D (2012) Structural equation modeling: theory and applications in forest management. Int J Forest Res 2012:1–16CrossRefGoogle Scholar
  39. Li LJ, You MY, Shi HA, Ding XL, Qiao YF, Han XZ (2013) Soil CO2 emissions from a cultivated Mollisol: effects of organic amendments, soil temperature, and moisture. Eur J Soil Biol 55:83–90CrossRefGoogle Scholar
  40. Liu HS (2013) Thermal response of soil microbial respiration is positively associated with labile carbon content and soil microbial activity. Geoderma 193–194:275–281CrossRefGoogle Scholar
  41. Lloyd J, Taylor JA (1994) On the temperature dependence of soil respiration. Funct Ecol 8:315–323CrossRefGoogle Scholar
  42. Luo YQ, Zhou XH (2006) Soil respiration and the environment. Academic Press, San Diego, pp 77–156Google Scholar
  43. Luo YQ, Wan SQ, Hui DF, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625PubMedCrossRefGoogle Scholar
  44. Maire V, Alvarez G, Colombet J, Comby A, Despinasse R, Dubreucq E, Joly M, Lehours AC, Perrier V, Shahzad T, Fontaine S (2012) An unknown respiration pathway substantially contributes to soil CO2 emissions. Biogeosci Disc 9:8663–8691CrossRefGoogle Scholar
  45. Makiranta P, Laiho R, Fritze H, Hytonen J, Laine J, Minkkinen K (2009) Indirect regulation of heterotrophic peat soil respiration by water level via microbial community structure and temperature sensitivity. Soil Biol Biochem 41:695–703CrossRefGoogle Scholar
  46. Martina JG, Bolstadb PV, Ryu SR, Chen JQ (2009) Modeling soil respiration based on carbon, nitrogen, and root mass across diverse Great Lake forests. Agric Forest Meteorol 149:1722–1729CrossRefGoogle Scholar
  47. Michopoulos P, Baloutsos G, Economou A (2008) Nitrogen cycling in a mature mountainous beech forest. Silva Fenn 42:5–17CrossRefGoogle Scholar
  48. Misson L, Baldocchi DD, Black TA, Brunet Y, Curiel Y, Dorsey JR, Falk M, Granier A, Irvine MR, Jarosz N, Lamaud E, Launiainen S, Law BE, Longdoz B, Loustau D, McKay M, Paw UKT, Vesala T, Vickers D, Wilson KB, Goldstein AH (2007) Partitioning forest carbon fluxes with overstory and understory eddy covariance measurements: a synthesis based on FLUX-NET data. Agric Forest Meteorol 144:14–31CrossRefGoogle Scholar
  49. Mo WH, Lee MS, Masaki U, Motoko I, Nobuko S, Shigeru M, Hiroshi K (2005) Seasonal and annual variations in soil respiration in a cool-temperate deciduous broad-leaved forest in Japan. Agric Forest Meteorol 134:81–94CrossRefGoogle Scholar
  50. Mohanty RB, Panda T (2011) Soil respiration and microbial population in a tropical deciduous forest soil of Orissa. Flora 206:1040–1044CrossRefGoogle Scholar
  51. Muyzer G, de Waal EC (1994) Determination of the genetic diversity of microbial communities using DGGE analysis of PCR amplified 16S rRNA. Nato Sci Ser 35:207–214Google Scholar
  52. Nakashizuka T (1987) Regeneration dynamics of beech forest in Japan. Vegetation 69:169–175CrossRefGoogle Scholar
  53. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2007) Microbial diversity and microbial activity in the rhizosphere. Cienc Suelo 2:89–97Google Scholar
  54. Niinisto SM, Silvola J, Kellomaki S (2004) Soil CO2 efflux in a boreal pine forest under atmospheric CO2 enrichment and air warming. Global Change Biol 10:1363–1376CrossRefGoogle Scholar
  55. Oberbauer SF, Tweedie CE, Welker JM, Fahnestock JT, Henry GHR, Webber PJ, Hollister RD, Walker MD, Kuchy A, Elmore E, Starr G (2007) Tundra CO2 fluxes in response to experimental warming across latitudinal and moisture gradients. Ecol Monogr 77:221–238CrossRefGoogle Scholar
  56. Okaura T, Harada K (2002) Phylogeographical structure revealed by chloroplast DNA variation in Japanese Beech (Fagus crenata Blume). Heredity 88:322–329PubMedCrossRefGoogle Scholar
  57. Ouyang Y, Li XY (2013) Recent research progress on soil microbial responses to drying-rewetting cycles. Acta Ecol Sin 33:1–6CrossRefGoogle Scholar
  58. Radojkovic D, Kušic J (2000) Macroprolactin reactivities in prolactin assays: an issue for clinical laboratories and equipment manufacturers. Clin Chem 46:884–885Google Scholar
  59. Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263CrossRefGoogle Scholar
  60. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam SJ, Kyrpides NC, Stepanauskas R, Rubin EM, Hugenholtz P, Woyke T (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437PubMedCrossRefGoogle Scholar
  61. Rinnan R, Michelsen A, Jonasson S (2008) Effects of litter addition and warming on soil carbon, nutrient pools and microbial communities in a subarctic heath ecosystem. Appl Soil Ecol 39:271–281CrossRefGoogle Scholar
  62. Rinnan R, Michelsen A, Bååth E (2011) Long-term warming of a subarctic heath decreases soil bacterial community growth but has no effects on its temperature adaptation. Appl Soil Ecol 47:217–220CrossRefGoogle Scholar
  63. Rodeghiero M, Cescatti A (2005) Main determinants of forest soil respiration along an elevation/temperature gradient in the Italian Alps. Global Change Biol 11:1024–1041CrossRefGoogle Scholar
  64. Saigusa N, Yamamoto S, Murayama S, Kondo H, Nishimura N (2002) Gross primary production and net ecosystem production of a cool-temperate deciduous forest estimated by the eddy covariance method. Agric Forest Meteorol 112:203–215CrossRefGoogle Scholar
  65. Schindlbachera A, Rodlera A, Kuffnerb M, Kitzlera B, Sessitschb A, Boltensterna SZ (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425CrossRefGoogle Scholar
  66. Schulze ED (2000) The carbon and nitrogen cycle of forest ecosystems. In: Schulze, E.D. (ed.), Carbon and nitrogen cycling in European forest ecosystems. Ecol Studies, vol 142, pp 3–13Google Scholar
  67. Strömgren M, Linder S (2002) Effects of nutrition and soil warming on stem-wood production in a boreal Norway spruce stand. Global Change Biol 8:1195–1204CrossRefGoogle Scholar
  68. Sullivan BW, Kolb TE, Hart SC, Kaye JP, Dore S, Montes-Helu M (2008) Thinning reduces soil carbon dioxide but not methane flux from southwestern USA ponderosa pine forests. Forest Ecol Manag 255:4047–4055CrossRefGoogle Scholar
  69. 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 22:955–963CrossRefGoogle Scholar
  70. Tang J, Baldocchi DD, Xu L (2005) Tree photosynthesis modulates soil respiration on a diurnal time scale. Global Change Biol 11:1298–1304CrossRefGoogle Scholar
  71. Tang YS, Wang L, Jia JW, Xia FH, Le YQ, Chen XiZ, Sun Y (2011) Response of soil microbial community in Jiuduansha wetland to different successional stages and its implications for soil microbial respiration and carbon turnover. Soil Biol Biochem 43:638–646CrossRefGoogle Scholar
  72. Thomson BC, Ostle NJ, McNamara NP, Whiteley AS, Griffiths RI (2010) Effects of sieving, drying and rewetting upon soil bacterial community structure and respiration rates. J Microbiol Methods 83:69–73PubMedCrossRefGoogle Scholar
  73. von Lützow M, Kögel-Knabner I (2009) Temperature sensitivity of soil organic matter decomposition-what do we know? Biol Fert Soils 46:1–15CrossRefGoogle Scholar
  74. Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Change Biol 15:1631–1639CrossRefGoogle Scholar
  75. Welker JM, Fahnestock JT, Henry G, O’dea K, Chimner RA (2004) CO2 exchange in the Canadian high arctic: response to long-term warming. Global Change Biol 10:1981–1995CrossRefGoogle Scholar
  76. Whitby TG, Madrith MD (2013) Native temperature regime influences soil response to simulated warming. Soil Biol Biochem 60:202–209CrossRefGoogle Scholar
  77. Wu X, Yao Z, Brüggemann N, Shen ZY, Wolf B, Dannenmann M, Zheng X, Butterbach-Bahl K (2010) Effects of soil moisture and temperature on CO2 and CH4 soil-atmosphere exchange of various land use/cover types in a semi-arid grassland in Inner Mongolia, China. Soil Biol Biochem 42:773–787CrossRefGoogle Scholar
  78. Xu X, Sherry RA, Niu SL, Zhou JH, Luo YQ (2012) Long-term experimental warming decreased labile soil organic carbon in a tall grass prairie. Plant Soil 361:307–315CrossRefGoogle Scholar
  79. Yuste JC, Nagy M, Janssens IA, Carrara A, Ceulemans R (2005) Soil respiration in a mixed temperate forest and its contribution to total ecosystem respiration. Tree Physiol 25:609–619CrossRefGoogle Scholar
  80. Yuste CJ, Ma S, Baldocchi DD (2010) Plant–soil interactions and acclimation to temperature of microbial-mediated soil respiration may affect predictions of soil CO2 efflux. Biol Chem 98:127–138Google Scholar
  81. Zhang XY, Meng XJ, Gao LP, Sun XM, Fan JJ, Xu LJ (2010) Potential impacts of climate warming on active soil organic carbon contents along natural altitudinal forest transect of Changbai Mountain. Acta Ecol Sin 30:113–117CrossRefGoogle Scholar
  82. Zhang SX, Lia Q, Zhang XP, Wei K, Chen LJ, Liang WJ (2012) Effects of conservation tillage on soil aggregation and aggregate binding agents in black soil of Northeast China. Soil Till Res 124:196–202CrossRefGoogle Scholar
  83. Zhang SX, Lia Q, Lüa Y, Zhang XP, Liang WJ (2013) Contributions of soil biota to C sequestration varied with aggregate fractions under different tillage systems. Soil Biol Biochem 62:147–156CrossRefGoogle Scholar
  84. Zhao X, Wang Q, Yoshitaka K (2009) Stand-scale spatial patterns of soil microbial biomass in natural cold-temperate beech forests along an elevation gradient. Soil Biol Biochem 41:1466–1474CrossRefGoogle Scholar
  85. Zhao X, Wang Q, Yoshitaka K (2011) Seasonal dynamics of soil microbial biomass C shows close correlation with environmental factors in natural Fagus crenata forests. Acta Agric Scand B S P 61:322–332Google Scholar
  86. Ziegler SE, Billings SA, Lane CS, Li JW, Fogel ML (2013) Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils. Soil Biol Biochem 60:23–32CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2014

Authors and Affiliations

  • Shuang Lu
    • 1
  • Shinitirou Katahata
    • 1
  • Masaaki Naramoto
    • 2
  • Hiromi Mizunaga
    • 2
  • Quan Wang
    • 2
  1. 1.Graduate School of Science and TechnologyShizuoka UniversityShizuokaJapan
  2. 2.Graduate School of AgricultureShizuoka UniversityShizuokaJapan

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