Skip to main content
Log in

Phenophases alter the soil respiration–temperature relationship in an oak-dominated forest

  • Original Article
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

Soil respiration (SR) represents a major component of forest ecosystem respiration and is influenced seasonally by environmental factors such as temperature, soil moisture, root respiration, and litter fall. Changes in these environmental factors correspond with shifts in plant phenology. In this study, we examined the relationship between canopy phenophases (pre-growth, growth, pre-dormancy, and dormancy) and SR sensitivity to changes in soil temperature (TS). SR was measured 53 times over 550 days within an oak forest in northwest Ohio, USA. Annual estimates of SR were calculated with a Q10 model based on TS on a phenological (PT), or annual timescale (AT), or TS and soil volumetric water content (VWC) on a phenological (PTM) or annual (ATM) timescale. We found significant (p<0.01) difference in apparent Q10 from year 2004 (1.23) and year 2005 (2.76) during the growth phenophase. Accounting for moisture-sensitivity increased model performance compared to temperature-only models: the error was −17% for the ATM model and −6% for the PTM model. The annual models consistently underestimated SR in summer and overestimated it in winter. These biases were reduced by delineating SR by tree phenophases and accounting for variation in soil moisture. Even though the bias of annual models in winter SR was small in absolute scale, the relative error was about 91%, and may thus have significant implications for regional and continental C balance estimates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Brewer LG, Vankat JL (2004) Description of vegetation of the oak openings of northwestern Ohio at the time of Euro-American settlement. Ohio J Sci 4:76–85

    Google Scholar 

  • Brooks PD, McKnight D, Elder K (2004) Carbon limitation of soil respiration under winter snowpacks: potential feedbacks between growing season and winter carbon fluxes. Global Change Biol 11:231–238

    Article  Google Scholar 

  • Campbell JL, Sun OJ, Law BE (2004) Supply-side controls on soil respiration among Oregon forest. Global Change Biol 10:1857–1869

    Article  Google Scholar 

  • Chen WJ, Black TA, Yang PC, Barr AG, Neumann HH, Nesic Z, Blanken PD, Novak MD, Eley J, Ketler RJ, Cuenca A (1999) Effects of climatic variability on the annual carbon sequestration by a boreal aspen forest. Global Change Biol 5:41–53

    Article  CAS  Google Scholar 

  • Concilio A, Ma S, Li Q, LeMoine J, Chen J, North M, Moorhead D, Jensen R (2005) Soil respiration response to prescribed burning and thinning in mixed-conifer and hardwood forests. Can J For Res 35:1581–1591

    Article  CAS  Google Scholar 

  • Curiel-Yuste JC, Janssens A, Carrara A, Ceulemans R (2004) Annual Q10 of soil respiration reflects plant phenological patterns as well as temperature sensitivity. Global Change Biol 10:161–169

    Article  Google Scholar 

  • Davidson EA, Belk E, Boone RD (1998) Soil water content and temperature as independent or confounded factors controlling soil respiration in a temperate mixed hardwood forest. Global Change Biol 4:217–227

    Article  Google Scholar 

  • Davidson EA, Janssens IA, Luo Y (2006) On the variability of respiration in terrestrial ecosystems: moving beyond Q10. Global Change Biol 12:154–164

    Article  Google Scholar 

  • Del Grosso SJ, Parton WJ, Mosier AA, Holland EA, Pendall E, Schimel DS, Ojima DS (2005) Modeling soil CO2 emissions from ecosystems. Biogeochemistry 73:71–91

    Article  Google Scholar 

  • Ekblad A, Boström B, Holm A, Comstedt D (2005) Forest soil respiration rate and d13C is regulated by recent above ground weather conditions. Oecologia 143:136–142

    Article  PubMed  Google Scholar 

  • Euskirchen E, Chen J, Gustafson EG, Ma S (2003) Soil respiration at dominant patch types within a managed northern Wisconsin landscape. Ecosystems 6:595–607

    Article  Google Scholar 

  • Goulden ML, Munger JW, Fan SM, Daube BC, Wofsy SC (1996) Excahnge of carbon dioxide by a deciduous forest; response to interannual climate variability. Science 271:1576–1578

    Article  CAS  Google Scholar 

  • Gu L, Post WP, King AW (2004) Fast labile carbon turnover obscure sensitivity of heterotrophic respiration form soil to temperature: A model analysis. Global Biogeochem Cycl 18:GB1022, DOI:10.1029/2003GB002119

    Article  CAS  Google Scholar 

  • Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: A review of methods and observations. Biogeochemistry 48:115–146

    Article  CAS  Google Scholar 

  • Hanson PJ, O’Neill EG, Chambers MLS, Riggs JS, Joslin JD, Wolfe MH (2003) Soil respiration and litter decomposition. In: Hanson PJ, Wullschleger SD, Eds, North American Temperate Deciduous Forest Responses to Changing Precipitation Regimes. Springer, New York, pp. 163–189

    Google Scholar 

  • Hanson PJ, Amthor JS, Wullschleger SD, Wilson KB, Grant RF, Hartley A, Hui D, Hunt Jr ER, Johhnson DW, Kimball JS, King AW, Luo Y, McNulty SG, Sun G, Thornton PE, Wang S, Williams M, Baldocchi DD, Cushman RM (2004) Oak forest carbon and water simulations: Model intercomparisons and evaluations against independent data. Ecol Monogr 74:443–489

    Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    Article  PubMed  Google Scholar 

  • Janssens IA, Lankreijer H, Matteucci G, Kowalski AS, Buchman N, Epron D, Pilegaard K, Kutsch W, Longdoz B, Grünwald T, Montagnani L, Dore S, Rebmann C, Moors EJ, Grelle A, Rannik Ü, Morgenstern K, Oltchev S, Clement R, Guðmundsson J, Minerbi S, Berbigier P, Ibrom A, Moncrieff J, Aubinet M, Bernohofer C, Jensen NO, Vesala T, Granier A, Schulze E-D, Lindroth A, Dolman AJ, Jarvis, PG, Ceulemans R, Valentini R (2001) Productivity overshadows temperature in determining soil and ecosystem respiration across European forests. Global Change Biol 7:269–278

    Article  Google Scholar 

  • Janssens IA, Pilegaard K (2003) Large seasonal changes in Q10 of soil respiration in a beech forest. Global Change Biol 9:911–918

    Article  Google Scholar 

  • Jenkinson DS, Adams DE, Wild A (1991) Model estimates of CO2 emissions from soil in response to global warming. Nature (London) 351:304–306

    Article  CAS  Google Scholar 

  • Kelting DL, Burger JA, Edwards GS (1998) Estimating root respirations, microbial respiration in the rhizosphere, and root-free soil respiration in forest soils. Soil Biol Biochem 30:961–968

    Article  CAS  Google Scholar 

  • Law BE, Baldocchi DD, Anthoni PM (1999) Below-canopy and soil CO 2 fluxes in a ponderosa pine forest. Agric For Meteorol 94:171–188

    Article  Google Scholar 

  • Lee MS, Nakane K, Nakatsubo T, Koizumi H (2003) Seasonal changes in the contribution of root respiration to total soil respiration in a cool-temperate deciduous forest. Plant and Soil 225:311–318

    Article  Google Scholar 

  • Lee X, Wu H-J, Sigler J, Oishi C, Siccama T (2004) Rapid and transient response of soil respiration to rain. Global Change Biol 10:1017–1026

    Article  Google Scholar 

  • Ma S, Chen J, Butnor JR, North M, Euskirchen ES, Oakley B (2005) Biophysical controls on soil respiration in dominant patch types of an old-growth mixed conifer forests.For Sci 51:221–232

    Google Scholar 

  • Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659

    Article  CAS  Google Scholar 

  • Morén AS, Lindroth A (2000) CO2 exchange at the floor of a boreal forest. Agric For Meteorol 1:1–14

    Article  Google Scholar 

  • Moseley EL (1928) Flora of the Oak Openings. Ohio Acad Sci special paper 20:79–134

    Google Scholar 

  • Potter CS, Randerson JT, Field JT, Matson CB, Vitousek PM, Mooney HA, Klooster SA (1993) Terrestrial ecosystem production: a process model based on global satellite and surface data. Global Biogeochem Cycl 7:811–841

    Google Scholar 

  • Qi Y, Xu M, Wu J (2002) Temperature sensitivity of soil respiration and its effects on ecosystem carbon budget: nonlinearity begets surprise. Ecol Model 153:131–142

    Article  CAS  Google Scholar 

  • Raich JW, Rastetter EB, Melillo JM, Kicklighter DW, Steudler PA, Peterson BJ, Grace AL, Moore B III, Vörösmarty CJ (1991) Potential net primary productivity in South America: application of a global model. Ecol Appl 1:399–429

    Google Scholar 

  • Schimel DS, Parton WJ, Kittel TGF, Ojima DS, Cole CV (1990) Grassland biogeochemistry: links to atmospheric processes. Climatic Change 17:13–25

    Article  Google Scholar 

  • Schimel DS, Melillo J, Tain H, McGuire AD, Kicklighter D, Kittel K, Rosenbloom N, Runner S, Thornton P, Ojima D, Parton W, Kelly R, Sykes M, Neilson R, Rizzo B (2000) Contribution of increasing CO2 and climate to carbon storage by ecosystems in United States. Science 287:2004–2006

    Article  PubMed  CAS  Google Scholar 

  • Schlesinger WH (1997) Biogeochemistry: An analysis of global change, 2nd ed., Academic, San Diego, CA

    Google Scholar 

  • Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the northern hemisphere. Global Change Biol 12:343–351

    Article  Google Scholar 

  • Takle ES, Brandle JR, Schmidt RA, Garcia R, Litvina IV, Massman WJ, Zhou XH, Doyle G, Rice CW (2003) High-frequency pressure variations in the vicinity of a surface CO2 flux chamber. Agric For Meteorol 114:245–250

    Article  Google Scholar 

  • Toland DE, Zak DR (1994) Seasonal patterns of soil respiration in intact and clear-cut northern hardwood forests. Can J For Res 24:1711–1716

    Google Scholar 

  • Vance ED, Chapin III FS (2001) Substrate limitations to microbial activity in taiga forest floors. Soil Biol Biochem 33:173–188

    Article  CAS  Google Scholar 

  • Wolfe DW, Schwartz MD, Lakso AN, Otsuki Y, Pool RM, Shaulis NJ (2005) Climate change and shifts in spring phenology of three horticultural woody perennials in northeastern USA. Int J Biometeorol 49:303–309

    Article  PubMed  Google Scholar 

  • Zogg GP, Zak DR, Ringelberg DB, MacDonald NW, Pregitzer KS, White DC (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61:475–481

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Southern Global Climate Change Program of the USDA Forest Service. Thanks to Ilona Ilnicki, Rachael Henderson, Katie Hammer, Brett Bias, Rui Zhou, and Qinglin Li for their field assistances and site maintenance. We acknowledge the Metroparks of Toledo Area for facilitating research at the Oak Openings Preserve. Partial support was provided by the US-China Carbon Consortium (USCCC) which promotes collaborative research among interested institutions in the US and China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jared L. DeForest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

DeForest, J.L., Noormets, A., McNulty, S.G. et al. Phenophases alter the soil respiration–temperature relationship in an oak-dominated forest. Int J Biometeorol 51, 135–144 (2006). https://doi.org/10.1007/s00484-006-0046-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-006-0046-7

Keywords

Navigation