Plant and Soil

, Volume 425, Issue 1–2, pp 351–361 | Cite as

Soil respiration and extracellular enzyme production respond differently across seasons to elevated temperatures

  • Heather A. KittredgeEmail author
  • Teresa Cannone
  • Joseph Funk
  • Samantha K. Chapman
Regular Article


Background and aims

The activity of extracellular enzymes is one control on soil organic matter decomposition and serves as a driver of heterotrophic soil respiration. To understand how temperature sensitive enzyme reactions will influence the processing of soil carbon substrates at elevated temperatures, we deployed a passive warming experiment in a deciduous forest with highly invaded understory plant communities and high soil nitrogen concentrations.


We seasonally assessed six extracellular enzyme activities and measured soil respiration in the field and in laboratory incubations, to determine if soil carbon use and nutrient cycling responded to 3.5 years of warming.


Field measurements indicate soil respiration was 24% lower and the production of the recalcitrant C-acquiring enzyme phenoloxidase was also lower in warmed plots during fall and winter. In the spring, phosphate (P) acquiring enzyme activity increased in response to warming. In lab incubations, soil respiration was not different between warmed and control soils.


Despite minimal changes to C stores after 3.5 years of warming, recalcitrant C-use and nutrient processing enzymes responded differentially to higher temperatures in fall, winter, and spring. This suggests that C- and nutrient cycle responses to warming can change throughout the seasons, perhaps mediated by plant phenological changes.


Carbon cycle Extracellular enzyme activity Seasonal shifts Soil respiration Warming 

Supplementary material

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  1. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944CrossRefGoogle Scholar
  2. Allison SD et al (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:36–340CrossRefGoogle Scholar
  3. Allison SD et al (2014) Substrate concentration constraints on microbial decomposition. Soil Biol Biochem 79:43–49CrossRefGoogle Scholar
  4. Ashton I et al (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272CrossRefGoogle Scholar
  5. Bahn M et al (2010) Soil respiration at mean annual temperature predicts annual total across vegetation types and biomes. Biogeosciences 7:2147–2157CrossRefPubMedPubMedCentralGoogle Scholar
  6. Baldrian P et al (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
  7. Bardgett RD et al (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME 2:805–814CrossRefGoogle Scholar
  8. Bölscher T et al (2017) Temperature sensitivity of substrate-use efficiency can result from altered microbial physiology without change to community composition. Soil Biol Biochem 109:59–69CrossRefGoogle Scholar
  9. Bradford MA et al (2008) Thermal adaptation of soil microbial respiration to elevated temperature. Ecol Lett 11:1316–1327CrossRefPubMedGoogle Scholar
  10. Bradford et al. (2010) Thermal adaptation of heterotrophic soil respiration in laboratory microcosms. Glob Chang Biol 16:1576–1588CrossRefGoogle Scholar
  11. Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427CrossRefGoogle Scholar
  12. Burns RG et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  13. Chapman SK et al (2016) Impacts of soil nitrogen and carbon additions on Forest understory communities with a long nitrogen deposition history. Ecosystems 19:142–154CrossRefGoogle Scholar
  14. Cleland EE et al (2007) Shifting plant phenology in response to global change. Ecol Evolut 22:357–365CrossRefGoogle Scholar
  15. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173CrossRefPubMedGoogle Scholar
  16. DeAngelis KM et al (2015) Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6:1–13CrossRefGoogle Scholar
  17. Deforest JL (2009) The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. Soil Biol Biochem 41:1180–1186CrossRefGoogle Scholar
  18. Dorrepaal E et al (2009) Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460:616–619CrossRefGoogle Scholar
  19. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  20. Eliasson PE et al (2005) The response of heterotrophic CO2 flux to soil warming. Glob Chang Biol 11:167–181CrossRefGoogle Scholar
  21. Estiarte M, Penuelas J (2015) Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob Chang Biol 21:1005–1017CrossRefPubMedGoogle Scholar
  22. Fierer N et al (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326CrossRefGoogle Scholar
  23. Frey SD et al (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang 3:395–398CrossRefGoogle Scholar
  24. Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362CrossRefPubMedGoogle Scholar
  25. German DP et al (2011) Soil Biology & Biochemistry Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397CrossRefGoogle Scholar
  26. German DP et al (2012) The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Glob Chang Biol 18:1468–1479CrossRefGoogle Scholar
  27. Giasson MA et al (2013) Soil respiration in a northeastern US temperate forest: a 22-year synthesis. Ecosphere 4:1–28CrossRefGoogle Scholar
  28. Gilliam FS et al (2006) Effects of atmospheric nitrogen deposition on the herbaceous layer of a central Appalachian hardwood Forest. J Torrey Bot Soc 133:240–254CrossRefGoogle Scholar
  29. Grandy AS et al (2007) Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol Biochem 39:2701–2711CrossRefGoogle Scholar
  30. Hartley et al. (2007) Effects of 3 years of soil warming and shading on the rate of soil respiration: substrate availability and not thermal acclimation mediates observed response. Glob Chang Biol 13:1761–1770CrossRefGoogle Scholar
  31. Jian S et al (2016) Soil extracellular enzyme activities, soil carbon and nitrogen storage under nitrogen fertilization: a meta-analysis. Soil Biol Biochem 101:32–43CrossRefGoogle Scholar
  32. Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436CrossRefGoogle Scholar
  33. Kallenbach CM et al (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630CrossRefPubMedPubMedCentralGoogle Scholar
  34. Karhu K et al (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513:81–84CrossRefPubMedGoogle Scholar
  35. Kirschbaum MUF (2006) Temporary carbon sequestration cannot prevent climate change. Mitig Adapt Strat GL 11:1151–1164CrossRefGoogle Scholar
  36. Knorr W et al (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433:298–301CrossRefPubMedGoogle Scholar
  37. Luo Y et al (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625CrossRefPubMedGoogle Scholar
  38. Melillo JM et al (2002) Soil warming and carbon-cycle feedbacks to the climate system. Science 298:2173–2176CrossRefPubMedGoogle Scholar
  39. Melillo JM et al (2017) Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358:101–105CrossRefPubMedGoogle Scholar
  40. Menzel A (2002) Phenology: its importance to the global change community. Clim Chang 54:379–385CrossRefGoogle Scholar
  41. Moyes AB, Bowling DR (2016) Plant community composition and phenological stage drive soil carbon cycling along a tree-meadow ecotone. Plant Soil 401:231–242CrossRefGoogle Scholar
  42. Oechel WC et al (2000) Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406:978–981CrossRefPubMedGoogle Scholar
  43. Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190CrossRefGoogle Scholar
  44. Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus 44B:81–99CrossRefGoogle Scholar
  45. Reyer CPO et al (2013) A plant’s perspective of extremes: terrestrial plant responses to changing climatic variability. Glob Chang Biol 19:75–89CrossRefPubMedGoogle Scholar
  46. Richardson AD et al (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173CrossRefGoogle Scholar
  47. Rochette P, Gregorich EG, Desjardins RL (1992) Comparison of static and dynamic closed chambers for measurement of soil respiration under field conditions. Can J Soil Sci 72:605–609CrossRefGoogle Scholar
  48. Saiya-cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer Saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  49. Schimel DS (1995) Terrestrial ecosystems and the carbon cycle. Glob Chang Biol 1:77–91CrossRefGoogle Scholar
  50. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  51. Sinsabaugh RL et al (1991) An enzymic approach to the analysis of microbial activity during plant litter decomposition. Agric Ecosyst Environ 34:43–54CrossRefGoogle Scholar
  52. Sinsabaugh RL et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264CrossRefPubMedGoogle Scholar
  53. Waldrop MP, Zak DR (2006) Response of oxidative enzyme activities to nitrogen deposition affects soil concentrations of dissolved organic carbon. Ecosystems 9:921–933CrossRefGoogle Scholar
  54. Wallenstein et al. (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Chang Biol 15:1631–1639CrossRefGoogle Scholar
  55. Wallenstein M et al (2011) Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates. In: Shukla G, Varma A (eds) Soil enzymology, soil biology. Springer, Berlin, Heidelberg, pp 245–258Google Scholar
  56. Weedon JT et al (2014) No effects of experimental warming but contrasting seasonal patterns for soil peptidase and glycosidase enzymes in a sub- arctic peat bog. Biogeochemistry 117:55–66CrossRefGoogle Scholar
  57. Wu L et al (2017) Alpine soil carbon is vulnerable to rapid microbial decomposition under climate cooling. ISME (9):2102–2111Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.W.K. Kellogg Biological Station, Department of Integrative BiologyMichigan State UniversityHickory CornersUSA
  2. 2.Department of BiologyVillanova UniversityVillanovaUSA

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