Skip to main content
Log in

Leaf phenological shifts and plant–microbe–soil interactions can determine forest productivity and nutrient cycling under climate change in an ecosystem model

  • Original Article
  • Published:
Ecological Research

Abstract

Climate change is expected to affect tree leaf phenology by extending the length of the growing season (LGS), which will affect the productivity and nutrient cycling of forests. Interactions between plants and microbes will mediate the ecosystem processes further through microbe-mediated plant–soil feedback (PSF). To investigate the possible consequences of interactions between the extension of the growing season (GS) and PSF under various conditions, we developed a simple theoretical model (LGS-PSF model). The LGS-PSF model predicts that microbe-mediated PSF will intensify the negative effects of increasing temperature on the size of soil carbon stock when compared with simulations without the PSF effect. The combined effects of increasing temperature and PSF on the size of soil carbon stock occurs through enhanced activity of individual microbes and increased microbial population size. More importantly, the model also demonstrated that a longer GS mitigates this negative effect on carbon accumulation in soil, not through increased net primary production, but through intensified competition for nutrients between plants and microbes, thus suppressing microbial population growth. Our model suggested that the interactive effects of the LGS and PSF on carbon and nitrogen dynamics in forests should be incorporated into larger scale quantitative models for better forecasting of future forest functions under climate change.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nature Geo 3:336–340

    Article  CAS  Google Scholar 

  • Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK (2005) A temporal approach to linking aboveground and belowground ecology. Trend Ecol Evol 20:634–641

    Article  Google Scholar 

  • Bever JD (1994) Feedback between plants and their soil communities in an old field community. Ecology 75:1965–1977

    Article  Google Scholar 

  • Christensen JH et al. (2007) Regional climate projections. In: Solomon S. et al. (eds.) Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK and New York, pp 847–940

  • Chuine I (2010) Why does phenology drive species distribution? Phil Trans Royal Soc B 365:3149–3160

    Article  Google Scholar 

  • Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510

    Article  Google Scholar 

  • Churkina G, Schimel D, Braswell BH, Xiao XM (2005) Spatial analysis of growing season length control over net ecosystem exchange. Global Change Biol 11:1777–1787

    Article  Google Scholar 

  • Cramer W et al (2001) Global response of terrestrial ecosystem structure and function to CO2 and climate change: results from six dynamic global vegetation models. Global Change Biol 7:357–373

    Article  Google Scholar 

  • Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173

    Article  CAS  PubMed  Google Scholar 

  • Doi H (2012) Response of the Morus bombycis growing season to temperature and its latitudinal pattern in Japan. Int J Biometeorol 56:895–902

    Article  PubMed  Google Scholar 

  • Doi H, Katano I (2008) Phenological timing of leaf budburst with climate change in Japan. Agric For Meteorol 148:512–516

    Article  Google Scholar 

  • Doi H, Gordo O, Katano I (2008) Heterogeneous intra-annual climatic changes drive different phenological responses at two trophic levels. Clim Res 36:181–190

    Article  Google Scholar 

  • Doi H, Takahashi M, Katano I (2010) Genetic diversity increases regional variations in phenological responses to climate change. Global Change Biol 17:373–379

    Article  Google Scholar 

  • Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant–soil system. Annu Rev Env Resour 30:75–115

    Article  Google Scholar 

  • Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691

    Article  CAS  PubMed  Google Scholar 

  • Forsythe WC, Rykiel EJ Jr, Stahl RS, We H, Schoolfield RM (1995) A model comparison for daylength as a function of latitude and day of year. Ecol Model 80:87–95

    Article  Google Scholar 

  • Franklin O (2007) Optimal nitrogen allocation controls tree responses to elevated CO2. New Phytol 174:811–822

    Article  CAS  PubMed  Google Scholar 

  • Frey SD, Lee J, Melillo JM, Six J (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nature Clim Change 3:395–398

    Article  CAS  Google Scholar 

  • Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495

    Article  PubMed  Google Scholar 

  • Gordo O, Sanz JJ (2009a) Long term temporal changes of plant phenology in the western Mediterranean. Global Change Biol 15:1930–1948

    Article  Google Scholar 

  • Gordo O, Sanz JJ (2009b) Long term temporal changes of plant phenology in the western Mediterranean. Global Change Biol 15:1930–1948

    Article  Google Scholar 

  • Grant RF, Jarvis PG, Massheder JM, Hale SE, Moncrieff JB, Rayment M, Scott SL, Berry JA (2001) Controls on carbon and energy exchange by a black spruce—moss ecosystem: testing the mathematical model Ecosys with data from the BOREAS experiment. Glob Biogeochem Cycles 15:129–147

    Article  CAS  Google Scholar 

  • Hu JIA, Moore DJP, Burns SP, Monson RK (2010) Longer growing seasons lead to less carbon sequestration by a subalpine forest. Global Change Biol 16:771–783

    Article  Google Scholar 

  • IPCC (2007) Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. Climate change 2007: impacts, adaptations, and vulnerability. Cambridge University Press, New York

  • Ke PJ, Miki T, Ding TS (2015) The soil microbial community predicts the importance of plant traits in plant–soil feedback. New Photol 206:329–341

    Article  CAS  Google Scholar 

  • Kirschbaum MUF, Watt MS, Tait A, Ausseil AGE (2012) Future wood productivity of Pinus radiata in New Zealand under expected climatic changes. Global Change Biol 18:1342–1356

    Article  Google Scholar 

  • Kramer K (1994) A modelling analysis of the effects of climatic warming on the probability of spring frost damage to tree species in The Netherlands and Germany. Plant Cell Environ 17:367–378

    Article  Google Scholar 

  • Kramer K, Leinonen I, Loustau D (2000) The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forests ecosystems: an overview. Int J Biometeorol 44:67–75

    Article  CAS  PubMed  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992

    Article  PubMed  Google Scholar 

  • Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669

    Article  CAS  PubMed  Google Scholar 

  • Manzoni S, Porporato A (2007) Theoretical analysis of nonlinearities and feedbacks in soil carbon and nitrogen cycles. Soil Biol Biochem 39:1542–1556

    Article  CAS  Google Scholar 

  • Manzoni S, Porporato A (2009) Soil carbon and nitrogen models: mathematical structure and complexity across scales. Soil Biol Biochem 41:1355–1379

    Article  CAS  Google Scholar 

  • Matala J, Ojansuu R, Peltola H, Sievanen R, Kellomaki S (2005) Introducing effects of temperature and CO2 elevation on tree growth into a statistical growth and yield model. Ecol Model 181:173–190

    Article  CAS  Google Scholar 

  • Matsumoto K, Ohta T, Irasawa M, Nakamura T (2003) Climate change and extension of the Ginkgo biloba L. growing season in Japan. Global Change Biol 9:1634–1642

    Article  Google Scholar 

  • Medlyn BE, Duursma RA, Zeppel MJB (2011) Forest productivity under climate change: a checklist for evaluating model studies. WIREs Clim Change 2:332–355

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Menzel A et al (2006) European phenological response to climate change matches the warming pattern. Global Change Biol 12:1969–1976

    Article  Google Scholar 

  • Miki T (2012) Microbe-mediated plant–soil feedback and its roles in a changing world. Ecol Res 27:509–520

    Article  CAS  Google Scholar 

  • Miki T, Kondoh M (2002) Feedbacks between nutrient cycling and vegetation predict plant species coexistence and invasion. Ecol Lett 5:624–633

    Article  Google Scholar 

  • Miki T, Ushio M, Fukui S, Kondoh M (2010) Functional diversity of microbial decomposers facilitates plant coexistence in a plant–microbe–soil feedback model. Proc Natl Acad Sci USA 107:14251–14256

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miller-Rushing AJ, Katsuki T, Primack RB, Ishii Y, Lee SD, Higuchi H (2007) Impact of global warming on a group of related species and their hybrids: cherry tree flowering at Mt. Takao, Japan. Am J Bot 94:1470–1478

    Article  PubMed  Google Scholar 

  • Ollinger SV, Goodale CL, Hayhoe K, Jenkins JP (2008) Potential effects of climate change and rising CO2 on ecosystem processes in northeastern U.S. forests. Mitig Adapt Strateg Glob Change 13:467–485

    Article  Google Scholar 

  • Pan Y et al (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993

    Article  CAS  PubMed  Google Scholar 

  • Parton WJ, Schimel DS, Cole CV, Ojima DS (2009) Analysis of factors controlling soil organic-matter levels in Great-Plains grasslands. Soil Sci Soc Am J 51:1173–1179

    Article  Google Scholar 

  • Peng C et al (2009) Quantifying the response of forest carbon balance to future climate change in Northeastern China: model validation and prediction. Global Planet Change 66:179–194

    Article  Google Scholar 

  • Piao S, Friedlingstein P, Ciais P, Viovy N, Demarty J (2007) Growing season extension and its impact on terrestrial carbon cycle in the Northern Hemisphere over the past 2 decades. Global Biogeochem Cy 21:GB3018

  • Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83:553–559

    Article  Google Scholar 

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30:1086–1106

    Article  CAS  PubMed  Google Scholar 

  • Saxe H, Cannell MGR, Johnsen B, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–399

    Article  CAS  Google Scholar 

  • Sitch S et al (2003) Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Global Change Biol 9:161–185

    Article  Google Scholar 

  • Ushio M, Miki T, Balser TC (2013) A coexisting fungal-bacterial community stabilizes soil decomposition activity in a microcosm experiment. PLoS One 8:e80320

    Article  PubMed Central  PubMed  Google Scholar 

  • Van der Putten WH, Van Dijk C, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune communities. Nature 362:53–56

    Article  Google Scholar 

  • White MA, Running SW, Thornton PE (1999) The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int J Biometeorol 42:139–145

    Article  PubMed  Google Scholar 

  • Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106

    Article  Google Scholar 

  • Xu XL et al (2011) Spatio-temporal patterns of plant-microbial competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571

    CAS  Google Scholar 

  • Zheng D, Hunt ER Jr, Running SW (1993) A daily soil temperature model based on air temperature and precipitation for continental applications. Clim Res 2:183–191

    Article  Google Scholar 

Download references

Acknowledgments

National Taiwan University (Grant No. 10R70604-3) and the Ministry of Science and Technology (Grant No. NSC101-2621-B-002-004-MY3) supported this research for T. M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hideyuki Doi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 944 kb)

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miki, T., Doi, H. Leaf phenological shifts and plant–microbe–soil interactions can determine forest productivity and nutrient cycling under climate change in an ecosystem model. Ecol Res 31, 263–274 (2016). https://doi.org/10.1007/s11284-016-1333-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-016-1333-3

Keywords

Navigation