Autumnal warming does not change root phenology in two contrasting vegetation types of subarctic tundra


Background and aims

Root phenology is important in controlling carbon and nutrient fluxes in terrestrial ecosystems, yet, remains largely unexplored, especially in the Arctic. We compared below- and aboveground phenology and ending of the growing season in two contrasting vegetation types of subarctic tundra: heath and meadow, and their response to experimental warming in autumn.


Root phenology was measured in-situ with minirhizotrons and compared with aboveground phenology assessed with repeat digital photography.


The end of the growing season, both below- and aboveground, was similar in meadow and heath and the belowground growing season ended later than aboveground in the two vegetation types. Root growth was higher and less equally distributed over time in meadow compared to heath. The warming treatment increased air and soil temperature by 0.5 °C and slightly increased aboveground greenness, but did not affect root growth or prolong the below- and aboveground growing season in either of the vegetation types.


These results imply that vegetation types differ in root dynamics and suggest that other factors than temperature control autumnal root growth in these ecosystems. Further investigations of root phenology will help to identify those drivers, in which including responses of functionally contrasting vegetation types will help to estimate how climate change affects belowground processes and their roles in ecosystem function.

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

Fig. 1
Fig. 2
Fig. 3




CO2 :

carbon dioxide


Growing Degree Days








open top chambers




plant functional type


photosynthetic photon flux density


warming treatment


  1. ACIA, Arctic Climate Impact Assessment (2004) Impacts of a warming arctic: arctic climate impact assessment. Cambridge University Press, Cambridge

    Google Scholar 

  2. Barichivich J, Briffa KR, Myneni RB, Osborn TJ, Melvin TM, Ciais P, Piao S, Tucker C (2013) Large-scale variations in the vegetation growing season and annual cycle of atmospheric CO2 at high northern latitudes from 1950 to 2011. Glob Chang Biol 19:3167–3183. doi:10.1111/gcb.12283

    Article  PubMed  Google Scholar 

  3. Bell KL, Bliss LC (1978) Root growth in a polar semidesert environment. Can J Bot 56:2470–2490

    Article  Google Scholar 

  4. Billings WD, Peterson KM, Shaver GR (1978) Growth, turnover, and respiration rates of roots and tillers in tundra graminoids, vegetation and production ecology of an Alaskan Arctic tundra. Springer, pp 415–434

  5. Björk RG, Klemedtsson L, Molau U, Harndorf J, Ödman A, Giesler R (2007) Linkages between N turnover and plant community structure in a tundra landscape. Plant Soil 294:247–261. doi:10.1007/s11104-007-9250-4

    Article  Google Scholar 

  6. Blume-Werry G, Wilson SD, Kreyling J, Milbau A (2015) The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient. New Phytol 209:978–986

    Article  PubMed  Google Scholar 

  7. Blume-Werry G, Jansson R, Milbau A (2017) Root phenology unresponsive to earlier snowmelt despite advanced above-ground phenology in two subarctic plant communities. Funct Ecol 31:1493–1502. doi:10.1111/1365-2435.12853

    Article  Google Scholar 

  8. Braun-Blanquet J (1964) Pflanzensoziologie. Grundzüge der Vegetationskunde, Springer, Berlin

    Google Scholar 

  9. Chapin FS (1974) Morphological and physiological mechanisms of temperature compensation in phosphate absorption along a latitudinal gradient. Ecology 55:1180–1198

    CAS  Article  Google Scholar 

  10. Chapin FS (1978) Phosphate uptake and nutrient utilization by barrow tundra vegetation, vegetation and production ecology of an Alaskan arctic tundra. Springer, pp 483–507

  11. Chapin FS (1983) Direct and indirect effects of temperature on arctic plants. Polar Biol 2:47–52. doi:10.1007/BF00258285

    Article  Google Scholar 

  12. Chapin FS, Bret-Harte MS, Hobbie SE, Zhong H (1996) Plant functional types as predictors of transient responses of arctic vegetation to global change. J Veg Sci 7:347–358

    Article  Google Scholar 

  13. Dorrepaal E, Aerts R, Cornelissen JHC, Callaghan TV, van Logtestijn RSP (2004) Summer warming and increased winter snow cover affect Sphagnum Fuscum growth, structure and production in a sub-arctic bog. Glob Chang Biol 10:93–104

    Article  Google Scholar 

  14. Dorrepaal E, Toet S, van Logtestijn RSP, Swart E, van de Weg MJ, Callaghan TV, Aerts R (2009) Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 460:616–619. doi:10.1038/nature08216

    CAS  Article  Google Scholar 

  15. Elmendorf SC, Henry GHR, Hollister RD, Björk RG, Bjorkman AD, Callaghan TV, Collier LS, Cooper EJ, Cornelissen JHC, Day TA, Fosaa AM, Gould WA, Grétarsdóttir J, Harte J, Hermanutz L, Hik DS, Hofgaard A, Jarrad F, Jónsdóttir IS, Keuper F, Klanderud K, Klein JA, Koh S, Kudo G, Lang SI, Loewen V, May JL, Mercado J, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Pieper S, Post E, Rixen C, Robinson CH, Schmidt NM, Shaver GR, Stenström A, Tolvanen A, Totland O, Troxler T, Wahren C-H, Webber PJ, Welker JM, Wookey PA (2012) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol Lett 15:164–175. doi:10.1111/j.1461-0248.2011.01716.x

    Article  PubMed  Google Scholar 

  16. Ernakovich JG, Hopping KA, Berdanier AB, Simpson RT, Kachergis EJ, Steltzer H, Wallenstein MD (2014) Predicted responses of arctic and alpine ecosystems to altered seasonality under climate change. Glob Chang Biol 20:3256–3269. doi:10.1111/gcb.12568

    Article  PubMed  Google Scholar 

  17. Henry GHR, Molau U (1997) Tundra plants and climate change. The international tundra Expemriment (ITEX). Glob Chang Biol 3:1–9. doi:10.1111/j.1365-2486.1997.gcb132.x

    Article  Google Scholar 

  18. IPCC (2013) Summary for policymakers. SPM. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley P (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 1–30

    Google Scholar 

  19. Iversen CM, Sloan VL, Sullivan PF, Euskirchen ES, McGuire AD, Norby RJ, Walker AP, Warren JM, Wullschleger SD (2015) The unseen iceberg: plant roots in arctic tundra. New Phytol 205:34–58. doi:10.1111/nph.13003

    Article  PubMed  Google Scholar 

  20. Johannessen OM, Kuzmina SI, Bobylev LP, Miles MW (2016) Surface air temperature variability and trends in the Arctic: new amplification assessment and regionalisation. Tellus A 68

  21. Johnson MG, Tingey DT, Phillips DL, Storm MJ (2001) Advancing fine root research with minirhizotrons. Environ Exp Bot 45:263–289. doi:10.1016/S0098-8472(01)00077-6

    Article  PubMed  Google Scholar 

  22. Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changes temperature, nutrient, and light regimes in the arctic. Ecology 80(6):1828–1843

  23. Keenan TF, Richardson AD (2015) The timing of autumn senescence is affected by the timing of spring phenology: implications for predictive models. Glob Chang Biol 21:2634–2641

    Article  Google Scholar 

  24. Keenan TF, Darby B, Felts E, Sonnentag O, Friedl MA, Hufkens K, O’Keefe J, Klosterman S, Munger JW, Toomey M, others (2014) Tracking forest phenology and seasonal physiology using digital repeat photography: a critical assessment. Ecol Appl 24:1478–1489

    CAS  Article  PubMed  Google Scholar 

  25. Körner C (2007) The use of 'altitude' in ecological research. Trends Ecol Evol 22:569–574. doi:10.1016/j.tree.2007.09.006

    Article  PubMed  Google Scholar 

  26. Linderholm HW (2006) Growing season changes in the last century. Agric For Meteorol 137:1–14. doi:10.1016/j.agrformet.2006.03.006

    Article  Google Scholar 

  27. Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443. doi:10.1038/nature02887

    CAS  Article  PubMed  Google Scholar 

  28. Marchand FL, Nijs I, Heuer M, Mertens S, Kockelbergh F, Pontailler J-Y, Impens I, Beyens L (2004) Climate warming postpones senescence in high Arctic tundra. Arct Antarct Alp Res 36:390–394

    Article  Google Scholar 

  29. Marion GM, Henry GH, Freckman DW, Johnstone J, Jones G, Jones MH, Levesque E, Molau U, Mølgaard P, Parsons AN, others (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3:20–32

  30. McCormack LM, Eissenstat DM, Prasad AM, Smithwick EAH (2013) Regional scale patterns of fine root lifespan and turnover under current and future climate. Glob Chang Biol 19(6):1697–1708

  31. McMaster GS, Wilhelm WW (1997) Growing degree-days: one equation, two interpretations. Agric For Meteorol 87:291–300

    Article  Google Scholar 

  32. Pau S, Wolkovich EM, Cook BI, Davies TJ, Kraft NJB, Bolmgren K, Betancourt JL, Cleland EE (2011) Predicting phenology by integrating ecology, evolution and climate science. Glob Chang Biol 17:3633–3643. doi:10.1111/j.1365-2486.2011.02515.x

    Article  Google Scholar 

  33. Pendall E, Bridgham S, Hanson PJ, Hungate B, Kicklighter DW, Johnson DW, Law BE, Luo Y, Megonigal JP, Olsrud M, Ryan MG, Wan S (2004) Below-ground process responses to elevated CO2 and temperature. A discussion of observations, measurement methods, and models. New Phytol 162:311–322. doi:10.1111/j.1469-8137.2004.01053.x

    Article  Google Scholar 

  34. Piao S, Ciais P, Friedlingstein P, Peylin P, Reichstein M, Luyssaert S, Margolis H, Fang J, Barr A, Chen A, Grelle A, Hollinger DY, Laurila T, Lindroth A, Richardson AD, Vesala T (2008) Net carbon dioxide losses of northern ecosystems in response to autumn warming. Nature 451:49–52. doi:10.1038/nature06444

    CAS  Article  PubMed  Google Scholar 

  35. Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B, Fox AD, Gilg O, Hik DS, Høye TT, others (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358

  36. Pregitzer KS, King JS, Burton AJ, Brown SE (2000) Responses of tree fine roots to temperature. New Phytol 147:105–115

    CAS  Article  Google Scholar 

  37. Radville L, McCormack ML, Post E, Eissenstat DM (2016a) Root phenology in a changing climate. Journal of experimental botany:erw062. doi:10.1093/jxb/erw062

  38. Radville L, Post E, Eissenstat DM (2016b) Root phenology in an Arctic shrub-graminoid community: the effects of long-term warming and herbivore exclusion. Climate Change Responses 3:4. doi:10.1186/s40665-016-0017-0

    Article  Google Scholar 

  39. Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173. doi:10.1016/j.agrformet.2012.09.012

    Article  Google Scholar 

  40. Shaver GR, Billings WD (1977) Effects of daylength and temperature on root elongation in tundra graminoids. Oecologia 28:57–65. doi:10.1007/BF00346836

    CAS  Article  PubMed  Google Scholar 

  41. Sloan VL, Fletcher BJ, Press MC, Williams M, Phoenix GK (2013) Leaf and fine root carbon stocks and turnover are coupled across Arctic ecosystems. Glob Chang Biol 19:3668–3676. doi:10.1111/gcb.12322

    Article  PubMed  Google Scholar 

  42. Sloan VL, Fletcher BJ, Phoenix GK, Bardgett R (2016) Contrasting synchrony in root and leaf phenology across multiple sub-Arctic plant communities. J Ecol 104:239–248. doi:10.1111/1365-2745.12506

    CAS  Article  Google Scholar 

  43. Steinaker DF, Wilson SD (2008) Phenology of fine roots and leaves in forest and grassland. J Ecol 96:1222–1229. doi:10.1111/j.1365-2745.2008.01439.x

    Article  Google Scholar 

  44. Sundqvist MK, Giesler R, Graae BJ, Wallander H, Fogelberg E, Wardle DA (2011) Interactive effects of vegetation type and elevation on aboveground and belowground properties in a subarctic tundra. Oikos 120:128–142. doi:10.1111/j.1600-0706.2010.18811.x

    CAS  Article  Google Scholar 

  45. Zhou L, Tucker CJ, Kaufmann RK, Slayback D, Shabanov NV, Myneni RB (2001) Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J Geophys Res: Atmos 106:20069–20083

    Article  Google Scholar 

Download references


This study was partly funded by the Kempe Foundation, Stiftelsen Oscar och Lili Lamms Minne, and the Humboldt-Ritter-Penck Foundation of the Berlin Geographical Society (Gesellschaft für Erdkunde zu Berlin). We thank Ellen Dorrepaal, Jacob Eckstein, Lea Fink, Laurenz Teuber and the staff of the Abisko Scientific Research Station for support.

Author information



Corresponding author

Correspondence to Sarah Schwieger.

Additional information

Responsible Editor: Amandine Erktan .

Electronic supplementary material


High resolution image (GIF 16 kb)


High resolution image (GIF 80 kb)


High resolution image (GIF 35 kb)


High resolution image (GIF 26 kb)


(EPS 79 kb)


(EPS 947 kb)


(EPS 622 kb)


(EPS 353 kb)


(DOCX 25 kb)


(DOCX 19 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schwieger, S., Kreyling, J., Milbau, A. et al. Autumnal warming does not change root phenology in two contrasting vegetation types of subarctic tundra. Plant Soil 424, 145–156 (2018).

Download citation


  • Belowground
  • Climate change
  • Fine roots
  • Plant phenology
  • Root growth
  • Subarctic tundra