Abstract
The aim of this study was to assess initial effects of warming on the CO2 balance of a lichen-rich dwarf shrub tundra, a widespread but little studied ecosystem type in the Arctic. We analyzed whole ecosystem carbon exchange rates as well as nutrient dynamics, microbial and plant community composition and biomass after 2 years of experimental temperature increase. Plant biomass increased significantly with warming, mainly due to the strong response of lichens, the dominant plant group within this ecosystem. Experimental warming also increased soil nitrogen pools and nitrogen turnover rates. Major changes in soil microbial and plant composition, however, were not detected. Although experimental warming increased gross ecosystem productivity, the higher plant biomass did not compensate for the much greater increase in C losses. Ecosystem respiration and net ecosystem CO2 losses were significantly higher in warmed plots compared to control ones. We suggest that this was due to increased soil respiration, since soil carbon pools were lower in warmed soils, at least in the upper horizons. Our study thus supports the general hypothesis that tundra ecosystems turn from a carbon sink to a carbon source when temperatures increase in the short-term. Since lichens, which produce low quality litter, increased their biomass significantly with warming in this specific ecosystem type, CO2 losses may slow down in the long-term.
Similar content being viewed by others
References
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jonsdottir IS, Laine K, Levesque E, Marion GM, Molau U, Molgaard P, Nordenhall U, Raszhivin V, Robinson CH (1999) Responses of tundra plants to experimental warming: meta-analysis of the international tundra experiment. Ecol Monogr 69:491–511
Bardgett RD, Kandeler E, Tscherko D, Hobbs PJ, Bezemer TM, Jones TH, Thompson LJ (1999) Below-ground microbial community development in a high temperature world. Oikos 85:193–203
Biasi C, Wanek W, Rusalimova O, Kaiser C, Meyer H, Barsukov P, Richter A (2005a) Microtopography and plant-cover controls on nitrogen dynamics in hummock tundra ecosystems in Siberia. Arct Antarct Alp Res 37:435–443
Biasi C, Rusalimova O, Meyer H, Kaiser C, Wanek W, Barsukov P, Junger H, Richter A (2005b) Temperature-dependent shift from labile to recalcitrant carbon sources of arctic heterotrophs. Rapid Commun Mass Spec 19:1401–1408
Boelman NT, Stieglitz M, Rueth HM, Sommerkorn M, Griffin KL, Shaver GR, Gamon JA (2003) Response of NDVI, biomass, and ecosystem gas exchange to long- term warming and fertilization in wet sedge tundra. Oecologia 135:414–421
Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012
CAVM Team (2003) Circumpolar arctic vegetation map. Scale 1:7,500,000. U.S. Fish and Wildlife Service, Anchorage, Alaska
Chapin FS, Shaver GR (1985a) Individualistic growth response of tundra plant species to enviromental manipulations in the field. Ecology 66:564–576
Chapin FSI, Shaver G (1985b) Individualistic growth response of tundra plant species to environmental manipulations in the field. Ecology 66:564–576
Chapin FSI, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA (1995) Responses of arctic tundra to experimental and observed changes in climate. Ecology 76:694–711
Cornelissen JHC, Callaghan TV, Alatalo JM, Michelsen A, Graglia E, Hartley AE, Hik DS, Hobbie SE, Press MC, Robinson CH, Henry GHR, Shaver GR, Phoenix GK, Jones DG, Jonasson S, Chapin FS, Molau U, Neill C, Lee JA, Melillo JM (2001) Global change and arctic ecosystems: is lichen decline a function of increases in vascular plant biomass? J Ecol 89:984–994
Dormann CF, Woodin SJ (2002) Climate change in the Arctic: using plant functional types in a meta-analysis of field experiments. Funct Ecol 16:4–17
Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390
Gough L, Wookey PA, Shaver GR (2002) Dry heath arctic tundra responses to long-term nutrient and light manipulation. Arct Antarct Alp Res 34:211–218
Griffiths BS, Kuan HL, Ritz K, Glover LA, McCaig AE, Fenwick C (2004) The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb Ecol 47:104–113
Grogan P, Chapin FS (2000) Initial effects of experimental warming on above- and belowground components of net ecosystem CO2 exchange in arctic tundra. Oecologia 125:512–520
Hartley AE, Neill C, Melillo JM, Crabtree R, Bowles FP (1999) Plant performance and soil nitrogen mineralization in response to simulated climate change in subarctic dwarf shrub heath. Oikos 86:331–343
Hobbie SE, Chapin FS (1998) The response of tundra plant biomass, aboveground production, nitrogen, and CO2 flux to experimental warming. Ecology 79:1526–1544
Hobbie SE, Shevtsova A, Chapin FS (1999) Plant responses to species removal and experimental warming in Alaskan tussock tundra. Oikos 84:417–434
Hobbie SE, Nadelhoffer KJ, Hogberg P (2002) A synthesis: the role of nutrients as constraints on carbon balances in boreal and arctic regions. Plant Soil 242:163–170
Hollister RD, Webber PJ, Tweedie CE (2005) The response of Alaskan arctic tundra to experimental warming: differences between short- and long-term responses. Glob Change Biol 11:525–536
Horz HP, Barbrook A, Field CB, Bohannan BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci U S A 101:15136–15141
Horz HP, Rich V, Avrahami S, Bohannan BJM (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl Environ Microb 71:2642–2652
IPCC (2001) IPCC third assessment report: climate change 2001. Intergovernmental panel on climate change. Cambridge University Press, Cambridge
Janse I, Bok J, Zwart G (2004) A simple remedy against artifactual double bands in denaturing gradient gel electrophoresis. J Microbiol Methods 57:279–281
Jonasson S, Michelsen A, Schmidt IK (1999) Coupling of nutrient cycling and carbon dynamics in the Arctic, integration of soil microbial and plant processes. Appl Soil Ecol 11:135–146
Jones MH, Fahnestock JT, Walker DA, Walker MD, Welker JM (1998) Carbon dioxide fluxes in moist and dry arctic tundra during season: responses to increases in summer temperature and winter snow accumulation. Arct Antarct Alp Res 30:373–380
Kaiser C, Meyer H, Biasi C, Rusalimova O, Barsukov P, Richter A (2005) Storage and mineralization of carbon and nitrogen in soils of a frost-boil tundra ecosystem in Siberia. Appl Soil Ecol 29:173–183
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils 6:68–72
Knorr W, Prentice IC, House JI, Holland EA (2005) Long-term sensitivity of soil carbon turnover to warming. Nature 433:298–301
Leadley PW, Drake BG (1993) Open top chambers for exposing plant canopies to elevated atmospheric CO2 and for measuring net gas exchange. Plant Ecol 104–105:3–15
Lechowicz MJ (1978) Carbon dioxide exchange in Cladina lichens from subarctic and south temperate habitats. Oecologia 32:225–237
Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS III (2005) Ecosystem carbon storage in arctic tundra reduced by long-term fertilization. Nature 431:440–443
Matveyeva NV (1994) Floristic classification and ecology of tundra vegetation of the Taymyr peninsula, northern Siberia. J Veg Sci 5:813–828
Mertens S, Nijs I, Heuer M, Kockelbergh F, Beyens L, Van Kerckvoorde A, Impens I (2001) Influence of high temperature on end-of-season tundra CO2 exchange. Ecosystems 4:226–236
Molau U, Molgaard P (1996) ITEX manual. Danish Polar Centre, Copenhagen
Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73:127–141
Muyzer G, Waal ECD, Uitterlinden AG (1993) Profiling of complex microbial populations by denatureing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rDNA. Appl Environ Microbiol 59:695–700
Muyzer G, Hottenträger S, Teske A, Wawer C (1995) Denaturing gradient gel electrophoresis of PCR-amplified 16S rDNA. A new molecular approach to analyse the genetic diversity of mixed microbial communities. In: Akkermans ADL, van Elsas JD & de Bruijn FJ (eds) Molecular Microbial Ecology Manual, 3.4.4 (pp 1–23). Kluwer
Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA (1991) Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72:242–253
Oechel WC, Billings WD (1992) Effects of global change on the carbon balance of arctic plants and ecosystems. In: Chapin FS, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J, Chu EW (eds) Arctic ecosystems in a changing climate. Academic, San Diego, pp 139–168
Oechel WC, Hastings SJ, Vourlitis G, Jenkins M, Riechers G, Grulke N (1993) Recent change of arctic tundra ecosystems from a net carbon dioxide sink to a source. Nature 361:520–523
Oechel W, Vourlitis G, Hastings MG, Bochkarev SA (1995) Change in Arctic CO2 flux over two decades: effects of climate change at Barrow, Alaska. Ecol Appl 5:846–855
Oechel WC, Vourlitis GL, Hastings SJ, Zulueta RC, Hinzman L, Kane D (2000) Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406:978–981
Panikov NS (1999) Understanding and prediction of soil microbial community dynamics under global change. Appl Soil Ecol 11:161–176
Paul EA, Harris D, Klug MJ, Ruess RW (1999) The determination of microbial biomass. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, Oxford, pp 291–317
Ping CL, Michaelson GJ, Kimble JM (1997) Carbon storage along a latitudinal transect in Alaska. Nutr Cycl Agroecosys 49:235–242
Press MC, Potter JA, Burke MJW, Callaghan TV, Lee JA (1998) Responses of a subarctic dwarf shrub heath community to simulated environmental change. J Ecol 86:315–327
Rastetter EB, Agren GI, Shaver GR (1997) Responses of N-limited ecosystems to increased CO2: A balanced-nutrition, coupled-element-cycles model. Ecol Appl 7:444–460
Rinnan R, Michelsen A, Baath E, Jonasson S (2007a) Mineralization and carbon turnover in subarctic heath soil as affected by warming and additional litter. Soil Biol Biochem 39:3014–3023
Rinnan R, Michelsen A, Baath E, Jonasson S (2007b) Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem. Glob Change Biol 13:28–39
Rustad LE, Campbell JL, Marion GM, Norby RJ, Mitchell MJ, Hartley AE, Cornelissen JHC, Gurevitch J, GCTE-NEWS (2001) A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecologia 126:543–562
Schimel J, Gulledge J (1998) Microbial community structure and global trace gases. Glob Change Biol 4:745–758
Schmidt IK, Jonasson S, Shaver GR, Michelsen A, Nordin A (2002) Mineralization and distribution of nutrients in plants and microbes in four arctic ecosystems: responses to warming. Plant Soil 242:93–106
Shaver G, Billings WD, Chapin FS, Giblin A, Nadelhoffer K, Oechel WC, Rastetter E (1992) Global change and the carbon balance of arctic ecosystems. Bioscience 42:433–441
Shaver GR, Johnson LC, Cades DH, Murray G, Laundre JA, Rastetter EB, Nadelhoffer KJ, Giblin AE (1998) Biomass and CO2 flux in wet sedge tundras: responses to nutrients, temperature, and light. Ecol Monogr 68:75–97
Shaver GR, Canadell J, Chapin FS, Gurevitch J, Harte J, Henry G, Ineson P, Jonasson S, Melillo J, Pitelka L, Rustad L (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50:871–882
Smith TM, Shugart HH (1993) The transient response of terrestrial carbon storage to a perturbed climate. Nature 361:523–526
Stieglitz M, Giblin A, Hobbie J, Williams M, Kling G (2000) Simulating the effects of climate change and climate variability on carbon dynamics in Arctic tundra. Glob Biogeochem Cycles 14:1123–1136
Sturm M, Racine C, Tape K (2001) Climate change—increasing shrub abundance in the Arctic. Nature 411:546–547
Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, Liston GE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert arctic tundra to shrubland. Bioscience 55:17–26
Tarnocai C (1999) The effect of climate warming on the carbon balance of cryosols in Canada. Permafr Periglac Process 10:251–263
Thompson JR, Pacocha S, Pharino C, Klepac-Ceraj V, Hunt DE, Benoit J, Sarma-Rupavtarm R, Distel DL, Polz MF (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science 307:1311–1313
Torsvik V, Goksoyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787
Trumbore SE, Chadwick OA, Amundsen R (1996) Rapid exchange between soil carbon and atmospheric carbon dioxide driven by temperature change. Science 272:393–396
Turunen J, Roulet NT, Moore TR, Richard PJH (2004) Nitrogen deposition and increased carbon accumulation in ombrotrophic peatlands in eastern Canada. Glob Biogeochem Cycles 18:GB3002
Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43
van Wijk MT, Clemmensen KE, Shaver GR, Williams M, Callaghan TV, Chapin FS, Cornelissen JHC, Gough L, Hobbie SE, Jonasson S, Lee JA, Michelsen A, Press MC, Richardson SJ, Rueth H (2004) Long-term ecosystem level experiments at Toolik Lake, Alaska, and at Abisko, northern Sweden: generalizations and differences in ecosystem and plant type responses to global change. Glob Change Biol 10:105–123
Vourlitis GL, Oechel WC (1999) Eddy covariance measurements of CO2 and energy fluxes of an Alaskan tussock tundra ecosystem. Ecology 80:686–701
Walker DA, Gould WA, Maier HA, Raynolds MK (2002) The Circumpolar Arctic Vegetation Map: AVHRR-derived base maps, environmental controls, and integrated mapping procedures. Int J Remote Sens 23:4551–4570
Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jonsdottir IS, Klein JA, Magnusson B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci U S A 103:1342–1346
Weintraub MN, Schimel JP (2005) Nitrogen cycling and the spread of shrubs control changes in the carbon balance of arctic tundra ecosystems. Bioscience 55:408–415
Welker JM, Fahnestock JT, Jones MH (2000) Annual CO2 flux in dry and moist arctic tundra: field responses to increases in summer temperatures and winter snow depth. Clim Change 44:139–150
Welker JM, Fahnestock JT, Henry GHR, O’Dea KW, Chimner RA (2004) CO2 exchange in three Canadian high arctic ecosystems: response to long-term experimental warming. Glob Change Biol 10:1981–1995
Wookey PA, Parsons AN, Welker JM, Potter JA, Callaghan TV, Lee JA, Press MC (1993) Comparative responses of phenology and reproductive development to simulated environmental change in sub-arctic and high arctic plants. Oikos 67:490–502
Zamolodchikov D, Karelin D, Ivaschenko A (2000) Sensitivity of tundra carbon balance to ambient temperature. Water Air Soil Poll 119:157–169
Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S (2005) Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Glob Change Biol 11:266–277
Zimov SA, Davidov SP, Voropaev YV, Prosiannikov SF, Semiletov IP, Chapin MC, Chapin FS (1996) Siberian CO2 efflux in winter as a CO2 source and cause of seasonality in atmospheric CO2. Clim Change 33:111–120
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
Acknowledgements
This work was supported by the Austrian Academy of Science (IGPB-25 to AR), the Austrian Federal Ministry of Education, Science and Culture (Payer-Weyprecht Society) and YamburgGazDobycha (a subsidiary company of Gazprom, Russia). We would like to express our collective thanks to all the people from YamburgGazDobycha who helped us in the field station arrangement and allocation of laboratory facilities. Christina Biasi was supported by a PhD grant from the Austrian Academy of Science.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Klaus Butterbach-Bahl.
Rights and permissions
About this article
Cite this article
Biasi, C., Meyer, H., Rusalimova, O. et al. Initial effects of experimental warming on carbon exchange rates, plant growth and microbial dynamics of a lichen-rich dwarf shrub tundra in Siberia. Plant Soil 307, 191–205 (2008). https://doi.org/10.1007/s11104-008-9596-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-008-9596-2