Oecologia

, Volume 183, Issue 4, pp 1167–1181 | Cite as

Four years of experimental warming do not modify the interaction between subalpine shrub species

  • Alba Anadon-Rosell
  • Josep M. Ninot
  • Sara Palacio
  • Oriol Grau
  • Salvador Nogués
  • Enrique Navarro
  • M. Carmen Sancho
  • Empar Carrillo
Global change ecology – original research

Abstract

Climate warming can lead to changes in alpine plant species interactions through modifications in environmental conditions, which may ultimately cause drastic changes in plant communities. We explored the effects of 4 years of experimental warming with open-top chambers (OTC) on Vaccinium myrtillus performance and its interaction with neighbouring shrubs at the Pyrenean treeline ecotone. We examined the effects of warming on height, above-ground (AG) and below-ground (BG) biomass and the C and N concentration and isotope composition of V. myrtillus growing in pure stands or in stands mixed with Vaccinium uliginosum or Rhododendron ferrugineum. We also analysed variations in soil N concentrations, rhizosphere C/N ratios and the functional diversity of the microbial community, and evaluated whether warming altered the biomass, C and N concentration and isotope composition of V. uliginosum in mixed plots. Our results showed that warming induced positive changes in the AG growth of V. myrtillus but not BG, while V. uliginosum did not respond to warming. Vaccinium myrtillus performance did not differ between stand types under increased temperatures, suggesting that warming did not induce shifts in the interaction between V. myrtillus and its neighbouring species. These findings contrast with previous studies in which species interactions changed when temperature was modified. Our results show that species interactions can be less responsive to warming in natural plant communities than in removal experiments, highlighting the need for studies involving the natural assembly of plant species and communities when exploring the effect of environmental changes on plant–plant interactions.

Keywords

Dwarf shrub Plant interactions Pyrenees Vaccinium myrtillus Passive warming 

Abbreviations

AG

Above-ground

BG

Below-ground

δ13C

Carbon isotope composition

δ15N

Nitrogen isotope composition

Notes

Acknowledgements

We thank Clara Borrull, Noelia Seguer, Estela Illa, Victoria Lafuente, Elena Lahoz and Santiago Pérez for their field and laboratory assistance. We are grateful to CCiT of the University of Barcelona for the use of their facilities and their technical assistance. This work was supported by Conselh Generau d’Aran and the project ARBALMONT/786-2012 (Organismo Autónomo Parques Nacionales, Ministerio de Agricultura, Alimentación y Medio Ambiente, Spain). AAR was funded by an FPU grant (Ministerio de Educación, Cultura y Deporte, Spain) and SP was funded by a Ramón y Cajal fellowship (RYC-2013-14164, Ministerio de Economía y Competitividad, Spain).

Author contribution statement

AAR, JMN, SP, OG and EC conceived and designed the experiments. AAR, JN and EC performed the experiments in the field. AAR, SP, MCS and EN performed laboratory analyses. AAR and EN analysed the data. AAR wrote the manuscript with the substantial advice, corrections and comments of SP, JMN, OG, EC, SN and EN. All the authors contributed to the discussion of the results.

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

442_2017_3830_MOESM1_ESM.pdf (330 kb)
Supplementary material 1 (PDF 329 kb)

References

  1. Anadon-Rosell A, Rixen C, Cherubini P, Wipf S, Hagedorn F, Dawes MA (2014) Growth and phenology of three dwarf shrub species in a six-year soil warming experiment at the alpine treeline. PLoS One 9(6):e100577. doi: 10.1371/journal.pone.0100577 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anadon-Rosell A, Palacio S, Nogués S, Ninot JM (2016) Vaccinium myrtillus stands show similar structure and functioning under different scenarios of coexistence at the Pyrenean treeline. Plant Ecol 217:115–1128. doi: 10.1007/s11258-016-0637-2 CrossRefGoogle Scholar
  3. Bai E, Li S, Xu W, Li W, Dai W, Jiang P (2013) A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytol 199:441–451. doi: 10.1111/nph.12252 CrossRefGoogle Scholar
  4. Bardgett RD, Wardle DA (2010) Aboveground–belowground linkages. Biotic interactions, ecosystem processes, and global change. Oxford University Press, OxfordGoogle Scholar
  5. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:187–191CrossRefGoogle Scholar
  6. Blume-Werry G, Wilson SD, Kreyling J, Milbau A (2016) The hidden season: growing season is 50% longer below than above ground along an arctic elevation gradient. New Phytol 209:978–986. doi: 10.1111/nph.13655 CrossRefPubMedGoogle Scholar
  7. Bokhorst S, Huiskes A, Aerts R, Convey P, Cooper EJ, Dalen L, Erschbamer B, Gudmundsson J, Hofgaard A, Hollister RD, Johnstone J, Jónsdóttir IS, Lebouvier M, Van de Vijver B, Wahren C-H, Dorrepaal E (2013) Variable temperature effects of Open Top Chambers at polar and alpine sites explained by irradiance and snow depth. Glob Change Biol 19:64–74. doi: 10.1111/gcb.12028 CrossRefGoogle Scholar
  8. Bolòs O, Vigo J, Masalles RM, Ninot JM (2005) Flora Manual dels Països Catalans. 3rd ed. rev. and ext. Ed. Pòrtic SA, BarcelonaGoogle Scholar
  9. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  10. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848. doi: 10.1038/nature00812 CrossRefPubMedGoogle Scholar
  11. Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA (1995) Responses of Arctic tundra to experimental and observed changes in climate. Ecology 76:694–711CrossRefGoogle Scholar
  12. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. doi: 10.1146/annurev.ecolsys.31.1.343 CrossRefGoogle Scholar
  13. Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  14. Christiansen CT, Haugwitz MS, Priemé A, Nielsen CS, Elberling B, Michelsen A, Grogan P, Blok D (2017) Enhanced summer warming reduces fungal decomposer diversity and litter mass loss more strongly in dry than in wet tundra. Glob Change Biol 23:406–420. doi: 10.1111/gcb.13362 CrossRefGoogle Scholar
  15. Chu C-J, Maestre FT, Xiao S, Weiner J, Wang Y-S, Duan Z-H, Wang G (2008) Balance between facilitation and resource competition determines biomass–density relationships in plant populations. Ecol Lett 11:1189–1197. doi: 10.1111/j.1461-0248.2008.01228.x PubMedGoogle Scholar
  16. Classen AT, Sundqvist MK, Henning JA, Newman GS, Moore JAM, Cregger MA, Moorhead LC, Patterson CM (2015) Direct and indirect effects of climate change on soil microbial and soil microbial-plant interactions: what lies ahead? Ecosphere 6(8):130. doi: 10.1890/ES15-00217.1 CrossRefGoogle Scholar
  17. Cornelissen JHC, Van Bodegom PM, Aerts R, Callaghan TV, Van Logtestijn RSP, Alatalo J, Stuart Chapin F, Gerdol R, Gudmundsson J, Gwynn-Jones D, Hartley AE, Hik DS, Hofgaard A, Jónsdóttir IS, Karlsson S, Klein JA, Laundre J, Magnusson B, Michelsen A, Molau U, Onipchenko VG, Quested HM, Sandvik SM, Schmidt IK, Shaver GR, Solheim B, Soudzilovskaia NA, Stenström A, Tolvanen A, Totland Ø, Wada N, Welker JM, Zhao X, Brancaleoni L, Brancaleoni L, De Beus MAH, Cooper EJ, Dalen L, Harte J, Hobbie SE, Hoefsloot G, Jägerbrand A, Jonasson S, Lee JA, Lindblad K, Melillo JM, Neill C, Press MC, Rozema J, Zielke M (2007) Global negative vegetation feedback to climate warming responses of leaf litter decomposition rates in cold biomes. Ecol Lett 10:619–627. doi: 10.1111/j.1461-0248.2007.01051.x CrossRefPubMedGoogle Scholar
  18. Cornelissen JHC, Song Y-B, Yu F-H, Dong M (2014) Plant traits and ecosystem effects of clonality: a new research agenda. Ann Bot. doi: 10.1093/aob/mcu113 PubMedPubMedCentralGoogle Scholar
  19. Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, MacK MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–992. doi: 10.1111/j.1469-8137.2009.02917.x CrossRefPubMedGoogle Scholar
  20. D’Odorico P, He Y, Collins S, De Wekker SFJ, Engel V, Fuentes JD (2013) Vegetation-microclimate feedbacks in woodland-grassland ecotones. Glob Ecol Biogeogr 22:364–379. doi: 10.1111/geb.12000 CrossRefGoogle Scholar
  21. Dawes MA, Hagedorn F, Zumbrunn T, Handa IT, Hättenschwiler S, Wipf S, Rixen C (2011) Growth and community responses of alpine dwarf shrubs to in situ CO2 enrichment and soil warming. New Phytol 191:806–818. doi: 10.1111/j.1469-8137.2011.03722.x CrossRefPubMedGoogle Scholar
  22. De Boeck HJ, De Groote T, Nijs I (2012) Leaf temperatures in glasshouses and open-top chambers. New Phytol 194:1155–1164. doi: 10.1111/j.1469-8137.2012.04117.x CrossRefPubMedGoogle Scholar
  23. de Mendiburu F (2010) agricolae: Statistical procedures for agricultural research. R package version 1.0-9Google Scholar
  24. DeAngelis KM, Pold G, Topcuoglu BD, van Diepen LTA, Varney RM, Blanchard JL, Melillo J, Frey SD (2015) Long-term forest soil warming alters microbial communities in temperate forest soils. Front Microbiol 6:104. doi: 10.3389/fmicb.2015.00104 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Díaz S, Symstad AJ, Chapin FS III, Wardle DA, Huenneke LF (2003) Functional diversity revealed by removal experiments. Trends Ecol Evol 18:140–146. doi: 10.1016/S0169-5347(03)00007-7 CrossRefGoogle Scholar
  26. Dijkstra FA, Blumenthal D, Morgan JA, Pendall E, Carrillo Y, Follett RF (2010) Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland. New Phytol 187:426–437. doi: 10.1111/j.1469-8137.2010.03293.x CrossRefPubMedGoogle Scholar
  27. Dormann CF, Van Der Wal R, Woodin SJ (2004) Neighbour identity modifies effects of elevated temperature on plant performance in the High Arctic. Glob Change Biol 10:1587–1598. doi: 10.1111/j.1365-2486.2004.00830.x CrossRefGoogle Scholar
  28. Dullinger S, Dirnböck T, Grabherr G (2003) Patterns of shrub invasion into high mountain grasslands of the Northern Calcareous Alps, Austria. Arct Antarct Alp Res 35:434–441. doi: 10.1657/1523-0430 CrossRefGoogle Scholar
  29. Fajardo A, McIntire EJB (2011) Under strong niche overlap conspecifics do not compete but help each other to survive: facilitation at the intraspecific level. J Ecol 99:642–650. doi: 10.1111/j.1365-2745.2010.01771.x Google Scholar
  30. Flower-Ellis JGK (1971) Age, structure and dynamics in stands of bilberry (Vaccinium myrtillus L.) Department of Forest Ecology and Forest Soils. Research Note 9. Royal College of Forestry, Stockholm, SwedenGoogle Scholar
  31. Fu G, Shen Z-X, Sun W, Zhong Z-M, Zhang X-Z, Zhou Y-T (2015) A meta-analysis of the effects of experimental warming on plant physiology and growth on the Tibetan Plateau. J Plant Growth Regul 34:57–65. doi: 10.1007/s00344-014-9442-0 CrossRefGoogle Scholar
  32. Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359PubMedPubMedCentralGoogle Scholar
  33. 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. doi: 10.2307/3546450 CrossRefGoogle Scholar
  34. Heskel M, Greaves H, Kornfeld A, Gough L, Atkin OK, Turnbull MH, Shaver G, Griffin KL (2013) Differential physiological responses to environmental change promote woody shrub expansion. Ecol Evol 3:1149–1162. doi: 10.1002/ece3.525 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522. doi: 10.2307/2963492 CrossRefGoogle Scholar
  36. Hollister RD, Flaherty KJ (2010) Above- and below-ground plant biomass response to experimental warming in northern Alaska. Appl Veg Sci 13:378–387. doi: 10.1111/j.1654-109X.2010.01079.x Google Scholar
  37. Hollister RD, Webber PJ (2000) Biotic validation of small open-top chambers in a tundra ecosystem. Glob Change Biol 6:835–842. doi: 10.1046/j.1365-2486.2000.00363.x CrossRefGoogle Scholar
  38. Hollister RD, Webber PJ, Nelson FE, Tweedie CE (2006) Soil thaw and temperature response to air warming varies by plant community: results from an open-top chamber experiment in northern Alaska. Arct Antarct Alp Res 38:206–215. doi: 10.1657/1523-0430 CrossRefGoogle Scholar
  39. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363. doi: 10.1002/bimj.200810425 CrossRefGoogle Scholar
  40. Insam H (1997) A new set of substrates proposed for community characterization in environmental samples. In: Insam H, Rangger A (eds) Microbial Communities. pp 259–260Google Scholar
  41. Kaneko S, Inagaki M, Morishita T (2010) A simple method for the determination of nitrate in potassium chloride extracts from forest soils. In: Gilkes RJ, Prakongkep N (eds) Proceedings of the 19th World Congress of Soil Science: Soil solutions for a changing world. pp 4–7Google Scholar
  42. Kempers AJ, Kok CJ (1989) Re-examination of the determination of ammonium as the indophenol blue complex using salicylate. Anal Chim Acta 221:147–155. doi: 10.1016/S0003-2670(00)81948-0 CrossRefGoogle Scholar
  43. Klanderud K (2005) Climate change effects on species interactions in an alpine plant community. J Ecol 93:127–137. doi: 10.1111/J.1365-2745.2004.00944.X CrossRefGoogle Scholar
  44. Klanderud K (2008) Species-specific responses of an alpine plant community under simulated environmental change. J Veg Sci 19:363–372. doi: 10.3170/2008-8-18376 CrossRefGoogle Scholar
  45. Klanderud K, Totland Ø (2005) The relative importance of neighbours and abiotic environmental conditions for population dynamic parameters of two alpine plant species. J Ecol 93:493–501. doi: 10.1111/j.1365-2745.2005.01000.x CrossRefGoogle Scholar
  46. Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2n edn. Springer, BerlinCrossRefGoogle Scholar
  47. Kudo G, Suzuki S (2003) Warming effects on growth, production, and vegetation structure of alpine shrubs: a five-year experiment in northern Japan. Oecologia 135:280–287. doi: 10.1007/s00442-003-1179-6 CrossRefPubMedGoogle Scholar
  48. Laine P, Bigot J, Ourry A, Boucaud J (1994) Effects of low temperature on nitrate uptake, and xylem and phloem flows of nitrogen, in Secale cereale L. and Brassica napus L. New Phytol 127:675–683. doi: 10.1111/j.1469-8137.1994.tb02970.x CrossRefGoogle Scholar
  49. Little CJ, Jägerbrand AK, Molau U, Alatalo JM (2015) Community and species-specific responses to simulated global change in two subarctic-alpine plant communities. Ecosphere. doi: 10.1890/ES14-00427.1 Google Scholar
  50. Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH, Lévesque E, Molau U, Mølgaard P, Parsons AN, Svoboda J, Virginia RA (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Change Biol 3:20–32. doi: 10.1111/j.1365-2486.1997.gcb136.x CrossRefGoogle Scholar
  51. Muñiz S, Lacarta J, Pata MP, Jiménez JJ, Navarro E (2014) Analysis of the diversity of substrate utilisation of soil bacteria exposed to Cd and earthworm activity using generalised additive models. PLoS One 9(1):e85057. doi: 10.1371/journal.pone.0085057 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, MacIas-Fauria M, Sass-Klaassen U, Lévesque E, Boudreau S, Ropars P, Hermanutz L, Trant A, Collier LS, Weijers S, Rozema J, Rayback SA, Schmidt NM, Schaepman-Strub G, Wipf S, Rixen C, Ménard CB, Venn S, Goetz S, Andreu-Hayles L, Elmendorf S, Ravolainen V, Welker J, Grogan P, Epstein HE, Hik DS (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett. doi: 10.1088/1748-9326/6/4/045509 Google Scholar
  53. Nogués-Bravo D, Araújo MB, Errea MP, Martínez-Rica JP (2007) Exposure of global mountain systems to climate warming during the 21st Century. Glob Environ Change 17:420–428. doi: 10.1016/j.gloenvcha.2006.11.007 CrossRefGoogle Scholar
  54. Nord EA, Lynch JP (2009) Plant phenology: a critical controller of soil resource acquisition. J Exp Bot 60:1927–1937. doi: 10.1093/jxb/erp018 CrossRefPubMedGoogle Scholar
  55. Olsen SL, Töpper JP, Skarpaas O, Vandvik V, Klanderud K (2016) From facilitation to competition: temperature-driven shift in dominant plant interactions affects population dynamics in seminatural grasslands. Glob Change Biol 22:1915–1926. doi: 10.1111/gcb.13241 CrossRefGoogle Scholar
  56. Pettersson M, Bååth E (2003) Temperature-dependent changes in the soil bacterial community in limed and unlimed soil. FEMS Microbiol Ecol 45:13–21. doi: 10.1016/S0168-6496(03)00106-5 CrossRefPubMedGoogle Scholar
  57. Piikki K, Temmerman LD, Högy P, Pleijel H (2008) The open-top chamber impact on vapour pressure deficit and its consequences for stomatal ozone uptake. Atmos Environ 42:6513–6522. doi: 10.1016/j.atmosenv.2008.04.014 CrossRefGoogle Scholar
  58. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-128Google Scholar
  59. Pohland B, Owen B (2009) Biolog EcoPlates Standard Methods. TAS Technical Bulletin. Biology, Hayward, CA, USA. pp 1–3Google Scholar
  60. Pornon A, Escaravage N, Lamaze T (2007) Complementarity in mineral nitrogen use among dominant plant species in a subalpine community. Am J Bot 94:1778–1785. doi: 10.3732/ajb.94.11.1778 CrossRefPubMedGoogle Scholar
  61. Pugnaire FI, Zhang L, Li R, Luo T (2015) No evidence of facilitation collapse in the Tibetan plateau. J Veg Sci 26:233–242. doi: 10.1111/jvs.12233 CrossRefGoogle Scholar
  62. Rangwala I, Sinsky E, Miller JR (2013) Amplified warming projections for high altitude regions of the northern hemisphere mid-latitudes from CMIP5 models. Environ Res Lett 8:024040. doi: 10.1088/1748-9326/8/2/024040 CrossRefGoogle Scholar
  63. Richardson SJ, Press MC, Parsons AN, Hartley SE (2002) How do nutrients and warming impact on plant communities and their insect herbivores? A 9-year study from a sub-Arctic heath. J Ecol 90:544–556. doi: 10.1046/j.1365-2745.2002.00681.x CrossRefGoogle Scholar
  64. Rinnan R, Stark S, Tolvanen A (2009) Responses of vegetation and soil microbial communities to warming and simulated herbivory in a subarctic heath. J Ecol 97:788–800. doi: 10.1111/j.1365-2745.2009.01506.x CrossRefGoogle Scholar
  65. Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22. doi: 10.18637/jss.v012.i05 CrossRefGoogle Scholar
  66. Ropars P, Boudreau S (2012) Shrub expansion at the forest-tundra ecotone: spatial heterogeneity linked to local topography. Environ Res Lett. doi: 10.1088/1748-9326/7/1/015501 Google Scholar
  67. Rundqvist S, Hedenås H, Sandström A, Emanuelsson U, Eriksson H, Jonasson C, Callaghan TV (2011) Tree and shrub expansion over the past 34 years at the tree-line near Abisko, Sweden. Ambio 40:683–692CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New YorkCrossRefGoogle Scholar
  69. Schimel J, Schaeffer S (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348. doi: 10.3389/fmicb.2012.00348 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Sharkhuu A, Plante AF, Enkhmandal O, Casper BB, Helliker BR, Boldgiv B, Petraitis PS (2013) Effects of open-top passive warming chambers on soil respiration in the semi-arid steppe to taiga forest transition zone in Northern Mongolia. Biogeochemistry 115:333–348. doi: 10.1007/s10533-013-9839-z CrossRefGoogle Scholar
  71. 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. doi: 10.1890/0012-9615 Google Scholar
  72. Shevtsova A, Haukioja E, Ojala A (1997) Growth response of subarctic dwarf shrubs, Empetrum nigrum and Vaccinium vitis-idaea, to manipulated environmental conditions and species removal. Oikos 78:440–458. doi: 10.2307/3545606 CrossRefGoogle Scholar
  73. Collins M, Knutti R, Arblaster J, Dufresne J-L, Fichefet T, Friedlingstein P, Gao X, Gutowski WJ, Johns T, Krinner G, Shongwe, M, Tebaldi C, Weaver AJ, Wehner W (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Quin D, Plattner G-K, Tignor M, Allen SK, Bosching J, Nauels A, Xia Y, Bex V, Midgley PM (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 1029–1136Google Scholar
  74. Streit K, Hagedorn F, Hiltbrunner D, Portmann M, Saurer M, Buchmann N, Wild B, Richter A, Wipf S, Siegwolf RTW (2014) Soil warming alters microbial substrate use in alpine soils. Glob Change Biol 20:1327–1338. doi: 10.1111/gcb.12396 CrossRefGoogle Scholar
  75. Sullivan PF, Welker JM (2005) Warming chambers stimulate early season growth of an arctic sedge: results of a minirhizotron field study. Oecologia 142:616–626. doi: 10.1007/s00442-004-1764-3 CrossRefPubMedGoogle Scholar
  76. Taulavuori K, Laine K, Taulavuori E (2013) Experimental studies on Vaccinium myrtillus and Vaccinium vitis-idaea in relation to air pollution and global change at northern high latitudes: a review. Environ Exp Bot 87:191–196. doi: 10.1016/j.envexpbot.2012.10.002 CrossRefGoogle Scholar
  77. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
  78. Tilman D, Lehman C (2001) Human-caused environmental change: impacts on plant diversity and evolution. Proc Natl Acad Sci 98:5433–5440. doi: 10.1073/pnas.091093198 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Volder A, Bliss LC, Lambers H (2000) The influence of temperature and nitrogen source on growth and nitrogen uptake of two polar-desert species, Saxifraga caespitosa and Cerastium alpinum. Plant Soil 227:139–148. doi: 10.1023/A:1026528830228 CrossRefGoogle Scholar
  80. Wheeler JA, Schnider F, Sedlacek J, Cortés AJ, Wipf S, Hoch G, Rixen C (2015) With a little help from my friends: community facilitation increases performance in the dwarf shrub Salix herbacea. Basic Appl Ecol 16:202–209. doi: 10.1016/j.baae.2015.02.004 CrossRefGoogle Scholar
  81. Yang Y, Wang G, Klanderud K, Wang J, Liu G (2015) Plant community responses to five years of simulated climate warming in an alpine fen of the Qinghai-Tibetan Plateau. Plant Ecol Divers 8:211–218. doi: 10.1080/17550874.2013.871654 CrossRefGoogle Scholar
  82. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Evolutionary Biology, Ecology and Environmental SciencesUniversity of BarcelonaBarcelonaSpain
  2. 2.Biodiversity Research Institute (IRBio)University of BarcelonaBarcelonaSpain
  3. 3.Instituto Pirenaico de Ecología (IPE-CSIC)JacaSpain
  4. 4.CSIC, Global Ecology Unit, CREAF-CSIC-UABCerdanyola Del VallèsSpain
  5. 5.2CREAFCerdanyola Del VallèsSpain
  6. 6.Instituto Pirenaico de Ecología (IPE-CSIC)SaragossaSpain

Personalised recommendations