Abstract
Climate change has pronounced impacts on plants, particularly in environments vulnerable to warming such as alpine zones. Although plant responses in tundra and alpine environments from high latitudes have been well-studied at the community level, the overall effect of warming on global alpine plant populations and species remains unclear. We collated global data from 46 open-top chamber (OTC) studies conducted on alpine plants from mountain belts worldwide and assessed potential effects of warming on plant performance. In addition, we examined warming responses of plants from the tundra zone (Arctic tundra and alpine tundra) in circumpolar regions. In terms of growth and reproductive output, the overall response of 91 plant species was highly positive. Shrubs grew significantly larger and expressed higher reproduction under warming compared to forbs and graminoids. Arctic tundra plants tended to respond more positively to warming compared to alpine tundra plants. We also found that plant responses were greater with increasing precipitation across circumpolar tundra, but not across alpine zones. Phenotypic plasticity in size- and fitness-related traits were similar for both alpine and tundra zones. Our findings support the notion that global warming can cause significant changes to alpine environments. Due to changes in biotic interactions, alpine tundra plants may be more negatively affected by warming compared to Arctic tundra plants which responded more positively to warming. Similarly, if shrubs are most advantaged under warming, their invasion into higher elevations may threaten the ecological functioning of alpine ecosystems, which is another serious challenge from climate change.
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References
Alatalo JM, Little CJ, Jägerbrand AK, Molau U (2015) Vascular plant abundance and diversity in an alpine heath under observed and simulated global change. Sci Rep 5(1):10197. https://doi.org/10.1038/srep10197
Alexander JM, Diez JM, Levine JM (2015) Novel competitors shape species’ responses to climate change. Nature 525:515–518. https://doi.org/10.1038/nature14952
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH et al (1999) Response patterns of tundra plant species to experimental warming: a meta-analysis of the International Tundra Experiment. Ecol Monogr 69(4):491–511. https://doi.org/10.2307/2657227
Baruah G, Molau U, Bai Y, Alatalo JM (2017) Community and species-specific responses of plant traits to 23 years of experimental warming across subarctic tundra plant communities. Sci Rep 7(1):2571. https://doi.org/10.1038/s41598-017-02595-2
Birks JHB (2019) Contributions of Quaternary botany to modern ecology and biogeography. Plant Ecol Divers 12:189–385. https://doi.org/10.1080/17550874.2019.1646831
Bjorkman AD, Myers-Smith IH, Elmendorf SC, Normand S, Rüger N, Beck PSA, Blach-Overgaard A, Blok D, Cornelissen JHC et al (2018) Plant functional trait change across a warming tundra biome. Nature 562(7725):57–62. https://doi.org/10.1038/s41586-018-0563-7
Boscutti F, Casolo V, Beraldo P, Braidot E, Zancani M, Rixen C (2018) Shrub growth and plant diversity along an elevation gradient: evidence of indirect effects of climate on alpine ecosystems. PLoS One 13:e0196653. https://doi.org/10.1371/journal.pone.0196653
Capers RS, Stone AD (2011) After 33 years, trees more frequent and shrubs more abundant in northeast U.S. Arct Antarct Alp Res 43(4):495–502. https://doi.org/10.1657/1938-4246-43.4.495
Chevin L-M, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8(4):e1000357. https://doi.org/10.1371/journal.pbio.1000357
Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11(12):1278–1286. https://doi.org/10.1111/j.1461-0248.2008.01243.x
Day TA, Ruhland CT, Strauss SL, PARK JH, Krieg ML, Krna MA, Bryant DM (2009) Response of plants and the dominant microarthropod, Cryptopygus antarcticus, to warming and contrasting precipitation regimes in Antarctic tundra. Glob Chang Biol 15(7):1640–1651. https://doi.org/10.1111/j.1365-2486.2009.01919.x
Dial RJ, Scott Smeltz T, Sullivan PF, Rinas CL, Timm K, Geck JE et al (2016) Shrubline but not treeline advance matches climate velocity in montane ecosystems of south-central Alaska. Glob Chang Biol 22(5):1841–1856. https://doi.org/10.1111/gcb.13207
Dunne JA, Harte J, Taylor KJ (2003) Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr 73(1):69–86. https://doi.org/10.1890/0012-9615(2003)073[0069:SMFPRT]2.0.CO;2
Elmendorf SC, Henry GHR, Hollister RD, Björk RG, Bjorkman AD, Callaghan TV et al (2012a) Global assessment of experimental climate warming on tundra vegetation: heterogeneity over space and time. Ecol Lett 15(2):164–175. https://doi.org/10.1111/j.1461-0248.2011.01716.x
Elmendorf SC, Henry GHR, Hollister RD, Björk RG, Boulanger-Lapointe N, Cooper EJ et al (2012b) Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nat Clim 2(6):453–457. https://doi.org/10.1038/nclimate1465
Flombaum P, Yahdjian L, Sala OE (2017) Global-change drivers of ecosystem functioning modulated by natural variability and saturating responses. Glob Chang Biol 23(2):503–511. https://doi.org/10.1111/gcb.13441
Fu G, Shen ZX, Sun W, Zhong ZM, Zhang XZ, Zhou YT (2015) A meta-analysis of the effects of experimental warming on plant physiology and growth on the Tibetan plateau. J Plant Growth Regul 34(1):57–65. https://doi.org/10.1007/s00344-014-9442-0
Gallagher RV, Hughes L, Leishman MR (2009) Phenological trends among Australian alpine species: using herbarium records to identify climate-change indicators. Aus J Bot 57(1):1–9. https://doi.org/10.1071/BT08051
Gardes M, Dahlberg A (1996) Mycorrhizal diversity in arctic and alpine tundra: an open question. New Phytol 133:147–157. https://doi.org/10.1111/j.1469-8137.1996.tb04350.x
Ghalambor CK, McKAY JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21(3):394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x
Gottfried M, Pauli H, Futschik A, Akhalkatsi M, Barančok P, Alonso JL, Coldea G, Dick J, Erschbamer B, Kazakis G, Krajči J (2012) Continent-wide response of mountain vegetation to climate change. Nat Clim 2:111–115
Grabherr G, Gottfried M, Pauli H (2010) Climate change impacts in alpine environments. Geogr Compass 4(8):1133–1153. https://doi.org/10.1111/j.1749-8198.2010.00356.x
Guittar J, Goldberg D, Klanderud K, Telford RJ, Vandvik V (2016) Can trait patterns along gradients predict plant community responses to climate change? Ecology 97:2791–2801. https://doi.org/10.1002/ecy.1500
Harsch MA, Hulme PE, McGlone MS, Duncan RP (2009) Are Treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol Lett 12(10):1040–1049. https://doi.org/10.1111/j.1461-0248.2009.01355.x
Harte J, Saleska SR, Levy C (2015) Convergent ecosystem responses to 23-year ambient and manipulated warming link advancing snowmelt and shrub encroachment to transient and long-term climate-soil carbon feedback. Glob Chang Biol 21(6):2349–2356. https://doi.org/10.1111/gcb.12831
Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, San Diego
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80(4):1150–1156. https://doi.org/10.1890/0012-9658(1999)080[1150:TMAORR]2.0.CO;2
Hollister RD, Webber PJ (2000) Biotic validation of small open-top chambers in a tundra ecosystem. Glob Chang Biol 6(7):835–842
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(2):206–215
Inouye DW (2008) Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89:353–362. https://doi.org/10.1890/06-2128.1
IPCC-Intergovernmental Panel on Climate Change (2013) In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung 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 and New York
Jump AS, Penuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8(9):1010–1020. https://doi.org/10.1111/j.1461-0248.2005.00796.x
Jurasinski G, Kreyling J (2007) Upward shift of alpine plants increases floristic similarity of mountain summits. J Veg Sci 18(5):711–718. https://doi.org/10.1111/j.1654-1103.2007.tb02585.x
Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, Zimmermann NE, Linder HP, Kessler M (2017) Climatologies at high resolution for the earth’s land surface areas. Sci Data 4:170122. https://doi.org/10.1038/sdata.2017.122
Kiełtyk P (2018) Variation of vegetative and floral traits in the alpine plant Solidago minuta: evidence for local optimum along an elevational gradient. Alp Bot 128(1):47–57. https://doi.org/10.1007/s00035-017-0197-7
Klady RA, Henry GHR, Lemay V (2011) Changes in high arctic tundra plant reproduction in response to long-term experimental warming. Glob Chang Biol 17(4):1611–1624. https://doi.org/10.1111/j.1365-2486.2010.02319.x
Körner CH (1995) Alpine plant diversity: a global survey and functional interpretations. In: Arctic and alpine biodiversity: patterns, causes and ecosystem consequences 1995. Springer, Berlin, pp 45–62
Körner C (2003) Alpine plant life, functional plant ecology of high mountain ecosystems. Springer, New York
Körner C, Hiltbrunner E (2018) The 90 ways to describe plant temperature. Perspect Plant Ecol Syst 30(SI):16–21. https://doi.org/10.1016/j.ppees.2017.04.004
Kulonen A, Imboden RA, Rixen C, Maier SB, Wipf S (2018) Enough space in a warmer world? Microhabitat diversity and small-scale distribution of alpine plants on mountain summits. Divers Distrib 24(2):252–261. https://doi.org/10.1111/ddi.12673
Lande R (2014) Evolution of phenotypic plasticity and environmental tolerance of a labile quantitative character in a fluctuating environment. J Evol Biol 27(5):866–875. https://doi.org/10.1111/jeb.12360
Lembrechts JJ, Lenoir J, Nuñez MA, Pauchard A, Geron C, Bussé G, Milbau A, Nijs I (2018) Microclimate variability in alpine ecosystems as stepping stones for non-native plant establishment above their current elevational limit. Ecography 41:900–909. https://doi.org/10.1111/ecog.03263
Lesica P, McCune B (2004) Decline of arctic-alpine plants at the southern margin of their range following a decade of climatic warming. J Veg Sci 15:679–690. https://doi.org/10.1111/j.1654-1103.2004.tb02310.x
Li H, Yu K, Ratajczak Z, Nippert JB, Tondrob D, Xu D, Li W, Du G (2016) When variability outperforms the mean: trait plasticity predicts plant cover and biomass in an alpine wetland. Plant Soil 407(1–2):401–415. https://doi.org/10.1007/s11104-016-2898-x
Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci 1206:35–55. https://doi.org/10.1111/j.1749-6632.2010.05704.x
Marion GM, Henry GHR, Freckman DW, Johnstone J, Jones G, Jones MH, Levesque E, Molau U, Molgaard P, Parsons AN et al (1997) Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob Chang Biol 3(S1):20–32. https://doi.org/10.1111/j.1365-2486.1997.gcb136.x
McVicar TR, Körner C (2013) On the use of elevation, altitude, and height in the ecological and climatological literature. Oecologia 171(2):335–337
Mondoni A, Rossi G, Orsenigo S, Probert RJ (2012) Climate warming could shift the timing of seed germination in alpine plants. Ann Bot 110(1):155–164. https://doi.org/10.1093/aob/mcs097
Myers-Smith I (2009) Shrub line advance in alpine tundra of the Kluane region: mechanisms of expansion and ecosystem impacts. Arctic 60(4):447–455. https://doi.org/10.14430/arctic208
Myers-Smith IH, Hik DS (2018) Climate warming as a driver of tundra shrubline advance. J Ecol 106(2):547–560. https://doi.org/10.1111/1365-2745.12817
Myers-Smith IH, Thomas HJD, Bjorkman AD (2019) Plant traits inform predictions of tundra responses to global change. New Phytol 221(4):1742–1748. https://doi.org/10.1111/nph.15592
Nakagawa S, Santos ESA (2012) Methodological issues and advances in biological meta-analysis. Evol Ecol 26:1253–1274. https://doi.org/10.1007/s10682-012-9555-5
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 Chang 17(3–4):420–428. https://doi.org/10.1016/j.gloenvcha.2006.11.007
Olson ME, Soriano D, Rosell JA, Anfodillo T, Donoghue MJ, Edwards EJ, Leon-Gomez C, Dawson T, Martinez JJC, Castorena M et al (2018) Plant height and hydraulic vulnerability to drought and cold. PNAS 115(29):7551–7556. https://doi.org/10.1073/pnas.1721728115
Pauli H, Gottfried M, Reiter K, Klettner C, Grabherr G (2007) Signals of range expansions and contractions of vascular plants in the high Alps: observations (1994–2004) at the GLORIA* master site Schrankogel, Tyrol, Austria. Glob Chang Biol 13:147–156
Pauli H, Gottfried M, Dullinger S, Abdaladze O, Akhalkatsi M, Alonso JLB, Coldea G, Dick J, Erschbamer B, Calzado R et al (2012) Recent plant diversity changes on Europe’s mountain summits. Science 336(6079):353–355. https://doi.org/10.1126/science.1219033
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42. https://doi.org/10.1038/nature01286
Peng F, Xue X, Xu M, You Q, Jian G, Ma SX (2017) Warming-induced shift towards forbs and grasses and its relation to the carbon sequestration in an alpine meadow. Environ Res Lett 12(4):044010. https://doi.org/10.1088/1748-9326/aa6508
Peng S, Kinlock NL, Gurevitch J, Peng S (2019) Correlation of native and exotic species richness: a global meta-analysis finds no invasion paradox across scales. Ecology 100(1):e02552. https://doi.org/10.1002/ecy.2552
Prevéy JS, Rixen C, Rüger N, Høye TT, Bjorkman AD, Myers-Smith IH, Elmendorf SC, Ashton IW, Cannone N, Chisholm CL et al (2019) Warming shortens flowering seasons of tundra plant communities. Nat Ecol Evol 3(1):45–52. https://doi.org/10.1038/s41559-018-0745-6
Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981e993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Rosbakh S, Bernhardt-Römermann M, Poschlod P (2014) Elevation matters: contrasting effects of climate change on the vegetation development at different elevations in the Bavarian Alps. Alp Bot 124(2):143–154. https://doi.org/10.1007/s00035-014-0139-6
Rumpf SB, Hülber K, Klonner G, Moser D, Schütz M, Wessely J, Willner W, Zimmermann NE, Dullinger S (2018) Range dynamics of mountain plants decrease with elevation. Proc Natl Acad Sci U S A 115(8):1848–1853. https://doi.org/10.1073/pnas.1713936115
Rühland KM, Paterson AM, Keller W, Michelutti N, Smol JP (2013) Global warming triggers the loss of a key Arctic refugium. Proc R Soc Lond B Biol Sci 280:20131887. https://doi.org/10.1098/rspb.2013.1887
Scharnagl K, Johnson D, Ebert-May D (2019) Shrub expansion and alpine plant community change: 40-year record from Niwot Ridge, Colorado. Plant Ecol Divers:1–10. https://doi.org/10.1080/17550874.2019.1641757
Scherrer D, Körner C (2010) Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J Biogeogr 38:406–416
Semenchuk PR, Elberling B, Cooper EJ (2013) Snow cover and extreme winter warming events control flower abundance of some, but not all species in high arctic Svalbard. Ecol Evol 3(8):2586–2599. https://doi.org/10.1002/ece3.648
Sierra-Almeida A, Cavieres LA (2010) Summer freezing resistance decreased in high-elevation plants exposed to experimental warming in the central Chilean Andes. Oecologia 163(1):267–276. https://doi.org/10.1007/s00442-010-1592-6
Sierra-Almeida A, Cavieres LA, Bravo LA (2018) Warmer temperatures affect the in situ freezing resistance of the Antarctic vascular plants. Front Plant Sci 9:1456
Smith JG, Sconiers W, Spasojevic MJ, Ashton IW, Suding KN (2012) Phenological changes in Alpine plants in response to increased snowpack, temperature, and nitrogen. Arct Antarct Alp Res 44(1):135–142. https://doi.org/10.1657/1938-4246-44.1.135
Steinbauer MJ, Grytnes JA, Jurasinski G, Kulonen A, Lenoir J, Pauli H, Rixen C, Winkler M, Bardy-Durchhalter M, Barni E et al (2018) Accelerated increase in plant species richness on mountain summits is linked to warming. Nature 556(7700):231–234. https://doi.org/10.1038/s41586-018-0005-6
Theurillat JP, Guisan A (2001) A potential impact of climate change on vegetation in the European Alps: a review. Clim Chang 50(1–2):77–109. https://doi.org/10.1023/A:1010632015572
Totland Ø (1999) Effects of temperature on performance and phenotypic selection on plant traits in alpine Ranunculus acris. Oecologia 120(2):242–251. https://doi.org/10.1007/s004420050854
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11(12):1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x
Valladares F, Wright S, Lasso E, Kitajima K (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936. https://doi.org/10.2307/177282
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116
Venn S, Pickering C, Green K (2014) Spatial and temporal functional changes in alpine summit vegetation are driven by increases in shrubs and graminoids. AoB Plants 6:plu008. https://doi.org/10.1093/aobpla/plu008
Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB et al (2006) Plant community response to experimental warming across the tundra biome. PNAS 103(5):1342–1346. https://doi.org/10.1073/pnas.0503198103
Walther G, Beißner S, Burga CA (2005) Trends in the upward shift of alpine plants. J Veg Sci 16:541–548. https://doi.org/10.1111/j.1654-1103.2005.tb02394.x
Wilson SD, Nilsson C (2009) Arctic alpine vegetation change over 20 years. Glob Chang Biol 15(7):1676–1684. https://doi.org/10.1111/j.1365-2486.2009.01896.x
Windmaißer T, Reisch C (2013) Long-term study of an alpine grassland: local constancy in times of global change. Alp Bot 123(1):1–6. https://doi.org/10.1007/s00035-013-0112-9
Wipf S, Stöckli V, Herz K, Rixen C (2013) The oldest monitoring site of the Alps revisited: accelerated increase in plant species richness on Piz Linard summit since 1835. Plant Ecol Divers 6(3–4):447–455. https://doi.org/10.1080/17550874.2013.764943
Yue K, Fornara DA, Yang W, Peng Y, Peng C, Liu Z, Wu F (2017) Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common. Ecol Lett 20(5):663–672. https://doi.org/10.1111/ele.12767
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Fatih Fazlioglu conceived the study, wrote the original draft, collected data, conducted the analyses, and created the figures. Justin SH Wan wrote and edited the draft, collected data, created the figures, and conducted the analyses.
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Fazlioglu, F., Wan, J.S.H. Warming matters: alpine plant responses to experimental warming. Climatic Change 164, 56 (2021). https://doi.org/10.1007/s10584-021-02996-3
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DOI: https://doi.org/10.1007/s10584-021-02996-3