Advertisement
GET OUR E-ALERTS
Special Issue Review

Above- and belowground linkages shape responses of mountain vegetation to climate change

Frank Hagedorn https://orcid.org/0000-0001-5218-7776 [email protected], Konstantin Gavazov https://orcid.org/0000-0003-4479-7202, and Jake M. Alexander https://orcid.org/0000-0003-2226-7913
Science • 13 Sep 2019 • Vol 365, Issue 6458 • pp. 1119-1123 • DOI: 10.1126/science.aax4737
get access

Abstract

Upward shifts of mountain vegetation lag behind rates of climate warming, partly related to interconnected changes belowground. Here, we unravel above- and belowground linkages by drawing insights from short-term experimental manipulations and elevation gradient studies. Soils will likely gain carbon in early successional ecosystems, while losing carbon as forest expands upward, and the slow, high-elevation soil development will constrain warming-induced vegetation shifts. Current approaches fail to predict the pace of these changes and how much they will be modified by interactions among plants and soil biota. Integrating mountain soils and their biota into monitoring programs, combined with innovative comparative and experimental approaches, will be crucial to overcome the paucity of belowground data and to better understand mountain ecosystem dynamics and their feedbacks to climate.
Get full access to this article

View all available purchase options and get full access to this article.

Get Access
Already a Subscriber?

Supplementary Material

Summary

Table S1
References (61–99)

Resources

File (aax4737-hagedorn-sm.pdf)
Download

References and Notes

1
A. von Humboldt, A. Bonpland, Essai sur la géographie des plantes - accompagné d’un tableau physique des régions équinoxiales, fondé sur des mesures exécutées, depuis le dixième degré de latitute boréale jusqu’au dixième degré de latitute australe, pendant les années 1799, 1800. Schoell, Paris 1805, (1801). 10.3931/e-rara-24316
2
P. Moret, P. Muriel, R. Jaramillo, O. Dangles, Humboldt’s Tableau Physique revisited. Proc. Natl. Acad. Sci. U.S.A. 116, 12889–12894 (2019). 10.1073/pnas.1904585116
3
M. J. Steinbauer, J.-A. Grytnes, G. Jurasinski, A. Kulonen, J. Lenoir, H. Pauli, C. Rixen, M. Winkler, M. Bardy-Durchhalter, E. Barni, A. D. Bjorkman, F. T. Breiner, S. Burg, P. Czortek, M. A. Dawes, A. Delimat, S. Dullinger, B. Erschbamer, V. A. Felde, O. Fernández-Arberas, K. F. Fossheim, D. Gómez-García, D. Georges, E. T. Grindrud, S. Haider, S. V. Haugum, H. Henriksen, M. J. Herreros, B. Jaroszewicz, F. Jaroszynska, R. Kanka, J. Kapfer, K. Klanderud, I. Kühn, A. Lamprecht, M. Matteodo, U. M. di Cella, S. Normand, A. Odland, S. L. Olsen, S. Palacio, M. Petey, V. Piscová, B. Sedlakova, K. Steinbauer, V. Stöckli, J.-C. Svenning, G. Teppa, J.-P. Theurillat, P. Vittoz, S. J. Woodin, N. E. Zimmermann, S. Wipf, Accelerated increase in plant species richness on mountain summits is linked to warming. Nature 556, 231–234 (2018). 10.1038/s41586-018-0005-6
4
C. Körner, Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems (Springer, 2003); https://link.springer.com/10.1007/978-3-642-18970-8.
5
N. Pepin, R. S. Bradley, H. F. Diaz, M. Baraer, E. B. Caceres, N. Forsythe, H. Fowler, G. Greenwood, M. Z. Hashmi, X. D. Liu, J. R. Miller, L. Ning, A. Ohmura, E. Palazzi, I. Rangwala, W. Schöner, I. Severskiy, M. Shahgedanova, M. B. Wang, S. N. Williamson, D. Q. Yang, Elevation-dependent warming in mountain regions of the world. Nat. Clim. Chang. 5, 424–430 (2015). 10.1038/nclimate2563
6
T. C. Parker, J.-A. Subke, P. A. Wookey, Rapid carbon turnover beneath shrub and tree vegetation is associated with low soil carbon stocks at a subarctic treeline. Glob. Change Biol. 21, 2070–2081 (2015). 10.1111/gcb.12793
7
P. Möhl, M. A. Mörsdorf, M. A. Dawes, F. Hagedorn, P. Bebi, D. Viglietti, M. Freppaz, S. Wipf, C. Körner, F. M. Thomas, C. Rixen, Twelve years of low nutrient input stimulates growth of trees and dwarf shrubs in the treeline ecotone. J. Ecol. 107, 768–780 (2019). 10.1111/1365-2745.13073
8
J. B. Fisher, Y. Malhi, I. C. Torres, D. B. Metcalfe, M. J. van de Weg, P. Meir, J. E. Silva-Espejo, W. H. Huasco, Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes. Oecologia 172, 889–902 (2013). 10.1007/s00442-012-2522-6
9
M. A. Dawes, P. Schleppi, S. Hättenschwiler, C. Rixen, F. Hagedorn, Soil warming opens the nitrogen cycle at the alpine treeline. Glob. Change Biol. 23, 421–434 (2017). 10.1111/gcb.13365
10
J. Paulsen, C. Körner, A climate-based model to predict potential treeline position around the globe. Alp. Bot. 124, 1–12 (2014). 10.1007/s00035-014-0124-0
11
E. Liang, Y. Wang, S. Piao, X. Lu, J. J. Camarero, H. Zhu, L. Zhu, A. M. Ellison, P. Ciais, J. Peñuelas, Species interactions slow warming-induced upward shifts of treelines on the Tibetan Plateau. Proc. Natl. Acad. Sci. U.S.A. 113, 4380–4385 (2016). 10.1073/pnas.1520582113
12
M. A. Harsch, P. E. Hulme, M. S. McGlone, R. P. Duncan, Are treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol. Lett. 12, 1040–1049 (2009). 10.1111/j.1461-0248.2009.01355.x
13
J. Dolezal, M. Dvorsky, M. Kopecky, P. Liancourt, I. Hiiesalu, M. Macek, J. Altman, Z. Chlumska, K. Rehakova, K. Capkova, J. Borovec, O. Mudrak, J. Wild, F. Schweingruber, Vegetation dynamics at the upper elevational limit of vascular plants in Himalaya. Sci. Rep. 6, 24881 (2016). 10.1038/srep24881
14
A. Ferrari, F. Hagedorn, P. A. Niklaus, Experimental soil warming and cooling alters the partitioning of recent assimilates: Evidence from a (14)C-labelling study at the alpine treeline. Oecologia 181, 25–37 (2016). 10.1007/s00442-015-3427-y
15
S. B. Rumpf, K. Hülber, G. Klonner, D. Moser, M. Schütz, J. Wessely, W. Willner, N. E. Zimmermann, S. Dullinger, Range dynamics of mountain plants decrease with elevation. Proc. Natl. Acad. Sci. U.S.A. 115, 1848–1853 (2018). 10.1073/pnas.1713936115
16
I. H. Myers-Smith, D. S. Hik, Climate warming as a driver of tundra shrubline advance. J. Ecol. 106, 547–560 (2018). 10.1111/1365-2745.12817
17
J. M. Alexander, L. Chalmandrier, J. Lenoir, T. I. Burgess, F. Essl, S. Haider, C. Kueffer, K. McDougall, A. Milbau, M. A. Nuñez, A. Pauchard, W. Rabitsch, L. J. Rew, N. J. Sanders, L. Pellissier, Lags in the response of mountain plant communities to climate change. Glob. Change Biol. 24, 563–579 (2018). 10.1111/gcb.13976
18
S. M. Crimmins, S. Z. Dobrowski, J. A. Greenberg, J. T. Abatzoglou, A. R. Mynsberge, Changes in climatic water balance drive downhill shifts in plant species’ optimum elevations. Science 331, 324–327 (2011). 10.1126/science.1199040
19
L. Lyu, Q.-B. Zhang, M. G. Pellatt, U. Büntgen, M.-H. Li, P. Cherubini, Drought limitation on tree growth at the Northern Hemisphere’s highest tree line. Dendrochronologia 53, 40–47 (2019). 10.1016/j.dendro.2018.11.006
20
P. D. Henne, C. M. Elkin, B. Reineking, H. Bugmann, W. Tinner, Did soil development limit spruce (Picea abies) expansion in the Central Alps during the Holocene? Testing a palaeobotanical hypothesis with a dynamic landscape model. J. Biogeogr. 38, 933–949 (2011). 10.1111/j.1365-2699.2010.02460.x
21
A. Kulonen, R. A. Imboden, C. Rixen, S. B. Maier, S. Wipf, Enough space in a warmer world? Microhabitat diversity and small-scale distribution of alpine plants on mountain summits. Divers. Distrib. 24, 252–261 (2018). 10.1111/ddi.12673
22
J. HilleRisLambers, M. A. Harsch, A. K. Ettinger, K. R. Ford, E. J. Theobald, How will biotic interactions influence climate change-induced range shifts? Ann. N. Y. Acad. Sci. 1297, 112–125 (2013). 10.1111/nyas.12182
23
W. H. van der Putten, M. A. Bradford, E. Pernilla Brinkman, T. F. J. van de Voorde, G. F. Veen, Where, when and how plant-soil feedback matters in a changing world. Funct. Ecol. 30, 1109–1121 (2016). 10.1111/1365-2435.12657
24
K. Streit, F. Hagedorn, D. Hiltbrunner, M. Portmann, M. Saurer, N. Buchmann, B. Wild, A. Richter, S. Wipf, R. T. W. Siegwolf, Soil warming alters microbial substrate use in alpine soils. Glob. Change Biol. 20, 1327–1338 (2014). 10.1111/gcb.12396
25
N. van Gestel, Z. Shi, K. J. van Groenigen, C. W. Osenberg, L. C. Andresen, J. S. Dukes, M. J. Hovenden, Y. Luo, A. Michelsen, E. Pendall, P. B. Reich, E. A. G. Schuur, B. A. Hungate, Predicting soil carbon loss with warming. Nature 554, E4–E5 (2018). 10.1038/nature25745
26
A. T. Nottingham, J. Whitaker, B. L. Turner, N. Salinas, M. Zimmermann, Y. Malhi, P. Meir, Climate Warming and Soil Carbon in Tropical Forests: Insights from an Elevation Gradient in the Peruvian Andes. Bioscience 65, 906–921 (2015). 10.1093/biosci/biv109
27
J. R. Mayor, N. J. Sanders, A. T. Classen, R. D. Bardgett, J.-C. Clément, A. Fajardo, S. Lavorel, M. K. Sundqvist, M. Bahn, C. Chisholm, E. Cieraad, Z. Gedalof, K. Grigulis, G. Kudo, D. L. Oberski, D. A. Wardle, Elevation alters ecosystem properties across temperate treelines globally. Nature 542, 91–95 (2017). 10.1038/nature21027
28
L. M. Kueppers, E. Conlisk, C. Castanha, A. B. Moyes, M. J. Germino, P. de Valpine, M. S. Torn, J. B. Mitton, Warming and provenance limit tree recruitment across and beyond the elevation range of subalpine forest. Glob. Change Biol. 23, 2383–2395 (2017). 10.1111/gcb.13561
29
A. Schindlbacher, J. Schnecker, M. Takriti, W. Borken, W. Wanek, Microbial physiology and soil CO2 efflux after 9 years of soil warming in a temperate forest - no indications for thermal adaptations. Glob. Change Biol. 21, 4265–4277 (2015). 10.1111/gcb.12996
30
T. W. N. Walker, C. Kaiser, F. Strasser, C. W. Herbold, N. I. W. Leblans, D. Woebken, I. A. Janssens, B. D. Sigurdsson, A. Richter, Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat. Clim. Chang. 8, 885–889 (2018). 10.1038/s41558-018-0259-x
31
M. A. Bradford, W. R. Wieder, G. B. Bonan, N. Fierer, P. A. Raymond, T. W. Crowther, Managing uncertainty in soil carbon feedbacks to climate change. Nat. Clim. Chang. 6, 751–758 (2016). 10.1038/nclimate3071
32
J. Harte, S. R. Saleska, C. Levy, 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. Change Biol. 21, 2349–2356 (2015). 10.1111/gcb.12831
33
M. Zimmermann, J. Leifeld, F. Conen, M. I. Bird, P. Meir, Can composition and physical protection of soil organic matter explain soil respiration temperature sensitivity? Biogeochemistry 107, 423–436 (2012). 10.1007/s10533-010-9562-y
34
A. B. Moyes, D. R. Bowling, Interannual variation in seasonal drivers of soil respiration in a semi-arid Rocky Mountain meadow. Biogeochemistry 113, 683–697 (2013). 10.1007/s10533-012-9797-x
35
F. Liu, L. Chen, B. W. Abbott, Y. Xu, G. Yang, D. Kou, S. Qin, J. Strauss, Y. Wang, B. Zhang, Y. Yang, Reduced quantity and quality of SOM along a thaw sequence on the Tibetan Plateau. Environ. Res. Lett. 13, 104017 (2018). 10.1088/1748-9326/aae43b
36
J. F. Knowles, P. D. Blanken, C. R. Lawrence, M. W. Williams, Evidence for non-steady-state carbon emissions from snow-scoured alpine tundra. Nat. Commun. 10, 1306 (2019). 10.1038/s41467-019-09149-2
37
A. Kammer, F. Hagedorn, I. Shevchenko, J. Leifeld, G. Guggenberger, T. Goryacheva, A. Rigling, P. Moiseev, Treeline shifts in the Ural mountains affect soil organic matter dynamics. Glob. Change Biol. 15, 1570–1583 (2009). 10.1111/j.1365-2486.2009.01856.x
38
J. T. Weedon, G. A. Kowalchuk, R. Aerts, J. van Hal, R. van Logtestijn, N. Taş, W. F. M. Röling, P. M. van Bodegom, Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Glob. Change Biol. 18, 138–150 (2012). 10.1111/j.1365-2486.2011.02548.x
39
S. E. Hobbie, Plant species effects on nutrient cycling: Revisiting litter feedbacks. Trends Ecol. Evol. 30, 357–363 (2015). 10.1016/j.tree.2015.03.015
40
E. F. Solly, B. D. Lindahl, M. A. Dawes, M. Peter, R. C. Souza, C. Rixen, F. Hagedorn, Experimental soil warming shifts the fungal community composition at the alpine treeline. New Phytol. 215, 766–778 (2017). 10.1111/nph.14603
41
D. R. Zak, P. T. Pellitier, W. Argiroff, B. Castillo, T. Y. James, L. E. Nave, C. Averill, K. V. Beidler, J. Bhatnagar, J. Blesh, A. T. Classen, M. Craig, C. W. Fernandez, P. Gundersen, R. Johansen, R. T. Koide, E. A. Lilleskov, B. D. Lindahl, K. J. Nadelhoffer, R. P. Phillips, A. Tunlid, Exploring the role of ectomycorrhizal fungi in soil carbon dynamics. New Phytol. 223, 33–39 (2019). 10.1111/nph.15679
42
R. K. Monson, D. L. Lipson, S. P. Burns, A. A. Turnipseed, A. C. Delany, M. W. Williams, S. K. Schmidt, Winter forest soil respiration controlled by climate and microbial community composition. Nature 439, 711–714 (2006). 10.1038/nature04555
43
S. Doetterl, A. Stevens, J. Six, R. Merckx, K. Van Oost, M. Casanova Pinto, A. Casanova-Katny, C. Muñoz, M. Boudin, E. Zagal Venegas, P. Boeckx, Soil carbon storage controlled by interactions between geochemistry and climate. Nat. Geosci. 8, 780–783 (2015). 10.1038/ngeo2516
44
S. Gosheva, L. Walthert, P. A. Niklaus, S. Zimmermann, U. Gimmi, F. Hagedorn, Reconstruction of historic forest cover changes indicates minor effects on carbon stocks in Swiss forest soils. Ecosystems (N. Y.) 20, 1512–1528 (2017). 10.1007/s10021-017-0129-9
45
K. Budge, J. Leifeld, E. Hiltbrunner, J. Fuhrer, Alpine grassland soils contain large proportion of labile carbon but indicate long turnover times. Biogeosciences 8, 1911–1923 (2011). 10.5194/bg-8-1911-2011
46
K. E. Clemmensen, A. Bahr, O. Ovaskainen, A. Dahlberg, A. Ekblad, H. Wallander, J. Stenlid, R. D. Finlay, D. A. Wardle, B. D. Lindahl, Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013). 10.1126/science.1231923
47
B. Adamczyk, O.-M. Sietiö, C. Biasi, J. Heinonsalo, Interaction between tannins and fungal necromass stabilizes fungal residues in boreal forest soils. New Phytol. 223, 16–21 (2019). 10.1111/nph.15729
48
A. A. Wackett, K. Yoo, J. Olofsson, J. Klaminder, Human-mediated introduction of geoengineering earthworms in the Fennoscandian arctic. Biol. Invasions 20, 1377–1386 (2018). 10.1007/s10530-017-1642-7
49
R. H. Smittenberg, M. Gierga, H. Göransson, I. Christl, D. Farinotti, S. M. Bernasconi, Climate-sensitive ecosystem carbon dynamics along the soil chronosequence of the Damma glacier forefield, Switzerland. Glob. Change Biol. 18, 1941–1955 (2012). 10.1111/j.1365-2486.2012.02654.x
50
D. L. Porazinska, E. C. Farrer, M. J. Spasojevic, C. P. Bueno de Mesquita, S. A. Sartwell, J. G. Smith, C. T. White, A. J. King, K. N. Suding, S. K. Schmidt, Plant diversity and density predict belowground diversity and function in an early successional alpine ecosystem. Ecology 99, 1942–1952 (2018). 10.1002/ecy.2420
51
G. Moser, C. Leuschner, D. Hertel, S. Graefe, N. Soethe, S. Iost, Elevation effects on the carbon budget of tropical mountain forests (S Ecuador): The role of the belowground compartment. Glob. Change Biol. 17, 2211–2226 (2011). 10.1111/j.1365-2486.2010.02367.x
52
M. Adamczyk, F. Hagedorn, S. Wipf, J. Donhauser, P. Vittoz, C. Rixen, A. Frossard, J.-P. Theurillat, B. Frey, The Soil Microbiome of GLORIA Mountain Summits in the Swiss Alps. Front. Microbiol. 10, 1080 (2019). 10.3389/fmicb.2019.01080
53
J. A. Bryant, C. Lamanna, H. Morlon, A. J. Kerkhoff, B. J. Enquist, J. L. Green, Colloquium paper: microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc. Natl. Acad. Sci. U.S.A. 105 (Suppl 1), 11505–11511 (2008). 10.1073/pnas.0801920105
54
S. N. Kivlin, J. S. Lynn, M. R. Kazenel, K. K. Beals, J. A. Rudgers, Biogeography of plant-associated fungal symbionts in mountain ecosystems: A meta-analysis. Divers. Distrib. 23, 1067–1077 (2017). 10.1111/ddi.12595
55
C. Poeplau, A. Don, L. Vesterdal, J. Leifeld, B. Van Wesemael, J. Schumacher, A. Gensior, Temporal dynamics of soil organic carbon after land-use change in the temperate zone - carbon response functions as a model approach. Glob. Change Biol. 17, 2415–2427 (2011). 10.1111/j.1365-2486.2011.02408.x
56
L. A. Cavieres, R. W. Brooker, B. J. Butterfield, B. J. Cook, Z. Kikvidze, C. J. Lortie, R. Michalet, F. I. Pugnaire, C. Schöb, S. Xiao, F. Anthelme, R. G. Björk, K. J. M. Dickinson, B. H. Cranston, R. Gavilán, A. Gutiérrez-Girón, R. Kanka, J.-P. Maalouf, A. F. Mark, J. Noroozi, R. Parajuli, G. K. Phoenix, A. M. Reid, W. M. Ridenour, C. Rixen, S. Wipf, L. Zhao, A. Escudero, B. F. Zaitchik, E. Lingua, E. T. Aschehoug, R. M. Callaway, Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol. Lett. 17, 193–202 (2014). 10.1111/ele.12217
57
A. Cardinaux, S. P. Hart, J. M. Alexander, Do soil biota influence the outcome of novel interactions between plant competitors? J. Ecol. 106, 1853–1863 (2018). 10.1111/1365-2745.13029
58
M. A. Nuñez, T. R. Horton, D. Simberloff, Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90, 2352–2359 (2009). 10.1890/08-2139.1
59
C. D. Brown, M. Vellend, Non-climatic constraints on upper elevational plant range expansion under climate change. Proc. Biol. Sci. 281, 20141779–20141779 (2014). 10.1098/rspb.2014.1779
60
C. P. Bueno de Mesquita, S. A. Sartwell, E. V. Ordemann, D. L. Porazinska, E. C. Farrer, A. J. King, M. J. Spasojevic, J. G. Smith, K. N. Suding, S. K. Schmidt, Patterns of root colonization by arbuscular mycorrhizal fungi and dark septate endophytes across a mostly-unvegetated, high-elevation landscape. Fungal Ecol. 36, 63–74 (2018). 10.1016/j.funeco.2018.07.009
61
M. A. Dawes, C. D. Philipson, P. Fonti, P. Bebi, S. Hättenschwiler, F. Hagedorn, C. Rixen, Soil warming and CO2 enrichment induce biomass shifts in alpine tree line vegetation. Glob. Change Biol. 21, 2005–2021 (2015). 10.1111/gcb.12819
62
A. Anadon-Rosell, M. A. Dawes, P. Fonti, F. Hagedorn, C. Rixen, G. von Arx, Xylem anatomical and growth responses of the dwarf shrub Vaccinium myrtillus to experimental CO2 enrichment and soil warming at treeline. Sci. Total Environ. 642, 1172–1183 (2018). 10.1016/j.scitotenv.2018.06.117
63
S. C. Elmendorf, G. H. R. Henry, R. D. Hollister, A. M. Fosaa, W. A. Gould, L. Hermanutz, A. Hofgaard, I. S. Jónsdóttir, J. C. Jorgenson, E. Lévesque, B. Magnusson, U. Molau, I. H. Myers-Smith, S. F. Oberbauer, C. Rixen, C. E. Tweedie, M. D. Walker, Experiment, monitoring, and gradient methods used to infer climate change effects on plant communities yield consistent patterns. Proc. Natl. Acad. Sci. U.S.A. 112, 448–452 (2015). 10.1073/pnas.1410088112
64
E. Kaarlejärvi, A. Eskelinen, J. Olofsson, Herbivory prevents positive responses of lowland plants to warmer and more fertile conditions at high altitudes. Funct. Ecol. 27, 1244–1253 (2013). 10.1111/1365-2435.12113
65
J. M. Melillo, S. Butler, J. Johnson, J. Mohan, P. Steudler, H. Lux, E. Burrows, F. Bowles, R. Smith, L. Scott, C. Vario, T. Hill, A. Burton, Y.-M. Zhou, J. Tang, Soil warming, carbon-nitrogen interactions, and forest carbon budgets. Proc. Natl. Acad. Sci. U.S.A. 108, 9508–9512 (2011). 10.1073/pnas.1018189108
66
H. Majdi, J. Ohrvik, Interactive effects of soil warming and fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden. Glob. Change Biol. 10, 182–188 (2004). 10.1111/j.1365-2486.2004.00733.x
67
E. F. Solly, I. Brunner, H.-S. Helmisaari, C. Herzog, J. Leppälammi-Kujansuu, I. Schöning, M. Schrumpf, F. H. Schweingruber, S. E. Trumbore, F. Hagedorn, Unravelling the age of fine roots of temperate and boreal forests. Nat. Commun. 9, 3006 (2018). 10.1038/s41467-018-05460-6
68
E. F. Solly, I. Djukic, P. A. Moiseev, N. I. Andreyashkina, N. M. Devi, H. Göransson, V. S. Mazepa, S. G. Shiyatov, M. R. Trubina, F. H. Schweingruber, M. Wilmking, F. Hagedorn, Treeline advances and associated shifts in the ground vegetation alter fine root dynamics and mycelia production in the South and Polar Urals. Oecologia 183, 571–586 (2017). 10.1007/s00442-016-3785-0
69
J. M. Melillo, S. D. Frey, K. M. DeAngelis, W. J. Werner, M. J. Bernard, F. P. Bowles, G. Pold, M. A. Knorr, A. S. Grandy, Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world. Science 358, 101–105 (2017). 10.1126/science.aan2874
70
H. Lim, R. Oren, T. Näsholm, M. Strömgren, T. Lundmark, H. Grip, S. Linder, Boreal forest biomass accumulation is not increased by two decades of soil warming. Nat. Clim. Chang. 9, 49–52 (2019). 10.1038/s41558-018-0373-9
71
M. Väisänen, H. Ylänne, E. Kaarlejärvi, S. Sjögersten, J. Olofsson, N. Crout, S. Stark, Consequences of warming on tundra carbon balance determined by reindeer grazing history. Nat. Clim. Chang. 4, 384–388 (2014). 10.1038/nclimate2147
72
S. B. Devi, S. S. S. S. Sherpa, Soil carbon and nitrogen stocks along the altitudinal gradient of the Darjeeling Himalayas, India. Environ. Monit. Assess. 191, 361 (2019). 10.1007/s10661-019-7470-8
73
M. G. Kramer, O. A. Chadwick, Controls on carbon storage and weathering in volcanic soils across a high-elevation climate gradient on Mauna Kea, Hawaii. Ecology 97, 2384–2395 (2016). 10.1002/ecy.1467
74
J. D. M. Speed, V. Martinsen, A. J. Hester, Ø. Holand, J. Mulder, A. Mysterud, G. Austrheim, Continuous and discontinuous variation in ecosystem carbon stocks with elevation across a treeline ecotone. Biogeosciences 12, 1615–1627 (2015). 10.5194/bg-12-1615-2015
75
J. Leifeld, M. Zimmermann, J. Fuhrer, F. Conen, Storage and turnover of carbon in grassland soils along an elevation gradient in the Swiss Alps. Glob. Change Biol. 15, 668–679 (2009). 10.1111/j.1365-2486.2008.01782.x
76
E. Kolb, M. Kohlpaintner, Tangel humus forms − genesis and co-evolution with vegetation. Appl. Soil Ecol. 123, 622–626 (2018). 10.1016/j.apsoil.2017.09.040
77
M. A. Dawes, P. Schleppi, F. Hagedorn, The fate of nitrogen inputs in a warmer alpine treeline ecosystem: A 15N labelling study. J. Ecol. 105, 1723–1737 (2017). 10.1111/1365-2745.12780
78
Z. Wu, P. Dijkstra, G. W. Koch, B. A. Hungate, Biogeochemical and ecological feedbacks in grassland responses to warming. Nat. Clim. Chang. 2, 458–461 (2012). 10.1038/nclimate1486
79
S. Zhang, D. Chen, D. Sun, X. Wang, J. L. Smith, G. Du, Impacts of altitude and position on the rates of soil nitrogen mineralization and nitrification in alpine meadows on the eastern Qinghai–Tibetan Plateau, China. Biol. Fertil. Soils 48, 393–400 (2012). 10.1007/s00374-011-0634-5
80
L. Wang, D. L. Godbold, Soil N mineralization profiles of co-existing woody vegetation islands at the alpine tree line. Eur. J. For. Res. 136, 881–892 (2017). 10.1007/s10342-017-1076-x
81
A. P. Baldos, M. D. Corre, E. Veldkamp, Response of N cycling to nutrient inputs in forest soils across a 1000-3000 m elevation gradient in the Ecuadorian Andes. Ecology 96, 749–761 (2015). 10.1890/14-0295.1
82
A. Fajardo, F. I. Piper, An assessment of carbon and nutrient limitations in the formation of the southern Andes tree line. J. Ecol. 105, 517–527 (2017). 10.1111/1365-2745.12697
83
A. Thébault, J.-C. Clément, S. Ibanez, J. Roy, R. A. Geremia, C. A. Pérez, A. Buttler, Y. Estienne, S. Lavorel, Nitrogen limitation and microbial diversity at the treeline. Oikos 123, 729–740 (2014). 10.1111/j.1600-0706.2013.00860.x
84
K. Gavazov, F. Hagedorn, A. Buttler, R. Siegwolf, L. Bragazza, Environmental drivers of carbon and nitrogen isotopic signatures in peatland vascular plants along an altitude gradient. Oecologia 180, 257–264 (2016). 10.1007/s00442-015-3458-4
85
R. Amundson, A. T. Austin, E. A. G. Schuur, K. Yoo, V. Matzek, C. Kendall, A. Uebersax, D. Brenner, W. T. Baisden, Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem. Cycles 17, (2003). 10.1029/2002GB001903
86
C. Körner, S. Leuzinger, S. Riedl, R. T. Siegwolf, L. Streule, Carbon and nitrogen stable isotope signals for an entire alpine flora, based on herbarium samples. Alp. Bot. 126, 153–166 (2016). 10.1007/s00035-016-0170-x
87
Y. Yang, R. T. W. Siegwolf, C. Körner, Species specific and environment induced variation of δ(13)C and δ(15)N in alpine plants. Front. Plant Sci. 6, 423 (2015). 10.3389/fpls.2015.00423
88
C. Heer, C. Körner, High elevation pioneer plants are sensitive to mineral nutrient addition. Basic Appl. Ecol. 3, 39–47 (2002). 10.1078/1439-1791-00075
89
K. Klanderud, Species-specific responses of an alpine plant community under simulated environmental change. J. Veg. Sci. 19, 363–372 (2008). 10.3170/2008-8-18376
90
B. Sveinbjornsson, O. Nordell, H. Kauhanen, Nutrient Relations of Mountain Birch Growth at and Below the Elevational Tree-Line in Swedish Lapland. Funct. Ecol. 6, 213 (1992). 10.2307/2389757
91
S. Bassin, M. Volk, J. Fuhrer, Species Composition of Subalpine Grassland is Sensitive to Nitrogen Deposition, but Not to Ozone, After Seven Years of Treatment. Ecosystems 16, 1105–1117 (2013). 10.1007/s10021-013-9670-3
92
K. E. Clemmensen, A. Michelsen, S. Jonasson, G. R. Shaver, Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytol. 171, 391–404 (2006). 10.1111/j.1469-8137.2006.01778.x
93
N. Fierer, C. M. McCain, P. Meir, M. Zimmermann, J. M. Rapp, M. R. Silman, R. Knight, Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92, 797–804 (2011). 10.1890/10-1170.1
94
J. N. Hendershot, Q. D. Read, J. A. Henning, N. J. Sanders, A. T. Classen, Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98, 1757–1763 (2017). 10.1002/ecy.1829
95
I. Djukic, F. Zehetner, A. Mentler, M. H. Gerzabek, Microbial community composition and activity in different Alpine vegetation zones. Soil Biol. Biochem. 42, 155–161 (2010). 10.1016/j.soilbio.2009.10.006
96
J. Donhauser, B. Frey, Alpine soil microbial ecology in a changing world. FEMS Microbiol. Ecol. 94, 1–31 (2018). 10.1093/femsec/fiy099
97
R. D. Bardgett, A. Richter, R. Bol, M. H. Garnett, R. Bäumler, X. Xu, E. Lopez-Capel, D. A. C. Manning, P. J. Hobbs, I. R. Hartley, W. Wanek, Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol. Lett. 3, 487–490 (2007). 10.1098/rsbl.2007.0242
98
M. Bahram, F. Hildebrand, S. K. Forslund, J. L. Anderson, N. A. Soudzilovskaia, P. M. Bodegom, J. Bengtsson-Palme, S. Anslan, L. P. Coelho, H. Harend, J. Huerta-Cepas, M. H. Medema, M. R. Maltz, S. Mundra, P. A. Olsson, M. Pent, S. Põlme, S. Sunagawa, M. Ryberg, L. Tedersoo, P. Bork, Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018). 10.1038/s41586-018-0386-6
99
C. Shen, Y. Shi, Y. Ni, Y. Deng, J. D. Van Nostrand, Z. He, J. Zhou, H. Chu, Dramatic increases of soil microbial functional gene diversity at the treeline ecotone of Changbai mountain. Front. Microbiol. 7, 1184 (2016). 10.3389/fmicb.2016.01184

Information & Authors

Information

Published In

Science
Volume 365 | Issue 6458
13 September 2019

Copyright

Copyright © 2019, American Association for the Advancement of Science.
This is an article distributed under the terms of the Science Journals Default License.

Submission history

Published in print: 13 September 2019

Permissions

Request permissions for this article.

Acknowledgments

We thank T. Walker for critical comments on the manuscript and the Stillberg team and P. Moiseev for their long-term support in treeline research. Funding: F.H. received funding from the Swiss National Science Foundation (grant no. 171171); K.G. was supported by funding from the Swiss National Science Foundation (grant no. PZ00P2_174047); and J.M.A. received funding from the European Union’s Horizon 2020 research and innovation program (grant no. 678841) and from the Swiss National Science Foundation (grant no. 31003A_176044). Competing interests: The authors declare no competing interests.

Authors

Affiliations

Frank Hagedorn* https://orcid.org/0000-0001-5218-7776 [email protected]
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, 8903 Birmensdorf, Switzerland.
View all articles by this author
Konstantin Gavazov† https://orcid.org/0000-0003-4479-7202
Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, 8903 Birmensdorf, Switzerland.
View all articles by this author
Jake M. Alexander† https://orcid.org/0000-0003-2226-7913
Institute of Integrative Biology, ETH Zurich, Universitätstrasse 16, 8092 Zürich, Switzerland.
View all articles by this author

Funding Information

Notes

*Corresponding author. Email: [email protected]
†
These authors contributed equally to this work.

Metrics & Citations

Metrics

Article Usage
Altmetrics

Citations

Export citation

Select the format you want to export the citation of this publication.

Cited by
    • Yu Zhou,
    • Lifeng Wang,
    • Yamei Chen,
    • Jian Zhang,
    • Zhenfeng Xu,
    • Li Guo,
    • Lixia Wang,
    • Chengming You,
    • Bo Tan,
    • Li Zhang,
    • LiangHua Chen,
    • JiuJin Xiao,
    • Peng Zhu,
    • Yang Liu,
    Temporal dynamics of mixed litter humification in an alpine treeline ecotone, Science of The Total Environment, 803, (150122), (2022).https://doi.org/10.1016/j.scitotenv.2021.150122
    Crossref
    • Carla Perez-Mon,
    • Beat Stierli,
    • Michael Plötze,
    • Beat Frey,
    Fast and persistent responses of alpine permafrost microbial communities to in situ warming, Science of The Total Environment, 807, (150720), (2022).https://doi.org/10.1016/j.scitotenv.2021.150720
    Crossref
    • Johanna Donhauser,
    • Weihong Qi,
    • Benoît Bergk‐Pinto,
    • Beat Frey,
    High temperatures enhance the microbial genetic potential to recycle C and N from necromass in high‐mountain soils, Global Change Biology, 27, 7, (1365-1386), (2021).https://doi.org/10.1111/gcb.15492
    Crossref
    • Bjorn J. M. Robroek,
    • Magalí Martí,
    • Bo H. Svensson,
    • Marc G. Dumont,
    • Annelies J. Veraart,
    • Vincent E. J. Jassey,
    Rewiring of peatland plant–microbe networks outpaces species turnover, Oikos, 130, 3, (339-353), (2021).https://doi.org/10.1111/oik.07635
    Crossref
    • Arnaud G. Barras,
    • Veronika Braunisch,
    • Raphaël Arlettaz,
    Predictive models of distribution and abundance of a threatened mountain species show that impacts of climate change overrule those of land use change, Diversity and Distributions, 27, 6, (989-1004), (2021).https://doi.org/10.1111/ddi.13247
    Crossref
    • Maria Shahgedanova,
    • Carolina Adler,
    • Aster Gebrekirstos,
    • H. Ricardo Grau,
    • Christian Huggel,
    • Robert Marchant,
    • Nicholas Pepin,
    • Veerle Vanacker,
    • Daniel Viviroli,
    • Mathias Vuille,
    Mountain Observatories: Status and Prospects for Enhancing and Connecting a Global Community, Mountain Research and Development, 41, 2, (2021).https://doi.org/10.1659/MRD-JOURNAL-D-20-00054.1
    Crossref
    • Hongfen Teng,
    • Zhongkui Luo,
    • Jinfeng Chang,
    • Zhou Shi,
    • Songchao Chen,
    • Yin Zhou,
    • Philippe Ciais,
    • Hanqin Tian,
    Climate change-induced greening on the Tibetan Plateau modulated by mountainous characteristics, Environmental Research Letters, 16, 6, (064064), (2021).https://doi.org/10.1088/1748-9326/abfeeb
    Crossref
    • Federica D'Alò,
    • Iñaki Odriozola,
    • Petr Baldrian,
    • Laura Zucconi,
    • Caterina Ripa,
    • Nicoletta Cannone,
    • Francesco Malfasi,
    • Lisa Brancaleoni,
    • Silvano Onofri,
    Microbial activity in alpine soils under climate change, Science of The Total Environment, 783, (147012), (2021).https://doi.org/10.1016/j.scitotenv.2021.147012
    Crossref
    • Chao Huang,
    • Yu Liang,
    • Hong S. He,
    • Mia M. Wu,
    • Bo Liu,
    • Tianxiao Ma,
    Sensitivity of aboveground biomass and species composition to climate change in boreal forests of Northeastern China, Ecological Modelling, 445, (109472), (2021).https://doi.org/10.1016/j.ecolmodel.2021.109472
    Crossref
    • Ulf Büntgen,
    • Alexander V. Kirdyanov,
    • Paul J. Krusic,
    • Vladimir V. Shishov,
    • Jan Esper,
    Arctic aerosols and the ‘Divergence Problem’ in dendroclimatology, Dendrochronologia, 67, (125837), (2021).https://doi.org/10.1016/j.dendro.2021.125837
    Crossref
  11. See more

View Options

Get Access

Log in to view the full text

AAAS ID LOGIN

AAAS login provides access to Science for AAAS Members, and access to other journals in the Science family to users who have purchased individual subscriptions.

Log in via OpenAthens.
via OpenAthens
Log in via Shibboleth.
via Shibboleth
More options

Purchase digital access to this article

Download and print this article for your personal scholarly, research, and educational use.

Purchase this issue in print

Buy a single issue of Science for just $15 USD.

View options

PDF format

Download this article as a PDF file

Download PDF

Media

Figures

Multimedia

Tables

Share

Current Issue

Go to Science
Table of Contents

LATEST NEWS