Warming shortens flowering seasons of tundra plant communities.


Journal

Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577

Informations de publication

Date de publication:
01 2019
Historique:
received: 03 04 2018
accepted: 06 11 2018
pubmed: 12 12 2018
medline: 24 5 2019
entrez: 12 12 2018
Statut: ppublish

Résumé

Advancing phenology is one of the most visible effects of climate change on plant communities, and has been especially pronounced in temperature-limited tundra ecosystems. However, phenological responses have been shown to differ greatly between species, with some species shifting phenology more than others. We analysed a database of 42,689 tundra plant phenological observations to show that warmer temperatures are leading to a contraction of community-level flowering seasons in tundra ecosystems due to a greater advancement in the flowering times of late-flowering species than early-flowering species. Shorter flowering seasons with a changing climate have the potential to alter trophic interactions in tundra ecosystems. Interestingly, these findings differ from those of warmer ecosystems, where early-flowering species have been found to be more sensitive to temperature change, suggesting that community-level phenological responses to warming can vary greatly between biomes.

Identifiants

pubmed: 30532048
doi: 10.1038/s41559-018-0745-6
pii: 10.1038/s41559-018-0745-6
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

45-52

Commentaires et corrections

Type : ErratumIn

Références

Fitter, A. H. & Fitter, R. S. R. Rapid changes in flowering time in British plants. Science 296, 1689–1691 (2002).
doi: 10.1126/science.1071617
Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).
doi: 10.1038/nature01286
Thackeray, S. J. et al. Phenological sensitivity to climate across taxa and trophic levels. Nature 535, 241–245 (2016).
doi: 10.1038/nature18608
Arft, A. M. et al. Responses of tundra plants to experimental warming: meta-analysis of the International Tundra Experiment. Ecol. Monogr. 69, 491–511 (1999).
Høye, T. T., Post, E., Meltofte, H., Schmidt, N. M. & Forchhammer, M. C. Rapid advancement of spring in the High Arctic. Curr. Biol. 17, R449–R451 (2007).
doi: 10.1016/j.cub.2007.04.047
Parmesan, C. Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob. Change Biol. 13, 1860–1872 (2007).
doi: 10.1111/j.1365-2486.2007.01404.x
Oberbauer, S. F. et al. Phenological response of tundra plants to background climate variation tested using the International Tundra Experiment. Phil. Trans. R. Soc. B 368, 20120481 (2013).
doi: 10.1098/rstb.2012.0481
Xu, L. et al. Temperature and vegetation seasonality diminishment over northern lands. Nat. Clim. Change 3, 581–586 (2013).
doi: 10.1038/nclimate1836
Park, T. et al. Changes in growing season duration and productivity of northern vegetation inferred from long-term remote sensing data. Environ. Res. Lett. 11, 084001 (2016).
doi: 10.1088/1748-9326/11/8/084001
Xu, C., Liu, H., Williams, A. P., Yin, Y. & Wu, X. Trends toward an earlier peak of the growing season in Northern Hemisphere mid‐latitudes. Glob. Change Biol. 22, 2852–2860 (2016).
doi: 10.1111/gcb.13224
Bradley, N. L., Leopold, A. C., Ross, J. & Huffaker, W. Phenological changes reflect climate change in Wisconsin. Proc. Natl Acad. Sci. USA 96, 9701–9704 (1999).
doi: 10.1073/pnas.96.17.9701
Høye, T. T., Post, E., Schmidt, N. M., Trøjelsgaard, K. & Forchhammer, M. C. Shorter flowering seasons and declining abundance of flower visitors in a warmer Arctic. Nat. Clim. Change 3, 759–763 (2013).
doi: 10.1038/nclimate1909
Bjorkman, A. D., Elmendorf, S. C., Beamish, A. L., Vellend, M. & Henry, G. H. R. Contrasting effects of warming and increased snowfall on Arctic tundra plant phenology over the past two decades. Glob. Change Biol. 21, 4651–4661 (2015).
doi: 10.1111/gcb.13051
Panchen, Z. A. & Gorelick, R. Flowering and fruiting responses to climate change of two Arctic plant species, purple saxifrage (Saxifraga oppositifolia) and mountain avens (Dryas integrifolia). Arct. Sci. 1, 45–58 (2015).
doi: 10.1139/as-2015-0016
Panchen, Z. A. & Gorelick, R. Prediction of Arctic plant phenological sensitivity to climate change from historical records. Ecol. Evol. 7, 1325–1338 (2017).
doi: 10.1002/ece3.2702
Price, M. V. & Waser, N. M. Effects of experimental warming on plant reproductive phenology in a subalpine meadow. Ecology 79, 1261–1271 (1998).
doi: 10.1890/0012-9658(1998)079[1261:EOEWOP]2.0.CO;2
Dunne, J. A., Harte, J. & Taylor, K. J. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol. Monogr. 73, 69–86 (2003).
doi: 10.1890/0012-9615(2003)073[0069:SMFPRT]2.0.CO;2
Menzel, A. et al. European phenological response to climate change matches the warming pattern. Glob. Change Biol. 12, 1969–1976 (2006).
doi: 10.1111/j.1365-2486.2006.01193.x
Miller-Rushing, A. J. & Inouye, D. W. Variation in the impact of climate change on flowering phenology and abundance: an examination of two pairs of closely related wildflower species. Am. J. Bot. 96, 1821–1829 (2009).
doi: 10.3732/ajb.0800411
Prevéy, J. S. et al. Greater temperature sensitivity of plant phenology at colder sites: implications for convergence across northern latitudes. Glob. Change Biol. 23, 2660–2671 (2017).
doi: 10.1111/gcb.13619
Shaver, G. R. & Kummerow, J. in Arctic Ecosystems in a Changing Climate: An Ecophysiological Perspective (eds Chapin, F. S., Jefferies, R. L., Reynolds, J. F., Shaver, G. R. & Svoboda, J.) 193–211 (Academic Press, San Diego, 1992).
Molau, U. Relationships between flowering phenology and life history strategies in tundra plants. Arct. Alp. Res. 25, 391–402 (1993).
doi: 10.2307/1551922
Keller, F. & Körner, C. The role of photoperiodism in alpine plant development. Arct. Antarct. Alp. Res. 35, 361–368 (2003).
doi: 10.1657/1523-0430(2003)035[0361:TROPIA]2.0.CO;2
Hollister, R. D., Webber, P. J. & Tweedie, C. E. The response of Alaskan arctic tundra to experimental warming: differences between short- and long-term responses. Glob. Change Biol. 11, 525–536 (2005).
doi: 10.1111/j.1365-2486.2005.00926.x
Semenchuk, P. R., Elberling, B. & Cooper, E. J. Snow cover and extreme winter warming events control flower abundance of some, but not all species in High Arctic Svalbard. Ecol. Evol. 3, 2586–2599 (2013).
doi: 10.1002/ece3.648
Iler, A. M. et al. Maintenance of temporal synchrony between syrphid flies and floral resources despite differential phenological responses to climate. Glob. Change Biol. 19, 2348–2359 (2013).
doi: 10.1111/gcb.12246
Post, E., Kerby, J., Pedersen, C. & Steltzer, H. Highly individualistic rates of plant phenological advance associated with arctic sea ice dynamics. Biol. Lett. 12, 20160332 (2016).
doi: 10.1098/rsbl.2016.0332
CaraDonna, P. J. & Inouye, D. W. Phenological responses to climate change do not exhibit phylogenetic signal in a subalpine plant community. Ecology 96, 355–361 (2015).
doi: 10.1890/14-1536.1
Körner, C. & Basler, D. Phenology under global warming. Science 327, 1461–1462 (2010).
doi: 10.1126/science.1186473
Cleland, E. E. et al. Phenological tracking enables positive species responses to climate change. Ecology 93, 1765–1771 (2012).
doi: 10.1890/11-1912.1
Wheeler, H. C., Høye, T. T., Schmidt, N. M., Svenning, J.-C. & Forchhammer, M. C. Phenological mismatch with abiotic conditions—implications for flowering in Arctic plants. Ecology 96, 775–787 (2015).
doi: 10.1890/14-0338.1
Inouye, D. W. Effects of climate change on phenology, frost damage, and floral abundance of montane wildflowers. Ecology 89, 353–362 (2008).
doi: 10.1890/06-2128.1
Wipf, S., Stoeckli, V. & Bebi, P. Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim. Change 94, 105–121 (2009).
doi: 10.1007/s10584-009-9546-x
Wheeler, J. A. et al. Increased spring freezing vulnerability for alpine shrubs under early snowmelt. Oecologia 175, 219–229 (2014).
doi: 10.1007/s00442-013-2872-8
Wheeler, J. A. et al. The snow and the willows: earlier spring snowmelt reduces performance in the low-lying alpine shrub Salix herbacea. J. Ecol. 104, 1041–1050 (2016).
doi: 10.1111/1365-2745.12579
Cooper, E. J., Dullinger, S. & Semenchuk, P. Late snowmelt delays plant development and results in lower reproductive success in the High Arctic. Plant Sci. 180, 157–167 (2011).
doi: 10.1016/j.plantsci.2010.09.005
Parsons, A. N. et al. Growth responses of four sub-Arctic dwarf shrubs to simulated environmental change. J. Ecol. 82, 307–318 (1994).
doi: 10.2307/2261298
Molau, U., Nordenhäll, U. & Eriksen, B. Onset of flowering and climate variability in an alpine landscape: a 10-year study from Swedish Lapland. Am. J. Bot. 92, 422–431 (2005).
doi: 10.3732/ajb.92.3.422
Grubb, P. J. The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol. Rev. 52, 107–145 (1977).
doi: 10.1111/j.1469-185X.1977.tb01347.x
Higgins, S. I., Delgado-Cartay, M. D., February, E. C. & Combrink, H. J. Is there a temporal niche separation in the leaf phenology of savanna trees and grasses? J. Biogeogr. 38, 2165–2175 (2011).
doi: 10.1111/j.1365-2699.2011.02549.x
Sanz-Aguilar, A., Carrete, M., Edelaar, P., Potti, J. & Tella, J. L. The empty temporal niche: breeding phenology differs between coexisting native and invasive birds. Biol. Invasions 17, 3275–3288 (2015).
doi: 10.1007/s10530-015-0952-x
Wolkovich, E. M. & Cleland, E. E. The phenology of plant invasions: a community ecology perspective. Front. Ecol. Environ. 9, 287–294 (2011).
doi: 10.1890/100033
Hegland, S. J., Nielsen, A., Lázaro, A. & Bjerknes, A.-L. How does climate warming affect plant–pollinator interactions?. Ecol. Lett. 12, 184–195 (2009).
doi: 10.1111/j.1461-0248.2008.01269.x
McKinnon, L., Picotin, M., Bolduc, E., Juillet, C. & Bêty, J. Timing of breeding, peak food availability, and effects of mismatch on chick growth in birds nesting in the High Arctic. Can. J. Zool. 90, 961–971 (2012).
doi: 10.1139/z2012-064
Kerby, J. T. & Post, E. Advancing plant phenology and reduced herbivore production in a terrestrial system associated with sea ice decline. Nat. Commun. 4, 2514 (2013).
doi: 10.1038/ncomms3514
Wipf, S. Phenology, growth, and fecundity of eight subarctic tundra species in response to snowmelt manipulations. Plant Ecol. 207, 53–66 (2010).
doi: 10.1007/s11258-009-9653-9
Post, E., Pedersen, C., Wilmers, C. C. & Forchhammer, M. C. Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proc. R. Soc. B 275, 2005–2013 (2008).
doi: 10.1098/rspb.2008.0463
Schmidt, N. M. et al. An ecological function in crisis? The temporal overlap between plant flowering and pollinator function shrinks as the Arctic warms. Ecography 39, 1250–1252 (2016).
doi: 10.1111/ecog.02261
Sherry, R. A. et al. Divergence of reproductive phenology under climate warming. Proc. Natl Acad. Sci. USA 104, 198–202 (2007).
doi: 10.1073/pnas.0605642104
Steltzer, H. & Post, E. Seasons and life cycles. Science 324, 886–887 (2009).
doi: 10.1126/science.1171542
Wolkovich, E. M. et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497 (2012).
doi: 10.1038/nature11014
Prevéy, J. S. & Seastedt, T. R. Seasonality of precipitation interacts with exotic species to alter composition and phenology of a semi-arid grassland. J. Ecol. 102, 1549–1561 (2014).
doi: 10.1111/1365-2745.12320
Diez, J. M. et al. Forecasting phenology: from species variability to community patterns. Ecol. Lett. 15, 545–553 (2012).
doi: 10.1111/j.1461-0248.2012.01765.x
Aldridge, G., Inouye, D. W., Forrest, J. R. K., Barr, W. A. & Miller-Rushing, A. J. Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J. Ecol. 99, 905–913 (2011).
doi: 10.1111/j.1365-2745.2011.01826.x
CaraDonna, P. J., Iler, A. M. & Inouye, D. W. Shifts in flowering phenology reshape a subalpine plant community. Proc. Natl Acad. Sci. USA 111, 4916–4921 (2014).
doi: 10.1073/pnas.1323073111
Cook, B. I. et al. Sensitivity of spring phenology to warming across temporal and spatial climate gradients in two independent databases. Ecosystems 15, 1283–1294 (2012).
doi: 10.1007/s10021-012-9584-5
Høye, T. T. et al. Phenology of High-Arctic butterflies and their floral resources: species-specific responses to climate change. Curr. Zool. 60, 243–251 (2014).
doi: 10.1093/czoolo/60.2.243
Hocking, B. Insect–flower associations in the High Arctic with special reference to nectar. Oikos 19, 359–387 (1968).
doi: 10.2307/3565022
Janzen, D. H. Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution 21, 620–637 (1967).
doi: 10.1111/j.1558-5646.1967.tb03416.x
Meng, F. D. et al. Changes in flowering functional group affect responses of community phenological sequences to temperature change. Ecology 98, 734–740 (2017).
doi: 10.1002/ecy.1685
Hulme, P. E. Contrasting impacts of climate-driven flowering phenology on changes in alien and native plant species distributions. New Phytol. 189, 272–281 (2011).
doi: 10.1111/j.1469-8137.2010.03446.x
Craine, J. M., Wolkovich, E. M., Gene Towne, E. & Kembel, S. W. Flowering phenology as a functional trait in a tallgrass prairie. New Phytol. 193, 673–682 (2012).
doi: 10.1111/j.1469-8137.2011.03953.x
Miller-Rushing, A. J., Høye, T. T., Inouye, D. W. & Post, E. The effects of phenological mismatches on demography. Philos. Trans. R. Soc. Lond. B 365, 3177–3186 (2010).
doi: 10.1098/rstb.2010.0148
Elmendorf, S. C. et al. Experiment, monitoring, and gradient methods used to infer climate change effects on plant communities yield consistent patterns. Proc. Natl Acad. Sci. USA 112, 448–452 (2015).
doi: 10.1073/pnas.1410088112
Hollister, R. D. et al. Warming experiments elucidate the drivers of observed directional changes in tundra vegetation. Ecol. Evol. 5, 1881–1895 (2015).
doi: 10.1002/ece3.1499
Molau, U. & Mølgaard, P. International Tundra Experiment (ITEX) Manual (Danish Polar Center, 1996).
Henry, G. H. R. & Molau, U. Tundra plants and climate change: the International Tundra Experiment (ITEX). Glob. Change Biol. 3, 1–9 (1997).
doi: 10.1111/j.1365-2486.1997.gcb132.x
Harris, I., Jones, P, Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 dataset. Int. J. Climatol. 34, 623–642 (2014).
doi: 10.1002/joc.3711
Marion, G. M. et al. Open-top designs for manipulating field temperature in high-latitude ecosystems. Glob. Change Biol. 3, 20–32 (1997).
doi: 10.1111/j.1365-2486.1997.gcb136.x
Hollister, R. D., Webber, P. J., Nelson, F. E. & Tweedie, C. E. 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 (2006).
doi: 10.1657/1523-0430(2006)38[206:STATRT]2.0.CO;2
Walker, M. D. et al. Plant community responses to experimental warming across the tundra biome. Proc. Natl Acad. Sci. USA 103, 1342–1346 (2006).
doi: 10.1073/pnas.0503198103
Latimer, A. M. Geography and resource limitation complicate metabolism-based predictions of species richness. Ecology 88, 1895–1898 (2007).
doi: 10.1890/06-1931.1
Stan Modeling Language User’s Guide and Reference Manual Version 2.17.0 (Stan Development Team, 2017).
RStan: the R Interface to Stan R Package Version 2.17.3 (Stan Development Team, 2018).
R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).
Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).
doi: 10.1214/ss/1177011136
Miller-Rushing, A. J., Inouye, D. W. & Primack, R. B. How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J. Ecol. 96, 1289–1296 (2008).
doi: 10.1111/j.1365-2745.2008.01436.x

Auteurs

Janet S Prevéy (JS)

Pacific Northwest Research Station, US Forest Service, US Department of Agriculture, Olympia, WA, USA. jprevey@fs.fed.us.
WSL Institute for Snow and Avalanche Research, Davos, Switzerland. jprevey@fs.fed.us.

Christian Rixen (C)

WSL Institute for Snow and Avalanche Research, Davos, Switzerland.

Nadja Rüger (N)

German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig, Leipzig, Germany.
Smithsonian Tropical Research Institute, Panama City, Panama.

Toke T Høye (TT)

Department of Bioscience and Arctic Research Centre, Aarhus University, Aarhus, Denmark.

Anne D Bjorkman (AD)

Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, Aarhus, Denmark.
Senckenberg Gesellschaft für Naturforschung, Biodiversity and Climate Research Centre, Frankfurt, Germany.

Isla H Myers-Smith (IH)

University of Edinburgh, Edinburgh, Scotland.

Sarah C Elmendorf (SC)

Institute for Arctic and Alpine Research, University of Colorado, Boulder, CO, USA.

Isabel W Ashton (IW)

Northern Great Plains Inventory and Monitoring Network, National Park Service, Rapid City, SD, USA.

Nicoletta Cannone (N)

Department of Science and High Technology, Università degli Studi dell'Insubria, Como, Italy.

Chelsea L Chisholm (CL)

WSL Institute for Snow and Avalanche Research, Davos, Switzerland.
Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, Copenhagen, Denmark.

Karin Clark (K)

Environment and Natural Resources, Government of the Northwest Territories, Yellowknife, Northwest Territories, Canada.

Elisabeth J Cooper (EJ)

Institute for Arctic and Marine Biology, UiT - The Arctic University of Norway, Tromsø, Norway.

Bo Elberling (B)

Center for Permafrost, Department of Geosciences and Natural Resource Management, University of Copenhagen, Copenhagen, Denmark.

Anna Maria Fosaa (AM)

Faroese Museum of Natural History, Hoyvík, Faroe Islands.

Greg H R Henry (GHR)

Department of Geography, University of British Columbia, Vancouver, British Columbia, Canada.

Robert D Hollister (RD)

Biology Department, Grand Valley State University, Allendale, MI, USA.

Ingibjörg Svala Jónsdóttir (IS)

Institute of Life and Environmental Sciences, University of Iceland, Reykjavík, Iceland.
University Centre in Svalbard, Longyearbyen, Norway.

Kari Klanderud (K)

Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway.

Christopher W Kopp (CW)

Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada.

Esther Lévesque (E)

Université du Québec à Trois-Rivières, Trois-Rivieres, Québec, Canada.

Marguerite Mauritz (M)

Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA.

Ulf Molau (U)

Department of Biology and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.

Susan M Natali (SM)

Woods Hole Research Center, Falmouth, MA, USA.

Steven F Oberbauer (SF)

Department of Biological Sciences, Florida International University, Miami, FL, USA.

Zoe A Panchen (ZA)

Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada.

Eric Post (E)

Department of Wildlife, Fish and Conservation Biology, University of California, Davis, Davis, CA, USA.

Sabine B Rumpf (SB)

Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.

Niels Martin Schmidt (NM)

Department of Bioscience and Arctic Research Centre, Aarhus University, Aarhus, Denmark.

Edward Schuur (E)

Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, AZ, USA.

Philipp R Semenchuk (PR)

Institute for Arctic and Marine Biology, UiT - The Arctic University of Norway, Tromsø, Norway.
Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.

Jane G Smith (JG)

Institute for Arctic and Alpine Research, University of Colorado, Boulder, CO, USA.

Katharine N Suding (KN)

Institute for Arctic and Alpine Research, University of Colorado, Boulder, CO, USA.
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.

Ørjan Totland (Ø)

Department of Biological Sciences, University of Bergen, Bergen, Norway.

Tiffany Troxler (T)

Department of Biological Sciences, Florida International University, Miami, FL, USA.

Susanna Venn (S)

Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, Victoria, Australia.

Carl-Henrik Wahren (CH)

Research Centre for Applied Alpine Ecology, La Trobe University, Melbourne, Victoria, Australia.

Jeffrey M Welker (JM)

UArctic and University of Oulu, Oulu, Finland.
Department of Biological Sciences, University of Alaska, Anchorage, AK, USA.

Sonja Wipf (S)

WSL Institute for Snow and Avalanche Research, Davos, Switzerland.

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