Abstract
Anthropogenic warming’s effects on phenology across environmental and temporal gradients are well recognized. Long-term phenological monitoring data are often limited in duration and geographic scope, but recent efforts to digitize herbaria collections make it possible to reliably reconstruct historic flowering phenology across broad geographic scales and multiple species, lending to an increased understanding of community response to climate change. In this study, we examined collection dates (1901 to 2015) of 8540 flowering specimens from 39 native species in the Pacific Northwest (PNW) region of North America. We hypothesized that flowering phenology would be sensitive to temperature but that sensitivity would vary depending on blooming season and geographic range position. As expected, we found that early-season bloomers are more sensitive to temperature than later-season bloomers. Sensitivity to temperature was significantly greater at low elevations and in the maritime (western) portion of the PNW than at higher elevations and in the eastern interior, respectively. The elevational and longitudinal effects on flowering sensitivity reflect spring “arriving” earlier at low elevations and in the maritime portion of the PNW. These results demonstrate that phenological responses to warming vary substantially across climatically diverse regions, warranting careful and nuanced consideration of climate warming’s effects on plant phenology.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amano T, Smithers RJ, Sparks TH, Sutherland WJ (2010) A 250-year index of first flowering dates and its response to temperature changes. Proc R Soc B Biol Sci 277:2451–2457. https://doi.org/10.1038/416389a
Cleland EE, Chuine I, Menzel A et al (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365. https://doi.org/10.1016/j.tree.2007.04.003
Cleland EE, Allen JM, Crimmins TM et al (2012) Phenological tracking enables positive species responses to climate change. Ecology 93:1765–1771. https://doi.org/10.1890/11-1912.1
Hamilton JA, Aitken SN (2013) Genetic and morphological structure of a spruce hybrid (Picea sitchensis x P. glauca) zone along a climatic gradient. Am J Bot 100:1651–1662. https://doi.org/10.3732/ajb.1200654
Hart R, Salick J, Ranjitkar S, Xu J (2014) Herbarium specimens show contrasting phenological responses to Himalayan climate. Proc Natl Acad Sci 111:10615–10619. https://doi.org/10.1073/pnas.1403376111
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
Kopp CW, Cleland EE (2015) A range-expanding shrub species alters plant phenological response to experimental warming. PLoS One 10:e0139029. https://doi.org/10.1371/journal.pone.0139029.s006
Lapenis A, Henry H, Vuille M, Mower J (2014) Climatic factors controlling plant sensitivity to warming. Clim Chang 122:723–734. https://doi.org/10.1007/s10584-013-1010-2
Matsumoto K, Ohta T, Irasawa M, Nakamura T (2003) Climate change and extension of the Ginkgo biloba L. growing season in Japan. Glob Chang Biol 9:1634–1642. https://doi.org/10.1046/j.1529-8817.2003.00688.x
Matthews ER, Mazer SJ (2015) Historical changes in flowering phenology are governed by temperature × precipitation interactions in a widespread perennial herb in western North America. New Phytol 210:157–167. https://doi.org/10.1111/nph.13751
Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659–659. https://doi.org/10.1038/17709
Menzel A, Sparks TH, Estrella N et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976. https://doi.org/10.1111/j.1365-2486.2006.01193.x
Mote PW, Hamlet AF, Clark MP, Lettenmaier DP (2005) Declining mountain snowpack in western North America. B Am Meteorol Soc 86:39–49
Myking T, Skrøppa T (2007) Variation in phenology and height increment of northern Ulmus glabra populations: implications for conservation. Scand J For Res 22:369–374. https://doi.org/10.1080/02827580701672121
Park IW, Mazer SJ (2018) Overlooked climate parameters best predict flowering onset: assessing phenological models using the elastic net. Glob Chang Biol 24:5972–5984
Park DS, Breckheimer I, Williams AC et al (2018) Herbarium specimens reveal substantial and unexpected variation in phenological sensitivity across the eastern United States. Philos Trans R Soc Lond Ser B Biol Sci 374:20170394–20170314. https://doi.org/10.1098/rstb.2017.0394
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669
Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13:1860–1872. https://doi.org/10.1111/j.1365-2486.2007.01404.x
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Polgar C, Gallinat A, Primack RB (2013) Drivers of leaf-out phenology and their implications for species invasions: insights from Thoreau’s Concord. New Phytol 202:106–115. https://doi.org/10.1111/nph.12647
Prevéy JS, Rixen C, Rüger N, Høye TT, Bjorkman AD, Myers-Smith IH, Elmendorf SC, Ashton IW, Cannone N, Chisholm CL, Clark K, Cooper EJ, Elberling B, Fosaa AM, Henry GHR, Hollister RD, Jónsdóttir IS, Klanderud K, Kopp CW, Lévesque E, Mauritz M, Molau U, Natali SM, Oberbauer SF, Panchen ZA, Post E, Rumpf SB, Schmidt NM, Schuur E, Semenchuk PR, Smith JG, Suding KN, Totland Ø, Troxler T, Venn S, Wahren CH, Welker JM, Wipf S (2018) Warming shortens flowering seasons of tundra plant communities. Nat Ecol Evol 3:1–11. https://doi.org/10.1038/s41559-018-0745-6
R Core Development Team (2018) R: a language and environment for statistical computing
Robbirt KM, Davy AJ, Hutchings MJ, Roberts DL (2011) Validation of biological collections as a source of phenological data for use in climate change studies: a case study with the orchid Ophrys sphegodes. J Ecol 99:235–241. https://doi.org/10.1111/j.1365-2745.2010.01727.x
Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60
Rosenthal R (1979) The file drawer problem and tolerance for null results. Psychol Bull 86:638–641
Rosenzweig C, Karoly D, Vicarelli M et al (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353–357. https://doi.org/10.1038/nature06937
Socker TF, Qin D, Plattner GK et al (2013) 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
Vitasse Y, Signarbieux C, Fu YH (2018) Global warming leads to more uniform spring phenology across elevations. Proc Natl Acad Sci 115:1004–1008. https://doi.org/10.1073/pnas.1717342115
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395. https://doi.org/10.1038/416389a
Wang C, Cao R, Chen J et al (2015a) Temperature sensitivity of spring vegetation phenology correlates to within-spring warming speed over the Northern Hemisphere. Ecol Indic 50:62–68. https://doi.org/10.1016/j.ecolind.2014.11.004
Wang H, Dai J, Zheng J, Ge Q (2015b) Temperature sensitivity of plant phenology in temperate and subtropical regions of China from 1850 to 2009. Int J Climatol 35:913–922. https://doi.org/10.1002/joc.4026
Wang T, Hamann A, Spittlehouse D, Carroll C (2016) Locally downscaled and spatially customizable climate data for historical and future periods for North America. PLoS One 11:e0156720. https://doi.org/10.1371/journal.pone.0156720
Willis CG, Ellwood ER, Primack RB, Davis CC, Pearson KD, Gallinat AS, Yost JM, Nelson G, Mazer SJ, Rossington NL, Sparks TH, Soltis PS (2017) Old plants, new tricks: phenological research using herbarium specimens. Trends Ecol Evol (Amst) 32:531–546. https://doi.org/10.1016/j.tree.2017.03.015
Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, Davies TJ, Kraft NJ, Ault TR, Bolmgren K, Mazer SJ, McCabe G, McGill B, Parmesan C, Salamin N, Schwartz MD, Cleland EE (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497. https://doi.org/10.1038/nature11014
Zhang X, Friedl MA, Schaaf CB, Strahler AH (2004) Climate controls on vegetation phenological patterns in northern mid-and high latitudes inferred from MODIS data. Glob Chang Biol 10:1133–1145. https://doi.org/10.1111/j.1365-2486.2004.00784.x
Acknowledgments
We thank the botanists that collected the specimens examined in this study. Jonathan Davies and Elizabeth Wolkovich provided feedback and advice on an early draft of this manuscript. Louisa Hsu assisted with data collection. We also thank the anonymous reviewers of this paper for their feedback and insight.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 1945 kb)
Rights and permissions
About this article
Cite this article
Kopp, C.W., Neto-Bradley, B.M., Lipsen, L.P.J. et al. Herbarium records indicate variation in bloom-time sensitivity to temperature across a geographically diverse region. Int J Biometeorol 64, 873–880 (2020). https://doi.org/10.1007/s00484-020-01877-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-020-01877-1