Whereas temporal variability of plant phenology in response to climate change has already been well studied, the spatial variability of phenology is not well understood. Given that phenological shifts may affect biotic interactions, there is a need to investigate how the variability in environmental factors relates to the spatial variability in herbaceous species' phenology by at the same time considering their functional traits to predict their general and species-specific responses to future climate change. In this project, we analysed phenology records of 148 herbaceous species, which were observed for a single year by the PhenObs network in 15 botanical gardens. For each species, we characterised the spatial variability in six different phenological stages across gardens. We used boosted regression trees to link these variabilities in phenology to the variability in environmental parameters (temperature, latitude and local habitat conditions) as well as species traits (seed mass, vegetative height, specific leaf area and temporal niche) hypothesised to be related to phenology variability. We found that spatial variability in the phenology of herbaceous species was mainly driven by the variability in temperature but also photoperiod was an important driving factor for some phenological stages. In addition, we found that early-flowering and less competitive species characterised by small specific leaf area and vegetative height were more variable in their phenology. Our findings contribute to the field of phenology by showing that besides temperature, photoperiod and functional traits are important to be included when spatial variability of herbaceous species is investigated.

Biodiversity Macroecology and Biogeography University of Goettingen Goettingen Germany

Biodiversity Research Institute IMIB Mieres Spain

Biology Department Boston University Boston MA USA

Botanic Garden Berlin Freie Universität Berlin Berlin Germany

Campus Institute Data Science University of Goettingen Goettingen Germany

Centre of Biodiversity and Sustainable Land Use University of Goettingen Goettingen Germany

Core Facility Botanical Garden University Vienna Vienna Austria

Department of Botany Faculty of Science Charles University Prague Czech Republic

Department of Botany University of Kashmir Srinagar Jammu and Kashmir India

Department of Ecosystem Services Helmholtz Centre for Environmental Research UFZ Leipzig Germany

Department of Environmental Biology Sapienza University of Rome Rome Italy

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig Germany

Institute of Biochemistry and Biology Department of Biodiversity Research Systematic Botany with Botanical Garden University of Potsdam Potsdam Germany

Institute of Biodiversity Friedrich Schiller University Jena Jena Germany

Institute of Biology Geobotany and Botanical Garden Martin Luther University Halle Wittenberg Halle Germany

Institute of Ecology and Evolution with Herbarium Haussknecht and Botanical Garden Friedrich Schiller University Jena Jena Germany

Institute of Evolution and Ecology University of Tübingen Tübingen Germany

Institute of Plant Sciences Ecology and Conservation Biology University of Regensburg Regensburg Germany

Max Planck Institute for Biogeochemistry Jena Germany

Palmengarten and Botanical Garden Frankfurt Frankfurt am Main Germany

Petrozavodsk Republic of Karelia Russia

Ringve Botanical Garden NTNU University Museum Norwegian University of Science and Technology Trondheim Norway

Royal Botanic Garden Edinburgh Edinburgh UK

Systematic Botany and Functional Biodiversity Life Science Leipzig University Leipzig Germany

Zobrazit více v PubMed

Ahmad M, Uniyal SK, Batish DR, Rathee S, Sharma P, Singh HP. Flower phenological events and duration pattern is influenced by temperature and elevation in Dhauladhar mountain range of Lesser Himalaya. Ecol Indic. 2021;129:107902. doi: 10.1016/j.ecolind.2021.107902. DOI

Basler D, Körner C. Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agric For Meteorol. 2012;165:73–81. doi: 10.1016/j.agrformet.2012.06.001. DOI

Bianchini K, Morrissey CA. Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds. Sci Rep. 2020;10(1):11706. doi: 10.1038/s41598-020-68497-y. PubMed DOI PMC

Bucher SF, König P, Menzel A, Migliavacca M, Ewald J, Römermann C. Traits and climate are associated with first flowering day in herbaceous species along elevational gradients. Ecol Evol. 2018;8(2):1147–1158. doi: 10.1002/ece3.3720. PubMed DOI PMC

Bucher SF, Römermann C. The timing of leaf senescence relates to flowering phenology and functional traits in 17 herbaceous species along elevational gradients. J Ecol. 2021;109(3):1537–1548. doi: 10.1111/1365-2745.13577. DOI

Büntgen U, Piermattei A, Krusic PJ, Esper J, Sparks T. Crivellaro A (2022) Plants in the UK flower a month earlier under recent warming. P Roy Soc B-Biol Sci. 1968;289:20212456. doi: 10.1098/rspb.2021.2456. PubMed DOI PMC

Cai L, Kreft H, Taylor A, Denelle P, Schrader J, Essl F. Global models and predictions of plant diversity based on advanced machine learning techniques. New Phytol. 2023;237(4):1432–1445. doi: 10.1111/nph.18533. PubMed DOI

Camarillo-Naranjo JM, Álvarez-Francoso JI, Limones-Rodríguez N, Pita-López MF, Aguilar-Alba M. The global climate monitor system: from climate data-handling to knowledge dissemination. Int J Digit Earth. 2019;12(4):394–414. doi: 10.1080/17538947.2018.1429502. DOI

Cornelius C, Petermeier H, Estrella N, Menzel A. A comparison of methods to estimate seasonal phenological development from BBCH scale recording. Int J Biometeorol. 2011;55:867–877. doi: 10.1007/s00484-011-0421-x. PubMed DOI

Craine JM, Wolkovich EM, Gene TE, Kembel SW. Flowering phenology as a functional trait in a tallgrass prairie. New Phytol. 2012;193(3):673–682. doi: 10.1111/j.1469-8137.2011.03953.x. PubMed DOI

Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM. Beyond predictions: biodiversity conservation in a changing climate. Science. 2011;332(6025):53–58. doi: 10.1126/science.1200303. PubMed DOI

Defila C, Clot B. Phytophenological trends in Switzerland. Int J Biometeorol. 2001;45:203–2007. doi: 10.1007/s004840100101. PubMed DOI

Diniz-Filho JAF, de Sant’Ana CER, Bini LM. An eigenvector method for estimating phylogenetic inertia. Evolution. 1998;52(5):1247–1262. doi: 10.1111/j.1558-5646.1998.tb02006.x. PubMed DOI

Dore MHI. Climate change and changes in global precipitation patterns: what do we know? Environ Int. 2005;31(8):1167–1181. doi: 10.1016/j.envint.2005.03.004. PubMed DOI

Dunne JA, Harte J, Taylor KJ. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Mono. 2003;73(1):69–86. doi: 10.1890/0012-9615(2003)073[0069:SMFPRT]2.0.CO;2. DOI

Elith J, Leathwick JR, Hastie T. A working guide to boosted regression trees. J Anim Ecol. 2008;77(4):802–813. doi: 10.1111/j.1365-2656.2008.01390.x. PubMed DOI

Ellenberg H, Leuschner C, Dierschke H (2010) Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht. 6., vollständig neu bearbeitete und stark erweiterte Aufl. / von Christoph Leuschner; mit einem Beitr. von Hartmut Dierschke (synsystematische Gliederung). E. Ulmer, Stuttgart

Facelli JM, Pickett STA. Plant litter: its dynamics and effects on plant community structure. Bot Rev. 1991;57(1):1–32. doi: 10.1007/BF02858763. DOI

Fajardo A, Siefert A. The interplay among intraspecific leaf trait variation, niche breadth and species abundance along light and soil nutrient gradients. Oikos. 2019;128(6):881–891. doi: 10.1111/oik.05849. DOI

Fitter AH, Fitter RSR. Rapid changes in flowering time in British plants. Science. 2002;296(5573):1689–1691. doi: 10.1126/science.1071617. PubMed DOI

Forrest JRK. Plant–pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations? Oikos. 2015;124(1):4–13. doi: 10.1111/oik.01386. DOI

Freiberg M, Winter M, Gentile A, Zizka A, Muellner-Riehl AN, Weigelt A, Wirth C. LCVP, The Leipzig catalogue of vascular plants, a new taxonomic reference list for all known vascular plants. Sci Data. 2020;7(1):416. doi: 10.1038/s41597-020-00702-z. PubMed DOI PMC

Funk JL, Larson JE, Ames GM, Butterfield BJ, Cavender-Bares J, Firn J, et al. Revisiting the Holy Grail: using plant functional traits to understand ecological processes. Biol Rev. 2017;92(2):1156–1173. doi: 10.1111/brv.12275. PubMed DOI

Gaudet CL, Keddy PA. A comparative approach to predicting competitive ability from plant traits. Nature. 1988;334(6179):242–243. doi: 10.1038/334242a0. DOI

Gherardi LA, Sala OE. Effect of interannual precipitation variability on dryland productivity: a global synthesis. Glob Chang Biol. 2019;25(1):269–276. doi: 10.1111/gcb.14480. PubMed DOI

Greenwell B, Boehmke B, Cunningham J, Developers G (2022) gbm: Generalized boosted regression models. R package version 2.1.8.1.https://CRAN.R-project.org/package=gbm. Accessed 29 Nov 2023

Gugger S, Kesselring H, Stöcklin J, Hamann E. Lower plasticity exhibited by high- versus mid-elevation species in their phenological responses to manipulated temperature and drought. Ann Bot. 2015;116(6):953–962. doi: 10.1093/aob/mcv155. PubMed DOI PMC

Harris I, Osborn TJ, Jones P, Lister D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci Data. 2020;7(1):109. doi: 10.1038/s41597-020-0453-3. PubMed DOI PMC

Hijmans RJ, Phillips S, Leathwick J, Elith J. dismo: species distribution modeling. R package version. 2022;1:3–9.

Horbach S, Rauschkolb R, Römermann C. Flowering and leaf phenology are more variable and stronger associated to functional traits in herbaceous compared to tree species. Flora. 2023;300:152218. doi: 10.1016/j.flora.2023.152218. DOI

Huang M, Piao S, Janssens IA, Thu Z, Wang T, Wu D, et al. Velocity of change in vegetation productivity over northern high latitudes. Nature Ecol Evol. 2017;1:1649–1654. doi: 10.1038/s41559-017-0328-y. PubMed DOI

Hunter AF, Lechowicz MJ. Predicting the timing of budburst in temperate trees. Appl Ecol. 1992;29(3):597. doi: 10.2307/2404467. DOI

Inouye DW. Climate change and phenology. WIRE Clim Change. 2022;13(3):e764. doi: 10.1002/wcc.764. DOI

IPCC et al. Summary for policymakers. In: Masson-Delmotte V, et al., editors. Climate change 2021: The physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press; 2021.

Jin Y, Qian H. V.PhyloMaker: an R package that can generate very large phylogenies for vascular plants. Ecography. 2019;42(8):1353–1359. doi: 10.1111/ecog.04434. DOI

Jump AS, Peñuelas J. Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett. 2005;8(9):1010–1020. doi: 10.1111/j.1461-0248.2005.00796.x. PubMed DOI

Kassambara A (2023) rstatix: Pipe-friendly framework for basic statistical tests. R package version 0.7.2. https://CRAN.R-project.org/package=rstatix. Accessed 29 Nov 2023

Kattge J, Bönisch G, Díaz S, Lavorel S, Prentice IC, Leadley P, et al. TRY plant trait database - enhanced coverage and open access. Glob Chang Biol. 2020;26(1):119–188. doi: 10.1111/gcb.14904. PubMed DOI

König P, Tautenhahn S, Cornelissen J, Hans C, Kattge J, Bönisch G, Römermann C. Advances in flowering phenology across the Northern Hemisphere are explained by functional traits. Glob Ecol Biogeogr. 2018;27(3):310–321. doi: 10.1111/geb.12696. DOI

Larcher W. Altitudinal variation in flowering time of Lilac (Syringa vulgaris L.) in the Alps in relation to temperatures. Sam. 2010;1:SBI-3–SBI-18. doi: 10.1553/SundA2006sSBI-3. DOI

Lee BR, Miller TK, Rosche C, Yang Y, Heberling JM, Kuebbing SE, Primack RB. Wildflower phenological escape differs by continent and spring temperature. Nat Commun. 2022;13:7157. doi: 10.1038/s41467-022-34936-9. PubMed DOI PMC

Liu L, Zhang X. Effects of temperature variability and extremes on spring phenology across the contiguous United States from 1982 to 2016. Sci Rep. 2020;10:17952. doi: 10.1038/s41598-020-74804-4. PubMed DOI PMC

Matesanz S, Ramíres-Valiente JA. A review and meta-analysis of intraspecific differences in phenotypic plasticity: implications to forecast plant responses to climate change. Glob Ecol Biogeogr. 2019;28(11):1682–1694. doi: 10.1111/geb.12972. DOI

Melaas EK, Friedl MA, Zhu Z. Detecting interannual variation in deciduous broadleaf forest phenology using Landsat TM/ETM+ data. Remote Sens Environ. 2013;132:176–185. doi: 10.1016/j.rse.2013.01.011. DOI

Menzel A, Fabian P. Growing season extended in Europe. Nature. 1999;397(6721):659. doi: 10.1038/17709. DOI

Menzel A, Sparks THIM, Estrella N, Koch E, Aasa A, Ahas R, et al. European phenological response to climate change matches the warming pattern. Glob Chang Biol. 2006;12(10):1969–1976. doi: 10.1111/j.1365-2486.2006.01193.x. DOI

Migliavacca M, Sonnentag O, Keenan TF, Cescatti A, O’Keefe J, Richardson AD. On the uncertainty of phenological responses to climate change, and implications for a terrestrial biosphere model. Biogeosciences. 2012;9(6):2063–2083. doi: 10.5194/bg-9-2063-2012. DOI

Miller-Rushing AJ, Katsuki T, Primack RB, Ishii Y, Lee SD, Higuchi H. Impact of global warming on a group of related species and their hybrids: cherry tree (Rosaceae) flowering at Mt. Takao, Japan. Am J Bot. 2007;94(9):1470–1478. doi: 10.3732/ajb.94.9.1470. PubMed DOI

Miller-Rushing AJ, Inouye DW, Primack RB. How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J Ecol. 2008;96(6):1289–1296. doi: 10.1111/j.1365-2745.2008.01436.x. DOI

Moles AT, Warton DI, Warman L, Swenson NG, Laffan SW, Zanne AE, et al. Global patterns in plant height. J Ecol. 2009;97(5):923–932. doi: 10.1111/j.1365-2745.2009.01526.x. DOI

Nordt B, Hensen I, Bucher SF, Freiberg M, Primack RB, Stevens A-D, et al. The PhenObs initiative: a standardised protocol for monitoring phenological responses to climate change using herbaceous plant species in botanical gardens. Funct Ecol. 2021;35(4):821–834. doi: 10.1111/1365-2435.13747. DOI

Osada N. Intraspecific variation in spring leaf phenology and duration of leaf expansion in relation to leaf habit and leaf size of temperate tree species. Plant Ecol. 2020;221(10):939–950. doi: 10.1007/s11258-020-01052-x. DOI

Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35(3):526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI

Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421(6918):37–42. doi: 10.1038/nature01286. PubMed DOI

Peaucelle M, Janssens IA, Stocker BD, Ferrando AD, Fu YH, Molowny-Horas R, Ciais P, Peñuelas J. Spatial variance of spring phenology in temperate deciduous forests is constrained by background climatic conditions. Nat Commun. 2019;10:5388. doi: 10.1038/s41467-019-13365-1. PubMed DOI PMC

Petterle A, Karlberg A, Bhalerao RP. Daylength mediated control of seasonal growth patterns in perennial trees. Curr Opin Plant Biol. 2013;16(3):301–306. doi: 10.1016/j.pbi.2013.02.006. PubMed DOI

Primack RB, Miller-Rushing AJ. The role of botanical gardens in climate change research. New Phytol. 2009;182(2):303–313. doi: 10.1111/j.1469-8137.2009.02800.x. PubMed DOI

Raunkiaer C. The life forms of plants and statistical plant geography. London: Oxford University Press; 1934.

Rauschkolb R, Durka W, Godefroid S, Dixon L, Bossdorf O, Ensslin A, Scheepens JF. Recent evolution of flowering time across multiple European plant species correlates with changes in aridity. Oecologia. 2023;202(3):497–511. doi: 10.1007/s00442-023-05414-w. PubMed DOI PMC

R Core Team . R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022.

Ren S, Vitasse Y, Chen X, Peichl M, An S. Assessing the relative importance of sunshine, temperature, precipitation, and spring phenology in regulating leaf senescence timing of herbaceous species in China. Agric For Meteorol. 2022;313:108770. doi: 10.1016/j.agrformet.2021.108770. DOI

Renner SS, Chmielewski F-M. The International Phenological Garden network (1959 to 2021): its 131 gardens, cloned study species, data archiving, and future. Int J Biometeorol. 2022;66(1):35–43. doi: 10.1007/s00484-021-02185-y. PubMed DOI PMC

Renner SS, Zohner CM. Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annu Rev Ecol Evol S. 2018;49(1):165–182. doi: 10.1146/ANNUREV-ECOLSYS-110617-062535. DOI

Rice KE, Montgomery RA, Stefanski A, Rich RL, Reich PB. Species-specific flowering phenology responses to experimental warming and drought alter herbaceous plant species overlap in a temperate-boreal forest community. Ann Bot-London. 2021;127(2):203–211. doi: 10.1093/aob/mcaa156. PubMed DOI PMC

Richards CL, Pennings SC, Donovan LA. Habitat range and phenotypic variation in salt marsh plants. Plant Ecol. 2005;176(2):263–273. doi: 10.1007/s11258-004-0841-3. DOI

Richardson AD, Anderson RS, Arain MA, Barr AG, Bohrer G Chen G et al. (2011) Terrestrial biosphere models need better representation of vegetation phenology: results from the North American carbon program site synthesis. Glob Chang Biol 18(2), 566–584. 10.1111/j.1365-2486.2011.02562.x.

Semmler T, Jacob D. Modeling extreme precipitation events—a climate change simulation for Europe. Global Planet Change. 2004;44(1-4):119–127. doi: 10.1016/j.gloplacha.2004.06.008. DOI

Shen M, Piao S, Cong N, Zhang G, Jassens IA. Precipitation impacts on vegetation spring phenology on the Tibetan Plateau. Glob Chang Biol. 2015;21(10):3647–3656. doi: 10.1111/gcb.12961. PubMed DOI

Sides CB, Enquist BJ, Ebersole JJ, Smith MN, Henderson AN, Sloat LL. Revisiting Darwin's hypothesis: does greater intraspecific variability increase species' ecological breadth? Am J Bot. 2014;101(1):56–62. doi: 10.3732/ajb.1300284. PubMed DOI

Sporbert M, Jakubka D, Bucher SF, Hensen I, Freiberg M, Katja H, et al. Functional traits influence patterns in vegetative and reproductive plant phenology - a multi-botanical garden study. New Phytol. 2022;235(6):2199–2210. doi: 10.1111/nph.18345. PubMed DOI

Steffen W, Broadgate W, Deutsch L, Gaffney O, Ludwig C. The trajectory of the Anthropocene: the Great Acceleration. Anthro Rev. 2015;2(1):81–98. doi: 10.1177/2053019614564785. DOI

Stemkovski M, Bell JR, Ellwood ER, Inouye BD, Kobori H, Lee SD, Lloyd-Evans T, Primack RB, Templ B, Pearse WD. Disorder or a new order: how climate change affects phenological variability. Ecology. 2023;104(1):e3846. doi: 10.1002/ecy.3846. PubMed DOI

Sultan SE. Phenotypic plasticity for fitness components in polygonum species of contrasting ecological breadth. Ecology. 2001;82(2):328–343. doi: 10.1890/0012-9658(2001)082[0328:PPFFCI]2.0.CO;2. DOI

Sun S, Frelich LE. Flowering phenology and height growth pattern are associated with maximum plant height, relative growth rate and stem tissue mass density in herbaceous grassland species. J Ecol. 2011;99(4):991–1000. doi: 10.1111/j.1365-2745.2011.01830.x. DOI

Tautenhahn S, Heilmeier H, Götzenberger L, Klotz S, Wirth C, Kühn I. On the biogeography of seed mass in Germany - distribution patterns and environmental correlates. Ecography. 2008;31(4):457–468. doi: 10.1111/j.0906-7590.2008.05439.x. DOI

Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. J Ecol. 2011;99(6):1299–1307. doi: 10.1111/j.1365-2745.2011.01867.x. DOI

Wadgymar SM, Ogilvie JE, Inouye DW, Weis AE, Anderson JT. Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment. New Phytol. 2018;218(2):517–529. doi: 10.1111/nph.15029. PubMed DOI

Waters CN, Zalasiewicz J, Summerhayes C, Barnosky AD, Poirier C, Gałuszka A, et al. The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science (New York, NY) 2016;351(6269):aad2622. doi: 10.1126/science.aad2622. PubMed DOI

Weigelt P, König C, Kreft H. GIFT – A global inventory of floras and traits for macroecology and biogeography. J Biogeogr. 2020;47(1):16–43. doi: 10.1111/jbi.13623. DOI

Weiher E, van der Werf A, Thompson K, Roderick M, Garnier E, Eriksson O. Challenging Theophrastus: a common core list of plant traits for functional ecology. J Veg Sci. 1999;10(5):609–620. doi: 10.2307/3237076. DOI

Westoby M. A leaf-height-seed (LHS) plant ecology strategy scheme. Plant and Soil. 1998;199:213–227. doi: 10.1023/A:1004327224729. DOI

Wetzel WC, Inouye BD, Hahn PG, Whitehead SR, Underwood N. Variability in plant–herbivore interactions. Annu Rev Ecol Evol S. 2023;54:451–474. doi: 10.1146/annurev-ecolsys-102221-045015. DOI

Willems FM, Scheepens JF, Ammer C, Block S, Bucharova A, Schall P, et al. Spring understory herbs flower later in intensively managed forests. Ecol Appl. 2021;31(5):e02332. doi: 10.1002/eap.2332. PubMed DOI

Yang LH, Rudolf VHW. Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett. 2010;13(1):1–10. doi: 10.1111/j.1461-0248.2009.01402.x. PubMed DOI

Yang Z, Du Y, Shen M, Jiang N, Liang E, Zhu W, et al. Phylogenetic conservatism in heat requirement of leaf-out phenology, rather than temperature sensitivity, in Tibetan Plateau. Agric For Meteorol. 2021;304-305:108413. doi: 10.1016/j.agrformet.2021.108413. DOI

Zhang X, Tan B, Yu Y. Interannual variations and trends in global land surface phenology derived from enhanced vegetation index during 1982–2010. Int J Biometeorol. 2014;58:547–564. doi: 10.1007/s00484-014-0802-z. PubMed DOI

Herbarium specimens reveal a cryptic invasion of polyploid Centaurea stoebe in Europe