Herbarium specimens reveal a significantly earlier flowering trend for Cypripedium acaule (Orchidaceae) in North Carolina (U.S.A.)
DOI :
https://doi.org/10.17348/jbrit.v19.i3.1424Mots-clés :
climate change, Cypripedium acaule, flowering times, herbarium specimens, linear regression, North Carolina, phenologyRésumé
Cypripedium acaule, the pink lady’s slipper, is an orchid native to eastern North America, ranging from central and eastern Canada to the southeastern United States. It is a rather common and striking spring wildflower in North Carolina (NC), extending from the mountains to the coastal plain region. A preliminary survey of herbarium specimens at Duke University (DUKE) suggested that flowering times for C. acaule collected in NC in recent years were notably earlier than for those from the last century. Here we set out to investigate this phenological hypothesis by accessing the Southeast Regional Network of Expertise and Collections (SERNEC) portal to extract the metadata from 57 herbaria for 502 herbarium records of C. acaule from NC. Of these, only 193 herbarium specimens from 55 counties, spanning the years 1886–2022, had been collected when the plant was in flower. Each of these “time-stamped” records was manually georeferenced to include latitude, longitude, and elevation coordinates, using tools in Google Earth Pro. Because NC varies by over 2037m in elevation, nearly 3° in latitude, and 10° in longitude, the flowering times recorded for C. acaule spanned 83 spring days. To control for the effect of location on flowering time, we implemented Hopkins’ Bioclimatic Law to normalize flowering times across the state. A linear regression of the 193 normalized flowering dates suggests an overall shift in blooming that has advanced by 21 days since 1886. A mixed-effects regression was performed to determine the relationship of elevation, latitude, average winter temperature, total winter precipitation, and the total number of winter frost days from the year and location of collection (as fixed variables) on the effect of flowering day of year (DOY). The most significant effect on the flowering DOY was from average winter temperature: for each increase in 1° C, the flowering DOY was 3.23 days earlier. If this trend continues, the flowering time of C. acaule could become decoupled from the peak activity of its pollinators, increasing the risk of reproductive failure. This study highlights the vital role of herbarium specimens in understanding the effects of climate change on shifts in phenological patterns.
Références
ALMOROX, J. & P. MARTÍ. 2022. Misuses of the terms Day of the Year and Julian Day in agricultural and environmental sciences. Agric. Water Managem. 267:107613. DOI:10.1016/j.agwat.2022.107613.
ARIETTA, A.Z.A. 2020. "Julian Date vs Day of the Year". Website (https://www.azandisresearch.com/2020/01/27/julian-date-vs-day-of-the-year/). Accessed May 2024.
BADECK, F.W., A. BONDEAU, K. BÖTTCHER, D. DOKTOR, W. LUCHT, J. SCHABER, & S. SITCH. 2004. Responses of spring phenology to climate change. New Phytol. 162:295–309. DOI:10.1111/j.1469-8137.2004.01059.x
BERG, C.S., J.L. BROWN, & J.J. WEBER. 2019. An examination of climate-driven flowering-time shifts at large spatial scales over 153 years in a common weedy annual. Amer. J. Bot. 106:1435–1443. DOI:10.1002/ajb2.1381
BLOMQUIST, H.L. & H.J. OOSTING. 1934. A guide to the spring flora of the Lower Piedmont, North Carolina. Seeman Printer, Durham, NC, U.S.A.
BOLMGREN, K., D. VANHOENACKER, & A.J. MILLER-RUSHING. 2012. One man, 73 years, and 25 species. Evaluating phenological responses using a lifelong study of first flowering dates. Int. J. Biometeorol. 57:367–375. DOI:10.1007/s00484-012-0560-8
CALINGER, K.M., S. QUEENBOROUGH, & P.S. CURTIS. 2013. Herbarium specimens reveal the footprint of climate change on flowering trends across north-central North America. Ecol. Lett. 16:1037–1044. DOI:10.1111/ele.12135
DAVIS, C.C. & J.M. YOST. 2020. The contribution of herbarium specimens to phenology research. Appl. Pl. Sci. 8:e11315. DOI:10.1002/aps3.11315
DAVIS, C.C., C.G. WILLIS, B. CONNOLLY, C. KELLY, & A.M. ELLISON. 2015. Herbarium records are reliable sources of phenological change driven by climate and provide novel insights into species’ phenological cueing mechanisms. Amer. J. Bot. 102:1599–1609. DOI:10.3732/ajb.1500237
GAIRA K.S., O.K. BELWAL, & I.D. BHATT. 2024. Potential of herbarium-based phenological studies to predict the climate change impacts. J. Pl. Sci. Phytopathol. 8:110–112. DOI:10.29328/journal.jpsp.1001141
GUPTON, O.W. & F.C. SWOPE. 1986. Wild orchids of the middle Atlantic states. University of Tennessee Press, Knoxville, U.S.A. DOI:10.2307/2996479
ETTINGER, A.K., C.J. CHAMBERLAIN, & E.M. WOLKOVICH. 2022. The increasing relevance of phenology to conservation. Nat. Clim. Change 12:305–307. DOI:10.1038/s41558-022-01330-8
FOX, J. & S. WEISBERG. 2019. An R Companion to applied regression, Third edition. Sage, Thousand Oaks CA, U.S.A. https://www.john-fox.ca/Companion/.
GEISSLER C., A. DAVIDSON, & R.A. NIESENBAUM. 2023. The influence of climate warming on flowering phenology in relation to historical annual and seasonal temperatures and plant functional traits. PeerJ 11:e15188. DOI:10.7717/peerj.15188.
HARRIS, I., T.J. OSBORN, P. JONES, & D. LISTER. 2020. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7:109. https://doi.org/10.1038/s41597-020-0453-3
HEDRICK, B., M. HEBERLING, E. MEINEKE, K. TURNER, C. GRASSA, D.S. PARK, J. KENNEDY, J. CLARKE, J. COOK, & D. BLACKBURN. 2020. Digitization and the future of natural history collections. Biosci. 70:243–251. DOI:10.1093/biosci/biz163
HOPKINS, A.D. 1919. The bioclimatic law as applied to entomological research and farm practice. Sci. Mon. 8:496–513. http://www.jstor.org/stable/6960.
HOPKINS, A.D. 1920. The bioclimatic law. J. Wash. Acad. Sci. 10:34–40. https://www.jstor.org/stable/24521154
JONES, C.A. & C.C. DAEHLER. 2018. Herbarium specimens can reveal impacts of climate change on plant phenology; a review of methods and applications. PeerJ 6:e4576. DOI:10.7717/peerj.4576.
KOPPEL, O. & J.T. KERR. 2022. Strong phenological shifts among bumblebee species in North America can help predict extinction risk. Biol. Conserv. 272:109675. DOI:10.1016/j.biocon.2022.109675
KUNKEL, K.E., D.R. EASTERLING, A. BALLINGER, ET AL. 2020: North Carolina Climate Science Report. North Carolina Institute for Climate Studies. 233 pp. https://ncics.org/nccsr
KUZNETSOVA, A., P.B. BROCKHOFF, & R.H.B. CHRISTENSEN. 2017. lmerTest Package: Tests in linear mixed effects models. J. Stat. Softw. 82:1–26. DOI: 10.18637/jss.v082.i13.
LIETH, H. 1974. Phenology and seasonality modeling. H. Lieth, ed. Springer Science & Business Media, Berlin, Germany.
LÜDECKE, D. 2018. ggeffects: Tidy data frames of marginal effects from regression models. J. Open Source Softw. 3:772. DOI: 10.21105/joss.00772
MEINEKE, E.K., C.C. DAVIS, & T.J. DAVIES. 2018. The unrealized potential of herbaria for global change biology. Ecol. Monogr. 88:505–525. DOI:10.1002/ecm.1307
MILLER-RUSHING, A.J., T.T. HØYE, D.W. INOUYE, & E. POST. 2010. The effects of phenological mismatches on demography. Philos. Trans. R. Soc. B, Biol. Sci. 365:3177–3186. DOI:10.1098/rstb.2010.0148
NOAA. National Centers for Environmental Information, Monthly Global Climate Report for Annual 2023, published online January 2024, retrieved on December 18, 2024 from https://www.ncei.noaa.gov/access/monitoring/monthly-report/global/202313.
PANCHEN, Z.A., R.B. PRIMACK, A.S. GALLINAT, B. NORDT, A.D. STEVENS, Y. DU, & R. FAHEY. 2014. Herbarium specimens, photographs, and field observa-tions show Philadelphia area plants are responding to climate change. Amer. J. Bot. 101:751–756. DOI:10.3732/ajb.1100198
PARK, D.S., I. BRECKHEIMER, A.C. WILLIAMS, E. LAW, A.M. ELLISON, & C.C. DAVIS. 2018. Herbarium specimens reveal substantial and unexpected variation in phenological sensitivity across the eastern United States. Phil. Trans. R. Soc. B 374:20170394. https://doi.org/10.1098/rstb.2017.0394
PARK, D.S., X. FENG, S. AKIYAMA, M. ARDIYANI, N. AVENDAÑO, Z. BARINA, B. BÄRTSCHI, M. BELGRANO, J. BETANCUR, R. BIJMOER, A. BOGAERTS, A. CANO, J. DANIHELKA, A. GARG, D.E. GIBLIN, R. GOGOI, A. GUGGISBERG, M. HYVÄRINEN, S.A. JAMES, R.J. SEBOLA, T. KATAGIRI, J.A. KENNEDY, T. SH. KOMIL, B. LEE, S.M.L. LEE, D. MAGRI, R. MARCUCCI, S. MASINDE, D. MELNIKOV, P. MRÁZ, W. MULENKO, P. MUSILI, G. MWACHALA, B.E. NELSON, C. NIEZGODA, C. NOVOA SEPÚLVEDA, S. ORLI, A. PATON, S. PAYETTE, K.D. PERKINS, M.J. PONCE, H. RAINER, L. RASINGAM, H. RUSTIAMI, N.M. SHIYAN, C.S. BJORÅ, J. SOLOMON, F. STAUFFER, A. SUMADIJAYA, M. THIÉBAUT, B.M. THIERS, H. TSUBOTA, A. VAUGHAN, R. VIRTANEN, T.J.S. WHITFELD, D. ZHANG, F.O. ZULOAGA, & C.C. DAVIS. 2023. The colo-nial legacy of herbaria. Nat. Hum. Behav. 7:1059–1068. DOI:10.1038/s41562-023-01616-7
PARK, I.W., S.J. MAZER, & T. RAMIREZ-PARADA. 2025. Herbarium specimens as sources of phenological data. In: M.D. Schwartz, eds. Phenology: An integrative environmental science. Springer, Cham, Switzerland. Pp. 405–428. DOI:10.1007/978-3-031-75027-4_18
PELÁEZ M., J.-M. GAILLARD, K. BOLLMANN, M. HEURICH, & M. REHNUS. 2020. Large-scale variation in birth timing and synchrony of a large herbivore along the latitudinal and altitudinal gradients. J. Anim. Ecol. 89:1906–1917. https://doi.org/10.1111/1365-2656.13251
PRIMACK, D., C. IMBRES, R.B. PRIMACK, A.J. MILLER-RUSHING, & P. DEL TREDICI. 2004. Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. Amer. J. Bot. 91:1260–1264. DOI:10.3732/ajb.91.8.1260
R CORE TEAM. 2023. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
RICHARDSON, A.D., K. HUFKENS, X. LI, & T.R. AULT. 2019. Testing Hopkins’ bioclimatic law with Phenocam data. Appl. Pl. Sci. 7. DOI:10.1002/aps3.1228.
SCHLEIP, C., T. RUTISHAUSER, J. LUTERBACHER, & A. MENZEL. 2008. Time series modeling and central European temperature impact assessment of phenological records over the last 250 years, J. Geophys. Res. 113: G04026. DOI:10.1029/2007JG000646.
SOLTIS, P.S. 2017. Digitization of herbaria enables novel research. Amer. J. Bot.104:1281–1284. DOI:10.3732/ajb.1700281
SONG, Z., Y.H. FU, Y. DU, L. LI, X. OUYANG, W. YE, & Z. HUANG. 2020. Flowering phenology of a widespread perennial herb shows contrasting re-sponses to global warming between humid and non-humid regions. Funct. Ecol. DOI:10.1111/1365-2435.13634
SERNEC Data Portal. 2024. https://sernecportal.org/index.php.
SUZUKI-OHNO, Y., J. YOKOYAMA, T. NAKASHIZUKA, & M. KAWATA. 2020. Estimating possible bumblebee range shifts in response to climate and land cover changes. Sci. Rep. 10:19622. DOI:10.1038/s41598-020-76164-5
SZABÓ, B., E. VINCZE, & B. CZÚCZ. 2016. Flowering phenological changes in relation to climate change in Hungary. Int. J. Biometeorol. 60:1347–1356. DOI:10.1007/s00484-015-1128-1
VISSER, M.E. & P. GIENAPP. 2019. Evolutionary and demographic consequences of phenological mismatches. Nat. Ecol. Evol. 3:879–885. DOI:10.1038/s41559-019-0880-8
WEAKLEY, A.S., & SOUTHEASTERN FLORA TEAM. 2024. Flora of the southeastern United States. University of North Carolina Herbarium, North Carolina Botanical Garden, Chapel Hill, U.S.A. Retrieved from https://fsus.ncbg.unc.edu.
WICKHAM, H. 2016. ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York, U.S.A.
WOLKOVICH, E.M., T.J. DAVIES, H. SCHAEFER, E.E. CLELAND, B.I. COOK, S.E. TRAVERS, C.G. WILLIS, & C.C. DAVIS. 2013. Temperature-dependent shifts in phenology contribute to the success of exotic species with climate change. Amer. J. Bot. 100:1407–1421. DOI:10.3732/ajb.1200478
Téléchargements
Publié-e
Comment citer
Numéro
Rubrique
Licence
(c) Tous droits réservés Botanical Research Institute of Texas 2025

Cette œuvre est sous licence Creative Commons Attribution - Pas d'Utilisation Commerciale - Pas de Modification 4.0 International.