Abstract
In recent years, a growing body of evidence has emerged indicating that the relationship between flowering phenology and climate may differ throughout various portions of the growing season. These differences have resulted in long-term changes in flowering synchrony that may alter the quantity and diversity of pollinator attention to many species, as well as altering food availability to pollenivorous and nectarivorous animal species. However, long-term multi-season records of past flowering timing have primarily focused on temperate environments. In contrast, changes in flowering phenology within humid subtropical environments such as the southeastern USA remain poorly documented. This research uses herbarium-based methods to examine changes in flowering time across 19,328 samples of spring-, summer-, and autumn-flowering plants in the southeastern USA from the years 1951 to 2009. In this study, species that flower near the onset of the growing season were found to advance under increasing mean March temperatures (−3.391 days/°C, p = 0.022). No long-term advances in early spring flowering or spring temperature were detected during this period, corroborating previous phenological assessments for the southeastern USA. However, late spring through mid-summer flowering exhibited delays in response to higher February temperatures (over 0.1.85 days/°C, p ≤ 0.041 in all cases). Thus, it appears that flowering synchrony may undergo significant restructuring in response to warming spring temperatures, even in humid subtropical environments.
Similar content being viewed by others
References
Abu-Asab MS, Peterson PM, Shetler SG, Orli SS (2001) Earlier plant flowering in spring as a response to global warming in the Washington, DC, area. Biodivers Conserv 10:597–612
Aldridge G, Inouye DW, Forrest JRK, Barr WA, Miller-Rushing AJ (2011) Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change. J Ecol 99:905–913
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 Lond B 277:2451–2457
Amano T, Freckleton RP, Queensborough SA, Doxford SW, Smithers RJ, Sparks TH, Sutherland WJ (2014) Links between plant species’ spatial and temporal responses to a warming climate. Proc R Soc Lond B 281
Borchert R (1996) Phenology and flowering periodicity of neotropical dry forest species: evidence from herbarium collections. J Trop Ecol 12(1):65–80
Borchert R, Meyer SA, Felger RS, Porter-Bollard L (2004) Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Glob Ecol Biogeogr 13:409–425
Borchet R (1994) Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75:1437–1449
Brearley FQ, Proctor J, Suriantata NL, Dalrymple G, Voysey BC (2007) Reproductive phenology over a 10-year period in a lowland evergreen rain forest of central Borneo. J Ecol 95(4):828–839
Calle Z, Schlumpberger BO, Piedharita L, Leftin A, Hammer SA, Tye A, Borchet R (2010) Seasonal variation in daily insolation induces synchronous bud break and flowering in the tropics. Trees 24:865–877
Callinger KM, Queenborough S, Curtis PS (2013) Herbarium specimins reveal the footprint of climate change on flowering trends across north-central North America. Ecol Lett 16:1037–1044
Cannell MGR, Smith RI (1986) Climatic warming, spring budburst and forest damage on trees. J Appl Ecol 23(1):177–191
Cayan DR, Kammerdiener SA, Dettinger MD, Caprio JM, Peterson DH (2001) Changes in the onset of spring in the western United States. Bull Am Meteorol Soc 82(3):399–415
Chuine I, Cour P (1999) Climatic determinants of budburst seasonality in four temperate-zone tree species. New Phytol 143(2):339–349
Diskin E, Proctor H, Jebb M, Sparks T, Donnelly A (2012) The phenology of Rubus fructicosus in Ireland: herbarium specimens provide evidence for the response of phenophases to temperature, with implications for climate warming. Int J Biometeorol 56(6):1103–1111
Estrella N, Sparks T, Menzel A (2007) Trends and temperature in the phenology of crops in Germany. Glob Chang Biol 13(8):1737–1747
Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691
Fitter AH, Fitter RSR, Harris ITB, Williamson MH (1995) Relationship between first flowering date and temperature in the flora of a locality in central England. Funct Ecol 9:55–60
Funderburk DO, Skeen JN (1976) Spring phenology in a mature piedmont forest. Castanea 41(1):20–30
Gaira KS, Dhar U, Belwal OK (2011) Potential of herbarium records to sequence phenological pattern: a case study of Aconitum heterophyllum in the Himalaya. Biodivers Conserv 20(10):2201–2210
Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495
Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Glob Chang Biol 16:1082–1106
Hegland SJ, Nielsen A, Lázaro A, Bjerknes A-L, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12(2):184–195
Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263
Lavoie C, Lachance D (2006) A new herbarium-based method for reconstructing the phenology of plant species across large areas. Am J Bot 93(4):512–516
Lawrimore JH, Menne MJ, Gleason BE, Williams CN, Wuertz DB, Vose RS, Rennie J (2011) An overview of the Global Historical Climatology Network monthly mean temperature data set, version 3. J Geophys Res 116(D19121):1–18
Ledneva A, Miller-Rushing AJ, Primack RB, Imbres C (2004) Climate change as reflected in a naturalist’s diary, Middleborough, Massachusetts. Wilson Bull 116(3):224–231
Loiselle BA, Jørgensen PM, Consiglio T, Jiménez I, Blake JG, Lohmann LG, Montiel OM (2008) Predicting species distributions from herbarium collections: does climate bias in collection sampling influence model outcomes? J Biogeogr 35(1):105–116
Marques MCM, Roper JJ, Salvalaggio APB (2004) Phenological patterns among plant life-forms in a subtropical forest in southern Brazil. Plant Ecol 173:203–213
McKinney AM, CaraDonna PJ, Inouye DW, Barr B, Bertelsen CD, Waser NM (2012) Asynchronous changes in phenology of migrating Broad-tailed Hummingbirds and their early-season nectar resources. Ecology 93(9):1987–1993
Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717
Menzel A (2003) Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Chang 57(3):243–263
Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397(659)
Menzel A, Estrella N, Fabian P (2001) Spatial and temporal variability of the phenological seasons in Germany from 1951 to 1996. Glob Chang Biol 7:657–666
Menzel A, Estrella N, Testka A (2005) Temperature response rates from long-term phenological records. Clim Res 30:21–28
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissoli P, Og B, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Fillella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen P, Remišová V, Scheifinger H, Striz M, Susnik A, van Vliet AJH, Wielgolaski F-E, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12(10):1969–1976
Miller-Rushing AJ, Primack RB (2008) Global warming and flowering times in Thoreau’s Concord: a community perspective. Ecology 89(2):332–341
Miller-Rushing AJ, Primack RB, Primack D, Mukunda S (2006) Photographs and herbarium specimens as tools to document phenological changes in response to global warming. Am J Bot 93(11):1667–1674
Miller-Rushing AJ, Inouye DW, Primack RB (2008) How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J Ecol 96(6):1289–1296
Opler PA, Gordon WF, Baker HG (1976) Rainfall as a factor in the release, timing, and synchronization of anthesis by tropical trees and shrubs. J Biogeogr 3(3):231–236
Panchen ZA, Primack RB, Anísko T, Lyons RE (2012) Herbarium specimens, photographs, and field observations show Philadelphia area plants are responding to climate change. Am J Bot 99(4):751–756
Park IW (2012) Digital herbarium archives as a spatially extensive, taxonomically discriminate phenological record; a comparison to MODIS satellite imagery. Int J Biometeorol 14(10):2029–2038
Peñuelas J, Filella I, Zhang X, Llorens L, Ogaya R, Lloret F, Comas P, Estiarte M, Terradas J (2004) Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol 161(3):837–846
Primack D, Imbres C, Primack RB, Miller-Rushing AJ (2004) Herbarium specimens demonstrate earlier flowering times in response to warming in Boston. Am J Bot 91(8):1260–1264
Rivera G, Borchert R (2001) Induction of flowering in tropical trees by a 30-minute reduction in photoperiod: evidence from field observations and herbarium specimens. Tree Physiol 21:201–212
Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the northern hemisphere. Glob Chang Biol 12:343–351
Schwartz MD, Ault TR, Betancourt J (2013) Spring onset variations and trends in the continental United States: past and regional assessment using temperature-based indices. Int J Climatol 33(13):2917–2922
Sherry RA, Zhou X, Gu S, Arnone JA III, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. PNAS 104(1):198–202
Spano D, Cesaraccio C, Duce P, Snyder RL (1999) Phenological stages of natural species and their use as climate indicators. Int J Biometeorol 42:124–133
Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long term phenological records from the UK. Int J Biometeorol 44:82–87
Staggemeier VG, Diniz-Filho JAF, Morellato LPC (2010) The shared influence of phylogeny and ecology on the reproductive patterns of Myrteae (Myrtaceae). J Ecol 98:1409–1421
Tachiki Y, Iwasa Y, Satake A (2010) Pollinator coupling can induce synchronized flowering in different plant species. J Theor Biol 267:153–163
Wall MA, Timmerman-Erskine M, Boyd RS (2003) Conservation impact of climatic variability on pollination of the federally endangered plant, Clematis socialis (Ranunculaceae). Southeast Nat 2(1):11–24
Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59(5):934
Wolfe DW, Schwartz MD, Lasko AN, Otsuki Y, Pool RM, Shaulis NJ (2005) Climate change and shifts in spring phenology of three horticultural woody perennials in northeastern USA. Int J Biometeorol 49(5):303–309
Wolkovich EM, Cook BI, Allen JM, Crimmins TM, Betancourt JL, Travers SE, Pau S, Regetz J, Davies TJ, Kraft NJB, Ault TR, Bolmgren K, Mazer SJ, McCabe GJ, McGill BJ, Parmesan C, Salamin N, Schwartz MD, Cleland EE (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 2(485):494–497
Zalamea P-C, Munoz F, Stevenson PR, Paine CET, Sarmiento C, Sabatier D, Heuret P (2011) Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens. Proc R Soc Lond B 278(1717):2437–2445
Acknowledgments
We would like to acknowledge the contributions of Dixie Damrel of the Clemson herbarium, John Nelson of the A. C. Moore herbarium at the University of South Carolina, and Austin Mast of the Florida State University herbarium for access to their records as well as Herrick Brown for assistance with herbarium database software and Gretchen Meyer and Alison Donnelly for advice that improved this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Park, I.W., Schwartz, M.D. Long-term herbarium records reveal temperature-dependent changes in flowering phenology in the southeastern USA. Int J Biometeorol 59, 347–355 (2015). https://doi.org/10.1007/s00484-014-0846-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-014-0846-0