Long-term herbarium records reveal temperature-dependent changes in flowering phenology in the southeastern USA

International Journal of Biometeorology

Volumn 59, Issue 3, 2015, Pages 347-355

  Park, Isaac W ^a   Schwartz, Mark D ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Climate change; Flowering; Herbarium; Phenology; Southeastern USA

Indexed keywords

FLOWER; PHYSIOLOGY; PLANT PHYSIOLOGY; SEASON; TEMPERATURE; UNITED STATES;

FLORIDA; FLOWERS; PLANT PHYSIOLOGICAL PHENOMENA; SEASONS; SOUTH CAROLINA; TEMPERATURE;

EID: 84939891955     PISSN: 00207128     EISSN: 14321254     Source Type: Journal    
DOI: 10.1007/s00484-014-0846-0     Document Type: Article

References (56)

1. 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
2. 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
3. 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
4. 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
5. Borchert R (1996) Phenology and flowering periodicity of neotropical dry forest species: evidence from herbarium collections. J Trop Ecol 12(1):65–80
6. 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
7. Borchet R (1994) Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75:1437–1449
8. 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
9. 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
10. 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
11. Cannell MGR, Smith RI (1986) Climatic warming, spring budburst and forest damage on trees. J Appl Ecol 23(1):177–191
12. 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
13. Chuine I, Cour P (1999) Climatic determinants of budburst seasonality in four temperate-zone tree species. New Phytol 143(2):339–349
14. 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
15. Estrella N, Sparks T, Menzel A (2007) Trends and temperature in the phenology of crops in Germany. Glob Chang Biol 13(8):1737–1747
16. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691
17. 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
18. Funderburk DO, Skeen JN (1976) Spring phenology in a mature piedmont forest. Castanea 41(1):20–30
19. 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
20. Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495
21. Gordo O, Sanz JJ (2010) Impact of climate change on plant phenology in Mediterranean ecosystems. Glob Chang Biol 16:1082–1106
22. 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
23. 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
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. Memmott J, Craze PG, Waser NM, Price MV (2007) Global warming and the disruption of plant-pollinator interactions. Ecol Lett 10:710–717
31. Menzel A (2003) Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Chang 57(3):243–263
32. Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397(659)
33. 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
34. Menzel A, Estrella N, Testka A (2005) Temperature response rates from long-term phenological records. Clim Res 30:21–28
35. 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
36. Miller-Rushing AJ, Primack RB (2008) Global warming and flowering times in Thoreau’s Concord: a community perspective. Ecology 89(2):332–341
37. 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
38. 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
39. 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
40. 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
41. 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
42. 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
43. 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
44. 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
45. Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the northern hemisphere. Glob Chang Biol 12:343–351
46. 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
47. 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
48. 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
49. 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
50. 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
51. Tachiki Y, Iwasa Y, Satake A (2010) Pollinator coupling can induce synchronized flowering in different plant species. J Theor Biol 267:153–163
52. 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
53. Waser NM (1978) Competition for hummingbird pollination and sequential flowering in two Colorado wildflowers. Ecology 59(5):934
54. 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
55. 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
56. 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