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An observation-based progression modeling approach to spring and autumn deciduous tree phenology

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Abstract

It is important to accurately determine the response of spring and autumn phenology to climate change in forest ecosystems, as phenological variations affect carbon balance, forest productivity, and biodiversity. We observed phenology intensively throughout spring and autumn in a temperate deciduous woodlot at Milwaukee, WI, USA, during 2007–2012. Twenty-four phenophase levels in spring and eight in autumn were recorded for 106 trees, including white ash, basswood, white oak, boxelder, red oak, and hophornbeam. Our phenological progression models revealed that accumulated degree-days and day length explained 87.9–93.4 % of the variation in spring canopy development and 75.8–89.1 % of the variation in autumn senescence. In addition, the timing of community-level spring and autumn phenophases and the length of the growing season from 1871 to 2012 were reconstructed with the models developed. All simulated spring phenophases significantly advanced at a rate from 0.24 to 0.48 days/decade (p ≤ 0.001) during the 1871–2012 period and from 1.58 to 2.00 days/decade (p < 0.02) during the 1970–2012 period; two simulated autumn phenophases were significantly delayed at a rate of 0.37 (mid-leaf coloration) and 0.50 (full-leaf coloration) days/decade (p < 0.01) during the 1970–2012 period. Consequently, the simulated growing season lengthened at a rate of 0.45 and 2.50 days/decade (p < =0.001), respectively, during the two periods. Our results further showed the variability of responses to climate between early and late spring phenophases, as well as between leaf coloration and leaf fall, and suggested accelerating simulated ecosystem responses to climate warming over the last four decades in comparison to the past 142 years.

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References

  • Archetti M, Richardson AD, O'Keefe J, Delpierre N (2013) Predicting climate change impacts on the amount and duration of autumn colors in a New England forest. PLoS One 8(3):e57373

    Article  CAS  Google Scholar 

  • Basler D, Korner C (2012) Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agric For Meteorol 165:73–81

    Article  Google Scholar 

  • Caffarra A, Donnelly A, Chuine I, Jones MB (2011) Modelling the timing of Betula pubescens budburst. I Temperature and photoperiod: a conceptual model. Clim Res 46(2):147–157

    Article  Google Scholar 

  • Cannell MGR, Smith RI (1983) Thermal time, chill days and prediction of budburst in Picea-Sitchensis. J Appl Ecol 20(3):951–963

    Article  Google Scholar 

  • Chen XQ, Xu L (2012) Phenological responses of Ulmus pumila (Siberian Elm) to climate change in the temperate zone of China. Int J Biometeorol 56(4):695–706

    Article  Google Scholar 

  • Chuine I (2000) A unified model for budburst of trees. J Theor Biol 207(3):337–347

    Article  CAS  Google Scholar 

  • Chuine I, Cour P, Rousseau DD (1998) Fitting models predicting dates of flowering of temperate-zone trees using simulated annealing. Plant Cell Environ 21(5):455–466

    Article  Google Scholar 

  • Chuine I, Cour P, Rousseau DD (1999) Selecting models to predict the timing of flowering of temperate trees: implications for tree phenology modelling. Plant Cell Environ 22(1):1–13

    Article  Google Scholar 

  • Chuine I, de Cortazar-Atauri IG, Kramer K, Hanninen H (2013) Plant development models. In: Schwartz MD (ed) Phenology: an integrative environmental science. Springer, Dordrecht, pp 275–293

    Chapter  Google Scholar 

  • Delpierre N, Dufrene E, Soudani K, Ulrich E, Cecchini S, Boe J, Francois C (2009) Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agric For Meteorol 149(6-7):938–948

    Article  Google Scholar 

  • Donnelly A, Cooney T, Jennings E, Buscardo E, Jones M (2009) Response of birds to climatic variability; evidence from the western fringe of Europe. Int J Biometeorol 53(3):211–220

    Article  Google Scholar 

  • Donnelly A, Salamin N, Jones MB (2006) Changes in tree phenology: an indicator of spring warming in Ireland? Biol Environ 106B(1):49–56

    Google Scholar 

  • Estrella N, Menzel A (2006) Responses of leaf colouring in four deciduous tree species to climate and weather in Germany. Clim Res 32(3):253–267

    Article  Google Scholar 

  • Fu YSH, Campioli M, Van Oijen M, Deckmyn G, Janssens IA (2012) Bayesian comparison of six different temperature-based budburst models for four temperate tree species. Ecol Model 230:92–100

    Article  Google Scholar 

  • Hanes JM, Richardson AD, Klosterman S (2013) Mesic temperate deciduous forest phenology. In: Schwartz MD (ed) Phenology: an integrative environmental science. Springer, Dordrecht, pp 211–224

    Chapter  Google Scholar 

  • Hunter AF, Lechowicz MJ (1992) Predicting the timing of budburst in temperate trees. J Appl Ecol 29(3):597–604

    Article  Google Scholar 

  • Jeong SJ, Ho CH, Gim HJ, Brown ME (2011) Phenology shifts at start vs. end of growing season in temperate vegetation over the Northern Hemisphere for the period 1982-2008. Glob Chang Biol 17(7):2385–2399

    Article  Google Scholar 

  • Jeong SJ, Medvigy D (2014) Macroscale prediction of autumn leaf coloration throughout the continental United States. Global Ecol Biogeogr 23(11):1245–1254

  • Keskitalo J, Bergquist G, Gardestrom P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139(4):1635–1648

    Article  CAS  Google Scholar 

  • Lechowicz MJ (1984) Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. Am Nat 124(6):821–842

    Article  Google Scholar 

  • Liang L, Schwartz M (2013) Testing a growth efficiency hypothesis with continental-scale phenological variations of common and cloned plants. Int J Biometeorol: 1–9

  • Libiseller C, Grimvall A (2002) Performance of partial Mann-Kendall tests for trend detection in the presence of covariates. Environmetrics 13(1):71–84

    Article  CAS  Google Scholar 

  • Lieth H (1974) Phenology and seasonality modeling. Springer, Berlin, Heidelberg, New York

    Book  Google Scholar 

  • Lopez OR, Farris-Lopez K, Montgomery RA, Givnish TJ (2008) Leaf phenology in relation to canopy closure in southern Appalachian trees. Am J Bot 95(11):1395–1407

    Article  Google Scholar 

  • McMaster GS, Wilhelm WW (1997) Growing degree-days: one equation, two interpretations. Agric For Meteorol 87(4):291–300

    Article  Google Scholar 

  • Meier U (2001) Growth stages of mono-and dicotyledonous plants, BBCH Monograph. 2 edn., Federal Biological Research Centre for Agriculture and Forestry

  • Menzel A (2003) Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Chang 57(3):243–263

    Article  Google Scholar 

  • Menzel A, Estrella N, Testka A (2005) Temperature response rates from long-term phenological records. Clim Res 30(1):21–28

    Article  Google Scholar 

  • Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kubler K, Bissolli P, Braslavska O, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl A, Defila C, Donnelly A, Filella Y, Jatcza K, Mage F, Mestre A, Nordli O, Penuelas J, Pirinen P, Remisova V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski FE, Zach S, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12(10):1969–1976

    Article  Google Scholar 

  • Morisette JT, Richardson AD, Knapp AK, Fisher JI, Graham EA, Abatzoglou J, Wilson BE, Breshears DD, Henebry GM, Hanes JM, Liang L (2009) Tracking the rhythm of the seasons in the face of global change: phenological research in the 21st century. Front Ecol Environ 7(5):253–260

    Article  Google Scholar 

  • NOAA (2015) Data Tools: 1981-2010 Normals (MILWAUKEE MITCHELL INTERNATIONAL AIRPORT, WI US). http://www.ncdc.noaa.gov/cdo-web/datatools/normals. Accessed March 2015

  • Parmesan C (2007) Influences of species, latitudes and methodologies on estimates of phenological response to global warming. Glob Chang Biol 13(9):1860–1872

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42

    Article  CAS  Google Scholar 

  • Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) (2007) Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Penuelas J, Rutishauser T, Filella I (2009) Phenology feedbacks on climate change. Science 324(5929):887–888

    Article  CAS  Google Scholar 

  • Polgar CA, Primack RB (2011) Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol 191(4):926–941

    Article  Google Scholar 

  • Richardson AD, Anderson RS, Arain MA, Barr AG, Bohrer G, Chen GS, Chen JM, Ciais P, Davis KJ, Desai AR, Dietze MC, Dragoni D, Garrity SR, Gough CM, Grant R, Hollinger DY, Margolis HA, McCaughey H, Migliavacca M, Monson RK, Munger JW, Poulter B, Raczka BM, Ricciuto DM, Sahoo AK, Schaefer K, Tian HQ, Vargas R, Verbeeck H, Xiao JF, Xue YK (2012) 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

    Article  Google Scholar 

  • Richardson AD, Bailey AS, Denny EG, Martin CW, O'Keefe J (2006) Phenology of a northern hardwood forest canopy. Glob Chang Biol 12(7):1174–1188

    Article  Google Scholar 

  • Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S, Migliavacca M, Montagnani L, Munger JW, Moors E, Piao SL, Rebmann C, Reichstein M, Saigusa N, Tomelleri E, Vargas R, Varlagin A (2010) Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philos Trans R Soc B-Biol Sci 365(1555):3227–3246

    Article  Google Scholar 

  • Richardson AD, Keenan TF, Migliavacca M, Ryu Y, Sonnentag O, Toomey M (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173

    Article  Google Scholar 

  • Rogerson P (2006) Statistical methods for geography. SAGE, London

    Google Scholar 

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421(6918):57–60

    Article  CAS  Google Scholar 

  • Schwartz MD (1996) Examining the spring discontinuity in daily temperature ranges. J Clim 9(4):803–808

    Article  Google Scholar 

  • Schwartz MD, Ahas R, Aasa A (2006) Onset of spring starting earlier across the Northern Hemisphere. Glob Chang Biol 12(2):343–351

    Article  Google Scholar 

  • Schwartz MD, Betancourt JL, Weltzin JF (2012) From Caprio's lilacs to the USA National Phenology Network. Front Ecol Environ 10(6):324–327

    Article  Google Scholar 

  • Schwartz MD, Chen XQ (2002) Examining the onset of spring in China. Clim Res 21(2):157–164

    Article  Google Scholar 

  • Schwartz MD, Hanes JM, Liang L (2013) Comparing carbon flux and high-resolution spring phenological measurements in a northern mixed forest. Agric For Meteorol 169:136–147

    Article  Google Scholar 

  • Schwartz MD, Liang L (2013) High-resolution phenological data. In: Schwartz MD (ed) Phenology: an integrative environmental science. Springer, Dordrecht, pp 351–365

    Chapter  Google Scholar 

  • Seiwa K (1999) Changes in leaf phenology are dependent on tree height in Acer mono, a deciduous broad-leaved tree. Ann Bot-London 83(4):355–361

    Article  Google Scholar 

  • Sparks TH, Menzel A (2002) Observed changes in seasons: an overview. Int J Climatol 22(14):1715–1725

    Article  Google Scholar 

  • Sperry JS, Tyree MT (1988) Mechanism of water stress-induced xylem embolism. Plant Physiol 88(3):581–587

    Article  CAS  Google Scholar 

  • Vitasse Y, Francois C, Delpierre N, Dufrene E, Kremer A, Chuine I, Delzon S (2011) Assessing the effects of climate change on the phenology of European temperate trees. Agric For Meteorol 151(7):969–980

    Article  Google Scholar 

  • Vitasse Y, Porte AJ, Kremer A, Michalet R, Delzon S (2009) Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology. Oecologia 161(1):187–198

    Article  Google Scholar 

  • Walther GR (2010) Community and ecosystem responses to recent climate change. Philos Trans R Soc B-Biol Sci 365(1549):2019–2024

    Article  Google Scholar 

  • Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416(6879):389–395

    Article  CAS  Google Scholar 

  • Wang J, Ives NE, Lechowicz MJ (1992) The relation of foliar phenology to xylem embolism in trees. Funct Ecol 6(4):469–475

    Article  Google Scholar 

  • 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 485(7399):494–497

    CAS  Google Scholar 

  • Xu L, Chen XQ (2013) Regional unified model-based leaf unfolding prediction from 1960 to 2009 across northern China. Glob Chang Biol 19(4):1275–1284

    Article  Google Scholar 

  • Zhang XY, Goldberg MD, Yu YY (2012) Prototype for monitoring and forecasting fall foliage coloration in real time from satellite data. Agric For Meteorol 158:21–29

    Article  Google Scholar 

  • Zhu KZ, Wan MW (1973) Wu hou xue. Ke xue chu ban she, Beijing

    Google Scholar 

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Acknowledgments

We wish to thank the University of Wisconsin-Milwaukee Field Station for providing background tree information in the study area; Dr. Gretchen Meyer for helping identify all sampled trees; and Dr. Jonathan Hanes, Dr. Isaac Park, and Holly Wojnicz for helping with the fieldwork. We kindly acknowledge Dr. Benjamin L. Ruddell, Dr. Gretchen Meyer, and Dr. Jonathan Hanes for their insightful comments on earlier drafts of this paper. We finally thank two anonymous reviewers for their valuable comments, which greatly improved our manuscript.

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Correspondence to Rong Yu.

Appendix

Appendix

Table 9 Correlation coefficients between canopy development/senescence and two environmental factors (accumulated growing/chilling degree-days and day length)

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Yu, R., Schwartz, M.D., Donnelly, A. et al. An observation-based progression modeling approach to spring and autumn deciduous tree phenology. Int J Biometeorol 60, 335–349 (2016). https://doi.org/10.1007/s00484-015-1031-9

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  • DOI: https://doi.org/10.1007/s00484-015-1031-9

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