International Journal of Biometeorology

, Volume 58, Issue 9, pp 1853–1864 | Cite as

Chilling and heat requirements for leaf unfolding in European beech and sessile oak populations at the southern limit of their distribution range

  • Cécile F. Dantec
  • Yann Vitasse
  • Marc Bonhomme
  • Jean-Marc Louvet
  • Antoine Kremer
  • Sylvain Delzon
Original Paper
First Online:
Received:
Revised:
Accepted:

Abstract

With global warming, an advance in spring leaf phenology has been reported worldwide. However, it is difficult to forecast phenology for a given species, due to a lack of knowledge about chilling requirements. We quantified chilling and heat requirements for leaf unfolding in two European tree species and investigated their relative contributions to phenological variations between and within populations. We used an extensive database containing information about the leaf phenology of 14 oak and 10 beech populations monitored over elevation gradients since 2005. In parallel, we studied the various bud dormancy phases, in controlled conditions, by regularly sampling low- and high-elevation populations during fall and winter. Oak was 2.3 times more sensitive to temperature for leaf unfolding over the elevation gradient and had a lower chilling requirement for dormancy release than beech. We found that chilling is currently insufficient for the full release of dormancy, for both species, at the lowest elevations in the area studied. Genetic variation in leaf unfolding timing between and within oak populations was probably due to differences in heat requirement rather than differences in chilling requirement. Our results demonstrate the importance of chilling for leaf unfolding in forest trees and indicate that the advance in leaf unfolding phenology with increasing temperature will probably be less pronounced than forecasted. This highlights the urgent need to determine experimentally the interactions between chilling and heat requirements in forest tree species, to improve our understanding and modeling of changes in phenological timing under global warming.

Keywords

Climate change Phenology Cuttings Heat/chilling requirement Leaf unfolding Sessile oak European beech 

Abbreviations

GDD

Growing degree days

Tb

Base temperature for chilling and heat accumulation

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank Marie-Laure Desprez-Loustau and Isabelle Chuine for their valuable comments on the study. We also thank Xavier Capdevielle and Yann Guengant for field assistance and Paul Fromage for assistance with computing and analysis. The research leading to these results was conducted as part of the Aquitaine “Phénologie et Stratégies Temporelles” project.

Supplementary material

484_2014_787_MOESM1_ESM.docx (47 kb)
ESM 1 (DOCX 46 kb)

References

  1. Acevedo-Rodriguez R, Vargas-Hernandez JJ, Lopez-Upton J, Mendoza JV (2006) Effect of geographic origin and nutrition on shoot phenology of Mexican Douglas-Fir (Pseudotsuga sp.) seedlings. Agrociencia 40:125–137Google Scholar
  2. Alberto F, Bouffier L, Louvet JM, Lamy JB, Delzon S, Kremer A (2011) Adaptive responses for seed and leaf phenology in natural populations of sessile oak along an altitudinal gradient. J Evol Biol 24:1442–1454CrossRefGoogle Scholar
  3. Balandier P, Gendraud M, Rageau R, Bonhomme M, Richard JP, Parisot E (1993) Bud break delay on single node cuttings and bud capacity for nucleotide accumulation as parameters for endo- and paradormancy in peach trees in a tropical climate. Sci Hortic-Amst 55:249–261CrossRefGoogle Scholar
  4. Baliuckas V, Lagerstrom T, Norell L, Erksson G (2005) Genetic variation among and within populations in Swedish species of Sorbus aucuparia L. and Prunus padus L. assessed in a nursery trial. Silvae Genet 54:1–8Google Scholar
  5. Basler D, Körner C (2012) Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agr Forest Meteorol 165:73–81CrossRefGoogle Scholar
  6. Battey NH (2000) Aspects of seasonality. J Exp Bot 51:1769–1780CrossRefGoogle Scholar
  7. Bennett JP (1949) Temperature and bud rest period. Calif Agric 4(9):12–14Google Scholar
  8. Billington HL, Pelham J (1991) Genetic-variation in the date of budburst in Scottish birch populations—implications for climate change. Funct Ecol 5:403–409CrossRefGoogle Scholar
  9. Bolte A, Czajkowski T, Kompa T (2007) The north-eastern distribution range of European beech—a review. Forestry 80:413–429CrossRefGoogle Scholar
  10. Caffarra A, Donnelly A (2011) The ecological significance of phenology in four different tree species: effects of light and temperature on bud burst. Int J Biometeorol 55:711–721CrossRefGoogle Scholar
  11. Campoy JA, Ruiz D, Egea J (2012) Temperature effect on dormancy release in apricot when applied in different dormant stages. Acta Horticult 966:155–161Google Scholar
  12. Cannell MGR (1989) Chilling, thermal time and the data of flowering of trees. In: Wright CJ (ed) Manipulation of fruiting. Butterworths, London, pp 99–113CrossRefGoogle Scholar
  13. Cannell MGR (1997) Spring phenology of trees and frost avoidance. Weather 52:46–52CrossRefGoogle Scholar
  14. Cannell MGR, Smith RI (1983) Thermal time, chill days and predictions of budburst in Picea sitchensis. J Appl Ecol 20:951–963CrossRefGoogle Scholar
  15. Cannell MGR, Smith RI (1986) Climatic warming, spring budburst and frost damage on trees. J Appl Ecol 23:177–191CrossRefGoogle Scholar
  16. Champagnat P (1989) Rest and activity in vegetative buds of trees. Ann Sci For 46:9s–26sCrossRefGoogle Scholar
  17. Charrier G, Bonhomme M, Lacointe A, Améglio T (2011) Are budburst dates, dormancy and cold acclimation in walnut trees (Juglans regia L.) under mainly genotypic or environmental control? Int J Biometeorol 55:763–774CrossRefGoogle Scholar
  18. Chmielewski FM, Rotzer T (2001) Response of tree phenology to climate change across Europe. Agr Forest Meteorol 108:101–112CrossRefGoogle Scholar
  19. Chmura DJ, Rozkowski R (2002) Variability of beech provenances in spring and autumn phenology. Silvae Genet 51:123–127Google Scholar
  20. Chuine I (2010) Why does phenology drive species distribution? Phil Trans R Soc B 365:3149–3160CrossRefGoogle Scholar
  21. Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510CrossRefGoogle Scholar
  22. Chuine I, Morin X, Bugmann H (2010) Warming, photoperiods and tree phenology. Science 329:277–278CrossRefGoogle Scholar
  23. Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728CrossRefGoogle Scholar
  24. Coville FC (1920) The influence of cold in stimulating the growth of plants. Proc Natl Acad Sci U S A 6:434–435CrossRefGoogle Scholar
  25. Čufar K, De Luis M, Saz MA, Črepinšek Z, Kajfež-Bogataj L (2012) Temporal shifts in leaf phenology of beech (Fagus sylvatica) depend on elevation. Trees 26:1091–1100CrossRefGoogle Scholar
  26. Darbyshire R, Webb L, Goodwin I, Barlow EWR (2013a) Evaluation of recent trends in Australian pome fruit spring phenology. Int J Biometeorol 57:409–421CrossRefGoogle Scholar
  27. Darbyshire R, Webb L, Goodwin I, Barlow EWR (2013b) Impact of future warming on winter chilling in Australia. Int J Biometeorol 57:355–366CrossRefGoogle Scholar
  28. Delpierre N, Soudani K, François C et al (2009) Exceptional carbon uptake in European forests during the warm spring of 2007: a data–model analysis. Glob Chang Biol 15:1455–1474CrossRefGoogle Scholar
  29. Derory J, Léger P, Garcia V et al (2006) Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol 170:723–738CrossRefGoogle Scholar
  30. Doorenbos J (1953) Review of the literature on dormancy in buds of woody plants. Medelingen Landbouwhogeschool Wageningen/Nederland 53:1–24Google Scholar
  31. Elloumi O, Ghrab M, Kessentini H, Ben Mimoun M (2013) Chilling accumulation effects on performance of pistachio trees cv. Mateur in dry and warm area climate. Sci Hortic 159:80–87CrossRefGoogle Scholar
  32. Falusi M, Calamassi R (1990) Bud dormancy in beech (Fagus sylvatica L.). Effect of chilling and photoperiod on dormancy release of beech seedlings. Tree Physiol 6:429–438CrossRefGoogle Scholar
  33. Falusi M, Calamassi R (1996) Geographic variation and bud dormancy in beech seedlings (Fagus sylvatica L). Ann Sci For 53:967–979CrossRefGoogle Scholar
  34. Faust M, Erez A, Rowland LJ, Wang SY, Norman HA (1997) Bud dormancy in perennial fruit trees: physiological basis for dormancy induction, maintenance, and release. Hortscience 32:623–629Google Scholar
  35. Fu YH, Campioli M, Deckmyn G, Janssens IA (2012a) The impact of winter and spring temperatures on temperate tree budburst dates: results from an experimental climate manipulation. PLoS One 7:e47324CrossRefGoogle Scholar
  36. Fu YH, Campioli M, Van Oijen M, Deckmyn G, Janssens IA (2012b) Bayesian comparison of six different temperature-based budburst models for four temperate tree species. Ecol Model 230:92–100CrossRefGoogle Scholar
  37. Gomory D, Paule L (2011) Trade-off between height growth and spring flushing in common beech (Fagus sylvatica L.). Ann For Sci 68:975–984CrossRefGoogle Scholar
  38. Hänninen H (1987) Effects of temperature on dormancy release in woody plants: implications of prevailing models. Silva Fenn 21:279–299CrossRefGoogle Scholar
  39. Hänninen H (1990) Modelling bud dormancy release in trees from cool and temperate regions. Acta For Fenn 213:1–47Google Scholar
  40. Harrington CA, Gould PJ, St. Clair JB (2010) Modeling the effects of winter environment on dormancy release of Douglas fir. For Ecol Manag 259:798–808CrossRefGoogle Scholar
  41. Hasenauer H, Nemani RR, Schadauer K, Running SW (1999) Forest growth response to changing climate between 1961 and 1990 in Austria. For Ecol Manag 122:209–219CrossRefGoogle Scholar
  42. Heide OM (1993) Dormancy release in beech buds (Fagus sylvatica) requires both chilling and long days. Physiol Plant 89:187–191CrossRefGoogle Scholar
  43. Honjo H (2007) Effects of global warming on dormancy and flowering behavior of temperate fruit crops in Japan. Hortic Res 6:1–5CrossRefGoogle Scholar
  44. Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540CrossRefGoogle Scholar
  45. Howe GT, Saruul P, Davis J, Chen THH (2000) Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplars. Theor Appl Genet 101:632–642CrossRefGoogle Scholar
  46. Karlsson PS, Bylund H, Neuvonen S, Heino S, Tjus M (2003) Climatic response of budburst in the mountain birch at two areas in northern Fennoscandia and possible responses to global change. Ecography 26:617–625CrossRefGoogle Scholar
  47. Kramer K (1994) Selecting a model to predict the onset of growth of Fagus sylvatica. J Appl Ecol 31:172–181CrossRefGoogle Scholar
  48. Kramer K (1995) Phenotypic plasticity of the phenology of seven European tree species in relation to climatic warming. Plant Cell Environ 18:93–104CrossRefGoogle Scholar
  49. Lang GA (1987) Dormancy—a new universal terminology. Hortscience 22:817–820Google Scholar
  50. Laube J, Sparks TH, Estrella N, Höflers J, Ankerst DP, Menzel A (2013) Chilling outweighs photoperiod in preventing precocious spring development. Glob Chang Biol. doi: 10.1111/gcb.12360 Google Scholar
  51. Legave JM, Blanke M, Christen D, Giovannini D, Mathieu V, Oger R (2013) Comprehensive overview of the spatial and temporal variability of apple bud dormancy release and blooming phenology in Western Europe. Int J Biometeorol 57:317–331CrossRefGoogle Scholar
  52. Luedeling E (2012) Climate change impacts on winter chill for temperate fruit and nut production: a review. Sci Hortic 144:218–229CrossRefGoogle Scholar
  53. Luedeling E, Gassner A (2012) Partial least squares regression for analyzing walnut phenology in California. Agric For Meteorol 158:43–52CrossRefGoogle Scholar
  54. Luedeling E, Guo L, Dai J, Leslie C, Blanke MM (2013) Differential responses of trees to temperature variation during the chilling and forcing phases. Agric For Meteorol 181:33–42CrossRefGoogle Scholar
  55. Mauget JC, Germain E (1980) Dormance et précocité de débourrement des bourgeons chez quelques cultivars de Noyer (Juglans regia L.). CR Acad Sci Paris Ser D 290:135–138Google Scholar
  56. Meier U (2001) Growth stages of mono- and dicotyledonous plants, BBCH monograph, 2nd edn. Federal Biological Research Centre for Agriculture and Forestry, BrunswickGoogle Scholar
  57. Menzel A, Sparks TH, Estrella N et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976CrossRefGoogle Scholar
  58. Morin X, Lechowicz MJ, Augspurger C, O’ Keefe J, Viner D, Chuine I (2009) Leaf phenology in 22 North American tree species during the 21st century. Glob Chang Biol 15:961–975CrossRefGoogle Scholar
  59. Morin X, Roy J, Sonié L, Chuine I (2010) Changes in leaf phenology of three European oak species in response to experimental climate change. New Phytol 186:900–910CrossRefGoogle Scholar
  60. Murray MB, Cannell MGR, Smith RI (1989) Date of budburst of fifteen tree species in Britain following climatic warming. J Appl Ecol 26:693–700CrossRefGoogle Scholar
  61. Myking T, Heide OM (1995) Dormancy release and chilling requirement of buds of latitudinal ecotypes of Betula pendula and B. pubescens. Tree Physiol 15:697–704CrossRefGoogle Scholar
  62. Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR (1997) Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386:698–702CrossRefGoogle Scholar
  63. Nienstaedt H (1966) Dormancy and dormancy release in white spruce. For Sci 12:374–384Google Scholar
  64. Nooden EA, Weber DP (1978) Environmental and hormonal control of dormancy in terminal buds of plants. In: Clutter M (ed) Dormancy and developmental arrest. Academic, New York, pp 221–268CrossRefGoogle Scholar
  65. Penuelas J, Filella I, Comas P (2002) Changed plant and animal life cycles from 1952 to 2000 in the Mediterranean region. Glob Chang Biol 8:531–544CrossRefGoogle Scholar
  66. Perry TO, Wu WC (1960) Genetic variation in the winter chilling requirement for date of dormancy break for Acer rubrum. Ecology 41:790–794CrossRefGoogle Scholar
  67. Phillimore AB, Proios K, O’Mahony N, Bernard R, Lord AM, Atkinson S, Smithers RJ (2013) Inferring local processes from macro-scale phenological pattern: a comparison of two methods. J Ecol 101:774–783CrossRefGoogle Scholar
  68. Polgar CA, Primack RB (2011) Leaf-out phenology of temperate woody plants: from trees to ecosystems. New Phytol 191:926–941CrossRefGoogle Scholar
  69. Pouget R (1963) Recherches physiologiques sur le repos végétatif de la vigne (Vitis vinifera L.): la dormance des bourgeons et le mécanisme de sa disparition. Ann Amélior Plantes 13:1–247Google Scholar
  70. Rageau (1978) Croissance et débourrement des bourgeons végétatifs de pêcher (Prunus persica L. Batsch) au cours d’un test classique de dormance. CR Acad Sci Paris Ser D 287:1119–1122Google Scholar
  71. Richardson AD, Bailey AS, Denny EG, Martin CW, O’Keefe J (2006) Phenology of a northern hardwood forest canopy. Glob Chang Biol 12:1174–1188CrossRefGoogle Scholar
  72. 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. Agr Forest Meteorol 169:156–173CrossRefGoogle Scholar
  73. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweigk C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60CrossRefGoogle Scholar
  74. Rousi M, Pusenius J (2005) Variations in phenology and growth of European white birch (Betula pendula) clones. Tree Physiol 25:201–210CrossRefGoogle Scholar
  75. Ruiz D, Campoy JA, Egea J (2007) Chilling and heat requirements of apricot cultivars for flowering. Environ Exp Bot 61:254–263CrossRefGoogle Scholar
  76. Samish RM (1954) Dormancy in woody plants. Annu Rev Plant Physiol 5:183–204CrossRefGoogle Scholar
  77. Sanz-Perez V, Castro-Diez P, Valladares F (2009) Differential and interactive effects of temperature and photoperiod on budburst and carbon reserves in two co-occurring Mediterranean oaks. Plant Biol 11:142–151CrossRefGoogle Scholar
  78. Sarvas R (1972) Investigations on annual cycle of development of forest trees. Active period. Commun Inst For Fenn 76:1–110Google Scholar
  79. Sarvas R (1974) Investigations on the annual cycle of development of forest trees. II. Autumn dormancy and winter dormancy. Commun Inst For Fenn 84:1–101Google Scholar
  80. Schieber B, Janik R, Snopkova Z (2013) Phenology of common beech (Fagus sylvatica L.) along the altitudinal gradient in Slovak Republic (Inner Western Carpathians). J For Sci 59:176–184Google Scholar
  81. Sherman WB, Soule J, Andrews CP (1977) Distribution of Florida peaches and nectarines in the tropics and subtropics. Fruit Var J 31:75–78Google Scholar
  82. Shirazi AM (2003) Standardizing methods for evaluating the chilling requirements to break dormancy in seeds and buds (including geophytes): introduction to the workshop. Spec Insert HortScience 38(3)Google Scholar
  83. Vitasse Y, Basler D (2013) What role for photoperiod in the bud burst phenology of European beech. Eur J For Res 132:1–8CrossRefGoogle Scholar
  84. Vitasse Y, Basler D (2014) Is the use of cuttings a good proxy to explore phenological responses of temperate forests in warming and photoperiod experiments? Tree Physiol (in press)Google Scholar
  85. Vitasse Y, Delzon S, Bresson CC, Michalet R, Kremer A (2009a) Altitudinal differentiation in growth and phenology among populations of temperate-zone tree species growing in a common garden. Can J For Res 39:1259–1269CrossRefGoogle Scholar
  86. Vitasse Y, Delzon S, Dufrêne E, Pontailler JY, Louvet JM, Kremer A, Michalet R (2009b) Leaf phenology sensitivity to temperature in European trees: do within-species populations exhibit similar responses? Agr Forest Meteorol 149:735–744CrossRefGoogle Scholar
  87. Vitasse Y, Bresson CC, Kremer A, Michalet R, Delzon S (2010) Quantifying phenological plasticity to temperature in two temperate tree species. Funct Ecol 24:1211–1218CrossRefGoogle Scholar
  88. Vitasse Y, François C, Delpierre N, Dufrêne E, Kremer A, Chuine I, Delzon S (2011) Assessing the effects of climate change on the phenology of European temperate trees. Agr Forest Meteorol 151:969–980CrossRefGoogle Scholar
  89. Vitasse Y, Hoch G, Randin CF, Lenz A, Kollas C, Scheepens JF, Körner C (2013) Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171:663–678CrossRefGoogle Scholar
  90. vonWuehlisch G, Krusche D, Muhs HJ (1995) Variation in temperature sum requirement for flushing of beech provenances. Silvae Genet 44:343–346Google Scholar
  91. Wareing PF (1953) Growth studies in woody species. V. Photoperiodism in dormant buds of Fagus sylvatica L. Physiol Planta 6:692–706CrossRefGoogle Scholar
  92. White MA, Running SW, Thornton PE (1999) The impact of growing-season length variability on carbon assimilation and evapotranspiration over 88 years in the eastern US deciduous forest. Int J Biometeorol 42:139–145CrossRefGoogle Scholar
  93. Zhou L, Tucker CJ, Kaufmann RK, Slayback D, Shabanov NV, Myneni RB (2001) Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J Geophys Res 106:20069–20083Google Scholar

Copyright information

© ISB 2014

Authors and Affiliations

  • Cécile F. Dantec
    • 1
    • 2
  • Yann Vitasse
    • 3
  • Marc Bonhomme
    • 4
    • 5
  • Jean-Marc Louvet
    • 1
    • 2
  • Antoine Kremer
    • 1
    • 2
  • Sylvain Delzon
    • 1
    • 2
  1. 1.INRA, UMR 1202 BIOGECOCestasFrance
  2. 2.Université de Bordeaux, UMR 1202 BIOGECOCestasFrance
  3. 3.Institute of BotanyUniversity of BaselBaselSwitzerland
  4. 4.INRA, UMRA547 PIAFClermont-FerrandFrance
  5. 5.Clermont Université, Université Blaise Pascal, UMRA547 PIAFClermont-FerrandFrance

Personalised recommendations