Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models

Annals of Forest Science

Volumn 73, Issue 1, 2016, Pages 5-25

  Delpierre, Nicolas ^a   Vitasse, Yann ^b,c,d   Chuine, Isabelle ^e   Guillemot, Joannès ^a   Bazot, Stéphane ^a   Rutishauser, This ^f   Rathgeber, Cyrille B K ^g  

^a UNIVERSITÉ PARIS SUD   (France)

^b UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^c SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^d WSL INSTITUTE FOR SNOW AND AVALANCHE RESEARCH SLF   (Switzerland)

^e CNRS   (France)

^f UNIVERSITY OF BERN   (Switzerland)

^g LERFoB   (France)

Author keywords

Autumn senescence; Budburst; Cambium; Dormancy; Fine roots; Models

Indexed keywords

AUTUMN; BOREAL FOREST; BUDBURST; CLIMATE EFFECT; DORMANCY; ECOSYSTEM MODELING; ENVIRONMENTAL CUE; FINE ROOT; PHENOLOGY; SENESCENCE; TEMPERATE FOREST; TERRESTRIAL ECOSYSTEM;

EID: 84958794046     PISSN: 12864560     EISSN: 1297966X     Source Type: Journal    
DOI: 10.1007/s13595-015-0477-6     Document Type: Review

References (236)

1. Abramoff RZ, Finzi AC (2014) Are above- and below-ground phenology in sync? New Phytol. doi:10.1111/nph.13111
2. Alberto FJ, Aitken SN, Alía R et al (2013) Potential for evolutionary responses to climate change—evidence from tree populations. Glob Chang Biol 19:1645–1661. doi:10.1111/gcb.12181
3. Aloni R (2013) The role of hormones in controlling vascular differentiation. In: Fromm J (ed) Cell. Asp. Wood Form. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 99–139
4. Alvarez-Uria P, Körner C (2007) Low temperature limits of root growth in deciduous and evergreen temperate tree species. Funct Ecol 21:211–218. doi:10.1111/j.1365-2435.2007.01231.x
5. Aono Y, Kazui K (2008) Phenological data series of cherry tree flowering in Kyoto, Japan, and its application to reconstruction of springtime temperatures since the 9th century. 914:905–914. doi: 10.1002/joc
6. 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:e57373. doi:10.1371/journal.pone.0057373
7. Arora R, Rowland LJ, Tanino K (2003) Induction and release of bud dormancy in woody perennials: a science comes of age. HortScience 38(5):911–921
8. Arora VK, Boer GJ (2005) A parameterization of leaf phenology for the terrestrial ecosystem component of climate models. Glob Chang Biol 11:39–59. doi:10.1111/j.1365-2486.2004.00890.x
9. Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525. doi:10.1093/treephys/23.8.517
10. Badeck F-W, Bondeau A, Bottcher K et al (2004) Responses of spring phenology to climate change. New Phytol 162:295–309. doi:10.1111/j.1469-8137.2004.01059.x
11. Barbaroux C, Bréda N (2002) Contrasting distribution and seasonal dynamics of carbohydrate reserves in stem wood of adult ring-porous sessile oak and diffuse-porous beech trees. Tree Physiol 22(17):1201–1210
12. Barbaroux C, Breda N, Dufrene E (2003) Distribution of above-ground and below-ground carbohydrate reserves in adult trees of two contrasting broad-leaved species (Quercus petraea and Fagus sylvatica). New Phytol 157:605–615. doi:10.1046/j.1469-8137.2003.00681.x
13. Barr AG, Black TA, Hogg EH et al (2004) Inter-annual variability in the leaf area index of a boreal aspen-hazelnut forest in relation to net ecosystem production. Agric For Meteorol 126:237–255. doi:10.1016/j.agrformet.2004.06.011
14. Basler D, Körner C (2014) Photoperiod and temperature responses of bud swelling and bud burst in four temperate forest tree species. Tree Physiol 34:377–388
15. Bazot S, Barthes L, Blanot D, Fresneau C (2013) Distribution of non-structural nitrogen and carbohydrate compounds in mature oak trees in a temperate forest at four key phenological stages. Trees 27:1023–1034. doi:10.1007/s00468-013-0853-5
16. Begum S, Nakaba S, Oribe Y et al (2007) Induction of cambial reactivation by localized heating in a deciduous hardwood hybrid poplar (Populus sieboldii × P. grandidentata). Ann Bot 100:439–447. doi:10.1093/aob/mcm130
17. Begum S, Nakaba S, Oribe Y et al (2010) Cambial sensitivity to rising temperatures by natural condition and artificial heating from late winter to early spring in the evergreen conifer Cryptomeria japonica. Trees 24:43–52. doi:10.1007/s00468-009-0377-1
18. Begum S, Nakaba S, Yamagishi Y et al (2013) Regulation of cambial activity in relation to environmental conditions: understanding the role of temperature in wood formation of trees. Physiol Plant 147:46–54. doi:10.1111/j.1399-3054.2012.01663.x
19. Begum S, Shibagaki M, Furusawa O et al (2012) Cold stability of microtubules in wood-forming tissues of conifers during seasons of active and dormant cambium. Planta 235:165–179. doi:10.1007/s00425-011-1500-2
20. Bergh J, McMurtrie RE, Linder S (1998) Climatic factors controlling the productivity of Norway spruce: a model-based analysis. For Ecol Manag 110:127–139. doi:10.1016/S0378-1127(98)00280-1
21. Burke M, Raynal D (1994) Fine root growth phenology, production, and turnover in a northern hardwood forest ecosystem. Plant Soil 162:135–146
22. Caffarra A, Donnelly A, Chuine I (2011a) Modelling the timing of Betula pubescens budburst. II. Integrating complex effects of photoperiod into process-based models. Clim Res 46:159–170. doi:10.3354/cr00983
23. Caffarra A, Donnelly A, Chuine I, Jones MB (2011b) Modelling the timing of Betula pubescens budburst. I. Temperature and photoperiod: a conceptual model. Clim Res 46:147–157. doi:10.3354/cr00980
24. Campbell R, Sugano A (1975) Phenology of bud burst in Douglas-fir related to provenance, photoperiod, chilling, and flushing temperature. Bot Gaz 290–298
25. Chaffey N (2013) Secondary growth of tree roots: cytoskeletal perspectives. In: Eshel A, Beeckman T (eds) Roots hidden half. Boca Raton, p 831
26. 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 55:763–774. doi:10.1007/s00484-011-0470-1
27. Chuine I (2010) Why does phenology drive species distribution? Philos Trans R Soc Lond B Biol Sci 365:3149–3160. doi:10.1098/rstb.2010.0142
28. Chuine I, Beaubien EG (2001) Phenology is a major determinant of tree species range. Ecol Lett 4:500–510. doi:10.1046/j.1461-0248.2001.00261.x
29. Chuine I, Cour P, Rousseau DD (1998) Fitting models predicting dates of flowering of temperate-zone trees using simulated annealing. Plant Cell Environ 21:455–466. doi:10.1046/j.1365-3040.1998.00299.x
30. Chuine I, Garcia de Cortazar-atauri I, Kramer K, Hänninen H (2013) Plant development models. In: Schwartz MD (ed) Phenol. an Integr. Environ. Sci., 2nd edn. Springer, Dordrecht, pp 275–293
31. Chuine I, Morin X, Bugmann H (2010) Warming, photoperiods, and tree phenology. Science 329:277–278, 80-
32. Chuine I, Yiou P, Viovy N et al (2004) Historical phenology: grape ripening as a past climate indicator. Nature 432:289–290. doi:10.1038/432289a
33. Clark JS, Salk C, Melillo J, Mohan J (2014) Tree phenology responses to winter chilling, spring warming, at north and south range limits. Funct Ecol. doi:10.1111/1365-2435.12309
34. Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol 6:393–407. doi:10.1093/treephys/6.4.393
35. Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728. doi:10.1111/j.1365-3040.2012.02552.x
36. Coville FV (1920) The influence of cold in stimulating the growth of plants. Proc Natl Acad Sci U S A 434–435. doi: 10.1175/1520-0493(1920)48<643b:TIOCIS>2.0.CO;2
37. Čufar K, Prislan P, de Luis M, Gričar J (2008) Tree-ring variation, wood formation and phenology of beech (Fagus sylvatica) from a representative site in Slovenia, SE Central Europe. Trees 22:749–758. doi:10.1007/s00468-008-0235-6
38. Cuny HE, Rathgeber CBK, Lebourgeois F et al (2012) Life strategies in intra-annual dynamics of wood formation: example of three conifer species in a temperate forest in north-east France. Tree Physiol 32:612–625. doi:10.1093/treephys/tps039
39. Dahl Å, Langvall O (2008) Observations of phenology in Sweden—past and present. In: Nekovar J, Koch E, Kubin E, et al. (eds) Hist. Curr. status plant Phenol. Eur. COST Office, Brussels, pp 161–165
40. Damesin C, Lelarge C (2003) Carbon isotope composition of current-year shoots from Fagus sylvatica in relation to growth, respiration and use of reserves. Plant Cell Environ 26:207–219. doi:10.1046/j.1365-3040.2003.00951.x
41. Dantec CF, Vitasse Y, Bonhomme M et al (2014) Chilling and heat requirements for leaf unfolding in European beech and sessile oak populations at the southern limit of their distribution range. Int J Biometeorol 58:1853–1864. doi:10.1007/s00484-014-0787-7
42. David A (2011) Modélisation de la croissance ligneuse chez le Hêtre et le Chêne sessile. Master's thesis dissertation. Université Paris-Sud. 43 pp
43. De Barba D, Rossi S, Deslauriers A, Morin H (2015) Effects of soil warming on nitrogen foliar applications on bud burst of black spruce. Trees. doi:10.1007/s00468-015-1152-0
44. Deckmyn G, Evans SP, Randle TJ (2006) Refined pipe theory for mechanistic modeling of wood development. Tree Physiol 26:703–717. doi:10.1093/treephys/26.6.703
45. Deckmyn G, Verbeeck H, Op de Beeck M et al (2008) ANAFORE: a stand-scale process-based forest model that includes wood tissue development and labile carbon storage in trees. Ecol Model 215:345–368. doi:10.1016/j.ecolmodel.2008.04.007
46. Delaporte A (2010) Le carbone assimilé par les feuilles de Charme (Carpinus betulus L.) est-il alloué aux réserves en début de saison de végétation? Master's thesis dissertation. Université Paris-Sud. 37 pp
47. Deleuze C, Houllier F (1998) A simple process-based xylem growth model for describing wood microdensitometric profiles. J Theor Biol 193:99–113
48. Delpierre N, Dufrêne E, Soudani K et al (2009a) Modelling interannual and spatial variability of leaf senescence for three deciduous tree species in France. Agric For Meteorol 149:938–948. doi:10.1016/j.agrformet.2008.11.014
49. Delpierre N, Soudani K, François C et al (2009b) Exceptional carbon uptake in European forests during the warm spring of 2007: a data-model analysis. Glob Chang Biol 15:1455–1474. doi:10.1111/j.1365-2486.2008.01835.x
50. Delpierre N, Soudani K, François C et al (2012) Quantifying the influence of climate and biological drivers on the interannual variability of carbon exchanges in European forests through process-based modelling. Agric For Meteorol 154–155:99–112. doi:10.1016/j.agrformet.2011.10.010
51. Demarée GR, Rutishauser T (2011) From “Periodical Observations” to “Anthochronology” and “Phenology”—the scientific debate between Adolphe Quetelet and Charles Morren on the origin of the word “Phenology”. Int J Biometeorol 55:753–761. doi:10.1007/s00484-011-0442-5
52. Denne M, Dodd R (1981) The environmental control of xylem differentiation. In: Barnett JR (ed) Xylem cell Dev. Castle House Publications, Tunbridge Wells, pp 236–255
53. Dietze MC, Sala A, Carbone MS et al (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687. doi:10.1146/annurev-arplant-050213-040054
54. Donnelly A, Caffarra A, O’Neill BF (2011) A review of climate-driven mismatches between interdependent phenophases in terrestrial and aquatic ecosystems. Int J Biometeorol 55:805–817. doi:10.1007/s00484-011-0426-5
55. Dougherty PM, Whitehead D, Vose JM (1994) Environmental influences on the phenology of pine. Ecol Bull 43:64–75
56. Dufour B, Morin H (2010) Tracheid production phenology of Picea mariana and its relationship with climatic fluctuations and bud development using multivariate analysis. Tree Physiol 30:853–865. doi:10.1093/treephys/tpq046
57. Dufrêne E, Davi H, François C et al (2005) Modelling carbon and water cycles in a beech forest. Ecol Model 185:407–436. doi:10.1016/j.ecolmodel.2005.01.004
58. Dünisch O, Bauch J (1994) Influence of soil substrate and drought on wood formation of spruce (Picea abies Karst.) under controlled conditions. Holzforschung-Int J Biol Chem Phys Technol Wood 48:447–457
59. Eissenstat DM, McCormack ML, Du Q (2013) Global change and root lifespan. In: Eshel A, Beeckman T (eds) Roots Hidden Half. CRC Press, Boca Raton, p 831
60. El Zein R, Maillard P, Bréda N et al (2011) Seasonal changes of C and N non-structural compounds in the stem sapwood of adult sessile oak and beech trees. Tree Physiol 31:843–854. doi:10.1093/treephys/tpr074
61. Estiarte M, Peñuelas J (2014) Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob Chang Biol. doi:10.1111/gcb.12804
62. Estrella N, Menzel A (2006) Responses of leaf colouring in four deciduous tree species to climate and weather in Germany. Clim Res 32:253–267
63. Fatichi S, Leuzinger S, Körner C (2014) Moving beyond photosynthesis: from carbon source to sink-driven vegetation modeling. New Phytol 201:1086–1095. doi:10.1111/nph.12614
64. Fischer C, Höll W (1991) Food reserves of Scots pine (Pinus sylvestris L.) I. Seasonal changes in the carbohydrate and fat reserves of pine needles. Trees 5:187–195
65. Fischer C, Höll W (1992) Food reserves of scots pine (Pinus sylvestris L.) II. Seasonal changes and radial distribution of carbohydrate and fat reserves in pine wood. Trees 6:147–155
66. Fonti P, Solomonoff N, García-González I (2007) Earlywood vessels of Castanea sativa record temperature before their formation. New Phytol 173:562–570
67. Frankenstein C, Eckstein D, Schmitt U (2005) The onset of cambium activity—a matter of agreement? Dendrochronologia 23:57–62. doi:10.1016/j.dendro.2005.07.007
68. Fu YSH, Campioli M, Vitasse Y et al (2014) Variation in leaf flushing date influences autumnal senescence and next year’s flushing date in two temperate tree species. Proc Natl Acad Sci U S A 111:7355–7360. doi:10.1073/pnas.1321727111
69. Fujii S (1993) Studies on acorn production and seed predation in Quercus serrata—growth, falling phenology, estimation of production, and insect seed predators. Bull Osaka Mus Nat Hist 47:1–17
70. Garcia de Cortazar-Atauri I, Brisson N, Ollat N et al (2009) Asynchronous dynamics of grapevine (Vitis vinifera) maturation: experimental study for a modeling approach. J Int des Sci la Vigne du Vin 43:83–97
71. Gaul D, Hertel D, Borken W et al (2008) Effects of experimental drought on the fine root system of mature Norway spruce. For Ecol Manag 256:1151–1159. doi:10.1016/j.foreco.2008.06.016
72. Geßler A, Kreuzwieser J, Dopatka T, Rennenberg H (2002) Diurnal courses of ammonium net uptake by the roots of adult beech (Fagus sylvatica) and spruce (Picea abies) trees. Plant Soil 240:23–32. doi:10.1023/A:1015831304911
73. Gilson A, Barthes L, Delpierre N et al (2014) Seasonal changes in carbon and nitrogen compound concentrations in a Quercus petraea chronosequence. Tree Physiol 34:716–729. doi:10.1093/treephys/tpu060
74. Gomez L, Faurobert M (2002) Contribution of vegetative storage proteins to seasonal nitrogen variations in the young shoots of peach trees (Prunus persica L. Batsch). J Exp Bot 53:2431–2439. doi:10.1093/jxb/erf098
75. González-González BD, García-González I, Vázquez-Ruiz RA (2013) Comparative cambial dynamics and phenology of Quercus robur L. and Q. pyrenaica Willd. in an Atlantic forest of the northwestern Iberian Peninsula. Trees 27:1571–1585. doi:10.1007/s00468-013-0905-x
76. Goulden ML, Munger JW, Fan S et al (1996) Exchange of carbon dioxide by a deciduous forest: response to interannual climate variability. Science 271:576–578
77. Greer DH, Wünsche JN, Norling CL, Wiggins HN (2005) Root-zone temperatures affect phenology of bud break, flower cluster development, shoot extension growth and gas exchange of “Braeburn” (Malus domestica) apple trees. Tree Physiol 26:105–111
78. Gričar J (2010) Xylem and phloem formation in Sessile Oak from Slovenia in 2007. Wood Res 55:15–22
79. Gričar J, Čufar K (2008) Seasonal dynamics of phloem and xylem formation in silver fir and Norway spruce as affected by drought. Russ J Plant Physiol 55:538–543. doi:10.1134/S102144370804016X
80. Gričar J, Zupančič M, Čufar K, Oven P (2007) Regular cambial activity and xylem and phloem formation in locally heated and cooled stem portions of Norway spruce. Wood Sci Technol 41:463–475. doi:10.1007/s00226-006-0109-2
81. Gruber A, Pirkebner D, Florian C, Oberhuber W (2012) No evidence for depletion of carbohydrate pools in Scots pine (Pinus sylvestris L.) under drought stress. Plant Biol 14:142–148. doi:10.1111/j.1438-8677.2011.00467.x
82. Gruber A, Strobl S, Veit B, Oberhuber W (2010) Impact of drought on the temporal dynamics of wood formation in Pinus sylvestris. Tree Physiol 30:490–501. doi:10.1093/treephys/tpq003
83. Guillemot J, Martin-StPaul NK, Dufrêne E et al (2015) The dynamic of annual carbon allocation to wood in European forests is consistent with a combined source-sink limitation of growth: implications for modelling. Biogeosci Discuss 12:2213–2255. doi:10.5194/bgd-12-2213-2015
84. Guo D, Xia M, Wei X et al (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683. doi:10.1111/j.1469-8137.2008.02573.x
85. Gyllenstrand N, Clapham D, Källman T, Lagercrantz U (2007) A Norway spruce FLOWERING LOCUS T homolog is implicated in control of growth rhythm in conifers. Plant Physiol 144:248–257. doi:10.1104/pp. 107.095802
86. Hanes JM, Richardson AD, Klosterman S (2013) Mesic temperate deciduous forest phenology. In: Schwartz MD (ed) Phenol. an Integr. Environ. Sci., 2nd edn. Springer, Dordrecht, p 610
87. Hänninen H (1990) Modelling bud dormancy release in trees from cool and temperate regions. Acta For Fenn 213:3–47
88. Hänninen H, Kramer K (2007) A framework for modelling the annual cycle of trees in boreal and temperate. Silva Fenn 41:167–205
89. Hänninen H, Tanino K (2011) Tree seasonality in a warming climate. Trends Plant Sci 16:412–416. doi:10.1016/j.tplants.2011.05.001
90. Harrington CA, Gould PJ, St.Clair JB (2010) Modeling the effects of winter environment on dormancy release of Douglas-fir. For Ecol Manag 259:798–808. doi:10.1016/j.foreco.2009.06.018
91. Hartmann H, Ziegler W, Trumbore S (2013) Lethal drought leads to reduction in nonstructural carbohydrates in Norway spruce tree roots but not in the canopy. Funct Ecol 27:413–427. doi:10.1111/1365-2435.12046
92. Heide O (1993) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540
93. Heide OM (2011) Temperature rather than photoperiod controls growth cessation and dormancy in Sorbus species. J Exp Bot 62:5397–5404. doi:10.1093/jxb/err213
94. Hendrick RL, Pregitzer KS (1992) The demography of fine roots in a northern hardwood forest. Ecology 73:1094–1104
95. Hmimina G, Dufrêne E, Pontailler J-Y et al (2013) Evaluation of the potential of MODIS satellite data to predict vegetation phenology in different biomes: an investigation using ground-based NDVI measurements. Remote Sens Environ 132:145–158. doi:10.1016/j.rse.2013.01.010
96. Hoch G (2005) Fruit-bearing branchlets are carbon autonomous in mature broad-leaved temperate forest trees. Plant Cell Environ 28:651–659. doi:10.1111/j.1365-3040.2004.01311.x
97. Hoch G (2015) Carbon reserves as indicators for carbon limitation in trees. In Progress in Botany (pp. 321–346). Springer International Publishing
98. Hoch G, Richter A, Körner C (2003) Non-structural carbon compounds in temperate forest trees. Plant Cell Environ 26:1067–1081
99. Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540. doi:10.1016/j.tplants.2003.09.013
100. Huang J-G, Deslauriers A, Rossi S (2014) Xylem formation can be modeled statistically as a function of primary growth and cambium activity. New Phytol 203:831–841. doi:10.1111/nph.12859
101. Hwang T, Band LE, Miniat CF et al (2014) Divergent phenological response to hydroclimate variability in forested mountain watersheds. Glob Chang Biol 20:2580–2595. doi:10.1111/gcb.12556
102. Jalkanen R, Aalto T, Kurkela T (1995) Development of needle retention in Scots pine (Pinus sylvestris) in 1957–1991 in northern and southern Finland. Trees 10(2):125–133
103. Jolly WM, Nemani R, Running SW (2004) Enhancement of understory productivity by asynchronous phenology with overstory competitors in a temperate deciduous forest. Tree Physiol 24:1069–1071. doi:10.1093/treephys/24.9.1069
104. Jolly WM, Nemani R, Running SW (2005) A generalized, bioclimatic index to predict foliar phenology in response to climate. Glob Chang Biol 11:619–632. doi:10.1111/j.1365-2486.2005.00930.x
105. Joslin JD, Wolfe MH (1998) Impacts of water input manipulations on fine root production and mortality in a mature hardwood forest. Plant Soil 204(2):165–174
106. Joslin JD, Wolfe MH, Hanson PJ (2001) Factors controlling the timing of root elongation intensity in a mature upland oak stand. Plant Soil 228:201–212
107. Kalliokoski T, Mäkinen H, Jyske T et al (2013) Effects of nutrient optimization on intra-annual wood formation in Norway spruce. Tree Physiol 33:1145–1155. doi:10.1093/treephys/tpt078
108. 2 exchange. Glob Chang Biol 18:1971–1987. doi:10.1111/j.1365-2486.2012.02678.x
109. Keenan TF, Darby B, Felts E et al (2014) Tracking forest phenology and seasonal physiology using digital repeat photography: a critical assessment. Ecol Appl 24:1478–1489. doi:10.1890/13-0652.1
110. Keenan TF, Richardson AD (2015) The timing of autumn senescence is affected by the time of spring phenology: implications for predictive models. Glob Chang Biol. doi:10.1111/gcb.12890
111. Kikuzawa K (1991) A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. Am Nat 138:1250–1263
112. Kikuzawa K (1995) Leaf phenology as an optimal strategy for carbon gain in plants. Can J Bot 73:158–163
113. Kikuzawa K (1996) Geographical distribution of leaf life span and species diversity of trees simulated by a leaf-longevity model. Vegetatio 122:61–67
114. King JS, Albaugh TJ, Allen HL et al (2002) Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154:389–398. doi:10.1046/j.1469-8137.2002.00393.x
115. Klein T, Hoch G, Yakir D, Körner C (2014) Drought stress, growth and nonstructural carbohydrate dynamics of pine trees in a semi-arid forest. Tree Physiol 34:981–992. doi:10.1093/treephys/tpu071
116. Koch E (2008) History of international phenology networks. In: Nekovar J, Koch E, Kubin E, et al. (eds) Hist. Curr. status plant Phenol. Eur. COST Office, Brussels, pp 12–16
117. Konôpka B, Yuste JC, Janssens IA, Ceulemans R (2005) Comparison of fine root dynamics in Scots pine and Pedunculate oak in sandy soil. Plant Soil 276:33–45. doi:10.1007/s11104-004-2976-3
118. Koppel A, Troeng E, Linder S (1987) Respiration and photosynthesis in cones of Norway spruce (Picea abies (L.) Karst.). Trees 1:123–128
119. Körner C, Basler D (2010) Phenology under global warming. Science 327:1461–1462, 80-
120. Kramer K (1995) Modelling comparison to evaluate the importance of phenology for the effects of climate change on growth of temperate-zone deciduous trees. Clim Res 5:119–130
121. Kramer K, Leinonen I, Loustau D (2000) The importance of phenology for the evaluation of impact of climate change on growth of boreal, temperate and Mediterranean forests ecosystems: an overview. Int J Biometeorol 44:67–75. doi:10.1007/s004840000066
122. Krinner G, Viovy N, de Noblet-Ducoudré N, et al. (2005) A dynamic global vegetation model for studies of the coupled atmosphere‐biosphere system. Global Biogeochem Cycles 19:GB 1015. doi: 10.1029/2003GB002199
123. Kuhns MR, Garrett HE, Teskey RO, Hinckley TM (1985) Root growth of black walnut trees related to soil temperature, soil water potential, and leaf water potential. For Sci 31:617–629
124. Lachaud S, Bonnemain J-L (1981) Xylogenèse chez les Dicotylédones arborescentes. I. Modalités de la remise en activite du cambium et de la xylogenèse chez les Hêtres et les Chênes Agés. Can J Bot 59:1222–1230
125. Lachaud S, Catesson A-M, Bonnemain J-L (1999) Structure and functions of the vascular cambium. Comptes Rendus l’Académie des Sci III-Sciences la Vie 322:633–650
126. Lang GA, Eearly JD, Martin GC, Darnell RL (1987) Endo-, para-, and ecodormancy: physiological terminology and classification for dormancy research. HortSci 22:371–377
127. Laube J, Sparks TH, Estrella N et al (2014) Chilling outweighs photoperiod in preventing precocious spring development. Glob Chang Biol 20:170–182. doi:10.1111/gcb.12360
128. Lebourgeois F, Pierrat J-C, Perez V et al (2010) Simulating phenological shifts in French temperate forests under two climatic change scenarios and four driving global circulation models. Int J Biometeorol 54:563–581. doi:10.1007/s00484-010-0305-5
129. Leuschner C, Backes K, Hertel D et al (2001) Drought responses at leaf, stem and fine root levels of competitive Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. trees in dry and. For Ecol Manag 149:33–46
130. Levins R (1966) The strategy of model building in population biology. Am Sci 54:421–431
131. Linder S, Troeng E (1981) The seasonal course of respiration and photosynthesis in strobuli of Scots pine (Pinus sylvestris L.). For Sci 27:267–276
132. Linkosalo T, Häkkinen R, Hänninen H (2006) Models of the spring phenology of boreal and temperate trees: is there something missing? Tree Physiol 26:1165–1172
133. Linkosalo T, Häkkinen R, Terhivuo J et al (2009) The time series of flowering and leaf bud burst of boreal trees (1846–2005) support the direct temperature observations of climatic warming. Agric For Meteorol 149:453–461. doi:10.1016/j.agrformet.2008.09.006
134. Little CHA, Bonga JM (1974) Rest in the cambium of Abies balsamea. Can J Bot 52:1723–1730
135. Lupi C, Morin H, Deslauriers A, Rossi S (2010) Xylem phenology and wood production: resolving the chicken-or-egg dilemma. Plant Cell Environ 33:1721–1730. doi:10.1111/j.1365-3040.2010.02176.x
136. Lyr H, Hoffmann G (1967) Growth rates and growth periodicity of tree roots. Int Rev For Res 2:181–236
137. McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235
138. Medvigy D, Wofsy SC, Munger JW et al (2009) Mechanistic scaling of ecosystem function and dynamics in space and time: Ecosystem Demography model version 2. J Geophys Res 114:G01002. doi:10.1029/2008JG000812
139. Mellerowicz EJ, Coleman WK, Riding RT, Little CHA (1992) Periodicity of cambial activity in Abies balsamea. 1. Effects of temperature and photoperiod on cambial dormancy and frost hardiness. Physiol Plant 85:515–525
140. Menzel A (2013) Phenological data, networks and research: Europe. In: Schwartz MD (ed) Phenol. an Integr. Environ. Sci., 2nd edn. Springer, Dordrecht, p 610
141. Menzel A, Sparks TH, Estrella N et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976. doi:10.1111/j.1365-2486.2006.01193.x
142. Meunier C, Sirois L, Bégin Y (2007) Climate and Picea mariana seed maturation relationships: a multi-scale perspective. Ecol Monogr 77:361–376. doi:10.1890/06-1543.1
143. Michelot A, Simard S, Rathgeber C et al (2012) Comparing the intra-annual wood formation of three European species (Fagus sylvatica, Quercus petraea and Pinus sylvestris) as related to leaf phenology and non-structural carbohydrate dynamics. Tree Physiol 32:1033–1045. doi:10.1093/treephys/tps052
144. Migliavacca M, Sonnentag O, Keenan TF et al (2012) On the uncertainty of phenological responses to climate change, and implications for a terrestrial biosphere model. Biogeosciences 9:2063–2083. doi:10.5194/bg-9-2063-2012
145. Millard P, Grelet G-A (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095. doi:10.1093/treephys/tpq042
146. Millard P, Proe MF (1992) Storage and internal cycling of nitrogen in relation to seasonal growth of Sitka spruce. Tree Physiol 10:33–43. doi:10.1093/treephys/10.1.33
147. Millard P, Sommerkorn M, Grelet G-A (2007) Environmental change and carbon limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New Phytol 175:11–28. doi:10.1111/j.1469-8137.2007.02079.x
148. Misson L, Degueldre D, Collin C et al (2011) Phenological responses to extreme droughts in a Mediterranean forest. Glob Chang Biol 17:1036–1048. doi:10.1111/j.1365-2486.2010.02348.x
149. Moser L, Fonti P, Büntgen U et al (2010) Timing and duration of European larch growing season along altitudinal gradients in the Swiss Alps. Tree Physiol 30:225–233. doi:10.1093/treephys/tpp108
150. Mutke S, Gordo J, Climent J, Gil L (2003) Shoot growth and phenology modelling of grafted Stone pine (Pinus pinea L.) in Inner Spain. Ann For Sci 60:527–537. doi:10.1051/forest
151. Myking T, Heide O (1995) Dormancy release and chilling requirement of buds of latitudinal ecotypes of Betula pendula and B. pubescens. Tree Physiol 15:697–704
152. Noguchi K, Sakata T, Mizoguchi T, Takahashi M (2005) Estimating the production and mortality of fine roots in a Japanese cedar (Cryptomeria japonica D. Don) plantation using a minirhizotron technique. J For Res 10:435–441. doi:10.1007/s10310-005-0163-x
153. Nord E, Lynch JP (2009) Plant phenology: a critical controller of soil resource acquisition. J Exp Bot 60:1927–1937. doi:10.1093/jxb/erp018
154. Oladi R, Pourtahmasi K, Eckstein D, Bräuning A (2010) Seasonal dynamics of wood formation in Oriental beech (Fagus orientalis Lipsky) along an altitudinal gradient in the Hyrcanian forest, Iran. Trees 25:425–433. doi:10.1007/s00468-010-0517-7
155. Oribe Y, Funada R, Kubo T (2003) Relationships between cambial activity, cell differentiation and the localization of starch in storage tissues around the cambium in locally heated stems of Abies sachalinensis (Schmidt) Masters. Trees 17:185–192. doi:10.1007/s00468-002-0231-1
156. Oribe Y, Kubo T (1997) Effect of heat on cambial reactivation during winter dormancy in evergreen and deciduous conifers. Tree Physiol 17:81–87. doi:10.1093/treephys/17.2.81
157. Palacio S, Hoch G, Sala A et al (2014) Does carbon storage limit tree growth? New Phytol 201:1096–1100
158. Pallardy SG (2008) Physiology of woody plants, 3rd edn. 469 pp
159. Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127:1513–1523. doi:10.1104/pp. 010816.1
160. Pregitzer K (2002) Fine roots of trees—a new perspective. New Phytol 154:267–270
161. Pregitzer K, King J, Burton A, Brown S (2000) Responses of tree fine roots to temperature. New Phytol 147:107–115
162. Prislan P, Gričar J, de Luis M et al (2013) Phenological variation in xylem and phloem formation in Fagus sylvatica from two contrasting sites. Agric For Meteorol 180:142–151. doi:10.1016/j.agrformet.2013.06.001
163. Puhe J (2003) Growth and development of the root system of Norway spruce (Picea abies) in forest stands: a review. For Ecol Manag 175:253–273
164. Quan X, Wang C, Zhang Q et al (2010) Dynamics of fine roots in five Chinese temperate forests. J Plant Res 123:497–507. doi:10.1007/s10265-010-0322-9
165. Rathgeber CBK, Longuetaud F, Mothe F et al (2011a) Phenology of wood formation: data processing, analysis and visualisation using R (package CAVIAR). Dendrochronologia 29:139–149. doi:10.1016/j.dendro.2011.01.004
166. Rathgeber CBK, Rossi S, Bontemps J-D (2011b) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438. doi:10.1093/aob/mcr168
167. Réaumur R-A (1735) Observations du thermomètre faites à Paris pendant l’année 1735, comparées avec celles qui ont été faites sous la ligne, à l'Isle de France, à Alger et quelques unes de nos iles de l'Amérique. Mémoires l’Académie R des Sci 545–576
168. Richardson AD, Anderson RS, Arain MA et al (2012) Terrestrial biosphere models need better representation of vegetation phenology: results from the North American Carbon Program Site Synthesis. Glob Chang Biol 18:566–584. doi:10.1111/j.1365-2486.2011.02562.x
169. Richardson AD, Keenan TF, Migliavacca M et al (2013) Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric For Meteorol 169:156–173. doi:10.1016/j.agrformet.2012.09.012
170. Rinne PLH, Kaikuranta PM, Van Der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J 26:249–264. doi:10.1046/j.1365-313X.2001.01022.x
171. Rohde A, Bastien C, Boerjan W (2011) Temperature signals contribute to the timing of photoperiodic growth cessation and bud set in poplar. Tree Physiol 31:472–482. doi:10.1093/treephys/tpr038
172. Rossi S, Anfodillo T, Cufar K et al (2013) A meta-analysis of cambium phenology and growth: linear and non-linear patterns in conifers of the northern hemisphere. Ann Bot 112:1911–1920. doi:10.1093/aob/mct243
173. Rossi S, Deslauriers A, Anfodillo T et al (2006) Conifers in cold environments synchronize maximum growth rate of tree-ring formation with day length. New Phytol 170:301–310
174. Rossi S, Deslauriers A, Griçar J et al (2008) Critical temperatures for xylogenesis in conifers of cold climates. Glob Ecol Biogeogr 17:696–707. doi:10.1111/j.1466-8238.2008.00417.x
175. Rossi S, Morin H, Deslauriers A (2012) Causes and correlations in cambium phenology: towards an integrated framework of xylogenesis. J Exp Bot 63:2117–2126. doi:10.1093/jxb/err423
176. Rossi S, Morin H, Deslauriers A, Plourde P-Y (2011) Predicting xylem phenology in black spruce under climate warming. Glob Chang Biol 17:614–625. doi:10.1111/j.1365-2486.2010.02191.x
177. Rossi S, Rathgeber CBK, Deslauriers A (2009) Comparing needle and shoot phenology with xylem development on three conifer species in Italy. Ann For Sci 66:1–8
178. Rötzer T, Chmielewski F-M (2001) Phenological maps of Europe. Clim Res 18:249–257
179. Rötzer T, Grote R, Pretzsch H (2004) The timing of bud burst and its effect on tree growth. Int J Biometeorol 48:109–118. doi:10.1007/s00484-003-0191-1
180. Saffell BJ, Meinzer FC, Woodruff DR et al (2014) Seasonal carbohydrate dynamics and growth in Douglas-fir trees experiencing chronic, fungal-mediated reduction in functional leaf area. Tree Physiol 34:218–228. doi:10.1093/treephys/tpu002
181. Salifu KF, Timmer VR (2003) Optimizing nitrogen loading of Picea mariana seedlings during nursery culture. Can J For Res 33:1287–1294
182. Salminen H, Jalkanen R (2007) Intra-annual height increment of Pinus sylvestris at high latitudes in Finland. Tree Physiol 27:1347–1353
183. Sanz-Pérez V, Castro-Díez P (2010) Summer water stress and shade alter bud size and budburst date in three Mediterranean Quercus species. Trees 24:89–97
184. Sarvas R (1974) Investigations on the annual cycle of development of forest trees. II. Autumn dormancy and winter dormancy. Commun Inst For Fenn 84:101
185. Sarvas R (1972) Investigations on the annual cycle of development of forest trees. 1. Active period. Commun Inst For Fenn 76:110
186. Sass-Klaassen U, Sabajo CR, den Ouden J (2011) Vessel formation in relation to leaf phenology in pedunculate oak and European ash. Dendrochronologia 29:171–175. doi:10.1016/j.dendro.2011.01.002
187. Schaber J, Badeck FW (2005) Plant phenology in Germany over the 20th century. Reg Environ Chang 5:37–46. doi:10.1007/s10113-004-0094-7
188. Schenker G, Lenz A, Körner C, Hoch G (2014) Physiological minimum temperatures for root growth in seven common European broad-leaved tree species. Tree Physiol 34:302–313. doi:10.1093/treephys/tpu003
189. Schiestl-Aalto P, Kulmala L, Harri M (2015) CASSIA—a dynamic model for predicting intra-annual sink demand and interannual growth variation in Scots pine. New Phytol. doi:10.1111/nph.13275
190. Schrader J, Baba K, May ST et al (2003) Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci U S A 100:10096–10101. doi:10.1073/pnas.1633693100
191. Sedgley M, Griffin A (1989) Sexual reproduction of tree crops. 392 pp
192. Seo J-W, Eckstein D, Jalkanen R et al (2008) Estimating the onset of cambial activity in Scots pine in northern Finland by means of the heat-sum approach. Tree Physiol 28:105–112. doi:10.1093/treephys/28.1.105
193. Sharp WM, Spargue VG (1967) Flowering and fruiting in the white oaks. Pistillate flowering, acorn development, weather and yields. Ecology 243–251
194. Shishkova S, Rost TL, Dubrovsky JG (2008) Determinate root growth and meristem maintenance in angiosperms. Ann Bot 101:319–340. doi:10.1093/aob/mcm251
195. Smart BYCM (1994) Gene expression during leaf senescence. New Phytol 126:419–448
196. Sparks T, Carey P (1995) The responses of species to climate over two centuries: an analysis of the Marsham phenological record, 1736–1947. J Ecol 83:321–329
197. Srivastava L (2002) Plant growth and development: hormones and environment. 772
198. Staswick PE (1994) Storage proteins of vegetative plant tissues. Annu Rev Plant Physiol Plant Mol Biol 45:303–322
199. Sudachkova NE, Milyutina IL, Romanova LI, Semenova GP (2004) The annual dynamics of reserve compounds and hydrolitic enzymes activity in the tissues of Pinus sylvestris L. and Larix sibirica Ledeb.—the metabolism of reserve compounds in the tissues of Siberian conifers. Eur J For Res 7:1–10
200. Suzuki M, Yoda K, Suzuki H (1996) Phenological comparison of the onset of vessel formation between ring-porous and diffuse-porous deciduous trees in a Japanese temperate forest. IAWA J 17:431–444
201. Takahashi K, Koike S (2014) Altitudinal differences in bud burst and onset and cessation of cambial activity of four subalpine tree species. Landsc Ecol Eng 10:349–354. doi:10.1007/s11355-014-0250-2
202. Takahashi S, Okada N, Nobuchi T (2013) Relationship between the timing of vessel formation and leaf phenology in ten ring-porous and diffuse-porous deciduous tree species. Ecol Res 28:615–624. doi:10.1007/s11284-013-1053-x
203. Tanino KK, Kalcsits L, Silim S et al (2010) Temperature-driven plasticity in growth cessation and dormancy development in deciduous woody plants: a working hypothesis suggesting how molecular and cellular function is affected by temperature during dormancy induction. Plant Mol Biol 73:49–65. doi:10.1007/s11103-010-9610-y
204. Teskey R, Hinckley T (1981) Influence of temperature and water potential on root growth of white oak. Physiol Plant 52:363–369
205. Thibeault-Martel M, Krause C, Morin H, Rossi S (2008) Cambial activity and intra-annual xylem formation in roots and stems of Abies balsamea and Picea mariana. Ann Bot 102:667–674. doi:10.1093/aob/mcn146
206. Tikkanen O-P, Julkunen-Tiitto R (2003) Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata. Oecologia 136:244–251. doi:10.1007/s00442-003-1267-7
207. Tooke F, Battey NH (2010) Temperate flowering phenology. J Exp Bot 61:2853–2862. doi:10.1093/jxb/erq165
208. Ursino DJ, Nelson CD, Krotkov G (1968) Seasonal changes in the distribution of photo-assimilated 14C in young pine plants. Plant Physiol 43:845–852
209. Vaganov EA, Hughes MK, Shashkin AV (2006) Modeling external influence on xylem development. Ecol Stud 183:189–243
210. Valenzuela Nuñez LM, Gérant D, Maillard P et al (2011) Evidence for a 26kDa vegetative storage protein in the stem sapwood of mature pedunculate oak. Interciencia 36:142–147
211. Valenzuela Nuñez LM, Gérant D, Maillard P, Bréda N (2010) Seasonal dynamics of total soluble proteins in adult trees of Quercus petraea (Matt.) Liebl. and Fagus sylvatica L. Rev Mex Ciencias For 1:75–83
212. Visser ME, Holleman LJ (2001) Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc Biol Sci 268:289–294. doi:10.1098/rspb.2000.1363
213. Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172. doi:10.1007/s00442-005-0299-6
214. Vitasse Y (2013) Ontogenic changes rather than difference in temperature cause understory trees to leaf out earlier. New Phytol 198:149–155. doi:10.1111/nph.12130
215. Vitasse Y, Basler D (2013) What role for photoperiod in the bud burst phenology of European beech. Eur J For Res 132:1–8. doi:10.1007/s10342-012-0661-2
216. 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 34:174–183. doi:10.1093/treephys/tpt116
217. Vitasse Y, François C, Delpierre N et al (2011) Assessing the effects of climate change on the phenology of European temperate trees. Agric For Meteorol 151:969–980. doi:10.1016/j.agrformet.2011.03.003
218. Vitasse Y, Hoch G, Randin CF et al (2013) Elevational adaptation and plasticity in seedling phenology of temperate deciduous tree species. Oecologia 171:663–678. doi:10.1007/s00442-012-2580-9
219. Vitasse Y, Porté AJ, Kremer A et al (2009) Responses of canopy duration to temperature changes in four temperate tree species: relative contributions of spring and autumn leaf phenology. Oecologia 161:187–198. doi:10.1007/s00442-009-1363-4
220. Wang S, Grant R, Verseghy D, Black T (2001) Modelling plant carbon and nitrogen dynamics of a boreal aspen forest in CLASS—the Canadian Land Surface Scheme. Ecol Model 142:135–154. doi:10.1016/S0304-3800(01)00284-8
221. Wang YP, Law RM, Pak B (2010) A global model of carbon, nitrogen and phosphorus cycles for the terrestrial biosphere. Biogeosciences 7:2261–2282. doi:10.5194/bg-7-2261-2010
222. Wareing PF, Saunders PF (1971) Hormones and dormancy. Annu Rev Plant Physiol 22:261–288. doi:10.1146/annurev.pp. 22.060171.001401
223. Way DA (2011) Tree phenology responses to warming: spring forward, fall back? Tree Physiol 31:469–471. doi:10.1093/treephys/tpr044
224. Way D, Montgomery R (2014) Photoperiod constraints on tree phenology, performance and migration in a warming world. Plant Cell Environ 1–48. doi: 10.1111/pce.12431
225. Weinberger JH (1950) Chilling requirements of peach varieties. Proc Am Soc Hortic Sci 56:122–128
226. 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 42:139–145. doi:10.1007/s004840050097
227. White MA, Thornton PE, Running SW (1997) A continental responses phenology model climatic for monitoring variability vegetation to interannual. Glob Biogeochem Cycles 11:217–234
228. Wiley E, Huepenbecker S, Casper BB, Helliker BR (2013) The effects of defoliation on carbon allocation: can carbon limitation reduce growth in favour of storage? Tree Physiol 33:1216–1228. doi:10.1093/treephys/tpt093
229. Wilson B (1984) The growing tree. 138 pp
230. Wilson B, Wodzicki T, Zahner R (1966) Notes: differentiation of cambial derivatives: proposed terminology. For Sci 12:438–440
231. Wilson KB, Baldocchi DD (2000) Seasonal and interannual variability of energy fluxes over a broadleaved temperate deciduous forest in North America. Agric For Meteorol 100:1–18. doi:10.1016/S0168-1923(99)00088-X
232. Yang X, Mustard JF, Tang J, Xu H (2012) Regional-scale phenology modeling based on meteorological records and remote sensing observations. J Geophys Res 117:G03029. doi:10.1029/2012JG001977
233. Yin X, Kropff MJ, McLaren G, Visperas RM (1995) A nonlinear model for crop development as a function of temperature. Agric For Meteorol 77:1–6
234. Yoshie F, Sakai A (1982) Freezing resistance of temperate deciduous forest plants in relation to their life form and microhabitat. In: Li PH, Sakai A (eds) Plant cold hardiness. Freez. Stress - Mech. Crop Implic. Academic Press, New York, p 686
235. Zaehle S, Friend A (2010) Carbon and nitrogen cycle dynamics in the O-CN land surface model: 1. Model description, site-scale evaluation, and sensitivity to parameter estimates. Glob Biogeochem Cycles. doi:10.1029/2009GB003522
236. Zeeman SC, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401:13–28. doi:10.1042/BJ20061393