Skip to main content
Log in

European larch phenology in the Alps: can we grasp the role of ecological factors by combining field observations and inverse modelling?

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript


Vegetation phenology is strongly influenced by climatic factors. Climate changes may cause phenological variations, especially in the Alps which are considered to be extremely vulnerable to global warming. The main goal of our study is to analyze European larch (Larix decidua Mill.) phenology in alpine environments and the role of the ecological factors involved, using an integrated approach based on accurate field observations and modelling techniques. We present 2 years of field-collected larch phenological data, obtained following a specifically designed observation protocol. We observed that both spring and autumn larch phenology is strongly influenced by altitude. We propose an approach for the optimization of a spring warming model (SW) and the growing season index model (GSI) consisting of a model inversion technique, based on simulated look-up tables (LUTs), that provides robust parameter estimates. The optimized models showed excellent agreement between modelled and observed data: the SW model predicts the beginning of the growing season (BGS) with a mean RMSE of 4 days, while GSI gives a prediction of the growing season length (LGS) with a RMSE of 5 days. Moreover, we showed that the original GSI parameters led to consistent errors, while the optimized ones significantly increased model accuracy. Finally, we used GSI to investigate interactions of ecological factors during springtime development and autumn senescence. We found that temperature is the most effective factor during spring recovery while photoperiod plays an important role during autumn senescence: photoperiod shows a contrasting effect with altitude decreasing its influence with increasing altitude.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others






  • Badeck FW, Bondeau A, Böttcher K, Doktor D, Lucht W, Schaber J, Sitch S (2004) Responses of spring phenology to climate change. New Phytologist 162:295–309

    Article  Google Scholar 

  • Baldocchi DD, Black TA, Curtis PS, Falge E, Fuentes JD, Granier A, Gu L, Knohl A, Pilegaard K, Schmid HP, Valentini R, Wilson K, Wofsy S, Xu L, Yamamoto S (2005) Predicting the onset of net carbon uptake by deciduous forests with soil temperature and climate data: a synthesis of FLUXNET data. Int J Biometeorol 49:377−387

    Article  PubMed  Google Scholar 

  • Baret F, Knyazikhin Y, Weiss M, Pragnère A, Myneni RB (1999). Overview of retrieval techniques for LAI and fAPAR. Proceedings of ALPS99 Workshop, Meribel, France

  • Beaubien EG, Freeland HJ (2000) Spring phenology trends in Alberta, Canada: links to ocean temperature. Int J Biometeorol 44:53−59

    Article  PubMed  CAS  Google Scholar 

  • Campbell GS, Norman LM (1998) Environmental biophysics. Springer, New York, p 286

    Google Scholar 

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

    Article  Google Scholar 

  • 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 82:399–415

    Article  Google Scholar 

  • Chen X, Tan Z, Schwartz MD, Xu C (2004) Determining the growing season of land vegetation on the basis of plant phenology and satellite data in Northern China. Int J Biometeorol 44:97–101

    Article  Google Scholar 

  • Chmielewski FM, Rötzer T (2001) Response of tree phenology to climate change across Europe. Agric For Meteorol 108:101–112

    Article  Google Scholar 

  • Chmielewski FM, Rötzer T (2002) Annual and spatial variability of the beginning of growing season in Europe in relation to air temperature changes. Climate Res 19:257–264

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chuine I, Cour P (1999) Climatic determinants of budburst seasonality in four temperate-zone tree species. New Phytol 143:339–349

    Article  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 21:455–466

    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 22:1–13

    Article  Google Scholar 

  • Chuine I, Yiou P, Viovy N, Seguin B, Daux V, Le Roy Ladurie E (2004) Grape ripening as a past climate indicator. Nature 432:289–290

    Article  PubMed  CAS  Google Scholar 

  • Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman and Hall, New York

    Google Scholar 

  • Fitter AH, Hay RK (2002) Environmental physiology of plants. Academic, London

  • Fitzjarrald DR, Acevedo OC, Moore KE (2001) Climatic consequences of leaf presence in the eastern United States. J Climate 14:598–614

    Article  Google Scholar 

  • Fu P, Rich PM (1999) Design and implementation of the solar analyst: an arcview extension for modelling solar radiation at landscape scales. Proceedings of the 19th Annual ESRI User Conference, San Diego, USA

  • Hadley JL (2000) Effect of daily minimum temperature on photosynthesis in eastern hemlock (Tsuga canadensis L.) in autumn and winter. Arct Antarct Alpine Res 32:368–374

    Article  Google Scholar 

  • Häkkinen R, Linkosalo T, Hari P (1998) Effects of dormancy and environmental factors on timing of bud burst in Betula pendula. Tree Physiol 18:707–712

    PubMed  Google Scholar 

  • Hänninen H (1991) Does climate warming increase the risk of frost damage in northern trees? Plant Cell Environ 14:449–454

    Article  Google Scholar 

  • Hari P, Häkkinen R (1991) The utilisation of old phenological time series of bud burst to compare models describing annual cycles of plants. Tree Physiol 8:281–287

    PubMed  Google Scholar 

  • Heide OM (1993) Daylength and thermal time responses of budburst during dormancy release in some northern deciduous trees. Physiol Plant 88:531–540

    Article  Google Scholar 

  • Heide OM (2003) High autumn temperature delays spring bud burst in boreal trees, counterbalancing the effect of climatic warming. Tree Physiol 23:931–936

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Janssen PHM, Heuberger PSC (1995) Calibration of process oriented models. Ecol Modell 83:55–66

    Article  Google Scholar 

  • Jolly WM, Nemani RR, Running SW (2005) A generalized, bioclimatic index to predict foliar phenology in response to climate. Glob Chang Biol 11:619–632

    Article  Google Scholar 

  • Keller F, Körner C (2003) The role of photoperiodism in alpine plant development. Arct Antarct Alpine Res 35:361–368

    Article  Google Scholar 

  • Kimes DS, Knyazikhin Y, Privette JL, Abuelgasim AA, Gao F (2000) Inversion of physically-based models. Remote Sens Rev 18:381–439

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Academic, New York

    Google Scholar 

  • Lieth H (1974) Phenology and seasonality modelling. Springer, Heidelberg

    Google Scholar 

  • Linderholm HW (2006) Growing season changes in the last century. Agric For Meteorol 137:1–14

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Loague K, Green RE (1991) Statistical and graphical methods for evaluating solute transport models: overview and application. J Contam Hydrol 7:51–73

    Article  CAS  Google Scholar 

  • Menzel A (2000) Trends in phenological phases in Europe between 1951 and 1996. Int J Biometeorol 44:76–81

    Article  PubMed  CAS  Google Scholar 

  • Menzel A, Fabian P (1999) Growing season extended in Europe. Nature 397:659

    Article  CAS  Google Scholar 

  • Mercalli L, Castellano L, Cat Berro D, Di Napoli G, Montuschi S, Mortara G, Ratti M, Guindani N (2003) Atlante Climatico della Valle d'Aosta. Ed. SMS, Torino, p 406, Italy

  • Meroni M, Colombo R, Panigada C (2004) Inversion of a radiative transfer model with hyperspectral observations for LAI mapping in poplar plantations. Remote Sens Environ 92(2):195–206

    Article  Google Scholar 

  • Monteith JL, Unsworth MH (1990) Principles of environmental physics. Arnold, New York

  • Myking T (1997) Effects of constant and fluctuating temperature on time to budburst in Betula pubescens and its relation to bud respiration. Trees 12:107–112

    Google Scholar 

  • Norby RJ, Hartz-Rubin JS, Verbrugge MJ (2003) Phenological responses in maple to experimental atmospheric warming and CO2 enrichment. Glob Chang Biol 9:1792–1801

    Article  Google Scholar 

  • Öquist G (1983) Effect of low temperature on photosynthesis. Plant Cell Environ 6:281–300

    Google Scholar 

  • Ozenda P (1985) La végétation de la chaine alpine dans l'espace montagnard européen. Masson, France

  • Paci M (1997) Ecologia Forestale. Edagricole, Italy

  • Partanen J, Koski V, Hänninen H (1998) Effects of photoperiod and temperature on the timing of bud burst in Norway spruce (Picea abies). Tree Physiol 18:811–816

    PubMed  Google Scholar 

  • Partanen J, Leinonen I, Repo T (2001) Effect of accumulated duration of the light period on bud burst in Norway spruce (Picea abies) of varying ages. Silva Fenn 35:111–117

    Google Scholar 

  • 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 161:837–846

    Article  Google Scholar 

  • Picard G, Quegan S, Delbart N, Lomas MR, Le Toan T, Woodward FI (2005) Bud-burst modelling in Siberia and its impact on quantifying the carbon budget. Glob Chang Biol 11:2164–2176

    Article  Google Scholar 

  • Pignatti S (1998) I boschi d'Italia. UTET, Torino

    Google Scholar 

  • Reichstein M, Tenhunen JD, Roupsard O, Ourcival JM, Rambal S, Miglietta F, Peressotti A, Pecchiari M, Tirone G, Valentini R (2002) Severe drought effects on ecosystem CO2 and H2O fluxes at three Mediterranean evergreen sites: revision of current hypotheses? Glob Change Biol 8:999–1017

    Article  Google Scholar 

  • Reichstein M, Tenhunen JD, Roupsard O, Ourcival JM, Rambal S, Miglietta F, Peressotti A, Pecchiari M, Tirone G, Valentini R (2003) Inverse modelling of seasonal drought effects on canopy CO2/H2O exchange in three Mediterranean ecosystems. J Geophys Res-Atmospheres 108 art-4726

  • Reichstein M, Falge E, Baldocchi D, Papale D, Aubinet M, Berbigier P, Bernhofer C, Buchmann N, Gilmanov T, Granier A, Grunwald T, Havrankova K, Ilvesniemi H, Janous D, Knohl A, Laurila T, Lohila A, Loustau D, Matteucci G, Meyers T, Miglietta F, Ourcival JM, Pumpanen J, Rambal S, Rotenberg E, Sanz M, Tenhunen J, Seufert G, Vaccari F, Vesala T, Yakir D, Valentini R (2005) On the separation of net ecosystem exchange into assimilation and ecosystem respiration: review and improved algorithm. Glob Change Biol 11:1424–1439

    Article  Google Scholar 

  • Repo T, Leinonen I, Ryyppo A, Finér L (2004) The effect of soil temperature on the bud phenology, chlorophyll fluorescence, carbohydrate content and cold hardiness of Norway spruce seedlings. Physiol Plant 121:93–100

    Article  PubMed  CAS  Google Scholar 

  • Rich PM, Dubayah R, Hetrick WA, Saving SC (1994) Using viewshed models to calculate intercepted solar radiation: applications in ecology. American Society for Photogrammetry and Remote Sensing Technical Papers, pp 524–529

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

    Article  Google Scholar 

  • Rolland C, Petitcolas V, Michalet R (2004) Changes in radial tree growth for Picea abies, Larix decidua, Pinus cembra and Pinus uncinata near the alpine timberline since 1750. Trees Struct Funct 13:40–53

    Google Scholar 

  • Rosenthal SI, Camm EL (1997) Photosynthetic decline and pigment loss during autumn foliar senescence in western larch (Larix occidentalis). Tree Physiol 17:767–775

    PubMed  Google Scholar 

  • Rötzer T, Chmielewski FM (2001) Phenological maps of Europe. Clim Res 18:249–257

    Article  Google Scholar 

  • Rötzer T, Wittenzeller M, Haeckel H, Nekovar J (2000) Phenology in central Europe-differences and trends of spring phenophases in urban and rural areas. Int J Biometeorol 44:60–66

    Article  Google Scholar 

  • Schaber J, Badeck FW (2002) Evaluation of methods for the combination of phenological time series and outlier detection. Tree Physiol 22:973–982

    PubMed  Google Scholar 

  • Schaber J, Badeck FW (2003) Physiology-based phenology models for forest tree species in Germany. Int J Biometeorol 47:193–201

    Article  PubMed  Google Scholar 

  • Schwartz MD, Reiter BE (2000) Changes in North American spring. Int J Climatol 20:929–932

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Strasburger E (1995) Trattato di Botanica-parte generale. XXXIII Edizione. Delfino, Romey

  • Studer S, Appenzeller C, Defila C (2005) Inter-annual variability and decadal trends in alpine spring phenology: a multivariate analysis approach. Clim Change 73:395–414

    Article  Google Scholar 

  • Suni T, Berninger F, Vesala T, Markkanen T, Hari P, Makela A, Ilvesniemi H, Hanninen H, Nikinmaa E, Huttula T, Laurila T, Aurela M, Grelle A, Lindroth A, Arneth A, Shibistova O, Lloyd J (2003) Air temperature triggers the recovery of evergreen boreal forest photosynthesis in spring. Glob Chang Biol 9:1410–1426

    Article  Google Scholar 

  • Tarantola A (2005) Inverse problem theory and methods for model parameter estimation. SIAM, Philadelphia

    Google Scholar 

  • Thornton PE, Running SW, White MA (1997) Generating surfaces of daily meteorological variables over large regions of complex terrain. J Hydrol 190:214–251

    Article  Google Scholar 

  • Van Wijk MT, Williams M, Laundre JA, Shaver GR (2003) Interannual variability of plant phenology in tussock tundra: modelling interactions of plant productivity, plant phenology, snowmelt and soil thaw. Glob Change Biol 9:743–758

    Article  Google Scholar 

  • Weiss M, Baret F, Myneni RB, Pragnere A, Knyazikhin Y (2000) Investigation of a model inversion technique to estimate canopy biophysical variables from spectral and directional reflectance data. Agronomie 20:3−22

    Article  Google Scholar 

  • White MA, Brunsell NA, Schwartz MD (2003) Vegetation phenology in global change studies. In: Schwartz MD (ed) Phenology: an integrative environmental science. Kluwer, Dordrecht, pp 453−466

    Google Scholar 

  • Worrall J (1993) Temperature effects on bud burst and leaf fall in subalpine larch. J Sustainable For 1:1−18

    Google Scholar 

  • Worrall J (1999) Phenology and the changing seasons. Nature 399:101

    Article  CAS  Google Scholar 

  • Wu Z, Skjelvag AO, Baadshaug OH (2004) Quantification of photoperiodic effects on growth of phleum pratense. Ann Bot 94:535−543

    Article  PubMed  Google Scholar 

Download references


This research was supported by the ARPA Valle d'Aosta REPHLEX (Remote Sensing of Phenology Larix Experiment) project. We thank L. Mercalli (SMI) for his suggestions and for providing meteorological data. We further thank A. Mammoliti Mochet and L. Cerise (ARPA VdA) M. Tardivo, E. Matta (UNIMIB) M. Brunod (UNITO) R. Accorsini and SSK group for their support in field surveys. Finally, we thank G. Agnesod (ARPA VdA) and M. Reichstein for fruitful discussions. We are also grateful to anonymous reviewers for their helpful and constructive comments.

Author information

Authors and Affiliations


Corresponding author

Correspondence to M. Migliavacca.



Symbols and abbreviations


Autumn phase


Automatic weather station


Beginning of growing season (day)


Coefficient of residual mass


Degree days (°C-day)


Day of the year

DOY0 :

Starting date for counting, set to 1 January

DOYbb :

Day of year of budburst


Modelling efficiency


End of growing season (day)


Critical forcing units (°C-day)


Growing season index


Daily indicator of the relative constraint of foliar development


Daily indicator of photoperiod

iTMin :

Daily indicator of minimum temperature


Daily indicator of vapour pressure deficit


Length of growing season (day)


Look-up table


Mean absolute error


Modelled data


Observed data

Photoi :

Daily photoperiod (h)

PhotoMax :

Upper minimum photoperiod threshold (h)

PhotoMin :

Lower minimum photoperiod threshold (h)

q :

Number of extraction from LUT


Vector of parameters

θ opt :

Optimized parameters vector

θ opt,q :

Optimized parameters vector from the q LUT extractions


Root mean square error


Springtime phase


Spring warming

Tair :

Daily mean air temperature (°C)

Tb :

Base air temperature (°C)

thresh :

Threshold for the definition of BGS and EGS in the GSI model

TMin :

Daily minimum air temperature (°C)

TMMax :

Upper minimum temperature threshold (°C)

TMMin :

Lower minimum temperature threshold (°C)


Vapour pressure deficit (Pa)

VPDi :

Daily vapour pressure deficit [Pa]

VPDMax :

Upper VPD threshold (Pa)

VPDMin :

Lower VPD threshold (Pa)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Migliavacca, M., Cremonese, E., Colombo, R. et al. European larch phenology in the Alps: can we grasp the role of ecological factors by combining field observations and inverse modelling?. Int J Biometeorol 52, 587–605 (2008).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: