Skip to main content

Advertisement

Log in

Current and future conifer seed production in the Alps: testing weather factors as cues behind masting

  • Original Paper
  • Published:
European Journal of Forest Research Aims and scope Submit manuscript

Abstract

Temporal patterns of masting in conifer species are intriguing phenomena that have cascading effects on different trophic levels in ecosystems. Many studies suggest that meteorological cues (changes in temperature and precipitation) affect variation in seed-crop size over years. We monitored cone crops of six conifer species in the Italian Alps (1999–2013) and analysed which seasonal weather factors affected annual variation in cone production at forest community level. Larch, Norway spruce and silver fir showed masting while temporal patterns in Pinus sp. were less pronounced. We found limited support for the temperature difference model proposed by Kelly et al. Both seasonal (mainly spring and summer) temperatures and precipitations of 1 and 2 years prior to seed maturation affected cone-crop size, with no significant effect of previous year’s cone crop. Next, we estimated future forest cone production until 2100, applying climate projection (using RCP 8.5 scenario) to the weather model that best predicted variation in measured cone crops. We found no evidence of long-term changes in average cone production over the twenty-first century, despite increase in average temperature and decrease in precipitation. The amplitude of predicted annual fluctuations in cone production varies over time, depending on study area. The opposite signs of temperature effects 1 and 2 years prior to seed set show that temperature differences are indeed a relevant cue. Hence, predicted patterns of masting followed by 1 or more years of poor-medium cone production suggest a high degree of resilience of alpine conifer forests under global warming scenario.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen CD, Macalady AK, Chenchouni H et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecol Manag 259:660–684

    Article  Google Scholar 

  • Archibald DW, McAdam AG, Boutin S, Fletcher QE, Humphries MM (2012) Within-season synchrony of a masting conifer enhances seed escape. Am Nat 179(4):536–544

    Article  PubMed  Google Scholar 

  • ARPA Lombardia (2014) www.arpalombardia.it. Accessed 15 Dec 2015

  • Barton K (2015) MuMIn: multi-model inference. R package version 1.13.4. http://CRAN.R-project.org/package=MuMIn. Accessed 15 Dec 2015

  • Bates D, Maechler M, Bolker B, Walker S (2014) _lme4: Linear mixed-effects models using Eigen and S4_. R package version 1.1-7. http://CRAN.R-project.org/package=lme4. Accessed 15 Dec 2015

  • Boutin S, Wauters LA, McAdam AG, Humphries MM, Tosi G, Dhondt AA (2006) Anticipatory reproduction and population growth in seed predators. Science 314:1928–1930

    Article  CAS  PubMed  Google Scholar 

  • Broome A, Hendry S, Peace A (2007) Annual and spatial variation in coning shown by the Forest Condition Monitoring programme data for Norway spruce, Sitka spruce and Scots pine in Britain. Forestry 80:17–28

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Callahan HS, Del Fierro K, Patterson AE, Zafar H (2008) Impacts of elevated nitrogen inputs on oak reproductive and seed ecology. Glob Change Biol 14(2):285–293

    Article  Google Scholar 

  • Casalegno S, Amatulli G, Camia A, Nelson A, Pekkarinen A (2010) Vulnerability of Pinus cembra L. in the Alps and the Carpathian mountains under present and future climates. Forest Ecol Manag 259:750–761

    Article  Google Scholar 

  • Cavanaugh JE (1997) Unifying the derivations of the Akaike and corrected Akaike information criteria. Stat Probab Lett 31:201–208

    Article  Google Scholar 

  • Centro Funzionale Regionale Regione Autonoma Valle d’Aosta (2014) Assessorato opere pubbliche, difesa del suolo e edilizia residenziale pubblica - Dipartimento programmazione, difesa del suolo e risorse idriche (Department of public works, soil conservation and public housing, Department planning, soil conservation and water resources). meteo@regione.vda.it

  • Crone EE, Rapp JM (2014) Resource depletion, pollen coupling, and the ecology of mast seeding. Ann N Y Acad Sci 1322(1):21–34

    Article  CAS  PubMed  Google Scholar 

  • Crone EE, Mcintire EJ, Brodie J (2011) What defines mast seeding? Spatio-temporal patterns of cone production by whitebark pine. J Ecol 99:438–444

    Google Scholar 

  • Cutini A, Chianucci F, Chirichella R, Donaggio E, Mattioli L, Apollonio M (2013) Mast seeding in deciduous forests of the northern Apennines (Italy) and its influence on wild boar population dynamics. Ann Forest Sci 70:493–502

    Article  Google Scholar 

  • Dixon A, Haffield JP (2013) Seed availability and timing of breeding of Common Crossbills Loxia curvirostra at Sitka Spruce Picea sitchensis dominated forestry plantations. Ardea 101:33–38

    Article  Google Scholar 

  • Eis S (1973) Cone production of Douglas-fir and grand fir and its climatic requirements. Can J Forest Res 3(1):61–70

    Article  Google Scholar 

  • Farmer RE (1997) Ecophysiology of temperate and boreal zone forest trees. St. Lucie Press, Florida

    Google Scholar 

  • Fletcher QE, Boutin S, Lane JE, LaMontagne JM, McAdam AG, Krebs CJ, Humphries MM (2010) The functional response of a hoarding seed predator to mast seeding. Ecology 91:2673–2683

    Article  PubMed  Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage Publications, Thousand Oaks

    Google Scholar 

  • Grace J, Berninger F, Nagy L (2002) Impacts of climate change on the tree line. Ann Bot Lond 90(4):537–544

    Article  CAS  Google Scholar 

  • Guarín A, Taylor AH (2005) Drought triggered tree mortality in mixed conifer forests in Yosemite National Park, California, USA. Forest Ecol Manag 218(1):229–244

    Article  Google Scholar 

  • Hastie TJ, Tibshirani RJ (1990) Generalized additive models, vol 43. CRC Press, Boca Raton

    Google Scholar 

  • Haylock MR, Hofstra N, Klein Tank AMG, Klok EJ, Jones PD, New M (2008) A European daily high-resolution gridded data set of surface temperature and precipitation for 1950–2006. J Geophys Res 113(D20):1–12

    Article  Google Scholar 

  • Hoch G, Siegwolf RT, Keel SG, Körner C, Han Q (2013) Fruit production in three masting tree species does not rely on stored carbon reserves. Oecologia 171(3):653–662

    Article  PubMed  Google Scholar 

  • Inouye DW (2000) The ecological and evolutionary significance of frost in the context of climate change. Ecol Lett 3(5):457–463

    Article  Google Scholar 

  • IPCC AR5 WG1 (2013) Stocker TF et al. (ed) Climate Change 2013: The Physical Science Basis. Working Group 1 (WG1) Contribution to the Intergovernmental Panel on Climate Change (IPCC) 5th Assessment Report (AR5), Cambridge University Press

  • Isotta FA, Frei C, Weilguni V, Perec Tadi M, Lassgues P, Rudolf B, Pavan V, Cacciamani C, Antolini G, Ratto SM, Munari M, Micheletti S, Bonati V, Lussana C, Ronchi C, Panettieri E, Marigo G, Vertanik G (2014) The climate of daily precipitation in the Alps: development and analysis of a high-resolution grid dataset from pan-Alpine rain-gauge data. Int J Climatol 34(5):1657–1675

    Article  Google Scholar 

  • ISPRA, Istituto Superiore per la Protezione e la Ricerca Ambientale (2010) La realizzazione in Italia del Progetto CORINE Land Cover 2006. ISPRA, Rapporti 131/2010. ISBN: 978-88-448-0477-0 (in Italian)

  • Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 465–492

  • Johnson AH, Friedland AJ, Dushoff JG (1986) Recent and historic red spruce mortality: Evidence of climatic influencee. Water Air Soil Poll 30(1–2):319–330

    Article  Google Scholar 

  • Juday GP, Barber V, Rupp S, Zasada JC, Wilming M (2003) A 200-year perspective of climate variability and the response of white spruce in interior Alaska. In: Greenland D, Goodin DG, Smith RC (eds) Climate variability and ecosystem response at long-term ecological research sites. Oxford University Press, Oxford, pp 226–250

    Google Scholar 

  • Kelly D (1994) The evolutionary ecology of mast seeding. Trends Ecol Evol 9:465–470

    Article  CAS  PubMed  Google Scholar 

  • Kelly D, Sork VL (2002) Mast Seeding Perennial Plants: why, how where? Annu Rev Ecol Syst 33:427–447

    Article  Google Scholar 

  • Kelly D, Hart DE, Allen RB (2001) Evaluating the wind-pollination benefits of mast seeding. Ecology 82:117–126

    Article  Google Scholar 

  • Kelly D, Geldenhuis A, James A et al (2013) Of mast and mean: differential temperature cue makes mast seeding insensitive to climate change. Ecol Lett 16:90–98

    Article  PubMed  Google Scholar 

  • Koenig WD, Knops JM (1998) Scale of mast-seeding and tree-ring growth. Nature 396(6708):225–226

    Article  CAS  Google Scholar 

  • Koenig WD, Knops JM (2013) Large-scale spatial synchrony and cross-synchrony in acorn production by two California oaks. Ecology 94:83–93

    Article  PubMed  Google Scholar 

  • Krebs CJ, LaMontagne JM, Kenney AJ, Boutin S (2012) Climatic determinants of white spruce cone crops in the boreal forest of southwestern Yukon. Botany 90:113–119

    Article  Google Scholar 

  • LaDeau SL, Clark JS (2001) Rising CO2 levels and the fecundity of forest trees. Science 292:95–98

    Article  CAS  PubMed  Google Scholar 

  • LaMontagne JM, Boutin S (2007) Local-scale synchrony and variability in mast seed production patterns of Picea glauca. J Ecol 95:991–1000

    Article  Google Scholar 

  • Lévesque M, Saurer M, Siegwolf R, Eilmann B, Brang P, Bugmann H, Rigling A (2013) Drought response of five conifer species under contrasting water availability suggests high vulnerability of Norway spruce and European larch. Glob Change Biol 19:3184–3199

    Article  Google Scholar 

  • Lindner M, Maroschek M, Netherer S et al (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Forest Ecol Manag 259:698–709

    Article  Google Scholar 

  • Lobo N, Millar JS (2011) The efficacy of conifer seeds as major food resources to deer mice (Peromyscus maniculatus) and southern red-backed voles (Myodes gapperi). Mamm Biol 76:274–284

    Google Scholar 

  • Lobo N, Green DJ, Millar JS (2013) Effects of seed quality and abundance on the foraging behavior of deer mice. J Mammal 94:1449–1459

    Article  Google Scholar 

  • Man R, Colombo S, Kayahara GJ, Duckett S, Velasquez R, Dang QL (2013) A case of extensive conifer needle browning in northwestern Ontario in 2012: winter drying or freezing damage? Forest Chron 89(5):675–680

    Article  Google Scholar 

  • Maslin M, Austin P (2012) Uncertainty: climate models at their limit? Nature 486(7402):183–184

    Article  CAS  PubMed  Google Scholar 

  • Mencuccini M, Piussi A, Zanzi S (1995) Thirty years of seed production in a subalpine Norway spruce forest: patterns of temporal and spatial variation. Forest Ecol Manag 76:109–125

    Article  Google Scholar 

  • Pearse SI, Koenig DW, Knops MHJ (2014) Cues versus proximate drivers: testing the mechanism behind masting behaviour. Oikos 123:179–184

    Article  Google Scholar 

  • Pelfini M, Leonelli G, Santilli M (2006) Climatic and Environmental Influences on Mountain Pine (Pinus montana Millere) growth in the Central Italian Alps. Arct Antarct Alp Res 38:614–623

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015). _nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1-120. http://CRAN.R-project.org/package=nlme. Accessed 15 Dec 2015

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 15 Dec 2015

  • Rodrigues D, Wauters LA, Romeo C et al (2010) Living on the edge: can Eurasian red squirrels (Sciurus vulgaris) persist in extreme high-elevation habitats? Arct Antarct Alp Res 42:106–112

    Article  Google Scholar 

  • Roland CA, Schmidt JH, Johnstone JF (2014) Climate sensitivity of reproduction in a mast-seeding boreal conifer across its distributional range from lowland to treeline forests. Oecologia 174:665–677

    Article  PubMed  Google Scholar 

  • Romeo C, Wauters LA, Preatoni D, Tosi G, Martinoli A (2010) Living on the edge: space use of Eurasian red squirrels in marginal high-elevation habitat. Acta Oecol 36:604–610

    Article  Google Scholar 

  • Sala A, Hopping K, McIntire EJ, Delzon S, Crone EE (2012) Masting in whitebark pine (Pinus albicaulis) depletes stored nutrients. N Phytol 196:189–199

    Article  CAS  Google Scholar 

  • Salmaso F, Molinari A, Di Pierro E et al (2009) Estimating and comparing food availability for tree-seed predators in typical pulsed-resource systems: Alpine conifer forests. Plant Biosyst 143:258–267

    Article  Google Scholar 

  • Satake A, Iwasa Y (2000) Pollen coupling of forest trees: forming synchronized and periodic reproduction out of chaos. J Theor Biol 203(2):63–84

    Article  CAS  PubMed  Google Scholar 

  • Selås V, Piovesan G, Adams JM, Bernabei M (2002) Climatic factors controlling reproduction and growth of Norway spruce in southern Norway. Can J Forest Res 32:217–225

    Article  Google Scholar 

  • Teutschbein C, Seibert J (2012) Bias correction of regional climate model simulations for hydrological climate-change impact studies: review and evaluation of different methods. J Hydrol 456457:12–29

    Article  Google Scholar 

  • Thomas PA, Wein RW (1985) Water availability and the comparative emergence of four conifer species. Can J Bot 63:1740–1746

    Google Scholar 

  • Tranquillini W (2012) Physiological ecology of the alpine timberline: tree existence at high altitudes with special reference to the European Alps, vol 31. Springer, New York

    Google Scholar 

  • Vittoz P, Bodin J, Ungricht S, Burga CA, Walther GR (2008) One century of vegetation change on Isla Persa, a nunatak in the Bernina massif in the Swiss Alps. J Veg Sci 19(5):671–680

    Article  Google Scholar 

  • Walker X, Henry GH, McLeod K, Hofgaard A (2012) Reproduction and seedling establishment of Picea glauca across the northernmost forest-tundra region in Canada. Glob Change Biol 18:3202–3211

    Article  Google Scholar 

  • Wauters LA, Gurnell J, Preatoni D, Tosi G (2001) Effects of spatial variation in food availability on spacing behaviour and demography of Eurasian red squirrels. Ecography 24(5):525–538

    Article  Google Scholar 

  • Wauters LA, Matthysen E, Adriaensen F, Tosi G (2004) Within-sex density dependence and population dynamics of red squirrels Sciurus vulgaris. J Anim Ecol 73(1):11–25

    Article  Google Scholar 

  • Wauters LA, Bertolino S, Adamo M, Van Dongen S, Tosi G (2005) Food shortage disrupts social organization: the case of red squirrels in conifer forests. Evol Ecol 19:375–404

    Article  Google Scholar 

  • Wauters LA, Vermeulen M, Van Dongen S, Bertolino S, Molinari A, Tosi G, Matthysen E (2007) Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography 30:51–65

    Article  Google Scholar 

  • Wauters LA, Githiru M, Bertolino S, Molinari A, Tosi G, Lens L (2008) Demography of alpine red squirrel populations in relation to fluctuations in seed crop size. Ecography 31:104–114

    Article  Google Scholar 

  • Wesołowski T, Rowiński P, Maziarz M (2015) Interannual variation in tree seed production in a primeval temperate forest: does masting prevail? Eur J For Res 134:99–112

    Article  Google Scholar 

  • Williams AP, Allen CD, Macalady AK et al (2013) Temperature as a potent driver of regional forest drought stress and tree mortality. Nat Climate Change 3:292–297

    Article  Google Scholar 

  • Williams CT, Lane JE, Humphries MM, McAdam AG, Boutin S (2014) Reproductive phenology of a food-hoarding mast-seed consumer: resource-and density-dependent benefits of early breeding in red squirrels. Oecologia 174:777–788

    Article  PubMed  Google Scholar 

  • Wood SN (2006) Generalized Additive Models: An introduction with R. Chapman & Hall/CRC, London, Boca Raton

    Google Scholar 

  • Zong C, Wauters LA, Van Dongen S et al (2010) Annual variation in predation and dispersal of Arolla pine (Pinus cembra L.) seeds by Eurasian red squirrels and other seed-eaters. Forest Ecol Manag 260:587–594

    Article  Google Scholar 

  • Zong C, Wauters LA, Rong K, Martinoli A, Preatoni DG, Tosi G (2012) Nutcrackers become choosy seed harvesters in a mast-crop year. Ethol Ecol Evol 24:54–61

    Article  Google Scholar 

  • Zong C, Mei S, Santicchia F, Wauters LA, Preatoni DG, Martinoli A (2014) Habitat effects on hoarding plasticity in the Eurasian red squirrel (Sciurus vulgaris). Hystrix 25:14–17

    Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

  • Zwiers FW, Alexander LV, Hegerl GC, Knutson TR, Kossin JP, Naveau P et al (2013) Climate extremes: challenges in estimating and understanding recent changes in the frequency and intensity of extreme climate and weather events. In: Asrar GR, Hurrell JW (eds) Climate science for serving society. Springer, Netherlands, pp 339–389

    Chapter  Google Scholar 

Download references

Acknowledgments

The project was supported by the Italian Minister of Education, University and Research (PRIN 2010–2011, 20108 TZKHC to Insubria University, Varese). Field work conducted in Valle d’Aosta was supported by a grant from Gran Paradiso National Park and another from NextData project. We thank all other participants of PRIN project who contributed in discussion and shared unpublished results giving important indication to improve first draft of this manuscript: Sassari University, Department of Science for Nature and Environmental Resources; Pavia University, Department of Earth and Environmental Sciences and Palermo University, Department of Biological, Chemical and Pharmaceutical Sciences and Technologies. We acknowledge ICTP for the production of the climate model simulations used in this work. We thank Marco Turco (ISAC-CNR) for providing the postprocessed and bias-corrected climate simulations. We acknowledge ARPA Lombardia and Centro Funzionale Regionale Regione Autonoma Valle d’Aosta for providing observed climate data. This is paper no. 27 of ASPER project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Bisi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Dr. Christian Ammer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Autocorrelation function estimates, in bold significant correlation (PDF 64 kb)

Online Resource 2

Seed production for each area and species (PDF 84 kb)

Online Resource 3

Cones prediction (PDF 102 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bisi, F., von Hardenberg, J., Bertolino, S. et al. Current and future conifer seed production in the Alps: testing weather factors as cues behind masting. Eur J Forest Res 135, 743–754 (2016). https://doi.org/10.1007/s10342-016-0969-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10342-016-0969-4

Keywords

Navigation