Factors affecting cone production in Pinus pinaster Ait.: lack of growth-reproduction trade-offs but significant effects of climate and tree and stand characteristics

  • Felipe Bravo 1 Sustainable Forest Management Research Institute, Universidad de Valladolid - INIA. 2 Universidad de Valladolid, Escuela Técnica Superior de Ingenierías Agrarias, Dept. Producción Vegetal y Recursos Forestales. Avda de Madrid 44, 34004 Palencia.
  • Douglas A. Maguire Oregon State University; College of Forestry; Dept. of Forest Engineering, Resources and Management. Corvallis, OR
  • Santiago C. González-Martínez UMR1202 BioGeCo: Biodiversity, Genes & Communities, Cestas
Keywords: ZIP model, NAO, Mediterranean, silviculture, dendrochronology


Aim of study: Our main goal is to determine the relationship between cone production and radial growth in Pinus pinaster Ait. under different climatic conditions across the Iberian Peninsula.

Area of study: Coca Intensive Sampling Plateau, Northern Plateau (Spain).

Material and methods: Cone counts were conducted on an intensive monitoring plot in Coca (North-Central Spain) during the years 2000, 2006 and 2007. A ZIP (zero-inflated Poisson) model was adjusted for simultaneously estimating the probability of obtaining crop cones and its amount. The Northern Atlantic Oscillation (NAO) index was used as explanatory variable, together with a wide variety of tree and local stand variables. Climate (as evaluated by NAO), local stand density (here estimated from the six nearest trees), tree size and vigor, competition and growth efficiency significantly influenced both occurrence and intensity of cone production.

Main results: ZIP models for predicting reproductive effort seems an adequate tool to predict reproductive responses to climatic fluctuations and the resulting future species distribution in the face of climate change, as well as to identify silviculture actions that would promote reproductive success in naturally-regenerated stands, list and discuss relevant results (including numeric values of experimental results).

Research highlights: Climate, stand density and tree conditions (size and vigor, competition and growth efficiency) influence significantly both cone occurrence and intensity of fruiting as shown by a ZIP model. As the climate variables included in the model (based on Northern Atlantic Oscillation, NAO) are general and easily obtained, the proposed model has practical applicability to predicting Pinus pinaster cone production in the Iberian Peninsula.


Download data is not yet available.


Alberto F, Aitken S, Alía R, González-Martínez SC, Hänninen H, Kremer A, Lefèvre F, Lenormand T, Yeaman S, Whetten R, Savolainen O, 2013. Evolutionary response to climate change -evidence from tree populations. Global Change Biol 19: 1645-1661. https://doi.org/10.1111/gcb.12181

Almqvist C, Jansson G, Sonesson J, 2001. Genotypic correlations between early cone-set and height growth in Picea abies clonal trials. Forest Genet 883: 197-204.

Barnett AG, Koper N, Dobson AJ, Schimiegelow F, Manseau M, 2010. Using information criteria to select the correct variance-covariance structure for longitudinal data in ecology. Meth Ecol Evol 1 (1): 15-24. https://doi.org/10.1111/j.2041-210X.2009.00009.x

Barringer BC, Koening WD, Knops JMH, 2013. Interrelationships among life-history traits in three California oaks. Oecologia 171: 129-139. https://doi.org/10.1007/s00442-012-2386-9

Bazzaz FA, Ackerly DD, Reekie EG, 2000. Reproductive allocation and reproductive effort in plants. In: Seeds: the ecology of regeneration in plant communities; Fenner M (ed.), 2nd edn, pp: 1-37. CAB Int, Oxford, UK. https://doi.org/10.1079/9780851994321.0001

Bell G, 1980. The costs of reproduction and their consequences. Am Nat 116: 45-76. https://doi.org/10.1086/283611

Bogino S, Bravo F, 2008. SOI and NAO impacts of Pinus pinaster Ait. growth in Spanish Forests. TRACE 2007 Tree Rings in Archaelogy, Climatology and Ecology 6: 21-26.

Calama R, Mutke S, Tomé J, Gordo J, Montero G, Tomé M, 2011. Modelling spatial and temporal variability in a zero-inflated variable: The case of stone pine (Pinus pinea L.) cone production. Ecol Model 222: 606-618. https://doi.org/10.1016/j.ecolmodel.2010.09.020

Campelo F, Nabais C, García-González I, Cherubini P, Gutiérrez E, Freitas H, 2009. Dendrochronology of Quercus ilex L. and its potential use for climate reconstruction in the Mediterranean region. Can J For Res 39: 2486-2493. https://doi.org/10.1139/X09-163

Climent J, Prada MA, Calama R, Chambel MR, Sánchez de Ron D, Alía R, 2008. To grow or to seed: ecotypic variation in reproductive allocation and cone production by young female Aleppo pine (Pinus halepensis, Pinaceae). Am J Bot 95 (7): 833-842. https://doi.org/10.3732/ajb.2007354

Despland E, Hoyles G, 1997. Climate influences on growth and reproduction of Pinus banksiana (Pinaceae) ata the limit of the species distribution in Eastern North America. Am J Bot 84 (8): 928-937. https://doi.org/10.2307/2446283

Dick J, Leakey RRB, Jarvis PG, 1990. Influence of female cones on the vegetative growth of Pinus contorta trees. Tree Phisiol 6: 151-163. https://doi.org/10.1093/treephys/6.2.151

Di Matteo G, Voltas J, 2016. Multienvironment evaluation of Pinus pinaster provenances: Evidence of genetic trade-offs between adaptation to optimal conditions and resistance to the Maritime Pine Bast Scale (Matsucoccus feytaudi). Forest Sci 62 (5): 553-563. https://doi.org/10.5849/forsci.15-109

Eis S, Garman EH, Ebell LF, 1965. Relation between cone production and diameter increment of Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco), Grand fir (Abies grandis (Dougl.) Lindl.) and western white pine (Pinus monticola Dougl.). Can J Bot 43: 1553-1559. https://doi.org/10.1139/b65-165

El-Kassaby YA, Barclay HJ, 1992. Cost of reproduction in Douglas-fir. Can J Bot 70: 1429-1432. https://doi.org/10.1139/b92-179

Etterson JR, Shaw RG, 2001. Constraint to adaptive evolution in response to global warming. Science 294: 151-154. https://doi.org/10.1126/science.1063656

Ferrenberg S, Kane JM, Langehan JM, 2015. To grow or defend? Pine seedlings grow less but induce more defences when a key resource is limited. Tree Physiol 35: 107-111. https://doi.org/10.1093/treephys/tpv015

Fowells HA, Schubert GH, 1956. Seed crops of forest trees in the pine region of California. U.S. Department of Agriculture, Technical Bulletin 1150, Government Print Office, Washington DC.

Fox JF, Stevens GC, 1991. Costs of reproduction in a willow: experimental responses vs. natural variation. Ecology 72: 1013-1023. https://doi.org/10.2307/1940601

Gomulkiewicz R, Holt RD, 1995. When does evolution by natural selection prevent extinction? Evolution 49: 201-207. https://doi.org/10.1111/j.1558-5646.1995.tb05971.x

Gomulkiewicz R, Houle D, 2009. Demographic and genetic constraints on evolution. Am Natur 174: E218-229. https://doi.org/10.1086/645086

González-Martínez SC, Burczyk J, Nathan R, Nanos N, Gil L, Alía R, 2006. Effective gene dispersal and female reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton). Mol Ecol 15 (14): 4577-4588. https://doi.org/10.1111/j.1365-294X.2006.03118.x

Hasegawa S, Takeda H, 2001. Functional specialization of current shoots as a reproductive strategy in Japanese alder (Alnus hirsuta var. sibirica). Can J Bot 79: 38-48. https://doi.org/10.1139/b00-143

Hurrell JW, Deser C, 2009. North Atlantic climate variability: The role of the North Atlantic Oscillation. J Mar Syst 78: 28-41. https://doi.org/10.1016/j.jmarsys.2008.11.026

Juez L, González-Martínez SC, Nanos N, de-Lucas AI, Ordóñez C, del Peso C, Bravo F, 2014. Can seed production and restricted dispersal limit recruitment in Pinus pinaster Aiton from the Spanish Northern Plateau? Forest Ecol Manage 313: 329-339. https://doi.org/10.1016/j.foreco.2013.10.033

Johnson JB, Omland KS, 2004. Model selection in ecology and evolution. Trends Ecol Evol 19 (2):101-108. https://doi.org/10.1016/j.tree.2003.10.013

Knops JMH, Koenig WD, Carmen WJ, 2007. Negative correlation does not imply a tradeoV between growth and reproduction in California oaks. Proc Natl Acad Sci USA 104: 16982-16985. https://doi.org/10.1073/pnas.0704251104

Krannitz PG, Duralia TE (2004) Cone and seed production in Pinus Ponderosa: A review. Wes North Am Natur 64: 208-218.

Lambert D, 1992. Zero-Inflated Poisson regression models with an application to defects in manufacturing. Technometrics 34: 1-14. https://doi.org/10.2307/1269547

Larson MM, Schubert GH, 1970. Cone crops of ponderosa pine in central Arizona including the influence of Abert squirrels. US Dept of Agric, For Serv Rep RM-58, Rocky Mount Forest and Range Exp Stat, Fort Collins, CO, USA.

Lindholm MM, Eggertsson O, Lovelius N, Raspopov O, Shumilov O, Läämelaid A, 2001. Growth indices of North European Scots pine record the seasonal North Atlantic Oscillation. Boreal Environ Res 6: 275-284.

Linhart YB, Mitton JB, 1985. Relationships among reproduction, growth rates, and protein heterozygosity in Ponderosa Pine. Am J Bot 722: 181-184. https://doi.org/10.2307/2443545

Lizarralde I, 2008. Dinámica de rodales y competencia en las masas de pino silvestre (Pinus sylvestris L.) y pino negral (Pinus pinaster Ait.) de los sistemas central e Ibérico meridional. Tesis Doctoral, Universidad de Valladolid, Spain.

Lovett Doust J, Lovett Doust L, 1988. Modules of production and reproduction in a dioecious clonal shrub Rhus typhina. Ecology 69: 741-750. https://doi.org/10.2307/1941023

Martín-Vide J, Fernández-Belmonte D, 2001. El índice NAO y la precipitación mensual en la España peninsular. Invest Geograf 26: 41-58. https://doi.org/10.14198/INGEO2001.26.07

Menzel A, 2003. Plant phenological anomalies in Germany and their relation to air temperature and NAO. Clim Change 57: 243-263. https://doi.org/10.1023/A:1022880418362

Miguel I, González-Martínez SC, Alía R, Gil L, 2002. Growth phenology and mating system of maritime pine (Pinus pinaster Ait.) in central Spain. Invest Agrar: Sist Recur For 11: 193-204.

Monks A, Kelly D, 2006. Testing the resource-matching hypothesis in the mast seeding tree Nothofagus truncata (Fagaceae). Austral Ecol 31: 366-375. https://doi.org/10.1111/j.1442-9993.2006.01565.x

Moreira X, Zas R, Solla A, Sampedro L, 2015 Differentiation of persistent anatomical defensive structures is costly and determined by nutrient availability and genetic growth-defence constraints. Tree Physiol 35: 112-123. https://doi.org/10.1093/treephys/tpu106

Mutke S, Gordo J, Gil L, 2005. Variability of Mediterranean Stone pine cone production: Yield loss as response to climate change. Agr Forest Meteor 132: 263-272. https://doi.org/10.1016/j.agrformet.2005.08.002

Nanos N, González-Martínez SC, Bravo F, 2004. Studying within-stand structure and dynamics with geostatistical and molecular marker tools. Forest Ecol Manage 189: 223-240. https://doi.org/10.1016/j.foreco.2003.08.016

Obeso JR, 1997. Costs of reproduction in Ilex aquifolium: effects at tree branch and leaf levels. J Ecol 85: 159-166. https://doi.org/10.2307/2960648

Pan W, 2001. Akaike's information criterion in generalized estimating equations. Biometrics 57 (1): 120-125. https://doi.org/10.1111/j.0006-341X.2001.00120.x

Pasho E, Camarero JJ, Luis M de, Vicente-Serrano SM, 2011. Spatial variability in large-scale and regional atmospheric drivers of Pinus halepensis growth in eastern Spain. Agric Forest Meteorol 151: 1106-1119. https://doi.org/10.1016/j.agrformet.2011.03.016

Philippe G, Baldet P, Héois B, Ginisty C, 2006. Reproduction sexuée des conifères et production de semences en vergers à graines. Cemagref, 570 pp.

Piovesan G, Schirone B, 2000. Winter North Atlantic oscillation effects on the tree rings of the Italian beech (Fagus sylvatica L.) Int J Biometeorol 44: 121-127. https://doi.org/10.1007/s004840000055

Piovesan G, Adams JM, 2001. Masting behaviour in beech: linking reproduction and climatic variation. Can J Bot 79: 1039-1047. https://doi.org/10.1139/b01-089

Ruano I, Rodríguez E, Bravo F, 2013. Effects of pre-commercial thinning on growth and reproduction in post fire regeneration of Pinus halepensis Mill. Ann Forest Sci 70 (4): 357-366. https://doi.org/10.1007/s13595-013-0271-2

Sampedro L, Moreira X, Zas R, 2011. Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. J Ecol 99: 818-827. https://doi.org/10.1111/j.1365-2745.2011.01814.x

Sánchez-Humanes B, Sork VL, Espelta J, 2011. Tradeoffs between vegetative growth and acorn production in Quercus lobata during a mast year: the relevance of crop size and hierarchical level within the canopy. Oecologia 166 (1): 101-110. https://doi.org/10.1007/s00442-010-1819-6

Santos-del-Blanco L, Climent J, González-Martínez SC, Pannell JR, 2012. Genetic differentiation for size at first reproduction through male versus female functions in the widespread Mediterranean tree Pinus pinaster. Ann Bot 110: 1449-1460. https://doi.org/10.1093/aob/mcs210

Schmidtling RC, 1981. The inheritance of precocity and its relationship with growth in Loblolly pines. Silvae Genetica 30: 188-192.

Selas V, Piovesan G, Adams JM, Bernabei M, 2002. Climatic factors controlling reproduction and growth of Norway spruce in southern Norway. Can J For Res 32: 217-225. https://doi.org/10.1139/x01-192

Stach A, Emberlin J, Smith M, Adams-Groom B, Myszkowska D, 2008. Factors that determine the severity of Betula spp. pollen seasons in Poland (Poznań and Krakow) and the United Kingdom (Worcester and London). Int J Biometeorol 52: 311-321. https://doi.org/10.1007/s00484-007-0127-2

Stenseth NC, Ottersen G, Hurrell JW, Mysterud A, Lima M, Chan KS, Yoccoz NG, Ådlandsvik B, 2003. Studying climate effects on ecology through the use of climate indices, the North Atlantic Oscillation, El Niño Southern Oscillation and beyond. Proc R Soc Lond, B Biol Sci 270: 2087-2096. https://doi.org/10.1098/rspb.2003.2415

Sugiyama S, Bazzaz FA, 1998. Size dependence of reproductive allocation: the influence of resource availability, competition and genetic identity. Funct Ecol 12: 280-288. https://doi.org/10.1046/j.1365-2435.1998.00187.x

Tapias R, Climent J, Pardos JA, Gil L, 2004. Life histories of Mediterranean pines. Plant Ecol 171: 53-68. https://doi.org/10.1023/B:VEGE.0000029383.72609.f0

Tappeiner JC, 1969. Effect of cone production on branch, needle, and xylem ring growth of Sierra Nevada Douglas-fir. For Sci 15: 171-174.

Thomas SC, 2011. Age-related changes in tree growth and functional biology: the role of reproduction. In: Size- and age-related changes in tree structure and function; Meinzer FC et al. (eds), pp: 33-64. Springer. https://doi.org/10.1007/978-94-007-1242-3_2

Verkaik I, Espelta JM, 2006. Post-fire regeneration thinning, cone production, serotiny and regeneration age in Pinus halepensis. Forest Ecol Manage 231 (1-3): 155-163. https://doi.org/10.1016/j.foreco.2006.05.041

Wang G, Schimel D, 2003. Climate change, climate modes, and climate impacts. Ann Rev Environ Resour 28: 1-28. https://doi.org/10.1146/annurev.energy.28.050302.105444

Wykoff WR, 1990. A basal area increment model for individual conifers in the northern Rocky Mountains. For Sci 36: 1077-1104.

How to Cite
Bravo, F., Maguire, D. A., & González-Martínez, S. C. (2017). Factors affecting cone production in Pinus pinaster Ait.: lack of growth-reproduction trade-offs but significant effects of climate and tree and stand characteristics. Forest Systems, 26(2), e07S. https://doi.org/10.5424/fs/2017262-11200