High seed dispersal ability of Pinus canariensis in stands of contrasting density inferred from genotypic data

  • Unai López de Heredia Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.
  • Nikos Nanos Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.
  • Eduardo García-del-Rey Departamento de Ecología, Facultad de Biología, Universidad de La Laguna, 38206 La Laguna, Tenerife, Canary Islands.
  • Paula Guzmán Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.
  • Rosana López Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.
  • Martin Venturas Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.
  • Pascual Gil-Muñoz Sección de Montes, Medio Ambiente, Cabildo Insular de Tenerife, Santa Cruz de Tenerife 38200, Canary Islands.
  • Luis Gil Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.


Aim of the study: Models that combine parentage analysis from molecular data with spatial information of seeds and seedlings provide a framework to describe and identify the factors involved in seed dispersal and recruitment of forest species. In the present study we used a spatially explicit method (the gene shadow model) in order to assess primary and effective dispersal in Pinus canariensis.

Area of study: Pinus canariensis is endemic to the Canary Islands (Spain). Sampling sites were a high density forest in southern slopes of Tenerife and a low density stand in South Gran Canaria.

 Materials and methods: We fitted models based on parentage analysis from seeds and seedlings collected in two sites with contrasting stand density, and then compared the resulting dispersal distributions.

Main results: The results showed that: 1) P. canariensis has a remarkable dispersal ability compared to other pine species; 2) there is no discordance between primary and effective dispersals, suggesting limited secondary dispersal by animals and lack of Janzen-Connell effect; and 3) low stand densities enhance the extent of  seed dispersal, which was higher in the low density stand.

Research highlights: The efficient dispersal mechanism of P. canariensis by wind inferred by the gene shadow model is congruent with indirect measures of gene flow, and has utility in reconstructing past demographic events and in predicting future distribution ranges for the species.

Keywords: Bayesian inference; Canary Islands; gene shadow model; microsatellites; parentage analysis.


Download data is not yet available.

Author Biography

Unai López de Heredia, Forest Genetics and Ecophysiology Research Group. E.T.S. Forestry Engineering. Technical University of Madrid (UPM). Ciudad Universitaria s/n. 28040. Madrid.
Departamento de Silvopascicultura. Profesor Contratado Doctor



Aboal JR, Jiménez MS, Morales MS, Gil P, 2000. Effect of thinning on throughfall in Canary Islands pine forest – the role of fog. J Hydrol 238(3-4): 218-230. http://dx.doi.org/10.1016/S0022-1694(00)00329-2

Auckland L, Bui T, Zhou Y, Shepherd M, Williams C, 2002. Conifer microsatellite handbook. Texas A&M University, College Station, Texas, 57 pp.

Arévalo JR, Naranjo A, Salas M, 2005. Regeneration in a mixed stand of native Pinus canariensis and introduced Pinus pinea species. Acta Oecol 28(2): 87-94. http://dx.doi.org/10.1016/j.actao.2005.03.001

Bannerman DA, Bannerman WM, 1963. Birds of the Atlantic Islands. A history of the birds of the Canary Islands and of the salvages. Oliver & Boyde, Edinburgh, UK. 358 pp.

Bohrer G, Katul GG, Nathan R, Walko RL, Avissar R, 2008. Effects of canopy heterogeneity, seed abscission and inertia on wind-driven dispersal kernels of tree seeds. J Ecol 96(4): 569-580. http://dx.doi.org/10.1111/j.1365-2745.2008.01368.x

Bontemps A, Klein EK, Oddou-Muratorio SO, 2013. Shift of spatial patterns during early recruitment in Fagus sylvatica: evidence from seed dispersal estimates based on genotypic data. For Ecol Manag 305: 67-76.

Briggs JS, Vander Wall SB, Jenkins SH, 2009. Forest rodents provide directed dispersal of Jeffrey pine seeds. Ecology 90(3): 675-687. http://dx.doi.org/10.1890/07-0542.1

Brooks S, Gelman A, 1998. General methods for monitoring convergence of iterative simulations. J Comput Graph Stat 7(4): 434-455.

Burczyk J, Adams WT, Birkes DS, Chybicki IJ, 2006. Using genetics markers to directly estimate gene flow and reproductive success parameters in plants on the basis of naturally regenerated seedlings. Genetics 173(1): 363-372. http://dx.doi.org/10.1534/genetics.105.046805

Carlo TA, Morales JM, 2008. Inequalities in fruit removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation. J Ecol 96(4): 609-618. http://dx.doi.org/10.1111/j.1365-2745.2008.01379.x

Clark JS, 1998. Why Trees Migrate So Fast: Confronting Theory with Dispersal Biology and the Paleorecord. Am Nat 152(2): 204-224. http://dx.doi.org/10.1086/286162

Clark JS, Silman M, Kern R, Macklin E, HilleRisLambers J, 1999. Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80: 1475-1494. http://dx.doi.org/10.1890/0012-9658(1999)080[1475:SDNAFP]2.0.CO;2

Climent J, Tapias R, Pardos JA, Gil L, 2004. Fire adaptations in the Canary Islands pine (Pinus canariensis). Plant Ecol 171(1-2): 185-196. http://dx.doi.org/10.1023/B:VEGE.0000029374.64778.68

Connell JH, 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and rain forest trees. In: Dynamics of Populations. (Den Boer PJ, Gradwell G, eds). Wageningen, The Netherlands, Centre for Agricultural Publishing and Documantation (PUDOC). pp. 298-312.

De Nascimento L, Willis KJ, Fernández-Palacios JM, Criado C, Whittaker RJ, 2009. The long-term ecology of the lost forests of La Laguna, Tenerife (Canary Islands). J Biogeogr 36(3):499-514. http://dx.doi.org/10.1111/j.1365-2699.2008.02012.x

Del Arco MJ, Pérez de Paz PL, Rodríguez O, Salas M, Wildpret W, 1992. Atlas cartográfico de los pinares canarios (II): Tenerife. Viceconsejería de Medio Ambiente, Consejería de Política Territorial, Gobierno de Canarias, Santa Cruz de Tenerife, Spain. 228 pp.

Dellaporta SL, Wood J, Hicks JB, 1983. A plant DNA minipreparation: version II. Plant Mol Biol Rep 1(4): 19-21. http://dx.doi.org/10.1007/BF02712670

Eckenwalder JF, 2009. Conifers of the world: the complete reference. Timber Press, Portland, OR, 720 pp.

García-del-Rey E, Delgado G, Gonzalez J, Wink M, 2007. Canary Island great spotted woodpecker (Dendrocopos major) has distinct mtDNA. J Ornithol 148(4): 531-536. http://dx.doi.org/10.1007/s10336-007-0142-4

García-del-Rey E, Gil L, Nanos N, Lopez-de-Heredia U, Gil Muñoz P, Fernandez-Palacios JM, 2009. Habitat characteristics and seed crops used by Blue Chaffinches Fringilla teydea in winter: implications for conservation management. Bird Study 56(2): 168-176. http://dx.doi.org/10.1080/00063650902792007

García-del-Rey E, Nanos N, López-de-Heredia U, Gil Muñoz P, Rüdiger O, Fernández-Palacios JM, Gil L, 2011. Spatiotemporal variation of a Pinus seed rain available for an endemic finch in an insular environment. Eur J Wildlife Res 57(2): 337-347. http://dx.doi.org/10.1007/s10344-010-0438-1

Gerber S, Chabrier P, Kremer A, 2003. FAMOZ: a software for parentage analysis using dominant, codominant and uniparentally inherited markers. Mol Ecol Notes 3(3): 479-481. http://dx.doi.org/10.1046/j.1471-8286.2003.00439.x

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. http://dx.doi.org/10.1111/j.1365-294X.2006.03118.x

Greene DF, Canham CD, Coates KD, Lepage PT, 2004. An evaluation of alternative dispersal functions for trees. J Ecol 92(5): 758-766. http://dx.doi.org/10.1111/j.0022-0477.2004.00921.x

Harper JL, 1977. Population Biology of Plants. London, Academic Press, 900 p.

Herrera CM, Jordano P, López-Soria L, Amat JA, 1994. Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugivore activity and seedling establishment. Ecol Monogr 64(3): 315-344. http://dx.doi.org/10.2307/2937165

Houle G, 1995. Seed dispersal and seedlings recruitment - The missing link(s). Ecoscience 2(3): 238-244.

Jamieson A, Taylor SC, 1997. Comparisons of three probability formulae for parentage exclusion. Anim Genet 28(6): 397-400. http://dx.doi.org/10.1111/j.1365-2052.1997.00186.x

Janzen DH, 1970. Herbivores and number of tree species in tropical forests. Am Nat 104(940): 501-528. http://dx.doi.org/10.1086/282687

Jones FA, Muller-Landau HC, 2008. Measuring long-distance seed dispersal in complex natural environments: an evaluation and integration of classical and genetic methods. J Ecol 96(4): 642-652. http://dx.doi.org/10.1111/j.1365-2745.2008.01400.x

Jordano P, Garcia C, Godoy JA, Garcia-Castano JL, 2007. Differential contribution of frugivores to complex seed dispersal patterns. P Natl Acad Sci USA 104(9): 3278-3282. http://dx.doi.org/10.1073/pnas.0606793104

Kass RE, Wasserman L, 1996. The selection of prior distributions by formal rules. J. Am Stat Assoc 91(435):1343-1370. http://dx.doi.org/10.1080/01621459.1996.10477003

Katul GG, Porporato A, Nathan R, Siqueira M, Soons MB, Poggi D,Horn HS, Levin SA, 2005. Mechanistic analytical models for long-distance seed dispersal by wind. Am Nat 166(3): 368-381. http://dx.doi.org/10.1086/432589

Klaus W, 1989. Mediterranean pines and their history. Plant Syst Evol 162(1-4): 133-163. http://dx.doi.org/10.1007/BF00936915

López R, López de Heredia U, Collada C, Cano FJ, Emerson BC, Cochard H, Gil L, 2013. Vulnerability to cavitation, hydraulic efficiency, growth and survival in an insular pine (Pinus canariensis). Ann. Bot.-London 111: 1167-1179. http://dx.doi.org/10.1093/aob/mct084

López de Heredia U, Venturas M, López R, Gil L, 2010. High biogeographical and evolutionary value of Canary Island pine populations out of the elevational pine belt: the case of a relict coastal population. J Biogeogr 37(12): 2371-2383. http://dx.doi.org/10.1111/j.1365-2699.2010.02367.x

López de Heredia U, López R, Collada C, Emerson BC, Gil L, 2014. Signatures of volcanism and aridity in the evolution of an insular pine (Pinus canariensis Chr. Sm. Ex DC in Buch). Heredity 113: 240-249. http://dx.doi.org/10.1038/hdy.2014.22

MacArthur RH, Diamond JH, Karr JR, 1972. Density compensation in island faunas. Ecology 53: 330-342. http://dx.doi.org/10.2307/1934090

Millerón M, López de Heredia U, Lorenzo Z, Perea R, Dounavi A, Alonso J, Gil L, Nanos N, 2012. Effect of canopy closure on pollen dispersal in a wind-pollinated species (Fagus sylvatica L.). Plant Ecol 213(11): 1715-1728. http://dx.doi.org/10.1007/s11258-012-0125-2

Millerón M, López de Heredia U, Lorenzo Z, Alonso J, Dounavi A, Gil L, Nanos N, 2013. Assessment of spatial discordance of primary and effective seed dispersal of European beech (Fagus sylvatica L.) by ecological and genetic methods. Mol Ecol 22(6): 1531-1545. http://dx.doi.org/10.1111/mec.12200

Moran EV, Clark JS, 2011. Estimating seed and pollen movement in a monoecious plant: a hierarchical Bayesian approach integrating genetic and ecological data. Mol Ecol 20(6): 1248-1262. http://dx.doi.org/10.1111/j.1365-294X.2011.05019.x

Nanos N, Larson K, Millerón M, Sjöstedt-de-Luna S, 2010. Inverse modeling for effective dispersal: Do we need tree size to estimate fecundity? Ecol Model 221(20): 2415-2424. http://dx.doi.org/10.1016/j.ecolmodel.2010.07.004

Nathan R, Muller-Landau HC, 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15(7): 278-285. http://dx.doi.org/10.1016/S0169-5347(00)01874-7

Nathan R, Katul GG, Horn HS, Thomas SM, Oren R, Avissar R, Pacala SW, Levin SA, 2002. Mechanisms of long-distance dispersal of seeds by wind. Nature 418: 409-413. http://dx.doi.org/10.1038/nature00844

Otto R, García-del-Rey E, Gil Muñoz P, Fernández-Palacios J, 2010. The effect of fire severity on first-year seedling establishment in a Pinus canariensis forest on Tenerife, Canary Islands. Eur J For Res 129(4): 499-508. http://dx.doi.org/10.1007/s10342-009-0347-6

Peakall R, Smouse PE, 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28: 2537-2539. http://dx.doi.org/10.1093/bioinformatics/bts460

Pérez de Paz P, del Arco M, Rodríguez O, Wildpret WY, Salas M, 1994. Atlas cartográfico de los pinares canarios: Gran Canaria, Lanzarote y Fuerteventura. Dir. Gral. de Medio Ambiente y Cons. de la Naturaleza, Gobierno de Canarias, Santa Cruz de Tenerife, Spain.

Pounden E, Greene DF, Quesada M, Contreras Sánchez JM, 2008. The effect of collisions with vegetation elements on the dispersal of winged and plumed seeds. J Ecol 96(4): 591-598. http://dx.doi.org/10.1111/j.1365-2745.2008.01380.x

R Development Core Team, 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

Ribbens E, Silander JA, Pacala SW, 1994. Seedling recruitment in forests - Calibrating models to predict patterns of tree seedling dispersion. Ecology 75(6): 1794-1806. http://dx.doi.org/10.2307/1939638

Robledo-Arnuncio JJ, Garcia C, 2007. Estimation of the seed dispersal kernel from exact identification of source plants. Mol Ecol 16(23): 5098-5109. http://dx.doi.org/10.1111/j.1365-294X.2007.03427.x

Rost J, Clavero M, Bas JM, Pons P, 2010. Building wood debris piles benefits avian seed dispersers in burned and logged Mediterranean pine forests. Forest Ecol Manag 260(1): 79-86. http://dx.doi.org/10.1016/j.foreco.2010.04.003

Rouget M, Reyers B, Jonas Z, Desmet P, Driver A, Maze K, Egoh B, Cowling RM, 2004. National Spatial Biodiversity Assessment 2004: Technical Report. Volume 1: Terrestrial Component, South African National Biodiversity Institute, Pretoria, South Africa. 88 p.

Schurr FM, Steinitz O, Nathan R, 2008. Plant fecundity and seed dispersal in spatially heterogeneous environments: models, mechanisms and estimation. J Ecol 96(4): 628-641. http://dx.doi.org/10.1111/j.1365-2745.2008.01371.x

Spiegelhalter D, Best N, Carlin B, van der Linde A, 2002. Bayesian measures of model complexity and fit. J R Stat Soc B 64(4): 583-639. http://dx.doi.org/10.1111/1467-9868.00353

Soranzo N, Provan J, Powell W, 1998. Characterization of microsatellite loci in Pinus sylvestris L. Mol Ecol 7(9): 1260-1261.

Steinitz O, Troupin D, Vendramin GG, Nathan R, 2011. Genetic evidence for a Janzen-Connell recruitment pattern in reproductive offspring of Pinus halepensis trees. Mol Ecol 20(19): 4152-4164. http://dx.doi.org/10.1111/j.1365-294X.2011.05203.x

van Oosterhout C, Hutchinson W, Wills D, Shipley P, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3): 535-538. http://dx.doi.org/10.1111/j.1471-8286.2004.00684.x

Vaxevanidou Z, González-Martínez SC, Climent J, Gil L, 2006. Tree populations bordering on extinction: a case study in the endemic Canary Island pine. Biol Conserv 129(4): 451-460. http://dx.doi.org/10.1016/j.biocon.2005.11.012

Vendramin GG, Lelli L, Rossi P, Morgante M, 1996. A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5(4): 595-598. http://dx.doi.org/10.1111/j.1365-294X.1996.tb00353.x

Volsoe H, 1955. The breeding birds of the Canary Islands, II: origin and history of the Canarian avifauna. Vidensk. Medd. Dan. Naturhist. 117(12): 117-178.

VVAA, 2011. Plan de Adaptación de Canarias al Cambio Climático. Agencia Canaria de Desarrollo Sostenible y Cambio Climático, Gobierno de Canarias, Spain. 170 pp.

How to Cite
López de Heredia, U., Nanos, N., García-del-Rey, E., Guzmán, P., López, R., Venturas, M., Gil-Muñoz, P., & Gil, L. (2015). High seed dispersal ability of Pinus canariensis in stands of contrasting density inferred from genotypic data. Forest Systems, 24(1), e015. https://doi.org/10.5424/fs/2015241-06351
Research Articles