The age of black pine (Pinus nigra Arn. ssp. salzmannii (Dunal) Franco) mother trees has no effect on seed germination and on offspring seedling performance

  • Reyes AlejanoEmail author
  • Marta Domínguez-Delmás
  • Ignacio García-González
  • Tomasz Wazny
  • Javier Vázquez-Piqué
  • Manuel Fernández-Martínez
Research Paper
Part of the following topical collections:
  1. Mediterranean Pines


Key message

We sampled Pinus nigra cones in 29 trees in an age range of 90 to 725 years. The mother tree age did not significantly influence the pinecone or pine seed size, seed germination capacity, or plant size or vigor displayed during the first year of growth in the nursery.


Pinus nigra Arn. ssp. salzmannii is a long-lived Mediterranean species, with millenary trees residing in an old-growth forest in the Cazorla Mountain Range in SE Spain which is home to the oldest known trees in the Iberian Peninsula.


This study aimed to assess how the mother tree age in Pinus nigra influences seed viability, germination capacity, and the seedling survival and growth during the first year under nursery conditions.


Twenty-nine trees aged 90 to 725 years were selected and 60 cones were harvested per tree to study the cone characteristics (size and weight), seed viability, and germination capacity in relation to the mother tree age. Eighty germinated seeds per tree were transferred to the nursery and seedling survival and growth were measured after the first growing season.


Significant between-tree differences were detected for cone characteristics (cone and seed weight, number of seeds per cone), as well as for germination capacity. Notably, however, the mother tree age did not significantly influence the aforementioned parameters.


Forest management and regeneration practices of Pinus nigra should take into account that trees of this species up to at least 725 years old produce seeds with a fairly high reproductive capacity.


Pinus nigra Aging Seed viability Old-growth forests 



We thank Teresa Moro and Valentín Badillo (from the Natural Park Forest Service, Junta de Andalucía, Spain) for providing the sampling permits required for the area and for their interest in the project. The dendrochronological fieldwork for this research was partially funded by the Netherlands Organisation for Scientific Research (NWO-number 236-61-001) and by the Spanish Ministry of Science, Innovation and Universities (Plan I+D+i AGL2017-83828-C2-2-R) and FEDER funds. We thank Antonio Jesús López- Soroche and Juan Manuel Castellano, students at the University of Huelva, Spain; Aldo Carrasco from the University Arturo Prat, Chile; and Ana J. Moreno, Y. Ramírez and Salvador Sarabia, from the University of Chapingo, Mexico, for their help with the lab and nursery work.


The dendrochronological fieldwork of this research was funded by the Netherlands Organisation for Scientific Research (NWO-number 236-61-001) and National Geographic Society (Waitts Grant W 329-14). The University of Huelva, Spain, provided the lab and nursery with the needed material to perform the experiment.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

13595_2019_801_MOESM1_ESM.docx (75 kb)
ESM 1 (DOCX 74 kb)


  1. Andivia E, Fernández M, Vázquez-Piqué J (2011) Autumn fertilization of Quercus ilex ssp. ballota (Desf.) Samp.nursery seedlings: effects on morpho-physiology and field performance. Ann ForSci 68(3):543–553. CrossRefGoogle Scholar
  2. Ayari A, Khouja ML (2014) Ecophysiological variables influencing Aleppo pine seed and cone production: a review. Tree Physiol. 34 (4):426–437.
  3. Beadle C, Duff G, Richardson A (2009) Old forests, new management: the conservation and use of old growth forests in the 21stcentury. For Ecol Manag 258(4):339–340CrossRefGoogle Scholar
  4. Brutovská E, Sámelová A, Dušička J, Mičieta K (2013) Ageing of trees: application of general ageing theories. Ageing Res Rev 12(4):855–866. CrossRefGoogle Scholar
  5. Carey EV, Sala A, Keane M, Callaway RM (2001) Are old forests underestimated as global carbon sinks? Glob Change Biol 7(4):339–344CrossRefGoogle Scholar
  6. Catalán G (1993) Semillas de árboles y arbustos forestales. Ministerio de Agricultura, Pesca y Alimentación. ICONA, Madrid, p 392 ISBN: 84-8014-007-0Google Scholar
  7. Creus J (1998) A propósito de los árboles más viejos de la España peninsular: los Pinus nigra Arnold subsp. salzmannii (Dunal) Franco de Puertollano-Cabañas Sierra de Cazorla, Jaén. Montes 54:68–76Google Scholar
  8. Davis AS, Jacobs DF (2005) Quantifying root system quality of nursery seedlings and relationship to outplanting performance. New For 30(2–3):295–311. CrossRefGoogle Scholar
  9. De Aranda G (1990) Los Bosques Flotantes: historia de un roble del siglo XVIII. Colección Técnica, Ministerio de Agricultura, Pesca y Alimentación. ICONA, Madrid, p 231 ISBN: 84-85496-50-7Google Scholar
  10. De la Cruz E (1994) La destrucción de los Montes (claves histórico-jurídicas). Universidad Complutense de Madrid, Madrid, p 287 ISBN: 84-86926-70-XGoogle Scholar
  11. Derridj A, Abdelli D, Adjaoud D, Asmani A, Fady B, Hedjam H, Larbi-Aidrous N, Zanndouche O, Krouchi F (2011) A synthesis on several years study on Pinus nigra ssp mauretanica in Algeria. In: Abstract Book. Medpine 4: 4th International Conference on Mediterranean Pines. June, 6-10, 2011. Avignon, France O8-2, p 76Google Scholar
  12. Dominguez-Delmás M, Alejano R, Wazny T, García-González I (2013) Radial growth variations of black pine along an elevation gradient in the Cazorla Mountains (South of Spain) and their relevance for historical and environmental studies. Eur J For Res 132(4):635–652. CrossRefGoogle Scholar
  13. Escudero A, Barrero S, Pita JM (1997) Efects of high temperatures and ash on seed germination of two Iberian pines (Pinus nigras sp salzmannii, P sylvestris var iberica). Ann Sci For 54(6):553–562CrossRefGoogle Scholar
  14. FAO (1985) A guide to forest seed handling. FAO forestry paper 20/2.Ed. Food and Agriculture Organization of the United Nations, Rome Available at: ISBN 92–5–102291-7Google Scholar
  15. Fernández M, Marcos C, Tapias R, Ruiz F, López G (2007) Nursery fertilization affects the frost-tolerance and plant quality of Eucalyptus globulus Labill. cuttings. Ann. For Sci 64(8):865–873. CrossRefGoogle Scholar
  16. Fernández M, Alejano R, Domínguez L, Tapias R (2008) Temperature controls cold hardening more effectively than photoperiod in four Mediterranean broadleaf evergreen species. Tree For Sci Biotechnol 2(1):43–49Google Scholar
  17. Ganatsas P, Tsakaldimi M, Thanos C (2008) Seed and cone diversity and seed germination of Pinus pinea in Strofylia site of the Natura 2000 network. Biodivers Conserv 17(10):2427–2439. CrossRefGoogle Scholar
  18. Gordo J, Calama R, Pardos M, Bravo F, Montero G, (Eds) (2012) La regeneración natural de los pinares en los arenales de la meseta castellana. In: Instituto Universitario de Investigación en Gestión Forestal Sostenible (Universidad de Valladolid-INIA). Valladolid. 254 p. ISBN: 978-84-615-9823-6Google Scholar
  19. Guariguata MR, Pinard MA (1998) Ecological knowledge of regeneration from seed in neotropical forest trees: implications for natural forest management. For Ecol Manag 112(1–2):87–99CrossRefGoogle Scholar
  20. Herrera CM (1991) Dissecting factors responsible for individual variations in plant fecundity. Ecology 72(4):1436–1448CrossRefGoogle Scholar
  21. Holloway DM, Brook B, Kang JH, Wong C, Wu M (2016) A quantitative study of cotyledon positioning in conifer development. Botany 94(11):1063–1074. CrossRefGoogle Scholar
  22. Kitajima K, Fenner M (2000) Ecology of seedling regeneration. Seeds: the ecology of regeneration in Plant Communities. CAB International, Wellington, p 410Google Scholar
  23. Klekovski EJ, Godfrey PJ (1989) Ageing and mutation in plants. Nature 340:389–391CrossRefGoogle Scholar
  24. Lanner RM (2002) Why do trees live so long? Ageing Res Rev 1(4):653–671CrossRefGoogle Scholar
  25. Lanner RM, Connor KF (2001) Does bristlecone pine senesce? Exp Gerontol 36(4–6):675–685CrossRefGoogle Scholar
  26. Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional groups. Springer-Verlag, Berlin, p 513CrossRefGoogle Scholar
  27. Lindenmayer DB, Franklin JF (2002) Conserving forest biodiversity. A Comprehensive Multiscaled Approach. Island Press, Washington DC, p 351Google Scholar
  28. Lindenmayer DB, McArthy MA (2002) Congruence between natural and human forest disturbance: a case study for Australian montane ash forest. For Ecol Manag 155(1–3):319–335CrossRefGoogle Scholar
  29. Lucas-Borja ME, Fonseca T, Parresol B, Silva-Santos P, García-Morote FA, Tíscar-Oliver PA (2011) Modelling Spanish black pine seedling emergence: establishing management strategies for endangered forest areas. For Ecol Manag 26(2):195–202. CrossRefGoogle Scholar
  30. Lucas-Borja ME, Fonseca TF, Lousada JL, Silva-Santos P, García EM, Abellán MA (2012) Natural regeneration of Spanish black pine [Pinus nigra Arn. ssp. salzmannii (Dunal) Franco] at contrasting altitudes in a Mediterranean mountain área. Ecol Res 27(5):913–921. CrossRefGoogle Scholar
  31. Lucas-Borja ME, Candel-Pérez D, Onkelinx T, Fule PZ, Moya D, Gómez R, de las Heras J (2017) Early Mediterranean pine recruitment in burned and unburned Pinus nigra Arn. ssp. salzmannii stands of Central Spain: influence of species identity, provenances and post-dispersal predation. For Ecol Manag 390:203–211. CrossRefGoogle Scholar
  32. Mao P, Han G, Wang G, Yu J, Shao H (2014) Effects of age and stand density of mother trees on early Pinus thunbergii seedling establishment in the coastal zone, China. Sci World J 2014(468036):9. CrossRefGoogle Scholar
  33. Mencuccini M, Oñate M, Peñuelas J, Rico L, Munné-Bosch S (2014) No signs of meristem senescence in old Scots pine. J Ecol 102(3):555–565. CrossRefGoogle Scholar
  34. Müller M, Siles L, Cela J, Munné-Bosch S (2014) Perennially young: seed production and quality in controlled and natural populations of Cistus albidus reveal compensatory mechanisms that prevent senescence in terms of seed yield and viability. J Exp Bot 65(1):287–297. CrossRefGoogle Scholar
  35. Munné-Bosch S (2008) Do perennials really senesce? Trends Plant Sci 13(5):216–220CrossRefGoogle Scholar
  36. Parker WC, Noland TL, Morneault AE (2006) The effects of seed mass on germination, seedling emergence, and early seedling growth of eastern white pine (Pinus strobus L.). New For 32(1):33–49. CrossRefGoogle Scholar
  37. Ruiz de la Torre J (2006). Mayor F (ed) Organismo Autónomo Parque Naturales. DGCONA. Ministerio de Medio Ambiente. Madrid. Spain. 1756 p. ISBN: 10: 84–8014–660-5Google Scholar
  38. Sauer M, Robert S, Kleine-Vehn J (2013) Auxin: simply complicated. J Exp Bot 64(9):2565–2577. CrossRefPubMedGoogle Scholar
  39. Serrada R, Domínguez S, Sánchez MI, Ruiz J (1994) El problema de la regeneración natural del Pinus nigra Arn. Montes 36:52–57Google Scholar
  40. Smith DM, Larson BC, Kelty MJ, Ashton PMS (1997) The practice of silviculture: applied forest ecology. John Wiley and Sons, New York, p 537Google Scholar
  41. Stephenson NL, Das AJ, Condit R, Russo SE, Baker PJ, Beckman NG, Coomes DA, Lines ER, Morris WK, Rüger N, Álvarez E, Blundo C, Bunyavejchewin S, Chuyong G, Davies SJ, Duque Á, Ewango CN, Flores O, Franklin JF, Grau HR, Hao Z, Harmon ME, Hubbell SP, Kenfack D, Lin Y, Makana JR, Malizia A, Malizia LR, Pabst RJ, Pongpattananurak N, Su SH, Sun IF, Tan S, Thomas D, van Mantgem PJ, Wang X, Wiser SK, Zavala MA (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature 507:90–93. CrossRefGoogle Scholar
  42. Temel F, Gülcü S, Ölmez Z, Göktürka A (2011) Germination of Anatolian black pine (Pinus nigra subsp. pallasiana) seeds from the lakes region of Turkey: geographic variation and effect of storage. Not Bot Horti Agrobo 39(1):267–274CrossRefGoogle Scholar
  43. Thomas H (2013) Senescence, ageing and death of the whole plant. New Phytol 197(3):696–711. CrossRefGoogle Scholar
  44. Tíscar Oliver PA (2002) Capacidad reproductiva de Pinus nigra subsp. salzmannii en relación con la edad de la planta madre. Invest Agr:Sist Recur For 11(2):357–371Google Scholar
  45. Tíscar Oliver PA (2007) Dinámica de regeneración de Pinus nigra ssp. salzmannii al sur de su área de distribución: etapas, procesos y factores implicados. Invest Agr: Sist Recur For 16(2):124–135Google Scholar
  46. Tíscar PA, Linares JC (2011) Pinus nigra subsp. salzmannii forests from Southeast Spain: using structure and process information to guide management. Chapter 11, 27 p. In: Frisiras CT (ed) Pine Forests: types, threats and management. Nova Science Publishers Inc. ISBN: 978-1-61324-493-7Google Scholar
  47. Tíscar PA, Lucas JC (2010) Seed mass variation, germination time and seedling performance in a population of Pinus nigra subsp. salzmannii. For Syst 19(3):344–353. CrossRefGoogle Scholar
  48. Viglas JN, Brown CD, Johnstone JF (2013) Age and size effects on seed productivity of northern black spruce. Can J For Res 43(6):534–543. CrossRefGoogle Scholar
  49. Wahid N, Bounoua L (2013) The relationship between seed weight, germination and biochemical reserves of maritime pine (Pinus pinaster Ait.) in Morocco. New For 44(3):385–397. CrossRefGoogle Scholar
  50. Xu Y, Cail N, He B, Zhang R, Zhao W, Mao J, Duan A, Li Y, Woeste K (2016) Germination and early seedling growth of Pinus densata Mast. provenances. J For Res 27(2):283–294. CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  • Reyes Alejano
    • 1
    Email author
  • Marta Domínguez-Delmás
    • 2
  • Ignacio García-González
    • 2
  • Tomasz Wazny
    • 3
    • 4
  • Javier Vázquez-Piqué
    • 1
  • Manuel Fernández-Martínez
    • 1
  1. 1.Agroforestry Sciences DepartmentUniversity of HuelvaHuelvaSpain
  2. 2.Department of BotanyUniversity of Santiago de CompostelaLugoSpain
  3. 3.Nicolaus Copernicus University, Institute for the Study, Conservation and Restoration of Cultural HeritageToruńPoland
  4. 4.Tree Ring LabUniversity of ArizonaTucsonUSA

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