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Plant Ecology

, Volume 220, Issue 11, pp 1057–1069 | Cite as

Germination response of woody species to laboratory-simulated fire severity and airborne nitrogen deposition: a post-fire recovery strategy perspective

  • Luz ValbuenaEmail author
  • Angela Taboada
  • Reyes Tárrega
  • Ainhoa De la Rosa
  • Leonor Calvo
Article

Abstract

Two drivers of global change that affect ecosystem function include wildland fire regimes characterised by frequent, severe fires and increased atmospheric nitrogen (N) deposition. However, their combined effect on the post-fire recovery of Mediterranean forests is still little known. We assessed the interactive effects of two fire severities and N addition on the rate and timing of seed germination of three woody species with different post-fire regeneration strategies in fire-prone forests: Pinus pinaster, an obligate-seeder species, and two facultative-seeder species, Pterospartum tridentatum (high-resprouting and low-seeding ability) and Halimium lasianthum (low-resprouting and high-seeding ability). Seeds were subjected to six combinations of temperature [control (no heat treatment), 60 °C (moderate fire severity) and 120 °C (high fire severity) for 5 min] and N fertilisation (without N and with addition of 4.17 g Nm−2 of solid granules of ammonium nitrate, equivalent to three times the current estimate of airborne N deposition in the study area) under laboratory conditions. We found that N fertilisation had a significant, negative effect on the rate of seed germination of the three species under study. Additionally, we detected no differences in P. pinaster germination among thermal treatments; while both P. tridentatum and H. lasianthum had significantly higher germination rates when submitted to high fire-severity conditions. Moreover, the average time of seed germination increased with N fertilisation for P. pinaster but increased after the thermal treatments for H. lasianthum. These results suggest that increased N availability under intense wildfire regimes may hinder post-fire seed germination, regardless of the species’ regeneration strategy, in fire-prone pine forests.

Keywords

Atmospheric nitrogen deposition Germination Halimium lasianthum Pinus pinaster Pterospartum tridentatum 

Notes

Acknowledgements

We thank the Environmental Department of the Regional Government of Castilla y León for the information provided.

Funding

This work was supported by the Spanish Ministry of Economy and Competitiveness, and the European Regional Development Fund (GESFIRE Project, AGL2013-48189-C2-1-R; FIRESEVES Project, AGL2017-86075-C2-1-R); and the Regional Government of Castilla and León (FIRECYL Project, LE033U14; SEFIRECYL Project, LE001P17).

References

  1. Alexander ME, Cruz MG (2012) Modelling the effects of surface and crown fire behaviour on serotinous cone opening in jack pine and lodgepole pine forests. Int J Wildland Fire 21:709–721.  https://doi.org/10.1071/WF11153 CrossRefGoogle Scholar
  2. Álvarez R, Valbuena L, Calvo L (2005) Influence of tree age on seed germination response to environmental factors and inhibitory substances in Pinus pinaster. Int J Wildland Fire 14:277–284.  https://doi.org/10.1071/WF04066 CrossRefGoogle Scholar
  3. Álvarez R, Valbuena L, Calvo L (2007) Effect of high temperatures on seed germination and seedling survival in three pine species (Pinus pinaster, P. sylvestris and P. nigra). Int J Wildland Fire 16:63–70.  https://doi.org/10.1071/WF06001 CrossRefGoogle Scholar
  4. Baeza MJ, Valdecantos A, Alloza JA, Vallejo VR (2007) Human disturbance and environmental factors as drivers of long-term post-fire regeneration patterns in Mediterranean forests. J Veg Sci 18:243–252.  https://doi.org/10.1111/j.1654-1103.2007.tb02535.x CrossRefGoogle Scholar
  5. Baskin CC, Baskin JM (2001) Seeds, ecology, biogeography, and evolution of dormancy and germination. Academic Press, New YorkGoogle Scholar
  6. Bell DT (2001) Ecological response syndromes in the Flora of southwestern western Australia: fire resprouters versus reseeders. Bot Rev 67:417–440CrossRefGoogle Scholar
  7. Bell DT, King LA, Plummer JA (1999) Ecophysiological effects of light quality and nitrate on seed germination in species from Western Australia. Aust J Ecol 24:2–10.  https://doi.org/10.1046/j.1442-9993.1999.00940.x CrossRefGoogle Scholar
  8. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59.  https://doi.org/10.1890/08-1140.1 CrossRefGoogle Scholar
  9. Britton AJ, Fisher JM (2007) Interactive effects of nitrogen deposition, fire and grazing on diversity and composition of low-alpine prostrate Calluna vulgaris heathland. J Appl Ecol 44:125–135.  https://doi.org/10.1111/j.1365-2664.2006.01251.x CrossRefGoogle Scholar
  10. Calvo L, Baeza J, Marcos E, Santana V, Papanastasis VP (2012) Post-fire management of shrublands. In: Moreira F, Arianoutsou M, Corona P, De las Heras J (eds), Post-fire management and restoration of southern European forests, managing forest ecosystems 24. Springer, Berlin, pp 293–319Google Scholar
  11. Calvo L, Hernández V, Valbuena L, Taboada A (2016) Provenance and seed mass determine seed tolerance to high temperatures associated to forest fires in Pinus pinaster. Ann For Sci 73:381–391.  https://doi.org/10.1007/s13595-015-0527-0 CrossRefGoogle Scholar
  12. Calvo L, Santalla S, Valbuena L, Marcos E, Tárrega R, Luis-Calabuig E (2008) Post-fire natural regeneration of a Pinus pinaster forest in NW Spain. Plant Ecol 197:81–90.  https://doi.org/10.1007/s11258-007-9362-1 CrossRefGoogle Scholar
  13. Calvo L, Torres O, Valbuena L, Luis-Calabuig E (2013) Recruitment and early growth of Pinus pinaster seedlings over five years after a wildfire in NW Spain. For Syst 22:582–586.  https://doi.org/10.5424/fs/2013223-04623 CrossRefGoogle Scholar
  14. Calvo-Fernández J, Taboada A, Fichtner A, Härdtle W, Calvo L, Marcos E (2018) Time- and age-related effects of experimentally simulated nitrogen deposition on the functioning of montane heathland ecosystems. Sci Total Environ 613–614:149–159.  https://doi.org/10.1016/j.scitotenv.2017.08.307 CrossRefPubMedGoogle Scholar
  15. Clarke PJ, Knox KJE, Wills KW, Campbell M (2005) Landscape patterns of woody plant response to crown fire: disturbance and productivity influence sprouting ability. J Ecol 93:544–555.  https://doi.org/10.1111/j.1365-2745.2005.00971.x CrossRefGoogle Scholar
  16. Côme D (1970) Les obstacles à la germination. Mason, ParisGoogle Scholar
  17. De las Heras J, Moya D, Vega JA, Daskalakou E, Vallejo R, Grigoriadis N, Tsitsoni T, Baeza J, Valdecantos A, Fernández C, Espelta J, Fernandes P (2012) Post-fire management of serotinous pine forests. In: Moreira F, Arianoutsou M, Corona P, De las Heras J (eds), Post-fire management and restoration of southern european forests, managing forest ecosystems 24. Springer, Berlin, pp 121–150Google Scholar
  18. Doblas-Miranda E, Alonso R, Arnan X, Bermejo V, Brotons L, De las Heras J, Estiarte M, Hódar JA, Llorens P, López-Serrano FR, Lloret F, Martínez-Vilalta J, Moya D, Peñuelas J, Pino J, Rodrigo A, Roura-Pascual N, Valladares F, Vilà M, Zamora R, Retana J (2017) A review of the combination among global change factors in forests, shrublands and pastures of the Mediterranean region: beyond drought effects. Glob Planet Chang 148:42–54.  https://doi.org/10.1016/j.gloplacha.2016.11.012 CrossRefGoogle Scholar
  19. Escudero A, Núñez Y, Pérez-García F (2000) Is fire a selective force of seed size in pine species? Acta Oecol 21:245–256.  https://doi.org/10.1016/S1146-609X(00)01083-3 CrossRefGoogle Scholar
  20. Escudero A, Sanz MV, Pita JM, Pérez-García F (1999) Probability of germination after heat treatment of native Spanish pines. Ann For Sci 56:511–520.  https://doi.org/10.1051/forest:19990608 CrossRefGoogle Scholar
  21. European Monitoring and Evaluation Programme (EMEP) (2016) Gridded emissions in Google Earth. https://www.ceip.at/ms/ceip_home1/ceip_home/webdab_emepdatabase/gridded_data/. Accessed November 2016
  22. Fernandes PM, Rigolot E (2007) The fire ecology and management of maritime pine (Pinus pinaster Ait.). For Ecol Manag 241:1–13.  https://doi.org/10.1016/j.foreco.2007.01.010 CrossRefGoogle Scholar
  23. Fernández C, Vega JA, Fonturbel T, Jiménez E, Pérez-Gorostiaga P (2008) Effects of wildfire, salvage logging and slash manipulation on Pinus pinaster Ait. recruitment in Orense (NW Spain). For Ecol Manag 255:1294–1304.  https://doi.org/10.1016/j.foreco.2007.10.034 CrossRefGoogle Scholar
  24. Fernández-García V, Marcos E, Fernández-Guisuraga JM, Taboada A, Suárez-Seoane S, Calvo L (2019a) Impact of burn severity on soil properties in a Pinus pinaster ecosystem immediately after fire. Int J Wildland Fire 28:354–364.  https://doi.org/10.1071/WF18103 CrossRefGoogle Scholar
  25. Fernández-García V, Miesel J, Baeza MJ, Marcos E, Calvo L (2019b) Wildfire effects on soil properties in fire-prone pine ecosystems: indicators of burn severity legacy over the medium term after fire. Appl Soil Ecol 135:147–156.  https://doi.org/10.1016/j.apsoil.2018.12.002 CrossRefGoogle Scholar
  26. Fernández-García V, Quintano C, Taboada A, Marcos E, Calvo L, Fernández-Manso A (2018) Remote sensing applied to the study of fire regime attributes and their influence on post-fire greenness recovery in pine ecosystems. Remote Sens 10:733.  https://doi.org/10.3390/rs10050733 CrossRefGoogle Scholar
  27. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vörösmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:312–318.  https://doi.org/10.1007/s10533-004-0370-0 CrossRefGoogle Scholar
  28. García-Gómez H, Garrido JL, Vivanco MG, Lassaletta L, Rábago I, Ávila A, Tsyro S, Sánchez G, González Ortiz A, González-Fernández I, Alonso R (2014) Nitrogen deposition in Spain: modeled patterns and threatened habitats within the Natura 2000 network. Sci Total Environ 485–486:450–460.  https://doi.org/10.1016/j.scitotenv.2014.03.112 CrossRefPubMedGoogle Scholar
  29. Gil L, López R, García-Mateos Á, González-Doncel I (2009) Seed provenance and fire-related reproductive traits of Pinus pinaster in central Spain. Int J Wildland Fire 18:1003–1009.  https://doi.org/10.1071/WF08101 CrossRefGoogle Scholar
  30. González-DeVega S, De las Heras J, Moya D (2016) Resilience of Mediterranean terrestrial ecosystems and fire severity in semiarid areas: responses of Aleppo pine forests in the short, mid and long term. Sci Total Environ 573:1171–1177.  https://doi.org/10.1016/j.scitotenv.2016.03.115 CrossRefGoogle Scholar
  31. Green ER, Ellis RJ, Gadsdon SRM, Milcu A, Power SA (2013) How does N deposition affect belowground heathland recovery following wildfire? Soil Biol Biochem 57:775–783.  https://doi.org/10.1016/j.soilbio.2012.08.025 CrossRefGoogle Scholar
  32. Henig-Sever N, Eshel A, Ne’eman G, (2000) Regulation of the germination of Aleppo pine (Pinus halepensis) by nitrate, ammonium, and gibberellin, and its role in post-fire forest regeneration. Physiol Plant 108:390–397.  https://doi.org/10.1034/j.1399-3054.2000.t01-1-100408.x CrossRefGoogle Scholar
  33. Hernández-Serrano A, Verdú M, González-Martínez SC, Pausas JG (2013) Fire structures pine serotiny at different scales. Am J Bot 100:2349–2356.  https://doi.org/10.3732/ajb.1300182 CrossRefPubMedGoogle Scholar
  34. Herranz JM, Ferrandis P, Martínez-Sánchez JJ (1999) Influence of heat on seed germination of nine woody Cistaceae species. Int J Wildland Fire 9:173–182.  https://doi.org/10.1071/WF00014 CrossRefGoogle Scholar
  35. Jaganathan GK (2015) Are wildfires an adapted ecological cue breaking physical dormancy in the Mediterranean basin? Seed Sci Res 25(2):120–126.  https://doi.org/10.1017/S0960258514000439 CrossRefGoogle Scholar
  36. Jones L, Provins A, Holland M, Mills G, Hayes F, Emmett B, Hall J, Sheppard L, Smith R, Sutton M, Hicks K, Ashmore M, Haines-Young R, Harper-Simmonds L (2014) A review and application of the evidence for nitrogen impacts on ecosystem services. Ecosyst Serv 7:76–88.  https://doi.org/10.1016/j.ecoser.2013.09.001 CrossRefGoogle Scholar
  37. Keeley JE (2009) Fire intensity, fire severity and burn severity: a brief review and suggested usage. Int J Wildland Fire 18:116–126.  https://doi.org/10.1071/WF07049 CrossRefGoogle Scholar
  38. Keeley JE, Pausas JG (2018) Evolution of ‘smoke’ induced seed germination in pyroendemic plants. S Afr J Bot 115:251–255.  https://doi.org/10.1016/j.sajb.2016.07.012 CrossRefGoogle Scholar
  39. Key CH, Benson NC (2006) Landscape assessment (LA) sampling and analysis methods, USDA Forest Service general technical report, RMRS-GTR-164-CDGoogle Scholar
  40. Knox KJE, Clarke PJ (2005) Nutrient availability induces contrasting allocation and starch formation in resprouting and obligate seeding shrubs. Funct Ecol 19:690–698.  https://doi.org/10.1111/j.1365-2435.2005.01006.x CrossRefGoogle Scholar
  41. Li Y, Yang H, Xia J, Zhang W, Wan S, Li L (2011) Effects of increased nitrogen deposition and precipitation on seed and seedling production of Potentilla tanacetifolia in a temperate steppe ecosystem. PLoS ONE 6(12):e28601.  https://doi.org/10.1371/journal.pone.0028601 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Luis-Calabuig E, Torres O, Valbuena L, Calvo L, Marcos E (2002) Impact of large fires on a community of Pinus pinaster. In: Trabaud L, Prodon R (eds) Fire and biological processes. Backhuys, Leiden, pp 1–12Google Scholar
  43. Luna B, Moreno JM (2009) Light and nitrate effects on seed germination of Mediterranean plant species of several functional groups. Plant Ecol 203:123–135.  https://doi.org/10.1007/s11258-008-9517-8 CrossRefGoogle Scholar
  44. Marcos E, Fernández-García V, Fernández-Manso A, Quintano C, Valbuena L, Tárrega R, Luis-Calabuig E, Calvo L (2018) Evaluation of composite burn index and land Surface temperature for assessing soil burn severity in Mediterranean fire-prone pine ecosystems. Forests 9:494.  https://doi.org/10.3390/f9080494 CrossRefGoogle Scholar
  45. Marcos E, Villalón C, Calvo L, Luis-Calabuig E (2009) Short-term effects of experimental burning on soil nutrients in the Cantabrian heathlands. Ecol Eng 35:820–828.  https://doi.org/10.1016/j.ecoleng.2008.12.011 CrossRefGoogle Scholar
  46. Martínez-Sánchez JJ, Marín A, Herranz JM, Ferrandis P, De las Heras J (1995) Effects of high temperatures on germination of Pinus halepensis Mill. and P. pinaster Aiton subsp. pinaster seeds in southeast Spain. Vegetatio 116:69–72.  https://doi.org/10.1007/BF00045279 CrossRefGoogle Scholar
  47. Mayor AG, Valdecantos A, Vallejo VR, Keizer JJ, Bloem J, Baeza J, González-Pelayo O, Machado AI, de Ruiter PC (2016) Fire-induced pine woodland to shrubland transitions in Southern Europe may promote shifts in soil fertility. Sci Total Environ 573:1232–1241.  https://doi.org/10.1016/j.scitotenv.2016.03.243 CrossRefPubMedGoogle Scholar
  48. Moreira B, Pausas JG (2018) Shedding light through the smoke on the germination of Mediterranean Basin flora. S Afr J Bot 115:244–250.  https://doi.org/10.1016/j.sajb.2016.10.008 CrossRefGoogle Scholar
  49. Moreira B, Tormo J, Estrelles E, Pausas JG (2010) Disentangling the role of heat and smoke as germination cues in Mediterranean Basin flora. Ann Bot 105:627–635.  https://doi.org/10.1093/aob/mcq017 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Moreira F, Viedma O, Arianoutsou M, Curt T, Koutsias N, Rigolot E, Barbati A, Corona P, Vaz P, Xanthopoulos G, Mouillot F, Bilgili E (2011) Landscape: wildfire interactions in southern Europe: implications for landscape management. J Environ Manag 92:2389–2402.  https://doi.org/10.1016/j.jenvman.2011.06.028 CrossRefGoogle Scholar
  51. Moya D, De las Heras J, Lopez-Serrano FR, Ferrandis R (2015) Post-fire seedling recruitment and morpho-ecophysiological responses to induced drought and salvage logging in Pinus halepensis Mill. stands. Forests 6:1858–1877.  https://doi.org/10.3390/f6061858 CrossRefGoogle Scholar
  52. Moya D, De las Heras J, Salvatore R, Valero E, Leone V (2013) Fire intensity and serotiny: response of germination and enzymatic activity in seeds of Pinus halepensis Mill from southern Italy. Ann For Sci 70:49–59.  https://doi.org/10.1007/s13595-012-0236-x CrossRefGoogle Scholar
  53. Moya D, Saracino A, Salvatore R, Lovreglio R, De las Heras J, Leone V (2008) Anatomic basis and insulation of serotinous cones in Pinus halepensis Mill. Trees 22:511–519.  https://doi.org/10.1071/BT10193 CrossRefGoogle Scholar
  54. Núñez MR, Bravo F, Calvo L (2003) Predicting the probability of seed germination in Pinus sylvestris L. and four competitor shrub species after fire. Ann For Sci 60:75–81.  https://doi.org/10.1051/forest:2002076 CrossRefGoogle Scholar
  55. Ochoa-Hueso R, Allen EB, Branquinho C, Cruz C, Dias T, Fenn ME, Manrique E, Pérez-Corona ME, Sheppard LJ, Stock WD (2011) Nitrogen deposition effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut 159:2265–2279.  https://doi.org/10.1016/j.envpol.2010.12.019 CrossRefPubMedGoogle Scholar
  56. Ochoa-Hueso R, Bell MD, Manrique E (2014) Impacts of increased nitrogen deposition and altered precipitation regimes on soil fertility and functioning in semiarid Mediterranean shrublands. J Arid Environ 104:106–115.  https://doi.org/10.1016/j.jaridenv.2014.01.020 CrossRefGoogle Scholar
  57. Ochoa-Hueso R, Stevens CJ, Ortiz-Llorente MJ, Manrique E (2013) Soil chemistry and fertility alterations in response to N application in a semiarid Mediterranean shrubland. Sci Total Environ 452–453:78–86.  https://doi.org/10.1016/j.scitotenv.2013.02.049 CrossRefPubMedGoogle Scholar
  58. Paula S, Pausas JG (2008) Burning seeds: germinative response to heat treatments in relation to resprouting ability. J Ecol 96:543–552. https://doi.org/10.1111/j.1365-2745.2008.01359x CrossRefGoogle Scholar
  59. Pausas JG, Keeley JE (2014) Evolutionary ecology of resprouting and seeding in fire-prone ecosystems. New Phytol 204:55–65.  https://doi.org/10.1111/nph.12921 CrossRefPubMedGoogle Scholar
  60. Pausas JG, Llovet J, Rodrigo A, Vallejo R (2008) Are wildfires a disaster in the Mediterranean basin? A review. Int J Wildland Fire 17:713–723.  https://doi.org/10.1071/WF07151 CrossRefGoogle Scholar
  61. Pausas JG, Paula S (2012) Fuel shapes the fire-climate relationship: evidence from Mediterranean ecosystems. Glob Ecol Biogeogr 21:1074–1082.  https://doi.org/10.1111/j.1466-8238.2012.00769.x CrossRefGoogle Scholar
  62. Pausas JG, Vallejo VR (1999) The role of fire in European Mediterranean ecosystems. In: Chuvieco E (ed) Remote sensing of large wildfires in the European Mediterranean Basin. Springer, Berlin, pp 3–16CrossRefGoogle Scholar
  63. Pérez-Fernández MA, Rodríguez-Echeverría S (2003) Effect of smoke, charred wood, and nitrogenous compounds on seed germination of ten species from woodland in central-western Spain. J Chem Ecol 29:237–251.  https://doi.org/10.1023/A:1021997118146 CrossRefPubMedGoogle Scholar
  64. Quintano C, Fernández-Manso A, Calvo L, Marcos E, Valbuena L (2015) Land surface temperature as potential indicator of burn severity in forest Mediterranean ecosystems. Int J Appl Earth Obs 36:1–12.  https://doi.org/10.1016/j.jag.2014.10.015 CrossRefGoogle Scholar
  65. Quintano C, Fernández-Manso A, Roberts DA (2017) Burn severity mapping from Landsat MESMA fraction images and land surface temperature. Remote Sens Environ 190:83–95.  https://doi.org/10.1016/j.rse.2016.12.009 CrossRefGoogle Scholar
  66. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  67. Reyes O, Casal M (2001) The influence of seed age on germinative response to the effects of fire in Pinus pinaster, P. radiata and Eucalyptus globulus. Ann For Sci 58:439–447.  https://doi.org/10.1051/forest:2001137 CrossRefGoogle Scholar
  68. Reyes O, Casal M (2002) Effect of high temperatures on cone opening and on the release and viability of Pinus pinaster and P. radiata seeds in NW Spain. Ann For Sci 59:327–334.  https://doi.org/10.1051/forest:2001137 CrossRefGoogle Scholar
  69. Reyes O, Casal M (2008) Regeneration models and plant regenerative types related to the intensity of fire in Atlantic shrubland and woodland species. J Veg Sci 19:575–583.  https://doi.org/10.3170/2008-8-18412 CrossRefGoogle Scholar
  70. Reyes O, Casal M, Castro Rego F (2009) Resprouting ability of six Atlantic shrub species. Folia Geobot 44:19–29.  https://doi.org/10.1007/s12224-009-9029-x CrossRefGoogle Scholar
  71. Rivas M (2016) Estrategia germinativa de especies de matorral atlántico en relación con incendios forestales. PhD thesis, University of Santiago de Compostela, SpainGoogle Scholar
  72. Rivas M, Reyes O, Casal M (2006) Influence of heat and smoke treatments on the germination of six leguminous shrubby species. Int J Wildland Fire 15:73–80.  https://doi.org/10.1071/WF05008 CrossRefGoogle Scholar
  73. Rodríguez-García E, Bravo F (2013) Plasticity in Pinus pinaster populations of diverse origins: Comparative seedling responses to light and nitrogen availability. For Ecol Manag 307:196–205.  https://doi.org/10.1016/j.foreco.2013.06.046 CrossRefGoogle Scholar
  74. Rodríguez-García E, Juez L, Bravo F (2010) Environmental influences on post-harvest natural regeneration of Pinus pinaster Ait. in Mediterranean forest stands submitted to the seed-tree selection method. Eur J For Res 129:1119–1128.  https://doi.org/10.1007/s10342-010-0399-7 CrossRefGoogle Scholar
  75. Salvatore R, Moya D, Pulido L, Lovreglio R, López-Serrano FR, De las Heras J, Leone V (2010) Morphological and anatomical differences in Aleppo pine seeds from serotinous and non-serotinous cones. New For 39:329–341.  https://doi.org/10.1007/s11056-009-9174-3 CrossRefGoogle Scholar
  76. San-Miguel-Ayanz J, Moreno JM, Camia A (2013) Analysis of large fires in European Mediterranean landscapes: lessons learned and perspectives. For Ecol Manag 294:11–22.  https://doi.org/10.1016/j.foreco.2012.10.050 CrossRefGoogle Scholar
  77. Santamaría JE (2015) El pino pinaster de la Sierra del Teleno. Historia, ordenación, crecimiento y producción. PhD thesis, University of Léon, SpainGoogle Scholar
  78. Saracino A, Pacella R, Leone V, Borghetti M (1997) Seed dispersal and changing seed characteristics in a Pinus halepensis Mill. forest after fire. Plant Ecol 130:13–19.  https://doi.org/10.1023/A:1009765129920 CrossRefGoogle Scholar
  79. Serrasolses I, Vallejo VR (1999) Soil fertility after fire and clear-cutting. In: Rodà F, Retana J, Gracia CA, Bellot J (eds) Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, 137. Springer, Berlin. pp 315–328. https://doi.org/10.1007/978-3-642-58618-7_22 Google Scholar
  80. Southon GE, Green ER, Jones AG, Barker CG, Power SA (2012) Long-term nitrogen additions increase likelihood of climate stress and affect recovery from wildfire in a lowland heath. Glob Change Biol 18:2824–2837.  https://doi.org/10.1111/j.1365-2486.2012.02732.x CrossRefGoogle Scholar
  81. Taboada A, Calvo-Fernández J, Marcos E, Calvo L (2018) Plant and vegetation functional responses to cumulative high nitrogen deposition in rear-edge heathlands. Sci Total Environ 637–638:980–990.  https://doi.org/10.1016/j.scitotenv.2018.05.092 CrossRefPubMedGoogle Scholar
  82. Taboada A, Tárrega R, Marcos E, Valbuena L, Suárez-Seoane S, Calvo L (2017) Fire recurrence and emergency post-fire management influence seedling recruitment and growth by altering plant interactions in fire-prone ecosystems. For Ecol Manag 402:63–75.  https://doi.org/10.1016/j.foreco.2017.07.029 CrossRefGoogle Scholar
  83. 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 CrossRefGoogle Scholar
  84. Tapias R, Gil L, Fuentes-Utrilla P, Pardos JA (2001) Canopy seed banks in Mediterranean pines of south-eastern Spain: a comparison between Pinus halepensis Mill., P. pinaster Ait., P. nigra Arn. and P. pinea L. J Ecol 89:629–638.  https://doi.org/10.1046/j.1365-2745.2001.00575.x CrossRefGoogle Scholar
  85. Thanos CA, Rundel PW (1995) Fire-followers in chaparral: nitrogenous compounds trigger seed germination. J Ecol 83:207–216.  https://doi.org/10.2307/2261559 CrossRefGoogle Scholar
  86. Torres O, Calvo L, Valbuena L (2006) Influence of high temperatures on seed germination of a special Pinus pinaster stand adapted to frequent fires. Plant Ecol 186:129–136.  https://doi.org/10.1007/s11258-006-9117-4 CrossRefGoogle Scholar
  87. Trabaud L, Casal M (1989) Réponses des semences de Rosmarinus officinalis à différents traitements simulant une action de feu. Acta Oecol Oecol Appl 10:355–363Google Scholar
  88. Trabaud L, Oustric J (1989) Influence du feu sur la germination des semences de quatre espèces ligneuses méditerranéennes à reproduction sexuée obligatoire. Seed Sci Technol 17:589–599Google Scholar
  89. Turner MG (2010) Disturbance and landscape dynamics in a changing world. Ecology 91:2833–2849.  https://doi.org/10.1890/10-0097.1 CrossRefPubMedGoogle Scholar
  90. Valbuena L (1995) El banco de semillas del suelo y su papel en la recuperación de comunidades incendiadas. PhD thesis, University of León, SpainGoogle Scholar
  91. Valbuena L, Luis-Calabuig E, Tárrega R (2002) Relationship between thermal shock and germination in five Mediterranean shrubs. In: Trabaud L, Prodon R (eds) Fire and biological processes. Backhuys, Leiden, pp 93–98Google Scholar
  92. Valbuena L, Tárrega R, Luis E (1992) Influence of heat on seed germination of Cistus laurifolius and Cistus ladanifer. Int J Widland Fire 2:15–20.  https://doi.org/10.1071/WF9920015 CrossRefGoogle Scholar
  93. Valbuena L, Vera ML (2002) The effects of thermal scarification and seed storage on germination of four heathland species. Plant Ecol 161:137–144.  https://doi.org/10.1023/A:1020387819222 CrossRefGoogle Scholar
  94. Vasques A, Maia P, Pedro M, Santos C, Vallejo VR, Keizer JJ (2012) Germination in five shrub species of Maritime Pine understory—does seed provenance matter? Ann For Sci 69:499–507.  https://doi.org/10.1007/s13595-012-0206-3 CrossRefGoogle Scholar
  95. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  96. Vourlitis GL, Pasquini SC (2009) Experimental dry-season N deposition alters species composition in southern Californian mediterranean-type shrublands. Ecology 90:2183–2189.  https://doi.org/10.1890/08-1121.1 CrossRefPubMedGoogle Scholar
  97. Zhang Y, Zhou Z, Yang Q (2013) Nitrogen (N) deposition impacts seedling growth of Pinus massoniana via N: P ration effects and the modulation of adaptive responses to low P (phosphorus). PLoS ONE 8(10):e79229.  https://doi.org/10.1371/journal.pone.0079229 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Area of Ecology, Department of Biodiversity and Environmental ManagementUniversity of LeónLeónSpain

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