Abstract
The natural expansion of forestry trees into habitats outside plantations is a concern for managers and conservationists. We studied seedling emergence and survival of the two main forestry species in Portugal: Eucalyptus globulus (exotic) and Pinus pinaster (native); using a seed addition experiment. Our main objective was to evaluate the combined effects of climate (mild-summer and warm-summer climate), habitat (oak forest and shrubland), and disturbance (vegetation removal and non-disturbance) on the seedling establishment of species in semi- and natural habitats. Furthermore, we tested the effect of the “sowing season” (autumn and spring) on seedling emergence and survival. Overall, seedling establishment of both species was enhanced by light and water. However, we found important interactions among climate, habitat, and disturbance on both species’ emergence and survival. The differences between habitats were more evident in the mild-summer climate than in the warm-summer climate. Our results also suggested that seedling survival may be enhanced by shrub cover in drier conditions (warm-summer climate). Eucalyptus globulus appears more sensitive to drought and disturbance changes than P. pinaster. In shrublands and mild-summer climate conditions, disturbance especially promoted E. globulus seedling establishment, while the forest canopy and the shade appeared to control it in both climatic conditions. After the first summer life, very low seedling survival was observed in both species, although the colonization of new areas appeared to be more limited for E. globulus. Our study suggests that climate conditions influence the effect (direction and intensity) of habitat and disturbance (plant–plant interactions) on seedling survival. Thus, the effect of light availability (forest canopy) and disturbance (vegetation removal) on these species establishment is climate context-dependent. This study presents very useful information to understand future shifts in these species distribution and has direct applications for the management of natural establishment outside the planted areas, and the management of the understorey to favor forest regeneration or limit forest colonization.
Similar content being viewed by others
References
Águas A, Ferreira A, Maia P, Fernandes PM, Roxo L, Keizer J, Silva JS, Rego FC, Moreira F (2014) Natural establishment of Eucalyptus globulus Labill. in burnt stands in Portugal. For Ecol Manag 323:47–56. doi:10.1016/j.foreco.2014.03.012
Aguiar C, Capelo J, Catry F (2007) A distribuição dos pinhais em Portugal. In: Silva JS (ed) Pinhais e eucaliptais—A floresta cultivada Colecção Árvores e Florestas de Portugal. Jornal Público, Lisbon, pp 89–104
Almeida MH, Chaves MM, Silva JC (1994) Cold acclimation in eucalypt hybrids. Tree Physiol 14:921–932. doi:10.1093/treephys/14.7-8-9.921
Alston KP, Richardson DM (2006) The roles of habitat features, disturbance, and distance from putative source populations in structuring alien plant invasions at the urban/wildland interface on the Cape Peninsula, South Africa. Biological Conservation. doi:10.1016/j.biocon.2006.03.023
Alves AM, Pereira JS, Silva JMN (2007) A introdução e a expansão do eucalipto em Portugal. In: Alves AM, Pereira JS, Silva JMN (eds) O eucaliptal em Portugal. Impactes ambientais e investigação científica. ISAPress, Lisboa, pp 13–24
Alves AM, Pereira JS, Correia AV (2012) Silvicultura – A Gestão dos Ecossistemas Florestais
Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean Basin. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 153–170
Barbier S, Gosselin F, Balandier P (2008) Influence of tree species on understory vegetation diversity and mechanisms involved—A critical review for temperate and boreal forests. For Ecol Manag 254:1–15. doi:10.1016/j.foreco.2007.09.038
Becerra PI, Bustamante RO (2011) Effect of a native tree on seedling establishment of two exotic invasive species in a semiarid ecosystem. Biol Invasions 13:2763–2773. doi:10.1007/s10530-011-9961-6
Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193. doi:10.1016/0169-5347(94)90088-4
Brundu G, Richardson DM (2016) Planted forests and invasive alien trees in Europe: a Code for managing existing and future plantings to mitigate the risk of negative impacts from invasions. NeoBiota 30:5–47. doi:10.3897/neobiota.30.7015
Callaham MA, Stanturf JA, Hammond WJ, Rockwood DL, Wenk ES, O’Brien JJ (2013) Survey to evaluate escape of eucalyptus spp. Seedlings from plantations in southeastern USA. Int J For Res. doi:10.1155/2013/946374
Calviño-Cancela M, Rubido-Bará M (2013) Invasive potential of Eucalyptus globulus: seed dispersal, seedling recruitment and survival in habitats surrounding plantations. For Ecol Manag 305:129–137. doi:10.1016/j.foreco.2013.05.037
Calvo L, Santalla S, Marcos E, Valbuena L, Tárrega R, Luis E (2003) Regeneration after wildfire in communities dominated by Pinus pinaster, an obligate seeder, and in others dominated by Quercus pyrenaica, a typical resprouter. For Ecol Manag 184:209–223. doi:10.1016/S0378-1127(03)00207-X
Castro J, Zamora R, Hodar JA, Gomez JM (2004) Seedling establishment of a boreal tree species (Pinus sylvestris) at its southernmost distribution limit: consequences of being in a marginal Mediterranean habitat. J Ecol 92:266–277. doi:10.1111/j.0022-0477.2004.00870.x
Catry FX, Moreira F, Deus E, Silva JS, Águas A (2015) Assessing the extent and the environmental drivers of Eucalyptus globulus wildling establishment in Portugal: results from a countrywide survey. Biol Invasions 17:3163–3181. doi:10.1007/s10530-015-0943-y
Cavender-Bares J, Bazzaz FA (2000) Changes in drought response strategies with ontogeny in Quercus rubra: implications for scaling from seedlings to mature trees. Oecologia 124:8–18. doi:10.1007/PL00008865
Chytrý M, Maskell LC, Pino J, Pyšek P, Vilà M, Font X, Smart SM (2008) Habitat invasions by alien plants: a quantitative comparison among Mediterranean, subcontinental and oceanic regions of Europe. J Appl Ecol 45:448–458. doi:10.1111/j.1365-2664.2007.01398.x
Correia I, Almeida H (2004) Variabilidade do Crescimento e da Forma de Proveniências de Pinus pinaster Aiton aos 8 Anos, na Mata Nacional do Escaroupim. Silva Lusitana 12:151–182
Correia MJ, Torres F, Pereira JS (1989) Water and nutrient supply regimes and the water relations of juvenile leaves of Eucalyptus globulus. Tree Physiol 5:459–471. doi:10.1093/treephys/5.4.459
da Silva PHM, Poggiani F, Sebbenn AM, Mori ES (2011) Can Eucalyptus invade native forest fragments close to commercial stands? For Ecol Manag 261:2075–2080. doi:10.1016/j.foreco.2011.03.001
Daehler CC, Denslow JS, Ansari S, Kuo H (2004) A risk-assessment system for screening out invasive pest plants from Hawaii and other Pacific islands. Conserv Biol 18:360–368. doi:10.1111/j.1523-1739.2004.00066.x
Davis MA, Pelsor M (2001) Experimental support for a resource-based mechanistic model of invasibility. Ecol Lett 4:421–428. doi:10.1046/j.1461-0248.2001.00246.x
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. doi:10.1046/j.1365-2745.2000.00473.x
Dodet M, Collet C (2012) When should exotic forest plantation tree species be considered as an invasive threat and how should we treat them? Biol Invasions 14:1765–1778. doi:10.1007/s10530-012-0202-4
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London
Essl F, Moser D, Dullinger S, Mang T, Hulme PE (2010) Selection for commercial forestry determines global patterns of alien conifer invasions. Divers Distrib 16:911–921. doi:10.1111/j.1472-4642.2010.00705.x
FAO (2015) Global Forest Resources Assessment (2015) How are the world’s forests changing?. Food and Agriculture Organization of the United Nations, Rome
Fernandes P, Antunes C, Pinho P, Máguas C, Correia O (2016) Natural regeneration of Pinus pinaster and Eucalyptus globulus from plantation into adjacent natural habitats. For Ecol Manag 378:91–102. doi:10.1016/j.foreco.2016.07.027
Figueiral I (1995) Charcoal analysis and the history of Pinus pinaster (cluster pine) in Portugal. Rev Palaeobot Palynol 89:441–454
Gassó N, Basnou C, Vilà M (2009) Predicting plant invaders in the Mediterranean through a weed risk assessment system. Biol Invasions 12:463–476. doi:10.1007/s10530-009-9451-2
Gil L, Gordo J, Catalán G, Pardos JA (1990) Pinus pinaster Aiton en el paisaje vegetal de la Península Ibérica. Ecologia 1:469–495
González-Muñoz N, Castro-Díez P, Fierro-Brunnenmeister N (2011) Establishment success of coexisting native and exotic trees under an experimental gradient of irradiance and soil moisture. Environ Manag 48:764–773. doi:10.1007/s00267-011-9731-3
Gordon DR, Flory SL, Cooper AL, Morris SK (2012) Assessing the invasion risk of Eucalyptus in the United States using the Australian weed risk assessment. Int J For Res 2012:1–7. doi:10.1155/2012/203768
Hardner CM, Potts BM (1995) Inbreeding depression and changes in variation after selfing in Eucalyptus globulus ssp. globulus. Silvae Genet 44:46–54
Higgins SI, Richardson DM (1998) Pine invasions in the southern hemisphere: modelling interactions between organism, environment and disturbance. Plant Ecol 135:79–93
Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975. doi:10.1890/0012-9658(1997)078[1966:TIOFAC]2.0.CO;2
Houle G (1996) Environmental filters and seedling recruitment on a coastal dune in subarctic Quebec (Canada). Can J Bot 74:1507–1513. doi:10.1139/b96-181
ICNF (2013) IFN6—Áreas dos usos do solo e das espécies florestais de Portugal continental. Resultados preliminares, Instituto da Conservação, da Natureza e das Florestas
IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge university press, Cambridge, UK and New York
Jacobs MR (1955) Growth habits of the Eucalypts. Forestry and Timber Bureau, Canberra
Jordan G, Potts BM, Wiltshire R (1999) Strong, independent quantitative genetic control of vegetative phase change and first flowering in Eucalyptus globulus ssp. globulus. Heredity (Edinb) 83:179–187
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? For Ecol Manag 313:329–339. doi:10.1016/j.foreco.2013.10.033
Kleinbaum GG, Klein M (2005) Survival analysis: a selp-learning text, second. Springer, New York
Larcombe MJ, Silva JS, Vaillancourt RE, Potts BM (2013) Assessing the invasive potential of Eucalyptus globulus in Australia: quantification of wildling establishment from plantations. Biol Invasions 15:2763–2781. doi:10.1007/s10530-013-0492-1
Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536. doi:10.1890/0012-9658(1999)080[1522:GPOPIA]2.0.CO;2
López M, Humara JM, Casares A, Majada J (2000) The effect of temperature and water stress on laboratory germination of Eucalyptus globulus Labill. Seeds of different sizes. Ann For Sci 57:245–250. doi:10.1051/forest:2000115
Lorentz KA, Minogue PJ (2015) Potential invasiveness for Eucalyptus species in Florida. Invasive Plant Sci Manag 8:90–97. doi:10.1614/IPSM-D-14-00030.1
Marchante H, Morais M, Freitas H, Marchante E (2014) Guia prático para a identificação de Plantas Invasoras em Portugal. Imprensa da Universidade de Coimbra, Coimbra
McAlpine KG, Jesson LK (2008) Linking seed dispersal, germination and seedling recruitment in the invasive species Berberis darwinii (Darwin’s barberry). Plant Ecol 197:119–129. doi:10.1007/s11258-007-9365-y
Mimura M, Barbour RC, Potts BM, Vaillancourt RE, Watanabe KN (2009) Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests. Mol Ecol 18:4180–4192. doi:10.1111/j.1365-294X.2009.04350.x
Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740. doi:10.1111/j.1461-0248.2006.00908.x
Niinemets Ü, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs. Ecol Monogr 76:521–547. doi:10.1890/0012-9615(2006)076[0521:TTSDAW]2.0.CO;2
Pheloung PC, Williams PA, Halloy SR (1999) A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. J Environ Manag 57:239–251. doi:10.1006/jema.1999.0297
Porte A, Loustau D (1998) Variability of the photosynthetic characteristics of mature needles within the crown of a 25-year-old Pinus pinaster. Tree Physiol 18:223–232. doi:10.1093/treephys/18.4.223
Prider JN, Facelli JM (2004) Interactive effects of drought and shade on three arid zone chenopod shrubs with contrasting distributions in relation to tree canopies. Funct Ecol 18:67–76. doi:10.1046/j.0269-8463.2004.00810.x
Procheş Ş, Wilson JRU, Richardson DM, Rejmánek M (2012) Native and naturalized range size in Pinus: relative importance of biogeography, introduction effort and species traits. Glob Ecol Biogeogr 21:513–523. doi:10.1111/j.1466-8238.2011.00703.x
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Springer-Verlag, Berlin, pp 97–125
Quezel P (1977) Forests of the Mediterranean basin. Mediterranean forests and maquis: ecology, conservation and management. UNESCO, Paris, pp 9–33
Rejmánek M, Richardson DM (2011) Eucalypts. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, pp 203–209
Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species - 2013 update of the global database. Divers Distrib 19:1093–1094. doi:10.1111/ddi.12075
Rejmánek M, Richardson DM, Pyšek P (2005) Plant invasions and invasibility of plant communities. In: Van der Maarel E (ed) Vegetation ecology. Blackwell, Oxford, pp 332–355
Reyes O, Casal M (1997) Germination of Pinus pinaster, P. radiata and Eucalyptus globulus in relation to the amount of ash produced in forest fires
Reyes O, Casal M (2001) The influence of seed age on germinative response to the effects of fire in Pinus pinaster, Pinus radiata and Eucalyptus globulus. Ann For Sci 58:439–447. doi:10.1051/forest:2001137
Richardson DM (1998) Forestry trees as invasive aliens. Conserv Biol 12:18–26. doi:10.1111/j.1523-1739.1998.96392.x
Richardson DM (2011) Forestry and Agroforestry. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, pp 241–248
Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr 30:409–431. doi:10.1191/0309133306pp490pr
Richardson DM, Rejmánek M (2004) Conifers as invasive aliens: a global survey and predictive framework. Divers Distrib 10:321–331. doi:10.1111/j.1366-9516.2004.00096.x
Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species - a global review. Divers Distrib 17:788–809. doi:10.1111/j.1472-4642.2011.00782.x
Richardson DM, Williams PA, Hobbs RJ (1994) Pine invasions in the southern hemisphere: determinants of spread and invadability. J Biogeogr 21:511. doi:10.2307/2845655
Richardson DM, Hui C, Nuñez MA, Pauchard A (2014) Tree invasions: patterns, processes, challenges and opportunities. Biol Invasions 16:473–481. doi:10.1007/s10530-013-0606-9
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. doi:10.1016/j.foreco.2013.06.046
Rodríguez-García E, Juez L, Guerra B, Bravo F (2007) Análisis de la regeneración natural de Pinus pinaster Ait. en los arenales de Almazán-Bayubas (Soria, España). Investig Agrar Sist y Recur For 16(1):25–38
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. doi:10.1007/s10342-010-0399-7
Rodríguez-García E, Bravo F, Spies TA (2011a) Effects of overstorey canopy, plant–plant interactions and soil properties on Mediterranean maritime pine seedling dynamics. For Ecol Manag 262:244–251. doi:10.1016/j.foreco.2011.03.029
Rodríguez-García E, Gratzer G, Bravo F (2011b) Climatic variability and other site factor influences on natural regeneration of Pinus pinaster Ait. In Mediterranean forests. Ann For Sci 68:811–823. doi:10.1007/s13595-011-0078-y
Rodríguez-García E, Ordóñez C, Bravo F (2011c) Effects of shrub and canopy cover on the relative growth rate of Pinus pinaster Ait. Seedlings of different sizes. Ann For Sci 68:337–346. doi:10.1007/s13595-011-0039-5
Ruano I, Pando V, Bravo F (2009) How do light and water influence Pinus pinaster Ait. Germination and early seedling development? For Ecol Manag 258:2647–2653. doi:10.1016/j.foreco.2009.09.027
Sabaté S, Gracia CA, Sánchez A (2002) Likely effects of climate change on growth of Quercus ilex, Pinus halepensis, Pinus pinaster, Pinus sylvestris and Fagus sylvatica forests in the Mediterranean region. For Ecol Manag 162:23–37. doi:10.1016/S0378-1127(02)00048-8
Sánchez-Gómez D, Valladares F, Zavala MA (2006a) Functional traits and plasticity in response to light in seedlings of four Iberian forest tree species. Tree Physiol 26:1425–1433
Sánchez-Gómez D, Zavala MA, Valladares F (2006b) Seedling survival responses to irradiance are differentially influenced by low-water availability in four tree species of the Iberian cool temperate–Mediterranean ecotone. Acta Oecol 30:322–332. doi:10.1016/j.actao.2006.05.005
Schwanz P, Polle A (2001) Differential stress responses of antioxidative systems to drought in pendunculate oak (Quercus robur) and maritime pine (Pinus pinaster) grown under high CO2 concentrations. J Exp Bot 52:133–143. doi:10.1093/jexbot/52.354.133
Silva FC, Shvaleva A, Maroco JP, Almeida MH, Chaves MM, Pereira JS (2004) Responses to water stress in two Eucalyptus globulus clones differing in drought tolerance. Tree Physiol 24:1165–1172. doi:10.1093/treephys/24.10.1165
Stoneman GL (1994) Ecology and physiology of establishment of eucalypt seedlings from seed: a review. Aust For 57:11–29
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. doi:10.1046/j.1365-2745.2001.00575.x
Wassie A, Sterck FJ, Teketay D, Bongers F (2009) Effects of livestock exclusion on tree regeneration in church forests of Ethiopia. For Ecol Manag 257:765–772. doi:10.1016/j.foreco.2008.07.032
Zar JH (1999) Biostatistical analysis. Prentice-Hall Inc, New Jersey
Acknowledgements
This research was funded by Fundação para a Ciência e Tecnologia (FCT) and the Navigator company in the frame of Patrícia Fernandes PhD scholarship from FCT (SFRH/BDE/51709/2011). The authors are grateful to RAIZ—Instituto de Investigação da Floresta e Papel—for logistical support and allowing the establishment of our field sites. Namely, we would like to thank: Alexandre, Carlos Valente and Sofia Corticeiro. We also express our gratitude to all colleagues who helped to perform field work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Sandor Bartha.
Rights and permissions
About this article
Cite this article
Fernandes, P., Máguas, C. & Correia, O. Combined effects of climate, habitat, and disturbance on seedling establishment of Pinus pinaster and Eucalyptus globulus . Plant Ecol 218, 501–515 (2017). https://doi.org/10.1007/s11258-017-0706-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-017-0706-1