Abstract
Natural regeneration is a critical step for the dispersal of alien plants and the establishment of new invasive foci. The adequate timing and location of germination, as well as the survival of the seedlings, have direct effects on the recruitment of the population, and are expected to depend on habitat characteristics. Understanding the dynamics of these processes, and their variations according to the landscape at different scales, can be particularly important to design and implement control strategies. In this article, we evaluate differences in seedling emergence and establishment of Pinus halepensis in highland grasslands of the Argentine pampas, according to altitude, orientation of the slope and vegetation cover. Our results showed spatial variation on the rate of seedling emergence, with topography as a determining factor, possibly due to a facilitating effect on the slopes with higher incident solar radiation (NE at the study site). Slope exposition, on the contrary, seemed to have the opposite effect on the survival of seedlings. Once established, seedlings also survived better in sites with less solar exposure, probably due to protection from high evapotranspiration during the summer. These results could explain variations in the invasive performance of the species and guide management actions aimed at preventing its further expansion in the study area and in other habitats with similar characteristics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability statement
The data sets generated and/or analysed during the current study will be available in the Zenodo repository [https://doi.org/10.5281/zenodo.4282914].
References
Alexander ME, Dick J, Weyl O, Robinson TB, Richardson DM (2014) Existing and emerging high impact invasive species are characterized by higher functional responses than natives. Biol Let 10:20130946. https://doi.org/10.1098/rsbl.2013.0946
Amiotti N, Bravo O, Zalba P, Peinemann N (2007) Effect of landscape position on the acidification of loess-derived soils under Pinus radiata. Austral Ecol 32:534–540. https://doi.org/10.1111/j.1442-9993.2007.01725.x
Amodeo M, Vázquez B, Zalba S (2017) Generalist dispersers promote germination of an alien Fleshy-fruited Tree Invading Natural Grasslands. PLoS ONE 12(2):e0172423. https://doi.org/10.1371/journal.pone.0172423
Andersen GL, Krzywinski K, Ha Gjessing, Pierce RH (2016) Seed viability and germination success of Acacia tortilis along land-use and aridity gradients in the Eastern Sahara. Ecol Evol 6:256–266. https://doi.org/10.1002/ece3.1851
Ayari A, Khouja ML (2014) Ecophysiological variables influencing Aleppo pine seed and cone production: a review. Tree Physiol 34:426–437. https://doi.org/10.1093/treephys/tpu022
Ayari A, Moya D, Rejeb MN, Ben Mansoura A, Albouchi A, De Las Heras J, Fezzani T, Henchi B (2011) Geographical variation on cone and seed production of natural Pinus halepensis Mill. forests in Tunisia. J Arid Environ 75:403–410. https://doi.org/10.1016/j.jaridenv.2011.01.001
Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and, evolution of dormancy and germination. Elsevier Science. https://books.google.com.ar/books?id=CYO-AQAAQBAJ
Bilenca D, Miñarro F (2004) Identificación de áreas valiosas de pastizal en las pampas y campos de Argentina, Uruguay y sur de Brasil. Fundación Vida Silvestre Argentina, Buenos Aires, Argentina
Boulant N, Kunstler G, Rambal S, Lepart J (2008) Seed supply, drought, and grazing determine spatio-temporal patterns of recruitment for native and introduced invasive pines in grasslands. Divers Distrib 14:862–874. https://doi.org/10.1111/j.1472.4642.2008.00494.x
Brancatelli GIE, Zalba SM (2018) Vector analysis: a tool for preventing the introduction of invasive alien species into protected areas. Nat Conserv 24:43. https://doi.org/10.3897/natureconservation.24.20607
Brancatelli GIE, Amodeo MR, Cuevas YA, Zalba SM (2020) Invasive pines in Argentinian grasslands: lessons from control operations. Biol Invasions 22:473–484. https://doi.org/10.1007/s10530-019-02103-9
Broncano MJ, Riba M, Retana J (1998) Seed germination and seedling performance of two Mediterranean tree species, holm oak (shape Quercus ilex L.) and Aleppo pine (shape Pinus halepensis Mill.): a multifactor experimental approach. Plant Ecol 138:17–26. https://doi.org/10.1023/A:1009784215900
Bueis T, Bravo F, Pando V, Turrión MB (2017) Site factors as predictors for Pinus halepensis Mill. productivity in Spanish plantations. Ann For Sci 74:6. https://doi.org/10.1007/s13595-016-0609-7
Cabrera AL (1976) Regiones Fitogeográficas Argentinas. In: Parodi LR (ed) Encyclopedia Argentina de Agricultura y Jardinería. Tomo II, Edición Acme, Buenos Aires, Argentina, pp 1–85
Calama R, Conde M, de-Dios-García J, Madrigal G, Vázquez-Piqué J, Gordo FJ, Pardos M (2019) Linking climate, annual growth and competition in a Mediterranean forest: Pinus pinea in the Spanish Northern Plateau. Agric For Meteorol 264:309–321. https://doi.org/10.1016/j.agrformet.2018.10.017
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. https://doi.org/10.1111/j.0022-0477.2004.00870.x
Castro J, Zamora R, Hodar JA, Gómez JM (2005) Ecology of seed germination of Pinus sylvestris L. at its southern, Mediterranean distribution range. For Syst 14:143–152
Condés S, García-Robredo F (2012) An empirical mixed model to quantify climate influence on the growth of Pinus halepensis Mill. stands in South-Eastern Spain. For Ecol Manage 284:59–68. https://doi.org/10.1016/j.foreco.2012.07.030
Cuevas YA (2010) Claves ecológicas para la restauración de un pastizal natural invadido por Pinus halepensis. Tesis de Doctorado. Universidad Nacional del Sur, Bahía Blanca, Buenos Aires, Argentina. http://repositoriodigital.uns.edu.ar/handle/123456789/2150
Daskalakou EN, Thanos CA (1996) Aleppo pine (Pinus halepensis) postfire regeneration: the role of canopy and soil seed banks. Int J Wildland Fire 6:59–66. https://doi.org/10.1071/WF9960059
de Villalobos AE, Schwerdt L (2020) Seasonality of feral horse grazing and invasion of Pinus halepensis in grasslands of the Austral Pampean Mountains (Argentina): management considerations. Biol Invasions 22:2941–2955. https://doi.org/10.1007/s10530-020-02300-x
de Villalobos A, Zalba S (2010) Continuous feral horse grazing and grazing exclusion in mountain pampean grasslands in Argentina. Acta Oecol 36:514–519. https://doi.org/10.1016/j.actao.2010.07.004
de Villalobos AE, Zalba SM, Peláez DV (2011) Pinus halepensis invasion in mountain pampean grassland: effects of feral horses grazing on seedling establishment. Environ Res 111:953–959. https://doi.org/10.1016/j.envres.2011.03.011
Del Campo AD, Cerrillo RMN, Hermoso J, Ibáñez AJ (2007) Relationships between site and stock quality in Pinus halepensis Mill. reforestation on semiarid landscapes in eastern Spain. Ann For Sci 64:719–731. https://doi.org/10.1051/forest:2007052
Del Río M, Calama R, Montero G (2008) Selvicultura de Pinus halepensis Mill. Serrada R, Montero G, Reque JA (eds) Compendio de Selvicultura Aplicada En España. INIA-FUCOVASA, Madrid, pp 289–312
Del Río M, Rodríguez-Alonso J, Bravo-Oviedo A, Ruíz-Peinado R, Cañellas I, Gutiérrez E (2014) Aleppo pine vulnerability to climate stress is independent of site productivity of forest stands in southeastern Spain. Trees 28:1209–1224. https://doi.org/10.1007/s00468-014-1031-0
Dickie IA, St John MG, Yeates GW, Morse CW, Bonner KI, Orwin K, Peltzer DA (2014) Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB PLANTS. https://doi.org/10.1093/aobpla/plu056
Eriksson O, Ehrlén J (1992) Seed and microsite limitation of recruitment in plant populations. Oecologia 91:360–364. https://doi.org/10.1007/BF00317624
Fonseca CR, Guadagnin DL, Emer C, Masciadri S, Germain P, Zalba SM (2013) Invasive alien plants in the Pampas grasslands: a tri-national cooperation challenge. Biol Invasions 15:1751–1763. https://doi.org/10.1007/s10530-013-0406-2
Frangi JL, Botinno OJ (1995) Comunidades vegetales de la Sierra de la Ventana, provincia de Buenos Aires, Argentina. Revista de La Facultad de Agronomía, La Plata 71:93–133
Gasque M, García-Fayos P (2004) Interaction between Stipa tenacissima and Pinus halepensis: consequences for reforestation and the dynamics of grass steppes in semi-arid Mediterranean areas. For Ecol Manage 189:251–261. https://doi.org/10.1016/j.foreco.2003.08.014
Gentili JO, Gil V (2013) Variabilidad temporal de las precipitaciones en vertientes opuestas del Sistema de Ventania, Buenos Aires, Argentina. Revista Universitaria de Geografía 22:147–166
Gorgens A, Van Wilgen B (2004) Invasive alien plants and water resources in South Africa: current understanding, predictive ability and research challenges: Working for Water. South African J Sci 100:27–33. http://hdl.handle.net/10204/761
Harper JL (1977) Population biology of plants. Academic Press, New York
Helluy M, Prévosto B, Cailleret M, Fernandez C, Balandier P (2020) Competition and water stress indices as predictors of Pinus halepensis Mill. radial growth under drought. For Ecol Manage. https://doi.org/10.1016/j.foreco.2020.117877
Jobbágy EG, Jackson RB (2003) Patterns and mechanisms of soil acidification in the conversion of grasslands to forests. Biogeochemistry 64:205–229. https://doi.org/10.1023/A:1024985629259
Jobbágy EG, Acosta AM, Nosetto MD (2013) Rendimiento hídrico en cuencas primarias bajo pastizales y plantaciones de pino de las sierras de Córdoba (Argentina). Ecología Austral 23:87–96. http://hdl.handle.net/10625/54821
Kassambara A, Kosinski A, Biecek P, Fabian S (2019) Survminer: drawing survival curves using’ggplot2’. 2019. R Package Version 0.4 4
Kristensen MJ, Frangi JL (1995a) La Sierra de la Ventana: una isla de biodiversidad. Ciencia Hoy 5:25–34
Kristensen MJ, Frangi JL (1995b) Mesoclimas de pastizales de la Sierra de la Ventana. Ecología Austral 5:55–64
Kristensen MJ, Frangi JL (1996) Mesoclimas de roquedales de la Sierra de la Ventana. Ecología Austral 6:115–122
Langdon B, Cavieres LA, Pauchard A (2019) At a microsite scale, native vegetation determines spatial patterns and survival of Pinus contorta invasion in Patagonia. Forests 10(8):654. https://doi.org/10.3390/f10080654
Lavi A, Perevolotsky A, Kigel J, Noy-Meir I, Hermy M (2005) Invasion of Pinus halepensis from plantations into adjacent natural habitats. Appl Veg Sci 8:85–92. https://doi.org/10.1658/1402-2001(2005)008%5b0085:IOPHFP%5d2.0.CO;2
Long MA, Peter G, Villamil CB (2004) La familia Asteraceae en el sistema de Ventania (Buenos Aires, Argentina). Boletín Sociedad Argentina de Botánica 39:159–169
Lövei GL, Lewinsohn TM (2012) Megadiverse developing countries face huge risks from invasives. Trends Ecol Evol 27:2–3. https://doi.org/10.1016/j.tree.2011.10.009
Manso R, Fortin M, Calama R, Pardos M (2013) Modelling seed germination in forest tree species through survival analysis. The Pinus pinea L. case study. For Ecol Manage 289:515–524. https://doi.org/10.1016/j.foreco.2012.10.028
Mast JN, Veblen TT, Hodgson ME (1997) Tree invasion within a pine/grassland ecotone: an approach with historic aerial photography and GIS modeling. For Ecol Manage 93:181–194. https://doi.org/10.1016/S0378-1127(96)03954-0
McConnachie MM, van Wilgen BW, Richardson DM, Ferraro PJ, Forsyth AT (2015) Estimating the effect of plantations on pine invasions in protected areas: a case study from South Africa. J Appl Ecol 52:110–118. https://doi.org/10.1111/1365-2664.12366
McNair JN, Sunkara A, Frobish D (2012) How to analyse seed germination data using statistical time-to-event analysis: non-parametric and semi-parametric methods. Seed Sci Res 22:77–95. https://doi.org/10.1017/S0960258511000547
Nathan R, Ne’eman G (2004) Spatiotemporal dynamics of recruitment in Aleppo pine (Pinus halepensis Miller). Plant Ecol 171:123–137. https://doi.org/10.1023/B:VEGE.0000029379.32705.0f
Nathan R, Safriel UN, Noy-Meir I, Schiller G (2000) Spatiotemporal variation in seed dispersal and recruitment near and far from Pinus halepensis trees. Ecology 81:2156–2169. https://doi.org/10.1890/0012-9658(2000)081%5b2156:SVISDA%5d2.0.CO;2
Olivar J, Bogino S, Spiecker H, Bravo F (2012) Climate impact on growth dynamic and intra-annual density fluctuations in Aleppo pine (Pinus halepensis) trees of different crown classes. Dendrochronologia 30:35–47. https://doi.org/10.1016/j.dendro.2011.06.001
Olivar J, Bogino S, Rathgeber C, Bonnesoeur V, Bravo F (2014) Thinning has a positive effect on growth dynamics and growth–climate relationships in Aleppo pine (Pinus halepensis) trees of different crown classes. Ann For Sci 71:395–404. https://doi.org/10.1007/s13595-013-0348-y
Omary AA (2011) Effects of aspect and slope position on growth and nutritional status of planted Aleppo pine (Pinus halepensis Miller) in a degraded land semi-arid areas of Jordan. New For 42:285–300. https://doi.org/10.1007/s11056-011-9251-2
Papadopoulos A, Tolica K, Pantera A, Maheras P (2009) Investigation of the annual variability of the Aleppo pine tree-ring width: the relationship with the climatic conditions in the Attica basin. Glob Nest J 11:583–592
Parodi LR (1942) ¿Por qué no existen bosques naturales en la llanura bonaerense? Revista del Centro de Estudiantes de la Facultad de Agronomía de la Universidad Nacional de Buenos Aires 30:387–390
Pretelli MG, Isacch JP, Cardoni DA (2015) Effects of fragmentation and landscape matrix on the nesting success of grassland birds in the Pampas grasslands of Argentina. Ibis 157:688–699. https://doi.org/10.1111/ibi.12292
Puértolas J, Gil L, Pardos JA (2003) Effects of nutritional status and seedling size on field performance of Pinus halepensis planted on former arable land in the Mediterranean basin. Forestry 76:159–168. https://doi.org/10.1093/forestry/76.2.159
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rathgeber CBK, Misson L, Nicault A, Guiot J (2005) Bioclimatic model of tree radial growth: application to the French Mediterranean Aleppo pine forests. Trees 19:162–176. https://doi.org/10.1007/s00468-004-0378-z
Retana J, Espelta JM, Gracia M, Riba M (1999) Seedling recruitment. In: Rodà F, Retana J, Gracia CA, Bellot J (eds) Ecology of Mediterranean evergreen oak forests. Springer, Berlin Heidelberg, pp 89–103
Richardson DM (1998) Forestry trees as invasive aliens. Conserv Biol 12:18–26. https://doi.org/10.1111/j.1523-1739.1998.96392.x
Richardson DM and Bond WJ (1991) Determinants of plant distribution: evidence from Pine invasions. Am Nat 137:639–668. www.jstor.org/stable/2462600
Richardson DM, Higgins SI (2000) Pines as invaders in the southern hemisphere. In: Richardson DM (ed) Ecology and biogeography of pinus. Cambridge University Press, Cambridge, pp 450–470
Richardson DM, Rundel PW (1998) Ecology and biogeography of Pinus: an introduction. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 3–49
Rubira JLP, Bueno LO, Lerena SD, Estrada IR (1996) Experiencias sobre control de la competencia herbácea en repoblaciones de terrenos agrícolas abandonados. Resultados de tres años en campo. Montes 45:30–36
Sagra J, Moya D, Plaza-Álvarez P, Lucas-Borja M, González-Romero J, De las Heras J, Alfaro-Sánchez R, Ferrandis P (2019) Prescribed fire effects on early recruitment of Mediterranean pine species depend on fire exposure and seed provenance. For Ecol Manage 441:253–261. https://doi.org/10.1016/j.foreco.2019.03.057
Simberloff D, Nuñez MA, Ledgard NJ, Pauchard A, Richardson DM, Sarasola M et al (2010) Spread and impact of introduced conifers in South America: lessons from other southern hemisphere regions. Austral Ecol 35:489–504. https://doi.org/10.1111/j.1442-9993.2009.02058.x
Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66. https://doi.org/10.1016/j.tree.2012.07.013
Skordilis A, Thanos C (1995) Seed stratification and germination strategy in the Mediterranean pines Pinus brutia and P. halepensis. Seed Sci Res 5:151–160
Skordilis A, Thanos CA (1997) Comparative ecophysiology of seed germination strategies in the seven pine species naturally growing in Greece. In: Ellis RH, Black M, Murdoch AJ, Hong TD (eds) Basic and applied aspects of seed biology. Springer, Netherlands, pp 623–632
Steinitz O, Troupin D, Vendramin G, Nathan R (2011) Genetic evidence for a Janzen-Connell recruitment pattern in reproductive offspring of Pinus halepensis trees. Mol Ecol 20:4152–4164. https://doi.org/10.1111/j.1365-294X.2011.05203.x
Taylor KT, Maxwell BD, McWethy DB, Pauchard A, Nuñez MA, Whitlock C (2017) Pinus contorta invasions increase wildfire fuel loads and may create a positive feedback with fire. Ecology 98:678–687. https://doi.org/10.1002/ecy.1673
Thanos CA, Daskalakou EN (2000) Reproduction in Pinus halepensis and Pinus brutia. In: Ne’eman G, Trabaud L (eds) Ecology, biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean Basin. Backhuys Publishers, Leiden, pp 79–90
Thanos CA, Daskalakou EN, Nikolaidou S (1996) Early post-fire regeneration of a Pinus halepensis forest on Mount Párnis, Greece. J Veg Sci 7:273–280. https://doi.org/10.2307/3236328
Therneau T (2015) A package for survival analysis in S. R package version 2.38. http://CRAN.R-project.org/package=survival
Trabaud L, Michels C, Grosman J (1985) Recovery of burnt Pinus halepensis Mill. forests. II. Pine reconstruction after wildfire. For Ecol Manage 13:167–179. https://doi.org/10.1016/0378-1127(85)90032-5
Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225–238. https://doi.org/10.1034/j.1600-0706.2000.880201.x
Vennetier M, Ripert C, Rathgeber C (2018) Autecology and growth of Aleppo pine (Pinus halepensis Mill.): a comprehensive study in France. For Ecol Manage 413:32–47. https://doi.org/10.1016/j.foreco.2018.01.028
Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21:1–20
Wickham H (2011) The split-apply-combine strategy for data analysis. J Stat Softw 40:1–29
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, NewYork
Williams MC, Wardle GM (2005) The invasion of two native Eucalypt forests by Pinus radiata in the Blue Mountains, New South Wales, Australia. Biol Conserv 125:55–64. https://doi.org/10.1016/j.biocon.2005.03.011
Yezzi AL, Nebbia AJ, Zalba SM (2018) Fragmentación de pastizales psamófilos por plantaciones de pinos: efectos sobre la riqueza y la composición vegetal. Ecología Austral 28:133–144. https://doi.org/10.25260/EA.18.28.1.0.640
Zalba SM, Villamil CB (2002) Woody plant invasion in Relictual Grasslands. Biol Invasion 4:55–72. https://doi.org/10.1023/A:1020532609792
Zalba SM, Cuevas YA, Boó RM (2008) Invasion of Pinus halepensis Mill. following a wildfire in an Argentine grassland nature reserve. J Environ Manage 88:539–546. https://doi.org/10.1016/j.jenvman.2007.03.018
Acknowledgements
This work was supported by the National Scientifc and Technical Research Council (CONICET), Argentina and Universidad Nacional del Sur, Bahía Blanca, Argentina. We are grateful to the Ernesto Tornquist Provincial Park rangers and authorities. We also wish to thank to the anonymous reviewers who provided helpful comments on earlier versions of the manuscript.
Author information
Authors and Affiliations
Contributions
GIEB and SMZ conceived the study; GIEB collected the data; MRA analysed the data. All the authors led the writing of the manuscript and contributed substantially to revisions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Brancatelli, G.I.E., Amodeo, M.R. & Zalba, S.M. Seedling emergence and survival of invasive pines in Argentinian mountain grasslands. Biol Invasions 23, 903–918 (2021). https://doi.org/10.1007/s10530-020-02410-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02410-6