Abstract
To understand current patterns of Pinus invasion in an Araucaria forest in southern Brazil, we quantified invasion at the local scale and compared it with habitat characteristics, propagule size, and number of source populations, using generalized linear models. We also compared observed and expected invasive species status based on a previously developed model (Z scores) using Chi square and correlation tests to evaluate the predictability of species status based on their traits. Of the 16 Pinus species currently present in the site, three are invasive (P. elliottii, P. glabra, and P. taeda), three are naturalized (P. clausa, P. oocarpa, and P. pseudostrobus), and ten are present only as the originally planted individuals. While P. taeda spread the farthest, P. glabra had greater overall density, but none of the invasive species has spread more than 250 m in 45 years. Invasive Pinus plants were found where forest tree density was below 805 trees ha−1, and invasive Pinus density decreased log-linearly with an increase in native tree density. Number of individuals introduced and number of source populations were strong predictors of naturalization, thus both propagule size and propagule diversity can potentially be driving invasion success. Z scores based on species traits did not predict which species would invade in Rio Negro. Our findings suggest that Araucaria forests might not resist invasion by Pinus as recently suggested and support the hypothesis that propagule pressure is a fundamental driver of invasions with propagule diversity being a possible component of this mechanism.
Similar content being viewed by others
References
Abreu RCR, Durigan G (2011) Changes in the plant community of a Brazilian grassland savannah after 22 years of invasion by Pinus elliottii Engelm. Plant Ecol Divers 4:269–278
Abreu RCR, de Assis GB, Frison S, Aguirre A, Durigan G (2011) Can native vegetation recover after slash pine cultivation in the Brazilian Savanna? For Ecol Manage 262:1452–1459
Ahlroth P, Alatalo R, Holopainen A, Kumpulainen T, Suhonen J (2003) Founder population size and number of source populations enhance colonization success in waterstriders. Oecologia 137:617–620
Baldanzi G, Araujo AJ (1971) Ensaio comparativo de espécies e procedências de Pinus, na Estação de Pesquisas Florestais de Rio Negro, Paraná. Floresta 3:86–89
Baldanzi G, Malinovski JR (1976) Ensaio comparativo de diferentes origens de Pinus taeda e P. elliotti. Floresta 7:5–8
Belcher E, Karrfalt R (1976) Cooperative approach to better tree seed. 20th Lab Rep. USDA Forest Service. Eastern Tree Seed Laboratory, Macon, GA, p 37
Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339
Bossdorf O, Auge H, Lafuma L, Rogers W, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11
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
Boulant N, Garnier A, Curt T, Lepart J (2009) Disentangling the effects of land use, shrub cover and climate on the invasion speed of native and introduced pines in grasslands. Divers Distrib 15:1047–1059
Bourscheid K, Reis A (2010) Dinâmica da invasão de Pinus elliottii Engelm. em restinga sob processo de restauração ambiental no Parque Florestal do Rio Vermelho, Florianópolis. SC. Biotemas 23:23–30
Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141
Colautti RI, Grigorovich IA, MacIsaac HJ (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037
Crawford KM, Whitney KD (2010) Population genetic diversity influences colonization success. Mol Ecol 19:1253–1263
Critchfield WB, Little EL (1966) Geographic distribution of the pines of the world. US Dept. of Agriculture Forest Service, USA
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534
Dawson W, Burslem DFRP, Hulme PE (2009) Factors explaining alien plant invasion success in a tropical ecosystem differ at each stage of invasion. J Ecol 97:657–665
Diez JM, Williams PA, Randall RP, Sullivan JJ, Hulme PE, Duncan RP (2009) Learning from failures: testing broad taxonomic hypotheses about plant naturalization. Ecol Lett 12:1174–1183
Dyer AR, Brown CS, Espeland EK, McKay JK, Meimberg H, Rice KJ (2010) The role of adaptive trans-generational plasticity in biological invasions of plants. Evol Appl 3:179–192
Eckert AJ, Bower AD, Gonzalez-Martinez SC, Wegrzyn JL, Coop G, Neale DB (2010a) Back to nature: ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Mol Ecol 19:3789–3805
Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, Gonzalez-Martinez SC, Neale DB (2010b) Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185:969–982
Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050
Emer C, Fonseca CR (2010) Araucaria forest conservation: mechanisms providing resistance to invasion by exotic timber trees. Biol Invasions 13:189–202
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
Essl F, Mang T, Dullinger S, Moser D, Hulme PE (2011) Macroecological drivers of alien conifer naturalizations worldwide. Ecography 34:1076–1084
Falleiros RM, Zenni RD, Ziller SR (2011) Invasão e manejo de Pinus taeda em campos de altitude do Parque Estadual o Pico Paraná, Paraná, Brasil. Floresta 41:123–134
Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Holle BV (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17
Grotkopp E, Rejmánek M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Am Nat 159:396–419
Higgins SI, Richardson DM (1998) Pine invasions in the southern hemisphere: modelling interactions between organism, environment and disturbance. Plant Ecol 135:79–93
Higgins SI, Richardson DM, Cowling RM (1996) Modeling invasive plant spread: the role of plant-environment interactions and model structure. Ecology 77:2043–2054
Hurrell JA, Bazzano DH (2007) Pinos ornamentales y forestales. L.O.L.A.—Literature of Latin America, Buenos Aires
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108
Keinert Junior S, Matos JLM (1987) Utilização de Pinus pinaster para fabricação de chapas de partículas. Floresta 17:113–120
Kozera C, Dittrich VAdO, Silva SM (2006) Phytosociology of the arboreal component of a patch of mixed ombrophilous montane forest at Curitiba, Paraná State, Brazil. Floresta 36:225–237
Krebs CJ (1999) Ecological methodology. Addison-Welsley Educational, CA, USA
Křivánek M, Pyšek P, Jarošík V (2006) Planting history and propagule pressure as predictors of invasion by woody species in a temperate region. Conserv Biol 20:1487–1498
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228
Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536
Muirhead JR, Gray DK, Kelly DW, Ellis SM, Heath DD, MacIsaac HJ (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035
Muth NZ, Pigliucci M (2006) Traits of invasives reconsidered: phenotypic comparisons of introduced invasive and introduced noninvasive plant species within two closely related clades. Am J Bot 93:188–196
Negrelle RRB, Leuchtenberger R (2004) Floristic composition and structure of an Araucarian forest remnant. Floresta 31:1–9
Nuñez MA, Medley KA (2011) Pine invasions: climate predicts invasion success; something else predicts failure. Divers Distrib 17:703–713
Nuñez MA, Simberloff D, Relva MA (2008) Seed predation as a barrier to alien conifer invasions. Biol Invasions 10:1389–1398
Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359
Nuñez MA, Moretti A, Simberloff D (2011) Propagule pressure hypothesis not supported by an 80-year experiment on woody species invasion. Oikos 120:1311–1316
Osem Y, Lavi A, Rosenfeld A (2011) Colonization of Pinus halepensis in mediterranean habitats: consequences of afforestation, grazing and fire. Biol Invasions 13:485–498
Palle SR, Seeve CM, Eckert AJ, Cumbie WP, Goldfarb B, Loopstra CA (2010) Natural variation in expression of genes involved in xylem development in loblolly pine (Pinus taeda L.). Tree Genet Genom 7:193–206
Peña E, Hidalgo M, Langdon B, Pauchard A (2008) Patterns of spread of Pinus contorta Dougl. ex Loud. invasion in a natural reserve in southern South America. For Ecol Manage 256:1049–1054
Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294
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. Global Ecol Biogeogr 21:513–523
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 97–125
Pyšek P, Křivánek M, Jarošík V (2009) Planting intensity, residence time, and species traits determine invasion success of alien woody species. Ecology 90:2734–2744
R Development Core Team (2011) R: a language and environment for statistical computing R Foundation for Statistical Computing. Austria, Vienna
Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103
Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661
Rejmánek M, Richardson DM, Higgins SI, Pitcairn MJ, Grotkopp E (2005) Ecology of invasive plants: state of the art. In: Mooney HA et al (eds) Invasive alien species. A new synthesis. Island Press, Washington, pp 104–161
Richardson DM (2006) Pinus: a model group for unlocking the secrets of alien plant invasions? Preslia 78:375–388
Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geog 30:409–431
Richardson DM, Rejmánek M (2004) Conifers as invasive aliens: a global survey and predictive framework. Divers Distrib 10:321–331
Richardson DM, Rejmánek M (2011) Trees and shrubs as invasive alien species—a global review. Divers Distrib 17:788–809
Richardson D, Williams P, Hobbs R (1994) Pine invasions in the southern hemisphere: determinants of spread and invadability. J Biogeogr 21:511–527
Richardson DM, Pysek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464
Rondon Neto RM, Watzlawick LF, Caldeira MVW, Schoeninger ER (2002) Floristic and structural analysis of a montane mixed ombrophylous forest fragment in Criúva, RS - Brazil. Ciência Florestal 12:29–37
Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445
Santos WC, Rosot NC, Rosot MAD (2010) Características edáficas relacionadas à produção de um povoamento de Araucaria angustifolia (Bert.) O. Kuntze. Floresta 40:37–48
Schultz RP (1997) Loblolly pine: the ecology and culture of the loblolly pine (Pinus taeda L.) U.S. Dept. of Agriculture, Forest Service Washington, DC
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102
Simberloff D, Nuñez MA, Ledgard NJ, Pauchard A, Richardson DM, Sarasola M, Van Wilgen BW, Zalba SM, Zenni RD, Bustamante R, Peña E, Ziller SR (2010) Spread and impact of introduced conifers in South America: lessons from other southern hemisphere regions. Austral Ecol 35:489–504
Simons AM (2003) Invasive aliens and sampling bias. Ecol Lett 6:278–280
Sol D (2007) Do successful invaders exist? pre-adaptations to novel environments in terrestrial vertebrates. In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 127–141
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218
Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144
Wilson JRU, Gairifo C, Gibson MR, Arianoutsou M, Bakar BB, Baret S, Celesti-Grapow L, DiTomaso JM, Dufour-Dror J-M, Kueffer C, Kull CA, Hoffmann JH, Impson FAC, Loope LL, Marchante E, Marchante H, Moore JL, Murphy DJ, Tassin J, Witt A, Zenni RD, Richardson DM (2011) Risk assessment, eradication, and biological control: global efforts to limit Australian acacia invasions. Divers Distrib 17:1030–1046
Zalba SM, Cuevas YA, Boo RM (2008) Invasion of Pinus halepensis Mill. Following a wildfire in an Argentine grassland nature reserve. J Environ Manage 88:539–546
Zanchetta D, Pinheiro LdS (2007) Análise biofísica dos processos envolvidos na invasão biológica de sementes de Pinus elliottii na Estação Ecológica de Itirapina—SP e alternativas de manejo. Climep 2:72–90
Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Rev bras Bot 34:431–446
Acknowledgments
We thank Martin A. Nuñez for ideas and comments on this manuscript, and Lara Souza, Dave Richardson, and anonymous referees for their comments on this manuscript. We are grateful to field assistants Renan M. Falleiros, Gilson Machado Rosa and Osmiro Valério Neto. The administration of the Rio Negro Experimental Station provided essential logistic support, especially Carlos Firkowski. R.D.Z. is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—Brazil) and this work was supported by a summer research grant from the Department of Ecology and Evolutionary Biology and a summer graduate research assistantship from the University of Tennessee.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zenni, R.D., Simberloff, D. Number of source populations as a potential driver of pine invasions in Brazil. Biol Invasions 15, 1623–1639 (2013). https://doi.org/10.1007/s10530-012-0397-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-012-0397-4