Biological Invasions

, Volume 14, Issue 7, pp 1415–1430 | Cite as

Brazilian peppertree (Schinus terebinthifolius) in Florida and South America: evidence of a possible niche shift driven by hybridization

  • A. Mukherjee
  • D. A. Williams
  • G. S. Wheeler
  • J. P. Cuda
  • S. Pal
  • W. A. Overholt
Original Paper


Brazilian peppertree (Schinus terebinthifolius Raddi, Anacardiaceae) was introduced into Florida from South America in the 1800s and commercialized as an ornamental plant. Based on herbaria records and available literature, it began to escape cultivation and invade ruderal and natural habitats in the 1950s, and is now considered to be one of Florida’s most widespread and damaging invasive plants. Historical records and molecular evidence indicate that two genetic lineages of Brazilian peppertree were established in Florida, one in Miami on the east coast and a second near Punta Gorda on the west coast. Since arriving, the distributions of these two types have greatly expanded, and they have extensively hybridized. Principal component analysis and reciprocal niche fitting were used to test the equivalency of climatic niches of the Florida populations with the climatic niches of the two South American chloroplast haplotype groups which established in Florida. Both approaches indicated a significant shift in niches between the parental populations in the native range and the invasive populations in Florida. The models, however, closely predicted the areas of initial establishment. We hypothesize that (1) Brazilian peppertree was able to gain an initial foothold in Florida due to niche similarity and (2) the current dissimilarity in native and exotic niches is due to hybridization followed by rapid selection of genotypes adapted to Florida’s climate. In addition, to examine the potential consequence of the introduction of additional genetic diversity from the native range on invasion success, a niche model constructed with occurrences of all native genotypes was projected onto the continental United States. The result of this test indicated that under such an event, the potential invasive range would greatly expand to cover most of the southeastern USA. Our study suggests that multiple introductions from disjunct regions in the native range can facilitate invasion success.


Invasive species Niche conservation Hybridization Range expansion Lag period 



Brazilian collections were conducted with the assistance of Dr. M. Vitorino, Universidade Regional de Blumenau, under the Instituto Brasileiro do Meio Ambiente permit 09BR003939/DF. Field assistance was generously provided by F. McKay, USDA/ARS/SABCL, Hurlingham, Argentina. We thank the Florida Department of Agriculture and Consumer Services, the Florida Fish and Wildlife Conservation Commission, South Florida Water Management District, and USDA/ARS for financial support for this work.

Supplementary material

10530_2011_168_MOESM1_ESM.doc (1.2 mb)
Supplementary material 1 (DOC 1185 kb)


  1. Akhisar I, Bener A (2002) Hierarchy analysis of three-way tables. Hacet J Math Stat 31:37–43Google Scholar
  2. Alexander TR, Crook AG (1984) Recent vegetational changes in southern Florida. In: Gleason PJ (ed) Environments of South Florida: present and past II. Miami Geological Soc., Coral Gables, Florida, p 210Google Scholar
  3. Anonymous (2007a) Other news: Brazilian pepper expands its range. Wildland Weeds 10:29Google Scholar
  4. Anonymous (2007b) Panhandlers beware! Wildland Weeds 11: 22Google Scholar
  5. Araújo MB, Luoto M (2007) The importance of biotic interactions for modelling species distributions under climate change. Glob Ecol Biogeogr 16:743–753CrossRefGoogle Scholar
  6. Austin MP, Van Niel KP (2011) Impact of landscape predictors on climate change modelling of species distributions: a case study with Eucalyptus fastigata in southern New South Wales, Australia. J Biogeogr 38:9–19CrossRefGoogle Scholar
  7. Barkley FA (1944) Schinus L. Brittonia 5:160–198CrossRefGoogle Scholar
  8. Barve N, Barve V, Jimenez-Valverde A, Lira-Noriega A, Maher SP, Peterson AT, Soberon J, Villalobos F (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol Model 222:1810–1819CrossRefGoogle Scholar
  9. Beaumont LJ, Gallagher RV, Thuiller W, Downey PO, Leishman MR, Hughes L (2009) Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions. Divers Distrib 15:409–420CrossRefGoogle Scholar
  10. Bennett FD, Habeck DH (1991) Brazilian peppertree: prospects for biological control in Florida. In: Center TD, Doren RF (eds) Proceedings of the symposium of exotic pest plants, pp 23–33, 2–4 November 1988. Miami, FLGoogle Scholar
  11. Bennett FD, Crestana L, Habeck DH, Berti-Filho E (1990) Brazilian peppertree: prospects for biological control. In: Delfosse ES (ed) Proceedings VII. International symposium on biological control of weeds, pp 293–297, 6–11 March 1988, Rome, Italy. Ministero dell’Agriculture e delle Foreste, Rome/CSIRO, Melbourne, AusraliaGoogle Scholar
  12. Broennimann O, Guisan I (2008) Predicting current and future biological invasions: both native and invaded ranges matter. Biol Lett 4:585–589PubMedCrossRefGoogle Scholar
  13. Broennimann O, Treier UA, Muller-Scharer H, Thuiller W, Peterson AT, Guisan A (2007) Evidence of climatic niche shift during biological invasion. Ecol Lett 10:701–709PubMedCrossRefGoogle Scholar
  14. Carhalho PER (1994) Especés Florestais Brasileiras Recomendações Silviculturais, Potencialidades e Uso da Madeira. Embrapa, Colombo, Parana, BrazilGoogle Scholar
  15. Cassani JJ (1986) Arthropods on Brazilian peppertree, Schinus terebinthifolius (Anacardiaceae), in south Florida. Fl Entomol 69:184–196CrossRefGoogle Scholar
  16. Cassani JJ, Maloney DR, Habeck DH, Bennett FD (1989) New insect records on Brazilian peppertree, Schinus terebinthifolius (Anacardiaceae), in south Florida. Fl Entomol 72:714–716CrossRefGoogle Scholar
  17. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  18. Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329CrossRefGoogle Scholar
  19. Cuda JP, Ferriter AP, Manrique V, Medal JC (2006) Florida’s Brazilian peppertree management plan. Recommendations from the Brazilian peppertree task force and Florida exotic pest plant council. Accessed 19 January 2011
  20. Davis JH (1943) The natural features of southern Florida. Fl Geol Sur Bull 25:1–311Google Scholar
  21. Donnelly MJ, Green DM, Walters LJ (2008) Allelopathic effects of fruits of the Brazilian peppertree Schinus terebinthifolius on growth, leaf production and biomass of seedlings of the red mangrove Rhizophora mangle and the black mangrovie Avicennia germinans. J Exp Mar Biol Ecol 357:149–156CrossRefGoogle Scholar
  22. Doren RF, Whiteaker LD, Larosa AM (1991) Evaluation of fire as a management tool for controlling Schinus terebinthifolius as secondary successional growth on abandoned agricultural land. Environ Manage 15:121–129CrossRefGoogle Scholar
  23. Ebeling SK, Welk E, Auge H, Bruelheide H (2008) Predicting the spread of an invasive plant: combining experiments and ecological niche model. Ecography 31:709–719CrossRefGoogle Scholar
  24. Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697CrossRefGoogle Scholar
  25. Elith J, Graham CH, Anderson RP, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton JM, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberon J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  26. Elith J, Kearny M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342CrossRefGoogle Scholar
  27. Elith J, Phillips SJ, Hastie T, Dudı′k M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57CrossRefGoogle Scholar
  28. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  29. Ewe SML, Sternberg L (2002) Seasonal water-use by the invasive exotic, Schinus terebinthifolius, in native and disturbed communities. Oecologia 133:441–448CrossRefGoogle Scholar
  30. Ewe SML, Sternberg LSL (2005) Growth and gas exchange responses of Brazilian pepper (Schinus terebinthifolius) and native South Florida species to salinity. Trees Struct Funct 19:119–128CrossRefGoogle Scholar
  31. Ewe SML, Sternberg LSL, Childers DL (2007) Seasonal plant water uptake patterns in the saline southeast Everglades ecotone. Oecologia 152:607–616PubMedCrossRefGoogle Scholar
  32. Ewel JJ (1986) Invasibility: lessons from south Florida. In: Mooney H, Drake J (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 214–230CrossRefGoogle Scholar
  33. Ewel JJ, Ojima DA, Karl DA, DeBusk WF (1982) Schinus in successional ecosystems of Everglades National Park. South Florida Research Center Report T-676. Everglades National Park, p 141Google Scholar
  34. Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49CrossRefGoogle Scholar
  35. Franklin J (2009) Mapping species distributions: spatial inference and prediction. Cambridge University Press, CambridgeGoogle Scholar
  36. Galen C (1990) Limits to the distributions of alpine tundra plants: herbivores and the alpine skypilot, Polemonium viscosum. Oikos 59:355–358CrossRefGoogle Scholar
  37. Gallagher RV, Beaumont LJ, Hughes L, Leishman MR (2010) Evidence for climatic niche and biome shifts between native and novel ranges in plant species introduced to Australia. J Ecol 98:790–799CrossRefGoogle Scholar
  38. Geiger JH, Pratt PD, Wheeler GS, Williams DA (2011) Hybrid vigor for the invasive exotic Brazilian peppertree (Schinus terebinthifolius Raddi., Anacardiaceae) in Florida. Int J Plant Sci 172:655–663CrossRefGoogle Scholar
  39. Gioeli K, Langeland K (2009). Brazilian pepper-tree control. University of Florida, Cooperative Extension Service. Institute of Food and Agricultural Sciences, SS-AGR-17. Accessed 19 January 2011
  40. Giovanelli JGR, Haddad CFB, Alexandrino J (2008) Predicting the potential distribution of the alien invasive American bullfrog (Lithobates catesbeianus) in Brazil. Biol Invasions 10:585–590CrossRefGoogle Scholar
  41. Gogue GJ, Hurst C, Bancroft L (1974) Growth inhibition by Schinus terebinthifolius. HortSci 9:301Google Scholar
  42. Hamilton M (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523PubMedGoogle Scholar
  43. Hijmans RJ, Guarino L, Cruz M, Rojas E (2001) Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter pp 15–19Google Scholar
  44. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  45. Hinojosa-Díaz IA, Feria Arroyo TP, Engel MS (2009) Potential distribution of orchid bees outside their native range: the cases of Eulaema polychroma (Mocsáry) and Euglossa viridissima Friese in the USA (Hymenoptera: Apidae). Divers Distrib 15:421–428CrossRefGoogle Scholar
  46. Hutchinson GE (1957) Population studies—animal ecology and demography—concluding remarks. Cold Spring Harb Sym 22:415–427CrossRefGoogle Scholar
  47. Jackson ST, Overpeck JT (2000) Response of plant populations and communities to environmental changes of the late quaternary. Paleobiology 26(Suppl):194–220CrossRefGoogle Scholar
  48. JBRJ (2009) Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Jabot—Banco de Dados da Flora Brasileira. Accessed 1 October 2010
  49. Jimenez-Valverde A, Peterson AT, Soberon J, Overton JM, Aragon P, Lobo JM (2011) Use of niche models in invasive species risk assessments. Biol Invasions 13:2785–2797CrossRefGoogle Scholar
  50. Joyner TA, Lukhnova L, Pazilov Y, Temiralyeva G, Hugh-Jones ME, Aikimbayev A, Blackburn JK (2010) Modeling the potential distribution of Bacillus anthracis under multiple climate change scenarios for Kazakhstan. PLoS One 5: 1–15 e9596Google Scholar
  51. Kolbe JJ, Glor RE, Schettino LR, Lara ADAC, Larson A, Losos JB (2007) Multiple sources, admixture, and genetic variation in introduced Anolis lizard populations. Conserv Biol 21:1612–1625PubMedCrossRefGoogle Scholar
  52. Louda SM, Rodman JE (1996) Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, bittercress). J Ecol 84:229–237CrossRefGoogle Scholar
  53. Lozier JD, Aniello P, Hickerson MJ (2009) Predicting the distribution of Sasquatch in western North America: anything goes with ecological niche modelling. J Biogeogr 36:1623–1627CrossRefGoogle Scholar
  54. Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  55. McKay F, Oleiro M, Walsh GC, Gandolfo D, Cuda JP, Wheeler GS (2009) Natural enemies of Brazilian peppertree (Schinus terebinthifolius: Anacardiaceae) from Argentina: their possible use for biological control in the USA. Fl Entomol 92:292–303CrossRefGoogle Scholar
  56. Medley KA (2010) Niche shifts during the global invasion of the Asian tiger mosquito, Aedes albopictus Skuse (Culicidae), revealed by reciprocal distribution models. Glob Ecol Biogeogr 19:122–133CrossRefGoogle Scholar
  57. Morgan EC, Overholt WA (2005) Potential allelopathic effects of Brazilian pepper (Schinus terebinthifolius Raddi, Anacardiaceae) aqueous extract on germination and growth of selected Florida native plants. J Torrey Bot Soc 132:11–15CrossRefGoogle Scholar
  58. Morton JF (1978) Brazilian peppertree: its impact on people, animals and the environment. Econ Bot 32:353–359CrossRefGoogle Scholar
  59. Mukherjee A, Christman MC, Overholt WA, Cuda JP (2011) Prioritizing areas in the native range of hygrophila for surveys to collect biological control agents. Biol Control 56:254–262CrossRefGoogle Scholar
  60. Nehrling H (1944) My garden in Florida. American Eagle, EsteroGoogle Scholar
  61. Nilsen ET, Muller WH (1980a) A comparison of the relative naturalizing ability of two Schinus species (Anacardiaceae) in southern California. II: Seedling establishment. Bull Torrey Bot Club 107:232–237CrossRefGoogle Scholar
  62. Nilsen ET, Muller WH (1980b) A comparison of the relative naturalization ability of two Schinus species in southern CaliforniaI. Seed germination. Bull Torrey Bot Club 107:51–56CrossRefGoogle Scholar
  63. Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species: influence of mating systems and introduction dynamics. In: Sax DF, Gaines SD, Stachpwicz JJ (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, pp 201–228Google Scholar
  64. NYBG (2009) New York Botanical Garden. Accessed 1 October 2009
  65. Panetta FD, McKee J (1997) Recruitment of the invasive ornamental, Schinus terebinthifolius, is dependent upon frugivores. Aust J Ecol 22:432–438CrossRefGoogle Scholar
  66. Pearman PB, Guisan A, Broennimann O, Randin CF (2008) Niche dynamics in space and time. Trends Ecol Evol 23:149–158PubMedCrossRefGoogle Scholar
  67. Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr 12:361–371CrossRefGoogle Scholar
  68. Pearson RG, Raxworthy CJ, Nakamura M, Peterson AT (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34:102–117CrossRefGoogle Scholar
  69. Peterson AT, Shaw J (2003) Lutzomyia vectors for cutaneous leishmaniasis in Southern Brazil: ecological niche models, predicted geographic distributions, and climate change effects. Int J Parasitol 33:919–931PubMedCrossRefGoogle Scholar
  70. Peterson AT, Papes M, Eaton M (2007) Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30:550–560Google Scholar
  71. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  72. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294PubMedCrossRefGoogle Scholar
  73. Rödder D, Engler JO (2011) Quantitative metrics of overlaps in Grinnellian niches; advances and possible drawbacks. Glob Ecol Biogeogr 20:915–927CrossRefGoogle Scholar
  74. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedCrossRefGoogle Scholar
  75. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Ann Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  76. Schierenbeck KA, Ellstrand NC (2009) Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions 11:1093–1105CrossRefGoogle Scholar
  77. Schmitz DC, Simberloff D, Hofstetter RH, Haller W, Sutton D (1997) The ecological impact of nonindigenous plants. Island Press, Washington, pp 9–61Google Scholar
  78. Soberon J, Peterson AT (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiv Informatics 2:1–10Google Scholar
  79. Soberson J, Nakamura M (2009) Niches and distributional areas: concepts, methods, and assumptions. Proc Natl Acad Sci USA 106:19644–19650CrossRefGoogle Scholar
  80. Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360PubMedCrossRefGoogle Scholar
  81. Templeton AR, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343PubMedGoogle Scholar
  82. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673PubMedCrossRefGoogle Scholar
  83. Thompson GD, Robertson MP, Webber BL, Richardson DM, Le Roux JJ, Wilson JRU (2011) Predicting the subspecific identity of invasive species using distribution models: Acacia saligna as an example. Divers Distrib 17:1001–1014CrossRefGoogle Scholar
  84. Thuiller W, Richardson D, PYŠEK P, Midgley G, Hughes G, Rouget M (2005) Niche-based modelling as a tool for predicting the risk of alien plant invasions at a global scale. Glob Change Biol 11:2234–2250CrossRefGoogle Scholar
  85. Thuiller W, Broennimann O, Hughesw G, Alkemade JRM, Midgley GF, Corsi F (2006) Vulnerability of African mammals to anthropogenic climate change under conservative land transformation assumptions. Glob Change Biol 12:424–440CrossRefGoogle Scholar
  86. (2009) Missouri botanical garden. Accessed 1 October 2009
  87. VanDerWal J, Shoo LP, Johnson CN, Williams SE (2009) Abundance and the environmental niche: environmental suitability estimated from niche models predicts the upper limit of local abundance. Am Nat 174:282–291PubMedCrossRefGoogle Scholar
  88. Ward SM, Gaskin JF, Wilson LM (2008) Ecological genetics of plant invasion: what do we know? Inv Plant Sci Manage 1:98–109CrossRefGoogle Scholar
  89. Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883PubMedCrossRefGoogle Scholar
  90. Wheeler GS, Massey L, Endries M (2001) The Brazilian peppertree drupe feeder Megastigmus transvaalensis (Hymenoptera: Torymidae): Florida distribution and impact. Biol Control 22:139–148CrossRefGoogle Scholar
  91. Wiens JJ, Graham CH (2005) Niche conservatism: integration of evolution, ecology and conservation biology. Ann Rev Ecol Syst 36:519–539CrossRefGoogle Scholar
  92. Williams DA, Overholt WA, Cuda JP, Hughes CR (2005) Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida. Mol Ecol 14:3643–3656PubMedCrossRefGoogle Scholar
  93. Williams DA, Muchugu E, Overholt WA, Cuda JP (2007) Colonization patterns of the invasive Brazilian peppertree, Schinus terebinthifolius, in Florida. Heredity 98:284–293PubMedCrossRefGoogle Scholar
  94. Wunderlin RP, Hansen BF (2004) Atlas of Florida vascular plants. Accessed 1 October 2010. Institute for Systematic Botany, University of South Florida, Tampa, FL

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • A. Mukherjee
    • 1
  • D. A. Williams
    • 2
  • G. S. Wheeler
    • 3
  • J. P. Cuda
    • 1
  • S. Pal
    • 4
  • W. A. Overholt
    • 5
  1. 1.Department of Entomology and NematologyUniversity of FloridaGainesvilleUSA
  2. 2.Department of BiologyTexas Christian UniversityFort WorthUSA
  3. 3.Invasive Plant Research LaboratoryUSDA/ARSFort LauderdaleUSA
  4. 4.Department of StatisticsUniversity of FloridaGainesvilleUSA
  5. 5.Indian River Research and Education CenterUniversity of FloridaFort PierceUSA

Personalised recommendations