Advertisement

Biological Invasions

, Volume 19, Issue 1, pp 109–129 | Cite as

Abiotic barriers limit tree invasion but do not hamper native shrub recruitment in invaded stands

  • Thalita G. Zimmermann
  • Antonio C. S. Andrade
  • David M. Richardson
Original Paper

Abstract

The interplay between the invasion of alien plant species and re-colonization of native plant species is important for conservation. Sandy coastal plains (called restinga in Brazil) were used as a model system to explore the abiotic barriers that potentially limit the initial establishment of alien and native woody plants in invaded and non-invaded areas. The study tested the influence of light availability, soil type and litter layer on recruitment of a wind-dispersed alien tree (Casuarina equisetifolia) and two bird-dispersed native shrubs under a Casuarina stand and in the preserved restinga. The effect of soil type and the physical and allelopathic effects of Casuarina litter on seedling emergence of the three species were also evaluated under greenhouse conditions. Low dispersal associated with low seedling emergence and zero survival of young plants (mainly due to microhabitat conditions) apparently prevents the spread of Casuarina in the preserved restinga. The main cause of low recruitment of native species in the Casuarina stand was the physical barrier of the litter. However, if seeds overcome this physical barrier, the presence of litter improves seedling emergence and survival of young plants, mainly because the litter increases soil moisture. Sowing seeds below litter and planting young plants of native shrubs on litter can improve the re-colonization of native plants in invaded areas. In conclusion, Casuarina invasion on sandy coastal plains is strongly limited by abiotic barriers, but anthropogenic disturbances are altering the key processes that naturally make the restinga resistant to invasion.

Keywords

Casuarina equisetifolia Litter Seed dispersal Seedling emergence Restinga Tree invasion 

Notes

Acknowledgments

Funding for this project was provided by the Instituto de Pesquisas Jardim Botânico do Rio de Janeiro (JBRJ), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). We thank, F. Silva and I.S. Matos for their field assistance and L.L. Leal for her assistance in the greenhouse. DMR acknowledges funding from the DST-NRF Centre of Excellence for Invasion Biology and the National Research Foundation of South Africa (grant 85417).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2016_1267_MOESM1_ESM.docx (105 kb)
Supplementary material 1 (DOCX 105 kb)

References

  1. Apfelbaum SI, Ludwig JP, Ludwig C (1983) Ecological problems associated with disruption of dune vegetation dynamics by Casuarina equisetifolia L. at Sand Island, Midway Atoll. Atoll Res Bull 261:1–19CrossRefGoogle Scholar
  2. Araújo DSD (1992) Vegetation types of sandy coastal plains of tropical Brazil: a first approximation. In: Seeliger U (ed) Coastal plant communities of Latin America. Academic Press, San Diego, pp 337–347CrossRefGoogle Scholar
  3. Araújo DSD, Pereira MCA (2002) Sandy coastal vegetation. Eolss Publishers, International Commission on Tropical Biology and Natural Resources, OxfordGoogle Scholar
  4. Araújo DSD, Sá CFC, Fontella-Pereira J, Garcia DS, Ferreira MV, Paixão RJ, Schneider SM, Fonseca-Kruel VS (2009) Área de proteção ambiental de Massambaba, Rio de Janeiro: caracterização fitofisionômica e florística. Rodriguésia 60:67–96Google Scholar
  5. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380CrossRefPubMedGoogle Scholar
  6. Barbiére EB (1984) Cabo Frio e Iguaba Grande, dois microclimas distintos a um curto intervalo espacial. In: Lacerda LD, Araújo DDD, Cerqueira R, Turcq B (eds) Restingas: origem, estrutura, processos. CEUFF, Niterói, pp 3–13Google Scholar
  7. Barroso GM, Morim MP, Peixoto AL, Ichaso CLF (1999) Frutos e sementes: morfologia aplicada à sistemática de dicotiledôneas. Universidade Federal de Viçosa, ViçosaGoogle Scholar
  8. Baskin CC, Baskin JM (2014) Seeds: Ecology, biogeography, and evolution of dormancy and germination 2nd. Elsevier, San DiegoGoogle Scholar
  9. Bechara FC, Reis A, Bourscheid K, Vieira NK, Trentin BE (2013) Reproductive biology and early establishment of Pinus elliottii var. elliottii in Brazilian sandy coastal plain vegetation: implications for biological invasion. Sci Agric 702:88–92CrossRefGoogle Scholar
  10. Benevides CR, Haddad IVN, Barreira NP, Rodarte ATA, Galetto L, Santiago-Fernandes LDR, Lima HA (2013) Maytenus obtusifolia Mart. (Celastraceae): a tropical woody species in a transitional evolutionary stage of the gynodioecy–dioecy pathway. Plant Syst Evol 299:1693–1707CrossRefGoogle Scholar
  11. Bittrich V, Trad RJ, Cabral FN, Nascimento-Jr JE, Souza VC (2015) Clusiaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB6836. Accessed 28 Aug 2015
  12. Blackburn TM, Pyšek P, Bacher S, Carlton JT, Duncan RP, Jarošík V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefPubMedGoogle Scholar
  13. Braz MIG, de Mattos EA (2010) Seed dispersal phenology and germination characteristics of a drought-prone vegetation in southeastern Brazil. Biotropica 42:327–335CrossRefGoogle Scholar
  14. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965CrossRefGoogle Scholar
  15. Cavalcante A, Braz MIG, de Mattos EA (2010) Germination biology and seedling growth of Clusia hilariana Schltdl., a dominant CAM-tree of drought-prone sandy coastal plains. Ecol Res 25:781–787CrossRefGoogle Scholar
  16. Cavalin PO, de Mattos EA (2007) Spatio-temporal variation of photosynthetic pigments in CAM tree Clusia hilariana Schlechtendal associated with dry spells during rainy season in south-eastern Brazil. Trees 21:671–675CrossRefGoogle Scholar
  17. Correia CMB, Dias ATC, Scarano FR (2010) Plant-plant associations and population structure of four woody plant species in a patchy coastal vegetation of Southeastern Brazil. Rev Bras Biol 33:607–613Google Scholar
  18. Coutts SR, van Klinken RD, Yokomizo H, Buckley YM (2011) What are the key drives of spread in invasive plants: dispersal, demography or landscape: and can we use this knowledge to aid management? Biol Invasions 13:1649–1661CrossRefGoogle Scholar
  19. de la Penã E, Bonte D, Roiloa S, Rodíguez-Echeverría S, Freitas H (2010) Plant-soil feedback as mechanism of invasion by Carpobrotus edulis. Biol Invasions 12:3637–3648CrossRefGoogle Scholar
  20. Dechoum MS, Zenni RD, Castellani TT, Zalba SM, Rejmánek M (2015) Invasions across secondary forest successional stages: effects of local plant community, soil, litter, and herbivory on Hovenia dulcis seed germination and seedling establishment. Plant Ecol 216:823–833CrossRefGoogle Scholar
  21. Dias ATC, Zaluar HLT, Ganade G, Scarano FR (2005) Canopy composition influencing plant patch dynamics in a Brazilian sandy coastal plain. J Trop Ecol 21:343–347CrossRefGoogle Scholar
  22. Dias ATC, de Mattos EA, Vieira SA, Azeredo JV, Scarano FR (2006) Aboveground biomass stock of native woodland on a Brazilian sandy coastal plains: estimates based on the dominant tree species. For Ecol Manag 226:364–367CrossRefGoogle Scholar
  23. Eckstein RL, Donath TW (2005) Interactions between litter and water availability affect seedling emergence in four familial pairs of floodplain species. J Ecol 93:807–816CrossRefGoogle Scholar
  24. Emer C, Fonseca CR (2011) Araucaria Forest conservation: mechanisms providing resistance to invasion by exotic timber tress. Biol Invasions 13:189–202. doi: 10.1007/s10530-010-9801-0 CrossRefGoogle Scholar
  25. Ens E, French K (2008) Exotic woody invader limits the recruitment of three indigenous plant species. Biol Conserv 141:590–595CrossRefGoogle Scholar
  26. Facelli JM, Pickett STA (1991) Plant litter: its dynamics and effects on plant community structure. Bot Rev 57:1–32CrossRefGoogle Scholar
  27. Faria APG, Matallana G, Wendt T, Scarano FR (2006) Low fruit set in the abundant dioecious tree Clusia hilariana (Clusiaceae) in a Brazilian restinga. Flora 201:606–611CrossRefGoogle Scholar
  28. Franco AC, Haag-Kerwer A, Herzog B, Grams T, Ball E, de Mattos EA, Scarano FR, Barreto SMB, Garcia MA, Mantovani A, Lutge U (1996) The effect of light levels on daily patterns of chlorophyll fluorescence and organic acid accumulation in the tropical CAM tree Clusia hilariana. Trees 10:359–365Google Scholar
  29. Fuentes-Ramírez A, Pauchard A, Cavieres LA, García RA (2011) Survival and growth of Acacia dealbata vs. native trees across an invasion front in south-central Chile. Forest Ecol Manag 261:1003–1009CrossRefGoogle Scholar
  30. Garwwod NC (1996) Functional morphology of tropical tree seedlings. In: Swaine MD (ed) The ecology of tropical forest tree seedlings man and the biosphere. Parthenon Publishing Group, New York, pp 59–129Google Scholar
  31. Gomes VSM (2006) Variação espacial e dieta de aves terrestres na Restinga de Jurubatiba, RJ. PhD Thesis, Universidade Federal do Rio de JaneiroGoogle Scholar
  32. Gómez-Aparicio L, Valladares F, Zamora R, Quero JL (2005) Response of tree seedlings to the abiotic heterogeneity generated by nurse shrubs: an experimental approach at different scales. Ecography 28:757–768CrossRefGoogle Scholar
  33. Grotkopp E, Rejmánek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:526–532CrossRefPubMedGoogle Scholar
  34. Guerrero PC, Bustamante RO (2007) Can Native Tree Species Regenerate in Pinus radiata Plantations in Chile? evidence from field and laboratory experiments. Forest Ecol Manag 253:97–102CrossRefGoogle Scholar
  35. Hastwell GT, Facelli JM (2003) Differing effects of shade-induced facilitation on growth and survival during the establishment of a chenopod shrub. J Ecol 91:941–950CrossRefGoogle Scholar
  36. Hata K, Kato H, Kachi N (2009) Community structure of saplings of native woody species under forests dominated by alien woody species, Casuarina equisetifolia, in Chichijima Island. Ogasawara Res 34:33–50Google Scholar
  37. Hata K, Kato H, Kachi N (2010a) Litter of an alien tree, Casuarina equisetifolia, inhibits seed germination and initial growth of a native tree on the Ogasawara Islands (subtropical oceanic islands). J For Res 15:384–390CrossRefGoogle Scholar
  38. Hata K, Kato H, Kachi N (2010b) Litterfall in forests dominated by an alien woody species, Casuarina equisetifolia, on Chichijima Island. Ogasawara Res 35:1–14Google Scholar
  39. Hata K, Kato H, Kachi N (2012) Seedlings of a native shrub can establish under forests dominated by an alien tree, Casuarina equisetifolia, on subtropical oceanic islands. J For Res 17:208–212CrossRefGoogle Scholar
  40. Hesp PA, Martínez ML (2007) Disturbance processes and dynamics in coastal dunes. In: Johnson EA, Miyanishi K (eds) Plant disturbance ecology. The process and the response. Academic Press, San Diego, pp 215–247CrossRefGoogle Scholar
  41. Hobbs RJ, Higgs ES, Hall CM et al (2014) Managing the whole landscape: historical, hybrid and novel ecosystems. Front Ecol Environ 12:557–564CrossRefGoogle Scholar
  42. Holmes PM, Richardson DM (1999) Protocols for restoration based on recruitment dynamics, community structure and ecosystem function: perspectives from South African fynbos. Restor Ecol 7:215–230CrossRefGoogle Scholar
  43. Hovstad KA, Ohlson M (2008) Physical and chemical effects of litter on plant establishment in semi-natural grasslands. Plant Ecol 196:251–260CrossRefGoogle Scholar
  44. Hulme PE (2007) Biological invasions in Europe: drivers, pressures, states, impacts and responses. In: Hester R, Harrison RM (eds) Biodiversity under Threat. Cambridge University Press, Cambridge, pp 56–80CrossRefGoogle Scholar
  45. Inderjit Seastedt TR, Callaway RM, Pollock JL, Kaur J (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875–890CrossRefGoogle Scholar
  46. INMET (2014) Instituto Nacional de Meteorologia. http://inmet.gov.br. Acessed 15 Jul 2014
  47. I3N Brazil. 2016. Base de dados nacional de espécies exóticas invasoras, I3N Brasil, Instituto Hórus de desenvolvimento e Conservação Ambiental. http://i3n.institutohorus.org.br. Accessed 12 Jan 2016
  48. Lacerda LD, Araújo DSD, Maciel NC (1993) Dry coastal ecosystems of the tropical Brazilian coast. In: Van der Maarel E (ed) Dry coastal ecosystems: Africa, America, Asia, Oceania. Elsevier, Amsterdam, pp 477–493Google Scholar
  49. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 10:975–989CrossRefGoogle Scholar
  50. Lombardi J, Groppo M, Biral L (2015) Celastraceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB6766. Accessed 28 Aug 2015
  51. Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536CrossRefGoogle Scholar
  52. Loydi A, Donath TW, Eckstein RL, Otte A (2015) Non-native species litter reduces germination and growth of resident forbs and grasses: allelopathic, osmotic or mechanical effects? Biol Invasions 17:581–595CrossRefGoogle Scholar
  53. Matos IS (2014) Crescimento, Sobrevivência e Plasticidade Fenotípica de Plântulas de Espécies de Restinga sob Gradientes Experimentais de Intensidade de Luz e de Disponibilidade Hídrica. Dissertation, Instituto de Pesquisas Jardim Botânico do Rio de JaneiroGoogle Scholar
  54. McAlpine KG, Jesson LK (2008) Linking seed dispersal, germination and seedling recruitment in the invasive species Berberis darwinii (Darwin’s barberry). Plant Ecol 197:119–129CrossRefGoogle Scholar
  55. Morton JF (1980) The Australian pine or beefwood (Casuarina equisetifolia L.) an invasive ‘‘weed’’ tree in Florida. Proc Fl State Horticult Soc 93:87–95Google Scholar
  56. Nakahira Y, Ohira T (2005) Study on the allelopathy of Casuarina glauca and C. equisetifolia. Kyushu J For Res 58:159–161Google Scholar
  57. Novoa A, González L, Moravcová L, Pyšek P (2012) Effects of soil characteristics, allelopathy and frugivory on establishment of the invasive plant Carpobrotus edulis and a cooccuring native Malcolmia littorea. PLoS One 7(12):e53166CrossRefPubMedPubMedCentralGoogle Scholar
  58. Novoa A, Rodríguez R, Richardson D, González L (2014) Soil quality: a key factor in understanding plant invasion? the case of Carpobrotus edulis (L.) N.E.Br. Biol Invasions 16:429–443CrossRefGoogle Scholar
  59. Parrotta JA (1993) Casuarina equisetifolia L. ex J.R. and G. Forst. SO-ITF-SM-46. International Institute of Tropical Forestry, U.S. Department of Agriculture, Forest Service, Puerto RicoGoogle Scholar
  60. Parrotta JA (1995) Influence of overstory composition on understory colonization by native species in plantations on a degraded tropical site. J Veg Sci 6:627–636CrossRefGoogle Scholar
  61. Parrotta JA (1999) Productivity, nutrient cycling and succession in single- and mixed-species plantations of Casuarina equisetifolia, Eucalyptus robusta and Leucaena leucocephala in Puerto Rico. For Ecol Manag 90:45–77CrossRefGoogle Scholar
  62. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of non-indigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  63. Potgieter LJ, Richardson DM, Wilson JRU (2014) Casuarina: biogeography and ecology of an important tree genus in a changing world. Biol Invasions 16:609–633CrossRefGoogle Scholar
  64. Pugnaire FI, Armas C, Valladares F (2004) Soil as a mediator in plant-plant interactions in a semi-arid community. J Veg Sci 15:85–92CrossRefGoogle Scholar
  65. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available via http://www.R-project.org/
  66. Reinert F, Roberts A, Wilson JM, de Ribas L, Cardinot G, Griffiths H (1997) Gradation in nutrient composition and photosynthetic pathways across the restinga vegetation of Brazil. Bot Acta 110:135–142CrossRefGoogle Scholar
  67. Rejmánek M, Richardson D (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661CrossRefGoogle Scholar
  68. Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species - 2013 update of the global database. Divers Distrib 19:1093–1094CrossRefGoogle Scholar
  69. Rentería JL (2007) Plan de manejo para la erradicación de Casuarina equisetifolia L. (Casuarinaceae), especie invasora de limitada distribución en la isla Santa Cruz, Galápagos. Estación Científica Charles Darwin, Galápagos, EcuadorGoogle Scholar
  70. Richardson DM (2006) Pinus: a model group for unlocking the secrets of alien plant invasions? Preslia 78:375–388Google Scholar
  71. Richardson DM, Higgins SI (1998) Pines as invaders in the southern hemisphere. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 450–473Google Scholar
  72. Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographic patterns. New Phytol 196:383–396CrossRefPubMedGoogle Scholar
  73. Rocha CFD, Van Sluys M, Alves MS, Jamel CE (2007) The remnants of restinga habitats in the Brazilian Atlantic Forest of Rio de Janeiro state, Brazil: habitat loss and risk of disappearance. Braz J Biol 67:263–273CrossRefPubMedGoogle Scholar
  74. Rotundo JL, Aguiar MR (2005) Litter effects on plant regeneration in arid lands: a complex balance between seed retention, longevity and soil–seed-contact. J Ecol 93:829–838CrossRefGoogle Scholar
  75. Rouget M, Robertson MP, Wilson JRU, Hui C, Essl F, Renteria JL, Richardson DM (2016) Invasion debt—quantifying future biological invasions. Divers Distrib 22:445–456CrossRefGoogle Scholar
  76. Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic Rainforest. Ann Bot 90:517–524CrossRefPubMedPubMedCentralGoogle Scholar
  77. Scarano FR (2009) Plant communities at the periphery of the Atlantic rain forest: rare-species bias and its risks for conservation. Biol Conserv 142:1201–1208CrossRefGoogle Scholar
  78. Stricker KB, Stiling P (2013) Seedlings of the introduced invasive shrub Eugenia uniflora (Myrtaceae) outperform those of its native and introduced non-invasive congeners in Florida. Biol Invasions 15:1973–1987. doi: 10.1007/s10530-013-0425-z CrossRefGoogle Scholar
  79. van Wilgen BW, Fill JM, Baard J, Cheney C, Forsyth AT, Kraaij T (2016) Historical costs and projected future scenarios for the management of invasive alien plants in protected areas in the Cape Floristic Region. Biol Conserv 200:168–177CrossRefGoogle Scholar
  80. Vilà M, Lloret F (2000) Seed dynamics of the mast seeding tussock grass Ampelodesmos mauritanica in Mediterranean shrublands. J Ecol 88:479–491CrossRefGoogle Scholar
  81. Vilà M, Espinar JL, Hejda M et al (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708CrossRefPubMedGoogle Scholar
  82. Wardle DA, Nicholson KS, Rahman A (1996) Use of a comparative approach to identify allelopathic potential and relationship between allelopathy bioassays and ‘‘competition’’ experiments for ten grassland and plant species. J Chem Ecol 22:933–994CrossRefPubMedGoogle Scholar
  83. Warren RJ, Bahn V, Bradford MA (2012) The interaction between propagule pressure, habitat suitability and density-dependent reproduction in species invasion. Oikos 121:874–881CrossRefGoogle Scholar
  84. West NM, Matlaga DP, Davis AS (2014) Quantifying targets to manage invasion risk: light gradients dominate the early regeneration niche of naturalized and pre-commercial Miscanthus populations. Biol Invasions 16:1991–2001CrossRefGoogle Scholar
  85. Whistler WA, Elevitch CR (2006) Casuarina equisetifolia (reach she-oak) and C. cunninghamiana (river she-oak). In: Elevitch CR (ed) Species profiles for Pacific Island agroforestry. Permanent Agriculture Resources (PAR), Holualoa, Hawaii, p 16pGoogle Scholar
  86. Xiong SJ, Nilsson C (1999) The effects of plant litter on vegetation: a meta-analysis. J Ecol 87:984–994CrossRefGoogle Scholar
  87. Zaluar HLT, Scarano FR (2000) Facilitação em restingas de moitas: um século de buscas por espécies focais. In: Esteves FA, Lacerda LD (eds) Ecologia de Restingas e Lagoas Costeiras. NUPEM-UFRJ, Rio de Janeiro, pp 3–23Google Scholar
  88. Zar JH (1999) Biostatistical Analysis, 4th edn. Prentice Hall, New JerseyGoogle Scholar
  89. Zefferman E, Stevens JT, Charles GK, Dunbar-Irwin M, Emam T, Fick S, Morales SV, Wolf KM, Young DJN, Young TP (2015) Plant communities in harsh sites are less invaded: a summary of observations and proposed explanations. AoB PLANTS 7:plv056Google Scholar
  90. Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Revista Brasil Bot 34:431–446CrossRefGoogle Scholar
  91. Zimmermann TG, Andrade ACS, Richardson DM (2016) Experimental assessment of factors mediating the naturalisation of a globally invasive tree on sandy coastal plains: a case study from Brazil. AoB PLANTS 8: plw042; doi:  10.1093/aobpla/plw042

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Thalita G. Zimmermann
    • 1
  • Antonio C. S. Andrade
    • 1
  • David M. Richardson
    • 2
  1. 1.Laboratório de SementesInstituto de Pesquisas Jardim Botânico Do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Centre for Invasion Biology, Department of Botany and ZoologyStellenbosch University, MatielandStellenboschSouth Africa

Personalised recommendations