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Biological Invasions

, Volume 20, Issue 12, pp 3621–3629 | Cite as

Impact of invasive grasses on Cerrado under natural regeneration

  • Gabriella Damasceno
  • Lara Souza
  • Vânia R. Pivello
  • Elizabeth Gorgone-Barbosa
  • Paula Z. Giroldo
  • Alessandra Fidelis
Original Paper

Abstract

Cerrado is the Brazilian neotropical savanna threatened by invasive African grasses. We aimed to quantify the impact of invasive Melinis minutiflora and Urochloa brizantha on the cover of different functional groups (native graminoids, forbs, shrubs) and the structure (bare soil and the cover of natives’ and invasives’ dead biomass) of regenerating plant communities. We hypothesized that the impact of invasives would be negative and more pronounced in the rainy period, given the great influence of seasonality in savannas. In three community types (non-invaded, invaded by M. minutiflora and invaded by U. brizantha) we evaluated the cover of functional groups and structural components by sampling 120 1 m × 1 m plots, four times a year. Using the Cohen’s D impact index, we showed that both invasive species reduced the cover of all native functional groups, decreased bare soil and increased total dead cover. Greatest effects occurred when M. minutiflora was present. M. minutiflora’s impact on total graminoids varied from positive in the Early-Dry season to negative in the Mid-Dry season, while the negative impact of U. brizantha on bare soil became more pronounced from the dry to the rainy season. Differences in the impacts caused by the invasive species are probably due to the large biomass produced by M. minutiflora versus the fast colonization and soil occupancy by U. brizantha. Overall, invaded versus non-invaded communities differed in structure, as well as both invaded communities differed from each other. Our results demonstrate the need to control these species for conservation and restoration of Cerrado ecosystems.

Keywords

Biodiversity conservation Community restoration Melinis minutiflora Neotropical savanna Urochloa brizantha 

Notes

Acknowledgements

The authors thank Ana Carolina Ferreira, Cíntia Souza, Evaldo Souza, Giovana Chiari, Heloiza Zirondi, Jonathan Galdi Rosa, Karen Castillioni, Lucas Barbosa, Luis Felipe Daibes, Mariana Dairel, Mariana Rissi, Natacha Silva, Priscilla Sperandio, Rafael Consolmagno, Tamires Zepon and Vagner Zanzarini for helping during the field work, and the staff of the Itirapina Ecological Station for their valuable help during the establishment and maintenance of the experimental plots. G.D. received financial support from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2015/10714-6), V.R.P. and A.F. were granted by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 305253/2015-8 and CNPq 306170/2015-9). This project was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2015/06743-0) and the Neotropical Grasslands Conservancy.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2018_1800_MOESM1_ESM.jpg (6.1 mb)
Supplementary material 1 (JPEG 6255 kb)

References

  1. Almeida ARP, Lucchesi AA, Abbado MR (1997) Efeito alelopático de espécies de Brachiaria Griseb. sobre algumas leguminosas forrageiras tropicais. II. Avaliações em casa de vegetação. Bol Ind Anim 54:45–54Google Scholar
  2. Almeida-Neto M, Prado PI, Kubota U, Bariani JM, Aguirre GH, Lewinsohn TM (2010) Invasive grasses and native Asteraceae in the Brazilian cerrado. Plant Ecol 209:109–122.  https://doi.org/10.1007/s11258-010-9727-8 CrossRefGoogle Scholar
  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Anten NPR, Hirose T (1999) Interspecific differences in above-ground growth patterns result in spatial and temporal partitioning of light among species in a tall-grass meadow. J Ecol 87:583–597.  https://doi.org/10.1046/j.1365-2745.1999.00365.x CrossRefGoogle Scholar
  5. Barbosa EG, Pivello VR, Meirelles ST (2008) Allelopathic evidence in Brachiaria decumbens and its potential to invade the Brazilian cerrados. Braz Arch Biol Technol 51:825–831.  https://doi.org/10.1590/S1516-89132008000400021 CrossRefGoogle Scholar
  6. Barreira S, Alvarenga Botelho S, Scolforo JR, Mello JM (2000) Efeitos de diferentes intensidades de corte seletivo sobre a regeneração natural de Cerrado. CERNE 6:40–51Google Scholar
  7. Baruch Z, Ludlow M, Davis R (1985) Photosynthetic responses of native and introduced C4 grasses from Venezuelan savannas. Oecologia 67:388–393.  https://doi.org/10.1007/BF00384945 CrossRefPubMedGoogle Scholar
  8. Baruch Z, Hernandez ABR, Montilla MG (1989) Dinamica del crecimiento, fenologia y reparticion de biomasa gramineas nativas e introducidas de una sabana neotropical. Ecotropicos 2:1–13Google Scholar
  9. Batmanian GJ, Haridasan M (1985) Primary production and accumulation of nutrients by the ground layer community of cerrado vegetation of central Brazil. Plant Soil 88:437–440.  https://doi.org/10.1007/BF02197500 CrossRefGoogle Scholar
  10. Brooks KJ, Setterfield SA, Douglas MM (2010) Exotic grass invasions: applying a conceptual framework to the dynamics of degradation and restoration in Australia’s tropical savannas. Restor Ecol 18:188–197.  https://doi.org/10.1111/j.1526-100X.2008.00470.x CrossRefGoogle Scholar
  11. Coutinho LM (1990) Fire in the ecology of the Brazilian cerrado. In: Goldammer J (ed) Fire in the tropical biota. Ecological studies, vol 84. Springer, Berlin, pp 82–105CrossRefGoogle Scholar
  12. D’Antonio CM, Meyerson LA (2002) Exotic plant species as problems and solutions in ecological restoration. Restor Ecol 10:703–713.  https://doi.org/10.1046/j.1526-100X.2002.01051.x CrossRefGoogle Scholar
  13. D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87CrossRefGoogle Scholar
  14. da Silveira ER, de Melo ACG, Contieri WA, Durigan G (2013) Controle de gramíneas exóticas em plantio de restauração de Cerrado. In: Durigan G, Ramos VSR (eds) Manejo Adaptativo: primeiras experiências na restauração de ecossistemas. Páginas e Letras Editora e Gráfica, São Paulo, pp 5–8Google Scholar
  15. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211.  https://doi.org/10.1146/132403 CrossRefGoogle Scholar
  16. de 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 Manag 262:1452–1459.  https://doi.org/10.1016/j.foreco.2011.06.046 CrossRefGoogle Scholar
  17. Deeks JJ, Douglas GA, Michael JB (2001) Statistical methods for examining heterogeneity and combining results from several studies in meta-analysis. In: Egger M, Altman DG, Smith GD (eds) Systematic reviews in health care: meta-analysis in context, 2nd edn. BMJ Publishing Group, London, pp 285–312CrossRefGoogle Scholar
  18. Drake JM, Cleland EE, Horner-Devine MC, et al (2008) Do Non-native Plant Species Affect the Shape of Productivity-diversity Relationships? Am Midl Nat 159:55-56. https://www.jstor.org/stable/20491311 CrossRefGoogle Scholar
  19. Durigan G, Contieri WA, Franco GADC, Garrido MAO (1999) Indução do processo de regeneração da vegetação de Cerrado em área de pastagem, Assis, SP. Acta Bot Brasilica 12:421–429CrossRefGoogle Scholar
  20. Durigan G, Ferreira De Siqueira M, Daher GA, Franco C (2007) Threats to the cerrado remnants. Sci Agric (Piracicaba) 64:355–363.  https://doi.org/10.1590/S0103-90162007000400006 CrossRefGoogle Scholar
  21. Eiten G (1972) The Cerrado vegetation of Brazil. Bot Rev 38:201–338.  https://doi.org/10.1007/BF02859158 CrossRefGoogle Scholar
  22. Emery SM (2007) Limiting similarity between invaders and dominant species in herbaceous plant communities? J Ecol 95:1027–1035.  https://doi.org/10.1111/j.1365-2745.2007.01274.x CrossRefGoogle Scholar
  23. Emery SM, Gross KL (2007) Dominant species identity, not community evennes, regulates invasion in experimental grassland plant communities. Ecology 88:954–964.  https://doi.org/10.1890/06-0568 CrossRefPubMedGoogle Scholar
  24. Engelhardt MJ, Anderson RC (2011) Phenological niche separation from native species increases reproductive success of an invasive species: Alliaria petiolata (Brassicaceae)—garlic mustard. J Torrey Bot Soc 138:418–433CrossRefGoogle Scholar
  25. Facelli JM, Facelli E (1993) Interactions after death: plant litter controls priority effects in a successional plant community. Oecologia 95:277–282.  https://doi.org/10.1007/BF00323500 CrossRefPubMedGoogle Scholar
  26. Fargione J, Tilman D (2005) Niche differences in phenology and rooting depth promote coexistence with a dominant C4 bunchgrass. Oecologia 143:598–606.  https://doi.org/10.1007/s00442-005-0010-y CrossRefPubMedGoogle Scholar
  27. Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. Proc Natl Acad Sci USA 100:8916–8920.  https://doi.org/10.1073/pnas.1033107100 CrossRefPubMedGoogle Scholar
  28. Fisher MJ, Kerridge PC (1996) The agronomy and physiology of Brachiaria species. In: Miles JW, Mass BL, Valle CB (eds) Brachiaria: Biology, agronomy and improvement. Centro Internacional de Agricultura Tropical (CIAT) and Empresa Brasileira de Pesquisa Agropecuária/Centro Nacional de Pesquisa de Gado de Corte (EMBRAPA/CNPGC), Cali, pp 43–52Google Scholar
  29. Flory SL, Clay K (2010) Non-native grass invasion suppresses forest succession. Oecologia 164:1029–1038.  https://doi.org/10.1007/s00442-010-1697-y CrossRefPubMedGoogle Scholar
  30. Franco AC (2002) Ecophysiology of wood plants. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil: Ecology and natural history of a neotropical savanna, Columbia University Press, New York, pp. 178–198. www.jstor.org/stable/10.7312/oliv12042.13, pp 178–200
  31. Gorgone-Barbosa E (2016) A relação entre fogo e uma gramínea invasora no Cerrado: O fogo pode ser utilizado como uma estratégia de controle? Thesis, Universidade Estadual Paulista “Júlio de Mesquita Filho”Google Scholar
  32. Gorgone-Barbosa E, Pivello VR, Bautista S, Zupo T, Rissi MN, Fidelis A (2015) How can an invasive grass affect fire behavior in a tropical savanna? A community and individual plant level approach. Biol Invasions 17:423–431.  https://doi.org/10.1007/s10530-014-0740-z CrossRefGoogle Scholar
  33. Hoffmann WA (1998) Post-burn reproduction of woody plants in a neotropical savanna: the relative importance of sexual and vegetative reproduction. J Appl Ecol 35:422–433.  https://doi.org/10.1046/j.1365-2664.1998.00321.x CrossRefGoogle Scholar
  34. Hoffmann WA, Haridasan M (2008) The invasive grass, Melinis minutiflora, inhibits tree regeneration in a Neotropical savanna. Austral Ecol 33:29–36.  https://doi.org/10.1111/j.1442-9993.2007.01787.x CrossRefGoogle Scholar
  35. Hoffmann WA, Hoffmann WA, Lucatelli VMPC, Silva FJ, Azeuedo INC, Marinho MS, Albuquerque AMS, Lopes AO, Moreira SP (2004) Impact of the invasive alien grass Melinis minutiflora at the savanna-forest ecotone in the Brazilian cerrado. Divers Distrib 10:99–103.  https://doi.org/10.1111/j.1366-9516.2004.00063.x CrossRefGoogle Scholar
  36. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefGoogle Scholar
  37. Klink CA (1994) Effects of clipping on size and tillering of native and African grasses of the Brazilian savannas (the cerrado). Oikos 70:365–376.  https://doi.org/10.2307/3545774 CrossRefGoogle Scholar
  38. Kuebbing SE, Souza L, Sanders NJ (2014) Effects of co-occurring non-native invasive plant species on old-field succession. For Ecol Manag 324:196–204CrossRefGoogle Scholar
  39. Kuebbing SE, Classen AT, Sanders NJ, Simberloff D (2015) Above- and below-ground effects of plant diversity depend on species origin: an experimental test with multiple invaders. New Phytol 208:727–735.  https://doi.org/10.1111/nph.13488 CrossRefPubMedGoogle Scholar
  40. Lannes LS, Bustamante MMC, Edwards PJ, Venterink HO (2012) Alien and endangered plants in the Brazilian cerrado exhibit contrasting relationships with vegetation biomass and N:P stoichiometry. New Phytol 196:816–823.  https://doi.org/10.1111/j.1469-8137.2012.04363.x CrossRefPubMedGoogle Scholar
  41. Martins CR, Leite LL, Haridasan M (2004) Molasses grass (Melinis minutiflora P. Beauv.): an exotic species compromising the recuperation of degraded areas in conservation units. Rev Árvore 28:739–747.  https://doi.org/10.1590/s0100-67622004000500014 CrossRefGoogle Scholar
  42. Martins CR, Hay JDV, Walter BMT, Proença CEB, Vivaldi LJ (2011) Impact of invasion and management of molasses grass (Melinis minutiflora) on the native vegetation of the Brazilian Savanna. Brazilian J Bot 34:73–90.  https://doi.org/10.1590/s0100-84042011000100008 CrossRefGoogle Scholar
  43. McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 55:259–294CrossRefGoogle Scholar
  44. Mozdzer TJ, Langley JA, Mueller P, Megonigal JP (2016) Deep rooting and global change facilitate spread of invasive grass. Biol Invasions 18:2619–2631.  https://doi.org/10.1007/s10530-016-1156-8 CrossRefGoogle Scholar
  45. Munhoz CBR, Felfili JM (2005) Fenologia do estrato herbáceo-subarbustivo de uma comunidade de campo sujo na Fazenda Água Limpa no Distrito Federal, Brasil. Acta Bot Brasilica 19:979–988.  https://doi.org/10.1590/S0102-33062005000400031 CrossRefGoogle Scholar
  46. Oksanen J, Blanchet FG, Kindt R et al (2016) Vegan: community ecology package. Commun Ecol. Package versionGoogle Scholar
  47. Oliveira APP, Pereira SR, Cândido ACS, Laura VA, Peres MTLP (2016) Can allelopathic grasses limit seed germination and seedling growth of mutambo? A test with two species of Brachiaria grasses. Planta Daninha 34:639–648.  https://doi.org/10.1590/s0100-83582016340400003 CrossRefGoogle Scholar
  48. Orlóci L (1967) An agglomerative method for classification of plant communities. Br Ecol Soc 55:193–206Google Scholar
  49. Pilon NAL, Buisson E, Durigan G (2018) Restoring Brazilian savanna ground layer vegetation by topsoil and hay transfer. Restor Ecol 26:73–81.  https://doi.org/10.1111/rec.12534 CrossRefGoogle Scholar
  50. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) nlme: linear and nonlinear mixed effects models. R package version 3.1-131. https://CRAN.R-project.org/package=nlme
  51. Pivello VR, Coutinho LM (1996) A qualitative successional model to assist in the management of Brazilian cerrados. For Ecol Manag 87:127–138.  https://doi.org/10.1016/S0378-1127(96)03829-7 CrossRefGoogle Scholar
  52. Pivello VR, Shida CN, Meirelles ST (1999a) Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodivers Conserv 8:1281–1294.  https://doi.org/10.1023/A:1008933305857 CrossRefGoogle Scholar
  53. Pivello V, Carvalho V, Lopes P (1999b) Abundance and distribution of native and alien grasses in a “Cerrado”(Brazilian Savanna) biological reserve. Biotropica 31:71–82.  https://doi.org/10.1111/j.1744-7429.1999.tb00117.x CrossRefGoogle Scholar
  54. Pokorny ML, Sheley RL, Zabinski CA, Engel RE, Svejcar TJ, Borkowski JJ (2005) Plant functional group diversity as a mechanism for invasion resistance. Restor Ecol 13:448–459.  https://doi.org/10.1111/j.1526-100X.2005.00056.x CrossRefGoogle Scholar
  55. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org
  56. Reed HE, Seastedt TR, Blair JM (2005) Ecological consequences of C4 grass invasion of a C4 grassland: a dilemma for management. Ecol Appl 15:1560–1569.  https://doi.org/10.1890/04-0407 CrossRefGoogle Scholar
  57. Rossi RD, Martins CR, Viana PL, Rodrigues EL, Eugênio JCF (2014) Impact of invasion by molasses grass (Melinis minutiflora P. Beauv.) on native species and on fires in areas of campo-cerrado in Brazil. Acta Bot Brasilica 28:631–637.  https://doi.org/10.1590/0102-33062014abb3390 CrossRefGoogle Scholar
  58. Rossiter N, Setterfield SA, Douglas MM et al (2004) Exotic grass invasion in the tropical savanna of northern Australia: ecosystem consequences. Fuel 2004:168–171Google Scholar
  59. Sampaio AB, Schmidt IB (2014) Espécies exóticas invasoras em unidades de conservação federais do Brasil. Biodivers Bras 3:32–49Google Scholar
  60. Silva JSO, Haridasan M (2007) Acúmulo de biomassa aérea e concentração de nutrientes em Melinis minutiflora P. Beauv. e gramíneas nativas do cerrado. Rev Bras Botânica 30:337–344.  https://doi.org/10.1590/S0100-84042007000200016 CrossRefGoogle Scholar
  61. Suding KN, Gross KL (2006) Modifying native and exotic species richness correlations: the influence of fire and seed addition. Ecol Appl 16:1319–1326.  https://doi.org/10.1016/j.tree.2003.10.005 CrossRefPubMedGoogle Scholar
  62. Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53.  https://doi.org/10.1016/j.tree.2003.10.005 CrossRefPubMedGoogle Scholar
  63. Vila 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 14:702–708.  https://doi.org/10.1111/j.1461-0248.2011.01628.x CrossRefPubMedGoogle Scholar
  64. Vitousek PM (1992) Effects of alien plants on native ecosystems. In: Stone CP, Smith CW, Tunison JT (eds) Alien plant species in native ecosystems of Hawai’i: management and research. University of Hawai’i Cooperative National Park Resources Studies Unit, Honolulu, pp 29–41Google Scholar
  65. Westoby M, Walker B, Noy-Meir I (1989) Opportunistic management for rangelands not at equilibrium. J Range Manag 42:266–274CrossRefGoogle Scholar
  66. Wikum DA, Shanholtzer GF (1978) Application of the Braun-Blanquet cover-abundance scale for vegetation analysis in land development studies. Environ Manag 2:323–329.  https://doi.org/10.1007/BF01866672 CrossRefGoogle Scholar
  67. Williams DG, Baruch Z (2000) African grass invasion in the Americas: ecosystem consequences and the role of ecophysiology. Biol Invasions 2:123–140.  https://doi.org/10.1023/A:1010040524588 CrossRefGoogle Scholar
  68. Wilsey BJ, Daneshgar PP, Hofmockel K, Polley HW (2014) Invaded grassland communities have altered stability-maintenance mechanisms but equal stability compared to native communities. Ecol Lett 17:92–100.  https://doi.org/10.1111/ele.12213 CrossRefPubMedGoogle Scholar
  69. Zanchetta D, Delgado JM, Silva CEF, Reis CM, Silva Da Luca EF, Fernandes FS, Dutra-Lutgens H, Tannus JLS, Pinheiro LS, Martins MR, Sawaya R (2006) Plano de manejo integrado—Estações Ecológica e Experimental de Itirapina—SP. 1ª Revisão. Instituto FlorestalGoogle Scholar
  70. Zanchi FB, Waterloo MJ, Aguiar LJG et al (2009) Estimativa do Índice de Área Foliar (IAF) e Biomassa em pastagem no estado de Rondônia, Brasil. Acta Amazon 39:335–348CrossRefGoogle Scholar
  71. Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Rev Bras Botânica 34:431–446.  https://doi.org/10.1590/S0100-84042011000300016 CrossRefGoogle Scholar
  72. Ziller SR, Dechoum MS (2013) Plantas e vertebrados exóticos invasores em unidades de conservação no Brasil. Biodivers Bras 3:4–31Google Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Laboratory of Vegetation Ecology, Instituto de BiociênciasUniversidade Estadual Paulista (UNESP)Rio ClaroBrazil
  2. 2.Oklahoma Biological Survey & Department of Microbiology and Plant BiologyUniversity of OklahomaNormanUSA
  3. 3.Departamento de EcologiaUniversidade de São PauloSão PauloBrazil

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