Landscape-level determinants of the spread and impact of invasive grasses in protected areas

Abstract

Anthropogenic disturbances play an important role in invasibility, and the traits of exotic species act as mediators of invasion success. The impact of exotic species can be evaluated through an association with invasion potential. The magnitude and potential severity of exotic species impacts can aid in decision making regarding the best conservation, restoration, management and control actions. In this sense, our objectives were to (1) evaluate the potential invasion risk of naturalized graminoid species in the Cerrado biome using risk analysis; (2) understand the magnitude of the impact of these species on protected areas by analysing the relationships between invasiveness, invasion potential and proximity to strictly protected areas, as well as to the biome as a whole; and (3) identify the drivers of spread contributing to species richness and abundance in the Cerrado. Our results showed that naturalized graminoid species in the Cerrado biome present invasion risks and potential impacts varying from medium to high. Additionally, these landscapes were vulnerable due to their proximity to protected areas, which act as filters against these species and against anthropogenic agents (human population and road density) that may increase the richness and population sizes of these plants. Based on our results, we recommend developing and prioritizing management and control strategies in strictly protected areas and in their surrounding areas to avoid the dispersal and establishment of aggressive species (African grasses) in their interiors, homogenization risks and the consequent loss of native biodiversity.

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References

  1. Alho CJR, Mamede S, Bitencourt K, Benites M (2011) Introduced species in the Pantanal: implications for conservation. Braz J Biol 71:321–325. https://doi.org/10.1590/S1519-69842011000200011

    Article  PubMed  CAS  Google Scholar 

  2. Almeida-Neto M, Prado PI, Kubota U et al (2010) Invasive grasses and native Asteraceae in the Brazilian Cerrado. Plant Ecol 209:109–122. https://doi.org/10.1007/s11258-010-9727-8

    Article  Google Scholar 

  3. Barbosa FG (2016) The future of invasive African grasses in South America under climate change. Ecol Inform 36:114–117. https://doi.org/10.1016/j.ecoinf.2016.10.006

    Article  Google Scholar 

  4. Barton K (2018) Multi-model inference. R package version 1.40.4. https://cran.r-project.org/web/packages/MuMIn/index.html. Accessed 20 Feb 2018

  5. Bellard C, Leroy B, Thuiller W et al (2016) Major drivers of invasion risks throughout the world. Ecosphere 7:1–14. https://doi.org/10.1002/ecs2.1241

    Article  Google Scholar 

  6. Blackburn TM, Essl F, Evans T et al (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol. https://doi.org/10.1371/journal.pbio.1001850

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton

    Google Scholar 

  8. Buckley YM, Anderson S, Catterall CP et al (2006) Management of plant invasions mediated by frugivore interactions. J Appl Ecol 43:848–857. https://doi.org/10.1111/j.1365-2664.2006.01210.x

    Article  Google Scholar 

  9. Burnham KP, Anderson DR (2004) Model selection and multimodel inference. Springer, New York

    Google Scholar 

  10. Christen D, Matlack G (2006) The role of roadsides in plant invasions: a demographic approach. Conserv Biol 20:385–391. https://doi.org/10.1111/j.1523-1739.2006.00315.x

    Article  PubMed  Google Scholar 

  11. Daehler CC, Denslow JS, Ansari S, Kuo HC (2004) A risk-assessment system for screening out invasive pest plants from Hawaii and other Pacific Islands. Conserv Biol 18:360–368. https://doi.org/10.1111/j.1523-1739.2004.00066.x

    Article  Google Scholar 

  12. 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. https://doi.org/10.1111/j.1365-2745.2009.01519.x

    Article  Google Scholar 

  13. Dick JTA, Laverty C, Lennon JJ et al (2017) Invader relative impact potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. J Appl Ecol 54:1259–1267. https://doi.org/10.1111/1365-2664.12849

    Article  Google Scholar 

  14. Dodonov P, Harper KA, de Oliveira XR, Silva Matos DM (2019) Spatial pattern of invasive and native graminoids in the Brazilian cerrado. Plant Ecol 220:741–756. https://doi.org/10.1007/s11258-019-00949-6

    Article  Google Scholar 

  15. Durigan G, de Siqueira MF, Franco GADC (2007) Threats to the Cerrado remnants of the state of São Paulo, Brazil. Sci Agric 64:355–363. https://doi.org/10.1590/S0103-90162007000400006

    Article  Google Scholar 

  16. Elgersma KJ, Ehrenfeld JG (2011) Linear and non-linear impacts of a non-native plant invasion on soil microbial community structure and function. Biol Invasions 13:757–768. https://doi.org/10.1007/s10530-010-9866-9

    Article  Google Scholar 

  17. Eviner VT, Garbach K, Baty JH, Hoskinson SA (2012) Measuring the effects of invasive plants on ecosystem services: challenges and prospects. Invasive Plant Sci Manag 5:125–136. https://doi.org/10.1614/IPSM-D-11-00095.1

    Article  Google Scholar 

  18. Ferreira LV, Parolin P, Matos DCL et al (2016) The effect of exotic grass Urochloa decumbens (Stapf) R.D.Webster (Poaceae) in the reduction of species richness and change of floristic composition of natural regeneration in the Floresta Nacional de Carajás, Brazil. An Acad Bras Cienc 88:589–597. https://doi.org/10.1590/0001-3765201620150121

    Article  PubMed  Google Scholar 

  19. Foxcroft LC (2009) Developing thresholds of potential concern for invasive alien species: hypotheses and concepts. Koedoe. https://doi.org/10.4102/koedoe.v51i1.157

    Article  Google Scholar 

  20. Foxcroft LC, Jarošík V, Pyšek P et al (2010) Protected-area boundaries as filters of plant invasions. Conserv Biol 25:400–405. https://doi.org/10.1111/j.1523-1739.2010.01617.x

    Article  PubMed  Google Scholar 

  21. Foxcroft LC, Pyšek P, Richardson DM et al (2017a) Plant invasion science in protected areas: progress and priorities. Biol Invasions 19:1353–1378. https://doi.org/10.1007/s10530-016-1367-z

    Article  Google Scholar 

  22. Foxcroft LC, van Wilgen NJ, Baard JA, Cole NS (2017b) Biological invasions in South African National Parks. Bothalia 47:1–12. https://doi.org/10.4102/abc.v47i2.2158

    Article  Google Scholar 

  23. Ganem RS, Drummond JA, de Franco JL (2013) Conservation polices and control of habitat fragmentation in the Brazilian Cerrado biome. Ambient Soc 16:99–118. https://doi.org/10.1590/S1414-753X2013000300007

    Article  Google Scholar 

  24. González-Moreno P, Diez JM, Ibáñez I et al (2014) Plant invasions are context-dependent: multiscale effects of climate, human activity and habitat. Divers Distrib 20:720–731. https://doi.org/10.1111/ddi.12206

    Article  Google Scholar 

  25. Gorgone-Barbosa E, Pivello VR, Bautista S et al (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

    Article  Google Scholar 

  26. Gorgone-Barbosa E, Pivello VR, Rissi MN, et al (2016) A importância da consideração de espécies invasoras no manejo integrado do fogo. In: Biodiversidade Bras. http://www.icmbio.gov.br/revistaeletronica/index.php/BioBR/article/view/522. Accessed 30 Aug 2017

  27. Hanley N, Roberts M (2019) The economic benefits of invasive species management. People Nat 1:124–137. https://doi.org/10.1002/pan3.31

    Article  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. Hoffmann WA, Lucatelli VMPC, Silva FJ et al (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

    Article  Google Scholar 

  30. Holm LRG, Plucknett DL, Pancho JV, Herberger JP (eds) (1977) The world’s worst weeds: distribution and biology, 1st edn. University Press of Hawaii, Honolulu

    Google Scholar 

  31. Instituto Hórus (2017) Protocolo para análise de risco de invasão por plantas exóticas. In: Análise risco para plantas exóticas (rede I3N – IABIN). https://institutohorus.org.br/analise-de-risco-para-especies-exoticas/. Accessed 2 Feb 2017

  32. Jeschke JM, Bacher S, Blackburn TM et al (2014) Defining the impact of non-native species. Conserv Biol 28:1188–1194. https://doi.org/10.1111/cobi.12299

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kissmann KG, Groth D (1997) Plantas infestantes e nocivas, 1st edn. BASF, São Paulo

    Google Scholar 

  34. Klink CA, Moreira AG (2002) Past and current human occupation, and land use. In: Oliveira P, Marquis R (eds) The cerrados of Brazil. Columbia University Press, New York, pp 69–88

    Google Scholar 

  35. Kumschick S, Nentwig W (2010) Some alien birds have as severe an impact as the most effectual alien mammals in Europe. Biol Conserv 143:2757–2762. https://doi.org/10.1016/j.biocon.2010.07.023

    Article  Google Scholar 

  36. Laverty C, Green KD, Dick JTA et al (2017) Assessing the ecological impacts of invasive species based on their functional responses and abundances. Biol Invasions 19:1653–1665. https://doi.org/10.1007/s10530-017-1378-4

    Article  Google Scholar 

  37. Lemke A, Kowarik I, von der Lippe M (2019) How traffic facilitates population expansion of invasive species along roads: the case of common ragweed in Germany. J Appl Ecol 56:413–422. https://doi.org/10.1111/1365-2664.13287

    Article  Google Scholar 

  38. Lewis JS, Farnsworth ML, Burdett CL et al (2017) Biotic and abiotic factors predicting the global distribution and population density of an invasive large mammal. Sci Rep 7:1–12. https://doi.org/10.1038/srep44152

    Article  Google Scholar 

  39. Lorenzi H (2000) Plantas daninhas do Brasil: terrestres, aquáticas, parasitas e tóxicas, 3rd edn. Instituto Plantarum, Nova Odessa

    Google Scholar 

  40. Marsh AS, Arnone JA, Bormann BT, Gordon JC (2000) The role of Equisetum in nutrient cycling in an Alaskan shrub wetland. J Ecol 88:999–1011. https://doi.org/10.1046/j.1365-2745.2000.00520.x

    Article  Google Scholar 

  41. Martins CR, Hay JDV, Walter BMT et al (2011) Impacto da invasão e do manejo do capim-gordura (Melinis minutiflora) sobre a riqueza e biomassa da flora nativa do Cerrado sentido restrito. Rev Bras Bot 34:73–90. https://doi.org/10.1590/S0100-84042011000100008

    Article  Google Scholar 

  42. Martins CR, Hay JDV, Scaléa M, Malaquias JV (2017) Management techniques for the control of Melinis minutiflora P. Beauv. (molasses grass): ten years of research on an invasive grass species in the Brazilian Cerrado. Acta Bot Brasilica 31(4):546–554. https://doi.org/10.1590/0102-33062016abb0433

    Article  Google Scholar 

  43. Mcdonald RI, Forman RTT, Kareiva P et al (2009) Urban effects, distance, and protected areas in an urbanizing world. Landsc Urban Plan 93:63–75. https://doi.org/10.1016/j.landurbplan.2009.06.002

    Article  Google Scholar 

  44. MMA (2011) SNUC – Sistema Nacional de Unidades de Conservação da Natureza

  45. MMA (2015) Mapeamento do Uso e Cobertura do Cerrado: Projeto TerraClass Cerrado 2013. In: Mapeamento do Uso e Cober. do Cerrado Proj. TerraClass Cerrado 2013. http://www.dpi.inpe.br/tccerrado/index.php?mais=1. Accessed 6 Apr 2016

  46. Oliveira JGD (Instituto de PJB do R de J (2014) Potencial da gramínea exótica braquiária, Urochloa decumbens (Stapf) R. D. Webster (Poaceae), como barreira à regeneração natural no Parque Nacional da Serra da Bodoquena. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro

  47. Panetta F, Gooden B (2017) Managing for biodiversity: impact and action thresholds for invasive plants in natural ecosystems. NeoBiota 34:53–66. https://doi.org/10.3897/neobiota.34.11821

    Article  Google Scholar 

  48. Parker IM, Simberloff D, Lonsdale WM et al (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19. https://doi.org/10.1023/A:1010034312781

    Article  Google Scholar 

  49. Pearson DE, Ortega YK, Eren Ö, Hierro JL (2016) Quantifying apparent impact and distinguishing impact from invasiveness in multispecies plant invasions. Ecol Appl 26:162–173. https://doi.org/10.1890/14-2345.1/suppinfo

    Article  PubMed  Google Scholar 

  50. Pivello VR (2011) The use of fire in the cerrado and Amazonian rainforests of Brazil: past and present. Fire Ecol 7:24–39. https://doi.org/10.4996/fireecology.0701024

    Article  Google Scholar 

  51. Pivello V, Carvalho V, Lopes P (1999a) 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

    Article  Google Scholar 

  52. Pivello VR, Shida CN, Meirelles ST (1999b) Alien grasses in Brazilian savannas: a threat to the biodiversity. Biodivers Conserv 8:1281–1294. https://doi.org/10.1023/A:1008933305857

    Article  Google Scholar 

  53. Pivello VR, Oliveras I, Miranda HS et al (2010) Effect of fires on soil nutrient availability in an open savanna in Central Brazil. Plant Soil 337:111–123. https://doi.org/10.1007/s11104-010-0508-x

    Article  CAS  Google Scholar 

  54. Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? Biol Invasions 193:97–125. https://doi.org/10.1007/978-3-540-36920-2_7

    Article  Google Scholar 

  55. Pyšek P, Jarošík V, Hulme PE et al (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob Change Biol 18:1725–1737. https://doi.org/10.1111/j.1365-2486.2011.02636.x

    Article  Google Scholar 

  56. Rauschert ESJ, Mortensen DA, Bloser SM (2017) Human-mediated dispersal via rural road maintenance can move invasive propagules. Biol Invasions 19:2047–2058. https://doi.org/10.1007/s10530-017-1416-2

    Article  Google Scholar 

  57. Ribeiro JF, Walter BMT (2008) As principais fitofisionomias do bioma Cerrado. In: Sueli Matiko Sano, Semíramis Pedrosa de Almeida JFR (ed) Cerrado: Ecologia e flora, 1st edn. Embrapa Cerrados/Embrapa Informação Tecnológica, pp 152–212

  58. Rossi RD, Martins CR, Viana PL et al (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 Bras 28:631–637. https://doi.org/10.1590/0102-33062014abb3390

    Article  Google Scholar 

  59. Rossiter NA, Setterfield SA, Douglas MM, Hutley LB (2003) Testing the grass-fire cycle: alien grass invasion in the tropical savannas of northern Australia. Divers Distrib 9:169–176. https://doi.org/10.1046/j.1472-4642.2003.00020.x

    Article  Google Scholar 

  60. Sampaio AB, Schmidt IB (2014) Espécies exóticas invasoras em unidades de conservação federais do Brasil. Biodiversidade Bras 32–49

  61. Sampaio AB, Guimarães TCS, Ziller SR et al (2019) Manejo De Espécies Invasoras Em Unidades De Conservação Federais, 3rd edn. Brasília, DF

    Google Scholar 

  62. Seabloom EW, Borer ET, Buckley Y et al (2013) Predicting invasion in grassland ecosystems: is exotic dominance the real embarrassment of richness? Glob Change Biol 19:3677–3687. https://doi.org/10.1111/gcb.12370

    Article  Google Scholar 

  63. Spear D, Foxcroft LC, Bezuidenhout H, McGeoch MA (2013) Human population density explains alien species richness in protected areas. Biol Conserv 159:137–147. https://doi.org/10.1016/j.biocon.2012.11.022

    Article  Google Scholar 

  64. Strassburg BBN, Latawiec AE, Barioni LG et al (2014) When enough should be enough: improving the use of current agricultural lands could meet production demands and spare natural habitats in Brazil. Glob Environ Change 28:84–97. https://doi.org/10.1016/j.gloenvcha.2014.06.001

    Article  Google Scholar 

  65. Strassburg BBN, Brooks T, Feltran-Barbieri R et al (2017) Moment of truth for the Cerrado hotspot. Nat Ecol Evol. https://doi.org/10.1038/s41559-017-0099

    Article  PubMed  Google Scholar 

  66. Stricker KB, Hagan D, Flory SL (2015) Improving methods to evaluate the impacts of plant invasions: lessons from 40 years of research. AoB Plants 7:plv028. https://doi.org/10.1093/aobpla/plv028

    Article  PubMed  PubMed Central  Google Scholar 

  67. Thiele J, Kollmann J, Markussen B, Otte A (2010) Impact assessment revisited: improving the theoretical basis for management of invasive alien species. Biol Invasions 12:2025–2035. https://doi.org/10.1007/s10530-009-9605-2.The

    Article  Google Scholar 

  68. Tripathi P, Dev Behera M, Roy PS (2017) Optimized grid representation of plant species richness in India-Utility of an existing national database in integrated ecological analysis. PLoS ONE 12:1–13. https://doi.org/10.1371/journal.pone.0173774

    Article  CAS  Google Scholar 

  69. Van Wilgen BW (2010) The evolution of fire management practices in savanna protected areas in South Africa. S Afr J Sci 105:343–349. https://doi.org/10.4102/sajs.v105i9/10.107

    Article  Google Scholar 

  70. Vicente J, Alves P, Randin C et al (2010) What drives invasibility? A multi-model inference test and spatial modelling of alien plant species richness patterns in northern Portugal. Ecography (Cop) 33:1081–1092. https://doi.org/10.1111/j.1600-0587.2010.6380.x

    Article  Google Scholar 

  71. Vicente JR, Pereira HM, Randin CF et al (2014) Environment and dispersal paths override life strategies and residence time in determining regional patterns of invasion by alien plants. Perspect Plant Ecol Evol Syst 16:1–10. https://doi.org/10.1016/j.ppees.2013.10.003

    Article  Google Scholar 

  72. Von Der Lippe M, Kowarik I (2007) Long-distance dispersal of plants by vehicles as a driver of plant invasions. Conserv Biol 21:986–996. https://doi.org/10.1111/j.1523-1739.2007.00722.x

    Article  PubMed  Google Scholar 

  73. Wang Y, Naumann U, Wright ST, Warton DI (2012) Mvabund: an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474. https://doi.org/10.1111/j.2041-210X.2012.00190.x

    Article  Google Scholar 

  74. 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

    Article  Google Scholar 

  75. Wittenberg R, Cock MJW (eds) (2001) Invasive alien species: a toolkit of best prevention and management practices. CABI, Wallingford

    Google Scholar 

  76. Zenni RD (2014) Analysis of introduction history of invasive plants in Brazil reveals patterns of association between biogeographical origin and reason for introduction. Austral Ecol 39:401–407. https://doi.org/10.1111/aec.12097

    Article  Google Scholar 

  77. Zenni RD (2015) The naturalized flora of Brazil: a step towards identifying future invasive non-native species. Rodriguesia 66:1137–1144. https://doi.org/10.1590/2175-7860201566413

    Article  Google Scholar 

  78. Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil. Rev Bras Bot 34:431–446. https://doi.org/10.1590/S0100-84042011000300016

    Article  Google Scholar 

  79. Zenni RD, Cunha WL, Musso C et al (2020) Synergistic impacts of co-occurring invasive grasses cause persistent effects in the soil-plant system after selective removal. Funct Ecol. https://doi.org/10.1111/1365-2435.13524

    Article  Google Scholar 

  80. Ziller SR, de Sá DM, Dudeque Zenni R (2019) Predicting invasion risk of 16 species of eucalypts using a risk assessment protocol developed for Brazil. Austral Ecol 44:28–35. https://doi.org/10.1111/aec.12649

    Article  Google Scholar 

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Acknowledgements

We would like to thank our colleagues at the Laboratory of Conservation Biology and Bioinvasion, Department of Biology, who contributed to the construction of the naturalized Cerrado species database and to the risk analysis. Additionally, we acknowledge the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq) and the Minas Gerais Research Support Foundation (Fundação de Amparo à Pesquisa de Minas Gerais – FAPEMIG) for supporting the Laboratory of Plant Ecology and the last author. The Brazilian Federal Agency for Support and Evaluation of Graduate Education (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES) provided a scholarship to the first author (Finance Code: 32004010017P3).

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Guimarães Silva, R., Zenni, R.D., Rosse, V.P. et al. Landscape-level determinants of the spread and impact of invasive grasses in protected areas. Biol Invasions 22, 3083–3099 (2020). https://doi.org/10.1007/s10530-020-02307-4

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Keywords

  • Risk analysis
  • Graminoids
  • Cerrado
  • Exotic species