Biological Invasions

, Volume 20, Issue 10, pp 2753–2765 | Cite as

Combining the effects of biological invasion and climate change into systematic conservation planning for the Atlantic Forest

  • Guilherme de Oliveira
  • Bruno de Souza Barreto
  • Daniela da Silva dos Santos
  • Vinícius Queiroz de Matos
  • Maria Cecília Seara Santos
Original Paper


Biological invasions and climate changes are the major causes of changes in biodiversity, which reduce, shift, and extinguish species ranges. While climate changes have been widely used in systematic conservation planning (SCP), biological invasions are rarely considered. Here, we combine the effects of climate changes and Artocarpus heterophyllus Lam. (Moraceae) invasion on the SCP for endemic aromatic fruit tree species from the Atlantic Forest (EFAF). We tested the effect of invasion on SCP measures of species turnover, biotic stability, and irreplaceability. Ecological niche models were used to establish species environmental suitability for the preindustrial period for both invasive species and EFAF and to forecast to the end of the century (2080–2100). We calculated the niche overlap between the invasive species and EFAF and tested the overlap significance using a null model. We tested the biological invasion effect on the results using results with no species invasion correction. The niche overlap between A. heterophyllus and EFAF was significant for 50% of species in the preindustrial period and for 33% in the future. The spatial patterns of species turnover, biotic stability, and irreplaceability had significant effects on biological invasion changing the spatial pattern in both shape and magnitude, which can misplace and overvalue conservation priorities. We showed that the disregard of biological invasion on SCP can cause negative effects on SCP under climate change. We strongly recommend accounting for biological invasion in the evaluation of SCP.


Ensemble forecast Endemism Conservation priorities Species turnover Biotic stability Irreplaceability 



This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [442103/2014-0] and developed in the context of the National Institutes for Science and Technology (INCT) in Ecology, Evolution and Biodiversity Conservation, supported by MCTIC/CNPq [465610/2014-5] and FAPEG. DSS and MCSS are grateful for the scholarship provided by FAPESB [6166/2014 and 5878/2015]. We are grateful to Dr. Thiago F. Rangel for providing the use of BioEnsembles, to the World Climate Research Programmer’s Working Group on Coupled Modeling for providing CMIP5, to the climate-modeling group from NCAR for producing and making available CCSM, to Dr. Alessandra N. Caiafa for the first insight on the risk of jackfruit invasion, and to two anonymous reviewers that helped with their suggestions to improve and clarify previous versions of our manuscript.

Supplementary material

10530_2018_1727_MOESM1_ESM.docx (888 kb)
Supplementary material 1 (DOCX 887 kb)


  1. Abreu RCR, Rodrigues PJFP (2010) Exotic tree Artocarpus heterophyllus (Moraceae) invades the Brazilian Atlantic Rainforest. Rodriguésia 61:677–688CrossRefGoogle Scholar
  2. Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232CrossRefGoogle Scholar
  3. Andelman S, Willig MR (2002) Alternative configurations of conservation reserves for Paraguayan bats: considerations of spatial scale. Conserv Biol 16:1352–1363CrossRefGoogle Scholar
  4. Andelman S, Ball I, Davis F, Toms D (1999) SITES v. 1.0, an analytical toolbox for designing ecoregional conservation portfolios. Technical report, The Nature Conservancy,
  5. Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends Ecol Evol 22:42–47CrossRefGoogle Scholar
  6. Baliga MS, Shivashankara AR, Haniadka R, Dsouza J, Bhat HP (2011) Phytochemistry, nutritional and pharmacological properties of Artocarpus heterophyllus Lam (jackfruit): a review. Food Res Int 44:1800–1811CrossRefGoogle Scholar
  7. Balmford A, Moore JL, Brooks T, Burgess N, Hansen LA, Williams P, Rahbek C (2001) Conservation conflicts across Africa. Science 291:2616–2619CrossRefGoogle Scholar
  8. Barbet-Massin M, Jiguet F, Albert CH, Thuiller W (2012) Selecting pseudo-absences for species distribution models: How, where, and how many? Methods Ecol Evol 3:327–338CrossRefGoogle Scholar
  9. Bellard C, Leclerc C, Leroy B, Bakkenes M, Veloz S, Thuiller W, Courchamp W (2014) Vulnerability of biodiversity hotspots to global change. Global Ecol Biogeogr 23:1376–1386CrossRefGoogle Scholar
  10. Bergallo HG, Bergallo AC, Rocha HB, Rocha CFD (2016) Invasion by Artocarpus heterophyllus (Moraceae) in an island in the Atlantic Forest Biome, Brazil: distribution at the landscape, level, density and need for control. J Coast Conserv 20:191–198CrossRefGoogle Scholar
  11. Bini LM, Diniz-Filho JAF, Rangel TLFVB, Bastos RP, Pinto MP (2006) Challenging Wallacean and Linnean shortfalls: knowledge gradients and conservation planning in a biodiversity hotspot. Divers Distrib 12:475–482CrossRefGoogle Scholar
  12. Bini LM, Diniz-Filho JAF, Rangel TFLVB, Akre TSB, Albaladejo RG, Albuquerque FS, Aparicio A, Araújo MB, Baselga A, Beck J, Belloq I, Böhning-Gaese K, Borges PAV, Castro-Parga I, Chey VK, Chown SL, De Marco P, Dobkin DS, Ferrer-Gastán D, Field R, Filloy J, Fleishman E, Gómez JF, Hortal J, Iverson JB, Kerr JT, Kissling D, Kitching IJ, León-Cortés JL, Lobo JM, Montoya D, Morales-Castilla I, Moreno JC, Oberdoff T, Olalla-Tárraga MÁ, Pausas JG, Qian H, Rahbek C, Rodríguez MÁ, Rueda M, Ruggiero A, Sackmann P, Sanders NJ, Terribile LC, Vetaas OR, Hawkins BA (2009) Coefficients shifts in geographical ecology: an empirical evaluation of spatial and non-spatial regression. Ecography 32:193–204CrossRefGoogle Scholar
  13. Boni R, Novelli FZ, Silva AG (2009) Um alerta para os riscos de bioinvasão de jaqueiras, Artocarpus heterophyllus Lam., na Reserva Biológica Paulo Fraga Rodrigues, antiga Reserva Biológica Duas Bocas, no Espírito Santo, Sudeste do Brasil. Natureza on Line 7:51–55Google Scholar
  14. Bregman TP, Lees AC, Seddon N, MacGregor HEA, Darski B, Aleixo A, Bonsall MB, Tobias JA (2015) Species interactions regulate the collapse of biodiversity and ecosystem function in tropical forest fragments. Ecology 96:2692–2704CrossRefGoogle Scholar
  15. Bregman TP, Lees AC, MacGregor HEA, Darski B, de Moura NG, Aleixo A, Barlow J, Tobias JA (2016) Using avian functional traits to assess the impact of land-cover change on ecosystem processes linked to resilience in tropical forests. Proc R Soc B 283:20161289CrossRefGoogle Scholar
  16. Brice MH, Pellerin S, Poulin M (2017) Does urbanization lead to taxonomic and functional homogenization in riparian forests? Divers Distrib 23:828–840CrossRefGoogle Scholar
  17. Buisson L, Thuiller W, Casajus N, Lek S, Grenouillet G (2010) Uncertainty in ensemble forecasting of species distribution. Global Change Biol 16:1145–1157CrossRefGoogle Scholar
  18. Cabeza M, Moilanen A (2001) Design of reserve networks and the persistency of biodiversity. Trends Ecol Evol 16:242–248CrossRefGoogle Scholar
  19. Collevatti RG, Terribile LC, Lima-Ribeiro MS, Nabout JC, de Oliveira G, Rangel TF, Rabelo SG, Diniz-Filho JAF (2012) A coupled phylogeographical and species distribution modelling approach recovers the demographical history of a neotropical seasonally dry forest tree species. Mol Ecol 21:5843–5863CrossRefGoogle Scholar
  20. Collevatti RG, Lima-Ribeiro MS, Diniz-Filho JAF, de Oliveira G, Dobrovolski R, Terribile LC (2013) Stability of Brazilian seasonally dry forests under climate change: inferences for long-term conservation. Am J Plant Sci 4:792–805CrossRefGoogle Scholar
  21. De Oliveira G (2018) Human occupation explains species invasion better than biotic stability: evaluating Artocarpus heterophyllus Lam. (Moraceae; jackfruit) invasion in the Neotropics. J Plant Ecol. CrossRefGoogle Scholar
  22. De Oliveira G, Diniz-Filho JAF (2011) Evaluating environmental and geometrical constraints on endemic vertebrates of the semiarid Caatinga (Brazil). Basic Appl Ecol 12:664–673CrossRefGoogle Scholar
  23. De Oliveira G, Diniz-Filho JAF, Bini LM, Rangel TFLVB (2009) Conservation biogeography of mammals in the Cerrado biome under the unified theory of macroecology. Acta Oecol 35:630–638CrossRefGoogle Scholar
  24. De Oliveira G, Rangel TF, Lima-Ribeiro MS, Terribile LC, Diniz-Filho JAF (2014) Evaluating, partitioning, and mapping the spatial autocorrelation component in ecological niche modeling: a new approach based on environmentally equidistant records. Ecography 37:637–647CrossRefGoogle Scholar
  25. De Oliveira G, Lima-Ribeiro MS, Terribile LC, Dobrovolski R, Telles MPC, Diniz-Filho JAF (2015) Conservation biogeography of the Cerrado’s wild edible plants under climate change: linking biotic stability with agricultural expansion. Am J Bot 102:1–8CrossRefGoogle Scholar
  26. Dietz H, Edwards PJ (2006) Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87:1359–1367CrossRefGoogle Scholar
  27. Diniz-Filho JAF, Bini LM (2005) Modelling geographical patterns in species richness using eigenvector-based spatial filters. Global Ecol Biogeogr 14:177–185CrossRefGoogle Scholar
  28. Diniz-Filho JAF, Bini LM, Hawkins BA (2003) Spatial autocorrelation and red herrings in geographical ecology. Global Ecol Biogeogr 12:53–64CrossRefGoogle Scholar
  29. Diniz-Filho JAF, Bini LM, Pinto MP, Terribile LC, de Oliveira G, Vieira CM, Blamires D, Barreto BS, Carvalho P, Rangel TFLVB, Tôrres NM, Bastos R (2008) Conservation planning: a macroecological approach using the endemic terrestrial vertebrates of the Brazilian Cerrado. Oryx 42:567–577CrossRefGoogle Scholar
  30. Diniz-Filho JAF, Bini LM, Rangel TF, Loyola RD, Hof C, Nogues-Bravo D, Araújo MB (2009) Partitioning and mapping uncertainties in ensembles of forecasts of species turnover under climate change. Ecography 32:897–906CrossRefGoogle Scholar
  31. Diniz-Filho JAF, Rodrigues H, Telles MP, de Oliveira G, Terribile LC, Soares TN, Nabout JC (2015) Correlation between genetic diversity and environmental suitability: taking uncertainty from ecological niche models into account. Mol Ecol Resour 15:1059–1066CrossRefGoogle Scholar
  32. Dobrovolski R, Loyola RD, Guilhaumon F, Gouveia SF, Diniz-Filho JAF (2013) Global agricultural expansion and carnivore conservation biogeography. Biol Conserv 165:162–170CrossRefGoogle Scholar
  33. Donoso I, Garcia D, Roduiguez-Perez J, Martinez D (2016) Incorporating seed fate into plant-frugivore networks increases interaction diversity across plant regeneration stages. Oikos 125:1762–1771CrossRefGoogle Scholar
  34. Eisenhauer N, Fisichelli NA, Frelich LE, Reich PB (2012) Interactive effects of global warming and ‘global worming’ on the initial establishment of native and exotic herbaceous plant species. Oikos 121:1121–1133CrossRefGoogle Scholar
  35. Fabricante JR, Araújo KCT, Andrade LA, Ferreira JVA (2012) Invasão biológica de Artocarpus heterophyllus Lam. (Moraceae) em um fragmento de Mata Atlântica no Nordeste do Brasil: impactos sobre a fitodiversidade e os solos dos sítios invadidos. Acta Bot Bras 26:339–407CrossRefGoogle Scholar
  36. Franklin J (2009) Mapping species distribution: spatial inference and prediction. Cambridge University Press, CambridgeGoogle Scholar
  37. Freitas WK, Magalhães LMS, Resende AS, Brasil FC, Vivès LR, Pinheiro MAS, Filho PL, Luz RV (2017) Invasion impact of Artocarpus heterophyllus Lam. (Moraceae) at the edge of an Atlantic Forest fragment in the municipality of Rio de Janeiro, Brazil. Biosci J 33:422–433CrossRefGoogle Scholar
  38. Giakoumi S, Guilhaumon F, Kark S, Terlizzi A, Claudet J, Felline S, Cerrano C, Coll M, Danovaro R, Fraschetti S, Koutsoubas D, Ledoux J, Mazor T, Merigot B, Micheli F, Katsanevakis S (2016) Space invaders; biological invasions in marine conservation planning. Divers Distrib 22:1220–1231CrossRefGoogle Scholar
  39. Giovanni RL, Bernacci C, Siqueira MF, Rocha FS (2012) The real task of selecting records for ecological niche models. Nat Conservacao 10:139–144CrossRefGoogle Scholar
  40. Griffith DA (2003) Spatial autocorrelation and spatial filtering—gaining understanding through theory and scientific visualization. Springer, BerlinCrossRefGoogle Scholar
  41. Griffith DA, Peres-Neto PR (2006) Spatial modeling in ecology: the flexibility of eigenfunction spatial analysis. Ecology 87:2603–2613CrossRefGoogle Scholar
  42. Hawkins BA, Diniz-Filho JAF (2002) The mid-domain effect cannot explain the diversity gradient of Neartic birds. Global Ecol Biogeogr 11:419–426CrossRefGoogle Scholar
  43. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15CrossRefGoogle Scholar
  44. IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Summaries, frequently asked questions, and cross-chapter boxes. A contribution of working group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. World Meteorological Organization, Geneva, Switzerland, p 190Google Scholar
  45. Jetz W, Rahbek C (2001) Geometric constraints explain much of the species richness pattern in African birds. Proc Natl Acad Sci USA 98:5661–5666CrossRefGoogle Scholar
  46. Legendre P (1993) Spatial autocorrelation—trouble or new paradigm. Ecology 74:1659–1673CrossRefGoogle Scholar
  47. Lemes P, Loyola RD (2013) Accommodating species climate-forced dispersal and uncertainties in spatial conservation planning. PLoS ONE 8:e54323CrossRefGoogle Scholar
  48. Levine JM (2008) Biological invasions. Curr Biol 18:57–60CrossRefGoogle Scholar
  49. Lima-Ribeiro MS, Varela S, González-Hernandez J, de Oliveira G, Diniz-Filho JAF, Terribile LC (2015) ecoClimate: a database of climate data from multiple models for past, present, and future for macroecologists and biogeographers. Biodivers Inform 10:1–21CrossRefGoogle Scholar
  50. Luck GW (2007) A review of the relationships between human population density and biodiversity. Biol Rev 82:607–645CrossRefGoogle Scholar
  51. Margules CR, Pressey RL (2000) Systematic conservation planning. Nature 405:243–253CrossRefGoogle Scholar
  52. Mata RA, Tidon R, de Oliveira G, Vilela B, Diniz-Filho JAF, Rangel TF, Terribile LC (2017) Stacked species distribution and macroecological models provide incongruent predictions of species richness for Drosophilidae in the Brazilian savanna. Insect Conserv Divers 10:415–424CrossRefGoogle Scholar
  53. Meir E, Andelman S, Possingham HP (2004) Does conservation planning matter in a dynamic and uncertain world? Ecol Lett 7:615–622CrossRefGoogle Scholar
  54. Mello JHF, Moulton TP, Raíces DSL, Bergallo HG (2015) About rats and jackfruit trees: modeling the carrying capacity of a Brazilian Atlantic Forest spiny-rat Trinomys dimidiatus (Günther, 1877)—Rodentia, Echimyidae—population with varying jackfruit tree (Artocarpus heterophyllus L.) abundances. Braz J Biol 75:208–215CrossRefGoogle Scholar
  55. Mittermeier RA, Robles-Gil P, Hoffman M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreaux J, Fonseca GAB (2004) Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX, Mexico CityGoogle Scholar
  56. Mittermeier RA, Turner WR, Larsen FW, Brooks TM, Gascon C (2011) Global biodiversity conservation: The critical role of hotspots. In: Zachos FE, Habel JC (eds) Biodiversity hotspots: distribution and protection of conservation priority areas. Springer, Berlin, pp 3–22CrossRefGoogle Scholar
  57. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–855CrossRefGoogle Scholar
  58. Peterson AT, Samy AM (2016) Geographic potential of disease caused by Ebola and Marburg viruses in Africa. Acta Trop 162:114–124CrossRefGoogle Scholar
  59. Peterson AT, Ortega-Huerta MA, Bartley J, Sánchez-Cordero V, Soberón J, Buddemeier RH, Stockwell DRB (2002) Future projections for Mexican faunas under global climate change scenarios. Nature 416:626–629CrossRefGoogle Scholar
  60. Peterson AT, Soberón J, Pearson RG, Anderson RP, Martínez-Meyer E, Nakamura M, Araújo MB (2011) Ecological niches and geographical distributions. Princeton University Press, PrincetonGoogle Scholar
  61. Pressey RL, Johnson IR, Wilson PD (1994) Shades of irreplaceability—towards a measure of contribution of sites to a reservation goal. Biodivers Conserv 3:242–262CrossRefGoogle Scholar
  62. Ribeiro MC, Metzer JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  63. Rossiter-Rachor NA, Setterfield SA, Douglas MM, Hutley LB, Cook GD, Schimdt S (2009) Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of nitrogen relations in Australian savanna. Ecol Appl 19:1546–1560CrossRefGoogle Scholar
  64. Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human- induced rapid environmental change. Evol Appl 4:367–387CrossRefGoogle Scholar
  65. Silva JMC, Sousa MC, Castelletti CHM (2004) Areas of endemism for passerine birds in the Atlantic Forest. Global Ecol Biogeogr 13:85–92CrossRefGoogle Scholar
  66. Tabarelli M, Pinto LP, Silva JMC, Hirota MM, Bedê LC (2005) Desafios e oportunidades para a conservação da biodiversidade na Mata Atlântica brasileira. Megadiversidade 1:132–138Google Scholar
  67. Taylor KE, Stouffer RJ, Meehl GA (2012) An overview of CMIP5 and the experiment design. Bull Am Meteorol Soc 93:485–498CrossRefGoogle Scholar
  68. Terrible LC, Lima-Ribeiro MS, Araújo M, Bizao N, Collevatti RG, Dobrovolski R, Franco A, Guilhaumon F, Lima JS, Murakami DM, Nabout JC, de Oliveira G, Oliveira LK, Rabello SG, Rangel TF, Simon LM, Soares TN, Telles MPC, Diniz-Filho JAF (2012) Areas of climate stability of species ranges in the Brazilian Cerrado: disentangling uncertainties through time. Nat Conservacao 10:152–159CrossRefGoogle Scholar
  69. Thomas CA (1980) Jackfruit, Artocarpus heterophyllus (Moraceae), as source of food and income. Econ Bot 34:154–159CrossRefGoogle Scholar
  70. Thuiller W (2004) Patterns and uncertainties of species’ range shifts under climate change. Global Change Biol 10:2020–2027CrossRefGoogle Scholar
  71. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interaction in terrestrial ecosystems. Ecol Lett 11:1351–1363CrossRefGoogle Scholar
  72. Varela S, Anderson RP, García-Valdés R, Fernádez-Gonzáles F (2014) Environmental filters reduce the effects of sampling bias and improve predictions of ecological niche models. Ecography 37:1084–1091Google Scholar
  73. Varela S, Terribile LC, de Oliveira G, González-Hernandez J, Lima-Ribeiro MS (2015) ecoClimate versus Worldclim: variables climáticas SIG para trabajar en biogeografia. Ecosistemas 24:88–92CrossRefGoogle Scholar
  74. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarosik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pysek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708CrossRefGoogle Scholar
  75. Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratório de Biogeografia da Conservação, Instituto de Biologia, Centro de Ciências Agrárias, Ambientais e BiológicasUniversidade Federal do Recôncavo da BahiaCruz das AlmasBrazil
  2. 2.Laboratório de Modelagem Ecológica, Coordenação de Ciência da Terra e EcologiaMuseu Paraense Emílio GoeldiBelémBrazil

Personalised recommendations