Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority

Abstract

Background

Botanists, ecologists and evolutionary biologists are familiar with the astonishing species richness and endemism of the fynbos of the Cape Floristic Region and the ancient and unique flora of the kwongkan of south-western Australia. These regions represent old climatically-buffered infertile landscapes (OCBILs) that are the basis of a general hypothesis to explain their richness and endemism. However, few ecologists are familiar with the campo rupestre of central and eastern Brazil, an extremely old mountaintop ecosystem that is both a museum of ancient lineages and a cradle of continuing diversification of endemic lineages.

Scope

Diversification of some lineages of campo rupestre pre-dates diversification of lowland cerrado, suggesting it may be the most ancient open vegetation in eastern South America. This vegetation comprises more than 5000 plant species, nearly 15 % of Brazil’s plant diversity, in an area corresponding to 0.78 % of its surface. Reviewing empirical data, we scrutinise five predictions of the OCBIL theory, and show that campo rupestre is fully comparable to and remarkably convergent with both fynbos and kwongkan, and fulfills the criteria for a classic OCBIL.

Conclusions

The increasing threats to campo rupestre are compromising ecosystem services and we argue for the implementation of more effective conservation and restoration strategies.

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References

  1. Abrahão A, Lambers H, Sawaya ACHF, Mazzafera P, Oliveira RS (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176:345–355

    PubMed  Article  Google Scholar 

  2. Alcântara S, Mello-Silva R, Teodoro GS, Drequeceler K, Ackerly D, Oliveira RS (2015) Carbon assimilation and habitat segregation in resurrection plants: comparison between desiccation- and non-desiccation-tolerant species of neotropical Velloziaceae (Pandanales). Funct Ecol

  3. Alkmim FF, Marshak S (1998) Transamazonian orogeny in the Southern São Francisco Craton Region, Minas Gerais, Brazil: evidence for Paleoproterozoic collision and collapse in the Quadrilátero Ferrífero. Precambrian Res 90:29–58

    CAS  Article  Google Scholar 

  4. Alkmin FF (2012) Serra do Espinhaço e Chapada Diamantina. In: Hasui Y, Carneiro CDR, Almeida FFM, Bartorelli A (eds) Geologia do Brasil. Beca, São Paulo, pp 236–244

    Google Scholar 

  5. Allsopp N, Colville JF, Verboom GA (eds) (2014) Fynbos: ecology, evolution, and conservation of a megadiverse region. Oxford University Press, New York

    Google Scholar 

  6. Alves RJV (1994) Morphological age determination and longevity in some Vellozia populations in Brazil. Folia Geobot 29:55–59

    Article  Google Scholar 

  7. Alves RJV, Kolbek J (1994) Plant species endemism in savanna vegetation on table mountais (Campo Rupestre) in Brazil. Vegetatio 113:125–139

    Google Scholar 

  8. Alves RJV, Kolbek J (2010) Can campo rupestre vegetation be floristically delimited based on vascular plant genera? Plant Ecol 207:67–79

    Article  Google Scholar 

  9. Alves RJV, Silva NG, Fernandes Júnior A, Guimarães AR (2013) Longevity of the Brazilian underground tree Jacaranda decurrens Cham. An Acad Bras Cienc 85:671–677

    PubMed  Article  Google Scholar 

  10. Alves RJV, Silva NG, Oliveira JA, Medeiros D (2014) Circumscribing campo rupestre megadiverse brazilian rocky montane savannas. Braz J Biol 74:355–362

    CAS  PubMed  Article  Google Scholar 

  11. Barbosa NPU, Fernandes GW, Carneiro MAA, Júnior LAC (2010) Distribution of non-native invasive species and soil properties in proximity to paved roads and unpaved roads in a quartzitic mountainous grassland of southeastern Brazil. Biol Invasions 12:3745–3755

    Article  Google Scholar 

  12. Barbosa NPU, Fernandes GW, Sanchez-Azofeita A (2015) A relict species restricted to a quartzitic mountain in tropical America: an example of microrefugium? Acta Bot Bras 29:299–309

    Article  Google Scholar 

  13. Beerling DJ, Osborne CP (2006) The origin of the savanna biome. Glob Chang Biol 12:2023–2031

    Article  Google Scholar 

  14. Benites VM, Schaefer CER, Simas FNB, Santos HG (2007) Soil associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Rev Bras Bot 30:569–577

    Article  Google Scholar 

  15. Berry PE, Riina R (2005) Insights into the diversity of the Pantepui flora and the biogeographic complexity of the Guayana Shield. Biol Skrif 55:145–167

    Google Scholar 

  16. Bitencourt C, Rapini A (2013) Centres of endemism in the Espinhaço Range: identifying cradles and museums of Asclepiadoideae (Apocynaceae). Syst Biodivers 11:525–536

    Article  Google Scholar 

  17. Blanche KR, Westoby M (1995) Gall-forming insect diversity is linked to soil fertility via host plant taxon. Ecology 76:2334–2337

    Article  Google Scholar 

  18. Bonatelli IAS, Perez MF, Peterson AT, Taylor NP, Zappi DC, Machado MC, Koch I, Pires AHC, Moraes EM (2014) Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Mol Ecol 23:3044–3063

  19. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77

    CAS  Article  Google Scholar 

  20. Bullock JM (1998) Community translocation in Britain: setting objectives and measuring consequences. Biol Conserv 84:199–214

    Article  Google Scholar 

  21. Carmo FF (2010) Importância ambiental e estado de conservação dos ecossistemas de cangas no Quadrilátero Ferrífero e proposta de áreas-alvo para a investigação e proteção da biodiversidade em Minas Gerais. Master Thesis: Universidade Federal de Minas Gerais

  22. Carmo FF, Jacobi CM (2012) The cangas of the Iron Quadrangle. In: Jacobi CM, Carmo FF (eds) Floristic diversity of the Quadrilátero Ferrífero cangas. IDM, Belo Horizonte, pp 14–30

  23. Carmo FF, Jacobi CM (2013) Canga vegetation in the Iron Quadrangle, Minas Gerais: characterization and phytogeographical context. Rodriguésia 64:527–541

    Article  Google Scholar 

  24. Carneiro MA, Borges RAX, Araújo APA, Fernandes GW (2009) Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG. Rev Bras Entomol 53:570–592

    Article  Google Scholar 

  25. Carstensen DW, Sabatino M, Trojelsgaard K, Morellato LPC (2014) Beta diversity of plant-pollinator networks and the spatial turnover of pairwise interactions. PLoS One 9, e112903

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  26. CBD - Convention of Biological Diversity (2010) COP Decision X/2. Strategic plan for biodiversity 2011–2020. http://www.cbd.int/decision/cop/?id=12268. Accessed 20 June 2014

  27. Cerabolini BEL, Brusa G, Ceriani RM, de Andreis R, Luzzaro A, Pierce S (2010) Can CSR classification be generally applied outside Britain? Plant Ecol 210:253–261

    Article  Google Scholar 

  28. Cheib AL, Garcia QS (2012) Longevity and germination ecology of seeds of endemic Cactaceae species from high-altitude sites in south-eastern Brazil. Seed Sci Res 21:45–53

    Article  Google Scholar 

  29. Coan AI, Scatena VL, Giulietti AM (2002) Anatomia de algumas espécies aquáticas de Eriocaulaceae brasileiras. Acta Bot Bras 16:371–384

    Article  Google Scholar 

  30. Coelho FF, Capelo C, Ribeiro LC, Figueira JEC (2008) Reproductive modes in Leiothrix (Eriocaulaceae) in south-eastern Brazil: the role of microenvironmental heterogeneity. Ann Bot 101:353–360

    PubMed  PubMed Central  Article  Google Scholar 

  31. Collevatti RG, Rabelo SG, Vieira RF (2009) Phylogeography and disjunct distribution in Lychnophora ericoides (Asteraceae), an endangered cerrado shrub species. Ann Bot 104:655–664

    PubMed  PubMed Central  Article  Google Scholar 

  32. Conceição AA, Pirani JR (2005) Delimitação de habitats em campos rupestres na Chapada Diamantina, Bahia: substratos, composição florística e aspectos estruturais. Bol Bot Univ São Paulo 23:85–111

    Google Scholar 

  33. Conceição AA, Funch LS, Pirani JR (2007a) Reproductive phenology, pollination and seed dispersal syndromes on sandstone vegetation in the “Chapada Diamantina”, northeastern Brazil: population and community analyses. Rev Bras Bot 30:475–485

    Google Scholar 

  34. Conceição AA, Pirani JR, Meirelles ST (2007b) Floristics, structure and soil of insular vegetation in four quartzite-sandstone outcrops of Chapada Diamantina, northeast Brazil. Rev Bras Bot 30:641–655

    Article  Google Scholar 

  35. Conceição AA, Alencar TG, Souza JM, Moura ADC, Silva GA (2013) Massive post-fire flowering events in a tropical mountain region of Brazil: high episodic supply of floral resources. Acta Bot Bras 27:847–850

    Article  Google Scholar 

  36. Costa FN, Trovó M, Sano PT (2008) Eriocaulaceae na Cadeia do Espinhaço: riqueza, endemismo e ameaças. Megadiversidade 4:117–125

    Google Scholar 

  37. Costanza R (2006) Nature: ecosystems without commodifying them. Nature 443:749

    CAS  PubMed  Article  Google Scholar 

  38. Cowling RM, Pressey RL, Rouget M, Lombard AT (2003) A conservation plan for a global biodiversity hotspot—the Cape Floristic Region, South Africa. Biol Conserv 112:191–216

    Article  Google Scholar 

  39. CNCFlora - Centro Nacional de Conservação da Flora (2015) Projeto Lista Vermelha. http://cncflora.jbrj.gov.br/portal/pt-br/projetos/lista-vermelha. Accessed 7 July 2015

  40. CPRM - Companhia de Pesquisas e Recursos Minerais (2004) Projeto APA Sul RMBH: hidrogeologia, mapa hidrogeológico escala 1:50.000.SEMAD/CPRM, Belo Horizonte

  41. Dayrell RLC (2015) Ecology and evolution of seed dormancy in campos rupestres. M.Sc. Thesis. Universidade Federal de Minas Gerais

  42. de Carvalho F, Souza FA, Carrenho R, Moreira FMS, Jesus EC, Fernandes GW (2012) The mosaic of habitats in the high-altitude Brazilian rupestrian fields is a hotspot for arbuscular mycorrhizal fungi. Appl Soil Ecol 52:9–19

    Article  Google Scholar 

  43. Domingues SA, Karez CS, Biondini IVF, Andrade MA, Fernandes GW (2012) Economic environmental management tools in the Serra do Espinhaço Biosphere Reserve. J Sustain Dev 5:180–191

    Google Scholar 

  44. Dycus AM, Knudson L (1957) The role of the velamen of the aerial roots of orchids. Bot Gaz 119:78–87

    Article  Google Scholar 

  45. Echternacht L, Trovó M, Sano PT (2010) Rediscoveries in Eriocaulaceae: seven narrowly distributed taxa from the Espinhaço Range in Minas Gerais, Brazil. Feddes Repert 121:117–126

    Article  Google Scholar 

  46. Echternacht L, Sano PT, Trovó M, Dubuisson J (2011a) Phylogenetic analysis of the Brazilian microendemic Paepalanthus subgenus Xeractis (Eriocaulaceae) inferred from morphology. Bot J Linn Soc 167:137–152

    Article  Google Scholar 

  47. Echternacht L, Trovó M, Oliveira CT, Pirani JR (2011b) Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782–791

    Article  Google Scholar 

  48. Echternacht L, Sano PT, Bonillo C, Cruaud C, Couloux A, Dubuisson J-Y (2014) Phylogeny and taxonomy of Syngonanthus and Comanthera (Eriocaulaceae): evidence from expanded sampling. Taxon 63:47–63

    Article  Google Scholar 

  49. Espírito-Santo MM, Neves FS, Andrade-Neto FR, Fernandes GW (2007) Plant architecture and meristem dynamics as the mechanism determining the diversity of gall-inducing insects. Oecologia 153:353–364

    PubMed  Article  Google Scholar 

  50. Faucon M-P, Meersseman A, Shutcha MN, Mahy G, Luhembwe MN, Malaisse F, Meerts P (2010) Copper endemism in the Congolese flora: a database of copper affinity and conservational value of cuprophytes. Plant Ecol Evol 143:5–18

    Article  Google Scholar 

  51. Faustino TC, Machado CG (2006) Frugivoria por aves em uma área de campo rupestre na Chapada Diamantina, BA. Ararajuba 14:137–143

    Google Scholar 

  52. Feres F, Zucchi MI, Souza AP, Amaral MCE, Bittrich V (2009) Phylogeographic studies of Brazilian “campo-rupestre” species: Wunderlichia mirabilis Riedel ex Baker (Asteraceae). Biotemas 22:17–26

    Article  Google Scholar 

  53. Fernandes GW, Price PW (1988) Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia 76:161–167

    Article  Google Scholar 

  54. Fernandes GW, Barbosa NPU, Negreiros D, Paglia AP (2014) Challenges for the conservation of vanishing megadiverse rupestrian grasslands. Nat Conservacao 12:162–165

    Article  Google Scholar 

  55. Fidelis A, Appezzato-da-Glória B, Pillar VD, Pfadenhauer J (2014) Does disturbance affect bud bank size and belowground structures diversity in Brazilian subtropical grasslands? Flora 209:110–116

    Article  Google Scholar 

  56. Flematti GR, Merritt DJ, Piggott MJ, Trengove RD, Smith SM, Dixon KW, Ghisalberti EL (2011) Burning vegetation produces cyanohydrins that liberate cyanide and promote seed germination. Nat Commun 2:360

    PubMed  Article  CAS  Google Scholar 

  57. Fonseca RBS, Funch LS, Borba EL (2012) Dispersão de sementes de Melocactus glaucescens e M. paucispinus (Cactaceae), no Município de Morro do Chapéu, Chapada Diamantina—BA. Acta Bot Bras 26:481–492

    Google Scholar 

  58. Forzza RC, Baumgratz JFA, Bicudo CE, Carvalho AA Jr, Costa A, Costa DP, Hopkins M, Leitman PM, Lohmann LG, Maia LC, Martinelli G, Menezes M, Morim MP, Coelho MAN, Peixoto AL, Pirani JR, Prado J, Queiroz LP, Souza VC, Stehmann JR, Sylvestre LS, Walter BMT, Zappi D (2010) Catálogo de Plantas e Fungos do Brasil, vol 1. Andrea Jakobsson Estúdio. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro

    Google Scholar 

  59. Frisby S, Hindy DJN (2014) Ichthyothere sasakiae, (Compositae: Heliantheae: Milleriinae), a new species from the Amazonian campo rupestre of northern Mato Grosso State, Brazil. Kew Bull 69:9504

    Article  Google Scholar 

  60. Fujita Y, Venterink HO, van Bodegom PM, Douma JC, Heil GW, Holzel N, Jablonska E, Kotowski W, Okruszko T, Pawlikowski P, de Ruiter PC, Wassen MJ (2014) Low investment in sexual reproduction threatens plants adapted to phosphorus limitation. Nature 505:82–86

    PubMed  Article  CAS  Google Scholar 

  61. Garcia RJF, Longhi-Wagner HM, Pirani JR, Meirelles ST (2009) A contribution to the phytogeography of Brazilian campos: an analysis based on Poaceae. Rev Bras Bot 32:703–713

    Article  Google Scholar 

  62. Garcia QS, Giorni VT, Müller M, Munné-Bosch S (2012) Common and distinct responses in phytohormone and vitamin E changes during seed burial and dormancy in Xyris bialata and X. peregrina. Plant Biol 14:347–353

    CAS  PubMed  Article  Google Scholar 

  63. Garcia QS, Oliveira PG, Duarte DM (2014) Seasonal changes in germination and dormancy of buried seeds of endemic Brazilian Eriocaulaceae. Seed Sci Res 24:113–117

    Article  Google Scholar 

  64. Gibson N, Yates CJ, Dillon R (2010) Plant communities of the ironstone ranges of South Western Australia: hotspots for plant diversity and mineral deposits. Biodivers Conserv 19:3951–3962

    Article  Google Scholar 

  65. Gibson N, Meissner R, Markey AS, Thompson WA (2012) Patterns of plant diversity in ironstone ranges in arid south western Australia. J Arid Environ 77:25–31

    Article  Google Scholar 

  66. Ginocchio R, Baker AJM (2004) Metallophytes in Latin America: a remarkable biological and genetic resource scarcely known and studied in the region. Rev Chil Hist Nat 77:185–194

    Article  Google Scholar 

  67. Giulietti AM, Menezes NL, Pirani JR, Meguro M, Wanderley MGL (1987) Flora da Serra do Cipó: caracterização e lista das espécies. Bol Bot Univ São Paulo 9:1–151

    Google Scholar 

  68. Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço Range region, eastern Brazil. In: Davis SD, Heywood VH, Herrera-Macbryde O, Villa-Lobos J, Hamilton AC (eds) Centres of plant diversity: a guide and strategy for their conservation. IUCN Publication Unit, Cambridge, pp 397–404

    Google Scholar 

  69. Giulietti AM, Rapini A, Andrade MJG, Queiroz LP, Silva JMC (eds) (2009) Rare plants of Brazil. Conservation International, Belo Horizonte

    Google Scholar 

  70. Goldblatt P, Manning JC (2002) Plant diversity of Cape region of Southern Africa. Ann Mo Bot Gard 89:281–302

    Article  Google Scholar 

  71. Gomes V, Madeira JA, Fernandes GW, LemosFilho JP (2001) Seed dormancy and germination of sympatric species of Chamaecrista (Leguminosae) in a rupestrian field. Int J Ecol Environ Sci 27:191–197

    Google Scholar 

  72. Gomes V, Collevatti RG, Silveira FAO, Fernandes GW (2004) The distribution of genetic variability in Baccharis concinna (Asteraceaea), an endemic, dioecious and threatened shrub of rupestrian fields of Brazil. Conserv Genet 5:157–165

    CAS  Article  Google Scholar 

  73. Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci 5:36

    PubMed  PubMed Central  Article  Google Scholar 

  74. Groppo M, Amaral MM, Ceccantini GCT (2007) Flora da Serra do Cipó, Minas Gerais: Apodanthaceae (Rafflesiaceae s.l.), e notas sobre a anatomia de Pilostyles. Bol Bot Univ São Paulo 25:81–86

    Google Scholar 

  75. Guerra TJ, Pizo MA (2014) Asymmetrical dependence between a Neotropical mistletoe and its avian seed disperser. Biotropica 46:285–293

    Article  Google Scholar 

  76. Gustafsson ALS, Verola CF, Antonelli A (2010) Reassessing the temporal evolution of orchids with new fossils and a Bayesian relaxed clock, with implications for the diversification of the rare South American genus Hoffmannseggella (Orchidaceae: Epidendroideae). BMC Evol Biol 10:177

    PubMed  PubMed Central  Article  Google Scholar 

  77. Harley RM (1988) Evolution and distribution of Eriope (Labiatae) and its relatives in Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a workshop on Neotropical distribution patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp 71–121

    Google Scholar 

  78. Hedberg O (1973) Adaptive evolution in a Tropical-Alpine environment. In: Heywood VH (ed) Taxonomy and ecology. Academic, London, pp 71–92

    Google Scholar 

  79. Hensold N (1988) Morphology and systematics of Paepalanthus subgenus Xeractis (Eriocaulaceae). Systematic Botany Monographs 23, Ann Arbor

  80. Holmes PM, Newton RJ (2004) Patterns of seed persistence in South African fynbos. Plant Ecol 172:143–158

    Article  Google Scholar 

  81. Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant Soil 322:49–86

    CAS  Article  Google Scholar 

  82. Huber O (2006) Herbaceous ecosystems on the Guayana Shield, a regional overview. J Biogeogr 33:464–475

    Article  Google Scholar 

  83. Hughes CE, Pennington RT, Antonelli A (2013) Neotropical plant evolution: assembling the big picture. Bot J Linn Soc 171:1–18

    Article  Google Scholar 

  84. Ilunga wa Ilunga E, Mahy G, Piqueray J, Séleck M, Shutcha MN, Meerts P, Faucon M-P (2015) Plant functional traits as a promising tool for the ecological restoration of degraded tropical metal-rich habitats and revegetation of metal-rich bare soils: a case study in copper vegetation of Katanga, DRC. Ecol Eng 82:214–221

    Article  Google Scholar 

  85. IUCN Standards and Petitions Subcommittee (2011) Guidelines for using the IUCN Red List categories and criteria. Version 9.0. IUCN Standards and Petitions Subcommittee

  86. Jacobi CM, Carmo FF (2011) Life-forms, pollination and seed dispersal syndromes in plant communities on ironstone outcrops, SE Brazil. Acta Bot Bras 25:395–412

    Article  Google Scholar 

  87. Jacobi CM, Carmo FF (2012) Diversidade florística nas cangas do Quadrilátero Ferrífero. IDM, Belo Horizonte

    Google Scholar 

  88. Jacobi CM, Carmo FF, Vincent RC, Stehmann JR (2007) Plant communities on ironstone outcrops—a diverse and endangered Brazilian ecosystem. Biodivers Conserv 16:2185–2200

    Article  Google Scholar 

  89. Jacobi CM, Carmo FF, Campos IC (2011) Soaring extinction threats to endemic plants in Brazilian metal-rich regions. AMBIO 40:540–543

    PubMed  PubMed Central  Article  Google Scholar 

  90. Keeley JE, Bond WJ (1997) Convergent seed germination in South African fynbos and Californian chaparral. Plant Ecol 133:153–167

    Article  Google Scholar 

  91. Kolbek J, Alves RJV (2008) Impacts of cattle, fire and wind in rocky savannas, southeastern Brazil. Acta Univ Carol Environ 22:111–130

    Google Scholar 

  92. Lambers H (ed) (2014) Plant life on the sandplains in Southwest Australia: a global biodiversity hotspot. UWA Publishing, Crawley

    Google Scholar 

  93. Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    PubMed  Article  Google Scholar 

  94. Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31

    CAS  Article  Google Scholar 

  95. Lambers H, Colmer TD, Hassiotou F, Mitchell PM, Poot P, Shane MW, Veneklaas EJ (2014a) Carbon and water relations. In: Lambers H (ed) Plantlife on the sandplains in Southwest Australia: a global biodiversity hotspot. UWA Publishing, Crawley, pp 129–146

    Google Scholar 

  96. Lambers H, Shane MW, Laliberté E, Swarts ND, Teste FP, Zemunik G (2014b) Plant mineral nutrition. In: Lambers H (ed) Plant life on the sandplains in Southwest Australia: a global biodiversity hotspot. UWA Publishing, Crawley, pp 101–128

    Google Scholar 

  97. Lamont BB, Le Maitre DC, Cowling RM, Enright NJ (1991) Canopy seed storage in woody plants. Bot Rev 57:277–317

    Article  Google Scholar 

  98. Le Stradic S (2012) Composition, phenology and restoration of campos rupestres mountain grasslands, Brazil. Ph.D. Thesis.Universidade Federal de Minas Gerais

  99. Le Stradic S, Buisson E, Fernandes GW (2014a) Restoration of Neotropical grasslands degraded by quarrying using hay transfer. Appl Veg Sci 17:482–492

    Article  Google Scholar 

  100. Le Stradic S, Buisson E, Negreiros D, Campagne P, Fernandes GW (2014b) The role of native woody species in the restoration of campos rupestres in quarries. Appl Veg Sci 17:109–120

    Article  Google Scholar 

  101. Le Stradic S, Buisson E, Fernandes GW (2015a) Vegetation composition and structure of some Neotropical mountain grasslands in Brazil. J Mount Sci 12:864–877

    Article  Google Scholar 

  102. Le Stradic S, Silveira FAO, Buisson E, Cazelles K, Carvalho V, Fernandes GW (2015b) Diversity of germination strategies and seed dormancy in herbaceous species of campo rupestre grasslands. Austral Ecol 40:537–546

    Article  Google Scholar 

  103. Leles B, Chaves AV, Russo P, Batista JAN, Lovato MB (2015) Genetic structure is associated with phenotypic divergence in floral traits and reproductive investment in a high-altitude orchid from the Iron Quadrangle, southeastern Brazil. PLoS One 10, e0120645

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  104. Lima MHC, Oliveira EG, Silveira FAO (2013) Interactions between ants and non-myrmecochorous fruits in Miconia (Melastomataceae) in a Neotropical Savanna. Biotropica 45:217–223

    Article  Google Scholar 

  105. Lopes-Mattos KLB, Azevedo AA, Soares AA, Meira RMSA (2013) Underground system of Mandevilla atroviolacea (Stadelm.) Woodson (Apocynaceae, Apocynoideae) from the Brazilian high-altitude grassland. S Afr J Bot 87:27–33

    Article  Google Scholar 

  106. Lousada JM, Borba EL, Ribeiro KT, Ribeiro LC, Lovato MB (2011) Genetic structure and variability of the endemic and vulnerable Vellozia gigantea (Velloziaceae) associated with the landscape in the Espinhaço Range, in southeastern Brazil: implications for conservation. Genetica 139:431–440

    PubMed  Article  Google Scholar 

  107. LSBF - List of Species of the Brazilian Flora (2015) Rio de Janeiro Botanical Garden. http://floradobrasil.jbrj.gov.br/. Accessed 26 May 2015

  108. Lusa MG, Appezzato-da-Glória B, Loeuille B, Bartoli G, Ciccarelli D (2014) Functional groups in Lychnophorinae (Asteraceae: Vernonieae) based on morphological and anatomical traits. Austral J Bot 62:150–163

    Article  Google Scholar 

  109. Lüttge U, Haridasan M, Fernandes GW, Mattos EA, Trimborn P, Franco AC, Caldas LS, Zielgler H (1998) Photosynthesis of mistletoes in relation to their host at various sites of tropical Brazil. Trees 12:167–174

    Article  Google Scholar 

  110. Lüttge U, Duarte HM, Scarano FR, Mattos EA, Cavalin PO, Franco AC, Fernandes GW (2007) Physiological ecology of photosynthesis of five sympatric species of Velloziaceae in the “campos rupestres” vegetation of Serra do Cipó, Minas Gerais, Brazil. Flora 202:637–646

    Article  Google Scholar 

  111. Machado NADM, Leite MGP, Figueiredo MA, Kozovits AR (2013) Growing Eremanthus erythropappus in crushed laterite: a promising alternative to topsoil for bauxite-mine revegetation. J Environ Manag 129:149–156

    Article  CAS  Google Scholar 

  112. Madeira JA, Ribeiro KT, Oliveira MJR, Paiva CL (2008) Distribuição espacial do esforço de pesquisa biológica na Serra do Cipó, Minas Gerais: subsídios ao manejo das unidades de conservação da região. Megadiversidade 4:257–271

    Google Scholar 

  113. Manning J (2007) Field guide to fynbos. Struik Publishers, Cape Town

    Google Scholar 

  114. Marques AR, Atman APF, Silveira FAO, Lemos-Filho JP (2014) Are seed germination and ecological breadth associated? Testing the regeneration niche hypothesis with bromeliads in a heterogeneous neotropical montane vegetation. Plant Ecol 215:517–529

    Article  Google Scholar 

  115. Martin CE, von Willert DJ (2000) Leaf epidermal hydathodes and the ecophysiological consequences of foliar water uptake in species of Crassula from the Namib Desert in Southern Africa. Plant Biol 2:229–242

    Article  Google Scholar 

  116. Martinelli G, Moraes MA (2013) Livro vermelho da flora do Brasil. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Centro Nacional de Conservação da Flora, Rio de Janeiro

    Google Scholar 

  117. Matias SR, Pagano MC, Muzzi FC, Oliveira CA, Carneiro AA, Horta SN, Scotti MR (2009) Effect of rhizobia, mycorrhizal fungi and phosphate-solubilizing microorganisms in the rhizosphere of native plants used to recover an iron ore area in Brazil. Eur J Soil Biol 45:259–266

    CAS  Article  Google Scholar 

  118. Medina MBO, Fernandes GW (2007) The potential of natural regeneration of rocky outcrop vegetation on rupestrian field soils in “Serra do Cipó”, Brazil. Rev Bras Bot 30:665–678

    Article  Google Scholar 

  119. MMA - Ministério do Meio Ambiente (2014) Tabela consolidada das Unidades de Conservação. http://www.mma.gov.br/cadastro_uc. Accessed 18 Nov 2014

  120. Meissner R, Owen G, Bayliss B (2009) Flora and vegetation of banded iron formations of the Yilgarn Craton: Cashmere Downs Range. Conserv Sci West Aust 7:349–361

    Google Scholar 

  121. Mello-Silva R (1989) Velloziaceae de Grão-Mogol, Minas Gerais, Brazil. MSc Thesis. Universidade de São Paulo

  122. Mello-Silva R, Santos DYAC, Salatino MLF, Motta LB, Cattai MB, Sasaki D, Lovo J, Pita PB, Rocini C, Rodrigues CDN, Zarrei M, Chase MW (2011) Five vicarious genera from Gondwana: the Velloziaceae as shown by molecules and morphology. Ann Bot 108:87–102

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  123. Mendonça MP, Lins LV (2000) Lista vermelha das espécies ameaçadas de extinção da flora do estado de Minas Gerais. Fundação Biodiversitas & Fundação Zoo-Botânica de Belo Horizonte, Belo Horizonte

    Google Scholar 

  124. Milberg P, Andersson L, Thompson K (2000) Large-seeded species are less dependent on light for germination then small-seeded ones. Seed Sci Res 10:99–104

    Article  Google Scholar 

  125. Milewski AV, Bond WJ (1982) Convergence of myrmecochory in Mediterranean Australia and South Africa. In: Buckley RC (ed) Ant-plant interactions in Australia. Junk Press, The Hague, pp 89–98

    Chapter  Google Scholar 

  126. Miola DTB, Fernandes GW (2015) Growing straight versus growing decumbent: soil quality and allometry in Syagrus glaucescens Becc. (Arecaceae), an endemic and threatened palm of the Espinhaço Mountains, Brazil. Acta Bot Bras 29:417–424

    Article  Google Scholar 

  127. Morales M, Garcia QS, Siqueira-Silva AI, Silva MC, Munné-Bosch S (2014) Tocotrienols in Vellozia gigantea leaves: occurrence and modulation by seasonal and plant size effects. Planta 240:437–446

    CAS  PubMed  Article  Google Scholar 

  128. Morales M, Garcia QS, Munné-Bosch S (2015) Ecophysiological response to seasonal variations in water availability in the arborescent, endemic plant Vellozia gigantea. Tree Physiol 35:253–265

    PubMed  Article  Google Scholar 

  129. Moreira ASFP, Lemos-Filho JP, Zotz G, Isaias RMS (2009) Anatomy and photosynthetic parameters of roots and leaves of two shade-adapted orchids, Dichaea cogniauxiana Shltr. and Epidendrum secundum Jacq. Flora 204:604–611

    Article  Google Scholar 

  130. Mourão FA, Carmo FF, Sousa PRA, Jacobi CM (2006) Hospedeiras de Struthanthus flexicaulis (Mart.) Mart. (Loranthaceae) em campos rupestres ferruginosos no Quadrilátero Ferrífero, Minas Gerais. Lundiana 7:103–110

  131. Mucina L, Laliberté E, Thiele KR, Dodson JR, Harvey J (2014) Biogeography of kwongan: origins, diversity, endemism, and vegetation patterns. In: Lambers H (ed) Plant life on the sandplains in Southwest Australia, a global biodiversity hotspot. UWA Publishing, Crawley, pp 35–79

    Google Scholar 

  132. Munné-Bosch S, Oñate M, Oliveira PG, Garcia QS (2011) Changes in phytohormones and oxidative stress markers in buried seeds of Vellozia alata. Flora 206:704–711

    Article  Google Scholar 

  133. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  Article  Google Scholar 

  134. Nativel N, Buisson E, Silveira FAO (2015) Seed storage-mediated dormancy alleviation in Fabaceae from campo rupestre. Acta Bot Bras 29:445–447

    Article  Google Scholar 

  135. Negreiros D, Fernandes GW, Silveira FAO, Chalub C (2009) Seedling growth and biomass allocation of endemic and threatened shrubs of rupestrian fields. Acta Oecol 35:301–310

    Article  Google Scholar 

  136. Negreiros D, Fernandes GW, Berbara RLL, Rodarte LHO, Barbosa NPU (2011) Caracterização físico-química de solos quartzíticos degradados e áreas adjacentes de campo rupestre na Serra do Cipó, MG, Brasil. Neotrop Biol Conserv 6:156–161

    Google Scholar 

  137. Negreiros D, Le Stradic S, Fernandes GW, Rennó HC (2014) CSR analysis of plant functional types in highly diverse tropical grasslands of harsh environments. Plant Ecol 215:379–388

    Article  Google Scholar 

  138. Neves SPS, Conceição AA (2010) Campo rupestre recém-queimado na Chapada Diamantina, Bahia, Brasil: plantas de rebrota e sementes, com espécies endêmicas na rocha. Acta Bot Bras 24:697–707

    Article  Google Scholar 

  139. Neves AC, Nogueira FB, Assis LR, Paglia AP, Bedê LC, Martins RP (2014) Reproductive allocation in rhizomatous, seminiferous, and pseudoviviparous Leiothrix (Eriocaulaceae) species. Plant Ecol 215:987–996

    Article  Google Scholar 

  140. Nishi AH, Vasconcellos-Neto J, Romero GQ (2013) The role of multiple partners in a digestive mutualism with a protocarnivorous plant. Ann Bot 111:143–150

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  141. Nobel PS, Schulte PJ, North GB (1990) Water influx characteristics and hydraulic conductivity for roots of Agave deserti Engelm. J Exp Bot 41:409–415

    Article  Google Scholar 

  142. Olesen JM, Valido A (2004) Lizards as pollinators and seed dispersers: an island phenomenon. Trends Ecol Evol 18:177–181

    Article  Google Scholar 

  143. Oliveira PG, Garcia QS (2011) Germination characteristics of Syngonanthus seeds (Eriocaulaceae) in campos rupestres vegetation in south-eastern Brazil. Seed Sci Res 21:35–41

    Article  CAS  Google Scholar 

  144. Oliveira MNS, Cruz SM, Sousa AM, Moreira FC, Tanaka MK (2014) Implications of the harvest time on Syngonanthus nitens (Bong.) Ruhland (Eriocaulaceae) management in the state of Minas Gerais. Braz J Bot 37:95–103

    Article  Google Scholar 

  145. Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205:1183–1194

    CAS  PubMed  Article  Google Scholar 

  146. Parr CL, Lehmann CER, Bond WJ, Hoffmann WA, Andersen AN (2014) Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol Evol 29:205–213

    PubMed  Article  Google Scholar 

  147. Pedreira AJ, De Waele B (2008) Contemporaneous evolution of the Palaeoproterozoic-Mesoproterozoic sedimentary basins of the São Francisco-Congo Craton. In: Pankhurst RJ, Trouw RAJ, Neves BBB, De Wit MJ (eds) West Gondwana: pre-cenozoiccorrelations across the South Atlantic region. Geological Society (Special Publications 294), London, pp 33–48

  148. Pereira CG, Almenara DP, Winter CE, Fritsch PW, Lambers H, Oliveira RS (2012) Underground leaves of Philcoxia trap and digest nematodes. Proc Natl Acad Sci U S A 109:1154–1158

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  149. Pignatti E, Pignatti S, Lucchese F (1993) Plant communities of Stirling Range, Western Australia. J Veg Sci 4:477–488

    Article  Google Scholar 

  150. Poot P, Lambers H (2008) Shallow-soil endemics: adaptive advantages and constraints of a specialized root-system morphology. New Phytol 178:371–381

    PubMed  Article  Google Scholar 

  151. Porembski S, Barthlott W (1995) On the occurrence of a velamen radicum in Cyperaceae and Velloziaceae. Nord J Bot 15:625–629

    Article  Google Scholar 

  152. Price PW, Fernandes GW, Lara ACF, Brawn J, Gerling D, Barrios H, Wright M, Ribeiro SP, Rothcliff N (1998) Global patterns in local number of insect galling species. J Biogeogr 25:581–592

    Article  Google Scholar 

  153. Ramsay PM, Oxley ERB (1997) The growth form composition of plant communities in the ecuadorian páramos. Plant Ecol 131:173–192

    Article  Google Scholar 

  154. Ranieri BD, Pezzini FF, Garcia QS, Chautems A, França MGC (2012) Testing the regeneration niche hypothesis with Gesneriaceae (tribe Sinningiae) in Brazil: implications for the conservation of rare species. Austral Ecol 37:125–133

    Article  Google Scholar 

  155. Rapini A, Ribeiro PL, Lambert S, Pirani JR (2008) A flora dos campos rupestres da Cadeia do Espinhaço. Megadiversidade 4:15–23

    Google Scholar 

  156. Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Article  Google Scholar 

  157. Resende FM, Fernandes GW, Coelho MS (2013) Economic valuation of plant diversity storage service provided by Brazilian rupestrian grassland ecosystems. Braz J Biol 73:709–716

    CAS  PubMed  Article  Google Scholar 

  158. Rezende LAL, Dias LE, Assis IR, Braga R, Rezende ML (2013) Restoration of ironstones outcrops degraded by iron minning activity in Minas Gerais State—Brazil. J Am Soc Min Reclam 2:151–159

    Article  Google Scholar 

  159. Rico-Gray V, Oliveira P (2007) The ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago

    Book  Google Scholar 

  160. Romero GQ, Mazzafera P, Vasconcellos-Neto J, Trivelin PC (2006) Bromeliad-living spiders improve host plant nutrition and growth. Ecology 87:803–808

    PubMed  Article  Google Scholar 

  161. Rull V (2004) Is the lost world really lost? Palaeoecological insights into the origin of the peculiar flora of the Guayana Highlands. Naturwissenschaften 91:139–142

    CAS  PubMed  Article  Google Scholar 

  162. Rull V (2005) Biotic diversification in the Guayana Highlands: a proposal. J Biogeogr 32:921–927

    Article  Google Scholar 

  163. Rull V, Vegas-Vilarrúbia T (2006) Unexpected biodiversity loss under global warmingin the neotropical Guayana Highlands: a preliminaryappraisal. Glob Chang Biol 12:1–9

  164. Rylands AB, Brandon K (2005) Brazilian protected areas. Conserv Biol 19:612–618

    Article  Google Scholar 

  165. Safford HD (2007) Brazilian Páramos IV. Phytogeography of the campos de altitude. J Biogeogr 17:1–22

    Google Scholar 

  166. Salas RM, Viana PL, Cabral EL, Dessein S, Janssens S (2015) Carajasia (Rubiaceae), a new and endangered genus from Carajás mountain range, Pará, Brazil. Phytotaxa 206:14–29

    Article  Google Scholar 

  167. Saravia ESR (2008) El costo de la conservación de los bosques tropicales. PhD Thesis, Universidad Autónoma G. René Moreno, Santa Cruz

  168. Schaefer CEGR (2013) Bases físicas da paisagem brasileira: estrutura geológica, relevo e solos. Tópicos Ciência Solo 8:1–69

    Google Scholar 

  169. Shane MW, Cawthray GR, Cramer MD, Kuo J, Lambers H (2006) Specialized ‘dauciform’ roots of Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’ roots. Plant Cell Environ 29:1989–1999

    CAS  PubMed  Article  Google Scholar 

  170. Silveira FAO, Mafia PO, Lemos-Filho JP, Fernandes GW (2012a) Species-specific outcomes of avian gut passage on germination of Melastomataceae seeds. Plant Ecol Evol 145:350–355

    Article  Google Scholar 

  171. Silveira FAO, Ribeiro RC, Oliveira DMT, Fernandes GW, Lemos-Filho JP (2012b) Evolution of physiological dormancy multiple times in Melastomataceae from Neotropical montane vegetation. Seed Sci Res 22:37–44

    Article  Google Scholar 

  172. Simon MF, Grether R, Queiroz LP, Skema C, Pennington RT, Hughes CE (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proc Natl Acad Sci U S A 106:20359–20364

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  173. Soares da Mota LAS, Garcia QS (2013) Germination patterns and ecological characteristics of Vellozia seeds from high-altitude in South-eastern Brazil. Seed Sci Res 23:67–74

    Article  Google Scholar 

  174. Sonter LJ, Barrett DJ, Soares-Filho BS (2014) Offsetting the impacts of mining to achieve no net loss of native vegetation. Conserv Biol 28:1068–1076

    CAS  PubMed  Article  Google Scholar 

  175. Souza ER, Lewis GP, Forest F, Schnadelbach AS, van den Berg C, Queiroz LP (2013) Phylogeny of Calliandra (Leguminosae: Mimosoideae) based on nuclear and plastid molecular markers. Taxon 62:1200–1219

    Article  Google Scholar 

  176. Stannard BL, Harvey YB, Harley RM (eds) (1995) Flora of the Pico das Almas, Chapada Diamantina—Bahia, Brazil. Kew Royal Botanic Gardens, London

    Google Scholar 

  177. Teixeira WA, Lemos Filho JP (2013) A flórula rupestre do Pico de Itabirito, Minas Gerais, Brasil: lista das plantas vasculares. Bol Bot Univ São Paulo 31:199–230

    Google Scholar 

  178. Teixeira WA, Lemos-Filho JP (2002) Fatores edáficos e a colonização de espécies lenhosas em uma cava de mineração de ferro em Itabirito, Minas Gerais. Rev Árvore 26:25–33

    CAS  Google Scholar 

  179. Trovó M, Andrade MJG, Sano PT, Ribeiro PL, van den Berg C (2012) Molecular phylogenetics and biogeography of Neotropical Paepalanthoideae with emphasis on Brazilian Paepalanthus (Eriocaulaceae). Bot J Linn Soc 171:225–243

    Article  Google Scholar 

  180. USDA (1998) Keys to soil taxonomy. United States Department of Agriculture, New York

    Google Scholar 

  181. Veldman JW, Buisson E, Durigan G, Fernandes GW, Le Stradic S, Mahy G, Negreiros D, Overbeck GE, Veldman RG, Zaloumis NP, Putz FE, Bond WJ (2015) Toward an old-growth concept for grasslands, savannas, and woodlands. Front Ecol Environ 13:154–162

    Article  Google Scholar 

  182. Veldtman R, McGeoch MA (2003) Gall-forming insect species richness along a non-scleromorphic vegetation rainfall gradient in South Africa: the importance of plant community composition. Austral Ecol 28:1–13

    Article  Google Scholar 

  183. Velten SB, Garcia QS (2007) Variation between three Eremanthus (Asteraceae) species in their ability to form a seed bank. Rev Bras Bot 30:713–719

    Article  Google Scholar 

  184. Versieux LM, Barbará T, Wanderley MGL, Calvente A, Fay MF, Lexer C (2012) Molecular phylogenetics of the Brazilian giant bromeliads (Alcantarea, Bromeliaceae): implications for morphological evolution and biogeography. Mol Phylogenet Evol 64:177–189

    PubMed  Article  Google Scholar 

  185. Vleeshouwers LM, Bouwmeester HJ, Karssen CM (1995) Redefining seed dormancy: an attempt to integrate physiology and ecology. J Ecol 86:1031–1037

    Article  Google Scholar 

  186. WRB, IUSS Working Group (2006) World reference base for soil resources 2006. World Soil Resources Reports No. 103. FAO, Rome

  187. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    CAS  PubMed  Article  Google Scholar 

  188. Yates CJ, Coates DJ, Elliott C, Byrne M (2007) Composition of the pollinator community, pollination and the mating system for a shrub in fragments of species rich kwongan in south-west Western Australia. Biodivers Conserv 16:1379–1395

    Article  Google Scholar 

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Acknowledgments

We thank Peter Reich, Ian Wright and Simon Pierce for original data on leaf functional traits and Marcos Callisto for providing coordinates. The comments of two reviewers and RC Colwell improved early versions of the manuscript. This research was funded by Conselho Nacional de Pesquisa e Desenvolvimento (APQ-03199-13, 561883/2010-6, 311301/2011-8, 482720/2012), Fundação de Amparo à Pesquisa de Minas Gerais (APQ-04105-10, APQ-02231-12), Sao Paulo Research Foundation (2013/50155-0, 2014/01594-4), the Ministère Français des affaires étrangères et européennes (EGIDE 2009/657176K) and French Embassy / UNESP Rio Claro Chairs 2012 and 2014. We thank CAPES for granting a PVE / Ciência sem fronteiras scholarship (88881.068071/2014-01) to HL and RSO. FAOS, AAC, LPCM, JPLF, CMJ, FSN, GWF, CES, RSO, and QSG received research productivity scholarships from CNPq.

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Silveira, F.A.O., Negreiros, D., Barbosa, N.P.U. et al. Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403, 129–152 (2016). https://doi.org/10.1007/s11104-015-2637-8

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Keywords

  • Biodiversity hotspot
  • Canga
  • Endemism
  • Functional ecology
  • Nutrient-impoverished soils
  • OCBIL theory
  • Plant biogeography