Ecophysiology of Campos Rupestres Plants

  • Rafael S. Oliveira
  • Anna Abrahão
  • Caio Pereira
  • Grazielle S. Teodoro
  • Mauro Brum
  • Suzana Alcantara
  • Hans Lambers


Campos rupestres are rocky seasonally-dry environments that occur over mountaintops in central Brazil. Plant growth is limited and prone to fire during the dry winter, and soils are severely nutrient-impoverished. Plants in these habitats exhibit a wide range of strategies to cope with these limitations. Campos rupestres plants show different rooting depths, according to plant habit and substrate. Water status in plants varies between stable water potentials in isohydric species to water potentials changing according to air humidity in anisohydric plants, some of them being dessication-tolerant and dormant during the dry season (resurrection plants). Carbon assimilation in the dry season is therefore limited by water availability, especially in dessication-tolerant species. A wide variety of mineral nutrition strategies allow effective nutrient acquisition in campos rupestres: mycorrhizas, non-mycorrhizal sand-binding root specializations, symbiotic nitrogen fixation, carnivory, parasitism. The incidence of natural fires may have played a role in the ecological and evolutionary processes that have molded the current flora of campos rupestres, as well as the occurrence of specific functional traits in these habitats. Unveiling the relative importance and prevalence of in situ adaptation and adaptive divergence in the lineages that diversified in campos rupestres will allow us to further discuss mechanisms related to trait evolution and adaptive radiation in campos rupestres.


Arbuscular Mycorrhiza Crassulacean Acid Metabolism Adaptive Radiation Nonstructural Carbohydrate Cluster Root 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We would like to acknowledge Fundo de Apoio à Pesquisa do Estado de São Paulo for funding our research (project 2010/17204-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico and Conselho Aperfeiçoamento de Pessoal de Nível superior for the scholarships, scholarship 2010/50327-8 to G.S. Teodoro, and project grant number CAPES PVE 88887.108541/2015-00. We thank Instituto Chico Mendes de Conservação da Biodiversidade (Sisbio 43511-2) and Instituto Estadual de Florestas de Minas Gerais (056/2014) for the licenses to work in campos rupestres. We also acknowledge the Graduate Programs of Ecology and Plant Biology at Universidade Estadual de Campinas. Finally, we would like to thank the editor for the invitation to write the chapter.


  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 176:345–355PubMedCrossRefGoogle Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67CrossRefGoogle Scholar
  3. Alcantara S, Mello-Silva R, Teodoro GS, Drequeceler K, Ackerly DD, Oliveira RS (2015) Carbon assimilation and habitat segregation in resurrection plants: a comparison between desiccation- and non-desiccation-tolerant species of Neotropical Velloziaceae (Pandanales). Funct Ecol. doi: 10.1111/1365-2435.12462 Google Scholar
  4. Almeida-Abreu PA, Pflug R (1994) The geodynamic evolution of the southern Serra do Espinhaço, Minas Gerais, Brazil. Zentralbl Geol Paläontol Teil 2 Hist Geol Paläontol 1:21–44Google Scholar
  5. Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5–17CrossRefGoogle Scholar
  6. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575–1584PubMedCrossRefGoogle Scholar
  7. Alves RJ, Silva NG (2011) O fogo é sempre um vilão nos campos rupestres? Biodivers Bras 1:120–127Google Scholar
  8. Alves RJV, da Silva NG, Fernandes Júnior AJ, Guimarães AR (2013) Longevity of the Brazilian underground tree Jacaranda decurrens Cham. An Acad Bras Cienc 85:671–678PubMedCrossRefGoogle Scholar
  9. Alves RJV, Silva NG, Oliveira JA, Medeiros D (2014) Circumscribing campo rupestre—megadiverse Brazilian rocky montane savanas. Braz J Biol 74:355–362PubMedCrossRefGoogle Scholar
  10. Amaral MM, Ceccantini G (2011) The endoparasite Pilostyles ulei (Apodanthaceae—Curcubitales) influences wood structure in three host species of Mimosa. IAWA J 32:1–13CrossRefGoogle Scholar
  11. Andrade MJG, Giulietti AM, Rapini A, de Queiroz LP, Conceição AS, de Almeida PRM, van den Berg C (2010) A comprehensive molecular phylogenetic analysis of Eriocaulaceae: evidence from nuclear ITS and plastid psbA-trnH and trnL-trnF DNA sequences. Taxon 59:379–388Google Scholar
  12. Antonelli A, Verola CF, Parisod C, Gustafsson ALS (2010) Climate cooling promoted the expansion and radiation of a threatened group of South American orchids (Epidendroideae: Laeliinae). Biol J Linn Soc 100:597–607CrossRefGoogle Scholar
  13. Appezzato-da-Glória B (2003) Morfologia de sistemas subterrâneos. Histórico e evolução do conhecimento no Brasil. Alexandre Sene Pinto, Ribeirão PretoGoogle Scholar
  14. Appezzato-da-Glória B, Cury G, Soares MKM, Rocha R, Hayashi AH (2008) Underground systems of Asteraceae species from the Brazilian Cerrado. J Torrey Bot Soc 135:103–113CrossRefGoogle Scholar
  15. Araújo KS (2014) Eficiência simbiotica e identificação de estirpes de Burkholderia oriundas de campos rupestres. Dissertation, Universidade Federal de LavrasGoogle Scholar
  16. Araya YN, Silvertown J, Gowing DJ, McConway GJ, Linder HP, Midgley G (2011) A fundamental, eco-hydrological basis for niche segregation in plant communities. New Phytol 189:253–258PubMedCrossRefGoogle Scholar
  17. Arruda R, Fadini RF, Carvalho LN, Del-Claro K, Mourão FA, Jacobi CM, Teodoro GS, van den Berg C, Caires CS, Dettke GA (2012) Ecology of neotropical mistletoes: an important canopy-dwelling component of Brazilian ecosystems. Acta Bot Bras 26:264–274Google Scholar
  18. Ataíde ES, Castro PTA, Fernandes GW (2011) Florística e caracterização de uma área de campo ferruginoso no Complexo Minerário Alegria, Serra de Antônio Pereira, Ouro Preto, Minas Gerais, Brasil. Rev Arv 35:1265–1275CrossRefGoogle Scholar
  19. Baêta HE (2012) Contribuição da deposição úmida (chuva e neblina) nas relações hídricas e nutricionais de fisionomias de campos ferruginosos na Serra da Brígida, Ouro Preto, MG. Dissertation, Universidade Federal de Ouro PretoGoogle Scholar
  20. Barbosa AR, Fiorini CF, Silva-Pereira V, Mello-Silva R, Borba EL (2012) Geographical genetic structuring and phenotypic variation in the Vellozia hirsuta (Velloziaceae) ochlospecies complex. Am J Bot 99:1477–1488PubMedCrossRefGoogle Scholar
  21. Bell TL, Pate JS, Dixon KW (1996) Relationships between fire response, morphology, root anatomy and starch distribution in South-West Australian Epacridaceae. Ann Bot 77:357–364CrossRefGoogle Scholar
  22. Benites VDM, Caiafa AN, de Mendonça ES, Schaefer CE, Ker JC (2003) Solos e vegetação nos complexos rupestres de altitude da Mantiqueira e do Espinhaço. Flor Ambient 10:76–85Google Scholar
  23. Benites VDM, de Sá Mendonça E, Schaefer CEGR, Schaefer CEGR, Novotny EH, Reis EL, Ker JC (2005) Properties of black soil humic acids from high altitude rocky complexes in Brazil. Geoderma 127:104–113CrossRefGoogle Scholar
  24. Benites VDM, Schaefer CEGR, Simas FNB, Santos HG (2007) Soils associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Rev Bras Bot 30:569–577CrossRefGoogle Scholar
  25. Benzing DH (1987) The origin and rarity of botanical carnivory. Trends Ecol Evol 2:364–369CrossRefGoogle Scholar
  26. Bitencourt C, Rapini A (2013) Centres of endemism in the Espinhaço range: identifying cradles and museums of Asclepiadoideae (Apocynaceae). Syst Biodiv 11:525–536CrossRefGoogle Scholar
  27. Borba EL, Felix JM, Solferini VN, Semir J (2001) Fly-pollinated Pleurothallis (Orchidaceae) species have high genetic variability: evidence from isozyme markers. Am J Bot 88:419–428PubMedCrossRefGoogle Scholar
  28. Bourguignon T, ŠObotnÍK JAN, Lepoint G, Martin J-M, Hardy OJ, Dejean A, Roisin Y (2011) Feeding ecology and phylogenetic structure of a complex neotropical termite assemblage, revealed by nitrogen stable isotope ratios. Ecol Entomol 36:261–269CrossRefGoogle Scholar
  29. Bradshaw SD, Dixon KW, Hopper SD, Lambers H, Turner SR (2011) Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci 16:69–76PubMedCrossRefGoogle Scholar
  30. Brum M Jr (2013) Partição de recursos hídricos em comunidades vegetais de campo rupestre e campo de altitude no Sudeste brasileiro—Brasil. Dissertation, University of CampinasGoogle Scholar
  31. 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 320:37–77CrossRefGoogle Scholar
  32. Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235–245PubMedCrossRefGoogle Scholar
  33. Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecol 113:151–161CrossRefGoogle Scholar
  34. Carmo FF, Sousa E, Fonseca FC, Ribeiro LC (2007) Jacobi CM (2007) Recrutamento pós-fogo em dois habitats de um campo rupestre ferruginoso (canga) na Serra da Moeda. Anais do VIII Congresso de Ecologia do Brasil, Caxambu, MG. InGoogle Scholar
  35. Chapin FS, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447CrossRefGoogle Scholar
  36. Conceição AA, Orr BJ (2012) Post-fire flowering and fruiting in Vellozia sincorana, a caulescent rosette plant endemic to Northeast Brazil. Act Bot Bras 26:94–100CrossRefGoogle Scholar
  37. Conceição AA, Pirani JR (2005) Delimitação de habitats em campos rupestres na Chapada Diamantina, Bahia: substratos, composição florística e aspectos estruturais. Bol Bot USP 23:85–111CrossRefGoogle Scholar
  38. Conceição AA, Pirani JR, Meirelles ST (2007) Floristics, structure and soil of insular vegetation in four quartzite-sandstone outcrops of “Chapada Diamantina”, Northeast Brazil. Braz J Bot 30:641–656CrossRefGoogle Scholar
  39. Coutinho LM (1990) Fire in the ecology of the Brazilian Cerrado. In: Goldammer JG (ed) Fire in the tropical biota: ecosystem, processes and global challenges. Springer-Verlag, Berlin, pp 82–105CrossRefGoogle Scholar
  40. Coutinho LM, Miranda HS, Morais HC (2002) O Bioma do Cerrado e o fogo I. Caracterização. Série Cien Amb 20:1–48Google Scholar
  41. Coutinho ES, Fernandes GW, Berbara RLL, Valério HM, Goto BT (2015) Variation of arbuscular mycorrhizal fungal communities along an altitudinal gradient in rupestrian grasslands in Brazil. Mycorrhiza. doi: 10.1007/s00572-015-0636-5 PubMedGoogle Scholar
  42. Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33:1419–1438PubMedGoogle Scholar
  43. de Carvalho F, de 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 52:9–19CrossRefGoogle Scholar
  44. de Oliveira M (1963) Chromatographic isolation of monofluoroacetic acid from Palicourea marcgravii St. Hil. Experientia 19:586–587CrossRefGoogle Scholar
  45. de Souza A, de Moraes MG, Ribeiro RDCLF (2005) Gramíneas do cerrado: carboidratos não-estruturais e aspectos ecofisiológicos. Acta Bot Bras 19:81–90CrossRefGoogle Scholar
  46. Dietrich RC, Bengough AG, Jones HG, White PJ (2012) A new physical interpretation of plant root capacitance. J Exp Bot 63:6149–6159PubMedPubMedCentralCrossRefGoogle Scholar
  47. Drummond CS, Eastwood RJ, Miotto STS, Hughes CE (2012) Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovations with incomplete taxon sampling. Syst Biol 61:443–460PubMedPubMedCentralCrossRefGoogle Scholar
  48. Dutra VF, Garcia FCP (2014) Mimosa L. (Leguminosae-Mimosoideae) dos campos rupestres de Minas Gerais, Brasil. Iheringia 69:49–88Google Scholar
  49. Echternacht L, Trovó M, Oliveira CT, Pirani JR (2011) Areas of endemism in the Espinhaço range in Minas Gerais, Brazil. Flora 206:782–791CrossRefGoogle Scholar
  50. Eiten G (1990) Vegetação. In: Pinto MN (ed) Cerrado: Caracterização, Ocupação e Perspectivas. Editora Universidade de Brasília, Brasília, pp 9–65Google Scholar
  51. Ellison A (2006) Nutrient limitation and stoichiometry of carnivorous plants. Plant Biol 8:740–747PubMedCrossRefGoogle Scholar
  52. FAO (1998) World soil resources report 84. FAO/ISRIC/ISSS, RomeGoogle Scholar
  53. Fernandes GW, Barbosa NP, Negreiros D, Paglia AP (2014) Challenges for the conservation of vanishing megadiverse rupestrian grasslands. Nat Conserv 12:162–165CrossRefGoogle Scholar
  54. Ferreira MMAA, Conceição AA (2012) Alocação preferencial de recursos e morfologia de órgãos subterrâneos em plantas resistentes ao fogo em vegetação campestre. Sitientibus 12:143–149Google Scholar
  55. Ferreira FM, Forzza RC (2009) Florística e caracterização da vegetação da Toca dos Urubus, Baependi, Minas Gerais, Brasil. Biota Neotrop 9:131–148CrossRefGoogle Scholar
  56. Fiaschi P, Pirani JR (2009) Review of plant biogeographic studies in Brazil. J Syst Evol 47:477–496CrossRefGoogle Scholar
  57. Fidelis A, Müller SC, Pillar VDP, Pfadenhauer J (2010) Population biology and regeneration of forbs and shrubs after fire in Brazilian Campos grasslands. Plant Ecol 211:107–117CrossRefGoogle Scholar
  58. Figueira JEC (1998) Dinâmica de populações de Paepalanthus polyanthus (Eriocaulaceae) na Serra do Cipó, MG. PhD Thesis, Universidade Estadual de CampinasGoogle Scholar
  59. Filella I, Peñuelas J (2003) Partitioning of water and nitrogen in co-occurring species of a mediterranean shrubland. Oecologia 137:51–61PubMedCrossRefGoogle Scholar
  60. French JRJ, Turner GL, Bradbury JF (1976) Nitrogen fixation by bacteria from the hindgut of termites. J Gen Microbiol 95:202–206CrossRefGoogle Scholar
  61. Fritsch PW, Almeda F, Renner SS, Martins AB, Cruz BC (2004) Phylogeny and circumscription of the near-endemic Brazilian tribe Microlicieae (Melastomataceae). Am J Bot 91:1105–1114PubMedCrossRefGoogle Scholar
  62. Fritsch PW, Almeda F, Martins AB, Cruz BC, Estes D (2007) Rediscovery and phylogenetic placement of Philcoxia minensis (Plantaginaceae), with a test of carnivory. Proc Calif Acad Sci 58:447–467Google Scholar
  63. Gaff DF (1987) Desiccation tolerant plants in South America. Oecol 74:133–136CrossRefGoogle Scholar
  64. Gaff DF, Oliver M (2013) The evolution of desiccation tolerance in Angiosperm plants: a rare yet common phenomenon. Funct Plant Biol 40:315–328CrossRefGoogle Scholar
  65. Garcia RJF, Longhi-Wagner HM, Pirani JR, Meirelles ST (2009) A contribution to the phytogeography of Brazilian campos: an analysis based on Poaceae. Braz J Bot 32:703–713CrossRefGoogle Scholar
  66. Garcia PM, Asega AF, Silva E, Carvalho MA (2011) Effect of drought and re-watering on fructan metabolism in Vernonia herbacea (Vell.) Rusby. Plant Physiol Biochem 49:664–670PubMedCrossRefGoogle Scholar
  67. Giulietti AM, Pirani JR (1988) Patterns of geographic distribution of some plant species from the Espinhaço range, Minas Gerais and Bahia, Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a workshop on neotropical distribution patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp 39–69Google Scholar
  68. Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço range region, eastern Brazil. In: Davis SD et al (eds) Centres of plant diversity: a guide and strategy for their conservation, vol 3. WWF/IUCN, Cambridge, pp 397–404Google Scholar
  69. Giulietti AM, Harley RM, de Queiroz LP, Wanderley MGL, van den Berg C (2005) Biodiversity and conservation of plants in Brazil. Cons Biol 19:632–639CrossRefGoogle Scholar
  70. Givnish TJ (1989) Ecology and evolution of carnivorous plants. In: Abrahamson WG (ed) Plant-animal interactions. McGraw-Hill, New York, pp 243–290Google Scholar
  71. Givnish TJ (2015) Adaptive radiation versus ‘radiation’ and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. New Phytol 2:297–303CrossRefGoogle Scholar
  72. Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. Am Nat 124:479–497CrossRefGoogle Scholar
  73. Givnish TJ, McDiarmid RW, Buck WR (1986) Fire adaptation in Neblinaria (Theaceae), a high-elevation rosette shrub endemic to a wet equatorial tepui. Oecol 70:481–485CrossRefGoogle Scholar
  74. Givnish TJ, Pires JC, Graham SW, McPherson MC, Prince LM, Rai HS, Patterson TB, Roalson EH, Evans TM, Hahn WJ, Millam KC, Meerow AW, Molvray M, Kores PJ, O’Brien HE, Hall JC, Kress WJ, Sytsma KJ (2006) Phylogenetic relationships of monocots based on the highly informative plastid gene ndhF: evidence for widespread concerted convergence. Aliso 22:28–51Google Scholar
  75. Glaser B (2007) Prehistorically modified soils of central Amazonia: a model for sustainable agriculture in the twenty-first century. Phil Trans Roy Soc B 362:187–196CrossRefGoogle Scholar
  76. Glatzel G, Geils BW (2009) Mistletoe ecophysiology: host-parasite interactions. Bot 87:10–15Google Scholar
  77. Gomes AL, Fernandes GW (1994) Influence of parasitism by Pilostyles ingae (Rafflesiaceae) on its host-plant, Mimosa naguirei (Leguminosae). Ann Bot 74:205–208CrossRefGoogle Scholar
  78. Gomes FCO, Safar SVB, Marques AR, Medeiros AO, Santos ARO, Carvalho C, Lachance MC, Sampaio JP, Rosa CA (2014) The diversity and extracellular enzymatic activities of yeasts isolated from water tanks of Vriesea minarum, an endangered bromeliad species in Brazil, and the description of Occultifur brasiliensis f.a., sp. nov. Antonie Van Leeuwenhoek 107:597–611PubMedCrossRefGoogle Scholar
  79. Gottsberger G, Silberbauer-Gottsberger I (2006) Life in the Cerrado, a South American tropical seasonal ecosystem, vol 1: Origin, structure, dynamics and plant use. Reta Verlag, UlmGoogle Scholar
  80. Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiol 8:4–15CrossRefGoogle Scholar
  81. Güsewell S (2004) N: P Ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  82. Haridasan M (2008) Nutritional adaptations of native plants of the cerrado biome in acid soils. Braz J Plant Physiol 20:183–195CrossRefGoogle Scholar
  83. 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 71–121Google Scholar
  84. Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410CrossRefGoogle Scholar
  85. 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 322:49–86CrossRefGoogle Scholar
  86. Jackson PC, Meinzer FC, Bustamante M, Goldstein G, Franco A, Rundel PW, Caldas L, Igler E, Causin F (1999) Partitioning of soil water among tree species in a Brazilian Cerrado ecosystem. Tree Physiol 19:717–724PubMedCrossRefGoogle Scholar
  87. Jacobi CM, Do Carmo FF, Vincent RC, Stehmann JR (2007) Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodiv Cons 16:2185–2200CrossRefGoogle Scholar
  88. Jacobi CM, Carmo FF, Vincent RC (2008) Estudo fitossociológico de uma comunidade vegetal sobre canga como subsídio para a reabilitação de áreas mineradas no Quadrilátero Ferrífero, MG. Rev Arv 32:345–353CrossRefGoogle Scholar
  89. Jesus FF, Solferini VN, Semir J, Prado PI (2001) Local genetic differentiation in Proteopsis argentea (Asteraceae), a perennial herb endemic in Brazil. Plant Syst Evol 226:59–68CrossRefGoogle Scholar
  90. Jesus FF, Abreu AG, Semir J, Prado PI (2009) Low genetic diversity but local genetic differentiation in endemic Minasia (Asteraceae) species from Brazil. Plant Syst Evol 277:187–196CrossRefGoogle Scholar
  91. Joaquim EDO, de Figueirado-Ribeiro RCL, Hayashi AH, de Carvalho MAM (2014) Inulin contents and tissue distribution in storage underground organs of Asteraceae from the Brazilian rocky fields. Bot 92:827–836CrossRefGoogle Scholar
  92. Joly AB (1970) Conheça a vegetação brasileira. EDUSP e Polígono, São PauloGoogle Scholar
  93. Jordan GJ, Weston PH, Carpenter RJ, Dillon RA, Brodribb TJ (2008) The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae. Am J Bot 95:521–530PubMedCrossRefGoogle Scholar
  94. Krebs H, Kemmerling W, Habermehl G (1994) Qualitative and quantitative determination of fluoroacetic acid in Arrabidea bilabiata and Palicourea marcgravii by 19F-NMR spectroscopy. Toxicon 32:909–913PubMedCrossRefGoogle Scholar
  95. Kuijt J (1969) The biology of parasitic plants. University of California Press, BerkeleyGoogle Scholar
  96. Lambers H, Cramer MD, Shane MW, Wouterlood M, Veneklaas EJ (2003) Structure and functioning of cluster roots and plant responses to phosphate deficiency. Plant Soil 248:693–713CrossRefGoogle Scholar
  97. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98:693–713PubMedPubMedCentralCrossRefGoogle Scholar
  98. Lambers H, Chapin FS, Pons TL (2008a) Plant physiological ecology. Springer, New YorkCrossRefGoogle Scholar
  99. Lambers H, Raven JA, Shaver GR, Smith SE (2008b) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103PubMedCrossRefGoogle Scholar
  100. 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 334:11–31CrossRefGoogle Scholar
  101. Lambers H, Ahmedi I, Berkowitz O, Lambers H, Ahmedi I, Berkowitz O, Dunne C, Finnegan PM, Hardy GEStJ, Jost R, Laliberté E, Pearse SJ, Teste FP (2013) Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Cons Physiol 1:cot010Google Scholar
  102. Lambers H, Clements JC, Nelson MN (2013b) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288PubMedCrossRefGoogle Scholar
  103. Lambers H, Colmer TD, Hassiotou F, Mitchell PM, Poot P, Shane MW, Veneklaas EJ (2014) Carbon and water relations. In: Lambers H (ed) Plant life on the sandplains in southwest Australia, a global biodiversity hotspot. UWA Publishing, CrawleyGoogle Scholar
  104. Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90PubMedCrossRefGoogle Scholar
  105. Lambert SM, Borba EL, Machado MC (2006) Allozyme diversity and morphometrics of the endangered Melocactus glaucescens (Cactaceae), and investigation of the putative hybrid origin of Melocactus × albicephalus (Melocactus ernestii × M. glaucescens) in north-eastern Brazil. Plant Spec 21:93–108CrossRefGoogle Scholar
  106. Landeweert R, Hoffland E, Finlay RD, Kuyper TW, Van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254PubMedCrossRefGoogle Scholar
  107. Le Stradic S (2012) Composition, phenology and restoration of campo rupestre mountain grasslands-Brazil. PhD Thesis, Université d’Avignon et des Pays de Vaucluse, Avignon and Universidade Federal de Minas GeraisGoogle Scholar
  108. Le Stradic S, Silveira FAO, Buisson E, Cazelles K, Carvalho V, Fernandes GW (2015) Diversity of germination strategies and seed dormancy in herbaceous species of campo rupestre grasslands. Aust Ecol 40:537–546CrossRefGoogle Scholar
  109. Lee ST, Cook D, Riet-Correa F, Pfister JA, Anderson WR, Lima FG, Gardner DR (2012) Detection of monofluoroacetate in Palicourea and Amorimia species. Toxicon 60:791–796PubMedCrossRefGoogle Scholar
  110. Lemes FOA (2009) Relações florísticas, fitossociológicas e aspectos edáficos de comunidades de campos rupestres da Serra do Itacolomi e Serra de Ouro Branco, Minas Gerais. Dissertation, Universidade Federal de Ouro PretoGoogle Scholar
  111. Linder HP (2003) The radiation of the Cape flora, southern Africa. Biol Rev 78:597–638PubMedCrossRefGoogle Scholar
  112. Litsios G, Wüest RO, Kostikova A, Forest F, Lexer C, Linder HP, Pearman PB, Zimmermann NE, Salamin N (2013) Effects of a fire response trait on diversification in replicated radiations. Evol 68:453–465CrossRefGoogle Scholar
  113. 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. South Afr J Bot 87:27–33CrossRefGoogle Scholar
  114. Losos JB (2011) Convergent, adaptation, and constraint. Evol 65:1827–1840CrossRefGoogle Scholar
  115. Louille B, Semir J, Lohmann LG, Pirani JR (2015) A phylogenetic analysis of Lychnophorinae (Asteraceae: Vernonieae) based on molecular and morphological data. Syst Bot 40:299–315CrossRefGoogle Scholar
  116. Lovo J, Winkworth RC, Mello-Silva R (2012) New insights into Trimezieae (Iridaceae) phylogeny: what do molecular data tell us? Ann Bot 110:689–702PubMedPubMedCentralCrossRefGoogle Scholar
  117. Lusa MG, Cardoso EC, Machado SR, Appezzato-da-Glória B (2014a) Trichomes related to an unusual method of water retention and protection of the stem apex in an arid zone perennial species. AoB Plants plu088Google Scholar
  118. Lusa MG, Appezzato-da-Glória B, Loeuille B, Bartoli G, Ciccarelli D (2014b) Functional groups in Lychnophorinae (Asteraceae: Vernonieae) based on morphological and anatomical traits. Aust J Bot 62:150–163CrossRefGoogle Scholar
  119. Lüttge U (2008) Savannas II. The environmental factors water, mineral nutrients and fire. In: Lüttge U (ed) Physiological ecology of tropical plants. Springer, Berlin, pp 313–377Google Scholar
  120. Lüttge U, Duarte HM, Scarano FR, Attos EA, Cavalin PO, Franco AC, Fernandes GW (2007) Physiological ecology of photosynthesis of five sympatric species of Velloziaceae in the rupestrian fields of Serra do Cipó, Minas Gerais, Brazil. Flora 202:637–646CrossRefGoogle Scholar
  121. Lynch JP, Ho MD (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269:45–56CrossRefGoogle Scholar
  122. Madriñán S, Cortés AJ, Richardson JE (2013) Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Front Gen 4:1–7Google Scholar
  123. Mamede MCH (1993) Anatomia dos orgãos Vegetativos de Camarea (Malpighiaceae). Acta Bot Bras 7:3–19CrossRefGoogle Scholar
  124. Marschner P (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, LondonGoogle Scholar
  125. Matias SR, Pagano MC, Muzzi FC, Oliveira C, Carneiro A, Horta N, Scotti M (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 45:259–266CrossRefGoogle Scholar
  126. McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol 50:695–718PubMedCrossRefGoogle Scholar
  127. McDowell NG, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739PubMedCrossRefGoogle Scholar
  128. McDowell NG, Fisher RA, Xu C, Domec JC, Höltta T, Mackay DS, Sperry JS, Boutz A, Dickman LT, Gehres N, Limousin M, Macalady A, Martınez-Vilalta J, Mencuccini M, Plaut JA, Ogée J, Pangle RE, Rasse DP, Ryan MG, Sevanto S, Waring RH, Williams AP, Yepez EA, Pockman WT (2013) Evaluating theories of drought-induced vegetation mortality using a multimodel—experiment framework. New Phytol 200:304–321PubMedCrossRefGoogle Scholar
  129. McPherson S (2010) Carnivorous plants and their habitats, 2nd edn. Red Fern Natural History, PooleGoogle Scholar
  130. Medina E (1982) Physiological ecology of neotropical Savanna plants. In: Huntles BJ, Walker BH (eds) Ecological studies, vol 42., Ecology of tropical savannasSpringer, Berlin, pp 308–335Google Scholar
  131. Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23:922–930CrossRefGoogle Scholar
  132. Meirelles ST, Pivello VR, Joly CA (1999) The vegetation of granite rock outcrops in Rio de Janeiro, Brazil, and the need for its protection. Environ Cons 26:10–20CrossRefGoogle Scholar
  133. Mello-Silva R (2004) Novitates Velloziacearum florae phanerogamicae Sancti Pauli. Rev Brasil Bot 27:453–462CrossRefGoogle Scholar
  134. 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 108:87–102PubMedPubMedCentralCrossRefGoogle Scholar
  135. Menezes NL, Müller C, Sajo MDG (1979) Um novo e peculiar tipo de sistema subterrâneo em espécies de Vernonia da Serra do Cipó. Bol Bot USP 7:33–38CrossRefGoogle Scholar
  136. Messias MCTB, Leite MGP, Meira-Neto JAA, Kozovits AR (2011) Life-form spectra of quartzite and itabirite rocky outcrop sites, Minas Gerais, Brazil. Biota Neotrop 11:255–268CrossRefGoogle Scholar
  137. Messias MCTB, Leite MGP, Meira-Neto JAA, Kozovits AR (2012) Fitossociologia de campos rupestres quartzíticos e ferruginosos no Quadrilátero Ferrífero, Minas Gerais. Acta Bot Bras 26:230–242CrossRefGoogle Scholar
  138. Messias MCTB, Leite MGP, Meira Neto JAA, Kozovits AR, Tavares R (2013) Soil-vegetation relationship in quartzitic and ferruginous Brazilian rocky outcrops. Folia Geobot 48:509–521CrossRefGoogle Scholar
  139. Miller RM (2005) The nonmycorrhizal root: a strategy for survival in nutrient-impoverished soils. New Phytol 165:655–658PubMedCrossRefGoogle Scholar
  140. 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 204:604–611CrossRefGoogle Scholar
  141. Morokawa R, Simões AO, Kinoshita LS (2013) Apocynaceae s. str. do Parque Nacional da Serra da Canastra, Minas Gerais, Brasil. Rodriguésia 64:179–199CrossRefGoogle Scholar
  142. Mourão FA, Carmo FF, Ratton P, Jacobi CM (2006) Hospedeiras da hemiparasita Struthanthus flexicaulis (Mart.) Mart. (Loranthaceae) em campos rupestres ferruginosos do Quadrilátero Ferrífero, Minas Gerais. Lundiana 7:103–109Google Scholar
  143. Mourão FA, Jacobi CM, Figueira JEC, Batista EKL (2009) Effects of the parasitism of Struthanthus flexicaulis (Mart.) Mart. (Loranthaceae) on the fitness of Mimosa calodendron Mart. (Fabaceae), an endemic shrub from rupestrian fields over ironstone outcrops, Minas Gerais State, Brazil. Acta Bot Bras 23:820–825. 2009Google Scholar
  144. Muler AL, Oliveira RS, Lambers H, Veneklaas EJ (2014) Does cluster-root activity benefit nutrient uptake and growth of co-existing species? Oecologia 174:23–31PubMedCrossRefGoogle Scholar
  145. Muller KF, Borsch T, Legendre L, Porembski S, Barthlott W (2006) Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol 8:748–757PubMedCrossRefGoogle Scholar
  146. Negreiros D, Borges Moraes ML, Wilson Fernandes G (2008) Caracterização da fertilidade dos solos de quatro leguminosas de campos rupestres, Serra do Cipó, MG, Brasil. Rev Cien Suelo Nutr Veg 8:30–39Google Scholar
  147. Negreiros D, Fernandes GW, Silveira FA, Chalub C (2009) Seedling growth and biomass allocation of endemic and threatened shrubs of rupestrian fields. Acta Oecol 35:301–310CrossRefGoogle Scholar
  148. 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 Cons 6:156–161Google Scholar
  149. 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 215:379–388CrossRefGoogle Scholar
  150. Neves SPS, Conceição AB (2010) Campo rupestre recém-queimado na Chapada Diamantina, Bahia, Brasil: plantas de rebrota e sementes, com espécies endêmicas na rocha. Acta Bot Bras 24:697–707CrossRefGoogle Scholar
  151. Neves SC, Abreu PAAS, Fraga LM (2005) Fisiografia. In: Silva AC, Pedreira LCVSF, Abreu PAA (eds) Serra do Espinhaço meridional—paisagens e ambientes. O Lutador, Diamantina, pp 45–58Google Scholar
  152. Nickrent DL, Musselman LJ (2004) Introduction to parasitic flowering plants. Plant Health Instructor. doi: 10.1094/PHI-I-2004-0330-01 Google Scholar
  153. Nielsen R (2009) Adaptionism - 30 years after Gould and Lewontin. Evolution 63:2487–2490PubMedCrossRefGoogle Scholar
  154. Nishi AH, Vasconcellos-Neto J, Romero GQ (2013) The role of multiple partners in a digestive mutualism with a protocarnivorous plant. Ann Bot 111:143–150PubMedPubMedCentralCrossRefGoogle Scholar
  155. Nogueira RE, Pereira OL, Kasuya MCM, Lanna MCS, Mendonça MP (2005) Fungos micorrízicos associados a orquídeas em campos rupestres na região do Quadrilátero Ferrífero, MG, Brasil. Acta Bot Bras 19:417–424CrossRefGoogle Scholar
  156. North GB, Nobel PS (1997) Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant Soil 191:249–258CrossRefGoogle Scholar
  157. Ogle K, Reynolds JF (2002) Desert dogma revisited: coupling of stomatal conductance and photosynthesis in the desert shrub, Larrea tridentata. Plant, Cell Environ 25:909–921CrossRefGoogle Scholar
  158. Oliveira RB, Godoy SAP (2007) Floristic composition of the rock outcrops of the Morro do Forno, Altinópolis-SP. Biota Neotrop 7:37–47CrossRefGoogle Scholar
  159. Oliveira RS, Dawson TE, Burgess SS (2005) Evidence for direct water absorption by the shoot of the desiccation-tolerant plant Vellozia flavicans in the savannas of central Brazil. J Trop Ecol 21:585–588CrossRefGoogle Scholar
  160. 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 205:1183–1194PubMedCrossRefGoogle Scholar
  161. Oriani A, Scatena VL (2007) Intracellular papillae of Actinocephalus (Eriocaulaceae-Poales) roots and their interaction with fungi: a light and transmission electron microscopy study. Micron 38:611–617PubMedCrossRefGoogle Scholar
  162. Overbeck GE, Pfadenhauer J (2007) Adaptive strategies in burned sub-tropical grassland in southern Brazil. Flora 202:27–49CrossRefGoogle Scholar
  163. Pate JS, Unkovich MJ, Erskine PD, Stewart GR (1998) Australian mulga ecosystems 13C and 15N natural abundances of biota components and their ecophysiological significance. Plant, Cell Environ 21:1231–1242CrossRefGoogle Scholar
  164. Pekin BK, Boer MM, Wittkuhn RS, Macfarlane C, Grierson PF (2012) Plant diversity is linked to nutrient limitation of dominant species in a world biodiversity hotspot. J Veg Sci 23:745–754CrossRefGoogle Scholar
  165. Peñuelas J, Terradas J, Lloret F (2011) Solving the conundrum of plant species coexistence: water in space and time matters most. New Phytol 189:5–8PubMedCrossRefGoogle Scholar
  166. 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 109:1154–1158PubMedPubMedCentralCrossRefGoogle Scholar
  167. Pillai SK, Pillai A (1961) Root apical organization in Monocotyledons—Xyridaceae. Proc Indian Acad Sci Sect B 54:234–240Google Scholar
  168. Pita PB, Menezes NL (2002) Anatomia da raiz de espécies de Dyckia Schult. f. e Encholirium Mart. ex Schult. & Schult. f. (Bromeliaceae, Pitcairnioideae) da Serra do Cipó (Minas Gerais, Brasil), com especial referência ao velame. Rev Bras Bot 25:25–34CrossRefGoogle Scholar
  169. Plaut JA, Yepez EA, Hill J, Pangle R, Pangle R, Sperry JS, Pockman WT, Mcdowell NT (2012) Hydraulic limits preceding mortality in piñon-juniper woodland under experimental drought. Plant Cell Environ 35:1601–1617PubMedCrossRefGoogle Scholar
  170. Pomerene JB (1964) Geology and ore deposits of the Belo Horizonte, Ibirite, and Macacos Quadrangles, Minas Gerais, Brazil. Geol Surv Prof Pap 341-D:1–84Google Scholar
  171. Poot P, Hopper SD, van Diggelen JM (2012) Exploring rock fissures: does a specialized root morphology explain endemism on granite outcrops? Ann Bot 110:291–300PubMedPubMedCentralCrossRefGoogle Scholar
  172. Porder S, Ramachandran S (2013) The phosphorus concentration of common rocks-a potential driver of ecosystem P status. Plant Soil 367:41–55CrossRefGoogle Scholar
  173. Porembski S, Barthlott W (1995) On the occurrence of a velamen radicum in Cyperaceae and Velloziaceae. Nord J Bot 15:625–629CrossRefGoogle Scholar
  174. Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol 151:19–28CrossRefGoogle Scholar
  175. Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751PubMedCrossRefGoogle Scholar
  176. Press MC, Scholes JD, Watling JR (1999) Parasitic plants: physiological and ecological interactions with their hosts. In: Press MC, Scholes JD, Barker MG (eds) Physiological plant ecology. Blackwell Science, Oxford, pp 175–197Google Scholar
  177. Proctor MCF, Tuba Z (2002) Poikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytol 156:327–349CrossRefGoogle Scholar
  178. Rapini A, Ribeiro PL, Lambert S, Pirani JR (2008) A flora dos campos rupestres da Cadeia do Espinhaço. Megadiv 4:15–23Google Scholar
  179. Raven JA (2012) Protein turnover and plant RNA and phosphorus requirements in relation to nitrogen fixation. Plant Sci 188–189:25–35PubMedCrossRefGoogle Scholar
  180. Reis FB Jr, Simon MF, Gross E, Boddey RM, Elliott GN, Neto NE, Loureiro MF, Queiroz LP, Scotti MR, Chen WM, Noren A, Rubio MC, Faria SM, Bontemps C, Goi SR, Young PW, Sprent JI, James EK (2010) Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil. New Phytol 186:934–946PubMedCrossRefGoogle Scholar
  181. Ribeiro KT, Fernandes GW (2000) Patterns of abundance of a narrow endemic species in a tropical and infertile montane habitat. Plant Ecol 147:205–218CrossRefGoogle Scholar
  182. Ribeiro KT, Medina BMO (2002) Estrutura, dinâmica e biogeografia das ilhas de vegetação sobre rocha do Planalto do Itatiaia, RJ. Bol Parque Nac Itatiaia 10:1–84Google Scholar
  183. Ribeiro JF, Walter BMT (2008) As principais fitofisionomias do bioma cerrado. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado: ecologia e flora. Embrapa/CPAC, PlanaltinaGoogle Scholar
  184. Ribeiro KT, Medina BMO, Scarano FR (2007) Composição de espécies e relações biogeográficas da flora sobre afloramentos rochosos no Planalto do Itatiaia, SE do Brasil. Rev Bras Bot 30:623–639CrossRefGoogle Scholar
  185. Ribeiro PL, Borba EL, Smidt EC, Lambert SM, Schnadelbach AS, van den Berg C (2008) Genetic and morphological variation in the Bulbophyllum exaltatum (Orchidaceae) complex occurring in the Brazilian campos rupestres: implications for taxonomy and biogeography. Plant Syst Evol 270:109–137CrossRefGoogle Scholar
  186. Ribeiro PL, Rapini A, Damascena LS, van den Berg C (2014) Plant diversification in the Espinhaço Range: insights from the biogeography of Minaria (Apocynaceae). Taxon 63:1253–1264CrossRefGoogle Scholar
  187. Rivadavia F, Vicentini A, Fleischmann A (2009) A new species of sundew (Drosera, Droseraceae), with water-dispersed seed, from the floodplains of the northern Amazon Basin, Brazil. Ecotropica 15:13–21Google Scholar
  188. Rodrigues KF, Batista LG, Carrenho R (2013) Micorrizas arbusculares em espécies de Microlicieae (Melastomataceae) da Chapada dos Veadeiros, Goiás. In: 64 Congresso Nacional de Botânica. Belo HorizonteGoogle Scholar
  189. Rossatto DR, da Silveira Lobo Sternberg L, Franco AC (2013) The partitioning of water uptake between growth forms in a Neotropical savanna: do herbs exploit a third water source niche? Plant Biol 15:84–92PubMedCrossRefGoogle Scholar
  190. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560PubMedCrossRefGoogle Scholar
  191. Saadi A (1995) A geomorfologia da Serra do Espinhaço em Minas Gerais e de suas margens. Geonomos 3:41–63CrossRefGoogle Scholar
  192. Safford HD (2001) Brazilian Páramos. III. Patterns and rates of postfire regeneration in Campos de Altitude. Biotrop 33:282–302Google Scholar
  193. Sala A, Piper F, Hoch G (2010) Physiological mechanisms of drought-induced tree mortality are far from being resolved. New Phytol 186:274–281PubMedCrossRefGoogle Scholar
  194. Santos TRD, Pinto JRR, Lenza E, Mews HA (2012) The tree-shrub vegetation in rocky outcrop cerrado areas in Goiás State, Brazil. Braz J Bot 35:281–294CrossRefGoogle Scholar
  195. Scatena VL, Oriani A, Sano PT (2005) Anatomia de raízes de Actinocephalus (Koern.) Sano (Eriocaulaceae). Acta Bot Bras 19:835–841CrossRefGoogle Scholar
  196. Schluter D (1990) Species-for-species matching. Am Nat 136:560–568CrossRefGoogle Scholar
  197. Schwinning S (2010) The ecohydrology of roots in rocks. Ecohydrol 3:238–245Google Scholar
  198. Schwinning S, Ehleringer JR (2001) Water use trade-offs and optimal adaptations to pulse-driven arid ecosystems. J Ecol 89:464–480CrossRefGoogle Scholar
  199. Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125CrossRefGoogle Scholar
  200. Shane MW, Dixon KW, Lambers H (2005) The occurrence of dauciform roots amongst western Australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae). New Phytol 165:887–898PubMedCrossRefGoogle Scholar
  201. 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 29:1989–1999PubMedCrossRefGoogle Scholar
  202. Shaw DC, Watson DM, Mathiasen RL (2004) Comparison of dwarf mistletoe (Arceuthobium spp., Viscaceae) in the weastern United States with mistletoe (Amyema spp., Loranthaceae) in Australia: ecological analogs and reciprocal models for ecosystem management. Aust J Bot 52:481–498CrossRefGoogle Scholar
  203. Silva ED, Martins AB (2013) Leguminosae-Papilionoideae in the Serra do Cabral, Minas Gerais State, Brazil. Hoehnea 40:293–314CrossRefGoogle Scholar
  204. Silva NG, Alves RJV, Pereira JF, Rivadavia F (2011) Lentibulariaceae, Serra de São José, Minas Gerais, Brazil. Checklist 7:120–127Google Scholar
  205. Silveira FAO, Negreiros D, Barbosa NPU, Buisson E, Carmo FF, Carstensen D, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TJ, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil (in press)Google Scholar
  206. Silvertown J, Araya Y, Gowing D (2015) Hydrological niches in terrestrial plant communities: a review. J Ecol 103:93–108CrossRefGoogle Scholar
  207. Simmons GC (1968) Geology and iron deposits of the Western Serra do Curral, Minas Gerais, Brazil. Geol Surv Prof Pap 341-G:1–57Google Scholar
  208. Simon MF, Grether R, de Queiroz LP, Skemae 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 USA 106:20359–20364PubMedPubMedCentralCrossRefGoogle Scholar
  209. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  210. Smith RJ, Hopper SD, Shane MW (2011) Sand-binding roots in Haemodoraceae: global survey and morphology in a phylogenetic context. Plant Soil 348:453–470CrossRefGoogle Scholar
  211. Souza JMS (2011) Efeitos do fogo na fenologia reprodutiva de angiospermas em vegetações campestres na Chapada Diamantina, Brasil. PhD Thesis, Universidade Estadual de Feira de SantanaGoogle Scholar
  212. Specht RL (1969) A comparison of the sclerophyllous vegetation characteristic of Mediterranean type climates in France, California, and Southern Australia. I. Structure, morphology, and succession. Aust J Bot 17:277–282CrossRefGoogle Scholar
  213. Sprent JI (1979) The biology of nitrogen-fixing organisms. McGraw-Hill, LondonGoogle Scholar
  214. Stock WD, Verboom GA (2012) Phylogenetic ecology of foliar N and P concentrations and N: P ratios across mediterranean-type ecosystems. Glob Ecol Biogeogr 21:1147–1156CrossRefGoogle Scholar
  215. Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. J Exp Bot 49:419–432CrossRefGoogle Scholar
  216. Tayasu I, Inoue T, Miller LR, Sugimoto A, Takeichi S, Abe T (1998) Confirmation of soil-feeding termites (Isoptera; Termitidae; Termitinae) in Australia using stable isotope ratios. Funct Ecol 12:536–542CrossRefGoogle Scholar
  217. Taylor P, Souza VC, Giulietti AM, Harley RM (2000) Philcoxia: a new genus of Scrophulariaceae with three new species from eastern Brazil. Kew Bull 55:155–163CrossRefGoogle Scholar
  218. Teixeira WA, Lemos-Filho JP (1998) Metais pesados em folhas de espécies lenhosas colonizadoras de uma área de mineração de ferro em Itabirito, Minas Gerais. Rev Árvore 22:381–388Google Scholar
  219. Teodoro GS (2014) Extreme drought effects on the phenology, growth and ecophysiology performance of campos rupestres species—Brazil. PhD Thesis, Universidade Estadual de CampinasGoogle Scholar
  220. Tertuliano MF, Figueiredo-Ribeiro RCL (1993) Distribution of fructose polymers in herbaceous species of Asteraceae from the cerrado. New Phytol 123:741–749CrossRefGoogle Scholar
  221. Trovó M, Andrade MJG, Sano PT, Ribeiro PL, Berg C (2013) Molecular phylogenetics and biogeography of Neotropical Paepalanthoideae with emphasis on Brazilian Paepalanthus (Eriocaulaceae). Bot J Linn Soc 171:225–243CrossRefGoogle Scholar
  222. Tuba Z, Protor CF, Csintalan Z (1998) Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective. Plant Growth Reg 24:211–217CrossRefGoogle Scholar
  223. Turner BL, Condron LM (2013) Pedogenesis, nutrient dynamics, and ecosystem development: the legacy of T.W. Walker and J.K. Syers. Plant Soil 367:1–10CrossRefGoogle Scholar
  224. Twigg LE (2014) Fluoroacetate, plants, animals and a biological arms race. In: Lambers H (ed) Plant life on the sandplains in southwest Australia, a global biodiversity hotspot. University of Western Australia Publishing, Crawley, pp 225–240Google Scholar
  225. USDA (1998) Keys to soil taxonomy. United States Department of Agriculture, New YorkGoogle Scholar
  226. Vasconcelos M (2011) O que são campos rupestres e campos de altitude nos topos de montanha do Leste do Brasil? Braz J Bot 34:241–246CrossRefGoogle Scholar
  227. 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 13:154–162CrossRefGoogle Scholar
  228. Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220CrossRefGoogle Scholar
  229. Vickery B, Vickery M (1972) Fluoride metabolism in Dichapetalum toxicarium. Phytochem 11:1905–1909CrossRefGoogle Scholar
  230. Vincent RDC, Meguro M (2008) Influence of soil properties on the abundance of plant species in ferruginous rocky soils vegetation, southeastern Brazil. Rev Bras Bot 31:377–388CrossRefGoogle Scholar
  231. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochem 57–58:1–45CrossRefGoogle Scholar
  232. Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  233. Walter H (1971) Ecology of tropical and subtropical vegetation. Oliver & Boyd, EdinburghGoogle Scholar
  234. West AG, Dawson TE, February EC, Midgley GF, Bond WJ, Aston TL (2012) Diverse functional responses to drought in a Mediterranean-type shrubland in South Africa. New Phytol 195:396–407PubMedCrossRefGoogle Scholar
  235. Williamson B (1973) Acid phosphatase and esterase activity in orchid mycorrhiza. Planta 112:149–158PubMedCrossRefGoogle Scholar
  236. Yao Q, Li X, Feng G, Christie P (2001) Mobilization of sparingly soluble inorganic phosphates by the external mycelium of an arbuscular mycorrhizal fungus. Plant Soil 230:279–285CrossRefGoogle Scholar
  237. Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1–4Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Rafael S. Oliveira
    • 1
    • 2
  • Anna Abrahão
    • 1
    • 2
  • Caio Pereira
    • 1
    • 2
  • Grazielle S. Teodoro
    • 1
    • 3
  • Mauro Brum
    • 1
  • Suzana Alcantara
    • 4
  • Hans Lambers
    • 2
  1. 1.Departamento de Biologia VegetalUniversidade Estadual de CampinasCampinasBrazil
  2. 2.School of Plant BiologyUniversity of Western AustraliaPerthAustralia
  3. 3.Departamento de Engenharia FlorestalUniversidade Federal de LavrasLavrasBrazil
  4. 4.Departamento de BotânicaUniversidade Federal de Santa CatarinaFlorianópolisBrazil

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