Plant biodiversity drivers in brazilian campos rupestres: Insights from phylogenetic structure

Frontiers in Plant Science

Volumn 8, Issue , 2017, Pages

  Zappi, Daniela C ^a,b   Moro, Marcelo F ^c   Meagher, Thomas R ^d   Lughadha, Eimear Nic ^e  

^a INSTITUTO TECNOLÓGICO VALE   (Brazil)

^b MUSEU PARAENSE EMÍLIO GOELDI   (Brazil)

^c FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

^e ROYAL BOTANIC GARDENS   (United Kingdom)

Author keywords

Campo rupestre; Canga; Eastern Brazil; Phylogenetic clustering; Rupestrian grasslands; Substrate; Vegetation types

Indexed keywords

EID: 85040508513     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2017.02141     Document Type: Article

References (67)

1. Alkmim, F. F. (2012). “Serra do espinhaço e chapada diamantina,” in Geologia do Brasil, eds Y. Hasui, C. D. R. Carneiro, F. F. M. Almeida, and A. Bartorelli (São Paulo: Editora Beca), 236–244.
2. Barbosa-Silva, R., Labiak, P. H., Dos Santos Bragança Gil, A., Goldenberg, R., Michelangeli, F. A., Martinelli, G., et al. (2016). Over the hills and far away: new plant records for the guayana shield in Brazil. Brittonia 68, 397–408. doi: 10.1007/s12228-016-9435-3
3. Bell, C. D., Soltis, D. E., and Soltis, P. S. (2010). The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97, 1296–1303. doi: 10.3732/ajb.0900346
4. BRAHMS (2015). University of Oxford: Botanical Research and Herbarium Management System (BRAHMS) [Online]. Available at: http://herbaria.plants. ox.ac.uk/bol/brahms [accessed November 25, 2015].
5. Brazil Flora Group [BFG] (2015). Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66, 1085–1113. doi: 10.1590/2175-7860201566411
6. Broadley, M. R., Willey, N. J., Wilkins, J. C., Baker, A. J. M., Mead, A., and White, P. J. (2001). Phylogenetic variation in heavy metal accumulation in angiosperms. New Phytol. 152, 9–27. doi: 10.1046/j.0028-646x.2001.00238.x
7. Carvalho, G. H., Cianciaruso, M. V., and Batalha, M. A. (2010). Plantminer: a web tool for checking and gathering plant species taxonomic information. Environ. Model. Softw. 25, 815–816. doi: 10.1016/j.envsoft.2009.11.014
8. Cavender-Bares, J., Kozak, K. H., Fine, P. V. A., and Kembel, S. W. (2009). The merging of community ecology and phylogenetic biology. Ecol. Lett. 12, 693–715. doi: 10.1111/j.1461-0248.2009.01314.x
9. Coelho, M. S., Carlos, P. P., Pinto, V. D., Meireles, A., Negreiros, D., Morellato, L. P. C., et al. (2018). Connection between tree functional traits and environmental parameters in an archipelago of montane forests surrounded by rupestrian grasslands. Flora (in press). doi: 10.1016/j.flora.2017.04.003
10. Dayrell, R. L., Garcia, Q. S., Negreiros, D., Baskin, C. C., Baskin, J. M., and Silveira, F. A. (2017). Phylogeny strongly drives seed dormancy and quality in a climatically buffered hotspot for plant endemism. Ann. Bot. 119, 267–277. doi: 10.1093/aob/mcw163
11. Dexter, K. G., Lavin, M., Torke, B. M., Twyford, A. D., Kursar, T. A., Coley, P. D., et al. (2017). Dispersal assembly of rain forest tree communities across the Amazon basin. Proc. Natl. Acad. Sci. U.S.A. 114, 2645–2650. doi: 10.1073/pnas. 1613655114
12. DRYFLOR, Banda, R. K., Delgado-Salinas, A., Dexter, K. G., Linares-Palomino, R., Oliveira-Filho, A., et al. (2016). Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353, 1383–1387. doi: 10.1126/science.aaf5080
13. Ferrari, L. T., Schaefer, C. E. G. R., Fernandes, R. B. A., Mendonça, B. A. F., Gjorup, D. F., Corrêa, G. R., et al. (2016). “Thermic and hydric dynamics of ironstone (Canga) and quartzite rupestrian grasslands in the Quadrilátero Ferrífero: the ecological importance of water,” in Ecology and Conservation of Mountaintop Grasslands in Brazil, ed. G. W. Fernandes (Cham: Springer International Publishing), 71–85.
14. Gastauer, M., and Meira-Neto, J. A. A. (2016). An enhanced calibration of a recently released megatree for the analysis of phylogenetic diversity. Braz. J. Biol. 76, 619–628. doi: 10.1590/1519-6984.20814
15. Gerhold, P., Cahill, J. F., Winter, M., Bartish, I. V., and Prinzing, A. (2015). Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Funct. Ecol. 29, 600–614. doi: 10.1111/1365-2435.12425
16. Giulietti, A. M., Pirani, J. R., and Harley, R. M. (1997). “Espinhaço Range region – Eastern Brazil,” in Centres of Plant Diversity: A Guide and Strategy for Their Conservation, the Americas, Vol. 3, eds S. D. Davis, V. H. Heywood, O. Herrera-MacBryde, J. Villa-Lobos, and A. C. Hamilton (Cambridge: WWF/IUCN Publications Unit), 397–404.
17. Giulietti, A. M., Wanderley, M. D. G. L., Longhi-Wagner, H. M., Pirani, J. R., and Parra, L. R. (1996). Studies in “sempre-vivas” (everlasting plants): taxonomy focusing the species from Minas Gerais, Brazil. Acta Bot. Brasilica 10, 329–377. doi: 10.1590/S0102-33061996000200007
18. Hedges, S. B., and Kumar, S. (2009). The Timetree of Life. New York, NY: Oxford University Press.
19. Hopper, S. D. (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. doi: 10.1007/s11104-009-0068-0
20. Hopper, S. D., Silveira, F. A. O., and Fiedler, P. L. (2016). Biodiversity hotspots and Ocbil theory. Plant Soil 403, 167–216. doi: 10.1007/s11104-015-2764-2
21. Jacobi, C. M., and Carmo, F. F. (2008). The contribution of ironstone outcrops to plant diversity in the iron quadrangle, a threatened Brazilian landscape. AMBIO 37, 324–326. doi: 10.1579/0044-7447(2008)37[324:TCOIOT]2.0.CO;2
22. Jacobi, C. M., Carmo, F. F., Vincent, R. C., and Stehmann, J. R. (2007). Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers. Conserv. 16, 2185–2200. doi: 10.1007/s10531-007-9156-8
23. Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464. doi: 10.1093/bioinformatics/btq166
24. Kraft, N. J., Cornwell, W. K., Webb, C. O., and Ackerly, D. D. (2007). Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am. Nat. 170, 271–283. doi: 10.1086/519400
25. Kraft, N. J. B., Adler, P. B., Godoy, O., James, E. C., Fuller, S., and Levine, J. M. (2015). Community assembly, coexistence and the environmental filtering metaphor. Funct. Ecol. 29, 592–599. doi: 10.1111/1365-2435.12345
26. Lawrence, K., and Nehring, M. (2015). Market structure differences impacting Australian iron ore and metallurgical coal industries. Minerals 5:473. doi: 10.3390/min5030473
27. Legendre, P., and Legendre, L. (2012). Numerical Ecology. Amsterdam: Elsevier.
28. Lehtonen, S., Jones, M. M., Zuquim, G., Prado, J., and Tuomisto, H. (2015). Phylogenetic relatedness within Neotropical fern communities increases with soil fertility. Glob. Ecol. Biogeogr. 24, 695–705. doi: 10.1111/geb.12294
29. Letunic, I., and Bork, P. (2016). Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245. doi: 10.1093/nar/gkw290
30. Lucas, E. J., and Bünger, M. O. (2015). Myrtaceae in the Atlantic forest: their role as a ‘model’ group. Biodivers. Conserv. 24, 2165–2180. doi: 10.1007/s10531-015-0992-7
31. Lucas, E. J., Matsumoto, K., Harris, S. A., Nic Lughadha, E. M., Benardini, B., and Chase, M. W. (2011). Phylogenetics, morphology, and evolution of the large genus Myrcia S.L. (Myrtaceae). Int. J. Plant Sci. 172, 915–934. doi: 10.1086/660913
32. Meguro, M., Pirani, J. R., Mello-Silva, R., and Giulietti, A. M. (1996a). Caracterização florística e estrutural de matas ripárias e capões de altitude na Serra do Cipó, Minas Gerais. Bol. Bot. Univ. São Paulo 15, 13–29. doi: 10.11606/issn.2316-9052.v15i1p13-29
33. Meguro, M., Pirani, J. R., Mello-Silva, R., and Giulietti, A. M. (1996b). Estabelecimento de matas ripárias e capões nos ecossistemas campestres da Cadeia do Espinhaço, Minas Gerais. Bol. Bot. Univ. São Paulo 15, 1–11. doi: 10.11606/issn.2316-9052.v15i1p1-11
34. Mello-Silva, R. D. (2009). Flora de grão-mogol, minas gerais: velloziaceae. Bol. Bot. 27, 10. doi: 10.11606/issn.2316-9052.v27i1p109-118
35. Messias, M. C. T. B., Leite, M. G. P., Meira-Neto, J. A. A., and Kozovits, A. R. (2012a). Fitossociologia de campos rupestres quartzíticos e ferruginosos no quadrilátero ferrífero, minas gerais. Acta Bot. Bras. 26, 230–242. doi: 10.1590/S0102-33062012000100022
36. Messias, M. C. T. B., Leite, M. G. P., Meira Neto, J. A. A., Kozovits, A. R., and Tavares, R. (2013). Soil-vegetation relationship in quartzitic and ferruginous Brazilian rocky outcrops. Folia Geobot. 48, 509–521. doi: 10.1007/s12224-013-9154-4
37. Messias, M. C. T. B., Tonaco, A. C., Meira Neto, J. A. A., and Leite, M. G. P. (2012b). Levantamento florístico de um campo rupestre ferruginoso na Serra de Antonio Pereira, Ouro Preto, Minas Gerais. MG BIOTA 5, 4–18.
38. Miazaki, A. S., Gastauer, M., and Meira-Neto, J. A. A. (2015). Environmental severity promotes phylogenetic clustering in campo rupestre vegetation. Acta Bot. Bras. 29, 561–566. doi: 10.1590/0102-33062015abb0136
39. Moraes, D. A., Cavalin, P. O., Moro, R. S., Oliveira, R. A. C., Carmo, M. R. B., and Marques, M. C. M. (2016). Edaphic filters and the functional structure of plant assemblages in grasslands in southern Brazil. J. Veg. Sci. 27, 100–110. doi: 10.1111/jvs.12331
40. Moro, M. F., Silva, I. A., de Araújo, F. S., Nic Lughadha, E., Meagher, T. R., and Martins, F. R. (2015). The role of edaphic environment and climate in structuring phylogenetic pattern in seasonally dry tropical plant communities. PLOS ONE 10:e0119166. doi: 10.1371/journal.pone.0119166
41. Mourão, A., and Stehmann, J. R. (2007). Levantamento da flora do campo rupestre sobre canga hematítica couraçada remanescente na Mina do Brucutu, Barão de Cocais, Minas Gerais, Brasil. Rodriguésia 58, 775–785.
42. Murray-Smith, C., Brummitt, N. A., Oliveira-Filho, A. T., Bachman, S., Moat, J., Nic Lughadha, E. M., et al. (2009). Plant diversity hotspots in the Atlantic coastal forests of Brazil. Conserv. Biol. 23, 151–163. doi: 10.1111/j.1523-1739. 2008.01075.x
43. Nadruz-Coelho, M., Costa, D., Martinelli, G., Moraes, A., and Forzza, R. (2015). Expedição às Montanhas da Amazônia. Jardim Botânico do Rio de Janeiro: Andrea Jacobsson Studio.
44. Negreiros, D., Le Stradic, S., Fernandes, G. W., and Rennó, H. C. (2014). CSR analysis of plant functional types in highly diverse tropical grasslands of harsh environments. Plant Ecol. 215, 379–388. doi: 10.1007/s11258-014-0302-6
45. Neves, D. M., Dexter, K. G., Pennington, R. T., Bueno, M. L., de Miranda, P. L. S., and Oliveira-Filho, A. T. (2018). Lack of floristic identity in campos rupestres— A hyperdiverse mosaic of rocky montane savannas in South America. Flora (in press). doi: 10.1016/j.flora.2017.03.011
46. Nic Lughadha, E. M., Lucas, E. J., and Woodgyer, E. M. (2012). Additions to Myrcia s.l. from Eastern Brazil — taxonomic and nomenclatural novelties in Myrcia s.l. (Myrtaceae). Kew Bull. 67, 235–243. doi: 10.1007/s12225-012-9350-z
47. Oksanen, J., Blanchet, P., McGlinn, D., Minchin, P. R., O’Hara, R. B., Simpson, G. L., et al. (2017). vegan: Community Ecology Package [Online]. Available at: https://CRAN.R-project.org/package=vegan
48. Oliveira, R. S., Galvão, H. C., de Campos, M. C. R., Eller, C. B., Pearse, S. J., and Lambers, H. (2015). Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol. 205, 1183–1194. doi: 10.1111/nph.13175
49. Pifano, D. S., Valente, A. S. M., Almeida, H. D., de Melo, P. H. A., de Castro, R. M., and van den Berg, E. (2010). Floristic and phytophysiognomies characterization of the Serra do Condado, Minas Gerais, Brazil. Biota Neotrop. 10, 51–71. doi: 10.1590/S1676-06032010000100005
50. Pugliesi, L., and Rapini, A. (2015). Tropical refuges with exceptionally high phylogenetic diversity reveal contrasting phylogenetic structures. Int. J. Biodivers. 2015:17. doi: 10.1155/2015/758019
51. SAS Institute Inc (2015). SAS/STATR® 14.1 User’s Guide. Cary, NC: SAS Institute Inc.
52. Scalon, V. R., Martins, C., and Cândido, E. S. (2012). Florística dos remanescentes de campo rupestre sobre canga no Campus Morro do Cruzeiro/UFOP, Ouro Preto, Minas Gerais, Brasil. MG.BIOTA 5, 19–47.
53. Schaefer, C. E. G. R., Corrêa, G. R., Candido, H. G., Arruda, D. M., Nunes, J. A., Araujo, R. W., et al. (2016). “The Physical environment of rupestrian grasslands (Campos Rupestres) in Brazil: geological, geomorphological and pedological characteristics, and interplays,” in Ecology and Conservation of Mountaintop Grasslands in Brazil, ed. G. W. Fernandes (Cham: Springer International Publishing), 15–53.
54. Silveira, F. A. O., Negreiros, D., Barbosa, N. P. U., Buisson, E., Carmo, F. F., Carstensen, D. W., et al. (2016). Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403, 129–152. doi: 10.1007/s11104-015-2637-8
55. Skirycz, A., Castilho, A., Chaparro, C., Carvalho, N., Tzotzos, G., and Siqueira, J. O. (2014). Canga biodiversity, a matter of mining. Front. Plant Sci. 5:653. doi: 10.3389/fpls.2014.00653
56. Stannard, B. L. (1995). Flora of the Pico das Almas, Chapada Diamantina. Richmond: Royal Botanic Gardens, Kew.
57. Stehmann, J. R., Forzza, R. C., Salino, A., Costa, D. P., and Kamino, L. H. Y. (2009). Plantas da Floresta Atlântica. Rio de Janeiro: Instituto de Pesquisas Jardim Botânico do Rio de Janeiro.
58. Swenson, N. G., and Enquist, B. J. (2007). Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation. Am. J. Bot. 94, 451–459. doi: 10.3732/ajb.94.3.451
59. Teixeira, W. A., and de Lemos Filho, J. P. (2013). A flórula rupestre do Pico de Itabirito, Minas Gerais, Brasil: lista das plantas vasculares. Bol. Bot. Univ. São Paulo 31, 199–230. doi: 10.11606/issn.2316-9052.v31i2p 199-230
60. Tucker, C. M., Cadotte, M. W., Carvalho, S. B., Davies, T. J., Ferrier, S., Fritz, S. A., et al. (2017). A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol. Rev. 92, 698–715. doi: 10.1111/brv.12252
61. Vamosi, S. M., Heard, S. B., Vamosi, J. C., and Webb, C. O. (2009). Emerging patterns in the comparative analysis of phylogenetic community structure. Mol. Ecol. 18, 572–592. doi: 10.1111/j.1365-294X.2008.04001.x
62. Viana, P. L., and Lombardi, J. A. (2007). Florística e caracterização dos campos rupestres sobre canga na Serra da Calçada, Minas Gerais, Brasil. Rodriguésia 58, 159–177. doi: 10.1590/S0100-67622011000700013
63. Vincent, R. D. C., and Meguro, M. (2008). Influence of soil properties on the abundance of plant species in ferruginous rocky soils vegetation, southeastern Brazil. Rev. Bras. Bot. 31, 377–388. doi: 10.1590/S0100-84042008000300002
64. Webb, C. O. (2000). Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am. Nat. 156, 145–155. doi: 10.1086/303378
65. Webb, C. O., Ackerly, D. D., and Kembel, S. W. (2008). Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24, 2098–2100. doi: 10.1093/bioinformatics/btn358
66. Webb, C. O., Ackerly, D. D., McPeek, M. A., and Donoghue, M. J. (2002). Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505. doi: 10.1146/annurev.ecolysis.33.010802.150448
67. Zappi, D. C., Milliken, W., Hind, D. J. N., Biggs, N., Rando, J. G., Malcolm, P., et al. (2014). Plantas do Setor Noroeste da Serra do Cipó, Minas Gerais, Guia Ilustrado. Richmond: Royal Botanic Gardens, Kew.