fpls-08-02141 December 15, 2017 Time: 17:17 # 1 ORIGINAL RESEARCH published: 19 December 2017 doi: 10.3389/fpls.2017.02141 Plant Biodiversity Drivers in Brazilian Campos Rupestres: Insights from Phylogenetic Structure Daniela C. Zappi1,2*, Marcelo F. Moro3, Thomas R. Meagher4 and Eimear Nic Lughadha5 1 Biodiversity and Ecosystem Services Team, Instituto Tecnológico Vale, Belém, Brazil, 2 Coordenação de Botânica, Museu Paraense Emílio Goeldi, Belém, Brazil, 3 Instituto de Ciências do Mar (Labomar), Universidade Federal do Ceará, Fortaleza, Brazil, 4 School of Biology, University of St Andrews, St Andrews, United Kingdom, 5 Conservation Science Department, Royal Botanic Gardens, Kew, Richmond, United Kingdom Old, climate-buffered infertile landscapes (Ocbils) have attracted increasing levels of interest in recent years because of their exceptionally diverse plant communities. Brazil’s campos rupestres (rupestrian grasslands) are home to almost 15% of Brazil’s native flora in less than 0.8% of Brazil’s territory: an ideal study system for exploring Edited by: Valentí Rull, variation in floristic diversity and phylogenetic structure in sites differing in geology Instituto de Ciencias de la Tierra and phytophysiognomy. We found significant differences in floristic diversity and Jaume Almera (CSIC), Spain phylogenetic structure across a range of study sites encompassing open vegetation Reviewed by: and forest on quartzite (FQ) and on ironstone substrates, commonly termed canga. Stephen Hopper, University of Western Australia, Substrate and physiognomy were key in structuring floristic diversity in the Espinhaço Australia and physiognomy was more important than substrate in structuring phylogenetic Fernando Augusto Oliveira Silveira, Universidade Federal de Minas diversity, with neither substrate nor its interaction with physiognomy accounting for Gerais, Brazil significant variation in phylogenetic structure. Phylogenetic clustering was significant *Correspondence: in open vegetation on both canga and quartzite, reflecting the potential role of Daniela C. Zappi environmental filtering in these exposed montane communities adapted to multiple [email protected]; [email protected] environmental stressors. In forest communities, phylogenetic clustering was significant only at relatively deep nodes of the phylogeny in FQ while no significant phylogenetic Specialty section: clustering was detected across forest on canga (FC), which may be attributable This article was submitted to Functional Plant Ecology, to proximity to the megadiverse Atlantic forest biome and/or comparatively benign a section of the journal environmental conditions in FC with relatively deep, nutrient-rich soils and access to Frontiers in Plant Science edaphic water reliable in comparison to those for open vegetation on canga and Received: 10 October 2017 Accepted: 04 December 2017 open or forest communities on quartzite. Clades representing relatively old lineages Published: 19 December 2017 are significantly over-represented in campos rupestres on quartzite, consistent with the Citation: Gondwanan Heritage Hypothesis of Ocbil theory. In contrast, forested sites on canga are Zappi DC, Moro MF, Meagher TR recognized as Yodfels. To be effective, conservation measures must take account of the and Nic Lughadha E (2017) Plant Biodiversity Drivers in Brazilian distinct communities which are encompassed within the broad term campos rupestres, Campos Rupestres: Insights from and the differing vulnerabilities of Ocbils and Yodfels. Phylogenetic Structure. Front. Plant Sci. 8:2141. Keywords: campo rupestre, canga, eastern Brazil, phylogenetic clustering, rupestrian grasslands, substrate, doi: 10.3389/fpls.2017.02141 vegetation types Frontiers in Plant Science| www.frontiersin.org 1 December 2017| Volume 8| Article 2141 fpls-08-02141 December 15, 2017 Time: 17:17 # 2 Zappi et al. Phylogenetic Structure in Campos Rupestres INTRODUCTION Found in different continents worldwide, old (ancient), climate- buffered, infertile landscapes (termed Ocbils) harbor high endemism and diversity, as exemplified by the Australian kwongkan, South African fynbos, Guayana shield tepuis (Hopper, 2009). These habitats are believed to have persisted over very long timeframes on the scale of many millions of years due to the geological stability and climatic buffering of their locations. The specialized environmental conditions of such habitats, and the long timeframe over which they have persisted, represent a useful system in which to explore the collective ecological and evolutionary response of plants that exist in them. Brazilian rupestrian habitats, locally known as ‘campos rupestres,’ are an example of a long-standing climate-buffered infertile landscape that contains many endemic species and lineages, which are adapted to very shallow and nutrient-poor soils (Silveira et al., 2016). The highlands in which most campos rupestres occur are situated primarily in the states of Minas Gerais and Bahia, with outliers in Goiás and Tocantins. Thus, they are set within three major Brazilian biomes: to the Southeast, they are embedded in the westernmost part of the Atlantic Rainforest in the state of Minas Gerais, while to the north and west of Minas Gerais state they are found within the Cerrado savannas. In Bahia state, the campos rupestres occur within the Caatinga semi-arid FIGURE 1 | Campos rupestres with different substrates in Minas Gerais. biome. The campos rupestres of the highlands of the Espinhaço (a) Landscape of the Serra do Cipó, Mun. Santana de Pirapama, showing range, which extends through Minas Gerais and Bahia, are the different open quartzite (OQ) vegetation types; (b) OQ - close-up of better botanically explored and have long been recognized as ‘cerrado-rupestre’ with Eriocaulaceae in the foreground at the Serra do Cipó; (c) forest on quartzite (FQ) - view of a forest grove in a matrix of open sites of exceptional biodiversity and endemism (Stannard, 1995; vegetation, Serra do Cipó; (d) FQ - Inside a riverine forest, Serra do Cipó; Giulietti et al., 1997) and, more recently, as fulfilling several (e) FC - forest formation on canga at the Serra da Gandarela, Mun. Rio Acima; of the criteria used to characterize Ocbils (Hopper et al., 2016; (f) open vegetation on canga (OC) - view of canga field at the Serra de Silveira et al., 2016). While campos rupestres are particularly Capanema, Mun. Catas Altas (photos a–d William Milliken; e–f Pedro L. associated with the Espinhaço range, they also occur on even Viana). more ancient rock formations in the Quadrilátero Ferrífero, to the south of the Espinhaço (Schaefer et al., 2016). Along the Espinhaço range, different vegetation types can be found Ocbil theory to be clearly applicable to campos rupestres, and (Figure 1). Forests and savannas mostly grow at lower altitudes further studies of specific subsets of the campo rupestre flora are or along the rivers (Figures 1c,d), while patches of campo rupestre adding to this emerging picture. For example, in a study of 210 grasslands develop at the more exposed sites of mountain tops plant species from campo rupestre Dayrell et al.(2017) found (Figure 1a). Occurring on either quartzitic, arenitic or ironstone that the majority (62.5%) had non-dormant seeds, the highest substrates, typically at altitudes >900 m above sea level, campos proportion of non-dormancy reported for any vegetation type rupestres are estimated to occupy 66,450 km2 and to be home to to date and consistent with predictions of reduced dispersability over five thousand known species (Silveira et al., 2016), of which in Ocbils. Although this study encompassed representatives of over two thousand are recorded as endemic to this habitat type 20% of the plant families represented in campo rupestre, fewer and occur over a relatively small area (Brazil Flora Group [BFG], than 5% of the plant species known from campo rupestre were 2015). treated, illustrating the scale of the challenge in understanding The high levels of floristic diversity and endemism for which this exceptional flora. campo rupestre vegetation is renowned have often been ascribed While campo rupestre can be associated with different to the disjunct (mosaic) distribution of campo rupestre sites substrates, such as quartzite, ironstone or sandstone, the and resulting floristic influences from other habitats, especially diversity and specificity of iron-ore plant communities and savannas (Giulietti et al., 1997; Neves et al., 2018). Recent their occurrence on iron-rich substrates of enormous mining recognition of campos rupestres as an Ocbil has provided a wider interest means that they are amongst the most threatened theoretical framework within which the ecology and evolution vegetation types in Brazil (Jacobi et al., 2007). Unprecedented of their extraordinary plant diversity is being interpreted in a pressure on natural resources such as iron-ore make Brazil global context and over extended geological timescales (Silveira second only to Australia in the quantity of seaborne iron- et al., 2016). Two recent in-depth reviews (Hopper et al., 2016; ore it exports to China (Lawrence and Nehring, 2015). There Silveira et al., 2016) have shown several of the predictions of are three major iron-mining districts in Brazil, namely Carajás Frontiers in Plant Science| www.frontiersin.org 2 December 2017| Volume 8| Article 2141 fpls-08-02141 December 15, 2017 Time: 17:17 # 3 Zappi et al. Phylogenetic Structure in Campos Rupestres in Pará, Urucum in Mato Grosso, and the campos rupestres (open and